Sustainable Agriculture Reviews
Volume 4
Series Editor
Eric Lichtfouse
For other volumes:
www.springer.com/series/8380
Other books by Dr. Eric Lichtfouse
Sustainable Agriculture
Volume 1, 2009
Organic Farming, Pest Control and Remediation of Soil Pollutants
Sustainable Agriculture Reviews. Volume 1, 2009
Climate Change, Intercropping, Pest Control, and Beneficial Microorganisms
Sustainable Agriculture Reviews. Volume 2, 2010
Sociology, Organic Farming, Climate Change and Soil Science
Sustainable Agriculture Reviews. Volume 3, 2010
Environmental Chemistry
Volume 1, 2005
Rédiger pour être publié! Conseils pratiques pour les scientifiques
2009
Forthcoming
Sustainable Agriculture
Volume 2
Biodiversity, Biofuels, Agroforestry and Conservation Agriculture
Sustainable Agriculture Reviews. Volume 5
Environmental Chemistry
Volume 2
Eric Lichtfouse
Editor
Genetic Engineering,
Biofertilisation, Soil Quality
and Organic Farming
Editor
Dr. Eric Lichtfouse
INRA-CMSE-PME
17 rue Sully
21000 Dijon
France
Eric.Lichtfouse@dijon.inra.fr
ISBN 978-90-481-8740-9
e-ISBN 978-90-481-8741-6
DOI 10.1007/978-90-481-8741-6
Springer Dordrecht Heidelberg London New York
Library of Congress Control Number: 2010926197
© Springer Science+Business Media B.V. 2010
No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any
means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written
permission from the Publisher, with the exception of any material supplied specifically for the purpose
of being entered and executed on a computer system, for exclusive use by the purchaser of the work.
Cover illustration: Couple of hoverflies (female left) on common chicory (Cichorium intybus). Cover
picture kindly provided by Alain Fraval. Copyright: Alain Fraval/INRA 2004.
Printed on acid-free paper
Springer is part of Springer Science+Business Media (www.springer.com)
Contents
1
Avidin and Plant Biotechnology to Control Pests...................................
Harry Martin, Elisabeth P.J. Burgess, Michal Masarik,
Karl J. Kramer, Miroslava Beklova, Vojtech Adam,
and Rene Kizek
1
2
Cover Crops for Sustainable Agrosystems in the Americas..................
Johannes M.S. Scholberg, Santiago Dogliotti, Carolina Leoni,
Corey M. Cherr, Lincoln Zotarelli, and Walter A.H. Rossing
23
3
Cover Crops in Agrosystems: Innovations and Applications................
Johannes M.S. Scholberg, Santiago Dogliotti,
Lincoln Zotarelli, Corey M. Cherr, Carolina Leoni,
and Walter A.H. Rossing
59
4
Improving Bioavailability of Phosphate Rock
for Organic Farming..................................................................................
Anthony C. Edwards, Robin L. Walker, Phillip Maskell,
Christine A. Watson, Robert M. Rees, Elizabeth A. Stockdale,
and Oliver G.G. Knox
99
5
Mixed Cropping and Suppression of Soilborne Diseases....................... 119
Gerbert A. Hiddink, Aad J. Termorshuizen,
and Ariena H.C. van Bruggen
6
Decreasing Nitrate Leaching in Vegetable Crops
with Better N Management....................................................................... 147
F. Agostini, F. Tei, M. Silgram, M. Farneselli, P. Benincasa,
and M.F. Aller
7
Manure Spills and Remediation Methods to Improve
Water Quality............................................................................................. 201
Shalamar D. Armstrong, Douglas R. Smith, Phillip R. Owens,
Brad Joern, and Candiss Williams
v
vi
Contents
8
Cropping Systems Management, Soil Microbial
Communities, and Soil Biological Fertility............................................ 217
Alison G. Nelson and Dean Spaner
9
Cyanobacterial Reclamation of Salt-Affected Soil................................ 243
Nirbhay Kumar Singh and Dolly Wattal Dhar
10
Measuring Environmental Sustainability of Intensive
Poultry-Rearing System.......................................................................... 277
Simone Bastianoni, Antonio Boggia, Cesare Castellini,
Cinzia Di Stefano, Valentina Niccolucci, Emanuele Novelli,
Luisa Paolotti, and Antonio Pizzigallo
11
Compost Use in Organic Farming.......................................................... 311
Eva Erhart and Wilfried Hartl
12
Beneficial Microorganisms for Sustainable Agriculture...................... 347
Arshad Javaid
13
Foliar Fertilization for Sustainable Crop Production........................... 371
Seshadri Kannan
Index.................................................................................................................. 403
Chapter 1
Avidin and Plant Biotechnology
to Control Pests
Harry Martin, Elisabeth P.J. Burgess, Michal Masarik, Karl J. Kramer,
Miroslava Beklova, Vojtech Adam, and Rene Kizek
Abstract The urgency of the global food crisis, coupled with the environmental
impact of global warming and fuel shortages, indicate that transgenic methods may
be required to enhance food production and quality. Widely used chemical insecticides, such as phosphine and methyl bromide, are losing their utility either due to
insect resistance or to the environmental damage they cause. It is most unlikely that
traditional plant-breeding methods for generating insect resistance will deliver the crop
improvements required in the available time frame. In this review, we discuss
the application of transgenic avidin, a protein naturally occurring in egg-white,
for the protection of rice, maize, potato and apple leaf from insect pests. Avidin binds
the vitamin biotin with extraordinary affinity (10−15 M). Biotin is a water-soluble
H. Martin and E.P.J. Burgess
The Horticulture and Food Research Institute of New Zealand Limited, Mt Albert Research
Centre, Private Bag 92169, Auckland, New Zealand
M. Masarik
Department of Pathological Physiology, Faculty of Medicine, Masaryk University, Kamenice 5,
CZ-625 00 Brno, Czech Republic
K.J. Kramer
Agricultural Research Service, US Department of Agriculture, Grain Marketing and Production
Research Center, KS 66502 Manhattan, USA
M. Beklova
Department of Veterinary Ecology and Environmental Protection, Faculty of Veterinary Hygiene
and Ecology, University of Veterinary and Pharmaceutical Sciences, Palackeho 1-3, CZ-612 42
Brno, Czech Republic
V. Adam and R. Kizek (*)
Department of Chemistry and Biochemistry, Mendel University of Agriculture and Forestry,
Zemedelska 1, CZ-613 00 Brno, Czech Republic
e-mail: kizek@sci.muni.cz
V. Adam
Department of Animal Nutrition and Forage Production, Faculty of Agronomy, Mendel
University of Agriculture and Forestry, Zemedelska 1, CZ-613 00 Brno, Czech Republic
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_1, © Springer Science+Business Media B.V. 2010
1
2
H. Martin et al.
vitamin required for normal cellular metabolism and growth. The presence of
avidin in the diet of insect pests is lethal since biotin is unavailable to them. The
use of streptavidin, a bacterial homologue of avidin, is also described. We discuss the
sub-cellular targeting of avidin expression in plants to avoid toxicity to the plant host
and we describe the qualities of avidin which make it suitable for crop protection
during cultivation and storage. Avidin is stable under normal conditions of crop storage
but biodegradable and destroyed by cooking. These combined qualities make it an
excellent choice for the protection of crops from insects. Finally, we discuss the
modification of the avidin gene to allow expression in plants, the methods for transfection of the gene into plants, and the approaches used to quantify gene expression
and avidin function in plant tissues. These methods include: polymerase chain reaction;
enzyme-linked immmunosorbent assay; polyacrylamide gel-electrophoresis; fluorescence polarisation (FP); capillary electrophoresis; tissue-printing; square-wave
voltammetry (SWV) and the measurement of larvae morbidity and mortality.
Keywords Transgenic plants • avidin–biotin technology • agriculture
• electrochemical method
Abbreviations
AC
AdTSV
CPE
DNA
ELISA
FP
PCR
SDS-PAGE
SWV
alternating current
adsorptive transfer stripping
carbon paste electrode
deoxyribonucleic acid
enzyme-linked immunosorbent assay
fluorescence polarization
polymerase chain reaction
sodium dodecyl sulfate polyacrylamide gel electrophoresis
square-wave voltammetry
1.1 Introduction
Insect pests cause severe economic damage to agricultural crops. Due to the prospect
of climate change and population increase, this problem has become a vitally important research topic. Stored products of agricultural and animal origin are attacked
by more than 600 species of beetle pests, 70 species of moths and about 355 species
of mites causing quantitative and qualitative losses (Rajendran 2002). The economic
hardship caused by insect pests is exacerbated by the fact that the chemical insecticides used to suppress them are declining sharply in utility. Phosphine and methyl
bromide are two common fumigants used for stored-product protection. Insect
resistance to phosphine is now a global issue (Collins et al. 2003; Nayak and
1
Avidin and Plant Biotechnology to Control Pests
3
Collins 2008) and methyl bromide, a broad-spectrum fumigant, has been declared
an ozone-depleting substance by the US Environmental Protection Agency and,
therefore, is being phased out completely.
Due to the urgency of the crisis in food production and demand, it is most unlikely
that traditional plant-breeding methods will deliver the crop improvements required,
in the available time frame. Thus, it is evident that transgenic methods may be required
to enhance food production and quality. Various transgenic modifications of crops
have already been developed to improve the nutritional yield of crops; for example,
potatoes have been transgenically modified to increase protein content (Chakraborty
et al. 2000), while transgenic rice has been developed with enhanced vitamin A
(Ye et al. 2000) and iron content (Lucca et al. 2001; Murray-Kolb et al. 2002).
Wheat has been modified transgenically to allow crop production in regions of high
salinity and in drought conditions (Abebe et al. 2003). Transgenic modification of
papaya (Ferreira et al. 2002) and potatoes (Gao et al. 2000) has been developed,
which resists viral and fungal infections, respectively.
Several transgenic crops have been developed specifically to deal with insect
pests. The most well-known and widely applied transgenic insecticide is the Bt-cry
toxin which is derived from the soil bacterium Bacillus thuringiensis (Torres et al.
2009). This toxin has been used transgenically in cotton and maize (Barry et al.
2000) to great effect. In addition, rice has been modified transgenically to express
an insecticidal lectin from the snowdrop plant (Galanthus nivali) (Nagadhara et al.
2004). Here, we review the transgenic use of the biotin-binding protein avidin to
control insect pests in a variety of important crops, including maize, rice, potatoes
and apples. Avidin is a natural protein present in the egg-whites of birds and its role
is to sequester free biotin. Biotin is an essential dietary component for insects, without which they are unable to grow. Avidin differs from other transgenic insecticidal
toxins because it is not directly damaging to tissues, rather it merely withholds an
essential nutrient from the insects. Biotin, as a normal dietary constituent, is, therefore, a natural antidote to avidin that, in its denatured (cooked) form, is already a
normal component of many people’s diets. We discuss the techniques for introducing the avidin gene into plants in ways which avoid toxicity to the host species and
we summarise the evidence that avidin can be expressed harmlessly in crops while
being lethal only to the insects which feed on these plants. Finally, we review the
varied methods for detecting and quantifying avidin expression in crops.
1.2 Avidin as a Tool to Protect Plants Against Pests
1.2.1 The Physiological Functions and Structures
of Biotin and Avidin
Biotin, vitamin H, or B8 (cis-hexahydro-2-oxo-1-H-thieno-[3,4]-imidazoline-4-valeric
acid) is a water-soluble vitamin that is required for normal cellular metabolism and
growth (Alban et al. 2000; Shellhammer and Meinke 1990) and functions as a
4
H. Martin et al.
carboxyl carrier in carboxylation, decarboxylation and transcarboxylation reactions.
Biotin is a dietary requirement of insects since synthesis occurs only in plants, bacteria and certain fungi. While biotin has traditionally been viewed as an essential cofactor of carboxylases, there have also been long-standing suggestions of a role for
biotin in the regulation of gene expression (Dakshinamurti 2005; Hassan and Zempleni
2006; Rodriguez-Melendez and Zempleni 2003; Vilches-Flores and Fernandez-Mejia
2005). Recently, a potential role for gene regulation has been shown by specific
biotinylation of histones. All five histone classes extracted from blood mononuclear
cells contain biotin (Ballard et al. 2002; Kothapalli et al. 2005; Zempleni 2005). The
insect central nervous system was shown to be rich in biotin-containing proteins
(Ziegler et al. 1995). The fundamental requirement of biotin for many cellular activities
of animals, including insects, therefore, suggests that the sequestration of biotin in the
diet of pests would profoundly inhibit pest growth and development.
Avidin is a glycosylated protein, composed of four sub-units with a molecular
weight of about 67 kDa. Each sub-unit contains one high-affinity, biotin-binding site
with a dissociation constant Kd = 10−15 M. This interaction exhibits one of the highest
known affinities in nature between a protein and its ligand, and it is employed in various fields, including immunohistochemistry, electron microscopy, DNA hybridisation
and biosensor technologies. In nature, avidin occurs as a minor component of bird,
reptile, and amphibian egg-white where it protects embryos by ensuring that there is
no free biotin in the egg-white. The absence of biotin inhibits the growth of many
pathogenic microorganisms. Streptavidin has very similar properties to avidin. Their
overall amino acid sequences show a low degree of similarity. Resolution of threedimensional (3D) structures of avidin and streptavidin shows them to share a high
degree of structural homology. Both are tetramers of identical sub-units, which fold
into an eight-stranded anti-parallel beta-barrel. The biotin-binding site within each
promoter is located in a deep pocket in the core of the barrel displaying both hydrophobic and polar residues for recognition of the tightly bound vitamin and consists of
residues of the barrel itself and of a loop of the adjacent sub-unit. Moreover, the binding pocket is partly closed in its outer rim by tryptophan residue 110 of a neighbouring
sub-unit. Once bound, biotin is almost completely buried in the protein core, with the
exception of the valeryl side-chain carboxylate group, which is exposed to solven.
Hydrogen bonds to residues Alanine 39, Threonine 40, and Serine 75 trigger the formation of a network of hydrogen-bonded water molecules. Two tryptophan residues
(Trp 70 and Trp 97) and phenylalanine 79 are in close contact with biotin (Fig. 1.1).
1.2.2 Avidin as a Pesticide in Food
Avidin and streptavidin are also resistant to proteolysis. However, both avidin and
streptavidin function is greatly reduced by cooking, rendering the avidin harmless
to humans following cooking, in the same way that cooked eggs are not harmful to
humans. These combined properties render these proteins ideal for inclusion in
foodstuffs as a pesticide. The insecticidal properties of avidin have been known since
1
Avidin and Plant Biotechnology to Control Pests
5
Fig. 1.1 Structural model of avidin and avidin linked to streptavidin (www.cryst.bbk.ac.uk/.../
rosano/vbp/avidin.html)
1959, when it was demonstrated that avidin is insecticidal when included in the diet
of housefly larvae (Levinson and Bergmann 1959) and subsequently, against a wide
range of insects (Table 1.1).
Due to their insecticidal properties, avidin, and the functionally related streptomyces protein, streptavidin, have been expressed in a variety of agriculturally important
plant species, for example, tobacco, apple, maize and rice. Table 1.1 summarises the
insecticidal effects of exogenous and transgenically expressed avidin on various insect
larvae. A single instance of an insect, which is not susceptible to the presence of avidin
in its diet, is the larger grain borer (Kramer et al. 2000), which tolerates high quantities
of dietary avidin. Kramer suggests that this might be due to unusually high proteinase
activity in the insects’ gut digesting the avidin and precluding biotin sequestration.
Alternatively, Kramer suggests that the larger grain borer may have a supply of
biotin from gut symbionts.
The remarkable safety of transgenic avidin was shown by Kramer (Kramer et al.
2000) who found that mice fed solely on transgenic avidin-maize containing insecticidal quantities of avidin over a 21-day period showed no toxic effects and thrived in
the same way as mice fed on control corn-meal. Furthermore, Yoza (Yoza et al. 2005)
demonstrated that 97% of avidin functional activity is lost by heat denaturation (i.e.
cooking) at 95°C for 5 min. In addition, avidin has the considerable added advantage
over conventional insecticides in that, as a component of the stored crop, it is not
washed away during processing and continues to act as an insecticide during storage.
6
H. Martin et al.
Table 1.1 Insecticidal properties of avidin demonstrated in these insect species
Binomial
Common name
nomenclature
Avidin source
Reference
Housefly larvae
Dietary
Benschoter 1967,
Musca domestica
supplement
Levinson and
Bergmann 1959
Blowfly larvae
Aldrichina grahami
Dietary supplement
Miura et al. 1967
Merchant grain
Oryzaephilus
Dietary supplement
Saxena and Kaul
beetle
mercator
1974
Red flour beetle
Tribolium castaneum
Dietary supplement
Morgan et al. 1993
Confused flour
Tribolium confusum
beetle
Sawtoothed grain
Oryzaephilus
beetle
surinamensis
Rice weevil
Sitophilus oryzae
Lesser grain borer
Rhizopertha dominica
European corn borer
Ostrinia nubilalis
Indian meal moth
Plodia interpunctella
Kramer et al. 2000
Maize weevil
Sitophilus zeamais
Transgenic
expression in
Angoumois grain
Sitotroga cerealella
maize
moth
Lesser grain borer
Rhyzopertha
dominica
Oryzaephilus
Saw-toothed grain
beetle
surinamensis
Red flour beetle
Tribolium castaneum
Potato tuber moth
Phthorimaea
Dietary supplement
Markwick et al.
operculella
2001
Light-brown apple
Epiphyas postvittana
moth
Green-headed leafPlanotortrix octo
roller
Brown-headed leafCtenopseustis
roller
obliquana
Burgess et al. 2002
Tobacco budworm
Helicoverpa
Transgenic
armigera
expression in
tobacco
Oriental leafworm
Spodoptera litura
Black field cricket
Teleogryllus
Dietary supplement
Malone et al. 2002
nymphs
commodus
Markwick et al.
Potato tuber moth
Phthorimaea
Transgenic
2003
operculella
expression in
tobacco and
Light-brown apple
Epiphyas postvittana
apple
moth
Meiyalaghan et al.
Potato tuber moth
Phthorimaea
Transgenic
2005
operculella
expression in
potato
Yoza et al. 2005
Confused flour
Tribolium confusum
Transgenic
beetle
expression
in rice
Angoumois grain
Sitotroga cerealella
moth
(continued)
1
Avidin and Plant Biotechnology to Control Pests
7
Table 1.1 (continued)
Common name
Binomial
nomenclature
Velvet bean
caterpillar
Beet armyworm
Cotton bollworm
Colorado potato
beetle
Anticarsia
gemmatalis
Spodoptera exigua
Helicoverpa zea
Leptinotarsa
decemlineata
Avidin source
Reference
Dietary supplement
Zhu et al. 2005
Dietary supplement
Cooper et al. 2006
Unlike insecticidal chemical sprays, avidin has a minimal effect as an environmental
pollutant. The inclusion of avidin in crops raises the possibility of the induction
of an allergic response to the protein. However, avidin is known not to be highly
allergenic and is absent from the World Health Organization’s official list of food
allergens, whereas many highly allergenic proteins from common fruit, nuts, corn, and
egg-white are present. The official website for the WHO/IUIS Sub-Committee on
Allergen Nomenclature is www.allergen.org. This site lists all allergens and
isoforms that are recognised by the committee and is updated on a regular basis.
1.2.3 Transgenic Expression of Avidin in Plants
Various strategies have been employed for the transgenic expression of avidin in
plants. Hood and co-workers expressed chicken egg-white avidin in maize, achieving
an expression level of greater than 2% of aqueous soluble protein extracted from
dry seed (Hood et al. 1997), the mature protein localising to the extracellular spaces.
The approach taken by Hood et al. was to reverse-translate the chicken egg-white
avidin amino acid sequence into DNA using the preferred maize codon usage
(Fig. 1.2a). This sequence was inserted into a plasmid, which contained the maize
ubiquitin promoter. The avidin-containing plasmid was introduced into an embryonic
maize cell line from which plants were cultivated. The aim of Hoods approach was
to maximise avidin expression for the commercial production of avidin rather than
to use the avidin to protect the maize. Although Hood used the ubiquitin promoter
because it is generally thought to be constitutive, the avidin expression was particularly strong in seed and Hood concluded that the ubiquitin promoter has strong seed
preference. Hood also noticed that the avidin expressed in this way had profound
physiological effects on the plant – the male transformants were sterile. Kramer and
co-workers (Kramer et al. 2000) used the same genetic constructs for their study of
the insecticidal properties of transgenic avidin-maize.
Yoza et al. (2005) adopted a similar approach to Hood for the expression of
avidin in rice except that the glutelin promoter GluB-1r, a seed-specific promoter, was
used instead of the ubiquitin promoter on the grounds that a seed-specific promoter
will lead to expression of avidin in all seeds whereas male sterility could lead to
half of the kernels of avidin-maize containing no avidin. Yoza argues that a
8
H. Martin et al.
Methods for transformation & detection of the avidin gene
a Chicken avidin gene is synthesised with codon usage of host plant
GCC AGA AAG TGC TCG CTG ACT GGG AAA .... chicken avidin cDNA
Ala Arg Lys Cys Ser Leu Thr Gly Lys .... amino acid sequence
cDNA codon usage converted from chicken to host plant
e.g. zea mays (amino acid sequence remains unchanged)
GCTAGG AAG TGCAGC CTC ACC GGTAAG.... "maize" avidin cDNA
Ala Arg Lys Cys Ser Leu Thr Gly Lys .... amino acid sequence
b Avidin cDNA is inserted into vacuolar targetting plasmid.
Transgenic plant is produced by agrobacterium mediated transformation. Avidin gene is
detected in transformed plants by Southern Blotting.
agrobacterium
mediated
transformation of
plant with vacuolar
targeted avidin
plant DNA analysed
by PCR and Southern
blotting confirms
presence of avidin
gene
Fig. 1.2 Methods for transformation and detection of the avidin gene. (a) Transforming the DNA
sequence of chicken avidin into a sequence which will be efficiently expressed in the maize plant.
(b) The avidin gene is inserted into plants so that the protein avidin is only expressed in plant
vacuoles where it does not interfere with the plants’ own biotin resources
seed-specific promoter would be more appropriate for the protection of a stored
product from pests. In addition, since the Glub-1 promoter is endosperm-specific
and is not expressed in pollen, transgenic avidin-rice is fertile. Since rice is
self-compatible, male sterility would be a fatal problem.
1.2.4 Targeted Vacuolar Expression of Avidin Reduces
Toxicity to Plants
A major function of avidin expression in rice and maize is to protect the seed from
pests during storage. In the case of crops such as potato and apples, the pest problem comes during cultivation in the form of damage to foliage, tubers and fruit by
the larvae of, for example, the potato tuber moth, the light-brown apple moth or
leaf-roller moth. In these cases, targeting avidin expression to seeds would be unproductive and disseminated avidin expression would be more appropriate. Avidin and
1
Avidin and Plant Biotechnology to Control Pests
9
the functionally similar protein streptavidin have been transgenically expressed in
tobacco and apple (Markwick et al. 2003; Murray et al. 2002). In these studies, the
Cauliflower Mosaic Virus promoter was employed which lead to a non-tissue-specific
expression of avidin. Male infertility did not occur. However, to prevent toxicity due
to sequestration of essential plant biotin, the avidin was targeted to intracellular vacuoles by the use of N-terminal vacuole targeting sequences from potato proteinase
inhibitors (Fig. 1.2b). If targeting sequences were not used then avidin expression
was lethal (Hood et al. 1997; Murray et al. 2002) since biotin is synthesised in
the plant cytoplasm and used in the mitochondrial and chloroplastic compartments
(Baldet et al. 1992, 1993). The leaf concentrations of avidin achieved by Murray
and Marckwick were approximately 10 mM. This is approximately a 7.5-fold molar
excess of avidin over the normal biotin levels in the plant leaf (Murray et al. 2002)
and is sufficient to ensure that insect pests feeding on the leaves are killed or never
reach reproductive maturity (Fig. 1.3). From a human toxicity aspect, the insecticidal
level of avidin in transgenic apple and tobacco leaves is somewhat lower than that
of chicken egg-white.
Insecticidal mechanism of avidin
normal plant
transgenic-avidin plant
In the presence of transgenic avidin, the biotin
is sequestered by the avidin. Biotin in not
available to the caterpillar’s carboxylases and
the caterpillars cannot grow.
carboxylase
avidin + biotin (blue)
In the normal leaf, insect carboxylase
function is normal and caterpillar pests
thrive. The leaves are destroyed.
carboxylase + biotin (blue)
Fig. 1.3 Insecticidal mechanism of avidin. Normal and transgenic-avidin plants develop normally. Transgenic avidin is restricted to vacuoles within the leaf cells and, therefore, cannot
interfere with normal leaf biotin function. Avidin is released from the vacuoles and binds the leaf
avidin when the caterpillar chews the leaf tissue
10
H. Martin et al.
1.2.5 Transgenic Avidin in Combination with Other
Pesticidal Transgenes
Avidin has been shown to have synergistic effects when used in conjunction with
other insect toxins. The Bacillus thuringiensis, toxin Bt-Cry3A is active against the
Colorado beetle larva (Leptinotarsa decemlineata) and has been transgenically
expressed in potato, Solanum tuberosum (Coombs et al. 2002). In addition, many
wild Solanum species possess an innate resistance to the Colorado beetle due to the
presence of naturally insecticidal leptine glycoalkaloids, expressed only in foliage
(Sinden et al. 1986). When potato leaves transgenically expressing Bt-Cry3A are
dipped in avidin there is a combined effect of the two insecticides. There is a similar
additive effect of combining the natural resistance of the leptine glycoalkaloids
with avidin (Cooper et al. 2006). Thus, transgenic expression of avidin is known to
be an effective insecticide in isolation and in combination with natural plant insecticides and with other transgenic insecticides.
It is conceivable that transgenic avidin might have adverse effects on the natural
predators of insect pests. A study by Burgess (Burgess et al. 2008) in which Spodoptera
litura (Oriental leafworm) that have been fed avidin, are themselves used as food
for Ctenognathus novaezelandiae (Carabid beetles) revealed no evidence of tritrophic toxicity occurring in the predator. The lack of morbidity in the Carabid
beetles related with de-activation and dilution of avidin in the prey of this leafworm.
The evidence to date does not support concerns about accumulation of poisonous
levels of avidin in the insect food chain.
1.3 Commonly Used Methods to Determine Avidin
in Transgenic Plants
1.3.1 Polymerase Chain Reaction (PCR) and Southern Blotting
The successful genomic insertion of the avidin gene in transgenic plants has been
confirmed by using the PCR technique (Saiki et al. 1988) and Southern blotting
(Southern 1975) in maize (Hood et al. 1999), tobacco (Murray et al. 2002), (Burgess
et al. 2002) and rice (Yoza et al. 2005). Southern blotting of restriction enzyme
digested plant genomic deoxyribonucleic acid (DNA) revealed three to five copies
of avidin gene in several transgenic plants (Hood et al. 1997). However, insertion of
the avidin gene into the host plant genomic DNA does not necessarily imply that the
avidin protein will be expressed. An essential step for efficient expression of transgenic
proteins is that the different codon usage of each host is taken into account. For
example, to express chicken avidin protein in maize, Hood (Hood et al. 1997) synthesised an avidin coding DNA sequence that corresponded to efficient codon usage
by maize, not chicken (Fig. 1.2b). Various methods are available to confirm expression of avidin protein.
1
Avidin and Plant Biotechnology to Control Pests
11
1.3.2 ELISA (Enzyme-Linked ImmunoSorbent Assay)
ELISA is the most common and simplest method employed for detecting avidin in
transgenic plants. Leaf homogenates containing transgenic avidin are applied to
microtitre plates and the avidin in the sample adheres to the microplate surface. After
extensive washing, an antibody directed against avidin is added to the plate and following a further washing step, a secondary antibody coupled to an enzyme, such as
alkaline-phosphatase or horseradish peroxidase, is added to the plate. The amount of
enzyme activity remaining on the washed microplate correlates with the amount
of avidin in the original sample. The enzyme activity is usually measured by cleavage
of a substrate whose product is coloured or fluorescent. This method, known as
indirect ELISA because the enzyme is coupled to the second antibody not the first,
has been used extensively to detect transgenic avidin in leaf tissue (Burgess et al.
2002; Christeller et al. 2005; Markwick et al. 2003; Murray et al. 2002; Yoza
et al. 2005). A more sensitive variant on this technique, called ‘sandwich’ or ‘capture’
ELISA, was used by Hood (Hood et al. 1997) and Kramer (Kramer et al. 2000) for
the measurement of transgenic avidin in maize. In this method, an antibody to avidin
is pre-coated onto the ELISA microplate to optimise adsorbing of the transgenic
avidin and minimise competition on the microplate for other leaf proteins. That is,
the first antibody in the sandwich ELISA concentrates avidin on the microplate
surface. Subsequent steps are the same as in the indirect ELISA method.
These antibody-dependent ELISA methods measure avidin protein as an antigen
present in a transgenic sample. However, for various reasons, the presence of transgenic avidin protein may not equate to functionally active (i.e. biotin-binding) avidin.
Christeller (Christeller and Phung 1998) showed that the level of biotin in apple leaf
varies seasonally from 200 to 800 ng biotin per gram of leaf. This equates approximately to a range of 0.8–3.3 mM biotin. Avidin has four biotin-binding sites per
molecule and, therefore, a transgenic avidin leaf homogenate containing avidin
with less than this level of biotin-binding sites will be saturated with endogenous
biotin. ELISA has been used to differentiate the total transgenic leaf avidin from
the unbound (functionally active) transgenic leaf avidin (Christeller et al. 2005).
In these assays enzyme-labelled antibody to avidin measured total avidin protein
while biotin-labelled enzyme detected biotin-binding sites unoccupied by endogenous
leaf biotin.
1.3.3 SDS-PAGE (Sodium Dodecylsulphate Polyacrylamide
Gel Electrophoresis) and Western Blotting
SDS-PAGE is a widely used technique that separates proteins according to their
size. Under the influence of an electric field, proteins are eletrophoresed through a
polyacrylamide gel matrix. Their mobility inversely correlates with their size
(Patterson 1994). The binding of the negatively charged detergent SDS to proteins
12
H. Martin et al.
denatures their unique 3D shape so that they acquire a ellipsoid 3D shape. Also, the
SDS confers a strong negative charge on proteins which overrides the normal substantial variation in net charge conferred by amino acid content. Thus, high resolution
is achieved because the molecular size of the proteins becomes the only important
factor influencing their migration through the gel matrix under the influence of an
electric field. For SDS-PAGE, purified protein samples must be applied to the gel since
the proteins are usually visualised by non-specific protein stains. The Western-Blotting
technique takes SDS-PAGE a step further, since it allows complex mixtures of samples,
separated on SDS-PAGE gels, to be analysed by antigen city or even functionality,
if non-denaturing conditions are used. Following size-separation on SDS-PAGE,
the proteins in the gel are electrophoretically transferred onto a sheet of nitrocellulose or polyvinylidene fluoride, which binds them in position (Fig. 1.4). The
membrane can then be probed with antibodies specific for certain proteins, for
example, anti-avidin antibodies. In this way, whole leaf homogenates can be analysed
to reveal the quantity and molecular size of the transgenic avidin protein they contain. Using non-denaturing conditions allows functional avidin to be visualised and
quantified. The avidin is usually visualised using similar reagents to the ELISA
procedure except that a chemiluminescent substrate is applied to the membrane whose
cleavage results in light emission and the image is captured by camera or on photographic film. Alternatively, the antigenic protein bands on the membrane can be
stained using a substrate whose enzymatic product is coloured and insoluble.
Avidin and streptavidin both form a tetramer structure. Each monomer of avidin
is 16 kDa in weight. In the case of denaturing SDS-PAGE electrophoresis, when
Methods for detection of avidin protein
avidin protein is detected in plant by various methods:
Western blotting confirms avidin
protein is present in leaf extract.
Plant and chicken avidin
glycosylation differ.
Transmission
electron microscopy
confirms presence
of avidin protein in
leaf vacuoles
tissue printing on nitrocellulose
reveals distribution of avidin
throughout leaf
Light microscopy using
fluorescently labelled
antibodies confirms
presence of avidin protein
in leaf vacuoles from
chicken avidin
Fig. 1.4 Methods for detecting and analysing avidin protein
1
Avidin and Plant Biotechnology to Control Pests
13
samples of avidin were boiled, protein migrated mainly as the monomer (Bayer
et al. 1996; Humbert et al. 2005). In comparative stability properties study of avidin
and streptavidin, it was determined that, in the absence of biotin, the quaternary
structure of streptavidin is more stable than that of avidin (Hytonen et al. 2003;
Williams et al. 2003). Biotin stabilises the tetrameric structure of both avidin and
streptavidin (Bayer et al. 1996).
The post-translational modification of proteins, including glycosylation, is speciesand tissue-dependent. This would imply that chicken avidin expressed in different
plant species would have different glycosylation patterns. The variation in glycosylation could potentially affect the avidin’s affinity for biotin, and the intracellular
location and stability of transgenic avidin. Several studies of transgenic chicken
avidin have confirmed that it is glycosylated differently in plants than its natural
host species. Using the Western-Blot method Hood (Hood et al. 1997) showed that
transgenic chicken avidin synthesised in maize had a molecular weight of 16.6 kDa,
800 Da less than the same gene expressed in its natural host. Treatment of both
avidins with N-glycosidase reduced the molecular weights of both proteins to 12.5
kDa confirming that the primary structure of the avidin was identical but that the
protein was glycosylated differently when expressed in maize. These results are not
surprising since it is well known that glycosylation varies even between closely
related species and the glycosylation systems of plants and animals are very different.
Even within an individual organism, protein glycosylation is tissue-specific and within
a single cell, the glycosylation of an protein is heterogeneous (reviewed by Spiro
(2002) and Lis (Lis and Sharon 1993)). Similarly, Murray et al. (2002) showed that
while egg-white avidin was fully deglycosylated by treatment with the N-glycosidase
F, tobacco-leaf avidin was only partially deglycosylated. A similar application of
Western-Blotting by Gatehouse (Gatehouse et al. 2008) showed that chicken avidin
and transgenic maize-avidin had clearly different sensitivities to treatment with
endoglycosidases F and H. These changes in avidin glycosylation did not cause any
noticeable alteration in the affinity of the transgenic protein for biotin.
1.3.4 Semiautomatic Capillary Electrophoresis
Experion is an automated microfluidic electrophoresis system that uses a combination of Caliper Life Sciences innovative LabChip microfluidic separation technology and sensitive fluorescent sample detection. It performs rapid and reproducible
analyses of protein, DNA and RNA samples, which allows the analysis of samples
within 30 min (Bradova and Matejova 2008). The separation, detection and data
analysis are performed within a single platform, so the time-consuming steps in classic
electrophoretic methods are minimised. Many types of samples, such as bacterial
lysates, protein extracts and chromatography fractions, can be analysed. In addition
to the significant shortening of time required, the chip-based method allows both
reproducible and accurate sizing and quantification of the proteins. Avidin has been
successfully analysed by this technique (Krizkova et al. 2008). The chip electrophoresis
14
H. Martin et al.
system provides very good reproducibility, simple handling, fast analysis and
results comparable with SDS-PAGE (Bradova and Matejova 2008).
1.3.5 Fluorescence Polarisation (FP)
This method exploits the fact that many small fluorescent molecules absorb and
emit polarised light in the same plane. For fluors such as fluorescein, Alexa or
BODIPY dyes, there is a delay of 4–6 ns between fluorescence excitation and emission. This is a sufficiently long delay for a small molecule the size of biotin to tumble
randomly in Brownian motion. However, if the fluorescent molecule is immobilised
by binding to a much larger protein molecule then very little movement will occur
between excitation and emission. Thus, if biotin is covalently attached to a fluorescent compound such as Alexa-594, then the concentration of avidin or biotin in a
sample can be measured from the degree to which the emitted fluorescent light is
polarised. A high polarisation signal means that the fluor is bound to avidin, while
a low polarisation means that the fluorescent ligand is unbound and, therefore, the
avidin concentration in the sample is low. The FP technique is simple, accurate,
sensitive and the reagents are inexpensive. FP analysis is often performed in 384 well
microplates and is therefore, suitable for high-throughput automated screening. FP
was recently applied to the quantification of biotin in normal apple leaves and also
used to quantify avidin expression in whole-leaf homogenates from transgenic plants
(Martin et al. 2008).
1.3.6 Electrochemical Methods
The strong affinity of avidin for biotin allows biotin binding to be detected electrochemically. Avidin contains a diversity of amino acids in its structure. From an
electrochemical point of view, only tyrosine and tryptophan have been found to be
electroactive using a variety of electrodes (Brabec and Mornstein 1980a, b; MacDonald
and Roscoe 1997). Square-wave voltammetric (SWV) analysis using solid carbon
electrodes is very sensitive and yields well-developed signals. However, using a
carbon paste electrode (CPE) and base line correction of the data, we can determine
well-defined voltammetric signals for both tyrosine and tryptophan at 0.78 and 0.92
V versus Ag/AgCl/3 M KCl, respectively. Electrochemical investigation at carbon
electrodes showed that avidin produced oxidation signals due to tyrosine and tryptophan residues.
Square-wave voltammetry at a carbon paste electrode using the adsorptive transfer
stripping (AdTS) technique simple is a fast method for determination of avidin
(Palecek and Postbieglova 1986). This technique is based on the immobilisation of
the analyte in the form of a small drop of solution at the carbon paste electrode,
followed by washing and detection steps in a cell containing a supporting electrolyte
1
Avidin and Plant Biotechnology to Control Pests
15
(Masarik et al. 2003; Petrlova et al. 2007b; Tomschik et al. 2000). The denatured
protein exhibits a fivefold higher response relative to that of the native protein,
indicating that there were substantially more aromatic residues exposed to the
electrode surface in the denatured state (Masarik et al. 2003). Under optimal
experimental conditions, the limit of detection of avidin is in the attomolar range
(Petrlova et al. 2007b). Recently, we described an easy-to-use electrochemical
technique for the detection of avidin in transgenic plants. Plant extract is added
into carbon paste (Fig. 1.5) and avidin present in the extract gives a very distinct
signal (Kizek et al. 2005; Masarik et al. 2003; Petrlova et al. 2007a). Krizkova
compared electrochemical method with gel electrophoresis and found that methods gave similar results on analysis of transgenic tobacco leaves (Krizkova et al.
2008). Moreover, Fojta et al. and others report on some less common electrochemical methods for the detection of avidin and avidin–biotin interactions (Fojta
2008; Havran 2004; Limoges 1996).
The application of AdTS SWV in conjunction with liquid chromatography,
diode array detection and flow injection analysis has allowed the extremely sensitive
detection of biotin and avidin in the femtomolar range (Kizek et al. 2005). Moreover,
Kizek and his colleagues have proposed an approach to detecting avidin–biotin
interaction in transgenic plants (Fig. 1.5). Sugawara and colleagues developed methods
for the electrochemical analysis of avidin–biotin interactions using various types of
labelled biotins. In particular, they used bisbiotinyl thionine (Sugawara et al. 2004),
iminobiotin (Sugawara et al. 2005), N-iodoacetyl-N-biotinylhexylenediamine
(Sugawara et al. 1996a), biotin labelled with Nile Blue A (Sugawara et al. 1996b)
and biotin/thionine modified Au electrode (Sugawara et al. 2002).
1.3.7 Tissue Printing
Another commonly applied technique to reveal the large-scale expression pattern
of transgenic proteins, including avidin, in plant tissue is tissue printing (Fig. 1.4).
Cross sections of plant stems, roots or tubers can simply be pressed against nitrocellulose leaving behind an imprint of the avidin in the tissue. For tissue printing of
leaves, the leaves should first be freeze-thawed to break open the cell walls and
intracellular organelles before pressing against the nitrocellulose. The tissue-printed
nitrocellulose can then be handled like a Western-Blot and probed with biotin-coupled
peroxidase to reveal the distribution of avidin expression in the plant sample. This
technique has been employed for the detection of transgenic avidin in tobacco
(Murray et al. 2002), and maize (Hood et al. 1997).
To determine the sub-cellular localisation of the transgenically expressed avidin,
Hood (Hood et al. 1997) performed in situ localisation experiments on thin sections
of embedded embryos using anti-avidin primary antibodies and fluorescently labelled
secondary antibodies (Fig. 1.4). As expected, Hood et al. observed the avidin being
secreted into the cell wall matrix since they had fused the avidin gene to a signal
sequence that targeted the protein to the endoplasmic reticulum. In plants, the default
16
H. Martin et al.
homogenization
leaf
stem
root
transgenic avidin plant
plant extract in to carbon paste electrode
Electrochemical detection
quantification
detection of avidin concentration in part plant
I
first - signal
E
confirmation
interaction avidin-biotin
biotin
second – no signal
I
E
Fig. 1.5 Scheme of fast electrochemical detection of avidin concentration and avidin–biotin
interaction in transgenic plants
pathway for proteins in the endoplasmic reticulum is secretion. Using similar
fluorescent-light-microscopy methods Murray et al. confirmed vacuolar expression
of avidin in tobacco, using a vacuolar targeting signal. Vacuolar expression of avidin in tobacco was also demonstrated by Murray using transmission electron
microscopy and gold-labelled antibodies (Fig. 1.4) (Murray et al. 2002).
1
Avidin and Plant Biotechnology to Control Pests
17
1.3.8 Mortality and Morbidity Assay
Finally, several researchers have used biological assays, for example, insect mortality,
morbidity, development and behaviour to measure the presence of functional avidin
in transgenic plants. In these experiments, the larvae of insect pests are placed onto
normal or transgenic leaves and their growth and development rates are recorded
(Fig. 1.3). These studies are summarised in Section 1.2 and Table 1.1.
The simplest and most direct measure of biological effect on the insect larvae
feeding on plants expressing avidin transgenically is mortality: Markwick (Markwick
et al. 2003) observed that potato tuber moth larvae fed on transgenic apple and tobacco
leaves had a mortality rate of up to 90% within 9 days compared with 100% survival
of larvae on normal leaves. By studying the behaviour of the leaf-mining potato
tuber moth larvae, Marckwick noted that the insects were unable to detect the insecticidal avidin since they did not leave their leaf mines. There was no evidence of
the larvae avoiding the transgenic leaf and seeking alternative food sources. This was
an interesting observation because avoidance behaviour had been observed for larvae
feeding on leaves containing B. thuringiensis toxins (Beuning et al. 2001; Gleave
et al. 1998).
Acknowledgement Financial support from grants MSMT 6215712402 is highly acknowledged.
References
Abebe T, Guenzi AC, Martin B, Cushman JC (2003) Tolerance of mannitol-accumulating transgenic wheat to water stress and salinity. Plant Physiol 131:1748–1755
Alban C, Job D, Douce R (2000) Biotin metabolism in plants. Annu Rev Plant Physiol Plant Mol
Biol 51:17–47
Baldet P, Alban C, Axiotis S, Douce R (1992) Characterization of biotin and 3-methylcrotonylcoenzyme a carboxylase in higher-plant mitochondria. Plant Physiol 99:450–455
Baldet P, Alban C, Axiotis S, Douce R (1993) Localization of free and bound biotin in cells from
green pea leaves. Arch Biochem Biophys 303:67–73
Ballard TD, Wolff J, Griffin JB, Stanley JS, van Calcar S, Zempleni J (2002) Biotinidase catalyzes
debiotinylation of histones. Eur J Nutr 41:78–84
Barry BD, Darrah LL, Huckla DL, Antonio AQ, Smith GS, O’Day MH (2000) Performance of
transgenic corn hybrids in Missouri for insect control and yield. J Econ Entomol 93:993–999
Bayer EA, EhrlichRogozinski S, Wilchek M (1996) Sodium dodecyl sulfate-polyacrylamide gel
electrophoretic method for assessing the quaternary state and comparative thermostability of
avidin and streptavidin. Electrophoresis 17:1319–1324
Benschoter CA (1967) Effect of dietary biotin on reproduction of the house fly. J Econ Entomol
60:1326–1328
Beuning LL, Mitra DS, Markwick NP, Gleave AP (2001) Minor modifications to the cry1Ac9
nucleotide sequence are sufficient to generate transgenic plants resistant to Phthorimaea operculella. Ann Appl Biol 138:281–291
Brabec V, Mornstein V (1980a) Electrochemical-behavior of proteins at graphite-electrodes. 1.
Electrooxidation of proteins as a new probe of protein-structure and reactions. Biochim Biophys
Acta 625:43–50
Brabec V, Mornstein V (1980b) Electrochemical-behavior of proteins at graphite-electrodes. 2.
Electrooxidation of amino-acids. Biophys Chem 12:159–165
18
H. Martin et al.
Bradova J, Matejova E (2008) Comparison of the results of SDS PAGE and chip electrophoresis
of wheat storage proteins. Chromatographia 67:S83–S88
Burgess EPJ, Malone LA, Christeller JT, Lester MT, Murray C, Philip BA, Phung MM, Tregidga EL
(2002) Avidin expressed in transgenic tobacco leaves confers resistance to two noctuid pests,
Helicoverpa armigera and Spodoptera litura. Transgenic Res 11:185–198
Burgess EPJ, Phillp BA, Christeller JT, Page NEM, Marshall RK, Wohlers MW (2008) Tri-trophic
effects of transgenic insect-resistant tobacco expressing a protease inhibitor or a biotin-binding
protein on adults of the predatory carabid beetle Ctenognathus novaezelandiae. J Insect
Physiol 54:518–528
Chakraborty S, Chakraborty N, Datta A (2000) Increased nutritive value of transgenic potato by
expressing a nonallergenic seed albumin gene from Amaranthus hypochondriacus. Proc Natl
Acad Sci USA 97:3724–3729
Christeller JT, Phung MM (1998) Changes in biotin levels in the leaves of two apple cultivars
during the season. N Z J Crop Horticult Sci 26:39–43
Christeller JT, Malone LA, Todd JH, Marshall RM, Burgess EPJ, Philip BA (2005) Distribution
and residual activity of two insecticidal proteins, avidin and aprotinin, expressed in transgenic
tobacco plants, in the bodies and frass of Spodoptera litura larvae following feeding. J Insect
Physiol 51:1117–1126
Collins PJ, Emery RN, Wallbank BE (2003) Two decades of monitoring and managing phosphine
resistance in Australia. Proceedings of the eighth international working conference on storedproduct protection, York, UK, 22–26 July 2002, pp 570–575
Coombs JJ, Douches DS, Li WB, Grafius EJ, Pett WL (2002) Combining engineered (Bt-cry3A)
and natural resistance mechanisms in potato for control of Colorado potato beetle. J Am Soc
Horticult Sci 127:62–68
Cooper SG, Douches DS, Grafius EJ (2006) Insecticidal activity of avidin combined with genetically
engineered and traditional host plant resistance against Colorado potato beetle (Coleoptera:
Chrysomelidae) larvae. J Econ Entomol 99:527–536
Dakshinamurti K (2005) Biotin – a regulator of gene expression. J Nutr Biochem 16:419–423
Ferreira SA, Pitz KY, Manshardt R, Zee F, Fitch M, Gonsalves D (2002) Virus coat protein transgenic
papaya provides practical control of papaya ringspot virus in Hawaii. Plant Dis 86:101–105
Fojta M, Billova S, Havran L, Pivonkova H, Cernocka H, Horakova P, Palecek E (2008) Osmium
tetroxide, 2,2 ‘-bipyridine: Electroactive marker for probing accessibility of tryptophan residues in proteins. Anal Chem 80:4598–4605
Gao AG, Hakimi SM, Mittanck CA, Wu Y, Woerner BM, Stark DM, Shah DM, Liang JH,
Rommens CMT (2000) Fungal pathogen protection in potato by expression of a plant defensin
peptide. Nat Biotechnol 18:1307–1310
Gatehouse LN, Markwick NP, Poulton J, Young VL, Ward VK, Christeller JT (2008) Expression
of two heterologous proteins depends on the mode of expression: comparison of in vivo and
in vitro methods. Bioprocess Biosyst Eng 31:469–475
Gleave AP, Mitra DS, Markwick NP, Morris BAM, Beuning LL (1998) Enhanced expression of
the Bacillus thuringiensis cry9Aa2 gene in transgenic plants by nucleotide sequence modification confers resistance to potato tuber moth. Mol Breeding 4:459–472
Hassan YI, Zempleni J (2006) Epigenetic regulation of chromatin structure and gene function by
biotin. J Nutr 136:1763–1765
Havran L, Billova S, Palecek E (2004) Electroactivity of avidin and streptavidin. Avidin signals at
mercury and carbon electrodes respond to biotin binding. Electroanalysis 16:1139–1148
Hood EE, Witcher DR, Maddock S, Meyer T, Baszczynski C, Bailey M, Flynn P, Register J,
Marshall L, Bond D, Kulisek E, Kusnadi A, Evangelista R, Nikolov Z, Wooge C, Mehigh RJ,
Hernan R, Kappel WK, Ritland D, Li CP, Howard JA (1997) Commercial production of avidin
from transgenic maize: characterization of transformant, production, processing, extraction
and purification. Mol Breed 3:291–306
Hood EE, Kusnadi A, Nikolov Z, Howard JA (1999) Molecular farming of industrial proteins
from transgenic maize. In: Chemicals via higher plant bioengineering, vol. 464, Kluwer/
Plenum, New York, pp 127–147
1
Avidin and Plant Biotechnology to Control Pests
19
Humbert N, Zocchi A, Ward TR (2005) Electrophoretic behavior of streptavidin complexed to a
biotinylated probe: a functional screening assay for biotin-binding proteins. Electrophoresis
26:47–52
Hytonen VP, Laitinen OH, Grapputo A, Kettunen A, Savolainen J, Kalkkinen N, Marttila AT, Nordlund
HR, Nyholm TKM, Paganelli G, Kulomaa MS (2003) Characterization of poultry egg-white avidins and their potential as a tool in pretargeting cancer treatment. Biochem J 372:219–225
Kizek R, Masarik M, Kramer KJ, Potesil D, Bailey M, Howard JA, Klejdus B, Mikelova R, Adam V,
Trnkova L, Jelen F (2005) An analysis of avidin, biotin and their interaction at attomole levels
by voltammetric and chromatographic techniques. Anal Bioanal Chem 381:1167–1178
Kothapalli N, Camporeale G, Kueh A, Chew YC, Oommen AM, Griffin JB, Zempleni J (2005)
Biological functions of biotinylated histones. J Nutr Biochem 16:446–448
Kramer KJ, Morgan TD, Throne JE, Dowell FE, Bailey M, Howard JA (2000) Transgenic avidin
maize is resistant to storage insect pests. Nat Biotechnol 18:670–674
Krizkova S, Hrdinova V, Adam V, Burgess EPJ, Kramer KJ, Masarik M, Kizek R (2008) Chipbased CE for avidin determination in transgenic tobacco and its comparison with square-wave
voltammetry and standard gel electrophoresis. Chromatographia 67:S75–S81
Levinson ZH, Bergmann ED (1959) Vitamin deficiencies in the housefly produced by antivitamins.
J Insect Physiol 3:293–305
Limoges B, Degrand C (1996) Ferrocenylethyl phosphate: An improved substrate for the detection
of alkaline phosphatase by cathodic stripping ion-exchange voltammetry. Application to the
electrochemical enzyme affinity assay of avidin. Anal Chem 68:4141–4148
Lis H, Sharon N (1993) Protein glycosylation – structural and functional-aspects. Eur J Biochem
218:1–27
Lucca P, Hurrell R, Potrykus I (2001) Fighting iron deficiency anemia with iron-rich rice. J Am
Coll Nutr 21:184S–190S
MacDonald SM, Roscoe SG (1997) Electrochemical oxidation reactions of tyrosine, tryptophan
and related dipeptides. Electrochim Acta 42:1189–1200
Malone LA, Burgess EP, Mercer CF, Christeller JT, Lester MT, Murray C, Phung MM, Philip BA,
Tregidga EL, Todd JH (2002) Effects of biotin-binding proteins on eight species of pasture
invertebrates. N Z Plant Prot 55:411–415
Markwick NP, Christeller JT, Docherty LC, Lilley CM (2001) Insecticidal activity of avidin and
streptavidin against four species of pest Lepidoptera. Entomol Exp Appl 98:59–66
Markwick NP, Docherty LC, Phung MM, Lester MT, Murray C, Yao J-L, Mitra DS, Cohen D,
Beuning LL, Kutty-Amma S, Christeller JT (2003) Transgenic tobacco and apple plants
expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber
moth and lightbrown apple moth, respectively. Transgenic Res 12:671–681
Markwick NP, Docherty LC, Phung MM, Lester MT, Murray C, Yao J-L, Mitra DS, Cohen D,
Beuning LL, Kutty-Amma S, Christeller JT (2004) Transgenic tobacco and apple plants
expressing biotin-binding proteins are resistant to two cosmopolitan insect pests, potato tuber
moth and lightbrown apple moth, respectively. Transgenic Res 12:671–681. DOI:
10.1023/B:TRAG.0000005103.83019.51
Martin H, Murray C, Christeller J, McGhie T (2008) A fluorescence polarization assay to quantify
biotin and biotin-binding proteins in whole plant extracts using Alexa-Fluor 594 biocytin. Anal
Biochem 381:107–112
Masarik M, Kizek R, Kramer KJ, Billova S, Brazdova M, Vacek J, Bailey M, Jelen F, Howard JA
(2003) Application of avidin-biotin technology and adsorptive transfer stripping square-wave
voltammetry for detection of DNA hybridization and avidin in transgenic avidin maize. Anal
Chem 75:2663–2669
Meiyalaghan S, Takla MFG, Jaimess OO, Shang Y, Davidson MM, Cooper PA, Barrell PJ, Jacobs
JME, Wratten SD, Conner AJ (2005) Evaluation of transgenic approaches for controlling tuber
moth in potatoes. Commun Agric Appl Biol Sci 70:641–650
Miura K, Takaya T, Koshiba K (1967) Effect of biotin deficiency on biosynthesis of fatty acids in
a blowfly Aldrichina grahami during metamorphosis under aseptic conditions. Archiv Int
Physiol Biochim 75:65–76
20
H. Martin et al.
Morgan TD, Oppert B, Czapla TH, Kramer KJ (1993) Avidin and streptavidin as insecticidal and
growth-inhibiting dietary proteins. Entomol Exp Appl 69:97–108
Murray C, Sutherland PW, Phung MM, Lester MT, Marshall RK, Christeller JT (2002) Expression
of biotin-binding proteins, avidin and streptavidin, in plant tissues using plant vacuolar targeting
sequences. Transgenic Res 11:199–214
Murray-Kolb LE, Takaiwa F, Goto F, Yoshihara T, Theil EC, Beard JL (2002) Transgenic rice is
a source of iron for iron-depleted rats. J Nutr 132:957–960
Nagadhara D, Ramesh S, Pasalu IC, Rao YK, Sarma NP, Reddy VD, Rao KV (2004) Transgenic
rice plants expressing the snowdrop lectin gene (gna) exhibit high-level resistance to the whitebacked planthopper (Sogatella furcifera). Theor Appl Genet 109:1399–1405
Nayak MK, Collins PJ (2008) Influence of concentration, temperature ana humidity on the toxicity of phosphine to the strongly phosphine-resistant psocid Liposcelis bostrychophila Badonnel
(Psocoptera: Liposcelididae). Pest Manage Sci 64:971–976
Palecek E, Postbieglova I (1986) Adsorptive Stripping voltammetry of biomacromolecules with
transfer of the adsorbed layer. J Electroanal Chem 214:359–371
Patterson SD (1994) From electrophoretically separated protein to identification – strategies for
sequence and mass analysis. Anal Biochem 221:1–15
Petrlova J, Krizkova S, Supalkova V, Masarik M, Adam V, Havel L, Kramer KJ, Kizek R (2007a)
The determination of avidin in genetically modified maize by voltammetric techniques. Plant
Soil Environ 53:345–349
Petrlova J, Masarik M, Potesil D, Adam V, Trnkova L, Kizek R (2007b) Zeptomole detection
of streptavidin using carbon paste electrode and square-wave voltammetry. Electroanalysis
19:1177–1182
Rajendran S (2002) Postharvest pest losses. In: Pimentel D (ed) Encyclopedia of pest management.
Marcel Dekker, New York, pp 654–656
Rodriguez-Melendez R, Zempleni J (2003) Regulation of gene expression by biotin (Review).
J Nutr Biochem 14:680–690
Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA (1988)
Primer-directed enzymatic amplification of DNA with a thermostable DNA-polymerase.
Science 239:487–491
Saxena SC, Kaul S (1974) Qualitative vitamin requirements of Oryzaephilus-Mercator Fauvel and
their deficiency effects on survival and growth of F1-progeny. Archiv Int Physiol Biochim
Biophys 82:49–54
Shellhammer J, Meinke D (1990) Arrested embryos from the bio1 auxotroph of Arabidopsis thaliana
contain reduced levels of biotin. Plant Physiol 93:1162–1167
Sinden SL, Sanford LL, Cantelo WW, Deahl KL (1986) Leptine glycoalkaloids and resistance to
the Colorado potato beetle (Coleoptera, Chrysomelidae) in Solanum-Chacoense. Environ Entomol
15:1057–1062
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gelelectrophoresis. J Mol Biol 98:503–517
Spiro RG (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease
implications of glycopeptide bonds. Glycobiology 12:43R–56R
Sugawara K, Hoshi S, Akatsuka K, Tanaka S, Nakamura H (1996a) Electrochemical evaluation of
avidin-biotin interaction using N-iodoacetyl-N-biotinylhexylenediamine. Bioelectrochem
Bioenerg 39:309–312
Sugawara K, Yamauchi Y, Hoshi S, Akatsuka K, Yamamoto F, Tanaka S, Nakamura H (1996b)
Accumulation voltammetry of avidin and biotin using a biotin labeled with Nile Blue A.
Bioelectrochem Bioenerg 41:167–172
Sugawara K, Kato R, Shirotori T, Kuramitz H, Tanaka S (2002) Voltammetric behavior of avidin–
biotin interaction at a biotin/thionine modified Au electrode. J Electroanal Chem 536:93–96
Sugawara K, Shirotori T, Hirabayashi G, Kamiya N, Kuramitz H, Tanaka S (2004) Voltammetric
investigation of avidin–biotin complex formation using an electroactive bisbiotinyl compound.
Anal Chim Acta 523:75–80
1
Avidin and Plant Biotechnology to Control Pests
21
Sugawara K, Kamiya N, Hirabayashi G, Kuramitz H (2005) Voltammetric homogeneous binding
assay of biotin without a separation step using iminobiotin labeled with an electroactive compound. Anal Sci 21:897–900
Tomschik M, Havran L, Palecek E, Heyrovsky M (2000) The “presodium” catalysis of electroreduction of hydrogen ions on mercury electrodes by metallothionein. An investigation by constant current derivative stripping chronopotentiometry. Electroanalysis 12:274–279
Torres JB, Ruberson JR, Whitehouse M (2009) Transgenic cotton for sustainable pest management: a review. E. Lichtfouse (ed.), Organic Farming, Pest Control and Remediation of Soil
Pollutants, Sustainable Agriculture Reviews 1, 15–53. DOI10.1007/978-1-4020-9654-9_4
Vilches-Flores A, Fernandez-Mejia C (2005) Effect of biotin upon gene expression and metabolism. Rev Invest Clin 57:716–724
Williams GJ, Domann S, Nelson A, Berry A (2003) Modifying the stereochemistry of an enzymecatalyzed reaction by directed evolution. Proc Natl Acad Sci U S A 100:3143–3148
Ye XD, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potrykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science
287:303–305
Yoza K, Imamura T, Kramer KJ, Morgan TD, Nakamura S, Akiyama K, Kawasaki S, Takaiwa F,
Ohtsubo K (2005) Avidin expressed in transgenic rice confers resistance to the stored-product
insect pests Tribolium confusum and Sitotroga cerealella. Biosci Biotechnol Biochem
69:966–971
Zempleni J (2005) Uptake, localization, and noncarboxylase roles of biotin. Annu Rev Nutr
25:175–196
Zhu YC, Adamczyk JJ, West S (2005) Avidin, a potential biopesticide and synergist to Bacillus
thuringiensis toxins against field crop insects. J Econ Entomol 98:1566–1571
Ziegler R, Engler DL, Davis NT (1995) Biotin-containing proteins of the insect nervous-system,
a potential source of interference with immunocytochemical localization procedures. Insect
Biochem Mol Biol 25:569–574
Chapter 2
Cover Crops for Sustainable Agrosystems
in the Americas
Johannes M.S. Scholberg, Santiago Dogliotti, Carolina Leoni,
Corey M. Cherr, Lincoln Zotarelli, and Walter A.H. Rossing
Abstract Rapid depletion of global fertilizer and fossil fuel reserves, combined
with concerns about global warming, have resulted in increased interest in alternative
strategies for sustaining agricultural production. Moreover, many farmers are being
caught in a vicious spiral of unsustainability related to depletion and degradation of
land and water resources, increasing labor and input costs, and decreasing profit
margins. To reduce their dependence on external inputs and to enhance inherent soil
fertility, farmers, thus, may opt to employ farm-generated renewable resources,
including the use of cover crops. However, perceived risks and complexity of
cover-crop-based systems may prevent their initial adoption and long-term use. In
this review article, we provide a historic perspective on cover-crop use, discuss their
current revival in the context of promotion of green technologies, and outline key
selection and management considerations for their effective use.
Based on reports in the literature, we conclude that cover crops can contribute to
carbon sequestration, especially in no-tillage systems, whereas such benefits may
be minimal for frequently tilled sandy soils. Due to the presence of a natural soil cover,
they reduce erosion while enhancing the retention and availability of both nutrients
J.M.S. Scholberg (*) and W.A.H. Rossing
Biological Farming Systems, Wageningen University, Postbox 563, 6700 AN Wageningen,
The Netherlands
e-mail: johannes.scholberg@wur.nl
S. Dogliotti
Facultad de Agronomía, Universidad de la República, Avda. Garzón 780,
Código Postal 12900, Montevideo, Uruguay
C. Leoni
Instituto Nacional de Investigación Agropecuaria - Estación Experimental Las Brujas,
Ruta 48 km 10 Código Postal 90200, Rincón del Colorado – Canelones, Uruguay
C.M. Cherr
Dept. of Plant Sciences, University of California, Davis, CA95616, USA
L. Zotarelli
Agricultural and Biological Engineering Dept, University of Florida, 234 Fraziers-Rogers Hall,
Gainesville, FL32611, USA
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_2, © Springer Science+Business Media B.V. 2010
23
24
J.M.S. Scholberg et al.
and water. Moreover, cover-crop-based systems provide a renewable N source, and
can also be instrumental in weed suppression and pest management in organic production systems. Selection of species that provide multiple benefits, design of sound
crop rotations, and improved synchronization of nutrient-release patterns and subsequent crop demands, are among the most critical technical factors to enhance the
overall performance of cover-crop-based systems. Especially under adverse conditions, use of mixtures with complementary traits enhances their functionality and
resilience. Since traditional research and extension approaches tend to be unfit for
developing suitable cover-crop-based systems adapted to local production settings,
other technology development and transfer approaches are required. The demonstration of direct benefits and active participation of farmers during system design,
technology development, and transfer phases, were shown to be critical for effective
adaptation and diffusion of cover-crop-based innovations within and across farm
boundaries. In conclusion, we would like to state that the implementation of suitable
policies providing technical support and financial incentives to farmers, to award
them for providing ecological services, is required for more widespread adoption
of cover crops.
Keywords Cover crops • green technologies • management • sustainable agro
systems • carbon sequestration Americas • pest control • tillage • rotation • weeds •
nematode • crimson clover • winter rye • black oats • living mulch • citrus • broccoli
• forage • ecological service • adapation • green manure
Abbreviation
SOM
soil organic matter
2.1 Introduction
“Cover crops” are herbaceous plants that alternate commercial crops during fallow
periods to provide a favorable soil microclimate, minimize soil degradation, suppress weeds, and enhance inherent soil fertility (Sarrantonio and Gallandt 2003;
Sullivan 2003; Anderson et al. 2001; Giller 2001). “Green manures” are cover
crops primarily used as a soil amendment and nutrient source for a subsequent crop
(Giller 2001). “Living mulches” are cover crops grown simultaneously with commercial crops that provide a living mulch layer throughout the season (Hartwig and
Ammon 2002). For the purpose of this review, we will not distinguish among these
uses, and use the term cover crop in its broadest context instead.
Historically, cover crops have been effective in closing nutrient cycles and were
integral part of food production systems that gave rise to modern agriculture
(Drinkwater and Snapp 2007; McNeill and Winiwarter 2004; Pieters 1927). However,
2
Cover Crops for Sustainable Agrosystems in the Americas
25
during the second part of the twentieth century, the “contemporary agricultural revolution” resulted in an uncoupling of C and N cycles (Drinkwater and Snapp 2007;
Mazoyer and Roudart 2006). As an integral part of the “agricultural revolution”
process, the use of inorganic fertilizer greatly increased, since these materials provide
growers with a concentrated and custom-designed nutrient source (Smil 2001).
The contemporary agricultural revolution, thus, directly contributed to an erosion
of traditional techniques for sustaining inherent soil fertility, including the use of
cover crops (Baligar and Fageria 2007; Sarrantonio and Gallandt 2003; Gliessman
et al. 1981). Farmers throughout the Americas are increasingly being caught in a
vicious spiral of unsustainability related to depletion and degradation of land and
water resources, increasing labor and input costs, and decreasing profit margins
(Cherr et al. 2006b; Dogliotti et al. 2005). In many cases, farmers were forced to
enhance family income via intensification, specialization, and production of cash
crops, or alternatively, abandon their operations (Dogliotti et al. 2005).
With current concerns related to global warming, rapid depletion of fertilizers
and fossil fuel reserves, agriculture is required to provide more diverse ecological
services and make more efficient use of natural/renewable resources (van der Ploeg
2008; Cherr et al. 2006b). Within this context, improved integration of the use of
cover crops may once again become the cornerstone of sustainable agroecosystems
(Baligar and Fageria 2007). However, the development of functional cover-crop-based
systems will require a more integrated and system-based approach, rather than
reinstating traditional production practices. The scope of this paper is to (i) provide
a historic perspective on the use of cover-crop-based systems in agroecosystems;
(ii) document specific services and benefits provided by cover crops with special
reference to their use in the Americas; (iii) discuss selection procedures for cover
crops; (iv) outline key management aspects that facilitate integration and performance
of cover crops into agrosystems; (v) discuss potential limitations and challenges
during the design and implementation of cover-crop-based systems.
2.2 Historic Perspective
Starting at the cradle of agriculture in southwest Asia, farmers utilized leguminous
crops, including peas and lentils, to restore inherent soil fertility and to sustain grain
crop production (McNeill and Winiwarter 2004). In England, fallows were replaced
by clovers in grain–turnip production systems to improve soil fertility, whereas in
the Americas, beans were used for this purpose (Russell 1913). During the early
1800s, continuous population growth and urbanization required the use of more
concentrated forms of fertilizer and mined mineral guano deposits to offset declining
inherent soil fertility in Western Europe and New World, but this resource was both
scarce and relatively expensive (McNeill and Winiwarter 2004). During the 1870s,
mucuna (Mucuna pruriens) was introduced in Florida as a forage crop and by 1897
it was used by hundreds of citrus growers as an affordable alternative to improve
soil fertility while it was also used as a forage crop (Crow et al. 2001; Buckles et al.
26
J.M.S. Scholberg et al.
1998; Tracey and Coe 1918). Mucuna was introduced in Guatemala during the
1920s as a forage source and as a rotational crop for maize-based systems. Its use
spontaneously spread and was adopted by farmers in neighboring countries as well
(Giller 2001). In Uruguay, vetch (Vicia villosa Roth) and oats (Avena sativa L.)
were introduced as green manures in vineyards around 1960, but due to increased
supply of inexpensive fertilizer and lack of suitable cultivation tools, this practice
was discontinued (Selaya Garvizu 2000).
Annual winter cover crops were integral part of many North American cropping
systems during the first part of the last century (Pieters 1927). However, their use
was gradually abandoned due to the availability of inexpensive synthetic fertilizer
during the 1950s, which provided growers with concentrated nutrient sources that
could be easily managed (Tonitto et al. 2006; Smil 2001). As a result, soil fertility
strategies shifted from building SOM and inherent soil fertility via sound crop rotations and supplementary use of (in)organic nutrient sources, to a system dominated
by external inputs used to boast labile nutrient pools and crop yields (Drinkwater
and Snapp 2007). Moreover, externalities associated with the excessive use of agrochemicals were typically ignored while inherent system’s functions and services
were gradually being lost (Cherr et al. 2006b). Additionally, the shift toward largescaled and highly specialized operations diminished inherent diversity and resilience
of local agricultural production systems (van der Ploeg 2008; Shennan 2008; Baligar
and Fageria 2007; Cherr et al. 2006b).
In terms of awareness of potential negative aspects of industrialized agriculture,
the “great dust bowl” occurring in the USA in the 1930s, gave rise to increased
emphasis on soil conservation, including the use of cover crops (Hartwig and Ammon
2002). During the 1970s, externalities associated with maintaining large labile nutrient pools became a major concern and practices were proposed to reduce environmental impacts, including the use of cover crops (Drinkwater and Snapp 2007; Mays
et al. 2003; Dabney et al. 2001). Although agricultural development resulted in an
unprecedented increase in productivity, it also promoted increased specialization and
required substantial capital investments, while “real” prices of agricultural commodities dropped by a factor 2–4 between 1950 and 2000. Especially small farmers were
not able to adapt to this transition and the majority of them was forced to abandon
farming (Mazoyer and Roudart 2006). Moreover, in many developing regions, green
revolution technologies were less effective in more adverse, risk-prone, and resourcelimited production environments (Shennan 2008; El-Hage Scialabba and Hattam
2008). During the 1960s a modified form of the agricultural revolution occurred in
Latin America which involved investments in local infrastructure, access to loans,
improved inputs, and price subsidies (Mazoyer and Roudart 2006). However, in
Brazil, increased mechanization and intensification of agriculture in hilly regions
resulted in rampant erosion and soil degradation, which undermined the inherent
production capacity of local production systems (Prado Wildner et al. 2004).
During the 1980s, adoption of cover crops as part of conservation technologies
increased exponentially by farmers in southern Brazil (Calegari 2003; Landers 2001).
This process has resulted in a gradual reversal of the degradation of the natural production base since farmers were able to partially restored SOM levels and also reduce
2
Cover Crops for Sustainable Agrosystems in the Americas
27
their dependence on external inputs. This kind of revolutionary success story inspires
confidence in potential role of cover-crop-based technology to reverse the downward
spiral of unsustainability that still prevails in many regions. This unprecedented successful expansion of no-tillage technology expansion in this region was clearly driven
by farmers who actively engaged in technology development and transfer, and combined with favorable government policies, this greatly facilitated the scaling out
process on a more regional scale. On the other hand, the use of no-tillage and/or cover
crops by commercial vegetable growers in the SE USA was limited. This was related
to the high crop value and risk-averse behavior of conventional producers (Phatak
et al. 2002). However, increased concerns related to environmental quality, energy
use, and global warming, have resulted in a shift toward resource preservation with
an increased focus on sustainability and/or ecological-based (organic) production
systems (Shennan 2008; Ngouajio et al. 2003; Hartwig and Ammon 2002; Lu et al.
2000). In summary, although cover crops were abandoned due to green revolution
technologies, due to the current interest in green technologies, they are once more
becoming the cornerstone of sustainable agrosystems (Baligar and Fageria 2007;
Cherr et al. 2006b; Sullivan 2003; Phatak et al. 2002; Shennan 1992).
2.3 Services and Benefits
Regarding the use of cover crops, it is important to distinguish “ecosystem goods”
from “ecosystem services” (Shennan 2008). From a producer’s perspective, cultivation of a cover crop may yield direct forage benefits and improved grain yields in
integrated systems, while from a policy view its use also provides environmental
benefits, e.g., erosion control and clean drinking water. Adoption of cover-cropbased systems tends to be strongly influenced by the perception of different stakeholders of what (direct) benefits cover crops will provide under local conditions and
increased awareness of such services is, thus, critical (Anderson et al. 2001). An
overview of a number of these direct and indirect services is provided in Fig. 2.1,
while specific aspects will be discussed in more detail below.
2.3.1 Soil Organic Matter
Maintaining soil organic matter (SOM) is critical for sustaining soil quality and
crop productivity, especially in the absence of external inputs (Fageria et al. 2005;
Sarrantonio and Gallandt 2003). Cover crops may enhance SOM content in the soil
provided that SOM addition rate exceeds SOM breakdown (Calegari 2003; Sullivan
2003). The use of cover crops, the presence of crop residues and SOM, have all been
linked to improved soil aggregation and soil structure and enhanced water infiltration,
retention, drainage, and soil aeration, thus, reducing runoff and erosion (Sainju et al.
2007; Fageria et al. 2005; Dabney et al. 2001; Miyao and Robins 2001; Creamer
28
J.M.S. Scholberg et al.
Process
Canopy
functions
Cover
crops
Root
functions
Primary effects
Secondary effects
• SOM (+)
• Carbon sequestration (+)
• Production costs (+/-)
Biomass
production
• Food, fuel, forage (+)
• Soil amendment (+)
• Mulch layer (+)
Nutrient
storage
• Soil nutrient supply (+)
Soil cover
• Weed suppression (+)
• Wind/water erosion (-)
• Runoff (-)
• Soil temperature (-)
• Soil moisture (+)
• Crop production (+)
• Nutrient leaching (-)
• Resource depletion (-)
• SOM (+)
• Crop water use effic. (+)
• Crop production (+)
• Sediment losses (-)
• Nutrient leaching (-)
Ecological
functions
• Biodiversity (+)
• Habitat (+)
• Pest dispersal (-)
• Beneficials (+)
• Pests (-/+)
• Crop production (+/-)
Soil/nutrient
retention
• Wind/water erosion (-)
• Nutrient retention(+)
• SOM (+)
• Crop production (+)
• Environm. impacts (-)
• Water infiltration (+)
• Water retention (+)
• Soil compaction (-)
• Runoff (-)
• Nutrient availability (+)
• Weed suppression (+)
• Nitrogen fixation (+)
• Mycorrhizalsymbiosis(+)
• SOM (+)
• Crop production (+)
• Flooding (-)
• Groundwater recharge (+)
• Environm. impacts (-)
Root growth
& exudates
Root
symbiosis
• Nutrient imbalance (-)
• SOM (+)
• Crop production (+)
Fig. 2.1 Schematic overview of cover crops and corresponding primary and secondary effects on
different agroecological services. SOM: soil organic matter
et al. 1996b; Gulick et al. 1994; Derpsch et al. 1986). Increasing SOM also favors
root growth, available water capacity (AWC), effective soil water storage, and
potential yield in water-limiting environments (Sustainable Agricultural Network
2007; Fageria et al. 2005; Anderson et al. 2001; Derpsch et al. 1986). Hudson
(1994) reviewed historic data sets on the effect of SOM on AWC and showed that
AWC was increased by 2.2–3.5% for each percent increase in SOM. Increased SOM
also greatly improves cation retention, and combined with complexation and mineralization of nutrients, it, thus, greatly improves crop nutrient availability (Anderson
et al. 2001). Cover-crop residues were shown to enhance the benefits of no-tillage
on aggregate stability, microbial biomass, SOM, and soil enzymes (Roldan et al.
2003; Zotarelli et al. 2005a, b, 2007; Fageria et al. 2005; Calegari 2003). Amado et al.
(2006) emphasized the importance of including leguminous cover crops in no-tillage
systems as a strategy for increasing carbon sequestration in tropical and subtropical
regions. However, for non-utrient limited systems and under adverse growth conditions, growing recalcitrant nonleguminous cover crops with a greater biomass
production, may be more effective in boasting SOM (Barber and Navarro 1994a).
Overall dry-matter production and nutrient accumulation by cover crops affects
their potential to increase SOM. The production capacity of cover crops is dictated by
genetic traits, including C3 versus C4 photosynthetic pathways, the ability of roots to
form symbiotic associations, canopy characteristics, tissue composition, and growth
duration. These traits, in turn, control crop radiation, water and nutrient use efficiencies,
2
Cover Crops for Sustainable Agrosystems in the Americas
29
and also provide limitations to how cover-crop-based systems will perform. A review
by Cherr et al. (2006b) showed that under optimal conditions, annual cover crop may
accumulate up to 4.4–5.6 Mg C ha−1 during a period of 3–5 months.
Overall decomposition of cover-crop residues is affected by (1) amount that is
applied; (2) biochemical composition; (3) physical properties as related to crop
development stage and/or termination practices; (4) soil texture, temperature, and
moisture conditions; (5) soil contact; (6) nutrient availability and fertilizer addition
(Balkcon and Reeves 2005; Sullivan 2003; Berkenkamp et al. 2002; Ma et al. 1999;
Honeycutt and Potaro 1990; Schomberg et al. 1994). The base temperature for
decomposition is assumed to be on the order of −2°C to 0°C, while decomposition
rates double when soil temperature increases by 9°C (Yang and Janssen 2002).
Decomposition is fastest at high temperatures (30–35°C), adequate moisture (e.g., at
field capacity), adequate N tissue levels (e.g. C:N ratios <25), and favorable lignin/N
ratios (Cherr et al. 2006b; Quemada et al. 1997). Under hot and humid conditions,
decomposition rates may be four to five times greater compared to temperate settings (Lal et al. 2000). Decomposition rates are on the order of 0.2, 0.05 and 0.0095
day−1 for glucose- versus cellulose- versus lignin-based carbon pools (Quemada
et al. 1997). Stems, which contain less N and more lignin and cellulose, thus, may
decompose up to five times slower compared to leaves (Cherr et al. 2006b).
The fraction remaining after 1 year (the effective SOM addition rate) may be relatively small (e.g. <0.1–0.4) depending on pedo-climatic conditions and residue properties (Yang and Janssen 2000). Compared to the more stable soil C-pool, the addition
of cover-crop residues to the stable SOM pool, thus, may be relatively small, since a
soil with 1% SOM contains 24 Mg C ha−1 in just the upper 0–30 cm. Additionally, as
discussed above, only a small fraction of the C from cover crops may be converted to
effective SOM, whereas most of it is lost during the decomposition process.
In Brazil soil C-enrichment, even under no-tillage, was only 10% of the
C-addition rate (Metay et al. 2007). In California, the use of cover-crop-based
no-tillage tomato system on a clay loam soil cover crops generated 1.8–2.3 Mg C
ha−1 year−1. After a period of 5 years, overall soil-C sequestration was 4.5 Mg C ha−1
compared to 3.8 Mg C−1 for standard tillage systems, while noncover-crop systems
showed a net loss of 0.1–0.4 Mg C ha−1 (Veenstra et al. 2007). Under these conditions,
crop carbon addition rate was more important than tillage management in terms of
SOM accumulation, where as in Brazil the opposite may be true (Metay et al. 2007;
Amado et al. 2006). Use of leguminous cover crop and/or fertilizers will result in a
decrease in C:N value of recently formed SOM compared to monocultures of gramineous cover crops (Ding et al. 2006). A biculture of hairy vetch (Vicia villosa Roth)
and rye (Secale cerale L.) was more effective in sequestering C compared to covercrop monocultures while adding fertilizer enhanced overall SOM accumulation
(Sainju et al. 2006). In India, continuous use of perennial cover crops in a coconut
plantation for 12 years greatly enhanced basal respiration, microbial C and N,
reduced C:N ratios of microbial biomass, while SOM values in the upper 20 cm
also increased by a factor 2–3 (Dinesh 2004; Dinesh et al. 2006).
Under the hot/humid weather conditions and sandy soils prevailing in Florida,
use of annual cover crops in a no-tillage sweet corn production system generated
30
J.M.S. Scholberg et al.
upto 7.2–9.6 Mg C ha−1 year−1. However, despite these high C addition rates, SOM
still declined from 1.4% (year 1) to 1.3% (year 2) which was related to the site
previously being under pasture (Cherr 2004). After 4 years of cover-crop-based
systems, SOM reached an equilibrium of about 1.2% in cover-crop-based systems,
while not adding any crop residues, combined with frequent tillage, resulted in a
decline in SOM to 0.8%. Under these conditions, alternating vegetable production
systems with semipermanent pastures, which tend to have higher effective C addition
rates, may be required to boast SOM values. This is in agreement with reports that
sod-forming grass-legume leys are more effective in enhancing SOM compared to
the use of annual green manures (Hansen et al. 2005; Sullivan 2003). However, for
production settings with more fine-textured soils, which is critical for occlusion
(protection) of soil organic matter (Zotarelli et al. 2007), the integrated use of cover
crops and no-tillage was shown to increase SOM in annual cropping systems as well
(Matus et al. 2008; Roldan et al. 2003; Sanchez et al. 2007; Amado et al. 2006;
Luna-Orea and Wagger 1996; Barber and Navarro 1994b).
Since changes in SOM are slow and may be masked by inherent variability, the
use of models may be useful. Simulations with models such as NDICEA (Van der
Burgt et al. 2006) allow improved assessment of how cover crops may affect SOM
trends over time. Using this model it was shown that for traditional vegetable cropping systems in Uruguay, SOM values decreased by 420–700 kg ha−1 year−1. Due
to erosion rates of 18–19 Mg ha−1 year−1 , total SOM loss amounted to 800–1,170
kg ha−1year−1 (Selaya Garvizu 2000). In cover-crop-based systems, approximately
4–5 Mg ha−1 year−1 crop residues were added, and SOM levels could be maintained
while soil erosion was reduced by 67% (Selaya Garvizu 2000).
2.3.2 Physical Functions
Cover crops will modify the microclimate by reducing kinetic energy of rainfall,
soil temperature fluctuations, wind speed, and crop damage associated with sand
blasting (Fageria et al. 2005; Bravo et al. 2004; Anderson et al. 2001; Dabney et al.
2001; Masiunas 1998). Their canopy and residues will diminish the impact of raindrops, thereby reducing soil crusting and erosion, while their stems and root system
also provides a physical barrier that can prevent sheet erosion and gully formation
(Sarrantonio and Gallandt 2003; Masiunas 1998; Derpsch et al. 1986). Their use on
sloping lands can provide a viable and labor-efficient alternative to the development
of stone embankments and terracing (Bunch 1996). Erosion control (as shown in
Fig. 2.2), thus, is one of the core services that cover crops provide (Prado Wildner
et al. 2004). Use of leguminous live mulches, thus, may reduce runoff and soil erosion by 50% and 97%, respectively (Hartwig and Ammon 2002). Cover crops, such
as deep-rooted radish, can penetrate compacted subsoil layers and prior root channels can enhance soil water infiltration, root penetration, soil water-holding capacity, and thus, crop water use efficiency of subsequent crops (Weil and Kremen 2007;
Sarrantonio and Gallandt 2003; Giller 2001). Cover crops provide a structural habitat
2
Cover Crops for Sustainable Agrosystems in the Americas
31
Fig. 2.2 Field demonstration of use of cover crop (left) to reduce soil degradation (right) in
Uruguay
for both beneficial insects and birds, and by reducing light levels and soil temperature
fluctuations at the soil surface, they also reduce weed germination (Bottenberg
et al. 1997; Bugg and Waddington 1994). Moreover, cover-crop residues conserve
soil moisture and favor beneficial fungi producing glomalin that, in turn, enhances
the formation of stable soil aggregates, water percolation, and retention (Sustainable
Agricultural Network 2007; Altieri 2002).
2.3.3 Soil Fertility
Cover crops and their residues accumulate and/or retain nutrients either by symbiotic
N fixation, uptake during growth, or immobilization after crop senescence. Thereby,
they enhance nutrient retention and recycling and reduce the risk of potential
nutrient-leaching losses by functioning as a “catch crop” (Cherr et al. 2006b;
Dabney et al. 2001). Cover-crop-derived nutrients are typically released gradually
over time, which may reduce the risk of toxicity, leaching, and thus, may enhance
nutrient efficiency compared to use of highly soluble inorganic fertilizers (Cherr
et al. 2006b). In many cases, actual yield benefits exceed those expected based merely
on cover-crop-derived nutrients, which may be related to cover crops providing a
much broader array of ecological services compared to the exclusive use of synthetic
fertilizer (Bhardwaj 2006). However, utilization of N released by cover crops can
also be poor if nutrient release is not synchronized with the crop demand of a
subsequent crop (Baijukya et al. 2006).
Leguminous crops provide supplementary nitrogen via symbiotic N fixation
and their relatively low C:N ratio also increases mineralization which reduces the
risk of N deficiency for subsequent and/or companion crops (Sanchez et al. 2007;
32
J.M.S. Scholberg et al.
Cherr et al. 2006b; Schroth et al. 2001). Use of leguminous cover crops, thus, provide
an on-farm renewable form of N, thereby, reducing energy cost associated with
production and transport of fertilizers (Cherr et al. 2006b). In organic systems, use
of leguminous cover crops also offset P accumulation and potential environmental
risks associated with the excessive use of animal manures (Cherr et al. 2006b), while
the use of a soil-building cover crop may also be required to meet certification requirements (Delate et al. 2003). Under favorable conditions, cover crops may accumulate
substantial amounts of N (150–328 kg N ha−1), with 31–93% of this N being derived
from biological N fixation (partially) offsetting N removal via harvesting of commercial crops (Cherr et al. 2006b; Giller 2001). Giller (2001) provided an overview
of reported N accumulation and fraction of N derived via symbiotic N fixation for
commonly used tropical legumes. Similar information for other cover crops and/
or nutrients may be obtained elsewhere (Cherr et al. 2006b; Fageria et al. 2005;
Calegari 2003).
Roots of cover crops also exude organic compounds which can enhance soil
microbial activity, mycorrhizal activity, soil structure, and nutrient availability
(Pegoraro et al. 2005; Calegari 2003; Dabney et al. 2001). Prolonged use of grassclover mixture or annual cover crops, in combination with no-tillage, may reduce
runoff and erosion, thereby reducing loss of fertile top soil and SOM, which in turn,
can further enhance soil water retention and nutrient use efficiency (Sanchez et al.
2007; Bunch 1996). Deep-rooted types such as rye (Secale cereal L.) and sunn
hemp (Crotalaria juncea L) can effectively scavenge nutrients from deep soil layers
and render them more readily available for subsequent crops (Wang et al. 2006;
Fageria et al. 2005; Calegari 2003; Sullivan 2003). Fast-growing and deep-rooting
cover crops such as winter rye, radish, and brassicas, deplete labile residual N pools
and are very effective in retaining nutrients (Vidal and Lopez 2005; Isse et al. 1999;
Dabney et al. 2001; Wyland et al. 1996). In Maryland, brassicas depleted residual
soil N up to a soil depth of 180 cm and took up more N compared to rye (Weil and
Kremen 2007). Leguminous cover crops have low C:N ratios and can release large
amounts of N instantaneously and their use, thus, may result in excessive N-leaching
especially on sandy soils (Avila 2006; Sainju et al. 2006).
2.3.4 Pest Management
2.3.4.1 Soil Ecology
In balanced ecosystems, pests are internally managed by natural enemies while
management practices should be geared toward favoring beneficial organisms rather
than erradicating pests (Sustainable Agriculture Network 2007) and promoting
disease-supression mechanisms (van Bruggen and Semenov 2000). During the past
decades, there has been increased concern in pesticide use in agriculture, especially
in intensively managed vegetable crops (Abdul-Baki et al. 2004; Masiunas 1998).
Effective use of cover crops may reduce herbicide use and cost associated with soil
2
Cover Crops for Sustainable Agrosystems in the Americas
33
fumigation (Abdul-Baki et al. 2004; Carrera et al. 2004) and they can reduce potential leaching of both nutrients and pesticides (Masiunas 1998; Wyland et al. 1996).
Moreover, cover-crop-based systems enhance ecological diversity, productivity,
and stability of agrosystems as well (Shenann 2008; Cherr et al. 2006b). Several
cultural practices such as crop rotation, cover crops, mulches, composts, and animal
manures affect SOM, disease supressiveness of soils, and thus, minimize both the
incidence and severity of soil-borne diseases.
2.3.4.2 Diseases
Cover crops suppress diseases by interfering with disease cycle phases such as
dispersal, host infection, disease development, propagation, population buildup, and
survival of the pathogen, in a number of ways. The presence of cover-crop mulches
minimizes pathogen dispersal via splashing, water runoff, and/or wind-borne processes (Cantonwine et al. 2007; Everts 2002; Ntahimpera et al. 1998; Ristaino et al.
1997). Organic residues also reduce the incidence and severity of soil-borne diseases
by inducing inherent soil suppressiveness, while excessive use of inorganic fertilizers
may cause nutrient imbalances and lower pest resistance (Altieri and Nicholls 2003).
When selecting cover crops, information on how effective these crops are in hosting
or suppressing pathogens is needed (Abawi and Widmer 2000). The host–nonhost–
tillage system interaction aspect should, thus, be considered carefully (Colbach et al.
1997). Saprophytic pathogens survive on cover-crop residues and this effect is also
greatly affected by tillage. In some cases, the cover crops can be a host for the pathogen but will not develop any disease symptoms itself. Fusarium oxysporum f.sp.
phaseoli may prevail in a leguminous cover crops when rotated with beans (Dhingra
and Coelho Netto 2001). When cover crops are not properly decomposed, pathogen
population such as Phytium spp. increase, causing severe epidemics (Manici et al
2004). Incorporation of crop residues greatly affect soil microbial populations and
can increase pathogen inhibitory activity as was shown for Phytopthora root rot in
alfalafa, Verticillium wilt in potato and Rhizoctonia solani root rot by changes in resident Streptomyces spp. community (Mazzola 2004; Wiggins and Kinkel 2005a, b).
Incorporation of crop residues with or without tarping can provide soil disinfestation
via biochemical mechanisms (Blok et al. 2000; Gamliel et al. 2000). For example,
breakdown of Brassica residues containing glucosinolates resulted in the formation
of bio-toxins, including isothiocyanates, that provide (partial) control of diseases,
weeds, and parasitic nematodes (Weil and Kremen 2007). Cover crops also promote
disease supressiveness by favoring certain groups of the resident soil microbial community, as related to the interactive effects of root exudates and root affinity of different
crops on beneficial organisms (van Elsas et al. 2002; Mazzola 2004).
However, in some cases, cover crops increase disease incidence as was shown
for pathogens with a wide host range such as Sclerotium rolfsii (Gilsanz et al. 2004;
Jenkins and Averre 1986; Taylor and Rodríguez-Kábana 1999b, Widmer et al.;
2002). The use of cover-crop residues for mulching enhanced disease suppression
of Sclerotinia sclerotiorum – beans pathosystem (Ferraz et al. 1999), while in a
34
J.M.S. Scholberg et al.
no-tillage small grain system, they promoted Rhizoctonia solani (Chung et al. 1988).
Brassica species were quite effective in controlling Sclerotinia diseases in lettuce,
whereas oats and broad beans did not provide any disease control (Chung et al.
1988). Verticilium wilt incidence in potato was reduced when potato was grown after
corn or sudangrass compared to planting it after rape or winter peas (Davis et al.
1996). Cover-crop-based systems (leguminous vs brassicas) had no effect on the
Fusarium incidence in processing tomatoes in California compared to control
systems. Although they showed yield benefits compared to noncover crop controls,
yields were still lower compared to the use of Metham which was more effective in
controlling Fusarium (Miyao et al. 2006).
2.3.4.3 Insects
Cover crops and their residues also reduce insect pest populations as was reported
for a range of insects, including aphids, beetles, caterpillars, leafhoppers, moths, and
thrips (detailed reviews are provided by Sarrantonio and Gallandt 2003; Masiunas
1998). This is related to changes in biophysical soil conditions, formation of protective niches for beneficial organisms, release of allelochemicals, and changes in soil
ecology (Tillman et al. 2004; Sarrantonio and Gallandt 2003). Cover crops also
increase biodiversity by creating more favorable conditions for free-living bactivores
and fungivors, and other predators. Combined with reduced proliferation of pests,
the presence of cover crops (residues) hampers dispersal of visual and olfactory
clues emitted by host crops, thus, resulting in more effective insect pest suppression
as well (Tillman et al. 2004; Masiunas 1998). However, in other cases, cover crops
provide a shelter for insect pests as well (Masiunas 1998).
2.3.4.4 Nematodes
Reduction of nematodes by cover crops is well-documented (Abawi and Widmer
2000; Taylor and Rodríguez-Kábana 1999a; Widmer et al. 2002). Several grassy
and leguminous cover crops, including Crotalaria, Mucuna, and Tagetes species,
were shown to be nonhost or a suppressor of selected parasitic nematodes (Wang
et al. 2007; Crow et al. 2001; McSorley 2001). Crop rotations, including such species,
disrupt the life cycle of parasitic nematodes and reduce the risk of breakdown of
inbred nematode resistance of commercial crops (McSorley 2001). In some cases,
nematode-suppression action is related to the beneficial effects of cover-crop residues
on predatory nematodes and nematode-trapping fungi (Cherr et al. 2006b). However,
no cover crop will function as a nonhost for all parasitic nematodes, while in several
cases, cover crops were shown to favor the growth of parasitic nematodes as well
(Isaac et al. 2007; Sanchez et al. 2007; Crow et al. 2001; Cherr et al. 2006b).
Reports on crops being a host versus nonhost may conflict at times, which can be
related to differences in pedo-climatic conditions, nematode races, and cover-crop
cultivars and thus, the results may need to be verified for local production settings.
2
Cover Crops for Sustainable Agrosystems in the Americas
35
2.3.4.5 Weeds
In organic systems, cost-effective weed control is the foremost production factor
hampering successful transition (Kruidhof 2008; Linares et al. 2008). Well-designed
cover-crop systems can reduce herbicide use and labor use for weed control, and
cover crops, thus, afford farmers with a cost-effective strategy for weed control,
which is a key deciding factor in their adaptive use (Gutiererez Rojas et al. 2004;
Anderson et al. 2001; Neill and Lee 2001; Teasdale and Abdul-Baki 1998; Bunch
1996; Barber and Navarro 1994a). Cover crops suppress weeds via resource competition, niche disruption, and release of phytotoxins from both root exudates and
decomposing residues, thereby minimizing seed banks, and the germination, growth,
and reproduction of weeds (Kruidhof 2008; Moonen and Barberi 2006; Fageria
et al. 2005; Sarrantonio and Gallandt 2003). Their effectiveness in suppressing
weeds is affected by plant density, initial growth rate, aboveground biomass, leaf
area duration, persistence of residues, and time of planting of a subsequent crop
(Kruidhof 2008; Linares et al. 2008; Sarrantonio and Gallandt 2003; Cassini 2004;
Dabney et al. 2001).
Although cover crops greatly reduced weed growth in conventional vegetablecropping systems, in some cases applying herbicide may still be required to minimize the risk of yield reductions (Teasdale and Abdul-Baki 1998). Annual cover
crops such as mucuna may also be used to control perennial weeds, provided that
they effectively shade out these weeds just prior to weeds starting replenishing
their storage organs (e.g., rhizomes) with assimilates (Teasdale et al. 2007).
Repeated use of annual cover crops combined with no-tillage in organic systems
did not control grassy weeds (Treadwell et al. 2007). Their continuous use can
also result in a shift toward perennial weeds which can be addressed by alternating crop systems with pastures (M. Altieri, 2008). Use of cover-crop mixtures
with complementary canopy characteristics (e.g., rye and clover as shown in
Fig. 2.3) and differential root traits (e.g., fibrous vs deep tap roots) will provide
superior cover-crop performance and thus, more effective weed control (Linares
et al. 2008; Drinkwater and Snapp 2007; Masiunas 1998). Use of a “cover crop
weed index” (ratio of aboveground dry weights of cover crops and weeds) was
shown to be a useful tool for assessing weed-suppression capacity of cover crops
(Linares et al. 2008).
Mowing in orchards can provide more effective weed control when combined
with a grassy vegetation compared to its use with annual legumes (Matheis and
Victoria Filho 2005). Use of mowed leguminous live mulches in an organic wheat
system reduced weed growth by 65–86% but grain yields were only a fraction of
those in weed-free controls possibly due to resource competition between cover
crops and the wheat crop (Hiltbrunner et al. 2007). Leguminous cover crops may
have a competitive edge on weeds under N-limiting conditions, whereas the use of
repeating mowing may be effective to control taller weeds for more fertile production sites.
Weed suppression by cover-crop residues is related to the effective soil coverage
which may be sustained for 30–75 days (as shown in Fig. 2.4). This depends on
36
J.M.S. Scholberg et al.
Fig. 2.3 Prostrate growth and flat-leaf angle of crimson clover complements more erect growth
characteristics of winter rye (left) and black oats (right) while these cereal crops also have higher initial
growth and are thus more effective in retaining residual soil nutrients on sandy soils in Florida
Fig. 2.4 Use of mowed cowpea residue as a mulch in a subsequent no-tillage broccoli crop (left)
and forage radish as a live mulch in an organic citrus orchard (right) in Florida
decomposition as related to residue amount and biochemical properties, rainfall,
soil temperature, and weed pressure/vigor (Teasdale et al. 2004; Ruffo and Bollero
2003; Masiunas 1998; Creamer et al. 1996). Incorporation of residues reduces their
weed-suppression capacity due to increased light levels, transfer of dormant seeds
to the soil surface, and also results in increased breakdown and dilution of allelochemicals (Masiunas 1998). Rye and barley residues were effective in suppressing broadleaf
weeds, while hairy vetch residues enhanced weed growth (Creamer et al. 1996),
2
Cover Crops for Sustainable Agrosystems in the Americas
37
which may be related to their releasing nutrients (Teasdale et al. 2007), while rye was
less effective in suppressing grassy weeds (Masiunas 1998).
2.3.5 Food and Forage Production
Although food and forage production may not be the main purpose of cover-crop
use, some systems may also provide products for human consumption, grazing,
and/or to produce fodder as was reported for, example, Canavalia ensifomis, Dilochis
lablab, Avena strigosa, Vicia villosa (Nyende and Delve 2004; Pieri et al. 2002;
Anderson et al. 2001). Examples of cover crops suited for human consumption
include Cajanus cajan (pigeon pea), Dolichos lablab, and cowpea (Vigna cinsensis).
Integrating livestock components into cover-crop-based systems can improve bioeconomic efficiencies, profits, and human health. Potential applications may include
the use of cover crops to regenerate degraded pasture land, improvement of the animal
diet, and enhancement of the intensification of small-scale farming systems (Anderson
et al. 2001). Ironically, mucuna may have been introduced in Central America to be
used as forage crop for mules employed in banana plantations (Anderson et al.
2001). In such integrated systems, (leguminous) cover crops may also provide
(high-quality) forages, but unless manures are internally recycled, this may reduce
soil improvement services and yield benefits provided by the cover crops (Anderson
et al. 2001). As an example, cattle grazing of mucuna prior to corn planting reduced
its effectiveness in suppressing weeds and improving corn yields (BernandinoHernandez et al. 2006).
2.3.6 Economic Benefits
In terms of conventional economics, key considerations are seed and labor costs
which tend to account for the largest cost factors of cover-crop-based systems
(Sullivan 2003; Lu et al. 2000). The seed costs of leguminous crops are twice as
high as small grains, but residues of grains have high C:N ratios and may require
additional N application of 25–35 kg N ha−1 to reduce the risk of N immobilization
which may offset potential seed cost savings (Sustainable Agriculture Network
2007). In South Georgia, self-reseeding systems of crimson clover were developed
in rotation with cotton. In this case, the absence of additional tillage and seed costs
combined with the automatic senescence of the cover crop prior to the maturation
of the cotton crop resulted in cost-effective systems (Cherr et al. 2006b; Dabney
et al. 2001).
Several studies documented significant yield benefits derived from the use of
cover crops (Sanchez et al. 2007; Avila 2006; Cherr et al. 2006b, c; Fontanetti et al.
2006; Abdul-Baki et al. 2004; Neill and Lee 2001; Derpsch and Florentin 1992).
These yield increases may be related to N benefits, improved soil structure and water
38
J.M.S. Scholberg et al.
retention, and reduced incidence of pests. In addition to yield benefits, cover crops
may also enhance crop quality as is the case of the use of winter rye interplanted
with melon that protects the young fruits from sand blasting and scarring. Combined
with reduced fertilizer and pesticide costs, this may offset the additional seed and
cultivation costs of cover-crop-based systems (Weil and Kremen 2007; Bergtold
et al. 2005; Fageria et al. 2005; Sullivan 2003). In addition to reducing fertilizer costs
on poor or compacted soils, the use of cover crop (residues) may also enhance aeration and intrinsic yield potential and/or reduce crop risk under water-limited conditions (Sustainable Agriculture Network 2007; Villarreal-Romero et al. 2006;
Bergtold et al. 2005; Schroth et al. 2001; Masiunas 1998). Lu et al. (2000) reviewed
several studies and commented that many studies only looked at relatively short
production cycles. Typically, there were no or only small significant differences in terms
of yield benefits. However, in a number of cases, cover-crop-based systems showed
appreciable yield fluctuations and higher labor and fuel costs. It was stated that many
systems and technologies were still being developed and system performance/yields
were either inconsistent or suboptimal. System design and adaptation, thus, may take
several years and a number of design and evaluation cycles may be required. This is
evident from research by Abdul-Baki during the past decades focusing on developing an integrated technology package, including no-tillage, mixed cover crops,
mechanical termination of cover-crop residues, and use of cover-crop-mulched
vegetable systems. After initial system design and development in Maryland, this
system was perfected, adapted, and successfully used for different crops, regions,
and production systems (Abdul-Baki et al. 1996, 1999, 2004; Carrera et al. 2004,
2005, 2007; Teasdale and Abdul-Baki 1998; Wang et al. 2005).
However, many leguminous cover-crop systems may not provide adequate N to
meet crop demand and supplemental N fertilizer is still required to reduce the risk of
yield reductions of subsequent commercial crops (Cherr et al. 2007; Lu et al. 2000).
This is confirmed by a meta-analysis of cropping systems in temperate regions, which
showed that legume-fertilized systems had 10% lower yields compared to N-fertilizer
systems unless N accumulation in cover-crop residues exceeded 110 kg N ha−1
(Tonitto et al. 2006). A similar study in North America showed that the use of grasses
did not affect subsequent maize yields; legumes increased these yields by 37% compared to nonfertilized control systems but yield benefits decreased as N-fertilizer rate
increased (Miguez and Bollero 2005). Based on past experiences, limited use of cover
crops in high-value commodities was often related to the low cost of inorganic fertilizers. Moreover, most conventional but also some organic nutrient sources have relatively constant and predictable nutrient content and release patterns, while for cover
crops, both the nutrient accumulation potential and release patterns tend to be highly
variable. Due to this added level of complexity, the integration of cover crops in conventional systems requires farmers to become better managers to ensure optimal system performance (Shennan 2008; Cherr et al. 2006b). However, the exponential (800%)
increase in fossil fuel prices between 1998 and 2008 resulted in increases of N- and
P-fertilizer prices of 226% and 307%. This unprecedented increase in energy and
fertilizer prices, along with the rapid depletion of mineral nutrient reserves, underlines
the need for alternative nutrient sources (Wilke and Snapp 2008).
2
Cover Crops for Sustainable Agrosystems in the Americas
39
2.3.7 Ecological Services
In the past, externalities and actual replacement costs of nonrenewable resources
were not included in production costs. Moreover, in many countries, including
India and Mexico, fertilizers are greatly subsidized to improve national food security (Cherr et al. 2006b). This undermines the viability of green technologies,
more sustainable development options, and puts a heavy burden on local economies.
In terms of ecological services, cover-crop-based systems greatly reduce sediment losses associated with erosion, which are the main agricultural pollutants that
also reduce the inherent production capacity of agroecosystems, especially in
regions such as Brazil and Uruguay (Dogliotti et al. 2004; Prado Wildner et al.
2004; Dabney et al. 2001). Although cover crops should be an integral part of
organic production systems, commercial organic growers may still, to a large extent,
depend on animal manures, waste products of other sectors, and allowable synthetic compounds. Pursuing an “input substitution” approach hampers the closing
of energy and nutrient cycles, and is in contrast with the farm-based integrated
organic approach (Cherr et al. 2006b).
For conventional systems, use of cover-crop-derived mulches may reduce the
need for plastic mulches and or soil fumigants (Abdul-Baki et al. 1996, 2004).
Replacing a bare fallow with cover crops may also enhance nutrient retention and
reduce N-leaching by upto 70% (Wyland et al. 1996). A meta-analysis of cropping-system studies showed that nitrate-leaching in legume-based systems was
40% lower compared to conventional systems (Tonitto et al. 2006). However, late
planting and slow initial growth will hamper the effectiveness of cover crops in
retaining residual soil nutrients (Mays et al. 2003). Poor system design and/or lack
of synchronization result in inefficient N use and poor yields (Cherr 2004; Avila
2006). Therefore, for cover-crop-based systems to be ecologically sound and
economically viable, development of integrated systems that provide multiple
benefits to offset potential risks and investment costs is essential (Cherr et al.
2006b). In the USA, the Natural Resource Conservation Services (NRCS) awards
growers for the environmental services associated with cover-crop use (Bergtold
et al. 2005). However, improved assessment of true fertilizer costs will be required
and farmers growing cover crops should also receive carbon credits as well
(Sainju et al. 2006).
In summary, steady-state SOM values and C-addition rates required to sustain
SOM will vary widely depending on pedo-climatic conditions and actual management practices. Models may provide an effective tool to assess potential benefits of
cover crops in enhancing SOM (Dogliotti et al. 2005; Lal et al. 2000). Although
cover crops can enhance inherent soil fertility and improve profits, inadequate management skills, poor system design, and lack of synchronization will greatly reduce
such benefits. Especially in organic systems, cover crops can provide cost-effective
weed suppression while in conventional systems, the use of cover crops may not be
viable unless they provide multiple benefits and farmers are being awarded for
ecological capital generated by growing cover crops.
40
J.M.S. Scholberg et al.
2.4 Selection
The selection of cover crops is based on pedo-climatic conditions, the set of services
required, current crop rotation schemes, and alternative management options
(Sustainable Agriculture Network 2007; Cherr et al. 2006b; Anderson et al. 2001).
An example of steps taken during the screening process of a large number of cover
crops (mixes) in Ohio was discussed by Creamer et al. (1997). Although cover
crops provide a myriad of services, the “perfect” cover crop simply does not exist.
Consequently, priorities among a set of critical services that cover crop (mixture)
should offer need to be determined first. These may include (i) providing nitrogen;
(ii) retaining/recycling nutrients and soil moisture; (iii) reducing soil degradation/
erosion; (iv) sustaining/increasing SOM levels; (v) reducing the incidence of pests;
and (vi) providing products and income (Sustainable Agricultural Network 2007;
Cherr et al. 2006b). First, a detailed analysis of the current crop management system
on a field level, including crop rotations, duration of commercial crops, inter-crop/
fallow period, tillage systems, along with an assesment of potential risk of pests
and diseases of commercial crops, is required. Some additional practical selection and
screening considerations include the following:
• Adaptation to drought, flooding, low pH, nutrient limitations, and shading
(live mulch)
• Combining species with complementary growth cycles, canopy traits, and root
functionality
• Lack of adverse traits
–– Unfavorable residue properties (e.g., excessively high C:N ratio, coarse, and
recalcitratant residues hampering seed bed preparation, allelopathetic properties
that hamper initial germination, and growth of subsequent commercial crops)
–– Competition with cash crops for light, land, water, nutrients, labor, and capital
–– Weediness and/or excessive vigor/regrowth after mowing or mechanical killing
–– Ability to promote (host) pests and diseases
• Availabilty of affordable seeds, suitable equipment, techniques, and information
to ensure optimal cover-crop growth, termination, and overall system performance
Following these steps, an initial assesment may be made of perceived benefits and
risks which may be used for ranking potential cover-crop (mixture) candidates and/
or cultivars; this typically will be based on expert knowledge since no actual data
may be available. The next step will be to provide an assessment of the actual services being rendered by such systems (either via field measurements/observation or
using computer simulations) to further refine the crop rotation design and covercrop management (Altieri et al. 2008; Cherr et al. 2006b). In practice, this may be
a process of “trial and error” to properly integrate all relevant information as related
to local pedo-climatic conditions into the decision-making process. The development
of management practices and a suitable site-specific cover-crop-based cropping
system that are relevant within the local context, thus, may require several years
2
Cover Crops for Sustainable Agrosystems in the Americas
41
and a number of experimental learning cycles, while cover-crop-based systems
may continue to evolve over time as well. Some of the most pertinent aspects of
cover-crop selection will be discussed in more detail below. The use of expert systems, such as GreenCover (Cherr et al. unpublished; http://lyra.ifas.ufl.edu/
GreenCover) and ROTAT (Dogliotti et al. 2003), may facilitate the first selection
step of designing suitable cover crops.
2.4.1 Adaptation
Adaptation may include day length, temperature, radiation, rainfall, soil, pests, and
crop duration aspects. Cover crops can be grouped as being adapted to “cold/temperate”
versus “warm/tropical” growth environments (Anderson et al. 2001). The first type
may survive a freeze upto −10°C while their growth may be hampered under hot
conditions (>25–30°C). Leguminous species within this group include Lupinus,
Trifolium, and Vicia species and they grow well in temperate climates, during the
winter season in subtropical climates, or in the tropical highlands (Cherr et al. 2006b;
Giller 2001). The second group does not tolerate freezes (<−2°C) but may thrive
under hot (>35°C) conditions. Some of the key leguminous species within this group
include the genus Canavalia (e.g., Jack bean C. ensiformis), Crotalaria (e.g., sunn
hemp C. Juncea), and Mucuna (e.g., velvet bean). Tropical species may also be more
easily grown during the summer months as one moves toward the subtropics or even
throughout the year (tropical regions). Both temperature and day length affect crop
development and growth duration. Use of simple phenology models facilitates the
selection of suitable species for different production environments, which can be
particularly important in hillside environments (Keatinge et al. 1998). Over-sowing
cover crops into existing crops (e.g., maize) requires the selection of species that
are adapted to low initial light regimes (Anderson et al. 2001).
Adaptation to local soil conditions, as related to soil drainage, texture, pH, and presence of compatible rhizobia strain for leguminous crops, is critical (Cherr et al. 2006b;
Giller 2001). On soils with adequate moisture storage capacities, cover crops may be
grown during the dry season, while in other cases, the growth may be limited by rainfall
since adequate soil moisture is required during initial growth. Crop water requirements
of cover crops depend on crop type and growth duration, but in many cases, cumulative
water use may be comparable to that of commercial crops, and in water-limited systems,
cover crops may deplete residual soil moisture reserves as well and may have to be
killed prematurely (Cherr et al. 2006b). Especially, leguminous crops may be poorly
adapted to either extremely acidic or alkaline soils or poorly drained soils (Cherr et al.
2006b; Giller 2001). When introducing new non-promiscuous leguminous types, the
presence of suitable inoculum is critical, since poor nodulation hampers crop growth and
N accumulation (Giller 2001). Leguminous crops, although adapted to N-limiting conditions, may have appreciable needs for other nutrients (including K, P, Mo), while due to
their slow initial growth, they are not very efficient in utilizing residual soil nutrients.
42
J.M.S. Scholberg et al.
2.4.2 Vigor and Reproduction
Initial growth of small-seeded cover crops, e.g., clovers, may not be as vigorous
compared to larger-seeded types which have more reserves and can be planted deeper,
especially when rainfall during initial growth is erratic (Cherr et al. 2006b). Selfseeding types, e.g., crimson clover, may provide an ample seed bank and thus,
germination may be triggered automatically when conditions are favorable (Cherr
et al. 2006b). However, reseeding types may also become a potential pest themselves, especially when they are hard- and/or large-seeded types. In this case, timely
mowing prior to seed set may be required although the original planted crop may
become a dormant seed bank in itself unless it is stratified in an appropriate manner.
Cover crops such as sunn hemp over time may become rather tall (>3 m) with very
thick and recalcitrant stems that may pose serious problems in subsequent vegetable crops, since they can hamper bed formation. In this case, repeated mowing may
be required (N. Roe, personal communication). Other cover crops may have a viny
and rather aggressive growth habit, e.g., cowpea and velvet bean, that can interfere
with commercial crops when used as green mulch as was reported in citrus (Linares
et al. 2008).
2.4.3 Functionality and Performance
In many hilly regions in Latin America, cover crops are an integral component of
no-tillage systems, since they can reduce soil erosion, labor, and herbicide costs,
and can alsoincrease yields (Prado Wildner et al. 2004). In organic systems, they can
be a critical component of integrated weed management strategies (Linares et al.
2008). The actual performance of cover crops depends on system design, inherent
soil fertility, pedo-climatic conditions, management (including the use of well-adapted
species), and crop duration (Cherr et al. 2006b; Giller 2001). Although potential
cover-crop production may be highest in warm and high rainfall environments,
SOM breakdown and potential nutrient losses under such conditions also tend to be
much greater, and thus, net benefits may be actually lower compared to more temperate climates. Information on adaption, growth, and performance may be obtained
from the literature (Baligar and Fageria 2007; Sustainable Agriculture Network 2007;
Cherr et al. 2006b). Even within cover-crop species, there may be appreciable differences in specific traits that can greatly affect their adaptation and functionality
as related to specific production settings (e.g., cold and drought tolerance; shoot:root
ratio) as was shown for hairy vetch (Wilke and Snapp 2008). Use of cover-crop
mixes with complementary traits may enhance the functionality, productivity, resilience, and adaptability of cover-crop-based systems and thus, facilitate more efficient
resource use capture under adverse conditions (Malézieux et al. 2009; Altieri et al.
2008; Linares et al. 2008; Drinkwater and Snapp 2007; Weil and Kremen 2007;
Teasdale et al. 2004; Dabney et al. 2001; Creamer et al. 1997). Moreover, a combination
2
Cover Crops for Sustainable Agrosystems in the Americas
43
of several species may provide the benefits of different included species within a
single year (Calegari 2003), whereas no single cover-crop species consistently performs superior across different years and field sections (Linares et al. 2008;
Carrera et al. 2005).
Typically, cover crops are not irrigated nor are they being fertilized. The growth
of cover crops may be superior on more fine-textured soils since these soils often
have higher SOM values, inherent soil fertility, and better water and nutrientretention capacities. This may result in a positive feedback mechanism that, in turn,
can further boast cover-crop performance over time (Cherr et al. 2006b). However,
on very heavy soils, limited drainage may also result in poor aeration and increased
incidence of diseases, thus, resulting in poor stands and suboptimal cover-crop performance. In organic tomato production systems in California, mixtures of grasses
with leguminous cover crops accumulated more biomass but less N, whereas their
residues had higher C:N ratios which delayed mineralization (Madden et al. 2004).
On very sandy soils, low inherent soil fertility, among other factors, may limit growth
of the cover crops, whereas nutrients accumulated in its residue may be also readily
lost due to leaching prior to the peak nutrient demand of a subsequent commercial
crop (Cherr et al. 2007). As a result, in adverse production environments, the growth
and the benefits that cover crops provide may be limited and integrated soil fertility
management practices may be required to enhance overall system performance
(Tittonell 2008; Giller 2001). In summary, a design of an appropriate cover-crop
system based on key desired ecological functions, is critical for system performance. The use of expert knowledge and computer-based evaluation tools can facilitate
initial screening, while optimal system design may require numerous design cycles
to tailor systems to local management conditions.
2.5 Management
2.5.1 Rotation
Developing suitable crop rotation schemes is critical for enhancing systems performance. The design of both spatial and temporal crop arrangements on a farm level
will be based on meeting a set of grower-defined production objectives along with
adhering to site-specific phyto-sanitory guidelines. Growers typically allocate cover
crops to underutilized temporal and/or spatial components of their cropping system,
e.g., fallow period or row middles, which constrain their use. The growth season
of cover crops is, thus, defined by the cropping season of commercial crops which,
in turn, is dictated by rainfall or temperature patterns. Although it requires special
equipment, undersowing of a cover crop in an existing crop may be desirable, since
it facilitates more efficient resource use while reducing potential nutrient losses and
erosion risks (Hartwig and Ammon 2002; Sullivan 2003). In the southern USA, cover
crops such as sorghum, sudan grass, or sunn hemp may be grown during times
44
J.M.S. Scholberg et al.
when it is too hot to grow commercial crops as is the case in Florida (Avila 2006).
In the case of more complex arable cropping systems, the use of software tools to
explore such options to generate viable alternatives greatly facilitates the design
process (Bachinger and Zander 2007; Dogliotti et al. 2003).
2.5.2 Biomass Production and Residue Quality
Most cover crops follow a “logistic” or “expo-linear” growth pattern, so after an
initial “lag-phase” prior to canopy closure, biomass accumulation rates tend to be
relatively constant before leveling off toward crop maturation (Kruidhof 2008; Yin
et al. 2003). Although there is a multitude of information on cover-crop performance in terms of biomass and N accumulation at maturity, narrow windows of
opportunity for planting commercial crops may require cover crops to be killed
prematurely (Cherr et al. 2006b). In this case, simple linear equations, thus, may be
developed to estimate the amount of residues as a function of crop yield (Steiner
et al. 1996). Alternatively, degree day-based models may be used to predict biomass
and N accumulation of cover crops as a function of accumulated temperature units
(Schomberg et al. 2007, Cherr et al. 2006c).
The carbon content of most plant material is relatively constant over time with
values being on the order of 40–44% (Avila 2006; Dinesh et al. 2006). Overall plant
N concentration typically follows an exponential decay curve over time (“N dilution
curve”) and final N tissue concentration is, thus, a function of crop type, crop age,
and N supply (Lemaire and Gaston 1997). In terms of N accumulation and subsequent N release of cover crops, based on data outlined by Cherr et al. (2006b)
calculated N concentrations for temperate versus tropical legumes are on the order
of 1.9–3.6% and 2.6–4.8% compared to 0.7–2.5% for nonleguminous crops which
translates to corresponding C:N ranges of 8–15, 11–21, and 16–57, respectively.
Calegari (2003) provided a detailed overview on the mineral composition and C:N
ratio of different cover crops grown in Brazil. Such information provides an insight
into the overall nutrient supply capacity of cover-crop residues, though values may
differ on the basis of local soil fertility regimes. As cover crops mature, there is a
gradual shift toward both structural and reproductive parts (Cherr et al. 2006c). With
aging, both the leaf fraction and the N content of leaves and stems decrease, whereas
more recalcitrant compounds and seed proteins may accumulate (Cherr 2004;
Cherr et al. 2006b; Lemaire and Gaston 1997). Increasing plant density will result
in early canopy closure, higher initial biomass accumulation rates, and dry matter
allocation to less recalcitrant and high-N plant parts, while excessive high plant
densities may reduce growth due to crowding (Cherr et al. 2006b). Repeated mowing
for sod-forming or indeterminate cover crops can delay the shift toward more recalcitrant plant parts, enhance N content, and increase total biomass production (Cherr
et al. 2006b; Snapp and Borden 2005). Planting density, time of “mowing” or “killing” cover crops, thus, affect both residue quantity and quality, and may be used to
manipulate system dynamics.
2
Cover Crops for Sustainable Agrosystems in the Americas
45
2.5.3 Cover-Crop Termination and Residue Management
At the end of the fallow season, cover crops may be killed by herbicide, mowing,
flaming, or by a crimper (Sustainable Agricultural Network 2007; Calegari 2003;
Sullivan 2003; Lu et al. 2000; Masiunas 1998). Mowing may result in the formation
of a compact mulch layer, that in turn, may help to conserve soil moisture and reduce
soil erosion (Fig. 2.4). Rolled residues decompose slower compared to the use of
mowing or herbicides, while the residue layer also tends to persist longer, and provides more effective long-term soil erosion control (Lu et al. 2000). Timing of
mowing, as related to cover-crop development stage, is critical in term of maximizing
biomass and N accumulation while reducing the risk that cover crops regrow or set
seed and thereby interfere with a subsequent commercial crop (Prado Wildner et al.
2004; Sullivan 2003). The optimal time of residue killing is also related to cover
crops’ main function. If soil conservation and SOM buildup are priorities, older and
more lignified residues may be preferable. However, delaying killing may hamper
the effectiveness of rollers/crimpers, whereas residues are also more likely to interfere with planting equipment, while the resulting augmented C:N ratio can also
increase the risk of initial N immobilization. Mowing and use of herbicide, on the
other hand, will increase residue decomposition and subsequent mineralization
(Snapp and Borden 2005). Many farmers may opt to delay planting after residue
kill to reduce the risk of transmittance of herbivores feeding on residues invading
the new crop, to ensure adequate settling of residues which facilitates planting
operations, and to prevent the negative effects of allelopathetic compounds on the
emerging crop (Prado Wildner et al. 2004). Alternatively, placement of seeds below
the residue layer can reduce the risk of potential allelopathetic substances hampering
initial growth (Altieri et al. 2008).
2.5.4 Tillage
Soil incorporation of cover crops enhances soil residue contact and also buffers its
moisture content which tends to speed up decomposition, while surface applied
residue may have a greater capacity for N immobilization (Cherr et al. 2006b). Surface
application of residues also favors saprophytic decomposition by fungi, whereas
bacterial decomposition is prevailing more for incorporated residues and repeated
tillage tends to greatly enhance mineralization (Lal et al. 2000). Leaving mulch
residues of cowpea, used as a cover crop in a lettuce production system, was much
more effective in suppressing weeds compared to tilling in residues but it also reduced
lettuce yields by 20% (Ngouajio et al. 2003). Use of no-tillage may reduce labor
costs, energy use, and potential erosion while increasing carbon sequestration, biodiversity, and soil moisture conservation (Triplett and Dick 2008; Peigné et al.
2007; Giller 2001). In Brazil, it was demonstrated that the integrated use of cover
crops with no-tillage is critical for enhancing/sustaining SOM (Calegari 2003).
These techniques are complementary work and work synergistically while the use
46
J.M.S. Scholberg et al.
of conventional tillage will promote rapid breakdown of SOM which may partially
offset cover-crop benefits (Phatak et al. 2002). However, in organic production
systems, no-tillage may result in increased incidence of grassy and perennial weeds,
while for poorly drained/structured soils and under excessive wet soil conditions,
its use may have unfavorable effects on soil tilth, crop growth, incidence of plant
pathogens, and it may also increase the risk of N immobilization (Peigné et al.
2007). Although no-tillage and the presence of crop residues near the surface may
reduce soil evaporation, it can promote root proliferation near the soil surface, thus,
rendering subsequent commercial crops more vulnerable to prolonged drought
stress (Cherr et al. 2006a).
2.5.5 Synchronization
Residue decomposition rates depend on both crop composition management and
pedo-climatic conditions (Snapp and Borden 2005). Release patterns tend to be
highly variable both in space and time. The release of readily available crop nutrients
from cover-crop residues, thus, may not coincide with peak nutrient requirements
of a subsequent crop (poor synchrony). This problem is evident from the large
number of studies reviewed by Sarrantonio and Gallandt (2003) in which nutrient
release was either premature or too late. Residue C:N values will, to a large degree,
determine initial decomposition rates together with factors such as the content of
water-soluble and intermediate available carbon compounds in the residue (Ma
et al. 1999). Nitrogen allocation to root systems may be on the order of 7–32% and
20–25% of its N may be released to the soil prior to crop senescence (Cherr et al.
2006b). Moreover, under hot and humid conditions, nutrient release from low C:N
residue materials may be premature and N-leaching losses can be very high (Cherr
et al. 2007; Giller 2001). However, under cold and/or dry conditions, use of more
recalcitrant residues, and N-limited conditions, will delay initial release and net N
immobilization may hamper initial growth of commercial crops (Cherr et al. 2006b;
Sarrantonio and Gallandt 2003). However, better synchronization requires improved
understanding of residue decomposition and net mineralization. However, since these
processes are affected by a large number of biotic, pedo-climatic, and management
factors, appropriate use of decomposition models may be required to provide a better insight on how interactions among management factors come into play. These
model tools may then be integrated into decision-support tools for farm managers/
advisors, which was the rationale for developing the NDICEA model (van der
Burgt et al. 2006). Thus, such tools can be effectively used to improve the synchronization of nutrient-release patterns with crop demand which should facilitate the
successful integration of cover crops in conventional systems. Based on predictions
of such models, management options such as use of different spatial and/or temporal
crop arrangements, use of cover-crop mixtures to modify initial C:N ratios, time
and method of killing, and method of incorporation, among others may be used to
enhance synchronization (Weil and Kremen 2007; Cherr et al. 2006b; Balkcon and
2
Cover Crops for Sustainable Agrosystems in the Americas
47
Reeves 2005; Sullivan 2003). As an example, using a biculture of rye and vetch and
modifying seed-mixture ratios can facilitate improved synchronization. Increasing
the vetch:rye ratio will speed up initial mineralization, reduce the risk of initial
immobilization, but may increase potential N-leaching risks (Kuo and Sainju 1997;
Teasdale and Abdul-Baki 1998). In summary, it is evident that poor synchronization favors inefficiencies and increases potential nutrient losses. This is one of the
key factors deterring conventional farmers from adopting cover-crop-based systems.
Use of cover-crop mixes, improved timing of mowing and/or incorporation, along
with use of decision-support tools such as NDICEA are some of the key options to
enhance synchronization.
2.6 Limitations and Challenges
2.6.1 Information and Technology Transfer
Although cover crops provide a myriad of services, their adaptation by conventional
farmers typically has been slow (Sarrantonio and Gallandt 2003). In Brazil, they were
introduced during the 1970s, but wide-scale adoption took several decades (Prado
Wildner et al. 2004). Some potential challenges may include: additional production
costs (in terms of land, labor, and inputs), the complexity of cover-crop-based systems, the lack of pertinent information and suitable technology transfer methods, the
uncertainty of release patterns from cover-crop residues, and lack of secure land
tenure (Singer and Nusser 2007; Cherr et al. 2006b; Nyende and Delve 2004;
Sarrantonio and Gallandt 2003; Lu et al. 2000). This additional level of complexity,
combined with lack of information on suitable management practices, along with the
perceived risks associated with cover-crop-based systems, prevents growers from
adopting cover-crop-based systems (Shennan 2008; Sarrantonio and Gallandt 2003).
Regarding information on cover crops, a search of the CAB citation index for
“cover crops” clearly indicated an increased interest in cover crops during the past
decades. The annual number of papers on this topic decreased from 74 (1961–1970)
to 37 (1971–1980), but then increased again from 56 (1981–1990) to 160 (1991–
2000), and then to 221 (2001–2007). Despite this impressive increase in publication
numbers, producers still cite lack of useful information about cover crops as one of
the greatest barrier to their use (Singer and Nusser 2007). Although, during the first
half of the last century, most farmers routinely used cover crops, this traditional
knowledge base has been gradually lost. Even within research and extension faculty,
there was a complete erosion of knowledge and experience as faculty members with
a more traditional farm background retired. Moreover, during the past decades,
academic interest has shifted toward genetic engineering technology, typically resulting
in the recruitment of scientists lacking basic agronomic knowledge. Furthermore,
most conventional farmers are not in a position to take the economic risk associated with
experimentation and exploration of suitable cover-crop technologies and thus,
48
J.M.S. Scholberg et al.
increasingly depend on external information sources (Weil and Kremen 2007;
Cherr et al. 2006b). Therefore, lack of appropriate information and technology
transfer approaches still continues to be among the key factors hampering the
adoption of cover-crop-based systems (Bunch 2000).
The traditional “top-down” approach used by research and development institutes
to provide technical solutions to farmers in the absence of a thorough understanding
of local socioeconomic conditions and agroecosystems appears to be especially ineffective for cover-crop-based systems (Anderson et al. 2001). Establishing “innovation
groups,” a technology development and exchange structure in which farmers play a
key role and/or “farmer-to-farmer” training networks, in which innovative farmers
assume an active role as educators, may be more appropriate for propagating covercrop-based technologies (Anderson et al. 2001; Horlings 1998). Since most university
programs are still poorly equipped to address the specific needs of organic farmers,
this producer group may still be forced to engage in some on-farm experimentation
with cover-crop-based systems, especially since this group appears to benefit greatly
from the use of cover crops (Linares et al. 2008).
2.6.2 Resource Management
The growth and nutrient accumulation among cover-crop-based systems may vary
greatly between fields and years, while subsequent nutrient-release patterns are also
affected by a great number of pedo-climatic and management factors. Limited
knowledge of these processes on a field scale will result in poor synchronization
between nutrient release by cover crops and subsequent crop demand of commercial
crops, thereby increasing the risk of inefficient N use and poor system performance
(Cherr et al. 2006b). Although simulation models could harness some of this complexity, most of these models were developed for scientists and are difficult to implement, whereas models for informed decision-making and improved management of
cover crops require a combination of a sound scientific basis with practice-oriented
model design (van der Burgt et al. 2006).
In terms of combining cover crops with no-tillage systems, although such systems provide multiple benefits, there are also several additional challenges. Cover
crops grown as live mulches or ineffective crop-kill of annual cover crops, such as
ryegrass or vetch, can result in cover crops competing with cash crops which may
reduce yields (Hiltbrunner et al. 2007; Teasdale et al. 2007; Madden et al. 2004).
Residues of cover crops can hamper soil cultivation and initial germination (due to
inconsistent seed cover), delay planting operations (since residues need some time
to decompose/die), harbor pests and diseases, decrease initial crop growth (due to
N immobilization, release of growth inhibiting compounds, or crop competition),
and/or reduce soil temperatures (Peigné et al. 2007; Teasdale et al. 2007; Weil and
Kremen 2007; Avila 2006; Cherr et al. 2006b; Masiunas 1998). However, in sweet
maize a reduction in initial plant stands in no-till rye–vetch cover-crop-based systems was offset by improved growth and yields were still higher compared to bare
2
Cover Crops for Sustainable Agrosystems in the Americas
49
soil control (Carrera et al. 2004). But for vegetable crops, the use of cover crops
delayed crop maturation and/or reduced both initial crop growth and final yield of
subsequent crops (Avila 2006; Sarrantonio and Gallandt 2003; Abdul-Baki et al.
1996, 1999; Creamer et al. 1996). Especially for high-value commodities such as
vegetables where precocity may translate into significant price premiums, such effects
may have a strong negative impact on profitability (Avila 2006; Creamer et al. 1996).
Only after researchers became aware of these issues and the system was redesigned
(e.g., by using strip-till) this problem could be addressed (Phatak et al. 2002). Such
adaptive learning and innovation cycles should be an integral part of training programs
to enhance the efficiency of technology transfer (Douthwaite et al. 2002).
Under water-limiting conditions, use of cover crops will also deplete residual
soil moisture levels and thereby, can reduce yields of subsequent crops (Sustainable
Agricultural Network 2007). Use of winter cover crops in semiarid conditions in
California, reduced soil water storage by 65–74 mm, thereby, impacting the preirrigation needs of subsequent crops and/or performance of subsequent annual crops
(Michell et al. 1999). In perennial systems (e.g., vineyards), perennial cover crops
were shown to have both higher root densities and deeper root systems, thus, resulting
in more pronounced soil water depletion but either one affects spatial and temporal
water supply. Grapevines may adapt its rooting pattern to minimize water stress,
while supplemental irrigation mainly benefits cover crops (Celette et al. 2008).
Although cover crops may provide a time-released source of N which is often perceived to be more efficient compared to inorganic N, poor synchronization will
result in high potential N losses and thereby, greatly reduce efficiencies from residuederived N and may also increase the risk of N-leaching (Cherr et al. 2007).
2.6.3 Socioeconomic Constraints
Local perceptions and political priorities can greatly hamper the adoption of covercrop-based systems. In many cases, local politicians, researchers, and extension
staff continue to favor green-revolution-based technologies and are reluctant to invest
in traditional legume-based cropping systems (Anderson et al. 2001). In other cases,
the perceived complexity and risk associated with the management of cover-cropbased systems may not offset direct benefits. Weil and Kremen (2007) reported that
in Maryland, cover crops were only grown on 20–25% of the agricultural land during winter fallow despite farmers receiving $50–$100 subsidies for growing such
crops. Therefore, unless cover crops provide multiple benefits and services and
such advantages are also considered, the use of cover crops may not be cost-effective
(Avila et al. 2006a, b; Cherr et al. 2006b; Abdul-Baki et al. 2004). Moreover, since
cover-crop-based systems often require several years to evolve and provide the
maximum benefits, their use is only viable if land tenure is secure (Neill and Lee
2001). Growers, despite their inherent desire to provide good stewardship of local
land resources, face the reality of economic survival and thus, may not be in a position
to provide certain environmental services unless they will also generate tangible
50
J.M.S. Scholberg et al.
and direct benefits (Weil and Kremen 2007). Moreover, researchers engaging in
interdisciplinary and participatory research may face appreciable risks and logistic
challenges. Many institutes are moving toward more fundamental research and more
practical geared research such as cover-crop management may be implemented by
extension service and the linkage with research may be poor. Therefore, a critical
re-assessment of both research and extension services and increased support for green
technologies will be critical. In many cases, the involvement of farmers and local
communities in structuring problem definitions and designing sustainable solutions
should be enhanced. Furthermore, additional government and corporate support is
needed for developing green technologies, especially when market mechanisms are
not yet in place to provide incentives for innovations geared toward enhancing sustainability. In summary, awarding researchers for developing and improving green
technologies and farmers for providing ecological services will be critical to offset some
of the perceived risks associated with engaging in cover-crop-based systems.
2.7 Conclusion
Based on our comprehensive review of the literature, it was shown that there is a
pronounced revival of cover crops during the past few decades. However, most of
these studies document cover-crop performance for specific pedo-climatic conditions, and there is need for a more system-based approach. Moreover, it is also critical to place potential performance of cover crops in the context of production goals
as related to existing system structure and management skills. Although cover crops
can contribute to carbon sequestration, such benefits are only significant when soil
tillage is minimized. Selection and use of cover crops is mainly based on tradition,
perceived benefits, seed availability, seed costs, and technical support. The time of
planting and termination of cover crops, as related to planting of commercial crops,
are essential to biomass production and nutrient accumulation, while poor synchronization readily offsets potential yield or environmental benefits. The use of decision-support tools such as NDICEA seems desirable to provide a better insight into
C and N dynamics in cover-crop-based systems. Despite the numerous benefits of
cover crops, the widespread use of cover crops is currently still mainly confined to
their integration into conservation tillage practices of conventional agricultural
systems in regions prone to soil erosion. In contrast, in organic systems, the use of
conservation tillage is still in its infancy. In this case, providing cost-effective weed
control and restoring nutrient imbalances associated with the excessive use of animal manures, are among the most critical factors governing their use. We conclude
that cover-crop-based systems are most likely to be used when they provide multiple
benefits, which is especially important in the absence of significant yield benefits
and/or relatively low opportunity costs of chemical fertilizers. Moreover, the use of
cover-crop mixes is highly desirable, since this favors system performance under
unfavorable/unpredictable growing conditions. Since cover crops have a central function in organic production systems, organic growers provide a critical role to preserve
2
Cover Crops for Sustainable Agrosystems in the Americas
51
traditional knowledge and to also generate technical innovations required to address
current challenges that may benefit conventional growers as well. Furthermore,
technological innovations, via government- and corporate-sponsored research, are
essential to further improve and promote green technologies such as cover crops.
Acknowledgments This review was possible as part of international and interdisciplinary collaborations fostered by the EULACIAS program (http://www.eulacias.org/). This program was
funded by the FP6-2004-INCO-DEV3-032387 project titled “Breaking the spiral of unsustainability in arid and semi-arid areas in Latin Americas using an ecosystems approach for co-innovation of farm livelihoods.”
References
Abawi GS, Widmer TL (2000) Impact of soil health management practices on soil-borne pathogens, nematodes and root diseases of vegetable crops. Appl Soil Ecol 15:37–47
Abdul-Baki AA, Bryan H, Klassen W, Carrera LM, Li YC, Wang Q (2004) Low production cost
alternative systems are the avenue for future sustainability of vegetable growers in the U.S. In:
Bertschinger L, Anderson JD (eds) Proceedings of XXVI IHC, Sustainability of Horticultural
Systems, Acta Hort 638, 419–423
Abdul-Baki AA, Morse RD, Teasdale JR (1999) Tillage and mulch effects on yield and fruit fresh
mass of bell pepper (Capsicum annum L.). J Veg Crop Prod 5:43–58
Abdul-Baki AA, Teasdale JR, Korcak R, Chitwood DJ, Huettel RN (1996) Fresh-market tomato
production in a low-input alternative system using cover-crop mulch. HortScience 31:65–69
Altieri MA (2002) Agroecology: the science of natural resource management for poor farmers in
marginal environments. Agric Ecosyst Environ 93:1–24
Altieri MA, Lovato PM, Lana M, Bittencourt H (2008) Testing and scaling-up agroecologically
based organic no tillage systems for family farmers in southern Brazil. In: Neuhoff D et al
(eds) Proceedings of the Second Scientific Conference of the International Society of
Organic Agriculture Research (ISOFAR). University of Bonn, Bonn, Germany, Bonn Vol II,
pp 662–665
Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests; harmonizing soil and
plant health in agroecosystems. Soil Tillage Res 72:203–211
Amado TJC, Bayer C, Conceição PC, Spagnollo E, Costa de Campos BH, da Veiga M (2006)
Potential of carbon accumulation in no-tillage soils with intensive use and cover crops in
southern Brazil. J Environ Qual 35:1599–1607
Anderson S, Gundel S, Pound B, Thriomphe B (2001) Cover crops in smallholder agriculture:
lessons from Latin America. ITDG Publishing, London, UK, 136 pp
Avila, L. (2006) Potential benefits of cover crop based systems for sustainable production of vegetables, MS thesis, University of Florida, Gainesville FL, 287 pp. http://etd.fcla.edu/UF/
UFE0015763/avilasegura_l.pdf. Accessed 6 June 2008; verified 1 October 2008.
Avila L, Scholberg JMS, Zotarelli L, McSorley R (2006a) Can cover crop-based systems reduce
vegetable crop fertilizer nitrogen requirements in the South eastern United States? HortScience
41:981
Avila L, Scholberg JMS, Roe N, Cherr CM (2006b) Can sunn hemp decreases nitrogen fertilizer
requirements of vegetable crops in the South Eastern United States? HortScience 41:1005
Bachinger J, Zander P (2007) ROTOR, a tool for generating and evaluating crop rotations for
organic farming systems. Eur J Agron 26:130–143
Baligar VC, Fageria NK (2007) Agronomy and physiology of tropical cover crops. J Plant Nutr
30:1287–1339
52
J.M.S. Scholberg et al.
Balkcon KS, Reeves DW (2005) Sunn-hemp utilized as a legume cover crops for corn production.
Agron J 97:26–31
Barber RG, Navarro F (1994a) Evaluation of the characteristics of 14 cover crops used in a soil
rehabilitation trial. Land Degrad Rehabil 5:201–214
Barber RG, Navarro F (1994b) The rehabilitation of degraded soils in Eastern Bolivia by subsoiling
and the incorporation of cover crops. Land Degrad Rehabil 5:247–259
Baijukya FP, de Ridder N, Giller KE (2006) Nitrogen release from decomposing residues of leguminous crops and their effect on maize yield on depleted soils of Bukoba district, Tanzania.
Plant Soil 279:77–93
Bergtold JS, Terra JA, Reeves DW, Shaw JN, Balkcom KS, Raper RL (2005) Profitability and risk
associated with alternative mixtures of high-residue cover crops, Proceedings of the Southern
Conservation Tillage Conference, Florence, SC, pp 113–121
Berkenkamp A, Priesack E, Munch JC (2002) Modelling the mineralization of plant residues on
the soil surface. Agronomie 22:711–722
Bernadino-Hernandez HU, Alvarez-Solis JD, Leon-Martinez NS, Pool-Novelo L (2006) Legume
cover crops in corn production in the highlands of Chiapas, Mexico. Terra Lat Am
24:133–140
Bhardwaj HL (2006) Muskmelon and sweet corn production with legume cover crops. HortScience
41:1222–1225
Blok WJ, Lamers JG, Termorshuizen AJ, Bollen GJ (2000) Control of soilborne plant pathogens
by incorporating fresh organic amendments followed by tarping. Phytopahtology
90:253–259
Bottenberg H, Masiunas J, Eastman C, Eastburn D (1997) The impact of rye cover crops on
weeds, insects and diseases in snapbean cropping systems. J Sustain Agr 9:131–155
Bravo C, Lozano Z, Hernandez RM, Pinango L, Moreno B (2004) Soil physical properties in a
typical savanna soil of the Guarico State, Venezuela, under direct drilling management of
maize with different cover crops, Bioagro 16, 163–172
Buckles D, Triomphe B, Sain G (1998) Cover crops in hillside agriculture. IDRC, Ottowa, 218 pp
Bugg RL, Waddington C (1994) Using cover crops to manage arthropod pests of orchards: a
review. Agric Ecosyst Environ 50:11–28
Bunch R (1996) The use of green manure by small-scale farmers: what we have learned to date.
Adult Educ Dev 47:133–140
Bunch R (2000) Keeping it simple: what resource-poor farmers will need from agricultural engineers during the next decade. J Agric Eng Res 76:305–308
Calegari A (2003) Cover crop management. In: García-Torres L, Benites J, Martinez-Vilela A,
Holgado-Cabrera A (eds) Conservation agriculture: environment, farmers-experiences, innovations, socio-economy, policy. Kluwer, Dordrecht, pp 191–199
Cantonwine EG, Culbreath AK, Stevenson KL (2007) Effects of cover crops residue and preplant
herbicide on early leaf spot of peanut. Plant Dis 91:822–827
Carrera LM, Abdul-baki AA, Teasdale JR (2004) Cover crop management and weed suppression
in no-tillage sweet corn production. HortScience 39:1262–1266
Carrera LM, Buyer JS, Vinyard B, Abdul-Baki AA, Sikora LJ, Teasdale JR (2007) Effects of cover
crops, compost, and manure amendments on soil microbial community structure in tomato
production systems. Appl Soil Ecol 37:247–255
Carrera LM, Morse RD, Hima BL, Abdul-Baki AA, Haynes KG, Teasdale JR (2005) A conservationtillage, cover cropping strategy and economic analysis for creamer potato production. Am
J Potato Res 82:471–479
Cassini P (2004) Groundcover and weed control of selected cover crops in acidic soil of Columbia.
J Agric Environ Int Dev 97:125–137
Celette F, Guadin R, Gary C (2008) Spatial and temporal changes to the water regime of a mediterranean vineyard due to the adaptation of cover cropping. Europ J Agron 29:153–162
Cherr CM (2004) Improved use of green manure as a nitrogen source for sweet corn. M.S. thesis.
University of Florida, Gainesville, FL. http://etd.fcla.edu/UF/UFE0006501/cherr_c.pdf.
Accessed 3 July 2008; verified October 1, 2008
2
Cover Crops for Sustainable Agrosystems in the Americas
53
Cherr CM, Avila L, Scholberg JMS, McSorley RM (2006a) Effects of green manure use on sweet
corn root length density under reduced tillage conditions. Renew Agric Food Syst 21:165–173
Cherr CM, Scholberg JMS, McSorley RM (2006b) Green manure approaches to crop production:
a synthesis. Agron J 98:302–319
Cherr CM, Scholberg JMS, McSorley RM (2006c) Green manure as nitrogen source for sweet
corn in a warm temperate environment. Agron J 98:1173–1180
Cherr CM, Scholberg JMS, McSorley RM, Mbuya OS (2007) Growth and yield of sweet corn
following green manure in a warm temperate environment on sandy soil. J Agron Crop Sci
193:1–9
Chung YR, Hoitink HAH, Lipps PE (1988) Interactions between organic matter decomposition
level and soil-borne disease severity. Agric Ecosyst Environ 24:183–193
Colbach N, Duby C, Avelier A, Meynard JM (1997) Influence of cropping systems on foot and
root diseases of winter wheat: fitting of statistical model. Eur J Agron 6:61–77
Creamer NG, Bennett MA, Stinner BR, Cardina J (1996a) A comparison of four processing
tomato production systems differing in cover crops and chemical inputs. J Am Soc Hort Sci
121:559–568
Creamer NG, Bennett MA, Stinner BR (1997) Evaluation of cover crops mixtures for use in vegetable production systems. HortScience 32:866–870
Creamer NG, Bennett MA, Stinner BR, Cardina J, Regnier EE (1996b) Mechanism of weed suppression in cover crop-based systems. HortScience 31:410–413
Crow WT, Weingartner DP, Dickson DW, McSorley R (2001) Effects of sorghum-sudangrass and
velvet bean cover crops on plant-parasitic nematodes associated with potato production in
Florida, Supplement. J Nematol 33:285–288
Dabney SM, Delgado JA, Reeves DW (2001) Using cover crops to improve soil and water quality.
Commun Soil Sci Plant Anal 32:1221–1250
Davis JR, Huisman OC, Esterman DT, Hafez SL, Everson DO, Sorensen LH, Schneider AT
(1996) Effects of green manures on Verticillium wilt of potato. Phytopathology 86:444–453
Delate K, Friedrich H, Lawson V (2003) Organic pepper production systems using compost and
cover crops. Biol Agric Horticult 21:131–150
Derpsch R, Florentin MA (1992) Use of green manure cover crops as tools for crop rotation in
small farmer no-tillage systems in Paraguay: effects on soil temperature and yield of cotton,
In: Kopke U, Schulz DG (eds) Proceedings of the 9th International Science Conference
IFOAM: Organic agriculture, a key to a sound development and a sustainable environment,
Nov 16–21, Sao Paulo, Brazil pp 9–18.
Derpsch R, Sidiras N, Roth CH (1986) Results of studies made from 1977 to 1984 to control erosion by cover crops and no-tillage techniques in Parana, Brazil. Soil Tillage Res 8:253–263
Dhingra OD, Coelho Netto RA (2001) Reservoir and non-reservoir hosts of bean-wilt pathogen,
Fusarium oxysporum f. sp. Phaseoli. J Phytopathol 149:463–467
Dinesh R (2004) Long-term effects of leguminous cover crops on microbial indices and their
relationships in soils of a coconut plantation of a humid tropical region. J Plant Nutr Soil Sci
167:189–195
Dinesh R, Suryanarayana MA, Ghoshal CS, Sheeja TE, Shiva KN (2006) Long-term effects of
leguminous cover crops on biochemical and biological properties in the organic and mineral
layers of soils of a coconut plantation. Eur J Soil Biol 42:147–157
Ding G, Liu Z, Herbert S, Novak J, Amarasiriwardena D, Xing B (2006) Effect of cover crop
management on soil organic matter. Geoderma 130:229–239
Dogliotti S, Rossing WAH, Van Ittersum MK (2003) ROTAT, a tool for systematically generating
crop rotations. Eur J Agron 19:239–250
Dogliotti S, Rossing WAH, Van Ittersum MK (2004) Systematic design and evaluation of crop
rotations enhancing soil conservation, soil fertility and farm income: a case study for vegetable
farms in South Urugay. Agric Syst 80:277–302
Dogliotti S, Van Ittersum MK, Rossing WAH (2005) A method for exploring sustainable development options at farm scale: a case study for vegetable farms in South Uruguay. Agric Syst
86:29–51
54
J.M.S. Scholberg et al.
Douthwaite B, Keatinge JDH, Park JR (2002) Learning selection: an evolutionary model for
understanding, implementing and evaluating participatory technology development. Agric
Syst 72:109–131
Drinkwater LE, Snapp SS (2007) Nutrients in agroecosystems: rethinking the management paradigm. Adv Agron 92:163–186
El-Hage Scialabba N, Hattam C (2008) Organic agriculture, environment and food security, environment and natural resources series-4, FAO, Rome
Everts KL (2002) Reduced fungicide applications and host resistance for managing three diseases
in pumpkin grown on a no-till cover crops. Plant Dis 86:1134–1141
Fageria NK, Baligar VC, Bailey BA (2005) Role of cover crops in improving soil and row crop
productivity. Commun Soil Sci Plant Anal 36:2733–2757
Ferraz LCL, Café Filho AC, Nasser LCB, Azevedo J (1999) Effects of soil moisture, organic matter and grass mulching on the carpogenic germination of sclerotia and infection of beans by
Sclerotinia sclerotiorum. Plant Pathol 48:77–82
Fontanetti A, de Carvalho GJ, Gomes LAA, de Almeida K, de Moraes SRG, Teixeira CM (2006)
The use of green manure in crisphead lettuce and cabbage production. Horticult Bras
24:146–150
Gamliel A, Austerweil M, Kirtzman G (2000) Non-chemical approach to soil-born pest
management – organic amendments. Crop Prot 19:847–853
Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CAB International,
Wallingford, UK, 423 pp
Gilsanz JC, Arboleda J, Maeso D, Paullier J, Behayout E, Lavandera C, Sanders DC, Hoyt GD
(2004) Evaluation of limited tillage and cover crop systems to reduce N use and disease population in small acreage vegetable farms mirror image projects in Uruguay and North Carolina,
USA. In: Bertschinger L, Anderson JD (eds) Proceedings of XXVI IHC, sustainability of
horticultural systems, Acta Hort 638:163–169
Gliessman SR, Garcia ER, Amador AM (1981) The ecological basis for the application of traditional agricultural technology in the management of tropical agro-ecosystems. Agro Ecosyst
7:173–185
Gulick SH, Grimes DW, Munk DS, Goldhamer DA (1994) Cover-crop-enhanced water infiltration
of a slowly permeable fine sandy soil. Soil Sci Soc Am J 58:1539–1546
Gutiererez Rojas IR, Perez R, Fones D, Borroto M, Lazo M, Rodriguez L, Diaz JA (2004) The use
of two life legume cover crops and their effects on weeds in citrus fields. III Congreso 2004
Sociedad Cubana de Malezologia, Memorias, Jardin Botanico Nacional, Ciudad Havana, pp
79–82
Hansen JP, Eriksen J, Jensen LS (2005) Residual nitrogen effect of dairy crop rotation as influenced by grass-clover ley management, manure type and age. Soil Use Manage 21:278–286
Hartwig NL, Ammon HU (2002) Cover crops and living mulches. Weed Sci 50:688–699.
Hiltbrunner J, Liedgens M, Bloch L, Stamp P, Streit B (2007) Legume cover crops as living
mulches for winter wheat: components of biomass and the control of weeds. Eur J Agron
26:21–29
Honeycutt CW, Potaro LJ (1990) Field evaluation of heat units for predicting crop residue carbon
and nitrogen mineralization. Plant Soil 125:213–220
Horlings I (1998) Agricultural change and innovation groups in the Netherlands. In: Haan H,
Kasims B, Redclift M (eds) Sustainable rural development. Ashgate Publishing Ltd, Aldershot,
UK, pp 159–175
Hudson BD (1994) Soil organic matter and available water capacity. J Soil Water Conserv
49:189–194
Isaac WA, Brathwaite RAI, Ganpat WG, Bekele I (2007) The impact of selected cover crops on
soil fertility, weed and nematode suppression through farmer participatory research by
Fairtrade banana growers in St. Vincent and the Grenadines. World J Agricult Sci 3:371–379
Isse AA, MacKenzie AF, Stewart K, Cloutier DC, Smith DL (1999) Cover crops and nutrient
retention for subsequent sweet corn production. Agron J 91:934–939
Jenkins SF, Averre C (1986) Problems and progress in integrated control of southern blight of
vegetables. Plant Dis 70:614–619
2
Cover Crops for Sustainable Agrosystems in the Americas
55
Keatinge JDH, Qi A, Wheeler TR, Ellis RH, Summerfield RJ (1998) Effects of temperature and
photoperiod on phenology as a guide to the selection of annual legume cover and green manure
crops for hillside farming systems. Field Crops Res 57:139–152
Kruidhof HM (2008) Cover crop-based ecological weed management: exploration and optimization. Dissertation Wageningen University, Wageningen, The Netherlands, 156 pp
Kuo S, Sainju UM (1997) Nitrogen mineralization and availability of mixed leguminous and nonleguminous cover crop residues. Biol Fertil Soils 26:346–353
Lal R, Kimble JM, Eswaran H, Alton B (2000) Global climate change and tropical ecosystems.
CRC Press, Boca Raton, FL, 438 pp
Landers JN (2001) How and why the Brazilian zero tillage explosion occurred. In: Stott DE,
Mohtar RH, Steinhardt GC (eds) Sustaining the global farm, Selected papers from the 10th
international soil conservation organisation, Purdue University, West Lafayette, 24–29 May
2001, pp 29–39.
Lemaire G, Gaston F (1997) Nitrogen uptake and distribution in plant canopies. In: Lemaire G
(ed) Diagnosis of the nitrogen status in crops. Springer, Heidelberg, pp 3–43
Linares JC, Scholberg JMS, Boote KJ, Chase CA, Ferguson JJ, McSorley RM (2008) Use of the
cover crop weed index to evaluate weed suppression by cover crops in organic citrus orchards.
HortScience 43:27–34
Lu Y, Watkins KB, Teasdale JR, Abdul-Baki AA (2000) Cover crops in sustainable food production. Food Rev Int 16:121–157
Luna-Orea P, Wagger MG (1996) Management of tropical legume cover crops in the Bolivian
Amazon to sustain crop yields and soil productivity. Agron J 88:765–776
Ma L, Peterson GA, Ahuja LR, Sherrod L, Shaffer MJ, Rojas KW (1999) Decomposition of surface crop residues in long-term studies of dryland agroecosystems. Agron J 91:401–409
Madden NM, Mitchell JP, Lanini WT, Cahn MD, Herrero EV, Park S, Temple SR, van Horn M
(2004) Evaluation of no tillage and cover crop systems for organic processing tomato production. HortTechnology 14:243–250
Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Rapidel B, de
Tourdonnet S, Valantin-Morison M (2009) Mixing plant species in cropping systems: concepts, tools and models. A review. Agron Sustain Dev 29:43–62
Manici LM, Caputo F, Babini V (2004) Effect of green manure on Phytium spp. Population and
microbial communities in intensive cropping systems. Plant Soil 263:133–142
Masiunas JB (1998) Production of vegetables using cover crops and living mulches: a review.
J Veg Crop Prod 4:11–31
Matheis HASM, Victoria Filho R (2005) Cover crops and natural vegetation mulch effect achieved
by mechanical management with lateral rotary mower in weed population dynamics in citrus.
J Environ Sci Health 40:185–190
Matus FJ, Lusk CH, Maire CR (2008) Effects of soil texture, carbon input rates, and litter quality
on free organic matter and nitrogen mineralization in Chilean rain forest and agricultural soil.
Commun Soil Sci Plant Anal 39:187–201
Mays DA, Sistani KR, Malik RK (2003) Use of winter annual cover crops to reduce soil nitrate
levels. J Sustain Agric 21:5–19
Mazoyer M, Roudart L (2006) A history of world agriculture: from the Neolithic to the current
crisis. Monthly Review Press, New York, 528 pp
Mazzola M (2004) Assessment and management of soil microbial community structure for disease suppression. Annu Rev Phytopathol 42:35–59
McNeill JR, Winiwarter V (2004) Breaking the sod: humankind, history, and soil. Science
304:1627–1629
McSorley R (2001) Multiple cropping systems for nematode management: a review. Proc Soil
Crop Sci Soc Fla 60:1–12
Metay A, Moreira JAA, Bernoux M, Boyer T, Douzet J, Feigl B, Feller C, Maraux F, Oliver R,
Scopel E (2007) Storage and forms of organic carbon in no-tillage under cover crops systems
on clayey Oxisol in dryland rice production (Cerrados, Brazil). Soil Tillage Res 94:122–132
Miguez FE, Bollero GA (2005) Review of corn yield response under winter cover cropping systems using meta-analytic methods. Crop Sci 45:2318–2329
56
J.M.S. Scholberg et al.
Mitchell JP, Peters DW, Shennan C (1999) Changes in soil water storage in winter fallowed and
cover cropped soils. J Sustain Agric 15:19–31
Miyao G, Hartz TK, Johnstone PR, Davis RM, Kochi M (2006) Influence of mustard cover crops
on tomato production in the Sacramento valley. In: Ashcroft WJ (ed) Proceedings of the 9th
international symposium on processing tomato. Acta Hort 724:177–181
Miyao G, Robins P (2001) Influence of fall-planted cover crops on rainfall run-off in a processing
tomato production system. In: Hartz TK (ed) Proceedings of the 7th international symposium
on processing tomato. Acta Hort 542:343–345
Moonen AC, Barberi P (2006) An ecological approach to study the physical and chemical effects
of rye cover crops residues on Amaranthus retroflex, Ecinochloa crus-galli and maize.
Ann Appl Biol 148:73–89
Neill SP, Lee DR (2001) Explaining the adoption and disadoption of sustainable agriculture: the
case of cover crops in Northern Honduras. Econ Dev Cult Change 49:793–820
Ngouajio M, McGiffen ME, Hutchinson CM (2003) Effect of cover crops and management system
on weed populations in lettuce. Crop Prot 22:57–64
Ntahimpera N, Ellis MA, Wilson LL, Madden LV (1998) Effects of a cover crops on splash
dispersal of Colletotrichum acutatum conidia. Phytopathology 88:536–543
Nyende P, Delve RJ (2004) Farmer participatory evaluation of legume cover crops and biomass
transfer technologies for soil fertility improvement using farmer criteria, preference ranking
and logit regression analysis. Expl Agric 40:77–88
Pegoraro RF, Silva IR, Novais RF, Mendonca ES, Alvarez VH, Nunes FN, Fonseca FM, Smyth
TJ (2005) Diffusive flux of cationic micronutrients in two oxisols as affected by low-molecular-weight organic acids and cover crops residues. J Plant Nutr Soil Sci 168:334–341
Peigné J, Ball BC, Roger-Estrade J, David C (2007) Is no tillage suitable for organic farming?
A review. Soil Use Manage 23:12–29
Phatak SC, Dozier JR, Bateman AG, Brunson KE, Martini NL (2002) Cover crops and no tillage
in sustainable vegetable production. In: van Santen E (ed) Making no tillage conventional:
building a Future on 25 Years of research. Proceedings of the 25th Annual Southern Conservation
Tillage Conference for Sustainable Agriculture, Auburn, AL, 24–26 June, pp 401–403
Pieri C, Evers G, Landers J, O’Connel P, Terry E (2002) A road map from conventional to no-till
farming, Agriculture & Rural Development Working Paper, The International Bank for
Reconstruction and Development, Washington D.C., 20 pp
Pieters AJ (1927) Green Manuring. Willey, New York
van der Ploeg JP (2008) The new peasantries, struggles for autonomy and sustainability in an era
of empire and globalization. Earthscan, London, 356 p
Prado Wildner do L, Hercilio de Freitas V, McGuire M (2004) Use of green manure/cover crops
and no tillage in Santa Catarina, Brazil. In: Eilittä M et al. (eds) Green manures/cover crops
systems of smallholder farmers: experiences from tropical and subtropical regions. Kluwer,
The Netherlands, pp 1–36
Quemada M, Cabrera ML, McCracken DV (1997) Nitrogen release from surface-applied cover
crops residues: evaluating the Ceres-N model. Agron J 89:723–729
Ristaino JB, Parra G, Campbell CL (1997) Suppression of Phytophthora blight in bell pepper by
a no-till wheat cover crops. Phytopathology 87:242–249
Roldan A, Caravaca F, Hernandez MT, Garcia C, Sanchez-Brito C, Velasquez M, Tiscareno M
(2003) No-tillage, crop residue addition, and legume cover cropping effects on soil quality
characteristics under maize in Patzcuaro watershed (Mexico). Soil Tillage Res 72:65–73
Ruffo ML, Bollero GA (2003) Modelling rye and hairy vetch residue decomposition as a function
of degree-days and decomposition-days. Agron J 95:900–907
Russell EJ (1913) The fertility of the soil. Cambridge University Press, London
Sainju UM, Singh BP, Whitehead WF, Wang S (2006) Accumulation and crop uptake of soil mineral
nitrogen as influenced by tillage, cover crops and nitrogen fertilization. Agron J 99:682–691
Sainju UM, Singh BP, Whitehead WF, Wang S (2007) Carbon supply and storage in tilled and
non-tilled soils as influenced by cover crops and nitrogen fertilization. J Environ Qual 35:
1507–1517
2
Cover Crops for Sustainable Agrosystems in the Americas
57
Sanchez EE, Giayetto A, Cichon L, Fernandez D, Aruani MC, Curetti M (2007) Cover crops
influence soil properties and tree performance in an organic apple (malus domestica Borkh)
orchard in northern Patagonia. Plant Soil 292:193–203
Sarrantonio M, Gallandt E (2003) The role of cover crops in North American cropping systems.
J Crop Prod 8:53–74
Schomberg HH, Martini NL, Diaz-Perez JC, Phatak SC, Balkcon KS, Bhardwaj HL (2007)
Potential for using sunn hemp as a source of biomass and nitrogen for the Piedmont and
coastal regions of the Southeastern USA. Agron J 99:1448–1457
Schomberg HH, Steiner JL, Unger PW (1994) Decomposition and nitrogen dynamics of crop residues: residue quality and water effects. Soil Sci Soc Am J 58:371–381
Schroth G, Salazar E, Da Silva JP (2001) Soil nitrogen mineralization under tree crops and a
legume cover crops in multi-strata agroforestry in Central Amazonia: spatial and temporal
patterns. Expl Agric 37:253–267
Selaya Garvizu NG (2000) The Role of Green Manure and Crop Residues in Cropping Systems
of South Uruguay, Wageningen University and Research Center, Wageningen, the Netherlands,
63 pp.
Shennan C (1992) Cover crops, nitrogen cycling, and soil properties in semi-irrigated vegetable
production systems. HortScience 27:749–754
Shennan C (2008) Biotic interactions, ecological knowledge and agriculture. Philos Trans R Soc
B 363:717–739
Singer JW, Nusser SM (2007) Are cover crops being used in the US corn belt? J Soil Water
Conserv 62:353–358
Smil V (2001) Enriching the earth; Fritz Haber, Carl Bosch, and the transformation of world food
production. MIT Press, Cambridge, MA
Snapp SS, Borden H (2005) Enhanced nitrogen mineralization in mowed or glyphosate treated
cover crops compared to direct incorporation. Plant Soil 270:101–112
Steiner JL, Schomberg HH, Unger PW (1996) Predicting crop erosion and cover for wind erosion
simulati006Fns. http://www.weru.ksu.edu/symposium/proceedings/steiner.pdf. Accessed 2
July 2008; verified 2 October 2008)
Sullivan P (2003) Overview of cover crops and green manures. ATTRA Publication #IP024,
National Center for Appropriate Technology, Butte, MT
Sustainable Agriculture Network (2007) Managing cover crops profitably. Sustainable agriculture
network handbook series. Book 3, 3rd edn. Sustainable Agriculture Network, Beltsville, MD.
www.sare.org/publications/covercrops/covercrops.pdf. Accessed 2 June 2008; verified 2008
Taylor CR, Rodríguez-Kábana R (1999a) Population dynamics and crop yield effects on nematodes
and white mold in peanuts, cotton and velvet beans. Agric Syst 59:177–191
Taylor CR, Rodríguez-Kábana R (1999b) Optimal rotation of peanuts and cotton to manage soilborne organisms. Agric Syst 61:57–68
Teasdale JR, Abdul-Baki AA (1998) Comparison of mixtures vs monocultures of cover crops for
fresh-market tomato production with and without herbicide. HortScience 33:1163–1166
Teasdale JR, Abdul-Baki AA, Mills DJ, Thorpe KW (2004) Enhanced pest management with
cover crops mulches. In: Bertschinger L, Anderson JD (eds) Proceedings of the XXVI IHC,
Sustainability of horticultural systems. Acta Hort 638:135–140
Teasdale JR, Brandsaeter LO, Calegari A, Neto FS (2007) Cover crops and weed management. In:
Upadhyaua MM, Blackshaw RE (eds) Non-chemical weed management: principles, concepts
and technology. CAB International, Wallingford, UK, pp 49–64
Tillman G, Schomberg H, Phatak S, Mullinex B, Lachnicht S, Timper P, Olson D (2004) Influence
of cover crops on insect pests and predators in no tillage cotton. J Econ Entomol 97:1217–1232
Tittonell P (2008) Targeting resources within diverse, heterogeneous and dynamic farming systems of east Africa. Ph.D. dissertation, Wageningen University, Wageningen, the Netherlands,
320 pp
Tonitto C, David MB, Drinkwater LE (2006) Replacing bare fallows with cover crops in fertilizerintensive cropping systems: a meta-analysis of crop yields and N dynamics. Agric Ecosyst
Environ 112:58–72
58
J.M.S. Scholberg et al.
Tracey SM, Coe HS (1918) Velvet beans. Farmers Bulletin 962. United States Department of
Agriculture, Washington, DC, USA
Treadwell DD, Creamer NG, Schultheis JR, Hoyt GD (2007) Cover crop management affects
weeds and yield in organically managed sweet potato systems. Weed Technol 21:1039–1048
Triplett GB, Dick WA (2008) No-tillage crop production: a revolution in agriculture! Agron J
100:S153–S165
Van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and
disease suppression. Appl Soil Ecol 15:13–24
Van der Burgt GJHM, Oomen GJM, Habets ASJ, Rossing WAH (2006) The NDICEA model, a
tool to improve nitrogen use efficiency in cropping systems. Nutr Cycl Agroecosyst
74:275–294
Van Elsas JD, Garbeva P, Salles J (2002) Effects of agronomical measures on the microbial diversity
of soils as related to the suppression of soil-borne plant pathogens. Biodegradation 13:29–40
Veenstra JJ, Horwath WR, Mitchell JP (2007) Tillage and cover cropping effects on aggregateprotected carbon in cotton and tomato. Soil Sci Soc Am J 71:362–371
Vidal M, Lopez A (2005) Cover crops and organic amendments to prevent nitrate contamination
under a wet climate. Agronomie 25:455–463
Villarreal-Romero M, Hernandez-Verdugo S, Sanchez-Pena P, Gracia-Estrada RS, Osuna-Enciso
T, Parra-Terrazas S, Arementa-Bojorquez AD (2006) Effect of cover crops on tomato yield and
quality. Terra Lat Am 24:549–556
Wang Q, Klassen W, Li Y, Codallo M (2005) Influence of cover crops and irrigation rates on
tomato yields and quality in a subtropical region. HortScience 40:2125–2131
Wang Q, Li Y, Klassen W (2006) Summer cover crops and soil amendments to improve growth
and nutrient uptake of Okra. HortTechnology 16:328–338
Wang Q, Li Y, Hando Z, Klassen W (2007) Influence of cover crops on populations of soil nematodes. Nematropica 37:79–92
Weil R, Kremen A (2007) Thinking across and beyond disciplines to make cover crops pay. J Sci
Food Agric 87:551–557
Widmer TL, Mitkowsky NA, Abawi GS (2002) Soil organic matter and management of plant–
parasitic nematodes. J Nematol 34:289–295
Wiggins BE, Kinkel LL (2005a) Green manures and crop sequences influence potato diseases and
pathogen inhibitory activity of indigenous streptomycetes. Phytopathology 95:178–185
Wiggins BE, Kinkel LL (2005b) Green manures and crop sequences influence alfalfa root rot and
pathogen inhibitory activity among soil-borne streptomycetes. Plant Soil 268:271–283
Wilke BJ, Snapp SS (2008) Winter cover crops for local ecosystems: linking plant traits and
ecosystems functions. J Sci Food Agric 88:551–557
Wyland LJ, Jackson LE, Chaney WE, Klonsky K, Koike ST, Kimple B (1996) Winter cover crops
in a vegetable cropping system: impacts on nitrate leaching, soil water, crop yield, pests and
management costs. Agric Ecosyst Environ 59:1–17
Yang HS, Janssen BH (2000) A mono component model of carbon mineralization with a dynamic
rate constant. Eur J Soil Sci 51:517–529
Yang HS, Janssen BH (2002) Relationship between substrate initial reactivity and residue ageing
speed in carbon mineralization. Plant Soil 239:215–224
Yin X, Goudriaan J, Lantinga E, Vos J, Spiertz HJ (2003) A flexible sigmoid function of determinate
growth. Ann Bot 91:361–371
Zotarelli L, Alves BJR, Urquiaga S, Torres E, dos Santos HP, Paustian K, Boddey RM, Six J
(2005a) Impact of tillage and crop rotation on light fraction and intra-aggregate soil organic
matter in two oxisols. Soil Tillage Res 95:196–206
Zotarelli L, Alves BJR, Urquiaga S, Torres E, dos Santos HP, Paustian K, Boddey RM, Six J
(2005b) Impact of tillage and crop rotation on aggregate-associated carbon in two oxisols. Soil
Sci Soc Am J 69:482–491
Zotarelli L, Alves BJR, Urquiaga S, Boddey RM, Six J (2007) Impact of tillage and crop rotation
on light fraction and intra-aggregate soil organic matter in two oxisols. Soil Tillage Res
95:196–206
Chapter 3
Cover Crops in Agrosystems: Innovations
and Applications
Johannes M.S. Scholberg, Santiago Dogliotti, Lincoln Zotarelli,
Corey M. Cherr, Carolina Leoni, and Walter A.H. Rossing
Abstract Cover crops can reduce the dependence of farmers on agrochemicals while
enhancing overall agrosystem’s performance. However, the inherent complexity of cover-crop-based systems hampers their adoption by conventional farmers.
Therefore, special management skills and alternative research and technology transfer
approaches may be required to facilitate their adoptive use by conventional farmers.
We propose that development and adoption of suitable cover-crop-based production
systems may require the use of an “innovation framework” that includes (1) identification of system constraints, (2) analysis of system behavior, (3) exploration of
alternative systems, and (4) system design and selection. We describe case studies
from four regions of the Americas (Florida, USA; Paraná and Santa Catarina,
Brazil; and Canelones, Uruguay) that illustrate the relationships between this innovation framework and the development and adoption of cover-crop-based production systems. Where successful, development and adoption of such systems appear
to relate to a number of attributes including (1) active involvement by farmers in
J.M.S. Scholberg (*) and W.A.H. Rossing
Biological Farming Systems, Wageningen University, Post Box 563, 6700 AN,
Wageningen, The Netherlands
e-mail: johannes.scholberg@wur.nl
S. Dogliotti
Facultad de Agronomía, Universidad de la República, Avda. Garzón 780, Código Postal 12900,
Montevideo, Uruguay
L. Zotarelli
Agricultural and Biological Engineering Department, University of Florida, 234 Fraziers-Rogers
Hall, Gainesville FL32611, USA
C.M. Cherr
Department of Plant Sciences and Graduate Group in Ecology, University of California,
Davis, CA95616, USA
C. Leoni
Instituto Nacional de Investigación Agropecuaria – Estación Experimental Las Brujas,
Ruta 48 km 10 Código Postal 90200, Rincón del Colorado – Canelones, Uruguay
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_3, © Springer Science+Business Media B.V. 2010
59
60
J.M.S. Scholberg et al.
research and dissemination programs; (2) integration of cover crops into production
systems without net loss of land or labor resources; (3) informing farmers of the
(direct) benefits of cover crop use; (4) provision of multiple benefits by cover crops,
(5) sufficient access to information, inputs, and technologies required for cover crop use;
and (6) provision of skills and experience necessary to manage cover crops effectively. Where these attributes are absent and failure to innovate has prevented
development and adoption of cover-crop-based systems, policy initiatives to reward
farmers for ecological services provided by cover crops may be required.
Keywords Cover crops • green technologies • system analysis • innovation
• adoption • sustainability • Americas • green manure • living mulch
Abbreviation
SOM
soil organic matter
3.1 Introduction
Cover crops are extensively used to provide a wide array of services (Scholberg
et al. 2009). In this review, we do not distinguish between specific applications
such as their use for enhancing soil fertility, e.g., green manures, and cultivation
techniques by which cover crops are grown simultaneously with commercial
crops, e.g., live mulches. We therefore use the term “cover crop” in its broadest
context instead.
Historically, cover crops have been an integral part of agricultural production
systems (Scholberg et al. 2009). Technological innovations have greatly enhanced
agricultural productivity over the last 60 years, but have also eroded many traditional techniques used to sustain inherent soil fertility – including the use of cover
crops (Altieri 2002). During this period, many farmers throughout Latin America
were caught in cycles of unsustainability related to overexploitation or pollution of
water resources, soil erosion, loss of inherent soil fertility, increasing impacts of
weeds and pests on crop yields, decreasing agricultural commodity values, and
increases in external input prices. Local producers often responded to decreasing
family income by intensifying their production (Dogliotti et al. 2005). Typically,
this resulted in a shift toward cash crops, increased use of marginal lands, and
greater dependence on external capital and labor and production inputs. This process favored further marginalization of local production systems (van der Ploeg
2008; Dogliotti et al. 2005; Cherr et al. 2006b) and saw many farmers and their
families leave agricultural production and rural areas altogether. Increased global
demand of crops for animal feed concentrates and biofuels has further intensified
pressure on land resources (Corral et al. 2008). Although such production systems
3
Cover Crops in Agrosystems: Innovations and Applications
61
may generate local income and employment, these short-term economic benefits do
not offset the loss of the long-term agricultural production capacity and human
capital of local agricultural communities. Moreover, with current concerns about
food security, global warming, and demands for a broader range of agricultural
services, unsustainable resource exploitation is highly undesirable. Therefore, there
is a need for more sustainable production options and more effective use of local or
renewable resources (van der Ploeg 2008; Cherr et al. 2006b). Within this context,
cover crops may once again become a cornerstone of sustainable agricultural systems (Scholberg et al. 2009). However, the complexity of cover-crop-based systems
combined with the need to maintain reliably high crop yields requires the use of
system analysis tools and active engagement of end-users (Shennan 2008; Cherr
et al. 2006b). Involvement of the main stakeholders is particularly important, since
any intentional change in production systems is always a result of changes in
human conduct and therefore requires an individual and collective learning process
(Leeuwis 1999). Moreover, solutions to complex problems do not come as “instant
technology packages.” Rather, they need to be designed within its context of application with the direct involvement of farmers at all stages of the process, from
diagnosis to dissemination (Leeuwis 1999; Masera et al. 2000). This is the only
way to ensure relevance, applicability, and adoption of such innovations. Thus,
technological innovations such as improved use of cover crops must be explored
more efficiently, while farmers must be allowed to more effectively contribute to
technology development and transfer, thereby fostering successful and sustainable
development (Rossing et al. 2007). Thus, the scope of this chapter is to
1. Provide a conceptual framework for innovation of cover-crop-based systems
2. Contextualize the components of this innovation framework as related to current
cover-crop research and development strategies, with emphasis on system
analysis tools
3. Describe innovation and technology transfer processed of cover-crop systems in
several regions in the Americas
3.2 A Framework for Innovation of Cover-Crop-Based
Systems
As biological organisms, cover crops interact with many aspects of a cropping
system and its environment. The use of reductionist approaches, small-plot studies,
and short-term research is common in agricultural science but may be poorly suited
for development and evaluation of suitable cover-crop management strategies
(Cherr et al. 2006b). Despite the large number of research and review publications
centered on cover crops over the past decade, a conceptual framework and a
systems’ perspective that critically evaluates cover crops is lacking. Systems
research uses an interdisciplinary approach to design and analyze agroecosystems
functioning at different spatiotemporal and qualitative scales (Malézieux et al.
62
J.M.S. Scholberg et al.
Re-assessments,
monitoring &
evaluation
(e.g., n =100)
Farm system typology,
socioeconomic clustering
Detailed system
characterisation
Case study farms
(e.g., n = 5 ×type)
Crop, livestock and
household sub-systems
typologies
Quantitative
subsystems
analysis
Simplified
ideotypes
(n = 1 ×type)
Quantified resource flows,
stocks, and allocation
decisions
Scenarios,
tradeoff analysis
and explorations
Contribution to
system (re-)design,
discussion support,
research agenda
and policy making
Model output
Computer-based
On-farm methods
Rapid system
characterisation
Sample of
farms
Integrated
assessment of the
farming system(s)
Fig. 3.1 Consecutive steps during farm analysis showing the complementation of both participatory and computer-based exploration and optimization approaches (Tittonell 2008)
2009; Shennan 2008; Drinkwater 2002). The underlying premise of system analysis
and design is the use of cyclic knowledge development requiring active involvement from all key stakeholders. Ideally, this framework complements conventional
research approaches, as shown in Fig. 3.1 (Tittonell 2008; Rossing et al. 2007). It
includes the following:
1. Characterization and diagnosis of constraints: Description of the biophysical and
socioeconomic system and defining constraints
2. Analysis of system behavior: explanation of the system behavior in terms of the
constraints. The design of such a research may involve an initial assessment of
native agricultural systems and models of ecological interactions (Shennan 2008;
Altieri and Nicholls 2004)
3. Exploration of alternative systems: For example, generating different crop rotations and management practices either in reality or via simulation
4. Design of alternative system: Development or utilization of more efficient, profitable, or sustainable systems (i.e., via the use of trade-off analysis, model simulations, and optimization; see Fig. 3.1)
We emphasize that each component of the innovation framework is a process rather
than an event, and there may be much overlap among the components. For example, integrating system analysis and design with applied field research and
3
Cover Crops in Agrosystems: Innovations and Applications
63
modeling techniques allows improved assessment of system constraints, explanation
of behavior, and exploration of alternatives (Tittonell 2008). Within this context,
field studies and data collection should be structured in such a manner that they can
be used for calibration of simulation models and verification of model performance
(Hasegawa et al. 1999). Such models, in turn, can then be used to explore more
sustainable development options (Selaya Garvizu 2000).
We also explore the fourth component (design or selection of a system) by using
the vehicle of technology development, adaptation, and transfer – which obviously
overlaps the other three components. Nonetheless, we believe that the innovation
framework we are proposing is a powerful approach for the development of viable
cover-crop-based production systems.
3.2.1 Characterization and Diagnosis of Constraints
We organize the constraints on cover crop systems into three broad categories:
biophysical, socioeconomic, and information and technology constraints. The categories are not necessarily mutually exclusive. We also briefly examine solutions
to some of these constraints, which involve further steps in the innovation framework we are suggesting.
3.2.1.1 Biophysical Constraints
Although the use of cover crops is perceived to enhance production and provide a
myriad of services, their adaptation by conventional farmers in North America has
been slow (Sarrantonio and Gallandt 2003). The key issue may include the additional cost (in terms of land, labor, and inputs), the complexity of cover-crop-based
systems, the lack of pertinent information, and the uncertainty of release patterns
from cover-crops residues, and the lack of secure land tenure (Cherr et al. 2006b;
Sarrantonio and Gallandt 2003; Lu et al. 2000). Since cover-crop-based systems
depend on biological and ecological processes, this makes their management more
complex when compared with the use of synthetic fertilizers. Most farmers are
poorly equipped to take the economic risk associated with experimentation and
exploration of suitable cover-crops technologies (Weil and Kremen 2007; Cherr
et al. 2006b).
For example, severe yield reduction can occur when increased plant competition
results from live mulch or incompletely killed cover crops (Hiltbrunner et al. 2007;
Teasdale et al. 2007; Madden et al. 2004). Without adequate precautions, covercrop residue may also interfere with soil cultivation, reduce subsequent crop seed
germination (owing to poor soil–seed contact), delay planting operations (since
residues need some time to decompose/die), harbor pests and diseases that attack
subsequent crops (if the cover crop and subsequent crop host the same pests or diseases),
decrease initial crop growth or delay crop maturity (owing to N immobilization,
64
J.M.S. Scholberg et al.
allelopathy, plant competition, or reduced soil temperatures), or reduce soil water
availability (Peigné et al. 2007; Sustainable Agricultural Network 2007; Teasdale
et al. 2007; Weil and Kremen 2007; Avila 2006; Cherr et al. 2006b; Sarrantonio and
Gallandt 2003; Abdul-Baki et al. 1996, 1999; Masiunas 1998; Creamer et al. 1996).
Poor synchronization of N release from decomposing cover crops and N uptake by
subsequent crops will also result in high N losses (Cherr 2004).
However, if researchers become aware of these issues, then it is often possible
to address them through redesign of the cover-crop system. In an example with
vegetable crops, use of cover crops combined with zero-tillage reduced initial
growth of vegetable crops and prevented growers from targeting the most profitable
market windows. Once growers and researchers communicated about the problem,
they identified a solution through the use of strip tillage. Such adaptive learning and
innovation cycles are critical and therefore will be discussed in more detail in a
subsequent section.
3.2.1.2 Socioeconomic Constraints
Technological development has often been perceived as a task of research institutions
that subsequently transfer solutions to farmers. Unfortunately, this “top-down”
approach frequently fails because it does not adequately include local socioeconomic and environmental conditions in the process of development (Anderson et al.
2001). On-station researcher-managed studies favor highly controlled conditions
and research that may not be relevant to growers unless they are actively involved
during the design of studies. Several alternative approaches for developing regions
have been outlined (e.g., Altieri 2002; Anderson et al. 2001; Giller 2001).
Karlen et al. (2007) outlined and discussed different institutional arrangements
(management models) for sharing resources and responsibilities between farmers
and researchers. On-farm research often appears risky and costly to participating
growers – especially when experimental treatments conflict with growers’ production
objectives. Grower intervention in such situations can lead to lack of adequate
experimental control (Karlen et al. 2007). From the researcher’s perspective, results
of such on-farm studies may be site- or farm-specific with confounding sources of
variation (Shennan 2008). However, on-farm studies also tend to be more realistic
in terms of scale (field vs. plot), management practices used, and actual production
constraints, while they also allow development of chronosequences (e.g., comparing system dynamic at different system development stages) within a relatively
short period of time (Drinkwater 2002).
A workshop elucidating opinions of key stakeholders involved in the transfer
and adoption of cover-crop-based systems in Latin America indicated that the key
factor controlling adaptation of cover crops were nontechnical and include poor
seed availability of annual cover crops (Anderson et al. 2001). In Northern
Honduras, adaptation of Mucuna spp. as a cover crop in maize systems was abandoned by farmers if land tenure was not secure (Neill and Lee 2001). Additional
hindrances for improved integration of cover crops in existing cropping systems
3
Cover Crops in Agrosystems: Innovations and Applications
65
may include local perceptions and policies (e.g., local research and extension staff
favoring conventional high-input-based technologies to risk-averse small producer
rather than fostering traditional legume-based mixed cropping systems (Anderson
et al. 2001)). In many cases, researchers and policy-makers may promote their own
political agenda (e.g., reducing environmental impacts, minimizing external inputs,
and enhancing sustainability) instead of addressing end-user needs. Weil and
Kremen (2007) reported that in Maryland, cover crops were only grown on 20–25%
of the agricultural land during winter fallow despite farmers receiving $50–100
subsidies for growing such crops. Despite their inherent desire to provide good
stewardship of local land resources, farmers face the reality of economic survival
and may not be in a position to provide environmental services without tangible,
direct benefits (Weil and Kremen 2007). Unless farmers are aware of these direct
benefits of the use of cover crops, they may be reluctant to integrate them into their
existing cropping systems. In many cases, the use of cover crops may not be
cost-effective unless they provide multiple benefits and services (Avila et al. 2006a, b;
Cherr et al. 2006b; Abdul-Baki et al. 2004).
3.2.1.3 Information and Technology Constraints
Constraints on cover crop use in Latin America include the lack of communication
among different stakeholders (Anderson et al. 2001). In the Mid-Western USA,
farmers indicated the greatest obstacle to development and adoption of cover-crop
technology was lack of basic information (Singer and Nusser 2007). Armed with
basic information about selection, management, and services of potential cover
crops, many farmers might independently test and evaluate these species.
Interestingly, much research has been conducted in these areas in North America.
A search of the ISI Web of Knowledge for journal publications including “cover
crop” or “green manure” or “living mulch” within the topic found over 10,000
manuscripts between 1923 and 2007. Over 61% of these manuscripts were recent
(published since 1990) and most seem to be focused on North American production
systems. Despite such an impressive increase in publication numbers, North
American producers still cite lack of information about green manure and cover
crops as one of the greatest barriers to their use (Singer and Nusser 2007). This
indicates that information is not lacking, but that it is not transferred effectively.
Historically, most international agricultural research was commodity-based with
the main focus being on increasing yields via intensification; use of interdisciplinary
and participatory research approaches was limited (Altieri 2002). Over time,
research has become more “integrated” and “holistic.” This may be related to
increased integration of ecological approaches into mainstream agricultural
research (Delate 2002) and the disillusion of green-revolution-based technologies
to enhance the livelihoods of farmers in more marginal production settings (Bunch
2000). Current advances in system ecology may be thus used to design and test
cropping systems with enhanced plant diversity to improve the functioning of
agroecosystems rather than reinstating traditional crop rotations (Drinkwater and
66
J.M.S. Scholberg et al.
Snapp 2007). However, considering the North American example, this evolution in
research will almost certainly not lift constraints to cover-crop use unless producer’s
involvement is improved as well.
3.2.2 System Analysis
Effective research on cover crops inherently requires a system focus and use of
long-term studies (Shennan 2008; Cherr et al 2006a). In the current academic
climate, implementing this on a field scale may be challenging; extramural funding
opportunities for applied long-term farming systems research are limited and
within research institutions there exists a growing demand for scientists to generate
information and publications quickly and focus more on fundamental research. As a
result, most cover-crop publications focus on single system aspects including
end-of-season biomass or N accumulation for specific production settings and final
yields of subsequent crops. There are some research examples where the relationship between cover-crop growth and environmental conditions were captured
(Cherr et al 2006b, Schomberg et al. 2007). When environmental conditions are
known or can be predicted, models may be used for assessing cover-crop growth
and subsequent decomposition, N release, and long-term impacts to other production systems. Likewise, such models can be applied for system analysis and design,
by using field studies for development and calibration of these models (Stoorvogel
et al. 2004). Within this context, the use of validated simulation tools will allow of
extrapolation of results to other production settings or future scenarios. By utilizing
on-farm data to develop and extrapolate such models, researchers therefore can
more effectively identify benefits and constraints of cover-crop-based systems.
Integration of cover crops requires modification of the existing crop rotation
schemes and design of the suitable alternative rotations (Selaya Garvizu 2000).
Although this may be accomplished by trial and error, this is time-consuming,
costly, and risky (van der Burgt et al. 2006; Keatinge et al. 1998). The need for
quantitative assessment of complex systems across different production environments
thus justifies the use of simulation models to integrate processes at a field scale in
a more cost-effective manner (Sommer et al. 2007; Stoorvogel et al. 2004; Lu et al.
2000). The use of such models may provide a better insight into both short-term
dynamics and long-term system behavior. This can facilitate an improved understanding of processes that are either difficult or costly to measure at different spatial
and temporal scales such as long-term effects of cover crop residue management on
erosion, production, profits, N leaching, and soil quality (Sommer et al. 2007;
Dabney et al. 2001; Lu et al. 2000; Selaya Garvizu 2000).
Lu et al. (2000) used the EPIC model to compare the use of conventional, covercrop-based, and manure-based corn–soybean systems for a period of 60 years. The
authors showed that the use of cover crops could greatly reduce external fertilizer
requirements and environmental risk, while gross margins were reduced only by 10%.
These approaches may also be used to rapidly design viable alternative crop rotation
3
Cover Crops in Agrosystems: Innovations and Applications
67
schemes (Bachinger and Zander 2007; Dogliotti et al. 2003) or alternative production
systems (Tittonell 2008; Dogliotti et al. 2005). Such models may range from simple
integration of user knowledge and expertise to complex mechanistic models
(Stoorvogel et al. 2004). Alternatively, models may focus on either tactical topics (e.g.,
with a focus on in-season management decisions) or strategic topics (e.g., design of
long-term crop rotation or design and evaluation of alternative farming systems).
In terms of cover-crops systems, short-term decomposition dynamics of soilapplied cover-crop residues are typically included in models such as CERES-N,
DAISY, NDICEA, and STICS (van der Burgt et al. 2006; Scopel et al. 2004;
Berkenkamp, et al. 2002; Gabrielle et al. 2002; Quemada et al. 1997). However,
surface-applied residues, which are a key aspect of no-tillage systems, tend to
decompose slower owing to poor contact with soil microbes, prevalence of fungal
decomposers, and drier conditions, while surface-applied residues also feature
greater and more prolonged N immobilization (Schomberg et al. 1994). Thus, most
crop growth models may not (accurately) model decomposition of surface-applied
residues, which hampers their use to assess long-term effects of residue management or no tillage systems on soil quality and soil erosion (Sommer et al. 2007;
Scopel et al. 2004; Schomberg and Cabrera 2001; Steiner et al. 1996). This limitation was overcome by developing surface decomposition modules or modifying
decomposition parameters (Scopel et al. 2004; Quemada et al. 1997).
Since the Brundtland report, sustainable development has become integral part
of the global policy agenda (Speelman et al. 2007). Within this context, when
designing and managing cover-crops systems, operational tools are needed to
evaluate their benefits in terms of enhancing sustainability of local natural
resource management (NRM) systems within a larger socioenvironmental context
(Lopez-Ridaura et al. 2002). This requires a conceptual framework that is participatory, comprehensive, meaningful, and practical, and MESMIS was developed
to provide such a tool. This approach uses a cyclic process to aggregate and integrate economic, environmental, and social indicators, and it has been extensively
used throughout Latin America (Speelman et al. 2007). The NRM systems are
characterized in terms of key attributes (e.g., productivity), critical points are
identified (e.g., poor adaptation of cover crops), and corresponding diagnostic
criteria (e.g., ability to adapt new technology) developed, which are then translated
into specific indicators (e.g., area in which cover crops are being used) that are
readily available on a farm scale. The resulting information is then integrated by
combining both qualitative and quantitative techniques with a multicriteria analysis
(Lopez-Ridaura et al. 2002). Although the MESMIS has greatly facilitated participatory sustainability assessment, it does not allow for long-term system assessment, while the involvement of end-users was also often limited. Further
modifications may thus be required so that it can be more effectively used for the
exploration of alternative management systems and system optimization as well
(Speelman et al. 2007). Moreover, use of simulation models may also facilitate
trade-off analysis of different production components such as labor costs, profits,
soil erosion, and environmental risk (Dogliotti et al. 2005; Stoorvogel et al. 2004;
Lu et al. 2000).
68
J.M.S. Scholberg et al.
3.2.3 Exploration of Alternative Systems
Model selection/development and application should fit into a larger system analysis
framework as shown in Figs. 3.1 and 3.2. However, most existing models aim to
enhance scientific understanding, whereas the use of such models for informed
decision-making and improved management of cover crops requires a combination of
sound scientific basis with practice-oriented model design (van der Burgt et al. 2006).
Ideally, model development and application should be inspired by insights provided
by farmers (e.g., participatory modeling). Examples of how models may be used in
this fashion for the exploration, and design of more sustainable cover-crops-based
vegetable production systems in Uruguay will be discussed in more detail later.
The use of the NDICEA model for exploration of more sustainable production
practices for vegetable cropping systems in southern Uruguay demonstrated that
cover crops could be effective in maintaining and/or enhancing SOM content while
reducing external N-fertilizer requirements. However, these benefits differed
between soil types (Selaya Garvizu 2000). This work was extended and modelbased explorative land use studies were implemented to evaluate a much larger
number of potential production systems, thereby providing a strategic support base
for re-orientation of local vegetable production systems (Dogliotti et al. 2004).
First, the ROTAT system (Dogliotti et al. 2003), a tool that was previously developed for generating crop rotation based on user-selected agronomic criteria, was
used to assess all possible crop rotations. One proposed technical intervention
was the introduction of cover crops and integrate pastures into vegetable cropping
systems to reduce soil erosion and increase SOM. Key input and output parameters,
including soil erosion, SOM and nutrient balances, environmental impacts, labor
use, and economic performance were assessed by different quantitative standard
methods using a target-oriented approach. This work generated a large number of
Deciding
Acting:
Implementing a
‘bright idea ?
Planning:
DESIGN
Which
Improvements ?
Quantitative
analysis,
discussion
DIAGNOSIS
Reflecting:
What are
implications ?
Measuring
Observing:
Find out
consequences
Quantitative
analysis,
discussion
Fig. 3.2 Key aspects (diagnosis vs. design), system development steps (observing, reflecting,
planning, and acting), and system develop actions (measuring, analysis/discussion, and deciding/
selecting) during experiential learning cycle (Rossing et al. 2007)
3
Cover Crops in Agrosystems: Innovations and Applications
69
alternative production systems, and across these systems, the use of cover crops
reduces soil erosion on the average by 45–50% (Dogliotti et al. 2004). By using a
mixed linear programming model (Farm Images), production activities could be
allocated to production fields differing in soil quality in such a manner that production
constraints were met, socioeconomic benefits were maximized, while soil degradation and environmental impacts were minimized. The model was then used to
redesign seven local farms, and results showed that erosion may be reduced by
200–400%, the decline in SOM may be reversed, and when compared with the current
situation, farm income could be improved for six out of seven farms (Dogliotti et al.
2005). Based on this work, it was concluded that using cover crops during the
intercrop period and decreasing the area under vegetable production provide a more
sustainable and profitable development option when compared with the current
farmer’s practice of increased intensification (Dogliotti et al. 2005). This work was
then extended to a large number of farm types (based on farm size, soil quality, and
supply of labor, irrigation, mechanization using a similar approach to assess the
impact of resource endowment on development options and strategic farm design).
An example of this approach for assessing the benefits of cover crops on reducing
soil erosion and improving SOM content is shown in Fig. 3.3. Finally, it was also
shown that farm resource endowment may limit sustainable development options,
while reducing environmental impacts is quite likely to reduce family income as
well (Dogliotti et al. 2006).
In terms of active farm participation, the FARMSCAPE approach (Carberry
et al. 2002) outlines strategies for integrating participatory action research with
simulation model approaches. One key finding was that it is critical to first establish
the credibility of such models by linking them with on-farm studies and farmers’
experiences. Moreover, active participation of pilot farmers was required and simulation tools needed to be flexible so that they can be adapted to specific on-farm
management conditions. Via interactive dialogues between farmers and researchers,
farmers were able to explore their production system and design alternative
management practices similar to the “learning from experience,” while this
approach can greatly reduce the cost and risk associated with “trying new things”
(van der Burgt et al. 2006; Carberry et al. 2002). However, assessing overall
ecosystem functioning and services using simulation models remains difficult
because of the inherent complexity of biophysical and human dimensions of these
systems combined with the ecological and economic processes that control them,
and the lack of site-specific data (Sommer et al. 2007). Alternative and more pragmatic
approaches may thus be required as well, including the development of sustainability indicators such as MESMIS as discussed earlier.
Another instance of a design tool for cover-crop-based systems includes
GreenCover (Cherr et al. unpublished; http://lyra.ifas.ufl.edu/GreenCover). This
expert system is based on a systematic approach and aims to render information
about cover-crops-based systems more relevant, accessible, and organized for
potential users by (1) distilling basic “rules” about successful use of cover crops
from published studies; (2) applying these rules to farm-specific environment,
management, and goals; and (3) using the application of the rules to identify potentially
70
J.M.S. Scholberg et al.
a
Soil erosion reduction (Mg ha−1 yr−1)
12
10
8
6
4
2
0
0
1000
2000
3000
4000
5000
6000
7000
8000
6000
7000
8000
b
400
Rate of SOM change (kg ha−1 yr−1)
Crop Rotation n°
300
200
100
0
−100
−200
− 300
0
1000
2000
3000
4000
5000
Crop Rotation n°
Fig. 3.3 Example of use of simulation models to explore potential benefits of including cover
crops during the fallow period on reducing annual soil erosion (a) and improving soil organic
matter content (b) for 7447 different crop rotation schemes in southern Uruguay. Overall soil erosion
values were 13.2 versus 6.9 Mg ha−1 year−1 for conventional versus cover-crop-based systems,
whereas corresponding values for soil organic matter (SOM) changes where −223 versus 100 kg
SOM ha−1 year−1 (Modified from Dogliotti et al. 2006)
3
Cover Crops in Agrosystems: Innovations and Applications
71
suitable cover-crop species from a database containing characteristics of roughly 50
species or species mixtures. In this tool, the user is provided with a list of the species
and/or species mixtures as well as links to online management information sources.
This kind of approach can be termed as an “information-access tool.” It allows
users to interactively explore how changes in management or targeted cover-crop
services affect the selection process of cover crops.
3.2.4 Design or Selection of a System
Here, we emphasize modes of cover-crop technology development, adaptation, and
transfer as examples of system design or selection. A more detailed discussion on
cover-crop management is presented elsewhere (Scholberg et al. 2009). As mentioned
earlier, this can also provide insights into the other components of the innovation
framework already described.
3.2.4.1 Technology Development and Adaptation
The process of technical innovation of agroecosystems includes elements of continuous generation of “novelties” (Roep and Wiskerke 2004). These may include
different constellations of evolutionary variations of native management techniques, local adaptation/simplification of imported high technology, and more revolutionary or external innovations (Douthwaite et al. 2002; Bunch 2000). Innovations
can be simple, e.g., new cover-crops species, or complex, e.g., complete technology
package including alternative rotations, new varieties, and equipment.
It is critical to first test a “promising technology,” which may be imported from
a different production environment on a limited field scale under controlled conditions (e.g., on-station initial screening and development). This may be followed by
on-farm testing and further adaptation of the technology in close collaboration with
local stakeholders prior to wide-scale promotion of such a technology (Giller
2001). As an example, zero tillage may be perceived as a revolutionary technology
that aims to enhance soil ecological functioning and minimize soil degradation of
arable cropping systems (Triplett and Dick 2008). Initial adoption of zero tillage
after its development in the 1950s was slow and only after a suitable “basket of
technology” was developed, e.g., development of special planters, suitable herbicide programs, and accumulation of local expertise. Transfer of cover-crop-based
zero tillage systems to other systems that also aimed to minimize the use of herbicides (e.g., organic systems) required development of special roller equipment as
well (Creamer and Dabney 2002; Kornecki et al. 2004).
During the adaption process (innovation cycle), close interactions occur between
developers (innovative farmers/engineers/researchers), novelties (technical innovations), facilitators (extension workers or pilot farmers), and end-users (farmers).
During this initial innovation cycle, developers elucidate farmers’ expert knowledge to design a suitable set of technological innovations (“best bet” technology),
72
J.M.S. Scholberg et al.
which is then adopted and implemented by pilot farmers on a field scale (“plausible
promise”), as discussed by Douthwaite et al. (2002). This may imply further refinement of technological innovations due to prevailing pedo-climatic conditions,
farmer’s knowledge and management practices, and socioeconomic factors
(Nyende and Delve 2004). During the overall innovation process, there is a gradual
transfer of participation and ownership of the innovation from the developer to the
adopter who in time becomes the main driving force behind technology transfer
(Douthwaite et al. 2002; Neill and Lee 2001).
The key to successful integration of cover crops in zero-tillage systems was the
development of appropriate equipment for seeding crops (Triplett and Dick 2008).
Such planters needed to be heavier and may also contain row cleaners to push aside crop
residues and spoked closing wheels to ensure optimal soil structure and seed–soil
contact along with the use of stronger and adjustable pressure springs to ensure a
constant seeding depth (Sustainable Agricultural Network 2007). However, this
“best bet” technology needed to be further adapted to include strip till (“plausible
promise”) for vegetable crops to prevent delays in crop development and thus
ensure that growers can benefit from favorable market windows (Phatak et al.
2002). As an example of scaling out, the use of cover crops is often closely linked
to zero tillage (Landers 2001), which was developed in the USA during the 1950s
and introduced in Brazil during the 1970s (Triplett and Dick 2008). However, it
only became more widely adopted in the 1980s. Currently, it is not only commonly
used in the USA but also spread to Brazil, Argentina, and Australia (Triplett and
Dick 2008). Another example of effective scaling-out of cover crops includes the
widespread success and adaptation of mucuna-based maize production systems in
Honduras. This process was driven by a spontaneous farmer-to-farmer diffusionbased dissemination. This mechanism for technology transfer was shown to be
much more effective than the traditional extension model of technical assistance in
different regions (Landers 2001; Neill and Lee 2001).
3.2.4.2 Approaches for Technology Transfer
In practice, promising technical interventions for enhancing the livelihood of farmers
and the sustainability of agriculture are often not effectively adopted by farmers
(Nyende and Delve 2004; Tarawali et al. 2002). As a result, especially resourcepoor farmers often did not benefit from most technological innovations in the past,
since they were typically neither appropriate nor affordable (Bunch 2000).
Furthermore, traditional approaches for research and technology transfer tend to be
reductionist (Drinkwater 2002), lack a “total system” approach (Phatak et al. 2002),
and thus are poorly suited for cover-crop-based systems (Cherr et al. 2006b).
Moreover, such systems should be designed based on specific biophysical conditions,
while technological innovations should also be appropriate within the local socioeconomic context (Cherr et al. 2006b; Douthwaite et al. 2003). Thus, limited adoption
of technical innovations may be related to (i) lack of farm-tested appropriate and
cost-effective technology; (ii) timing conflicts with the existing operations; (iii)
3
Cover Crops in Agrosystems: Innovations and Applications
73
lack of tangible/direct benefits and/or multiple services; (iv) limited access to
resources (including capital and seeds); (v) poor matching of interventions with
farmers’ priorities; (vi) lack of active participation of farmers during technology
development, adaptation, and transfer; (vii) lack of suitable policies and legislation
to provide a broader societal support network (Morse and McNamara 2003; Nyende
and Delve 2004; Tarawali et al. 2002; Landers 2001). These adaptation factors may
vary greatly among regions; for example, the integration of cover crops in some
systems (e.g., Brazil) has been successful on a regional scale (Calegari 2003;
Landers 2001), while their adaptation in other regions (e.g., SE USA) lagged behind
(Phatak et al. 2002). Moreover, technologies should be linked to local traditional
knowledge, practices, and experience. Technological innovations thus need to be
appropriate within the local context while direct involvement of farmer’s at all critical
development and adoption stages appears to be critical (Leeuwis 1999). Furthermore,
active participation of early adopters during the refinement and dissemination of
cover crops systems tends to greatly enhance technology transfer efficiency
(Tarawali et al. 2002).
A large number of alternative approaches to conventional research and extension
approaches have been proposed and are being used including (i) farming systems
research and extension (Weil and Kremen 2007), (ii) farmer participatory research
(Giller 2001, Bentley 1994), (iii) campesino-to-campesino approach (Anderson
et al. 2001), (iv) prototyping (Vereijken 1997), (v) prototyping combined with
model-oriented approach (Bouma et al. 1998), and (vi) co-innovation (Rossing
et al. 2007). The first approach aimed to use a more “holistic” and interdisciplinary
team approach to facilitate improved understanding of local farming systems and
constraints, thereby facilitating the design of more appropriate development options
(Douthwaite et al. 2003). However, this method is often rather descriptive and also
does not effectively use technological tools including simulation models (Stoorvogel
et al. 2004). The second method recognizes that farmers have valuable experiencebased knowledge that complements science-based research approaches and that
farmers can also be instrumental in structuring both research objectives and suitable
technical innovations (Cardoso et al. 2001). Moreover, active involvement of farmers
is critical, since any intentional change requires awareness while change in human
conduct is also rooted in both individual and collective learning processes (Leeuwis
1999). Fostering active involvement will induce empowerment, which in turn
further enhances technical innovation (Cardoso et al. 2001). Although this sounds
appealing, its implementation may be challenging owing to social, cultural, and
intellectual barriers between farmers and researchers. Moreover, for this method to
be successful, a long-term commitment is required from both parties involved
(Bentley 1994), which is exemplified by successful participatory projects (Altieri
et al. 2008; Cardoso et al. 2001).
The “campesino-to-campesino” approach in Latin America dates back to the
1970s. It has its roots in the popular education movement, and it includes
“reflection-action-reflection” elements and emphasizes local empowerment, which
is implemented by transferring the control of the development process to the local
community. Locally selected farmers (campesinos) also assume leadership, are
74
J.M.S. Scholberg et al.
actively involved in experimentation, coordinate the promotion and transfer of
technical innovations, and at times may be paid part time for their contributions
(Anderson et al. 2001). However, this approach requires an appropriate social environment as was the case in, e.g., Nicaragua. In other regions (e.g., Florida), commercial farmers may perceive their technological innovations as a tool to provide
them with a competitive edge and may be reluctant to share intrinsic knowledge on
such innovations.
Prototyping involves close interaction with farmers to define/rank objectives and
to select the corresponding parameters that can be readily quantified (diagnosis and
analysis phase). These parameters are then integrated using multiobjective methods
to develop a conceptual design (prototype) of an alternative production system
(design phase). Subsequently, this “prototype” is implemented, tested, and refined
on a field scale in collaboration with selected pilot farmers (rediagnosis and/or
redesign phase), before being disseminated to a larger group of farmers (Vereijken
1997). One limitation of this approach is that only a few production systems can be
tested in the field (Dogliotti et al. 2004). Stoorvogel et al. (2004) combined the
prototyping approach with a model-oriented system analysis approach. However,
the active contribution of farmers appeared to be limited (e.g., top-down approach)
and the basis for sustainability assessment rather narrow when compared with, e.g.,
MESMIS (Lopez-Ridaura et al. 2002).
The co-innovation approach is based on the premises that development is a
“social” rather than a “technical” process (Douthwaite et al. 2003) and that technology
development occurs through a continuous evolving experimental learning and
selection process by farmers (Douthwaite et al. 2002). However, use of a system
approach to foster systemic innovation rather than incremental change is also critical to revolutionize the technology transfer process. Moreover, the use of an interdisciplinary approach combined with effective use of simulation models may
greatly facilitate the selection of suitable development options (Rossing et al.
2007). Full integration of all these components (co-innovation) thus seems to provide a powerful tool for fostering technology development, system design while
also enhancing the efficiency of technology transfer and adaptation. Active participation of farmers during the problem identification phase (e.g., development of
“problem trees,” as shown in Fig. 3.4) and “fine-tuning” of technical interventions
(e.g., during the exploration and design phase) aim to structure solutions that are
appropriate within the local context (Anderson et al. 2001). Moreover, use of the
“impact pathways” approach, which involves a frequent self-reflection and monitoring of the mutual learning process and development trajectory, allows both
researchers and end-users to carefully monitor how development tracks and corresponding impacts evolve over time (Douthwaite et al. 2003).
An example of key aspects of the integration of a system analysis method used
in the co-innovation approach will be illustrated based on an Uruguay case study.
In this case, the decline in sustainability of local vegetable systems could not be
reversed by simple adjustments of single production components or using standard
technological innovation packages. Instead, a redesign of the farm systems as a
whole was required. However, such a redesign of farm systems at the strategic level
3
Cover Crops in Agrosystems: Innovations and Applications
75
Poor crop and
animal
husbandry
Low family
income
Low gross
product
Low
commercial
yields
High
production
costs
High
diversification
and area of crops
Lack of
irrigation
High impact
of weeds and
diseases
Farm system
unsustainability
Long bare fallows,
high frequency of
crops with low
cover
Deteriorated
soil quality
High
erosion
risk
Negative
Soil organic
matter
balance
High slopes
without proper
sistematization
Low organic
matter inputs
High frequency
of the same
crop or family
Fig. 3.4 Problem tree, which serves as an initial system diagnosis tool, as identified by a commercial vegetable producer in Uruguay. This diagram exemplifies potential benefits of cover crops
to enhance crop diversity, suppress weeds, improve soil cover, and inherent soil fertility of erosion-prone intensive vegetable production systems
could only be achieved by a participatory, interdisciplinary systems approach. Field
surveys showed that none of the farmers used cover crops as a standard practice
during the intercrop periods and only 27% of the farmers had ever grown a cover
crop. Most of the farmers used a tillage fallow during the 3–8 month period in
between crops. Only 40% of the farmers intentionally tried not to grow the same
crop in the same field next season, while 88% of the farmers did not follow an
intentional succession of two specific crops (Dogliotti et al., 2003). Moreover, the
maximum time horizon for planning the use of a particular field was less than 1
year for 80% of the farmers (Klerkx 2002). The added costs of growing cover crops
accounted for just a fraction of total production cost of vegetables and this extra
cost was also readily offset by reduced fertilizer cost and increased crop yields
(Dogliotti et al. 2005). The lack of machinery for mowing and incorporating large
amounts cover crops residues was perceived to be a constraint by some farmers.
But the main limitation for adoption appeared to be the short time horizon of
planning of farms’ fields use and the lack of defined crop successions or rotations.
This survey thus revealed that allocation of crops to fields is rather an “operational”
76
J.M.S. Scholberg et al.
or “tactical” decision than a “strategic” one, and despite the promising results of
cover-crops-based systems in experimental stations and farmers’ fields, their use
was not adopted by farmers in the region. The use of simulation-models and expert
systems (e.g., ROTAT, Dogliotti et al. 2003) facilitated the exploration of
cover-crop-based crop rotation systems that were appropriate within the local context.
These initial explorations were then modified based on discussions with local
producers, and their feedback was used to “fine-tune” system design prior to
on-farm implementation of these systems.
3.2.4.3 Sustainability of Technology Adoption
In addition to inducing change and improvements, technological innovation should
also aim to harness long-term sustainable development. Although farmers may be
enticed to adopt innovations based on perceived short-term benefits, it may be more
difficult to assess how such innovation meets the stability, resilience, and reliability
criteria listed by Lopez-Ridaura et al. (2002). Assessing the medium to long-term
effects of innovations on agroecosystem functioning is difficult and time-consuming
(Drinkwater 2002) and may require use of simulation models (Stoorvogel et al.
2004). Increased management complexity and greater perceived risk may hamper
adoption and long-term use of ecology-based systems (Shennan 2008), which can
hamper both short-term adoption and long-term use of cover-crops-based systems.
In Honduras, extensive adoption of mucuna-based corns systems was abandoned by
many farmers within a few years due to changes in land-tenure, invasion of an
obnoxious weed, and extreme weather conditions (Neill and Lee 2001). Although
simulation models may not capture all potential contributing factors, they may
facilitate improved risk assessment for different scenarios. This may be especially
important in the context of current trends in climate change and more frequent
occurrence of erratic and extreme weather and rainfall patterns (Stoorvogel et al.
2004). Finally, it was also argued that broadening the global genetic base of cover
crops proposed for development options needs to be considered (in order to minimize the risk of build up of pests as was the case of Leacaeana psyllid). Therefore,
diversification of the proposed innovations and developed options will be critical
for long-term sustainability of cover-crop-based systems (Anderson et al. 2001).
However, preservation and improved integration of traditional knowledge on cover
crop practices will be critical as well to prevent an erosion of a collective heritage
that took thousands of years to evolve (Altieri 2002).
3.3 Innovations in Cover-Crop-Based Systems in Case
Study Regions
Below, we provide a brief historic perspective on key factors related to innovation
in cover-crop-based systems in four regions of the Americas (Florida, USA; Paraná
and Santa Catarina, Brazil; and Canelones, Uruguay). Special emphasis is placed
3
Cover Crops in Agrosystems: Innovations and Applications
77
on the components of the innovation framework discussed in the previous section:
(1) characterization and diagnosis of constraints, (2) analysis of system behavior,
(3) exploration of alternative systems, and (4) design of more sustainable production systems. In most cases, we also outline key factors affecting technology transfer
and adoption within the context of local socioeconomic conditions and prevailing
management practices.
3.3.1 Florida
3.3.1.1 Biophysical Production Environment
The study region (North Central Florida) is located in the Southeastern U.S. (29°25¢
N and 82°10¢ W). The average temperature is 19°C, and frosts may occur between
November and March. Average annual rainfall is 1,200 mm with 52% of this rainfall occurring from June to September. With an area of 2.5 million ha and a total
revenue of $7.8 billion, agriculture is a key component of Florida’s economy
(NASS 2007). The statewide average farm size is 99 ha and citrus (251,568 ha),
sugarcane (163,968 ha), hay production (105,263 ha), vegetable crops (179,800
ha), peanuts (130,000 ha), and cotton (103,000) are some of the key agricultural
crops. Their corresponding contributions to statewide farm revenues were 21.1, 5.5,
1.4, 24.0, 0.9, and 0.4%. In comparison, ornamental crop and livestock operations
contributed 12.6% and 18.7% to statewide farm revenues, respectively (NASS
2007). The dominant soil types in the study region include excessively drained
sandy soils (>95% sand) containing only 1–2% soil organic matter and soils typically have poor water and nutrient retention capacities (Cherr et al. 2006c; Zotarelli
et al. 2007a, b). Most vegetable crops are produced using raised beds covered with
plastic mulch in combination with drip irrigation (Zotarelli et al. 2008a, b).
3.3.1.2 Characterization and Diagnosis of Constraints
Within the US, Florida is the largest producer of citrus, tomatoes, sweet corn,
watermelon, and snap bean and the second largest producer of bell peppers, cucumbers, and strawberries (NASS 2007). Current concerns about global warming and
environmental quality issues will require growers to make more efficient use of
water and nutrients and reduce inorganic fertilizer use (Cherr et al. 2006c; Zotarelli
et al. 2008a, b). Historically, Florida has greatly depended on the use of fumigants
to control weeds, pathogens, nematodes, and insects, and it is one of the largest
users of methyl bromide. Future restrictions on the use of methyl bromide may
undermine the viability of vegetable production in this region because the
cost-effectiveness of alternatives to this fumigant remains an issue (Abdul-Baki
et al. 2004). Increased globalization and lifting of trade barriers have also resulted
in increased competition with other production regions (e.g., Brazil and Mexico),
which have lower labor cost and less restrictive environmental regulations.
78
J.M.S. Scholberg et al.
Steep increases in fertilizer, fuel, and labor costs along with citrus canker, and citrus
greening disease epidemics are among the main concerns for citrus growers in the
region. Since inherent soil fertility is poor and potential nutrient losses are appreciable, conventional growers mainly depend on chemical fertilizers (Zotarelli et al.
2008a, b). Organic growers often use external nutrient sources that are expensive,
and their use may be restricted by food safety or certification issues (for example,
animal manure). For organic growers, effective weed control is one of the key factors hampering successful transition, and cover crops may thus provide them with
a cost-effective option to manage weeds (Linares et al. 2008). In our experience,
the presence of coarse sandy soils hampered build up of SOM and effective inoculation of leguminous winter cover crops, and supplemental K-fertilizer was required
to enhance cover crops performance. Warm-season cover crops, on the other hand,
generally thrived on these sandy soils and are readily colonized by native rhizobium species (Linares et al. 2008).
3.3.1.3 System Analysis and Exploration of Alternative Systems
Use of Cover Crops for Weed Suppression in Orchard Systems
Organic vegetable growers in Florida tend to use a weed fallow during the hot and
humid summer months, since high pest and disease pressures prevent the cultivation
of most commercial crops. However, this practice may also favor build-up of weeds
(Collins et al. 2007), while effective weed control remains a key concern of most
organic growers (Ngouajio et al. 2003). Therefore, the use of summer cover crops
such as sunn hemp (Crotalaria juncea) and cowpea (Vigna unguiculata) may provide
growers with an option to improve inherent soil fertility, prevent the build-up of weed
seedbank, and suppress noxious weeds such as yellow nutsedge (Cyperus esculentus)
and Pigweed (Amaranthus hybridus). Greenhouse studies showed that sunn hemp
provided relatively poor weed control during initial growth when compared with a
more compact crop such as cowpea (Collins et al. 2007). However, field studies
showed that sunn hemp was most effective in suppressing weeds toward the end of
the growing season, which may be related to its slow initial growth (Linares et al.
2008). Thus, effective weed suppression in annual Florida organic systems may
require use of cover crops with complementary growth and canopy characteristics.
Cover crops have been used extensively in perennial production systems throughout the world – especially tree-crop and shrub-crop production systems (Anderson
et al. 2001). Some of the main issues of their use are related to effective weed control,
uniform and compact growth, adequate erosion control, provision/retention of nutrients, and potential competition for water under water-limiting conditions. Effective
use of cover crops may reduce establishment (e.g., fertilizer) cost and/or provide financial returns (e.g., forages and pulses) during the tree establishment period (Anderson
et al. 2001). In terms of perennial production systems in the subtropical and tropical
regions, the following warm-temperature adapted perennial and annual species may
be viable candidates: perennial peanut (Arachis pinto and A. glabrata), Canavalia
3
Cover Crops in Agrosystems: Innovations and Applications
79
spp., pigeonpea (Cajanus cajan), Crotalaria spp., indigos (Idigofera spp.), velvetbean
(Mucuna spp.), and Vigna spp. (Linares et al. 2008; Anderson et al. 2001). However,
use of A. pinto is not feasible in North Florida due to winter freezes. In this region,
winter annuals most commonly used in perennial systems include winter rye, vetch,
black oats (Avena strigosa), crimson clover (Trifolium incarnatum), lupin, and forage
radish (Raphanus sativus). We tested each of these species for weed control potential
in an organic citrus production system in North Florida.
Of the warm-temperature cover-crop species we tested, sunn hemp (Crotalaria
juncea) was the most prolific cover crop. It generated 5.3–12.6 Mg ha−1 when compared with 5.9–9.5 Mg ha−1 for hairy indigo, 3.7–7.6 Mg ha−1 for pigeon pea, 2.4–5.1
for Mg ha−1 for cowpea (Vigna unguiculata), and 1.0–2.8 Mg ha−1 for velvetbean
(Mucuna pruriens). Both sunn hemp and cowpea were most effective in suppressing
weeds and reduced weed biomass by 83–97% (Linares et al. 2008). Pigeon pea did not
provide effective weed control; similar observations were made with citrus in Bolivia
(Anderson et al. 2001) and Brazil (Matheis and Victoria Filho 2005). We used both
“bushy” and “vining” Mucuna types, but neither performed well under our conditions;
this may have been related to the poor water retention capacity of our sandy soils. This
is in contrast with studies in Central America where velvetbean grew more vigorously
and provided effective weed suppression (Neill and Lee 2001). Although we tested
jackbean (Canavalia ensiformis) on a small plot basis and this crop appeared to be well
adapted to sandy soils, lack of access to seed sources prevented detailed assessment of
its performance. In other regions, this crop is a prolific biomass producer, grows well
under adverse conditions, is used for forage production as well, and is also suitable for
intercropping (Nyende and Delve 2004; Anderson et al. 2001).
In terms of winter cover crops, the best performing species were winter rye (3.2–
6.0 Mg ha−1), forage radish (3.2–4.3 Mg ha−1), crimson clover (1.7–5.0 Mg ha−1), and
black oats (1.3–3.6 Mg ha−1). Use of cover-crop mixtures (one or more species)
greatly enhanced biomass production (3.6–8.0 Mg ha−1). Crop performance and weed
suppression by winter leguminous cover crops were erratic during the first years,
which were related to the poor adoption to sandy soils, but over time, their performance improved. Rye and radish were more effective in suppressing weeds while
mixes of these two cover crops reduced weed biomass to less then 2% of that in controls and thus may provide a very effective weed control (Linares et al. 2008).
The initial growth of perennial peanut (A. glabrata) in this system was very slow
and its initial weed suppression ability was poor. Repeated mowing improved the
performance of this species over time, and it may provide a valuable forage for
additional farm income. However, its growth and weed suppression during the first
3 years of study was clearly inferior to the annual cover crops tested.
Annual Cover Crops as a Green Manure in Vegetable Crops
Historically, crops such as velvet bean were used as a green manure until about the
1930s. After this time, the availability of cheap inorganic fertilizers reduced their
attractiveness as N sources (Buckles et al. 1998). Currently, cover crops in Florida
80
J.M.S. Scholberg et al.
vegetable cropping systems are usually incorporated via tillage. However, since
tillage enhances soil mineralization, this may offset carbon sequestration and soil
quality benefits (Phatak et al. 2002). Conventional production systems for crops such
as tomato and pepper include the use of black mulch, which serves to facilitate
fumigation, suppress weeds, reduce evaporation, leaching, increase soil temperatures
and initial growth, and prevent soil contact of harvestable products (Carrera et al. 2007).
However, its use involves energy, economic and environmental costs for production,
and purchase and disposal, while their use also can enhance run-off of pesticides
(Abdul-Baki et al. 1996, 1999). Experiments conducted by Abdul-Baki et al. (2004)
in South Florida demonstrated that cover-crop-based systems (e.g., growing cowpea
or velvet bean) had similar marketable tomato yields when compared with the use
of mulch and methyl bromide, while production cost could be reduced by $1,544
ha−1. On-farm demonstration trials by Avila (2006c) in South Florida showed that
use of sunn hemp-based systems could offset marketing risk of conventional tomato
systems by increasing yields and reducing use of herbicide and external fertilizer
inputs. These findings were similar to those of previous studies in which systems
based on cover crops and zero-tillage improved soil quality and nutrient retention
while reducing agrochemicals, external input use, production costs, environmental
impacts, and soil erosion (Abdul-Baki et al. 1996, 2002, 2004).
Another field study was conducted in north central Florida to assess the benefits
of a reduced-tillage cover-crop-based system for vegetable crops between 2001 and
2005. This study included different combinations of both summer and winter cover
crops [sunn hemp, rye (Secale cereale), lupin (Lupinus angustifolus), and vetch
(Vicia spp.); Avila et al. 2006a, b; Cherr 2004). Overall biomass and N accumulation of summer cover crops were on the order of 8.0–12.2 Mg ha−1 and 146–172 kg
N ha−1 whereas production of leguminous winter cover crops was much lower
(2.0–4.0 Mg ha−1 and 51–104 kg N ha−1) (Cherr et al. 2006c). However, in the warm
and humid climate, most of the N from winter-killed sunn hemp was released
quickly, and growth of subsequent cover crops and economic crops was too slow to
effectively utilize it (Cherr 2004; Cherr et al. 2006a, c). The use of a vetch and rye
biculture allowed uptake of this N and also resulted in improved winter-cover-crop
growth and N accumulation (7.2 Mg ha−1 and 135 kg N ha−1; Avila et al. 2006a, b).
Changing rye and vetch proportions in this mixture greatly affected the C:N ratio
of the cover-crop residue (e.g., 69 for pure rye system, 26 for 67% rye–33% vetch
system, and 14 for pure vetch system). Although total biomass was greatest for
mixed systems, N accumulation was greatest for pure vetch systems.
In terms of yield benefits to subsequent crops, cover-crops-based systems provided clear yield benefits for sweet corn, broccoli, and watermelon (Cherr et al.
2007; Avila et al. 2006a, b). However, unlike studies at more northern locations
(Bhardwaj 2006; Carrera et al., 2007; Burkett et al., 1997), the cover-crops-based
systems in Florida only provided limited yield benefits and inorganic N-fertilizer
savings. Although the cover-crop-based systems provided N-benefits on the order
of 60–70 kg N ha−1, enhanced early economic crop growth, and N accumulation,
these systems were still out-yielded by conventional controls receiving 267 kg N ha−1
3
Cover Crops in Agrosystems: Innovations and Applications
81
(Cherr et al. 2007). Generally, the low soil fertility combined with the poor nutrient
retention capacity of Florida soils does not support top production levels unless
substantial amounts of supplemental nutrients are supplied throughout the growing
season. This is related to the prevailing sandy soils that hamper efficient nutrient
retention and build-up of SOM even in the absence of tillage. Although cover-cropbased systems provide substantial amounts of both C and N, the enhancement of
the inherent long-term nutrient supply capacity of the system appears to be limited,
since SOM is poorly protected and nutrients released by residues are prone to
leaching. Therefore, the system is poorly buffered, and thus pools are exhausted
rapidly prior to the development of an extensive root system of the commercial
crop. Pasture systems thus may be more effective in improving inherent soil fertility when compared with annual cover crops. Moreover, maize crops may be particularly unsuited to cover-crop-based systems in these conditions because its
capacity for N uptake during early growth is limited. Detailed 15N studies (Zotarelli
unpublished data) showed that N-uptake efficiency of sweet maize was only 14%
for soil nitrate present at planting when compared with 48% for N released 1 month
after planting.
3.3.1.4 Technology Adoption
The adoption of cover-crop-based systems in Florida by farmers is limited and
mainly confined to organic producers. Conventional growers may opt to use sorghum Sudan grass (Sorghum bicolor var. Sudan grass) during summer fallow and
winter rye as a soil cover in commercial vegetable cropping systems. Although
cover crops may be perceived as an environmentally sound management option,
their use can interfere with the standard management practices in conventional
systems in this region. In an on-farm study, it was observed that full-grown sunn
hemp was very tall (>2 m), and the thick-stemmed plants produced a recalcitrant
residue layer. During subsequent bed formation of tomatoes, this material hampered bed formation and thereby reduced the effectiveness of fumigation and subsequent weed suppression since the residue caused tearing of the plastic mulch.
Based on suggestions of the participating grower, use of repeated mowing resulted
in a less coarse residue material and acceptable biomass benefits, which underlines
the importance of active farm participation during technology development.
In Florida, the absence of incentives, lack of appropriate recommendations, and
suitable equipment may hamper widespread adoption of cover-crop-based systems
in vegetable cropping systems. Since the use of zero- or reduced-tillage on sandy
soils in Florida is limited and there is a lack of suitable planters, the risk of poor
initial crop establishment and yield reductions of subsequent commercial crops also
increases. These factors may further hamper the use of cover-crops-based conservation systems in the region. In contrast, 58–64% of the farmers in neighboring
Alabama use reduced- or zero-tillage for crops such as cotton and maize (Bergtold
et al., 2005). Even in North Florida, there may be producers within subregions or
82
J.M.S. Scholberg et al.
niche markets for whom cover-crop use is more feasible. On the heavier soils in the
northwest Florida panhandle, there is more of a tradition to integrate reduced tillage into
conventional operations while leguminous winter cover crop also tend to perform
better on these soils. Moreover, proximity to Alabama and Georgia may provide
opportunities for farmers in this subregion to successfully adapt cover crops
systems developed in these neighboring states as well. Both positive and negative
incentives (price premiums and regulatory requirements, respectively) may also
encourage organic growers in Florida to use cover-crop-based systems. In this
case, lack of technical information by traditional local extension approaches and
different pedo-climatic conditions from other key organic production regions may
force growers to engage themselves with on-farm experimentation and technology
development of cover-crop-based systems. So, it appears that lack of incentives and
suitable technologies continues to hamper the adoption of cover-crop-based in
conventional production systems. While in organic systems, where cover crops can
provide a much broader array of services, the lack of viable alternatives justifies
development of cover-crop-based systems.
3.3.2 Brazil
3.3.2.1 Biophysical Production Environment
The study region (Paraná) is located in the Southern region of Brazil between
latitudes 22°29¢S and 26°42¢S and longitudes 48°02¢W and 54°37¢W. Paraná is
located in the tropical and subtropical transition zone. The climate is humid-subtropical
with hot summers and drought periods no longer than three to four weeks. The
mean annual precipitation ranges between 1,400 and 2,000 mm. Most rain occurs
during the summer (October–March). Almost 40% of Paraná’s area consists of
soils derived from basalt beds with heavy clay and fertile soils. In this region,
agricultural cropping systems mainly include annual crops such as soybean,
wheat, cassava, sugarcane, cotton, and coffee. In the northwest, soils derived from
sandstones dominate, and in this region beef cattle and orange production are of
greater importance. The agricultural acreage in Paraná amounts to 17.6 million
hectare, of which 4.0 and 2.7 million hectare have been planted with soybean and
maize, respectively. Nationally, Paraná is the largest producer of beans, maize, and wheat;
and second in soybeans, cassava, and sugar cane; third in tobacco; and fourth in
coffee. In 2007, Paraná grain production represented 22% of the national production
(IBGE 2008). The grain production in 2006 was 11.9 million tons of soybean, 14.3
million tons of maize; 1.9 million tons of wheat; 0.7 million tons of beans. Key
factors such as climate and soil have made it possible to produce a wide variety of
crops. However, the success of agriculture in Paraná was possible due to efforts of
the state research and extension agencies to implement long-term watershed-based
soil and water conservation programs including a combination of zero tillage
and cover-crop-based crop rotations.
3
Cover Crops in Agrosystems: Innovations and Applications
83
3.3.2.2 Characterization and Diagnosis of Constraints
Intensive agriculture in Paraná started upon colonization during the early 1900s and
the state was the main coffee producer for several decades. The area planted with
coffee reached 1.8 million ha by 1975. At that time, however, a severe frost decimated
coffee and most of the coffee fields were converted to mechanized annual cropping
systems and pastures. Additional land was converted to arable land as well as more
people moved into the area. Soybean–wheat-based crop rotations became the dominant cropping system during the 1970s and 1980s. These cropping systems featured
burning of crop residues followed by tillage with heavy disc harrows and moldboard
plows. Soil surface disaggregation, reduced soil water infiltration, soil crusting,
and soil compaction led to severe erosion problems (10–40 Mg soil erosion ha−1
year−1) and a steep decline in inherent soil fertility (Calegari 2003; Derpsch et al.
1986). Initially, terracing and planting along contour lines was promoted to minimize
further erosion. However, during the early 1970s, zero tillage systems were also
introduced in Paraná (Calegari 2003; Landers 2001). During the early 1990s, the
acreage under zero tillage in Brazil reached 1 million hectare.
However, the adoption of zero tillage systems intensified other problems such as
weeds and pests, and also exacerbated soil compaction, while it also posed problems
associated with thatch layer accumulation. The development of soil management
and cropping systems strategies, including the use of cover crops, thus became
important research topics to improve the sustainability of local agriculture production
systems in Paraná (Calegari 2003). In particular, research showed that diversification of crop rotations under zero tillage increased the average yield of soybean and
maize and lowered fuel, fertilizer, pesticides, and labor requirements (Muzilli 2006;
Calegari 2003). Additional benefits such as increase in soil carbon stock and cation
exchange capacity, greater soil water infiltration and soil aggregation, and reduction
of runoff have been frequently reported in the literature (Triplett and Dick 2008;
Zotarelli et al. 2005a, b, 2007a; Sisti et al. 2004; Calegari 2003; Sa et al. 2001;
Six et al. 2000; Boddey et al. 1997; Derpsch et al. 1986).
3.3.2.3 System Analysis and Exploration of Alternative Systems
Weed suppression by cover crops has provided a critical component in the successful
adaptation of zero tillage systems in Paraná by cutting herbicide use and weed control
costs by up to 25–42% (Teasdale et al. 2007; Derpsch 1998). Use of species,
e.g., oats, rye, radish, lupin, and sunn hemp, that can be killed mechanically may
further reduce or eliminate herbicide use but some manual weeding during the growth
season may still be required (Teasdale et al. 2007). Selection of cover crops is based
on local availability of affordable seeds, their effectiveness in providing soil cover and
suppressing weeds, and to supply nutrients to a subsequent cash crop. Recommended
cover crops in Paraná include oats (Avena spp.), white radish (R. sativus), pigeon pea,
mucuna, vetches, lupins, lablab (Lablab purpureus), sunflower (Helianthus annuus),
pearl millet (Pennisetum glaucum), and pastures (see also Calegari 2003).
84
J.M.S. Scholberg et al.
Table 3.1 Examples of crop rotation systems recommended to Paraná (Embrapa 2006)
Percent of
State region
Year 1
Year 2
Year 3
Year 4
Year 5
soybean
North/West
OA/MA
CA/SO
PM+M/SO
WH/SO
–
75
North/West/Central LU/MA
OA/SO
WH/SO
–
–
66
Southeast
VE/MA
WH/SO
OA/MA
WH/SO
BA/SO
60–80
BA = barley; CA = canola; LU = lupin; M = mucuna; MA = maize; OA=oats; PM = pearl millet;
SO = soybean; VE= vetch; WH = wheat
Soybean is the most important cash crop that is also grown most frequently
(60–80% of rotations). Table 3.1 provides a brief description of standard recommended crop rotation for zero tillage systems in Paraná for different production
regions. Crop rotation design is based on (1) species characteristics (legume vs.
gramineae), (2) residue quality and quantity, and (3) occurrence of diseases and
nematodes. In terms of fertility management, biological nitrogen fixation (BNF)
plays an important role in the improvement of sustainability of local cropping
systems. Soybean accumulates large quantities of N, 80% of which is generally
supplied by BNF in rhizobium-inoculated varieties (Alves et al. 2006; Zotarelli
2000, 2005). However, owing to the high amount of N removed with the harvested
product, relatively little of the N is left in the field (Alves et al. 2002). Under zero
tillage conditions, the inclusion of winter legume cover crops such as lupin or vetch
every 3–4 years in the crop rotation thus is critical to maintain SOM and inherent
soil fertility and to minimize runoff and erosion via enhanced crop water infiltration
and soil and nutrient retention. This has been shown to greatly enhance the yields
and sustainability of local cropping systems (Derpsch et al. 1986). Well-managed
zero tillage/cover-crop-based systems can reduce erosion by 95% (Prado Wildner
et al. 2004). On-farm studies in North Paraná showed that zero tillage increased
soybean and wheat yields by 34% and 14%, respectively; whereas corresponding
additional yield benefits associated with integration of cover crops in crop rotations
were 19% and 6% (Calegari et al. 1998).
Recent experiments in this region showed that lupin accumulated up to 10 Mg
ha−1 of dry biomass with N accumulation around 250 kg ha−1. The BNF contribution
for lupin was approximately 70%, which translates to an input of approximately
175 kg ha−1 of external N being added. Lupin-based maize systems receiving no
other N inputs yielded 47% more when compared with maize following oats receiving
typical fertilizer rates of 80 kg N ha−1 (Zotarelli 2005). Integrating zero-tillage with
winter cover crops also increased soil C accumulation (Sisti et al. 2004) via
stabilization of aggregate-associated C (Denef et al. 2007; Zotarelli et al. 2007a).
However, as soybean is the main cash crop, use of certain legume cover crops that
host soybean diseases must be restricted [such as pigeon pea and lupin cover crops
that also host stem canker (Phomopsis phaseoli)]. These problems may be solved
by changing crop sequence within rotations and/or by using resistant soybean
cultivars. Other challenges with cover crops include insufficient mulch layer formation
3
Cover Crops in Agrosystems: Innovations and Applications
85
or reduced emergence of subsequent economic crops when an adequate mulch layer
is sufficient to provide other benefits. Again, these problems can be solved by
relatively simple changes in management, such as lengthening the interval between
the killing of the cover crop and maize planting and use of relatively recalcitrant
cover crops (small grains or cover-crop mixtures including small grains).
3.3.2.4 Technology Adoption
One of the key contributing factors to the success of zero tillage systems was the
diversification of crop rotations including the use of cover crops. More than 25
million hectare have been cultivated under zero tillage in Brazil in 2006 and, in the
same year around 95% of grain crop land was under zero tillage in Paraná. Rapid
expansion of cover crop and no till systems was greatly facilitated by participatory
farming system approaches. These approaches gave farmers a central role during
the problem identification, structuring of solutions and aimed also to strengthen
linkages between researchers and extension workers (Sempeho et al. 2000). In
general, farmer-to-farmer demonstration and dissemination approaches were the
most effective. For larger farmers, both the private sector and experts from nongovernmental organizations (NGOs) also contributed to this process, whereas for
smaller farmers, state extension agencies played a more important role (Landers
2001). However, the main boost in adoption occurred when production costs of zero
tillage systems were less than those of conventional tillage, suitable recommendations were in place and the method was also effectively integrated in standard
teaching and extension programs (Landers 2001). Other factors affecting adoption
included: creating awareness of clear incentives for adoption of cover crop and zero
tillage systems; active contribution of pilot farmers that championed zero tillage
and adapted such systems to local conditions; presence of effective farm organizations; and access to subsidies or credit permitting farmers to invest in technology
(Pieri et al. 2002; Sempeho et al. 2000). Moreover, local supply networks for affordable seeds, tools, equipment, and local knowledge were also critical to sustain the
continuous development as they promoted local self-reliance ensured long-term
sustainability of the effort (Pieri et al. 2002; Landers 2001).
3.3.2.5 Innovations in Cover-Crop-Based Conservation Tillage Systems
in Santa Catarina
Santa Catarina is a hilly region in southern Brazil with heavy soils and high annual
rainfall (1,200–2,370 mm), and 40–80% of the agricultural land is prone to medium
to severe erosion (Prado Wildner et al., 2004). Similar to southern Uruguay, this
region features relatively small-scale family-based intensive crop production
systems. Some of the key crops include maize, beans, potato, and tobacco as well
as intensively managed vegetable systems such as onion, garlic, tomato, cauliflower,
pepper, and beets (Prado Wildner et al., 2004). Although there has been a trend of
86
J.M.S. Scholberg et al.
increased intensification and a rural exodus of farm workers, the hilly topography
has hampered development of large-scale mechanized agriculture. During the
1960s, the use of terracing was promoted to stem soil erosion, but (as in Paraná)
neither did this address the real problem (e.g., lack of soil cover) nor did it fit local
needs, so adoption was poor. During the 1970s, increased mechanization resulted
in extensive and devastating soil erosion.
Technical assistance to solve these problems was provided by neighboring
institutes in Paraná state. Local extension agents initiated cover-crops-based zero
tillage systems on pilot farms in 1978. To ensure availability of cover crops, farmers
were provided with small quantities of common vetch (Vicia sativa), but they were
required to multiply this seed locally. Availability of suitable seeds in Santa
Catarina greatly varies depending on the species, year, and region. Relatively, few
farmers specialize in the production of cover crops seeds, and in some years, seeds
of leguminous cover crops may still not be available; therefore, this remains one of
the main constraining factors for adoption of cover-crop-based systems. Despite
this constraint, farmland in cover-crop-based zero tillage systems in the region
increased from 5% in 1987 to 44% in 1997. This rapid expansion was related to a
number of factors: (1) farmer-driven technology, (2) development of a variety of
equipment by local entrepreneurs tailored to the specific needs of different farm
management types and distribution of this equipment by larger agro-industrial
companies, (3) reduced labor requirements from mechanization, which enhanced
the livelihood of local farmers, (4) presence of an effective local agricultural
research and extension network, (5) government abandoning subsidies for use of
agroechemicals during the 1980s, (6) strong presence of family-based farming
systems with secure land tenure, and (7) presence of NGOs that helped structure
local education and research programs (Prado Wildner et al., 2004). Reported yield
of local cover-crop-based maize systems were 30% higher when compared with the
conventional systems. The use of cover crops combined with reduced tillage in this
region was capable of increasing both SOM and fertilizer-use efficiency and lowering
operational costs, but has increased herbicide requirements (Amado et al. 2006;
Prado Wildner et al., 2004).
Onion production expanded greatly during the 1970s and 1980s in the Upper
Itajai River Valley of the Santa Catarina region. The use of mechanical tillage on
steep slope combined with fine textured soils in onion cropping systems that have
sparse canopies and add very little residues resulted in pronounced soil erosion
(Prado Wildner et al., 2004). Reduced-tillage systems were introduced to combat
this problem and were adopted by 60–70% of the farms. Black oat, oilseed radish,
and/or vetch are used as cover crops and these are rotated with onions, although
onions still must receive supplemental N applications to minimize the risk of
N-immobilization. Maize is frequently grown following onion and benefits from
residual soil nutrients. In some cases, maize may be intercropped with mucuna,
while Canavalia and Crotalaria species also can be effectively grown as summer
cover crops, but farmers usually prefer intercropping with edible beans during this
time. Over the years, these systems evolved and were also adapted by local organic
farmers. However, in these systems, farmers opted to use a mix of different cover
3
Cover Crops in Agrosystems: Innovations and Applications
87
crops (e.g., a rye, radish, vetch mixtures) to enhance the functionality and performance
of the cover-crops system (Altieri et al. 2008). The use of cover crops allowed the
development of innovative organic reduced-tillage systems and reduced weed
growth by more than 90% and thus provided farmers with a cost-effective
weed management option (Altieri et al. 2008). On-farm studies in this region
have used systems developed by local farmers based on native knowledge and innovations. The main role of researchers has been to provide suggestions and to
make benefits of locally developed systems more explicit to a broader (international) audience. The success story of cover-crop-based systems in Brazil is closely
linked to their integrative use in conservation tillage systems. Such initiative may
serve as a development framework for other regions and systems with similar
conditions, including both conventional and organically managed vegetable production
systems in Uruguay.
3.3.3 Uruguay
3.3.3.1 Biophysical Environment
The study region (Canelones) is a hilly region located in Southern Uruguay (34°25¢
S and 56°15¢ E). The average annual temperature is 16°C (10°C in July to 23°C in
January), and light frosts may occur between June and September. Average annual
rainfall is 1,100 mm and water deficits tend to occur between October and March,
while water surplus may be observed between May and August. Clay and silty clay
loam soils prevail and SOM content for native undisturbed soils may range between
4.5% and 6.5% but may decline to 1–3% under continuous cultivation of conventional agricultural systems. Soil erosion due to intense rainfall events may result in
soil losses of 9–15 Mg ha−1 year−1. Soil degradation has resulted in soil crusting,
reduced aeration, infiltration, and water retention capacity. More than 70% of the
farms are smaller than 20 ha and vegetable production is the main source of income
for 27% of growers. The main vegetable crops grown in the area include squash,
carrot, onion, garlic, potato, sweet potato and sweet maize, and tomato.
3.3.3.2 Characterization and Diagnosis of Constraints
The Uruguayan vegetable production sector has been facing a cycle of increased
production intensity and input prices, falling commodity prices, and depletion of natural
resources. Between 1990 and 1998, vegetable production increased by 24%, crop
yields increased by 29% while cropped area decreased by 9% (DIEA-PREDEG
1999). Simultaneously, inflation corrected prices of vegetable products between
1992 and 2001 decreased by 34% (CAMM 2002) and an additional 15% between
2001 and 2004 (CAMM 2005). Southern Uruguay has the highest concentration of small
or family farms (farms where most of the labor is provided by family members).
88
J.M.S. Scholberg et al.
Around 88% of the farms with vegetable production as main source of income are
family farms (Tommasino and Bruno 2005). Between 1990 and 2000, the number
of these vegetable farms decreased by 20% (DIEA 2001). Those farms remaining
in business had to increase production and product quality, while reducing product
prices to maintain family income.
The strategy followed by most farmers was to intensify and specialize their
production systems. The average vegetable cropped area per farm in southern
Uruguay increased, while the average total area per vegetable farm stayed approximately the same. The average number of crops per farm also decreased. The
observed increase in crop yields was attained via increased use of irrigation, external
inputs (fertilizers, biocides, and energy), and higher quality seeds (Aldabe 2005).
However, this strategy intensified the pressure on the already deteriorated soils and
limited farm resources. Only 27% of the farmers may at times use cover crops,
while 90% of the farmers depend exclusively on chemical fertilizers (Klerkx 2002).
Increasing crop area and narrowing crop types without an adequate planning has
often interfered with farm operations and caused inefficient use of production
resources, increased dependence on external inputs, and greater environmental
impacts. Consequently, farm incomes are inadequate to cover basic family needs, to
maintain farm infrastructure and preserve the natural resource base.
When farmers in Canelón Grande were asked what they perceived to be the main
environmental problems, the most common responses were global climate (39%),
pollution by residues of agrochemical products (15%), and problems with pests and
diseases (11%). Only 9% indicated soil erosion as their main environmental problem
(Klerkx 2002). However, 88% of the interviewed farmers were aware of the occurrence
of soil erosion on their own farms. The use of terracing and maintaining a rough soil
surface were practices that farmers typically perceived to be effective in controlling
erosion, while only 8% mentioned the use of cover crops or the importance of maintaining
adequate vegetation cover (Klerkx 2002). Lack of farmer knowledge about the benefits
of cover crops, therefore, appeared to be a significant constraint to their use, thus
hampering development and adoption of cover-crop-based systems in this region.
3.3.3.3 System Analysis and Exploration of Alternative Systems
During the 1990s, several experiments were conducted on experimental stations
and commercial farms in South Uruguay to investigate the effects of cover crops
and organic amendments on vegetable crop yields and soil quality. When compared
with conventional management, these experiments showed significant increases in
vegetable crop yields after cover crops and animal manure applications. In crops
such as potato, sweet potato, onion, carrot, garlic, and sweet pepper, yield increases
ranged from 9% to 65% after summer or winter green manures when compared
with fallow (Docampo and Garcia, 1999; Garcia and Reyes, 1999; Gilsanz et al.
2004). Winter cover crops tested included oats, black oats, wheat (Triticum aestivum),
and peas (Vicia spp.) in pure stands or in mixtures; summer cover crops were maize,
sorghum (Sorghum bicolor), foxtail millet (Setaria italica), mucuna, cowpea, and
Crotolaria species. Aboveground biomass production ranged from 3.5 to 11 Mg
3
Cover Crops in Agrosystems: Innovations and Applications
89
DM ha−1 and 3 to 19 Mg DM ha−1 for winter and summer cover crops, respectively
(Peñalva and Calegari 2000; Docampo and Garcia, 1999; Garcia and Reyes, 1999;
Gilsanz et al. 2004).
Dogliotti et al. (2005) showed that erosion control support practices such as
terracing are not adequate to decrease soil erosion below the tolerance limits in
vegetable farms in South Uruguay. However, inclusion of cover crops during the
intercrop periods and alternation of horticultural crops with pastures do have the
potential to reduce soil erosion by a factor of 2–4 while reversing SOM losses,
since SOM values increased with 130–280 kg ha−1 year−1 (Dogliotti et al. 2005).
In 2005, a project was initiated by a local team of scientists to develop sustainable
vegetable farming systems in six farms in the region. The study was extended to
16 conventional and organic farms in 2007. On each farm, the development
process involved a continuous cycle of diagnostic-design-implementation-evaluation
components, and initial results were used during a subsequent design and testing
cycle as well.
In mixed farming systems, the use of perennial rye grass and red clover (Lolium
perenne and Trifolium pratense) mixtures or alfalfa (Medicago sativa) can be a
viable production option since it can provide a source of high-quality forage while
also enhancing SOM (Selayu Garvizu 2000). Use of cover crops that include a
small grain species was considered preferable, since they produce greater amounts
of more recalcitrant residues and may be more effective in improving SOM and
minimizing erosion. Selection of annual cover crops was based on seed costs, local
seed availability, and familiarity to farmers. Based on this, suggested species
including black oats (Avena strigosa), foxtail millet (Setaria italica), oat (Avena
sativa), sudan grass (Sorghum × drummondii), and wheat (Triticum aestivum L.)
were integrated into the existing vegetable crop rotations. Above-ground biomass
accumulation by these cover crops ranged from 4.4 to 7.7 Mg ha−1. Where these
cover crops were combined with additions of chicken manure, SOM content
increased from roughly 2.1% to 2.7% within the first 2 years of the study (Rietberg
2008). Long-term (40 years) assessment of the cropping system performance using
the ROTSOM model [based on the approach for modeling outlined by Yang and
Janssen (2000)] SOM values upto 3.5% may be attained, depending on the cropping system, while in the absence of organic amendments, SOM declined to steadystate values around 1.7–1.8% (Rietberg 2008). Although the progress of the
expansion of cover-crop-based systems in Uruguay still lags behind by that in
Brazil, the proven benefits of such systems and the lack of cost-effective alternatives seem to create a situation that will favor their future use.
3.3.4 Interpretive Summary of Case Studies
In general, the innovation of successful cover-crop-based systems has been
relatively successful in Paraná and in Santa Catarina, but relatively unsuccessful in
Florida. Attributes that appear to have facilitated the innovation processes in Paraná
and Santa Catarina include:
90
J.M.S. Scholberg et al.
1. Active involvement by farmers in research and dissemination programs
2. Integration of cover crops into production systems without net loss of land or
labor resources
3. Informing farmers of the (direct) benefits of cover-crop use
4. Provision of multiple benefits by cover crops
5. Sufficient access to information, inputs, and technologies required for covercrop use
6. Provision of skills and experience necessary to manage cover crops effectively
In the case of Florida, many of these attributes have been absent. Unlike Florida, in
Brazil, suitable cover-crops-based systems for small farms have been developed
and successfully implemented in both row crops and vegetable production systems,
zero-tillage equipment is readily available, and these technologies are fully integrated into standard production systems (Prado Wildner et al., 2004; Calegari 2003;
Landers 2001). Moreover, as indicated before, Florida farmers tend to be more
individualistic, may also develop their own technologies to develop a competitive
edge, and may not be willing to share these with other farmers. In this region, innovation in cover-crop-based production systems may thus be required to reward of
farmers for ecological services provided by cover crops. The growth of certified
organic production in Florida and the USA in general may provide a successful
example of such a reward. In this case, the US federal government created a labeling
and certification standard that provided a reliable market “niche.” Within this
market, consumers and producers have allowed to set price premiums that adequately reward producers for organic practices. However, provided that energy and
fertilizer prices continue to rise, there may be a direct economic incentive for use
of cover crops by conventional farmers as well, provided they will have access to
suitable information and cost-effective technologies that can be integrated into their
existing systems.
In Canelones, the innovation of cover-crop-based systems remains in an early
development stage. In this region, experiences in Paraná and Santa Catarina may
provide appropriate development models for implementation of cover-crop-based
systems. However, use of system analysis tools such as ROTAT may actually be
critical to speed up to technology development and adaptation process since they
can provide a systematic structure to streamline the exploration of viable covercrop-based alternatives to the existing conventional rotations. In this manner, land
use options could be evaluated rather effectively, and a limited number of viable
alternatives were then further refined during the on-farm testing and development
stage. Farmer involvement and participation during system design and development
of suitable management options varied from proactive to more passive assimilation
of new technologies. Similar to Paraná and Santa Catarina, farmers who joined the
project during its inception stage played a critical role during the technology adaptation and transfer processes, and their contributions seem to be invaluable to
enhance the regional impact and momentum of technological innovations.
Currently, pilot farmers have assumed ownership of new technologies and provided
leadership during field demonstrations.
3
Cover Crops in Agrosystems: Innovations and Applications
91
3.4 Conclusion
It is concluded that cover crops can contribute to resource conservation and may
provide a viable production option for resource-limited production systems, provided they fit into underutilized niches in the existing agroecosystems. Based on
experiences with functional networks within local farm communities (e.g.,
campesino-to-campesino system), efficient technology transfer of cover-crop-based
systems may occur spontaneously with a minimum requirement of external intervention and/or support structures. This development model can foster local development in regions where traditional local social networks favor such an approach.
However, in other regions, more extensive interventions may be needed. In this
case, the use of co-innovation approach may provide a viable option since it integrates both “science-based intervention” with “farm-based” technology adaptation
mechanisms. In this manner, current systems characteristics, challenges and constraints can be mapped out more effectively and models are being used to explore
and design desirable development tracks. The use of simulation models to harness
some of the complexity of agroecosystems is particularly relevant for cover-cropbased systems. Such an approach may greatly facilitate system design (e.g., development of suitable rotations), assessment of both short-term dynamics (e.g,.
nutrient synchronization) and long-term impacts (e.g., SOM trends as effected by
erosion), and exploration of different development scenarios, e.g., system performance under different climate change scenarios.
Acknowledgments This review was possible as part of international and interdisciplinary collaborations fostered by the EULACIAS program (http://www.eulacias.org/). This program was
funded by the FP6-2004-INCO-DEV3-032387 project titled “Breaking the spiral of unsustainability in arid and semi-arid areas in Latin Americas using and ecosystems approach for coinnovation of farm livelihoods.” The authors also thank Boru Doughwaite for providing conceptual
ideas that helped to structure parts of this review.
References
Abdul-Baki AA, Bryan H, Klassen W, Carrerar L, Li YC, Wang Q (2004) Low production cost
alternative systems are the avenue for future sustainability of vegetable growers in the U.S. In:
Bertschinger L, Anderson JD (eds) Proceedings of the XXVI IHC, Sustainability of
Horticultural Systems. Acta Hort 638:419–423
Abdul-Baki AA, Teasdale JR, Goth RW, Haynes KG (2002) Marketable yields of fresh-market
tomatoes grown in plastic and hairy vetch mulches. HortSci 37:378–881
Abdul-Baki AA, Morse RD, Teasdale JR (1999) Tillage and mulch effects on yield and fruit fresh
mass of bell pepper (Capsicum annum L.). J Veg Crop Prod 5:43–58
Abdul-Baki AA, Teasdale JR, Korcak R, Chitwood DJ, Huettel RN (1996) Fresh-market tomato
production in a low-input alternative system using cover-crop mulch. HortScience 31:65–69
Aldabe L (2005) Una mirada al Sector Hortícola. In: X Congreso Nacional de Hortifruticultura,
23 al 25 de mayo de 2005, Montevideo, Uruguay
Altieri MA (2002) Agroecology: the science of natural resource management for poor farmers in
marginal environments. Agr Ecosyst Environ 93:1–24
92
J.M.S. Scholberg et al.
Altieri MA, Lovato PM, Lana M, Bittencourt H (2008) Testing and scaling-up agroecologically
based organic no tillage systems for family farmers in southern Brazil. In: Neuhoff D et al
(eds) Proceedings of the Second Scientific Conference of the International Society of
Organic Agriculture Research (ISOFAR). University of Bonn, Bonn Vol II, Bonn,
Germany, pp 662–665
Altieri MA, Nicholls CI (2004) An agroecological basis for designing diversified cropping systems in the tropics. J Crop Improv 11:81–103
Alves BJR, Zotarelli L, Boddey RM, Urquiaga S (2002) Soybean benefit to a subsequent wheat
crop in a cropping system under zero tillage. Nuclear techniques in integrated plant nutrient,
water and soil management. Proceedings of an International Symposium held in Vienna,
Austria, 16–20 Oct 2000. International Atomic Energy Agency (IAEA), Vienna, Austria,
pp 87–93
Alves BJR, Zotarelli L, Fernandes FM, Heckler JC, de Macedo RAT, Boddey RM, Jantalia CP,
Urquiaga S (2006) Biological nitrogen fixation and nitrogen fertilizer on the nitrogen balance
of soybean, maize and cotton. Pesqui Agropecuaria Bras 41:449–456
Amado TJC, Bayer C, Conceição PC, Spagnollo E, Costa de Campos BH, da Veiga M (2006)
Potential of carbon accumulation in no-tillage soils with intensive use and cover crops in
southern Brazil. J Environ Qual 35:1599–1607
Anderson S, Gundel S, Pound B, Thriomphe B (2001) Cover crops in smallholder agriculture:
lessons from Latin America. ITDG Publishing, London, 136 pp
Avila L (2006) Potential benefits of cover crop based systems for sustainable production of vegetables, MS thesis, University of Florida, Gainesville, FL, 287 pp. http://etd.fcla.edu/UF/
UFE0015763/avilasegura_l.pdf. Accessed 6 June 2008; verified 15 Oct 2008)
Avila L, Scholberg JMS, Zotarelli L, McSorley R (2006a) Can cover crop-based systems reduce
vegetable crop fertilizer nitrogen requirements in the South eastern United States? HortScience
41:981
Avila L, Scholberg JMS, Roe N, Cherr CM (2006b) Can sunn hemp decreases nitrogen fertilizer
requirements of vegetable crops in the South eastern United States? HortScience 41:1005
Bachinger J, Zander P (2007) ROTOR, a tool for generating and evaluating crop rotations for
organic farming systems. Eur J Agron 26:130–143
Bentley JW (1994) Facts, fantasies, and failures of farmer participatory research. Agric Hum
Values 11:140–150
Bergtold JS, Terra JA, Reeves DW, Shaw JN, Balkcom KS, Raper RL (2005) Profitability and risk
associated with alternative mixtures of high-residue cover crops. Proceedings of the southern
conservation tillage conference, Florence, SC, pp 113–121
Berkenkamp A, Priesack E, Munch JC (2002) Modelling the mineralization of plant residues on
the soil surface. Agronomie 22:711–722
Bhardwaj HL (2006) Muskmelon and sweet corn production with legume GMCCs. HortScience
41:1222–1225
Boddey RM, Sa JCM, Alves BJR, Urquiaga S (1997) The contribution of biological nitrogen fixation for sustainable agricultural systems in the tropics. Soil Biol Biochem 27:787–799
Bouma BAM, Schipper RA, Nieuwehuyse A, Hengsdijk H, Jansen HGP (1998) Quantifying
economic and biophysical sustainability trade-offs in land use exploration at the regional level:
a case study for the Northern Atlantic zone of Costa Rica. Ecol Model 114:95–109
Buckles D, Triomphe B, Sain G (1998) Cover Crops in Hillside Agriculture. IDRC, Ottowa, 218 pp
Bunch R (2000) Keeping it simple: what resource-poor farmers will need from agricultural engineers during the next decade. J Agric Eng Res 76:305–308
Burkett JZ, Hemphill DH, Dick RP (1997) Winter GMCCs and nitrogen management in sweet
corn and broccoli rotations. HortScience 32:664–668
Calegari A, Ferro M, Darolt M (1998) Towards sustainable agriculture with a no-tillage system.
Adv Geoecol 19:1017–1024
Calegari A (2003) Cover crop management. In: Garcia-Tores L, Benites J, Martinez-Vilela
A, Holgado-Cabrera A (eds) Conservation agriculture: environment, farmers-experiences,
innovations, socio-economy, policy. Kluwer, Dordrecht, The Netherlands, pp 191–199
3
Cover Crops in Agrosystems: Innovations and Applications
93
CAMM (2002) Comisión Administradora del Marcado Modelo. http://www.chasque.net/prensa/.
Accessed 1 Sept 2008; verified 15 Oct 2008
CAMM (2005) Comisión Administradora del Marcado Modelo. http://www.chasque.net/prensa/.
Accessed 1 Sept 2008; verified 15 Oct 2008
Carberry PS, Hochman Z, McCown RL, Dalgliesh NP, Foale MA, Poulton PL, Hargreaves JNG,
Hargreaves DMG, Cawthray S, Hillcoat N, Robertson MJ (2002) The FARMSCAPE approach
to decision support: farmers’, advisers’, researchers’ monitoring, simulation, communication
and performance evaluation. Agricult Syst 74:141–177
Cardoso IM, Guijt I, Franco FS, Carvalho AF, Ferreira Neto PS (2001) Continual learning for
agroforestry system design: university, NGO and farmer partnership in Minas Gerais, Brazil.
Agricult Syst 69:235–257
Carrera LM, Buyer JS, Vinyard B, Abdul-Baki AA, Sikora LJ, Teasdale JR (2007) Effects of cover
crops, compost, and manure amendments on soil microbial community structure in tomato
production systems. Appl Soil Ecol 37:247–255
Cherr CM (2004) Improved use of green manure as a nitrogen source for sweet corn. M.S. thesis,
University of Florida, Gainesville, FL. http://etd.fcla.edu/UF/UFE0006501/cherr_c.pdf.
Accessed 3 July 2008; verified 15 Oct 2008
Cherr CM, Avila L, Scholberg JMS, McSorley RM (2006a) Effects of green manure use on sweet
corn root length density under reduced tillage conditions. Renew Agric Food Syst
21:165–173
Cherr CM, Scholberg JMS, McSorley RM (2006b) Green manure approaches to crop production:
a synthesis. Agron J 98:302–319
Cherr CM, Scholberg JMS, McSorley RM (2006c) Green manure as nitrogen source for sweet
corn in a warm temperate environment. Agron J 98:1173–1180
Cherr CM, Scholberg JMS, McSorley RM, Mbuya OS (2007) Growth and yield of sweet corn
following green manure in a warm temperate environment on sandy soil. J Agron Crop Sci
193:1–9
Collins AS, Chase CA, Stall WM, Hutchinson CM (2007) Competiveness of three leguminous
cover crops with yellow nutsedge (Cyperus esculentus) and smooth pigweed (Amaranthus
hybridus). Weed Sci 55:613–618
Corral J, Arbeletche P, Burges JC, Morales H, Continanza G, Couderc J, Courdin V Bommel P
(2008) Multi-agent systems applied to land use and social changes in Río De La Plata Basin
(South America), presentation at the “Empowerment of the rural actors: a renewal of farming
systems perspectives, 8th European International Farming Systems Association (IFSH) symposium”, 6–10 July 2008, Clermont Ferrand, France
Creamer NG, Bennett MA, Stinner BR, Cardina J, Regnier EE (1996) Mechanism of weed suppression in cover crop-based systems. HortSci 31:410–413
Creamer NG, Dabney SM (2002) Killing cover crops mechanically: review of recent literature and
assessment of new research results. Am J Altern Agric 17:32–40
Dabney SM, Delgado JA, Reeves DW (2001) Using cover crops to improve soil and water quality.
Comm Soil Sci Plant Anal 32:1221–1250
Delate K (2002) Using an agroecological approach to farming systems research. HortTechnology
21:345–354
Denef K, Zotarelli L, Boddey RM, Six JW (2007) Microaggregate-associated carbon as a diagnostic fraction for management-induced changes in soil organic carbon in two oxisols. Soil
Biol Biochem 39:1165–1172
Derpsch R (1998) Historical review of no-tillage cultivation of crops. Japan International Research
Center for Agricultural Science (IRCAS), Working Report No 12, 1–18, Paraguay
Derpsch R, Sidiras N, Roth CH (1986) Results of studies made from 1977 to 1984 to control erosion
by cover crops and no-tillage techniques in Parana, Brazil. Soil Till Res 8:253–263
DIEA (2001) Censo general agropecuario 2000. Ministerio de Ganadería Agricultura y Pesca,
Montevideo, Uruguay
DIEA-PREDEG (1999) La horticultura en el Uruguay. Ministerio de Ganadería Agricultura y
Pesca, Montevideo, Uruguay
94
J.M.S. Scholberg et al.
Docampo R, Garcia C (1999) Sistemas de cultivos para la producción hortícola sostenible en el
Región Sur. PRENADER Proyect no. 35, Montevideo, Uruguay
Dogliotti S, Rossing WAH, Van Ittersum MK (2003) ROTAT, a tool for systematically generating
crop rotations. Eur J Agron 19:239–250
Dogliotti S, Rossing WAH, Van Ittersum MK (2004) Systematic design and evaluation of crop
rotations enhancing soil conservation, soil fertility and farm income: a case study for vegetable
farms in South Urugay. Agric Syst 80:277–302
Dogliotti S, Van Ittersum MK, Rossing WAH (2005) A method for exploring sustainable development options at farm scale: a case study for vegetable farms in South Uruguay. Agric Syst
86:29–51
Dogliotti S, Van Ittersum MK, Rossing WAH (2006) Influence of farm resource endowment on
possibilities for sustainable development: a case study for vegetable farms in South Uruguay.
J Environ Manage 78:305–316
Douthwaite B, Keatinge JDH, Park JR (2002) Learning selection: an evolutionary model for
understanding, implementing and evaluating participatory technology development. Agric
Syst 72:109–131
Douthwaite B, Kuby T, Van de Fliert E, Schulz S (2003) Impact pathway evaluation: an approach
for achieving and attributing impact in complex systems. Agric Syst 78:243–265
Drinkwater LE (2002) Cropping systems research: reconsidering agricultural experimental
approaches. HortTechnology 21:355–361
Drinkwater LE, Snapp SS (2007) Nutrients in agroecosystems: rethinking the management
paradigm. Adv Agron 92:163–186
EMBRAPA (2006) Tecnologias de Produção de Soja- Paraná, Londrina, Bazil. Embrapa Soja
Press, Londrina, Brazil, p 217
Gabrielle B, Mary B, Roche R, Smith P, Gosse G (2002) Simulation of carbon and nitrogen
dynamics in arable soils: a comparison of approaches. Eur J Agron 18:107–120
Garcia M, Reyes C (1999) Estudio de sistemas productivos horticolas en el largo plazo, teniendo
como base el manejo de suelos. PRENADER Project no. 35, Montevideo, Uruguay
Giller KE (2001) Nitrogen fixation in tropical cropping systems, 2nd edn. CABI Publishing,
Wallingford, UK, 423 pp
Gilsanz JC, Arboleya J, Maeso D, Paullier J, Behayout E, Lavandera C, Sanders DC, Hoyt GD
(2004) Evaluation of limited tillage and cover crop systems to reduce N use and disease population in small acreage vegetable farms mirror image projects in Uruguay and North Carolina,
USA. In: Bertschinger L, Anderson JD (eds) Proceedings of the XXVI IHC, sustainability of
horticultural systems. Acta Hort 638:163–169
Hasegawa H, Labavitch JM, McGuire AM, Bryant DC, Denison RF (1999) Testing CERES model
predictions of N release from legume cover crop residue. Field Crops Res 63:255–267
Hiltbrunner J, Liedgens M, Bloch L, Stamp P, Streit B (2007) Legume cover crops as living mulches
for winter wheat: components of biomass and the control of weeds. Eur J Agron 26:21–29
IBGE, Instituto Brasileiro de Geografia e Estatística (2008) http://www.ibge.gov.br. Accessed 2
July 2008; verified 2 Sept 2008).
Karlen DL, Cambardella CA, Bull CT, Chase CA (2007) Producer–researcher interactions in onfarm research: a case study on developing a certified organic research site. Agron J 99:779–790
Keatinge JDH, Qi A, Wheeler TR, Ellis RH, Summerfield RJ (1998) Effects of temperature and
photoperiod on phenology as a guide to the selection of annual legume cover and green manure
crops for hillside farming systems. Field Crops Res 57:139–152
Klerkx LWA (2002) Using information on farming and farmers in a model-based exploration of
horticultural production systems in the south of Uruguay. M.Sc. Thesis, Wageningen
University, Wageningen, The Netherlands
Kornecki TS, Raper RL, Price AJ (2004) Effectiveness in terminating cover crops using different
roller implements. Proceedings of the southern conservation tillage conference for sustainable
agriculture, Raleigh, NC, pp 336–345
Landers JN (2001) How and why the Brazilian zero tillage explosion occurred. In: Stott DE,
Mohtar RH, Steinhardt GC (eds) Sustaining the global farm, selected papers from the 10th
3
Cover Crops in Agrosystems: Innovations and Applications
95
international soil conservation organisation meeting held May 24–29, 1999, Purdue University,
West Lafayette, IN, pp 29–39
Leeuwis C (1999) Integral design: innovation in agriculture and resource management. Mansholt
Institute/Backhuys Publishers, Wageningen/Leiden, the Netherlands, 277 pp
Linares JC, Scholberg JMS, Boote KJ, Chase CA, Ferguson JJ, McSorley RM (2008) Use of the
cover crop weed index to evaluate weed suppression by cover crops in organic citrus orchards.
HortScience 43:27–34
Lopez-Ridaura S, Masera O, Astier M (2002) Evaluating the sustainability of complex socioenvironmental systems: the MESMIS framework. Ecol Indic 2:135–148
Lu Y, Watkins KB, Teasdale JR, Abdul-Baki AA (2000) Cover crops in sustainable food production. Food Rev Int 16:121–157
Madden NM, Mitchell JP, Lanini WT, Cahn MD, Herrero EV, Park S, Temple SR, van Horn M
(2004) Evaluation of no tillage and cover crop systems for organic processing tomato production. HortTechnology 14:243–250
Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Rapidel B, de
Tourdonnet S, Valantin-Morison M (2009) Mixing plant species in cropping systems: concepts,
tools and models. A review. Agron Sustain Dev 29:43–62
Masera O, Astier M, López-Ridaura S (2000) Sustentabilidad y manejo de recursos naturales.
Mundi-Prensa Mexico, S.A., 109 pp
Masiunas JB (1998) Production of vegetables using cover crops and living mulches: a review.
J Veg Crop Prod 4:11–31
Matheis HASM, Victoria Filho R (2005) Cover crops and natural vegetation mulch effect achieved
by mechanical management with lateral rotary mower in weed population dynamics in citrus.
J Environ Sci Health 40:185–190
Morse S, McNamara N (2003) Factors affecting the adoption of leguminous cover crops in
Nigeria and a comparison with the adoption of new crop varieties. Exp Agric 39:81–97
Muzilli O (2006) Soil management in direct planting systems. Sistema plantio direto com qualidade.
Instituto Agronomico de Parana (IAPAR), Londrina, Brazil, pp 9–27
NASS (2007) Florida Ag Statistics, National Agricultural Statistics Service Florida Field Office.
http://www.nass.usda.gov/Statistics_by_State/Florida/index.asp. Accessed 6 June 2008; verified
15 Oct 2008)
Neill SP, Lee DR (2001) Explaining the adoption and disadoption of sustainable agriculture: the
case of cover crops in Northern Honduras. Econ Dev Cult Change 49:793–820
Ngouajio M, McGiffen ME, Hutchinson CM (2003) Effect of cover crops and management system on weed populations in lettuce. Crop Prot 22:57–64
Nyende P, Delve RJ (2004) Farmer participatory evaluation of legume cover crops and biomass
transfer technologies for soil fertility improvement using farmer criteria, preference ranking
and logit regression analysis. Exp Agric 40:77–88
Peigné J, Ball BC, Roger-Estrade J, David C (2007) Is no tillage suitable for organic farming?
A review. Soil Use Man 23:12–29
Peñalva M, Calegari A (2000) Usos de los abonos verdes en sistemas de producción hortícolas.
Editorial Peri, Montevideo, Uruguay
Phatak SC, Dozier JR, Bateman AG, Brunson KE, Martini NL (2002) Cover crops and no tillage
in sustainable vegetable production. In van Santen E (ed) Making no tillage conventional:
building a future on 25 years of research. Proceedings of the 25th Annual Southern
Conservation Tillage Conference for Sustainable Agriculture, Auburn, AL, 24–26 June,
pp 401–403
Pieri C, Evers G, Landers J, O’Connel P, Terry E (2002) A road map from conventional to no-till
farming, Agriculture and Rural Development Working Paper, The international bank for reconstruction and development, Washington D.C., 20 pp
Prado Wildner L, Hercilio de Freitas V, McGuire M (2004) Use of green manure/cover crops and
no tillage in Santa Catarina, Brazil. In: Eilittä M et al (eds) Green manures/cover crops systems
of smallholder farmers: experiences from tropical and subtropical regions. Kluwer, The
Netherlands, pp 1–36
96
J.M.S. Scholberg et al.
Quemada M, Cabrera ML, McCracken DV (1997) Nitrogen release from surface-applied cover
crop residues: evaluating the Ceres-N model. Agron J 89:723–729
Rietberg P (2008) Nutrient balances and evolution of organic matter for two vegetable farms in
South-Uruguay. Report of an internship, Departamento de Produccion Vegetal, Universidad de
la Republica, Montevideo, Uruguay, 56 p
Roep D, Wiskerke JSC (2004) Reflecting on novelty production and niche management in agriculture. In: Wiskerke JSC, van der Ploeg JD (eds) Seeds of transition: essays on novelty production, niches and regimes in agriculture. Van Gorcum, Assen, pp 341–356
Rossing WAH, Groot JCJ, Scholberg JMS (2007) Ecosystem modelling toolkit: mobilizing quantitative systems approaches for co-innovation. Wageningen University, Wageningen, The
Netherlands, 43 pp
Sa JCM, Cerri CC, Dick WA, Lal R, Venske Filho SP, Picollo MC, Feigl BE (2001) Organic matter dynamics and carbon sequestration rates for tillage chronosequence in a brazilian oxisol.
Soil Sci Soc Am J 65:1486–1499
Sarrantonio M, Gallandt E (2003) The role of cover crops in North American cropping systems.
J Crop Prod 8:53–74
Scholberg JMS, Dogliotti S, Leoni C, Cherr CM, Zotarelli L (2010) Cover crops for sustainable
agrosystems in the Americas. A review
Schomberg HH, Cabrera ML (2001) Modeling in situ N mineralization in no tillage fields: comparison of two versions of the CERES nitrogen submodel. Ecol Model 145:1–15
Schomberg HH, Martini NL, Diaz-Perez JC, Phatak SC, Balkcon KS, Bhardwaj HL (2007)
Potential for using sunn hemp as a source of biomass and nitrogen for the Piedmont and
coastal regions of the Southeastern USA. Agron J 99:1448–1457
Schomberg HH, Steiner JL, Unger PW (1994) Decomposition and nitrogen dynamics of crop residues: residue quality and water effects. Soil Sci Soc Am J 58:371–381
Scopel E, Da Silva FAM, Corbeels M, Maraux F (2004) Modelling crop residue mulching effects
on water use and production of maize under semi-arid and humid conditions. Agronomie
24:383–395
Selaya Garvizu NG (2000) The role of green manure and crop residues in cropping systems of
South Uruguay, Wageningen University and Research Center, Wageningen, the Netherlands,
63 pp
Sempeho G, Moshi AJ, Shetto RM (2000) Safari report on the third world bank study tour of
Brazil, 6–15 Nov 2000, The international bank for reconstruction and development,
Washington D.C., 9 pp
Shennan C (2008) Biotic interactions, ecological knowledge and agriculture. Philos Trans R Soc
B 363:717–739
Singer JW, Nusser SM (2007) Are cover crops being used in the US corn belt? J Soil Water
Conserv 62:353–358
Sisti CPJ, Santos HP, Kohhan R, Alves BJR, Urquiaga S, Boddey RM (2004) Change in carbon
and nitrogen stocks in soil under 13 years of conventional or zero tillage in southern Brazil.
Soil Till Res 76:39–58
Six J, Elliot ET, Paustian K (2000) Soil macroaggregate turnover and microaggregate formation:
a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem
32:2099–2103
Sommer R, Wall PC, Govaerts B (2007) Model-based assessment of maize cropping under
conventional and conservation agriculture in highland Mexico. Soil Till Res 94:83–100
Speelman EN, Lopez-Ridaura S, Colomer NL, Astier M, Masera OR (2007) Ten years of sustainability
evaluations using the MESMIS framework: lessons learned from its application in 28 Latin
American case studies. Int J Sustain Dev World Ecol 14:345–361
Steiner JL, Schomberg HH, Unger PW (1996) Predicting crop erosion and cover for wind erosion
simulations. http://www.weru.ksu.edu/symposium/proceedings/steiner.pdf. Accessed 2 July
2008; verified 15 Oct 2008
Stoorvogel JJ, Bouma J, Orlich RA (2004) Participatory research for systems analysis: prototyping for a Costa Rican banana plantation. Agron J 96:323–336
3
Cover Crops in Agrosystems: Innovations and Applications
97
Sustainable Agriculture Network (2007) Managing cover crops profitably. Sustainable agriculture network handbook series. Book 3. 3rd edn. Sustainable Agriculture Network, Beltsville,
MD. www.sare.org/publications/covercrops/covercrops.pdf. Accessed 2 June 2008; verified
15 Oct 2008
Tarawali G, Douthwaite B, de Haan NC, Tarawali SA (2002) Farmers as co-developers and adopters of green-manure cover crops in West and Central Africa. In: Barrett CB, Place F, Aboud
AA (eds) Natural resources management in African agriculture: understanding and improving
current practices. CAB International, Wallingford, UK, pp 235–249
Teasdale JR, Brandsaeter LO, Calegari A, Neto FS (2007) Cover crops and weed management. In:
Upadhyaua MM, Blackshaw RE (eds) Non-chemical weed management: principles, concepts
and technology. CABI, Wallingford, UK, pp 49–64
Tittonell P (2008) Targeting resources within diverse, heterogeneous and dynamic farming systems of east Africa. Ph.D. Dissertation, Wageningen University, Wageningen, The Netherlands,
320 pp.
Tommasino H, Bruno Y (2005) Algunos elementos para la definición de productores familiares,
medios y grandes. In: Anuario 2005, OPYPA – MGAP, Montevideo, Uruguay, pp 267–278.
http://www.mgap.gub.uy/opypa/PUBLICACIONES/Publicaciones.htm. Accessed 15 Sept
2008; verified 15 Oct 2008
Triplett GB, Dick WA (2008) No-tillage crop production: a revolution in agriculture. Agron
J 100:S153–S165
Van der Burgt GJHM, Oomen GJM, Habets ASJ, Rossing WAH (2006) The NDICEA model, a
tool to improve nitrogen use efficiency in cropping systems. Nutr Cycl Agroecosyst
74:275–294
Van der Ploeg JP (2008) The New Peasantries, struggles for autonomy and sustainability in an era
of empire and globalization. Earthscan, London, 356 p
Vereijken P (1997) A methodological way of prototyping integrated and ecological arable farming
systems (I/EAFS) in interaction with pilot farms. Eur J Agron 7:235–250
Weil R, Kremen A (2007) Thinking across and beyond disciplines to make cover crops pay. J Sci
Food Agric 87:551–557
Yang HS, Janssen BH (2000) A mono component model of carbon mineralization with a dynamic
rate constant. Eur J Soil Sci 51:517–529
Zotarelli L (2000) Nitrogen balance of crop rotation under no-tillage and conventional tillage in
Londrina-PR. MSc Thesis, Universidade Federal Rural do Rio de Janeiro, Seropédica, RJ,
pp 164
Zotarelli L (2005) Influence of no tillage and conventional tillage and crop rotation on soil aggregation, soil carbon accumulation and nitrous oxide emission in a Rhodic Ferralsol. Ph.D.
Thesis, Universidade Federal Rural de Rio de Janeiro, Seropédica, pp 117
Zotarelli LA, Alves BJR, Urquiaga S, Torres E, dos Santos HP, Paustian K, Boddey RM, Six J
(2005a) Impact of tillage and crop rotation on light fraction and intra-aggregate soil organic
matter in two oxisols. Soil Till Res 95:196–206
Zotarelli L, Alves BJR, Urquiaga S, Torres E, dos Santos HP, Paustian K, Boddey RM, Six J
(2005b) Impact of tillage and crop rotation on aggregate-associated carbon in two oxisols. Soil
Sci Soc Am J 69:482–491
Zotarelli L, Alves BJR, Urquiaga S, Boddey RM, Six J (2007a) Impact of tillage and crop rotation
on light fraction and intra-aggregate soil organic matter in two oxisols. Soil Till Res
95:196–206
Zotarelli L, Scholberg JMS, Dukes MD, Munoz-Carpena R (2007b) Monitoring of Nitrate leaching
in sandy soils: comparison of three methods. J Environ Qual 36:953–962
Zotarelli L, Dukes MD, Scholberg JMS, Hanselman T, Le Femminella K, Munoz-Carpena R (2008a)
Nitrogen and water use efficiency of zucchini squash for a plastic mulch bed system on a sandy
soil. Sci Hort 116:8–16
Zotarelli L, Scholberg JMS, Dukes MD, Munoz-Carpena R (2008b) Fertilizer residence time
affects nitrogen uptake efficiency and growth of sweet corn. J Environ Qual 37:
1271–1278
Chapter 4
Improving Bioavailability of Phosphate Rock
for Organic Farming
Anthony C. Edwards, Robin L. Walker, Phillip Maskell,
Christine A. Watson, Robert M. Rees, Elizabeth A. Stockdale,
and Oliver G.G. Knox
Abstract The sustainable use of nutrients in agricultural food production represents
a major emphasis for international research, and evidence that clearly demonstrates
the imbalance between nutrient inputs and outputs exists. Nutrient surpluses exist
and are most commonly associated with intensive livestock production and present
a particular range of environmentally related issues. Nutrient deficiency can also
develop, and organically managed systems highlight the difficulties that are
involved in maintaining agronomically acceptable concentrations of soil phosphorus (P). A restricted range of P-containing sources, often having poor solubility,
exacerbate these difficulties, and obvious benefits would arise if the availability
could be “naturally” enhanced. Slow rates of phosphate rock (PR) solubilization
under prevailing soil conditions reduce the general agronomic usefulness and
potential benefits that any direct applications might provide. Being able to improve
rates of dissolution through some control of the solubilization process would offer
widespread potential advantages, particularly with respect to better matching
patterns of P supply with crop demand. A variety of pre and postapplication opportunities exist to improve the solubility of rock phosphate. Some of these have particular
relevance to organic agriculture where phosphate rock represents an important and
acceptable “external” source of P. A range of post-application, farm management
practices that include green manures and rotations using crops with favorable traits
that improve P utilization have been successfully employed. Here, we emphazise
pre-application techniques, especially the co-composting of phosphate rock with
A.C. Edwards (*)
Nether Backhill, Ardallie, Peterhead, AB42 5BQ, UK
e-mail: t.edwards25@btinternet.com; t.edwards@macaulay.ac.uk
R.L. Walker and C.A. Watson
SAC, Craibstone Estate, Bucksburn Aberdeen, AB21 9YA, UK
P. Maskell, R.M. Rees, and O.G.G. Knox
SAC, West Mains Road, Edinburgh, EH9 3JG, UK
E.A. Stockdale
Newcastle University, NE1 7RU, UK
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_4, © Springer Science+Business Media B.V. 2010
99
100
A.C. Edwards et al.
various organic by-product materials that include livestock manures and residual
vegetable matter. A range of laboratory incubations have demonstrated the underlying
mechanisms involved with solubilization. The significance of microbially induced
production of organic acids and acidity during composting is particularly important
in this respect. While co-composting with phosphate rock offers a great potential
that could be developed for use at the individual farm scale, the key controlling
factors and underlying mechanisms are far from being fully understood. A possible
time sequence of reactions that might be envisaged include an initial production of
protons and organic acids leading to the mineralogical dissolution and release of Ca
and P, followed finally by an extended period during aging of the compost where
secondary reactions appear to influence the form of P. The consequences of
composting conditions and individual processes on immediate and longer-term
bioavailability of P once field applied are still poorly defined.
Keywords Phosphate rock • composting • sustainability • nutrient use efficiency
Abbreviations
AM
FYM
K
N
P
PSM
SB
arbuscular mycorrhizal
farmyard manure
potassium
nitrogen
phosphorus
phosphate solubilizing micro-organisms
sugar beet
4.1 Introduction
There is a global requirement for increased food production, which must be
achieved while also minimizing potential environmental impacts. Maintaining a
balanced supply of the major plant nutrients is a central requirement of sustainable
resource management, and maximizing nutrient use efficiency can help achieve this
objective (Topp et al. 2007). The sales of agricultural products from farms are
inevitably associated with nutrient export that must be replaced through some combination of fertilizer and recycled by-products, for example, manures and crop residues, biological fixation and atmospheric deposition in the case of nitrogen (N),
and geochemical release through mineral weathering and dissolution in the case of
phosphorus (P) and potassium (K). An imbalance between nutrient offtake and
inputs is a common feature of many global agricultural systems (Smaling et al.
1999). Imbalances can take the form of large accumulated surpluses for N and P in
intensive livestock (Domburg et al. 2000) and peri-urban (Khai et al. 2007) systems
4
Improving Bioavailability of Phosphate Rock for Organic Farming
101
compared to deficits associated with less intensive and some organically managed
agricultural systems (Watson et al. 2002). Links between the build-up of nutrient
surpluses in terrestrial systems and an environmental impact, such as nutrient enrichment and eutrophication of aquatic ecosystems, are commonly assumed. Individual
nutrient imbalances can give rise to a general inability to fully utilize other soil
nutrients efficiently giving rise to an increased risk of loss and environmental
impact.
Increasing costs together with a greater general awareness of the energy and
resource issues associated with the manufacture and use of fertilizer is shifting the
emphasis towards a more sustainable use of nutrients (Kumar and Singh 2001).
This has been given particular international emphasis as a result of the recent oil
price increase. Placing a greater reliance on the recycling of organic waste is not
straightforward. The variability in composition and uncertainty in nutrient bioavailability of recycled materials are important aspects making it difficult to balance
inputs with removals for individual elements. The synchronization of nutrient
supply and crop demand can also be more of a challenge when using nutrients
sources with low solubility. The extent to which imbalances develop varies as a
consequence of site-specific management and farm-related factors that include the
type of material available for recycling together with farm enterprise and soil type.
For example, systems that utilize manure for meeting crop N demand have the
tendency to develop a P surplus (Nelson and Janke 2007) while legumes and associated biological fixation contribute only N.
The narrower range of acceptable materials, and therefore general flexibility to
manage nutrient availability, means these types of issues are particularly relevant
for organic systems. Recent evidence of a declining trend suggests that maintaining
an adequate soil P status is especially difficult. For example, soil sampled from five
Norwegian organic dairy farms on two occasions (minimum 6 years apart) has
demonstrated a general decline in P status (Løes and Øgaard 2001). While in this
example most soils still retained an adequate agronomic P status, a negative P balance suggests that an external source of P will be required sometime in the future.
Similar concerns over low soil P status have been raised for organically managed
Ohio dairy and arable farms (Martin et al. 2007) and negative P balances for Swiss
organic farms (Oehl et al. 2002). Increasing the practical options for improving the
balance and availability of soil P is considered a priority within an organic management context while also having a general relevance to most agricultural systems
(Stockdale et al. 2006).
The general acceptability of phosphate rock (PR) for organic agriculture makes
it an obvious choice for common use. However, a major disadvantage associated
with direct use of phosphate rock is the limited range of situations where the combination of prevailing cropping systems and soil properties offer conditions that
allow dissolution rates to match short-term crop P demand. It is evident that a need
exists to be able to better manage phosphate rock dissolution and subsequent availability of P. An increasing range of management options that offer the potential to
enhance the within field solubilization of phosphate rock avoiding the need for
energy-intensive industrial processes involved in the production of soluble
102
A.C. Edwards et al.
phosphate fertilizers are being explored. Here we review processes of solubilization
relevant to organic agriculture giving particular emphasis to the co-composting of
phosphate rock with various organic materials. Where possible some of the underlying
mechanisms responsible are explored and areas requiring further investigation
highlighted.
4.2 Direct Application of Phosphate Rock
Potential deficits of P in organically managed systems can be offset through the use
of materials acceptable within the organic standards (EEC 1976; 2007) which
include a range of recycled composted vegetable matter and manures together with
phosphate rock. Recommended application rates for phosphate rock are generally
poorly defined. Typically large phosphate rock applications are used, often equivalent to three or more times expected annual crop removal (Scholefield et al. 1999)
potentially increasing the environment risk of P loss occurring during surface soil
erosion events. Poor water solubility of most phosphate rock also represents a
major agronomic disadvantage in the short-term for many crops grown either on
soils with low P status or for more P-demanding crops, such as potatoes.
Comparisons of the agronomic effectiveness between direct applications of phosphate rock and triple super phosphate (TSP) have been more favorable where soil
conditions favor phosphate rock dissolution, such as, temperate grasslands. A longterm comparison of large single applications of phosphate rock and TSP resulted in
significantly greater herbage dry matter yields with the former; although when
smaller annual amounts were compared TSP was superior to phosphate rock
(Scholefield et al. 1999).
Compiling a database of agronomic effectiveness for individual phosphate rock
sources has advantages (Szilas et al. 2007) which (i) make data accessible, (ii)
permit a combined interpretation and allow drawing up conclusions with a wide
scope and relevance, (iii) form a basis for assessing the suitability or otherwise of
phosphate rock in different agroecological zones, and (iv) the database represents a
valuable tool in the determination of research needs regarding utilization and the
development of recommendation systems and would be useful to do within the
present context.
The direct application of phosphate rock is generally successfully used where (i)
local sources represent an economically viable option, a situation often found in
developing countries (Nishanth and Biswas 2008), (ii) properties of soil-cropping
systems offer conditions favorable for dissolution of phosphate rock. Poor mineral
solubility is a common property associated with many types of phosphate rock and
particularly in soils with a pH greater than 5.5–6 (Khasawneh and Doll 1978). The
three most important soil-related factors that influence the rate of dissolution of
phosphate rock in soil are pH, P status, and Ca status (Robinson and Syers 1991).
Sources of phosphate rock differ widely in mineralogy and composition that influences
their dissolution patterns. For example, while the total P contents of various
4
Improving Bioavailability of Phosphate Rock for Organic Farming
103
Table 4.1 A comparison of the total phosphorus (percent P) contents of various phosphate rock
sources (source of data include Schnug et al. 2006 and FAO 2004). The proportion (%) of total P
that is citric acid soluble is also shown
Proportion (%) of total P
Fertilizer
Total P (%)
extractable using citric acid
Reference
a
Tilemsi (Africa)
12.2
29.7
Truong et al. 1978
Hahotoea (Africa)
15.5
19.1
Truong et al. 1978
Gafsaa (Africa)
13.2
37.8
Truong et al. 1978
North Carolina
13.0
15.8
FAO 2004
(USA)a
14.2
8.5
FAO 2004
Central Florida
(USA)a
Araxa (Brazil)b
16.2
3.5
FAO 2004
a
b
Sedimentary
Igneous
phosphate rocks might be similar (Table 4.1) the proportion which is citric acid
soluble varies widely (<5% to more that >35% of the total P). Various methods
have been used to compare the relative effectiveness of individual phosphate rocks
(Chien et al. 1990). One popular approach has been to group according to the
degree to which the phosphate component of apatite has been substituted by carbonate. Kpomblekou and Tabatabai (2003) compared dissolution properties of 12
phosphate rocks that had been grouped into low (Hahotoe, Kodjari, Parc W,
Tahoua), medium (Central Florida, North Florida, Khourigba, Tilemsi Valley) and
high (Gafsa, Minjingu, N. Carolina, Sechura) reactivity. The degree of substitution
by carbonate has important implications for certain mechanisms described in later
sections, which directly influence the rate of dissolution.
4.3 Improving P Utilization from Phosphate Rock
Opportunities exist to improve utilization efficiency of phosphate rock through
some combination of optimizing the conditions to increase phosphate rock dissolution rates, reduce the capacity of soil to fix/immobilize P or select crop traits that
increase uptake/utilization efficiency of P. Here the emphasis is placed upon the
first two aspects (dissolution rate and reduced fixation/immobilization) and an
operational definition which enables those improvements to solubility that take
place during either pre- or post-field application stages to be made (Fig. 4.1).
One of the most common and widespread pre-treatments is a simple physical
grinding to reduce the particle size (Kanabo and Gilkes 1988; Watkinson 1994)
and increase surface area of rock phosphate, which can improve relative
effectiveness by up to three times (Lim et al. 2003). Van Straaten (2002) and
Kpomblekou and Tabatabai (2003) listed several alternatives that have been used
to increase P availability of phosphate rocks: (i) incorporation with various additives
104
A.C. Edwards et al.
Direct application
Rock properties
Mineralogy origin
Chemical composition
Particle size
Pre-application treatments
Mixing with agricultural ‘wastes’
e.g. silage bree or manure
Composting/fermentation
With or without microbial
innoculants
Pre-application
Biological properties of soil/plant system
Plant properties
Cropping system, root morphology, exudation properties
Microbiological inoculants
P solubilizing bacteria/fungi, Mycorrhizal infection
Post-application
Soil physical and chemical properties
Physical aspects
Soil texture, mineralogy,
Chemical aspects
pH, cation and anion exchange capacity, P status
Fig. 4.1 Schematic plan of the factors significantly influencing the dissolution, reactivity, and
uptake of P derived from phosphate rock (PR). A major distinction is made between those factors
which are likely to apply to either pre- or post-application situations
(e.g., Evans et al. 2006), (ii) partial acidulation of phosphate rock (e.g., Chien and
Menon 1995), (iii) compaction of rock phosphate with water-soluble P fertilizers
(e.g., Kpomblekou and Tabatabai 1994) and, (iv) microbial methods.
The biologically mediated options for enhancing the agronomic effectiveness of
phosphate rock have been recently summarized (FAO 2004) as (i) composting
organic wastes with phosphate rock (phospho-composts); (ii) inoculation of seeds
or seedlings with phosphorus-solubilizing microorganisms (fungi, bacteria, and
actinobacteria); and (iii) the inclusion in the cropping system of crop genotypes that
exhibit favorable root attributes (in terms of exudate production and soil exploration
(Gahoonia and Nielsen 2004)), recently reviewed in White and Hammond (2008).
The current focus upon exploring opportunities for improving the solubility of
phosphate rock within organically managed systems means options (i) and (iv)
listed above (often in combination) appear particularly relevant. Improved dissolution rates have been achieved by manipulating conditions during pre-application
treatments, such as co-composting, which utilizes readily available organic materials together with specific microbial inoculants. Typically these biologically mediated decomposition processes provide the necessary conditions that enhance
dissolution rates. A comparatively simple example described by Stamford et al.
(2007) involved the incubation of phosphate rock with elemental sulfur. Mixing
phosphate rock and sulfur inoculated with Acidithiobacillus produced biofertilizers
in field furrows. The requirement for Acidithiobacillus to be added in combination
4
Improving Bioavailability of Phosphate Rock for Organic Farming
105
with sulfur to produce the necessary acidity resulted in six times the quantity of P
solubilized than phosphate rock alone or phosphate rock plus sulfur (Stamford et al.
2007). There are also reports of the direct feeding of phosphate rock to livestock,
although no advantage in terms of solubilizing P was apparent from supplementing
feed for steers with phosphate rock (Odongo et al. 2007).
The enrichment of organic waste products with minerals is of general interest in
the development of sustainable farming. The co-application with on-farm organic
materials such as farmyard manure (FYM) and crop residues has frequently been
employed in developing countries and recently reviewed by Aery et al. (2006). The
incubation of phosphate rock with various types of organic materials and their
decomposition products offers potential for “low technology” widely adoptable
solutions. There is also an added advantage of being able to incorporate minerals in
addition to phosphate rock, such as mica to specifically increase the K content of
composts (Nishanth and Biswas 2008). Dissolution rates and release patterns of P
and K between the two mineral components differed. The range of processes that
contribute to the modified conditions that favor the solubilization of phosphate rock
are essentially similar within both pre- and post-application stages. Dissolution
rates of most sedimentary phosphate rock can be improved through the combined
act of increasing the supply of protons (H+) and the continuous removal of the reaction products of dissolution (e.g., Ca and P, Equation 4.1) from the dissolution zone
(Khasawneh and Doll 1978).
Ca10 (PO 4 )6F2 + 12H + ↔ 10Ca 2 + + 6H 2 PO 4− + 2F −
(4.1)
Raising soil cation exchange capacity will increase the ability to remove Ca and
can be achieved through application of organic amendments (Nying and Robinson
2006) and adopting management practices that favor the build-up of soil organic
matter. The dissolution of calcareous material in the phosphate rock appears to
follow two stages, an initial fast rate followed by a second slower stage (Sengul
et al. 2006). An increase in the availability of soil P has also been attributed to
the addition of organic matter with possible mechanisms include (i) competition
for P adsorption sites; (ii) dissolution of adsorbents; and (iii) changes in the surface
charge on adsorbents (Iyamuremye et al. 1996). The addition of specific organic
acids were demonstrated to decrease soil P adsorption in the order tricarboxylic
acid > dicarboxylic acid > monocarboxylic acid (Bolan et al. 1994). Although
short-lived in soils, their continual production makes the presence of these acids
important (Jones 1998).
Chemically induced changes in the rhizosphere that maximize P uptake through
influencing bioavailability of soil inorganic P have been reviewed by Hinsinger
(2001) and vary considerably with (i) plant species, (ii) plant nutritional status, and
(iii) ambient soil conditions. Kpomblekou and Tabatabai (2003) suggested that
“results from direct additions of phosphate rock to soil have been controversial’…
‘while only a limited amount of literature exists on chemical ways to increase P
availability of phosphate rocks; on the other hand, biological means to increase
available P of phosphate rocks are even more limited.”
106
A.C. Edwards et al.
The solubilization of phosphatic compounds by naturally abundant phosphorus
solubilizing microbes (PSM) appears to be a common attribute under in vitro conditions;
the performance of PSM in situ has been contradictory. The underlying principle of
the microbially mediated processing of natural phosphates is the production of
organic acids that attack and dissolve the phosphates, converting the P to a bioavailable form. Organic acids (including succinic, citric, and formic) have been used for
the industrial beneficiation (refinement) of phosphate rock through the selective
removal of accessory minerals such as carbonates (Ashraf et al. 2005). Ivanova
et al. (2006) reported the optimization of the industrial process reacting Tunisian
phosphorite solubilization with citric, oxalic, and gluconic acids in relation to the
following main factors; the acid concentration, reaction time, ratio of solid/liquid
phases, and natural phosphate fraction. The variability in the performance is
restricting the large-scale direct application of PSM in sustainable agriculture and
has been reviewed under a wide range of agro-ecological conditions by Khan et al.
(2007). Potential technical solutions include those where conditions are optimized
through biotechnological advances, such as selective screening for P solubilizing
activity (e.g., Harris et al. 2006), and molecular techniques including genetic
modification (Rodriguez et al. 2006). Commercially available products include
JumpstartTM that contains Penicillium bilaiane, in which excretion of H+ and
production of organic acid anions reduce Ca2+ activity in solution through complexation. Importantly this treatment can contribute to a short-term solution for P
deficiency; it does lead to depletion of the soil P reserve and therefore does not
replace the need for some external source of P (Takeda and Knight 2006).
4.3.1 Composting
The objective of most pre-application incubations is to provide conditions that
favor the production of acidity and/or chelators of cations (Ca, Al or Fe) (Banik and
Dey 1982). Quantifying the individual significance of either mechanism is difficult
although some partial insight was gained by Reyes et al. (2001) using a UV-induced
mutant of Penicillium rugulosum, which had a greatly reduced capability to solubilize phosphate rock as it lacked the capability of secreting organic acids. There is a
combined role for organic acids and acidity that are produced during the incubation; the actual significance is highly sensitive to the composition of phosphate rock
used. Using closed laboratory incubation systems Kpomblekou and Tabatabai
(2003) compared a range of organic acids, mono-carboxylic acids (glycolic, pyruvic and salicylic), di-carboxylic acids (oxalic, malonic, fumaric, and tartaric), and
tri-carboxylic acids (cis-aconitic and citric) to solubilize P from 12 phosphate
rocks. Generally the oxalic was most effective, but interestingly this was not the
situation for high reactive phosphate rock. Average amounts of P released by all
organic acids were 65.5, 55.1, and 11.1 mmol kg−1 for low, medium, and high
reactivity phosphate rocks respectively. There was a negative correlation with equilibrium pH and a positive one with Ca released. The following trend, from strongest
4
Improving Bioavailability of Phosphate Rock for Organic Farming
107
to weakest: citrate>oxalate >tartarate>malate>HCl has been suggested by Johnston
(1959) and Johnston and Miller (1959). Struthers and Seiling (1960) found citric,
oxalic, butyric, malonic, and lactic acid to be effective in increasing P availability.
Importantly, many of these laboratory-based incubation systems because they are
physically isolated, differ from what might be expected under more open and
dynamic field conditions. The dynamic situation where mixed organic acids are
continuously produced and utilized resulting in highly variable concentrations is
difficult to mimic in the laboratory. It has been suggested that currently unidentified
P-solubilizing compound(s) (molecular weight > 500 Da) may be responsible for
the partial P solubilization (Chuang et al. 2007).
Singh and Amberger (1998) reported the presence of glycolic, oxaloacetic, succinic, fumaric, malic, tartaric, and citric acids in a water extract of a wheat-straw
based compost. These authors made the important observation that initial (up to 30
days) organic acid concentrations were very high and resulted in greater rates of
phosphate rock solubilization; this was followed by a rapid decline, reaching negligible amounts after 120 days of composting. The importance of a balanced general nutrient availability was also demonstrated; addition of N increased the
production of all the listed organic acids and therefore the overall effectiveness of
dissolution. It is clear therefore that the production of reactive organic acids can be
high, but their general persistence is largely dependent on the type and properties
of organic composted material together with its anaerobic decomposition state
(Estaun et al. 1985; Gotoh and Onikura 1971). In mature compost many of these
organic acids are likely to be present only in trace amounts. Several of these acids
are also phyto-toxic and immature compost may be detrimental to germinating
seeds, seedlings, and young plants (De Vleeschauwer et al. 1981). Sundberg and
Jönsson (2005) studied the composting process and conditions under which production of organic acids, mainly lactic and acetic acid, are frequently produced
during initial microbial degradation of food waste, in a process that reduces the pH
to 4–5. This acid-producing process has been observed during storage and collection of waste (Eklind et al. 1997) and during the initial phase of batch composting
(Day et al. 1998). During successful composting, the acids are decomposed and pH
increases (Day et al. 1998). Bangar et al. (1985) reported the capability of
Na-humate to solubilize Mussoorie, a sedimentary phosphate rock, and their significance as chelating agents during composting. Similarly, Satisha and Devarajan
(2005) demonstrated the significant role of humic and fulvic acids for chelating Ca
and retaining P during composting of a sugarcane residue with Mussoorie phosphate rock.
Some of the reason for the conflicting findings may be explained by differences
in phosphate rock properties. For example, Minjingu phosphate rock (Ikerra et al.
2006) or Busumbu phosphate rock (Savini et al. 2006) mixed with a similar
Tithonia-based green manure, showed different results. While the former phosphate
rock showed a positive dissolution effect of the combination no enhanced effectiveness was observed in the latter case. Poor dissolution rates and limited subsequent
plant P uptake from Busumbu phosphate rock may have been related to its high Fe
content. Some evidence of a selective action of organic acids on individual
108
A.C. Edwards et al.
phosphate rock types exists and was well demonstrated by Reyes et al. (2001) who
suggested a difference in action between citric and gluconic acids released by
mutant strains of P. rugulosum with individual fungi showing a phosphate rock type
preference for growth. Similarly, Chuang et al. (2007) demonstrated differences in
organic acid effectiveness between various types of phosphate rock: gluconic acid
was predominantly produced in the presence of Ca–P, whereas oxalic acid predominated with Fe–P and Al–P associated phosphate rock. General differences in the
complexing capabilities of organic acids was reported by Hue et al. (1986) who
found that the Al3+ detoxifying capacities of organic acids (and by inference Al3+
chelating ability) were correlated with the relative positions of hydroxyl and
carboxylic groups on their main carbon chain. Many effective chelators of Al3+ had
hydroxyl groups adjacent to carboxylic groups (i.e., a-hydroxy acid structures),
positions that favored the formation of stable 5-bond ring structures with Al3+.
Gluconic acid has a hydroxyl acid structure and is able to chelate Al3+ and to a
lesser extent, Ca2+ and Fe3+.
4.4 Composting Conditions
The type of organic acids produced during the composting process represents a
potentially important attribute that can be used to enhance phosphate rock solubility. There is scope to modify the composting process through some combination of
altering the composting/fermentation conditions and/or addition of specific microbial inocula. In reality, manipulating conditions in a controlled and reproducible
way in order to regulate decomposition reactions can prove difficult. The chemical
composition or quality of plant residues, as an important regulator of the decomposition system, controls the production of P-solubilizing compounds (Oladeji et al.
2006). The inocula that have been used vary widely (see Table 4.2) but the general
mechanism involved appears to be related to organic acid production. Many isolates
are selected from soil and therefore may not be adapted to composting conditions.
Five strains that were isolated from various composted materials (including farm
waste and rice straw), Enterobacter cloacae EB 27, Serratia marcescens EB 67,
Serratia sp. EB 75, Pseudomonas sp. CDB 35, and Pseudomonas sp. BWB 21,
showed gluconic acid production and solubilized phosphate rock when added to a
broth (Hameeda et al. 2006). The mechanism seemed to include a reduction in pH
and a direct correlation between production of gluconic acid and phosphate rock
dissolution. Zayed and Abdel-Motaal (2005) demonstrated the benefits of using a
phosphate-dissolving fungal strain (A. niger) in addition to a cellulose-degrading
one (Trichoderma viride) added in combination to a mixture of sugarcane residue
(one of the largest agro-industrial byproducts in Egypt) and farmyard manure
(FYM) that not only improved the fermentation process but also compost quality
and the solubilization of phosphate rock measured subsequently using a pot experiment. Acidic conditions (pH 4–5) at the end of the experiment were obtained in all
piles receiving A. niger and there was a correlation between the amounts of soluble
(continued)
Table 4.2 A summary of the literature and experimental conditions employed to test the potential for improving availability of phosphate rock (PR) prior to
any field application
Exp.
Phosphate rock
Particle
Reference
Amendments
Country
details
type/source
size
Test crop
Inocula
Livestock wastes
Alloush 2003
Cattle manure
USA
Linc, p
NC and Syrian
Switch
Penicillium spp
grass
Zayed and AbdelCattle manure plus SB
Egypt
Lp
100 g kg−1, w/w
Broad
Aspergillus niger
Motaal 2005
beans
or Trichoderma viride
Agyin-Birikorang
Poultry manure
West
p
Togo PR
Maize
et al. 2007
Africa
Mahimairaja et al.
Composted with poultry
Linc
1995
manure
India
Linc
Mussourie RP
Included
Bangar et al. 1985
Farm wastes, cattle
(8.1 %P)
CaCO3
dung, soil, and well
decomposed compost
Crop Residues
Egypt
Lp,
ni added at100
Zayed and AbdelRice straw and compost,
Cowpea
A. niger and
g kg−1(dw)
Motaal 2005
fermentation for 106
T. viride
days, turned every 15
days
Caravaca et al. 2004
SB
Spain
F
Morocco (12.8%
<1 mm
Sorghum
A. niger and
P)
Glomus sps to
field
Rodrıguez et al. 1999
SB/Fermentation (10–30
Spain
Lp
Alfalfa
A. niger NB2
days)
Medina et al. 2006
SB/Fermentation (20 days)
Spain
Morocco
<1 mm
T. repens
Glomus
(12.8% P)
4
Improving Bioavailability of Phosphate Rock for Organic Farming
109
Spain
Spain
India
SB/Fermentation
SB/Fermentation
Rice straw + urea (0.25 kg
N) and fresh cow dung
(5 kg) per 100 kg straw
Composting N, mollases,
PR
Virmicompost
Vassilev et al. 2006b
Medina et al. 2007
Biswas and
Narayanasamy
2006
Singh and Amberger
1998
Kumar and Singh
2001
Banik and Dey 1982
India
Spain
Spain
Lp
F
Lp
Exp.
details
<1 mm
<1 mm
Particle
size
Mussourie
Sedimentary PR (high CaCO3)
Morocco (12.8%
<1 mm
P)
Four different PR types
7–10% P
Morocco
(12.8% P)
Morocco
(12.8% P)
Phosphate rock
type/source
Mungbean
T. repens
T. repens
Shrubs
Test crop
A. awamori.
A. niger
A. niger plus AM
A. niger
A. niger
A. niger
Inocula
Pseudomonas
striata
FYM + P, rice + PR
India
Linc
Ca3PO4
A. eandidus, B.
firmus B-7651
Laboratory – L; Laboratory incubation – Linc; pot experiment – p; field experiment – F; ni – no information; SB – sugar beet; NC – North Carolina; dw – dry
weight
Vassilev et al. 1996
Caravaca et al. 2005
Spain
Four Agri wastes/
Fermentation
SB
SB
Vassilev et al., 2006a
Country
Amendments
Reference
Table 4.2 (continued)
110
A.C. Edwards et al.
4
Improving Bioavailability of Phosphate Rock for Organic Farming
111
P released
(mg / kg)
1000
manure and microbes
750
microbes
500
manure
control
250
0
30
45
60
75
Time (Days)
90
105
Fig. 4.2 Phosphorus (water extractable) released from sugarcane residue (bagasse) mixed with
and without farmyard manure (FYM) that had been enriched with phosphate rock and composted
for 105 days (data from Zayed and Abdel-Motaal 2005). After 30 days samples were collected and
analyzed after 15-day intervals. Standard deviations are shown and the treatments are: Without
any treatment (black filling), Treated with FYM (light gray), Treated with A. niger and T. viride
(open), Treated with A. niger, T. viride, and FYM (dark gray)
P and the reduction in pH values in the compost piles. There may be various practical
and cost implications associated with using inocula.
The complex series of reactions that can be involved during co-compositing
together with some of the potential difficulties that can arise from interpolation of research findings are highlighted in Fig. 4.2. A phosphate rock/sugar
residue mixture was incubated in the presence or absence of FYM and a mixed
inocula (Zayed and Abdel-Motaal 2005). The results appear to demonstrate a
straightforward response to additions of FYM and/or the inocula although it is
extremely difficult to actually quantify the relative contribution of “solubilized” P that derives from either the FYM or the phosphate rock. The complexity
of mechanisms that operate during these incubations is also clearly demonstrated by the commonly reported feature that a peak in soluble P occurs, which
in this example occurred around day 75. The following decline in water-soluble
P suggests secondary reactions perhaps involving a change in chemical form
to organic or polyphosphates.
4.5 Forms of P Present in Compost
There has been little direct study on the composition of P that had been solubilized during composting. This is despite the potential importance that
chemical form might have upon subsequent bioavailability and reactivity within
112
A.C. Edwards et al.
soil. It could be postulated that a wide range of P forms might be produced, from
simple orthophosphate ions to polyphosphates and a wide range of organic
P-containing compounds. Some information could be gained from the few detailed
studies made on manure (e.g., Leinweber et al. 1997). Reddy (2007) who applied
low-grade phosphate rock to the litter of soybean showed that approximately
71–92% of the total solubilized P was converted to organic P. While changes in C
and N forms have been reported, evidence for changing forms of P during the
compost period is more circumstantial. For example, Bangar et al. (1985) described
some changes in P during decomposition. An increase in Total P content over time
was proportional to the loss in organic matter during decomposition. Water soluble
P significantly increased when composting was done without phosphate rock, but
decreased during composting with phosphate rock. The P soluble in citric acid
increased significantly during initial composting with phosphate rock but after 60
days citric acid soluble P decreased. Various possible reasons might explain this
observation which include some form of precipitation/sorption reaction of soluble P
with phosphate rock components (e.g., Singh et al. 1980) while Mishra et al.
(1984) observed that initially there was an increase in soluble P, which later converted to di- and tricalcium phosphates that were citric acid soluble when
Aspergillus awarnori was grown in a medium with phosphate rock as the only
source of P. In vitro studies with A. awarnori also revealed that after a certain
period of incubation citric acid soluble P also decreased and was converted into a
citric acid insoluble apatite form (Biswas and Narayanasamy 2006). Goenadi and
Siswanto (2000) also reported an increase in citric acid soluble, but not water
soluble P during an incubation of Moroccan phosphate rock with A. niger.
4.6 Evidence of Utilization
Microbially mediated solubilization of insoluble phosphates through release of
organic acids is often combined with the production of other metabolites, which
take part in biological control against soil-borne phytopathogens. The increase
in plant growth may therefore be due to the release of certain plant growth promoting substances (Kucey et al. 1989). In vitro studies show the potential of
P-solubilizing microorganisms for the simultaneous synthesis and release of
pathogen-suppressing metabolites; mainly siderophores, phytohormones, and
lytic enzymes (Vassilev et al. 2006a). Studies including dual inoculation with
arbuscular mycorrhizal (AM) fungi and other P-solubilizing microorganisms
(Vassilev et al. 2006b) can be expected as the combinations of two such partners
with complementary mechanisms might increase overall biocontrol and plantgrowth-promoting efficacy, thus providing an environmentally safe alternative to
chemicals. The simultaneous application of Rhizobium and PSM (Perveen et al.
2002) and PSM and AM fungi (Zaidi et al. 2003) has been shown to stimulate
plant growth more than inoculation of each microorganism alone especially
under P-deficient soil conditions.
4
Improving Bioavailability of Phosphate Rock for Organic Farming
113
4.7 Future Research Emphasis
The co-composting of phosphate rock with various organic materials offers a
cheap, low technology and therefore widely applicable method of improving P
solubility and bioavailability of P over both short- and long-term timescales.
Published work on the agronomic effectiveness of phospho-composts are scarce
(FAO 2004) and further research is recommended (e.g., Davis and Abbott 2006).
Co-composting with phosphate rock could be developed for use at the individual
farm scale, but for this to become a widely adopted practice some clear protocol
is required. Understanding the range of mechanisms involved and optimizing
the composting conditions to maximize processes that result in solubilizing phosphate rock is necessary. Despite an increasing number of studies that describe the
enhanced solubilization of phosphate rock actual mechanisms involved have not
been fully explained. Interpretation and extrapolation of research findings are being
hampered by a general lack of background information coupled with a lack of any
standardized experimental methodology. On some occasions even the source of
phosphate rock actually used in the experiments is not reported. The change in P
solubility that occurs with time during co-composting operations has occasionally
been monitored, but this has really only highlighted the complexity of the reactions
actually involved. Initial increases in concentrations of soluble P appear to be followed by a decline. This suggests that a series of secondary reactions may be
involved in modifying the chemical form of solubilized P as composting proceeds.
The effects of any subsequent storage stages or consequences for short- or longterm bioavailability after field application are poorly quantified.
Acknowledgments This work forms part of a LINK funded project (http://www.sac.ac.uk/
research/projects/cropsoil/featured/plink/). This work was sponsored by the Department of
Environment Food and Rural Affairs together with the various industrial partners, (The Bulmer
Foundation, Tio Ltd, Scottish Organic Producers Association (SOPA), J & H Bunn Ltd, Abbey
Home Farm, The Leen, Organic Recycling Ltd, Organic Farm Foods Ltd, Soil Association) are
gratefully acknowledged.
References
Aery NC, Rathore NS, Katewa MK, Masih MR (2006) Phosphate rich organic manure. Volume 1.
Himanshu Publications, Udaipur, New Delhi, p 248
Agyin-Birikorang S, Abekoe MK, Oladeji OO (2007) Enhancing the agronomic effectiveness of
natural phosphate rock with poultry manure: a way forward to sustainable crop production.
Nutr Cycl Agroecosys 79:113–123
Alloush GA (2003) Dissolution and effectiveness of phosphate rock in acidic soil amended with
cattle manure. Plant Soil 251:37–46
Ashraf M, Zafar ZI, Ansari TM (2005) Selective leaching kinetics and upgrading of low-grade
calcareous phosphate rock in succinic acid. Hydrometallurgy 80:286–292
Bangar KC, Yadav KS, Mishra MM (1985) Transformation of rock-phosphate during composting
and the effect of humic acid. Plant Soil 85:259–266
114
A.C. Edwards et al.
Banik S, Dey BK (1982) Available phosphate content of an alluvial soil as influenced by inoculation
of some isolated phosphate-solubilizing micro-organisms. Plant Soil 69:353–364
Biswas DR, Narayanasamy G (2006) Rock phosphate enriched compost: an approach to improve
low-grade Indian rock phosphate. Biores Technol 97(18):2243–2251
Bolan NS, Naidu R, Mahimairaja S, Baskaran S (1994) Influence of low-molecular-weight
organic acids on the solubilization of phosphates. Biol Fertil Soils 18:311–319
Caravaca F, Alguacil MM, Azcón R, Dỉaz G, Roldán A (2004) Comparing the effectiveness of
mycorrhizal inoculation and amendment with sugar beet, rock phosphate and Aspergillus niger
to enhance field performance of the leguminous shrub Dorycnium pentaphyllum L. Appl Soil
Ecol 25:169–180
Caravaca F, Alguacil MM, Azcón R, Parlade J, Torres P, Diaz G, Roldán A (2005) Establishment
of two ectomycorrhizal shrub species in a semiarid site after in situ amendment with sugar
beet, rock phosphate, and Aspergillus niger. Micro Ecol 49:73–82
Chien SH, Menon RG (1995) Agronomic evaluation of modified phosphate rock products: IFDC’s
experience. Fert Res 41:197–209
Chien SH, Sale PWG, Friesen DK (1990) A discussion of the methods for comparing the relative
effectiveness of phosphate fertilizers varying in solubility. Fert Res 24:149–157
Chuang CC, Kuo YL, Chao CC, Chao WL (2007) Solubilization of inorganic phosphates and
plant growth promotion by Aspergillus niger. Biol Fertil Soils 43(5):575–584
Davis J, Abbott L (2006) Soil fertility in organic farming systems. In: Kristiansen P, Taji A,
Reganold J (eds) Organic agriculture, a global perspective. CSIRO Publishing, Melbourne,
pp 25–51, Chapter 2
Day M, Krzymien M, Shaw K, Zaremba L, Wilson WR, Botden C, Thomas B (1998) An investigation of the chemical and physical changes occurring during commercial composting.
Compost Sci Util 6:44–66
De Vleeschauwer D, Verdoneck O, Van Assche P (1981) Phyto-toxicity of refuse compost.
Biocycle 22:44–46
Domburg P, Edwards AC, Sinclair AH (2000) A comparison of N and P inputs to the soil from
fertilizers and manures summarized at farm and catchment scale. J Agric Sci 134:147–158
EEC (1976) OJ No L 24, 30. 1
EEC (2007) OJ No L 189/1. Council Regulation (EC) No 834/2007 of 28 June 2007 on organic
production and labelling of organic products and repealing Regulation (EEC) No 2092/91
Eklind Y, Beck-Friis B, Bengtsson S, Ejlertsson J, Kirchmann H, Mathisen B, Nordkvist E,
Sonesson U, Svensson BH, Torstensson L (1997) Chemical characterization of source separated organic household waste. Swed J Agric Res 27:167–178
Estaun V, Calvet C, Pages M, Grases JM (1985) Chemical determination of fatty acids, organic
acids and phenols, during olive marc composting process, Acta Hort 172
Evans J, McDonald L, Price A (2006) Application of reactive phosphate rock and sulphur fertilisers to
enhance the availability of soil phosphate in organic farming. Nutr Cycl Agroecosyst 75:233–246
FAO (2004) Use of phosphate rock for sustainable agriculture. Fertiliser and Plant Nutrient
Bulletin No.13
Gahoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260:47–57
Goenadi DH, Siswanto SY (2000) Bioactivation of poorly soluble phosphate rocks with a phosphorus-solubilizing fungus. Soil Sci Soc Am J 64:927–932
Gotoh S, Onikura Y (1971) Organic acids in a flooded soil receiving added rice straw and their
effect on the growth of rice. Soil Sci Plant Nutr 17:1–8
Hameeda B, Reddy Y, Rupela OP, Kumar GN, Reddy G (2006) Effect of carbon substrates on rock
phosphate solubilization by bacteria from composts and macrofauna. Current Microbiol 53:298–302
Harris JN, New PB, Martin PM (2006) Laboratory tests can predict beneficial effects of phosphate-solubilising bacteria on plants. Soil Biol Biochem 38:1521–1526
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by rootinduced chemical changes: a review. Plant Soil 237:173–195
Hue NV, Craddock GR, Adams F (1986) Effect of organic acids on aluminium toxicity in subsoils.
Soil Sci Soc Am J 50:28–34
4
Improving Bioavailability of Phosphate Rock for Organic Farming
115
Ikerra ST, Semu E, Mrema JP (2006) Combining Tithonia diversifolia and Minjingu phosphate
rock for improvement of P availability and maize grain yields on a chromic acrisol in
Morogoro, Tanzania. Nutr Cycl Agroecosyst 76(2–3):249–260
Ivanova RP, Bojinova DY, Gruncharov IN, Damgaliev DL (2006) The solubilization of rock phosphate by organic acids. Phosphorus Sulphur Silicon Relat Elem 181(11):2541–2554
Iyamuremye F, Dick RP, Graham J (1996) Organic amendments and phosphorus dynamics 1:
phosphorus chemistry and sorption. Soil Sci 161:426–453
Johnston HW (1959) The solubilization of ‘insoluble’ phosphates: V. The action of some organic
acids on iron and aluminium phosphates. N Z J Sci 2:215–218
Johnston HW, Miller RB (1959) The solubilization of ‘insoluble’ phosphate. IV. The reaction
between organic acids and tricalcium phosphates. N Z Jou Sci 2:109–120
Jones DL (1998) Organic acids in the rhizosphere – a critical review. Plant Soil 205:25–44
Kanabo I, Gilkes RJ (1988) The effect of particle size of North Carolina phosphate rock on its
dissolution in soil and on levels of bicarbonate-soluble phosphorus. Fert Res 15:137–145
Khai NM, Ha PQ, Öborn I (2007) Nutrient flows in small-scale peri-urban vegetable farming
systems in Southeast Asia – A case study in Hanoi. Agri Ecosyst Environ 122:192–202
Khasawneh FE, Doll EC (1978) The use of phosphate rock for direct application to soils. Adv
Agron 30:159–206
Khan MS, Zaidi A, Wani PA (2007) Role of phosphate-solubilizing microorganisms in sustainable
agriculture – a review. Agron Sustain Dev 27:29–43
Kpomblekou-A K, Tabatabai MA (1994) Effect of organic acids on release of phosphorus from
phosphate rocks. Soil Sci 158:442–453
Kpomblekou-A K, Tabatabai MA (2003) Effect of low-molecular weight organic acids on phosphorus release and phytoavailabilty of phosphorus in phosphate rocks added to soils. Agric
Ecosyst Environ 100:275–284
Kumar V, Singh KP (2001) Enriching vermicompost by nitrogen fixing and phosphate solubilizing
bacteria. Biores Technol 76:173–175
Kucey RMN, Jenzen HH, Leggett ME (1989) Microbially mediated increase in plant available
phosphorus. Adv Agron 42:199–228
Leinweber P, Haumaier L, Zech W (1997) Sequential extractions and 31P-NMR spectroscopy of
phosphorus forms in animal manures, whole soils and particle-size separates from a densely
populated livestock area in northwest Germany. Bio Fert Soils 25:89–94
Lim HH, Gilkes RJ, McCormick PG (2003) Beneficiation of rock phosphate fertilisers by mechano-milling. Nut Cycl Agroecosyst 67:177–186
Løes A-K, Øgaard AF (2001) Long-term changes in extractable soil phosphorus (P) in organic
dairy farming systems. Plant Soil 237:321–332
Martin RC, Lynch DH, Frick B, van Straaten P (2007) Phosphorus status on Canadian organic
farms. J Sci Food Agric 87:2737–2740
Mahimairaja S, Bolan NS, Hedley MJ (1995) Dissolution of phosphate rock during the composting
of poultry manure: an incubation experiment. Fert Res 40:93–104
Medina A, Vassileva M, Barea J-M, Azcόn R (2006) The growth-enhancement of clover by
Aspergillus-treated sugar beet waste and Glomus mosseae inoculation in Zn contaminated soil.
App Soil Ecol 33:87–98
Medina A, Jakobsen I, Vassilev N, Azcon R, Larsen J (2007) Fermentation of sugar beet waste by
Aspergillus niger facilitates growth and P uptake of external mycelium of mixed populations
of arbuscular mycorrhizal fungi. Soil Biol Biochem 39:485–492
Mishra MM, Khurana AL, Dudeja SS, Kapoor KK (1984) Effect of phosphocompost on the yield
and P uptake of red gram (Cajanus cajan (L.) Millsp.). Trop Agric (Trinidad) 61:174–176
Nelson NO, Janke RR (2007) Phosphorus sources and management in organic production systems. Horttechnology 17:442–454
Nishanth D, Biswas DR (2008) Kinetics of phosphorus and potassium release from rock phosphate and waste mica enriched compost and their effect on yield and nutrient uptake by wheat
(Triticum aestivum). Biores Technol 99:3342–3353
Nying CS, Robinson SJ (2006) Factors influencing the dissolution of phosphate rock in a range
of high P-fixing soils from Cameroon. Commun Soil Sci Plant Anal 37(15–20):2627–2645
116
A.C. Edwards et al.
Odongo NE, Hyoung-Ho K, Choi H-C, van Straaten P, McBride BW, Romney DL (2007)
Improving rock phosphate availability through feeding, mixing and processing with composting
manure. Biores Technol 98:2911–2918
Oehl F, Oberson A, Tagmann HU, Besson JM, Dubois D, Roth H, Frossard E (2002) Phosphorus
budget and phosphorus availability in soils under organic and conventional farming. Nut Cycl
Agroecosyst 62:25–35
Oladeji OO, Kolawole GO, Adeoye GO, Tian G (2006) Effects of plant residue quality, application rate, and placement method on phosphorus availability from Sokoto rock phosphate. Nutr
Cycl Agroecosyst 76:1–10
Perveen S, Khan MS, Zaidi A (2002) Effect of rhizospheric microorganisms on growth and yield
of greengram (Phaseolus radiatus). Ind J Agric Sci 72:421–423
Reddy DD (2007) Phosphorus solubilization from low-grade rock phosphates in the presence of
decomposing soybean leaf litter. Commun Soil Sci Plant Anal 38(1–2):283–291
Reyes I, Baziramakenga R, Bernier L, Antoun H (2001) Solubilization of phosphate rocks and
minerals by a wild-type strain and two UV-induced mutants of Penicillium rugulosum. Soil
Biol Biochem 33:1741–1747
Robinson JS, Syers JK (1991) Effects of calcium concentration and calcium-sink size on the dissolution of Gafsa phosphate rock material in soils. J Soil Sci 42:389–397
Rodriguez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its
potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21
Rodrıguez R, Vassilev N, Azcόn R (1999) Increases in growth and nutrient uptake of alfalfa grown
in soil amended with microbially treated sugar beet waste. Appl Soil Ecol 11:9–15
Satisha GC, Devarajan L (2005) Humic substances and their complexation with phosphorus and
calcium during composting of pressmud and other biodegradables. Commun Soil Sci Plant
Anal 36:805–818
Savini I, Smithson PC, Karanja NK, Yamasaki H (2006) Influence of Tithonia diversifolia and
triple superphosphate on dissolution and effectiveness of phosphate rock in acidic soil. J Plant
Nutr Soil Sci-Z Pflanzenernahr Bodenkund 169(5):593–604
Schnug E, Haneklaus S, Kratz S, Fan X (2006) Aspects of phosphorus fertilisation in organic
farming. Aspects Appl Biol 79:277–281
Scholefield D, Sheldrick RD, Martyn TM, Lavender RH (1999) A comparison of triple superphosphate and Gafsa ground rock phosphate fertilisers as P-sources for grass-clover swards on a
poorly-drained acid clay soil. Nutr Cycl Agroecosyst 53(2):147–155
Sengul H, Ozer AK, Gulaboglu MS (2006) Beneficiation of Mardin-Mazidagi (Turkey) calcareous
phosphate rock using dilute acetic acid solutions. Chem Eng J 122(3):135–140
Singh CP, Amberger A (1998) Organic acids and phosphorus solubilization in straw composted
with rock phosphate. Biores Technol 63:13–16
Singh CP, Mishra MM, Yadav KS (1980) Solubilization of insoluble phosphates by thermophilic
fungi. Annal Microbiol (L. Institut Pasteur) 131 B:289–296
Smaling EMA, Oenema O, Fresco LO (eds) (1999) Nutrient disequilibria in global agro-ecosystems. Concepts and case studies. CAB International, Cambridge
Stamford NP, Santos PR, Santos CES, Freitas ADS, Dias SHL, Lira MA (2007) Agronomic effectiveness of biofertilizers with phosphate rock, sulphur and Acidithiobacillus for yam bean
grown on a Brazilian tableland acidic soil. Biores Technol 98(6):1311–1318
Stockdale EA, Watson CA, Edwards AC (2006) Phosphate rock: using biological processes to
increase its effectiveness as a fertiliser. The International Fertiliser Society, Proceedings No:
592, Cambridge
Struthers PH, Seiling GH (1960) Effect of organic anions on phosphate precipitation by iron and
aluminum as influenced by pH. Soil Sci 69:205–213
Sundberg C, Jönsson H (2005) Process inhibition due to organic acids in fed-batch composting of
food waste – influence of starting culture. Biodegradation 16:205–213
Szilas C, Semoka JMR, Borggaard OK (2007) Can local Minjingu phosphate rock replace superphosphate on acid soils in Tanzania? Nutr Cycl Agroecosyst 77:257–268
4
Improving Bioavailability of Phosphate Rock for Organic Farming
117
Takeda M, Knight JD (2006) Enhanced solubilization of rock phosphate by Penicillium bilaiae in
pH-buffered solution. Can J Microbiol 52:1121–1129
Topp CFE, Stockdale EA, Watson CA, Rees RM (2007) Estimating resource use efficiencies in
organic agriculture: a review of budgeting approaches used. J Sci Food Agric 87:2782–2790
Truong B, Pichot J, Beunard P (1978) Caracterisation et comparaison des phosphates naturels
tricalciques d’Afrique de l’Ouest en vue de leur utilisation directe en agriculture. Agron Trop
33:136–145
Van Straaten P (2002) Rocks for crops: agrominerals of sub-Saharan Africa. ICRAF, Nairobi,
Kenya, p 338
Vassilev N, Fenice M, Federici F (1996) Rock phosphate solubilization with gluconic acid produced by immobilized Penicillium variabile P16. Biotechnol Technol 10:585–588
Vassilev N, Medina A, Azcon R, Vassileva M (2006a) Microbial solubilization of rock phosphate
on media containing agro-industrial wastes and effect of the resulting products on plant growth
and P uptake. Plant Soil 287(1–2):77–84
Vassilev N, Vassileva M, Nikolaeva I (2006b) Simultaneous P-solubilizing and biocontrol activity
of microorganisms: potentials and future trends. Appl Microbiol Biotechnol 71(2):137–144
Watkinson JH (1994) Dissolution rate of phosphate rock particles having a wide range of sizes.
Aust J Soil Res 32:1009–1014
Watson CA, Bengtsson H, Ebbesvik M, Løes A-K, Myrbeck A, Salomon E, Schroder J, Stockdale
EA (2002) A review of farm-scale nutrient budgets for organic farms as a tool for management
of soil fertility. Soil Use Manage 18 (Suppl):264–273
White PJ, Hammond JP (eds) (2008) The ecophysiology of plant–phosphorus interactions, vol 7.
Plant Ecophysiology Series. Springer, Dordrecht, The Netherlands
Zaidi A, Khan MS, Amil M (2003) Interactive effect of rhizotrophic microorganisms on yield and
nutrient uptake of chickpea (Cicer arietinum L.). Eur J Agro 19:15–21
Zayed G, Abdel-Motaal H (2005) Bio-production of compost with low pH and high soluble phosphorus from sugar cane bagasse enriched with rock phosphate. World J Microbiol Biotechnol
21:747–752
Chapter 5
Mixed Cropping and Suppression
of Soilborne Diseases
Gerbert A. Hiddink, Aad J. Termorshuizen, and Ariena H.C. van Bruggen
Abstract Soilborne pathogens are difficult to manage, especially since the use of
methyl bromide has been phased out in most countries. Resistance against many
soilborne pathogens is hardly available and fungicides are effective only to a limited
extent. In organic agriculture, many problems related to soilborne pathogens are
avoided by applying wide rotations, but still some polyphagous soilborne pathogens
can be highly problematic, especially since most chemical crop protectants are not
allowed. In addition, wide rotations are often economically unprofitable. Therefore,
alternative practices to manage soilborne pathogens are needed. In this review, the
occurrence of soilborne pathogens in three types of cropping systems are evaluated:
(i) continuous cultivation of single crops in monoculture, (ii) crop rotation, and
(iii) mixed cropping, i.e., cultivation of multiple crops in the same field at the same
time. Both continuous cropping and crop rotation have been investigated extensively.
Therefore, in this chapter we focus on mixed-cropping systems in relation to soilborne pathogens, their potential to suppress soilborne diseases, and the mechanisms
underlying disease suppression. In general, mixed cropping is practiced to optimize
nutrient uptake, control soil erosion, suppress the epidemic spread of airborne pathogens, and improve crop yields per unit of area. While mixed cropping has received
attention for its effects on airborne pests and pathogens, the effects on soilborne
pathogens are poorly known. In 30 out of 36 publications, mixed cropping showed
a significant reduction in soilborne disease and in six, no or a positive effect on
disease incidence or severity was found. Diseases caused by splash-dispersed pathogens
were less severe in mixed-cropping systems in ten out of 15 studies. The magnitude
G.A. Hiddink (*)
Enza Zaden, Seed Operations BV, Haling 1e, 1602 DB Enkhuizen, The Netherlands
e-mail: g.hiddink@enzazaden.nl
A.J. Termorshuizen
Blgg, Nieuwe Kanaal 7-f, 6709 PA Wageningen, The Netherlands
A.H.C. van Bruggen
Plant Pathology Department, IFAS, University of Florida, 1453 Fifield Hall,
Gainesville, FL, USA
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_5, © Springer Science+Business Media B.V. 2010
119
120
G.A. Hiddink et al.
of disease reduction in mixed compared to single crops varied, from a 63% reduction
to a 100% increase in disease. Host dilution appeared to be the most important
mechanism of disease suppression for both soilborne and splash-dispersed pathogens
(12 and five cases, respectively). Although the use of mixed cropping for soilborne
disease suppression is still in its infancy, the wide range of biological effects and
interactions observed holds promise for further optimization and management of
soilborne diseases, for example, by selecting plant species and cultivars that provide
an optimal combination of root architectures.
Keywords Mixed cropping • intercropping • soilborne pathogens • crop rotation
• microclimate • monocropping • multiple cropping • disease management • allelopathy • ISR (induced systemic resistance) • SAR (systemic acquired resistance)
• microbial antagonism
5.1 Introduction
During the past decades, intensified mechanization and the use of synthetic fertilizers and crop protectants have substantially increased agricultural yields. However,
these practices also resulted in an array of adverse environmental side effects,
including soil erosion, water pollution, eutrophication, and reduced innate soil fertility (Gliessman 2001). Acquisition of capital-intensive and crop-specific machinery further narrowed rotations. Although these negative side effects of intensive
agriculture counteract the initial increase in food production per unit of area
(Matson et al. 1997), ultimately they may lead to a decline in total food production
because of land becoming unproductive due to soil erosion and pollution. On the
other hand, increasing demands for agricultural products can be met only when
high yields per unit of area are achieved, especially when productive land is falling
short (Hill 2007). Therefore, it is necessary to find more sustainable ways of cultivating crops without sacrificing on the yield.
Narrow rotations of cash crops have resulted in a high incidence of soilborne diseases (Garrett and Cox 2006). Although genetic resistance and effective pesticides are insufficiently available, many soilborne pathogens, such as
Gaeumannomyces graminis var. graminis, can be managed by wide crop rotations
(Werker and Gilligan 1990) and other cultural measures (Cook 2001). However,
wide crop rotations are, from an economic point of view, undesirable in areas where
arable land is limited. Soil fumigants can be highly effective, especially for the
control of nematodes, but they have a strong negative impact on non-target organisms and therefore their use is discouraged or prohibited (Martin 2003; Schneider
et al. 2003). Methyl bromide, the most common soil fumigant for decades, was
added to the list adopted by the Montreal protocol in 1997 and will be banned
completely in 2015 (Gullino et al. 2003, Liu et al. 2007). Most soil fumigants are
5
Mixed Cropping and Suppression of Soilborne Diseases
121
costly and generally too expensive for low-value crops like cereals or for use by
subsistence farmers in the developing countries. The application of methods specifically designed to control soilborne pathogens, such as biological soil disinfestation, soil solarization, and flooding, is also often too costly, so they are applicable
only to capital-intensive crops (Blok et al. 2000).
While mixed cropping has received attention for its effects on airborne pests
(Björkman et al. 2008; Bukovinszky et al. 2004; Risch et al. 1983) and pathogens (Mundt 2002a; Wolfe 1985), the effects on soilborne pathogens barely
have attracted attention. In this review, we evaluate how cropping systems and
in particular mixed cropping can affect soilborne pathogens. We first define the
different types of cropping systems and specifically continuous single-crop
cultivation (monoculture), crop rotation (i.e., change of crop diversity in time),
and mixed cropping (i.e., any type of growing multiple crops in the same field
at the same time). Then we will in short assess and discuss how these cropping
systems can affect the dynamics of soilborne diseases. The effects of mixed
cropping on soilborne and splash-dispersed fungal and bacterial pathogens will
be discussed as well as the mechanisms underlying disease suppression by
mixed cropping. We end this review with recommendations and options for the
use of mixed cropping that may contribute to improving the sustainability of
agricultural production.
5.2 Design of Cropping Systems to Manage Soilborne Diseases
In modern agriculture, cultivation of single crops in a rotation is the most common
cropping system for a vast range of crop species worldwide. If properly designed,
crop rotation is the most efficient (cultural) practice to reduce the incidence and
severity of soilborne diseases (Cook and Veseth 1991). However, crop rotation is
not always practiced. In highly mechanized productions, continuous cultivation
of the same single crop is regularly practiced, whereas in areas where mechanization, artificial fertilizers, and crop protectants are too costly, diverse forms of
mixed cropping are encountered regularly. Disease suppression related to crop
rotation and continuous single-crop production has been extensively investigated
(Mazzola 2002; Schneider 1982; Weller et al. 2002). However, the effects of
mixed cropping on soilborne pathogens have received considerably less attention.
Where in literature effects of mixed cropping on soilborne pathogens are reported,
they often appear just as a co-observation in studies on crop productivity. The
main reasons why the effects on soilborne pathogens have received little attention
are the inconspicuous nature of soilborne diseases (Cook 2001), the aspecific
disease symptoms, and the inherent difficulty of designing experiments with
mixed-cropping systems. A typical example of a disease with aspecific symptoms
is Potato Early Dying (Rowe et al. 1987), caused by Verticillium dahliae, which
is often erroneously held for drought stress. Furthermore, disease can go unnoticed
for some time as is the case for spinach wilt caused by Verticillium dahliae, which
122
G.A. Hiddink et al.
induces symptoms only after bolting so that disease is not observed in fresh
produce (duToit et al. 2005).
5.2.1 Successive Cultivation of a Single Crop
Continuous cultivation of the same single crop in the same field is practiced in areas
where the number of crops that can be grown is agronomically and economically
limited (Cook 2001). Under these conditions, mechanization makes cultivation
more economically feasible but at the same time hinders the adoption of a more
diversified crop rotation. In continuous crop cultivation, inoculum densities of
soilborne pathogens increase without exception and a certain degree of damage has
to be accepted (Shipton 1975). Some cultural measures including reduced tillage
can enhance the survival of certain pathogens (Meynard et al. 2003; Pankhurst et al.
2002). Regular tillage can lead to burial of inoculum of Pseudocercosporella herpotrichoides and limit disease progress in the following season (Colbach and
Meynard 1995). On the other hand, reduced tillage and direct drilling resulted in
suppression of Gaeumannomyces graminis var. graminis (Pankhurst et al. 2002)
because of increased soil organic carbon concentrations and consequently higher
microbial activity compared to conventional tillage. Also stimulation of microbial
activity through organic amendments can reduce pathogen inoculum or activity
(Hoitink and Boehm 1999).
For certain pathosystems, natural disease suppression is known to be induced
during continuous cultivation (Schneider 1982; Weller et al. 2002), e.g.,
Gaeumannomyces graminis in wheat and barley (Gerlagh 1968; Raaijmakers and
Weller 1998; Weller et al. 2002), Rhizoctonia solani in sugar beet (Hyakumachi
and Ui in Sturz and Christie 2003), Streptomyces scabies in potato (Menzies
1959), and Fusarium oxysporum f. sp. melonis in melon (Alabouvette 1999).
Induction of disease suppression can take multiple years and generally it is lost
after growing other crops (Shipton 1975). The mechanisms involved have been
studied extensively and are linked to the microbial community in soil or the
rhizosphere. The best-known mechanisms include antibiotic production (e.g., by
strains of Pseudomonas fluorescens), competition by closely related non-pathogenic
strains (e.g., competition for carbon by nonpathogenic Fusarium oxysporum),
and parasitism (e.g., by Trichoderma spp.) (Weller et al. 2002). For these types of
disease suppression to develop and to sustain, both the pathogen and a susceptible
host plant need to be present and a certain level of damage has to be accepted.
Overall, adequate disease suppression in continuous monocropping systems can
be induced in several pathogen–crop combinations. However, other pathogens on
the same crop can become problematic. Moreover, the unpredictable time span
needed for induction of specific disease suppression and the inflexibility of the
cropping system, result in limited applicability of this system for soilborne
disease management.
5
Mixed Cropping and Suppression of Soilborne Diseases
123
5.2.2 Crop Rotation
Crop rotation is the practice of growing crops on the same field sequentially in
time. Crop rotation is commonly practiced to avoid the buildup of soilborne pathogens
(Cook and Veseth 1991), to maintain a balanced soil fertility, and to avoid intensive soil tillage before planting root crops (Termorshuizen 2001). The beneficial
effect of crop rotation against many soilborne pathogens is due to their limited
host range (Krupinsky et al. 2002). The host-dependent reproduction of most
pathogens (Garrett and Cox 2006) limits inoculum buildup and viability of the
inoculum present diminishes in time when nonhosts are grown (Cook 2001).
Alternations of dicotyledonous with monocotyledonous crops are effective in limiting the inoculum levels of the majority of soilborne plant pathogens (Agrios
1997). Alternation with hosts that do not support inoculum production can be a
measure to reduce the amount of pathogen inoculum. For example, sugar beet is a
host to Verticillium dahliae, but hardly contributes to inoculum buildup, as microsclerotia have not yet been produced at the time when roots are harvested
(A.J. Termorshuizen, personal observation).
Green manure or cover crops cultivated in wintertime can be part of the crop
rotation. The main reason to grow a green manure crop is to protect soil from
erosion and to prevent leaching of mineralized nitrogen. In narrow rotations with
a high pressure of soilborne pathogens, the choice of the optimal green manure
crop can be a challenge. For example, to reduce nitrate leaching in sandy soils
in wintertime in the Netherlands, it is now obligatory to grow a green manure
crop following maize cultivation. Due to the late harvest of maize, the choice of
green manure crops is usually limited to a grass or winter cereal, which to a great
extent resembles maize with respect to its host status for nematodes. The single
option farmers have is to harvest their maize earlier, so that they can still sow
mustard. Several green manures are known for their capacity to reduce diseases
caused by soilborne pathogens. Incorporation of several Brassica species has
been shown to reduce disease incidence caused by Rhizoctonia solani,
Phytophthora erythroseptica, Pythium ultimum, Sclerotinia sclerotiorum, or
Fusarium sambucinum in potato (Larkin and Griffin 2007). The underlying
mechanism involves the production of toxic volatiles during decomposition of
the cruciferous organic matter. Marigold (Tagetes spp.) is grown as a green
manure to specifically suppress Pratylenchus penetrans (Kimpinski et al. 2000),
which is likely due to toxic plant exudates.
The effective length of crop rotation as a method to manage specific soilborne
pathogens depends on the survival of the pathogen. For example, the resting spores
of Spongospora subterranea, the causal agent of powdery scab of potato, can survive for many years in the absence of a host (Jeger et al. 1996), while the survival
of Gaeumannomyces graminis is limited to only a few years at most (Gerlagh
1968). Crop rotation is therefore not suitable to manage powdery scab, but it can be
a valuable measure to manage take-all disease caused by G. graminis (Cook 2001).
For various other soilborne pathogens, e.g., Verticillium dahliae, Rhizoctionia
124
G.A. Hiddink et al.
solani, root knot nematodes (Meloidogyne spp.) and root lesion nematodes
(Pratylenchus spp.), the design of a proper rotation can be difficult because these
pathogens are capable of infecting and/or surviving on multiple hosts.
Crop rotation is a flexible disease management system that is capable of reducing
disease losses caused by many soilborne pathogens. However, the need for rotating
high-value crops with lower-value crops and the relatively high risk of losing a
complete crop make this system often less attractive to farmers.
5.2.3 Mixed-Cropping Systems
Mixed cropping is defined as the cultivation of a mixture of two (or more) crops
together in the same field (Trenbath 1976; Willey 1979). There are various types of
mixed cropping (Geno and Geno 2001; Vandermeer 1990), each of which may
affect soilborne pathogens differently (Table 5.1, Fig. 5.1). Mixed-cropping systems
can be characterized according to the degree to which roots of different crop species
interact, which is determined not only by the mixed-cropping system but also
by the root architecture of each of the crops in the mixture (de Kroon 2007;
Weaver 1926).
We define here mixed cropping sensu stricto as the practice of growing multiple
crops simultaneously without a specific spatial structure. This way of cropping is
used frequently in slash-and-burn fallow agriculture or ley farming with multilines
or species mixtures (e.g., broadcast-sown grass-clover mixes). In a mixed setting,
distances between hosts are generally greater than when grown as single crops and
disease will spread more slowly (host dilution). Also allelopathy (Natarajan et al.
1985), microclimate change (Luthra and Vasudeva 1940), root camouflage (Gilbert
et al. 1994), and microbial antagonism have been proposed as potential mechanisms underlying the disease suppression induced by mixed cropping (Abadie et al.
1998; Soleimani et al. 1996).
Strip mixed cropping is the “strip-wise simultaneous cultivation of multiple
crops in rows, wide enough to permit independent cultivation but still sufficiently
narrow to interact agronomically” (quoted from: Vandermeer 1990) (Fig. 5.2).
Typically, the width of the strips is adapted to the size of the machinery to be used.
Since the crops co-occur on a narrow strip, belowground interactions between the
different crop species occur relatively infrequently and therefore the effects on
soilborne pathogens are considered to be minor.
Relay mixed cropping is the simultaneous cultivation of multiple crops during
only part of their field period. The second crop is planted at the time when the first
crop reaches its reproductive stage but has not yet been harvested. When root systems of both crops overlap sufficiently, disease-suppressive effects due to allelopathy, microbial antagonism, or physical separation between pathogen and host may
occur. Because of the time gap between sowing of both crops (strip), tillage
between rows of the standing crop can affect pathogen establishment and spread by
burial of inoculum (Colbach and Meynard 1995; Meynard et al. 2003).
Absence of host
- Between rows barrier
effect, within rows no
effect
- Reduced genetic
susceptibility
- Microclimate
(induction of disease)
- ISRa
- Reduced genetic
susceptibility
- Barrier affect/ spore
trapping
- Microclimate
(Induction of disease)
- ISRa
Diversity between
species
Diversity between
species
Diversity between
species
Crops sown
widespread or
in rows
A row of one crop
is at both sides
accompanied by a
row of the other
One crop sown
in rows or
widespread, the
other widespread
Relay cropping
Row mixed
cropping
Mixed cropping
- Barrier effect/ spore
trapping
- Microclimate
(induction of disease)
Sown in more than Diversity between
one row of the same species
crop next to each
other
Strip cropping
- Barrier effect (splash
dispersal)
- Reduced genetic
susceptibility
- Distance effect
- Reduced chemotaxis
- Allelopathy
- ISRa
- Microclimate (inoculum
reduction and induction
of disease)
- Antagonists/competition
- Barrier effect (splash
dispersal)
- Distance effect
- Allelopathy
- ISRa
- Microclimate (inoculum
reduction and induction
of disease)
- Absence of host
- Allelopathy
- Inoculum reduction
- Microclimate
(induction of disease)
- Distance effect
At the same
time
Same or
different
planting time
Delayed
planting time
Same or
different
planting time
Table 5.1 Mixed-cropping systems (Geno and Geno 2001; Vandermeer 1990) and theoretical disease-reducing mechanisms
Possible disease-reducing mechanisms
Name
Sowing layout
Diversity
Airborne pathogens
Soilborne pathogens
Planting time
(continued)
No mechanization
to fully
mechanized
No mechanization
to fully
mechanized
Fully mechanized
Fully mechanized
Mechanization
grade
Crops grown
widespread
or in rows but
having different
dimensions
(height, volume,
and size)
Completely
random, no
predetermined
layout
Multistorey
cropping
Natural
ecosystems
Induced systemic resistance
Completely
random
widespread or in
rows
Multiline
cropping
a
Sowing layout
Name
Table 5.1 (continued)
- Absence of host
- Reduced genetic
susceptibility
- ISRa
- Barrier affect/spore
trapping
- Microclimate
(induction of disease)
- Barrier effect/spore
trapping
- Microclimate
(induction of disease)
- ISRa
Diversity between
height levels
Diversity within
and between
species
- Reduced genetic
susceptibility
Diversity within
species
Same planting
time
Planting time
susceptibility
- Barrier effect (splash
dispersal)
- Distance effect
- Reduced chemotaxis
- Allelopathy
- ISRa
- Microclimate (inoculum
reduction and induction
of disease)
- Antagonists/competition
At the same
- Barrier effect (splash
time
dispersal)
- Microclimate (inoculum
reduction and induction of
disease)
- Reduced chemotaxis
- Allelopathy
- Antagonists/competition
Can be any
- Absence of host
time
- Reduced genetic
- Reduced genetic
susceptibility
Possible disease-reducing mechanisms
Airborne pathogens
Soilborne pathogens
Diversity
No mechanization
No mechanization
to fully
mechanized
Fully mechanized
Mechanization
grade
5
Mixed Cropping and Suppression of Soilborne Diseases
127
Fig. 5.1 Mixed-cropping systems
Row mixed cropping is defined as the production of multiple crops alternately
planted in rows. It can be done in an additive design, where both crops are sown at
their single densities (Fig. 5.3) or in a replacement design, where one crop is
replaced by the other (Fig. 5.4). Irrespective of plant density, disease can spread
within rows like in single-culture cropping systems, but between rows the alternate
crop(s) can act as a barrier (Michel et al. 1997). Here, host dilution (replacement
design), allelopathy, root camouflage, and microbial antagonism may play a role in
disease suppression.
128
G.A. Hiddink et al.
Fig. 5.2 Strip mix crop (Photo courtesy of Tim McCabe 1999, USDA-NRCS)
Fig. 5.3 Mixed crop, Brussels sprouts–barley, additive design (Photo: G.A. Hiddink)
5
Mixed Cropping and Suppression of Soilborne Diseases
129
Fig. 5.4 Mixed crop, triticale–clover, replacement design (Photo: G.A. Hiddink)
Multistorey mixed cropping (Fig. 5.5) is the cultivation of tall perennials combined
with shorter biannual or annual crops and is practiced in orchards, tree nurseries,
and agroforestry. The area between the rows is used to grow a cover crop to suppress weeds, fix nitrogen, reduce nutrient leaching, and increase the productive
surface area. Allelopathy is a possible mechanism of disease suppression, but also
roots can act as a physical barrier for pathogen spread, root camouflage, and microbial antagonism.
Natural vegetation consists mostly of multiple species and can be considered to
be closely related to (zero-tillage) mixed cropping. The disease-suppressive mechanisms that operate in natural ecosystems are probably comparable to the mixed
cropping or multistorey mixed-cropping system.
As may be clear from the definitions of the different types of mixed cropping,
mixed cropping can have many appearances and characteristics. These characteristics often determine if soilborne diseases can be suppressed and what mechanisms
for suppression can be held responsible for this disease suppression.
130
G.A. Hiddink et al.
Fig. 5.5 Multistorey mix crop (Photo courtesy of: Gary Kramer 2001, USDA-NRCS)
5.3 Disease Reduction in Mixed-Cropping Systems
In 30 out of the 36 studies where the fate of soilborne pathogens was investigated
in mixed-cropping systems, soilborne disease was significantly reduced in the mixtures. In the remaining six studies, there was no or a negative effect of mixed cropping on disease suppression (Table 5.2). In ten cases, a positive effect was reported
for splash-dispersed pathogens against five with no or negative effects (Table 5.2).
The most investigated crop appeared to be wheat, where in nine out of 15 cases
(wheat as main crop) disease was reduced in the mixture. Clover was most important as secondary crop in six mixtures with a disease reduction in five of those
mixtures. In the following sections, we will discuss the most important proposed
disease-suppressive mechanisms and try to explain how they could be operational
in mixed-cropping systems.
Type
Mixed cropb
Mixed cropb
Mixed cropb
Mixed cropc
Mixed cropb
Mixed cropb
Mixed cropb
Mixed cropb
Nr
1
2
3
4
5
6
7
8
sb
sb
Ralstonia
solanacearum
Ralstonia
solanacearum
Ralstonia
solanacearum
Rhizoctonia solani
sb
sb
sb
sb
sb and
Fusarium spp.,
insect
Phoma spp.,
Cercospora spp., and
black leafhopper
Fusarium spp.
Tomato
Tomato
Tomato
Radish
Oat
Barley
Barley
Alfalfa
Pathogen
typea
Main crop
Rhizoctonia cerealis, sb
Fusarium spp.
Pythium irregulare
Pathogen
Table 5.2 Effects of mixed cropping on soilborne pathogens
Welsh onion
Soybean
Cowpea
Mustard
Berseem
clover
Wheat
Oats
Wimmera
ryegrass
Second crop
16%
12% and
38% (fraction
mustard in mix
resp 25% and
50%)
12%
50%
R. cerealis: 6%;
Fusarium spp:
23%
13–44%
No wilt reduction –
No significant
reduction in wilt
Reduced wilt
Reduced disease
progress
Improved plant
health
Reduced disease
incidence
Reduced disease
incidence
Reduced
infection rate
Effect
magnitude
relative
Effect in mixture to sole crop
No barrier present
at transplanting
Physical barrier
Physical barrier
Host dilution
No mechanisms
mentioned
(continued)
Michel et al.
1997
Michel et al.
1997
Michel et al.
1997
Otten et al.
2005
Holland and
Brummer
1999
Vilich-Meller
1992
Vilich-Meller
1992
Host dilution/
physical barrier
Physical barrier/
host dilution
Burdon and
Chilvers 1976
Reference
Host dilution
Proposed
mechanism
Type
Mixed cropb
Mixed cropb
Mixed cropc
Mixed cropb
Mixed cropb
Mixed cropc
Mixed cropc
Nr
9
10
11
12
13
14
15
Table 5.2 (continued)
sb
Gaeumannomyces
graminis var. tritici
Gaeumannomyces
graminis var. tritici
Gaeumannomyces
graminis var. tritici
Rhizoctonia cerealis
Gaeumannomyces
graminis var. tritici
sb
sb
sb
sb
sb
Wheat
Wheat
Wheat
Wheat
Wheat
Watermelon
Triticale
Pathogen
typea
Main crop
Fusarium oxysporum sb
f. sp. niveum
Gaeumannomyces
graminis var. tritici
Pathogen
Grasses
Clover
Barley
Barley
Clover
Rice
White clover
Second crop
10–35%,
depending on
the previous
crop
5–30%,
Depending on
the previous
crop
67%
Reduced disease
severity and
incidence in
bioassay
4–34%,
Depending on
grass species
cultivated
Reduced disease 42% (Avg of 2
rating in bioassay years)
Reduced disease
severity
Reduced disease
incidence
No significant
effect on yield
Reduced wilt
Reduced disease 1–1.8 Disease
pointd
severity after 5
successive cycles
Effect
magnitude
relative
Effect in mixture to sole crop
Garrett and
Mann 1948
Host root dilution or Gutteridge
et al. 2006
direct suppression
effect
Reduced survival
of the pathogen
due to increased
nitrogen uptake
Vilich 1993
Vilich 1993
Host dilution
Host dilution
Zogg 1963
Ren et al.
2007
Reference
–
Allelopathy of
root exudates on
Fusarium spores
Changed microbial
community
structure
Proposed
mechanism
Type
Mixed cropc
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Nr
16
17
18
19
20
21
22
23
24
25
sb
sb
sb
sb
sb
Sclerotium
cepivorum
Macrophomina
phaseoli and
Rhizoctonia solani
sb
sb
Fusarium oxysporum sb
f. sp. ciceris
Erwinia carotovara
ssp. carotovora
Fusarium oxysporum sb
f. sp. laganariae
Garlic
Cotton
Chicken pea
Chinese
cabbage
Bottle gourd
Bottle gourd
Bean
Bean
Bean
Wheat
Pathogen
typea
Main crop
Fusarium oxysporum sb
f. sp. laganariae
Colletotrichum
lindemuthianum
Phoma exigua var.
diversispora
Sclerotinia
sclerotiorum
Gaeumannomyces
graminis var. tritici
Pathogen
Ethiopian
mustard
Sorghum
and moth
Linseed
Wheat
Welsh onion
Chinese
chive
Maize
Maize
Maize
Trefoil
Second crop
25%
Reduced disease
incidence
Reduced
mortality
Reduced disease
incidence
No effect
Reduced disease
incidence
Reduced disease
incidence
Reduced disease
incidence and
severity
Reduced disease
incidence and
severity
Decreased soil
temperature
–
–
Stimulation of
antagonists
Stimulation of
antagonists
Present in mono Release of
crops, absent in glucosinolates
(biofumigation)
mixed crops
65%
18 % disease
incidence in
mixturee
–
60%
73%
(continued)
Zewde et al.
2007
Luthra and
Vasudeva
1940
Agrawal et al.
2002
Toshio 1999
Arie et al.
1987
Arie et al.
1987
Van Rheenen
et al. 1981
1.0 (mono) vs
0.8 (mix)d
- Not mentioned
Van Rheenen
et al. 1981
3.0 (mono)
- Not mentioned
versus 2.6 (mix)d
Lennartsson
1988
Reference
Van Rheenen
et al. 1981
Increased densities
of Pseudomonas
fluorescens
Proposed
mechanism
- Not mentioned
Increased disease 1.8 (mono) vs
2.0 (mix)d
incidence and
severity
Reduced root
infection
Effect
magnitude
relative
Effect in mixture to sole crop
Type
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Row mix crop
Multilines
Nr
26
27
28
29
30
31
Table 5.2 (continued)
Rhizoctonia solani
Ralstonia
solanacearum
Macrophomina
phaseoli
Fusarium udum
Ralstonia
solanacearum
Ralstonia
solanacearum
Pathogen
sb
sb
sb
sb
sb
sb
Sugar beet
Tomato
Sorghum
Pigeon pea
Potato
Potato
Pathogen
typea
Main crop
Reduced wilt
Reduced wilt
incidence
Sugar beet
Reduced crown
and root rot
Chinese chive Reduced wilt
incidence
Allelopathic
reduction of
pathogen
Host dilution
Approx. 60%
No data
Doubling of
host
Delayed
germination
of spores due
to Sorghum
root exudates
(allelopathy)
30%
Halloin and
Johnson 2000
Yu 1999
Singh et al.
1990
Natarajan
et al. 1985
Autrique and
Pots 1987
Spatial
arrangement;
host dilution
3.5 (NS) and
9.7% at low and
high density of
the monocrop
resp.
Reference
Autrique and
Pots 1987
Proposed
mechanism
Spatial
arrangement;
host dilution
2.0 (NS) and
8.2% at low and
high densitiy of
the monocrop,
resp.
Pigeon pea or Increased
100% Increase
cow pea
inoculum density
Sorghum
Haricot beans Reduced wilt
Maize
Second crop
Effect
magnitude
relative
Effect in mixture to sole crop
Type
Multilines
Multilines
Multilines
Multilines
Multistorey
crop
Mixed cropb
Nr
32
33
34
35
36
37
Pseudocercosporella
herpotrichoides
Fusarium spp.
Cephalosporium
gramineum
Wheat mosaic
virus (vectored by
Polymyxa graminis)
Helminthosporium
victoria
Phytophthora sojae
Pathogen
Wheat
sb
Splash
Barley
Palm tree
Wheat
sb
sb
Oats
Soja
sb
sb
Pathogen
typea
Main crop
Oats
Tropical
kudzu
Wheat
Wheat
Oats
Soja
Second crop
Proposed
mechanism
Reduced disease
incidence
10%
Host dilution/
physical barrier
Increased
competition by
non-pathogenic
fusaria
–
No reduction of –
disease incidence
as measured
by presence of
whiteheads
20–40%
Host dilution with
the unsusceptible
host
32%
Reduced virus
disease incidence
symptoms
Increased halflife time of
flax plants in
bioassays
Buffering effect
of resistant plants
(host dilution)
Reduction in
23%
disease incidence
Effect depending Monoculture of Compensation of
resistant cultivar: yield by resistant
on cultivar
5% lower yield or tolerant variety
susceptibility
in multiline
cropping (NS);
monoculture
of susceptible
cultivar: 14%
higher yield
in multiline
cropping
Effect
magnitude
relative
Effect in mixture to sole crop
(continued)
Vilich-Meller
1992a
Abadie et al.
1998
Mundt 2002b
Hariri et al.
2001
Ayanru and
Browning
1977
Wilcox and
St. Martin
1998
Reference
Type
Mixed cropb
Mixed cropb
Mixed cropc
Mixed crop
Row mix crop
Row mix crop
Nr
38
39
40
41
42
43
Table 5.2 (continued)
Bean
Splash
Pepper
Wheat
Wheat
Wheat
Barley
Splash
Splash
Splash
Splash
Pathogen
typea
Main crop
Phytophthora capsici Splash
Pseudomonas
syringae pv.
phaseolicola
Septoria tritici
Pseudocercosporella
herpotrichoides
Pseudocercosporella
herpotrichoides
Pseudocercosporella
herpotrichoides
Pathogen
Wheat
Maize
Clover
Clover
Barley
Wheat
Second crop
Sieving effect
clover
Approx. 50%
Reduced disease
incidence or
severity when
sown in stubble
2.5–43%
Reduction of
inoculum dispersal
Favorable
microclimate in
mixed crop
Physical barrier,
reduction of
inoculum
by increased
decomposition
(active microbial
biomass?)
–
Physical
barrier/host
dilution
Proposed
mechanism
Spore dispersal
50%
–
50%
Increased disease 20–24%
severity
Reduced number
of lesions per
flag leaf
Reduced spore
dispersal
No effect
Reduced disease
incidence
Effect
magnitude
relative
Effect in mixture to sole crop
Ristaino et al.
1997
Mabagala and
Saettler 1992
Bannon and
Cooke 1998
Soleimani
et al. 1996
Vilich 1993
Vilich-Meller
1992a
Reference
Row mix crop
Row mix crop
Multilines
Multilines
Multilines
Multilines
Multilines
Multilines
44
45
46
47
48
49
50
51
Pseudocercosporella
herpotrichoides
Mycosphaerella
graminicola
Mycosphaerella
graminicola
Rhynchosporium
secalis
Pseudocercosporella
herpotrichoides
Rhynchosporium
secalis
Diplocarpon
earlianum
Colletotrichum
acutatum
Pathogen
Splash
Splash
Wheat
Wheat
Wheat
Barley
Splash
Splash
Wheat
Barley
Strawberry
Strawberry
Splash
Splash
Splash
Splash
Pathogen
typea
Main crop
Wheat
Wheat
Wheat
Barley
Wheat
Barley
Grass
Sudan grass
Second crop
b
a
Sb is soilborne, splash is splash-dispersed pathogen
Crops completely widespread sown, at least not sown in rows
c
One crop sown in rows, other crop broadcast sown
d
Disease scores on a scale from 1 (no disease) to 5 (crop completely destroyed)
e
No data from incidence in single crop
Type
Nr
No disease
reduction
Contradictory
results
Reduced disease
severity
Reduced disease
severity
No effect
No effect
Reduced spread
of diplocarpon
spores
Reduced spread
of C. acutatum
spores
–
17%
Up to 50%
depending
on mixture
composition
–
–
Host dilution
Mundt et al.
1995
Cowger and
Mundt 2002
Mundt et al.
1995
Newton et al.
1997
Host dilution,
morphological
factors influencing
dispersal
Host dilution
Saur and
Mille 1997
Abbott et al.
2000
–
–
Reduction of
dispersal
–
–
Ntahimpera
et al. 1998
Reduction of
dispersal
19–49%
Less spores
depending on
rain and crop
density
Newenhouse
and Dana
1989
Reference
Proposed
mechanism
Effect
magnitude
relative
Effect in mixture to sole crop
138
G.A. Hiddink et al.
5.3.1 Host Dilution
In most studies that report a reduction in soilborne diseases or pathogens in
mixed-cropping systems, host dilution is assumed to play a crucial role (Table 5.3).
The magnitude of disease reduction is variable but can be as much as 50%
(Table 5.2). Host dilution is also regarded as the dominant disease-reducing mechanism for airborne pathogens in mixed-cropping systems (Mundt 2002a). The effect
of host dilution will likely be a reduction in disease incidence rather than disease
severity on infected plants (Burdon and Chilvers 1982). Host dilution might have
direct (an effect on the pathogen itself) as well as indirect effects (influencing other
factors than the pathogen) on disease suppression in mixed crops. An increased
inter-host distance reduces the spread of pathogens. In Pythium garden cress experiments, a distance of 6 cm or more prevented disease spread (Burdon and Chilvers
1975). Similarly, spread of Rhizoctonia damping-off in radish–mustard mixtures
decreased with increasing densities of the nonhost mustard plants and spread halted
at host densities below a threshold density (Otten et al. 2005). When the distance
between host plants becomes shorter than the threshold distance, pathogen expansion can become invasive. The threshold distance is affected by the availability of
nutrient resources and interactions with competing microbial communities. These
thresholds can be determined based on the percolation theory developed in physics
(Bailey et al. 2000). Based on this theory Bailey et al. (2000) calculated the probability of invasive spread of Rhizoctonia solani in microcosms with hosts at varying
distances. This, however, is only applicable for pathogens that are able to bridge the
gaps between hosts from a nutrient base.
At increasing densities of susceptible roots, disease spread may accelerate if
secondary root infections occur as can be the case for G. graminis (Bailey and
Gilligan 2000) and R. solani (Otten et al. 2005). Such secondary infections likely
Table 5.3 Disease-reducing mechanisms in mixed-cropping systems for soilborne and splashdispersed pathogens described in the literature
Splash-dispersed
Mechanism
Soilborne pathogens
pathogens
Total
Host dilution
12
5
17
Allelopathy (including biofumigation)
4
0
4
Antagonists
5
0
5
Inoculum reduction
2
0
2
Unfavorable microclimate
1
1a
1
Compensation (yield)
1
0
1
Physical barrier
0
5
5
Not mentioned
5
0
5
Total positive effects
Negative or no effects
30
6
10
5
40
11
Total
36
15
51
Both physical barrier and unfavorable microclimate are mentioned for disease suppression, in
totals therefore only taken up once (as physical barrier)
a
5
Mixed Cropping and Suppression of Soilborne Diseases
139
occur at a lower rate because of larger inter-root distances in mixed-crop systems.
For pathogens with a wide host range such as R. solani, slightly or moderately
susceptible plants may also serve as nutrient source without expressing striking
disease symptoms (Otten et al. 2005), thus reducing the host dilution effect. The
intensity of root intermingling in mixed cropping may be an important determinant
for the interference processes (Kroon 2007) and the level of disease suppression
may therefore be determined by the crops or cultivars grown and their root architectures. In contrast to pathogens capable of bridging the gaps between host plants
by transporting nutrients from a substrate base, host dilution has hardly an effect on
pathogens without this capacity, such as powdery scab (Spongospora subterranea),
Verticillium wilt, and clubroot (Plasmodiophora brassicae).
For splash-dispersed pathogens in mixed cropping, the host dilution effect is
comparable to that of airborne pathogens, influencing disease incidence more than
disease severity. The non-host crop simply acts as a physical barrier, thus reducing
disease spread as has been shown for Pseudocercosporella herpotrichoides, the
causal agent of eyespot in cereals (Villich-Meller 1992). The barrier function can
reduce the impact of raindrops thus reducing dispersal, and it can intercept splashing spores that would reach a host plant under conditions of monoculture
(Ntahimpera et al. 1998; Soleimani et al. 1996).
5.3.2 Allelopathy
Allelopathy is defined as any biochemical interaction among plants, including those
mediated by microorganisms, resulting in either detrimental or beneficial effects on
the interacting plants (Wu et al. 2001). In four studies, allelopathy was suggested
to play a role in disease suppression in mixed cropping (Table 5.2). When watermelon was intercropped with rice, allelopathic substances from rice roots reduced
production and germination of conidia of Fusarium oxysporum f. sp. melonis, leading
to a 67% reduction in wilt (Ren et al. 2007). The allelopathic exudates only reduced
Fusarium conidial density in the rhizosphere and not in bulk soil indicating a
limited diffusion. Delayed germination of spores of F. udum, causing wilt in pigeon
pea, has been attributed to allelopathic substances exuded from sorghum roots
(Natarajan et al. 1985). To be effective in inhibiting rhizosphere-inhabiting pathogens,
allelopathic substances should be present at sufficiently high concentrations in the
micro sites where the pathogen is located, and roots of mixed crops should be in
close proximity.
An interesting question is whether allelopathy causes death of the pathogen
propagules (Ren et al. 2007) or only delays germination (Natarajan et al. 1985). In
the latter case, the effect would resemble fungistasis, which is the general phenomenon
of restriction of germination and growth of fungal propagules in soil (Lockwood
1977). A high level of soil fungistasis is often assumed to be accompanied by a high
level of general disease suppression (Hornby 1983; Janvier et al. 2007; Lockwood
1977). Fungistasis can however also be regarded as a mechanism of delayed
140
G.A. Hiddink et al.
activity if conditions are unfavorable for the pathogen, which is also the case if
non-lethal allelopathic substances are formed temporarily. The effect can be detrimental, but beneficial to the pathogen as germination in absence of a host plant is,
generally, not a desirable trait for pathogens. Roots of non-hosts can sometimes
stimulate the germination of the survival propagules of the pathogen (Mol and van
Riessen 1995) leading to a decline in the inoculum density. In relay mixed crops,
this premature germination might have a disease-suppressive effect, especially in
combination with inoculum burial and enhanced microbial antagonism.
Biofumigation has been proposed as a mechanism to suppress soilborne pathogens when Brassica species are used in mixed-cropping systems (HauggaardNielsen and Jensen 2005; Kirkegaard and Sarwar 1998). However, with the
exception of the work by Zewde et al. (2007), convincing field data are not yet
available. This is in contrast with studies on the biofumigation potential of Brassica
crop residues (Kirkegaard and Sarwar 1998, Smolinska et al. 2003), which showed
disease suppression for various soilborne pathogens especially in controlled greenhouse experiments.
5.3.3 Microbial Antagonists
In five of the cropping systems listed in Table 5.2, enhanced antagonistic populations
were proposed as a main mechanism for disease reduction in mixed-cropping
systems. In three cases, pseudomonads and probably antibiotics were involved. For
example, wheat root infection by G. graminis var. tritici was reduced by 25% in
wheat-trefoil (Medicago lupulina) mixes (Lennartsson 1988). Maximum reduction
(73%) in fusarium wilt was reached when bottle gourd was mixed with Chinese chive
because of stimulation of Pseudomonas gladioli populations on the Chinese
chive roots (Arie et al. 1987). Also, increased occupation of available niches by
non-pathogenic Fusaria was held responsible for increased disease suppression in
oil-palm–legume mixed cropping (Abadie et al. 1998). The build up of populations
of antagonistic microorganisms has been studied mostly in single-crop systems. It
seems that the natural build up of antagonists to levels where they are effective
takes place mostly as a result of selection or coevolution, i.e., continuous cultivation
of the same single crop in the presence of the pathogen (Schneider 1982; Weller
et al. 2002). Nevertheless, also in these agro-ecosystems the fate of the same, but
introduced antagonistic microorganisms is often inconsistent (Whipps 2001).
Rhizosphere microbial communities, including pathogens, antagonists, and
plant-growth-promoting bacteria are crop- and cultivar-specific (Germida and
Siciliano 2001; Smith et al. 1999) and it might be worthwhile to investigate if these
communities can be manipulated by the choice of cultivars in a mixed-crop setting.
Crop- or cultivar-specific resistance against races of pathogens is widely known and
often applied in mixed crops (Mundt 2002a). Mazzola and Gu (2002) used wheat
to stimulate the natural antagonistic populations of fluorescent pseudomonads,
which led to control of apple replant disease. The rhizospheres of old wheat cultivars
5
Mixed Cropping and Suppression of Soilborne Diseases
141
were less aggressively colonized by fluorescent pseudomonads than those of modern ones (Germida and Siciliano 2001). Among tomato lines, genetic differences
correlated with Pythium suppression by Bacillus cereus and growth of this biocontrol agent on seeds (Smith et al. 1999). Also legumes may stimulate and support
antagonistic Rhizobium bacteria in the rhizosphere (Dakora 2003; Simpfendorfer
et al. 1999), which might result in increased pathogen suppression in mixed
crops. When growing white clover together with triticale, take-all disease was
reduced (Hiddink et al. 2004; Hiddink 2008), although the exact disease-suppressive mechanism remains elusive.
In mixed crops, increased plant diversity leads to more diverse root exudates and
consequently to a more diverse rhizosphere-inhabiting microbial community
(Kowalchuk et al. 2002; Westover et al. 1997). Rhizospheres of mixed crops support different bacterial and fungal microbial communities compared to the corresponding single-crop rhizospheres (Hiddink et al. 2004; Song et al. 2007). On the
other hand, the effect of mixed cropping on the bulk soil microbial community has
not been shown (Hiddink et al. 2005a; Kowalchuk et al. 2002). In a more biodiverse
setting, the likelihood to encounter microorganisms with antagonistic properties is
higher, but at the same time their densities are expected to be lower under these
conditions. However, if a higher biodiversity would mean a higher diversity in functions, a higher rate of consumption of root exudates could be expected, which
relates to the root camouflage concept proposed by Gilbert et al. (1994). Although
increased microbiological diversity is often referred to as an important indicator for
soil health (Doran and Zeiss 2000; Mäder et al. 2002; Van Elsas et al. 2002), with
respect to disease suppression, its effects can be both positive (more consumption
of root exudates, more antagonists) and negative (potentially effective antagonists
suffer more from competition and fail to establish and be active).
For bulk soil, an increased bacteria diversity is sometimes related to increased
disease suppression. Hiddink et al. (2005a) reported that higher diversity indices for
bulk soil bacteria were correlated with a lower disease severity. Suppression of
corky root of tomato, caused by Pyrenochaeta lycopersici, was related to a more
diverse actinomycete community in bulk soil (Workneh and van Bruggen 1994).
Although mixed cropping could increase rhizosphere microbial diversity at intensive intermingling of different roots, the effect on bulk soil biodiversity seems
limited (Hiddink et al. 2005a).
Discussing the effect of microbial diversity on disease suppression is complicated since proper methods to quantify diversity are still under development.
Cultivation-based approaches do not take into account the non-culturable species,
whereas cultivation-independent approaches such as analysis by Denaturing
Gradient Gel Electrophoresis (DGGE) underestimate the microbial diversity in soil
as only the most abundant species (approximately 0.1–1% of the microorganisms
present) are detected (Muyzer et al. 1993). One may assume, however, that the
abundant species will also harbor species that contribute to competition for nutrients
and space. Another challenge is linking microbial diversity to ecological function
(Hiddink et al. 2005a; Nannipieri et al. 2003). The degree of functional redundancy
(with respect to disease suppression) could perhaps be regarded as a reliable
142
G.A. Hiddink et al.
measure for disease suppression, but how this redundancy could be measured is as
yet unclear (Giller et al. 1997; Nannipieri et al. 2003). This could explain why a
high biodiversity can be considered a desirable trait, but until indicators quantifying
functional redundancy have developed this topic will remain largely speculative.
There clearly is a contradiction between desiring a high functional diversity on
the one hand and a high establishment of a given antagonist on the other hand. In soils
with a high microbial diversity, a low conduciveness for establishment and growth
of an introduced antagonist or pathogen is to be expected. If disease suppression
would be controlled by a single antagonist, a high microbial diversity would then
be an undesirable trait of soils. This is in line with the observation that establishment of pseudomonads in organic soils (which showed a higher microbial diversity)
is more limited than in conventional soils (Hiddink et al. 2005b).
5.3.4 Microclimate
Mixed cropping generally changes the microclimate. Higher soil coverage leads to
lower soil temperatures which have been associated with lower disease incidence
of Macrophomina phaseolina and Rhizoctonia solani in cotton–sorghum mixtures
(Luthra and Vasudeva 1940). The lower level of disease severity of the splash-dispersed
Pseudocercosporella herpotrichoides in wheat–clover systems was attributed to a
higher decomposition rate of organic material that serves as a base for survival of
the pathogen spores (Soleimani et al. 1996). However, increased moisture content
in the mixed crop could have increased soilborne pathogens such as Pythium spp.,
which can survive and disperse more easily in moist soils. Likewise, airborne
diseases such as halo blight caused by Pseudomonas syringae pv. phaseolicola
could be more severe in mixed bean/maize than in a single bean crop (Mabagala
and Saettler 1992).
5.3.5 Induced Systemic Resistance (ISR) and Systemic Acquired
Resistance (SAR)
Mixed cropping can bring about ISR (induced by non-pathogenic microorganisms)
or SAR (stress inducers like water stress, salinity, allelopathic substances, or pathogens)
if one crop creates the right condition for ISR/SAR inducers for which the alternate
crop is sensitive (Hamerschmidt et al. 2001). Both ISR and SAR can be interpreted
as a form of increased generalized resistance in response to an external stress
(Agrios 1997). The response starts from a localized point and can spread throughout the whole plant as a result of signal transduction. Induced resistance could be
due to direct effects of stress-inducing root exudates or indirect effects via
root-exudate-affected microbial populations (Kloepper et al. 1992). ISR has been
mentioned as a mechanism for reduction of several airborne pathogens such as
5
Mixed Cropping and Suppression of Soilborne Diseases
143
powdery mildew in barley cultivar mixtures (Chin and Wolfe 1984). However,
neither ISR nor SAR have been suggested to play a role in suppression of soilborne
pathogens in mixed crops (Table 5.2), probably because of difficulties to prove this
experimentally.
5.3.6 Nutrients and Disease Development
Nutrients can affect disease development above and belowground (Walters and
Bingham 2007). In mixed crops, uptake of nitrogen from undersown clover reduced
take-all disease severity in barley (Garrett and Mann 1948). Not only the amount
but also the form of nitrogen is important. Exudation of ammonium from clover
roots (Paynel and Cliquet 2003) may lead to a reduction in the rhizosphere pH in
cereal roots, thereby influencing the antagonistic microbial population and decreasing infection by G. graminis (Sarniquet et al. 1992; Smiley 1978). Also, availability
of several other elements such as potassium, phosphorus, sulfur, and silicon will
influence disease development directly or indirectly (e.g., Walters and Bingham
2007) in mixed crops but are not further discussed in this review.
5.4 Similarities and Differences Between Disease-Suppressive
Mechanisms in the Different Cropping Systems
All three cropping systems, continuous monocropping, crop rotation, and mixed
cropping, can contribute to the management of certain soilborne pathogens. Crop
rotation is the most commonly applied method to manage soilborne pathogens.
However, while rotation schemes can reduce specific soilborne pathogens, for
several other, more generalist pathogens, crop rotation is not necessarily a proper
solution. Also, wide crop rotations can be undesirable from an economic point of
view. Continuous cultivation of the same crop can result in a persistent decline of a
pathogen, as is the case for take-all disease of cereal crops. Continuous cultivation
of the same crop has not been “invented” as a management tool for soilborne pathogens
perse, but induction of disease suppression is a complementary benefit in situations
where no options other than continuous cultivation of single crops are available.
This specific suppression usually is only active against a single pathogen leaving
opportunities for other soilborne pathogens to develop and cause disease. Mixed
cropping has been practiced for ages in all sorts of combinations, although not
specifically designed for suppression of soilborne pathogens, but rather as an insurance
against crop failures and soil erosion.
In all three types of cropping systems, multiple disease-reducing mechanisms
are active, but mixed cropping offers the most diverse form of disease suppression
because root systems of different crop species interact. In mixed cropping systems,
144
G.A. Hiddink et al.
the most important disease-reducing mechanism appears to be host dilution.
The magnitude of this effect depends on the planting density, the type of mixed cropping,
and root architecture of the crops grown. Competition will affect the distribution of
roots in mixed crops (de Kroon 2007; reviewed by Hauggaard-Nielsen and Jensen
2005). Allelopathic effects, nutrient concentrations, and water flow will determine
how the roots interact and the diversity of (microbial) interactions in the rhizosphere
(Bowen and Rovira 1976). Furthermore, as long as host species are mix-cropped
with non-hosts in lower densities, host dilution will inevitably lead to a reduction
in the number of diseased plants per area.
Other factors that result in disease suppression, such as allelopathy and antagonism
induced by the non-host crop, depend on characteristics of all crops present in the
mix. Biofumigation using Brassica species in mixed cultivation has received attention
recently, but its effectiveness is still limited (Hiddink et al. 2005a). Breeding for
Brassica species exhibiting higher glucosinolate contents is an option to increase
their effectiveness (Matthiessen and Kirkegaard 2006). More effective suppression
can be expected from legumes, which can excrete allelopathic root exudates and
support potentially antagonistic microorganisms, besides fixing nitrogen (Dakora
2003). Also the use of specific crops and cultivars that support antagonistic microorganisms (Mazzola and Gu 2002; Smith et al. 1999) can be a valuable tool to
create mixtures that actively suppress soilborne pathogens.
5.5 Practical Feasibility of Mixed Cropping
Although it is clear that mixed cropping can reduce soilborne diseases, it also has
an inherent weakness: the presence of multiple crop species may bring about a
greater variety of soilborne pathogens albeit likely at lower densities for each of the
crops. An important question is whether and how mixed crops should be rotated
and what the choice of rotation crops in time should be. When rotated, mixtures of
wheat or barley containing oats resulted in lower disease levels in the crops the following year than mixtures of barley and wheat (Vilich 1993). An additional question that should be addressed is: Does mixed cropping of two crops continuously
for two (or more) years lead to less disease than growing those same two crops in
rotation? It is surprising that, to the best of our knowledge, no answer to this question is available in the literature. The answer to this question can be complex, as
was shown by Hiddink (2008). In this study, take-all disease was lower during
three consecutive years in a triticale–white clover field compared to single-cropping triticale. However, in the fourth year, Fusarium infected white clover and
reduced its stand, which in turn caused an increase in take-all in triticale in the
mixture to a disease level above that obtained in the single-cropped triticale.
Soilborne pathogens with broad host ranges or long-term survival structures are
likely to be less suppressed in mixed crops grown repeatedly. If pathogens like
Fusarium in clover (Hiddink 2008) are not actively suppressed by the co-occurring
crop, inoculum will continue to build up and rotating the crops in the mixture would
have been a better tool to suppress the pathogens. To manage mixed crops for the
5
Mixed Cropping and Suppression of Soilborne Diseases
145
suppression of soilborne diseases requires advanced skills of the farmer and knowledge of the pathogens that might cause diseases in both mixed-crop components. It
can be more labor-intensive and not suitable for mechanized production of all
crops. Certain crops are not suitable to grow in mixed crops because of their weak
competiveness. The degree of intercrop competition is decisive whether a certain
combination can be grown. Thus, although club root, caused by Plasmodiophora
brassicae, was reduced in a barley–Brussels sprouts mixed crop, yield of Brussels
sprouts was reduced by nearly 50% because of competition by barley (Hiddink
2008). However, often an overall yield increase is observed in mixed crops. This
effect is generally expressed as the Land Equivalent Ratio (LER) (Vandermeer
1990). The LER is the sum of the yields of both components per unit of land area
combined divided by the area of land needed to obtain the same yields when both
components are grown as single crops (Vandermeer 1990). Mixed crops have been
grown for ages, because of their yield stability and mixed cropping is still practiced
for this reason in tropical regions (Vandermeer 1990). Co-occurring crops compensate for failure of one of the crops due to soil and airborne pathogens, weeds, temperature-, and water stress (Vandermeer 1990). This kind of growth compensation
is an important reason for mixed cropping.
Overall, we conclude that it is interesting to consider mixed cropping where
land-use efficiency and yield assurance are important reasons for practicing mixed
cropping. However, application of mixed crops as tools for soilborne pathogen
management is still in its infancy and not yet reliable enough.
5.6 Conclusion
In spite of the frequently observed disease or pathogen suppression (40 out of 51
observations) in mixed cropping, this system will not be a panacea for combating
soilborne plant pathogens. However, in some cases it can contribute substantially to
the management of soilborne pathogens. Design of mixed-cropping systems as a tool
for suppressing plant pathogens is still in its infancy compared to continuous monocropping and crop rotation. The available literature is limited and scattered. In this
literature review we showed that the most frequently observed disease-suppressive
mechanism is host dilution (17 times for soilborne and splash-dispersed pathogens
combined). Likely, however, multiple factors affect the extent of disease suppression.
We think that much can be done to optimize the disease-suppressive effects based on
allelopathy and antagonism. Although we focused on effects of mixed cropping on
soilborne pathogens, other benefits should also be considered when evaluating mixed
cropping. Reduction in plant pests and weeds has been reported widely (Baumann
et al. 2001; Bukovinszky 2004). Reduced growth of one crop results in lower competition and can increase the production of the accompanying crop and thus increase
overall yield stability per unit of area. This could be especially useful when no direct
control measures such as pesticides are available. Another important benefit of mixed
cropping is the higher potential yield per unit of area of cultivated land. This would
reduce the plant production acreage needed to produce a certain amount thus using
146
G.A. Hiddink et al.
the available production factors more efficiently and reducing nutrient leaching, water
runoff, and soil erosion per unit of yield. More production per area of land also means
that competing claims for land needed for the production of human food and animal
feed and for the production of bio-fuels can be relieved to some extent if they can be
grown on the same area of land at the same time.
Acknowledgments We thank Dr. J.M. Raaijmakers for his valuable comments and suggestions
after reviewing this manuscript. This work was part of the project “Enhanced Biodiversity” funded
by the section Earth and Life Sciences of the Dutch Scientific Organization (NWO-ALW, project
number 014.22.032).
References
Agrios GN (1997) Plant pathology. Academic, London, UK, pp. 635
Arie T, Namba S, Yamashita S, Doi Y, Kijima T (1987) Pseudomonas gladioli (Japanes title).
Annu Rev Phytopathol Soc Jpn 53:531–539
Bailey DJ, Otten W, Gilligan CA (2000) Saprotrophic invasion by the soil-borne fungal plant
pathogen Rhizoctonia solani and percolation thresholds. New Phytol 146:535–544. http://
www.jstor.org/stable/2588935
Garrett KA, Cox CM (2006) Applied biodiversity science: managing emerging diseases in agriculture and linked natural systems using ecological principles. In: Ostfeld R, Keesing F, Eviner V
(eds) Infectious disease ecology: the effects of ecosystems on disease and of disease on ecosystems. Princeton University Press, Princeton, NJ, pp 368–386
Geno L and Geno B (2001) Polyculture production – principles, benefits and risks of multiple
cropping land management systems for Australia, pp 105. Publication No. 01/34, Rural
Industries Research and Development Corporation (RIRDC), Kingston, ACT
Gu Y-H, Mazzola M (2003) Modification of fluorescent pseudomonad community and control of
apple replant disease induced in a wheat cultivar-specific manner. Appl Soil Ecol 24:57–72.
doi: 10.1016/S0929-1393(03)00066-0
Hiddink GA, Termorshuizen AJ, Raaijmakers JM, van Bruggen AHC (2004) Effect of mixed
cropping on rhizosphere microbial communities and plant health. In: Book of abstracts international congress rhizosphere 2004, Munich, Germany, 12–17 Sept 2004
Lennartsson M (1988) Effects of organic soil amendments and mixed species cropping on take-all
disease of wheat. In: Allen P, van Dusen D (eds) Global perspectives on agroecology and sustainable agricultural systems: proceedings of the sixth International scientific conference of the
international federation of organic agriculture movements, Santa Cruz, August 18–20, 1986, pp
575–580
Trenbath BR (1976) Plant interactions in mixed crop communities. In: Papendick RI, Sanchez PA,
Triplett GB (eds) Multiple cropping. ASA Special Publication No. 27, ASA, SSSA, CSSA,
Madison, WI, pp 129–169
Vandermeer JH (1990) Intercropping. In: Carrol CR, Vandermeer JH, Rosset P (eds) Agroecology.
Mcgraw Hill, New York, pp 481–516
Van Rheenen HA, Hasselbach OE, Muigai SGS (1981) The effect of growing beans together with
maize on the incidence of bean diseases and pests. Neth J P1ant Pathol 87:193–199
Weaver JE (1926) Root development of field crops. McGraw-Hill, New York. http://www.
soilandhealth.org. Accessed on 2010
Wu H, Pratley J, Lemerle D, Haig T (2001) Allelopathy in wheat (Triticum aestivum). Ann Appl
Biol 139:1–9
Zewde T, Fininsa C, Sakhuja PK, Ahmed S (2007) Association of white rot (Sclerotium cepivorum) of garlic with environmental factors and cultural practices in the North Shewa highlands
of Ethiopia. Crop Protection 26:1566–1573. doi: 10.1016/j.cropro.2007.01.007
Chapter 6
Decreasing Nitrate Leaching in Vegetable Crops
with Better N Management
F. Agostini, F. Tei, M. Silgram, M. Farneselli, P. Benincasa, and M.F. Aller
Abstract The relatively low cost of fertiliser and the increasing demand and
competition for cheap food have encouraged the over-fertilisation of field
vegetables over the past few decades. However, more recent scientific and public
concern over eutrophication of water and the accumulation of nitrates in vegetables for human consumption requires a more effective use of nitrogen fertilisers
in a more sustainable manner, which minimises the potential risk of negative
effects on the environment and human health. In this review, we present the current state of the art in knowledge of N dynamic in vegetable crops and the latest
advances in nutrient management, which could be used to mitigate nitrate losses
from vegetables fields to the wider environment. Findings are based on published
data and personal communications with researchers and consultants across
Europe. Areas of research where further work is required are identified and
described. A conclusive chapter reports on the economic and environmental
impact of technology transfer of improved nitrogen management in three south
European states and in the Netherlands.
Keywords Vegetable crops • nitrate leaching • nutrient management • soil and
water pollution • Decision Support System • Integrated Crop Management • soil N
• chlorophyll meter • fertigation • slow release fertiliser • nitrification inhibitor
• intercropping • mulch • cover crop
F. Agostini (*)
Department of Energy and Technology, SLU, Uppsala Ulls Väg 30A 756 51, Sweden
e-mail: Francesco.agostini@et.slu.se
F. Tei, M. Farneselli, and P. Benincasa
Department of Agricultural and Environmental Sciences, University of Perugia, Borgo XX
giugno 74, 06121 Perugia, Italy
M. Silgram and M.F. Aller
ADAS UK Ltd., Wergs Road Wolverhampton, WV6 8TQ, UK
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_6, © Springer Science+Business Media B.V. 2010
147
148
F. Agostini et al.
6.1 Introduction
Nitrogen fertilisation is a conventional practice in the management of field vegetables
to ensure a good yield and quality of the marketable product (Bianco 1990).
However, the amount of nitrogen fertiliser applied may often exceed the actual crop
demand, taking account of other sources of plant-available nitrogen such as the soil,
decomposing residues, and applied manures and slurries. This occurs because
fertiliser costs are relatively modest compared to the price of the crop product, and
the negative environmental effects of supra-optimal application rates of nitrogen
fertiliser are often not immediately obvious. In recent years, there has been scientific
and public concern about the relationship between land management practices and
the enrichment of freshwaters and groundwater (Greenwood 1990; Meinardi
et al. 1995; European Commission 1998, 1999; Neeteson and Carton 2001; Tilman
et al. 2001; Ramos et al. 2002) and nitrate accumulation in edible portions of
vegetables (Maynard et al. 1976).
In order to protect the environment and human health (Cantor 1997; Barret et al.
1998), several organisations have set NO3–N concentration limits for drinkable
water: the World Health Organization and the European Union impose limits of
11.3 mg NO3–N L−1, which is equivalent to 50 mg NO3 L−1 (European Commission
1998), while the US Environmental Protection Agency (1989) and Health Canada
(Health Canada 1996) set the limit at 10 mg NO3–N L−1 (equivalent to 43 mg NO3
L−1). Moreover, the European Commission has promulgated several directives
(CEC 1991; European Commission 1998, 1999) concerning the protection of
waters against pollution caused by nitrates from agricultural sources, in order to respect
the above-mentioned limits and minimise the risk of excess nutrient loss to rivers
promoting eutrophic status in freshwater and coastal environments. As an overall
consequence, ecologically sound fertilisation strategies for field vegetable production
(Greenwood 1990; Greenwood and Neeteson 1992; Hochmuth 1992; Neeteson
1995; Rahn 2002; Hartz 2003; Remie et al. 2003; Bertschinger 2004) can allow a
significant reduction in both environmental and health risks associated with
vegetable production.
The nitrogen (N) fertiliser consumption in the world in 2005–2006 was
estimated about 98 Mt, of which 15% was used to support the growing of fruit and
vegetables (Heffer 2008). In the EU-15 states, N fertiliser consumption in fruit
and vegetables was about 720,000 t (Heffer 2008), and in field vegetables, it was
only nearly 0.3 million tonnes (FAO 2000). Typically, the potential nitrate-leaching
losses from land growing vegetable crops exceed that from arable cropped soils
(Goulding 2000), as a result of the combination of the short crop growth cycle,
relatively high N fertiliser requirements, the high water requirements by vegetable
crops, which are often partly provided via irrigation (Greenwood et al. 1989), and
the nitrogenous nature of vegetable crop residues (e.g. peas), which can mineralise
rapidly and lead to increased nitrate leaching in the months following harvest
(e.g. Silgram 2005). In addition, lighter sandy textured soils, which are more prone to
leaching losses, represent often some of the main production areas of vegetable
crops in several European countries.
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
149
Land management practices can affect the N fate and the availability of potentially
leachable NO3–N (Li et al. 2007), since there is a direct relationship between large
NO3–N losses and inefficient fertilisation and irrigation management. The nitrate
not captured by plant roots can move in drainage waters promoted by rainfall and/
or irrigation because nitrate has a weak negative charge and is not strongly adsorbed
to soil particles. The downward movement of NO3 through the soil profile occurs
when significant irrigation water is applied, or under European conditions primarily
in autumn and spring when precipitation exceeds evapotranspiration and the soil is
at field capacity (Belanger et al. 2003; Kraft and Stites 2003).
In most agricultural areas, drainage represents the main cause of off-site transport
of NO3–N (Randall and Goss 2001). In some regions, irrigation or intense precipitation events on sloping landscapes can represent the main mechanism of NO3–N loss
in surface run-off to water bodies, especially for soils with low permeability
(Bjorneberg et al. 2002). In particular, in Mediterranean countries, the relatively dry
growing season during spring and summer creates a relatively low risk of drainage
(and hence nitrate leaching) from vegetables. However, the relatively high amount
of mineral nitrogen left in soil and/or residues after the harvest of some crops, such
as sweet peppers, tomatoes and lettuce, coupled with intense rainfall in the autumn–
winter period, which can far exceed the soil infiltration rate, can present a high risk
of nitrate losses to groundwaters (Tei et al. 1999).
Moreover, with excessive or poorly timed irrigation, readily available N sources
such as ammonium nitrate will be readily leached and present a potential hazard for
the environment as the ammonium is rapidly nitrified, and the drainage and/or
run-off caused by the intense irrigation application will promote NO3–N loss. Some
ammonium and organic-N compounds do also leach from agricultural soils, but in
intensively managed systems, their contribution to total loss is typically relatively
small (except where livestock manures or slurries have been applied).
Leaching losses can be extremely variable depending on the intensity and
distribution of rainfall, on the amount and location of soil and fertiliser N in the
profile, on soil physical properties that influence the efficiency with which N is
displaced in the percolating water and on plant root distribution. In general, there
is a positive relationship between fertiliser N applied and nitrate-leaching losses,
given sufficient drainage volume (Fig. 6.1). There is also strong evidence that
encouraging farmers to reduce fertiliser N inputs can reduce losses of nitrate, leaving
the soil root zone – although due to the transit time of percolating water, it can take
many years before this impact may be detected in reduced nitrate concentrations in
groundwaters (e.g. Silgram et al. 2004).
At the same time, the irrigation management also influences the amount of
nitrate leached and taken up by the crops (Karaman et al. 2005) because of the
effects on the width and depth of root distribution in soils. Indeed, leaching of
nitrate–N from the root zone depends on the drainage of water out of this zone
(Knox and Moody 1991, Zhang et al. 2005; Li et al. 2007) and water-use efficiency
(Shaffer and Delgado 2002; Delgado et al. 2006).
Not only do nitrogen losses from agriculture relate to nitrate leaching but they
also include gaseous losses as nitrous oxide and ammonia, which are both pollutants
150
F. Agostini et al.
Dry matter yield
N loss kg/ha
80
9
8
7
6
60
5
Nitrate leaching
40
4
3
2
20
1
Premium scheme
0
0
100
200
Dry matter (t/ha)
100
0
300
400
Fertilizer N applied, kg/ha
Fig. 6.1 Example of N losses by leaching and yield as dry matter versus amount of applied N
fertilised to grass (Modified from Lord et al. 1999)
linked to climate change and acidification (Neeteson and Carton 2001). Therefore,
a holistic approach that broadens concerns over nitrate leaching to include the management of nitrogen in the soil–plant system (accounting for N in crop residues
and biomass) must also take into consideration the extent of the impact of gaseous
losses related to agricultural practices. If practices lead to increased gaseous N emissions by buffering against nitrate losses from fields to water bodies, the environmental pollution risk has only been shifted from one point of impact or ‘receptor’
(water) to another (air). Recent studies on fertiliser management have highlighted
the danger of this so-called pollution-swapping between nitrate leaching and ammonia
loss in fruit production as a function of the type of nitrogen fertilisers and the
application schedule (Cantarella et al. 2003, Stevens and Quinton 2009).
So in order to achieve more sustainable nitrogen management, the research
activity should be focused on determining the most effective N-fertilisation systems
by investigating the whole dynamic of N in the soil, plant, water and atmosphere.
The aim of this review is to present some of the current advances in nutrient
management applied to vegetable production, to highlight the effective application
of such methods within the EU as tools to reduce nitrate leaching and to identify
areas of research and technology transfer where further work is required.
6.2 Fertiliser Management in Vegetable Crops
Efficient fertiliser management requires adequate tools such as an integrated
approach to plant nutrition, while further work is needed to optimise the use of
high-tech irrigation–fertilization systems (Battilani et al. 2003). The main consideration, which must be kept in mind in planning measures to limit nitrate leaching,
is that only a small proportion of the nitrogen applied to land is actually utilised by
plants, in the cases about 40–45% and an even smaller proportion is contained in
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
151
the commercially harvested material (Davies 2000). Sound N-fertiliser management, which is necessary to avoid excessive nitrate concentrations both in vegetables and in drainage (and hence drinking) water, requires the farmer to judge the
balance between processes that contribute nitrogen to the soil for crop uptake and
growth (inputs) and processes that remove mineral nitrogen from the plant root
zone (outputs). Since nitrogen in the soil is in a continuous state of flux between
organic and mineral pools, these pools, fluxes and losses need to be considered
across the whole crop-management cycle. Once all the elements in the N balance
have been assessed, the optimum N rate can be evaluated as a result of the difference between inputs and outputs that occur for a specific crop, location, soil and
climate situation. Proper N management also requires careful management of other
technical aspects, such as the timing and method of application and the choice of
the fertiliser to apply (slow or fast release).
However, studies carried out on the impact of good practices in the USA suggest
that only a minority of growers may follow fertiliser-management programmes, and
empirical criteria are still often preferred by farmers over objective-monitoring
methods (Hartz 2003). It is well known that the ‘general’ assessment of nitrogen in
the soil–water–plant–air system is not an issue, but the extreme variability due to
local conditions makes its practical management a demanding challenge in agriculture (Owen et al. 2003). Some countries, i.e. UK farming press and magazines
(http://www.fwi.co.uk; http://www.farmersguardian.com) produced recommendations to the industry adjusted every spring based on that specific winter’s data on
soil mineral nitrogen (SMN) levels and over-winter drainage volumes.
6.2.1 N Balance
Burns (2006) defined that the amount of N taken up by a crop (UN) is equal to the
sum of that recovered from the fertiliser (UF) and from the soil (US) as in the following equation:
UN = UF + US + fF • NF + fS • NS
(6.1)
where NF and NS are the amounts of N available to the crop from fertiliser and soil,
respectively and fF and fS are the corresponding average recovery factors for the two
types of N supply. Since the amount of N from natural source is not often sufficient
to meet crops needs, the remainder must be applied as fertiliser. Burns (2006) also
defined the optimum rate of N fertiliser as the minimum amount needed to achieve
the required response. At the plant’s optimum N-fertiliser rate (NFopt), UN becomes
equivalent to the total N demand of the crop (TN), so
TN = fF • NFopt + fS • NS
where NFopt is also referred to as the N-fertiliser requirement of the crop.
(6.2)
152
F. Agostini et al.
A detailed N balance should take into account many inputs (mineral soil N available
at planting, N from the mineralisation of crop residues and indigenous soil organic
matter, irrigation and precipitation, and fertilisation) and outputs (N plant uptake,
N immobilisation, denitrification, volatilisation and leaching). Since N is vulnerable
to a complex variety of processes brought about by the mediating effects of weather
on soil microbes, changing physical and chemical soil properties, cultural practices
and the effect of preceding crops, the optimum N-fertiliser rate often varies quite
considerably from site to site and from year to year (Goodlass et al. 1997). As a
consequence, the reliability of N-fertiliser recommendations depends on the accuracy
in the estimation of the inputs and outputs of the N balance. In some situations, this
has been assisted by sampling soil cores to 90 cm depth and analysing for soil
mineral nitrogen levels within the soil in autumn or spring to guide cost-effective
fertiliser recommendation strategies (Burns 2006).
However, the evaluation of the optimal N rate is peculiar in vegetables because not
only the yield but also other aspects such as fruit size and quality must be considered
in the crop nutrient requirement concept (Olson and Simonne 2006). In fact, the concept of economic optimum yields is particularly important for vegetables because a
certain amount of nutrients might produce a moderate amount of biomass, but produce negligible marketable product because of small fruit size. Farmers really need
to consider the economic optimum fertiliser rate, which will be lower than the plants’
optimum rate and depends on the relationship between fertiliser prices and yield
price. Burns (2006) pointed out that the commonest methods to measure N requirements are based on maximising marketable or economic yields, but the former has
the advantage to be independent of the price of the produce, which can vary.
Furthermore, as the value of most vegetable crops far outweighs the cost of fertiliser,
there is usually little difference between the two optima.
For all these reasons, in order to improve N management in a sustainable agricultural scenario, an accurate analysis of all the parameters of N balance must be done.
6.2.1.1 Total Crop N Demand
Total N demand is defined as the minimum amount of N a crop must accumulate in
its tissues for optimum growth. Total crop N demand depends mainly on its total
biomass since the relationship between the critical N concentration, i.e. the minimum
N concentration required for maximum plant growth, %Nc (as defined by Greenwood
et al. 1990) and the above-ground plant dry weight (DW, t ha−1) is similar within C3
species1 (Greenwood et al. 1990; Lemaire and Gastal 1997). Nevertheless, every
species has its own N-dilution curve according to its own histological, morphological
and ecophysiological characteristics, so species-specific critical N-dilution curves
have been determined, for example, for potato (Greenwood et al. 1990), cabbage
(Riley and Guttormsen 1999), processing tomato (Tei et al. 2002) and lettuce
1
(%Nc = 4.8 DW−0.34 as an average relationship for C3 species) and C4 (%Nc = 3.6 DW−0.34)
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
153
(Tei et al. 2003). Information on total crop N demand are often summarised and
generalised in look-up tables based on past reliable agronomic experiments, for
practical use of the farmers and technicians (see e.g. MAFF 2000). Models are also
used in some cases, and European Union (EU) research efforts have included attempts
to develop and test predictive models of fertiliser N requirements in European
vegetable systems (Battilani et al. 2003; Karaman et al. 2005).
6.2.1.2 N Supply from Soil
The N supply from soil is the net result of inputs such as mineral soil N available
at planting Nmin; N mineralized from soil organic matter Nm; N released from residues of previous crop NR, and outputs, such as mineral N losses due to immobilisation NI; denitrification ND; volatilisation NV; and leaching NL.
Mineral soil N available at planting depends mainly on the previous crop and its
management, cultural practices such as applied N-fertiliser rate and irrigation, prevailing weather conditions (rainfall, temperature) and can be easily measured by laboratory analysis or quick field tests by using ion-specific electrodes (Sibley 2008). For
example, in field research carried out in Central Italy (Tei et al. 1999) at optimum
fertiliser rates, the mineral N remaining in the soil after harvest of lettuce, processing
tomato and sweet pepper was 90–101, 73–89 and 223 kg/ha, respectively.
Soil organic matter mineralisation is a microbially mediated process and in most
cultivated soils ranges from around 0.6 to 0.9 kg N ha−1 day−1 during the growing
season. The amount of N from mineralisation process is usually estimated by lookup tables (CRPV-RER 2007) or empirical function (Rühlmann 1999), both based
on soil organic matter content and soil physical characteristics (i.e. soil texture).
Effects such as cultivation method and timing can have a mediating effect on the
mineralisation process as microbes are brought into contact with fresh, previously
unavailable substrate (Silgram and Shepherd 1999).
Crop residues and green manures represent the highest potential source of N for
vegetable cropping system with the exception of chemical fertilizer (Rahn et al.
1992, 1993; Müller and Thorup-Kristensen 2001; Thorup-Kristensen 1994; ThorupKristensen and Nielsen 1998, 2003). For instance, brassica residues can contain up to
250 kg N ha−1, which is more than equivalent to the total N demand of many vegetable
crops (Burns et al. 1997), sweet pepper up to 130 kg ha−1 and processing tomato about
100 kg ha−1 (Tei et al. 1999, 2002). Guerette et al. (2000) reported that vegetables crops
leave behind more mineral nitrogen for the next crop than cereal crops. A wide range
of residues quality factors have been found to be correlated with N release (Harrison
and Silgram 1998); these include the C/N ratio (Giller and Cadisch 1997; Bending
et al. 1998; Bending and Turner 1999), N content (Janzen and Kucey 1988; Vigil
and Kissel 1991), lignin content (Frankenberger and Abdelmagid 1985; De Neve
et al. 1994; Giller and Cadisch 1997) and lignin-to-N ratio (Vigil and Kissel 1991).
The C/N ratio is easy to calculate and is a highly reliable indicator of the nitrogen
mineralization from organic compounds. Tremblay et al. (2003) summarised mean
values of potential N released as affected by the residues from the previous crop
154
F. Agostini et al.
in order to develop a more practical approach for N-fertiliser management in vegetable
systems. However, although the mineralisation of organic nitrogen into mineral N
forms available to plants or for leaching has been widely studied, it is a complicated
process and results are difficult to predict with confidence.
Recent land use, cultivations and fertilisation history should be taken into
account when evaluating the risks of nitrate leaching through their effect on
mineralisation, nitrification and hence on the magnitude of the pool of N available for plant uptake or leaching (Neeteson and Carton 2001). For example, longterm monitoring of a field receiving pig slurry applications indicated an enhanced
nitrate leaching over 10 years after the applications had ceased (Mantovani et al.
2005). This is an indication that a large, highly labile pool of organic and mineral
N had been established over many years and this should be taken into account by
reducing future fertiliser N recommendations. In a similar manner, the ploughing
up of rotational or long-term grass for vegetable production can release large
quantities of mineral N as soil micro-organisms are brought into contact with
fresh, previously unavailable substrate (Silgram and Shepherd 1999), and this
effect can last for several years after the original cultivation event took place
(Silgram 2005). Despite attempts to adjust fertiliser applications to match crop
requirements, some rotation systems are at inherently greater risk of nitrate leaching
than others due to the release of nitrate from the mineralisation of crop residues
which can be difficult to predict and may not be synchronised with the N demands
of the subsequent crop. For example, late-harvested crops such as sugar beet leaf
tops may mineralise rapidly and may either leach nitrate that same winter when
the land is bare, or alternatively may contribute to leaching risk the following winter
(termed a ‘grandfather effect’, Lord and Mitchell 1998). Neeteson and Carton
(2001) reported that residual soil nitrogen after the application of the recommended amount of nitrogen is relatively low in Brussels sprouts, white cabbage
and onions (20–75 kg N ha−1), but for spinach, leeks and cauliflower the residual
(i.e. post-harvest) soil nitrogen can reach values as high as 200 kg N ha−1. In
contrast, the incorporation of carbon-rich residues (e.g. wheat straw) has wellknown abatement effects against nitrate leaching by temporarily stimulating net
N immobilisation (NI). However these effects are transient, can be subtle (Silgram
and Chambers 2002; Agostini and Scholefield 2005) and may be antagonistic
(Garnier et al. 2003). A practical application of the effect has been tested in field
vegetables (Brassica napus) to control nitrate leaching from plant residues: several biodegradable materials rich in carbon including straw and paper mill byproducts were added to the soil or composted with the crop residues before
application, and both treatments induced a decrease in nitrogen lost as leached
and as nitrous oxide (Rahn et al. 2003).
Denitrification losses (ND) in arable soils are important only when heavy rainfall
occurs after a recent N-fertiliser application, but in that case no more than 15–20
kg N ha−1 are denitrified per major rainfall event. In practice, both denitrification
and volatilisation losses are usually deemed negligible in an N balance for a vegetable crop and so they can be omitted as occurs in calculations carried out by the
Organisation for Economic Co-operation and Development or OECD.
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
155
Leaching can occur at any time during the growing season in relation to the
pattern and intensity of rainfall and the frequency, intensity and method of irrigation
applications, the amount and distribution of N within the soil profile, the biochemical
and physical soil properties, and the depth and the architecture of roots, i.e. all factors
that influence the soil solution movement below the root zone. For example, the
amount and chemical characteristics of the clay-sized fraction in the soil will influence the adsorption of ammonium and consequently nitrate availability, creating a
potential retardation mechanism for mineral N leaching; however this delay can
only be effectively exploited if deep-rooted plants can subsequently recover the
N (Suprayago et al. 2002). In general, most of the N leached during the growing
season originates from NS rather than from NF, because the former tends to be more
uniformly distributed to depth, and is more readily displaced from the lower parts
of the rooting zone (Burns 1976). While the dynamics of soil N transformation and
movement have been comprehensively studied, predicting the net effect of the
interplay of immobilization, denitrification, N cycling and leaching processes on
the soil–plant system is complex and still deemed problematic (Hartz 2003),
especially in a predictive context.
6.2.1.3 N Supply from Irrigation and Rainfall
Nitrogen concentrations in irrigation water can be significant, depending on its
source, and particularly in areas with high livestock density. Land also receives wet
and dry atmospheric N deposition derived from nitrogen oxides generated by the
use of fossil fuels from individual or industrial users (Scudlark et al. 1998; Cape
et al. 2004), although the relative importance of industrial inputs varies greatly on
a regional and national basis.
6.2.1.4 N Recovery
Greenwood et al. (1989) defined the apparent recovery (REC) of fertilizer N by the
crop as
REC = (UF – U0 ) / NF
(6.3)
where NF = fertiliser-N rate; UF = N uptake when NF is applied; U0 = N uptake when
no fertiliser is applied. REC corresponds to fF in equations (6.1) and (6.2).
The same authors showed that in vegetables the relationship between N-fertiliser
rates and N uptake decreased linearly according to the following general equation:
REC = REC0 – bNF
(6.4)
where REC0 = the fitted value of REC with an infinitely small amount of fertiliser
N; (−b) = the gradient of REC against NF.
156
F. Agostini et al.
Table 6.1 Typical apparent recoveries from yield expressed as Dry Matter (DM) at optimum
N-fertiliser rates for a range of field vegetable crops (D.J. Greenwood, personal communication
in Burns 2006)
Percent of
Crop
Yield (t/ha DM)
Uptake (kg/ha)
Recovery
Response value
Carrots
10.7
193
49
19
Leeks
13.7
268
35
108
Lettuce
2.0
53
7
68
Onion (bulb)
5.1
120
28
214
Radish
1.0
35
14
13
Red beet
11.3
298
34
162
Spinach
1.7
87
11
190
Summer cabbage
7.0
211
85
210
Swede
8.8
356
39
28
Turnip
7.7
309
54
24
The relationship (6.4) is species-specific (Greenwood et al. 1989; Jones and
Schwab 1993; Karitonas 2003; Tei et al. 1999, 2000, 2002, Burns 2006) because it
depends on the efficiency with which plants extract N from the soil due to differences in root functioning and architecture (Thorup-Kristensen and Sørensen 1999;
Thorup-Kristensen and Van der Boogard 1999), but it is also affected by soil conditions, weather conditions, agronomic practices and fertiliser application methods.
Although it was a rough estimation of the N-recovery efficiency of a crop, the
knowledge of REC value for a species (Table 6.1) is useful for the determination of
the optimum N-fertiliser requirements and gives clear information on the proportion
of N fertiliser not taken up by the crop and so at risk of leaching (Burns 2006).
The recovery factor for soil N (fS in equations 6.1 and 6.2) is usually estimated
from the uptake of N when no fertiliser is applied (U0 in equation 6.3), although it is
a rough estimation because there is an interaction between N-fertiliser rate, available
N from soil and recovery factor for soil N (i.e. in general all crops are more efficient
at recovering N when the N-fertiliser rate is relatively small) (Burns 2006).
Instead of the apparent recovery, some authors introduce the concept of a
‘safety margin’ (Tremblay et al. 2003) that is an amount of additional nitrogen
to be present in the soil to safeguard the crop from nitrogen shortages that could
occur if only the amount of nitrogen required for uptake were present in the soil.
In fact below a critical concentration of soil nitrogen, represented by the safety
margin (Table 6.2), a plant’s efficiency at extracting soil nitrogen is diminished
and so the safety margin allows the plant to extract its full quotient of nitrogen
from the soil. Crops that have small, shallow roots with few root hairs (leeks and
onions) are inefficient at extracting nitrogen, so the safety margin provided must
be relatively large. Conversely, plants with long, deep, extensive root systems
are more likely to extract soil nitrogen in its different form, so a smaller safety
margin can be assumed.
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
157
Table 6.2 Mineral nitrogen safety margin required up until harvest (Tremblay et al. 2003)
Mineral nitrogen safety margin required up until harvest (kg/ha)
<30
30–60
60–90
Carrots (planted late)
Brussels sprouts
Cabbage (planted late)
Broccoli (harvested in fall)
Beans
Chinese cabbage
Iceberg lettuce
Endive
Curly kale
Kohlrabi
Cabbage (planted early)
Garden lettuce
Carrots (planted early)
Radicchio
Radishes
Beets
Celery
Cauliflower
Broccoli (harvested in summer)
Leeks
Spinach
6.2.1.5 Perspectives
Nutrient budgets are being used increasingly by farmers and policy makers at farm
and country scales either to increase the understanding of nutrient cycling, as performance indicators and awareness raisers for improved nutrient management and
environmental policy, or as regulating policy instruments to enforce a certain nutrient
management policy in practice (De Walle and Sevenster 1998).
However, some uncertainties are associated with the budgeting approach due to
wrong combination of N type, N source and N-application frequency, which should be
taken into consideration for proper uses of the N balance (Oenema et al. 2003). Tests
on irrigated crops in high-intensity agricultural regions between the French Alps and
the Rhone valley were carried out for 3 years and showed how more than 30% of the
applied nitrogen was lost due to irrational timing and unnecessarily high dosages
(Normand et al. 1997). Further work is needed to educate farm managers to better
exploit the pool of mineralised nitrogen already present in the soil, and consider nitrate
leaching losses as ‘lost fertiliser’ (= money) in the context of farm profitability.
Given the limited efficiency of fertiliser use by crops, and the associated residual
N available for leaching after harvest, a further consideration is that some authors
of N cycle studies comment that they cannot realistically envisage annual reductions of more than 20 kg N ha−1 in open field farming. This implies that regions with
low drainage will risk breaking the Nitrates Directive limit on nitrate concentration
in surface and groundwaters (e.g. Silgram et al. 2003), and in some areas the only
practical solution may be the change from intensively managed and fertilised horticultural systems to a lower input and more extensive land used based on pasture
land (Goulding 2000).
158
F. Agostini et al.
So several methods for estimating the different components of the N balance and
for relating them to the N requirements have been developed by researchers and used
by technicians and farmers although they differ in terms of feasibility, reliability
and accuracy.
6.3 Methodologies and Strategies for Improved N Fertilisation
Several methods are available to estimate the N-fertiliser requirements of vegetable
crops. The most simple and practical methods, spread among farmers but entirely
empirical, are based on experience and observations. The experience method considers the average N rate applied in the past, which was associated with good yields for
a specific local condition, then reduces or increases fertiliser N rates in light of
empirical observations such as a large quantity of crop residues, a dry or wet previous
winter, later planting, and yields below average, applying traditional ‘rules of thumb’.
The observation method judges the nitrogen requirement of a crop by the use of
diverse ‘diagnostic tools’ (Tremblay et al. 2003) such as plant colour, non-fertilised
window (an adjustment of the N fertilisation by comparison of unfertilised plot within
the crop used as a soil N availability indicator) or indicator plants (fast-growing plants
that have a deep rooting system and a strong ability to extract nutrients from the soil,
for example radishes, grown on a small non-fertilised section of the field).
Look-up tables are widely used throughout the world and their complexity varies
in relation to the required information, such as previous crop, crop residues, soil
texture and depth, average rainfall, to be used for estimating soil N availability at
planting and during the crop growth (see e.g. MAFF 2000). Burns (2006) pointed
out that ‘the advantage of this method is that it is relatively simple and makes use of
accumulated wisdom built up from response data for a wide range of crops grown on
different soils over many years, but recent evidence suggests that this approach may
not be as reliable as others where Nmin is measured directly (Goodlass et al. 1997)’.
The possibility to keep monitoring measurements of soil and plant N ongoing
during the period of crop growth is pivotal to the sustainable management of vegetable crop production, where large spatial variability in soil and plant nutrient status
is a well-known issue that tends to lead to over-irrigation and over-fertilisation as
farmers ‘play safe’ (De Tourdonnet et al. 2001), due to the variability in N supply
and because economics dictate extra ‘contingency’ fertiliser is less costly than the
(potential risk of) lost yield. However, the recent sharp increase in fertiliser prices
could help to limit the risk of supra-optimal fertiliser applications.
6.3.1 Methods Based on Soil Mineral N Content
Soil analyses aim to characterise the soil nitrogen status or to predict its availability
during the crop growth phase (Dachler 2001). Several tests are available to determine
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
Table 6.3 Rooting depth of some
vegetable crops (Scharpf 1991a)
0–30 cm
Kohlrabi
Lettuce, leaf
Lettuce, iceberg
Peas
Radish
Spinach
30–60 cm
Beans
Broccoli
Cabbage, early
Cauliflower
Celery
Endive
Leek
Potato
159
60–90 cm
Asparagus
Brussels sprouts
Cabbage, late
Cereals
Corn
Rape
N requirements and their reliability depends on many variables. Nmin and KNS
(Kulturebegleitende Nmin Sollwerte) are two methods for developing fertilizer recommendations based on measurements of soil mineral nitrogen.
In the Nmin method (Wehrmann and Scharpf 1986), the N-fertiliser requirement
of the crop (Nrate) is estimated as Nrate = Ntarget − Nmin. Ntarget is a specific target level
of nitrogen that must be available for maximum growth and yield to occur (Feller
and Fink 2002); the target value is determined experimentally and takes into
account both nitrogen already in the soil and nitrogen supplied by the application
of fertilisers. Nmin is determined from soil samples collected early in the field season, just before seeding or transplanting, taken to a depth of 0.3, 0.6 or 0.9 m
depending on the root depth of the crop (Table 6.3). The method makes no adjustment for N mineralised during growth.
The KNS (Kulturebegleitende Nmin Sollwerte) method, instead of just one target
value, uses target values that differ throughout the season (Lorenz et al. 1989), so
the KNS method recommends nitrogen to apply at planting and as top-dress or sidedress applications during the growing season.
Goodlass et al. (1997) found that the recommendations from an Nmin method
were marginally closer to experimental estimates of the N-fertiliser requirement of
the crop based on maximum yields than most other methods tested. However, some
other researchers have found the Nmin method less robust (e.g. Neeteson 1989).
The soil tests can be done at the laboratory or by a quick test using several tools
(e.g. Nitracheck 404, Mercoquant, Cardy meter), but their reliability is limited by
the representativeness of the field sampling procedure, since the spatial distribution
of nitrate in soils is not homogeneous. Moreover, the samples must be chilled
quickly to prevent any changes in nitrate content while awaiting analysis, as poor
protocols for sample storage and transit can lead to large additional releases of
mineral N which can render results meaningless.
However, the measurement of the magnitude of the soil mineral nitrogen (SMN)
pool accessible to plant roots is not very reliable when there are periods with high
rainfall during the growing season, or under high temperatures, or in soils with high
organic matter contents (Wehrmann and Scharpf 1986). Stoniness is also a factor,
as laboratory results in milligrams per kilogram need to be converted to kilograms
per hectare to a given sample depth using an assumed bulk density for the soil. Bulk
density values vary with soil texture and organic matter content, and stone content
160
F. Agostini et al.
will reduce this soil bulk density. Application or incorporation of high amounts of
slurry or green manure and crop residues can also produce misleadingly high values
(Dachler 2001). The accuracy of soil N content and load indicators should also be
verified (Makowsky et al. 2005). An attempt to improve the use of SMN data is the
creation of spatial statistic maps as has been tested within the Nitrogen Sustainable
Management Programme in Agriculture (PGDA) implemented in Wallonia,
Belgium (Curtois et al. 2005). A nitrogen balance based even on single local determination (i.e. before the growing season) can differ by 10–20 kg ha−1 or more from
a balance calculated from empirical tables. However, direct analysis of soil sampled
at farm level presents the problem of correct sampling methodology and appropriate
storage. It is easy to understand how the required facilities and technical skills to
correctly sample, handle, store and analyse soil samples are seldom available to
vegetable producers. Therefore, direct determination in the field of soil and plant
nitrogen through sensors can be a more practical and cost-effective methodology
(Dachler 2001).
The different methods to predict nitrogen availability and their modifications
look not only to the current state of mineral N in the soil but also to the soil mineralisable N pools, which are more stable than mineral nitrogen. Several soil analytical techniques have been developed and modified (Table 6.4) for this purpose, and
the joint use of this methodology with the measuring of mineral nitrogen could
provide a better evaluation of the soil nitrogen supply to the crop (Dachler 2001).
However, in soils with high organic matter content or treated with organic matter and
crop residues, the estimation of Nmin is a problematic task. The nitrogen released
from humus during the vegetable growing period is affected by environmental events,
soil characteristics and cropping practices, and therefore the Nmin target values can
vary spatially and must be measured at a local level (Tremblay et al. 2003). However,
even with soil analysis results, farmers do not always translate knowledge of adequate
nutrient supply in the soil into a lower input of fertilisers as suggested by findings
in Finnish vegetable production (Salo et al. 2001).
An alternative method to complement conventional soil analysis, where several
determinations are required over a long period, is the use of electrical conductivity
(EC) measurements carried out on the soil solution by probes based on Time Domain
Reflectometry (TDR) (De Neve et al. 1999) or Frequency Domain Reflectometry
Table 6.4 Determination method for available nitrogen (Adapted from Dachler 2001)
Method for determination of available soil N
Year of development
Hot-water-soluble N
1976
Organic soil substances
1978
Electro-ultrafiltration extractable N
1979
Free organic N
1982
Soluble organic N
1987
Water-soluble organic substances
1988
Anaerobic incubation, organic N
1988
N-rich non-humic substances
1990
Potential mineralisable nitrogen
1993
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
161
(ThetaProbe). The use of TDR probes allows the estimation of available soil nitrogen
and immobilised N in non-saline soils (De Neve and Hofmann 2001), and further
calibration and development of specific TDR instruments could extend the use of
this method, which has so far been limited to experimental work on study farms.
The time and the frequency of a reflected TDR wave in the soil depends on its water
content and on the quality and quantities of the ions in it, while mathematical models
can be built to use the quality of the reflected wave to calculate the concentration
of such ions (Krishnapillai and Sri Ranjan 2009, Souza et al. 2006). However, an
extended comparison between chemical and EC based N measurements has proved
how only the first one can give a constant reliable assessment of N soil (Baumgarten
2006), and factors such as soil texture, organic matter and stone content can influence
the accuracy of results.
6.3.2 Methods Based on Evaluation of the Crop
Nutritional Status
Various measurements can be made to determine nitrogen-fertiliser requirements
based on plant tissue nitrogen content. The use of these methods in vegetable production systems is deemed particular relevant in the ‘dynamic optimisation of N
supply’, i.e. a method of N management based on periodic monitoring of nitrogen
content in vegetables during their growth.
As with soil sampling, plant analysis must be conducted carefully, because also the
nitrate concentration in plants is heterogeneous (Mills and Jones 1996; Lorenz and
Tyler 2007). Standard laboratory analysis involves analysing the most recently
matured leaf of the plant for an array of nutrients based on dried plant parts. The
resulting analyses can be compared against published ranges for the specific crop
(Mills and Jones 1996; Lemaire and Gastal 1997; Gastal and Lemaire 2002; Tei et al.
2002, 2003) to determine if the crop is at sub-optimal, optimal or at ‘luxury’ (i.e.
supra-optimal) levels of uptake. Standard laboratory analysis can result in very accurate measurements (Mills and Jones 1996), and therefore it can represent one of the
most accurate methods of estimating plant N status. However, this procedure is time
consuming for most diagnostic situations in the field (Lemaire 2008); especially if a
rapid crop N status evaluation is required to adjust the N recommendation rate in a
dynamic N-management system. Thus, quick tests like sap test or chlorophyll readings have been developed and are increasingly used operationally (Matthaus and Gysi
2001, Simonne and Hochmuth 2006; Farneselli et al. 2007a, b).
The ‘sap test’ measures the NO3–N present in xylem and phloem sap plus the
apoplastic, citosolic and vacuolar water on the leaves; thus, it results a direct measure of current N supply. Once absorbed by roots, nitrogen is transported to the
leaves where it is transformed and incorporated into living material. Thus, nitrate
concentrations in the aerial part of the plant provide a good indication of the adequacy of N applied to the crop. In particular, nitrate in the leaf petioles seems to
give the best indication of crop nutritional status because it is more sensitive to
162
F. Agostini et al.
fluctuations in N availability than the sap extracted by leaf blades. Nitrate content
in sap can be measured by different tools which, in general, are highly correlated
with results from conventional laboratory analysis (Errebhi et al. 1998; Coulombe
et al. 1999; Hartz et al. 2000). The most common are: Merkoquant test strips, which
react to the NO3–N content by producing a colour, the intensity of which varies
directly with the concentration; an ion-specific electrode, as Horiba-Cardy Meter,
which reads directly the NO3–N concentration in the sap. Several plant sap quick
test kits have been calibrated for N in many crops including vegetables (Coltman
1987; Vitosh and Silvia 1994; Delgado and Follet 1998; Errebhi et al. 1998;
Coulombe et al. 1999; Taber 2001; Jimenez et al. 2006; Farneselli et al. 2006a;
Erdal et al. 2007). Even if the sap test procedure is markedly affected by many factors (Paschold and Scheunemann 1989; Vitosh and Silvia 1996; Farneselli et al.
2006a), when carefully undertaken it can be a reliable tool for monitoring the crop
nutritional status of many vegetable crops (such as processing tomato) and with
results consistent with the critical N-curve method (Tei et al. 2002) for the most
important time period in fertiliser management (Farneselli et al. 2007a).
The chlorophyll meter readings, such as SPAD-502 meter by Minolta, is another
common quick test (Hoel 2003; Swiader and Moore 2002; Sexton and Carroll
2002; Arregui et al. 2006). It detects differences in leaf nitrate content by measuring
the light transmittance through leaves. The device is simple to use and, since it
estimates the nitrate content in the tissue of intact and growing leaves, it is not
destructive and does not require the preparation of any chemical samples for analysis. SPAD readings are an accurate method to evaluate the crop nutritional status
because the chlorophyll content is usually highly correlated with the nitrogen level
and yield, but, at the same time, it is affected by several factors such as cultivar,
environmental conditions, plant growth stage, pests and diseases (Piekielek and Fox
1992; Gianquinto et al. 2006). The SPAD meter is therefore best used together with
other crop and meteorological monitoring tools. The reliability of the SPAD
method has been tested with good results on several crops including corn (Piekielek
and Fox 1992), cereals (Arregui et al. 2006), potato (Gianquinto et al. 2003; Olivier
et al. 2006), tomato (Gianquinto et al. 2006, Farneselli et al. 2007a), pumpkins
(Swiader and Moore 2002) and beets (Sexton and Carroll 2002).
These approaches helped to implement good practices in vegetable N management in several Canadian states (Westerveld et al. 2003). Tremblay et al. (2003), in
their guide to vegetable nitrogen fertilisation, give a very good judgement on the
use of these field devices, but consider them as a complement to more conventional
soil analysis. Others (Neurkirchen and Lammel 2002; Schroder et al. 2000) judged
such methods – if calibrated according to different varieties and environments – to
be so precise as to be able to provide all the necessary laboratory determinations for
plants and soils. However, most crop indicators seem to be more effective at diagnosing N deficiencies rather than N excesses, with the exception of the sap test
(Radersma and van Evert 2005). The main benefit of the new methods tested is
mostly as a ‘field troubleshooter’ for identifying low nitrogen status situations – in
contrast, their use for reducing over-fertilisation could be more problematic.
Indeed, a review of the available quick test tools including test strips and SPAD
meters, Hartz (2003) highlighted this method’s limitations due to the high
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
163
equipment cost and demanding calibration process, and the sometimes weak
relationship between apparent plant N status and the real plant N demand.
Nevertheless, if the scope of the recommendation is limited to fertiliser topdressings of nitrogen during vegetable growth, then sap nitrogen content has proved
to be cheap, more accurate in characterising spatial variability (i.e. in broccoli CV
= 9% against CV = 29% where CV is coefficient of variability), faster, and less
weather-dependent compared to conventional Nmin determination (Matthaus and
Gysi 2001). An improvement on the crop indicators approach can be achieved
using ‘crop windows’, which are field plots where the crop is kept at maximal N
status, if the difference between the crop indicator index between the window crop
and the field crop is large, an additional application amount can be calculated for
the field crop (Radersma and van Evert. 2005, Wiesler et al. 2002). Such reference
plots should also set accordingly the growth stage when each diagnostic system is
planned to be used (Tremblay and Belec 2005).
Another contemporary approach, which is currently being studied in France and
in Italy for tomatoes, melon, aubergine and other uncovered field vegetables, is the
“Index of Nitrogen Nutrition” (INN), which is the ratio of the percentage N content
in the plant to the critical percentage N content at which the plant stops growing.
Its development implies the identification of a part of the plant in which the N
content is representative of the whole plant N status, and the development of a
specific function linking N dose applied and plant growth. This methodology is
applicable only if a diagnostic instrument is developed and calibrated for plant N
testing in the field (Le Bot et al 2001; Dumoulin et al. 2002a, b).
The choice of the best method of assessing N requirement using soil or plant analyses
depends on the crop and soil type. While researchers agree that adjusting fertiliser recommendations according to soil mineral nitrogen test is a good practice especially in high
N situations (Goodlass et al. 1997; Hartz 2003; Burns 2006), there is no consensus on
the best method for monitoring dynamic crop nutritional status during the growing season. For evaluating crop nutrient status, results from different studies have lead to different conclusions: certain crops appear to be assessed accurately using the sap test, while
others do not show as strong a correlation between sap nitrate content and crop nitrogen
supply and are therefore better managed using soil nitrate testing. Research carried out
in lettuce and broccoli concluded that there was a higher accuracy associated with soil
testing compared to sap testing (Coulombe et al. 1999; Hartz et al. 2000); while in potato,
fertiliser cost and leaching losses were reduced based on the sap test. However, other
researchers have found that the status of many others vegetables crops such as potato,
cabbage, carrots, onion and tomato was accurately assessed using the sap test (University
of Minnesota 1996; Westerveld et al. 2003; Farneselli et al. 2007a).
6.4 Nutrient Modelling and System Analysis
Concerns in recent decades over the loss of nutrients from agriculture to water bodies
have had to balance the commercial pressure for yield maximisation against environmental policy agendas including water quality legislation, climate change targets
164
F. Agostini et al.
and environmental sustainability. The resulting investigations have led to a ‘holistic’
new approach to nitrogen fertilisation in vegetable production at farm and regional
scale (Huffman et al. 2001). Although some general recommendations can be
derived from experimental results for specific case study scenarios, the variability
in soils, climate, hydrology and management means that it is not possible to provide
a fully exhaustive range of fertiliser parameters for all the species of vegetable
produced in the EU on all the different soils (Goulding 2000).
Mechanistic simulation models have been developed representing system processes at different levels of detail in order to simulate, test and explore the interactions in soil–plant systems for crop growth and nutrient uptake (Le Bot et al. 1998;
Marcelis et al. 1998). In general, simulation models are intended for researchers in
order to study the nitrogen interaction in the plant–soil system, by supplying data
sets collected from experiment with data on local meteorological conditions. With
the application of those models, researchers are able to evaluate which parameters
are important in the nitrogen balance and may be modified to determine which factors are critical in the nitrogen balance. Since simulation models usually need
accurate information on several eco-physiological parameters they are generally
unsuitable for providing practical advice to farmers and technical advisory services
(Grignani and Zavattaro 2000) unless they are embedded in user-friendly computerbased Decision Support Systems (DSS) for use in commercial practice (Battilani
and Fereres 1999).
Exploring system dynamics and responses using simulation models is clearly
less labour-intensive and more flexible than field-based experimental work
(Whitmore 1996) but very few N models are based specifically on vegetable studies.
One widely used software packages is WELL_N (Greenwood et al. 1987; Rahn
et al. 1996) that since its release has been used widely by large sectors of the UK
field vegetable industry (Burns 2006). It was developed by Greenwood et al.
(1987) to present the response of winter wheat to N fertilizer and was later extended
to include the simulation of growth of 25 vegetables and major arable crops and
the release of N from crop residues. The DSS WELL-N uses an embedded simulation model of crop N response (N_ABLE) simulation model (Greenwood et al.
1996), which includes a complete crop rotation, and is able to evaluate the effects
of different soil management strategies on nitrate leaching from intensive vegetables rotations. Other examples of DSS are N-Expert (Fink and Scharpf 1992;
Stenger et al. 1999), Irriguide (Bailey and Spackman 1996; Silgram et al. 2007),
Conseil-Champs (http://www.agrigestion.ca) and Agri-Champs (htpp://www.
lavoieagricole.ca). Battilani et al. (2003) also developed a simple tool-model
(FERTIRRIGERE) for managing water and nutrient supply in drip-irrigated processing
tomatoes.
Catchment-scale assessments based on models using spatial data on soil,
weather and crops are needed for planning the reorganisation of (and scenarios for)
changes in agricultural activity in a more sustainable way. Such methods can estimate the potential for nitrate leaching over a large area from different production
and nitrogen-management systems by linking simulation models, soil and climate
data and geographical information systems (Hoffmann and Johnsson 1999; Lilburn
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
165
and Web 2002). The end results are tools that allow judgments of the potential
impacts of ‘good practice’ (Huffman et al. 2001; Haberlandt et al. 2002), and help
identify ‘hot spots’ at high risk of nutrient pollution due to a combination of land
use, soils, climate and hydrological conditions. Areas posing a high risk of diffuse
pollution from agriculture (due to the combination of land use, soil, management,
climate, slope, location, etc.) can then be targeted in a focused, spatially defined
manner either within the EC Nitrates Directive (within Nitrate Vulnerable Zones
(NVZs)) or the EC Water Framework Directive (within River Basin Management
Plans). Member States are already developing such approaches, at national or
regional level, for some or all crop types (e.g. Italy - project for Soil Quality for
Sustainable Agriculture and Forestry, M. Pagliai, personal communication; UK –
‘MAGPIE’, Lord and Anthony 2000, in UK same approach is followed for P management also, PSYCHIC, Davison et al. 2008; Collins et al. 2007). Ideally, the
models should provide also a ‘cost curve’ analysis of the required costs and benefits
associated with different mitigation measures in a range of farm systems involved
(Anthony et al. 2005).
However, the use of mechanistic models at field/farm level is often hampered
by the lack of localised data or the required level of competence (Grignani and
Zavattaro 2000). With limited relevant calibration datasets, it is not surprising that
in many cases, Decision Support Systems (DSS) at farm level related to vegetable
production tend to underestimate nitrate leaching (Uhte 1995). However, this does
not imply that the systems approach is not highly valuable in terms of its potential
for improving the sustainability of horticulture (Rabbinge and Rossing 2000;
Visser de et al. 2005). At regional scale, advanced statistical methods (such as
fuzzy statistics: Bardossy et al. 2003) and research techniques (e.g. linear programming, neural networking or genetic algorithms: Gary 2003) can provide the
required data and expert knowledge to fully exploit the potential associated with
different modelling approaches. For simulation exercises at this scale, a smaller
(e.g. 2 × 2 km) grid and the use of more detailed datasets are always advisable
(Borgensen et al. 2005).
Similar exercises have been carried out also at smaller scales (100–200 km2) on
vegetable production in the Valencia region in Spain (De Paz and Ramos 2002).
Their results, supported by the application of spatial and multivariate analyses,
helped to define critical patterns in soils and climate, which were then used to limit
N fertilisation according to crop demand to minimise the risk of leaching associated
with periods of greatest drainage. From the farmers’ point of view, nitrate leached
out of the soil root zone represents money wasted on ‘lost’ fertiliser.
These kinds of projects can also generate information for developing farm-level
databases to identify agro-ecological indicators, which can evaluate the sustainability of different elements in vegetable production systems (Mempel and Meyer
2002). For instance, the ‘Indigo method’, developed in France to analyse vineyards
and fruit production (Gary 2003), allows the linking and ranking of each factor in
the cropping system in relation to a set of environmental parameters. Each user can
then select a minimal number of variables to monitor in a specific strategy such as
nitrate-leaching reduction, pesticide limitation etc.
166
F. Agostini et al.
5
Send the soil samples
Chambre of Agriculture (Eure et Loir)
Laboratory
Communication Service
Agronomical service
Send the results of
the analysis
6
Experiments
4
If you need it, we can
measure mineral N in
the soil of your plots
1
Advisory service
7
Make of synthesis of all
the lab results, compare
them to last year results
and send them to groups
of farmers
Sampling
work
3
2
First advice use the
balance sheet method
to calculate the N
dose
Farmer
plots
Call: please, I
need 3 reliquat
measures
Farmer
plots
Farmer
plots
7
Give an individual
advice using the
lab results and
AZOBIL model
Farmer
plots
Farmer
7
Farmer
plots
Write an article in
the local
newspaper which
gives the mean
dose to apply
according to the
previous crop and
the soil type
Farmer
plots
plots
Farmer
plots
8
Network of plots used by advisors to build up their collective advice
Use this synthesis to calculate
their dose with the balance
sheet method
1 Different phases of the decision process
Fig. 6.2 Interaction between technical consultants and vegetable farmers using a Decision
Support System (Meynard et al. 2002)
However, the implementation of DSSs over large areas cannot be effective without
a well-connected network including farmers, technical advisory services, and local
authorities. Meynard et al. (2002) described this interaction between farmers and
advisory services using a DSS to generate guidelines in crop management (Fig. 6.2).
However, care is required to prevent the quality of the information supplied losing
detail and integrity during the communication process from farmer or farm adviser
to modeller, which could result in misleading recommendations being produced. The
use of such DSS tools is necessarily limited to the range of typical situations (crop,
soil, climate, hydrology) for which they were originally developed. Realisation of the
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
167
potential advantages of using DSSs to guide more sustainable vegetable management and production systems is dependent on (i) appropriate tools to allow upscaling from field to regional level, (ii) appropriate parameters at different spatial scales
and (iii) specific procedures to promote dialogue and help disseminate the resulting
information and advice back to farmers.
At a farm level, a careful monitoring of nitrogen status in soils and crops at a local
level coupled with simulation models of water and N cycling in the plant–soil system can be translated into targeted crop management based on the spatial variability
of agronomic characteristics using geographic positioning system (GPS) instruments linked to geographic information system (GIS) references. This methodology
of ‘precision farming’ is becoming more widely used in open field vegetables and
fruit orchards (Van Alphen and Stoorvogel 2000, Smit et al. 2000). For example, in
Sweden, this precision farming technique is being used to characterise within-field
variability in fertiliser N requirements, water status, or pest/disease risk in vegetable
systems, where it has proved to be cost-effective (H. Sandin, August 2006). Although
such methods can prove cost-effective, such approaches require high technological
input in terms of equipment and training of the operator, which means that this is not
a practical option in some situations. Some researchers have suggested coupling
biophysical simulations with economic modelling at the planning stage to identify
the most profitable management of N inputs (Smit et al. 2000). Carrying out such an
economic optimisation, Smit et al. (2000) found the use of precision agricultural
systems was highly cost-effective for N input management in ware potato in the
Netherlands, and concluded that in precision farming the best economic return was
reached when applying good agricultural practices.
6.5 Agronomic Options in N-Fertilizer Management
There is a broad recognition of the need to improve the adoption of best management irrigation and fertiliser management practices in vegetable growing. Since
NO3–N is mobile and relatively unreactive (Rajput and Patel 2006) and, therefore,
susceptible to movement through diffusion and mass transport in the soil water,
water management is inevitably linked to N management. Careful timely applications of N fertiliser and irrigation water can limit the amount of nitrate leaching
below the root zone (Drost and Koeing 2001), such as occurs with well-managed
fertigation techniques. Once the optimum N rate is applied, a suitable evaluation of
plant nutritional status during the growing season is necessary to make adjustments
accounting for N availability (Coltman 1987; Smith and Loneragan 1997; Simonne
and Hochmuth 2006). Other key aspects of N fertilization and irrigation management which must be correctly evaluated to improve N management include rate,
application timing and method and type of fertiliser (Neeraja et al. 1999). For
example, field experiments carried out for 3 years on irrigated crops in high intensity agricultural regions between the French Alps and the Rhone valley showed that
more than 30% of the applied nitrogen was lost due to inappropriate timings, which
168
F. Agostini et al.
were not synchronised with crop N demand and comprised unnecessarily high
dosages (Normand et al. 1997).
Since the relationship between N applied and nitrate leaching is non-linear,
with nitrate leaching increasing sharply once optimal N application rates are
approached, nitrate leaching could be disproportionately reduced for a relatively
modest reduction in N application rates. If farmers were somehow compensated for
the resulting lower yield, a possibility could be modifying the Common Agricultural
Policy to include a grant-type payment for lower impact agriculture, then this
approach could be the solution for high-risk land uses such as vegetable production
systems (Tremblay et al. 2003). However, this is unlikely to be compatible with the
‘polluter pays principle’ underpinning EC environmental legislation.
Compared to other agricultural land uses, the growing of vegetable crops are
associated with amongst the highest soil mineral nitrogen values in the spring (e.g.
Silgram 2005). The mineralisation of N from these residues can proceed rapidly
(especially under warm Mediterranean conditions in the spring) thereby making it
difficult to capture this N using cover crops except if rainfall is limited during the
growing season (Kraft and Stites 2003). Possible solutions include considering low
or zero fertiliser input systems (i.e. organic land management), soil-less systems
(hydroponics), or reversion to low impact vegetable crops to compensate for the
decreased yield due to low fertiliser inputs (Kraft and Stites 2003). There is also the
relatively new idea of accepting a limited reduction of yield through a sub-optimal
fertiliser regime, with the reduction varying as a function of crop type. Such suboptimal applications may also promote a higher concentration of sugar and vitamin
C in the harvested material, which may have implications for market prices with
traders (such as supermarkets and food manufacturers).
Where the nitrate leaching risk is high post-harvest, then the irrigation and fertilisation management have limited potential as control tools (by improving fertiliser use efficiency through placement, timing, rooting, or variety), with alternative
solutions involving modifications to the crop rotation and/or *inter-cropping with
deep rooted crops providing a potential solution to reduce the N available for leaching (Sidat et al. 2000).
6.5.1 Localised Fertilisation
Placement of N fertilisers close to the plant can play an important role to help prevent or minimise the risk of nitrate leaching, especially in vegetable crops which are
usually grown in rows, by increasing N fertiliser recovery. This localised placement
of N is particularly efficient in reducing leaching risks at the beginning of the growing
season (i.e. starter fertiliser technique) as when plants are small, roots exploit a
very limited soil volume and the N uptake is slow. The use of starter fertiliser, in
comparison with conventional N application timings, promotes both faster and
higher root and top growth, increasing yield and reducing N losses (Costigan 1988;
Ma and Kalb 2006; Osborne 2006). This placement of soluble nutrients close to the
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
169
seed is especially important in cold, wet soil in which nutrient availability and root
growth are generally reduced. Localised fertiliser placement can also be performed
by banding fertiliser on the crop rows. I.G. Burns (personal communication) suggested to restrict first applications to a narrow band and to apply a second application
as top dressing at the normal rate. For example, in cauliflower, roots expanded laterally to exploit about half the row width within 4–8 weeks of planting and crops
planted with the optimum rate of base dressing recovered most of the applied N
within 8 weeks. Such banded fertiliser approaches can be effectively used for cauliflower, onion, lettuce and potato. However, the most effective technique to synchronize as much as possible N uptake with N availability is fertigation.
6.5.2 Fertigation Techniques
Fertigation methods tend to increase the nitrogen use efficiency (NUE) while N
losses to the environment are minimised, maintaining a balance between food production and environmental quality (Farneselli 2008). Since micro-irrigation has
emerged as an appropriate water-saving technique especially for row crops, and
applying fertiliser in the water via drip irrigation can be a more efficient fertiliser
management practice, the fertigation technique is becoming very common on vegetable crop systems. The advantages of the fertigation over broadcast method of
fertilizer applications are emphasized by several researchers (Phene 1999;
Singandhupe et al. 2003; Mohammad 2004).
The high water- and N-use efficiency of fertigation (which represent the major
benefits of this technique) are due to rate splitting according to the crop requirement at any growth phase and due to the localised placement of fertiliser close to
the roots. As a consequence, fertigation can reduce the risks of nitrate leaching,
surface evaporation and deep percolation without any decrease of yield and quality
in produce (Battilani 2001, 2006; Singandhupe et al. 2003; Hebbar et al. 2004;
Janat 2004; Battilani and Solimando 2006). Several studies conducted on different
crops (Li et al. 2004) showed an increase in yield of crops grown with fertigation
techniques compared to conventional ones: Singandhupe et al. (2003) recorded a
3.7–12.5% increase in yield and 31–37% decrease in water consumption for tomato
grown with drip irrigation compared to furrow irrigation systems; while Hebbar
et al. (2004) recorded a tomato fruit yield 19% higher in drip irrigation compared
to furrow irrigation. Nevertheless, fertigation is often managed empirically, both for
irrigation and mineral nutrition aspects, so that its advantages are not fully
exploited, and mismanagement of fertigation can lead to nitrate contamination of
surface waters, groundwaters and soils (Battilani 2001).
Achieving maximum fertigation efficiency requires knowledge of crop-specific
water and nutrient requirements at any site throughout the growth cycle (Tei et al.
2002) and attention to the timing of water and N delivery to meet (but not overwhelm) crop needs. At a given water and nutrient supply, fertigation frequency
affects water volume and N rate per application, and thus soil moisture and nutrient
170
F. Agostini et al.
concentration in the rhizosphere between irrigations, with consequent changes in
crop growth, N uptake and yield (Cook and Sanders 1991; Locascio and Smajstrla
1995; Silber et al. 2003). As a consequence, the careful management of irrigation
and/or fertigation frequency is one of the major management variables affecting
fertigation efficiency. High fertigation frequency is often advocated in the technical
literature (Bar-Yosef and Sagiv 1982) because it keeps soil moisture and nutrient
concentration constant near the root zone, so that nutrient diffusion in the soil is
easy (Silber et al. 2003). At the same time, water movement is mainly controlled
by capillary forces instead of gravitational ones (Phene 1999) with consequent
leaching reduction. Moreover, high fertigation frequency makes it possible to more
precisely modulate the concentration of the nutrient solution in the irrigated root
zone according to crop needs at any growth stage (Bravdo 2003).
Some authors (Cook and Sanders 1991; Locascio and Smajstrla 1995; Silber
et al. 2003) have found that for processing tomato, a daily or weekly fertigation
significantly increased yield compared to less frequent fertigation; although differences between daily and weekly intervals were not significant even on a sandy soil.
The authors hypothesised that yield limitation at low fertigation frequency is
mainly the result of nutrient deficiency rather than water deficiency. However,
crops are able to counteract small, short-lived nutrient concentration variations, and
therefore plants do not necessarily show nutrient stress. Moreover, some studies
have demonstrated that if a little stress is given, root penetration increases and the
yield may increase with reduction in the cost of irrigation (Dalvi et al. 1999).
There is a need to evaluate lower-fertigation frequency in greater detail, because
there is limited evidence of the benefit of higher-frequency fertigation. This is
because frequent fertigation regimes are not easy to manage and increase water
waste due to both evaporation from the constantly wet soil surface and the large
portion of the irrigation cycle used for system charge and flush (Simonne et al.
2005). Previous research conducted by Li et al. (2003, 2004) observed that the
water distribution pattern is affected by several variables with consequences on the
root growth and N leaching. The emitter discharge rate and the application rates of
water and nitrogen affect the wetting pattern and solute movement; in particular an
increase in the water application rate allows greater water distribution in a vertical
direction for a given volume applied (Farneselli et al. 2008). The fertigation–irrigation
frequency may also affect biomass accumulation and partitioning because a different water and nutrient availability in the root zone can affect plant water and nutritional status with possible consequences on root growth and shoot/root ratio, leaf
assimilation and transpiration, canopy architecture, light absorption and distribution inside the canopy (Hebbar et al. 2004). Results from experiments carried out
in Central Italy in processing tomato have suggested that high fertigation–irrigation
frequencies increased the above-ground crop dry matter (DM) accumulation and
N uptake only when N supply was very high and exceeded crop critical requirements
(i.e. for luxury N consumption) while for optimal and sub-optimal crop N status it
had no effect (Farneselli et al. 2007b). In contrast to patterns of biomass and N
accumulation, the size ratio between the different parts of the plant did not change
with the fertigation frequency. Moreover fertigation frequency can affect the timing
of ripening and/or fruit quality (breaks, rottenness, size and size uniformity, nutritional
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
171
parameters) (Hebbar et al. 2004; Colla et al. 2001; Erdal et al. 2007). However, the
strategy of controlling nitrate leaching based on split fertiliser applications and
careful irrigation management may only have a low impact on nitrate-demanding
crops with shallow-rooting systems (i.e. potato, faba bean) especially under heavy
unpredictable rainfall (Andrasky and Bundy 1999). In the slightly more strict
regime applied in the USA, where the nitrate (NO3–N) limit in agricultural groundwater is 43 mg L−1 against the 50 mg L−1 applied in the EU, the control of nitrate
leaching through the management of irrigation and fertilisers has proved a complete
failure (Kraft and Stites 2003).
6.5.3 Slow-Release Fertilisers
The use of slow-release fertilisers serves the same purpose as split applications,
providing nitrogen more slowly as the plant requires it (Li 2003; Khah 2003). This
kind of fertiliser has the benefit of saving time, since all fertiliser can be applied in
a single dressing at the beginning of the season, although it also has some notable
disadvantages such as the need for special application equipment and the more
expensive product compared to conventional fertilisers (Jin 1996; Schaller 2000;
Khah 2003; Prasad et al. 2004) with N release not always coinciding with crop N
requirements (Peltonen 1994). Moreover, the use of organic fertiliser (Heeb 2005;
Herencia 2007; Pavlou 2007) or fertiliser with the appropriate nitrate–N/ammonium–N
ratio or nitrification inhibitors could also be a valuable strategy for improving
N-fertiliser management (Narayan 2002).
6.5.4 Nitrification Inhibitors
The use of new nitrification inhibitors 3.4 Dimethylpirazole phosphate (DMPP) has
also been considered in addition to urea (Pasda et al. 2001). Linaje et al. (2005) in
central Spain measured a reduction of 50% of N leaching with the application of DMPP
to broccoli. Mantovani et al. (2005) obtained similar results by adding DMPP to pig
slurry. This approach could be considered as an alternative to calendar-linked
applications of manure (e.g. in the context of restrictions on the timing of manure applications imposed by the EC Nitrates Directive), thus avoiding the costly need for
storage facilities.
6.5.5 Intercropping
The aim of an intercropping system is to increase the crop root density, and this
approach is most successful when implemented using ‘compatible’ species, which have
different peak times of N uptake and different rooting depths (Baumann et al. 2003).
When implemented in this manner there need not be significant effects on overall yields.
172
F. Agostini et al.
One species may exploit available nitrogen, which is not accessible or required by
the other crop. For example, testing different intercropping systems with faba bean
undersown with brassicas such as oil radish (Raphanus sativus var. oleiformis) or
white mustard (Sinapis alba) proved more efficient than ryegrass and cereal which
reduced the faba grain yield (Justus and Kopke 1995). The depth of the rooting zone
will give an indication of potentially viable intercrop combinations in vegetable
systems (see Table 6.3). Paschold et al. (2003) carried out research in intensive
vegetable production systems in Germany which provided evidence of the potential
for intercropping in vegetable production in Europe to serve as an effective tool for
controlling nitrate leaching. These authors reported that the growth of oil radish
(Raphanus sativus var. oleiformis) between asparagus ridges was a useful technique
for reducing nitrate leaching after the growing season of asparagus had ended (rather
than leaving the soil bare over winter). The Nmin residual in the soil (0–90 cm depth)
decrease in average from 250 kg ha−1 to 150 kg ha−1, with an average increase in
asparagus yield of 1.2 t ha−1. A further element of a mixed-intercropping system is
the creation of a green cover, which covers the soil surface otherwise unoccupied
by growing plants and thereby achieves the same effect as mulching. This is an
established feature of the management of some vegetable fields and fruit orchards,
which is carried out using inert materials such as polyethylene.
6.5.6 Mulching
Sweeney et al. (1987) worked in an open field growing tomato with overhead
irrigation and mulching with polyethylene. This system reduced water drained from
the soil and enabled nitrogen uptake to reach 53% of the applied amount, with 42%
of N applied remaining in the soil and 5% lost as leached nitrate. Similar results
have been reported for the growth of pepper (Romic et al. 2003).
6.5.7 Cover Crops
Many researchers have pointed out the feasibility of using autumn crop covers to
manage the nitrogen husbandry for the succeeding cash crop, prevent the nitrogen
leaching and improve the soil characteristics especially by increasing the soil
organic matter (Harrison and Silgram 1998; Thorup-Kristensen et al. 2003;
Macdonald et al. 2005). As broadly accepted, the phrase ‘catch crop’ is used when
dealing with cover crops that are grown to catch available nitrogen in the soil and
thereby minimising nitrate-leaching losses, while the term ‘green manure’ is used
when dealing with cover crops that are grown mainly to improve the nutrition of
the subsequent crops (Tosti 2008). A good catch crop (e.g. cereals and crucifers)
should have an early sowing date (Thorup-Kristensen and Pedersen 2006), a
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
173
prompt germination and fast growth rate at both above and below-ground levels
(Thorup-Kristensen 2001), and a deep root apparatus (Kristensen and ThorupKristensen 2004). Green manures for supplying N are usually leguminous species
able to accumulate considerable amount of nitrogen: in a Mediterranean environment like central Italy, values ranging from 150 to 250 kg ha−1 for annual clover
(Campiglia et al. 2005) with maximum values of more than 300 kg ha−1 (Benincasa
et al. 2004) for faba bean and hairy vetch green manures. In southern Italy nitrogen
supply of 45 and 165 kg ha−1 are reported for vetch and cow pea respectively, while
faba bean supply was between 72 and 193 kg N ha−1 (Fagnano et al. 2005; De Luca
et al. 2006; Sulas et al. 2007). The net contribution in terms of nitrogen input to the
system (i.e. the nitrogen derived from atmosphere) was estimated 70–80% of the
total nitrogen supplied by legumes (Seddaiu et al. 2007; Sulas et al. 2007).
Recent research found that it is possible to modulate N supply and release from
green manures to a subsequent crop by mixing grass and legumes (Boldrini et al.
2006; Tosti et al. 2008) and that the unit cost of nitrogen from green manures is
much lower if compared to nitrogen from organic fertilisers (Chaves et al. 2006;
Guiducci et al. 2004). However, because the N release will depend on the C/N ratio
in residuals and the mineralisation rate, experimental results can be contradictory
(Harrison and Silgram 1998). The use of mixtures of hairy vetch (Vicia villosa
Roth.) and barley (Hordeum vulgare L.) with high proportion of vetch (>50%), for
example, allowed an optimal N nutritional status of processing tomato without
promoting luxury N consumption (Tosti et al. 2008).
The use of cover crops or catch crops is limited by farmers’ reluctance to adopt
voluntarily a practice which demands extra time associated with establishment and
destruction, possible extra seed costs, and the risk of encouraging the persistence of
weeds, pests, or diseases which may interfere with the growth and yield of the next
main crop (Tremblay et al. 2003). Only some form of incentive scheme or their compulsory use as a requirement under Code of Good Agriculture Practice would assure
their more widespread adoption by farmers (Vos and Putten 2004; Vos et al. 2005).
6.5.8 Cultivar Nitrogen Efficiency
For nitrogen, it has been noted that differences in nitrogen efficiency occur at the
crop level and also in some cases at the cultivar level. N-efficient crops and cultivars
are characterised by deep rooting depths (with enhance N uptake efficiency) and
high utilisation efficiency. Schenk (2006) stated that ‘nutrient use efficiency is a
potential tool for sustainable vegetable production in the field. Some breeders are
going down this avenue and are selecting cultivars under nutrient limiting conditions.
The development of nutrient efficient cultivars is a challenge for horticultural
science not only with a view to reducing the flow of nutrients into natural compartments
of the environment but also taking into consideration production conditions in
countries where access to fertilisers is limited’.
174
F. Agostini et al.
6.6 N-Leaching Assessment
The quantification of nitrate leaching from soils to water has specific difficulties
(Kucke and Kleeberg 1997). A rapid and reliable estimation of NO3–N moving
below the root zone is crucial to reducing the risk of nitrate leaching (Aveline and
Guichard 2005; Makowsky et al. 2005). Since water movement in the soil and
NO3–N concentrations in the soil solution are strictly linked, both these phenomena
have to be investigated. Several different approaches could be adopted to assess
N leaching. Load may be determined directly by soil sample analysis or by collecting leachate from drainage lysimeters. Mathematical simulation models have
become also useful tools in assessing and understanding the movement of fertilisers
through soil into groundwater (Shaffer et al. 1991; Jabro et al. 1994; Bailey and
Spackman 1996; Karaman et al. 2005; Silgram et al. 2007).
Monitoring the NO3–N concentrations in the soil solution by suction cup lysimeters
placed at different depths, is also another method to assess nitrate leaching below
the root zone. This method seems to be particularly useful when the measurements
of nitrate–N concentration are used to calculate the N leached by integrating them
with estimates of drainage volume between successive samplings, or by changes in
soil moisture readings taken simultaneously using soil moisture probes (Moreno
et al. 1996; Vazquez et al. 2005, 2006; Farneselli et al. 2007b). The accuracy of the
resulting load assessment greatly depends on the hydraulic conductivity of the soil
and the evapo-transpiration of the crop. The nitrate concentration component is
affected mainly by the accuracy in sampling the soil solution, which is affected by
the resident soil nitrogen pools and applied fertilisers or manures. The different
sampling methods of the soil solution may sample the nitrate from the two sources
in different proportions, and may sample different pore sizes of soil water, and
therefore results are most reliable when incorporated into long-term monitoring
programmes with replication (Kerft and Zuber 1978; Lord et al. 2007). However,
due to difficulties in maintaining good hydraulic contact between the soil and the
ceramic (or similar) material, suction cups often do not operate well in chalk soils
where water is held very tightly in the smallest pores. Another method of nitrateleaching assessment could be to calculate the load by multiplying the NO3–N concentration in soil samples by the wetted soil volume (Farneselli et al. 2006b,
2007b). Results produced using this method can be useful in drip irrigation systems, where knowledge of the wetted zone volume can be gained by visualising soil
water movement using soluble blue dye (German-Heins and Flury 2000; Simonne
et al. 2003, 2005, 2006; Farneselli et al. 2006b, 2007b).
6.7 Research and Technology Transfer in European Union:
Case Studies
EU States have applied the Nitrates Directive by developing research frameworks,
funding specific research projects, and developing consulting committees, which
have produced documents to help advising farmers on agriculture practices with
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
175
more sustainable environmental impacts. Some specific documents have been
designed to address nitrogen and phosphorus management issues, whereas in others
instances, case studies and initiatives have been more holistic and have focused on
the management of a given crop or crop group. Several examples are given below,
focusing on Mediterranean countries with specific case studies.
6.7.1 Italy
In Italy field vegetables in 2005 were grown in about 470,000 ha with a total production of about 13 million tonnes. Organic vegetable production was about 12,000 ha
(i.e. about 1% of total land in organic cultivation) (Pimpini et al. 2005). Greenhouse
production was about 34,000 ha with a total production of 1.5 million tonnes (mainly
Solanaceae, Cucurbitaceae, lettuce and strawberry). Total value of vegetable production was about €6.6 billion. Fresh markets represent the main destination of
vegetables, but minimally processed vegetables show the highest rate of increase
(about +17% year-1). Vegetable production is widespread in all the regions even if
production from the south are mainly destined for the fresh market while those from
the north mostly go to processing (except Puglia region in the south that is the lead
area for processing tomato with about 30% of national production).
Peculiar characteristics of vegetable production in Italy are the small farm size
(c. 1.7 ha) with two to three crops per year in a wide range of crop combinations
(e.g. pepper–fennel–spinach; early potato–tomato–fennel; tomato–French bean–
cauliflower; peas–beans–spinach; carrots/peas–chicory; tomato/zucchini–fennel/
salads; potato–eggplant) and products destined for the fresh market. Large farms
are not frequent, with cropping systems usually simpler and oriented around the
food industry (e.g. processing tomato; spinach or peas for frozen food), wellmechanised and with use of external manpower.
Due to the Mediterranean climate, spring–summer vegetables are always irrigated, often using saline or partially saline waters. This has pushed towards the
more widespread use of low-pressure irrigation systems, which also produce little
or no risk of leaching.
According to a study from the Istituto Sperimentale per l’Orticoltura (Research
Institute for Horticulture), published as an integration of the PANDA framework,
Italian vegetable production is a strange dichotomy: horticulture is the most highly
productive agricultural sector (on a gross income basis) after beef, but it is also
associated with the smallest average farm investment in terms of land use.
A large framework project (Produzione Agricola Nella Difesa dell’Ambiente,
PANDA) has been carried out since 1996 in Italy to develop environmentally sustainable agricultural technologies. The whole framework deals with soil resilience,
pollution from agriculture, and pollution from non-agricultural sources. The
PANDA project comprised three elements (Environmental vulnerability, Field trials, Analytical systems), which did not explicitly cover vegetable production, but
which included related technical management practices. Great importance was paid
176
F. Agostini et al.
to soil protection, which was judged as the most critical environmental factor in the
Mediterranean area. Among the aims of PANDA was an inventory of areas vulnerable to inputs of nitrogen and other nutrients from agriculture as well the design of
a Code of Good Agriculture Practice (‘Codice di buona pratica agricola’) for Italy
according to the framework given in the Nitrates Directive. Research projects were
undertaken on irrigation and fertiliser management with special attention to nitrogen and phosphorus inputs from organic sources including biomass and livestock
effluents (Mastrorilli 1999). The field experiments were focused mainly on cereals,
or mixed cereal and dairy/beef systems, and in smaller scale on peach and citrus
fruit systems. Considerable emphasis was given to modelling studies for several
different example crops (Francavigli and Benedetti 1995) and at a larger scale for
regional assessment of pollution from agriculture (Coccato and Di Luzio 1996;
Boatto et al. 1996). The Good Agricultural Practices designed within the PANDA
framework was adopted by the Italian government (DM 19/04/99) as a general
framework for the rules designed at regional level for each crop. In Italy, each
regional government is responsible for the application of environmental and agricultural EU Directives. Concerning the inputs of nitrogen, the code gave very
general background information and proposed accounting for the nitrogen already
present in the soil or returned in crop residues when calculating the N requirement
for the next crop. The code does not detail sampling methodologies or specific
analyses, or the use of DSS at farm level. For some open field vegetable crops, the
suggested amounts of nitrogen input (kilograms per hectare) for standard expected
yields (tonne per hectare) are provided in Table 6.5.
A national advisory system on vegetable fertilisation does not exist, but instead
there is an advisory service at a local level through farmer associations and local
governments. The local network provides the farmers with recommended amounts
of nutrient inputs for each growth stage using results from monitoring trials. The
codes for Integrated Production applied by each Regional Government often
include Nutrient Balance Systems (NBS) for calculation of the fertiliser crop
Table 6.5 Suggested N inputs based on standard yields for different vegetable crops
(http://www.politicheagricole.it/norme/mezzitec/19990419__DM.htm)
N-fertiliser
N-fertiliser
requirement
requirement
Target yield
kg N ha−1
Species
Species
t ha−1
kg N ha−1
Garlic
120
12
Asparagus
180
Carrots
150
40
Artichokes
200
Onions
120
30
Cabbage
200
Rape
120
25
Broccoli
150
Cucumber
150
60
Melon
120
Watermelon
100
50
Sweet
180
pepper
Strawberry
150
20
Tomatoes
160
Aubergine
200
40
Courgette
200
in Italy
Target
yield
t ha−1
5
15
30
15
35
50
60
30
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
177
requirements. However, several researchers consider that a more ‘scientific’
approach is needed with a monitoring network for soil mineral nitrogen (Nmin) and
the use of DSS within the local advisory services due to the high variability of
Italian soils and climates.
Extensive programmes of research and monitoring on nitrogen management in
vegetable crops, mainly in open fields, have been undertaken since 1990 by several
universities in Italy via EU (e.g. LIFE) and national (e.g. COFIN, PRIN, FISR)
framework projects. These research programmes have studied the effect of
N-fertiliser rate, fertilisation methods and N-fertiliser source (i.e. mineral, organic
and green manures) on growth and N uptake of the most important vegetables (i.e.
processing tomato, lettuce, sweet pepper, aubergine, potato) to provide parameters
needed to model growth and N uptake in vegetables, and indices to evaluate the
nutritional condition of the crop, and the environmental risks associated with different cropping systems. Within this context, in June 2004, an ISHS international
meeting ‘Towards ecologically sound fertilisation strategies for field vegetable
production’ was organised by the Department of Agricultural and Environmental
Sciences, University of Perugia (proceedings published in Acta Horticulturae 700,
2006) with about 100 participants from 26 countries throughout the world and 50
scientific contributions. In the conclusion of this symposium, it was noted that the
development of sound fertilisation strategies has to take into account the needs and
suggestions of, researchers, policy makers, farmers and consumers who have to
interact with each other.
In Italy, fertigation is becoming the standard method of nutrient applications to
vegetables in order to increase fertiliser-use efficiency and limit the risk of diffuse
pollution via run-off and leaching. This technique is applied on about 70% of the
open field production area. However, if the high nitrate content in irrigation water
is not adequately taken into account in the calculation of N-fertiliser crop requirements, then this can lead to an over-fertilisation of vegetable crops. For example, in
the South Lazio region, nitrate levels in water tables at 10 m depth can easily fluctuate between 50 and 300 mg L−1 (V. Magnifico, personal communication).
6.7.2 Spain
The highly differentiated climate present within Spain, coupled with large differences in soil types, results in high spatial variability in nitrogen-fertiliser requirements and use. Considering scientific literature and statistical data, in Spain only
around 35% of the total N applied is effectively used by crops, which is much less
than the global average efficiency of around 50% (Soler-Rovira et al. 2005).
The Autonomous Communities (Spanish local governments) are the main authorities responsible for implementing the Nitrates Directive (91/676/EEC) including the
associated codes of Good Agricultural Practices relevant for their areas. However,
the responsibility to carry out and implement agricultural and environmental
178
F. Agostini et al.
research is shared between the Spanish government, Autonomous Communities and
universities, sometimes with the collaboration of private companies.
In order to group all researchers and projects about nitrogen in agriculture and to
properly disseminate their results, in 2002 the Spanish government, many Spanish
universities, and Autonomous Communities Research Centre created the Network of
Efficient Use of Nitrogen in Agriculture (RUENA), (Red del Uso Eficiente del
Nitrogeno en la Agricultura). The aims of the network are (i) to provide a forum for
all people investigating the efficient use of nitrogen fertilizer in agricultural systems
and (ii) to create a ‘round table’ to support the development of consensus and consistent recommendations concerning the management of nitrogen fertilizer applied
to crops. The RUENA network is involved in the development of all relevant
European, National and Regional legislations on nitrogen in agriculture, including
those concerning fruit and vegetable crops, and includes researchers and institutions
specifically involved in such area of study. A specific website (http://www.ruena.
csic.es) provides information on the current and past projects, publications, and
contact details for the thematic area of nitrogen use in agriculture.
Before RUENA, Spain had developed some national research projects on the
correct use of nitrogen in agriculture such as the ‘Dynamic of nutrients and
improvement of fertilisation techniques in citrus trees’ (1993–1996); the ‘Monitoring
of nitrate contamination in aquifers in Jarama river basin’ (1992–1995); ‘The efficient
use of water and nitrogen in horticultural crops in the open air by application of
plastic padding and fertigation’ (1998–2001) and ‘The application of pig slurry to
olive crops’ (1998–2000). Under the RUENA umbrella, there are currently several
framework research programmes relevant to the use and misuse of nutrients in
agriculture, including some dealing with the environmental impact of vegetables
and fruit crops.
Within the RUENA framework projects, investigations identify optimum nitrogen-fertiliser rates and timings to obtain optimal yields and harvest quality, and to
limit potential risks of nitrate leaching to water bodies. The main aspects include
studies on the spatial and temporal distribution of nitrogen fertilisers applied to
crops, the methods of quantifying nitrogen demand, the role of crop rotations in N
requirements and the use of models to predict fertiliser nitrogen requirements.
However, current activities are focused on maize crops, which have the highest rate
of nitrate leaching due to the common practices of applying nitrogen at a rate 2 or
2.5 higher than the recommended amount. In this same framework, the Agricultural
Research Technologic Institute of Calaluña (IRTA) jointly with Fundació Mas
Badia (Estació Experimental Agrícola) and regional governments have developed
the ‘Programme to improve nitrogen fertiliser use in agriculture in Baix Emporda
(Cataluña)’ (Plan Pilot per la Millora de la Fertilització Nitrogenada a L’agricultura
del Baix Empordà). The research objective is the identification of optimal nitrogen
rates, maintaining high crop yield and quality, but minimising the negative effect to
the environment (F.D. Olivé, personal communication). Recently, this programme
has been extended to cover horticultural crops and fruit trees.
Several investigations were carried out on plant demand for nitrogen, optimal
timing for nitrogen-fertiliser applications, the most efficient use of irrigation
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
179
systems in nitrogen application to crops and nitrogen supply in the soil. The design
and development of a software family to manage sustainable irrigation systems (or
ADOR: ‘una familia de programas de ordenador para la gestión y la planificación
del uso del agua de riego y sus implicaciones medioambientales’; http://web.eead.
csic.es/oficinaregante/ador) have been carried out within this framework since 2001
by researchers from Estación Experimental de Aula Dei (CSIC), technical personnel from Aragon Regional Government, and Aragon farmers, funded by the Spanish
Government. The ADOR software helps farmers to manage irrigation systems by
planning the irrigation season, and supporting cost analysis evaluating the opportunities to modernise irrigation facilities. A large database was implemented to support the software, which can be used with any irrigation system (surface, drip,
sprinkling) and in any water distribution net (canal or piping). No information is
available on the dissemination of the software and its use by farmers and its impact
on the current practices. However, comments collected by researchers in the field
suggest that even when farmers were involved, they did not adopt new practices
until there was an economic incentive to do so.
In the main vegetable production areas of Spain (i.e. Aragon, Valencia, Murcia,
Extremadura, Andalucia, Aragon, Rioja, Cataluňa, Navarra), prior to the introduction of the Nitrates Directive legislation there was a general lack of consideration
by farmers about the environmental problems associated with nutrient leaching
caused by irrigation and fertilisation. This led to a high level of mineral nitrogen
(from 173 to 232 kg ha−1) in the soil profile (0–90 cm depth) and to the subsequent
high risk of groundwater contamination by nitrate leaching (Gimenez et al. 2001).
The unwillingness of the farmers to comply with this Directive suggests that the
situation even after its implementation remains unchanged; however, no monitoring
studied has been so far carried out to effectively quantify the real impact of the
Nitrates Directive.
More recently, however, several monitoring studies have been implemented to
assess the potential and actual contamination caused by nitrogen applications to
agricultural soils. The results of those activities have highlighted problems in several horticultural and fruit regions. In the AC of Valencia, Ramos et al. (2002) has
shown that around 8% of the Valencia Community population have water supplies
with nitrate concentrations above 50 mg L−1. This is confirmed by the studies of the
Instituto Valenciano de Investigaciones Agraria (IVIA), which demonstrated that
agricultural nitrogen inputs were much higher than the values recommended by
research, and that nitrate leaching values were in most cases within the range of
150–300 kg N ha−1. In the Valencia region, GIS/modelling studies (De Paz and
Ramos 2001) on a typical 2-year crop rotation (potato-lettuce-onion-cauliflower)
showed that the whole open field vegetables area of about 230 km2 in the North of
Valencia is at high risk of nitrate leaching due to the lack of awareness of farmers
on the risks posed by excessive fertiliser N applications. As shown in Table 6.6, the
N-fertiliser rates applied to vegetable crops in Valencia are higher than actual N
crop requirements. Artichoke, early potato and onion were the three crops with
higher leaching rates than other crops. From these crops, nitrate leaching typically
varied between 240 and 340 kg N ha−1 depending on the nitrogen-fertiliser treatment,
180
Table 6.6 Crops and N fertilizer
applied and N uptake by crops (kg
ha−1) in AC of Valencia (Ramos et al.
2002)
Table 6.7 Maximum values of nitrogen
applied in vegetable crops in Andalucia,
Spain
F. Agostini et al.
Crop
Artichoke
Onion
Lettuce
Potato
Pepper
Tomato
Cauliflower
N fertilizer applied
kg N ha−1
470 ± 260
500 ± 280
460 ± 210
700 ± 450
1030 ± 630
940 ± 245
220
Crops
Artichoke
Asparagus
Aubergine
Broad Bean
Cabbage
Carrot
Cauliflower
Courgette
Cucumber
Garlic
Green beans
Lettuce
Melon
Onion
Peas
Pepper
Potatoes
Tomato
Watermelon
N crop uptake
kg N ha−1
130–210
110–210
45–54
180–270
180–270
225–365
40–310
N rates
kg N t−1 of yield
11.5
5.0
11.5
11.5
11.5
5.0
5.0
11.5
2.6
6.8
11.5
5.0
3.5
3.5
11.5
5.0
4.2
3.5
3.5
representing about 66–70% of total N input in the onion crop and 38–65% of total
N input in the potato crop (Ramos et al. 2002).
Also in Andalucia (Table 6.7) and Navarra (Table 6.8) N crop requirements
recommended by the codes for Good Agricultural Practice are by default increased
by the farmers who wish to apply additional fertiliser as a safety margin to guarantee high yields.
In Almeria province (Andalucia region), there are approximately 25,000 ha of
plastic greenhouses used for intensive vegetable production and which represent a
significant potential source of nitrate leaching. Studies carried out on nitrate leaching
from greenhouse pepper (Gallardo et al. 2006) showed that fertigation with a reduced
Table 6.8 Optimal N-fertiliser rates recommended for vegetable crops in Navarra, Spain
Fertilisation (kg N ha−1)
Total rate
Crop
Cultural practices
Artichoke
First year with manure
160
First year without manure
220
Second year
80
Sprinkling irrigation
180–200
Garlic
140
Aubergine
With manure
120–180
Courgette
145
Onion
160
Cauliflower
175–200
Brussels sprouts
180–200
Asparagus
Without irrigation
100
With irrigations
180–200
Spinach
Sprinkling irrigation
140
Green pea
30
Melon
160
Potato
110
Pepper
100–130
Leek
150
Mechanical harvest
90–110
Processing tomato
Manual harvest
190–200
Before crop
0
60
0
60
40
0
45
60
50
50
0
0
40
30
50
40
0–30
50
40–50
70–80
During crop cycle
160
160
80
120–140
100
120–180
100
100
125–150
130–150
100
180–200
100
0
110
70
100
100
50–60
120
No. applications
during crop cycle
2–3
2–3
1–2
3
2
2–3
2–3
2–3
2–3
2–3
1
2–3
3–4
0
2–3
2
2–3
2–3
2
2–3
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
181
182
F. Agostini et al.
concentration of N (i.e. 7–9 mmol N L−1 = 168 kg N ha−1) compared to the standard
(i.e. 10–12 mmol N L−1 = 194 kg N ha−1) reduced nitrate leaching by 7%. Thompson
et al. (2002, 2005) confirmed that in Almeria region the contribution to nitrate leaching to surface water was much higher, in terms of surface area, from open hydroponic
systems than from conventional vegetable production in clay soils.
6.7.3 France
The former Agriculture and Environment Ministry of France, now Ministry of
Ecology and Sustainable Development, has organised a consulting committee for
dealing with pollution from agriculture (CORPEN) since 1984. This committee has
been in charge of the Code of Good Practice since 2001, with special attention to
N and P losses. CORPEN produces several documents and studies, some of which
are focused on vegetable crops.
The French legislation applying the Nitrates Directive demands generally that
the fertilisation must be done according to a nitrogen balance which accounts for
irrigation water and soil mineral nitrogen (SMN). SMN is calculated differently
according to the environmental conditions and crop type. Specifically for vegetable
crops, it details different timings and amounts for the application of N fertilisers
taking into account the soil organic matter contents, climatic regime and soil characteristics in different regions. CORPEN produced edited tables for the most common
vegetables (beans, tomatoes, lettuce, etc.) where the N balance was described for
the more common crop rotations used in France.
In some leguminous vegetables (e.g. peas), N fertilisation is largely avoided
because the symbiotic N fixation is assumed to supply 75% of the vegetable crops’
N requirements in French soils. Also, early sowing to increase the root depth and
the use of catch crops has been suggested for vegetables with high N contents in
their residues. The implementation of the Nitrates Directive in France is undertaken at Regional and Departmental (county) level after ‘contracting’ with the
professional association of producers and advisers. Results have an extremely
variable impact in relation to crops and regions with a little evidence of coordination and consistency at a broader national level. CORPEN has so far limited
itself to scientific advice and providing communication between the different
stakeholders.
Vegetable crops of primary interest for controlling nitrate leaching are tomatoes,
lettuce, strawberry and melon in the South East; cauliflowers in Brittany, carrot in
Normandy, Brittany and the southern part of Bordeaux (where sandy soils once
used for intensive corn crops have been converted to high-quality carrot production). Soil-less and soil-based systems in glasshouses are widespread in the South
West in the Pyrenees region.
In contrast to Italy, France has a strong national network of support and technical advice to the producers based on professional associations and local authorities. This allows an easier transfer of knowledge from main research institutions
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
183
(Universities and INRA) to farmers (mainly the units based at Rennes, Avignon
and Montpellier). For fruit and vegetables this role is played by the CTIFL (http://
www.ctifl.fr) jointly with regional research station and local agriculture associations (Chambres d’agriculture). This organisation offers support in designing
sustainable fertilisation and rotation plans, and publishes fertilisation tables for
the main vegetable and fruit production systems. However the efficacy of this
knowledge transfer depends mainly on the dialogue between advisory services
and producers’ associations and this is extremely variable between different
regions and departments.
In France, help to the horticultural sector is equivalent to only 5% of farm
income compared to 50% of farm income for a farmer involved in grain production. This difference makes the regional associations more sensitive to the
requirements of the Nitrates Directive. Many producers are too preoccupied with
the introduction of a pest management initiative required under other EC
Directives to have the time and will to tackle fertilisation issues. For example, in
the processing tomato production area around Avignon, most farmers still apply
300 kg N ha−1 when uptake is only 120–150 kg N ha−1, largely because they perceive it as too complicated and potentially risky to switch to new, reduced N-input
management. (P. Robin, personal communication). However, an alternative
example is the intensive production of cauliflower in Brittany, which is traditionally based on widespread use of pig slurry. After long-standing pressure from the
authorities and with the support of INRA in Rennes, producer associations suspended N applications for 5 years and are now slowly introducing a more rational
approach to fertilisation based on N balance.
In the South West, only the more ‘enlightened’ producers in open field vegetables tend to use N-balance systems and some simple Decision Support System
tools. In the ‘Midi’, the main area for melon, lettuce and chicory production, 80%
of farmers use a sap test and 20% use an N-balance system for determining
N-fertiliser crop requirements.
At national level, the original methodology promoted by CORPEN (before the
Nitrates Directive) included a programme to monitor and advise farmers on their
fertiliser management (‘Fertimiuex’), which was on a voluntary basis and mainly
tackled grain production. In the south-west of Normandy region in 2000, partially
in response to the Nitrates Directive, an integrated management programme (i.e.
30% reduction of fertiliser rates, crop rotations with less vegetables and at least
30% of cereals, establishment of hedgerows) was introduced to reduce eutrophication of the coastal area: results showed a decrease of about 30% in nitrate concentrations in groundwaters (P. Robin, personal communication). Many technical
advisers and researchers consider this scheme a good demonstration of a practical
approach for the effective implementation of the Nitrates Directive. CTIFL and
INRA are continuing similar trials on fertilisation management for the main vegetable crops, mainly tomatoes, cauliflowers and melon, in the Midi region and in
Brittany.
The design of a sustainable N management for melon production has been the
aim of joint research between INRA in Avignon and CTIFL-Balandran: a diagnostic
184
F. Agostini et al.
method (PILazo-melon) for N requirements based on petiole sap test has been
successfully tested across a wide range of soil and climate in France on different
varieties of melon (Le Bot, personal communication; Dumoulin et al. 2002a, b).
6.7.4 The Netherlands
In most parts of North and Central Europe, national advisory systems are all based on
Nmin target values (Scharpf 1991b; Rahn et al. 2001). This, however, does not avoid
the risk that amounts of nitrogen applied may exceed requirements, because of either
the limitations of the method or the unwillingness of farmers to strictly adhere to the
advice provided. The determination of soil mineral nitrogen often takes place in the
autumn; although the long time lag between this sampling and the period of highest
N demand can generate errors in estimating fertiliser requirements (Paschold et al.
2001) it can also provide a useful measure of the N potentially available for leaching
following harvest of the previous crop. Improved systems (e.g. KNS, Nitrogen
Balance System) which account for the Nmin level through the growing season, still
sometimes overestimates the crop demand and requires large amounts of soil analysis
and careful fertiliser management, which may result in a less user-friendly solution
for the farmer. However, a similar approach in the USA (pre-side dressing nitrate test
[PSNT]) seems capable of equivalent or better results by only measuring soil nitrate
in the top 30 cm of soil just before the application (Hartz 2003). Those methodologies
could be greatly improved if coupled with models specifically developed for vegetable crops, accounting for the potential N losses during the season as a function of
weather conditions (EU_Rotate_N project newsletter 2003), which is definitely the
most unpredictable factor involved (Paschold et al. 2001).
A completely different approach that avoids the use of models and can be an
improved ‘rule of thumb’ for farmers to top-dress crops is the so-called Nil-N-plot
system, based on the concept of ‘unfertilised windows’. A 2-year test on 12 different vegetable fields in Germany (Weier et al. 2001) showed great differences due to
the use of the Nmin system. The suggested application rates were from 20% lower
to 10% higher than those calculated as a function of the amount of mineral N at the
start of the season, but no yield decrease was recorded. This method may be a simpler way to take account of the effect of nitrogen released from crop residues during
the growing season without the use of expensive soil analysis or complex mechanistic models, although soil mineral nitrogen testing certainly still retains value in
situations where levels are expected to be high (e.g. in fields with a manure/slurry
history, of fields following legumes, potatoes, etc.).
In the last 3 years, a worldwide network of researchers, mainly based in
Germany and Quebec, have developed a set of recommendations to improve the
N-balance approach as a main tool for controlling N leaching. The result of their
efforts has been synthesised in a guide to sustainable nitrogen management in fruit
and vegetable crops which is published on-line and has been designed to be updated
to ensure continued relevance (Owen et al. 2003).
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
185
In the Netherlands, a group of regulations has been set up to support implementation
of the Nitrates Directive and to consider the need to reduce ammonia emissions
from agriculture. The main measure to reduce nitrate leaching is a ban on the spreading of animal manure, and to keep overall control of the nutrient input in agricultural systems, levies have been designed linked to annual surpluses of nitrogen and
phosphorus (Neeteson et al. 2003). This system, originally known as the MINAS or
MINerals Accounting System, was introduced in the 1998 with the aim to cut down
in 5 years the allowable N surplus in grassland from 300 to 180 kg N ha−1 and in
arable land from 175 to 100 kg N ha−1; in case of over-surplus, a levy is required of
€2.3 kg−1 of nitrogen and €9 kg−1 of phosphate.
However, the system’s compatibility with the Nitrates Directive was overestimated and the system was challenged by the EC. Several technical differences in
nutrient balance persisted between MINAS and the Nitrates Directive: nutrient
balance in the Nitrates Directive was fixed ahead of the crop cycle, in MINAS is
calculated instead immediately before the grown season with the nutrient supplies from soil, crop residues, animal manure, atmosphere and biological N2 fixation accurately estimated; however, the nutrient from manure generated in farm
was not explicitly accounted. The system has been updated several times, but
eventually was found to be incompatible with the Nitrates Directive and was
ultimately closed in 2005.
To test the effect of these policies, a joint project (‘Telen met toekomst’ or
‘Farming with a future’) on four experimental farms and 33 commercial ones
(where land management was based on the initial results from the experimental
units) was established. Two main systems were tested: one, ‘economically feasible’, where nitrogen was applied according to measurements carried out by the
NBS Dutch scheme, and second, ‘environmentally desirable’, where the nitrogen
application was carried out with strategy tailored to the different farms with the
aim of cutting down nitrogen inputs. The project also accounts for phosphorus
inputs. The main aim was to explore if it was possible for commercial farming to
reduce inputs over a 5-year period without a significant decrease in farm income
(Neeteson et al. 2001). The overall results reported so far vary greatly between
crop types and locations. However, the nitrogen surplus was still much higher than
the target of 100 kg N ha−1 in both systems. Even if the project continued into
2005, evidence reviewed so far suggests that decreasing nitrogen inputs in isolation is not sufficient to reduce N inputs to this target value, but this needs to be
combined with site-specific management initiatives (e.g. timing, placement, variety) to help increase the nitrogen-use efficiency, even if these actions cause an
increase in costs (Van Dijk and Smit 2006, Smit et al. 2005). The nitrogen inputs
on the farms under the ‘economically feasible’ system were higher than the recommendations due to incomplete account of the nitrogen added in organic manures;
the decrease in manure applications was also compensated by a slight increase in
chemical N to avoid a yield penalty. However, the complete cessation of organic
manure applications without replacing with fertiliser under the environmentally
feasible system had no effect on yield. Under both the schemes low phosphorus
inputs were applied and no yield reduction occurred.
186
F. Agostini et al.
Results from trials in leek fields (Neeteson et al. 2003) showed how operating
under an ‘environmentally desirable’ management scenario induced a soil mineral
nitrogen reduction of around 50% without any notable yield loss. However, the
system used in this case to limit the N input was a fertigation scheme which cost
about €1,000 ha−1 more than the classical Nutrient Balance scheme. Further investigations (Radersma et al. 2005) also found that N-crop quick tests were more
effective than N-soil quick tests for managing N split application in crop and
decreasing N leaching.
6.7.5 Final Considerations
The technical impact of the most recent research on N management in fruit and
vegetable production systems has been reviewed in relation to the implementation
of the Nitrates Directive in some EU states. The state of knowledge in management
practices is generally fairly advanced and there are tested methodologies supported
by published data which allow a more sustainable horticultural sector without
decreases in yield or quality. However, although there is still scope to refine and
improve the technologies, the major challenge is disseminating results to farmers
and farm advisers and promoting changes in farm management practices that minimise the risk of diffuse pollution from vegetable production systems.
Some issues, such as nitrate concentrations in surface water systems used for
irrigation, are increasingly becoming an environmental pollution risk (e.g. in Spain
and Italy, Padana valley). Measures such as more widespread use of drip irrigation
systems have become more widely applied at field level over the past few years
through the broader adoption of advanced technologies, which are more efficient in
terms of water use. Other measures have had more limited success, including the
farm-scale use of software tools (Decision Support Systems, DSS), the use of regular soil nutrient analyses, and the use of nitrogen probes and sensors.
In all the countries investigated, the farmers have rarely taken into account the
suggestions evolving from the latest research, and they often continue to over-fertilise
at levels between 20% (Italy, France) and 200% (Spain) above recommended levels.
The high irrigation input required by some crops makes this behaviour increasingly
dangerous for the environment. This is the case for crop systems such as tomatoes,
strawberry in protected systems; aubergine, pepper and lettuce in open fields and
citrus trees in Spain where immersion irrigation is still in use. In the case of open
field crops in North France and North Italy, specific tests to measure N status in
certain crops and the associated crop N requirement are still missing (cauliflower,
carrots, cabbage, Brussels sprouts, spinach, onion). Simpler approaches to calculating N balances and N requirements, which may include soil mineral nitrogen testing, are still not as widely used as they could be to help estimate crop N requirements
more accurately in these high-residue situations. The amount of leaching from
vegetables crops varies greatly across the countries reviewed. For example, glasshouse tomatoes in south France can leach up to 1,000 kg N ha−1 (Le Bot et al. 2001).
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
187
Although leaching is much less from similar systems in south and central Italy, it
is still sufficient to contribute to nitrate levels in water tables fluctuating from 50 to
300 mg l−1 (V Magnifico, personal communication). The evidence reviewed suggests that open field vegetable crops in southern Europe can leach 100–300 kg N
ha−1 year−1 from the soil root zone towards groundwaters depending on the soil,
precipitation, irrigation, and management factors.
6.8 Conclusion
This review has described advances in N management to reduce nitrate leaching
applied to vegetable production and their effective application. Areas of research
where further investigations are required have been recognised such as (i) relation
between crop residues and following crop management, (ii) prediction of the net
effect of the different components of the soil N cycle on the soil-plant system, (iii)
farmers’ perception of N leaching as monetary loss, (iv) creation of spatial statistical maps of soil mineral nitrogen, (v) relation between N plant status and N plant
effective demand.
Current research in nitrogen management aims to design the most effective
N-fertiliser management systems that are able to produce a profitable and highquality yield together with a more sustainable environmental ‘footprint’. This
research combines investigations on nitrogen soil dynamic and its use by crops,
focusing on understanding the merits of alternative methods, tailored to each crop,
climate and soil, for assessing (i) the effective plant N requirement; (ii) the soil
availability of N which the plant roots can access; (iii) the associated losses, mainly
due to nitrate leaching, which can be particularly high in field vegetable crops
where irrigation is required. This fundamental research is currently leading to
sophisticated technical solutions such as (i) innovative measurement instrumentations and methods, (ii) computerised tools for management and simulation of ‘if
then’ scenarios, (iii) new crop-management systems. However, these advances are
not always implemented by farmers at the scale required to produce an effective and
lasting impact on the environment. The proper N budget, which all these techniques
allow, implies an increase of available data from local datasets, whose realisation is
demanding in terms of time and finance. The empirical approaches are generally
still preferred because they can be more reliable for specific local conditions when
detailed data are missing. Moreover, some tools (the so-called decision support
systems) are generally not sufficiently user-friendly for farmers; they have been
designed for farm advisers and agronomists, who are professionally qualified to
choose from the large number of available techniques and methods and interpolate
their results using their own experience tailored to specific regional conditions.
Recent advances in agronomy such as improved irrigation timing schemes, localisation of fertiliser applications in time and space and the combination of these elements in fertigation schemes where a crop calibration frequency is a key point all
appear effective for decreasing N leaching without yield losses. In some specific
188
F. Agostini et al.
cases, the use of slow-release fertilisers or nitrification inhibitors have also yielded
encouraging results, but their more widespread use is difficult to generalise. In many
cases, other more classic agronomical methods such as catch crops, mulching and
intercropping that are unappealing for conventional farming due to the increased
input of time and resources needed can be considered when the higher value of yield
can justify the increased inputs as occur sometime in organic farming.
Finally, it must be noted that there is a natural limit on our ability to minimise
nitrate leaching, which is governed by plant physiology, soil characteristics and
weather conditions; even with the most advanced cultural tools a sustainable but
still profitable management of field vegetable is not always within reach and so the
only option left can be a land use different from vegetable crop.
Acknowledgements The authors thank the following researchers for useful suggestions and
valuable information on several aspects of the topic reported in this review: Professor P Sequi and
Dr. A. Benedetti, CRA-Centro di Ricerca per lo Studio delle Relazioni tra Pianta e Suolo, ISNP,
Roma, Italy; Dr.M. Pagliai, Centro di ricerca per l’agrobiologia e la Pedologia, ISSDS, Firenze,
Italy; Dr. M. Mastrorilli, Istituto Sperimentale Agronomico, ISA, Bari; Dr. A. Rosati, CRA-Centro
di ricerca per l’olivicoltura e l’industria olearia, Spoleto, Italy; Dr. V. Magnifico, CRA-Centro
Ricerca per l’Orticultura, Pontecagnano, Italy; Dr. Jose Antonio Diez Lopez, Centro de Ciencias
Mediambientales (CSIC) Departamento de Contaminacion ambiental. Control de la contaminacion nitrogenada, Madrid, Spain; Frances Domingo, Instituto de Investigacion y Tecnologia
Agraroalimentaria (IRTA) Estacion Experimental Mas Badia, Gerona, Spain; Dr. Carlos Ramos
Monpo, Instituto Valenciano de Investigaciones Agrarias (IVIA), Valencia, Spain; Dr. Rod
Thompson, Depto. Producion Vegetal, Universidad de Almeria, Spain; Dr. C. Gary, CIRAD
Montpellier, France; Dr. J. Le Bot and Dr. Stéphane Bellon, INRA Avignon, France; Dr. Paul
Robin, INRA-ENSAM, Montpellier, France; C. Reynal, CTIFL, France.
References
AA.VV (2006) Acta Hortic 700
Agostini F, Scholefield P (2005). Simulation of carbon and nitrogen in the soil after straw incorporation. Ital J Agron (8) 2:63–71
Andrasky TW, Bundy LG (1999) Nitrogen cycling in crop residues and cover crops on an irrigated
sandy soil. Agron Abstr 1999, 224
Anthony S, Chadwick D, Granger S, Haygart P, Harris D (2005) Cost-cube: a measure centric
model for characterization of diffuse pollution. In: Schroder JJ, Neeteson JJ (eds) N
Management in agrosystems in relation to the Water Frame Directive, Proceedings of 14th N
workshop, 2005, Maastricht, The Netherlands, pp 7–11
Arregui LM, Lasa B, Lafarga A, Iraeta I, Baroja E, Quemada M (2006) Evaluation of chlorophyll
meters as tools for N fertilization in winter wheat under humid Mediterranean conditions. Eur
J Agron 24:140–148
Aveline A, Guichard L (2005) Comparing indicators of nitrate leaching in various cropping systems. In: Schroder JJ, Neeteson JJ (eds) N Management in agro-systems in relation to the
Water Frame Directive. Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands,
pp 64–67
Bailey RJ, Spackman E (1996) A model for estimating soil moisture changes as an aid to irrigation
scheduling and crop water use studies. I. Operational details and description. Soil Use Manage
12:122–128
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
189
Bardossy A, Haberlandt U, Krysanova V (2003) Automatic fuzzy-rule assessment and its application
to the modelling of nitrogen leaching for large regions. Soft Comput 6:370–385
Barret JH, Parslow RC, McKinney PA, Law GR, Forman D (1998) Nitrate in drinking water and
incidence of gastric, esophageal, and brain cancer in Yorkshire, England. Cancer Cause
Control 9:153–159
Bar-Yosef B, Sagiv B (1982) Response of tomatoes to N and water applied via trickle irrigation
system. Nitrogen Agron J 74:633–637
Battilani A (2006) Water and nitrogen use efficiency, dry matter accumulation and nitrogen uptake
in fertigated processing tomato. Acta Hortic 724:67–74
Battilani A, Solimando D (2006) Yield, quality and nitrogen use efficiency of fertigated watermelon. Acta Hortic 700:85–90
Battilani A, Bussieres P, Dumas Y (2003) FERTIRRIGERE: a simple tool-model for managing
water and nutrient supply in drip-irrigated processing tomatoes. Acta Hortic 613:155–158
Battilani A (2001) Calcolare correttamente la fertirrigazione con il minimo input. Inf Agrario
57:35–42
Battilani A, Fereres E (1999) The use of decision support systems to manage fertigation and to
minimize enviromental effects: a challange for the future. Acta Hortic 487:547–555
Baumann DT, Bastiaans L, Kropff MJ (2003) Analysis and design of a leek-celery intercropping
system using mechanistic and descriptive models. Acta Hortic 638:59–68
Baumgarten A (2006) Evaluation of field methods for the assessment of soil Nmin–content. Acta
Hortic 700:205–209
Belanger G, Ziadi N, Walsh JR, Richards JE, Milburn PH (2003) Residual soil nitrate after potato
harvest. J Environ Qual 32:607–612
Bending GD, Turner MK (1999) Interaction of biochemical quality and particle size of crop residues and its effect on the microbial biomass and nitrogen dynamics following incorporation
into soil. Biol Fertil Soils 29:319–327
Bending GD, Turner MK, Burns IG (1998) Fate of nitrogen from crop residues as affected by
biochemical quality and the microbial biomass. Soil Biol Biochem 30:2055–2065
Benincasa P, Boldrini A, Tei F, Guiducci M (2004) N release from several green manure crops.
Proceedings of the VIII ESA Congress, Copenhagen, Denmark, 11–15 July 2004, pp
971–972
Bertschinger L (2004) Making sustainability an issue in applied horticultural research. Acta Hortic
638:17–22
Bianco VV (1990) Environment, agricultural practices and quality of vegetable crops. Riv di
Agron 24(2/3):81–131
Bjorneberg DL, Westermann DT, Aase JK (2002) Nutrient losses in surface irrigation runoff.
J Soil Water Conserv 57:524–529
Boatto V, Pilati L, Defrancesco E, Galletto L (1996) Implicazioni economiche delle politiche di
contenimento della fertilizzazione: il caso del Bacino del Meolo. Agric Ric 164:163–180
Boldrini A, Guiducci M, Benincasa P, Tosti G, Tei F (2006) Can we modulate N supply and
release from green manure crops? Proceedings of the IX ESA (European Society for
Agronomy) Congress, 4–7 Sept 2006, Warszawa, Poland, pp 371–372
Borgensen CD, Heidmeann T, Jorgense U (2005) Sensitivity of using different soil type representations for field and regional simulation of N leaching. In: Schroder JJ, Neeteson JJ (eds) N
Management in Agrosystems in relation to the Water Frame Directive. Proceedings of 14th N
Workshop, 2005, Maastricht, The Netherlands
Bravdo BA (2003) Crop improvement and production strategies in arid environments: salt,
drought and heat stress. Acta Hortic 618:255–265
Burns IG (2006) Assessing N fertiliser requirements and the reliability of different recommendation systems. Acta Hortic 700:35–48
Burns IG, Rahn CR, Greenwood DJ, Draycott A, Richardson AS (1997) A user-friendly decision
support system for adjusting N fertiliser requirements to local conditions. Managing soil fertility for intensive vegetable production systems in Asia. Proceedings of an international conference, AVRDC, Taiwan, 4–10 November, 1996, pp 314–324
190
F. Agostini et al.
Burns IG (1976) Equations to predict the leaching of nitrate uniformly incorporated to a known
depth or uniformitly distributed throughout a soil profile. J Agric Sci (Cambridge) 86:305–313
Campiglia E, Caporali F, Paolini R, Mancinelli R (2005) Ruolo delle leguminose annuali autoriseminanti nei sistemi colturali biologici in ambiente mediterraneo. In: Cicia G et al (eds)
L’agricoltura biologica fuori dalla nicchia. Edizioni Scientifiche Italiane, Napoli
Cantarella H, Mattos D, Quaggio J, Rigolin A (2003) Fruit yield of Valecnia sweet orange with
different N sources and the loss of applied N. Nutr Cycl Agroecosyst 67:215–233
Cantor KP (1997) Drinking water and cancer. Cancer Cause Control 8:292–208
Cape J, Anderson M, Rowland A, Wilson D (2004) Organic nitrogen in precipitation across the
United Kingdom. Water Air Soil Pollut: Focus 4:25–35
CEC (1991) Council directive of 12th December 1991 concerning the protection of waters against
pollution caused by nitrates from agricultural sources (91/676/EEC). Off J Eur Commun 30
Dec 1991, L135/1–8
Chaves B, Mateu PL, De Neve S, Hofman G, Van Cleemput O (2006) Conserving N from high N
crop residues under field conditions by using on- and off-farm organic biological waste materials. Acta Horticul 700:255–261
Coccato M, Di Luzio M (1996) Applicazioni di un modello idrologico distribuito per il controllo
dell’inquinamento agricolo di origine diffusa: il caso del Bacino del Meolo. Agricult Ric
164:181–191
Colla G, Battistelli A, Moscatello S, Proietti S, Casa R, Lo CB, Leoni C (2001) Effects of reduced
irrigation and nitrogen fertigation rate on yield, carbohydrate accumulation and quality of
processing tomatoes. Acta Hortic 542:187–196
Collins AL, Strőmqvist J, Davison PS, Lord EI (2007) Appraisal of phosphorus and sediment
transfer in three pilot areas identified for the catchment sensitive farming initiative in England:
application of the prototype PSYCHIC model. Soil Use Manage 23(Suppl 1):117–132
Coltman RR (1987) Sampling consideration for nitrate quick test of greenhouse tomatoes. J Am
Soc Hortic Sci 112:922–927
Cook WP, Sanders DC (1991) Nitrogen application frequency for drip irrigated tomatoes.
HortScience 26:250–252
Costigan PA (1988) The placement of starter fertilizers to improve the early growth of drilled and
transplanted vegetables. Proc Fertil Soc 274:1–24
Coulombe J, Villeneuve S, Belec C, Tremblay N (1999) Evaluation of soil and petiole sap nitrate
quick tests for broccoli in Quebec. Acta Hortic 506:147–152
CRPV-RER (2007) Disciplinari di Produzione Integrata 2007. (ed. Centro Ricerche Produzioni
Vegetali – Regione Emilia Romagna). Bologna, Italy; http://www.crpv.it/; Access date 3/03/2007.
Curtois P, Destain P, Renardad S, Cuvelier M (2005) Field scale N-management: soil and plant
diagnostic tools applied within the agricultural Surface Survey (Belgium). In: Schroder JJ,
Neeteson JJ (eds) N Management in agrosystems in relation to the Water Frame Directive.
Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands, pp 257–261.
Dachler M (2001) Sampling and analytical methods for the determination of available soil nitrogen in Australia. Acta Hortic 506:239–245
Dalvi VB, Tiwari KN, Pawade MN, Phirke PS (1999) Response surface analysis of tomato production under microirrigation. Agric Water Manage 41:11–19
Davies DB (2000) The nitrate issue in England and Wales. Soil Use Manage 16:142–144
Davison PS, Withers PJA, Lord EI, Betson MJ, Strömqvist J (2008) PSYCHIC – A process-based
model of phosphorus and sediment mobilisation and delivery within agricultural catchments.
Part 1: Model description and parameterisation. J Hydrol 350 (3–4):290–302
De Luca S, Fagnano M, Quaglietta-Chiaranda F (2006) The effect of organic fertilization on yields
of tomato crops in the Sele River Plain. Acta Hortic 700:103–106
De Neve S, Van Desteene J, Hartmann R, Hofmann G (1999) N mineralisation and soil solution
electrical conductivity changes: on line monitoring of the mineralisation process using TDR.
Proceedings of the 10th nitrogen workshop, Copenhagen, Denmark, 2, pp 122–125.
De Neve S, Hofmann G (2001) Time domain reflectometry for monitoring soil nitrogen dynamics.
Acta Hortic 506:233–238
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
191
De Neve S, Pannier J, Hofmann G (1994) Fractionation of vegetable crop residues in relation to
in situ N mineralization. Eur J Agron 3:267–272
De Paz JM, Ramos C (2002) Linkage of a geographical information system with the GLEAMS
model to assess nitrate leaching in agricultural areas. Environ Pollut 118:249–258
De Paz JM, Ramos C (2001) The Use of a GIS_N model system to assess nitrate leaching in
agricultural areas. Acta Hortic 506:225–229
De Tourdonnet S, Meynard JM, La Folie F, Roger-Estrade J, Lagier J, Sebillotte M (2001) Nonuniformity of environmental conditions in greenhouse lettuce production increases the risk of
N pollution and lower product quality. Agronomie 21:297–309
De Walle FB, Sevenster J (1998) Agriculture and environment: minerals, manure and measures.
Kluwer, Dordrecht, The Netherlands, 21 pp
Delgado JA, Shaffer MJ, Hu C, Lavado RS, Cueto WJ, Joose P, Li X, Rimski KH, Follet R, Colon
W, Sotomayor D (2006) A decade of change in nutrient management: a new nitrogen index.
J Soil Water Conserv 61:71
Delgado JA, Follet R (1998) Sap test to determine nitrate–nitrogen concentrations in aboveground
biomass of winter cover crops. Commun Soil Sci Plant Anal 29:545–559
Drost D, Koeing R (2001) Improving onion productivity and N use efficiency with a polymer
coated nitrogen source. Western Management Conferences, Salt Lake City, UT
Dumoulin J, Le Bot J, Mounier A, Fevre P (2002a) Azote du melon, la pratique du pilotage. Info
CTIFL 185:45–48
Dumoulin J, Le Bot J, Mounier A, Fevre P (2002b) Azote du melon, de la recherche à la pratique.
Info CTIFL 184:48–53
Ebrahim MKH, Aly MM (2005) Physiological Response of Wheat to Foliar Application of Zinc
and Inoculation with some Bacterial Fertilizers. J Plant Nutrition 27:1859–1874. DOI:
10.1081/PLN-200026442
Erdal I, Ertek A, Senyigit U, Koyuncu MA (2007) Combined effects of irrigation and nitrogen on
some quality parameters of processing tomato. World J Agric Sci 3:57–62
Errebhi M, Rosen CJ, Birong DE (1998) Calibration of a petiole sap nitrate test for irrigated
“Russet Burbank” potato. Commun Soil Sci Plant Anal 29:23–35
European Commission (1999) Agriculture, environment, rural development: facts and figures – a
challance for agriculture. Office for official publications of the European communities,
Luxembourg
European Commission (1998) The implementation of council directive 91/676/EEC concerning
the protection of waters against pollution caused by nitrates from agricultural sources. Office
for official publications of the European communities, Luxembourg
FAO Land and Plant Nutrition Management Service FAO (2000) http:// www.fao.org/waicent/
faoinfo/agricult/agl/agll/oldocsl.asp. Accessed 10/0972007 August 2009
Fagnano M, Merola G, De Luca S, Mori M, Zena A, Caputo R, Quaglietta Chiarandà F (2005)
Ricerche Agronomiche per Sistemi Colturali Sostenibili in Italia Meridionale. In: Cicia G et al
(eds) L’agricoltura biologica fuori dalla nicchia. Edizioni Scientifiche Italiane, Napoli
Farneselli M (2008) Improving fertigation management in processing tomato. Doctoral Thesis,
University of Perugia, Italy, 174 pp
Farneselli M, Studstill DW, Simonne EH, Hochmuth RC, Hochmuth GJ, Tei F (2008). Depth and
width of the wetted zone in a sandy soil after leaching drip-irrigation events and implications
for nitrate-load calculation. Commun Soil Sci Plant Anal 39 (7&8)
Farneselli M, Benincasa P, Guiducci M, Tei F (2007a) Validazione di metodi di misura dello stato
nutrizionale azotato del pomodoro da industria. Italus Hortus 14:154
Farneselli M, Benincasa P, Guiducci M, Tei F (2007b) Fertigation-irrigation frequency in processing tomato: effect on plant growth, N uptake and N leaching. Proceedings of 15th N Workshop
“Towards a better efficiency in N use”, Lleida, Spain, 28–30 May 2007, pp 179–184
Farneselli M, Simonne E, Studstill D, Tei F (2006a) Washing and/or cutting petioles reduces
nitrate nitrogen and potassium sap concentrations in vegetables. J Plant Nutr 29:1975–1982
Farneselli M, Studstill DW, Simonne EH, Hochmuth B (2006b) Depth and width of the wetted
zone after leaching irrigations on a sandy soil. HortScience 41:508
192
F. Agostini et al.
Feller C, Fink M (2002) Nmin target values for field vegetables. Acta Hortic 571:195–201
Fink M, Scharpf HC (1992) Dünger-Dosierung im Freiland-Gemüsebau, Entscheidung
sunterstützung durch; N-Expert“. Dtsch Gartenbau 46:1688–1690
Francavigli R, Benedetti A (1995) The Italian project PANDA for sustainable agriculture and
protection of the environment. Hrvat Vode 3(12):289–292
Frankenberger WT Jr, Abdelmagid HM (1985) Kinetic parameters of nitrogen mineralization rates
of leguminous crops incorporated into soil. Plant Soil 87:257–271
Gallardo M, Thompson RB, Lopez-Toral JR, Fernandez MD, Granados R (2006) Effect of applied
N concentration in a fertigated vegetable crop on soil solution nitrate and nitrate leaching loss.
Acta Hortic 700:227–230
Garnier P, Neel C, Aita C, Recous S, Lafolie F, Mary B (2003) Modelling carbon and nitrogen
dynamics in a bare soil with and without straw incorporation. Eur J Soil Sci 54:555–568
Gary C (2003) Evaluation design and control of sustainable horticultural cropping systems. Acta
Hortic 638:45–51
Gastal F, Lemaire G (2002) N uptake and distribution in crops: an agronomical and ecophysiological perspective. J Exp Bot 53:789–799
German-Heins J, Flury J (2000) Sorption of brilliant blue FCF in soils as affected by PH and ionic
strength. Geoderma 97:87–101
Gianquinto G, Sambo P, Borsato D (2006) Determination of SPAD threshold values in order to
optimise the nitrogen supply in processing tomato. Acta Hortic 700:159–166
Gianquinto G, Sambo P, Bona A (2003) The use of SPAD-502 CHLOROPHYLL METER for
dynamically optimising the nitrogen supply in potato crop: a methodological approach. Acta
Hortic 627:217–224
Giller KE, Cadisch G (1997) Driven by nature: a sense of arrival or departure. In: Cadisch G,
Giller KE (eds) Driven by nature. Plant litter quality and decomposition. CAB International,
Wallingford, UK, pp 393–399
Gimenez C, Parra M, Diaz M (2001) Characterization of current management practices with
high risk of nitrate contamination in agricultural areas of Southern Spain. Acta Hortic
506:73–80
Goodlass G, Rahn CR, Shephered MA, Chalmers AG, Seeney FM (1997) The nitrogen requirement of vegetables; comparison of yield response models and recommendation systems.
J Hortic Sci 72:239–254
Goulding K (2000) Nitrate leaching from arable and horticultural land. Soil Use Manage
16:145–151
Greenwood DJ, Verstraeten LMJ, Draycott A, Shutherland RA (1987) Response of winter wheat
to N-fertilizer:dynamic model. Fertiliz Res 12:139–156
Greenwood DJ, Kubo K, Burns IG, Draycott A (1989) Apparent recovery of fertilizer N by vegetable crops. Soil Sci Plant Nutr 35(3):367–381
Greenwood DJ, Lemaire G, Gosse G, Cruz P, Draycott A, Neeteson JJ (1990) Decline in percentage N of C3 and C4 crops with increasing plant mass. Ann Bot 66:425–436
Greenwood DJ (1990) Production and productivity: the nitrate problem? Ann Appl Biol
117:209–231
Greenwood DJ, Neeteson JJ (1992) High yield nutrient management systems and environmental
constraints: the world scene. In: Scaife A (ed) Proceedings of the 2nd European Society for
Agronomy Congress, Warwick, UK, pp 386–397
Greenwood DJ, Rahn C, Draycott A, Vaidyanatha LV, Paterson C (1996) Modelling and measurement of the effects of fertilizer-N and crop residue incorporation on N-dynamics in vegetable
cropping. Soil Use Manage 12:13–24
Grignani C, Zavattaro L (2000) A survey on actual agricultural practices and their effects on the
mineral nitrogen concentration of the soil solution. Eur J Agron 12:251–268
Guerette V, Belec C, Tremblay N, Weier U, Scharpf H C (2000) N contribution from mineralization of vegetable crop residues. International society of horticultural sciences workshop
“Toward an ecologically sound fertilization in field vegetable production,” 11–13 Sept 2000,
Wageningen, The Netherlands
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
193
Guiducci M, Bonciarelli U, Stagnari F, Benincasa P (2004) Total N supply and profit from several
green manure crops. VIII Congress of the European Society of Agronomy, 11–15 July 2004,
Copenhagen, DK
Haberlandt U, Krysanova V, Bardossy A (2002) Assessment of nitrogen leaching from arable land
in large river basins: Part II: Regionalisation using fuzzy rule based modelling. Ecol Model
150:277–294
Harrison R, Silgram M (1998). Final report to UK Ministry of Agriculture Fisheries and Food
(MAFF) on project NT1508 (cover crops). Includes Appendix: the mineralisation of nitrogen
in cover crops – a review
Hartz TK, Bendixen WE, Wierdsma L (2000) The value of presidedress soil nitrate testing as a
nitrogen management tool in irrigated vegetables production. HortScience 35:651–656
Hartz TK (2003) The assessment of soil and crop nutrient status in the development of efficient
fertilizer recommendations. Acta Hortic 627:231–240
Health Canada (1996) Guidelines for canadian drinking water quality (ed. Canadian Government
Publisher). Canadian Government Publisher, Ottawa.
Hebbar SS, Ramachandrappa BK, Nanjappa HV, Prabhakar M (2004) Studies on NKP drip fertigation in field grown tomato (Lycopersicon esculentum Mill.). Eur J Agron 21:117–127
Heeb A (2005) Nitrogen form affects yield and taste of tomatoes. J Sci Food Agric 85:1409–1414
Heffer P (2008) Assessment of fertilizer use by crop at the global level. International Fertilizer
Industry Association, Paris, France, 6 pp
Herencia JF (2007) Comparison between organic and mineral fertilization for soil fertility levels,
crop macronutrient concentrations, and yield. Agron J 99:973–983
Hochmuth GJ (1992) Concepts and practices for improving nitrogen management for vegetables.
HortTechnology 2:121–125
Hoel BO (2003) Chlorophyll meter readings in winter wheat: cultivar differences and prediction
of grain protein content. Acta-Agric Scand Sect B, Soil Plant Sci 524:147–157
Hoffmann M, Johnsson H (1999) A method for assessing generalised nitrogen leaching estimates
for agricultural land. Environ Model Assess 4:35–44
Huffman EC, Yang JY, Gameda S, de Jong R (2001) Using simulation and budget models to scaleup nitrogen leaching from field to region in Canada. Sci World 1:699–706
Jabro DJ, Jemison JM, Fox RH, Frittion DD (1994) Predicting bromide leaching under field conditions using SLIM and MACRO. Soil Sci 157:215–223
Janat M (2004) Assessment of nitrogen content, uptake, partitioning and recovery by cotton crop
grown under surface irrigation and drip fertigation by using isotopic technique. Commun Soil
Sci Plant Anal 35:2515–2535
Janzen HH, Kucey RMN (1988) C, N, and S mineralization of crop residues as influenced by crop
species and nutrient regime. Plant Soil 106:35–41
Jimenez S, Ales JI, Lao MT, Plaza B, Perez M (2006) Evaluation of nitrate quick tests to improve
fertigation management. Commun Soil Sci Plant Anal 37:2461–2469
Jin Il Cheong (1996) Effects of slow-release fertilizer application on rice grain quality at different
culture methods Korean-Journal-of-Crop-Science 41(3), 286–294
Jones RD, Schwab AP (1993) Nitrate leaching and nitrite occurrence in a fine-texured soil. Soil
Sci 4:272–282
Justus M, Kopke U (1995) Strategies to reduce nitrogen losses via leaching and to increase precrop effects when growing faba beans, nitrogen leaching in ecological agriculture. Proceedings
of an international workshop, Royal Veterinary and Agricultural University, Copenhagen,
Denmark, pp 145–155
Karaman MR, Saltali K, Ersahin S, Gulec H, Derici MR (2005) Modelling nitrogen uptake and
potential nitrate leaching under different irrigation programs in nitrogen-fertilized tomato
using the computer program NLEAP. Environ Monit Assess 101:249–259
Karitonas R (2003) Development of a nitrogen management tool for broccoli. Acta Hortic
627:125–129
Kerft A, Zuber A (1978) On the physical meaning of the dispersion equation and its solutions for
different initial bounary conditions. Chem Eng Sci 33:1471–1480
194
F. Agostini et al.
Khah EM (2003) Effect of fertilizers on lettuce (Lactuca sativa) yield, physical and organoleptic
properties. Adv Hortic Sci 17(1):47–57
Knox E, Moody DW (1991) Influence of hydrology, soil proprieties and agricultural land use on
nitrogen in groundwater. Soil Sci Soc Am J 6:77
Kraft GJ, Stites W (2003) Nitrate impacts on groundwater from irrigated-vegetable systems in a
humid north-central US sand plain, Agriculture. Ecosyst Environ 100:63–74
Krishnapillai M, Sri Ranjan R (2009) Non-destructive monitoring of nitrate concentration in a laboratory flow experiment using time domain reflectometry (TDR). Environ Technol 30(1):101–109
Kristensen HL, Thorup-Kristensen K (2004) Root growth and nitrate uptake of three different
catch crops in deep soil layers. Soil Sci Soc Am J 68:529–537
Kucke M, Kleeberg P (1997) Nitrogen balance and soil nitrogen dynamics in two areas with different soil, climatic and cropping conditions. Eur J Agron 6:89–100
Le Bot J, Jeanniquin B, Fabre R (2001) Impacts of N-deprivation on the yield and nitrogen budget
of rockwool grown tomatoes. Agronomie 21:341–350
Le Bot J, Adamowicz S, Robin P (1998) Modelling plant nutrition of horticultural crops: a review.
Sci Hortic 74:47–82
Lemaire G (2008) Diagnostic tool (s) for plant and crop N status. In vegetative stage. Theory and
practice for crop N management. Eur J Agron 28:614–624
Lemaire G, Gastal F (1997) N uptake and distribution in plant canopies. Diagnosis of nitrogen status
in crops. In: Lemaire G (ed) Diagnosis of nitrogen status in crops. Springer, Berlin, pp 3–41
Li Z (2003) Use of surfactant-modified zeolite as fertilizer carriers to control nitrate release.
Microporous and Mesoporous Material 61:181–188
Li J, Zhang J, Rao M (2004) Wetting pattern and nitrogen distributions as affected by fertigation
strategies from a surface point source. Agric Water Manage 67:89–104
Li J, Hu C, Delgado JA, Zhang Y, Ouyang Z (2007) Increasing nitrogen use efficiencies as a key
mitigation alternative to reduce nitrate leaching in North China Plain. Agric Water Manage
89:137–147
Lilburne L, Web T (2002) Effect of soil variability, within and between soil taxonomic units, on simulated nitrate leaching under arable farming. Australian Journal of Soil Research 40:1187–1199
Linaje A, Munoz-Guerra L, Carrasco I (2005) Evaluation of the use of nitrification inhibitor
DMPP on the risk of nitrate leaching in different crop system in Spain. In: Schroder JJ,
Neeteson JJ (eds) N Management in Agrosystems in relation to the Water Frame Directive.
Proceedings of 14th N Workshop, 2005, Maastricht, The Netherlands, pp 149–152
Locascio SJL, Smajstrla AG (1995) Fertilizer timing and pan evaporation scheduling for drip
irrigated tomato. In: Lamm FR (ed) Microirrigation for a changing world: conserving
resources/preserving the environment 4-95. ASAE, Los Angeles, CA, pp 175–180
Lord EI, Mitchell RD (1998) Effect of nitrogen inputs to cereals on nitrate leaching from sandy
soils. Effect of nitrogen inputs to cereals on nitrate leaching from sandy soils. Soil Use Manage
14(2):78–83
Lord EI, Johnson PA, Archer JR (1999) Nitrate sensitive areas: a study of large scale control of
nitrate loss in England. Soil Use Manage 15:201–207
Lord EI, Anthony S (2000) MAGPIE: a modelling framework for evaluating nitrate losses at
national and catchment scales. Soil Use Manage 16:167–174
Lord EI, Shepherd M, Silgram M, Goodlass G, Gooday R, Anthony A, Davison P, Hodgkinson R
(2007). Investigating the effectiveness of NVZ Action Programme measures: development of
a strategy for England. Final report for UK Defra project NIT18. 116pp + 11 Appendices.
http://www.defra.gov.uk
Lorenz HP, Schaghecken J, Engl G, Maync A, Zegler J (1989) Ordnungsgemäbe StikstoffVersorgung im Freiland – Gem_sebau - KNS system. Rheinland Pfhalz: Ministerium fur
Landwritschaf, Weinbau und Forsten ISSN 0931-9026 1089391-3000
Lorenz OA, Tyler KB (2007) Plant tissue analysis of vegetable crops. vric.ucdavis.edu/veginfo/
topics/fertilizer/tissueanalysis.pdf Accessed on August 2009
Ma CH, Kalb T (2006) Development of starter solution technology as a balanced fertilization
practice in vegetable production. Acta Hortic 700:173–185
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
195
Macdonald AJ, Poulton PR, Howe MT, Goulding KWT, Powlson DS (2005) The use of cover
crops in cereal-based cropping systems to control nitrate leaching in SE England. Plant Soil
273:355–373
MAFF (2000) Fertiliser recommendations for agricultural and horticultural crops. MAFF reference book 209. HMSO, London
Makowsky D, Guichard L, Beaudoin N, Aveline A, Lurent F (2005) A method to compare the
accuracy of inidators of water pollution by nitrates. In: Schroder JJ, Neeteson JJ (eds) N management in agrosystems in relation to the Water Frame Directive. Proceedings of 14th N
workshop, 2005, Maastricht, The Netherlands, pp 33–35
Mantovani P, Soldano M, Moscatelli G, Tabaglio V (2005) Nitrification inhibitors addition to
summer and autumn-applied pig slurry: effects on soil, water and atmosphere. In: Schroder JJ,
Neeteson JJ (eds) N Management in Agrosystems in relation to the Water Frame Directive.
Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands, pp 152–157
Marcelis L-FM, Heuvelink E, Goudriaan J (1998) Modelling biomass production and yield of
horticultural crops: a review. Sci Hortic 74:83–111
Mastrorilli M (1999) Modellizzazione. Sviluppo di modelli idrologici per ambienti mediterranei.
Boll SISS 48(1):245–250
Matthaus D, Gysi E (2001) Plant sap analysis in vegetables a tool to decide on nitrogen top dressing. Acta Hortic 506:93–102
Maynard DN, Barker AV, Minotti PL, Peck NH (1976) Nitrate accumulation in vegetables. Adv
Agron 28:71–117
Meinardi CR, Beusen AHW, Bollen MJS, Klepper O, Willems WJ (1995) Vulnerability to diffuse
pollution and average nitrate contamination of european soils and groundwater. Water Sci Tech
31:159–165
Mempel H, Meyer J (2002) Environmental system analysis for horticultural crop production. Acta
Hortic 638:45–51
Meynard JM, Guichard L, Jeuffroy MH, Makowsky D (2002) Which decision support tools for
the environmental management of nitrogen? Agronomie 22:817–829
Mills HA, Jones JB (1996) Plant analysis handbook II. Macro-Micro Publishing, Athens, GA
Mohammad MJ (2004) Squash yield, nutrient content and soil fertility parameters in response to
methods of fertilizer application and rates of nitrogen fertigation. Nutr Cycl Agroecosyst
68:99–108
Moreno F, Cayuela JA, Fernandez JE, Fernandez-Boy E, Murillo JM, Cabrera F (1996) Water balance
and nitrate leaching in an irrigated maize crop in SW Spain. Agric Water Manage 32:71–83
Müller T, Thorup-Kristensen K (2001) N-fixation of selected green manure plants in an organic
crop rotation. Biol Agric Hortic 18:345–363
Narayan MS (2002) Effect of sugar and nitrogen on the production of anthocyanin in cultured
carrot (Daucus carota) cells. J Food Sci 67(1):84–86
Neeraja G, Reddy KM, Reddy IP, Reddy YN (1999) Effect of irrigation and nitrogen on
growth yield and yield attributes of rabi onion (Allium cepa) in Andhra Pradesh. Veg Sci
26:64–68
Neeteson J, Langeveld J, de Haan J (2003) Nutrient balances in field vegetable production systems. Acta Hortic 627:13–23
Neeteson JJ, Carton OT (2001) The environmental impact of nitrogen in field vegetable production. Acta Hortic 563:21–28
Neeteson JJ, Booij R, Dijk W van, Haan J de, Pronk A, Brinks H, Dekker P, Langeveld H (2001)
Projectplan Telen met toekomst. Appl Plant Res, Publicatie nr. 2, Lelystad
Neeteson JJ (1995) Nitrogen management for intensively grown arable crops and field vegetables.
In: Bacon PE (ed) Nitrogen fertilization in the environment. Marcel Dekker, New York,
Chapter 8, pp 295–325
Neeteson JJ (1989) Evaluation of the performance of three advisory methods for nitrogen fertilisation of sugar beet and potatoes. Neth J Agric Sci 37:143–155
Neurkirchen D, Lammel J (2002) The chlorophyll content meter as an indicator for nutrient and
quality management. Fertiliz Fert 2:89–109
196
F. Agostini et al.
Normand B, Recous S, Vachaud G, Kengni L, Garino B (1997) Nitrogen-15 tracers combined with
tensio-neutronic method to estimate the nitrogen balance of irrigated maize. Soil Sci Soc Am
J 61:1508–1518
Oenema O, Kros H, de Vries W (2003) Approaches and uncertainties in nutrient budgets: implications for nutrient management and environmental policies. Eur J Agron 20:3–16
Olivier M, Goffart JP, Ledent JF (2006) Threshold value for chlorophyll meter as decision tool for
nitrogen management of potato. Agron J 98:496–506
Olson SM, Simonne EH (eds) (2006) Vegetable production handbook for Florida. University of
Florida, IFAS Extension, Gainesville, FL
Osborne SL (2006) Starter nitrogen fertilizer impact on soybean yield and quality in the Northern
Great Plains. Agron J 98:1569–1574
Owen J, Scharpf HC, Weier U, Laurence H, Tremblay N (2003) Extension of practical solutions
for efficient nitrogen management of vegetables crops: a comprehensive guide developed
using a unique approach. Acta Hortic 627:161–163
Paschold J, Artelt B, Hermann G (2003) Influence of N-nutritional and catch crops on the yield
of asparagus (Asparagus officinalis L.) and N-leaching. Acta Hortic 627:57–64
Paschold J, Artelt B, Hermann G (2001) Influence of Nmin target values on Fertilisers need, yield
and Nmin residues in Asparagus. Acta Hortic 563:53–58
Paschold J, Scheunemann Ch (1989) Controlling output level in the white cabbage by assessing
N-fertilization on the basic of soil and plant analyses. Acta Hortic 260:313–328
Pasda G, Hahndel R, Zerella W (2001) Effect of fertilizers with the new nitrification inhibitor
DMPP (3.4 Dimethylpirazole phosphate) on yield and quality of agricultural and horticultural
crops. Biol Fertil Soils 34:85–97
Pavlou GC (2007) Effect of organic and inorganic fertilizers applied during successive crop seasons on growth and nitrate accumulation in lettuce. Sci Hortic 111(4):319–325
Peltonen J (1994) Effect of nitrogen fertilizers differing in release characteristics on the quantity
of storage proteins in wheat. Cereal-Chem 71:1–5
Phene CJ (1999) Efficient irrigation systems and irrigation scheduling for processing tomato: the
challange. Acta Hortic 487:479–485
Piekielek WP, Fox RH (1992) Use of a chlorophyll meter to predict sidedress nitrogen requirements for maize. Agron J 84:59–65
Pimpini F, Gianquinto G, Sambo P (2005) Organic vegetable production: evolution, base principles and quality of products. Italus Hortus 12(4):31–44
Prasad M, Simmons P, Maher MJ (2004) Release characteristics of organic fertilisers. Acta Hortic
644:163–170
Rabbinge R, Rossing W (2000) Meeting the demand for ecological modernization in horticulture:
the role of systems approaches. Acta Hortic 525:115–121
Radersma S, van Evert F (2005) Crop related indicators: is the crop able to tell the farmers what
to do? In: Schroder JJ, Neeteson JJ (eds) N management in agrosystems in relation to the
Water Frame Directive. Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands,
pp 247–249
Radersma S, van Geel W, Smit A, van Wess N (2005) Decision support systems for nitrogen
fertilization to maintain production and reduce potential N-Losses: main questions ad answers
in the Netherlands. In: Schroder JJ, Neeteson JJ (eds) N management in agrosystems in relation to the Water Frame Directive. Proceedings of 14th N Workshop, 2005, Maastricht, The
Netherlands, pp 266–269
Rahn CR, Bending GD, Lillywhite RD, Turner MK (2003) Novel techniques to reduce environmental N pollution from high nitrogen content crop residues. Acta Hortic 627:105–111
Rahn C (2002) Management strategies to reduce nutrient losses from vegetables crops. Acta
Hortic 571:19–25
Rahn C, DeNeve S, Bath B, Bianco V, Dachler M, Cordovil C, Fink M, Gysi C, Hofman G,
Koivunen M, Panagiotopoulos L, Poulain D, Ramos C, Riley H, Setatou H, Sorensen J,
Titulaer H, Weier U (2001) A comparison of fertiliser recommendation systems for cauliflowers in Europe. Acta Hortic 563:39–45
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
197
Rahn CR, Greenwood DJ, Draycott A (1996) Prediction of nitrogen fertilizer requirement with
HRI WELL_N Computer Model. Progress in Nitrogen Cycling. Proceedings of the8th nitrogen fixation workshop, University of Ghent, Belgium, 5–7 Sept 1994 Kluwer, Dordrecht, pp
255–258
Rahn CR, Paterson C, Vaidyanatha LV (1993) Improving the use of nitrogen in brassicae rotations.
Acta Hortic 339:207–218
Rahn CR, Vaidyanathan LV, Paterson CD (1992) Nitrogen residues from Brassica crops. Aspects
Appl Biol 30:263–270
Rajput TBS, Patel N (2006) Water and nitrate movement in drip-irrigated onion under fertigation
and irrigation treatments. Agric Water Manage 79:293–311
Ramos C, Agut A, Lidon A (2002) Nitrate leaching in important crops of the Valencian community region (Spain). Environ Pollut 118:215–223
Randall GW, Goss MJ (2001) Nitrogen losses to surface water through subsurface, tile drainage.
In: Follet RF, Hatfield JL (eds) Nitrogen in the environment: sources, problems and management. Elsevier Science, Amsterdam, pp 95–122
Remie B, Groenwold K, Rovres J, Clevering O, Pijnenburg H, Hekkert M, Lagenveld H (2003)
Nutrient management on vegetables farms: what will be the future? Acta Hortic 627:275–282
Riley H, Guttormsen G (1999) Alternative equations for critical N-concentration in cabbage. Acta
Hortic 506:123–128
Romic D, Romic M, Borosic J, Poljak M (2003) Mulching decreases nitrate leaching in bell pepper (Capsicum annuum L.) cultivation. Agric Water Manage 60(2):87–97
Rühlmann J (1999) Calculation of net nitrogen mineralization from the decomposable soil organic
matter pool. Acta Hortic 506:167–174
Salo T, Raisio R, Tiilikkala K (2001) Effectiveness of fertilizer recommendation in Finnish carrot
and pea production. Acta Hortic 506:37–40
Schaller RG (2000) Nitrogen nutrition and flavour compounds of carrots (Daucus carota L) cultivated in Mitscherlich pots. J Sci Food Agric 80:49–56
Scharpf HC (1991a) Dungenfenster: Fruhwarnsysteme fur dien-VersotgungLnad Und Forst, Heft,
10:S.24
Scharpf HC (1991b) Stickstoffdünung im Gemüsebau., AID-Heft 1223. Bonn; AuswertungsundInformationdienst für Ernährung, Landwirstschaft und Forsten e.V
Schenk MK (2006) Nutrient efficiency of vegetable crops. Acta Hortic 700:25–38
Schroder J, Neeteson J, Oenema O, Struik P (2000) Does the crop or the soil indicate how to save
nitrogen in maize production? Reviewing the state of the art. Field Crop Res 66:151–164
Scudlark JR, Russell KM, Galloway JN, Church TM, Keene WC (1998) Organic nitrogen in
precipitation at the Mid-Atlantic U.S. coast – methods evaluation and preliminary measurements. Atmos Environ 32:1719–1728
Seddaiu G, Iezzi G, Roggero PP (2007) Fissazione e trasferimento dell’azoto fissato dal favino al
frumento duro in successione. Atti del “XXXVII Convegno Nazionale della Società Italiana di
Agronomia”, 13–14 Settembre 2007, Catania, Italy
Sexton P, Carroll J (2002) Comparison of SPAD chlorophyll meter readings vs. petiole nitrate
concentration in sugarbeet. J Plant Nutr 25:1975–1986
Shaffer MJ, Delgado JA (2002) Essentials of a national nitrate leaching index assessment tool.
J Soil Water Conserv 57:327–335
Shaffer MJ, Halvardson DA, Pierce FC (1991) Nitrate leaching and economic analysis package
(NLEAP): model description and application. In: Follet RF, Keeney DR, Cruse RM (eds)
Managing nitrogen for groundwater quality and farm profitability. ASA, SSA and CSSA,
Madison, WI, pp 285–322
Sibley KJ (2008) Development and use of an automated on-the-go soil nitrate mapping system.
Doctoral Thesis, Wageningen University, Wageningen, The Netherlands
Sidat Y, Upendra M, Bharat P (2000) Fresh market tomato yield and soil nitrogen as affected by
tillage, cover cropping and nitrogen fertilisation. HortScience 35:1258–1262
Silber A, Xu G, Wallach R (2003) High irrigation frequency: the effect on plant growth and on
uptake of water and nutrients. Acta Hortic 627:89–96
198
F. Agostini et al.
Silgram M, Hatley D, Gooday R (2007) IRRIGUIDE: a decision support tool for drainage estimation and irrigation scheduling. Proceedings of the 6th biennial conference of the European
federation of IT in agriculture (EFITA)/world congress on computing in agriculture (WCCA)
2007 joint conference “Environmental and rural sustainability”, Glasgow, UK, 2–5 July 2007
Silgram M (2005) Effectiveness of the nitrate sensitive areas scheme (1994–2003). Final report to
UK Defra under project M272/56. 22pp. http://www.defra.gov.uk. Accessed on August 2009
Silgram M, Williams A, Waring R, Neumann I, Hughes A, Mansour M (2004) Effectiveness of
the nitrate sensitive areas scheme in reducing groundwater concentrations. Q J Environ Geol
Hydrogeol 38:117–127
Silgram M, Williams A, Waring R, Neumann I, Hughes A, Gaus I, Mansour M (2003) Assessment
of the effectiveness of the nitrate sensitive areas scheme in reducing nitrate concentrations in
groundwater. Technical report for UK Environment Agency R&D Project P2-267/2/TR. ISBN
1844320758. Environment Agency, Bristol, UK. 90 pp + 2 Appendices
Silgram M, Chambers BJ (2002) The effects of repeated straw incorporation on soil mineral nitrogen supply, fertiliser N requirements and nitrate leaching losses. J Agric Sci (Cambridge)
139(2):115–127
Silgram M, Shepherd M (1999) The effects of cultivation on soil nitrogen mineralisation. Adv
Agron 65:267–311
Simonne EH, Hochmuth GJ (2006) Soil and fertilizer management for vegetable production in
Florida. In: Olson SM, Simonne EH (eds) Vegetable production handbook for Florida,
2005/2006. Vance Publishing, Lenexa, KS, pp 3–15
Simonne EH, Studstill DW, Hochmuth RC (2006) Understanding water movement in mulched bed
on sandy soils: an approach to ecologically sound fertigation in vegetable production. Acta
Hortic 700:173–178
Simonne EH, Studstill DW, Hochmuth RC, Jones JT, Starling CW (2005) On-farm demonstration
of soil water movement in vegetables grown with plasticulture. Electronic Database Info.
System, HS 1008. http://edis.ifas.ufl.edu/HS251
Simonne EH, Studstill D, Hochmuth RC, McAvoy G, Dukes MD, Olson SM (2003) Visualization
of water movement in mulched beds with injections of dye with drip irrigation. Proc Fla State
Hortic Soc 116:88–91
Singandhupe RB, Rao GGSN, Patil NG, Brahmanand PS (2003) Fertigation studies and irrigation
scheduling in drip irrigation system in tomato crop (Lycopersicon esculentum L.). Eur J Agron
19:327–340
Smit A, Hann de J, Zwart K (2005) Farming for the future; can arable and horticultural on sandy
soils comply with the EU nitrate directive. Results from the nucleus farms Vredepeel and
Meterik. Telen net toekomst raposrt, Plant Research International, Wageningen, The
Netherlands.
Smit AB, Stoorvogel JJ, Wossink GAA (2000) A methodology to support the decision to invest in
spatially variable nitrogen fertilisation. Neth J Agric Sci 48(3–4):273–290
Smith FW, Loneragan JF (1997) Interpretation of plant analysis: concepts and principles. In:
Reuter DJ, Robinson JB (eds) Plant analysis: an interpretation manual, 2nd edn. Commonwealth
Scientific and industrial research organization, Collingwood, Victoria, pp 3–33
Soler-Rovira J, Aroyo-Sanz J, Soler-Rovira P (2005) Nitrogen flow analysis in the Spanish agriculture and flow production system. In: Schroder JJ, Neeteson JJ (eds) N Management in
agrosystems in relation to the Water Frame Directive. Proceedings of 14th N workshop, 2005,
Maastricht, The Netherlands, pp 36–39
Souza CF, Folegatti MV, Matsura EE, Or D (2006) Time domain reflectometry (TDR) calibration
for estimating soil solution concentration. Engenharia Agricola 28(1):282–291
Stenger R, Priesack E, Barkle G, Sperr G (1999) A tool for simulating nitrogen and carbon
dynamics in the soil-plant atmosphere system. In: Tomer M, Robinson, M, Gielen G (eds)
Proceedings of the technical session No 20. New Zealand Land Treatment Collective, New
Plymouth, NZ, pp 19–28
Stevens CJ, Quinton John N (2009) Pollution swapping in arable agricultural systems. Crit Rev
Environ Sci Technol 39(6):478–520
6
Decreasing Nitrate Leaching in Vegetable Crops with Better N Management
199
Sulas L, Canu S, Muresu R (2007) Azotofissazione e sovescio di una coltura di favino per la
gestione della fertilità in sistemi cerealicolo-foraggeri biologici mediterranei. 3rd Workshop
GRAB-IT, Roma
Suprayago D, Van Noordwijk M, Hairiah K, Cadisch G (2002) The inherent ‘safety-net’ of an
Acrisol: measuring and modelling retarded leaching of mineral nitrogen. Eur J Soil Sci
53(2):185–194
Sweeney D, Graetz D, Bottcher A, Locascio S, Campbell K (1987) Tomato yield and nitrogen
recovery as influenced by irrigation method, nitrogen source and mulch. HortScience
22:27–29
Swiader J, Moore A (2002) SPAD-chlorophyll response to nitrogen fertilization and evaluation of
nitrogen status in dryland and irrigated pumpkins. J Plant Nutr 25:1089–1100
Taber HG (2001) Petiole sap nitrate sufficiency values for fresh market tomato production. J Plant
Nutr 24:945–959
Tei F, Benincasa P, Guiducci M (2003) Critical nitrogen concentration in lettuce. Acta Hortic
627:187–194
Tei F, Benincasa P, Guiducci M (2002) Critical nitrogen concentration in processing tomato. Eur
J Agron 18:45–55
Tei F, Benincasa P, Guiducci M (2000) Effect of nitrogen availability on growth and nitrogen
uptake in lettuce. Acta Hortic 533:385–392
Tei F, Benincasa P, Guiducci M (1999) Nitrogen fertilisation on lettuce, processing tomato and
sweet pepper: yield, nitrogen uptake and the risk of nitrate leaching. Acta Hortic 506:61–67
Thompson RB, Granado M, Gasquez J, Gallardo M, Giménez C (2005) Nitrate leaching losses from
a recently developed intensive horticultural system in a previously disadvantaged region. In:
Schroder JJ, Neeteson JJ (eds) N management in agrosystems in relation to the Water Frame
Directive. Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands, pp 420–423
Thompson RB, Gallardo M, Giménez C (2002) Assessing risk of nitrate leaching from the horticultural industry of Almeria, Spain. Acta Hortic 571:243–245
Thorup-Kristensen K, Pedersen L (2006) Cropping systems with winter wheat or spring wheat?
Root growth, catch crops, nitrogen leaching, and baking quality. Proceedings of European joint
organic congress, 30–31 May 2006, Odense, DK.
Thorup-Kristensen K, Magrid J, Stroumann Jensen L (2003) Catch crops and green manures as
biological tools in nitrogen management in temperate zones. Adv Agron 79:227–302
Thorup-Kristensen K (2001) Are differences in root growth of nitrogen catch crops important for
their ability to reduce soil nitrate-N content, and how can this be measured? Plant Soil
230:185–195
Thorup-Kristensen K, Van der Boogard R (1999) Vertical and horizontal development of the root
system of carrots following green manure. Plant Soil 212:145–153
Thorup-Kristensen K, Sørensen JN (1999) Soil nitrogen depletion by vegetable crops with variable root growth. Acta Agric Scand, Sect B – Soil Plant Sci 49:92–97
Thorup-Kristensen K, Nielsen NE (1998) Modelling and measuring the effect of nitrogen catch
crops on the nitrogen supply for succeeding crops. Plant Soil 203:79–89
Thorup-Kristensen K (1994) The effect of nitrogen catch crop species on the nitrogen nutrition of
succeeding crops. Fertliz Res 37:227–234
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger
WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284
Tosti G (2008) Green manure and nitrogen fertility management in organic farming systems.
Doctoral Thesis, University of Perugia, Italy
Tosti G, Boldrini A, Benincasa P, Tei F, Guiducci M (2008) The N Nutritional Status of Processing
Tomato Grown after Green Manures. Proceedings of the 10th congress of the European society
for agronomy “Agriculture as resource for energy and environmental preservation-multifunctional agriculture”, Bologna, Italy, 15–18 Sept 2008
Tremblay N, Belec C (2005) Strategies for environmental responsible N management using state
of the art crop sensing tools. In: Schroder J.J. and Neeteson J.J (eds) N management in
200
F. Agostini et al.
agrosystems in relation to the Water Frame Directive. Proceedings of 14th N workshop, 2005,
Maastricht, The Netherlands, pp 279–281
Tremblay N, Scharpf HC, Weier U, Laurence H, Owen J (2003) Nitrogen management in field
vegetables. Ed Agriculture et Agroalimentaire Canada, Cat. No. A42-92/2001E-INISBN
0-662-30494-2
Uhte R (1995) Integration of ecological aspects within economical decision support models for
vegetable crop production. Ber Landwirtsch 73:33–50
University of Minnesota (1996) Nitrate test offers economic, environmental benefits for potato
farmers. News information, Minnesota’s Future 64
US Environmental Protection Agency (1989). National Primary and Secondary Drinking Water
Regulations, proposed Rule, Fedd. Reg., 54: 22077. USEPA, Washington, DC
Van Alphen BJ, Stoorvogel JJ (2000) A methodology for precision nitrogen fertilization in highinput farming systems. Precision Agric 2(4):319–332
Van Dijk W, Smit AL (2006) How to meet the EC-nitrate directive in Dutch vegetable growing?
Acta Hortic 700:197–204
Vazquez N, Pardo A, Suso ML, Quemada M (2006) Drainage and nitrate leaching under processing tomato growth with drip irrigation and plastic mulching. Agric Ecosyst Environ
112:313–323
Vazquez N, Pardo A, Suso ML, Quemada M (2005) A methodology for measuring drainage and
nitrate leaching in unevenly irrigated vegetables crops. Plant Soil 269:297–308
Vigil MF, Kissel DE (1991) Equations for estimating the amount of nitrogen mineralized from
crop residues. Soil Sci Soc Am J 55:757–761
Visser de P, Voogt W, Heinen M, Assinck F (2005) Reduction of nitrate from intensive arable
cropping y specific crop management. In: Schroder JJ, Neeteson JJ (eds) N Management in
agrosystems in relation to the Water Frame Directive. Proceedings of 14th N workshop, 2005,
Maastricht, The Netherlands
Vitosh ML, Silvia GH (1996) Factors affecting potato petiole sap nitrate tests. Commun Soil Sci
Plant Anal 27:1137–1152
Vitosh ML, Silvia GH (1994) A rapid petiole sap nitrate–nitrogen test for potatoes. Commun Soil
Sci Plant Anal 25:183–190
Vos J, Vereijken P, van der Werf A (2005) Managing N by catch crops and buffer strips. In:
Schroder JJ, Neeteson JJ (eds) N Management in agrosystems in relation to the Water Frame
Directive. Proceedings of 14th N workshop, 2005, Maastricht, The Netherlands, pp 225–227
Vos J, van der Putten P (2004) Nutrient cycling in cropping system with potato, spring wheat,
sugar beet, oats and nitrogen catch crops. II Effect of catch crop on nitrate leaching in autumn
and winter. Nutr Cycl Agroecosyst 70:23–31
Wehrmann J, Scharpf H (1986) The Nmin method-an aid to integrating various objectives of
nitrogen fertilization. Z Pflanzenernaerh Bodenk 149:337–344
Weier U, van Riesen U, Scharpf HC (2001) Nmin-N-plots: a system to estimate the amount of
nitrogen top dressing of vegetables. Acta Hortic 563:47–52
Westerveld SM, McKeown AW, Scott-Dupree CD (2003) Chlorophyll and nitrate meters as nitrogen monitoring tools for selected vegetables in Southern Ontario. Acta Hortic 627:259–266
Whitmore AP (1996) Modellling the release and loss of nitrogen after vegetable crops. Neth
J Agric Sci 44:73–86
Wiesler F, Bauer M, Kamh M, Engels Th, Reusher S (2002) The crops as indicators for side-dress
nitrogen demand in sugar beet production, limitations and perspectives. J Plant Nutr Soil Sci
165:93–99
Zhang YM, Hu CS, Zhang JB, Chen DL, Li XX (2005) Nitrate leaching in an irrigated wheatmaize rotation field in the North China Plain. Pedosphere 15:196–203
Chapter 7
Manure Spills and Remediation Methods
to Improve Water Quality
Shalamar D. Armstrong, Douglas R. Smith, Phillip R. Owens,
Brad Joern, and Candiss Williams
Abstract Within the last 2 decades the transition in livestock production technology
and intensity has resulted in an increase in annual livestock production and a drastic
decrease in the number of livestock operations. Consequently, the susceptibility
of current livestock operations to experience manure spills is far greater relative to
livestock farms 20 years ago, due to increased herd size per farm. Therefore, manure
spills in agricultural communities have become a pervasive issue and have led to the
catastrophic contributions of nutrients and pathogens to surface and groundwaters,
human health issues, and large fish kills. Furthermore, the current remediation methods for manure spills that reach surface waters focus on mitigating contaminants in
the water column and give no attention to the manure-exposed ditch sediments that
remain in the fluvial system and continue to impair the water column. Therefore,
this chapter addresses the causes, environmental impacts, and current and alternative
remediation methods for manure spills in agricultural streams. Geographic data suggest that the location of animal-feeding operations and the occurrence of manure
spills were highly correlated with the location of tile-drained agriculture fields.
In addition, at least 14% of reported manure spills were separately attributed to the
failure in waste storage equipment and over-application of manure in the states of
Iowa and Ontario, Canada. Evaluations of the downstream impacts of manure spills
have reported ammonia, total phosphorus, and total N concentrations that were at
least 28 times the average upstream concentrations before the spill occurred. Studies
have also determined that the current manure spill remediation method results in
soluble phosphorus and nitrogen concentrations significantly greater than the
Environmental Protection Agency total phosphorus nutrient critical limit, 24 h after
S.D. Armstrong (*), P.R. Owens, B. Joern, and C. Williams
Agronomy Department, Purdue University, 915 West State St., West Lafayette,
IN 47907-2054, USA
e-mail: sarmstro@purdue.edu
S.D. Armstrong and D.R. Smith
USDA-ARS, National Soil Erosion Research Laboratory, 275 South Russell St.,
West Lafayette, IN 47907, USA
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_7, © Springer Science+Business Media B.V. 2010
201
202
S.D. Armstrong et al.
the plume of the spill has passed. However, supplemental treatment of manure
exposed sediments resulted in at least a 50% decrease in the soluble phosphorus
concentrations which was in compliance with the phosphorus nutrient criteria.
Keywords Manure spills • manure spill remediation methods • alum • ammonium
• phosphorus • sediments
7.1 Introduction
Surface and groundwater degradation from agricultural losses of nitrogen and phosphorus are global environmental issues. Throughout the world, the consequence of
nitrogen and phosphorus losses from agricultural fields to enriched waterways is
realized in hypoxia zones such as the Gulf of Mexico (Alexander et al. 2008), the
Black Sea (Tolmazin 1985), and the Baltic Sea (Rabalais et al., 1999). Thus, the US
Environmental Protecting Agency has identified agricultural drainage, both surface
and subsurface, as the primary source of nutrient losses to freshwater systems in the
USA (USEPA 1995). Environmental studies have also found that manure spills are a
major source of nutrient loading to agriculture streams and that the use of livestock
manure in agricultural practices has contributed to 15% of the nitrogen loading in the
Mississippi River drainage basin that discharges into the Gulf of Mexico (Hoorman
et al. 2005; Ribaudo et al. 2003). Therefore, this chapter focuses on the causes,
impacts, and current and alternative remediation methods of manure spills.
In the USA, between the years 1982 and 1997, the number of livestock per feeding
operation increased by 10%, while the number of feeding operations decreased by
50% (Gollehon et al. 2001; Fig. 7.1). Between the years 1980 and 1995, the number
of swine farms in the Netherlands decreased by 32%, while swine production
increased or remained constant (van der Peet-Schwering et al. 1999). Similarly, in
France there was a 25% increase in swine production between the years 1985 and
1995 and the province of Brittany accounted for 55% of swine production within a
land area that was only 6% of the total agricultural land of France (Dourmada et al.
1999). This trend is a reflection of the industrialization of livestock production that
has increased production efficiency, the quantity of manure produced daily, and the
pressure applied on the related manure-management systems (Fig. 7.1). Consequently,
the occurrence of manure spills in agricultural communities and the degradation of
surface and groundwater have become more prevalent and have led to the contribution of nutrient and pathogen loading to source, surface and groundwaters globally
(Burkholder et al. 1997; Mallin 2000; Hoorman et al. 2005). Therefore, nitrogen and
phosphorus contamination of surface and groundwaters have been heavily associated
with intensive livestock production, whether gradually through feedlot runoff events
and leaching of waste lagoons, or catastrophically through animal waste spills. For
example, animal feeding operations have contributed to the impairment of 50% of the
lakes and 20% of the rivers in the USA (USEPA 2003).
7
Manure Spills and Remediation Methods to Improve Water Quality
203
Number of farms
200
160
120
80
Medium-large
Small
Very small
40
0
1982 87 92 97
Feedlot beef
1982 87 92 97
Dairy
Very Small
Small
1982 87 92 97
Swine
1982 87 92 97
Poultry
Medium and large combined
Fig. 7.1 The results of an assessment of confined animal farms by species and size within the
years 1982–1997. The findings clearly illustrate the decline in very small and small livestock farms
and the emergence of medium-to-large livestock operations (Gollehon et al. 2001)
Nitrogen and phosphorus losses from manure spills pose a significant threat to the
health of humans and aquatic ecosystems. Manure spills have been found to result in
nitrate contamination of groundwater and source water that leads to methemoglobinemia (Blue-baby syndrome) (Townsend et al. 2003). A survey of nutrient levels in
the groundwater of the USA found that 9% of rural wells and 1% of community
wells had concentrations of nitrate–N greater than the 10 mg L−1, which is the maximum contaminant level for drinking water (Mueller et al. 1995). They also found
that in areas near intensive livestock operations, wells were more likely to be contaminated above 10 mg L−1 nitrate–N. In addition, manure spills from livestock operations have led to contamination of surface water and source water by Escherichia
coli, Campylobacter, and Cryptosporidium that resulted in widespread diarrhea,
vomiting, fever, and even death (Guan and Holley 2003; Hoxie et al. 1997). Aquatic
ecosystems that receive excessive loading of nitrogen and phosphorus could lead to
eutrophic conditions, due to nitrogen and phosphorus being nutrient that contribute
to eutrophication in freshwater ecosystems (Correll 1998), fish kills from toxic
levels of NH3 and NH4 (Mallin 2000; De La Torre et al. 2004; Kater et al. 2006).,
7.2 Causes of Manure Spills
In addition to the drastic increased herd size per farm, government and state regulations affect the susceptibility of animal-feeding operations to experience a manure
spill. The most current regulation that affects confined animal-feeding operations
manure-management systems is the ruling made by the Environmental Protection
204
S.D. Armstrong et al.
Table 7.1 Chemical analysis of various animal wastes, suggesting that total
phosphorus (TP) is most prominent in swine effluent (Hutchins et al. 2007).
TN: total nitrogen
NH4–N
TN
TP
CAFO type
(mg L−1)
Beef feedlot (sl)
33
63
Dairy (pl)
84
185
Poultry (pl)
656
802
Poultry (sl)
289
407
Poultry (tl)
58
96
Swine sow (tl)
944
1,290
Swine finisher (tl)
1,630
2,430
Swine nursery (tl)
1,370
2,040
Secondary lagoon (sl), primary lagoon (pl), tertiary lagoon (tl)
14
30
50
23
30
264
324
368
Agency in 2003 (USEPA 2003). This regulation requires confined animal-feeding
operations and large animal-feeding operations to develop and implement a nutrientmanagement plan in conjunction with applying for a National Pollution Discharge
Elimination System permit. The permit specifies how manure is managed and disposed on each qualified livestock operation. However, the pressing issue is that permit
holders’ nutrient-management plans must comply with the agronomic nutrient requirement of the crops in the fields where manure is applied. Therefore, the volume of
manure disposed is restricted to a rate that cannot exceed the nitrogen and phosphorus
demand of the receiving agricultural field. For swine producers, phosphorus is the
nutrient that results in the greatest limitations of manure application rate, since swine
waste contains more phosphorus relative to the phosphorus demand of most crops
(Table 7.1).
Contamination of surface water through manure violations often occurs on tiledrained fields where liquid manure is applied (Kinley et al. 2007). The function of
tile drainage is to provide a pathway for excess water from poorly drained soils to
be removed from agricultural fields. However, tile drainage has become a conduit
for nutrients to surface waters when liquid manure is applied in excess (Kinley
et al. 2007). This issue is most documented in the Midwestern USA and Canada
where agricultural tile drainage is necessary for crop production (Fig. 7.2), and
coincidentally, confined animal-feeding operations are prevalent. For example, in
the southern portion of Ontario, Canada, over 70% of the agricultural fields are tile
drained (Spaling and Smit 1995) and at least 20% of the total area is tile-drained
cropland in Midwestern USA such as in Indiana, Ohio, Iowa, and Illinois (USDA
1987). Furthermore, studies have demonstrated that the application rate of manure
is the driving factor of phosphorus and nitrogen loss after liquid manure is applied
in the presence of tile drainage (Ball et al. 2007; Cook and Baker 2001). It has also
been noted that fields that contain macropores and shallow water tables are more
susceptible to manure violations after land application (Steenhuis et al. 1994; Stone
and Wilson 2006). Macropores such as root channels, warm holes, and natural soil
cracks allow liquid manure to bypass the soil matrix to be intercepted by the tile
drain that facilitates transport to surface waters (Watson and Luxmoore 1986).
7
Manure Spills and Remediation Methods to Improve Water Quality
205
Subsurface Tile Drainage
Percent Total County Land
With Subsurface Tile Drainage
0% − 6%
7% − 16%
17% − 32%
33% − 51%
52% − 82%
Sources: 1992 National Resources Inventory and World Resources Institute
Fig. 7.2 The similarity in subsurface drainage density which is related to the density of swine
density in the USA (Sugg 2007)
During a 1-year study Muller et al. (2003) monitored the concentrations of NO3–,
NH4+, and pH in tile flow in an agricultural field. As a result of a manure application
and preferential flow they observed a spike in the load of NH4+ (22.0 g NH4–N),
which resulted in a daily nitrogen load that was 65% greater than before the manure
application.
Hoorman et al. (2005) investigated the factors that caused manure violations in
the state of Ohio within a 4-year period. They found that between the years of 2000
and 2003 there were 98 manure spills reported. Heavy precipitation after land application of liquid waste accounted for 41 of the 98 manure violations, making it a primary cause of manure violations. The next contributing factor was manure storage
mismanagement and equipment failure (e.g., ruptured pipes, holes, and failure of
on-site manure transport equipment) that accounted for 33 of the 98 manure violations. According to Osterberg and Wallinga (2004), in Iowa, from 1992 to 2002, 304
manure spills were reported. Both manure storage overflow and equipment failure
were responsible for 24% of the spills, runoff from animal feeding operations accounted
for 18%, and over-application accounted for 14% (Fig. 7.3). In Southwest Ontario,
Canada, 229 manure spills were reported between the years of 1988–1998. Spray
irrigation application accounted for 40%, insufficient storage accounted for 16%, and
equipment failure was the cause of 14% of the manure spills (Fig .7.3, Merkel 2004).
206
S.D. Armstrong et al.
Deliberate
spills
6%
Other
14%
Storage
overflow
24%
Equipment
failure
24%
Improper
application to
cropland
14%
Runoff from
open feedlots
18%
Fig. 7.3 The causes of major manure spill in Iowa, leading swine producing state, between the
years 1992 and 2002 (Osterburg and Wallinga 2004)
In February 2008, a manure spill in Quebec, Canada resulted in the release of
over 26,400 l of liquid cattle manure that drained into a nearby creek and contaminated a neighboring domestic well. This spill was caused by a broken valve on a
pipe that was used to transport manure to a manure storage tank (Johnston 2008).
Similarly in February of 2008, a 6 in. pipe on a cattle farm in Walkersville, MD
resulted in approximately 21.8 million liters of manure to be pumped into Glade
Creek and the contamination of the town’s water supply, leaving citizens to boil
their drinking water or purchase bottled water for 2 weeks. Bacteria counts in surface
water and groundwater were 57 and 20 E. coli per 100 ml, and both were significantly higher than the drinking water standard of one bacteria colony forming
units per 100 ml (Hauck 2008).
7.3 The Impact of Manure Spills
Unintentional manure spills in the past have impacted both aquatic ecological systems
and human health (Novak et al. 2000; Mallin and Cahoon 2003; Mead 2004).
Manure spills are large contributors of nutrients and pathogens, which are two of the
top three water impairments in the USA, according the Environmental Protection
Agency (USEPA 2000). As mentioned previously, the excess of nutrients and pathogens
leads to elevated biochemical oxygen demand (BOD), fish kills, and accelerated
eutrophication (USDA 1997; Frey et al. 2000) and manure spills can lead to catastrophic loading of these water contaminants. According to Indiana department of
environmental management (1995), agricultural feedlots are one of the possible sources
7
Manure Spills and Remediation Methods to Improve Water Quality
207
Fig. 7.4 Average concentration of total N, P, and ammonia from upstream, entry point, and downstream sampling location of 97 manure spills (Hoorman et al. 2005)
of E. coli contamination, which has been identified as being responsible for over
80% of 6,451 river miles in Indiana being declared unsafe for swimming or human
contact. Hoorman et al. (2005) collected upstream, entry point, and downstream water
samples during investigations of 97 manure spills (Fig. 7.4). The results of this study
suggested that the downstream impacts of manure spills are catastrophic. The average
downstream ammonia, total phosphorus, and total nitrogen concentrations after a
manure spill were 49, 28, and 68 times greater than the average upstream concentrations, respectively (Fig. 7.4). Contamination of water with bacteria, such as E. coli
and salmonella, are commonly associated with manure spills and when ingested,
bodily illnesses such as hemorrhagic colitis, hemolytic uremic syndrome, and thrombotic thrombocytopaenic purpura may occur (Thu 2002). In addition, nitrate losses
from manure spills pose a significant threat to the health of humans through the
contamination of groundwater and drinking water (Townsend et al. 2003).
Nitrogen from a manure spill has an immediate impact on fish and benthic
organisms through ammonia toxicity. Manure spills contribute excessive concentrations of nitrogen, and cations such as Ca2+ and Mg2+ that increase pH creating
optimum conditions for ammonia toxicity (Poxton 2003). Studies have demonstrated that ammonia toxicity in fish and benthic organisms occur under alkaline
conditions where the acid base reaction between OH– and NH4+ produces toxic
concentrations of NH3 (Kater et al. 2006).
In addition, studies have indicated that at pH <8.3 both NH4+ and NH3 contribute
to toxicity (Scholten et al. 2005). Fish naturally excrete metabolic NH3 concentrated
waste from their blood through diffusion to the water column (Kater et al. 2006).
However, this diffusion of waste will only occur when the concentration gradient
of NH3 is greater in the blood of the fish relative to the water column. Additionally,
208
S.D. Armstrong et al.
if the NH3 concentration in water column becomes elevated enough, the concentration
gradient could reverse, and NH3 has the potential to be actively transported into the
organism through an exchange with Na+ on the gills of the fish (Kater et al. 2006).
Therefore, after the occurrence of a catastrophic manure spill, the NH3 excretion of
fish is inhibited and toxic levels of NH3 builds up within the fish, which ultimately
leads to severe ammonia toxicity and high fish mortality.
Initial phosphorus loading from a manure spill and phosphorus desorption from
manure-exposed sediments in streams and drainage ditches can lead to accelerated
algal blooms and enhanced eutrophic conditions in receiving lakes, ponds, and
reservoirs. Lakes and ponds receiving elevated phosphorus additions from manure
spills could result in explosive algal blooms and the growth of other aquatic plants
that eventually cover the water surface. After the death of the algae and aquatic plants,
decomposition occurs through microorganisms that consume large fractions of dissolved oxygen (Scholten et al. 2005). This oxygen depletion ultimately leads to
reduced oxygen supply for fish and benthic organisms, reduced growth of benthic
organism, and fish kills. Moreover, carbon loading in fluvial systems can also result in
oxygen depletion due to increased microbial activity and high oxygen consumption
by microorganisms.
7.4 Current Manure Spill Remediation Methods
Currently, the recommended emergency response actions for manure spills that
contaminate a drainage ditch or streams are (i) to contain and isolate the contaminated
area using earthen or temporary dams, (ii) de-water the contained area using pumping
equipment, and (iii) redistribute the recovered waste into an alternative storage system or to land-apply the waste in compliance with state regulations (IDEM 2002).
However, the major inadequacy of the conventional spill remediation plan is the lack
of attention given to the phosphorus-enriched ditch sediments that have been exposed
to manure and remain in the fluvial system. Studies have demonstrated that phosphorus
and nitrogen desorption from untreated contaminated sediments continue to impair
the water column for weeks, after the spill has occurred.
For example, Burkholder et al. (1997) evaluated the impacts of a manure spill
from a farm in Onslow, North Carolina, that released 97.5 million liters of swine
manure into the surrounding drainage ditches. This spill resulted from heavy precipitation from a hurricane and faulty farm-operator management of manure storage.
They found that the average total phosphorus concentration 2 days after the spill
was 100 times greater than the total phosphorus average of 0.047 mg P L−1from the
previous 10 months (Table 7.2). Furthermore, with continual sampling of the water
column at 5, 14, and 61 days after the spill they observed that total phosphorus
concentrations were 7.6, 2.1, and 5.5 times greater than the previous 10-month
average, respectively (Burkholder et al. 1997). A possible explanation for elevated
total phosphorus concentrations days and weeks after the manure spill had occurred
could be that sediment phosphorus concentrations exist in equilibrium with the
7
Manure Spills and Remediation Methods to Improve Water Quality
209
Table 7.2 The ability of sediments to act as a phosphorus source for up
to 61 days after a manure spill has occurred due to sediment phosphorus
desorption (Burkholder et al. 1997)
Phosphorus concentration
Time
(mg P L−1)
Ten months before spill
0.047
Two days after spill
4.79
Five days after spill
0.36
Fourteen days after spill
0.106
Sixty-one days after spill
0.29
phosphorus concentration of the overlying water column within a fluvial system.
Therefore, these elevated phosphorus concentrations observed days and weeks after
the contamination plume had passed clearly indicate that the sediments became significant sources of phosphorus thereby releasing phosphorus into the water column.
In other words, the sediments that contained elevated concentrations of phosphorus,
release phosphorus to the subsequent flow with low phosphorus concentrations to
maintain equilibrium with the water column.
Burkholder et al. (1997) also found that the density of fecal coliform bacteria at
5, 14, and 61 (7.0 × 102, 71.9 × 104, and 1.2 × 103 colony-forming units) days after
the spill was greater than the state standard of 200 colony-forming units/100 ml.
Therefore, this could be evidence that fecal coliform bacteria is surviving for days
after the spill and is being redistributed back into the water column.
7.5 Alternative Sediment Amendments
Environmental and waste management scientists have provided vital findings that
demonstrated the efficacy of aluminum sulfate (alum) as a treatment to reduce
phosphorus availability in manure storage, after land application of manure, in ponds
and wetlands, and in phosphorus-enriched sediments that have been contaminated
by waste water treatment plants (Ann et al. 1999; Dao et al. 2001; Steinman et al.
2004; Choi and Moore 2008). There are two proposed mechanism in which alum
reduces the availability of phosphorus in manure, soil solution, and sediment pore
water. The first is shown in equation 7.1 where aluminum disassociates from SO4− in
solution and forms a coprecipitate with PO4− (Moore and Miller 1994).
Al2(SO4)3 . 14H2O + 2H3PO4 ® 2AlPO4 + 6H+ + 3SO42– + 14H2O
(7.1)
The second proposed mechanism involves the formation of amorphous aluminum
oxide that adsorbs soluble phosphorus from solution (Peak et al. 2002; Hunger
et al. 2004).
Al(OH)3 + H2po4 ® Al(OH)3 – H2PO4
(7.2)
210
S.D. Armstrong et al.
Moreover, as time after phosphorus adsorption to amorphous aluminum oxide
increases the formation of minerals such as varisite (AlPO4·2H2O) and wavellite
[Al3(PO4)2(OH)3·5H2O)] may form and persist under acidic conditions.
Sims and Luka-McCafferty (2002) conducted a large-scale on-farm poultry litter
study where alum was amended to poultry litter in 97 poultry houses for a 16-month
period. They found that alum amendment at a rate 1.0 kg alum m−2 flock−1 (approximately 0.09 kg alum per bird) decreased the dissolved phosphorus content in manure
by 67%. Similar studies have also demonstrated that the addition of alum to poultry
litter resulted in a reduction of phosphorus loss via runoff by as much as 52–87%
using the following application rates 1:5 ratio of alum to poultry litter (Shreve et al.
1995); applications of 5%, 10%, 15% alum to poultry litter on a weight basis (Delaune
et al. 2004); and 10% alum application by weight to poultry litter (Smith et al. 2004).
Smith et al. (2005) investigated the effect of alum application on the phosphorus concentration and adsorption properties of sediments from tile-fed drainage ditches in an
agricultural watershed in northeast Indiana. They determined that applying alum
reduced the extractable phosphorus in sediments by 50–90% and the portioning index
by 50% (Fig. 7.5). Haggard et al. (2004) evaluated the use of alum as a chemical
amendment to sediments from streams that received a daily influx of phosphorus from
a municipal waste water treatment plant’s effluent discharge. Results from their study
demonstrated that applying alum with CaCO3 to phosphorus-enriched sediments
resulted in a significant reduction in sediment labile phosphorus, equilibrium phosphorus concentrations, and a significantly increased in the phosphorus-buffering
capacity of the sediments. The sediment equilibrium concentration is the concentration at which the net phosphorus adsorption and desorption of fluvial sediment is zero
10
Pre-alum
9
8
7
6
5
4
3
Alum treated
2
1
0
Small
Large
Xlarge
A Watershed
Small
Large
B Watershed
Small
Large
C Watershed
Fig. 7.5 The effect of alum application on the soluble phosphorus concentration of sediments
collected from three watersheds within the St. Joseph River Watershed in North East Indiana
(Smith et al. 2005)
7
Manure Spills and Remediation Methods to Improve Water Quality
211
(Taylor and Kunishi 1971) and the buffering capacity is a measure of the sediments
ability to adsorb phosphorus per unit increase in phosphorus water concentration.
The efficacy of the current and an alternative manure spill remediation, where
alum was used to reduce soluble phosphorus desorption from sediment following a
manure spill were evaluated through a series of manure spills using fluvarium techniques. The manure spills were simulated for 24 h within a stream simulator using
sandy and clayey stream bed sediments. The current manure spill remediation
method was simulated by draining the contaminated water column, and uncontaminated water was circulated over alum treated and untreated sediments to simulate
subsequent flow after the spill has occurred. Results from this study demonstrate
that the current manure spill remediation method removes phosphorus from the
contaminated water column, but does not adequately remediate manure exposed
sediments that remain in the water column. Thus, sediments that received only the
current manure spill remediation treatment desorbed soluble phosphorus in the
water column to a maximum of 0.22 mg P L−1 which was significantly greater than
the Environmental Protection Agency nutrient criteria for soluble phosphorus in
that region. Furthermore, results suggested that a surface application of alum to
clay and sandy sediments following a manure spill decreased phosphorus released
from manure-exposed sediments by over 70% and mitigated the soluble phosphorus concentration in the water column below the Environmental Protection Agency
nutrient criteria for phosphorus (Author’s unpublished data).
Although the effectiveness of alum to reduce the availability of soluble phosphorus in sediments is well-known, the impact of alum on benthic organism is death.
Steiman and Ogdahl (2008) studied the ecological effect of using alum as an amendment to reduce the phosphorus concentrations in Spring Lake, Michigan. The alum
treatment was applied in 2006; data from an ecological assessment were collected
eight months later, and were compared to a control (pretreatment) set of ecological
data from the same lake recorded in 2003. In a laboratory experiment they found that
the phosphorus flux from untreated sediments in 2003 was 43 times greater relative
to sediments collected in 2006 after being treated with alum and that alum treatment
reduced the mean pore water phosphorus and significantly reduced the extractable
phosphorus. Additionally, they determined that the population of benthic invertebrates declined following alum applications, while Narf (1990) observed an increase
in invertebrate density. Smeltzer et al. 1999 observed a decline in sediment invertebrate density 1 year after alum treatment, a recovery to the pretreated levels within
2 years, and a significant increase above pretreatment levels 10 years after the alum
treatment.
7.6 Conclusion
Increased livestock production efficiency due to the emergence of new technology
and confined animal-feeding operations has severely impacted the surface and source
water of agricultural communities. Furthermore, it has been observed that greater
212
S.D. Armstrong et al.
herd sizes per livestock operation have led to enormous volumes of waste produced
daily and excessive pressure on waste-management systems to maintain waste storage
capacity. As a result, in Ohio, 41% of manure spills that occurred during a 3-year
period were attributed to lagoon breaches and excessive precipitation. In Iowa, 48%
of manure spills within a 10-year period were attributed to manure storage equipment failure and lagoon breaches, and in Ontario, Canada 40% of manure spills that
occurred within a 10-year period were due to over-application of animal waste
through spray irrigation.
Data have also suggested that the current remediation plan for manure spills is
efficient in removing the nutrient contamination in the water column following a
manure spill, but was not effective in remediating the sediment of the fluvial system.
Due to astronomical loading of phosphorus and nitrogen during a manure spill
benthic sediments initially act as sinks and are saturated. However, when subsequent flow enters the fluvial system after the plume of the spill has passed, the
sediment acts as a phosphorus source to water column due to greater phosphorus
and nitrogen in the sediment relative to the water column. Studies of the manure
spills have demonstrated that the water column total phosphorus 3 months after the
passing of the manure spill plume was five times greater than the 10-month average
total phosphorus of the water column. Therefore, supplemental treatment is needed
to remediate the entire fluvial system following a manure spill. The uses of alum
on a small plot and watershed scale to reduce the vulnerability of soluble phosphorus have been effective in reducing phosphorus in runoff by as much as 50%.
Moreover, data from a manure spill simulation experiment determined that with a
molar application of alum the phosphorus desorption following a manure spill was
reduced by at least 50%. Results from the studies in this chapter have raised the
awareness of the impact associated with manure spills in agricultural streams and
have presented novel, practical, and affordable solutions that can be used to remediate
surface and source water following manure spills.
References
Alexander RB, Smith R, Schwartz G, Boyer E, Nolan J, Brakebill J (2008) Differences in phosphorus
and nitrogen delivery to the Gulf of Mexico from the Mississippi river basin. Environ Sci
Technol 42:822–830
Ann Y, Reddy KR, Delfino JJ (1999) Influence of chemical amendments on phosphorus immobilization in soils from a constructed wetland. Ecol Eng 14:157–167
Ball Coelho B, Roy RC, Topp E, Lapen DR (2007) Tile water quality following liquid swine
manure application into standing corn. J Environ Qual 36:580–587
Burkholder JM, Mallin MA, Glasgow HB, Larsen LM, McIver MR, Shank GC, Deamer-Melia N,
Briley DS, Springer J, Touchette BW, Hannon EK (1997) Impacts to a coastal river and estuary
from rupture of a large swine waste holding lagoon. J Environ Qual 26:1451–1466
Choi IH, Moore PA Jr (2008) Effects of liquid aluminum chloride additions to poultry litter on
broiler performance, ammonia emissions, soluble phosphorus, total volatile fatty acids, and
nitrogen contents of litter. Poult Sci 87:1955–1963
7
Manure Spills and Remediation Methods to Improve Water Quality
213
Cook MJ, Baker JL (2001) Bacteria and nutrient transport to tile lines shortly after application of
large volumes of liquid swine manure. Trans ASAE 44:495–503
Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: a review.
J Environ Qual 2:261–266
De La Torre A, Dminguez L, Gonzalez M, Aguayo S, Carballo M, Munoz MJ (2004) Impact from a
cattle waste lagoon rupture on a downstream fish farm: a case study. Ecol Austr 14:135–139
DeLaune PB, Moore PA Jr, Carman DK, Shareply AN, Haggard BE, Daniel TC (2004)
Development of a phosphorus index for pastures fertilized with poultry litter – factors affecting
phosphorus runoff. J Environ Qual 33:2183–2191
Dao TH, Sikora LJ, Hamasaki A, Chaney RL (2001) Manure phosphorus extractability as affected
by aluminum-and iron by-products and aerobic composting. J Environ Qual 30:1693–1698
Dourmada JY, Guingand N, Latimier P, Se`ve B (1999) Nitrogen and phosphorus consumption,
utilisation and losses in pig production: France. Livest Prod Sci 58:199–211
Frey M, Hopper R, Fredregill A (2000) Spills and kills: manure pollution and America’s livestock
feedlots. Clean water network. Izaak walton league of America, and natural resources defense
council
Guan TY, Holley RA (2003) Pathogen survival in swine manure environments and transmission
of human enteric illness – a review. J Environ Qual 32:383–392
Gollehon N, Caswell M, Ribaudo M, Kellogg R, Lander C, Letson D (2001) Confined animal
production and manure nutrients. Resource Economics Division, Economic Research Service,
U.S. Department of Agriculture. Agriculture Information Bulletin No. 771
Haggard BE, Ekka SA, Matlock MD, Chaubey I (2004) Phosphate equilibrium between stream sediments and water: potential effect of chemical amendments. Am Soc Agric Eng 47:1113–1118
Hauck J (2008) Walkerville works to flush away E. coli-tainted water. http://gazette.net/stories/
022108/walknew71843_32358.shtml
Hoorman JJ, Jonathan N Rausch, Martin J Shipitalo (2005) Ohio livestock manure violations.
ASAE Meeting Presentation, Paper Number: 052060
Hoxie NJ, Davis JP, Vergeront JM, Nashold RD, Blair KA (1997) Cryptosporidiosis-associated
mortality following a massive waterborne outbreak in Milwaukee, Wisconsin. Am J Public
Health 87:2032–2035
Hunger S, Cho H, Sims JT, Sparks DL (2004) Direct speciation of phosphorus in alum-amended
poultry litter: solid state 31P NMR investigation. Environ Sci Technol 38:674–681
Hutchins SR, White MV, Hudson FM, Fine DD (2007) Analysis of lagoon samples from different concentrated animal feeding operations for estrogens and estrogen conjugates. Environ Sci
Technol 41:738–744
Indiana Department of Environmental Management (2002) Indiana confined feeding regulation
program: guidance manual, p 22
Indiana Department of Environmental Management (1995) Office of Water Management, Indiana
305(b) Report, 1994–1995, p 9
Johnston D (2008) Drinking water near lachute contaminated by liquid manure from nearby farm.
http://www.canada.com
Kater BJ, Dubbeldam K, Postma JF (2006) Ammonium toxicity at high pH in a marine bioassay
using corophium colutator. Arch Environ Contam Toxicol 51:347–351
Kinley RD, Gordon RJ, Stratton GW, Patterson GT, Hoyle J (2007) Phosphorus losses through
agricultural tile drainage in Nova Scotia. Can J Environ Qual 36:469–477
Mallin MA (2000) Impacts of industrial-scale swine and poultry production on rivers and estuaries.
Am Sci 88:26–37
Mallin MA, Cahoon LB (2003) Industrialized animal production-a major source of nutrient and
microbial pollution to aquatic ecosystems. Popul Eviron 24(5):369–385
Mead R (2004) Fish and invertebrate recolonization in a Missouri prairie stream after an acute
pollution event. N Am J Fisher Manage 24:7–19
Merkel M (2004) Threatening Iowa’s future: Iowa’s failure to implement and enforce the clean
water act for livestock operations. Washington, DC: Environmental Integrity Project; 2004:20.
http://www.environmentalintegrity.org/pub194.cfm
214
S.D. Armstrong et al.
Moore PA, Miller DM (1994) Decreasing phosphorus solubility in poultry litter with aluminum,
calcium, and iron amendments. J Environ Qual 23:325–330
Mueller DK, Hamilton PA, Helsel DR, Hitt KJ, Ruddy BC (1995) Nutrients in ground water and
surface water of the United States: an analysis of data through 1992. Water-Resour Invest Rep
95-4031. USGS, Reston, VA
Müller B, Reinhardt M, Gächter R (2003) High temporal resolution monitoring of inorganic nitrogen load in drainage waters. J Environ Monit 5:808–812
Narf RP (1990) Interactions of Chironomidae and Chaoboridae (Diptera) with aluminum sulfate
treated lake sediments. Lake Reserv Manage 6:33–42
Novak JM, Watts DW, Hunt PG, Stone KC (2000) Phosphorus movement through a coastal plain
soil after a decade of intensive swine manure application. J Environ Qual 29:1310–1315
Osterburg D, Wallinga D (2004) Addressing externalities from swine production to reduce public
health and environmental impact. Am J Public Health 94:1703–1708
Peak D, Sims JT, Sparks DL (2002) Solid-state speciation of natural and alum-amended poultry
litter using XANES spectroscopy. Environ Sci Technol 36:4253–4261
Poxton M (2003) Water quality. In: Lucus JS, Southgate PC (eds) Aquaculture: farming aquaculture
animals and plants. Blackwell, Iowa, pp 47–73
Rabalais NN, Turner RE, Justic D, Dortch Q, Wiseman WJ (1999) Characterization of hypoxia:
topic 1 report for the integrated assessment on hypoxia in the Gulf of Mexico. NOAA Coastal
Ocean Office, Silver Spring, MD. Decision Analysis Series no. 15
Ribaudo M, Gollehon N, Aillery M, Kaplan J, Johansson R, Agapoff J, Christensen L, Breneman
V, Peters M (2003) Manure management for water quality: costs to animal feeding operations
of applying manure nutrients to land. Agricultural Economic Report No. (AER824). Economic
Research Service. US Department of Agriculture. Washington, DC
Scholten MCTh, Foekema EM, Van Dokkum HP, Kaag NHBM, Jak RG (2005) Eutrophication
and the ecosystem. In: Eutrophication management and ecotoxicology. Springer, New York,
pp 1–13
Shreve BR, Moore PA Jr, Daniel TC, Edwards DR (1995) Reduction of phosphorus in runoff from
field applied poultry litter using chemical amendments. J Environ Qual 24:106–111
Sims JT, Luka-McCafferty NJ (2002) On-farm evaluation of aluminum sulfate (alum) as a poultry
litter amendment: effects on litter properties. J Environ Qual 31:2066–2073
Smeltzer E, Kirn RA, Fiske S (1999) Long-term water quality and biological effects of alum
treatment of Lake Morey, Vermont. Lake Reserv Manage 15:173–184
Smith DR, Haggard BE, Warnemuende EA, Huang C (2005) Sediment phosphorus dynamics for
three tile fed drainage ditches in Northeast Indiana. Agric Water Manage 71:19–32
Smith DR, Moore PA Jr, Miles DM, Haggard BE, Daniel TC (2004) Decreasing phosphorus
runoff losses from land-applied poultry litter with dietary modifications and alum addition.
J Environ Qual 33:2210–2216
Spaling H, Smit H (1995) A conceptual model of cumulative environmental effects of agricultural
drainage. Agric Ecosyst Environ 53:99–108
Steenhuis TS, Boll J, Shalit G, Selker JS, Merwin IA (1994) A simple equation to predict preferential flow solute concentration. J Environ Qual 23:1058–1064
Steinman AD, Ogdahl M (2008) Ecological effects after an alum treatment in Spring Lake. Mich
J Environ Qual 37:22–29
Steinman AD, Rediske R, Reddy KR (2004) The reduction of internal phosphorus loading using
alum in Spring Lake. Mich J Environ Qual 33:2040–2048
Stone WW, Wilson JT (2006) Preferential flow estimates to an agricultural tile drain with implications for glyphosate transport. J Environ Qual 32:1825–1835
Sugg Z (2007) Assessing U.S. farm drainage: can GIS lead to better estimates of subsurface drainage
extent? World Resource Institute, Washington, D.C
Taylor AW, Kunishi HM (1971) Phosphate equilibria on stream sediment and soil in a watershed
draining an agricultural region. J Agric Food Chem 19:827–831
Thu KM (2002) Public health concerns for neighbors of large-scale swine production operations.
J Agric Safety Health 8:175–184
7
Manure Spills and Remediation Methods to Improve Water Quality
215
Tolmazin D (1985) Changing coastal oceanography of the black sea. 1: Northwestern shelf. Prog
Oceanogr 15:217–276
Townsend A, Howarth RW, Bazzaz FA, Booth MS, Cleveland CC, Collinge SK, Dobson AP,
Epstein PR, Holland EA, Keeney DR, Mallin MA, Rogers CA, Wayne P, Wolfe AH (2003)
Human health effects of a changing global nitrogen cycle. Front Ecol Environ 1:240–246
USEPA (2003) National pollutant discharge elimination system permit regulation and effluent
limitations guidelines and standards for concentrated animal feeding operations: final rule. Fed
Regist 69:7175–7274, Feb
USEPA (2000) Water quality conditions in the United States: a profile from the 2000 national
water quality inventory. http://www.epa.gov/305b/2000report/factsheet.pdf
USDA (1997) Agricultural waste management field handbook. Part 651, National Engineering
Handbook. Published in 1992, with revisions through 1997. Washington, D.C.: USDA-NRCS.
http://www.ftw.nrcs.usda.gov/awmfh.html
USEPA (1995) National water quality inventory. Report to Congress. U.S. Government Printing
Office, Washington, D.C.
USDA (1987) Farm drainage in the United States: history, status, and prospects. In: Pavelis GA
(ed) USDA-ARS Miscellaneous Publication Number 1455, Washington, DC
van der Peet-Schwering CMC, Jongbloed AW, Aarnink AJA (1999) Nitrogen and phosphorus
consumption, utilisation and losses in pig production: The Netherlands. Livest Prod Sci
58:213–224
Watson KW, Luxmoore RJ (1986) Estimating macroporosity in a forest watershed by use of a
tension infiltrometer. Soil Sci Soc Am J 50:578–582
Chapter 8
Cropping Systems Management, Soil Microbial
Communities, and Soil Biological Fertility
Alison G. Nelson and Dean Spaner
Abstract Consumers are demanding more organic products, in part because of
concerns over environmental issues in conventional agriculture. Modern, highinput agriculture can cause groundwater contamination, soil erosion, and eutrophication of surface waters. It may be possible to enhance natural nutrient cycling
and reduce our dependence on inorganic fertilizers in cropping systems. To do so,
we have to manage our cropping systems to encourage diverse soil microbial
communities and arbuscular mycorrhizal fungi. This chapter reviews the impacts
of cropping management practices on soil microbial diversity and arbuscular
mycorrhizal communities. Systems that have reduced tillage, diverse crop rotations or intercrops, low applications of inorganic fertilizers and pesticides, and
some organic fertility inputs tend to encourage a large and diverse microbial community with mycorrhizal fungi. Organic systems should strive for minimum tillage and the avoidance of bare soil fallow in rotation. Well-managed conventional
systems with minimum tillage and inorganic crop inputs can be as effective as
organic systems in encouraging soil biological fertility. Both organic and conventional cropping systems should incorporate intercrops into their systems to
encourage diversity within the soil system.
Keywords Diversity • arbuscular mycorrhizal fungi • organic management
• conventional management • tillage • crop rotation • fertilizers and pesticides
• organic farming • soil biodiversity • tillage • no till • crop rotation
A.G. Nelson and D. Spaner (*)
Department of Agricultural, Food and Nutritional Science, University of Alberta, 4-10
Agriculture/Forestry Centre, Edmonton, AB, Canada T6G 2P5
e-mail: dean.spaner@ualberta.ca
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_8, © Springer Science+Business Media B.V. 2010
217
218
A.G. Nelson and D. Spaner
8.1 Introduction
Consumers are becoming increasingly concerned with food safety, the presence of
pesticides and genetically modified organisms in their grain products, and the
negative environmental effects of conventional agriculture (Klonsky 2000). This
increase in suspicion of industrial food production systems has, in part, translated
into increased demand for organic food products. In Canada, there are now over
3,600 organic farms on more than 500,000 ha (Macey 2006). The organic market
in Canada has been growing by 15–20% per year since the late 1990s, while the
food industry overall has grown 2% per year 1992–2000 (Sahota et al. 2004;
Klonsky 2000).
Consumers purchase organic food products because they perceive these foods to
have unique attributes and/or superior quality attributes compared with conventional foods (Yiridoe et al. 2005). Modern, high-input cropping systems have created numerous environmental, social, and economic problems, including
groundwater contamination, increased farm specialization, exacerbation of crop
pest problems, soil erosion, energy dependency, high-input expenses, less farm
economic resilience, and eutrophication of surface waters (Soule and Piper 1992;
McRae et al. 2000). Organic systems of production are often believed to have lower
negative environmental impacts than conventional systems, including maintaining
biodiversity within the agroecosystem. However, many of the perceived attributes
of organic products cannot be measured, and necessitate faith on the part of the
consumer that the desired attributes are present (Ritson and Oughton 2007).
Organic systems of production may or may not increase soil biodiversity.
Soil microbes play important roles in agroecosystems. This review is concerned
with the microflora in the soil system, which are the smallest organisms in the soil
and include bacteria, actinomycetes, fungi, and algae. The soil is a habitat for large
numbers of diverse soil microbes. Within a gram of soil there can be thousands of
millions of fungi and bacteria; about 95% of the species in the soil still remain
unknown (Uphoff et al. 2006). Bacteria and archaea are single-celled microbes
and have roles in organic matter decomposition, biological transformation of
nutrients, as well as some plant, animal, or other soil microbe symbionts. Fungi
are present in many forms in the soil, and have many roles within the soil system.
These roles include plant or animal symbionts, organic matter decomposition, soil
aggregation, plant and animal pathogens, etc. Actinomycetes are a particular form
of prokaryote whose morphology resembles that of fungi; they have roles in soil
aggregation, production of antibiotic compounds, organic matter turnover, and
nitrogen fixation (Brady and Weil 2002). Algae have roles in the cycling of carbon, nitrogen, and water; stabilizing soil, and forming symbiotic associations with
plants (Belnap 2005).
Soil fertility refers to the soil’s ability to supply nutrients to crops (Watson
et al. 2002). Soil microbes affect soil fertility in many ways, including plant symbioses with arbuscular mycorrhizal fungi and Rhizobia bacteria, organic matter
turnover, mineral immobilization and dissolution, and soil aggregation (Davis
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 219
and Abbott 2006). Managing soil biological fertility may be a key to successful
sustainable agricultural systems producing high-quality food products (Lee and
Pankhurst 1992).
For environmental and economic reasons, in addition to market demand,
improvements in cropping systems and the food products they create must be
achieved through improvements in the efficiency of natural nutrient cycling and not
through the use of additional inputs (Patriquin 1986; Yeates et al. 1997; Galvez
et al. 1995). Soil microbial communities have a large role in nutrient cycling, and
can be affected by agricultural management practices. It may be possible and feasible to tailor cropping systems management to encourage diverse microbial communities and specific beneficial microorganisms, and thereby promote efficient
nutrient cycling and plant nutrient uptake. This chapter will discuss some of the
roles of soil microbial diversity and mycorrhizae in nutrient cycling and plant nutrient uptake, and review the literature on the effects of management practices on soil
microbial diversity and mycorrhizal colonization in agricultural systems. We will
then examine the impact of combining the reviewed management practices on
microbial diversity in organic and conventional cropping systems. We will discuss
the feasibility of managing an agroecosystem for soil biodiversity.
8.2 Soil Microbiological Diversity in Agroecosystems
Plants are autotrophs, creating the organic molecules they require for growth and
development using elements absorbed mainly from the soil solution (Salisbury
and Ross 1992). Plants mainly take up elements in inorganic forms (Schimel and
Bennett 2004; Xu et al. 2006). Microbes play a critical role in soil nutrient cycling,
decomposing organic matter and mineralizing nutrients into inorganic, plant-available
forms (Kennedy and Gewin 1997; Prasad and Power 1997; Stark et al. 2004;
Uphoff et al. 2006).
Soil microbial diversity can be defined in terms of structural diversity, referring to the organisms present within the community, and functional diversity,
referring to the functions carried out by the community. A population refers to a
group of organisms of the same species within an environment, while the community refers to the interacting group of organisms within the environment
(Fig. 8.1). Diversity is a measure of the variety of organisms within the community. Soil microbial diversity can impart resistance and resilience to disturbance and stress within agroecosystems (Brussaard et al. 2004, 2007). Soil
fungal communities under organic management were reported to be more resistant to environmental disturbance, such as a hurricane (Wu et al. 2007). One
requirement of a well-functioning soil is “diversified and abundant populations
of soil organisms to mobilize nutrients” (Uphoff et al. 2006). Diverse microbial
communities more effectively use complex organic compounds, are more efficient carbon users, and are better able to mobilize nitrogen than less complex
microbial communities (Bonkowski and Roy 2005). All of these factors suggest
220
A.G. Nelson and D. Spaner
Species richness:
5
Species evenness:
19
Population
3
within a
community
1
Community
contains many
populations
1
5
Fig. 8.1 A drawing to show the difference between a population, all one species within a soil
system, and a community, a grouping of populations within a soil system. A population is present
within a community. Species richness is a measure of how many different species are present within
a soil system. Species evenness is a measure of how even the numbers of the various species
are within a soil system. Diversity is a measure that incorporates both species richness and evenness
that lowered soil microbial diversity will have negative effects on the efficiency
of nutrient cycling in the soil (Bonkowski and Roy 2005). The relationship
between soil biological diversity and ecosystem functioning has not been fully
elucidated (Anderson 2003; Coleman et al. 1994; Robertson and Grandy 2006),
Giller et al. 1997). Also, we do not know the relative importance of soil biological diversity on the integrity and sustainability of a given soil system (Welbaum
et al. 2004). However, we do know that at some point in the loss of soil microbial
diversity there will be a loss of ecosystem functioning (Coleman et al. 1994;
Giller et al. 1997). A change in microbial community structure due to disturbance can result in a reduction of soil functional stability (Griffiths et al. 2004).
This means that until we know the functions carried out by specific organisms,
maintaining diversity is a way of ensuring ecosystem functionability. Numerous
studies have examined the effects of agricultural management practices on soil
microbial community and diversity. It may be possible to manage an agroecosystem to increase soil biodiversity and soil biological fertility; however, this is
mainly managed indirectly. We influence soil microbial communities by altering
crop rotations, crop choice, tillage, and inputs (Brussaard et al. 2007).
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 221
8.3 Arbuscular Mycorrhizal Fungi in Agroecosystems
Within the diverse community of soil microbes, arbuscular mycorrhizal fungi play
an important role in nutrient cycling and uptake in crop plants. Arbuscular mycorrhizal fungi form, generally, mutualistic associations with the roots of over 80% of
known plant species, including wheat and other cereal crops, corn, rice, and
legumes (Habte 2006; Rillig 2004). Arbuscular mycorrhizal fungi get their name
from the arbuscules, or tree-shaped clusters of hyphae which form within a plant
root after infection (Habte 2006). The arbuscles are where nutrient exchange with
plants occurs; carbon products from the plant host flow to the fungus, while nutrients taken up by the fungus flow to the plant (Sylvia 2005; Figure 1). Mycorrhiza
are important in nutrient uptake for plants, because the fungal hyphae not within the
plant root represent increased surface area for absorption of essential plant nutrients, as well as an increase in the soil area explored. Mycorrhiza can take up a
number of nutrients, including: nitrogen, phosphorus, potassium, calcium, magnesium, sulfur, iron, manganese, copper, and zinc (Al-Karaki et al. 2004; Mohammad
et al. 2005; Ryan et al. 2004; Cruz et al. 2004; Mohammad et al. 2003). However,
where mycorrhiza are most beneficial is in the uptake of relatively immobile nutrients such as phosphorus, copper, and zinc (Habte 2006). The importance of mycorrhiza in the uptake of immobile nutrients is due to the hyphae accessing nutrients
that are not within reach of the plant roots, and because these nutrients do not flow
to root surfaces by mass flow (Habte 2006). Increased uptake of phosphorus
through mycorrhizal colonization can significantly increase phosphorus concentrations in wheat grains, with the intensity of the effect altered by wheat cultivar,
mycorrhizal species, and the soil environment (Al-Karaki et al. 2004) (Fig. 8.2).
In addition to plant nutrient uptake, mycorrhiza can generate a number of other benefits to the soil system and the plant. Some other benefits of mycorrhiza within the soil
system are stabilization of soil aggregates, suppression of plant fungal pathogens, reduction of plant parasitic infection by nematodes, protection of plants from drought and
saline conditions, and protection of plants from heavy metals (Habte 2006). Mycorrhiza
also have an effect on the community structure of other soil microorganisms, by contributing carbon compounds to the soil system as well as influencing soil structure (Hamel
2004; Hamel and Strullu 2006). The benefits of mycorrhiza have resulted in researchers
pointing to AMF as critical to the development of sustainable agricultural systems
(Douds et al. 1997; Rabatin and Stinner 1989; Hamel 2004), Plenchette et al. 2005).
8.4 Management Practices Affecting Soil Microbiological
Diversity
Soil microbes need water, energy (in the form of soil organic matter or plant and
animal residues), and essential elements from the soil solution, soil minerals, or soil
atmosphere. Physically, the critical controlling factors of microbial diversity are: soil
222
A.G. Nelson and D. Spaner
Spore
Extramatrical
hyphae
Auxillary
cell
Epidermis
Exodermis
Cortex
Endodermis
Arbuscule
Vesicle
Fig. 8.2 An example of an arbuscular mycorrhizal fungi association with a plant root showing
some of the typical structures present. Arbuscules form within the apoplastic space of root cortical
cells and are believed to be the site of nutrient exchange between the fungi and plant. Vesicles can
form in some species/strains of mycorrhizae, their function is not fully known, but is believed to
have a role in storage. Extramatrical hyphae (hyphae extending beyond the root) take up nutrients
from the soil. Hyphae can access areas beyond the root depletion zone for some nutrients (hyphae
can go about 10mm beyond the root – the P depletion zone is about 1mm around the root). Spores
are structures of asexual reproduction. Auxillary cells can also be found on the extramatrical
hyphae; their positioning on the hyphae and their shape are species/strain-dependent
organic matter content, the composition of the mineral fraction, and the relative
proportions of air and water (Thies and Grossman 2006). Chemically, important
factors affecting microbial diversity are: pH, cation- and anion-exchange capacity,
mineral content and solubility, buffering capacity, concentration of nutrient elements
in the soil, concentration of gases; e.g., oxygen, carbon dioxide, in the soil, soil
water content, and salinity or sodicity (Thies and Grossman 2006). While management practices can alter microbial communities directly, for the most part,
management practices change microbial communities indirectly by altering a number of the above-named soil properties affecting microbial diversity. Because most
microbes are heterotrophic, soil organic matter content and the type and amount of
organic materials added to the soil are two critical soil factors affecting microbial
diversity (Shannon et al. 2002). Some management practices that have been studied
for their effect on soil microbial communities are tillage, crop choice, and rotation
practices and chemical use (Fig. 8.3).
Practice
Soil
Lower soil
porosity
Buries crop
residue
Decrease
biomass
Increase
soil temp. &
fluctuations
Increases P
availability
Lower mycorrhiza
population and
effectiveness
Change microbial
community
structure
Soil
Moisture
Destroys
mycellal
network
Decrease
microbial diversity
Change
Soil pH
Fertilizers
No change in
microbial
structure
Decreases
plant
diversity
Pesticides
Stable
organic
matter
Increase
microbial diversity
Increase microbial
biomass
Increase
soil organic
matter
Increase
crop growth
Manure
Fig. 8.3 Flow chart of the reviewed management practices and their impact on the soil microbial community. Management practices generally affect the soil
microbial community indirectly by altering the microbes’ soil habitat
Microbes
Tillage
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 223
224
A.G. Nelson and D. Spaner
8.4.1 Tillage
Tillage has negative effects on soil structure, breaking aggregates, compacting
the soil, and adversely affecting pore size distribution and structure (Huwe and
Titi 2003). Tillage also buries crop residue and changes soil water and temperature
regimes (Kladivko 2001). In general, lower tillage intensities will have a positive
effect on soil microbial communities. Zero tillage systems are characterized as
having increased soil moisture and fewer fluctuations in soil temperature than
conventional tillage systems, thereby increasing soil microbial populations
(Kladivko 2001). Tillage alters the soil microbial community structure, both
immediately following, and with increasing time after a tillage event (Calderón
et al. 2000; Jackson et al. 2003). Changes in microbial communities due to
tillage can be measured 7 years following the cessation of cultivation, with
microbes responding to soil conditions taking a long time to change following
disturbance (Buckley and Schmidt 2001; Buckley and Schmidt 2003). Increased
tillage intensities alter microbial community composition and substrate
utilization (Cookson et al. 2008). In Alberta, Canada, tillage was found to
decrease soil microbial diversity and evenness (Lupwayi et al. 1998). Microbial
activity also decreases with increasing tillage intensity. In comparing zero-till,
organic, low-input, continuous corn and grassland systems, soil metabolic activity and nitrogen mineralization were highest in systems of minimal tillage (the
zero-till and grassland systems) (Weil et al. 1993). Tillage disturbs the soil biotic
community, possibly having a negative effect on the efficiency of nutrient
cycling (Werner and Dindal 1990).
Tillage intensity has a large effect on the fungal fraction of the soil microbial
community. It is generally believed that zero-tillage systems are fungal dominated, while conventional tillage systems are bacterial dominated (Kladivko
2001). Tillage decreases the fungal component of a soil microbial community for
at least 2 weeks following an operation (Jackson et al. 2003). Tillage negatively
affects mycorrhiza populations. Mycorrhizal colonization potential of the soil is
related more to the presence of fungal hyphae and colonized root pieces than to
spore populations (Douds et al. 1997). Thus, tillage has a direct effect on mycorrhizal colonization, as tillage destroys the mycelial network within the soil
(Evans and Miller 1990; Boddington and Dodd 2000). Conventional tillage systems have lower levels of mycorrhizal survival and proliferation than zero-tillage
systems, thereby reducing the benefits of mycorrhizal associations to plants and
soils (Kabir 2005). Tillage can also have negative effects on the sporulation of
some AMF species and the distribution of spores through the soil profile (Jansa
et al. 2002; Rabatin and Stinner 1989; Abbott and Robson 1991, Boddington and
Dodd 2000). In addition to reducing mycorrhiza abundance, differences in mycorrhiza community structure due to tillage system (conventional vs zero) have
been observed (Jansa et al. 2002). The reduction in mycorrhiza populations by
tillage has been linked to reduced P absorption in crops (Abbott and Robson
1991; Evans and Miller 1990).
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 225
8.4.2 Crop Choice and Rotation
Most soil microbes are heterotrophic and thus the type and amount of organic
materials added to the soil has a significant impact on microbial community structure (Shannon et al. 2002). Crop rotation is one of the most important tools available to farmers to manage agronomic issues (von Fragstein et al. 2006). Differential
effects of plant species on soil microbial communities may be caused by differences
in plant material composition and differences in plant root exudates. Root exudates
are influenced by environmental and plant factors, including the nutritional status
of the plant, so the influences of plant root exudates on microbial communities may
be site- and time-specific (Grayston et al. 1998; Koo et al. 2006). Greater crop rotation intensity and diversity can positively affect microbial communities.
Different field crops may or may not have differing effects on soil microbial
community and diversity. The rhizosphere of monocropped wheat (Triticum aestivum L.) had more bacteria and fungi present than the rhizospheres of forage species
such as ryegrass (Lolium perenne L.) or bentgrass (Agrostis capillaries L.)
(Grayston et al. 1998). The differences in the microbial communities of various plant
rhizospheres led to differences in carbon source utilization patterns, indicating that
plant species affected microbial functional diversity (Grayston et al. 1998). Other
studies have reported little to no difference amongst the rhizospheres of various crop
species. Microbial diversity has been reported to be similar under wheat, maize
(Zea mays L.), and faba bean (Vicia faba L.) (Song et al. 2007). Of the bacteria
associated with red clover (Trifolium pretense L.) and potato (Solanum tuberosum
L.), 73% were of the same species (Sturz et al. 1998).
Crop species may or may not have differential effects on soil microbial communities, depending on environmental and plant factors. However, soil microbial diversity does increase with increased aboveground plant diversity (Garbeva
et al. 2006). Intercropping can increase microbial diversity when compared with
crops grown in monoculture (Song et al. 2007). Increasing rotational diversity
can also increase microbial diversity. A legume green manure–wheat rotation
exhibited greater microbial diversity than continuous wheat (Lupwayi et al.
1998). Replacement of the tilled fallow phase of a fallow–wheat rotation with
green legume fallow increased soil microbial community biomass, carbon, nitrogen and microbial community, due to an increase in soil organic matter
(Biederbeck et al. 2005).
Genetic differences within a crop species also play a role in the structure of the
microbial community. Differences have been found in microbial communities associated with different wheat and canola (Brassica napus L.) cultivars (Siciliano et al.
1998; Germida and Siciliano 2001). The microbial community structure associated
with the wheat cultivar Cadet was altered when a pair of homeologous chromosomes conferring root-rot resistance were substituted from the wheat variety
Rescue to Cadet (Neal et al. 1972).
Crop cultivars that have been developed through genetic engineering can have a
temporary impact on microbial diversity and community structure that lasts the life
226
A.G. Nelson and D. Spaner
cycle of the plant (Dunfield and Germida 2003, 2004). Plants with transgenes affect
soil microbes directly by releasing transgene proteins into the environment as well
as indirectly through a change in root exudates (Liu et al. 2005). Lower diversity,
or altered structure, in the community of bacteria within the roots of transgenic,
glyphosate-tolerant canola cultivars versus non-transgenic or other herbicide-tolerant
transgenic cultivars has been reported (Siciliano and Germida 1999). While genetically engineered crops do affect the soil microbial community, these effects (being
temporary and dependent on the type of transgene) are likely not as important in
comparison to the effect of other management practices like rotation, tillage, and
chemical use (Dunfield and Germida 2004).
Crop species and varietal selection can also greatly affect mycorrhiza populations.
Plant species from the Chenopodiaceae and Cruciferae families, including the
western Canadian canolas Brassica napus L. and Brassica rapa L., are not generally colonized by mycorrhiza (Plenchette et al. 1983). About 80% of all plants form
mycorrhizal symbiosis, although some species are more dependent on mycorrhiza
than others. Mycorrhizal dependency is measured as the percent increase in growth
of a plant when colonized by mycorrhiza. Field crops have an average mycorrhizal
dependency of 44%, compared to 70% for wild plant species, with a large degree
of variation between species within these averages (Tawaraya 2003). Legume species have mycorrhizal dependency values of around 90%, maize has a medium
mycorrhizal dependency of about 50%, while modern wheat, oat (Avena sativa L.),
rye (Secale cereale L.), and barley (Hordeum vulgare L.) varieties are considered
weakly dependent, with values between −13% and 50% (Plenchette et al. 1983;
Hetrick et al. 1992; Mosse 1986; Tawaraya 2003). While examining modern wheat
cultivars and their ancestors, researchers concluded that mycorrhizal dependency is
being bred out of modern wheat varieties, and is a challenge to the optimization of
mycorrhizal in cropping systems (Hetrick et al. 1993; Rillig 2004). To successfully
manage mycorrhiza populations in agricultural systems there needs to be crop
breeding aimed at “mycorrhizal effectiveness” (Hamel 2004). Mycorrhiza can
improve plant nutrient status in lower soil nutrient levels, providing benefits to
organic and conventional systems, by lowering the fertility input requirements.
The loss of mycorrhizal dependency would mean the loss of an important natural
advantage to agricultural systems.
Crop rotation plays a large role in determining the mycorrhiza population in the
soil and colonization potential. A diversity of host plants can increase the diversity
of the mycorrhiza population and increase colonization levels (Rabatin and Stinner
1989; Sattelmacher et al. 1991). Non-mycorrhizal plants in rotation have lower soil
mycorrhiza spore populations than mycorrhizal plants, thus lowering the infectivity
of the soil in the subsequent year (Douds et al. 1997). Conversely, the presence of
a host plant species helps maintain the mycorrhizal inoculum potential of a soil
(Kabir 2005; Kabir and Koide 2000). Some crops tend to encourage a larger mycorrhizal community, with greater species richness (Douds and Millner 1999). An
overwintering cover crop can maintain AMF populations when no crop is present.
Mycorrhizal colonization potential was higher in soil with a hairy vetch (Vicia villosa
Roth) winter cover crop than in soil without a cover crop (Galvez et al. 1995).
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 227
The host plant species can also affect mycorrhizal diversity, with greatest diversity
under soybean (Glycine max L.) or sunflower (Helianthus annuus L.) (Jansa et al.
2002). The specificity of some mycorrhiza to certain crop species in rotation may
influence the diversity and infectivity of the mycorrhiza populations in the following
crop (Hamel and Strullu 2006).
8.4.3 Chemical Inputs
Agriculture is essentially an extractive system. Nutrients are taken out of fields and
exported in the form of grain, crop biomass, and/or animal protein. At some point,
nutrients must be added back to both organic and conventional systems to ensure
their sustainability. In conventional systems, this mainly takes the form of inorganic
fertilizers, while in organic systems fertility inputs include manures and composts.
The effect of inorganic and organic fertility amendments on soil microbes has been
studied by some researchers.
The addition of manure to a soil increases microbial biomass, and may alter the
community structure of soil microbes by increasing soil organic carbon (Frostegård
et al. 1997; Fauci and Dick 1994). The type of substrate added (e.g., compost versus
fresh plant material) may or may not affect community structure (Drenovsky et al.
2004; Fauci and Dick 1994). The handling of manure prior to application also
appears to have an effect. Biodynamic agricultural systems are a form of organic
farming that includes metaphysical and spiritual aspects, and prescribes specific
compost treatments to be applied to the soil at specific calendar dates. Fließbach
and Mäder (2000) reported that microbial communities supplied greater stabilized
organic matter in biodynamically composted manure, with a lower metabolic quotient than those supplied uncomposted manure. Comparing traditionally and biodynamically composted manure, soil biological activity was similar but metabolic
quotient higher in biodynamic treatments. Thus, researchers hypothesized that biodynamic compost treatments had a more diverse microbial community (Zaller and
Köpke 2004). The reasons for the greater performance of biodynamic composts are
unclear; however, we believe that if care is taken in the preparation and composting
of manure, it should be as good as biodynamic preparations.
Inorganic fertilizers, in comparison to manures and composts, do not directly
add organic carbon to the soil, but can alter soil chemistry, specifically soil pH,
thereby changing soil microbial habitats (Bünemann et al. 2006; O’Donnell et al.
2001). Soil treated with inorganic fertilizers tend to have lower microbial biomass,
as well as a different community structure than soil treated with organic fertility
amendements, such as manures or composts (Marschner et al. 2003; O’Donnell
et al. 2001; Peacock et al. 2001; Seghers et al. 2003; Suzuki et al. 2005). Up to 10
days following fertility input, there can be a change in community structure; however, these effects generally disappear by 91 days after application (Stark et al.
2007). Following long-term application of organic and inorganic fertilizers, researchers
reported an increase in the amount of bacteria present (Marschner et al. 2003).
228
A.G. Nelson and D. Spaner
However, this change in structure was not accompanied by a change in enzyme
activity, indicating that ecosystem functioning was not affected by this change in
structure. Inorganic fertilizers can also alter microbial communities indirectly
through increased plant production. In some cases, the impact of inorganic fertilizers and the change in soil pH have a greater effect on soil microbial community,
than organic fertilizers, which tend to increase soil organic matter (Suzuki et al.
2005). An extreme case of an agricultural field polluted by inorganic fertilizers had
higher organic carbon, total nitrogen, and C/N ratio, but lower diversity and richness
of microbial DNA sequences than fields with no, or normal agrichemical use (Yang
et al. 2000).
The application of phosphorus fertilizers can have a positive, neutral, or negative
effect on mycorrhizal colonization (Manske 1990; Abbott and Robson 1991;
Rabatin and Stinner 1989). The negative effect of phosphorus fertilizers on mycorrhiza populations has been attributed to increased soil levels of available phosphorus (Hamel and Strullu 2006). With high levels of phosphorus, root cell membranes
are more stable, reducing root exudates, thereby reducing colonization levels
(Habte 2006; Mosse 1986). Lower mycorrhizal colonization levels in wheat have
been attributed to the application of superphosphate, a soluble P fertilizer (Ryan
et al. 2004).
As well as decreasing mycorrhizal colonization, high levels of available nutrients serve to decrease the relative benefits of mycorrhiza and can actually decrease
plant productivity (Aikio and Ruotsalainen 2002; Ryan and Graham 2002; Stewart
et al. 2005). The mycorrhizal demand for crop carbon may actually decrease yields
in some conventional, high-fertility environments (Ryan and Graham 2002). The
relationship between higher phosphorus levels and lower mycorrhizal colonization
is specific to plant species and cultivars (Habte 2006). Roughly half of 44 spring
wheat varieties grown under high phosphorus conditions exhibited parasitic effects
of AMF inoculation, with lower shoot dry weight in inoculated plants (Manske
1990).
Results are less clear when comparing organic and inorganic fertility inputs.
Clay soil treated with manure had higher levels of active hyphae than soils treated
with inorganic fertilizers (Kabir et al. 1997). Another study reported AMF colonization to be greater under composted manure versus raw manure or inorganic fertilizer (Douds et al. 1997). Mycorrhizal infection was found to decrease with
increasing amounts of manure inputs; as well as a smaller mycorrhizal effect on
plants when using sterile versus unsterile manure (Brechelt 1990). The decreased
effects of mycorrhiza with increasing amounts of applied manure were attributed to
greater nutrient availability.
Conventional systems rely (at least in part) on chemical pesticides to control
weed, disease, and insect problems in the field. The impact of pesticides on microbial population biomass has been studied, and, in general, when pesticides are
applied at recommended rates, there is little to no impact on microbial populations
(Fraser et al. 1988; Seghers et al. 2005; Shannon et al. 2002). However, Johnsen
et al. (2001) suggested that insufficient studies have been conducted to assess the
effect of pesticide use on microbial diversity. We do know that some pesticides can
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 229
have a harmful effect on soil microbes, but which pesticides, and the long-term
impact of changes to the soil community because of those pesticides is unknown
(Bünemann et al. 2006). Herbicides have little effect on the soil community, while
some insecticides and fungicides had negative effects on soil microbes (Bünemann
et al. 2006). In a case of field-scale pesticide pollution, microbial biomass declined
on fields with normal application rates, but pesticide pollution did not appear to
alter the diversity of the microbial population (Yang et al. 2000). However, because
plant diversity affects soil microbial diversity (discussed in previous section), the
use of herbicides may indirectly affect microbial diversity by killing weeds and
reducing plant species diversity.
Pesticides can have a negative effect on mycorrhizal communities, lowering
colonization and sporulation of certain species; however, these effects seem to be
temporary (Gosling et al. 2006). The use of the herbicide diclofop lowered dry
weights of wheat inoculated with AMF, possibly due to a decline in colonization
(Rejon et al. 1997). Another study reported that AMF colonization levels were not
affected by herbicides (Ryan et al. 1994). At recommended rates, most herbicides
do not appear to alter mycorrhizal communities (Mosse 1986). Some fungicides
can lower mycorrhizal numbers, by directly affecting the fungi (Bünemann et al.
2006). Herbicides may reduce mycorrhizal numbers through a reduction of host
weeds (Gosling et al. 2006).
8.5 Organic and Conventional Cropping Systems
The preceding sections examined the effects of management practices individually
(see Fig. 8.1). Cropping system comparisons present challenges as reductionist science because many factors must vary in order to ensure proper functioning of the
respective systems (Lampkin and Padel 1994). Organic and conventional systems
are not defined by a set group of practices; they are an aggregate of a number of
management practices dictated by farmer choice and site-specific requirements,
rendering generalizations about cropping systems quite difficult (Harrier and
Watson 2003). This implies there is no clear definition of the two separate systems,
but rather a spectrum of systems, into which all farms would fall (Lampkin and
Padel 1994). The International Federation of Organic Movements defines organic
agriculture as “a production system that sustains the health of soils, ecosystems and
people. It relies on ecological processes, biodiversity and cycles adapted to local
conditions, rather than the use of inputs with adverse effects. Organic agriculture
combines tradition, innovation and science to benefit the shared environment and
promote fair relationships and a good quality of life for all involved” (IFOAM
2008). At its most basic, and common to all organic agricultural systems, organic
agriculture is defined by the absence of synthetic pesticides and fertilizers. For this
chapter, we consider conventional cropping systems to be all systems of production
not including biodynamic and organic. Despite the difficulties in studying and comparing organic and conventional cropping systems, there is value in such studies.
230
A.G. Nelson and D. Spaner
Both organic and conventional cropping systems consist of a number of different
management practices (chemical use, tillage, crop rotation, and crop choice) used
in combination. Despite the ranges of management practices used on organic and
conventional cropping systems, there are a number of factors that are commonly
found to differ in the two systems.
Organic systems tend to have higher organic matter, more weeds, lower yields,
and lower phosphorus levels than conventional systems (Entz et al. 2001;
Pimentel et al. 2005). The absence of inorganic fertilizers and pesticides in
organic systems generally leads to greater weed populations, higher tillage intensities, and lower soil nutrient levels. As well, organic systems often have more
diverse crop rotations and higher plant diversity within fields than conventional
systems. Soil organic matter is an important determinant of microbial populations, serving as a source of energy for microbes, and ultimately an important
pool of nitrogen, phosphorus, and sulphur (Stockdale et al. 2002). Organic systems employ a number of practices that serve to increase organic matter content,
generally resulting in slightly higher levels of organic matter in organic systems
versus conventional systems (Bossio et al. 1998; Drinkwater et al. 1995; Shepherd
et al. 2002). Organic management exhibited greater or equal soil organic carbon
levels to conventional management in long-term studies (Wander et al. 1994;
Fließbach and Mäder 2000). In some cases, organic management has resulted in
lower organic matter contents than conventional management (Girvan et al. 2003;
Stark et al. 2004). This may be due to lower yields in organic systems returning
lower levels of organic matter to the soil. In the case of extensive dryland cropping systems in western Canada that tend to rely on tillage for weed control, it is
suspected that these organic systems would have similar, or lower organic matter
and organic carbon levels to their conventional counterparts.
8.6 Cropping Systems Management and Microbial
Communities
With greater organic matter to provide an energy source for microbes, it is not surprising that a number of studies have reported higher microbial biomass in organic
systems than conventional systems (Fließbach et al. 1997; Hole et al. 2005; Mäder
et al. 2002; Fließbach and Mäder 2000; Wander et al. 1995). The diversity and
structure of soil microbial communities is also important in these systems. Some
studies have reported shifts in microbial communities with organic versus conventional management, while others have reported no differences between microbial
communities under the two management systems (Bossio et al. 1998; Yeates et al.
1997; Girvan et al. 2003; Wander et al. 1995; Lundquist et al. 1999). Differences
are generally expected between microbial communities in organic versus conventional management, and the absence of differences in some studies has been attributed
to the greater effects of soil type and time of sampling (Bossio et al. 1998; Girvan
et al. 2003; Stark et al. 2004; Wander et al. 1995). A comparison of organic and
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 231
conventional pastures reported no difference in soil biological diversity (Parfitt
et al. 2005). In this case, the similarity between the two systems may be due to a
lack of sufficient management differences, with only fertility regime differing.
Additionally, perennial intercrops may have exhibited a greater effect on microbial
diversity than the fertility inputs. Differences in soil microbial community structure
between organic and conventional systems is not necessarily negative, but indicative that these systems have very different soil conditions and perhaps require different functions from the soil microbes. While studying the effect of moisture stress
on organic and conventional soils, Lundquist et al. (1999) reported different community structure in the two soils, but no differences in community response to
stress. However, if we are to strive toward a reduced dependence on inorganic fertilizers, we must ensure that the soil microbial community can carry out functional
requirements to recycle nutrients efficiently.
Mycorrhizal potential and actual colonization has been reported to be greater in
grasslands, organic and low-input systems versus conventional systems (Eason
et al. 1999; Entz et al. 2004; Galvez et al. 1995; Mäder et al. 2000, 2002; Oehl et al.
2003, 2004; Sattelmacher et al. 1991; Scullion et al. 1998). This is in large part due
to the fact that the application of phosphorus fertilizers, even at low rates, decreases
root colonization of mycorrhiza (Clapperton et al. 1997; Mäder et al. 2000; Ryan
et al. 1994, 2004). Differential mycorrhizal community structure has been reported,
with organic systems maintaining community structures similar to natural systems.
Conventional systems tend to have lower species richness, with the associated risk
of lower mycorrhizal functioning (Oehl et al. 2003, 2004). Exceptions, of course,
have been reported. No differences were reported in diversity of soil fungal communities in organic and conventional systems in Florida (Wu et al. 2007). Eason
et al. (1999) reported the percent mycorrhizal infection of roots was one-third
greater on organic farms than conventional farms; however, there was a great deal of
variation in management practices between the farms, and therefore a great deal
of variation in the mycorrhizal infection rates amongst farms (Eason et al. 1999).
Mycorrhizal host plants need not be crop plants. Weeds may host mycorrhiza
during rotation phases with non-host crops or during the overwintering period. The
presence of weeds may also have a positive effect on soil processes, through the
addition of plant residues and root exudates (Werner and Dindal 1990). Weeds present
during the crop season may also provide greater plant diversity for the mycorrhiza,
as plant diversity is usually positively correlated to a diversity of AMF (Douds et al.
1997; Rabatin and Stinner 1989). Mycorrhizal weed species can increase mycorrhizal diversity and abundance, as well as influence community structure, improving
the mycorrhizal potential of soil (Vatovec et al. 2005). (Table 8.1 provides a list of
some mycorrhizal and non-mycorrhizal weed species.) One field study maintaining
dandelions (Taraxacum officinale Weber ex Wigg) as a winter cover crop reported
that the weed provided mycorrhizal inoculum potential for a subsequent maize
crop, increasing mycorrhizal colonization and phosphorus concentration of the
maize (Kabir and Koide 2000). Wheat grown in the presence of a non-mycorrhizal
weed, Chenopodium album, experienced lowered levels of mycorrhizal colonization, while maize experienced an increase in colonization (Stejskalova 1990).
232
A.G. Nelson and D. Spaner
Table 8.1 Summary of mycorrhizal colonization ability of various weed species (Adapted from
Vatovec et al. 2005, source is Vatovec et al. 2005 unless otherwise specified)
Mycorrhizal or
Common
non-mycorrhizal? name
Family
Species
Source
Mycorrhizal
Ragweed
Asteraceae
Ambrosia
artemisifolia
Mycorrhizal
Canada thistle
Asteraceae
Cirsium arvense
Mycorrhizal
Dandelion
Asteraceae
Taraxacum
Kabir and
officinale
Koide 2000
Mycorrhizal
Cocklebur
Asteraceae
Xanthium
strumarium
Mycorrhizal
Velvetleaf
Malvaceae
Abutilon
theophrasti
Mycorrhizal
Quackgrass
Poaceae
Agropyron repens
Mycorrhizal
Giant foxtail
Poaceae
Setaria faberi
Mycorrhizal
Yellow foxtail
Poaceae
Setaria lutescens
Mycorrhizal
Nightshade
Solanaceae
Solanum nigrum
Non-mycorrhizal Pigweed
Amaranthaceae
Amaranthus
retroflexus
Non-mycorrhizal Mustard
Brassicaceae
Brassica kaber
Non-mycorrhizal Lambsquarters
Chenopodiaceae Chenopodium
album
Non-mycorrhizal Smartweed
Polygonaceae
Polygonum
lapathifolium
Non-mycorrhizal Purslane
Polygonaceae
Portulaca oleracea
Non-mycorrhizal Curly dock
Polygonaceae
Rumex crispus
Mycorrhizal colonization can also increase or decrease the growth of weeds in the
field, depending on the soil and species (Vatovec et al. 2005). The presence of
mycorrhiza can change the composition of weed communities, selecting for host
species. Conversely, the weed community can alter mycorrhiza communities, with
diverse weed hosts encouraging increased mycorrhizal diversity (Jordan et al. 2000).
Soil taken from fields under organic, transitioning to organic and conventional
management had similar mycorrhizal colonization levels of various weed species
(Vatovec et al. 2005). The presence of weeds within a crop lowers crop productivity.
However, it appears that organic fields may derive some benefits from weed pressure
that is ubiquitous within these systems.
8.7 Interactions and the Relative Importance
of Management Practices
Rotation and tillage practices interact to alter microbial communities, with previous
crop effects greater under zero-tillage management (Lupwayi et al. 1998). Tillage
may have a greater effect on soil microbial populations than herbicides (Table 8.2).
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 233
Table 8.2 Summary of the management practices and their relative impact on the soil microbial
community and mycorrhizal community
Effect of management practice on:
Management practices
Microbial community
Mycorrhizal community
Tillage
Reduced tillage
Heavy tillage
Rotation
Diverse rotation
Intercrops
Fallow in rotation
Non-mycorrhizal crop in rotation
Transgenic crop in rotation
Crop inputs
Organic fertility amendments
Inorganic fertility amendements
Fungicides
Insecticides
Herbicides
Positive*
Negative
Positive
Positive
Negative
?
Negative
Negative
?
Positive
Positive or Negative (depends on fertilizer effects
organic matter inputs to soil, soil pH, etc.)
Negative
Negative
Negative
Negative
*Items in bold indicate that the management practice has a large effect on the community in question.
Items not in bold have a small effect on the community
In a study comparing zero- and conventional-tillage systems, researchers reported
that any effect of increased herbicide use on microbial diversity in a zero-tillage
system was overridden by the greater effects of tillage (Lupwayi et al. 1998). Other
researchers concluded that fertilizers can affect microbial populations more than
pesticides (Yang et al. 2000). The use of transgenic crops in rotation was concluded
to be less important to microbial community structure than rotation, tillage, or
chemical use (Dunfield and Germida 2004). Still others have suggested that longterm management histories have a greater effect on microbial communities than
current practices and crop selection (Buckley and Schmidt 2003). Similarily, it was
reported that soil and environmental factors had a greater effect on microbial structure than short-term management practices such as fertility inputs (Stark et al.
2007; Wakelin et al. 2008). An Australian study reported that soil pH was the most
important soil characteristic when determining microbial community diversity and
function (Wakelin et al. 2008).
While tillage is important in determining mycorrhiza abundance and diversity, other
management practices play important roles. Studies have reported host plant species
to have a greater effect on mycorrhizal diversity, and cropping system (organic vs
conventional) to have a greater effect on mycorrhizal abundance than tillage (Galvez
et al. 2001; Jansa et al. 2002). The greater effect of cropping system on mycorrhizal
colonization is most likely due to differences in soil phosphorus levels. However,
rotation phase has been reported to have a greater effect on infection potential of the
mycorrhizal population than the fertility amendment used (Douds et al. 1997).
234
A.G. Nelson and D. Spaner
Site-specific factors play a role in the relative importance of management
practices on soil microbial communities, as well as how management practices will
impact soil microbes. In general, farming practices that sustain or create soil conditions that are optimal for plant growth will also encourage abundant and diverse soil
microbial communities (Thies and Grossman 2006). While site-specific characteristics are important in determining the structure of the soil biological community
and how management practices affect that biological community, the general
principles of managing for a productive, sustainable system remain the same across
ecosystems (Uphoff et al. 2006).
8.8 The Management of Soil Biological Fertility
While certain organisms or functional groups play specific roles in soil nutrient
cycling (e.g., Rhizobia bacteria fixing atmospheric nitrogen into ammonia), it is
likely impossible to manage the agricultural soil system specifically for all the
beneficial organisms and functions desired. It is estimated that, at most, 5% of the
soil microorganisms have been identified and their role studied (Anderson 2003;
Uphoff et al. 2006). Because the environmental control of soil nutrient release is
complicated and because we have a limited ability to predict soil processes, manipulating individual microbial processes affecting soil fertility is not a viable option
(De Neve et al. 2004; Robertson and Grandy 2006; Watson et al. 2002). Realistic
management strategies to improve biological nutrient cycling must rely on wellestablished knowledge. To improve biological nutrient cycling, cropping systems
can be managed to ensure diverse microbial communities and abundant mycorrhizal populations.
Maintaining soil biological diversity is important to maintain the integrity of the
functioning of the soil system. There is some functional redundancy in soil systems; however, our limited understanding of microbial systems makes any theory
about functional redundancy speculatory (Anderson 2003; Kennedy and Smith
1995). Lowered soil microbial diversity, or a change in soil community structure
within an agroecosystem may not have negative impacts on soil biological fertility.
However, despite our incomplete understanding of the connections between microbial diversity, ecosystem functioning, and functional redundancy, we do know that
at some point in the loss of soil microbial biodiversity there will be a loss of function (Coleman et al. 1994). Diversity in the soil microbial community should be
maintained to ensure nutrient cycles and other soil functions continue.
In organic systems, there is already effort expended on improving soil fertility
through the creation of diverse soil microbial communities, because these systems
rely on biological fertility for the production of crops (Davis and Abbott 2006).
Organic systems, with manure and compost fertility inputs, low (or no) fertilizer
and pesticide inputs and diverse plant communities, seem fairly well-designed to
encourage a healthy and diverse soil microbial community. However, in dryland
prairie systems, with extensive farms, tillage is a large component of weed control
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 235
of organic systems. Lowered tillage would improve the soil conditions for microbial
diversity and mycorrhizal colonization; organic systems should strive for minimum tillage. As well, avoiding bare soil fallow in crop rotations would help to
maintain the microbial community, especially the mycorrhizal component (Gosling
et al. 2006).
Conventional systems represent a large range and combination of management
practices, making generalizations difficult. A well-managed conventional cropping
system, with minimum tillage, and low fertilizer inputs should experience similar
or identical microbial diversity and mycorrhizal levels as a well-managed organic
cropping system. If soil biological fertility is encouraged, through careful management (including reduced tillage, lowered fertility and pesticide inputs, and diverse
crop choices), conventional systems should be able to lower fertilizer rates.
Lowered fertilizer inputs, especially in reduced tillage systems where mycorrhizal
communities can thrive, can offset some of the negative impacts of high-input
systems. Both organic and conventional systems should begin to incorporate intercrops into rotations. Aboveground diversity is very important in determining
belowground diversity.
8.9 Conclusion
The impact of production practices on soil microbial diversity and mycorrhizal
colonization has been studied to varying degrees (Vandermeer et al. 1998). This
paper reviewed work in the area of crop management practices and their impact on
soil microbial diversity and mycorrhizal communities. We have not reached a point
where definitive relationships between production practices and microbial community structure can be defined. All of the management practices discussed in this
paper have aspects of site-specificity in their effect on microbial communities,
making broad generalizations about the effect of a particular practice on microbial
structure difficult. Knowing the ecological principles guiding microbial community
structure can help farm managers tailor their cropping practices to a particular set
of conditions. In general, lowered fertilizer and pesticide use, diverse crop rotations
that include mycorrhizal plant species, reduced tillage systems as well as the use of
intercrops and cover crops can maintain or improve indigenous mycorrhizal communities and microbial diversity (Plenchette et al. 2005; Thies and Grossman
2006). Organic cropping systems should strive for minimum tillage systems while
conventional systems should work toward lowered reliance on fertilizers to supply
crop nutrients. Both organic and conventional cropping systems should begin to
grow intercrops to encourage diversity within the soil system.
Acknowledgments The first author has been supported by a Canadian Graduate Scholarship
from the Natural Sciences and Engineering Research Centre (NSERC) and an Alberta Ingenuity
Scholarship. The second author was supported by a Discovery grant from NSERC and research
grants from Alberta Crop Industry Development Fund Inc.
236
A.G. Nelson and D. Spaner
References
Abbott LK, Robson AD (1991) Factors influencing the occurrence of vesicular–arbuscular mycorrhizas. Agric Ecosyst Environ 35:121–150. doi:10.1016/0167-8809(91)90048-3
Aikio S, Ruotsalainen AL (2002) The modelled growth of mycorrhizal and non-mycorrhizal
plants under constant versus variable soil nutrient concentration. Mycorrhiza 12:257–261.
doi:10.1007/s00572-002-0178-5
Al-Karaki G, McMichael B, Zak J (2004) Field response of wheat to arbuscular mycorrhizal fungi
and drought stress. Mycorrhiza 14:263–269. doi:10.1007/s00572-003-0265-2
Anderson T-H (2003) Microbial eco-physiological indicators to assess soil quality. Agric Ecosyst
Environ 98:285–293
Belnap J (2005) Cyanobacteria and algae. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA
(eds) Principles and applications of soil microbiology. Pearson Prentice Hall, Upper Saddle
River, NJ, pp 162–180
Biederbeck VO, Zentner RP, Campbell CA (2005) Soil microbial populations and activities as
influenced by legume green fallow in a semiarid climate. Soil Biol Biochem 37:1775–1784.
doi:10.1016/j.soilbio.2005.02.011
Boddington CL, Dodd JC (2000) The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. I. Field studies in an Indonesian Ultisol. Plant Soil
218:137–144. doi:10.1023/A:1014966801446
Bonkowski M, Roy J (2005) Soil microbial diversity and soil functioning affect competition
among grasses in experimental microcosms. Oecologia 143:232–240. doi:10.1007/s00442004-1790-1
Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12. doi:10.1007/s002489900087
Brady NC, Weil RR (2002) The nature and properties of soils. Prentice Hall, Upper Saddle
River, NJ
Brechelt A (1990) Effect of different organic manures on the efficiency of VA mycorrhiza. Agric
Ecosyst Environ 29:55–58. doi:10.1016/0167-8809(90)90254-B
Brussaard L, Kuyper TW, Didden WAM, de Goede RGM, Bloem J (2004) Biological soil quality
from biomass to biodiversity – importance and resilience to management stress and disturbance. In: Schjønning P, Elmholt S, Christensen BT (eds) Managing Soil Quality: Challenges
in Modern Agriculture. CABI Publishing, Cambridge, MA, pp 139–161
Brussaard L, de Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability.
Agric Ecosyst Environ 121:233–244. doi:10.1016/j.agee.2006.12.013
Buckley DH, Schmidt TM (2001) The structure of microbial communities in soil and the lasting
impact of cultivation. Microb Ecol 42:11–21. doi:10.1007/s002480000108
Buckley DH, Schmidt TM (2003) Diversity and dynamics of microbial communities in soils from
agroecosystems. Environ Microbiol 5:441–452. doi:10.1046/j.1462-2920.2003.00404.x
Bünemann EK, Schwenke GD, Van Zwieten L (2006) Impact of agricultural inputs on soil organisms – a review. Aust J Soil Res 44:379–406. doi:10.1071/SR05125
Calderón FJ, Jackson LE, Scow KM, Rolston DE (2000) Microbial responses to simulated tillage
and in cultivated and uncultivated soils. Soil Biol Biochem 32:1547–1559. doi:10.1016/
S0038-0717(00)00067-5
Clapperton MJ, Janzen HH, Johnston AM (1997) Suppression of VAM fungi and micronutrient
uptake by low-level P fertilization in long-term wheat rotations. Am J Alternat Agric 12:59–63
Coleman DC, Dighton J, Ritz K, Giller KE, Ritz K, Dighton J, Giller KE (1994) Perspectives on the
compositional and functional analysis of soil communities. In: Ritz K, Dighton J, Giller KE
(eds) Beyond the biomass: compositional and functional analysis of soil microbial communities.
Wiley, Toronto, ON, pp 261–271
Cookson WR, Murphy DV, Roper MM (2008) Characterizing the relationships between soil
organic matter components and microbial function and composition along a tillage disturbance
gradient. Soil Biol Biochem 40:763–777. doi:10.1016/j.soilbio.2007.10.011
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 237
Cruz C, Green JJ, Watson CA, Wilson F, Martins-Loução MA (2004) Functional aspects of root
architecture and mycorrhizal inoculation with respect to nutrient uptake capacity. Mycorrhiza
14:177–184. doi:10.1007/s00572-003-0254-5
Davis J, Abbott L (2006) Soil fertility in organic farming systems. In: Kristiansen P, Taji A,
Reganold J (eds) Organic agriculture: a global perspective. Comstock Publishing Associates,
Ithaca, NY, pp 25–51
De Neve S, Sáez SG, Daguilar BC, Sleutel S, Hofman G (2004) Manipulating N mineralization
from high N crop residues using on- and off-farm organic materials. Soil Biol Biochem
36:127–134. doi:10.1016/j.soilbio.2003.08.023
Douds DD Jr, Galvez L, Franke-Snyder M, Reider C, Drinkwater LE (1997) Effect of compost
addition and crop rotation point upon VAM fungi, Agric Ecosyst Environ 65:257–266. doi:
10.1016/S0167-8809(97)00075-3
Douds DD, Millner P (1999) Biodiversity of arbuscular mycorrhizal fungi in agroecosystems.
Agric Ecosyst Environ 74:77–93. doi:10.1016/S0167-8809(99)00031-6
Drenovsky RE, Vo D, Graham KJ, Scow KM (2004) Soil water content and organic carbon availability are major determinants of soil microbial community composition. Microb Ecol
48:424–430. doi:10.1007/s00248-003-1063-2
Drinkwater LE, Letourneau DK, Workneh F, van Bruggen HC, Shennan C (1995) Fundamental
differences between conventional and organic tomato agroecosystems in California, Ecol Appl
5:1098–1112
Dunfield KE, Germida JJ (2003) Seasonal changes in the rhizosphere microbial communities
associated with field-grown genetically modified canola (Brassica napus). Appl Environ
Microbiol 69:7310–7318. doi:10.1128/AEM.69.12.7310-7318.2003
Dunfield KE, Germida JJ (2004) Impact of genetically modified crops on soil- and plant-associated microbial communities. J Environ Qual 33:806–815
Eason WR, Scullion J, Scott EP (1999) Soil parameters and plant responses associated with arbuscular mycorrhizas from contrasting grassland management regimes. Agric Ecosyst Environ
73:245–255. doi:10.1016/S0167-8809(99)00054-7
Entz MH, Guilford R, Gulden R (2001) Crop yield and soil nutrient status on 14 organic farms in
the eastern portion of the northern Great Plains. Can J Plant Sci 81:351–354
Entz MH, Penner KR, Vessey JK, Zelmer CD, Thiessen Martens JR (2004) Mycorrhizal colonization
of flax under long-term organic and conventional management. Can J Plant Sci 84:1097–1099
Evans DG, Miller MH (1990) The role of the external mycelial network in the effect of soil
disturbance upon vesicular–arbuscular mycorrhizal colonization of maize. New Phytol 114:
65–71. doi:10.1111/j.1469-8137.1990.tb00374.x
Fauci MF, Dick RP (1994) Soil microbial dynamics: short- and long-term effects of inorganic and
organic nitrogen. Soil Sci Soc Am J 58:801–806
Fließbach A, Mäder P (2000) Microbial biomass and size-density fractions differ between soils of
organic and conventional agricultural systems. Soil Biol Biochem 32:757–768. doi:10.1016/
S0038-0717(99)00197-2
Fließbach A, Mäder P, Insam H, Rangger A (1997) Carbon source utilization by microbial
communities in soils under organic and conventional farming practice. In: Insam H, Rangger
A (eds)Microbial communities – functional versus structural approaches. Springer, Berlin,
Germany, pp 109–120
Fraser DG, Doran JW, Sahs WW, Lesoing GW (1988) Soil microbial populations and activities
under conventional and organic management. J Environ Qual 17:585–590
Frostegård Å, Petersen SO, Bååth E, Nielsen TH (1997) Dynamics of a microbial community
associated with manure hot spots as revealed by phospholipid fatty acid analyses. Appl
Environ Microbiol 63:2224–2231
Galvez L, Douds DD Jr, Wagoner P (2001) Tillage and farming system affect AM fungus populations,
mycorrhizal formation, and nutrient uptake by winter wheat in a high-P soil. Am J Alternat
Agric 16:152–160
Galvez L, Douds DD Jr, Wagoner P, Longnecker LR, Drinkwater LE, Janke RR (1995) An overwintering cover crop increases inoculum of VAM fungi in agricultural soil. Am J Alternat
Agric 10:152–156
238
A.G. Nelson and D. Spaner
Garbeva P, Postma J, van Veen JA, van Elsas JD (2006) Effect of above-ground plant species on
soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3.
Environ Micro 8:233–246. doi:10.1111/j.1462-2920.2005.00888.x
Germida JJ, Siciliano SD (2001) Taxonomic diversity of bacteria associated with the roots of
modern, recent and ancient wheat cultivars. Biol Fertil Soils 33:410–415. doi:10.1007/
s003740100343
Giller KE, Beare MH, Lavelle P, Izac AMN, Swift MJ (1997) Agricultural intensification, soil
biodiversity and agroecosystem function. Appl Soil Ecol 6:3–16. doi:10.1016/S09291393(96)00149-7
Girvan MS, Bullimore J, Pretty JN, Osborn AM, Ball AS (2003) Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. Appl
Environ Microbiol 69:1800–1809. doi:10.1128/AEM.69.3.1800-1809.2003
Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic
farming. Agric Ecosyst Environ 113:17–35. doi:10.1016/j.agee.2005.09.009
Grayston SJ, Wang S, Campbell CD, Edwards AC (1998) Selective influence of plant species on
microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378. doi:10.1016/S00380717(97)00124-7
Griffiths BS, Kuan HL, Ritz K, Glover LA, McCaig AE, Fenwick C (2004) The relationship
between microbial community structure and functional stability, tested experimentally in an
upland pasture soil. Microb Ecol 47:104–113. doi:10.1007/s00248-002-2043-7
Habte M (2006) The roles of arbuscular mycorrhizas in plant and soil health. In: Uphoff N, Ball
AS, Fernandes ECM, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P (eds)
Biological approaches to sustainable soil systems. Taylor & Francis Group LLC, Boca Raton,
FL, pp 129–148
Hamel C (2004) Impact of arbuscular mycorrhizal fungi on N and P cycling in the root zone. Can
J Soil Sci 84:383–395
Hamel C, Strullu DG (2006) Arbuscular mycorrhizal fungi in field crop production: potential and
new direction. Can J Plant Sci 86:941–950
Harrier LA, Watson CA (2003) The role of arbuscular mycorrhizal fungi in sustainable cropping
systems. Adv Agron 79:185–225
Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties,
landraces, and ancestors. Can J Bot 70:2032–2040
Hetrick BAD, Wilson GWT, Cox TS (1993) Mycorrhizal dependence of modern wheat cultivars
and ancestors: a synthesis. Can J Bot 71:512–518
Hole DG, Perkins AJ, Wilson JD, Alexander IH, Grice PV, Evans AD (2005) Does organic farming
benefit biodiversity? Biol Conserv 122:113–130. doi:10.1016/j.biocon.2004.07.018
Huwe B, Titi AE (2003) The role of soil tillage for soil structure. In: El TiTi A (ed) Soil tillage in
agroecosystems. CRC Press, Washington, D.C., pp 27–50
IFOAM (2008) The definition of organic agriculture. International Federation of Organic Movements.
http://www.ifoam.org/growing_organic/definitions/doa/index.html. Accessed 17 March 2009
Jackson LE, Calderon FJ, Steenwerth KL, Scow KM, Rolston DE (2003) Responses of soil microbial processes and community structure to tillage events and implications for soil quality.
Geoderma 114:305–317. doi:10.1016/S0016-7061(03)00046-6
Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of
AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234.
doi:10.1007/s00572-002-0163-z
Johnsen K, Jacobsen CS, Torsvik V, Sorensen J (2001) Pesticide effects on bacterial diversity in
agricultural soils – a review. Biol Fertil Soils 33:443–453. doi:10.1007/s003740100351
Jordan N, Zhang J, Huerd S (2000) Arbuscular–mycorrhizal fungi: potential roles in weed management. Weed Res 40:397–410. doi:10.1046/j.1365-3180.2000.00207.x
Kabir Z (2005) Tillage or no-tillage: impact on mycorrhiza. Can J Plant Sci 85:23–29
Kabir Z, Koide RT (2000) The effect of dandelion or a cover crop on mycorrhiza inoculum potential, soil aggregation and yield of maize. Agric Ecosyst Environ 78:167–174. doi:10.1016/
S0167-8809(99)00121-8
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 239
Kabir Z, O’Halloran IP, Fyles JW, Hamel C (1997) Seasonal changes of arbuscular mycorrhizal
fungi as affected by tillage practices and fertilization: hyphal density and mycorrhizal root
colonization. Plant Soil 192:285–293. doi:10.1023/A:1004205828485
Kennedy AC, Gewin VL (1997) Soil microbial diversity: present and future considerations. Soil
Sci 162:607–617
Kennedy AC, Smith KL (1995) Soil microbial diversity and the sustainability of agricultural soils.
Plant Soil 170:75–86. doi:10.1007/BF02183056
Kladivko EJ (2001) Tillage systems and soil ecology. Soil Till Res 61:61–76. doi:10.1016/S01671987(01)00179-9
Klonsky K (2000) Forces impacting the production of organic foods. Agric Hum Values 17:233–
243. doi:10.1023/A:1007655312687
Koo B-J, Adriano DC, Bolan NS, Barton CD (2006) Root exudates and microorganisms. Curr
Opin Biotechnol 17:421–428. doi:10.1016/B0-12-348530-4/00461-6
Lampkin NH, Padel S (1994) Researching organic farming systems. In: Lampkin NH, Padel S
(eds) The economics of organic farming: an international perspective. CAB International,
Wallingford, Oxon, pp 27–43
Lee KE, Pankhurst CE (1992) Soil organisms and sustainable productivity. Aust J Soil Res
30:855–892. doi:10.1071/SR9920855
Liu B, Zeng Q, Yan F, Xu H, Xu C (2005) Effects of transgenic plants on soil microorganisms.
Plant Soil 271:1–13. doi:10.1007/s11104-004-1610-8
Lundquist EJ, Scow KM, Jackson LE, Uesugi SL, Johnson CR (1999) Rapid response of soil
microbial communities from conventional, low input, and organic farming systems to a wet/
dry cycle. Soil Biol Biochem 31:1661–1675. doi:10.1016/S0038-0717(99)00080-2
Lupwayi NZ, Rice WA, Clayton GW (1998) Soil microbial diversity and community structure
under wheat as influenced by tillage and crop rotation. Soil Biol Biochem 30:1733–1741.
doi:10.1016/S0038-0717(98)00025-X
Macey A (2006) Certified Organic Production in Canada 2005. [Online] Available: http://
www.cog.ca/documents/certifiedorganicproduction05E_000.pdf [March 16, 2008]
Mäder P, Edenhofer S, Boller T, Wiemken A, Niggli U (2000) Arbuscular mycorrhizae in a
long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol Fertil Soils 31:150–156. doi:10.1007/
s003740050638
Mäder P, Fließbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity
in organic farming. Science 296:1694–1697
Manske GGB (1990) Genetical analysis of the efficiency of VA mycorrhiza with spring wheat.
Agric Ecosyst Environ 29:273–280
Marschner P, Kandeler E, Marschner B (2003) Structure and functionl of the soil microbial community in a long-term fertilizer experiment. Soil Biol Biochem 35:453–461. doi:10.1016/
S0038-0717(02)00297-3
Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels
of salts. J Plant Nutr 26:125–137. doi:10.1081/PLN-120016500
Mohammad MJ, Pan WL, Kennedy AC (2005) Chemical alteration of the rhizosphere of the
mycorrhizal-colonized wheat root. Mycorrhiza 15:259–266. doi:10.1007/s00572-004-0327-0
Mosse B (1986) Mycorrhiza in a sustainable agriculture. Biol Agric Hortic 3:191–209
Neal JL, Larson RI, Atkinson TG (1972) Changes in rhizosphere populations of selected physiological groups of bacteria related to substitution of specific pairs of chromosomes in spring
wheat. Plant Soil 39:209–212. doi:10.1007/BF00018061
O’Donnell AG, Seasman M, Macrae A, Waite I, Davies JT (2001) Plants and fertilisers as drivers
of change in microbial community structure and function in soils. Plant Soil 232:135–145.
doi:10.1023/A:1010394221729
Oehl F, Sieverding E, Ineichen K, Mäder P, Boller T, Wiemken A (2003) Impact of land use
intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of central
Europe. Appl Environ Microbiol 69:2816–2824. doi:10.1128/AEM.69.5.2816-2824.2003
240
A.G. Nelson and D. Spaner
Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of
long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi.
Oecologia 138:574–583. doi:10.1007/s00442-003-1458-2
Parfitt RL, Yeates GW, Ross DJ, Mackay AD, Budding PJ (2005) Relationships between soil
biota, nitrogen and phosphorus availability, and pasture growth under organic and conventional
management. Appl Soil Ecol 28:1–13. doi:10.1016/j.apsoil.2004.07.001
Patriquin DG (1986) Biological husbandry and the “nitrogen problem”. Biol Agric Hortic 3:167–189
Peacock AD, Mullen MD, Ringelberg DB, Tyler DD, Hedrick DB, Gale PM, White DC (2001)
Soil microbial community responses to dairy manure or ammonium nitrate applications. Soil
Biol Biochem 33:1011–1019. doi:10.1016/S0038-0717(01)00004-9
Pimentel D, Hepperly P, Hanson J, Douds D, Seidel R (2005) Environmental, energetic, and economic comparisons of organic and conventional farming systems. BioScience 55:573–582.
doi:10.1641/0006-3568(2005) 055[0573:EEAECO]2.0.CO;2
Plenchette C, Clermont-Dauphin C, Meynard JM, Fortin JA (2005) Managing arbuscular mycorrhizal fungi in cropping systems. Can J Plant Sci 85:31–40
Plenchette C, Fortin JA, Furlan V (1983) Growth responses of several plant species to mycorrhiza
in a soil of moderate P-fertility. Plant Soil 70:199–209. doi:10.1007/BF02374780
Prasad R, Power JF (1997) Soil fertility management for sustainable agriculture. CRC Press LLC,
Boca Raton, FL
Rabatin SC, Stinner BR (1989) The significance of vesicular–arbuscular mycorrhizal fungal-soil
macroinvertebrate interactions in agroecosystems. Agric Ecosyst Environ 27:195–204.
doi:10.1016/0167-8809(89)90085-6
Rejon A, Garcia-Romera I, Ocampo JA, Bethlenfalvay GJ (1997) Mycorrhizal fungi influence
competition in a wheat-ryegrass association treated with the herbicide diclofop. Appl Soil Ecol
7:51–57. doi:10.1016/S0929-1393(97)00025-5
Rillig MC (2004) Arbuscular mycorrhiza, glomalin, and soil aggregation. Can J Soil Sci
84:355–363
Ritson C, Oughton E (2007) Food consumers and organic agriculture. In: Frewer L, van Trijp H
(eds) Understanding consumers of food products. CRC Press, Boca Raton, FL, pp 254–272
Robertson GP, Grandy AS (2006) Soil system management in temperate regions. In: Uphoff N, Ball
AS, Fernandes ECM, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P (eds) Biological
approaches to sustainable soil systems. Taylor & Francis Group LLC, Boca Raton, FL, pp 27–39
Ryan MH, Chilvers GA, Dumaresq DC (1994) Colonization of wheat by VA-mycorrhizal fungi
was found to be higher on a farm managed in an organic manner than on a conventional neighbour. Plant Soil 160:33–40. doi:10.1007/BF00150343
Ryan MH, Derrick JW, Dann PR (2004) Grain mineral concentrations and yield of wheat grown
under organic and conventional management. J Sci Food Agric 84:207–216. doi:10.1002/
jsfa.1634
Ryan MH, Graham JH (2002) Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271. doi:10.1023/A:1020207631893
Sahota M, Willer H, Yussefi M (2004) Overview of the global market for organic food and drink.
In: Willer H, Yussefi M (eds) The world of organic agriculture: statistics and emerging trends
2004. IFOAM, Bonn, Germany, pp 21–26
Salisbury FB, Ross CW (1992) Plant physiology. Wadsworth, Belmont, CA
Sattelmacher B, Reinhard S, Pomikalko A (1991) Differences in mycorrhizal colonization of rye
(Secale cereale L.) grown in conventional or organic (biological-dynamic) farming systems.
J Agron Crop Sci 167:350–355
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm.
Ecology 85:591–602. doi:10.1890/03-8002
Scullion J, Eason WR, Scott EP (1998) The effectivity of arbuscular mycorrhizal fungi from high
input conventional and organic grassland and grass-arable rotations. Plant Soil 204:243–254.
doi:10.1023/A:1004319325290
Seghers D, Top EM, Reheul D, Bulcke R, Boeckx P, Verstraete W, Siciliano SD (2003) Long-term
effects of mineral versus organic fertilizers on activity and structure of the methanotrophic
8 Cropping Systems Management, Soil Microbial Communities, and Soil Biological Fertility 241
community in agricultural soils. Environ Microbiol 5:867–877. doi:10.1046/j.1462-2920.
2003.00477.x
Seghers D, Siciliano SD, Top EM, Verstraete W (2005) Combined effect of fertilizer and herbicide
applications on the abundance, community structure and performance of the soil methanotrophic community. Soil Biol Biochem 37:187–193. doi:10.1016/j.soilbio.2004.05.025
Shannon D, Sen AM, Johnson DB (2002) A comparitive study of the microbiology of soils managed under organic and conventional regimes. Soil Use Manag 18:274–283. doi:10.1111/j.
1475-2743.2002.tb00269.x
Shepherd MA, Harrison R, Webb J (2002) Managing soil organic matter – implications for soil
structure on organic farms. Soil Use Manag 18:284–292
Siciliano SD, Germida JJ (1999) Taxonomic diversity of bacteria associated with the roots of
field-grown transgenic Brassica napus cv. Quest, compared to the non-transgenic B. napus cv.
Excel and B. rapa cv. Parkland. FEMS Microbiol Ecol 29:263–272. doi:10.1016/S01686496(99)00019-7
Siciliano SD, Theoret CM, de Freitas JR, Hucl PJ, Germida JJ (1998) Differences in the microbial
communities associated with the roots of different cultivars of canola and wheat. Can J
Microbiol 44:844–851
Song YN, Zhang FS, Marschner P, Fan FL, Gao HM, Bao XG, Sun JH, Li L (2007) Effect of
intercropping on crop yield and chemical and microbiological properties in rhizosphere of
wheat (Triticum aestivum L.), maize (Zea mays L.), and faba bean (Vicia faba L.). Biol Fertil
Soils 43:565–574. doi:10.1007/s00374-006-0139-9
Soule JD, Piper JK (1992) Farming in nature’s image. Island Press, Washington D.C.
Stark CHE, Condron LM, Stewart A, Di HJ, O’Callaghan M (2004) Small-scale spatial variability
of selected soil biological properties. Soil Biol Biochem 36:601–608. doi:10.1016/j.
soilbio.2003.12.005
Stark C, Condron LM, Stewart A, Di HJ, O’Callaghan M (2007) Influence of organic and mineral
amendments on soil microbial properties and processes. Appl Soil Ecol 35:79–93. doi:10.1016/j.
apsoil.2006.05.001
Stejskalova H (1990) The role of mycorrhizal infection in weed–crop interactions. Agric Ecosyst
Environ 29:415–419. doi:10.1016/0167-8809(90)90308-Z
Stewart LI, Hamel C, Hogue R, Moutoglis P (2005) Arbuscular mycorrhizal inoculated strawberry
plant responses in a high soil phosphorus rotation crop system. Mycorrhiza 15:612–619.
doi:10.1007/s00572-005-0003-z
Stockdale EA, Shepherd MA, Fortune S, Cuttle SP (2002) Soil fertility in organic farming systems –
fundamentally different? Soil Use Manag 18:301–308. doi:10.1111/j.1475-2743.2002.tb00272.x
Sturz AV, Christie BR, Matheson BG (1998) Associations of bacterial endophyte populations from
red clover and potato crops with potential for beneficial allelopathy. Can J Microb 44:162–167
Suzuki C, Kunito T, Aono T, Liu C-T, Oyaizu H (2005) Microbial indices of soil fertility. J Appl
Microbiol 98:1062–1074. doi:10.1111/j.1365-2672.2004.02529.x
Sylvia DM (2005) Mycorrhizal symbioses. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA
(eds) Principles and applications of soil microbiology. Pearson Prentice Hall, Upper Saddle
River, NJ, pp 263–282
Tawaraya K (2003) Arbuscular mycorrhizal dependency of different plant species and cultivars.
Soil Sci Plant Nutr 49:655–668
Thies JE, Grossman JM (2006) The soil habitat and soil ecology. In: Uphoff N, Ball AS, Fernandes
ECM, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P (eds) Biological approaches
to sustainable soil systems. Taylor & Francis Group LLC, Boca Raton, FL, pp 59–78
Uphoff N, Ball AS, Fernandes ECM, Herren H, Husson O, Palm C, Pretty J, Sanginga N, Thies JE
(2006) Understanding the functioning and management of soil systems. In: Uphoff N, Ball AS,
Fernandes ECM, Herren H, Husson O, Laing M, Palm C, Pretty J, Sanchez P (eds) Biological
approaches to sustainable soil systems. Taylor & Francis Group LLC, Boca Raton, FL, pp 3–13
Vandermeer J, van Noordwijk M, Anderson J, Ong C, Perfecto I (1998) Global change and multispecies agroecosystems: concepts and issues. Agric Ecosyst Environ 67:1–22. doi:10.1016/
S0167-8809(97)00150-3
242
A.G. Nelson and D. Spaner
Vatovec C, Jordan N, Huerd S (2005) Responsiveness of certain agronomic weed species to arbuscular mycorrhizal fungi. Renew Agric Food Syst 20:181–189. doi:10.1079/RAF2005115
von Fragstein M, Niemsdorff P, Kristiansen P (2006) Crop agronomy in organic agriculture. In:
Kristiansen P, Taji A, Reganold J (eds) Organic agriculture: a global perspective. Comstock
Publishing Associates, Ithaca, NY, pp 53–82
Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat
selective factors influencing the structural composition and functional capacity of microbial
communities in agricultural soils. Soil Biol Biochem 40:803–813. doi:10.1016/j.soilbio.
2007.10.015
Wander MM, Hedrick DS, Kaufman D, Traina SJ, Stinner BR, Kehrmeyer SR, White DC (1995)
The functional significance of the microbial biomass in organic and conventionally managed
soils. Plant Soil 170:87–97. doi:10.1007/BF02183057
Wander MM, Traina SJ, Stinner BR, Peters SE (1994) Organic and conventional management
effects on biologically active soil organic matter pools. Soil Sci Soc Am J 58:1130–1139
Watson CA, Atkinson D, Gosling P, Jackson LR, Rayns FW (2002) Managing soil fertility in
organic farming systems. Soil Use Manag 18:239–247. doi:10.1111/j.1475-2743.2002.
tb00265.x
Weil RR, Lowell KA, Shade HM (1993) Effects of intensity of agronomic practices on a soil
ecosystem. Am J Alternat Agric 8:5–14
Welbaum GE, Sturz AV, Dong Z, Nowak J (2004) Managing soil microorganisms to improve productivity of agro-ecosystems. Crit Rev Plant Sci 23:175–193. doi:10.1080/07352680490433295
Werner MR, Dindal DL (1990) Effects of conversion to organic agricultural practices on soil biota.
Am J Alternat Agric 5:24–32
Wu T, Chellemi DO, Martin KJ, Graham JH, Rosskopf EN (2007) Discriminating the effects of
agricultural land management practices on soil fungal communities. Soil Biol Biochem
39:1139–1155. doi:10.1016/j.soilbio.2006.11.024
Xu X, Ouyang H, Kuzyakov Y, Richter A, Wanek W (2006) Significance of organic nitrogen
acquisition for dominant plant species in an alpine meadow on the Tibet plateau, China. Plant
Soil 285:221–231. doi:10.1007/s11104-006-9007-5
Yang YH, Yao J, Hu S, Qi Y (2000) Effects of agricultural chemicals on DNA sequence diversity
of soil microbial community: a study with RAPD marker. Microb Ecol 39:72–79. doi:10.1007/
s002489900180
Yeates GW, Bardgett RD, Cook R, Hobbs PJ, Bowling PJ, Potter JF (1997) Faunal and microbial
diversity in three Welsh grassland soils under conventional and organic management regimes.
J Appl Ecol 34:453–470
Yiridoe EK, Bonti-Ankomah S, Martin RC (2005) Comparison of consumer perceptions and
preference toward organic versus conventionally produced foods: a review and update of the
literature. Renew Agric Food Syst 20:193–205. doi:10.1079/RAF2005113
Zaller JG, Köpke U (2004) Effects of traditional and biodynamic farmyard manure amendment on
yields, soil chemical, biochemical and biological properties in a long-term field experiment.
Biol Fertil Soils 40:222–229. doi:10.1007/s00374-004-0772-0
Chapter 9
Cyanobacterial Reclamation
of Salt-Affected Soil
Nirbhay Kumar Singh and Dolly Wattal Dhar
Abstract Salinity has been an important historical factor which has influenced
the life span of agricultural systems. Around 10% of the total cropped land surface is covered with different types of salt-affected soils and the Asian continent accounts for the largest area affected by the salinity of various intensities.
Cyanobacteria are capable of not only surviving, but thriving in conditions which
are considered to be inhabitable, tolerating desiccation, high temperature, extreme
pH and high salinity, illustrating their capacity to acclimatise to extreme environments. Until recently, the responses of cyanobacteria to salinity stresses were poorly
documented as compared to heterotrophic bacteria and phototrophic eukaryotic
algae. Cyanobacteria can be used to reclaim alkaline soils and fertility can be
improved for subsequent cultivation of cereal crops, sugarcane and horticultural
crops. Therefore we present here a review on cyanobacterial reclamation of saltaffected soil.
Substantial progress has been made towards better understanding of the
physiological mechanisms responsible for salinity tolerance and osmotic adjustment in cyanobacteria. Many researchers throughout the world have worked on
probable mechanisms of salt tolerance studies in cyanobacteria. These organisms evolved about 3,000 million years ago and are considered to be the
primary colonisers of the inhospitable ecosystems. The physiological aspects
for the adaptation of cyanobacteria to high salinities include (a) synthesis and
N.K. Singh (*)
Department of Microbiology, C.P. College of Agriculture, S.D.A.U., S.K. Nagar,
Gujarat-385506, India
e-mail: nirbhaysingh78@gmail.com
D.W. Dhar
Centre for Conservation and Utilization of Blue Green Algae (CCUBGA),
IARI, New Delhi-110012, India
e-mail: dollywattaldhar@yahoo.com
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_9, © Springer Science+Business Media B.V. 2010
243
244
N.K. Singh and D.W. Dhar
accumulation of osmoprotective compounds, (b) maintenance of low internal
concentrations of inorganic ions and (c) expression of a set of salt-stress proteins. Exposure of cyanobacterial cells to different abiotic stresses resulted in
rapid expression of several stress-regulated proteins and modifications in protein synthesis programme. The synthesis of organic solutes like disaccharides
(sucrose, trehalose and glucosyl glycerol), quaternary amines (glycine betaine)
and free amino acids (glutamine) are well-documented. The protection against
alkaline environment is provided by the synthesis of specific fatty acids,
sucrose- and osmotic-stress-induced proteins. In cyanobacteria, accumulation
of internal osmoticum in the form of inorganic ions and prevention of intracellular Na+ accumulation by the curtailment of Na influx and by efficient active
efflux mechanisms or metabolic adjustments have been investigated in depth.
The Na+ extrusion in cyanobacteria is driven by a Na+/H+ antiporter, which is
energised by enhanced activity of cytochrome oxidase. The inhibition of
sodium ion influx appears to be a major mechanism for the survival of
cyanobacteria against salt stress and synthesis of salt-stress proteins have been
found in cyanobacteria. These organisms have been recognised as an important
agent in the stabilisation of soil surfaces primarily through the production of
extracellular polysaccharides which are prominent agents in the process of
aggregate formation and increase in soil fertility. Cyanobacterial application
results in the enrichment of soil with fixed nitrogen, soil structure improvement
and declining trend of pH, electrical conductivity (EC) and Na+. The extracellular polysaccharides excreted by cyanobacteria have been reported to be
responsible for binding of soil particles, thus, leading to the formation of a
tough and entangled superficial structure that improves the stability of soil surface and protects it from erosion. The potential impact of these organisms on
agriculture through their use as soil conditioners, plant growth regulators and
soil health ameliorators has been well-recognised. Besides bringing about an
improvement in the yield of rice, cyanobacteria produce direct and indirect
beneficial changes in the physical, chemical and biological properties of soil
and soil–water interface in the rice fields, which are of agronomic importance. Certain cyanobacteria have been found not only to grow in saline ecosystems but also improve the physico-chemical properties of the soil by enriching
them with carbon, nitrogen and available phosphorus. Flushing of field may not
be effective for the reclamation of saline soils and the addition of cyanobacterium inoculum along with the addition of gypsum is required before irrigation
to ameliorate saline soils. Nitrogen-fixing cyanobacteria can be used as biological input to improve soil texture, conserve moisture, scavenge the toxic sodium
cation from the soil complex and improve the properties of soils. Virtually negligible information exists on the genetics of cyanobacterial halotolerance. The
presence of combined nitrogen which effectively curtails sodium accumulation
and supports extra nitrogen demand for osmoregulation during slat stress confers considerable salt tolerance on cyanobacteria.
9
Cyanobacterial Reclamation of Salt-Affected Soil
245
Keywords Cyanobacteria • saline/alkaline • reclamation • technology • crop
response • blue-green algae • salt stress
9.1 Introduction
Salt stress is one of the most serious factors limiting the productivity of crops including
staple diet in many countries. Around 10% of the total cropped land surface is
covered with different types of salt-affected soils (Boyer 1982; Nelson et al. 1998).
Such soils are distributed throughout the world including deserts, plains, coastal
areas, river valleys, and over-irrigated lands. The Asian continent accounts for the
largest area (410 million hectares) affected by salinity of various intensities (Szabolcs
1993). In arid and semi-arid regions of the world, salt-affected soils can be primarily
divided into saline and alkaline soils. Salinity and alkalinity are the major problems
associated with soil management in arid and semi-arid regions of the world (Szabolcs
1979). Saline soils are the soils that have developed due to the influence of sodium
salt (mainly NaCl or Na2SO4) whereas alkaline soils have developed mainly due to
the influence of Na2CO3 and NaHCO3 (Szabolcs 1993). The saturated pH of saline
soil is less than 8.5 and the electrical conductivity is generally more than 4.0 dS m−1
whereas pH of alkaline soil is more than 8.5 and electrical conductivity is less than
4.0 dS m−1 at 25°C. Saline soils are not suitable for crop production although they
have high agricultural potential. Salt-affected soils generally contain sufficient
neutral soluble salts in the root zone and adversely affect crop growth and production.
Soluble salts are predominantly the chlorides and sulphates of sodium, calcium and
magnesium of which sodium chloride is the dominant salt (Hashem 2001). Alkaline
(sodic) soils have a high pH and exchangeable sodium (ES), measurable amounts of
carbonates, and undergo extensive clay dispersion leading to poor hydraulic conductivity
and reduced soil aeration resulting in poor crop production in such soils. Different
types of factors which cause crop stress under salt-affected areas have been reported
in literature (Gupta and Abrol 1990).
Blue-green algae or cyanobacteria have been reported to grow extensively on alkaline or ‘usar’ soils in India (Singh 1950) and on the saline soils of the USSR (Gollerbach
et al. 1956). These are capable of not only surviving, but thriving in conditions which are
considered to be inhabitable, tolerating desiccation, high temperatures, extreme pH and
high salinity, illustrating their capacity to acclimatise to extreme environments (Stal
2007). Cyanobacteria can be used to reclaim alkaline soils and fertility can be improved
for subsequent cultivation of cereals crops, sugarcane and horticultural crops (Singh
1950, 1961; Aziz and Hashem 2003). A large number of researchers throughout the
world have worked on probable mechanisms of salt tolerance studies in cyanobacteria
and lot of information has been generated (Pandhal et al. 2008). Cyanobacterial reclamation of salt-affected soil is moreover a neglected field and very little work has been
done in this context; however, the main thematic areas on which salt studies in
cyanobacteria are centred can be grouped into four major classes (Table 9.1).
246
N.K. Singh and D.W. Dhar
Table 9.1 Main thematic areas for salt-related studies in cyanobacteria
Thematic areas for salt-related studies
in cyanobacteria
References
1. Biochemical- and physiologyTang et al. 2007; Wiangnon et al. 2007; Bhadauriya
based studies
et al. 2007; Abhishek et al. 2006; Ferjani et al.
2003; Hagemann et al. 1994; Marin et al. 2002,
2003; Singh et al. 2002; Kempf and Bremer
1998; Mikkat et al. 1997; Reed et al. 1986;
Gabbay-Azaria and Tel-Or 1993; Roberts 2005
2. Salt intake and cell signalling
Elanskaya et al. 2002; Shoumskaya et al. 2005; Buck
and Smith 1995; Waditee et al. 2001, 2002; Apte
et al. 1987; Reed et al. 1984; Reddy et al. 1989;
Hagemann and Marin 1999; Mikkat et al. 1996
Billini et al. 2008; Marin et al. 2004; Vinnemeier et al.
3. Gene level responses, e.g. salt1998; Bohnert et al. 2001; Kanesaki et al. 2002;
regulated genes, microarrays,
Marin et al. 1998; Miao et al. 2003; Chauhan et al.
mutational analysis of salt
1999; Joset et al. 1996; Karandashova et al. 2002
tolerance determinants
4. Post-genomics
Fulda et al. 1999, 2000, 2006; Hagemann et al. 2001;
Hagemann and Erdmann 1994; Pinner et al. 1992;
Huang et al. 2006
9.2 Cyanobacterial Distribution in Salt-Affected Ecosystems
Cyanobacteria, both heterocystous and non-heterocystous, evolved about 3,000 million years ago and are considered to be the primary colonisers of inhospitable ecosystems (Fig. 9.1). One of the most unique features of these organisms is their
versatile occurrence (Brock 1973). Due to their early evolutionary history, cyanobacteria occur abundantly in a wide range of habitats, including saline soils and coastal
swamps (Amsaveni 1995; Komarek 1998; Hoffmann 1989). The predominant genera that are ubiquitous in tropical soils are Anabaena, Aulosira, Calothrix, Nostoc,
Plectonema and Westiellopsis, while localised distribution of Haplosiphon, Scytonema
and Cylindrospermum has also been reported (Gopalaswamy et al. 2007). The
microbes which have growth optima above pH 9.0 and require salt for growth have
been termed as alkalophilic or halophilic and those which have growth optima below
pH 9.0 but can survive extended exposure above it and can tolerate high salt concentration have been termed halotolerant (Hoffmann 1989). The occurrence of
cyanobacteria in saline/alkaline soil has been described by many workers (Singh
1950, 1961; Ali and Sandhu 1972). Cyanobacteria, particularly belonging to the
genera Anabaena, Synechocystis and Aphanothece, have been classified into three
groups relating to their salt tolerance: salt sensitive (or stenohaline), moderately
halotolerant, and extremely halotolerant (Reed and Stewart 1988; Pandhal et al.
2008). pH is particularly considered an important factor in influencing cyanobacterial distribution and abundance in soil (Sardeshpande and Goyal 1981). These organisms initially appear on land after the first shower of monsoon and prefer neutral to
slightly alkaline conditions (Singh 1978). The sequence of cyanobacterial appearance in an alkaline (saline) soil having monsoon type of character indicated their
dominance in such soils (Whitton and Potts 2000; Pandey et al. 2005). A large
9
Cyanobacterial Reclamation of Salt-Affected Soil
247
Fig. 9.1 Heterocystous halotolerant cyanobacteria (a) Cylindrospermum; (b) Aulosira; (c) Scytonema;
(d) Anabaena; (e) Haplosiphon; (f) Westiellopsis. Non-heterocystous halotolerant cyanobacteria
(g) Plectonema; (h) Phormidium; (i) Oscillatoria; (j). Lyngbya; (k) Microcystis; (l) Synechocystis
248
N.K. Singh and D.W. Dhar
n umber of cyanobacterial strains, irrespective of their morphological organisation,
ecological distribution and nature of carbon and nitrogen nutrition, have potential to
scavenge toxic sodium (Na+) cation from the soil and subsequently improve soil
properties (Kratz and Myers 1955). Cyanobacteria have been found to differ considerably in their ability to resist salt stress (Apte and Thomas 1983).
9.3 Uptake of Na+ and Ca2+ Salts by Cyanobacteria
9.3.1 Na+ Uptake
Although cyanobacteria are known to require Na+ for growth (Allen and Arnon
1955) and nitrogen fixation (Apte and Thomas 1980), the exact physiological
processes involved in their salt tolerance are not yet known. The ability to absorb
Na+ have been studied in a freshwater cyanobacterium Anabaena L-31 and a saline
form Anabaena torulosa (Apte and Thomas 1974). The kinetics of Na+ transport in
these cyanobacteria as revealed by the use of radiotracer 22Na+ suggested that their
Na+ transport properties are better suited for their survival in such environments.
There have been several reports emphasising the need for Na+ by cultures of
many unicellular non-diazotrophs, e.g. Chroococcus sp. (Emerson and Lewis
1942), Anacystis nidulans (Kratz and Myers 1955) and Microcystis aeruginosa
(McLachlan and Gorham 1961) as well as the diazotrophic filamentous cyanobacteria
Anabaena variabilis, Nostoc muscorum (Kratz and Myers 1955) and Anabaena
cylindrica (Brownell and Nicholas 1967). Allen and Arnon (1955) reported Na+
requirement by cyanobacteria lies in the range of 1–5 ppm (17–85 mM) whereas
Kratz and Myers (1955) found a much higher requirement (680 mM). About 20–25
mM was the minimum level of Na+ required for detectable N2-supported growth of
both the freshwater and brackish water cyanobacterium (Apte and Thomas 1984).
In Anacystis nidulans, Na+ transport has been shown to be regulated by an active
extrusion of the cation by a proton antiport system (Dewar and Barber 1973;
Paschinger 1977). Na+ influx in A. torulosa and Anabaena L-31 is probably a
passive-carrier-mediated diffusion process while the regulation of Na+ transport is
achieved by an active extrusion of Na+. The Na+ extrusion appears to be mediated
by a Na+–K+ ATPase which is distinct from the conventional F1-F0 ATPase
(Paschinger 1977; Heefner and Harold 1982). In A. torulosa, Na+ uptake saturates
quickly, follows Michaelis-Mentor kinetics and shows a high affinity for Na+.
Anabaena L-31 also shows a Michaelis-Mentor type of rapid uptake but it has a
much lower affinity for Na+ than A. torulosa. The difference in Km is probably in
accordance with the metabolic requirement of Na+ in a brackish water and a freshwater form (Apte and Thomas 1983). Salt-tolerance of Anabaena torulosa resembles
those of glycophytes rather than halophytes. It is known that organic acids, amino
acids or carbohydrates accumulate under stress to build up the osmotic potential
(Flowers et al. 1977). High nitrogenase activity favouring enhanced accumulation
9
Cyanobacterial Reclamation of Salt-Affected Soil
249
of amino acids for better osmoregulation and ability of mat formation and sporulation
can contribute to the success of this cyanobacterium in saline environment (Fernandes
and Thomas 1982).
9.3.2 Ca2+ Uptake
Calcium is required by cyanobacteria for heterocyst differentiation, nitrogen fixation
(Chen et al. 1988; Smith et al. 1987), PS-II activity (Baker and Brand 1985;
England and Evans 1983; Piccioni and Mauzerall 1978), and for phosphate uptake
(Keurson et al. 1984). Ca2+ transports in bacteria occur through two routes of cation
transport, import and export. Import of Ca2+ via a uniporter or a leak is driven by
the membrane potential across the membrane. Export of Ca2+ occurs against the
membrane potential and often against concentration gradient (Rosen 1982).
The Ca2+ uptake kinetics is influenced by the different concentrations of cation
itself, light, ATP, specific inhibitors/uncouplers, and calcium antagonist, agonist,
and calmodulin antagonists in the cyanobacterium (Pandey et al. 1996).
The cyanobacterial cells remove Ca2+ from the medium in two possible ways, the
first involving rapid binding/uptake of metal cation (first 10 min) followed by the
slower second phase of 1 h (Pandey et al. 1996). Similar biphasic cation uptake has
also been reported in yeast (Norris and Kelly 1977) and cyanobacteria (Khummongkol
et al. 1982). A number of experiments reported that cyanobacteria exhibit a concentration-dependent uptake of Ca2+ (Shehata and Whitton 1982; Singh 1985).
Ca2+ uptake in Nostoc is an energy-dependent process (Pandey et al. 1996).
Light-dependent Ca2+ uptake is similar to those for Cu2+ and Hg2+ uptake in Nostoc
calcicola (Pandey and Singh 1993; Verma and Singh 1990), in contrast to cadmium
uptake in Anacystis nidulans (Singh and Yadav 1985) and Al uptake in Anacystis
nidulans (Pettersson et al. 1986), where metal uptake was independent of light. The
vital role in active ion transport played by PSII-mediated energy generation is
reported in the membrane vesicles of Anabaena variables (Lockau and Pfeffer
1983).
The deficiency of calcium resulted in disruption of the outer membrane, irreversible
reduction in swimming speed, changes in the morphology of the cell surface and
appearance of carotenoid-containing subcellular particles in the medium containing
motile Synechococcus strain (Brahamsha 1996) and in a non-motile freshwater
Synechococcus species (Resch and Gibson 1983). The addition of calcium restored
motility to the level of untreated cells. This effect was specific as no other divalent
ion tested could substitute for calcium. The plot of motility restoration was a steep
sigmoid, indicating that the binding or effect of calcium is highly cooperative (Tisa
et al. 1993; Tisa and Adler 1995). It is thought that this action potential is used to
communicate the reversal signal to all the cells in the trichome (Murvanidze and
Glagolev 1982). Womack et al. (1989) showed that calcium is required both for
gliding (0.1–0.3 mM) and induction (1 mM) of the gliding machinery in
myxobacteria.
250
N.K. Singh and D.W. Dhar
9.4 Mechanisms of Salt Tolerance in Cyanobacteria
Cyanobacteria are able to tolerate stresses predominant in salt-affected soils such as
nutrient deficiency, salinity, drought and temperature up-shift (Apte et al. 1997). Adaptation
to salt stress in cyanobacteria consists of at least three phenomena: (a) accumulation of
internal osmoticum in the form of inorganic ions (Miller 1976) or organic solutes
(Blumwald et al. 1983; Mackay et al. 1983; Reed et al. 1984); (b) contribution of ion
transport processes (Apte et al. 1987; Apte and Thomas 1983, 1986; Reed et al. 1985;
Reed and Stewart 1985; Thomas and Apte 1984); and (c) metabolic adjustments
(Blumwald and Tel-Or 1984; Thomas and Apte 1984). Several workers have pointed
out the various mechanisms adopted by cyanobacteria for salt tolerance (Table 9.2).
Table 9.2 Mechanisms adopted for salt tolerance by cyanobacteria
Mechanisms for salt tolerance
References
1. Production of stressApte and Bhagwat 1989; Bhagwat and Apte 1989; Iyer
responsive protein
et al. 1994; Apte et al. 1998; Hengge-Aronis 1993;
Nystrom and Neidhardt 1993; Volker et al. 1994;
Huang et al. 2006; Wilkinson and Northcote 1980;
Fulda et al. 2000; Kroll et al. 2001; Pandhal et al.
2008
2. Restricted entry of Na+
Roychoudhury et al. 1985; Jha et al. 1987; Kaushik and
Nagar 1993; Jha and Kaushik 1988; Hu et al. 2003;
Acea et al. 2003; Pandey et al. 2005; Singh 1950;
Thomas 1978; Malam et al. 2007; Nisha et al. 2007
3. Na+ Efflux
Paschinger 1977; Heefner and Harold 1982; Apte and
Thomas 1983; Ardelean 1966; Thomas and Apte 1984;
Krulwich 1983; Waditee et al. 2001, 2002; Padan and
Schuldiner 1996; Krulwich and Guffanti 1989; Espie and
Kandasamy 1994; Mochizuki-Oda and Oosawa 1985
4. Na+-dependent K+ Uptake
Bray 1997; Shinozaki and Yamaguchi-Shinozaki 1997;
in prokaryotes
Bremer and Kramer 2000; Hasegawa et al. 2000;
Morbach and Kramer 2002; Reed and Stewart 1985;
Dinnbier et al. 1988; Record et al. 1998; Whatmore et al.
1990; Whatmore and Reed 1990; Holtmann et al. 2003;
Bakker 1993; Stumpe et al. 1996; Oren 1999; Reed et al.
1985; Marin et al. 1998; Ferjani et al. 2003; Berry et al.
2003; Matsuda et al. 2004; Mikami et al. 2002; Suzuki
et al. 2000.
5. Compatible solutes and
Goel et al. 1997; Mackay et al. 1984; Reed et al. 1986; Joset
lipids in salt tolerance
et al. 1996; Hagemann and Erdmann 1997; Hagemann
et al. 1987, 2001; Erdmann et al. 1992; Mikkat and
Hagemann 2000; Deshnium et al. 1995, 1997; Ishitani
et al. 1995; Nakamura et al. 1997; Hufleijt et al. 1990;
Khamutov et al. 1990; Ritter and Yopp 1993; Tasaka
et al. 1996; Allakhverdiev et al. 1999, 2000a, b, 2001;
Singh et al. 2002; Blumwald et al. 1984; Padan and
Schuldiner 1994; Kates et al. 1984; Kamada et al. 1995
Apte et al. 1987; Reddy et al. 1989; Cheeseman and Delvin
6. Enhancement of
1985; Suput 1984; Sprott et al. 1984.
Cyanobacterial Salt Tolerance
by Combined Nitrogen
9
Cyanobacterial Reclamation of Salt-Affected Soil
251
9.4.1 Role of Stress-Responsive Proteins
The polypeptides induced in response to high NaCl content is referred to as Ionic
Stress Proteins (ISPs) and by heat stress are called Heat Shock Proteins (HSPs).
Stress proteins induced both by high NaCl and sucrose but not by heat shock are
called Osmotic Stress Proteins (OSPs). There are some commonly induced proteins
by heat, salinity as well as osmotic stress and these are called General Stress
Proteins (GSPs). Thus, large number of proteins described as ISPs, HSPs or OSPs,
etc. actually belong to the category of GSPs (Apte and Bhagwat 1989; Bhagwat and
Apte 1989; Iyer et al. 1994). These stress proteins are generally expressed at low
levels and for a short period (Apte et al. 1998). Many of the starvation-induced
proteins overlap with proteins synthesised under heat shock, high osmolarity, nitrogen
and phosphate starvation, exposure to heavy metals and other stresses and interfere
with the flow of carbon in the central catabolic pathway of carbon breakdown
(Hengge-Aronis 1993; Nystrom and Neidhardt 1993; Volker et al. 1994). Some of
the stress-tolerance mechanisms are expressed at all times and are used to encounter
some frequently encountered stresses, e.g. low-level constitutive expression of
major Heat Shock Proteins (HSPs). On the other hand, most of the adaptive nature of
responses remains shutting off under normal conditions of growth and are expressed
in a need-based manner (Apte et al. 1998).
Exposure of cyanobacterial cells to different abiotic stresses resulted in rapid
expression of several stress-regulated proteins and modifications in protein synthesis
programme (Iyer et al. 1994). The expression of almost all the abiotic stress-induced
proteins in Anabaena appears to be brought about by transcriptional activation of
stress-responsive genes and even a mild change in growth conditions significantly
alters the protein synthesis pattern in cyanobacteria (Apte et al. 1998).
Many proteins from the plasma membrane associated with salt stress were
screened for proteomic changes in the plasma membranes of Synechocystis in
response to salt (Huang et al. 2006). Increases in phosphate and nitrite/nitrate
binding proteins have been hypothesised as a necessity for cells to overcome
salt-induced nutrient deficiency, a problem resulting from plasma membrane
structural changes (Wilkinson and Northcote 1980). Further salt-induced proteins,
thought to play significant roles in stress, included vesicle-inducing protein
(Kroll et al. 2001); membrane-bound peptidyl-prolyl isomerase B, which could
be involved in maintaining the integrity of proteins in the plasma membrane and
CoxB, which plays a role in managing photosynthesis in stressed cells (Fulda
et al. 2006).
Nitrate induces Osmotic Stress Proteins expression and this is related to the
enhanced osmotolerance exhibited by nitrogen-supplemented Anabaena cultures
(Iyer et al. 1994). Most salt-related cyanobacterial proteomic studies have utilised the
model organism Synechocystis sp. PCC6803. At 2–4% w/v NaCl concentrations this
organism is reported to respond and adapt to the salt stress through synthesis of
general and specific stress proteins, altering the protein composition of extracellular
layers, and re-directing control of complex central intermediary pathways (Pandhal
et al. 2008).
252
N.K. Singh and D.W. Dhar
9.4.2 Restricted Entry of Na+
Cyanobacteria respond to high salinity in the soil by restricting the entry of sodium
ions and thus, preventing the cell injury by keeping a low internal concentration of
Na+ (Roychoudhury et al. 1985; Jha et al. 1987). A high level of Na+ adsorption in
presence of K+ over other cations could be a prelude to the greater uptake of
sodium, but it remained trapped in the polysaccharides (Kaushik and Nagar 1993).
The adsorption of various cations to the polysaccharides may be a purely passive
process; although a minor variation in the quantity of cations may be due to the
nature of polysaccharides (Jha and Kaushik 1988).
9.4.2.1 Polysaccharides
Cyanobacteria have been recognised as an important agent in the stabilisation of
soil surfaces primarily through the production of extracellular polysaccharides,
which are prominent agents in the process of aggregate formation and increase in
soil fertility (Hu et al. 2003; Acea et al. 2003; Pandey et al. 2005). Salt tolerance of
cyanobacteria has a potential biological utility in the reclamation of salt-affected
agricultural soils (Singh 1950). The advantage of this approach probably lies in the
apparent ability of cyanobacterial polysaccharides to ‘chelate’ considerable
amounts of Na+ and temporarily immobilise the excess Na+. However, the removal
of the algal-bound Na+ from soil ecosystems is a big challenge (Thomas 1978).
There are a large number of N-fixing cyanophyceae that produce extracellular
polysaccharides and this division offers potential for the development of soil
conditioners and significantly increased productivity (Malam et al. 2007). The amount
of polysaccharides produced was reported to increase with increasing NaC1
concentration in salt-tolerant Westiellopsis prolifica (Jha et al. 1987).
9.4.3 Na+ Efflux
An active Na+ efflux is driven by a Na+/H+ antiporter involving a proton translocating
ATPase in Anacystis nidulans (Paschinger 1977), and resembles that in Streptococcus
faecalis, where efflux is mediated by a Na+-stimulated ATPase which is insensitive
to several inhibitors of conventional ATPase (Heefner and Harold 1982). While
ATP-driven Na+ pump in S. faecalis requires only ATP and does not require proton
motive force, in Anabaena spp., Na+ efflux probably requires an H+ gradient.
Therefore, the ‘Na+ pump’ of Anabaena spp. can be described as a Na+/H+ or Na+/
K+ antiporter similar to Na+/H+ antiporter in A. nidulans but involving a ATPase
distinct from the conventional one. The energy source for Na+ extrusion may be
ATP derived from oxidative phosphorylation (Heefner and Harold 1982).
Maintenance of low intracellular Na+ concentrations and exclusion of Na+
appear to be responsible for the salt tolerance of Anabaena torulosa, a brackish
9
Cyanobacterial Reclamation of Salt-Affected Soil
253
water species (Apte and Thomas 1983). Presence of nitrate or ammonium severely
reduced influx and stimulated efflux of Na+ in Anabaena species (Thomas and Apte
1984). A higher respiratory activity was observed in light under salt-stress conditions
than in control, which suggests the involvement of respiratory activity in the extrusion
of Na+ ions outside the cell (Ardelean 1966).
Distinct from the enzyme-linked primary transport involving Na+ and related
processes, secondary active transport such as the Na+/H+ antiporter, first predicted by
Mitchell in 1966, has been since elucidated (Krulwich 1983). The Na+/H+ antiporter which
catalyses translocation of Na+ and H+ in opposite directions may operate in either direction
across the cell membrane. Moreover, movement of Na+ ions coupled to another metabolite
in the same direction by the symport mechanism also facilitates substrate transport
(Waditee et al. 2002). It is reported that Anabaena halophytica contains a Na+/H+
antiporter which can confer salt tolerance on the cells (Waditee et al. 2001).
During the generation of a pH gradient across the membrane, an increase in the
extracellular pH would lead to a decrease in the pH gradient and consequently the intracellular Na+ might also decrease. The observed increase of nitrate uptake at increasing extracellular pH might be accounted for by an increase of Na+-gradient
mediated by Na+/H+ antiporter. Indeed, the activity of Na+/H+ antiporter in
Anabaena halophytica has shown to increase with increasing pH (Waditee et al.
2001). A reduction of nitrate uptake was observed in Anabaena halophytica in the
presence of an inhibitor of Na+/H+ antiporter which shows the involvement of Na+/
H+ antiporter in the uptake of nitrate (Mochizuki-Oda and Oosawa 1985). The role of
Na+/H+ antiporter in the generation of sodium motive force to power Na+/solute
symport has also been proposed for the transport of anions across the membranes
(Krulwich and Guffanti 1989; Espie and Kandasamy 1994).
9.4.4 Na+-Dependent K+ Uptake in Prokaryotes
The condition of hyperosmolality caused by high salinity or drought constitutes a
major challenge to the growth of prokaryotes (Bray 1997; Shinozaki and
Yamaguchi-Shinozaki 1997; Bremer and Kramer 2000; Hasegawa et al. 2000;
Morbach and Kramer 2002). During the first phase, bacterial cells accumulate
additional K+ from the medium through their K+ uptake systems and synthesise
glutamate concomitantly. Thereby, they increase the ion content of their cytoplasm
and counteract plasmolysis brought about by water efflux. During its second phase
of the cellular adaptation, cyanobacteria replace this internal potassium glutamate by
synthesising high concentrations of glucosylglycerol and sucrose, which are accumulated as compatible solutes in their cytoplasm (Reed and Stewart 1985). Within
a few minutes, Na+ is replaced by K+ and subsequently, it takes lot of time to replace
the high K+ concentration in the cytoplasm by glucosylglycerol as well as minor
amounts of sucrose (Reed et al. 1985).
During its long-term adaptation to high NaCl concentrations, Synechocystis sp.
PCC 6803 also synthesises and accumulates glucosylglycerol (Marin et al. 1998;
Ferjani et al. 2003). Strain PCC 6803 has been predicted to contain at least three
254
N.K. Singh and D.W. Dhar
types of K+ uptake systems; Kdp system, which is probably of minor importance
(Berry et al. 2003); a Ktr system (Nakamura et al. 1998), which appears to play a
role in salt stress by high NaCl concentrations (Berry et al. 2003) and K+ channels.
It has been reported that in Synechocystis sp. PCC 6803, the ntpJ gene (slr1509) is
essential for both the adaptation to high NaCl concentrations and the bicarbonate
transport via the SbtA system. SbtA-mediated bicarbonate transport was also
dependent on the presence of external Na+. It was interpreted that NtpJ functions as
a Na+ efflux system required for the removal of Na+ from the cells after a hyperosmotic shock with NaCl and/or Na+ uptake due to Na+/HCO3− symport via SbtA
(Matsuda et al. 2004).
Transmembrane ion transport processes play a key role in the adaptation of cells
to hyperosmotic conditions. Heterologous expression experiments in Escherichia
coli show that three Synechocystis genes are required for K+ transport activity. They
encode an NAD+-binding peripheral membrane protein, an integral membrane
protein (belonging to a superfamily of K+ transporters) and a novel type of ktr gene
product (Matsuda et al. 2004). The genome of Synechocystis sp. PCC 6803 contains
43 genes that encode putative histidine kinases, identified as a sensor of osmotic
stress (Mikami et al. 2002; Suzuki et al. 2000).
9.4.5 Role of Compatible Solutes and Lipids in Salt Tolerance
The protection against alkaline environment is also provided by the synthesis of
certain fatty acids, sucrose and osmotic-stress-induced proteins (Goel et al. 1997).
The inducible synthesis of compatible solutes such as sucrose is synthesised in
salt-sensitive strains of cyanobacteria such as Synechococcus (Mackay et al. 1984;
Reed et al. 1986; Joset et al. 1996; Hagemann and Erdmann 1997); glucosylglycerol
is synthesised in strains with intermediary tolerance such as Synechocystis sp. PCC
6803 (Hagemann et al. 1987, 2001; Erdmann et al. 1992; Mikkat and Hagemann
2000); glycine betaine is synthesised in salt-tolerant Synechococcus sp. PCC 7418
(Mackay et al. 1984; Joset et al. 1996). Direct evidence for the ability of these
compatible solutes to protect the cyanobacterial cells may be seen from studies of
transgenic systems (Deshnium et al. 1995, 1997; Ishitani et al. 1995; Nakamura
et al. 1997).
Many reports have suggested the role of lipids in the protection of cyanobacteria
against salt stress (Hufleijt et al. 1990; Khamutov et al. 1990; Ritter and Yopp
1993). When photosynthetic organisms are exposed to salt stress, the fatty acids of
membrane lipids are desaturated (Allakhverdiev et al. 2001). Targeted mutagenesis
has been used to alter genes for fatty acid desaturases in Synechocystis and have
produced strains with decreased levels of unsaturated fatty acids in their membrane
lipids (Tasaka et al. 1996) as well as decreased tolerance to salt (Allakhverdiev
et al. 1999). Their results demonstrated that an increase in the unsaturation of fatty
acids in membrane lipids enhanced the tolerance to salt stress of the photosynthetic
and Na+/H+ antiport systems of Synechococcus (Allakhverdiev et al. 2000a, b;
Singh et al. 2002).
9
Cyanobacterial Reclamation of Salt-Affected Soil
255
The unsaturation of fatty acids in membrane lipids might activate the Na+/H+
antiport system through enhanced fluidity of the membrane with resultant protection
of PSII and PSI activities (Blumwald et al. 1984; Padan and Schuldiner 1994).
The activities of several membrane-bound enzymes are known to be affected by
changes in membrane fluidity (Kates et al. 1984; Kamada et al. 1995). The unsaturation of fatty acids might stimulate the synthesis of the Na+/H+ antiporter(s) and/
or H+ ATPase(s). The increased density in the membrane of these components of
the antiport system might result in a decrease in the concentration of Na+ in the
cytosol, which would tend to protect PSII and PSI against NaCl-induced inactivation and to accelerate the recovery of PSII and PSI activities (Allakhverdiev et al.
2001).
9.4.6 Enhancement of Cyanobacterial Salt Tolerance
by Combined Nitrogen
Enhanced salt tolerance in the presence of combined nitrogen is suggested by (a)
all nitrogen compounds which protect against salt, reduce Na+ influx; (b) proline
and glycine which are ineffective against Na+ influx, offer no protection against salt
stress; (c) the effectiveness of different nitrogen compounds in protecting against
salt stress follows the order of efficiency with which they inhibit Na+ influx; (d)
moreover, the relationship between inhibition of Na+ influx and enhancement of
salt tolerance is found to be independent of the inherent ability of cyanobacteria to
tolerate NaCl, i.e. not only a salt-sensitive strain becomes salt-tolerant, but tolerance
of A. torulosa is further enhanced beyond its normal abilities (Apte et al. 1987;
Reddy et al. 1989). Provision of nitrate, ammonium, glutamine, glutamate, and
aspartate in the medium enhances the salt tolerance of Anabaena by two- to threefold
(Apte et al. 1987). Presence of NH4, NH3, or certain amino acids in the medium has
been shown to prevent intracellular accumulation of Na+ or K+ in certain animal
systems (Cheeseman and Delvin 1985; Suput 1984) and microbes (Sprott et al.
1984) usually by stimulating the efflux of the cation (Reddy et al. 1989).
9.5 Influence of Cyanobacterial Application on Salinity
Related Soil Properties
Cyanobacterial application results in the enrichment of soil with fixed nitrogen, soil
structure improvement and declining trend of pH, electrical conductivity and Na+. These
changes improved the crop vigour and yield in salt-affected soil (Kaushik et al. 1981;
Subhashini and Kaushik 1981; Kaushik and Krishnamurti 1981; Kaushik and Subhashini
1985) (Table 9.3). Enrichment of salt-affected soils with native cyanobacterial isolates,
over a period of time improved the soil quality and resulted in the decrease of pH,
exchangeable sodium (ES), Na/Ca and overall increase in N, P, organic matter and
256
N.K. Singh and D.W. Dhar
Table 9.3 Influence on pH, electrical conductivity (EC) and exchangeable sodium (ES) of sodic
soils after 3 years of BGA (blue-green algae) application (initial soil pH = 10, exchangeable
Na+ = 10.44 meq 100 g−1, CEC = 11.19 meq 100 g−1)
After summer paddy of
1985
1986
1987
Treatments
pH
EC
ES
pH
EC
ES
pH
EC
ES
Control
9.65
1.93
9.72
9.67
0.6
9.51
9.30
0.64
5.21
BGA
10.45
1.36
5.44
9.20
1.1
4.67
7.71
1.08
1.26
Gypsum
9.35
1.61
4.78
9.13
2.13
5.97
7.7
1.31
1.15
BGA +
9.30
1.59
4.78
8.73
1.52
2.39
7.66
1.03
0.87
gypsum
water-holding capacity of soil. This reduced the sodium adsorption ratio, which is an
index of alkalinity and improved the hydraulic conductivity of sodic soils (Subhashini
and Kaushik 1981; Rai et al. 1998). These results compared favourably to the use of
chemical amendments such as gypsum in such soils (Kaushik and Krishnamurti 1981).
9.5.1 Soil pH
Under natural conditions, most of the cyanobacteria grow in neutral to alkaline conditions
(Fogg 1956) and sometimes the growth of diazotrophic cyanobacteria in rice fields is
limited by low pH (Whitton and Potts 2000). Alkaline soil with high pH and Na+
content favour the growth of diazotrophic cyanobacteria with a consequent decrease in
pH. Indeed, cyanobacteria are reported to decrease soil pH from 9.2 to 7.5 under natural
conditions and pyrite application speed up the process of saline soil reclamation (Singh
1961; Verma and Abrol 1980). The application of Westiellopsis decreased the soil pH
from 8.05 to 7.71 which was due to combined influence of leaching and release of
organic acids through microbial decomposition of amendments (Prabu and Udayasoorian
2007). Such reduction in pH had been reported in laboratory experiments, without any
crop (Subhashini and Kaushik 1984) and with rice (Elayarajan 2002).
9.5.2 Electrical Conductivity
The application of cyanobacteria to saline soil reduces the electrical conductivity of
saline soil (Kannaiyan et al. 1992). Leaching of salt-affected soil alone cannot
result in a substantial reduction in the electrical conductivity. But algalisation with
Westiellopsis and amendments with gypsum showed progressive decrease in soil
electrical conductivity, followed by leaching (Prabu and Udayasoorian 2007).
The extracellular polysaccharide production by cyanobacteria offers some temporary
9
Cyanobacterial Reclamation of Salt-Affected Soil
257
relief by chelating exchangeable cations in soil and thereby decreases the soil
electrical conductivity (Apte and Thomas 1997). In salt-affected areas in India,
application of cyanobacteria combined with gypsum or sulphur changed the soil pH
from alkaline to neutral, reduced exchangeable Na and electrical conductivity, and
led to the development of soil aggregates in the long term (Kaushik and Krishnamurti
1981; Kaushik 1989).
9.5.3 Exchangeable Sodium
Reduction in soil exchangeable Na content was recorded with the application of
gypsum and Westiellopsis. This in turn, exhibited a favourable effect on leaching of Na
in soil complex (Rogers and Burns 1994). The extracellular polysaccharide production
by cyanobacteria offers some temporary relief by chelation of excess Na+ present
in soil (Apte and Thomas 1997). Cyanobacteria also reduce sodium ion content of
the soil by making calcium ions available through solubilisation of calcium carbonate
nodules, possibly by releasing various organic acids, like oxalic, oxaloacetic, lactic
and succinic acids (Bhatnagar and Roychoudhury 1992).
9.5.4 Sodium Absorption Ratio and Exchangeable Sodium
Percentage
High toxicity due to sodium can be reduced by decreasing the sodium absorption
ratio and exchangeable sodium percentage which can be augmented by increasing
the proportion of Ca2+ and Mg2+ to Na+ in soil exchange complex by the addition of
their salts (Pandey et al. 2005). Application of Westiellopsis cultures along with high
exchangeable Ca and Mg amendments caused significant changes in soil sodium
absorption ratio and exchangeable sodium percentage (Rogers and Burns 1994).
9.6 Improvement of Soil Properties
9.6.1 Soil Structure
The extracellular polysaccharides excreted by cyanobacteria have been reported to be
responsible for binding of soil particles leading to the formation of tough and entangled
superficial structure that improves the stability of soil surface and protects it from
erosion (Rogers and Burns 1994). The mucilaginous sheath of Aphanothece sp. formed
a grey substratum firmly holding the soil particles together which checked wind- and
water-mediated soil erosion, particularly in light and sandy soils (Singh 1961).
258
N.K. Singh and D.W. Dhar
Cyanobacterial sheaths and extracellular polysaccharides also play a significant
role in water storage due to the hygroscopic properties of polysaccharides. Several
workers have reported that the application of cyanobacterial cultures to problem
soils improved the soil physical properties with enhanced hydraulic conductivity (Malam et al. 2001a, b) which increased the productivity of rice and rapeseed
crop. Enhanced hydraulic conductivity resulted in better root penetration and
increased nutrient uptake from nutrient-limiting sodic and saline soils (Fernandez
et al. 2000).
9.6.2 Nutrient Content
As early as 1950, cyanobacterial inoculation was reported to build up organic
matter in soil (De and Sulaiman 1950). The application of cyanobacteria to saline
soil enhances the soil organic carbon content due to the addition of organic matter in
the form of algal biomass (Kannaiyan et al. 1992; Apte et al. 1997). Cyanobacterium
Nostoc muscorum is also reported to increase the organic carbon content of soil
(Rogers and Burns 1994). This content increased significantly in the post-harvest
soil in response to cyanobacterial application in the paddy field (Hashem 2001). In
the Westiellopsis inoculated soil at 90 day, the organic matter content was three
times greater than that of non-inoculated soil (Prabu and Udayasoorian 2007).
The photosynthetic nitrogen-fixing cyanobacteria are well-equipped to handle
deficiency of nitrogen which otherwise decreases the overall tolerance of cyanobacteria
to different environmental stresses (Apte et al. 1997; Apte 1992, 1993). The available
nitrogen content of soil increased during the incubation of arid environments with
Westiellopsis sp. (Rogers and Burns 1994; Lange et al. 1994). Both heterocystous
and non-heterocystous cyanobacteria have the capability to scavenge available
nitrogen (NO3− and NH4+) and phosphorous from secondary treated sewage effluent
and produce massive biomass which can in turn strengthen the soil with valuable
nutrients (Singh and Dhar 2006, 2007). Cyanobacteria can also fix a significant
amount of atmospheric nitrogen and the amount of nitrogen fixed on average is
30–40 kg N ha−1 crop−1 which in turn can improve soil fertility (Roger and
Kulasooriya 1980; Aziz and Hashem 2003; Metting 1990).
Available soil phosphorous and sulphur also increased in response to cyanobacterial
application (Hashem 2001). Solubilisation of mussorrie rock phosphate – a source
of P2O5 and a raw material for fertilizer industry, by nitrogen fixing Tolypothrix
tenuis, Scytonema cincinnatum and Hapalosiphon fontinalis was observed under
in vitro studies (Roychoudhury and Kaushik 1989). Other cyanobacterial strains
namely Calothrix braunii, Tolypothrix ceylonica, Scytonema cincinnatum,
Haplosiphon fontinalis and Westiellopsis prolifica have been reported to solubilise
insoluble rock phosphate and make it available to the crop plants (Roychoudhary
and Kaushik 1989). Vitamin B12 synthesis and liberation by Tolypothrix tenuis,
Nostoc muscorum and Haplosiphon frontalis has also been demonstrated (Misra
and Kaushik 1989a). In addition to free amino acids, like serine, arginine, glycine,
9
Cyanobacterial Reclamation of Salt-Affected Soil
259
aspartic acid, threonine, glutamic acid, etc. strains of Nostoc and Haplosiphon also
produce growth-promoting substances, namely indole-3-acetic acid and indole-3
propionic acid (Misra and Kaushik 1989b).
9.7 Crop Response in Saline–Alkaline and Sodic Soils
The role of cyanobacteria in the sustained fertility of flooded/irrigated rice field
soils is well-established (Singh 1961; Venkataraman 1975; Roger 1996). The
potential impact of these organisms on agriculture through their use as soil conditioners, plant growth regulators and soil health ameliorators has also been wellrecognised (Venkataraman 1975, 1979; Vaishampayan et al. 2001; Whitton 2000).
The positive effect of cyanobacterial inoculation often increases with time and only
a fraction (2–10%) of nitrogen fixed is immediately available to the crop and the
remainder is released following death and decomposition of the algae (Venkataraman
1979). The salt tolerance of cyanobacteria has been exploited with some success in
the reclamation of saline and sodic soils (Thomas and Apte 1984). The practice of
utilising cyanobacteria as an efficient source of biofertilizer for rice has been advocated
and adopted in the tropical countries, where conditions are favourable for their
mass multiplication (Venkataraman 1981; Kannaiyan 1990).
Species of Nostoc, Anabaena, Tolypothrix, Aulosira, Cylindrospermum,
Scytonema, Westiellopsis and several other genera are widespread in tropical rice
field soils and are known to contribute significantly to their fertility (Venkataraman
1981; Kaushik 1994). A series of experiments lead to the conclusion that (i) bluegreen algae are effective as bioameliorant in saline and sodic soils, (ii) the benefits
of blue-green algae can further be enhanced if gypsum at 50% of its required dose
is applied along with blue-green algae, (iii) both grain and straw yields are enhanced
by the combined application of blue-green algae and gypsum at all the levels (25%,
50%, 75% and 100% of gypsum or blue-green algae alone). Such improved crop
yields may be due to reduction of soil pH, exchangeable sodium and electrical
conductivity (Kaushik et al. 1981; Subhashini and Kaushik 1981; Kaushik and
Krishnamurti 1981) as well as enrichment of soil with fixed nitrogen, increased
availability of phosphorous, improved soil aggregation and hydraulic conductivity
(Subhashini and Kaushik 1984; Kaushik and Subhashini 1985).
9.8 Crop Yield
It is well-known that besides bringing about an improvement in yield of rice (ranging
from 5% to 25%), cyanobacteria produce indirect or direct beneficial changes in the
physical, chemical and biological properties of soil and soil–water interface in rice
fields, which are of agronomic importance (Mandal et al. 1998). In tropical rice
260
N.K. Singh and D.W. Dhar
Table 9.4 Yield (q ha−1) of paddy (var. Pusa 33) and wheat
(var. 2393) in salt-affected soils after 2 years of reclamation
with different treatments including BGA (blue-green algae)
Paddy
Treatments
Grain
Straw
Control
6.15
5.15
BGA
41.0
30.6
Gypsum 100%
42.0
30.40
BGA + Gypsum 100%
45.4
33.2
Wheat
BGA
28.50
32.75
90 kg N
32.75
37.75
BGA +90 kg N
35.25
42.25
120 kg N
35.70
41.75
BGA +120 kg N
39.75
52.38
150 kg N
39.25
49.38
fields, biological nitrogen fixation is mainly a cyanobacterial process and part of
the nitrogen demand of the rice crop is met through the indigenous populations or
through their application as biofertilizers (Mitra 1951). The yields obtained in bluegreen-algae-treated plots were observed at par with gypsum (41–42 q ha−1),
although combined application of both was still better. The yield of wheat recorded
after 2 years of reclamation with blue-green algae and/or gypsum, was also better
in the treatment with combination of blue-green algae and chemical fertilizer than
the fertilizer alone (Kaushik 1994; Table 9.4).
Extracellular products of cyanobacteria counteracted NaCl-induced inhibition
on shoot length and increased root dry weight, nullified the salt effect on shoot dry
weight (Aziz and Hashem 2004; Rodríguez et al. 2006). Extracellular products
from Scytonema hofmanni reverted completely or partially many of the NaCl-induced
effects on growth and biochemical attributes of rice seedlings. The cyanobacterial
extracellular products also contain gibberellin-like substances which may be responsible for the alleviation of adverse effect of salt stress on crop productivity
(Rodríguez et al. 2006). Seed priming in Lupinus termis with cyanobacterial culture
filtrate increased chlorophyll ‘a’ and ‘b’, reduced carotenoids content, increased
auxin, gibberellic acid and cytokinin content and decreased abscissic acid content
(Haroun and Hussein 2003; El-Shahaby 1992).
Water infiltration and soil surface stability are related to cyanobacterial
biomass which favourably influences the crop yield (Jeffries et al. 1993a, b).
In greenhouse experiments, nitrogen levels in Sorghum halepense were higher
when the plant was in pots with cyanobacteria than in the pots without cyanobacteria.
Dry weight of plants in pots with cyanobacteria was up to four times greater than
in pots without cyanobacteria (Harper and Pendleton 1993; Shields and Durrell
1964; Brotherson and Rushforth 1983; Pendleton and Warren 1995).
9
Cyanobacterial Reclamation of Salt-Affected Soil
261
9.9 Residual Effect of Cyanobacterial Application
in Crop Field
Certain cyanobacteria have been found not only to grow in saline ecosystems but
also improve the physico-chemical properties of the soil by enriching them with
carbon, nitrogen and available phosphorus (Antarikanonda and Amarit 1991).
Cyanobacteria fix as much as 28 kg Nha−1year−1 and are important because algalisation may affect plant size, number of tillers, ears, spikelets and filled grains per
panicle (Metting 1990). In addition, cyanobacterial sheath material is often coated
with negatively charged clay particles which are more nutrient rich than sand
(Black 1968), as they bind positively charged macronutrients and prevent them
from leaching through the soil profile (Belnap and Gardner 1993). Compounds in
the gelatinous sheath material of several cyanobacterial taxa were able to chelate iron,
copper, molybdenum, zinc, cobalt, and manganese. Four cyanobacterial genera
(Anabaena, Anacystis, Lyngbya, and Nostoc) reported to possess this ability, are
commonly represented in biological crusts (Lange 1974; Shields and Durrell
1964). It is also possible that the nutrient differences result from thermal effects,
as crusted soils are darker and warmer than uncrusted soils; nutrient uptake by
vascular plants would occur at a higher rate (Shields and Durrell 1964).
The organic metabolites produced by cyanobacterial growth are released in the
extracellular soil environment and their degradation products can accumulate and
increase the organic N content, which subsequently maintains the fertility of soil
year after year (Roger and Kulasooriya 1980; Ladha and Reddy 1995). Growth of
cyanobacteria in soil decreases the C/N ratio due to N2 fixation (Watanabe et al.
1977). An increase in C/N ratio in the experiment conducted under natural conditions
with natural inoculum compared to Nostoc calcicola inoculation may be due to the
growth of many non-N2–fixers. Soil properties such as soil structure can be improved
via the production of extracellular substances by cyanobacteria (Whitton and Potts
2000).
Polysaccharides produced by cyanobacteria excrete a number of compounds
which diffuse around soil particles, glue and hold them together in the form of
micro-aggregates (Brotherson and Rushforth 1983; Alexander and Calvo 1990).
Well-developed aggregate stability and surface roughness resist soil particle dislodgement by wind (Chepil and Woodruff 1963). Enrichment of saline soils with
the indigenous cyanobacterial strains may help in ameliorating the land and making them suitable for obtaining higher yields. Benefits other than nitrogen fixation include solubilisation of phosphorus, improved soil structure and synthesis
of growth promoting substances which also has beneficial effect on the succeeding crop and helps in improving the physico-chemical properties of soil and crop
yield (Khan et al. 1994; Saxena and Kaushik 1992). A long-term fertility experiment indicated that the use of chemical fertilizers is not sufficient to restore soil
fertility and under such conditions, biofertilizers like cyanobacteria could provide
essential nutrient and organic matter to the soil (Singh and Bisoyi 1993).
262
N.K. Singh and D.W. Dhar
9.10 Technology for Soil Health Improvement
The reclamation of sodic soils involves chemical amendment with gypsum or Fe
pyrites and leaching to remove excess salts. Reclamation by biological methods is
slower and depends on the incorporation of green manures (Rao and Burns 1990).
Saline soils can be reclaimed easily by irrigating the field with good quality of water
so as to facilitate leaching of salts. The salts move below the root zone and thus, crops
escape the injurious effects of salts. Only flushing of the field may not be effective and
the addition of cyanobacterium inoculum along with addition of gypsum is required
before irrigation to ameliorate saline soils (Kaushik and Krishnamurti 1981).
Pyrite used as a chemical corrective to reclaim sodic soil lacks complete oxidation
and may cause toxicity by releasing ferrous and sulphide ions. However, cyanobacteria growing in soils utilise iron and sulphide for their growth. Nitrogenase induction
by sulphide in non-heterocystous cyanobacteria is optimal at high pH (Villbrandt
and Stal 1996). The sulphide acts as a reducing agent and its addition to the
diazotrophic Plectonema boryanum enhanced nitrogenase activity (Kashyap et al.
1996). In microbial mats, iron may participate as iron sulphide (FeS) or pyrite
(FeS2). Iron reacts with oxygen and keeps the partial pressure of oxygen sufficiently
low to allow efficient photosynthesis and N2 fixation by cyanobacteria (Whitton and
Potts 2000).
The gypsum requirement for reclaiming the saline soil depends upon the level
of Na+ present in the soil. The calcium ion (Ca2+) present in the gypsum (CaSO4.
2H2O) replaces the Na+ on the cation exchange site and results in the formation of
insoluble salt (Na2SO4). This can be easily removed from the root zone by impounding
sufficient water in the field. The calcium acts as flocculating agent and helps in the
formation of soil aggregates and thus, improves the physical and chemical properties
of soil for production of cereals and plantation crops (Singh 1961). The results
become more satisfactory if gypsum is applied along with good amount of inoculum
of halotolerant cyanobacterial strains (Kaushik 2005).
The calcareous saline soil contains huge amounts of carbonate. Addition of pyrite
in such soils may result in the formation of sulphurous and sulphuric acid, which
may react with carbonate and eventually produce CO2. The growth of cyanobacteria
in such soils increased soluble CO2 (Singh 1961). The inoculation of HCO3-resistant
mutants of Nostoc calcicola in pyrite-treated alkaline soil led to better reclamation
results as determined by pH coupled with growth (population) compared to the same
treated soil inoculated with the wild type (Pandey et al. 2005).
The area to be ameliorated should be first of all levelled and divided into
sub-plots (size 200 m2), bound by thick earthen embankment of 45 cm height and
should be puddled properly before flooding. Then algal ameliorant (usually halotolerant nitrogen fixing) should be broadcasted at 20 kg ha−1 (soil based) or 2 kg ha−1
(straw based) in the standing water which should remain stagnant in the field for at
least 2 weeks for algal proliferation with a total incubation period of the soil with algae
of at least 10 weeks. Lastly the soil should be puddled and transplanted with paddy
seedlings with normal required dose of fertilizer (Kaushik 2005).
9
Cyanobacterial Reclamation of Salt-Affected Soil
263
9.11 Amelioration of Saline Soils Using Halotolerant
Nitrogen-Fixing Cyanobacteria
Cyanobacterial reclamation of saline and alkaline soils has been suggested as early
as 1950 (Singh 1950). It has been noticed that nitrogen-fixing blue green algae can
be used as biological input to improve soil texture, conserve moisture, scavenge the
toxic sodium cation from the soil complex and improve the properties of such soils
(Subhashini and Kaushik 1981). They have reported that Tolypothrix ceylonica,
Haplosiphon intricatus and two species of Calothrix (C. braunii and C. membranacea)
showed absorption of sodium 0.8 mg mg−1 algal dry weight grown in the medium
containing 1.425 mg Na ml−1 (Subhashini and Kaushik 1982).
Systematic work done in IARI (New Delhi, India), has led to the conclusion that
(i) incubation of soil with blue-green algae (native/mixture of known blue-green
algae) improves the physico-chemical properties of saline and alkaline soil
(Kaushik et al. 1981). (ii) Nostoc, Anabaena, Calothrix and Plectonema are the
common forms of cyanobacteria observed in soils of pH 9.0 and above. (iii) The
distribution of nitrogen-fixing cyanobacterial forms seems to be localised. The strains
colonising salt-affected soils are mostly similar to those observed in normal paddy
field soils; however, those found in highly alkaline soils are different (Subhashini
and Kaushik 1982). (iv) These halotolerant strains secrete excessive extracellular
polysaccharides in response to salts and thus chelate some of the toxic cations
(Roychoudhury et al. 1985). (v) Some of the cations undergo temporary immobilisation as their salts are taken up by the organisms for their own growth. (vi) Some
halotolerant nitrogen-fixing cyanobacterial strains liberate organic acids and enzyme
alkaline phosphatase which solubilises the insoluble CaCo3 in soil, and make Ca2+
available to replace Na+ from the soil complex. (vii) Inoculation of soil-based bluegreen algae results in improvement of soil aggregation, hydraulic conductivity,
organic carbon and total nitrogen of the saline soils (Subhashini and Kaushik 1984).
(viii) Some of the forms are also phosphate solubilisers; hence, available content of
soil phosphorous increases and lastly (ix) raising of paddy crops after amelioration
gives crop yield as good as in normal soils (Kaushik 1994).
9.12 Conclusion
Physical and chemical methods such as addition of gypsum and sulphur, or excessive irrigation used in the reclamation of alkaline soils do not completely remove
the soluble salts and exchangeable sodium. These organisms, by virtue of their dual
capacity for photosynthesis and N2 fixation, are capable of contributing to productivity in a variety of agricultural and ecological situations (Fogg et al. 1973).
Understanding the salt response in cyanobacteria will make a relevant impact on
understanding the detrimental effects of salinity on crops plants (Pandhal et al.
264
N.K. Singh and D.W. Dhar
2008). These organisms can be used to reclaim alkaline soils because they form a
thick stratum on the surface of the soil during the rainy season and the winter
months. The algal material incorporated in the soil conserves organic C and N,
and organic P as well as moisture, and converts Na+ clay to Ca2+ clay. Organic
matter and N added by cyanobacteria bind the soil particles, and thus improve
soil permeability and aeration (Singh 1961). They are capable of solubilising
microbial nutrients and dissolving insoluble carbonate nodules through the secretion of oxalic acid (Singh 1961). Improvement of soil aggregation by lowering the
pH and electrical conductivity and by increasing the hydraulic conductivity of
saline and alkaline soils by cyanobacteria has been well-documented (Kaushik and
Subhashini 1985).
Specific metabolic requirement of sodium (<100 mM) in cyanobacteria especially
under N2-fixing conditions has been reported. Sodium does not influence several
structural and functional features associated with diazotrophic growth like heterocyst differentiation, synthesis of nitrogenase proteins, transport of molybdenum and
protection of nitrogenase from oxygen. However, vital functions like nitrogenase
activity, photosynthesis, quality and quantity of proteins, membrane potential and
energy status of N2-fixing cells are affected by sodium deficiency. A primary effect
of Na+ deficiency is inhibition of uptake and utilisation of phosphate leading to
depletion of nucleotide phosphate pools. This in turn results in inhibition of N2
fixation apparently due to limitation of ATP supply.
Accumulation of K+, exclusion of Na+ and maintenance of low intracellular Na+
levels, synthesis of carbohydrates, polyols, amino acids and quaternary amines for
osmoregulation and other adaptations of metabolism are principal features associated with and contributing to the salt tolerance in cyanobacteria. Extracellular
mucopolysaccharides chelate significant amounts of sodium. Intracellular sodium
exists as a free cation and is not incorporated into any biomolecule, especially
proteins. Na+ influx in N2-fixing Anabaena spp. is carrier-mediated and is regulated by the proton-motive force, particularly the membrane potential of cells.
Low intracellular concentrations are maintained by active efflux. While the nature
of this efflux is uncertain in N2-fixing cyanobacteria, in Anacystis nidulans it
is mediated by Na+/H+ antiporter and decreases the efficiency of oxidative
phosphorylation.
Virtually negligible information exists on the genetics of cyanobacterial halotolerance. Genetic engineering of these photoautotrophic diazotrophs for enhanced
halotolerance and subsequent agricultural exploitation is an attractive area of future
research. The presence of combined nitrogen, which effectively curtails sodium
accumulation and also supports extra nitrogen demand for osmoregulation during
salt stress, confers considerable salt tolerance on cyanobacteria. Exploiting the
potential of cyanobacteria for reclamation of saline sodic soils needs more serious
efforts than those made in the past.
Acknowledgements The authors gratefully acknowledge the assistance provided by the
Department of Microbiology, C.P. College of Agriculture (SDAU, S. K. Nagar) and the Department
of Microbiology, Indian Agricultural Research Institute, New Delhi for preparation of this
chapter.
9
Cyanobacterial Reclamation of Salt-Affected Soil
265
References
Abhishek C, Mohammad Z, Abraham G, Prasad SM (2006) Proline accumulation in
Cylindrospermum sp. Environ Exp Bot 57:154–159
Acea MJ, Prieto-Fernandez A, Diz-Cid N (2003) Cyanobacterial inoculation of heated soils: effect
on microorganisms of C and N cycles and on chemical composition in soil surface. Soil Biol
Biochem 35:513–524
Alexander RW, Calvo A (1990) The influence of lichens on slope processes in some Spanish
badlands. In: Thornes JB (ed) Vegetation and erosion. Wiley, Chichester, England, pp 385–398
Ali S, Sandhu GR (1972) Blue green algae of the saline soils of the Punjab. Oikos 23:268–272
Allakhverdiev SI, Kinoshita M, Inaba M, Suzuki I, Murata N (2001) Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt induced damage in Synechococcus.
Plant Physiol 125:1842–1853
Allakhverdiev SI, Nishiyama Y, Osuzuki I, Tasaka Y, Murata N (1999) Genetic engineering of the
unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt
stress. Proc Natl Acad Sci U S A 96:5862–5867
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000a) Ionic and osmotic
effects of NaCl-induced inactivation of photosystem I and II in Synechococcus sp. Plant
Physiol 123:1047–1056
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000b) Inactivation of photosystem I and II in response to osmotic stress in Synechococcus: contribution of water channels.
Plant Physiol 122:1201–1208
Allen MB, Arnon DI (1955) Studies on nitrogen fixing blue green algae. I. Growth and nitrogen
fixation by Anabaena cylindrica Lemm. Plant Physiol 30:366–372
Amsaveni P (1995). Effect of certain nutrients on the growth and ammonia excretion by the saline
tolerant cyanobacteria and their role as biofertilizers for bioreclamation of saline and sodic
soils. Ph.D. Thesis, TNAU, Coimbatore, Tamilnadu, India
Antarikanonda P, Amarit P (1991) Influence of blue-green algae and nitrogen fertilizer on rice
yield in saline soils Kasctsart. J Nat Sci 25:18–25
Apte SK (1992) Molecular biology of cyanobacterial nitrogen fixation: recent advances. Indian
J Microbiol 32:103–126
Apte SK (1993) Cyanobacterial nitrogen fixation; molecular genetic aspects. Proc Indian Natl Sci
Acad B59:367–386
Apte SK, Bhagwat AA (1989) Salinity-stress-induced proteins in two nitrogen-fixing Anabaena
strains differentially tolerant to salt. J Bacteriol 171:909–915
Apte SK, Thomas J (1980) Sodium is required for nitrogenase activity in cyanobacteria. Curr
Microbiol 3:291–293
Apte SK, Thomas J (1974) Use of radiations and radioisotopes in studies of plant productivity. In:
Proceedings of the symposium of the department of atomic energy, Government of India,
Bombay, pp 783
Apte SK, Thomas J (1983) Sodium transport in filamentous nitrogen-fixing cyanobacteria.
J Biosci 5:225–234
Apte SK, Thomas J (1984) Effect of sodium on nitrogen fixation in Anabaena torulosa and
Plectonema boryanum. J Gen Microbiol 130:1161–1168
Apte SK, Thomas J (1986) Membrane electrogenesis and sodium transport in filamentous nitrogen-fixing cyanobacteria. Eur J Biochem 154:395–401
Apte SK, Thomas J (1997) Possible amelioration of coastal soil salinity using halo tolerant nitrogen fixing cyanobacteria. Plant Soil 189:205–211
Apte SK, Fernandes T, Badran H, Ballal A (1998) Expression and possible role of stress-responsive
proteins in Anabaena. J biosci 23(4):399–406
Apte SK, Fernandes TA, Iyer V, Alahari A (1997) Molecular basis of tolerance to salinity and drought
stresses in photosynthetic nitrogen-fixing cyanobacteria. In: Tewari KK, Singhal GS (eds) Plant
molecular biology and biotechnology. Narosa Publications, New Delhi, pp 258–268
266
N.K. Singh and D.W. Dhar
Apte SK, Reddy BR, Thomas J (1987) Relationship between sodium influx and salt tolerance of
nitrogen-fixing cyanobacteria. Appl Environ Microbiol 53:1934–1939
Ardelean II (1966). Biosensors with intact cyanobacteria for environmental protection. In: Subramanian
G, Kaushik BD, Venkataraman GS (eds) Cyanobacterial biotechnology. Science Publishers.
Inc., USA, pp 75
Aziz MA, Hashem MA (2003) Role of cyanobacteria in improving fertility of saline soil. Pak J
Biol Sci 6(20):1751–1752
Aziz MA, Hashem MA (2004) Role of Cyanobacteria on yield of rice in saline soil. Pak J Biol Sci
7:309–311
Baker DW, Brand JJ (1985) Anacystis nidulans demonstrates a photosystem II cation requirement
satisfied only by Ca21 or Na21. Plant Physiol 79:552–558
Bakker EP (1993). Alkali cation transport systems in prokaryotes. CRC Press, Boca Raton, FL,
pp 205–224
Belnap J, Gardner JS (1993) Soil microstructure of the Colorado Plateau: the role of the cyanobacterium Microcoleus vaginatus. Great Basin Nat 53:40–47
Berry S, Esper B, Karandashova I, Teuber M, Elanskaya I, Rogner M, Hagemann M (2003)
Potassium uptake in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803
depends on a Ktr-like system encoded by slr1509 (ntpJ). FEBS Lett 548:53–58
Bhadauriya P, Gupta R, Singh S, Bisen P (2007) Physiological and biochemical alterations in a
diazotrophic cyanobacterium Anabaena cylindrica under NaCl Stress. Curr Microbiol
55:334–338
Bhagwat AA, Apte SK (1989) Comparative analysis of proteins induced by heat shock, salinity
and osmotic stress in the nitrogen fixing cyanobacterium Anabaena sp. strain L-31. J Bacteriol
171:5187–5189
Bhatnagar A, Roychoudhury P (1992) Dissolution of limestone by cyanobacteria. In: Kaushik BD
(ed) Proceedings of the national symposium on cyanobacterial nitrogen fixation. Today &
Tomorrow’s Printers and Publishers, IARI, New Delhi, pp 331–335
Billini M, Stamatakis K, Sophianopoulou V (2008) Two members of a network of putative Na+/
H+ antiporters are involved in salt and pH tolerance of the freshwater cyanobacterium
Synechococcus elongates. J Bacteriol 190(19):6318–6329
Black CA (1968) Soil–plant relationships. Wiley, New York, p 790
Blumwald E, Tel-Or E (1984) Salt adaptation of cyanobacterium Synechococcus 6311 growing in
continuous culture (turbidostat). Plant Physiol 74:183–185
Blumwald E, Mehlhorn RJ, Packer L (1983) Studies of osmoregulation in salt adaptation of
cyanobacteria with ESR spin probe technique. Proc Natl Acad Sci U S A 80:2599–2602
Blumwald E, Wolosin JM, Packer L (1984) Na+/H+ exchange in the cyanobacterium Synechococcus
6311. Biochem Biophys Res Commun 122:452–459
Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA,
Deyholos M, Galbraith DW, Hasegawa PM, Jenks M, Kawasaki S, Koiwa H, Kore-eda S, Lee
BH, Michalowski CB, Misawa E, Nomura M, Ozturk M, Postier B, Prade R, Song CP, Tanaka Y,
Wang H, Zhu JK (2001) A genomics approach towards salt stress tolerance. Plant Physiol
Biochem 39:295–311
Boyer JS (1982) Plant productivity and environment. Science 218(4571):443–448
Brahamsha B (1996) An abundant cell-surface polypeptide is required for swimming by the nonflagellated marine cyanobacterium Synechococcus. Proc Natl Acad Sci U S A 93:6504–6509
Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54
Bremer E, Kramer R (2000). In: Storz G, Hengge-Aronis R (eds) Bacterial stress responses. ASM
Press, Washington DC, pp 79–97
Brock TD (1973) Evolutionary and ecological aspects of the cyanophytes. In: Carr NG, Whitton
BA (eds) The biology of blue-green algae. Blackwell Scientific Publications Ltd, Oxford,
pp 487–500
Brotherson JD, Rushforth SR (1983) Influence of cryptogamic crusts on moisture relationships of
soils in Navajo National Monument, Arizona. Great Basin Nat 43:73–78
Brownell PF, Nicholas DJD (1967) Some effect of sodium on nitrate assimilation and nitrogen
fixation in Anabaena cylindrica. Plant Physiol 42:915–921
9
Cyanobacterial Reclamation of Salt-Affected Soil
267
Buck D, Smith G (1995) Evidence for a Na+/H+ electrogenic antiporter in an alkaliphilic
cyanobacterium Synechocystis. FEMS Microbiol Lett 128:315–320
Chauhan VS, Singh S, Pandey PK, Bisen PS (1999) Isolation and partial characterization of NaCltolerant mutant strain of Anabaena variabilis with impaired glutamine synthetase activity.
J Basic Microbiol 39:219–226
Cheeseman CI, Delvin D (1985) The effect of amino acids and dipeptides on sodium ion transport
in rat enterocytes. Biochim Biophys Acta 812:767–773
Chen TH, Huang TC, Chow TJ (1988) Calcium requirement in nitrogen fixation in the cyanobacterium Synechococcus RF-1. Planta 173:253–256
Chepil WS, Woodruff NP (1963) The physics of wind erosion and its control. Adv Agron
15:211–302
De PK, Sulaiman M (1950) The influence of algal growth in the rice fields on the yield of crops.
Indian J Agric Sci 20:327–342
Deshnium P, Gombos Z, Nishiyama Y, Murata N (1997) The action in vivo of glycine betaine in enhancement
of tolerance of Synechococcus sp. strain PCC 7942 to low temperature. J Bacteriol 179:339–344
Deshnium P, Los DA, Hayashi H, Mustardy L, Murata N (1995) Transformation of Synechococcus
with a gene for choline oxidase enhances tolerance to salt stress. Plant Mol Biol 29:897–907
Dewar MA, Barber J (1973) Cation regulation in Anacystis nidulans. Planta 113:143–155
Dinnbier U, Limpinsel E, Schmid R, Bakker EP (1988) Transient accumulation of potassium
glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia
coli K-12 to elevated sodium chloride concentrations. Arch Microbiol 150(4):348–357
Elanskaya IV, Karandashova IV, Bogachev AV, Hagemann M (2002) Functional analysis of the
Na+/H+ antiporter encoding genes of the cyanobacterium Synechocystis PCC 6803.
Biochemistry 67:432–440
Elayarajan M (2002). Land application of treated paper board mill effluent on soil- water-plant
ecosystem. Ph.D. Thesis, (Soil Science), TNAU, Coimbatore.
El-Shahaby OA (1992) Internal water status, endogenous levels of hormones, photosynthetic
activity in well watered and previously water stressed Vigna sinensis plants under ABA effect.
Mans Sci Bull 19:229–245
Emerson R, Lewis CM (1942) The photosynthetic efficiency of phycocyanin in Chroococcus and
the problem of carotenoid participation in photosynthesis. J Gen Physiol 25:579–595
England RR, Evans EH (1983) A requirement of Ca21 in the extraction of O2-evolving photosystem
2 preparations from the cyanobacterium Anacystis nidulans. Biochem J 210:473–476
Erdmann N, Fulda S, Hagemann M (1992) Glucosylglycerol accumulation during salt acclimation
of two unicellular cyanobacteria. J Gen Microbiol 138:363–368
Espie GS, Kandasamy RA (1994) Monensin inhibition of Na+-dependent HCO3- transport distinguishes it from Na+-independent transport and provides evidence for Na+/HCO3-symport in the
cyanobacterium Synechococcus UTEX 625. Plant Physiol 104:1419–1428
Ferjani A, Mustardy L, Sulpice R, Marin K, Suzuki I, Hagemann M, Murata N (2003)
Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol
131(4):1628–1637
Fernandes T, Thomas J (1982) Control of sporulation in the filamentous cyanobacterium
Anabaena torulosa. J Biosci 4:85–94
Fernandez VE, Ucha A, Quesada A, Leganes F, Carreres R (2000) Contribution of N2 fixing
cyanobacteria to rice production: availability of nitrogen from 15N labeled cyanobacteria and
ammonium sulphate to rice. Plant Soil 221:107–112
Flowers TJ, Troke PK, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Ann Rev
Plant Physiol 28:89–121
Fogg GE (1956) Nitrogen fixation by photosynthetic organism. Ann Rev Plant Physiol 7:51–70
Fogg GE, Stewart WDP, Fay P, Walsby AE (1973) The blue-green algae. Academic, London
Fulda S, Huang F, Nilsson F, Hagemann M, Norling B (2000) Proteomics of Synechocystis sp.
strain PCC 6803: Identification of periplasmic proteins cells grown at low and high salt
concentrations. Eur J Biochem 267:5900–5907
Fulda S, Jeremias I, Steiner HH, Pietsch T, Debatin KM (1999) Betulinic acid: a new cytotoxic
agent against malignant brain-tumor cells. Int J Cancer 82:435–441
268
N.K. Singh and D.W. Dhar
Fulda S, Mikkat S, Huang F, Huckauf J, Marin K, Norling B, Hagemann M (2006) Proteome
analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803.
Proteomics 6(9):2733–2745
Gabbay-Azaria R, Tel-Or E (1993) Mechanisms of salt tolerance in cyanobacteria. In: Gresshoff
PM (ed) Plant responses to the environment. CRC Press, Boca Raton, FL, pp 692–698
Goel S, Gautam M, Kaushik BD (1997) Nitrogen fixation and protein profiles of halotolerant
Nostoc muscorum-R strain isolated from rice fields and ARM-221 strain. Indian J Exp Biol
35:746–750
Gollerbach MM, Novichkova LN, Sdubrikova NV (1956) The algae of takyrs. In: Takyrs of
Western Turkmenia and routes of their agricultural conquest. Izd AN SSSR, Moscow,
pp 610–635
Gopalaswamy G, Karthikeyan CV, Raghu R, Udayasuriyan V, Apte SK (2007) Identification of
acid-stress-tolerant proteins from promising cyanobacterial isolates. J Appl Phycol
19:631–639
Gupta RK, Abrol IP (1990) Salt affected soils: their reclamation and management for crop production.
Adv Soil Sci 9:223–286
Hagemann M, Erdmann N (1994) Activation and pathway of glucosylglycerol synthesis in the
cyanobacterium Synechocystis sp. PCC 6803. Microbiology 140:1427–1431
Hagemann M, Erdmann N (1997). Environmental stresses. In: Rai AK (ed) Cyanobacterial nitrogen
metabolism and environmental biotechnology. Springer, Heidelberg; Narosa Publishing
House, New Delhi, pp 156–221
Hagemann M, Marin K (1999) Salt-induced sucrose accumulation is mediated by sucrosephosphate-synthase in cyanobacteria. J Plant Physiol 155:424–430
Hagemann M, Effmert U, Kerstan T, Schoor A, Erdmann N (2001) Biochemical characterization
of glucosylglycerol-phosphate synthase of Synechocystis sp. strain PCC 6803: comparison of
crude, purified, and recombinant enzymes. Curr Microbiol 43:278–283
Hagemann M, Erdmann N, Wittenberg E (1987) Synthesis of glucosylglycerol in salt stressed
cells of the cyanobacterium Microcystis firma. Arch Microbiol 148:275–279
Hagemann M, Fulda S, Schubert H (1994) DNA, RNA, and protein synthesis in the cyanobacterium
Synechocystis sp. PCC 6803 adapted to different salt concentrations. Curr Microbiol 28(4):
201–207
Haroun SA, Hussein MH (2003) The promotive effect of algal biofertilizers on growth, protein
pattern and some metabolic activities of Lupinus termis plants grown in siliceous soil. Asian J
Plant Sci 2:944–951
Harper KT, Pendleton RL (1993) Cyanobacteria and cyanolichens: can they enhance availability
of essential minerals for higher plants? Great Basin Nat 53:59–72
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Ann Rev Plant Physiol Plant Mol Biol
51:463–499
Hashem MA (2001) Role of blue-green algal inoculum for improving soil fertility and reclaiming
salinity of soil. Research report. BARC Dhaka, Bangladesh, p 2
Heefner DL, Harold FM (1982) ATP-driven sodium pump in Streptococcus faecalis. Proc Natl
Acad Sci U S A 79(9):2798–2802
Hengge-Aronis R (1993) Survival of hunger and stress: the role of rpoS in early stationary phase
gene regulation in E. coli. Cell 72:165–168
Hoffmann L (1989) Algae of terrestrial habitats. Bot Rev 55:77–105
Holtmann G, Bakker EP, Uozumi N, Bremer E (2003) KtrAB and KtrCD: two K+ uptake systems
in Bacillus subtilis and their role in adaptation to hypertonicity. J Bacteriol 185:1289–1298
Hu C, Zhang D, Huang Z, Liu Y (2003) The vertical micro distribution of cyanobacteria and green
algae within desert crusts and the development of the algal crusts. Plant Soil 257:97–111
Huang F, Fulda S, Hagemann M, Norling B (2006) Proteomic screening of salt-stress-induced
changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 6(3):910–920
Hufleijt M, Tremolieres A, Pineau B, Lang J, Hatheway J, Packer L (1990) Changes in membrane
lipid composition during saline growth of the fresh water cyanobacterium Synechococcus
6311. Plant Physiol 94:1512–1521
9
Cyanobacterial Reclamation of Salt-Affected Soil
269
Ishitani M, Nakamura T, Han SY, Takabe T (1995) Expression of the betaine aldehyde
dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Mol Biol
27:307–315
Iyer V, Fernandes TA, Apte SK (1994) A role of osmotic stress-induced proteins in the osmotolerance
of a nitrogen-fixing cyanobacterium Anabaena sp. strain L-31. J Bacteriol 176:5868–5870
Jeffries DL, Link SO, Klopatek JM (1993a) CO2 fluxes of cryptogamic crusts. I Response to
resaturation. New Phytol 125:163–174
Jeffries DL, Link SO, Klopatek JM (1993b) CO2 fluxes of cryptogamic crusts II. Response to
dehydration. New Phytol 125:391–396
Jha MN, Kaushik BD (1988) Response of Westiellopsis prolifica and Anabaena sp. to salt stress II.
Uptake of Na+ in the presence of K+ as chloride, nitrate and phosphate. Curr Sci 57:667–668
Jha MN, Venkataraman GS, Kaushik BD (1987) Response of Westiellopsis prolifica and Anabaena
sp. to salt stress. Mircen J 3:99–103
Joset F, Jeanjean R, Hagemann M (1996) Dynamics of response of cyanobacteria to salt stress:
deciphering the molecular events. Physiol Plant 96:738–744
Kamada Y, Jung US, Piotrowski J, Levin DE (1995) The protein kinase C-activated MAP kinase
pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response.
Genes Dev 9:1559–1571
Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic
stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803.
Biochem Biophys Res Commun 290:339–348
Kannaiyan S (1990) Biotechnology of biofertilizer for rice crop. TNAU, Coimbatore, Tamil Nadu,
India, p 212
Kannaiyan S, Kumar K, Pandiyarajan P (1992) The use of saline tolerance cyanobacteria for salt
affected lands. In: Proceedings of the international symposium on strategies for utilizing salt
affected lands. Bangkok, Thailand, pp 394–404.
Karandashova I, Elanskaya I, Marin K, Vinnemeier J, Hagemann M (2002) Identification of genes
essential for growth at high salt concentrations using salt-sensitive mutants of the cyanobacterium
Synechocystis sp. strain PCC 6803. Curr Microbiol 44:184–188
Kashyap AK, Pandey KD, Sarkar S (1996) Enhanced hydrogen photoproduction by non-heterocystous cyanobacterium Plectonema boryanum. Int J Hydrogen Energy 21:107–109
Kates M, Pugh EL, Ferrante G (1984) Regulation of membrane fluidity by lipids desaturases.
Biomembranes 12:379–395
Kaushik BD (1989) Reclamative potential of cyanobacteria in salt-affected soils. Phykos 28:101–109
Kaushik BD (1994) Algalization of rice in salt-affected soils. Ann Agric Res 14:105–106
Kaushik BD (2005). Reclamation of salt affected soil through cyanobacteria. In: Advances in
microbiology at IARI 1961–2004, pp 160
Kaushik BD, Krishnamurti GSR (1981) Effect of blue-green algae and gypsum application on
physico-chemical properties of alkali soils. Phykos 20:91–94
Kaushik BD, Nagar AP (1993) Sodium uptake by halotolerant Westiellopsis prolifica in presence
of K, Ca, Mg, Fe and Li. Indian J Microbiol 33:93–96
Kaushik BD, Subhashini D (1985) Amelioration of salt affected soils with blue green algae II.
Improvement in soil properties. Proc Indian Nat Sci Acad B51:386–389
Kaushik BD, Krishnamurti GSR, Venkataraman GS (1981) Influence of blue-green algae on
saline alkali soils. Sci Cult 47:169–170
Kempf B, Bremer E (1998) Uptake and synthesis of compatible solutes as microbial stress
responses to high-osmolality environments. Arch Microbiol 170:319–330
Keurson GW, Miernyk JA, Budd K (1984) Evidence for the occurrence of, and possible physiological role for, cyanobacterial calmodulin. Plant Physiol 75:222–224
Khamutov G, Fry IV, Hufleizt ME, Packer L (1990) Membrane lipid composition, fluidity and
surface change in response to growth of the freshwater cyanobacterium Synechococcus 6311
under high salinity. Arch Biochem Biophys 277:263–267
Khan ZUM, Tahmida Begum ZN, Mandal R, Hossain R (1994) Cyanobacteria in rice soils. World
J Microbiol Biotechnol 10:296–298
270
N.K. Singh and D.W. Dhar
Khummongkol D, Canterford GS, Fryer C (1982) Accumulation of heavy metals in unicellular
algae. Biotechnol Bioeng 24:2643–2660
Komarek J (1998) Studies on the cyanophytes of Cuba. Folia Glo-Bot Phytotaxon 30:81–90
Kratz WA, Myers J (1955) Photosynthesis and respiration of three blue-green algae. Plant Physiol
30:275–280
Kroll D, Meierhoff K, Bechtold N, Kinoshita M, Westphal S, Vothknecht UC, Soll J, Westhoff P
(2001) VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane
formation. Proc Natl Acad Sci U S A 98(7):4238–4242
Krulwich TA (1983) Na+/H+ antiporters. Biochim Biophys Acta 726(4):245–264
Krulwich TA, Guffanti AA (1989) The Na+ cycle of extreme alkalophiles: a secondary Na+/H+
antiporter and Na+/ solute symporters. J Bioenerg Biomembr 21:663–677
Ladha JK, Reddy PM (1995) Extension of nitrogen fixation to rice: necessity and possibilities.
Geol J 35:363–372
Lange OL, Meyer A, Zellner H, Heber U (1994) Photosynthesis and water relations of lichen
soil-crusts: field measurements in the coastal fog zone of the Namib Desert. Funct Ecol
8:253–264
Lange W (1974) Chelating agents and blue-green algae. Can J Microbiol 20:1311–1321
Lockau W, Pfeffer S (1983) ATP-dependent calcium transport in membrane vesicles of the
cyanobacterium, Anabaena variabilis. Biochim Biophys Acta 733:124–132
Mackay MA, Horton RS, Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria.
J Gen Microbiol 130:2177–2191
Mackay MA, Norton RS, Borowitzka LJ (1983) Marine blue-green algae have a unique osmoregulatory system. Mar Biol 73:301–307
Malam IO, Le Bissonnais Y, Defarge C, Trichet J (2001a) Role of a microbial cover on structural
stability of a sandy soil in Sahelian part of western Niger. Geoderma 101:15–30
Malam IO, Stal JL, Defarge C, Coute A, Trichet J (2001b) Nitrogen fixation by microbial crusts
from desiccated Sahelian soils (Niger). Soil Biol Biochem 33:1425–1428
Malam Issa O, Défarge C, Bissonnais LY, Marin B, Duval O, Bruand A, D’Acqui LP, Nordenberg S,
Annerman M (2007) Effects of the inoculation of cyanobacteria on the microstructure and the
structural stability of a tropical soil. Plant Soil 290:209–219
Mandal B, Vlek PLG, Mandal LN (1998) Beneficial effect of blue green algae and Azolla excluding
supplying nitrogen, on wetland rice fields: a review. Biol Fertil Soils 27:329–342
Marin K, Huckauf J, Fulda S, Hagemann M (2002) Salt-dependent expression of glucosylglycerolphosphate synthase, involved in osmolyte synthesis in the cyanobacterium Synechocystis sp.
strain PCC 6803. J Bacteriol 184:2870–2877
Marin K, Kanesaki Y, Los DA, Murata N, Suzuki I, Hagemann M (2004) Gene expression profiling
reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803. Plant
Physiol 136(2):3290–3300
Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata
N (2003) Identification of histidine kinases that act as sensors in the perception of salt stress
in Synechocystis sp. PCC 6803. Proc Natl Acad Sci U S A 100:9061–9066
Marin K, Zuther E, Kerstan T, Kunert A, Hagemann M (1998) The ggpS Gene from Synechocystis
sp. Strain PCC 6803 encoding glucosyl-glycerol-phosphate synthase is involved in osmolyte
synthesis. J Bacteriol 180:4843–4849
Matsuda N, Kobayashi H, Katoh H, Ogawa T, Futatsugi L, Nakamura T, Bakker PE, Uozumi N
(2004) Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC
6803 and its role in the early phases of cell adaptation to hyperosmotic shock. The J of. Biol
Chem 279(52):54952–54962
McLachlan J, Gorham PR (1961) Growth of Microcystis aeruginosa Kütz. in a precipitate-free
medium buffered with Tris. Can J Microbiol 7:869–882
Metting B (1990) Microalgae applications in agriculture. Dev Ind Microbiol 31:265–270
Miao X, Wu Q, Wu G, Zhao N (2003) Changes in photosynthesis and pigmentation in an agp
deletion mutant of the cyanobacterium Synechocystis sp. Biotechnol Lett 25(5):391–396
Mikami K, Kanesaki Y, Suzuki I, Murata N (2002) The histidine kinase Hik33 perceives osmotic
stress and cold stress in Synechocystis sp. PCC 6803. Mol Microbiol 46:905–915
9
Cyanobacterial Reclamation of Salt-Affected Soil
271
Mikkat S, Hagemann M (2000) Molecular analysis of the ggtBCD operon of Synechocystis sp.
strain PCC 6803 encoding the substrate-binding protein and the transmembrane proteins of an
ABC transporter for the osmoprotective compound glucosylglycerol. Arch Microbiol 174:
273–282
Mikkat S, Effmert U, Hagemann M (1997) Uptake and use of the osmoprotective compounds
trehalose, glucosylglycerol, and sucrose by the cyanobacterium Synechocystis sp. PCC6803.
Arch Microbiol 167:112–118
Mikkat S, Hagemann M, Schoor A (1996) Active transport of glucosylglycerol is involved in salt
adaptation of the cyanobacterium Synechocystis sp. strain PCC 6803. Microbiology
142:1725–1732
Miller A (1976) The climate of Chile. In: Schwerdfeger W (ed) World survey of climatology:
climate of Central and South America. Elsevier, Amsterdam, vol 12, pp 113–145
Misra S, Kaushik BD (1989a) Growth promoting substances of cyanobacteria. I. Vitamins and
their influence on rice plant. Proc Indian Natl Sci Acad B55:295–300
Misra S, Kaushik BD (1989b) Idems. II. Detection of amino acids, sugars and auxins. Proc Indian
Natl Sci Acad B55:499–504
Mitra AK (1951) The algal flora of certain Indian soils. Indian J Agric Sci 21:357–373
Mochizuki-Oda N, Oosawa F (1985) Amiloride-sensitive Na+/H+ antiporter in Escherichia coli.
J Bacteriol 163:395–397
Morbach S, Kramer R (2002) Body shaping under water stress: osmosensing and osmoregulation
of solute transport in bacteria. ChemBioChem 3:384–397
Murvanidze GV, Glagolev AN (1982) Electrical nature of taxis signal in cyanobacteria. J Bacteriol
150:239–244
Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K, Takabe T (1997) Expression
of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine non-accumulator, and
possible localization of its protein in peroxisomes. Plant J 11:1115–1120
Nakamura T, Yuda R, Unemoto T, Bakker EP (1998) KtrAB, a new type of bacterial K+ uptake
system from Vibrio alginolyticus. J Bacteriol 180:3491–3494
Nelson DE, Shen B, Bohnert HJ (1998). Salinity tolerance mechanisms, models and the metabolic
engineering of complex traits. In: Setlow J (ed) Genetic engineering, principles and methods,
vol. 20. Plenum Press, New York, pp 153–176
Nisha R, Kaushik A, Kaushik CP (2007) Effect of indigenous cyanobacterial application on
structural stability and productivity of an organically poor semi-arid soil. Geoderma 138:49–56
Norris PR, Kelly DP (1977) Accumulation of cadmium and cobalt by Saccharomyces cerevisiae.
J Gen Microbiol 99:317–324
Nystrom T, Neidhardt FC (1993) Isolation and properties of a mutant of Escherichia coli with an
insertional inactivation of the uspA gene, which encodes a universal protein. J Bacteriol
175:3949–3956
Oren A (1999) Bioenergetic aspects of halophilism. Microbiol Mol Biol Rev 63:334–348
Padan E, Schuldiner S (1994) Molecular physiology of Na+/H+ antiporters, key transporters in
circulation of Na+ and H+ in cells. Biochim Biophys Acta 1185:129–151
Padan E, Schuldiner S (1996) Bacterial Na+/H+ antiporters: molecular biology, biochemistry, and
physiology. In: Konings WN, Kaback HR, Lolkema JS (eds) Handbook of biological physics.
Elsevier Science, Amsterdam, Netherlands, pp 501–531
Pandey KD, Shukla PN, Giri DD, Kashyap AK (2005) Cyanobacteria in alkaline soil and the
effect of cyanobacteria inoculation with pyrite amendments on their reclamation. Biol Fertil
Soils 41:451–457
Pandey PK, Singh SP (1993) Hg+2 uptake in a cyanobacterium. Curr Microbiol 26:155–159
Pandey PK, Singh BB, Mishra R, Bisen PS (1996) Ca+2 uptake and its regulation in the cyanobacterium Nostoc MAC. Curr Microbiol 32:332–335
Pandhal J, Snijders APL, Wright PC, Biggs CA (2008) A cross-species quantitative proteomic
study of salt adaptation in a halotolerant environmental isolate using 15N metabolic labelling.
Proteomics 8:2266–2284
Paschinger H (1977) DCCD induced sodium uptake by Anacystis nidulans. Arch Microbiol
113:285–291
272
N.K. Singh and D.W. Dhar
Pendleton RL, Warren SD (1995) Effects of cryptobiotic soil crusts and VA mycorrhizal inoculation on growth of five rangeland plant species. In: West NE (ed) Proceedings of the
fifth international rangeland congress. Society for Range Management, Salt Lake City, UT,
pp 436–437
Pettersson A, Hallbom L, Bergman B (1986) Aluminium uptake by Anabaena cylindrica. J Gen
Microbiol 132:1771–1774
Piccioni RG, Mauzerall DC (1978) Calcium and photosynthetic oxygen evolution in cyanobacteria. Biochim Biophys Acta 504:384–397
Pinner E, Padan E, Schuldiner S (1992) Cloning, sequencing, and expression of the nhaB gene,
encoding a Na+/H+ antiporter in Escherichia coli. J Biol Chem 267:11064–11068
Prabu PC, Udayasoorian C (2007) Native cyanobacteria Westiellopsis (TL-2) sp for reclaiming
paper mill effluent polluted saline sodic soil habitat of India. EJEAFChe 6(2):1775–1786
Rai LC, Singh S, Pradhan S (1998) Biotechnological potential of naturally occurring and laboratory grown Microcystis in biosorption of Ni+2 and Cd+2. Curr Sci 74:461–463
Rao DLN, Burns RG (1990) The effect of surface growth of blue-green algae and bryophytes
on some microbiological, biochemical, and physical soil properties. Biol Fertil Soils 9:
239–244
Record MT Jr, Courtenay ES, Cayley DS, Guttman HJ (1998) Responses of E. coli to osmotic
stress: large changes in amounts of cytoplasmic solutes and water. Trends Biochem Sci
23:143–148
Reddy BR, Apte SK, Thomas J (1989) Enhancement of cyanobacterial salt tolerance by combined
nitrogen. Plant Physiol 89:204–210
Reed RH, Stewart WDP (1988) The responses of cyanobacteria to salt stress. In: Rogers JRG
LJ (ed) Biochemistry of the algae and cyanobacteria. Oxford Science, Oxford, pp 217–231
Reed RH, Borowitzka LJ, Mackay MA, Chudek JA, Foster R, Warr SRC, Moore DJ, Stewart
WDP (1986) Organic solute accumulation in osmotically stressed cyanobacteria. FEMS
Microbiol Lett 39(1–2):51–56
Reed RH, Chudek JA, Foster R, Stewart WDP (1984) Osmotic adjustments in cyanobacteria from
hypersaline environments. Arch Microbiol 138:333–337
Reed RH, Richardson DL, Stewart WDP (1985) Na+ uptake and extrusion in the cyanobacterium
Synechocystis PCC 6714 in response to hypersaline treatment. Evidence for transient changes
in plasmalemma Na+ permeability. Biochim Biophys Acta 814:347–355
Reed RH, Stewart WDP (1985) Evidence for turgor sensitive K+ influx in cyanobacteria
Anabaena variabilis ATCC 29413 and Synechocystis PCC 6714. Biochim Biophys Acta
812:155–162
Resch CM, Gibson J (1983) Isolation of the carotenoid-containing cell wall of three unicellular
cyanobacteria. J Bacteriol 155:345–350
Ritter D, Yopp JH (1993) Plasma membrane lipid composition of the halophilic cyanobacterium
Aphanothece halophytica. Arch Microbiol 159:435–439
Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms.
Saline Syst 2005:1–5
Rodríguez AA, Stella AM, Storni MM, Zulpa G, Zaccaro MC (2006) Effects of cyanobacterial
extracellular products and gibberellic acid on salinity tolerance in Oryza sativa L. Saline Syst
2:7. doi:10.1186/1746-1448-2-7
Roger PA (1996) Biology and management of the floodwater ecosystem in rice fields. IRRI,
Manila, pp 229–243
Roger PA, Kulasooriya SA (1980) Blue green algae and rice. The International Rice Research
Institute, Manila, Philippines, p 112
Rogers SL, Burns RG (1994) Changes in aggregate stability nutrient status, indigenous microbial
populations, and seedling emergence following inoculation of soil with Nostoc muscorum.
Biol Fert Soils 18:209–215
Rosen BP (1982) Calcium transport in microorganisms. In: Carafoli E (ed) Membrane transport
of calcium. Academic, London, pp 187–216
Roychoudhury P, Kaushik BD (1989) Solubilization of Mussorie rock phosphate by cyanobacteria.
Curr Sci 58:569–570
9
Cyanobacterial Reclamation of Salt-Affected Soil
273
Roychoudhury P, Kaushik BD, Venkataraman GS (1985) Response of Tolypothrix ceylonica to
sodium stress. Curr Sci 54:1181–1183
Sardeshpande JS, Goyal SK (1981) Distributional pattern of blue green algae in rice field soils of
Konkan region of Maharashtra State. Phykos 20:102–106
Saxena S, Kaushik BD (1992) Polysaccharides (biopolymers) from halotolerant cyanobacteria.
Indian J Exp Biol 30:433–434
Shehata FHA, Whitton BA (1982) Zinc tolerance in strains of blue-green alga Anacystis nidulans.
Br Phycol J 17:5–12
Shields LM, Durrell LW (1964) Algae in relation to soil fertility. Bot Rev 30:92–128
Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in waterstress response. Plant Physiol 115:327–334
Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M,
Suzuki I, Murata N (2005) Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to
different extents in Synechocystis. J Biol Chem 280(22):21531–8
Singh DP (1985) Cu+2 transport in the unicellular cyanobacterium Anacystis nidulans. J Gen Appl
Microbiol 31:277–284
Singh NK, Dhar DW (2006) Sewage effluent: a potential nutrient source for microalgae. Proc
Indian Natl Sci Acad 72:113–120
Singh NK, Dhar DW (2007) Nitrogen and phosphorous scavenging potential in microalgae. Indian
J Biotechnol 6:52–56
Singh PK, Bisoyi RN (1993) Biofertilizers for restoration of soil fertility. In: Singh JS (ed)
Restoration of degraded land: concept and strategies. Rastogi, Meerut, pp 25–47
Singh RN (1950) Reclamation of “Usar” lands in India through blue-green algae. Nature
165:325–326
Singh RN (1961) Role of blue-green algae in nitrogen economy of Indian agriculture. Indian
Council of Agricultural Research, New Delhi, p 175
Singh SC, Sinha RP, Hader DP (2002) Role of lipids and fatty acids in stress tolerance in
cyanobacteria. Acta Protozool 41:297–308
Singh SP (1978) Succession of blue green algae on certain sites near Varanasi. Indian J Microbiol
18:128–130
Singh SP, Yadav V (1985) Cadmium uptake in Anacystis nidulans, effect of modifying factor.
J Gen Appl Microbiol 31:39–48
Smith RJ, Hobson S, Ellis I (1987) Evidence for calcium mediated regulation of heterocyst frequency and nitrogenase activity in Nostoc 6720. New Phytol 105:531–541
Sprott GD, Shaw KM, Jarell KF (1984) Ammonia/potassium exchange in methanogenic bacteria.
J Biol Chem 259:12602–12608
Stal L (2007) Cyanobacteria. Algae and cyanobacteria in extreme environments 11:659–680
Stumpe S, Schlosser A, Schleyer M, Bakker EP (1996) K+ circulation across the prokaryotic cell
membrane: K+ uptake systems. In: Konings WN, Kaback HR, Lolkema JS (eds) Handbook of
biological physics. Elsevier Science BV, Amsterdam, pp 473–499
Subhashini D, Kaushik BD (1981) Amelioration of sodic soils with blue-green algae. Aust J Soil
Res 19:361–366
Subhashini D, Kaushik BD (1982) Nitrogen fixing potential of blue-green algae from saline and
alkali soils. Acta Bot Indica 10:321–322
Subhashini D, Kaushik BD (1984) Amelioration of salt affected soils with blue green algae.
I. Influence of algalization on the properties of saline-alkali soils. Phykos 23:273–277
Suput D (1984) Effect of external ammonium on the kinetics of the sodium current in frog muscle.
Biochim Biophys Acta 771:1–8
Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and
transduction of low-temperature signals in Synechocystis. EMBO J 19:1327–1334
Szabolcs I (1979) Review of research on salt affected soils. Nat Resour Res 28:313–324.
UNESCO, Paris
Szabolcs I (1993) Soils and salinaization. In: Pessarakli M (ed) Handbook of plant and crop stress,
vol 32. Marcel Dekker, New York, pp 344–346
274
N.K. Singh and D.W. Dhar
Tang D, Shi S, Li D, Hu C, Liu Y (2007) Physiological and biochemical responses of Scytonema
javanicum (cyanobacterium) to salt stress. J Arid Environ 71(3):312–320
Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Okhi K, Murata N (1996) Targeted
mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of
polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:
6416–6425
Thomas J (1978) Dinitrogen fixation by blue-green algae from paddy fields. In: Proceedings of an
advisory group meeting, isotopes of biological dinitrogen fixation. International Atomic
Energy Agency, Vienna, pp 89–103
Thomas J, Apte SK (1984) Sodium requirement and metabolism in nitrogen-fixing cyanobacteria.
J Biosci 6:771–794
Tisa LS, Adler J (1995) Cytoplasmic free-Ca+2 level rises with repellents and falls with attractants
in Escherichia coli chemotaxis. Proc Natl Acad Sci U S A 92:10777–10781
Tisa LS, Olivera BM, Adler J (1993) Inhibition of Escherichia coli chemotaxis by v-conotoxin, a
calcium ion channel blocker. J Bacteriol 175:1235–1238
Vaishampayan A, Sinha RP, Hader DP, Dey T, Gupta AK, Bhan U, Rao AL (2001) Cyanobacterial
biofertilizers in rice agriculture. Bot Rev 6:453–516
Venkataraman GS (1975) The role of blue green algae in tropical rice cultivation. In: Stewart WDP
(ed) Nitrogen fixation by free-living microorganisms. Cambridge University Press, London,
pp 207–268
Venkataraman GS (1979). Algal inoculation of rice fields. In: Nitrogen and rice. International Rice
Res. Institute, Los Banos, Philippines, pp 311–321
Venkataraman GS (1981) Blue-green algae for rice production – a manual for its promotion. FAO
Soils bulletin no. 46. FAO, Rome, p 102
Verma KS, Abrol IP (1980) Effect of gypsum and pyrite on soil properties in a highly sodic soil.
Indian J Agric Sci 50:844–851
Verma SK, Singh SP (1990) Factors regulating copper uptake in cyanobacterium. Curr Microbiol
21:33–37
Villbrandt M, Stal LJ (1996) The effect of sulfide on nitrogen fixation in heterocystous and nonheterocystous cyanobacterial mat communities. Algol Stud 83:549–563
Vinnemeier J, Kunert A, Hagemann M (1998) Transcriptional analysis of the isiAB operon in
salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett
169:323–330
Volker U, Engelmann S, Maul RS, Volker A, Schmid R, Mach H, Hecker M (1994) Analysis of
the induction of general stress proteins of Bacillus subtilis. Microbiology 140:741–752
Waditee R, Hibino T, Nakamura T, Incharoensakdi A, Takabe T (2002) Overexpression of Na+/H+
antiporter confers salt tolerance on a fresh water cyanobacterium, making it capable of growth
in sea water. Proc Natl Acad Sci U S A 99:4109–4114
Waditee R, Hibino T, Tanaka Y, Nakamura T, Incharoensakdi A, Takabe T (2001) Halotolerant
cyanobacterium Aphanothece halophytica contains a Na+/H+ antiporter, homologous to
eukaryotic ones, with novel ion specificity affected by C-terminal tail. J Biol Chem
276:36931–36938
Watanabe I, Lee KK, Alimagno BV, Sato M, Del Rosario DC, De Guzman MR (1977) Biological
N2-fixation in paddy field studied by in-situ acetylene reduction assay. Int Rice Res Inst Res
Pap Ser 3:1–16
Whatmore AM, Reed RH (1990) Determination of turgor pressure in Bacillus subtilis: a possible
role for K+ in turgor regulation. J Gen Microbiol 136(12):2521–2526
Whatmore AM, Chudek JA, Reed RH (1990) The effects of osmotic upshock on the intracellular
solute pools of Bacillus subtilis. J Gen Microbiol 136:2527–2535
Whitton BA (2000) Soils and rice fields. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer, Dordrecht, The Netherlands, pp 233–255
Whitton BA, Potts M (2000) The ecology of cyanobacteria, their diversity in time and space.
Kluwer, Dordrecht, The Netherlands, p 669
9
Cyanobacterial Reclamation of Salt-Affected Soil
275
Wiangnon K, Raksajit W, Incharoensakdi A (2007) Presence of a Na+-stimulated P-type ATPase
in the plasma membrane of the alkaliphilic halotolerant cyanobacterium Aphanothece halophytica. FEMS Microbiol Lett 270(1):139–45
Wilkinson MJ, Northcote DH (1980) Plasma membrane ultrastructure during plant protoplast
plasmolysis, isolation and wall regeneration: a freeze-fracture study. J Cell Sci 42(1):401–415
Womack BJ, Gilmore DF, White D (1989) Calcium requirement for gliding motility in myxobacteria.
J Bacteriol 171:6093–6096
Chapter 10
Measuring Environmental Sustainability
of Intensive Poultry-Rearing System
Simone Bastianoni, Antonio Boggia, Cesare Castellini,
Cinzia Di Stefano, Valentina Niccolucci, Emanuele Novelli,
Luisa Paolotti, and Antonio Pizzigallo
Abstract Sustainability of human activities is one of the most important concerns
of the European Union. Consequently, the need to assess the level of sustainability
achieved both at local and at government level is increasing. This process involves
all economic sectors, including agriculture and, in particular, livestock. Until several
years ago livestock production systems were mainly focused on production efficiency and qualitative characteristics of meat. However, nowadays rules regarding
animal welfare and environmental impact are becoming more and more compulsory
and require attention by all the poultry chain. European subsidies are in many cases
linked to an environmentally sound behaviour of farms. However, there is still an
ongoing discussion regarding the definition of sustainable-agriculture strategic
objectives, the criteria to take into account, the actions to develop, and the methodological tools to use for the evaluation. This chapter provides suggestions for
improving the environmental evaluation part of a process of sustainability assessment specific for intensive poultry production. The environmental sustainability
of an intensive poultry-rearing system is evaluated through the use of three different methods: Emergy Evaluation, Ecological Footprint Analysis and Life Cycle
Assessment (LCA). For each of the three methods a review of its application in
agriculture, and specifically in poultry breeding, is presented. Through Emergy
Evaluation we found that diet is the most important impact factor for the analysed
system, accounting for more than 82% of the total emergy flow. Our results obtained
from Ecological Footprint Analysis point out that cropland, which is connected
S. Bastianoni, V. Niccolucci, and A. Pizzigallo
Department of Chemical and Biosystems Sciences and Technologies, University of Siena,
Via A. Moro, 2, 53100 Siena, Italy
A. Boggia (*), C. Di Stefano, E. Novelli, and L. Paolotti
Department of Economics, Appraisal and Food Sciences, University of Perugia,
Borgo XX Giugno, 74, 06121 Perugia, Italy
e-mail: boggia@unipg.it
C. Castellini
Department of Applied Biology, University of Perugia, Borgo XX Giugno, 74,
06121 Perugia, Italy
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_10, © Springer Science+Business Media B.V. 2010
277
278
S. Bastianoni et al.
with chicken diet, is the main land component in the indicator, accounting for 73%
of the total. Particularly, the high quantity of maize and soya needed for feed requires
much cropland. Finally, using LCA, we found that feed production is the element
which contributes the most to the environmental impacts of the system, influencing
the impact category ‘land use’. As Ecological Footprint, LCA regards the cultivation and the transformation of maize and soya as the processes with the strongest
impact. Therefore, although the three methods use specific indicators and methodology, they come to the same conclusions for the system investigated. After applying each method to the poultry system, we propose a comparative analysis between
the three methods, based on four different criteria: representativeness, verifiability, reproducibility, comprehensibility. By comparing the methods according to
these criteria, we found that each of them shows both positive and negative
aspects, strengths and weaknesses, but all of them are effective in representing the
environmental features of a given activity, and the results can be used as input in the
sustainability assessment process. The choice to use Emergy Evaluation, Ecological
Footprint Analysis, or LCA can depend upon the main objective of the assessment
process. However, in many cases it is not necessary a choice because the three
methods can be used together, and the results can be integrated to build combined
indicators, capable to ensure a wide and complete analysis.
Keywords Emergy • ecological footprint • life-cycle assessment • poultry
• sustainability
10.1 Introduction
Poultry is one of the major and fastest growing sources of meat, representing over
25% of European meat production in 2007. Because of their nutrient content and
relatively low caloric value, egg and poultry products are natural candidates to meet
consumer demands of Western countries. Until several years ago, the livestock
production systems were mainly focused on production efficiency and qualitative
characteristics of meat; however, nowadays rules regarding animal welfare and environmental impact are becoming more and more compulsory and require attention
by all the poultry chain. It is widely known that the production of food requires
resources such as land, water, materials, and energy, and causes emissions such as
greenhouse gases, pesticides, heavy metals, and various other wastes. This is particularly evident for intensive animal production that uses a large amount of world grain
(36%) which could be directly used for human nutrition.
However, the rapid evolution of the poultry industry toward intensive production
systems has strongly enhanced the efficiency, the growth and the feed conversion
of birds, but has reduced the resource use per kilogram produced.
Indeed, a recent UK study on the impact of several animal species showed
that poultry resulted as the most environmentally efficient meat comparing
resources used in the production of beef, sheep meat, poultry meat, eggs and milk
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
279
(Williams et al. 2006). Next comes pork, followed by sheep meat and beef. The
efficiency of chicken in converting its feed into meat plays a big part. This efficiency
had been achieved through a strong selection of traditional breeding and through better
matching of feed to the birds’ dietary needs at each stage of their development. The
poultry industry of the future needs to meet increasing consumer demand while
addressing issues of health, safety, animal welfare and environmental impact. At the
same time the increasing relevance of sustainability has initiated a debate on appropriate frameworks and tools that will provide guidance for a measure of sustainability which should capture, address and suggest solutions for a series of issues that affect
different stakeholders. However, sustainability assessment is still not a mature framework and several indexes have been developed with different responses.
The agricultural and rural policy of EU has increased the attention to the environment in the last 10 years; however, there is still an ongoing discussion regarding the
definition of sustainable-agriculture strategic objectives, the criteria to take into account,
the actions to develop, and the methodological tools to use for the evaluation of the
same. Sustainability is a multi-dimensional concept: economic, social and environmental aspects must be considered simultaneously. ‘Sustainable economic development involves maximizing the net benefits of economic development, subject to
maintaining the services and quality of natural resources over time’ (Pearce et al. 1988).
The Renewed EU Sustainable Development Strategy, published in 2006, encourages
development of sustainable indicators to ensure proper assessment of the situation in
each challenge, and not only for an overall monitoring of the strategy. In this way, the
development of indicators and a proper assessment of sustainability are key issues.
This chapter aims to provide suggestions for improving the environmental evaluation part of a process of sustainability assessment specific for intensive poultry
production. In this study environmental sustainability of an intensive poultry-rearing system is evaluated, through the use of three different methods: Emergy
Evaluation, Ecological Footprint Analysis and Life Cycle Assessment (LCA). For
each of the three methods a review of its application in agriculture, and specifically
in poultry breeding, is presented.
After applying each method to the poultry system, we propose a comparative
analysis among the three methods, based on four different criteria: representativeness, verifiability, reproducibility, comprehensibility.
10.2 The Intensive Poultry-Rearing System
The farm surface area is 1.5 ha. Part of this area belongs to the animals’ buildings
(2,585 m2 of covered surface), and the remaining surface to firm’s road network.
The construction materials are mainly steel tubes, bricks, polyvinyl chloride, polyurethane and concrete for the foundations. The shelters are air conditioned to maintain a constant humidity level (65–85%) and the right temperature (17–28°C) in
order to maximize the chickens’ performances. Feed and drinking systems are
completely automatic. Table 10.1 shows the main characteristics of the farm. The
280
S. Bastianoni et al.
Table 10.1 Main characteristics
of poultry-rearing system
Buildings and space allowance
Total birds per cycle (n)
Surface area covered (m2)
Density (birds/m2 covered surface)
Productive performancea
Final weight (kg)
Age at slaughtering (days)
Daily weight gain (g/day)
Cycles of production/year (n)
Feed index
Mortality rate (%)
Output after slaughtering (%)
a
Table 10.2 Diet composition for poultry rearing,
from the Ross Breeders–
Broiler management manual
(Aviagen Technical Team
1999)
45.334
2.585
17.5
2.6
50
51.2
6
2.02
4
83
Mean performance considering a female/male ratio = 1
Total ingredients
Maize
Wheat bran
Sorghum
Soybean oil
Soybean meal
Salt
Bicalcium phosphate
Calcium bicarbonate
Additives
Coccidiostatic
DL-methionine
100%
40.00%
8.00%
12.00%
1.00%
34.00%
2.00%
1.00%
1.00%
0.80%
0.03%
0.01%
analysis concerns the poultry production of a whole year. Energy and material
requirements for poultry were assessed at the end of the growing period without
taking into account transport to the slaughtering house, slaughtering, processing of
carcasses and distribution.
The accounted animals in a year are 261,120, depurated of mortality rate. The
duration of each cycle is 50 days which implies six cycles of production in a year.
The genetic strain of birds is ROSS 308. When animals arrive at the farm they are
about 40 g, while their mean weight when they leave is 2.6 kg; therefore feed index
is 2.02. After the end of every production cycle the rearing buildings are cleaned
and sanitised and there is an all-in all-out period of 10 days. All the indicators containing a reference to weight measure units took into account the carcass weight,
calculated as 83% of the live weight.
The diet is formulated with common ingredients according to the standard
recommendations of Ross Breeders-Broiler management manual (Aviagen Technical
Team 1999). Table 10.2 illustrates the diet composition. For each productive cycle
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
281
several vaccines and antibiotic treatments are administered. Coccidiostatic molecules
are also administered until 10 days before slaughtering age.
10.3 The Methods
10.3.1 Life Cycle Assessment
Life Cycle Assessment (LCA) has been defined by International Standardization
Organization (ISO) 14040 of 2006 as a ‘compilation and evaluation of the inputs
and outputs and the potential environmental impacts of a product system throughout its life cycle’. It is a method to evaluate the environmental impacts of products,
activities and services, based on a ‘cradle-to-grave’ approach. This means that it is
based on the identification and quantification of the flows of substances, materials
and energy, to and from the techno sphere (which is the set of all human activities)
and the environment, during the entire life cycle of the product or activity. The life
cycle consists of the following phases: extraction of raw materials, production and
assembly of the materials, use, and disposal of the product. Figure 10.1 shows a
scheme of the overall structure of an LCA and of the considered elements.
LCA is an iterative method. This means that initial choices and initial requirements can be adapted later when more information becomes available (Goedkoop
et al. 2008). Also old data can be replaced with new ones or with more precise data,
re-evaluating in this way the earlier actions.
Emissions in air
Raw materials
-Transformation
of raw materials
-Production and
assembly
Energy
-Use and
maintenance
Water
-Disposal
(recycling,
waste
management,
reuse)
Emissions in water
Emissions in soil
Co-products
Fig. 10.1 Structure of a Life Cycle Assessment (ISO 14040)
282
S. Bastianoni et al.
Life Cycle Assessment Framework
Goal
and Scope
Definition
Inventory
Analysis
Interpretation
Direct Applications
•
•
Product Development
and Improvement
•
Strategic Planning
•
Public Policy Making
•
Marketing
•
Other
Impact
Assessment
Fig. 10.2 The general methodological framework for Life Cycle Assessment (ISO 14044)
The implementation of LCA products, services, or production processes is
developing quickly in all the sectors of economic system. In agriculture, and particularly in animal husbandry, the LCA approach is fundamental to have a complete
view of environmental impacts, emissions and resources consumptions which are
involved in every step of the productive chain, from the cultivation of crops and
their transformation for making feed, to the phase of breeding.
Figure 10.2 shows the main methodological framework of LCA, established by
ISO. ISO 14044 sets the requirements for every phase of the LCA. ISO standards
contain the elements that should be considered when conducting an LCA, and when
communicating the results. They are very important guidelines that provide an
international reference on principles, framework and terminology for conducting
and reporting LCA studies. The LCA methodology, according to ISO requirements,
consists of four main phases enumerated below.
10.3.1.1 Goal and Scope Definition
Defining the goal of the study means determining clearly the reasons for carrying out
the study and determining the application, and the intended audiences (Goedkoop
et al. 2008). Some LCA studies could serve more than one purpose and the results
may be used both internally and externally to the subject conducting the study.
The scope definition describes instead the most important methodological choices,
assumptions and limitations made in the study. Initially the Functional Unit or
comparison basis must be defined. It describes the primary function(s) fulfilled by
a product system, and indicates how much of this function is to be considered in the
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
283
intended LCA study. It will be used as a basis for selecting one or more alternative
product systems that might provide these function(s) (Guinée et al. 2002). Therefore
all the process inputs and outputs will refer to the Functional Unit.
After the Functional Unit, it is necessary to determine the system boundaries
intended as the level of tracing of the system; the spatial, temporal, geographical
and technological characteristics of the used data; the criteria for the inputs and
outputs inclusion; and the level of sophistication of the study.
10.3.1.2 Life Cycle Inventory
This phase consists in collecting all the necessary data, and quantifying the inputs
and outputs of the considered production system. Its main result is an inventory
table listing the quantified inputs and outputs associated with the Functional Unit.
The system under study must be modelled as a complex sequence of unitary operations that communicate among themselves and with the environment through inputs
and outputs (Pizzigallo et al. 2008). Two main types of data can be distinguished:
the foreground data, which are typically specific data describing a particular production system, and the background data, which relate to general materials, energy,
transport, waste management. The first should be determined, if possible, by communicating with data providers and developing questionnaires, while background
data can be easily found in databases or the literature.
10.3.1.3 Life Cycle Assessment
This third phase consists in the evaluation of environmental impacts deriving from
the data collected in the Inventory. Life cycle impact assessment is defined by ISO
as the phase in the LCA aimed at understanding and evaluating the magnitude and
significance of the potential environmental impacts of a product system (Goedkoop
et al. 2008). Different impact categories and assessment methods can be selected,
depending on the goal and the scope of the study. Initially, the results of the Inventory
analysis are assigned to relevant impact categories. For example CO2 and CH4
emissions are both assigned to the impact category ‘global warming’, while SO2
and NH3 emissions are both assigned to the impact category ‘acidification’. The
‘baseline’ impact categories are: depletion of abiotic resources, impacts of land use,
climate change, stratospheric ozone depletion, human toxicity, ecotoxicity (aquatic
and terrestrial), photo-oxidant formation, acidification and eutrophication. Moreover,
there are ‘study-specific’ impact categories, which could be included in the LCA
study, depending on its goal and scope (Goedkoop et al. 2008).
Once the impact categories are selected and the Inventory results are assigned to
them, it is necessary to define the characterisation factors. These factors should
reflect the relative contribution of an inventory result to the impact category indicator result. For example, on a time scale of 100 years the contribution of 1 kg CH4
to global warming is 42 times higher than the emission of 1 kg CO2. This means
284
S. Bastianoni et al.
that if the characterisation factor of CO2 is 1, the characterisation factor of CH4 is
42. Thus, the impact category indicator result for global warming can be calculated
by multiplying the LCI result by the characterisation factor.
After characterisation, the normalisation step can be carried out, as optional
step. Normalisation is a procedure needed to show to what extent an impact category contributes to the overall environmental problem. This is done by dividing the
impact category indicators by a ‘Normal’ value. There are different ways to determine the ‘Normal’ value. The most common procedure is to calculate the impact
category indicators for a region during a year, and divide this result by the number
of inhabitants in that area. Finally, it will be necessary to determine which phases
of the production system contribute the most to the identified impacts.
10.3.1.4 Life Cycle Interpretation
This last phase consists in interpreting the results, and compiling conclusions and
recommendations to improve the environmental performances of the studied system.
In the field of animal husbandry several LCA researches have been conducted,
especially for cattle and pig production systems. An interesting article of Halberg
et al. (2005) compares different environmental assessment tools for the evaluation
and improvement of European livestock production systems. Among them, Life
Cycle Assessment and Ecological Footprint Analysis are considered.
Another study evaluates the effectiveness of environmental indicators derived
from three methods that are widely used in animal production: Input–Output
Accounting, Ecological Footprint Analysis and LCA (Thomassen and de Boer
2005). The data used to evaluate the environmental indicators effectiveness were
collected from eight organic dairy farms in the Netherlands.
During the past years several LCA studies comparing different milk production
systems have been conducted. In a Swedish study an LCA is performed on organic
and conventional milk production at farm level in Sweden, focusing especially on
concentrate feed production (Cederberg and Mattsson 2000). Other studies on similar topics consider different aspects of the livestock productions systems, i.e. the
differences in terms of energy flows, in the production of conventional and organic
milk (Grönroos et al. 2006). The study of Haas et al. (2001) applies the LCA methodology to evaluate the impacts caused by three different typologies of pasture:
intensive, extensive and organic.
There are also several LCA studies performed in the sector of pig breeding: for
example, the research by Basset-Mens and van der Werf (2005) compares three
different production systems, while Eriksson et al. (2005) focus on the impact of
feed choice in three pig production scenarios. Other studies consider the environmental impacts of different pig production potential scenarios to illustrate environmental benefits and disadvantages integrated in the production systems (Cederberg
and Flysjö 2004), or to analyse the implications of uncertainty and variability in the
LCA of pig production systems (Basset-Mens et al. 2006).
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
285
Only few researches have been conducted in reference to LCA studies in the poultry
sector. Bennett et al. (2006) present the results of an LCA applied to an Argentinean
conventional production of maize grain, compared with a similar production from a
genetically modified variety, showing its impact when fed to broiler chickens. Another
study (Ellingsen and Aanondsen 2006) aims to assess the environmental impacts of
Norwegian cod fishing and salmon farming, compared with chicken farming.
The study of Pelletier (2008) about the environmental performance in the US
broiler poultry sector aims to analyse, through LCA, the macro scale environmental
impacts of material and energy inputs and emissions along the US broiler supply
chain, as opposed to the most published research regarding the potential environmental impacts of broiler production, which is focused principally only on farmspecific emissions.
10.3.2 Ecological Footprint Analysis
The Ecological Footprint Analysis is a biophysical resources accounting method
able to measure the load that a population or a production activity imposes on the
ecosphere. The Ecological Footprint is an area-based indicator as it expresses the
impact in terms of area (real and virtual) that is effectively required to sustain that
population or activity (Rees 1992; Wackernagel and Rees 1996). Formally, the
Ecological Footprint of a certain population or a production activity is defined as
the area of productive land and water ecosystems required, on a continuous basis,
to produce the resources consumed and to assimilate the waste produced, wherever
on the earth the relevant land/water may be located and with the prevailing technology (Wackernagel and Rees 1996; Monfreda et al. 2004, Wackernagel and Kitzes
2008, Kitzes et al. 2007). The methodology also proposes a second indicator called
Bio-capacity that measures the annual production of biologically provided resources
(Wackernagel and Rees 1996).
Both Bio-capacity and Ecological Footprint are expressed in terms of global
hectares (gha), or hectares with global average productivity (Kitzes et al. 2007;
Galli et al. 2007). It is a normalised unit useful to make a comparison among lands
with different productivity (Monfreda et al. 2004).
Six categories of productive areas are usually included in the calculation: crop
land, grazing land, fishing grounds, forest area, built-up land and energy land (or
carbon footprint, that is the amount of forest land required to capture those carbon
dioxide emissions not sequestered by the oceans) (Wackernagel and Rees 1996).
Yield factor and Equivalence factor are used to translate these six land types into
global hectares (Monfreda et al. 2004). Equivalence factor represents the relative
productivity of the six categories of land and water area, while yield factor represents local to global average productivity of the same land category.
The difference between Bio-capacity and Ecological Footprint defines a sort of
ecological balance. When Ecological Footprint exceeds the Bio-capacity, the region
runs an ecological deficit, which means that a population uses more resources than
286
S. Bastianoni et al.
annually available. The opposite of ecological deficit is ecological reserve or surplus.
The Footprint method is widely used to give a measure of the (un)sustainability of
consumption patterns at different scales: regional (see for example Folke et al.
1997; Bagliani et al. 2008), national (see for example Erb 2004; Medved 2006;
Moran et al. 2008) and global (Van Vuuren and Bouwman 2005; WWF 2006).
Ecological Footprint has also been analysed as temporal series together with
economic indicators such as Gross Domestic Product – GDP (Jorgenson and Burns
2007) and Index of Sustainable Economic Welfare - ISEW (Niccolucci et al. 2007),
or incorporated in thermodynamic-based methods (Zhao et al. 2005, Chen and
Chen 2006; Nguyen and Yamamoto 2007).
Up-to-date industrial and agricultural Footprint applications are still rare. Studies
on cultivation of tomatoes (Wada 1993), conventional versus organic wine farming
(Niccolucci et al. 2008), shrimp and tilapia aquaculture (Kautsky et al. 1997) have
been carried out to highlight the appropriation of natural capital, the efficiency of
natural resource use, and the environmental pressure. Evaluations of the environmental impact of farms (van der Werf et al. 2007) and dairy production (Thomassen
and de Boer 2005) as well as assessment of economic and ecological carrying
capacity of crops (Cuandra and Björklund 2007) proposed the Footprint jointly with
other methods, such as Life Cycle Assessment, Emergy Analysis and Economic
Cost and Return Estimation.
10.3.3 Emergy Evaluation
Solar Emergy (from now Emergy) represents the total amount of available solar
energy (i.e. exergy), directly or indirectly required to make a product or to support
a process; the Emergy of a product is therefore related to the way it is produced. It
is expressed in solar emergy joule (sej). All process inputs (i), including energy of
different types and energy inherent in materials and services, are converted into
Emergy by means of a conversion factor called transformity (Tr, Emergy per unit
energy, sej J−1) and the Emergy flow to a product (Em, sej) is calculated as
Em = ∑ i Tri Ei
(10.1)
where Ei is the available energy. A higher transformity means that more Emergy is
needed to produce a unit amount of output. (See Equation 10.2, where Eo is the
energy of the output (measured), while Tro is the transformity of the output
(calculated).
Tr0 =
Em
E0
(10.2)
The circularity of Equations 10.1 and 10.2 is avoided since, by definition, transformity of solar energy is 1 sej J−1. In this way all inputs are converted into the solar
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
287
equivalent energy needed to create those energy flows; each flow is multiplied by
its transformity and summed, and the result is the amount of total resources (renewable and non-renewable) that have been necessary in order to obtain a product or a
process (Equation 10.1). When an input is available in mass unit, instead of Joules,
a specific emergy is used, measured in sej g−1.
Emergy analysis obeys a logic of memorization (i.e. emergy is ‘accumulated’
over time and not simply ‘conserved’) and therefore needs its own algebra that was
summarised in four main rules by Brown and Herendeen (1996):
1. All emergy sources of a process are assigned to the processes output.
2. By-products from a process have the total emergy assigned to each pathway.
3. When a pathway splits, the emergy is assigned to each ‘leg’ of the split based on
its percentage of the total energy flow on the pathway.
4. Emergy cannot be counted twice within a system: (a) emergy in feedbacks cannot be double counted; (b) by-products, when reunited, cannot be added to equal
a sum greater than the source emergy from which they were derived.
For an in-depth discussion of this issue and the differences between energy and
emergy analyses, see Brown and Herendeen (1996) and Odum (1996). For our
purpose it is important to note that in our calculations among solar energy, rain and
wind, only the highest of the three contributions to the total emergy flow will be
considered, since they are co-products of the same phenomenon, i.e. the sunlight
reaching the biosphere (Odum 1996). The baseline of global emergy flow used in
this paper is 9.44 × 1024 sej year−1. Emergy analysis separates renewable from nonrenewable inputs and local from external inputs. These distinctions allow to define
several emergy-based indicators that can provide decision support tools, especially
when there are several alternatives (Bastianoni and Marchettini 1996; Brown and
McClanahan 1996; Odum 1996; Ulgiati et al. 1995).
Emergy evaluation classifies inputs into different categories (i.e. local renewable,
R, local non-renewable, N; and purchased, F). On the basis of these classes, some
indicators can be computed in order to assess the sustainability of the use of
resources.
The environmental loading ratio (ELR) is the ratio of purchased (F) and nonrenewable local emergy (N) to renewable environmental emergy (R). A high value
of this ratio indicates a low proportion between the use of non-renewable resources
and that of renewable resources, so that environmental cycles are overloaded. The
emergy investment ratio (EIR) is the emergy of purchased inputs (F) divided by
local emergy, both renewable and non-renewable (N + R). A high level of this index
represents a certain fragility of the system because of its dependence on inputs from
other economic systems. The emergy flow density (ED) is given by the total emergy
flow (R + N + F) supporting a system divided by its area. If this ratio is high, a large
quantity of emergy is used in a certain area: this can mean a high stress on the environment and regards the land surface as a limiting factor for future development.
Emergy evaluation is particularly suitable for studies in agriculture, as it is a
system in which natural and man-made contributions interact in order to obtain the
final product, emphasising the role of ecological inputs that constitute the basic life
288
S. Bastianoni et al.
support for living beings, for instance, in primary production (Lagerberg and
Brown 1999; Brandt-Williams 2002).
In the past, emergy was already applied to several agricultural systems, both for
comparative evaluations and simple agricultural systems (see for example Cavalett
et al. 2006; Lefroy and Rydberg 2003; Liu and Chen 2007; La Rosa et al. 2008),
and in particular to grape or wine productions together with exergy and Life Cycle
Assessment (Bastianoni et al. 2003; Pizzigallo et al. 2008). Castellini et al. (2006)
have already emphasised the importance of poultry farming production for Italian
agriculture.
10.4 Results
10.4.1 Life Cycle Assessment
An LCA of an intensive poultry-rearing system has been carried out, considering
data related to the farm for what concerns the breeding phase. The data have been
collected through a direct survey of the farm reality. The goal of the LCA was to
evaluate the environmental impacts associated to the system. The LCA results are then
involved in the comparison with the results of the other two methods, the Emergy
Analysis and the Ecological Footprint. The Functional Unit considered in the LCA
is 1 kg of poultry meat.
For what concerns the scope definition, in this LCA only the phases of production
of raw materials and production of the product ‘poultry meat’ have been taken into
account, leaving out the phases related to the product use and disposal. This choice
has been made to obtain the same basis of comparison of the methods, as the
other two methods do not consider the use and disposal phases, but they only take
into account the production phase. In reference to spatial and temporal boundaries,
European and Italian production systems, during the most recent years, have been
considered as boundaries for the analysis.
With regard to the implementation of the inventory, local data (related to Umbrian
reality) have been used where possible, in particular for the processes ‘maize cultivation’, ‘sorghum cultivation’, and ‘soya cultivation’, which represent some of the
components of the poultry feed, and also for the processes ‘transformation of maize
in feed’, ‘transformation of soya in feed’, and for the overall phase of poultry rearing.
The database Ecoinvent from SimaPro 7 software has been used for the other data
(Nemecek et al. 2004).
The impact assessment phase has been developed using the method ‘EcoIndicator 99’ (Goedkoop and Spriensma 2001). It is a method to measure various
environmental impacts, and it is based on a damage function approach. The damage
function presents the relation between the impact and the damage to human health
or to the ecosystem. Impacts can be computed according to 11 different impact
categories, or they can also be aggregated into three wider categories (Human Health,
Ecosystem Quality, Resources). In our study we present the impact assessment for
the 11 impact categories.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
289
Results of impact assessment are already presented in the normalised version.
Normalisation consists in dividing the impact category indicators by a ‘normal’
value. As said above, the most common procedure is to determine the impact category
indicators for a region during a year and divide this result by the number of inhabitants in that area. Therefore, final results are expressed in Points: the higher the
score, the more important is the impact.
The LCA carried out consists of three main phases: cultivation, feed production
and breeding. Every phase includes different sub-processes. The cultivation phase
involves the cultivation processes of maize, sorghum, soya and grain, which constitute the raw materials of the feed. Every single process includes all the necessary
inputs to obtain the cultivated product (seed, fertilizers, pesticides, use of machinery,
transport inside and outside of the farm), and the related emissions. Regarding emissions derived from the use of fertilizers, a national manual of emissions has been
considered (Bini and Magistro 2002). The second phase investigated consists in the
feed production. It includes, for each crop, the transformation process from crop to
feed, involving mainly water, energy and fuel consumption. In this case emissions
have been evaluated through direct surveys of the firms’ realities. The final product
is then obtained by assembling the transformed crops together with other minor
components (calcium carbonate, sodium chloride, bi-calcium phosphate, and other
chemical organic additives). Finally, in the poultry-breeding phase the main input is
the feed, and the other inputs considered are water, fuel and energy consumption,
and all the infrastructures materials (steel, aluminum, synthetic rubber, glass, plastic,
copper, zinc). The principal emissions related to breeding are also taken into account
(ammonia, methane, dinitrogen monoxide) (European Commission 2003). Table 10.3
reports the main emissions for each phase.
Figure 10.3 shows the principal components belonging to the system life cycle.
Feed production is the element which contributes the most to the environmental
Table 10.3 Principal emissions in the Life Cycle Assessment study (database Ecoinvent; method
of impact assessment Ecoindicator 99)
Process mainly
Value in the
Substance
Unit
Value
contributing
process
(g/FUa)
3.8
Feed production
3.0
NOx
CO2 biogenic
(g/FU)
10.2
Feed production
10.0
CO2 fossil
(g/FU)
677.0
Feed production
567.4
CO biogenic
(mg/FU)
95.1
Feed production
88.6
CO fossil
(g/FU)
1.3
Feed production
1.0
Particulates, <2 mmb
(mg/FU)
382.0
Feed production
335.6
Particulates, >10 mm
(mg/FU)
387.0
Feed production
328.5
Particulates, 2–10 mm
(mg/FU)
197.0
Feed production
174.7
SO2
(g/FU)
2.5
Feed production
2.1
Methane
(mg/FU)
463.0
Breeding phase
463.0
Methane biogenic
(mg/FU)
18.4
Feed production
18.1
Nitrates
(g/FU)
4.3
Feed production
4.1
a
b
FU = Functional unit
mm= Micrometers
290
S. Bastianoni et al.
1 kg
convent
meat
0.63 Tkm
transport
4.26%
1.95 kg
feed
78.8%
0.78 kg
maize feed
21.3%
0.78 kg
maize
20%
0.156 kg
grain feed
5.6%
0.682 kg
soya feed
41.3%
0.156 kg
grain
5.4%
0.682 kg
soya
38.2%
0.234 kg
sorghum feed
7.95%
89.5 m
lorry 32 T
3.45%
0.234 kg
sorghum
7.52%
0.03 kg
diesel
2.96%
Fig. 10.3 Conventional poultry system life cycle. This figure shows the principal processes
involved in the conventional poultry system. For each process the relative quantity (in kg) necessary to produce 1 kg of poultry meat (Functional Unit) and the process contribution to the environmental impact of the system, in percentage, are presented
impacts in the system. In particular the cultivation and then the transformation of
maize and soya are the processes with the strongest impact.
With regard to the impacts assessment, Fig. 10.4 reports the analysis conducted
with Eco-Indicator 99. The figure shows the normalised impact categories. The
category showing the greatest impact is ‘land use’, followed by ‘fossil fuels’ and
‘respiratory inorganics’ categories. The impact assessment carried out for each
phase shows that feed production weighs the most on these three impact categories,
while the breeding phase influences especially the two categories, ‘acidification
and eutrophication’ and ‘respiratory inorganics’ and, to a minor extent, the ‘climate
change’ category.
10.4.2 Ecological Footprint
The Ecological Footprint of a product is defined as the sum of the Footprint of all
the activities required to create, use, and/or dispose of that product (Global Footprint
Network 2009). As suggested by the document ‘Ecological Footprint Standard
2009’ (Global Footprint Network 2009) there are two widely used approaches for
calculating the Footprint of a complex finished product: process-based life-cycle
assessment and extended input–output life cycle assessment.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
291
Points
4.00E−04
3.50E−04
3.00E−04
2.50E−04
2.00E−04
1.50E−04
1.00E−04
5.00E−05
ls
il f
ue
al
ss
er
Fo
in
M
us
s
e
n
nd
La
ca
tio
ty
hi
Eu
O
Ec
tro
p
ot
ox
la
ne
zo
ici
ye
r
n
at
io
di
ge
at
e
ch
an
ni
rg
a
Ac
id
ific
at
io
n/
Cl
im
no
.i
sp
Re
Ra
cs
cs
ni
rg
a
.o
sp
Re
Ca
rc
in
og
en
s
0.00E+00
Fig. 10.4 Conventional poultry system impact assessment. The figure shows the environmental
impact of the conventional poultry system relative to the 11 different impact categories by the
method Eco-Indicator 99. Results are expressed in normalised Points. The higher the score, the
more important is the impact. 4.00E-04 refers to 0.0004
In this study a ‘life cycle approach’ is used. All relevant inputs, from cradle to
gate (until the animals leave the farm, without taking into account slaughtering
processes and retailing), are accounted to give an estimation of environmental
impacts. Information is provided directly by the farm and refer to 2008. Table 10.4
reports the inventory of energy and material data (considered on the basis of their
lifetime) required to sustain this conventional poultry production.
As first step each input is converted into relative bio-productive areas by means
of specific conversion factors as indicated in the footnotes of Table 10.4. When
opportune conversion factors are not directly available, energy intensity coefficients
are adopted to convert data into energy units. A conversion into emission of CO2
and then into the area of forest needed for sequestration is then performed. A worldaverage carbon absorption factor of 0.2071 ha tCO2−1 is used to translate the emissions into forest land necessary to absorb them (Global Footprint Network 2006).
Furthermore, due to the lack of detailed information on the feed, data for 1–12
input are extracted from ECOINVENT® database (Nemecek et al. 2004). In this
way it is possible to know how much carbon dioxide is emitted and how wide are
cropland and built-up land necessary to support the production of one functional
unit of a given input by considering similar production processes. For example, it
was found that the production of 1 kg of maize emits 0.31 kg of CO2 and requires
0.28 m2 of built-up and 1.28 m2 of cropland.
292
S. Bastianoni et al.
Table 10.4 Energy and material data, with relative conversion factor, for conventional poultry
production
Conversion factors
Energy land
Built-up land Crop land
Unit
Quantity
(kg CO2/unit)
(m2/unit)
(m2/unit)
Input
1 Maize
kg
5.48E+05
0.31a
0.28a
1.28a
2 Wheat bran
kg
1.10E+05 0.20a
0.01a
1.26a
a
a
3 Sorghum
kg
1.64E+05 0.20
0.01
1.34b
a
a
4 Soya meal
kg
4.66E+05 0.50
0.05
2.80a
5 Sodium chloride
kg
2.74E+04 0.20a
0.002a
0.00002a
6 Bicalcium
kg
1.37E+04 0.04a
0.003a
0.0001a
phosphate
7 Calcium
kg
1.37E+04 0.04a
0.001a
0.0001a
bicarbonate
8 Additives
kg
1.10E+04 1.60a
0.003a
0.00003a
9 Coccidiostatic
kg
4.52E+02 1.60a
0.003a
0.00003a
10 DL-Methionine
kg
1.37E+02 1.60a
0.003a
0.00003a
a
a
11 Drugs and
kg
2.67E+02 1.60
0.003
0.00003a
antibiotics
12 Disinfectants
kg
2.75E+02 0.40a
0.004a
0.00005a
13 Buildings and
sheltere
14 Machinery
t
3.20E-01
2,770a
15 Steel
t
2.20E-01
2,770a
16 Plastic
t
2.41E-02
1,700a
17 Human labour
Work-days 597.50
–
–
–
18 Electricity
kWh
3.08E+04
0.48c
19 Diesel
l
6.00E+02 2.65d
20 Liquid
l
2.50E+04 1.69d
petroleum gas
21 Copper
kg
1.81E+00 1.53a
0.72a
0.00076a
f
22 Water
l
1.94E+06 0.00037
23 Buildings and
m2
1.50E+03
–
–
–
roads
Output
1
Poultry
kg
5.63E+05
5.48E+05 is for 5.48 × 105.
From Ecoinvent database.
b
Our estimation.
c
Our evaluation on Italian electricity system in 2006.
d
IPCC 2006.
e
This input is the sum of several inputs of different kind. It is not possible to provide a single value
for this input or a single conversion factor. All these data are available upon request.
f
Chambers et al. 2000.
a
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
293
Human labour contribution is also included by allocating the Footprint of an
average Italian citizen (WWF 2006) on the basis of the number of work hours per
year. Each kind of land (energy, cropland and built-up) is then normalised into
global hectares by means of its equivalence factor obtained from the WWF Living
Planet Report (WWF 2006). Finally, the Ecological Footprint for poultry production is given as the sum of all croplands, energy lands and built-up areas.
Results show that the total amount of bio-productive land, or Ecological
Footprint, required for the conventional poultry production is 721.60 gha year that
means 12.81 gm2 year kg−1 of chicken. Comparison with other kind of meat production is not possible due to the lack of specific Footprint literature. However,
Gerbens-Leenes and Nonhebel (2005) estimated the land requirement (values are
expressed in m2 year kg−1) for producing three different types of meat: beef (20.9),
pork (8.9) and chicken (7.3).
The ratio of the total Footprint value with respect to Bio-capacity (item 23 in
Table 10.4, expressed in gm2) measures how much the overall demand exceeds the
local supply of resources. The value calculated for this production is 172. This
means a very high dependence on resources imported from outside of the system
that generally are not renewable. The lower this ratio, the lower the request of natural capital from outside (or greater is the virtual land-component).
Figures 10.5 and 10.6 show the Footprint results by land and consumption categories, respectively. The main Footprint land component is cropland (73%). This
can be related to chickens’ diet that requires high quantities of feed, especially
Built up
Land
6%
Energy
land
21%
Cropland
73%
Fig. 10.5 Ecological Footprint for conventional poultry production disaggregated by land categories.
The main contribution is due to cropland which is highly needed to cultivate maize and soya meal
294
S. Bastianoni et al.
Soya Meal
49%
Sorghum
8%
Wheat
bran
5%
Maize
33%
Others
5%
Fig. 10.6 Ecological Footprint for conventional poultry production disaggregated by consumption categories. Main contributions are related to chickens’ diet
maize and soya meal, which, in turn, requires wide cropland. Energy land (or the
land needed to absorb the carbon dioxide emissions) accounts for 21%, while builtup is just 6%. The other land components are not relevant. These values are quite
typical for this kind of product.
When Footprint is considered according to consumption categories, it is possible
to detect the contribution of each input. Results show that the 95% of the total
Footprint is given by the diet component. In particular, soya meal and maize are
Footprint-intensive cultivation. Footprint results agree with those derived from
Emergy evaluation.
10.4.3 Emergy Analysis
All the results are related to the whole system under analysis. Table 10.5 shows the
emergy evaluation of the system considered. Moreover, all the inputs to the system
are differentiated by their categories, as described in the methods paragraph. Some
of the emergy flows listed in the tables are considered only partially renewable,
according to the percentage of renewable inputs required for their production.
For all the inputs that determine the diet we have considered their characteristics
of renewability/non-renewability. Human labour is also considered partially renewable in emergy evaluation, according to Ulgiati et al. (1994). The diet is the most
important factor in the whole emergy evaluation, accounting for more than 82% of
the total emergy flow. The percentage of renewability of these inputs is not very
high since they come from industrialised agriculture. Conventional poultry production uses techniques that utilise various additives, growth hormones and other
chemicals to help produce their chickens faster and larger in size, aiming to be
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
g
g
J
g
g
g
g
g
g
g
g
g
g
g
g
1.38E+07
3.29E+06
4.41E+04
1.38E+06
1.81E+03
4.06E+05
5.48E+08
1.10E+08
1.64E+08
1.08E+07
4.66E+08
2.74E+07
1.37E+07
1.37E+07
1.10E+07
5.83E+13 c
1.03E+10
1.32E+11
4.73E+10
5.01E+11
2.67E+07
5.84E+11
1.09E+09
2.21E+09
4.30E+03
4.18E+09
6.24E+10
9.86E+09
7.82E+08
5.41E+09
6.92E+08
1.66E+05
1.82E+09
1.00E+09
3.90E+09
1.00E+09
1.48E+10
1.00E+00
8.99E+04
1.50E+03
2.55E+04
7.38E+04
4.74E+07
5.54E+04
d
e
f
d
d
f
f
f
f
f
f
f
f
f
b
a
a
a
a
b
f
d
1.50E+16
7.26E+15
1.90E+08
5.78E+15
1.13E+14
4.01E+15
4.28E+17
5.93E+17
1.14E+17
1.79E+12
8.47E+17
2.74E+16
5.34E+16
1.37E+16
1.62E+17
5.83E+13
9.28E+14
1.98E+14
1.20E+15
3.70E+16
1.27E+15
3.24E+16
J
g
J
J
J
g
J
1
2
3
4
5
6
7
Solar energy
Rain
Wind
Geothermal heat
Erosion of soil
Water
Liquefied petroleum
gas (LPG)
Concrete
Bricks
Straw for litter
Steel
Copper
Plastics
Maize
Wheat bran
Sorghum
Soybean oil
Soy flour
Salt
Bicalcium phosphate
Calcium bicarbonate
Additives
Emergy flow
(sej year−1)
Table 10.5 Raw inputs and emergy evaluation of the poultry production analysed in this study
# Inputs
Unit
Flow
Transformity
Referencea
−1
−1
(unit year )
(sej unit )
(continued)
F
F
42 % R 58 % F
F
F
F
22% R 78% F
42% R 58 % F
37 % R 63 % F
10 % R 90 % F
10 % R 90 % F
F
F
F
F
R
R
R
R
N
N
F
Type of resourcesb
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
295
g
g
g
g
J
J
J
g
23
24
25
26
27
28
29
30
4.52E+05
1.37E+05
2.67E+05
2.75E+05
4.40E+09
1.11E+11
2.06E+10
5.63E+08
Flow
(unit year−1)
1.48E+10
1.48E+10
1.48E+10
1.48E+10
7.38E+06
1.24E+05
6.60E+04
4.27E+09
Transformity
(sej unit−1)
b
b
b
b
f
d
d
Referencea
6.69E+15
2.03E+15
3.95E+15
4.07E+15
3.25E+16
1.38E+16
1.36E+15
2.41E+18
Emergy flow
(sej year−1)
F
F
F
F
10% R 90% F
F
F
Y
Type of resourcesb
a
References for transformity and specific emergy: (a) Odum et al. 2000; (b) Brandt-Williams 2002; (c) Odum 1996; (d) Brown and Arding 1991; (e) Brown
and Buranakarn 2003; (f) Castellini et al. 2006.
b
Local renewable input (R), local non-renewable input (N), purchased input (F).
c
5.83E+13 is for 5.83 × 1013
Coccidiostatic
DL-Methionine
Drugs
Disinfectants
Human labour
Electricity
Diesel
Total emergy flow
Unit
Table 10.5 (continued)
# Inputs
296
S. Bastianoni et al.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
297
Table 10.6 Summary of the main emergy-based indexes for the conventional poultry production
analysed
Emergy index
Expressiona
Value
Unit
Investment ratio (EIR)
F/(N + R)
3.69
–
Environmental loading
(N + F)/R
4.07
–
ratio (ELR)
Empower density (ED)
(R + N+ F)/area
1.61E+14b
sej ha−1·year−1
a
b
Local renewable input (R), local non-renewable input (N), purchased input (F).
1.61E+14 is for 1.61 × 1014.
competitive in the current market. These inputs reach 10% of the total emergy flow
supporting the system and are considered as non-renewable.
Energetic resources, such as fuels, electricity and liquid petroleum gas, human
labour and buildings materials make up the rest of the inputs since the other natural
renewable inputs, such as sun, rain and wind, represent less than 1% of the total.
Table 10.6 shows how the characteristics of renewability and the location of the
inputs are reflected in the emergy indicators. The investment ratio is quite high,
indicating that the emergy acquired from outside the system is 3.69 times higher
than the local emergy. The environmental loading ratio (ELR) indicates that the nonrenewable resources are more than four times higher than the renewable ones,
demonstrating a high concentration of non-renewable inputs in the area, confirmed
by the empower density (ED), that can highly impact the environmental characteristics of the area. The impact suggested by this ratio can be located anywhere, since
the exploitation of non-renewable resources has an impact per se, while their use
implies another impact, the empower density, which is around two orders of magnitude higher that in the case of agricultural or extensive breeding systems; it suggests that the main impact is local. This explains the need of further inputs for the
cleaning up and the additional energy, material (and economic!) expenses for the
environmental and health safety of the system.
10.5 Discussion
In order to assess the quality of the information that each method provides on sustainability, we adopted the following judgement criteria:
1. Representativeness: ability to describe all the features of the observed
phenomenon
2. Verifiability: possibility to check the information of the model
3. Reproducibility: ability to achieve the same results in future time
4. Comprehensibility: ability to be easily understandable for people who do not
deal with the specific research argument
298
S. Bastianoni et al.
10.5.1 Representativeness
Representativeness is the most important feature of the four above-mentioned criteria
because it corresponds to the link between the object to judge and the way it is represented in the analysis. The objective of the analysis, as stated in the introductory
part of the chapter, is to assess the environmental sustainability of a poultry-rearing
system by means of three different methods. Generally, sustainability is connected
with three main dimensions: economic, environmental and social. In the specific case
of the poultry-rearing system we focus particularly on the environmental one.
Two aspects must be analysed to evaluate the state of environmental sustainability of a system: the impact or exploitation of a resource, and the availability of
that resource (Bell and Morse 1999). In our specific case the resource corresponds
to the environment as a whole. In assessing the ability of the three methods to bring
out information on environmental sustainability, we analyse how they reflect the
two aspects just mentioned.
In the three assessment methods the impact on the environment is evaluated in
different ways. This can be easily noticed by the measure unit employed in each
analysis (Table 10.7). LCA has several categories of impact. For each category
there are several indicators. Depending on the aspect observed by the indicators
(damage to human health, damage to ecosystem or damage to mineral and fossil
resources) the measure unit can be Disability Adjusted Life Years (DALY),
Potentially Disappeared Fraction of plant species (PDF m2 year) or additional
energy requirement to compensate lower future ore grade (MJ surplus energy).
LCA provides information about direct and indirect effects on human being caused
by environmental changes. The direct effects are captured by the categories concerning the impact on human health while the indirect effects by the categories
concerning the ecosystem and the mineral and fossil resources. Our results for LCA
(Fig. 10.4) show that the main impact categories affected are in ascending order:
respiratory inorganics, fossil fuels, land use.
In the Ecological Footprint Analysis the indicator used to describe the impact on
the environment is one, the Ecological Footprint. The measure unit is the global
hectare (gha). The Ecological Footprint allows understanding which type of land
category is mainly used or impacted: crop land, land to absorb greenhouse gas emissions, or built-up land (Fig. 10.5). Thanks to the Ecological Footprint, we found that
9.35 gha of the 12.81 gha of impacted land used to produce 1 kg of poultry in a year
belong to the category crop land. Therefore the main human pressure on the ecosystem
for the production of poultry meat derives from crop cultivation.
Among the indicators developed by Emergy Analysis, the Environmental
Loading Ratio is the one focusing more on environmental sustainability. The measure unit is the Solar joule. Our Emergy Analysis shows that four trillion solar joule
are employed to produce 1 kg of meat. This indicator represents the ratio between
resources provided by the economic system (external to the analysed production system and not renewable) and renewable resources, describing in this way
how much the system relies on resources exploited in a not-sustainable manner.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
299
Table 10.7 Denomination of indicators and measure units used in the analysis (Goedkoop and
Spriensma 2001)
Ecological Footprint
Life Cycle Assessment
Analysis
Emergy Analysis
Measure
Measure
Indicators
Measure unit
Indicators
Categories of
unit
unit
employed for
employed for
the indicators
the analysis
the analysis
employed for
the analysis
Carcinogens
DALY
Ecological
gha
Free renewable
sej
Footprint
emergy (R)
sej
Resp. organics
DALY
Bio-capacity
gha
Free nonrenewable
emergy (N)
sej
Resp. inorganics DALY
Purchased
emergy
brought
by the
economic
system (F)
Climate change
DALY
Radiation
DALY
Ozone layer
DALY
Ecotoxicity
PDF m2 year
Acidif./Eutrop.
PDF m2 year
Land use
PDF m2 year
Minerals
MJ surplus
energy
Fossil fuels
MJ surplus
energy
DALY: Disability Adjusted Life Years PDF m2 year: Potentially Disappeared Fraction of plant
species
MJ surplus energy: Additional energy requirement to compensate lower future ore grade
gha: Global hectare
sej: Solar joule
R: local renewable input, N: local non-renewable input, F: purchased input
However, without classifying the type of emergy used, Emergy Analysis is not able
to provide significant information about human counteractions to the impact
produced.
Therefore, considering these differences in terms of measure unit and type and
quantity of indicators used, we can state that the multi-dimensionality of LCA
brings out much more information on the impacts than Ecological Footprint or
Emergy Analysis, also because it considers the indirect effects on human being
caused by environmental changes. The information on the environmental impacts
is broader than in the other methods. A common information that all the three
300
S. Bastianoni et al.
methods convey (Figs. 10.3, 10.6 and Table 10.5) is that the major source of the
impacts is the feed for animals.
On the other hand, Ecological Footprint and Emergy Analysis have other advantages which LCA does not offer. LCA allows giving judgements on the impacts
generated by the poultry production, in relation to a previous state of the environment taken as reference point (Goedkoop and Spriensma 2001). However, a trend
from a previous state does not provide any information about the resources availability and LCA analysis is not able to evaluate how much of the consumed
resources are still available. Although it is not possible to define precisely a sustainable state (Bell and Morse 1999) we cannot affirm that a production system is
environmentally sustainable only considering the dynamism of its impacts.
Instead Ecological Footprint Analysis uses the bio-productive land effectively
owned by the breeding system (Bio-capacity) as an indicator of resources availability. The measure unit of this indicator is the global square meter. The monodimensionality of the method allows comparing the value of impact with the value
of available resource, thus to define if the production system, concerning only the
category of the ecosystem exploitation, is sustainable. In our study the ratio
between Ecological Footprint and Bio-capacity shows that the production system is
not sustainable (Fig. 10.7) because the bio-productivity used by the system is 172
times higher than the bio-productivity really owned.
For what concerns Emergy Analysis, as stated above it is possible to classify the
type of Emergy source used in the system (Fig. 10.8). In our study, 79% of the total
amount of emergy necessary to produce 1 kg of poultry derives from external and
non-renewable factors provided by the economy (F), 1.5% derives from nonrenewable factors available in the spatial boundary of the breeding system, and
19.5% derives from renewable factors. Through the Environmental Loading Ratio,
we can see that the non-renewable emergy is four times higher than the renewable
one. As in the Ecological Footprint Analysis, the mono-dimensionality of the
method allows to compare resources depletion with resources availability (which in
this case can be identified with the rate of renewable factors). Finally the results
show that the breeding is not sustainable.
We can conclude that every method gives useful but different information for the
representativeness of environmental sustainability in the analysed rearing system.
LCA has a micro-focus approach; through its multi-dimensionality it describes in
detail how the human well-being is affected, allowing a real intervention on concrete
problems and indicating the direction to follow with respect to a previous system
state. On the other hand, Ecological Footprint and Emergy Analysis consider the
availability of natural resources and not only the impact produced. This allows to
state if a production system is sustainable from the environmental point of view.
However, only one measure unit and dimension is used, leading to a reduced amount
of information.
Since LCA is composed of multiple indicators it is possible, as some software
allow, to integrate also the indicators concerning Ecological Footprint and Emergy
Analysis. In this way the information on environmental sustainability could be
complete, thanks to the fusion of the three different methods perspectives.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
301
13,00
Built up land
12,00
11,00
global square meter
10,00
9,00
Energy land
8,00
7,00
6,00
Crop land
5,00
4,00
3,00
2,00
1,00
Biocapacity
0,00
Natural resources
availability ( gm2) per Kg
produced
Natural resources
consumption ( gm2) per
Kg produced
Fig. 10.7 Resources exploitation and resources availability in Ecological Footprint Analysis
The analysis refers to a single case study. Nevertheless, the three methods turn
out to be more useful in the environmental sustainability decision-making process
when considering the same production system over time, or comparing two production systems that provide the same output.
There are other important information to take into account about representativeness. The three methods can be considered systemic because the researcher has the
possibility to set the boundaries (spatial and time limits) of the analysed system
(Bell and Morse 1999). A negative aspect concerning Ecological Footprint is the
absence of computation of matter and water depletion, unlike Emergy Analysis and
LCA, in which these two aspects are taken into account for the final values of their
indicators.
A general weakness of LCA method is that often available databases offer data
coming from realities which are very different from the one represented in the study.
In this case the results are not properly representative of the situation investigated.
The resilience effect can be regarded as the strength of Ecological Footprint. In
fact the sub-category of required productive land to absorb carbon dioxide (energy
land) includes the environment mitigation of human greenhouse gases production.
302
S. Bastianoni et al.
4,50E+12
4,00E+12
3,50E+12
Nonrenewable
emergy ( N )
Renewable
emergy ( R )
solar joule
3,00E+12
2,50E+12
Emergy from the
economy ( F )
2,00E+12
1,50E+12
1,00E+12
Renewable
emergy ( R )
5,00E+11
0,00E+00
Natural resources
availability (solar joule) per
Kg produced
Natural resources
consumption (solar joule)
per Kg produced
Fig. 10.8 Resources exploitation and resources availability in Emergy Analysis
Negative and more relevant aspects of Emergy Analysis about representativeness
are strictly related to the general validity of the theory. Ayres (in Hau and Bakshi
2004) argues that it is hard to connect a defined value of solar joule to the matter
(rocks and minerals) and its several specific states. Also Hammond (2007) raises
doubts on the physical validity of Emergy.
10.5.2 Verifiability
In LCA the verifiability of the model is possible but not for the overall set of the
data. In fact foreground data derive from the communication with data providers.
As a consequence they are generally obtained from real measurements or surveys.
On the contrary, background data derive from databases or literature; hence they
could be also assessed values.
Although Ecological Footprint and Bio-capacity are composite indicators based
on a mono-dimensional value they can be considered quite verifiable. In fact both
are a sum of many productive land categories; hence the values of the latter are
measurable with real and existent tools.
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
303
The verifiability of Emergy Analysis information is a major problem. The
measure unit of the model is mono-dimensional and the solar joule values are necessarily assessed since, at the moment, there are no available tools that can directly
measure them.
10.5.3 Reproducibility
Reproducibility of results is one of the advantages of LCA. In fact this assessment
method has a consistent set of specific databases which contain a huge amount of
information. However, the results of the LCA study are strictly dependent upon the
initial assumptions and upon the type of data used, and they can significantly
change if using different information from the databases or starting from different
assumptions. Moreover, if the complexity and the scope of the LCA study increase,
processing time and costs will grow considerably.
Despite the easy computation in Ecological Footprint, the information reproducibility on sustainability pays the consequences of the lack of a specific database.
This problem is highlighted by the calculation of the productive land required to
absorb CO2. There is no matter-specific direct conversion factor to assess this value.
When considering each evaluated item, first of all it is indispensable to find the
amount of greenhouse gas emissions and secondly to get the corresponding productive land to absorb them.
Emergy computation corresponds to a simple product of two factors. The reproducibility of the information raises problems only in reference to the conversionfactor (transformity). In fact, the same transformity was used for many assessed
factors of the breeding system because of the lack of appropriate and specific
conversion factors.
10.5.4 Comprehensibility
Regarding comprehensibility, unfortunately LCA language is not easily understandable by a ‘not expert public’. This is because one of the main outputs of the
method is the inventory table, which represents a long series of data; that is, all the
set of emissions deriving from the system.
On the contrary, comprehensibility is probably the strongest feature of Ecological
Footprint. The indicators language is easily understandable even though specific.
Explaining the concept to farmers from whom data have been collected did not seem
difficult as happened in the case of other models. This was twice as effective on the
survey: first of all because farmers were able to provide more appropriate data to
build the indicator, secondly because this reinforced in themselves the awareness of
being an active part of the survey team. Therefore, the quantity of available information was higher than usual.
304
S. Bastianoni et al.
Unlike Ecological Footprint, the language of Emergy Analysis is not quickly
comprehensible. People who are not used to deale with this specific subject have
difficulties in understanding what a solar joule corresponds to.
Table 10.8 reports the main characteristics of the three different methods and
allows to appreciate the differences for each of the above mentioned criteria. Each
method presents both positive and negative aspects.
10.6 Conclusion
The appropriate instrument for a multi-dimensional representation of sustainability
is a suitable set of indicators that must be an integral part of an assessment methodology. The three methods that we compared in this study provide a solution,
since they are able to cover most of the information needs for the environmental
dimension of sustainability in agriculture. We have detected several analogies when
comparing the methods in terms of results related to the analysed system, that is,
the intensive poultry-rearing farm.
Thanks to the Emergy Evaluation we found that for the analysed system the diet
is the most important factor in the whole analysis, accounting for more than 82%
of the total emergy flow. Our results obtained from Ecological Footprint Analysis
point out that crop land, which is connected with chickens’ diet, is the main land
component, accounting for 73% of the total. The high quantities of maize and soya
needed for feed require much crop land. Finally, thanks to the use of LCA, we
found that feed production is what contributes the most to the environmental
impacts of the system, influencing the impact category ‘land use’. Our LCA analysis comes to the same conclusion as Ecological Footprint: the cultivation and the
transformation of maize and soya are the processes with the strongest impact.
Finally, in our study both Emergy and LCA pointed out that the percentage of
non-renewability of the inputs is high, with respect to the renewable ones. Emergy
leads to this conclusion thanks to the Environmental Loading Ratio, while LCA
thanks to the use of ‘fossil fuels’ impact category. Therefore, although the three
methods use specific indicators and methodology, they come to the same conclusions for the system investigated.
By comparing the methods according to the four criteria of representativeness,
verifiability, reproducibility and comprehensibility, we conclude that each of the
three methods shows both positive and negative aspects, strengths and weaknesses,
but all of them are effective in representing the environmental features of a given
activity; therefore, the results can be used as input in a sustainability assessment
process.
The choice to use Emergy Evaluation, Ecological Footprint Analysis, or LCA
depends upon the main objective of the assessment process. If we are dealing with
a problem of environmental impacts, LCA is a reliable tool to analyse the situation
from a multi-dimensional perspective. On the contrary, if we are dealing with a
problem of resources availability, Ecological Footprint or Emergy Analyses are
Measurable values
Presence of
specific
databases
Verifiability
Reproducibility
Comprehensibility
Many impact
categories
considered
Representativeness
Absence of
specific
database
Easy computation
Results strictly
dependent from
the type of data.
Complexity of
the study implies
more costs and
time
No easy access
language
Easy access
language
Mono-dimensional
Measurable subcategories
Resilience
Ecological Footprint Analysis
Positive aspects
Negative aspects
Systemic.
No matter
and water
depletion
computation
Carrying capacity
Some values
necessarily
assessed
Data from realities
different from the
one investigated
No resilience
Table 10.8 The three methods positive and negative aspects
Life Cycle Assessment
Positive aspects
Negative aspects
Systemic
No carrying
capacity
Easy
computation
Matter and water
computation
Carrying
capacity
Emergy Analysis
Positive aspects
Systemic
No easy access
language
Mono-dimensional.
Values
necessarily
assessed.
Absence of specific
database
Uncertainty of
basic theory
assumptions
Negative aspects
No resilience
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
305
306
S. Bastianoni et al.
better ways to evaluate the exploitation level of the analysed resources. However,
in many cases it is not necessary a choice because the three methods can be used
together, and the results can be integrated to build combined indicators, capable to
ensure a wide and complete analysis.
Therefore, all environmental impact indicators used in our study, resulting from
the application of the three methods to the case study, constitute a proper set of
environmental indicators, to be used for sustainability assessment. So far, there are
too few applications of the three methods in agriculture. In particular, in the livestock
sector they are really rare, and the situation in poultry breeding is even worse. On
the other hand, the need to conduct studies on the relationships between livestock
and the environment is widespread throughout the world.
References
Aviagen Technical Team (1999) Ross breeders broiler management manual. Aviagen Ltd.,
Newbridge, Midlothian, Scotland
Bagliani M, Galli A, Niccolucci V, Marchettini N (2008) Ecological footprint analysis applied to
a sub-national area: the case of the Province of Siena (Italy). J Environ Manage
86(2):354–364
Basset-Mens C, van der Werf HMG (2005) Scenario-based environmental assessment of farming systems: the case of pig production in France. Agric Ecosyst Environ 105(1–2):
127–144
Basset-Mens C, van der Werf HMG, Durand P, Leterme P (2006) Implications of uncertainty and
variability in the life cycle assessment of pig production systems. Int J Life Cycle Assess
11(5):298–304
Bastianoni S, Marchettini N (1996) Ethanol production from biomass: analysis of process efficiency and sustainability. Biomass Bioenergy 11(5):411–418
Bastianoni S, Nielsen SN, Marchettini N, Jørgensen SE (2003) Use of thermodynamic functions
for expressing some relevant aspects of sustainability. Int J Energy Res 29(1):53–64
Bell S, Morse S (1999) Sustainability indicators: measuring the immeasurable. Earthscan,
London
Bennett RM, Phipps RH, Strange AM (2006) The use of life cycle assessment to compare the
environmental impact of production and feeding of conventional and genetically modified
maize for broiler production in Argentina. J Anim Feed Sci 15(1):71–82
Bini G, Magistro S (a cura di) (2002) Manuale dei fattori di emissione nazionali. Centro Tematico
Nazionale Atmosfera Clima ed Emissioni in Aria, Rapporto n.01.
Brandt-Williams S (2002) Emergy of Florida agriculture, folio #4, Handbook of emergy evaluation. Center for Environmental Policy, University of Florida, Gainesville, FL
Brown MT, Arding J (1991) Transformities Working Paper. Center for Wetlands, University of
Florida, Gainesville, FL
Brown MT, Buranakarn V (2003) Emergy indices and ratios for sustainable material cycles and
recycle options. Resour Conserv Recycl 38(1):1–22
Brown MT, Herendeen RA (1996) Embodied energy analysis and emergy analysis: a comparative
view. Ecol Econ 19:219–235
Brown MT, McClanahan T (1996) Emergy analysis perspectives of Thailand and Mekong river
dam proposals. Ecol Model 91:105–130
Bukovac MJ, Wittwer SH (1957) Absorption and mobility of foliar applied nutrients. Plant
Physiol 32:428–435. PMCID: PMC540953
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
307
Castellini C, Bastianoni S, Granai C, Dal BA, Brunetti M (2006) Sustainability of poultry production using the emergy approach: comparison of conventional and organic rearing systems.
Agric Ecosyst Environ 114:343–350
Cavalett O, Queiroz JF, Ortega E (2006) Emergy assessment of integrated production systems of
grains, pig and fish in small farms in the South Brazil. Ecol Model 193:205–224
Cederberg C, Flysjö A (2004) Environmental Assessment of Future Pig Farming Systems –
Quantifications of Three Scenarios from the FOOD 21 Synthesis Work, SIK Report No. 723.
Swedish Institute for Food and Biotechnology, Göteborg, Sweden, 54 pp
Cederberg C, Mattsson B (2000) Life Cycle Assessment of milk production – a comparison of
conventional and organic farming. J Cleaner Prod 8(1):49–60
Chen B, Chen GQ (2006) Modified ecological footprint accounting and analysis based on embodied exergy – a case study of the Chinese society 1981–2001. Ecol Econ 61:355–376
Cuandra M, Björklund J (2007) Assessment of economic and ecological carrying capacity of
agricultural crops in Nicaragua. Ecol Indic 7(1):133–149
Eggelston S, Buendia L, Miwa K, Ngara T, Tanabe K (Eds) (2006) IPCC (Intergovernmental Panel
on Climate Change) Guidelines for National Greenhouse Gas Inventories. Institute for Global
Environmental Strategies for the IPCC
Ellingsen H, Aanondsen A (2006) Environmental impacts of wild caught cod and farmed salmon
– a comparison with chicken. Int J Life Cycle Assess 11(1):60–65
Erb KH (2004) Actual land demand of Austria 1926–2000: a variation on Ecological Footprint
assessments. Land Use Policy 21:247–259
Eriksson IS, Elmquist H, Stern S, Nybrant T (2005) Environmental systems analysis of pig production, the impact of feed choice. Int J Life Cycle Assess 10(2):143–154
European Commission (2003) Integrated Pollution Prevention and Control (IPPC). Reference
Document on Best Available Techniques for Intensive Rearing of Poultry and Pigs
Folke C, Jansson Å, Larsson J, Costanza R (1997) Ecosystems appropriation by cities. Ambio
26:167–172
Galli A, Kitzes J, Wermer P, Wackernagel M, Niccolucci V, Tiezzi E (2007) An exploration of the
mathematics behind the ecological footprint. Int J Ecodyn 2(4):250–257
Gerbens-Leenes W, Nonhebel S (2005) Food and land use. The influence of consumption patterns
on the use of agricultural resources. Appetite 45:24–31
Global Footprint Network (2006) National footprint and biocapacity accounts. Global Footprint
Network, Oakland, CA
Global Footprint Network (2009) Ecological Footprint Standards 2009. Global Footprint Network,
Oakland, CA. www.footprintstandards.org. Accessed on September 2008
Goedkoop M, De Schryver A, Oele M (2008) Introduction to LCA with SimaPro 7. Report of
Product Ecology Consultants, Plotterweg, Netherlands
Goedkoop M, Spriensma R (2001) The Eco-indicator 99 – a damage oriented method for Life
Cycle Impact Assessment. Methodology Report, Product Ecology Consultants, 3rd edn.
Plotterweg, Netherlands
Grönroos J, Seppiala J, Voutilainen P, Seuri P, Koikklainen K (2006) Energy use in conventional and
organic milk and rye bread production in Finland. Agric Ecosyst Environ 117(2–3):109–118
Guinée JB, Gorrée M, Heijungs R, Huppes G, Kleijn R, De Koning A, Van Oers L, Wege-ner SA,
Suh S, Udo de Haes HA, De Bruijn H, Huijbregts MAJ, Lindeijer E, Roorda AAH, Van derVen
BL, Wiedema BP (2002) Handbook on Life Cycle Assessment; operational guide to the ISO
standards. Kluwer, Dordrecht, The Netherlands
Haas G, Wetterich F, Köpke U (2001) Comparing intensive, extensified and organic grassland farming in southern Germany by process life cycle assessment. Agric Ecosyst Environ 83:43–53
Halberg N, van der Werf HMG, Basset-Mens C, Dalgaard R, de Boer IJM (2005) Environmental
assessment tools for the evaluation and improvement of European livestock production systems.
Livest Prod Sci 96(1):33–50
Hammond GP (2007) Energy and sustainability in a complex world: reflections on the ideas of
Howard T. Odum. Int J Energy Res 31:1105–1130
308
S. Bastianoni et al.
Hau JL, Bakshi BR (2004) Promise and problems of emergy analysis. Short communication. Ecol
Model 178:215–225
Jorgenson AK, Burns TJ (2007) The political-economic causes of change in the ecological footprints of nations, 1991–2001: a quantitative investigation. Soc Sci Res 36(2):834–853
Kautsky N, Berg H, Folke C, Larsson J, Troell M (1997) Ecological footprint for assessment of
resource use and development limitations in shrimp and tilapia aquaculture. Aquacult Res
28:753–766
Kitzes J, Peller A, Goldfinger S, Wackernagel M (2007) Current methods for calculating national
ecological footprint accounts. Sci Environ Sustain Soc 4(1):1–9
La Rosa AD, Siracusa G, Cavallaro R (2008) Emergy evaluation of Sicilian red orange production.
A comparison between organic and conventional farming. J Cleaner Prod 16(17):1907–1914
Lagerberg C, Brown MT (1999) Improving agricultural sustainability: the case of Swedish greenhouse tomatoes. J Cleaner Prod 7:421–434
Lefroy E, Rydberg T (2003) Emergy evaluation of three cropping systems in southwestern Australia.
Ecol Model 161(3):193–209
Liu X, Chen B (2007) Efficiency and sustainability analysis of grain production in Jiangsu and
Shaanxi Provinces of China. J Cleaner Prod 15:313–322
Medved S (2006) Present and future ecological footprint of Slovenia – the influence of energy
demand scenarios. Ecol Model 192:25–36
Monfreda C, Wackernagel M, Deumling D (2004) Establishing national natural capital accounts
based on detailed ecological footprint and biological capacity assessments. Land Use Policy
21:231–246
Moran DD, Wackernagel M, Kitzes J, Goldfinger SH, Boutaud A (2008) Measuring sustainable
development – nation by nation. Ecol Econ 64:470–474
Nemecek T, Heil A, Huguenin O, Meier S, Erzinger S, Blaser S, Dux D, Zimmermann A (2004)
Life cycle inventories of agricultural production systems. Final report ecoinvent 2000 No. 15,
Agroscope FAL Reckenholz and FAT Taenikon, Swiss Centre for Life Cycle Inventories,
Dübendorf, CH. www.ecoinvent.ch
Nguyen HX, Yamamoto R (2007) Modification of ecological footprint evaluation method to
include non-renewable resource consumption using thermodynamic approach. Resour Conserv
Recycl 51(4):870–884
Niccolucci V, Galli A, Kitzes J, Pulselli RM, Borsa S, Marchettini N (2008) Ecological Fooprint
analysis applied to the production of two Italian wines. Agric Ecosyst Environ 128:162–166
Niccolucci V, Pulselli FM, Tiezzi E (2007) Strengthening the threshold hypothesis: economic and
biophysical limits to growth. Ecol Econ 60:667–672
Odum HT (1996) Environmental accounting. Emergy and environmental decision making. Wiley,
New York
Odum HT, Brown MT, Brandt-Williams S (2000) Introduction and global budget, folio #1.
Handbook of emergy evaluation. Center for Environmental Policy, University of Florida,
Gainesville, FL
Pearce DW, Barbier E, Markandya A (1988) Sustainable development and cost benefit analysis.
Paper 88/03. IIED/UCL London. Environmental Economics Centre
Pelletier N (2008) Environmental performance in the US broiler poultry sector: life cycle energy
use and greenhouse gas, ozone depleting, acidifying and eutrophying emissions. Agric Syst
98:67–73
Pizzigallo ACI, Granai C, Borsa S (2008) The joint use of LCA and emergy evaluation for the
analysis of two Italian wine farms. J Environ Manage 86:396–406
Rees WE (1992) Ecological Footprints and appropriated carrying capacity: what urban economics
leaves out. Environ Urban 4:121–130
Thomassen MA, de Boer IJM (2005) Evaluation of indicators to assess the environmental impact
of dairy production systems. Agric Ecosyst Environ 111(1–4):185–199
Ulgiati S, Brown MT, Bastianoni S, Marchettini N (1995) Emergy-based indices and ratios to
evaluate the sustainable use of resources. Ecol Eng 5:519–531
10
Measuring Environmental Sustainability of Intensive Poultry-Rearing System
309
Ulgiati S, Odum HT, Bastianoni S (1994) Emergy use, environmental loading and sustainability.
An emergy analysis of Italy. Ecol Model 73:215–268
Van der Werf HMG, Tzilivakis J, Lewis K, Basset-Mens C (2007) Environmental impacts of farm
scenarios according to five assessment methods. Agric Ecosyst Environ 118(1–4):327–338
Van Vuuren DP, Bouwman LF (2005) Exploring past and future changes in the ecological footprint for world regions. Ecol Econ 52:43–62
Wackernagel M, Kitzes J (2008) Ecological footprint. In: Jorgensen SE, Fath BD (eds)
Encyclopedia of ecology. Elsevier B.V., Amsterdam, The Netherlands, pp 1031–1037
Wackernagel M, Rees WE (1996) Our Ecological Footprint: reducing human impact on the Earth.
New Society Publishers, Gabriola Island, British Columbia, Canada
Wada Y (1993) The appropriated carrying capacity of tomato production: the Ecological Footprint
of hydroponic greenhouse versus mechanized open field operations. M.A. Thesis, School of
Community and Regional Planning, University of British Columbia, Vancouver, Canada
Williams AG, Audsley E, Sandars DL (2006) Final report to Defra on project ISO205: Determining
the environmental burdens and resource use in the production of agricultural and horticultural
commodities. Defra, London
WWF (2006) Living Planet Report 2006. WWF, Gland, Switzerland
Zhao S, Li Z, Li W (2005) A modified method of ecological footprint calculation and its application.
Ecol Model 185:65–75
Chapter 11
Compost Use in Organic Farming
Eva Erhart and Wilfried Hartl
Abstract Organic farming is a sustainable agricultural system that respects and
relies on natural ecological systems. Its principles exclude the use of synthetic
pesticides and fertilizers. Instead it is based on management practices that sustain
soil quality and health. Composting of organic residues and the use of compost in
agriculture bring back plant nutrients and organic matter to the soil that otherwise
would be lost. Nevertheless, there are some potential risks associated with compost
use, such as the accumulation of heavy metals or organic pollutants, which must
not be neglected.
Some types of organic farms, such as stockless farms or vegetable farms, have
difficulties sustaining soil humus using only organic farming sources. For such
farms, using biowaste compost from separately collected organic household waste
might be a solution, which in addition helps to close nutrient and organic matter
loops of the whole society. Here we compile information on beneficial effects and
potential risks associated with compost use and on crop yields and quality, with
compost under an organic farming perspective.
The most important benefit of using compost is the increase in soil organic matter (SOM). Under temperate climate conditions, 6–7 t ha−1 year−1 (dry wt.) compost
is sufficient to maintain the soil humus level of medium-textured soils; higher rates
increase the soil humus content. Regular compost addition enhances soil fauna and
soil microbial biomass and stimulates enzyme activity, leading to increased mineralization of organic matter and improved resistance against pests and diseases, both
features essential for organic farming. Through the significant increase in the soil’s
content of organic carbon, compost fertilization may make agricultural soil a carbon sink and thus contribute to the mitigation of the greenhouse effect.
Phosphorus and potassium in compost become nearly completely plant-available
within a few years after compost application. The nitrogen-fertilizer value of
compost is lower. In the first years of compost application, N mineralization may
E. Erhart (*) and W. Hartl
Bio Forschung Austria, formerly Ludwig Boltzmann-Institute for Biological Agriculture
and Applied Ecology, Rinnboeckstrasse 15, A-1110 Vienna, Austria
e-mail: e.erhart@bioforschung.at
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_11, © Springer Science+Business Media B.V. 2010
311
312
E. Erhart and W. Hartl
vary from −15% to +15%. Nitrogen recovery in the following years depends on the siteand cultivation-specific mineralization characteristics and will roughly be the same
as that of soil organic matter (SOM).
Soil cation exchange capacity (CEC) increases with compost use, improving nutrient
availability. Moderate rates of compost of 6–7 t ha−1 year−1 dry wt. are sufficient to
substitute regular soil liming. In the available micronutrient status of the soil, only minor
changes are to be expected with high-quality composts. Increasing soil organic matter
exerts a substantial influence on soil structure, improving soil physical characteristics
such as aggregate stability, bulk density, porosity, available water capacity, and infiltration.
Increased available water capacity may protect crops against drought stress.
Plant-disease suppression through compost is well established in container
systems. In field systems, the same processes involving the suppression of pathogens
by a highly active microflora supported by the supply of appropriate organic matter
are likely at work.
When using high-quality composts, such as specified by the EU regulation
2092/91, the risk of heavy metal accumulation in the soil is very low. Nitrogen
mineralization from compost takes place relatively slowly and there are virtually no
reports of uncontrollable N-leaching. Concentrations of persistent organic pollutants
such as polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls
(PCBs), or polychlorinated dibenzodioxins and dibenzofurans (PCDD/F) in highquality composts usually approach the usual soil background values. Also the overall hygiene and hygiene concerning plant diseases and weeds are not a problem if
quality composts produced in a monitored system are used.
Most studies found positive yield effects of biowaste compost. However, the effect
of biowaste compost applied at moderate rates usually takes some years to develop.
It depends on the factors determining nutrient mineralization from soil and compost
and also on crop-related factors such as the nutrient requirements and uptake dynamics
of the respective crop rotation. Crops with longer growth periods can make better use
of compost. Many vegetable crops respond favorably to compost fertilization, often
immediately after the first application. Crop quality is usually not affected by
compost fertilization in cereals and slightly positively influenced in vegetable crops.
Keywords Soil humus • nitrogen • phosphorus • potassium • soil structure • heavy
metals • organic pollutants • yield • crop quality • compost • organic farming • Cd
• Zn • Ni • Pb • Hg • Cu • Cr • PAH • dioxin • CEC • soil pH • soil N • nitrate, P, K
• micronutrients • soil aggregate • soil water • plant disease • maize • wheat • barley
• potato • tomato broccoli • cabbage • cauliflower • cantaloupe • legume • onion
11.1 Introduction
Organic farmers do not use synthetic fertilizers and pesticides but seek to augment
ecological processes that foster plant nutrition and yet conserve soil and water
resources. Maintaining and improving the soil’s quality and fertility are central to
11
Compost Use in Organic Farming
313
organic farming (EU regulation 2092/91). Therefore, practices that add organic
material are routinely a feature of organically farmed soils to sustain soil humus as
the basis of soil’s natural fertility.
One of the principles of organic farming is to close the nutrient cycles in the farm.
However, there is some controversy among organic farmers about whether the principle
of the closed nutrient cycle is to be regarded in a strict sense and external inputs to
the farm are to be minimized or whether nutrient cycles may also include the
consumers of agricultural products and biowaste compost from separately collected
organic household wastes may be returned to an organic farm, thus closing the
larger loops of nutrients and organic matter of the whole society. There are some
types of organic farms, such as stockless farms or vegetable farms, which find it
difficult to sustain the humus content of their soils. In other cases, management
before conversion has left a soil organic-matter content too low to ensure soil functions.
For such farms, and for farms that are unable to remedy some nutrient deficiency
through organic farming sources such as manure or leguminous crops, the use of
high-quality biowaste compost might be a viable alternative.
In organic farming, only the following types of compost are allowed:
–– Compost from organic material derived from organic farms is permitted without
restrictions.
Other composts, such as listed below, may be applied only if adequate nutrition of the crop
being rotated or soil conditioning is not possible by the methods listed in the regulation.
The need for such composts must be recognized by the inspection body.
––
––
––
––
Composts from animal excrements (factory farming origin forbidden)
Composts from mixtures of vegetable matter
Composted bark from wood not chemically treated after felling
Compost from source-separated household waste, produced in a closed and
monitored collection system and not exceeding the following heavy metal limits
(in mg/kg dry matter): Cd 0.7, Cu 70, Ni 25, Pb 45, Zn 200, Hg 0.4, Crtot 70, Cr (VI) 0
(EU regulation 2092/91).
The aim of this study is to compile the information on compost use, which is
documented in scientific publications, under an organic farming perspective.
11.2 Beneficial Effects of Compost Use
11.2.1 Soil Organic Matter
The most important benefit of using compost is the increase in soil organic matter.
Most arable soils contain only 2–4% organic matter by weight, yet very little about
these soils is not significantly influenced by the organic matter in them. Organic
matter provides much of the soil’s capacity to store nutrients and water. It plays
314
E. Erhart and W. Hartl
a critical role in the formation and stabilization of soil structure, which in turn produces good tilth and drainage and resistance to erosion. It cannot only carry and
make available nitrogen, sulfur, and phosphorus but also improve the availability of
nearly all nutrients, whether applied as fertilizer or weathered from minerals. It
promotes the health of the soil ecosystem and stimulates organisms that cycle
carbon and protect plants from disease (Weil and Magdoff 2004).
The concentration of organic matter in soils is primarily related to climate
(temperature and precipitation), to soil texture (clay content) and to soil drainage status.
Crop rotation and management usually play a smaller, but important role (Shepherd
et al. 2002). Organic matter accumulation in soils is maximum when the difference
between annual plant productivity and annual decomposition is highest. In cropped
soils, organic matter accumulation also depends on the balance between what is
exported from the soil and what remains as residues. Low mean annual temperatures tend to slow decomposition much more than productivity. Within limits, more
rainfall tends to increase plant growth more than it does decomposition; therefore,
soil organic matter tends to be positively correlated with annual precipitation. If
environmental factors are similar, finer-textured soils tend to accumulate higher
amounts of organic carbon (Weil and Magdoff 2004).
Nearly all the nitrogen and large proportions of the phosphorus and sulfur
found in soils occur as constituents of soil organic matter. The soil organic matter
serves as both the principal long-term storage medium and as the primary shortterm source of these and other nutrients. The nutrients in soil humus are transformed into plant-available forms by microorganisms. Humus exerts important
physical effects on the soil. It promotes the formation of a stable aggregate structure,
which improves soilwater-holding capacity and aeration. Humus itself also has a
high water-holding capacity. Humic substances buffer the pH of the soil. The dark
color of the uppermost soil layer, which is due to humic substances, promotes
soil warming in spring and thus elongates the growth period. A high humus
content allows also moist soil to be tilled without causing compaction
(Golueke 1975; Schachtschabel et al. 1998; Stevenson 1982; Weil and Magdoff
2004).
Soil organic matter is subject to biochemical decomposition and transformation
and there are different levels of fragmentation, transformation, and biodegradation.
Parts of newly added organic material, which are of greater stability, may persist for
many years in the soil. Some of the functions of soil humus, however, are not due
to the long-term persistance of soil organic matter (SOM), but to its permanent
turnover and short-lived metabolic products. The maintenance of a large and active
soil microflora, for instance, which mineralizes nitrogen and mobilizes other nutrients,
depends on a repeated supply of organic material (Sauerbeck 1992). A relatively
small portion of soil organic matter with a half-life measured in months or a few
years accounts for most of the biological activity in soil and plays a particularly
important role in maintaining soil quality. The active pool of soil organic carbon
provides the fuel that drives the soil food web (Weil and Magdoff 2004). A significant
increase in the soil’s content of organic carbon may make agricultural soil a carbon
sink and thus contribute to the mitigation of the greenhouse effect.
11
Compost Use in Organic Farming
315
The profound effects that organic matter has on almost all soil properties make
soil organic matter management on the farm the basis for sustainable agricultural
production. In general it is assumed that between 1% and 5% of the soil organic
matter, depending on the kind and intensity of soil cultivation, are mineralized
annually in temperate climate agroecosystems. In order to maintain the soil’s
humus level and to refill the active pool of soil organic carbon, which nourishes the
soil food web, at least the same amounts of organic matter must be added to the soil
every year.
Compost typically has a high organic matter content and organic matter in well-cured
compost is highly humified, its C/N ratio being similar to that of soil humus.
Compost organic matter contents range between 15% and 50% d.m. (dry matter)
and humic acid contents between 15% and 45% o.d.m. (organic d. m.) (Diez and
Krauss 1997; Smidt and Tintner 2007; Zethner et al. 2000). Therefore, well-cured
compost has a very high humus-reproduction value (VDLUFA 2004; Leithold et al.
1997; Kolbe 2007).
11.2.1.1 Humus Content
Numerous experiments show that compost fertilization regularly leads to a distinctive
increase in the humus content of the soil. Such increases were reported from field
trials with 1–28 years duration, with annual compost applications ranging from 6
to 90 t ha−1 and situated on a broad range of sites and soil types.
One year after application of 80 t ha−1 compost made from the organic fraction
of household waste to an infertile Rensic Leptosol near Madrid, Spain, soil organic
carbon was significantly increased (by 9 g kg−1) as compared to the untreated
control (Illera et al. 1999).
In 3-year compost field trials situated near Kassel, Germany, biowaste compost
was applied at rates of 30 and 100 t ha−1 year−1 (wet wt.), respectively, to a sandy
soil and to a loamy silt loess soil. On the sandy soil, soil Corg increased from 14.3
to 14.5 and 16.5 g kg−1, respectively. On the loamy silt loess soil, soil Corg increased
from 11.0 to 13.0 and 17.8 g kg−1, respectively (Stöppler-Zimmer and Petersen
1997).
When 30 t ha−1 (wet wt.) compost from pruning waste and crop residues was
applied to each of five crops during a 3-year experiment on a loam soil with a
vegetable rotation near Seville, Spain, soil total organic carbon increased from 7.8
to 13.5 g kg−1, while in the treatment with mineral fertilization, Corg amounted to 8.5 g
kg−1 (Melero et al. 2007).
Timmermann et al. (2003) conducted six field trials with biowaste compost for
5 and 8 years, respectively, on mostly silty loam soils in Baden-Württemberg,
Germany, under a maize–winter wheat–winter barley rotation.With annual biowaste-compost applications the Corg content of the soil increased by 1.3 g kg−1 Corg
per 5 t ha−1 (dry wt.) of compost applied on average.
Clark et al. (1998) investigated the changes in soil quality during the transition from
conventional to organic farming on silty loam in Sacramento Valley, USA. The organic
316
E. Erhart and W. Hartl
treatment received 4–7 t ha−1 (dry wt.) composted manure every second year and
vetch cover-crop residues every fourth year. After 8 years, soil total carbon content
in the organic treatment had increased significantly from 9.11 to 10.21 g kg−1, while
it remained the same in the conventional treatment.
Biowaste-compost fertilization in organic farming (at average annual rates of 6, 11
and 16 t ha−1 dry wt.) was compared to conventional mineral fertilization and to no
fertilization on a silty loam Fluvisol near Vienna, Austria. The crops grown were mainly
cereals, with potatoes every fourth year. After 10 years, soil organic carbon content had
increased from 19.9 to 20.5–21.7 g kg−1 in the three treatments with increasing rates of biowaste-compost fertilization, while it remained the same with mineral fertilization and
decreased to 18.3 g kg−1 without fertilization (Hartl and Erhart 2005), Fig. 11.1.
Diez and Krauss (1997) recorded increases in soil Corg content from 14.5 to 16.9
g kg−1 on a loamy loess soil and from 19.2 to 22.2 g kg−1 on a gravelly soil, with an
average annual input of 4.4 t ha−1 organic matter (in 14.8 t ha−1 compost dry wt.) in
field experiments of 20 years duration, under the humid climatic conditions of
Bavaria, Germany. The crop rotation of the experiments included sugar beet/potatoes,
winter wheat, and summer barley.
The DOK-experiment in Therwil, Switzerland, compares, among other treatments,
fertilization with composted manure at a rate corresponding to 1.4 livestock units
in biodynamic farming with conventional mineral fertilization on a sandy loam
Luvisol. The crop rotation includes potatoes + green manure, winter wheat + intercrop,
cabbage/beets, winter barley, and 2–3 years grass clover. After 21 years of compost
fertilization, soil organic carbon had increased by 1% in the biodynamic treatment
(using manure compost), while the soils in the organic treatment (with rotted
Fig. 11.1 Soil organic-carbon contents (g kg−1) at 0–30 cm depth in spring 2003 (bars) as compared
to the initial level in spring 1993 (horizontal line: 20 g/kg). Treatments with the same letters are not
significantly different at P £ 0.05 (From Hartl and Erhart 2005. With permission from Wiley-VCH)
11
Compost Use in Organic Farming
317
manure) and in the conventional treatment with manure had lost 9% and 7% of their
Corg, respectively. With mineral fertilization 15% and with no fertilization 22% of
soil Corg were lost (Fliessbach et al. 2007). Although the crop rotation included
plenty of green manuring, intercrops, and grass clover, additional compost fertilization
distinctly increased soil humus content.
No significant increases in soil humus were found in 3 years’ trials with moderate
annual inputs (24 and 30 t ha−1 year−1 wet wt., respectively) on a Cambisol (Ebertseder
et al. 1997) and on sandy podsols and gley soils (Boisch 1997), most probably due to
the low clay content of the soils and the short duration of the experiments.
From these experimental results it may be concluded that in general for mediumtextured soils under temperate climate conditions, around 6–7 t ha−1 year−1 (dry wt.)
of compost application are usually sufficient for the maintenance of the soil humus
level; higher rates increase the soil humus content.
11.2.1.2 Humus Composition, Soil Microbiology, and Soil Fauna
Besides the effects of compost fertilization on the total humus content of the soil,
there are also effects on the composition of soil organic matter. Humus fractionation
showed that the humin fraction with compost application was approximately 50%
higher than in the other soils of the study (Fliessbach et al. 2000). Microbial
biomass C and N as well as their ratios to the total and light fraction C and N pools
in the soils of the organic systems were higher. This is interpreted as an enhanced
decomposition of the easily available light fraction pool of soil organic matter,
which points to a more efficient utilization of organic matter by a large and diverse
microbial biomass (Fliessbach and Mäder 2000; Mäder et al. 2002). Composts are
very diverse in respect of their feedstocks; they are in different stages of biodegradation and of different biochemical composition, such as their contents of soluble
C, cellulose, and lignin. The type and diversity of plants and organic residues added
to a soil can influence the type and diversity of organisms that make up the soil
community, and vice versa (Weil and Magdoff 2004). Soil microbial populations
are also altered through the addition of the compost microflora (Ros et al. 2006).
Regular addition of organic matter (compost) increases soil microbial biomass
and stimulates enzyme activity (Fliessbach and Mäder 2000; Lalande et al. 1998;
Pascual et al. 1997; Schwaiger and Wieshofer 1996; Serra-Wittling et al. 1995),
leading to increased mineralization of organic matter and improved resistance
against pests and diseases. By providing an additional food source compost fertilization also enhances earthworm abundance and biomass (Kromp et al. 1996;
Mäder et al. 2002; Pfotzer and Schüler 1999).
11.2.1.3 Cation Exchange Capacity
Negatively charged soil particles such as clay minerals and humic substances are
able to adsorb cations. Adsorbed cations are kept in a status in which they cannot
318
E. Erhart and W. Hartl
be leached, but may only enter the soil solution through exchange for other cations.
Only after that they may be leached or taken up by plants. This property enables
soils to hold nutrients in the soil–plant cycle or at least to delay their being lost into
adjacent ecosystems (such as lakes and rivers or groundwater). The total exchangeable
cations are referred to as the cation exchange capacity (CEC). Soil CEC is greatly
influenced by the input of organic matter. The average CEC of organic matter is 2
mmolc g−1, whereas the CEC of clay is around 0.5 mmolc g−1 and that of silt around
0.1 mmolc g−1 (Schachtschabel et al. 1998).
In an experiment with biowaste-compost fertilization at average annual rates of
15–39 t ha−1 (wet wt.), the CEC was closely correlated with the humus content of
the soil and increased linearly with the amount of organic matter added via compost
during 5 years. Compared with the unfertilized control, CEC rose by 3–7% in the
compost treatments. In the treatments receiving mineral fertilizer only, the CEC
was the same as in the unfertilized control. In a second experiment, with compost
application at a total rate of 130 t ha−1 compost in different doses and intervals
during 6 years, CEC increased by 4–10%, in proportion with the increase in humus
content (Hartl and Erhart 2003).
Also Businelli et al. (1996) recorded a significant increase in CEC in a 6-year
experiment on a clayey loam soil near Perugia. The same was reported by Frohne
(1990) after a single application of 240 t ha−1 biowaste compost on a compacted
loess Luvisol.
11.2.2 Soil pH
Biowaste-compost pH is usually around 7.5–7.8 (Timmermann et al. 2003;
Vogtmann et al. 1993a; Zethner et al. 2000). Numerous field experiments show that
compost fertilization increases the soil pH in acidic soils (Alin et al. 1996; Hue
et al. 1994; Timmermann et al. 2003) and slightly acidic soils (Alföldi et al. 1993;
Diez and Krauss 1997; Ebertseder et al. 1997; Stöppler-Zimmer and Petersen 1997;
Timmermann et al. 2003). In neutral to slightly alkaline soils pH is usually
unaffected (Diez and Krauss 1997; Erhart et al. 2002; Timmermann et al. 2003).
In summary, the amount of base-forming cations supplied to the soil with the application of moderate doses of compost (6–7 t ha−1 year−1 dry wt.) is sufficient for the maintenance or a slight increase in pH, and therefore can substitute regular soil liming.
11.2.3 Nitrogen
11.2.3.1 N Mineralization
On average, biowaste compost contains 11.5–16.4 g kg−1 total nitrogen (Timmermann
et al. 2003; Vogtmann et al. 1993a; Zethner et al. 2000), which is present mostly in
11
Compost Use in Organic Farming
319
humus-like organic compounds. More than 90% of total compost N is bound to the
organic N pool (Amlinger et al. 2003a). Between 30% and 62% of the total N of biowaste and yard-waste composts are present in humic acids (Smidt and Tintner 2007).
Therefore, a large portion of the nitrogen present in compost is not readily
available to plants, but it can to a certain degree be mineralized and subsequently
be taken up by the plant, or immobilized, denitrified, and/or leached. N mineralization
from composts is affected by the same factors that affect the N mineralization of
organic N in soils. Compost-related factors include the C and N content of the
compost, the C/N ratio, the biodegradability of compost C and the compost microflora. The biochemical composition, such as contents of soluble C, cellulose, and
lignin, appears to play a crucial role for mineralization (Gagnon and Simard
1999, Mary et al. 1996). For instance, compost organic N derived from vegetal
tissues was much more resistant to mineralization than organic N derived from
animal wastes (Canali et al. 2003). Site-related factors include soil texture, pH, and
climate.
The N-mineralization rate of composts can be determined either in incubation
experiments or in pot or field trials. In the latter, nitrogen uptake by the compostfertilized crop is compared to that of a crop without fertilization or with mineral N
fertilization. In incubation experiments using composts from different feedstocks and
of varying maturity, N-mineralization rates ranging from −30.3% to +14.3% of the
organic N were recorded (Chodak et al. 2001; Gagnon and Simard 1999, Hadas and
Portnoy 1997, Siebert et al. 1998). In general, incubation experiments show that
N-mineralization rates of mature composts are higher than of immature composts.
In pot studies with compost-amended soil, plant N recovery ranged from 2% to 15%
(Hartz and Giannini 1998, Iglesias-Jimenez and Alvarez 1993, Scherer et al. 1996).
In field experiments, mineralization is further influenced by soil-cultivation
measures and plant–soil interactions, and so it is important to know this dynamic
to adjust the time of the compost application. The N uptake of field crops depends
also on the respective crop N requirements and N-uptake dynamics. Therefore,
N mineralization calculated from the results of field trials varied from −14% to
+15% (Brandt and Wildhagen 1999; von Fragstein and Schmidt 1999; Gagnon
et al. 1997; Hartl and Erhart 2005; Nevens and Reheul 2003). High N-mineralization
and N-recovery rates are reported when N-rich, well-biodegradable composts and/
or crops with high nutrient demand and a long growth period are used, while immature
composts and yard-waste composts with low N content usually show low
N-mineralization and N-recovery rates.
Subsequently, the remaining portion of compost N and compost humus is incorporated into soil humus. Therefore, on the longer term, the mineralization rate of
this portion will be the same as that of soil organic matter.
A survey of numerous field experiments showed, that nitrogen recovery in the
first year after compost application was between 2.6% and 10.7% (Amlinger et al.
2003b). Therefore, around 5% of the compost N may be assumed to be plantavailable in the first year. Nitrogen recovery in the following years was dependent
on the site- and cultivation-specific mineralization characteristics and was around
2–3% of the compost N applied (Amlinger et al. 2003b).
320
E. Erhart and W. Hartl
One strategy therefore might be to apply compost to leguminous cover crops.
Legume residues decompose quickly and provide available nitrogen whereas
compost decomposes more slowly and contributes more to organic matter buildup.
Targeting the application of compost to a legume or mixed legume–grass crop
permits the legume to act as an N buffer against the variable or negative N release
from composts (Lynch et al. 2004). Incorporating residues with a range of C/N
ratios can lead to the timely mineralization of available soil N for crop uptake.
Sanchez et al. (2001) found that nitrogen mineralization (of the same added material)
was distinctively higher in a diverse system which had received diverse crop residues
plus composted manure than in a conventional corn plus mineral-fertilizer system. Also
Drinkwater et al. (1998) showed that the application of relatively diverse residues that
differ in terms of biochemical composition can significantly increase soil C while meeting
crop N needs. On the other hand, applying compost to leguminous cover crops might
also buffer excess nitrogen to reduce the risk of N-leaching (Lynch et al. 2004).
Organic sources of N, such as manures, composts, or legume cover crops, can
furnish adequate crop nutrition to full-season crops while maintaining relatively
low levels of available N for most of the growing season. On the other hand, N
mineralization from organic sources might lag behind in the needs of early shortseason crops and might continue in the fall after full-season crops have been
harvested. Therefore, when organic sources of fertility are used, additional available
N might be needed for early-season crops, and catch crops should be used to
prevent excess N-leaching following the growing season (Magdoff and Weil 2004).
Due to the large amounts of organic matter present in compost, significant
increases in soil total nitrogen content are quite common with compost fertilization.
Such increases were reported from numerous field trials on a broad range of sites
and soil types (Alin et al. 1996; Businelli et al. 1996; Cortellini et al. 1996; Diez
and Krauss 1997; Hartl and Erhart 2005).
11.2.3.2 Nitrogen-Leaching
For one, the increased mineralization potential which results from the rise in soil
total nitrogen content is desired and necessary in organic farming in order to feed
the crop plants from the soil resources, but for another, it holds the risk of increased
nitrogen-leaching to the groundwater. Several experiments, conducted under varying soil and climate conditions, showed that compost fertilization usually resulted
in equal or lower nitrate-leaching losses than corresponding mineral fertilization.
With compost fertilization at rates of 43 and 86 t ha−1, respectively, drainage
water nitrate concentrations in the first year were not significantly different from
the unfertilized control, which amounted to 5.2 ppm, while with mineral N fertilization
at 400 kg ha−1, drainage water nitrate concentrations increased to 41.5 ppm. Maize
grain yields with compost were the same as in the control, while they increased
significantly with mineral fertilization. In the second year, when neither compost
nor mineral fertilizer was applied, NO3-leaching losses of the mineral fertilized
treatments were still 300% of those in the compost-only treatments. Wheat yields
in the compost treatments were twice and three times, respectively, as high as in the
11
Compost Use in Organic Farming
321
control. In the mineral fertilizer treatment wheat yields amounted to 170% of those
without mineral fertilizer (Pardini et al. 1993). When five different fertilization
regimes were applied to lysimeters filled with sandy soil, total nitrate-leaching
losses decreased in the order mineral fertilization, fertilization with manure
compost, refuse compost, unfertilized, yard-trimmings compost. Cumulative nitrogen
export through the crops decreased in the same order (Leclerc et al. 1995). Small
lysimeters were fertilized during 6 years with composts of varying origin (Jakobsen
1996). When the residual effect was tested in the seventh year without fertilization,
NO3-leaching losses were higher in the lysimeters with compost owing to the
decomposition of compost in the soil. After a new fertilization, however, NO3leaching losses were smaller in the lysimeters with compost than in those with
mineral fertilization. Dry matter yields of barley in the last experimental year were
50% higher with mineral fertilization than with compost.
Nitrate in groundwater was measured beneath a 3-year field trial with vegetables
on a sandy soil over a shallow groundwater table (Maynard 1993). Nitrate concentrations
in the groundwater were lower in the compost treatments (with annual rates of 56 and
112 t ha−1, sufficient to provide the fertilizer requirements for intensive vegetable
production) than in the control plots, which had received mineral fertilizer. In 3-year
field experiments with biowaste compost on podsolic, gley-podsolic, and Luvisol
soils in Northern Germany, none of the compost treatments (total application 26 and
42 t compost ha−1) resulted in clear increases in soil water nitrate contents (Boisch
et al. 1993). Yields in the compost treatments were not significantly higher than in the
unfertilized control in most years (Boisch 1997). Nitrate concentrations in soil water
in a field experiment with yard-trimmings compost, manure, manure compost, and
mineral fertilization were also similar in all treatments on a Luvisol in Switzerland
and the same was true for the yields (Berner et al. 1995). With biowaste-compost
fertilization at 16 and 23 t ha−1 year−1, respectively, on average of 11 years, nitrogenleaching to the groundwater as determined using ceramic suction cups was not
increased as compared to mineral fertilization at 41 and 56 kg N ha−1 year−1, respectively, in an 11-year crop-rotation experiment on a Molli-gleyic Fluvisol near Vienna,
Austria. Even intensive nitrogen mineralization during a 4-month period of bare
fallow did not cause pronounced differences between the fertilization treatments
(Erhart et al. 2007). The yields did not differ significantly between compost and
mineral-fertilizer treatments in most years (Erhart et al. 2005).
The results of these experiments show that normally compost fertilization does
not pose a risk for groundwater eutrophication. N mineralization from compost
takes place relatively slowly and there are virtually no reports of a sudden, ecologically
problematic rise in soluble N pools and uncontrollable N-leaching.
11.2.4 Phosphorus
Phosphorus concentrations in biowaste composts generally range from 2.7 to 4.0 g
kg−1 (Timmermann et al. 2003; Vogtmann et al. 1993a; Zethner et al. 2000). On the
one hand, composts enrich the soil phosphorus status by their direct contribution,
322
E. Erhart and W. Hartl
as 20–40% of the P in compost is immediately plant-available (Vogtmann et al.
1993a). Organic P in composts from plant materials is readily decomposed to
release ortho-phosphate, which is available to plants (He et al. 2001). But organic
matter does not only provide a source of P from mineralization but also can reduce
the capacity of acid soils and of soils with a pH > 8 to lock up P by fixation. Organic
soil amendments reduce the sorption of P in soils and increase the equilibrium P
concentration in the soil solution (Hue et al. 1994; Weil and Magdoff 2004).
Increased soil contents of available P frequently occur after compost application
(Businelli et al. 1996, Cortellini et al. 1996, Diez and Krauss 1997, Parkinson et al.
1999). With application of 39 t ha−1 year−1 (wet wt.) biowaste compost, plantavailable soil contents of phosphorus were significantly higher than in the unfertilized
control. In the treatments which had received 27 and 15 t ha−1 year−1 the soil contents of plant-available phosphorus were in the same range as with 48 kg P2O5 ha−1
year−1 in mineral superphosphate or triplephosphate fertilizer. Also plant phosphorus
contents showed that the phosphorus supply with compost fertilization was approximately as high as in the mineral fertilizer treatments (Hartl et al. 2003). In the DOK
experiment, soluble fractions of phosphorus were lower in the compost treatment
than in the conventional treatment, but the flux of phosphorus between the matrix
and the soil solution was highest in the system with compost application.
Phosphorus flux through the microbial biomass was faster in compost-treated soils,
and more phosphorus was bound in the microbial biomass (Mäder et al. 2002; Oehl
et al. 2001).
Phosphorus availability is crucial for optimum N fixation by legumes. Greenwaste compost, applied on acid soils (pH 5.4) very low in P, provided sufficient P
for red clover to achieve optimal nitrogen fixation. The effect of green-waste
compost was nearly equivalent to that of triple-superphosphate (Römer et al. 2004).
Most studies found that P in compost became nearly completely plant-available
within three vegetation periods after compost application (Amlinger et al. 2006).
Therefore, it may be concluded that the total P content of composts can be calculated as a substitute for mineral P fertilization.
11.2.5 Potassium
The concentrations of potassium in composts vary from 8.4 to 12.5 g kg−1
(Timmermann et al. 2003; Vogtmann et al. 1993a; Zethner et al. 2000), depending
on different sources of feedstocks. Green-waste compost, for example, often exhibits
elevated K contents. However, the composting process may also have a substantial
influence on K availability. Due to the high water solubility of K, leaching losses
may occur if the compost is exposed to rainfall. Immediate plant availability of K
in composts can be more than 85% of the total K content (Vogtmann et al. 1993a)
and the remainder is easily mineralizable.
Soil contents of available K typically increase with application of composts
made from plant residues (Businelli et al. 1996, Cabrera et al. 1989, Diez and
11
Compost Use in Organic Farming
323
Krauss 1997, Parkinson et al. 1999). For example, application of 27 and 39 t ha−1
year−1 (wet wt.) of biowaste compost for 5 years significantly increased plantavailable soil contents of potassium in a field experiment in Austria, while they
remained the same in the control and increased slightly, not significantly with
mineral fertilization at rates of 74 kg K2O ha−1 year−1. Plant potassium contents
showed that the potassium supply with compost fertilization was approximately as
high as with mineral fertilization (Erhart et al. 2003).
In the DOK experiment, under rather humid conditions, soluble fractions of
potassium were lower with manure-compost fertilization than in the conventional
treatments (Mäder et al. 2002).
Clear increases in plant-available soil potassium contents were found in field
experiments in Baden-Württemberg (Timmermann et al. 2003). Average compost
rates of 10 t ha−1 (dry wt.) year−1 were sufficient to counteract or even overcompensate
the decrease in soil potassium contents caused by plant uptake and leaching.
From these findings it may be concluded that the total K content of composts
can be accounted for in the fertilizer calculation.
11.2.6 Micronutrients
Iron (Fe), Mn, Cu, Zn, B, and Mo are essential elements for crop production and
food quality (Marschner 1995). A long-term diet containing low concentrations of
Fe, Mn, Cu, and Zn has been reported to cause human malnutrition. The availability
of Fe, Cu, and Zn in calcareous soils is generally low, and an external source of
these nutrients is needed for improved crop yield and food quality (He et al.
2001).
Addition of organic matter to soil can either decrease or increase metal availability, solubility, and plant uptake. Insoluble organic matter usually forms insoluble
organometal complexes or sorbs metal ions, making them less available for plant
uptake or leaching. However, many organic amendments have a soluble C component
or produce soluble decomposition products, and the soluble organic matter can
increase metal solubility by forming soluble organometal complexes. Metals are
also released through the biodegradation of organic matter by microorganisms.
The influence of soil organic matter on metal mobility can also be modified by the
solution pH (Weil and Magdoff 2004). Crops, and even cultivars, differ considerably
in their sensitivity to individual trace elements, and within the plant, trace elements
are not uniformly distributed among plant tissues (Adriano 1986).
Incorporating a municipal-waste compost at 48 t ha−1 or a municipal-waste
biosolids co-compost at 24 t ha−1 into a calcareous limestone soil increased
concentrations of soil-extractable metals, but caused no significant changes in
tomato and squash (Cucurbita pepo L.) fruit concentrations of Cu and Zn compared
to an unamended control (Ozores-Hampton et al. 1997).
Leaves of tomato plants grown in soil amended with municipal-waste compost
showed decreased Mn and Cu contents compared to leaves from plants grown in
324
E. Erhart and W. Hartl
unamended soil in a study by Stilwell (1993). These results were attributed to
reduced availability of Mn and Cu in the compost-amended soil due to increases in
pH and organic matter content.
In the DOK experiment in Switzerland, amounts of plant-available Mn, Zn, and
Cu in the sandy loam Luvisol (measured using CaCl2/DTPA extraction) were not
significantly different between the organic and biodynamic treatments receiving
rotted and composted manure, respectively, and the mineral fertilizer treatment and
the unfertilized control after 26 years (Fischer et al. 2005).
In a long-term fertilization trial in Darmstadt, Germany, plant-available Zn
contents (measured using CaCl2/DTPA extraction) of the very sandy soil were significantly higher after 24 years of cattle-manure compost fertilization than with mineral
fertilization, while Mn and Cu contents did not differ between the treatments
(Fischer et al. 2005).
With increasing rates of biowaste compost (5–20 t ha−1 dry wt.) applied to
mostly silty loam soils in Baden-Württemberg, Germany, with a maize–winter
wheat–winter barley rotation for 5 and 8 years, mobile Cu concentrations in soil
(measured using NH4NO3 as extractant) increased slightly and Cu contents of crop
products showed a slightly increasing trend. Mobile Zn concentrations in soil
(in NH4NO3 extract) decreased slightly with increasing compost rates, while Zn
contents of crop products were largely unaffected (Timmermann et al. 2003).
Similar trends were reported from a field experiment in Austria where 9.5–25.5
t ha−1 year−1 (wet wt.) of biowaste compost were applied for 10 years to a calcareous
Molli-gleyic Fluvisol and compared to mineral and no fertilization. Cu and Zn
concentrations measured in soil saturation extract did not differ between the fertilization treatments. Cu concentrations in the potentially bioavailable fraction
(measured in LiCl extract) were higher in the medium and high compost treatments
than in the unfertilized control (Erhart et al. 2008). As total Cu concentrations in
the compost treatments were only slightly, not significantly, increased, this was
attributed to the higher soil organic matter concentrations and microbial activity in
the compost treatments. Plant Cu uptake was higher with compost fertilization than
with no fertilization, even though not in all crops. All Cu concentrations in crops
were in the normal range reported in the literature or below that (Bartl et al. 2002).
Total soil Zn concentrations were increased with high application rates of compost.
In the LiCl extract, Zn was not detectable. Plant-uptake data showed increased Zn
concentrations in compost-fertilized oat grains, while spelt and potatoes did not
differ from the unfertilized control (Bartl et al. 2002). Manganese uptake by plants
was lower with compost fertilization in oats, and about the same in spelt and potatoes.
Molybdenum uptake by plants was increased in compost-fertilized spelt and unaffected in oats and potatoes (Bartl et al. 1999).
When 30 and 60 t ha−1 (wet wt.) of compost made from cotton wastes, sewage
sludge, and olive-mill waste water (whose chemical characteristics and micronutrient
content, however, were similar to those of biowaste compost) were applied to a
calcareous, sandy clay loam textured soil in Spain, the Fe and Mn contents in the
chard (Beta vulgaris) plants grown were higher than in the control which
received mineral fertilizer. Cu and Zn contents in chard were unaffected by treatment.
11
Compost Use in Organic Farming
325
The micronutrient contents of salad and barley, which were grown after chard, were
only slightly affected (Cegarra et al. 1996).
In conclusion, with the use of high-quality compost (EU regulation 2092/91),
only minor changes in the available micronutrient status of the soil are to be
expected. As for crop plants, different species show varying micronutrient-uptake/
exclusion patterns and micronutrients are not distributed uniformly between plant
roots, stem, leaves, and fruits.
11.2.7 Soil Structure
In agronomic terms, a “good” soil structure is one which shows the following attributes:
optimal soil strength and aggregate stability, which offer resistance to structural
degradation (capping/crusting, slaking, and erosion, for example); optimal bulk
density, which aids root development and contributes to other soil physical parameters
such as water and air movement within the soil; optimal water-holding capacity and
rate of water infiltration (Shepherd et al. 2002). Crops yield better in well-structured soils: Körschens et al. (1998) suggest a 5–10% benefit of good structure. Of
course, root restriction may not necessarily penalize crop productivity, but it will do
so if the supply of water and nutrients is inadequate (Shepherd et al. 2002). This is
particularly important in organic farming, where deficits in soil structure may not
be compensated by mineral fertilization.
It is not the optimum soil structure per se, which is decisive, however, but rather
the ability of the soil to withstand structural degradation by the impact of rain,
termed aggregate stability (Sekera and Brunner 1943). Increased aggregate stability
protects the soil from compaction and erosion. Decreased bulk density and higher
porosity improve soil aeration and drainage.
Increasing soil organic matter exerts a substantial influence on soil structure,
particularly if – as in the case of compost application – CaO is supplied to the soil
at the same time (Martins and Kowald 1988), improving soil physical characteristics
like aggregate stability, bulk density, porosity, available water capacity, and infiltration
(Giusquiani et al. 1995, Kahle and Belau 1998, Khalilian et al. 2002). To a remarkable
degree, increased organic matter can counteract the ill effects of too much clay or
too much sand (Weil and Magdoff 2004).
11.2.7.1 Aggregate Stability
As shown by Tisdall and Oades (1982), the water stability of aggregates depends
on organic materials. The organic binding agents have been classified into (a) transient,
mainly polysaccharides; (b) temporary, roots and fungal hyphae; and (c) persistent, resistant aromatic components associated with polyvalent metal cations, and
strongly sorbed polymers. Roots and hyphae stabilize macro-aggregates, defined
as >250 µm in diameter. Consequently, macroaggregation is controlled by soil
326
E. Erhart and W. Hartl
management, as crop rotation, cover crops, mulches, organic fertilization, and tillage
practices influence the growth of plant roots and the oxidation of organic carbon.
The water stability of microaggregates (<250 µm in diameter) depends on the
persistent organic binding agents, organomineral complexes, and humic acids (Chaney
and Swift 1986), and appears to be a characteristic of the soil, independent of
management (Tisdall and Oades 1982).
Increasing the soil organic matter content usually increases aggregate stability.
Within a limited range of soil organic matter contents, the relationship for a given
soil is nearly linear. However, across a wider range of soil organic matter, the relationship between these two variables is likely to be curvilinear, because at very high
levels of soil organic matter, additional organic matter has little further effect on
soil aggregation (Haynes 2000).
Addition of easily degradable organic material such as green manures leads to a
rapid, but short-lived rise in aggregate stability. Addition of compost, in contrast,
causes a slow, but long-standing increase in aggregate stability as its organic matter
mainly consists of humic substances, which constitute relatively stable binding
agents (Haynes and Naidu 1998). Therefore, a combination of green manures and
compost application is optimal, because it combines the advantages of both.
Compost application usually influences aggregate stability immediately after a relatively short time (less than 3 years; (Asche et al. 1994; Kahle and Belau 1998; Steffens
et al. 1996). With continued compost application, the effect continues also on the longer term (Ebertseder 1997; Martins and Kowald 1988, Petersen and Stöppler-Zimmer
1999; Sahin 1989; Siegrist et al. 1998; Timmermann et al. 2003). Soil bulk density
decreases with compost application, although that takes longer than improving aggregate stability (Ebertseder 1997; Lynch et al. 2005; Timmermann et al. 2003).
The maturity of the compost used may impact its effect on aggregate stability.
In an agricultural field experiment on loamy silt loess soil situated near Kassel,
Germany, mature composts, which had been processed for 3 months had a greater
effect on aggregate stability than immature composts, which had been processed for
only 12–25 days (Petersen and Stöppler-Zimmer 1999). Heavy silt and clay soils
benefit most from improved aggregate stability through compost application
(Timmermann et al. 2003).
11.2.7.2 Porosity
Also soil pore volume typically increases with compost application. The proportion
of large, continuous vertical coarse pores (>50 µm) is decisive for soil aeration and
warming, and thus for root growth, and for soil water infiltration. Soil friability is
improved with increasing pore volume of large and medium pores (Wegener and
Moll 1997). In the subsoil, the proportion of large, continuous pores correlates with
earthworm abundance (Poier and Richter 1992).
The increase in pore volume with compost application was found to be due to a
rise in the proportion of coarse pores (Ebertseder 1997; Giusquiani et al. 1995;
Martins and Kowald 1988; Sahin 1989) or in the proportion of medium and coarse
pores, respectively (Steffens et al. 1996). Giusquiani et al. (1995) reported the
11
Compost Use in Organic Farming
327
greater porosity in the compost-treated plots to be due to an increase in the amount
of elongated pores, which are considered most important both in soil–water–plant
relationships and in maintaining good soil structure conditions.
11.2.7.3 Soil Water Availability
The water regime in soils is influenced by soil organic matter in several ways. First,
organic matter increases the soil’s capacity to hold plant-available water, defined as
the difference between the water content at field capacity and that held at the
permanent wilting point. It does so both by direct absorption of water and by
enhancing the formation and stabilization of aggregates containing an abundance of
pores that hold water under moderate tensions (Weil and Magdoff 2004). Hudson
(1994) assessed the effect of the soil organic-matter content on the available water
content of surface soils of three textural groups. Within each group, as organic matter
increased, the volume of water held at field capacity increased at a much greater
rate than that held at the permanent wilting point. As a result, highly significant
positive correlations were found between organic-matter content and available water
capacity. As organic-matter content increased from 0.5% to 3%, the available
water capacity of the soil more than doubled (Hudson 1994).
An increase in soil water-holding capacity was observed in many studies with
compost use, though it appears to take some time to come into effect. Evanylo and
Sherony (2002), for example, did not find an increase in soil water-holding capacity
after 2 years of compost application, and the effect was not very pronounced in
other short-term trials (Avnimelech and Cohen 1993; Kahle and Belau 1998).
In longer compost trials on the contrary, clear increases in water-holding capacity
were reported (Giusquiani et al. 1995) (Fig. 11.2).
Fig. 11.2 Effects of compost addition on the available water in the surface layer; means of four
replications. The linear term of regression (physical parameters : compost rates was significant at
P £ 0.01 (Drawn from data from Giusquiani et al. 1995)
328
E. Erhart and W. Hartl
Changes in the soil water regime may also be documented by measuring the soil
water content, although this is more difficult because soil water content is also influenced
significantly by crop water uptake. Zauner and Stahr (1997) and Lynch et al. (2005)
observed higher soil water contents with compost fertilization, while Gagnon et al.
(1998) found differences only in summer and only on a sandy loam, not on clayey soil.
Increased available water capacity may protect crops against drought stress. In
dryland farming systems, where moisture is normally the most yield-limiting
factor, improving soil moisture retention is an important nonnutrient benefit of
compost application, which may exceed nutrient benefits (Stukenholtz et al. 2002).
11.2.7.4 Soil Water Infiltration
However, as important as the provision of ample water for plant growth is the
capacity of the soil to absorb water as it impacts from rain or irrigation. When,
because of structural properties at the soil surface, the rate of water infiltration into
the soil surface is lower than the rate of rainfall, a portion of the rain is lost as
surface runoff. The effect on the supply of water available for plants growing in that
soil is similar to a significant reduction in rainfall (Weil and Magdoff 2004).
Improved soil structure through compost application increases soil water infiltration (Ebertseder 1997), although this also seems to take some time, as the small
effects reported from short-term experiments show (Evanylo and Sherony 2002).
There is a close connection between soil infiltration and floods. Increased infiltration cannot influence the number of heavy rain events, but arguably their consequences. As agriculture occupies large areas, it may be supposed that even small
changes in soil infiltration rate have significant effects on the number and magnitude
of floods (Schnug and Haneklaus 2002).
11.2.8 Plant-Disease Suppression
There are numerous reports of composts suppressing plant diseases caused by
Pythium, Phytophthora, Rhizoctonia, Fusarium, and Aphanomyces spp. and
Sclerotinia sclerotiorum in growing media (Bruns and Schüler 2002; Erhart and
Burian 1997; Hoitink and Fahy 1986; Hoitink et al. 2001; Lievens et al. 2001).
Today composts are recognized to be as effective as fungicides for the control of
root rots such as Phytophthora and Pythium. In some cases composts have successfully
replaced methyl bromide in the US ornamental plant industry (Hoitink et al. 2001).
Plant protection through composts is of particular importance in cultivation systems
where the use of fungicides is impossible or not allowed, as in organic production
or in production of potted herbs for fresh home consumption (Fuchs 2002; Raviv
et al. 1998).
Disease control with compost is attributed to four factors: competition between
beneficial organisms and the pathogen, antibiosis, parasitism, and induced systemic
11
Compost Use in Organic Farming
329
resistance. Two classes of biological control mechanisms known as “general” and
“specific” suppression have been described for compost-amended substrates
(Hoitink et al. 2001). The “general suppression” phenomen is related to the total
amount of microbiological activity in composts and is known to suppress pathogens
such as Pythium and Phytophthora spp. The second type of suppression, elicited by
a specialist group of microorganisms capable of eradicating a certain pathogen,
such as Rhizoctonia solani, is referred to as “specific” suppression.
The most critical factors for plant-disease suppression are the colonialization of
the compost by an appropriate microflora and the decomposition level of the
organic fraction in composts (maturity/stability), which affects biological control
through supporting adequate activity of biocontrol agents (Hoitink and Boehm
1999). As shown by Stone (2002), the same processes involving active organic matter
are likely at work in field systems.
High-rate, single-term amendments of organic matter can generate disease
suppression in the first season after amendment. When composted dairy manure
solids were applied at 28 and 56 t ha−1 (dry wt.), they reduced the severity of
Pythium damping-off of cucumber by 30%, of bean root rot by 29% and of corn
root rot by 67% 2 months after amendment (Darby et al. 2006). Such high amendment
rates, however, cannot be applied year after year for environmental and economic
reasons.
Field studies that assess low-rate single-season organic matter amendments
report highly variable impacts on disease incidence and yield (Lewis et al. 1992;
Lumsden et al. 1983), whereas longer-term studies report more predictable
improvements in yield, quality, and disease suppression (Daamen et al. 1989;
Workneh et al. 1993).
11.3 Potential Risks Associated with Compost Use
11.3.1 Heavy Metals
The accumulation of heavy metals in soils and crop plants is the most often cited
potential risk of compost application. Heavy metal contents in composts vary
widely dependent on compost feedstocks. For organic household and yard wastes,
source separation, as introduced in Europe, proved to be effective in largely reducing
compost heavy metal contents.
In organic farming, there are strict heavy metal limits for biowaste composts to
be used. Composts from source-separated household waste must be produced in a
closed and monitored collection system and must not exceed the following heavy
metal limits (in mg/kg dry matter): Cd 0.7, Cu 70, Ni 25, Pb 45, Zn 200, Hg 0.4,
Crtot 70, Cr (VI) 0 (EU regulation 2092/91).
Key interactive processes in the soil system affecting the partitioning of trace metals between the aqueous, bioavailable, and the solid phase include precipitation, ion
exchange, adsorption onto organic matter, oxides and allophanes, and absorption into
330
E. Erhart and W. Hartl
biological material. The major factors driving the biogeochemical processes in soils
are pH, cation exchange capacity. and redox potential. Soil microorganisms interact
with trace metals in various ways which may render them more or less bioavailable.
Crops differ considerably not only in their general sensitivity to trace elements, but
also in their relative sensitivity to individual trace elements. The uptake of trace elements may vary considerably among cultivars; and within the plant, trace elements
are not uniformly distributed among plant tissues (Adriano 1986).
The results of field experiments show that with the use of high-quality biowaste
composts, increases in soil heavy metal concentrations are not measurable in the
shorter term.
In the experiments of Kluge and Mokry (2000), 7–9 t ha−1 (dry wt.), compost
from biowaste and green waste per year were applied for 3 years to six different
agricultural sites. The soil total heavy metal concentrations were unaffected by the
compost fertilization. In the mobile heavy metal concentrations (measured using
NH4NO3 as extractant) even a decrease was reported (Kluge and Mokry 2000).
Strumpf et al. (2004) applied 20 and 50 t ha−1 (dry wt.) biowaste compost of
urban origin in a single dose to an experimental field, where 12 vegetable species
were grown in the following 3 years. Soil total heavy metal concentrations were not
affected by the compost application. No difference was found in the heavy metal
concentrations of the soil solution (extracted by suction cups) between the compost
treatments and the untreated control. Also the heavy metal concentrations in the
vegetables grown in the experiment did not differ between the treatments.
In the experiment of Oehmichen et al. (1994), 4–24 t ha−1 compost was applied
annually to agricultural crop rotations on two experimental sites for 3 years. Soil
heavy metal concentrations at the end of the experiment were not significantly
different from the unfertilized control.
No increases in total soil heavy metal concentrations were measurable after 10
experimental years with total applications of 95, 175, and 255 t biowaste compost (wet
wt.) ha−1, respectively, to a Molli-gleyic Fluvisol cropped with cereals and potatoes,
except for Zn in the treatments with the highest application rate. In the mobile heavy
metal fractions measured in soil saturation extract and LiCl extract, no significant
increases were detected except for Cu in LiCl extract (Erhart et al. 2008). Plant heavy
metal uptake data showed no significant differences in Ni uptake between the fertilization treatments. Pb was not detectable in crops. Cd concentrations in grains of oat
and spelt and potato tubers were significantly lower with compost fertilization than
with no fertilization. In the potatoes which had received mineral fertilizer, significantly
higher Cd concentrations were found, most probably due to the Cd input via superphosphate and triple superphosphate fertilizer (Bartl et al. 2002) (Fig. 11.3). The total
Cd loads imported via phosphorus fertilization appear small, but they are much more
likely available to biota than the Cd bound in the soil (Sager 1997).
It might be concluded, that with the use of high-quality composts, such as specified
by the EU regulation 2092/91, the risk of heavy metal accumulation in the soil is
very low. As compost application usually leads to a rise in soil organic matter and,
with that, improves the sorption capacity of soils, mobile heavy metal fractions in
most cases remain the same or even decrease with compost use.
11
Compost Use in Organic Farming
331
Fig. 11.3 Cd contents (mg kg−1 d.m.) in crops fertilized with biowaste compost at 32 t (wet wt.)
ha−1 year−1 for 7 years, as compared to mineral fertilization (71 kg N, 19 kg P, and 68 kg K ha−1
year−1) and to no fertilization. Treatments with the same letters are not significantly different at P
£ 0.05 (Drawn from data from Bartl et al. 2002)
11.3.2 Organic Compounds
In high-quality biowaste composts, the contents of organic pollutants such as polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), or polychlorinated dibenzodioxins and dibenzofurans (PCDD/F) and other compounds are
low due to the separate collection of the compost feedstock (Brändli et al. 2007a, b;
Timmermann et al. 2003; Zethner et al. 2000). Investigations of pesticide residues in
compost detected few of the target pesticides. The compounds that were found
occurred at low concentrations (Büyüksönmez et al. 2000). The composting process
contributes to the degradation of organic compounds by the heat generated and by
microbiological and biochemical oxidative processes (Amlinger et al. 2006).
The application of compost to the soil may have varying effects concerning
organic pollutants. Due to their high organic-matter content, composts may bind
pollutants and thus lower their availability and toxicity. The increased activity of
the soil microflora provides improved conditions for biological (oxidative) degradation of pollutants (Amlinger et al. 2006).
Accumulation scenarios of persistent pollutants (PAHs, PCBs, PCDD/F) show
that, assuming realistic half-lives in soil, the average input through deposition and
compost will not lead to an accumulation in soil (except a slight increase in PAHs
in the case of very low soil background values). The input is more than offset by
natural degradation (Amlinger et al. 2004). The absence of changes in the soil
concentrations of PCBs and PCDD/F was confirmed by measurements in field
experiments in Germany (Timmermann et al. 2003).
The pollutant loads are so small, that even with overly high compost rates no
measurable increase in soil contents may be expected (Amlinger et al. 2006).
332
E. Erhart and W. Hartl
11.3.3 Hygiene, Plant Diseases, Weeds
Most plant pathogens are inactivated during proper aerobic composting. For bacterial
plant pathogens and nematodes, the majority of fungal plant pathogens, and a number
of plant viruses, a compost temperature of 55°C for 21 days is sufficient for ensuring
eradication. For Plasmodiophora brassicae, the causal agent of clubroot of
Brassicas, and Fusarium oxysporum f. sp. lycopersici, the causal agent of tomato
wilt, a compost temperature of at least 65°C for up to 21 days is required for eradication. Several plant viruses, particularly Tobacco Mosaic Virus (TMV) are temperature-tolerant. However, there is evidence that TMV and Tomato Mosaic Virus are
degraded over time in compost, even at temperatures below 50°C (Noble and
Roberts 2003; Termorshuizen et al. 2005).
Timmermann et al. (2003) found in their examination of numerous composts for
the RAL-GZ quality control, that the overall hygiene (e.g., concerning E. coli) and
hygiene concerning plant diseases of biowaste composts was always warranted, if
sufficiently high temperatures (65°C) were attained during at least 7 days in the
composting process. The same was true for viable weed seeds and plant parts in the
composts. As their analyses showed, quality composts were virtually free of viable
weed seeds and plant parts.
In the field experiments in Baden-Württemberg, weed ratings were conducted
routinely (at a total of 42 experiment years) and the occurrence of weeds was found
to be not increased with biowaste-compost use (Timmermann et al. 2003).
11.4 Crop Yields and Quality with Compost Use
11.4.1 Agricultural Crops
The total of all effects of compost use is reflected best in crop yields. The effect of
compost fertilization on crop yields depends on the factors determining nutrient
mineralization from soil and compost, but also on crop-related factors such as the
nutrient requirements and uptake dynamics of the respective crop.
11.4.1.1 Cereals
With cereals, a wide range of yield responses to compost fertilization has been
recorded. Nonsignificant wheat yield increases followed the application of 6.9 t ha−1
(dry wt.) biowaste compost on a parabrown soil in Germany (von Fragstein and
Schmidt 1999). Also in the experiment of Oehmichen et al. (1995), small and only
partly significant yield increases were found. In a trial in Southeast England, however,
with municipal solid-waste compost at 50 and 100 t ha−1 (wet wt.) on a loamy clay
soil, compost-treated plots produced grain yields comparable to those which
11
Compost Use in Organic Farming
333
received 75 or 150 kg ha−1 mineral N fertilizer (Rodrigues et al. 1996). On a Gray
Luvisolic soil with low inherent soil fertility and relatively poor soil structure in
Alberta, Canada, municipal solid-waste compost was applied at rates of 50, 100,
and 200 t ha−1 (wet wt.). Wheat yields were 170% and barley yields were 270% of
the untreated control in the 50 t ha−1 treatment (Zhang et al. 2000).
In the DOK experiment in Switzerland, winter wheat yields with manurecompost fertilization in organic farming reached 90% of the grain harvest of the
conventional system in the third crop rotation period (Mäder et al. 2002).
In a 3-year field experiment on a podsolic soil in Germany, rye yield increased
for 5–12%, when 30 and 60 m3 ha−1 (corresponding to approx. 20 and 40 t ha−1 wet
wt.) yard-trimmings compost were applied annually (Klasink and Steffens 1996).
Oehmichen et al. (1995) reported rye yield increases in the range of 9–15% after
annual application of 6–18 t compost (wet wt.) ha−1 on a Luvisol.
While barley yields were significantly higher than the control with 4.1 t ha−1 (dry
wt.) biowaste compost on a parabrown soil in Germany (von Fragstein and Schmidt
1999), 150 t ha−1 (wet wt.) of garden-waste compost was necessary to give significantly higher barley yields on a sandy loam soil in Britain (Cook et al. 1998).
In five field experiments in Baden-Württemberg, Germany, with a duration of
5–8 years and a maize–winter wheat–winter barley rotation, average yield increases
between 11% and 28% were recorded with biowaste-compost fertilization at 5, 10,
and 20 t ha−1 (dry wt.) as compared to the unfertilized control (Timmermann et al.
2003) (Fig. 11.4).
With application of 9–23 t ha−1 year−1 (wet wt.) biowaste compost, yields of cereals
and potatoes increased for 7–10% compared to the unfertilized control (average of
10 years). On a fertile Fluvisol under relatively dry climatic conditions, the yield
Fig. 11.4 Average yields 1995–2002 of five field experiments with a maize–wheat–barley rotation with biowaste-compost fertilization at 5 t ha−1 year−1 (dry wt.) = C1, 10 t ha−1 year−1 = C2, and
20 t ha−1 year−1 = C3 as compared to no fertilization = C0. Stars indicate statistically significant
differences at P £ 0.01 (Drawn from data from Timmermann et al. 2003)
334
E. Erhart and W. Hartl
response to the compost applications was very low in the beginning and increased
slightly with the duration of the experiment (Erhart et al. 2005).
11.4.1.2 Potatoes
Little influence of compost application (at 43 and 86 t (wet wt.) ha−1, respectively)
on potato tuber production was recorded by Volterrani et al. (1996) on a sandy soil
in Italy. In the experiment of Klasink and Steffens (1996), potato yield increased
for maximally 4%. In the DOK experiment in Switzerland, potato yields with
manure-compost fertilization in organic farming were 40% lower than in the
conventional system mainly due to low potassium supply and the incidence of
Phytophthora infestans (Mäder et al. 2002).
In an experiment of Vogtmann et al. (1993b), 80, 20, and 50 t ha−1 (wet wt.)
biowaste compost had been applied in subsequent years to a silty loam Luvisol. The
potato yield in the compost treatment was significantly higher than in the control,
and comparable to that produced with 200 kg N ha−1 mineral fertilizer.
11.4.1.3 Maize
Maize has a very high N requirement, and also a longer growth period than cereals.
On a shaly silt loam in Pennsylvania, dairy manure leaf compost was applied at 27
t ha−1 (dry wt.) annually for 3 years. In the first year, maize yields were significantly
lower than with mineral fertilization at 146 kg N ha−1, but in the second and third
year they were not significantly different (Reider et al. 2000). Parkinson et al.
(1999) applied green-waste compost at 15, 30, and 50 t ha−1 (wet wt.) on a silty
loam soil in South West England. There was a positive yield response of 1–18% to
the application of compost in each of the 3 years.
In a field experiment at Wye, Britain, manure compost at 25 and 50 t ha−1 was
compared with inorganic N fertilizer at 50 and 100 kg N ha−1 using two forage
maize varieties. While the fresh yield of the late-maturing variety was higher, the
yield of the early maturing variety was only about equivalent to that with inorganic
fertilizer, showing the positive influence of a longer growth period on the N uptake
from compost (De Toledo et al. 1996).
11.4.2 Vegetable Crops
In vegetable production, intensive soil cultivation promotes rapid mineralization of
soil organic matter, which may lead to a gradual loss of soil fertility. Most vegetable
crops need a soil that is rich in organic matter, well-structured, and with a high
water-holding capacity. Therefore many vegetable crops, particularly the highly
nutrient-demanding ones, respond favorably to compost fertilization, often already
11
Compost Use in Organic Farming
335
after the first application. Supplying the total N requirements of vegetables with
compost is possible, as several experiments have shown, but as N mineralization
from compost is often as low as 5–15% of total N, large amounts of compost are
required. In order to achieve high yields, but avoid a buildup of nutrient concentrations
in the soil through excessive compost rates, compost could be combined with either
legumes or organic fertilizers in which N is more readily available.
11.4.2.1 Solanaceous Crops
For the solanaceous crops, tomatoes (Lycopersicon esculentum), peppers (Capsicum
annuum), and eggplant (Solanum melongena), equal to significantly greater yields
with compost compared with mineral fertilizer, were reported. For example, in a
3-year trial on two sites (one with sandy soil, one with loamy soil), in which fertilization with chicken-manure compost at 56 and 112 t ha−1, respectively, was compared to mineral fertilization at 146N-64P-121K (kg ha−1; Maynard 1994), and in
an experiment with sugarcane filtercake compost at 224 t ha−1, compared to mineral fertilizer at up to 153 kg N ha−1 on a fine sand soil (Stoffella and Graetz
1996).
When a processing tomato–proteic pea–rotation on a silty clay soil in southern
Italy was fertilized for 4 years with 7.1 t ha−1 (dry wt.) compost from olive mill residues,
sludge, straw, and orange wastes, tomato yields did not differ significantly from
those in the treatment receiving 100 kg N ha−1 as ammonium nitrate (Rinaldi et al.
2007).
11.4.2.2 Cruciferous Crops
In the cruciferous crops broccoli, cauliflower (Brassica oleracea convar. botrytis
var. italica, and var. botrytis, respectively), kohlrabi (B. oleracea convar. caulorapa
var. gongylodes), and cabbage (B. oleracea convar. capitata), improved crop
responses with compost fertilization compared to fertilizer-only treatments were
recorded, provided crop nutrient demands were satisfied. For example in a study by
Roe and Cornforth (1997), who used dairy manure compost at rates of 22, 45, and
90 t ha−1 plus mineral fertilizer at 112 kg ha−1 N to grow autumn broccoli. Broccoli
yields were up to twice as high as with mineral fertilizer alone. When biowaste
compost was applied at 60 t ha−1 (dry wt.) to kohlrabi, yields were similar to those
with 70 kg ha−1 N as mineral fertilizer (Vogtmann and Fricke 1989).
In the chicken-manure compost experiment by Maynard (1994) described above,
yield of broccoli and cauliflower from the compost plots equaled the fertilized
control at both sites in all 3 years with two exceptions (one higher, one lower). In
another experiment with leaf compost at 56 and 112 t ha−1 plus fertilizer at 0,
73N-32P-61K,and 146N-64P-121K (kg ha−1), respectively, broccoli and cauliflower
did not obtain optimum yields on the reduced fertilizer plots until the second and
third years (Maynard 2000).
336
E. Erhart and W. Hartl
11.4.2.3 Cucurbitaceae
When cantaloupe (Cucumis melo) was grown with manure compost at 22, 45, and
90 t ha−1, respectively, plus 23N-14P (kg ha−1), cantaloupe yields were up to three
times as high as with mineral fertilization only (Roe and Cornforth 1997).
11.4.2.4 Legumes
The response of legumes to compost may differ from that of other crops due to their
ability to fix N, but nevertheless they may profit from nutrients other than N and
from improved soil conditions. Snap bean (Phaseolus vulgaris) seedling emergence
and plant survival were increased by the addition of 2.5 cm of leaf compost as a
mulch over rows after seeding. Pod yields were equal to significantly higher with
compost mulch (Gray and Tawhid, 1995). Baziramakenga and Simard (2001) used
a paper residues/poultry-manure compost at 0, 14, 28, and 42 t ha−1 (dry wt.),
supplemented or not with mineral fertilizer at 0, 60, 120, and 180 kg P2O5-K2O ha−1.
Snap bean yields in the compost treatments increased significantly compared with
the untreated control and were similar to those in the mineral-fertilizer treatments.
11.4.2.5 Onions
In a 3-year trial with four cultivars of onions (Allium cepa) annual applications of
112 t ha−1 leaf compost plus 146N-66P-121K (kg ha−1) were compared to mineral
fertilization only (Maynard and Hill 2000). After 3 years of compost additions,
yields of the three Spanish onion cultivars from the compost plots were significantly greater than from unamended plots. Year-to-year variability in yields in
response to variable rainfall was significantly lower and percentage of colossal and
jumbo-sized onions was greater in compost-amended plots. Repeated compost
additions also reduced the incidence of soft rot disease.
11.4.3 Crop Quality
The crop quality of cereals is usually not affected by compost fertilization (Cook
et al. 1998, Erhart et al. 2005, von Fragstein and Schmidt 1999, Oehmichen et al.
1995). In potatoes and cabbage, lower concentrations of nitrate and free amino
acids with compost than with mineral fertilization were observed (Vogtmann et al.
1993b, Roinila et al. 2003; Erhart et al. 2005). Those lower nitrate concentrations
in vegetables are supposedly due not only to lower soil nitrate levels in the compost
plots, but also to the slow-release nature of compost. In tomatoes, compost fertilization
was reported to yield higher titratable acidity values, higher electrical conductivity
11
Compost Use in Organic Farming
337
(E.C.), and a somewhat superior sensory quality (Madrid et al. 1998, Vogtmann
et al. 1993b).
As a general trend, Vogtmann et al. (1993b) found compost to positively influence
food quality, to improve storage performance of vegetables, and to yield a slightly
better sensory quality.
11.5 Conclusion
Probably the most important benefit of using compost is the increase in soil organic
matter. Numerous experiments show that compost fertilization regularly leads to a
distinctive increase in the humus content of the soil. Moderate levels of compost
application (around 6–7 t ha−1 year−1 dry wt.) are usually sufficient for the maintenance of the soil humus level. Regular compost addition increases soil fauna and
soil microbial biomass and stimulates enzyme activity, leading to increased mineralization of organic matter and improved resistance against pests and diseases, both
features essential for organic farming. Composting permits to recycle leftover
organic matter, which otherwise would be lost. Through the significant increase in
the soil’s content of organic carbon, compost fertilization may make agricultural
soil a carbon sink and thus contribute to the mitigation of the greenhouse effect.
As phosphorus and potassium in compost become nearly completely plantavailable within a few years after compost application, the total P and K content of
composts can be accounted for in the fertilizer calculation. The nitrogen-fertilizer
value of compost is lower. In the first years of compost application, N mineralization
calculated from the results of field trials varied from −14% to +15%. Nitrogen
recovery in the following years depends on the site- and cultivation-specific mineralization characteristics and will be roughly the same as that of soil organic matter.
Moderate rates of compost are sufficient to substitute regular soil liming.
Increasing soil organic matter exerts a substantial influence on soil structure,
improving soil physical characteristics like aggregate stability, bulk density, porosity,
available water capacity, and infiltration. Increased aggregate stability protects the
soil from compaction and erosion. Decreased bulk density and higher porosity
improve soil aeration and drainage. Increased available water capacity may protect
crops against drought stress. These effects gradually improve soil fertility. And they
improve soil qualities such as soil workability, resistance to erosion, water-holding
capacity and soil activity, which are essential for crop production particularly in
organic farming, where deficits in soil structure may not be compensated by
mineral fertilization. On the medium and long term the soil-improving effects of compost application have at least the same, if not a greater importance than its fertilizer
effects.
When using high-quality composts, such as specified by the EU regulation
2092/91, the risk of heavy metal accumulation in the soil is very low. Nitrogen
mineralization from compost takes place relatively slowly and there are virtually no
reports of a sudden, ecologically problematic rise in soluble N pools and uncontrollable
338
E. Erhart and W. Hartl
N-leaching. Therefore, compost fertilization does not pose a risk of groundwater
eutrophication.
Concentrations of persistent organic pollutants (PAHs, PCBs, PCDD/F) in highquality composts usually approach the usual soil background values. Also the
overall hygiene and hygiene concerning plant diseases and weeds is not a problem
if quality composts produced in a monitored system are used.
Most studies found positive yield effects of biowaste compost. However, the
effect of biowaste compost applied at moderate rates usually takes some years to
develop. It depends on the factors determining nutrient mineralization from soil and
compost, but also on crop-related factors such as the nutrient requirements and
uptake dynamics of the respective crop rotation. Crops with longer growth periods
can make better use of compost. Many vegetable crops respond favorably to
compost fertilization, often already after the first application.
Crop quality is usually not affected by compost fertilization in cereals, and
slightly positively influenced in vegetable crops.
References
Adriano DC (1986) Trace elements in the terrestrial environment. Springer, New York
Alföldi T, Mäder P, Oberson A, Spiess E, Niggli U, Besson J-M (1993) DOK-Versuch: vergleichende
Langzeit-Untersuchungen in den drei Anbausystemen biologisch-Dynamisch, Organischbiologisch und Konventionell. III. Boden: Chemische Untersuchungen, 1. und 2. Fruchtfolge
periode. Schweizer Landwirtschaftl. Forschung 32(4):479–507
Alin S, Xueyuan L, Kanamori T, Arao T (1996) Effect of long-term application of compost
on some chemical properties of wheat rhizosphere and non-rhizosphere soils. Pedosphere 6:355–363
Amlinger F, Götz B, Dreher P, Geszti J, Weissteiner C (2003a) Nitrogen in biowaste and yard
waste compost: dynamics of mobilisation and availability – a review. Eur J Soil Biol 39:107–116
Amlinger F, Peyr S, Dreher P (2003b) Kenntnisstand zur Frage des Stickstoffaustrags in KompostDüngungssystemen. Endbericht. Bundesministerium für Land- u. Forstwirtschaft, Umwelt- und
Wasserwirtschaft (Hrsg.)., Wien
Amlinger F, Favoino E, Pollak M, Peyr S, Centemero M, Caima V (2004) Heavy metals and
organic compounds from wastes used as organic fertilisers. Study on behalf of the European
Commission, Directorate-General Environment, ENV.A.2
Amlinger F, Peyr S, Geszti J, Dreher P, Weinfurtner K, Nortcliff S (2006) Evaluierung der nachhaltig positiven Wirkung von Kompost auf die Fruchtbarkeit und Produktivität von Böden.
Literaturstudie. Bundesministerium für Land- u. Forstwirtschaft, Umwelt- und Wasserwirtschaft
(Hrsg.)., Wien
Asche E, Steffens D, Mengel K (1994) Düngewirkung und Bodenstruktureffekte durch den
Einsatz von Bioabfallkompost auf landwirtschaftlichen Kulturflächen. VDLUFA-Schriftreihe
Nr. 38. Kongreßband 1994:321–324
Avnimelech Y, Cohen A (1993) Can we expect a consistent efficiency of municipal waste compost
application? Compost Sci Utiliz 4(2):7–14
Bartl B, Hartl W, Horak O (1999) Auswirkungen langjähriger Biotonnekompostdüngung und
mineralischer NPK-Düngung auf den Spurenelementgehalt von Hafer, Dinkel und Kartoffel.
In: Pfannhauser W., Sima A. (Hrsg.): Tagungsband der 15. Jahrestagung der Gesellschaft für
Spurenelemente und Mineralstoffe. Graz, 1.-2. 10. 1999
Bartl B, Hartl W, Horak O (2002) Long-term application of biowaste compost versus mineral
fertilization: effects on the nutrient and heavy metal contents of soil and plants. J Plant Nutr
Soil Sci 165:161–165
11
Compost Use in Organic Farming
339
Baziramakenga R, Simard R (2001) Effect of deinking paper sludge compost on nutrient uptake
and yields of snap bean and potatoes grown in rotation. Compost Sci Utiliz 9:115–126
Berner A, Scherrer D, Niggli U (1995) Effect of different organic manures and garden waste
compost on the nitrate dynamics in soil, N uptake and yield of winter wheat. Biol Agric Hortic
11:289–300
Boisch A (1997) Auswirkung der Biokompostanwendung auf Boden, Pflanzen und Sickerwasser
an sechs Ackerstandorten in Norddeutschland. Hamburger Bodenkundliche Arbeiten Bd. 36
Boisch A, Rubbert M, Goetz D (1993) Stickstoffhaushalt verschiedener Bodentypen bei der
Anwendung von Biokompost. VDLUFA-Kongreßband 1993. VDLUFA-Schriftenr 37:621–624
Brändli R, Bucheli T, Kupper T, Furrer R, Stahel W, Stadelmann F, Tarradellas J (2007a) Organic
pollutants in compost and digestate. Part 1. Polychlorinated biphenyls, polycyclic aromatic
hydrocarbons and molecular markers. J Environ Monit 9:456–464
Brändli R, Kupper T, Bucheli T, Zennegg M, Huber S, Ortelli D, Müller J, Schaffner C, Iozza S,
Schmid P, Berger U, Edder P, Oehme M, Stadelmann F, Tarradellas J (2007b) Organic pollutants
in compost and digestate. Part 2. Polychlorinated dibenzo-p-dioxins, and –furans, polychlorinated biphenyls, brominated flame retardants, perfluorinated alkyl substances, pesticides, and
other compounds. J Environ Monit 9:465–472
Brandt M, Wildhagen H (1999) Netto-N-Mineralisation nach mehrjähriger ackerbaulicher
Verwertung von Bioabfallkompost und Grünguthäcksel. Mitt Dt Bodenk Gesellsch 91:
743–746
Bruns C, Schüler C (2002) Suppressive effects of composted yard wastes against soil borne plant
diseases in organic horticulture. In: Michel F, Rynk R, Hoitink H (eds) Composting and
compost utilization, Proc. 2002 International Symposium, May 6–8, Columbus, OH
Businelli M, Gigliotti G, Giusquiani P (1996) Trace element fate in soil profile and corn plant after
massive applications of urban waste compost: a six-year study. Agrochimica 40:145–152
Büyüksönmez F, Rynk R, Hess T, Bechinski E (2000) Occurrence, degradation and fate of pesticides
during composting. Part II: Occurrence and fate of pesticides in compost and composting
systems. Compost Sci Utiliz 8:61–81
Cabrera F, Diaz E, Madrid L (1989) Effect of using urban compost as manure on soil contents of
some nutrients and heavy metals. J Sci Food Agric 47:159–169
Canali S, Trinchera A, Intrigliolo F, Pompili L, Nisini L, Mocali S, Alianello A, Torrisi B
(2003) Effect of long term compost utilisation on soil quality of citrus orchards in southern
Italy. In: Pullammanappallil P, McComb A, Diaz L, Bidlingmaier W (eds): ORBIT 2003
Organic Recovery and Biological Treatment, Proceedings of the 4th International Conference
ORBIT Association on Biological Processing. Organics: Advances for a Sustainable Society,
Perth, Australia, Murdoch University, Perth, Australia, 30 April–2 May 2003, pp 505–514
Cegarra J, Paredes C, Roig A, Bernal M, Garcia D (1996) Use of olive mill wastewater compost
for crop production. Int Biodeterior Biodegrad 38:193–203
Chaney K, Swift RS (1986) Studies on aggregate stability. II. The effect of humic substances on
the stability of re-formed soil aggregates. J Soil Sci 37:337–343
Chodak M, Borken W, Ludwig B, Beese F (2001) Effect of temperature on the mineralization of
C and N of fresh and mature compost in sandy material. J Plant Nutr Soil Sci 164:289–294
Clark MS, Horwath WR, Shennan C, Scow KM (1998) Changes in soil chemical properties resulting
from organic and low-input farming practices. Agron J 90:662–671
Cook J, Keeling A, Bloxham P (1998) Effect of green waste compost on yield parameters in spring
barley (Hordeum vulgare) v. Hart. Acta Hortic 469:283–286
Cortellini L, Toderi G, Baldoni G, Nassisi A (1996) Effects on the content of organic matter,
nitrogen, phosphorus and heavy metals in soil and plants after application of compost and
sewage sludge. In: De Bertoldi M, Sequi P, Lemmes B, Papi T (eds) The science of composting.
Blackie Academic & Professional, London, pp 457–467
Daamen R, Wijnands F, van der Vliet G (1989) Epidemics of diseases and pests of winter wheat
at different levels of agrochemical input. J Phytopathol 125:305–319
Darby H, Stone A, Dick R (2006) Compost and manure mediated impacts on soilborne pathogens
and soil quality. Soil Sci Soc Am J 70:347–358
340
E. Erhart and W. Hartl
De Toledo V, Lee H, Watt T, Lopez-Real J (1996) The use of dairy manure compost for maize
production and its effect on soil nutrients, maize maturity and maize nutrition. In: De Bertoldi M,
Sequi P, Lemmes B, Papi T (eds) The science of composting. Blackie Academic & Professional,
London, pp 1126–1129
Diez T, Krauss M (1997) Wirkung langjähriger Kompostdüngung auf Pflanzenertrag und
Bodenfruchtbarkeit. Agribiol Res 50:78–84
Drinkwater L, Wagoner P, Sarrantonio M (1998) Legume-based cropping systems have reduced
carbon and nitrogen losses. Nature 396:262–265
Ebertseder T (1997) Qualitätskriterien und Einsatzstrategien für Komposte aus Bioabfall auf
landwirtschaftlich genutzten Flächen. Dissertation TU München. Shaker Verlag, Aachen
Ebertseder T, Gutser R, Claassen N (1997) Bioabfallkompost – Qualität und Anwendung in der
Landwirtschaft. In: Gronauer A, Claassen N, Ebertseder T, Fischer P, Gutser R, Helm M, Popp
L, Schön H (eds) Bioabfallkompostierung – Verfahren und Verwertung. Bayerisches
Landesamt für Umweltschutz, Schriftenreihe Heft 139, pp 133–256
Erhart E, Burian K (1997) Quality and suppressiveness of Austrian biowaste composts. Compost
Sci Utiliz 5(3):15–24
Erhart E, Feichtinger F, Hartl W (2007) Nitrogen leaching losses under crops fertilized with biowaste compost compared with mineral fertilization. J Plant Nutr Soil Sci 170:608–614
Erhart E, Hartl W, Bartl B (2003) Auswirkungen von Kompostdüngung unter den Bedingungen
des Biologischen Landbaus auf die Kaliumversorgung der Kulturpflanzen und den Kaliumgehalt
des Bodens. In: Freyer B (Hrsg.): Ökologischer Landbau der Zukunft: Beiträge zur 7.
Wissenschaftstagung zum Ökologischen Landbau, 24. - 26. 2. 2003 in Wien. Verlag Univ.
f. Bodenkultur, Wien, pp 509–510
Erhart E, Hartl W, Feichtinger F (2002) Nutrient contents in the soil profile after five years of
compost fertilization versus mineral fertilization. In: Michel F, Rynk R, Hoitink H (eds)
Composting and compost utilization. Proceedings of the 2002 International Symposium,
Columbus, OH, May 6–8
Erhart E, Hartl W, Putz B (2005) Biowaste compost affects yield, nitrogen supply during the
vegetation period and crop quality of agricultural crops. Eur J Agron 23:305–314
Erhart E, Hartl W, Putz B (2008) Total soil heavy metal contents and mobile fractions after
10 years of biowaste compost fertilization. J Plant Nutr Soil Sci 171:378–383
EU Council Regulation No 2092/91 of 24 June 1991 on organic production of agricultural products
and indications referring thereto on agricultural products and foodstuffs. Official Journal L 198,
22. 7. 1991, p. 1 ff
Evanylo G, Sherony C (2002) Agronomic and environmental effects of compost use for sustainable
vegetable production. Composting and compost utilization. In: International symposium,
Columbus, OH, 6–8 May 2002
Fischer M, Raupp J, Mäder P, Dubois D, Römheld V (2005) Micronutrient status in two long-term
trials with fertilisation treatments and different cropping systems. In: Poster presented at the
international conference on organic agriculture‚‘Researching Sustainable Systems’, Adelaide,
Australia, 21–23 Sept 2005
Fliessbach A, Hany R, Rentsch D, Frei R, Eyhorn F (2000) DOC trial: soil organic matter quality
and soil aggregate stability in organic and conventional soils. In: Alföldi T, Lockeretz W,
Niggli U (Hrsg.) Proceedings of the 13th international IFOAM scientific conference. vdf
Hochschulverlag, Zürich, Switzerland
Fliessbach A, Mäder P (2000) Microbial biomass and size-density fractions differ between soils
of organic and conventional agricultural systems. Soil Biol Biochem 32:757–768
Fliessbach A, Oberholzer H-R, Gunst L, Mäder P (2007) Soil organic matter and biological soil
quality indicators after 21 years of organic and conventional farming. Agric Ecosyst Environ
118:273–284
von Fragstein P, Schmidt H (1999) External N sources in an organic stockless crop rotation – useful
or useless additives? In: Olesen J, Eltun R, Gooding M, Jensen E, Köpke U (eds) Designing
and testing of crop rotations for organic farming. Proceedings from an international workshop.
Danish Research Centre for Organic Farming, Denmark, pp 203–212
11
Compost Use in Organic Farming
341
Frohne R (1990) Kompostdüngung als Meliorationsmaßnahme auf verdichteten Böden. In: Dott
W, Fricke K, Oetjen R (eds) Biologische Verfahren der Abfallbehandlung. EF-Verlag für
Energie und Umwelttechnik, Berlin
Fuchs J (2002) Practical use of quality compost for plant health and vitality improvement. In:
Insam H, Riddech N, Klammer S (eds) Microbiology of composting. Springer Berlin, pp 435–444
Gagnon B, Simard R (1999) Nitrogen and phosphorus release from on-farm and industrial composts. Can J Soil Sci 79:481–489
Gagnon B, Simard R, Robitaille R, Goulet M, Rioux R (1997) Effect of composts and inorganic
fertilizers on spring wheat growth and N uptake. Can J Soil Sci 77:487–495
Gagnon B, Simard R, Goulet M, Robitaille R, Rioux R (1998) Soil nitrogen and moisture as
influenced by composts and inorganic fertilizer rate. Can J Soil Sci 78:207–215
Giusquiani P, Pagliai M, Gigliotti G, Businelli D, Benetti A (1995) Urban waste compost: effects
on physical, chemical, and biochemical soil properties. J Environ Qual 24:175–182
Golueke CG (1975) Composting. A study of the process and its principles, 3rd edn. Rodale Press,
Emmaus, PA
Gray E, Tawhid A (1995) Effect of leaf mulch on seedling emergence, plant survival, and production
of bush snap beans. J Sustain Agric 6:15–20
Hadas A, Portnoy R (1997) Rates of decomposition in soil and release of available nitrogen from
cattle manure and municipal waste compost. Compost Sci Utiliz 5(3):48–54
Hartl W, Erhart E (2003) Long term fertilization with compost – effects on humus content and
cation exchange capacity. Ecol Future, Bulgarian J Ecol Sci 2(3–4):38–42
Hartl W, Erhart E (2005) Crop nitrogen recovery and soil nitrogen dynamics in a 10-year field
experiment with biowaste compost. J Plant Nutr Soil Sci 168:781–788
Hartl W, Erhart E, Bartl B, Horak O (2003) Beitrag von Biotonnekompost zur Phosphorversorgung
in viehlosen biologisch wirtschaftenden Betrieben. In: Freyer B (Hrsg.) Ökologischer Landbau
der Zukunft: Beiträge zur 7. Wissenschaftstagung zum Ökologischen Landbau, 24–26 Feb
2003 in Wien. Verlag University of Bodenkultur, Wien, pp 517–518
Hartz T, Giannini C (1998) Duration of composting of yard wastes affects both physical and
chemical characteristics of compost and plant growth. HortScience 33:1192–1196
Haynes RJ (2000) Interactions between soil organic matter status, cropping history, method of
quantification and sample pretreatment and their effects on measured aggregate stability. Biol
Fertil Soils 30:270–275
Haynes R, Naidu R (1998) Influence of lime, fertilizer and manure applications on soil organic
matter content and soil physical conditions: a review. Nutr Cycl Agroecosyst 51:123–137
He Z, Yang X, Kahn B, Stoffella P, Calvert D (2001) Plant nutrition benefits of phosphorus, potassium,
calcium, magnesium, and micronutrients from compost utilization. In: Stoffella PJ, Kahn BA
(eds) Compost utilization in horticultural cropping systems. Lewis Publishers, Boca Raton,
FL, pp 307–320
Hoitink H, Boehm M (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu Rev Phytopathol 37:427–446
Hoitink H, Fahy P (1986) Basis for the control of soilborne plant pathogens with composts. Annu
Rev Phytopathol 24:93–114
Hoitink H, Krause M, Han D (2001) Spectrum and mechanisms of plant disease control with
composts. In: Stoffella PJ, Kahn BA (eds) Compost utilization in horticultural cropping
systems. Lewis Publishers, Boca Raton, FL, pp 263–273
Hudson BD (1994) Soil organic matter and available water capacity. J Soil Water Conserv 49:189–194
Hue N, Ikawa H, Silva J (1994) Increasing plant-available phosphorus in an ultisol with yardwaste compost. Commun Soil Sci Plant Anal 25:3291–3303
Iglesias-Jimenez E, Alvarez C (1993) Apparent availability of nitrogen in composted municipal
refuse. Biol Fertil Soils 16:313–318
Illera V, Walter I, Cuevas G, Cala V (1999) Biosolid and municipal solid waste effects on physical
and chemical properties of a degraded soil. Agrochimica 43:178–186
Jakobsen ST (1996) Leaching of nutrients from pots with and without applied compost. Resour
Conserv Recycl 17:1–11
342
E. Erhart and W. Hartl
Kahle P, Belau L (1998) Modellversuche zur Prüfung der Verwertungsmöglichkeiten von
Bioabfallkompost in der Landwirtschaft. Agribiol Res 51:193–200
Khalilian A, Sullivan M, Mueller J, Shiralipour A, Wolak F, Williamson R, Lippert R (2002)
Effects of surface application of MSW compost on cotton production – soil properties, plant
responses, and nematode management. Compost Sci Utiliz 10:270–279
Klasink A, Steffens G (1996) Grünkomposteinsatz in der Landwirtschaft - Ergebnisse aus einem
Feldversuch. In: Braun C (ed) Sekundärrohstoffe im Stoffkreislauf der Landwirtschaft.
VDLUFA Kongreßband 1996, VDLUFA-Verlag, Darmstadt, pp 385–388
Kluge R, Mokry M (2000) Ist der produktionsbezogene Bodenschutz bei der landbaulichen
Verwertung von Komposten zu gewährleisten? – Ergebnisse eines Forschungsprojektes aus
Baden-Württemberg. Mitt Dt Bodenkundl Gesellsch 93:311–314
Kolbe H (2007) Einfache Methode zur standortangepassten Humusbilanzierung von Ackerland
unterschiedlicher Anbauintensität. In: Zikeli S, Claupein W, Dabbert S, Kaufmann B, Müller T,
Valle Zárate A (Hrsg.) Zwischen Tradition und Globalisierung. Beiträge zur 9. Wissenschaftstagung
Ökologischer Landbau. Universität Hohenheim, 20–23 March 2007. Verlag Dr. Köster, Berlin,
pp 5–8
Körschens M, Weigel A, Schulz E (1998) Turnover of soil organic matter (SOM) and long-term
balances – tools for evaluating sustainable productivity of soils. Pflanzenernähr Bodenk
161:409–424
Kromp B, Pfeiffer L, Meindl P, Hartl W, Walter B (1996) The effects of different fertilizer regimes
on the populations of earthworms and beneficial arthropods found in a wheat field. In: IOBC/
WPRS-Bulletin 19(11) Working group meeting “Integrated control in field vegetable crops”,
6–8 Nov 1995, Giutte, France, pp 184–190
Lalande R, Gagnon B, Simard R (1998) Microbial biomass C and alkaline phosphatase activity in
two compost amended soils. Can J Soil Sci 78:581–587
Leclerc B, Georges P, Cauwel B, Lairon D (1995) A five year study on nitrate leaching under
crops fertilised with mineral and organic fertilisers in lysimeters. In: International workshop
on nitrogen leaching in ecological agriculture. Biol Agric Hortic 11:301–308
Leithold G, Hülsbergen K-J, Michel D, Schönmeier H (1997) Humusbilanzierung – Methoden
und Anwendung als Agrar-Umweltindikator. In: DBU (Deutsche Bundesstiftung Umwelt, ed)
Umweltverträgliche Pflanzenproduktion – Indikatoren, Bilanzierungsansätze und ihre
Einbindung in Ökobilanzen. Fachtagung, 11–12 July 1996, Wittenberg. Zeller Verlag, Osnabrück
Lewis J, Lumsden R, Milner P, Keinath A (1992) Suppression of damping-off of peas and cotton
in the field with composted sewage sludge. Crop Prot 11:260–266
Lievens B, Vaes K, Coosemans J, Ryckeboer J (2001) Systemic resistance induced in cucumber
against Pythium root rot by source separated household waste and yard trimmings composts.
Compost Sci Utiliz 9:221–229
Lumsden R, Lewis J, Millner P (1983) Effect of composted sewage sludge on several soilborne
pathogens and diseases. Phytopathology 73:1543–1548
Lynch D, Voroney R, Warman P (2004) Nitrogen availability from composts for humid region
perennial grass and legume-grass forage production. J Environ Qual 33:1509–1520
Lynch D, Voroney R, Warman P (2005) Soil physical properties and organic matter fractions under
forages receiving composts, manure or fertilizer. Compost Sci Utiliz 13:252–261
Mäder P, Fliessbach A, Dubois D, Gunst L, Fried P, Niggli U (2002) Soil fertility and biodiversity
in organic farming. Science 296:1694–1697
Madrid F, Trasierra M, Lopez R, Murillo J, Cabrera F (1998) Municipal solid waste compost
utilization in greenhouse-cultivated tomato. Acta Hortic 469:297–304
Magdoff F, Weil RR (2004) Soil organic matter management strategies. In: Magdoff F,
Weil RR (eds) Soil organic matter in sustainable agriculture. CRC Press, Boca Raton, FL,
pp 45–65
Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, New York
Martins O, Kowald R (1988) Auswirkung des langjährigen Einsatzes von Müllkompost auf einen
mittelschweren Ackerboden. Z Kulturtech Flurbereinigung 29:234–244
11
Compost Use in Organic Farming
343
Mary B, Recous S, Darwis D, Robin D (1996) Interactions between decomposition of plant residues
and nitrogen cycling in soil. Plant Soil 181:71–82
Maynard A (1993) Nitrate leaching from compost-amended soils. Compost Sci Utiliz 1:65–72
Maynard A (1994) Sustained vegetable production for three years using composted animal
manures. Compost Sci Utiliz 2:88–96
Maynard A (2000) Compost: the process and research, Bulletin 966. The Connecticut Agricultural
Experiment Station, New Haven, CT
Maynard A, Hill D (2000) Cumulative effect of leaf compost on yield and size distribution in
onions. Compost Sci Utiliz 8:12–18
Melero S, Madejon E, Herencia J, Ruiz J (2007) Biochemical properties of two different textured
soils (loam and clay) after the addition of two different composts during conversion to organic
farming. Span J Agric Res 5(4):593–604
Nevens F, Reheul D (2003) The application of vegetable, fruit and garden waste (VFG) compost
in addition to cattle slurry in a silage maize monoculture: nitrogen availability and use. Eur J
Agron 19:189–203
Noble R, Roberts SJ (2003) A review of the literature on eradication of plant pathogens and nematodes during composting, disease suppression and detection of plant pathogens in compost.
The Waste and Resources Action Programme, The Old Academy, Oxon, UK
Oehl F, Oberson A, Probst M, Fliessbach A, Roth HR, Frossard E (2001) Kinetics of microbial
phosphorus uptake in cultivated soils. Biol Fertil Soils 34:31–41
Oehmichen J, Gröblinghoff F-F, Reinders A, Dörendahl A (1994) Mit Bio-Kompost Mineraldünger
einsparen. Dtsch Landtech Z 12(94):32–36
Oehmichen J, Gröblinghoff F, Reinders A, Dörendahl A (1995) Untersuchung über die
Verwendung von Bio-Kompost als Kreislaufdünger im Landbau. Müll Abfall 2(95):74–82
Ozores-Hampton M, Hanlon E, Bryan H, Schaffer B (1997) Cadmium, copper, lead, nickel and
zinc concentrations in tomato and squash grown in MSW compost-amended calcareous soil.
Compost Sci Utiliz 5(4):40–45
Pardini G, Volterrani M, Grossi N (1993) Effects of municipal solid waste compost on soil fertility
and nitrogen balance: lysimetric trials. Agric Med 123:303–310
Parkinson R, Fuller M, Groenhof A (1999) An evaluation of greenwaste compost for the production
of forage maize (Zea mays L.). Compost Sci Utiliz 7:72–80
Pascual J, Garcia C, Hernandez T, Ayuso M (1997) Changes in the microbial activity of an arid
soil amended with urban organic wastes. Biol Fertil Soils 24:429–434
Petersen U, Stöppler-Zimmer H (1999) Orientierende Feldversuche zur Anwendung von
Biokomposten unterschiedlichen Rottegrades. In: UBA (Hrsg., 1999) Stickstoff in Bioabfall- und
Grünschnittkompost – Bewertung von Bindungsdynamik und Düngewert. Runder Tisch
Kompost. Wien, 29–30 Sept 1998. Umweltbundesamt, Wien
Pfotzer GH, Schüler C (1999) Effects of different compost amendments on soil biotic and faunal
feeding activity in an organic farming system. In: Kromp B (ed) Entomological research in
organic agriculture. A. B. Academic, Bicester, UK, pp 1–4
Poier KR, Richter J (1992) Spatial distribution of earthworms and soil properties in an arable loess
soil. Soil Biol Biochem 24:1601–1608
Raviv M, Krasnovsky A, Medina S, Reuveni R, Freiman L, Bar A (1998) Compost as a controlling
agent against Fusarium wilt of sweet basil. Acta Hortic 469:375–381
Reider C, Herdman W, Drinkwater L, Janke R (2000) Yields and nutrient budgets under composts,
raw dairy manure and mineral fertilizer. Compost Sci Utiliz 8:328–339
Rinaldi M, Vonella A, Garofalo P (2007) Organic fertilization in a “tomato-pea” rotation in southern
Italy. In: Niggli U, Leifert C, Alföldi T, Lück L, Willer H (eds) Improving sustainability in
organic and low input food production systems. Proceedings of the 3rd international congress
of the European integrated project quality low input food (QLIF). University of Hohenheim,
Germany, 20–23 March 2007. Research Institute of Organic Agriculture FiBL, CH-Frick
Rodrigues M, Lopez-Real J, Lee H (1996) Use of composted societal organic wastes for sustainable
crop production. In: De Bertoldi M, Sequi P, Lemmes B, Papi T (eds) The science of composting.
Blackie Academic & Professional, London, pp 447–456
344
E. Erhart and W. Hartl
Roe N, Cornforth G (1997) Yield effects and economic comparison of using fresh or composted
dairy manure amendments on double-cropped vegetables. HortScience 32:462
Roinila P, Väisänen J, Granstedt A, Kunttu S (2003) Effects of different organic fertilization practices
and mineral fertilization on potato quality. Biol Agric Hortic 21:165–194
Römer W, Gerke J, Lehne P (2004) Phosphate fertilisation increases nitrogen fixation of legumes.
Ökol Landbau 132(4):37–39
Ros M, Klammer S, Knapp B, Aichberger K, Insam H (2006) Long-term effects of compost
amendment of soil on functional and structural diversity and microbial activity. Soil Use
Manag 22:209–218
Sager M (1997) Possible trace metal load from fertilizers. Die Bodenkultur 48:217–223
Sahin H (1989) Auswirkung des langjährigen Einsatzes von Müllkompost auf den Gehalt an
organischer Substanz, die Regenwurmaktivität, die Bodenatmung sowie die Aggregatstabilität
und die Porengrößenverteilung. Mitt Dt Bodenkundl Ges 59/II:1125–1130
Sanchez J, Willson T, Kizilkaya K, Parker E, Harwood R (2001) Enhancing the mineralizable nitrogen pool through substrate diversity in long term cropping systems. Soil Sci Soc Am
J 65:1442–1447
Sauerbeck D (1992) Funktionen und Bedeutung der organischen Substanzen für die Bodenfrucht
barkeit – ein Überblick. Berichte über Landwirtschaft Sdh. 206. Landwirtschaftsverlag
Münster-Hiltrup
Schachtschabel P, Blume H-P, Brümmer G, Hartge K, Schwertmann U (1998) Lehrbuch der
Bodenkunde. 14. Aufl., Enke Verlag, Stuttgart
Scherer H, Werner W, Neumann A (1996) N-Nachlieferung und N-Immobilisierung von
Komposten mit unterschiedlichem Ausgangsmaterial, Rottegrad und C/N-Verhältnis. Agribiol
Res 49:120–129
Schnug E, Haneklaus S (2002) Landwirtschaftliche Produktionstechnik und Infiltration von
Böden – Beitrag des ökologischen Landbaus zum vorbeugenden Hochwasserschutz.
Landbauforsch Völkenrode 52:197–203
Schwaiger E, Wieshofer I (1996) Auswirkungen von Biotonnenkompost auf bodenmikrobiologische und enzymatische Parameter im biologischen Landbau. Mitt Dt Bodenk Ges 81:229–232
Sekera F, Brunner A (1943) Beiträge zur Methodik der Gareforschung. Bodenk Pflanzenern 29:169–212
Serra-Wittling C, Houot S, Barriuso E (1995) Soil enzymatic response to addition of municipal
solid-waste compost. Biol Fertil Soils 20:226–236
Shepherd M, Harrison R, Webb J (2002) Managing soil organic matter – implications for soil
structure on organic farms. Soil Use Manag 18:284–192
Siebert S, Leifeld J, Kögel-Knabner I (1998) Stickstoffmineralisierung von Bioabfallkomposten
unterschiedlicher Rottegrade nach Anwendung auf landwirtschaftlich genutzte und rekultivierte
Böden. Z Kulturtech Landentwicklung 39:69–74
Siegrist S, Schaub D, Pfiffner L, Mäder P (1998) Does organic agriculture reduce soil erodibility? The
results of a long-term field study on loess in Switzerland. Agric Ecosyst Environ 69:253–264
Smidt E, Tintner J (2007) Application of differential scanning calorimetry (DSC) to evaluate the
quality of compost organic matter. Thermochim Acta 459:87–93
Steffens D, Pape H, Asche E (1996) Einfluß von Bioabfallkompost verschiedener Reifegrade auf
die Bodenfruchtbarkeit. VDLUFA-Kongreßband 1996, VDLUFA-Schriftenr 44:405–408.
VDLUFA-Verlag, Darmstadt
Stevenson FJ (1982) Humus chemistry. Wiley, New York
Stilwell D (1993) Evaluating the suitability of MSW compost as a soil amendment in field grown
tomatoes. Part B: Elemental analysis. Compost Sci Utiliz 1(3):66–72
Stoffella P, Graetz D (1996) Sugarcane filtercake compost influence on tomato emergence, seedling
growth, and yields. In: De Bertoldi M, Sequi P, Lemmes B, Papi T (eds) The science of
composting. Blackie Academic & Professional, London, pp 1351–1356
Stone A (2002) Organic matter-mediated suppression of Pythium, Phytophthora and Aphanomyces
root rots in field soils. In: Michel F, Rynk R, Hoitink H (eds) Composting and compost utilization,
Proceedings of 2002 international symposium, Columbus, OH, 6–8 May 2002
11
Compost Use in Organic Farming
345
Stöppler-Zimmer H, Petersen U (1997) Bewertungskriterien für Qualität und Rottestadium von
Bioabfallkompost unter Berücksichtigung der verschiedenen Anwendungsbereiche. Orientierende
Feldversuche mit Bioabfallkomposten unterschiedlichen Rottegrades. In: Umweltbundesamt
(ed) Neue Techniken zur Kompostierung, Verwertung auf landwirtschaftlichen Flächen. Band
I. Verlag UBA, Berlin
Strumpf T, Pestemer W, Buchhorn R (2004) Nähr- und Schadstoffstatus in Boden und Pflanze
nach Anwendung von Bioabfallkompost aus Ballungsgebieten im Gemüseanbau. Nachrichtenbl
Dtsch Pflanzenschutzd 56:264–268
Stukenholtz P, Koenig R, Hole D, Miller B (2002) Partitioning the nutrient and nonnutrient
contributions of compost to dryland-organic wheat. Compost Sci Utiliz 10:238–243
Termorshuizen A, von Rijn E, Blok W (2005) Phytosanitary risk assessment of composts.
Compost Sci Utiliz 13:108–115
Timmermann F, Kluge R, Bolduan R, Mokry M, Janning S (2003) Nachhaltige Kompostverwertung
– pflanzenbauliche Vorteilswirkungen und mögliche Risiken. In: Gütegemeinschaft Kompost
Region Süd e.V. (Hrsg.) Nachhaltige Kompostverwertung in der Landwirtschaft.
Abschlußbericht. LUFA Augustenberg, Karlsruhe
Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci
33:141–163
VDLUFA (ed) (2004) Standpunkt Humusbilanzierung. Methode zur Beurteilung und Bemessung
der Humusversorgung von Ackerland. VDLUFA Verlag, Bonn
Vogtmann H, Fricke K (1989) Nutrient value and utilization of biogenic compost in plant production.
Agric Ecosyst Environ 27:471–475
Vogtmann H, Fricke K, Turk T (1993a) Quality, physical characteristics, nutrient content, heavy
metals and organic chemicals in biogenic waste compost. Compost Sci Utiliz 1:69–87
Vogtmann H, Matthies K, Kehres B, Meier-Ploeger A (1993b) Enhanced food quality: effects of
composts on the quality of plant foods. Compost Sci Utiliz 1:82–100
Volterrani M, Pardini G, Gaetani M, Grossi N, Miele S (1996) Effects of application of municipal
solid waste compost on horticultural species yield. In: De Bertoldi M, Sequi P, Lemmes B, Papi
T (eds) The science of composting. Blackie Academic & Professional, London, pp 1385–1388
Wegener H-R, Moll W (1997) Beeinflussung des Bodens in physikalischer und chemischer
Hinsicht. Handbuch Müll und Abfall, Lieferung 2/97
Weil RR, Magdoff F (2004) Significance of soil organic matter to soil quality and health. In: Magdoff
F, Weil RR (eds) Soil organic matter in sustainable agriculture. CRC Press, Boca Raton, FL,
pp 1–43
Workneh F., van Bruggen A., Drinkwater L., Shennan C (1993) Variables associated with corky
root and Phytophthora root rot of tomatoes in organic and conventional farms. Phytopathology
83:581–589
Zauner G, Stahr K (1997) Kompost- und Grünguthäckselanwendung in der Landwirtschaft – Erste
Ergebnisse zu bodenphysikalischen und –mikrobiologischen Parametern. Mitt Dt Bodenkundl
Ges 83:391–392
Zethner G, Götz B, Amlinger F (2000) Qualität von Komposten aus der getrennten Sammlung.
UBA Monographien, Bd. 133. Umweltbundesamt, Wien
Zhang M, Heaney D, Solberg E, Heriquez B (2000) The effect of MSW compost on metal uptake
and yield of wheat, barley and canola in less productive farming soils of Alberta. Compost Sci
Utiliz 8:224–235
Chapter 12
Beneficial Microorganisms for Sustainable
Agriculture
Arshad Javaid
Abstract There was a desperate need for food to recover the economy of the 1950s
and 1960s. Farmers all over the world were advised to rely on intensive production
methods and synthetic pesticide inputs to increase the productivity. No doubt, these
chemical-based agricultural practices substantially increased crop yield. However,
indiscriminate use of agrochemicals have contributed significantly to the environmental pollution and adversely affected human and animal health. In addition, the
increasing cost of these agrochemicals has continued to lower the farmer’s net cash
return. The global use of synthetic pesticides at the start of this millennium exceeded
2.5 million tons per year. A growing worldwide concern for these problems has
motivated researchers, administrators, and farmers to seek alternatives to chemicalbased, conventional agriculture. One such product is effective microorganisms (EM)
developed by Japanese scientists. Effective microorganisms are a mixed culture of
beneficial and naturally occurring microorganisms, such as species of photosynthetic
bacteria (Rhodopseudomonas palustris and Rhodobacter sphaeroides), lactobacilli
(Lactobacillus plantarum, L. casei, and Streptococcus lactis), yeasts (Saccharomyces
spp.), and Actinomycetes (Streptomyces spp.). These beneficial microorganisms
improve crop growth and yield by increasing photosynthesis, producing bioactive
substances such as hormones and enzymes, controlling soil diseases, and accelerating
decomposition of lignin materials in the soil. Experiments conducted on various
agricultural crops in different parts of the world have shown good prospects for the
practical application of these beneficial microorganisms in improving crop yield
and soil fertility. Application of beneficial microorganisms generally improves soil
physical and chemical properties and favors the growth and efficiency of symbiotic
microorganisms such as nitrogen fixing rhizobia and arbuscular mycorrhizal (AM)
fungi. Nonetheless experiences of some researchers revealed that the effect of these
microorganisms on crop growth and yield was usually not evident or even negative
in the first test crop. However, this adverse effect can be overcome through repeated
A. Javaid (*)
Institute of Mycology and Plant Pathology, University of the Punjab,
Quaid-e-Azam Campus, Lahore, Pakistan
e-mail: arshadjpk@yahoo.com
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_12, © Springer Science+Business Media B.V. 2010
347
348
A. Javaid
applications of these microorganisms. Research on these microorganisms has shown
that crop yields tend to increase gradually as subsequent crops are grown. Foliar
application of beneficial microorganisms avoids many of the biotic and abiotic
factors and constraints of the soil environment, and thus increases the crop growth
and yield significantly. Application of beneficial microorganisms also reduces seed
bank of weeds in agricultural soils by enhancing the rate of weed seeds germination.
There are reports of management of various fungal and bacterial pathogens as well
as insect pests due to application of beneficial microorganisms. These microorganisms
have shown a great promise in dairy wastewater treatment. They can reduce NH3
concentration in poultry manure up to 70% possibly by transforming NH4+ to NO3−.
Research conducted so far concludes that benefits of beneficial microorganisms can
be best exploited through their repeated applications for few years in combination with
organic amendments and applying them as foliar spray. Integrated use of organic
matter plus beneficial microorganisms with half mineral NPK can yield equivalent
to that of full recommended NPK fertilizers dose. Beneficial microorganisms can
also be used for wastewater treatment, pest and disease management, and to reduce
the abiotic stresses on crop growth and yield.
Keywords Biofertilizer • effective microorganisms • nature farming • sustainable
agriculture
12.1 Introduction
Fertilizers as a source of plant nutrients and pesticides as plant protection measures
are being used to increase the crop production. The global use of synthetic pesticides at the start of this millennium exceeded 2.5 million tons per year (Bhanti and
Taneja 2007). However, imbalance and frequent use of these agrochemicals have
polluted the environment to a great extent. There is a growing concern that food
produced under such farm management may not be safe or of good quality. This has
shifted the scientific approach toward some alternative measures (Shaxson 2006).
In the recent past, some successful efforts have been made to at least partially
substitute agrochemicals with natural substances to minimize the bad effects of the
former (Kannaiyan 2002). One such effort was made by Dr. Teruo Higa, Professor
of Horticulture, University of the Ryukyus, Okinawa, Japan, who conducted
pioneering work in advancing the concept of “Effective Microorganisms” (EM)
(Higa 1991). EM consists of mixed cultures of beneficial and naturally occurring
microorganisms that can be applied as inoculants to increase the microbial diversity
of soils and plants. EM is not a substitute for other management practices. It is,
however, an added dimension for optimizing our best soil and crop management
practices such as crop rotations, use of organic amendments, conservation tillage,
crop residue recycling, and biocontrol of pests. If used properly, these beneficial
microorganisms can significantly enhance the beneficial effects of these practices
(Higa and Wididana 1991).
12
Beneficial Microorganisms for Sustainable Agriculture
349
12.2 Beneficial Microorganism’s Cultures
First solution of beneficial microorganisms contained over 80 microbial species
from 10 genera, isolated in Japan. However, with time the technology was refined
to include predominant populations of lactic acid bacteria and yeast and smaller
numbers of photosynthetic bacteria, actinomycetes, and other types of microorganisms.
All of these are mutually compatible with one another and can coexist in liquid
culture (Higa and Parr 1994). The functions of principle microorganisms in EM are
as follows.
12.2.1 Photosynthetic Bacteria
Photosynthetic bacteria include Rhodopseudomonas palustris and Rhodobacter
sphaeroides. These bacteria are a group of independent, self-supporting microbes.
These are considered the pivot of EM activity and support the activity of other
microorganisms in EM culture. They synthesize useful substances from secretions
of plant roots, organic matter, and harmful gases such as hydrogen sulfide, by using
sunlight and the heat of soil as sources of energy (Kim et al. 2004). The useful
substances produced by these bacteria include amino acids, polysaccharides,
nucleic acids, bioactive substances and sugars, all of which promote plant growth
and development (Higa 2000). The metabolites developed by these microbes are
absorbed directly by plants (Kim and Lee 2000; Ranjith et al. 2007).
12.2.2 Lactic Acid Bacteria
Lactic acid bacteria include Lactobacillus plantarum, L. casei, and Streptococcus
lactis. They produce lactic acid from sugars and other carbohydrates produced by
photosynthetic bacteria and yeasts (Hussain et al. 2002). Lactic acid is a strong
sterilizing compound, suppresses harmful microorganisms such as Fusarium and
enhances decomposition of organic matter (Higa and Kinjo 1991). These bacteria
promote the fermentation and decomposition of materials such as lignin and
cellulose, thereby removing the undesirable effect of undecomposed organic matter
(Gao et al. 2008; Valerio et al. 2008).
12.2.3 Yeasts
Yeasts include Saccharomyces cerevisiae. Yeasts synthesize useful substances
required for plant growth from amino acids and sugars secreted by photosynthetic
bacteria, organic matter, and plant roots (Higa 2000). The bioactive substances such
350
A. Javaid
as hormones and enzymes produced by yeast promote active cell and root division.
The secretions are also useful substrates for other microorganisms in EM culture
viz. lactic acid bacteria and actinomycetes (Hussain et al. 2002).
In the beginning, five formulations of beneficial microorganisms were developed
starting from EM1 to EM5. EM1 had predominantly filamentous fungi that are heat
resistant and hasten the decomposition of organic amendments. It was initially
developed for preparing compost quickly but it is not produced any more. EM2
is used primarily to protect plants from soil-borne pathogens, diseases, and
insects. It contains predominantly the species of genus Streptomyces, which
produces antibiotics that suppress harmful microorganisms. It also contains
smaller numbers of photosynthetic bacteria, yeast, and molds. EM3 is comprised
predominantly of photosynthetic bacteria with smaller numbers of yeast and
actinomycetes. It enhances the growth, yield and quality of crop, and improves
soil physical properties (Anonymous 1995). EM4 consists mainly of the lactobacilli
with smaller number of photosynthetic bacteria, Streptomyces spp. and yeast.
It increases the availability of nutrients to plants by enhancing the decomposition
of organic wastes and residues. It also suppresses the activity of harmful insects
and pathogenic microorganisms (Sajjad et al. 2003). EM5 is prepared by mixing
EM2, EM3, and EM4. It is used to suppress pathogens and to ward off harmful
insects. It is especially used for cultivating fruit trees and vegetables (Anonymous
1995).
EM is often inoculated to organic matter fermented and the mixture is called EM
Bokashi. It can improve the ability of microorganisms to break down organic matter,
thereby providing plant nutrients to make better yield and quality (Xu et al. 2000;
Yan and Xu 2002).
In Pakistan, EM is being produced at Nature Farming Research Center,
Faisalabad and is available in the form of EM-Bioab, EM-Biovet, and
EM-Biocontrol. EM-Bioab is used in agricultural crops along with organic
manures as a substitute of chemical fertilizers. EM-Biovet is used in livestock and
poultry production while EM-Biocontrol is used in crops, vegetables, and orchards
for prevention and remedy of diseases and insect pest attack (Hussain et al.
2002).
12.3 Soil Application of Beneficial Microorganisms
12.3.1 Positive Effects on Plant Growth
Experiments conducted throughout Japan as well as in many other countries have
shown good prospects for the practical application of beneficial microorganisms.
Research has shown that the inoculation of these beneficial microorganisms
cultures to the soil/plant ecosystem can improve soil quality, soil health, and yield
and quality of crops.
12
Beneficial Microorganisms for Sustainable Agriculture
351
12.3.1.1 Cereal Crops
Most of the research work on beneficial microorganisms technology has been
conducted on cereals crops, particularly rice and wheat. Hussain et al. (1999,
2000) conducted a long-term field experiment in Pakistan to determine the agronomic
and economic merits of beneficial microorganisms in a rice–wheat cropping system.
They found that when NPK fertilizers and organic manures were combined with
EM, higher straw and grain yields were obtained as compared to corresponding
treatments without EM application for both the test crops. Beneficial microorganisms
applied in combination with NPK, green manure, and farmyard manure caused
a significant increase in nutrient uptake by the grains and straw of each crop.
The average net profit from rice and wheat production using beneficial microorganisms
was US$ 44.9 and 62.35 ha−1, respectively. Corales et al. (1997) studied the effect
of beneficial microorganisms in transplanted and wet direct seeded rice. Results
showed that the reduced inorganic fertilizers (by 25–50%) in combination with EM
or EM Bokashi gave comparatively better results in increasing yield of rice as
compared to inorganic fertilizers alone. Xu (2000) conducted a study under glass
house to determine the effects of beneficial microorganisms and various organic
amendments on the growth, photosynthesis, and yield of sweet corn, compared with
chemical fertilizers. Beneficial microorganisms applied with organic fertilizers
promoted root growth and activity, and enhanced photosynthetic efficiency and
capacity, which resulted in increased grain yield. This was attributed largely to a
higher level of nutrient availability facilitated by beneficial microorganisms application over time. Similar experiments conducted in many other countries including
China, Japan, Vietnam, Korea, Nepal, and Bangladesh have also revealed increase
in crop growth and yield of rice and/or wheat when beneficial microorganisms
application was carried out in combination with various organic amendments and
different doses of inorganic fertilizers (Lee 1994; Ta and Chanh 1996; Iwaishi
2000; Sherchand 2000; Chowdhury et al. 2002).
12.3.1.2 Vegetable Crops
The demand for organically grown food crops has increased markedly in the recent
years as consumers have become more concerned about pesticide residues in the
human diet. Consequently, organic crop production system is gaining popularity
worldwide. Generally, farmers utilize available crop residues, animal manures and
off-farm vegetative materials as organic amendments to supply plant nutrients and
maintain soil productivity. However, the yields of food crops grown in these
systems are generally low. Use of beneficial microorganisms has been shown to
increase the yield and quality of food crops in organic farming systems. Daly and
Stewart (1999) investigated the effect of beneficial microorganisms on vegetable
crops on organic farms in Canterbury, New Zealand. They found that beneficial
microorganisms plus molasses increased the onion yield by 29%, pea yield by 31%,
and sweet corn cob weights by 23%. Daiss et al. (2008) reported that Swiss chard
352
A. Javaid
(Beta vulgaris L.) treated EM plus EM Bokasi had higher phosphorus and magnesium
contents than control plants. Enhanced nutrient utilization efficiencies of the plants
in beneficial microorganisms-applied treatments have also been reported in capsicum
(Capsicum annuum L.) and cowpea (Vigna unguiculata L.) by Sangakkara et al.
(1998). Sangakkara (1998) suggested that yields of sweet potato (Ipomoea batatas L.)
and bush bean (Phaseolus vulgaris L.) were significantly increased by the application of beneficial microorganisms to traditional organic system in Sri Lanka.
Increase in yield due to beneficial microorganisms application has also been
reported for certain other vegetables, viz. radish, cabbage, and lettuce (Lee 1994;
Naseem 2000).
12.3.1.3 Fruit Crops
Higa (1988) conducted experiments on various horticultural crops and concluded
that beneficial microorganisms can increase the yield and quality of fruits. Similarly,
Paschoal et al. (1998) have reported an increase in the yield of oranges owing to the
application of beneficial microorganisms. Xu et al. (2000) reported that beneficial
microorganisms inoculation to both Bokashi and chicken manure increased photosynthesis and fruit yield of tomato plants. Application of beneficial microorganisms
also increased vitamin C concentration in fruits from all fertilization treatments.
They concluded that both fruit quality and yield could be significantly increased
either by inoculation of beneficial microorganisms to the organic fertilizers or
application directly to the soil. According to Joo and Lee (1991), with beneficial
microorganisms application, yield of citrus increased significantly as compared to
traditional method of farming. Fuel cost index was also declined with beneficial
microorganisms farming system. Wibisono et al. (1996) obtained a significant
effect on plant height, number of shoots, and number of leaves in Citrus medica
when beneficial microorganisms were applied along with rice straw at 2.5 t ha−1.
Tokeshi and Chagas (1997) studied the hormonal effect of beneficial microorganisms on citrus germination. They concluded that beneficial microorganisms have
hormonal action as gibberellic acid. The potential of seedling survival and vigo r
was measured by emergence speed. There was rapid emergence speed with beneficial
microorganisms as compared to control.
12.3.1.4 Other Crops
Application of beneficial microorganisms is also known to enhance crop growth
and yield in certain other crops of economic importance such as cotton, coffee, and
sugarcane. Khaliq et al. (2006) conducted a field experiment to determine the
effects of integrated use of organic and inorganic nutrient sources with and without
beneficial microorganisms on growth and yield of cotton. They observed that
organic material and beneficial microorganisms did not increase the yield and
yield-attributing components significantly but integrated use of both resulted in
a 44% increase over control. Integrated use of organic matter plus beneficial
12
Beneficial Microorganisms for Sustainable Agriculture
353
microorganisms with half mineral NPK yielded equivalent to that of full recommended
NPK fertilizers dose. Economic analysis suggested the use of half mineral NPK
with organic matter and EM saves the mineral N fertilizer by almost 50% compared
to a system with only mineral NPK application. Increased yield in sugarcane due
to beneficial microorganisms application in combination with various organic
materials have been reported. However, the increase in yield over control was not
as much pronounced as in other crops (Punyaprueg et al. 1993; Zacharia 1995).
Chagas et al. (1997) suggested that coffee plant propagation could be substantially
improved by replacing the chemical fertilizers with Bokashi plus EM. Beneficial
microorganisms application in combination with cow dung significantly increased the
germination and physical growth parameters including shoot and root length and
biomass, vigor index, collar diameter, and leaf number of Albizia saman, a mediumto-large-sized tree native to Central America, West Indies, and Guyana and is
widely distributed in the tropical forests of Asia (Khan et al. 2006).
12.3.2 Negative or No Effects on Plant Growth
Majority of the scientists who are engaged in promoting EM technology have no
doubt that plant growth is just as good or better and the quality of plant products is
superior to conventional farming (Daly and Stewart 1999; Hussain et al. 1999;
Yamada and Xu 2000; Iwaishi 2000; Khaliq et al. 2006; Khan et al. 2006). In contrast to that, experience of some workers revealed that the effect of beneficial
microorganisms on crop growth and yield was usually not evident or even negative
particularly in the first test crop. Rashid et al. (1993) noted that beneficial microorganisms applied along with farmyard manure did not improve wheat grain yield
and N uptake in wheat over farmyard manure alone and standard dose of chemical
fertilizers. Similarly, Yousaf et al. (1993) did not find any significant effect on crop
growth in maize when beneficial microorganisms were applied along with different
soil amendments such as farmyard manure, poultry manure, sewage sludge, and
NPK fertilizers. Bajwa et al. (1998a) noted an inhibitory effect of EM application
on plant growth in Brassica campestris L. In another study, Bajwa et al. (1999a)
observed similar effect of beneficial microorganisms application on root and shoot
biomass production in Trifolium alexandrinum L. Priyadi et al. (2005) conducted a
field experiment to elucidate the effect of chicken manure and beneficial microorganisms on the yield of corn and chemical and microbial properties of two types of
acidic wetland soils. The results showed that the interaction between soil types and
chicken manure application affected the corn yield, while beneficial microorganisms
had no effect. Bajwa et al. (1995a) showed that application of beneficial microorganisms in heat-sterilized soil induced a significant positive effect on crop growth
and yield in wheat while adversely affected crop growth in non-sterilized soil, indicating that microorganisms in EM solution had to face a competition with soil
indigenous microflora. However, in a recent study, Javaid et al. (2008) reported
negative or no effects of EM application on yield of wheat both in heat-sterilized
and unsterilized soils.
354
A. Javaid
It has been found that in beneficial microorganisms treated soils, generally crop
yields tend to increase gradually as subsequent crops are grown. Sangakkara and
Higa (1994a) studied the effect of beneficial microorganisms application on growth
and yield of eggplant (Solanum melongena L.), capsicum (Capsicm annum L.), and
tomato (Lycopersicum esculentum L.) for two seasons. During the first season, the
effect of beneficial microorganisms application was insignificant while in the
second season significant effect of these microorganisms for increasing crop
growth and yield was evident. Sangakkara et al. (1998) conducted a 3-year study to
evaluate the efficiency of beneficial microorganisms and organic matter on crop growth
and nutrient uptake in capsicum and cowpea (Vigna unguiculata L.). They reported
that the effect of beneficial microorganisms application was pronounced in the
second and third year as compared to the first one. Similar responses of crop growth
to beneficial microorganisms application have also been reported in wheat (Javaid
et al. 2000a), Phaseolus vulgaris L. (Javaid et al. 2002) and pea (Javaid and Bajwa
2002). According to Kinjo et al. (2000) the lack of consistency in results of the
experiments regarding beneficial microorganisms application may be due to variable cultural conditions employed in previous studies. They tested this hypothesis
by applying beneficial microorganisms and chemical fertilizers in soils with different
cultural practices. One soil was collected from an organic farm and the other from
a conventional farm. They observed useful effects of beneficial microorganisms on
yield of radish in soil collected from organic farm but these effects were not evident
in the soil collected from conventional farm. Imai and Higa (1994) stated that the
observed decline in crop yields can often be attributed to the fact that soils, where
conventional farming is practiced, have become disease-inducing or putrefactive soils from long-term use of pesticides and chemical fertilizers. Consequently,
it takes time to establish a disease-suppressive or zymogenic soil. Until this conversion
process is completed, it is virtually impossible to exceed crop yields that were
obtained with conventional farming methods.
12.3.3 Effect on Soil Properties
Studies have shown that beneficial microorganisms significantly improved certain
physical and chemical properties of the soil. Higa (1989) found that the application
of beneficial microorganisms to soil increased NO3– concentration from 4.5 to 5.1
mg 100 g−1 dry soil. Zhao (1998) noted that application of beneficial microorganisms
significantly increased the available nutrients, organic matter, and total nitrogen and
lowered the C:N ratio in the soil. Paschoal et al. (1998) showed that beneficial
microorganisms application in Citrus agro-ecosystem significantly increased soil organic
matter content, level of some macronutrients including Ca, Mg, and K; soil cation
exchange capacity, and lowered soil base saturation. Park (1993) reported that
application of manure and beneficial microorganisms improved the topsoil by
reducing bulk density and dispersion ratio thus made the soil less compact and
more resistant to erosion. Improvements in soil physical properties like bulk density
12
Beneficial Microorganisms for Sustainable Agriculture
355
and hydraulic conductivity due to beneficial microorganisms application has also
been reported by Hussain et al. (1994). Lee (1994) reported the increased levels of
available P2O5, Ca, and Mg in the soil due to EM solution and EM plus compost
application. Beneficial microorganisms application is known to enhance nodulation
and nitrogen fixation efficacy of soil rhizobia (Rhizobium/Bradyrhizobium) in leguminous crops (Sangakkara and Higa 1994b; Javaid et al. 2000b; Yan and Xu 2002;
Javaid 2006). Similarly, beneficial microorganisms application also stimulated
development and functioning of other soil-borne symbiotic microorganisms such as
arbuscular mycorrhizal fungi and thereby enhance soil fertility and plant nutrient
acquisition (Javaid et al. 1995; Mridha et al. 1997; Bajwa et al. 1999b).
12.4 Foliar Application of Beneficial Microorganisms
Foliar application of beneficial microorganisms avoids many of the biotic and
abiotic factors and constraints of the soil environment. Farmers of Indonesia have
learnt to use beneficial microorganisms on vegetable crops much like a foliar fertilizer,
akin to the foliar application of micronutrients. On-farm tests and demonstrations
have shown that foliar applications of beneficial microorganisms can increase the
growth and yield of vegetable crops in a relatively short time, even though no
organic amendment is added to the soil (Widdiana and Higa (1998). These authors
conducted a field study to determine the effects of foliar-applied beneficial microorganisms on the production of garlic, onion, tomato, and watermelon, compared
with the recommended application of chemical fertilizers. Foliar solutions of
beneficial microorganisms at a concentration of 0.1%, 0.5%, and 1% were applied
at 1- and 2-week intervals. Most vegetable yields were generally higher with foliarapplied beneficial microorganisms compared with the chemical fertilizer control.
The highest yield of garlic was obtained with beneficial microorganisms at
0.1% applied at 1-week intervals, and was 12.5% greater than the fertilized control.
The highest yield of onion and tomato resulted from weekly applications of beneficial
microorganisms at 1%. Yield for these two crops were 11.5% and 19.5% higher
than the fertilized control. However, there was no significant increase in watermelon yield from foliar application of beneficial microorganisms at any dilution
level.
Xiaohou et al. (2001) conducted various studies in China to investigate the effect
of foliar application of beneficial microorganisms on yield and quality of various
crops. He reported that in field trials, sprinkling of 0.1% beneficial microorganisms
solution improved the quality and enhanced yields of tea, cabbage, and sugar corn
by 25%, 14%, and 12.5%, respectively. Yousaf et al. (2000) investigated the effect
of seed treatment and foliar application of beneficial microorganisms on growth
and yield of two varieties of groundnut (Arachis hypogaea L.). They recorded an 18%
and 17% increase in yield in varieties CG-2261 and CGV-86550 due to seed treatment, and 58.1% and 58.3% increase due to combined application of seed treatment
plus foliar application over control, respectively.
356
A. Javaid
The type of soil amendment also affects the performance of foliar applied
beneficial microorganisms. However, the mechanism is not known so far. Javaid
(2006) compared the effect of foliar and soil application of beneficial microorganisms on growth and yield of pea (Pisum sativum L.) in soils amended with NPK
fertilizers, farmyard manure, and green manure. The results showed that soil and
soil plus foliar application of beneficial microorganisms either exhibited insignificant
effect or suppressed the plant growth and yield. However, foliar application alone
significantly enhanced shoot biomass by 70% in NPK treated soil. Similarly, foliar application of beneficial microorganisms significantly increased the number and biomass of
pods by 157% and 266%, and 126% and 145% in NPK fertilizers and green manure
amended soils, respectively.
12.5 Effect of Beneficial Microorganisms on Symbiotic
Microorganisms
12.5.1 N2-Fixing Rhizobia
Legumes are unique among crop plants in that they are capable of contributing a
limiting resource to the agroecosystem by fixing N2. The history of crop husbandry
is replete with examples of yield enhancement of a non-legume crop by legumes
grown either in rotation (Voss and Shrader 1984) or as multicrops (Heichel and
Henjum 1991). Historically, these management practices were the mainstay of
N replacement in cropping systems until the advent of economical commercial N
fertilizers (Heichel and Barnes 1984). Soil bacteria belonging to the family
Rhizobiaceae and falling in the genera Rhizobium, Bradyrhizobium, Sinorhizobium,
Mesorhizobium, Allorhizobium, and Azorhizobium are capable of forming nodules
on leguminous plants (Wei et al. 2008). The species of Azorhizobium form nodules
on the stems of tropical legumes Sesbania and Aeschynomene while species of
other genera form nodules on roots of leguminous plants. While colonizing the
nodules, the bacteria develop into N2-fixing bacteroids providing the host plant with
NH4+ as nitrogen source. In return, the plant supplies the bacteroids with vital
organic compounds. During the establishment of active symbiosis, a well-coordinated
exchange of molecular signaling between the legume host and bacterial partner
occurs leading ultimately to the formation of nodules (Lakshminarayana and
Sharma 1994).
Application of beneficial microorganisms is known to have variable effects on
the development of nodulation and nitrogen fixation in legumes. It caused a significant
reduction in nodule number but increased the size and biomass of nodules in
Trifolium alexandrinum (Bajwa et al. 1999a). In a similar experiment Javaid et al.
(2000c) noted a significant increase in nodulation in Vigna radiata due to beneficial
microorganisms application. Javaid et al. (2002) have reported similar effects of
long-term beneficial microorganisms application and organic manures on nodulation
12
Beneficial Microorganisms for Sustainable Agriculture
357
in Phaseolus vulgaris L. Sangakkara and Higa (1994b) studied the effect of EM on
nodulation parameters of vegetable beans (Phaseolus vulgaris) and mungbean
[Vigna radiata (L.) Wilczek] in soils with low and high population of rhizobia.
Application of beneficial microorganisms significantly increased the most probable
number counts of bacteria in the soils. The greatest change was observed in soil
with low inherent microbial populations. Nodulation and nitrogenase activity,
characteristics of both the legumes, were also significantly enhanced by beneficial
microorganisms application especially when grown in nutrient-depleted soil.
Addition of fertilizer decreased the process of biological nitrogen fixation. However,
this adverse impact was reduced with beneficial microorganisms application.
Application of EM Bokashi significantly increased both the nodule numbers per
plant and fresh weight per nodule in peanut (Yan and Xu 2002). Recently Javaid
(2006) conducted a pot experiment to evaluate the efficacy of foliar and soil application of EM on nodulation in pea in soil amended with NPK fertilizers, farmyard
manure, and Trifolium green manure. Results indicated that at flowering stage,
beneficial microorganisms application depressed the nodulation and maximum
number of nodules were recorded in uninoculated control in all the three soil
amendments. Difference between control and microbial inoculated treatments was
more pronounced in NPK and farmyard manure amendments than in green manure
amendment. At maturity, foliar spray of effective microorganisms significantly
enhanced the number of nodules in NPK fertilizers amendment. A similar but insignificant increase in the number of nodules was also recorded due to foliar spray in
green manure amendment. Soil and soil plus foliar application of effective microorganisms depressed nodulation in all the three soil amendment systems at this
growth stage. Effect of foliar spray and soil application of effective microorganisms
on nodules biomass in different soil amendment systems was generally similar to
that of nodules number. This variation in nodulation could be attributed to various
factors including the soil physical and chemical properties, soil amendment, cropping
and agricultural practices history, soil indigenous rhizobial and other microbes
population, environmental conditions of the area, and concentration of beneficial
microorganisms.
12.5.2 Arbuscular Mycorrhizal Fungi
The fungi that are probably most abundant in agricultural soils are arbuscular mycorrhizal (AM) that account for 5–50% of the biomass of soil (Olsson et al. 1999).
These fungi are multifunctional in ecosystems. Colonization of roots by AM fungi
has been shown to improve growth and productivity of several field crops (Javaid
et al. 1994; Kapoor et al. 2004; Cavagnaro et al. 2006; Chen et al. 2007) by increasing
nutrient element uptake (Al-Karaki 2002; Pasqualini et al. 2007); enhanced tolerance
to various biotic (Khaosaad et al. 2007) and abiotic stress factors (Arriagada et al.
2007); and improving physical, chemical, and biological properties of soil (Rillig
and Mummey 2006).
358
A. Javaid
Few studies, mostly by our research group, have been conducted to assess the
effect of beneficial microorganisms application on mycorrhizal colonization, and
effect of dual inoculation of beneficial microorganisms and mycorrhizae on crop
growth and yield of test species. Variable results were obtained in these interactive
studies. The variation in response of crop growth, yield, and mycorrhizal colonization
to beneficial microorganisms application or co-inoculation of beneficial microorganisms and mycorrhizae was generally associated with the nature of the test
species, soil amendment, and history of beneficial microorganisms application.
Bajwa and Jilani (1994) studied the interaction of beneficial microorganisms and
mycorrhizal fungi in sterilized pot soil and found that beneficial microorganisms
significantly enhanced the mycorrhizal colonization in maize and the combined
inoculation resulted in significantly increased crop growth and yield. Bajwa et al.
(2002) found that beneficial microorganisms application increased maize growth in
both farmyard and green manure amended soils while mycorrhizal colonization
was favored by beneficial microorganisms only in farmyard manure amended soil.
Similarly Bajwa et al. (1995b) assessed the usefulness of dual inoculation of beneficial
microorganisms and two mycorrhizal species viz. Glomus mosseae and G. fasciculatum
in improving growth and yield of tomato. They noted a significantly greater shoot
dry biomass and fruit yield in G. mosseae plus beneficial microorganisms and
G. mosseae plus G. fasciculatum plus beneficial microorganisms as compared to
respective sole mycorrhizal treatments. In another experiment, Bajwa et al. (1995c)
studied the effect of beneficial microorganisms application on crop growth, mycorrhizal colonization, and nutrient uptake in soybean by introducing extra-mycorrhizal
spores. They reported that indigenous mycorrhizal flora of field soil did not respond
positively to beneficial microorganisms application and mycorrhizal infection failed
to develop properly with subsequent adverse effects on host plant growth. However,
beneficial microorganisms significantly supported externally introduced mycorrhizal inoculum and marked influence was observed on crop growth and nutrient
uptake. Javaid et al. (1995) showed that application of beneficial microorganisms
in unsterilized field soil enhanced mycorrhizal colonization in the roots of pea,
resulting in increased growth, yield, nodulation, and nitrogen nutrition in host plant.
Similarly, Bajwa et al. (1998b) observed a significant increase in root and shoot
growth, and shoot P and N content in chickpea due to co-inoculation of beneficial
microorganisms and mycorrhiza. Beneficial microorganisms application also
favored mycorrhizal development in root cortex of host chickpea plants. In another
study, the authors also noted similar effects of beneficial microorganisms and mycorrhizae under allelopathic stress caused by aqueous leaf extract of Syzygium
cumini (L.) Skeels (Bajwa et al. 1999b). Javaid et al. (1999) conducted a field study
to evaluate the effectiveness of beneficial microorganisms application on mycorrhizal colonization and subsequent growth and yield in sunflower, at two growth
stages viz. 40 and 70 days after sowing. In 40-day-old plants, beneficial microorganisms supported mycorrhizal association, which resulted in a parallel increase
in number and biomass of leaves as well as stem length while stem biomass
remained unaffected. However, beneficial microorganisms application failed to
induce any remarkable change in extent of mycorrhizal colonization at 70 days
12
Beneficial Microorganisms for Sustainable Agriculture
359
growth stage. However, the number of arbuscules was enhanced by beneficial
microorganisms application at this growth stage that resulted in a parallel increase
in vegetative growth and yield of the host plant. By contrast, Bajwa et al. (1999a)
while studying the effect of beneficial microorganisms on mycorrhizal colonization,
nodulation, and crop growth in Trifolium alexandrium L., in soils amended with
farmyard manure and green manure, noted that EM significantly enhanced mycorrhizal colonization but exhibited an inhibitory effect on crop growth. Javaid et al.
(2000b) conducted pot experiment in farmyard and green manure amended soils
with two different histories of beneficial microorganisms application using Vigna
mungo as test species. They observed a better response of crop growth, nodulation,
and mycorrhizal colonization to beneficial microorganisms application in soil 1
where beneficial microorganisms application was started 6 months prior than the
soil 2. In a similar experiment, Javaid et al. (2000c) noted a significant increase in
mycorrhizal colonization in Vigna radiata due to beneficial microorganisms application. In another study, Javaid et al. (2000a) assessed the effects of long-term
application of beneficial microorganisms and organic manures on mycorrhizal colonization, crop growth, and yield of wheat in soils with three different histories of
beneficial microorganisms application. Beneficial microorganisms proved more
effective in increasing mycorrhizal colonization and yield in wheat in soil with oldest
history of application of these microorganisms. Similarly, Javaid et al. (2002) have
reported similar effects of long-term application of beneficial microorganisms and
organic manures on crop growth and mycorrhizal colonization in Phaseolus vulgaris
L. Mridha et al. (1997) reported that dual inoculation of arbuscular mycorrhizae
and EM resulted in significant better plant growth in Sesbania rostrata as compared
to either beneficial microorganisms or mycorrhizal inoculation. Furthermore,
beneficial microorganisms application enhanced percentage root colonization and
mycorrhizal spores.
12.6 Pest Management with Beneficial Microorganisms
12.6.1 Weed Management
Weeds compete with crops for nutrients, available moisture, space and sunlight,
which results in yield reduction. Weeds also deteriorate the quality of farm products
and hence reduce the market value. Since weeds are present in all food crop
systems irrespective of the intensity of the crop management (Schroeder et al.
1993), thus their control is vital to achieving high yields. Weeds have traditionally
been controlled by manual and cultural methods. With the development of synthetic
agrochemicals in the 1940s, the reliance on chemicals to obtain weed-free cropping
systems increased. However, the indiscriminate use of these synthetic chemicals
has led to pollution problems in most agricultural systems, and more importantly
the development of herbicide-resistant and problematic weed species (Chhokar
et al. 2008; Doole and Pannell 2008). Modern biological agricultural systems do
360
A. Javaid
not permit the use of synthetic herbicides for weed control because of their potential
to become environmental pollutants and harmful residues in the food chain. There
is a growing interest in nonchemical weed control methods worldwide.
Application of beneficial microorganisms is known to stimulate seed germination
and early growth of food crops (Sangakkara and Higa 1994a) and can create a more
favorable root surface-rhizosphere environment for crop plants that improves plant
growth and protection (Sangakkara 1996). It is likely that these documented beneficial
effects of beneficial microorganisms on crop plants would also be extended to
weeds, and could enhance weed seed germination, early growth and development,
and their level of infestation. Consequently, there is considerable interest in whether
beneficial microorganisms through this process, over time, could reduce soil weed
seed-bank. Maramble and Sangakkara (1998) conducted a study to determine the
effect of beneficial microorganisms on weed population and weed growth grown
with organic amendments during the dry season of 3 consecutive years in Sri
Lanka. The application of organic amendments alone suppressed weed growth,
although the variation among the years was insignificant. Beneficial microorganisms
applied with organic amendments enhanced weed growth during the first year
which then declined significantly during the succeeding years. In a similar study,
Maramble et al. (1996a) investigated the influence of beneficial microorganisms
and organic matter on weed populations of two annual food legumes in consecutive
wet and dry season over 2 years. The lowest weed populations and crop yields were
obtained from plots not receiving beneficial microorganisms or chemical fertilizers.
Application of beneficial microorganisms especially with organic matter having a
low C:N ratio enhanced weed populations in the first year. The impact was more
pronounced in dry than in wet season. In the second year, beneficial microorganisms
increased crop yields and reduced weed populations and biomass significantly. The
authors suggested that long-term studies are required to get more benefits of beneficial
microorganisms as an alternative method for controlling weeds. Maramble et al.
(1996b) reported that application of beneficial microorganisms significantly
increased tuber germination and subsequent growth of purple nutsedge (Cyperus
rotundus L.) plants. However, beneficial microorganisms significantly lowered the
number of tubers and tuber biomass at the time of flowering. The authors suggested
the poor tuber formation in beneficial microorganisms treated nutsedge plants
during the first season would reduce the weed infestation during the following
season.
12.6.2 Control of Fungal Pathogens
Different species of turfgrass are widely used worldwide for golf courses, athletic
fields, and landscaping. Sclerotinia homoeocarpa (Lib.) Korf & Dumont, causal
agent of dollar spot disease is considered the most prevalent turfgrass pathogen in
North America, Central America, Australia, New Zealand, and Europe. Fungicides are
a major input for controlling this disease. To evaluate effective alternative approach,
12
Beneficial Microorganisms for Sustainable Agriculture
361
Kremer et al. (2000) conducted in vitro laboratory bioassays to determine the effects
of beneficial microorganisms on growth and development of S. homoeocarpa. The
results showed that beneficial microorganisms amendment in potato dextrose agar
medium at 1.0% and 4.0% significantly inhibited hyphal growth of S. homoeocarpa.
Following in vitro bioassays, greenhouse study was conducted to investigate the
effect of beneficial microorganisms on disease development by S. homoeocarpa in
turfgrass and turf quality. They found that beneficial microorganisms treated compost
treatment had significantly less disease than the standard golf green substrate.
According to Tokeshi et al. (1998) soils treated beneficial microorganisms were
found to be suppressive to the soil-borne plant pathogen Sclerotinia sclerotiorum.
Similarly Jonglaekha et al. (1995) reported that root rot in strawberry, caused by
Rhizoctonia fragariae, can be considerably controlled either by mixing beneficial
microorganisms compost in the soil or applying beneficial microorganisms solution
for 4–6 times at weekly intervals. Application of beneficial microorganisms also
reduced the incidence of wilt disease of potato (Jonglaekha et al. 1993). Encouraging
results have also been recorded in the management of anthracnose of sweet potato
caused by Colletotrichum gloeosporioides, suppressing populations of soil-borne
phytopathogenic fungus Phytophthora cinnamomi, and control of black sigatoka
disease of bananas caused by Mycospherella fijiensis (Tokeshi and Chagas 1996;
Aryantha and Guest 1997; Elango et al. 1997). Control of fungal pathogens may be
attributed to the activity of lactic acid bacteria in the beneficial microorganisms
mixture that produce lactic acid, a strong sterilizing compound (Higa and Kinjo
1991; Higa 2000).
12.6.3 Control of Bacterial Pathogens
Few studies have been conducted to investigate the effect of beneficial microorganisms
on bacterial diseases. Castro et al. (1996a) conducted an in vitro study and found
that beneficial microorganisms inhibited the growth of Xanthomonas campestris
pv. vesicatoria and Pseudomonas solanacearum. They extended the study to evaluate
the potential of these microorganisms for control of X. campestris pv. vesicatoria
in sweet pepper (Capsicum annum cv. margareth) under field conditions and
obtained promising results in the management of the disease (Castro et al. 1996b).
The suppressive effects of beneficial microorganisms have also been reported
against bacterial leaf blight of rice caused by Xanthomonas oryzae pv. oryzae
(Myint et al. 1996).
12.6.4 Control of Insect Pests
Very little work has been carried out regarding the effectiveness of beneficial
microorganisms against insect pests. Nasiruddin and Karim (1996) conducted a
362
A. Javaid
field trial to test the efficacy of one formulation of beneficial microorganisms (EM5)
in reducing the damages caused by the red pumpkin beetle (Aulacophora foveicollis)
and the melon fly (Bactrocera cucurbitae) in cucurbitaceous vegetable crops. EM5
reduced the beetle infestation by 38% and melon fly infestation by 28.3–35.8%
over the untreated control. Chemical insecticides showed more than 80% reduction
of infestation of the two insect pests. Pickleworm (Diaphania nitidalis) is a serious
pest of cucumber and other vegetables of the Cucurbitaceae family. The conventional control of this pest calls for excessive use of synthetic pesticides which
pollute both product and environment. Wood et al. (1997) reported that incidence
of disease and damage by the pickleworm was significantly reduced by foliar applications of beneficial microorganisms fermented plant extracts in combination with
EM5.
12.7 Role of Beneficial Microorganisms under Abiotic Stresses
Few reports are available in the literature regarding the role of beneficial microorganisms under abiotic stress factors such as allelopathy, acidity, and salinity. Bajwa
et al. (1999a) reported that application of beneficial microorganisms significantly
reduced the adverse impact of aqueous leaf extract of an allelopathic tree Syzygium
cumini (L.) Skeels on plant growth, yield, and shoot nitrogen content of chickpea
(Cicer arietinum L.). The efficacy of beneficial microorganisms was further
enhanced by dual inoculation with arbuscular mycorrhizal fungi.
Pairintra and Pakdee (1994) suggested that beneficial microorganisms treated
compost can be used as an efficient soil amendment in ameliorating a slightly saline
soil. Aluminum toxicity is considered to be the most important growth limiting
factor in many acid soils in Malaysia, especially those having pH levels below 5.0.
Anuar et al. (1997) conducted a field experiment to evaluate the use of beneficial
microorganisms in reducing the aluminum toxicity of an acid soil, its effect on the
yield of sweet potato and selected chemical changes of the soil. The results showed
that exchangeable aluminum was reduced with the application of beneficial microorganisms. Furthermore, these microorganisms increased the yield of sweet potato
and also influenced the chemical characteristics of the acid soil.
12.8 Treatment of Dairy Wastewater with Beneficial
Microorganisms
Wastewater originated from dairy operations may contain certain human pathogens
including Escherichia coli. In addition, excess nutrients present in dairy wastewater
can also pollute surface and ground waters. Beneficial microorganisms and duckweed have shown a great promise in dairy wastewater treatment. According to
12
Beneficial Microorganisms for Sustainable Agriculture
363
Rashid and West (2006) combined application of beneficial microorganisms and
duckweed growth significantly reduced the ammonium nitrogen, total phosphorus,
total suspended solids, and biological oxygen demand after 3 months and is a very
efficient way of dairy wastewater treatment. Li and Ni (2000) reported 42–70%
reduction in NH3 concentration in poultry manure when beneficial microorganisms
were added to both drinking water and feed. The mechanism involved suggests that
as EM is a mixed culture of many species of microorganisms, some of which can
transform NH4+ to NO3−, thereby decreasing the potential for N-fraction.
12.9 Conclusion
Extensive studies carried out in various countries of Asia Pacific Region have
shown that beneficial microorganisms enhance the growth, yield, and quality of
various agricultural and horticultural crops possibly through rapid decomposition
of organic matter, production of biogenic substances, improved soil quality, and
enhanced growth and efficacy of symbiotic. However, the affectivity of beneficial
microorganisms varies with soil type, source and amount of soil nutrients, and test
crop species. The negative or no effects of beneficial microorganisms as reported
by some workers can be overcome through repeated applications of these microorganisms. For the best exploitation of advantages of beneficial microorganisms, they
should be used in combination with organic matter plus half dose of NPK fertilizers.
Furthermore, they should be used as foliar spray as this practice avoids many of the
biotic and abiotic factors and constraints of the soil environment.
Most of the studies with beneficial microorganisms limited to their effects on
crop growth and yield. However, in other areas of agriculture such as management
of pests like weeds and insects, and control of plant pathogens including bacteria
and fungi, only few studies have been undertaken. These few studies, however,
exhibited very encouraging results in the management of pests and diseases with
beneficial microorganisms. Similarly, few studies conducted so far to manage the
environmental problems like treatment of wastewater and poultry manure revealed
that the benefits of beneficial microorganisms can also be exploited in these areas.
However, more intensive and systematic studies are required in these areas to
provide a better understanding of the usefulness of beneficial microorganisms
technology in various farming systems and environmental issues to provide safe
food products to the consumers.
References
Al-Karaki GN (2002) Benefit, cost and phosphorus use efficiency of mycorrhizal field grown
garlic at different soil phosphorus levels. J Plant Nutr 25:1175–1184. doi:10.1081/PLN120004381
364
A. Javaid
Anonymous (1995) EM application manual for APNAN countries. APNAN Asia-Pacific Natural
Agricultural Network
Anuar AR, Shariffudin HAH, Jamal T (1997) Use of EM for production of sweet potato on an acid
soil. In: HAH Shariffudin and UR Sangakkara (eds.). Proceedings of the 5th Conference on
EM, December 8–12, 1996, Sara Buri, Thailand
Arriagada CA, Herrera MA, Ocampo JA (2007) Beneficial effect of saprobe and arbuscular mycorrhizal fungi on growth of Eucalyptus globulus co-cultured with Glycine max in soil contaminated with heavy metals. J Environ Manage 84:93–99. doi:10.1016/j.jenvman.2006.05.005
Aryantha NP, Guest DI (1997) Bokashi EM as a biocontrol agent to suppress the growth of
Phytophthora cinnamomi. In: Sharifuddin HAH, Sangakkara UR (eds) Proceedings of 5th
conference on effective microorganisms, Sara Buri, Thailand, 8–12 Dec 1996
Bailey DJ, Otten W, Gilligan CA (2000) Saprotrophic invasion by the soil-borne fungal plant
pathogen Rhizoctonia solani and percolation thresholds. New Phytol 146L535–544. http://
www.jstor.org/stable/2588935
Bajwa R, Jilani S (1994) Mycorrhizal colonization and subsequent growth response to co-inoculation with VA mycorrhiza and EM in maize. In: Proceeding of 2nd national seminar on nature
farming, University of Agriculture, Faisalabad, pp 11–18, 18 Sept 1994
Bajwa R, Javaid A, Tasneem Z (1995a) Response of indigenous soil microflora to EM (effective
microorganisms) inoculation in Pakistan. Biota 1:73–79
Bajwa R, Tasneem Z, Javaid A. (1995b) EM and VAM technology in Pakistan. I. Effect of coinoculation of VA mycorrhizal fungi and EM4 on growth and yield in tomato (Lycopersicon
esculentum Miler). Biota 1:123–129
Bajwa R, Akhtar T, Javaid A (1995c) EM and VAM technology in Pakistan. II. Effect of coinoculation of EM and VAM on plant growth, uptake of nitrogen and phosphorus and VA
mycorrhizal colonization in soybean. Acta Sci 5:13–24
Bajwa R, Javaid A, Uzma M (1998a) Effects of organic amendments and effective microorganisms (EM) on growth of Brassica campestris L. Acta Sci 8:141–144
Bajwa R, Javaid A, Haneef B (1998b) EM and VAM technology in Pakistan. Effect of co-inoculation
of effective microorganisms(EM) and VA mycorrhiza on plant growth and nutrient uptake in
chickpea (Cicer arietinum L). Pak J Phytopathol 10:48–52
Bajwa R, Javaid A, Rabbani N (1999a) EM and VAM technology in Pakistan. VII: Effect of
organic amendments and effective microorganisms (EM) on VA mycorrhiza, nodulation and
crop growth in Trifolium alexandrinum L. Pak J Biol Sci 2:590–593
Bajwa R, Javaid A, Haneef B (1999b) EM and VAM Technology in Pakistan V: Response of
chickpea (Cicer arietinum L.) to co-inoculation of effective microorganisms (EM) and VA
mycorrhiza under allelopathic stress. Pak J Bot 31:387–396
Bajwa R, Javaid A, Javaid A (2002) Effect of soil sterilization, organic amendments and EM
Application on growth, yield and VA mycorrhizal colonization in maize. Pak J Phytopathol
14:62–67
Bhanti M, Taneja A (2007) Contamination of vegetables of different seasons with organophosphorous pesticides and related health risk assessment in northern India. Chemosphere 69:63–68.
doi:10.1016/j.chemosphere.2007.04.071
Castro CM, Motta SD, Akiba F, Ribeiro RLD (1996a) Potential use of EM for control of phytopathogenic fungi and bacteria. In: Parr JF, Homick SB, Simpson ME (eds) Proceedings of the
3rd international conference on Kyusei nature farming, USDA, Santa Barbara, CA, pp 236–
238, 5–7 Oct 1993
Castro CM, Motta SD, Pereira DS, Akiba F, Ribeiro RLD (1996b) Effective microorganisms for
control of Xanthomonas campestris pv. vesicatoria in sweet pepper. In: Parr JF, Homick SB,
Simpson ME (eds). Proceedings of the third international conference on Kyusei nature farming,
USDA, Santa Barbara, CA, pp 239–241, 5–7 Oct 1993
Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular
mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic
tomato production. Plant Soil 282:209–225. doi:10.1007/s11104-005-5847-7
12
Beneficial Microorganisms for Sustainable Agriculture
365
Chagas PRR, Tokeshi H, Zonatti NH (1997) Production of plants of Coffee conephora cv.
Conilion with conventional fertilizers and bokashi plus effective microorganisms. In:
Senanayake YDA, Sangakkara UR (eds) 5th International Conference on Kyusei Nature
Farming, Bangkok, Thailand, pp 133–150, 23–26 Oct 1997
Chen B, Xiao X, Zhu Y, Smith FA, Xie ZM, Smith SE (2007) The arbuscular mycorrhizal fungus
Glomus mosseae gives contradictory effects on phosphorus and arsenic acquisition by
Medicago sativa Linn. Sci Total Environ 379:226–234. doi:10.1016/j.scitotenv.2006.07.038
Chhokar RS, Singh S, Sharma RK (2008) Herbicides for control of isoproturon-resistant
Littleseed Canarygrass (Phalaris minor) in wheat. Crop Prot 27:719–726. doi:10.1016/j.
cropro.2007.10.004
Chowdhury MHU, Mridha MAU, Khan BM, Xu HL (2002) Effects of effective microorganisms
on seed germination and seedling growth of Oryza sativa L. Nat Farm Environ 3:23–30
Corales RG, Obien SR, Cruz RT (1997) Effective microorganisms in transplanted and wet directed
seeded rice. In: Sharifuddin HAH, Sangakkara UR (eds) Proceedings of 5th Conference on
Effective Microorganisms (EM), Saraburi, Thailand, 8–12 Dec 1996
Daly MJ, Stewart DPC (1999) Influence of ‘‘effective microorganisms’’ (EM) on vegetative
production and carbon mineralization – a preliminary investigation. J Sustain Agric 14:
15–25
Daiss N, Lobo MG, Socorro AR, Bruckner U, Heller J, Gonzalez M (2008) The effect of three
organic pre-harvest treatments on Swiss chard (Beta vulgaris L. var. cycla L.) quality. Eur
Food Res Technol 226:345–353. doi:10.1007/s00217-006-0543-2
Doole GJ, Pannell DJ (2008) Role and value of including lucerne (Medicago sativa L.) phases in
crop rotations for the management of herbicide-resistant Lolium rigidum in Western Australia.
Crop Prot 27:497–504. doi:10.1016/j.cropro.2007.07.018
Elango F, Tabora P, Vega JM (1997) Control of black sigatoka disease (Mycospherella fijiensis)
using EM. In: 5th International Kyusei Nature Farming Conference, Bangkok, Thailand,
23–26 Oct 1997
Gao L, Yang H, Wang X, Huang Z, Ishii M, Igarashi Y, Cui Z (2008) Rice straw fermentation
using lactic acid bacteria. Bioresour Technol 99:2742–2748. doi:10.1016/j.
biortech.2007.07.001
Heichel GH, Barnes DK (1984) Opportunities for meeting crop nitrogen needs from symbiotic
nitrogen fixation. In: Bezdicek DF, Power JF (eds) Organic farming: current technology and
its role in sustainable agriculture. ASA Special Publication No. 46, ASA, CSSA, and SSSA,
Madison, WI
Heichel GH, Henjum KI (1991) Dinitrogen fixation, nitrogen transfer, and productivity of forage
legume-grass communities. Crop Sci 31:202–208
Higa T (1988) Studies on the application of effective microorganism in nature farming. In: 6th
IFOAM Conference, California University, CA, 18–21 Aug 1986
Higa T (1989) Studies on the application of effective microorganism in nature farming. II – The
practical application of effective microorganism. In: Proceedings of 7th IFOAM Conference,
Ouagadogua, West Africa
Higa T (1991) Effective microorganisms: a biotechnology for mankind. In: Parr JF, Hornick SB,
Whiteman CE (eds) Proceedings of the first International Conference on Kyusei Nature
Farming, USDA, Washington, DC, pp 8–14
Higa T (2000) What is EM technology? EM World J 1:1–6
Higa T, Kinjo S (1991) Effect of lactic acid fermentation bacteria on plant growth and soil humus
formation. In: Parr JF, Hornick SB, Whiteman CE (eds) Proceedings of the First International
Conference on Kyusei Nature Farming. UDSA, Washington, DC, pp 140–147
Higa T, Wididana GN (1991) Changes in the soil microflorainduced by effective microorganisms.
In: Parr JF, Hornick SB, Whiteman CE (eds) Proceedings of the First International Conference
on Kyusei Nature Farming. USDA, Washington, DC, pp 153–162
Higa T, Parr JF (1994) Beneficial and effective microorganisms for a sustainable agriculture and
environment. International Nature Farming Research Centre, Atami, Japan
366
A. Javaid
Hussain T, Jilani G, Ahmad R (1994) Sustaining crop yields and soil fertility by using effective
microorganisms. In: Abstracts, 5th National Congress of Soil Science, Peshawar, Pakistan,
23–25 Oct 1994
Hussain T, Javaid T, Parr JF, Jilani G, Haq MA (1999) Rice and wheat production in Pakistan with
effective microorganisms. Am J Alter Agric 14:30–36
Hussain T, Anwar-ul-Haq M, Ahmad I, Zia MH, Ali TI, Anjum S (2000) Technology of effective
microorganisms as an alternative for rice and wheat production in Pakistan. EM World J
1:57–67
Hussain T, Anjum AD, Tahir J (2002) Technology of beneficial microorganisms. Nat Farm
Environ 3:1–14
Imai S, Higa T (1994) Kyusei nature farming in Japan. Effect of EM on growth and yield of spinach.
In: Proceedings of 2nd International Conference of Kyusei Nature Farming, Brazil, pp 92–96,
7–11 Oct 1991
Iwaishi S (2000) Effect of organic fertilizer and effective microorganisms on growth, yield and
quality of paddy-rice varieties. J Crop Prod 3:269–273. doi:10.1300/J144v03n01_22
Javaid A (2006) Foliar application of effective microorganisms on pea as an alternative fertilizer.
Agron Sustain Dev 26:257–262. doi:10.1051/agro:2006024
Javaid A, Iqbal SH, Hafeez FY (1994) Effect of different strains of Bradyrhizobium and two types
of vesicular arbuscular mycorrhizae (VAM) on biomass and nitrogen fixation in Vigna radiata
(L.) Wilczek var. NM 20-21. Sci Int (Lahore) 6:265–267
Javaid A, Bajwa R, Rabbani N, Ahmad Q (1995) Growth, nodulation, nitrogen nutrition and VAM
colonization of pea (Pisum sativum L.) in soil treated with EM. Acta Sci 5:1–6
Javaid A, Bajwa R, Siddiqi I (1999) EM and VAM technology in Pakistan. VI: Effect of EM
(effective microorganisms) on VA mycorrhizal development and subsequent crop growth and
yield in sunflower. Pak J Biol Sci 2: 586–589
Javaid A, Siddiqi I, Bajwa R (2000a) EM and VAM technology in Pakistan. X: Effect of long term
application of EM on growth, yield and VA mycorrhizal colonization in wheat (Triticum
aestivum L.). Pak J Phytopathol 12:26–30
Javaid A, Bajwa R, Siddiqi I, Bashir U (2000b) EM and VAM technology in Pakistan. VIII:
Nodulation, yield and VAM colonization in Vigna mungo L. in soils with different histories of
EM application. Int J Agric Biol 2:1–5
Javaid A, Bajwa R, Rabbani N, Uzma M (2000c) EM and VAM Technology in Pakistan. IX:
Effect of EM application on growth, yield, nodulation and VA mycorrhizal colonization in
Vigna radiata (L) Wilczek. Pak J Biol Sci 3:694–698
Javaid A, Bajwa R (2002) EM and VAM technology in Pakistan. XIII: Growth and mycorrhizal
response of pea to EM in soils with different histories of EM application. Pak J Phytopathol
14:120–124
Javaid A, Anjum T, Bajwa R (2002) EM and VAM technology in Pakistan. XII: Growth, nodulation and VA mycorrhizal response of Phaseolus vulgaris to long-term EM application. Pak J
Phytopathol 14:57–61
Javaid A, Bajwa R, Anjum T (2008) Effect of heat-sterilization and EM (effective microorganisms)
application of wheat (Triticum aestivum L.) grown in organic-amended sandy loam soil. Cereal
Res Com 36(3):489–499. doi:10.1556/CRC.36.2008.3.13
Jonglaekha N, Dar-anum Y, Mekamol S (1993) The use of effective microorganisms for control
of wilt disease of potato. In: Pairintra C, Sangakkara UR (eds) Proceedings of the 1st APNAN
conference on effective microorganisms technology, Saraburi, Thailand, pp 104–111, 22–25
June 1992
Jonglaekha N, Pumsatit W, Mekamol S (1995) The use of EM for control of root rot of strawberry.
In: Sharifuddin HAH, Anuar AR, Shahbuddin MF (eds) Proceedings of 2nd Conference on
Effective Microorganisms, Saraburi, Thailand, pp 28–30, 17–19 Nov 1993
Joo YH, Lee KN (1991) Effect of EM on the production of citrus in Korea. In: Proceedings of the
1st International Conference on Kyusei Nature Farming, Khon Kaen, Thailand, USDA,
Washington DC, pp 101–107, 17–21 Oct 1989
12
Beneficial Microorganisms for Sustainable Agriculture
367
Kannaiyan S (2002) Biofertilizers for sustainable production. In: Kannaiyan S (ed) Biotechnology
of biofertilizers. Narosa Publishing House, New Delhi, India, pp 9–49
Kapoor R, Giri B, Mukerji KG (2004) Improved growth and essential oil yield and quality in
Foeniculum vulgare mill on mycorrhizal inoculation supplemented with P-fertilizer. Bioresour
Technol 93:307–311
Khaliq A, Abbasi MK, Hussain T (2006) Effect of integerated use of organic and inorganic nutrient
sources with effective microorganisms (EM) on seed cotton yield in Pakistan. Bioresour
Technol 97:967–972. doi::10.1016/j.biortech.2005.05.002
Khan BM, Hossain MK, Mridha MAU (2006) Effect of microbial inoculants on Albizia saman
germination and seedling growth. J Forest Res 17:99–102. doi:10.1007/s11676-006-0023-3
Khaosaad T, García-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically
reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734
Kim JK, Lee BK (2000) Mass production of Rhodopseudomonas palustris as diet for aquaculture.
Aquacult Eng 23:281–293. doi:10.1016/S0144-8609(00)00057-1
Kim MK, Choi KM, Yin CR (2004) Odorous swine wastewater treatment by purple non-sulfur
bacteria, Rhodopseudomonas palustris, isolated from eutrophicated ponds. Biotechnol Lett
26:819–822. doi:10.1023/B:BILE.0000025884.50198.67
Kinjo T, Perez K, de Almeida E, Ramos MAG, de Oliveia JO (2000) Plant growth affected by
EM-Bokashi and chemical fertilizers. Nat Farm Environ 1:33–38
Kremer RJ, Ervin EH, Wood MT, Abuchar D (2000) Control of Sclerotinia homoeocarpa in
turfgrass using effective microorganisms. EM World J 1:16–21
Lakshminarayana K, Sharma PK (1994) Molecular biology of nodulation in legume-Rhizobium
symbiosis. In: Prasad AB, Vaishampayan A (eds) Biology and application of nitrogen fixing
organisms. Scientific Publishers, Jodhpur, India, pp 155–172
Lee KH (1994) Effect of organic amendmentsand EM on the growth and yield of crops and on soil
properties. In: Parr JF, Homick SB, Simpson ME (eds) Proceedings of the 2nd International
Conference on Kyusei Nature Farming, USDA, Washington, DC, pp 142–147
Li WJ, Ni Y (2000) Use of effective microorganisms to suppress malodour of poultry manure.
J Crop Prod 3:215–221. doi:10.1300/J144v03n01_17
Maramble B, Sangakkara UR, Galahitiyawa N (1996a) Impact of effective microorganisms on
weed dynamics – a case study. In: Sharifuddin HAH, Anuar AR (eds) Proceedings of 3rd
Conference on Effective Microorganisms (EM), Saraburi, Thailand, pp 9–16, 16–19 Nov 1994
Maramble B, Sangakkara UR, Piyadasa ER, Ramayake SK (1996b) Growth and development of
purple nutsedge (Cyperus rotundus) as affected by effective microorganisms. In: Sharifuddin
HAH, Sangakkara UR (eds) Proceedings of 4th Conference on Effective Microorganisms,
Saraburi, Thailand, pp 84–89, 19–22 Nov 1995
Maramble B, Sangakkara UR (1998) Effect of EM on weed populations, weed growth and tomato
production in Kyusei nature farming. In: Parr JF, Homick SB (eds) Proceedings of 4th
Conference on Kysei Nature Farming, Paris, France, pp 211–216, 19–21 June 1995
Mridha MAU, Mahmud R, Anwar UR (1997) Interaction of EM and VAM on the growth of
Sesbania. In: Sharifuddin HAH, Sangakkara UR (eds) Proceedings of 5th Conference on
Effective Microorganisms, Saraburi, Thailand, 8–12 Dec 1996
Myint L, Myint H, Lwin T, Baw A (1996) Control of bacterial leaf blight of rice using effective
microorganisms (EM). In: Sharifuddin HAH, Anuar AR (eds) Proceedings of 3rd Conference
on Effective Microorganisms (EM), Saraburi, Thailand, 16–19 Nov 1994, pp 122–127
Naseem F (2000) Effect of organic amendments and effective microorganisms on vegetable
production and soil characteristics. Pak J Biol Sci 3:1803–1804
Nasiruddin M, Karim MA (1996) Evaluation of effective microorganisms for the control of insect
pests of cucurbitaceous vegetable crops. In: Sharifuddin HAH, Sangakkara UR (eds)
Proceedings of 4th Conference on Effective Microorganisms, Saraburi, Thailand, pp 76–83,
19–22 Nov 1995
Olsson PA, Thingstrup I, Jakobsen I, Baath E (1999) Estimation of the biomass of arbuscular
mycorrhizal fungi in a linseed field. Soil Biol Biochem 31:1879–1887
368
A. Javaid
Pairintra C, Pakdee P (1994) Population dynamic of effective microorganisms under saline soil
conditions in Thailand. In: Parr JF, Hornick SB, Simpson ME (eds) Proceedings of the 2nd
International Conference on Kyusei Nature Farming, USDA, Washington, DC, pp. 164–170
Park EK (1993) Biological control of root rot by using microbial control agent. In: Pairintra C,
Sangakkara UR (eds) Proceedings of 1st APNAN Conference on Effective Microorganisms
Technology, Saraburi, Thailand, pp 42–52, 22–25 June 1992
Paschoal AD, Homma SK, Sanches AB (1998) Effect of EM on soil quality, fruit quality and yield
of orange trees in a Brazil citrus orchard. In: 4th Proceedings International Conference on
Kysei Nature Farming, Paris, France, pp 103–111, 19–21 June 1995
Pasqualini D, Uhlmann A, Sturmer SL (2007) Arbuscular mycorrhizal fungal communities influence growth and phosphorus concentration of woody plants species from the Atlantic rain
forest in South Brazil. Forest Ecol Manage 245:148–155
Priyadi K, Hadi A, Siagian TH, Nisa C, Azizah A, Raihani N, Inubushi K (2005) Effect of soil
type, applications of chicken manure and effective microorganisms on corn yield and microbial properties of acidic wetland soils in Indonesia. Soil Sci Plant Nutr 51:689–691.
doi:10.1111/j.1747-0765.2005.tb00092.x
Punyaprueg S, Kanchana S, Pairintra C (1993) Effect of EM, residual incorporation and mulching
on soil fertility and sugarcane yield. In: Pairintra C, Sangakkara UR (eds) Proceedings of 1st
APNAN Conference on Effective Microorganisms (EM) Technology, Saraburi, Thailand,
pp 121–130, 22–25 June 1992
Ranjith NK, Sasikala C, Ramana CV (2007) Catabolism of l-phenylalanine and l-tyrosine by
Rhodobacter sphaeroides OU5 occurs through 3, 4-dihydroxyphenylalanine. Res Microbiol
158:506–511. doi:10.1016/j.resmic.2007.04.008
Rashid A, Siddique G, Gill SM, Aslam M (1993) Contribution of microbes in crop production. In:
Hussan T, Jilani G, Ahmad A, Ahmad S (eds) Proceedings of 1st National Seminar on Nature
Farming, Faisalabad, Pakistan, pp 50–53, 28 June 1993
Rashid MT, West J (2006) Dairy wastewater treatment with effective microorganisms and
duckweed for pollutants and pathogen control. In: Zaidi MK (ed) Wastewater reuse – risk
assessment, decision-making and environmental security. Springer, Netherlands, pp 93–102.
doi:10.1007/978-1-4020-6027-4
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53
Sajjad Z, Ahmad MS, Abbasi NA (2003) Effect of phosphorus levels and effective microorganisms.
Sarhad J Agric 19:193–197
Sangakkara UR (1996) Effect of EM on nitrogen and potassium levels in the rhizosphere of bush
bean. In: Parr JF, Homick SB, Simpson ME (eds) Proceedings of the 3rd International Conference
on Kyusei Nature Farming, USDA, Santa Barbara, CA, pp 216–222, 5–7 Oct 1993
Sangakkara UR (1998) Effect of EM on vegetable production in Sri Lanka: an economic analysis.
In: Parr JF, Hornick SB (eds) Proceedings of 4th International Conference on Kysei Nature
Farming, Paris, France, pp 217–222, 19–21 June 1995
Sangakkara UR, Higa T (1994a) Effect of EM on the growth and yield of selected food crops in
Sri Lanka. In: Parr JF, Homick SB, Simpson ME (eds) Proceedings of the 2nd International
Conference on Kyusei Nature Farming, USDA, Washington, DC, pp 118–124
Sangakkara UR, Higa T (1994b) Effect of EM on nitrogen fixation by Bush bean and Mung bean
In: Parr JF, Hornick SB, Simpson ME (eds) Proceedings of the 2nd International Conference
on Kyusei Nature Farming, USDA, Washington, DC, pp 64–71
Sangakkara UR, Marambe B, Attanayake AMU, Piyadasa ER (1998) Nutrient use efficiency of
selected crops grown with effective microorganisms in organic systems. In: Parr JF, Hornick
SB (eds) Proceedings of the 4th International Conference on Kyusei Nature Farming, Paris,
France, pp 111–117, 19–21 June 1995
Schroeder D, Muller-Scharer H, Stintson CSA (1993) A European weed survey in 10 major crop
systems to identify targets for biological control. Weed Res 33:449–468
Shaxson TF (2006) Re-thinking the conservation of carbon, water and soil: a different perspective.
Agron Sustain Dev 26:9–19. doi:10.1051/agro:2005054
12
Beneficial Microorganisms for Sustainable Agriculture
369
Sherchand K (2000) Reponse of effective microorganisms (EM) and other nutrients to rice and
wheat under field conditions in Khumaltar, Nepal. EM World J 1:40–44
Ta K, Chanh KK (1996) Use of EM for rice production in Vietnam. In: Sharifuddin HAH, Anuar
AR (eds) Proceedings of 3rd Conference on Effective Microorganisms (EM), Saraburi,
Thailand, 16–19 Nov 1994
Tokeshi H, Chagas PRR (1997) Control of sweet pepper anthracnose with effective microorganisms
under greenhouse conditions. In: 11th IFOAM International Science Conference, Copenhagen,
Denmark, 11–15 Aug 1996
Tokeshi H, Alves MC, Sanches AB, Harada DY (1998) Effective microorganisms for controlling
the phytopathogenic fungus Sclerotinia sclerotiorum in lettuce. In: Parr JF, Hornick SB (eds)
Proceedings of 4th International Conference on Kysei Nature Farming, Paris, France,
pp 131–139, 19–21 June 1995
Valerio F, Bellis PD, Lonigro SL, Visconti A, Lavermicocca P (2008) Use of Lactobacillus plantarum fermentation products in bread-making to prevent Bacillus subtilis ropy spoilage. Int J
Food Microbiol 122:328–332. doi:10.1016/j.ijfoodmicro.2008.01.005
Voss RD, Shrader WD (1984). Rotation effects and legume sources of nitrogen for corn. In:
Bezdicek DF et al. (eds) Organic farming: current technology and its role in sustainable agriculture. ASA Special Publication No. 16, ASA, CSSA, and SSSA, Madison, WI, pp 61–68
Wei GH, Zhang ZX, Chen C, Chen WM, Ju WT (2008) Phenotypic and genetic diversity of rhizobia
isolated from nodules of the legume genera Astragalus, Lespedeza and Hedysarum in northwestern China. Microbiol Res 163:651–662. doi:10.1016/j.micres.2006.09.005
Wibisono A, Buwonowat T, Wididana GN (1996) Effect of effective microorganisms on the
growth of Citrus medica. In: Proceedings of 3rd Conference on EM, Saraburi, Thailand,
pp 87–91, 16–19 Nov 1994
Widdiana GN, Higa T (1998) Effect of EM on the production of vegetable crops in Indonesia. In:
Proceedings of the 4th International Conference on Kysei Nature Farming, Paris, France,
pp 79–84, 19–21 June 1995
Wood MT, Miles R, Tabora P (1997) EM fermented plant extract and EM5 for controlling pickleworm (Diaphania nitidalis) in organic cucumber. In: 5th International Conference on Kyusei
Nature Farming, Bangkok, Thailand, 23–26 Oct 1997
Xiaohou S, Diyou L, Liang Z, Hu W, Hui W (2001) Use of EM-technology in agriculture and
environmental management in China. Nat Farm Environ 2:9–18
Xu HL (2000) Effects of a microbial inoculant and organic fertilizers on the growth, photosynthesis and yield f sweet corn. J Crop Prod 3:183–214. doi:10.1300/J144v03n01_16
Xu HL, Wang R, Amin M, Mridha U (2000) Effects of organic fertilizers and a microbial inculant
on leaf photosynthesis and fruit yield and quality of tomato plants. J Crop Prod 3:173–182.
doi:10.1300/J144v03n01_15
Yan PS, Xu HL (2002) Influence of EM Bokashi on nodulation, physiological characters and yield
of peanut in nature farming fields. J Sustain Agric 19:105–112. doi:10.1300/J064v19n04_10
Yamada K, Xu HL (2000) Properties and applications of an organic fertilizer inoculated with
effective microorganisms. J Crop Prod 3:255–268. doi:10.1300/J144v03n01_21
Yousaf M, Khan MA, Wahed A (1993) Use of effective microorganisms as substitute for chemical
fertilizers. In: Hussan T, Jilani G, Ahmad R, Ahmad S (eds) Proceedings of 1st National
Seminar on Nature Farming, Faisalabad, Pakistan, pp 71–75, 28 June 1993
Yousaf Z, Jilani G, Qureshi RA, Awan AG (2000) Effect of EM on groundnut (Arachis hypogaea
L.) growth. Pak J Biol Sci 3:1803–1804
Zacharia PP (1995) Studies on the application of effective microorganisms in paddy, sugarcane
and vegetables in India. In: Shariffun HAH, Anuar AR, Shahabuddin MF (eds) Proceedings of
the 2nd Conference on Effective Microorganisms, Saraburi, Thailand, pp 31–41, 17–19 Nov
1993
Zhao Q (1998) Effect of EM on Peanut production and soil fertility in the red soil region of China.
In: Proceedings of the 4th International Conference on Kysei Nature Farming, Paris, France,
pp 99–102, 19–21 June 1995
Chapter 13
Foliar Fertilization for Sustainable Crop
Production
Seshadri Kannan1
Abstract Plants require inorganic nutrients in addition to carbon dioxide and
water for growth and production. Nutrients are present in soil, but get depleted
unless supplied through fertilization. Soil feeding is the normal practice, but has
limitations with respect to its availability to the plants. The elements such as phosphorus, potassium, and most of the micronutrients are fixed in the soil complex,
while the more soluble nutrients such as nitrogen are easily leached down the soil.
What is lost through leaching reaches the aquifer and pollutes the groundwater.
For instance nitrates and phosphates can be harmful to humans. With increasing costs
of fossil fuel, which provides the raw materials for fertilizer manufacture, there is
a need to find innovations in fertilizer usage techniques. Foliar application is one
such technique. Here I review the extensive work that has been carried out on the
effectiveness of foliar-applied nutrients, the mechanisms of foliar absorption, and
transport. The leaf components such as the cuticular membranes, the trichomes,
the cuticular pores, ectoteichodes, their properties, and their role in the nutrient
transport into the plant leaf are reviewed. Cuticles are permeable to nutrient ions
present in aqueous forms and have distinct structures like pores. But it is not known
if these pores facilitate easy entry into the leaf cells. The trichomes increase the
amount transported into the leaf by providing more area for absorption. The cuticles
have two types of lipophilic substances, the cutin and the cuticular wax, which
influence the permeability of nutrient ions to varying degrees.
It is clear that nutrients reach the leaf cells, after penetrating the cuticle, and
are further transported to other parts through plasmadesmata. Some micronutrients
are not as freely mobile as the major nutrient elements such as N, P, or K. The age
Retired. Present address: 38 South Mada St., Thiruvanmiyur, Chennai 600041.
This review marks the 82nd birthday on 28 December.
1
S. Kannan (*)
Biology and Agriculture Division, Bhabha Atomic Research Centre,
400085 Mumbai, India
e-mail: seshkann@yahoo.co.in
E. Lichtfouse (ed.), Genetic Engineering, Biofertilisation, Soil Quality
and Organic Farming, Sustainable Agriculture Reviews 4,
DOI 10.1007/978-90-481-8741-6_13, © Springer Science+Business Media B.V. 2010
371
372
S. Kannan
of the leaf and the pH of the spray liquid are important for foliar absorption.
The absence of plasmadesmatic connections between the guard cells and the epidermal
cells is also important. One element Cl has been found to be transported from the
applied leaf to other parts rapidly, showing it is freely mobile. This should be true for
many anions.
The concept of limiting factors and the law of the maximum proposed by
Wallace group are useful in raising the yield plateau, and when soil supply poses
the “limiting” factor, foliar feeding will help increase the crop yield. Modern
technique of sprinkler irrigation system can be exploited to supply the nutrient
elements in the irrigation water, which will be economical in foliar fertilization.
Foliar nutrition is very practical to correct micronutrient deficiencies, which are
very important for maximizing the yield. Crop breeders could also help evolve
cultivars, which give good response to foliar feeding.
Keywords Critical growth stage • cuticle • eutrophication • inorganic nutrients
• leaf uptake • sprinkler irrigation
13.1 Introduction
The fact that food production has to be increased over the coming few decades to
feed the growing population needs no emphasis. The population is predicted to
reach nine billion in 2030, and feeding them is the greatest challenge for scientists
(Gomiero et al. 2008), and the agricultural land is dwindling in area, one main
reason being the large-scale urbanization, while the existing arable land is getting
impoverished in nutrients owing to continuous cropping. The environmental impact
of intensive agriculture and the adverse effects of climate change also threaten food
security in many parts of the world and there is an urgent need to develop more
innovative agricultural technologies, which would help preserve the agro-ecosystems,
and to deal with the reduced availability of fossil fuels, which are presently used for
fertilizer production. One of the methods is to increase the nutrient-use efficiency
of crops. Besides the nutrients, the other most important input is carbon dioxide that
is derived from the atmosphere. In order to improve crops’ ability to convert the
atmospheric carbon dioxide into food, plant engineers directed their attention to
RuBisCo (Ribulose-1, 5-bisphosphate carboxylase/oxygenase), which catalyzes the
photosynthetic process, and yet is considered a very inefficient enzyme (Mann
1999). While other efficient forms of catalysts found in red algae could not be yet
harnessed for higher plants, the geneticists have but to stay with RuBisCo at least
for some time. The tools that helped double the food production since 1960 have
lost their edge, putting an end to the productivity increases. Efforts to engineer the
crop plants to get over the yield plateau and push yields to a new level of a projected
40% increase in global demand for rice, wheat, and maize by the end of next decade
are needed. While on the one side, plant breeders could concentrate on the development
13
Foliar Fertilization for Sustainable Crop Production
373
of new cultivars through genetic engineering, they also fear that farmers may not
have enough water to grow the new crops or may be forced to use more fertilizers
especially when less fertile lands have to be brought under cultivation. This recourse
will undoubtedly poison the ecosystems and permanently damage the soils. Furthermore,
the geneticists have hitherto made selection or evolved high-yielding cultivars,
which nevertheless are more responsive to higher fertilizer input, adequate water,
and the right environment for efficient photosynthesis. But water and nutrients do
impose new constraints for higher yields. Interestingly, it is not true that given all
these inputs, the yield increase will reach without any limitations. The old and wellfounded concept of “limiting factors” explains how various inputs influence the
yield, and how the yield plateau could be raised by providing the input that imposes
a limit, and crop production can be increased (Wallace and Wallace 2003).
There has been a growing tendency with the farmers to “over-fertilize” when
they do not obtain good response to a particular input, for example, fertilizers.
This leads to an excessive loss of fertilizers from the soil to the aquifers or these
inorganic elements get accumulated in the crop production and finally into the
biological cycle causing health hazards. Due to that the amount of nitrogen lost
in the runoff is very high, raising the nitrate levels in the water system. Such a
situation has arisen in the Gulf of Mexico, and the high nitrate levels in the sea
are traced to agriculture. In California where half of the country’s vegetables are
grown, there are about 120 water sources classified as containing “excessive
nutrients.” The drinking water in a community in Salinas Valley is banned
because of high nitrate levels in the water system. Nitrate-N concentrations in
groundwater in Japan have increased greatly in the last 2 decades (Kumazawa
2002). With the use of controlled-release fertilizers, nitrogen-use efficiency was
increased considerably, bringing down the level of nitrate-N in the groundwater.
Increasing levels of atmospheric gases, especially carbon dioxide as a result of
burning fossil fuels, not only cause health hazards but also affect crop yield.
Contrarily, there is one school which believes and has produced evidence that this
increase actually will enhance crop production instead of reduction, provided
other inputs such as water and nutrients are increased proportionately. In the coming sections these will be discussed as also the different views on the inputs
required for increasing crop production.
Advances in an understanding of plant nutrition, development of slow-release
fertilizers and soluble nutrients, and improvement in soil- and tissue-testing methods
have all contributed to the increase in the yield and quality of crops. Future developments will have to focus on fertilization in an increasingly competitive global
economy. Foliar application of nutrients has been in practice over 6 decades with
the objectives to provide the required nutrients most effectively and in a few cases
economically for crops that have larger leaf area. Several papers appeared on the
field experiments on foliar sprays of nutrients especially N, P, and K on crops from
the work at Rothamsted experiment station during the 1950s. The great response
for foliar absorption by apple leaves led to an extensive usage of urea sprays on fruit
trees, pineapples, and vegetable crops in many countries.
374
S. Kannan
There was a renewed interest in foliar nutrition in the 1960s when radioisotopes
became available to trace the movement of nutrient elements within the plant as
also in the understanding of the mechanisms of leaf uptake, and the means to
increase its effectiveness. Now sprinkler irrigation has become a common practice
in field crops and with the advent of computers and electronic devices, the supply
of water could be regulated with great precision. Taking advantage of the sprinkler
irrigation supplying nutrients too could be included in the spray liquid and nutrient
supply could also be regulated using computer technology. Fertilization through the
soil serves the most convenient means and will continue to be so in the future too.
However, for the aforesaid reasons like over-fertilization, and eutrophication, other
methods of feeding need serious consideration. Foliar feeding is one method which
can meet the requirement as a supplement to soil feeding in many cases. Bi and
Scagel (2007) recommend foliar N application for raising nursery plants. While this
can correct the N deficiency in the early growth stages, it can decrease the amount
of total N necessary and minimize N runoff. Supplementing a traditional
N-fertilization program with foliar applications gives growers more management
options. One of these is the timing of foliar application which is based on the
specific goals of production, and the benefits which are desired.
In a recent review, Fernández and Eichert (2009) state that foliar fertilization is
an agricultural practice of increasing importance in practical terms. In theory, application of nutrient sprays may indeed be an environmentally friendly fertilization
method since the nutrients are directly delivered to the plant in limited amounts,
thereby helping to reduce the environmental impact associated with soil fertilization. However, response to foliar sprays is often variable and not reproducible due
to the existing lack of knowledge of many factors related to the penetration of the
leaf-applied solution. It is the objective of this review to examine what has been so
far studied and outline the prospects of this technology.
13.1.1 Ability of the Leaf to Absorb Nutrients
The fact that leaves as well as other aboveground parts are capable of absorbing
nutrients has been known for over a century (Gris 1844). The acquisition of S, N,
Mg, and Cu from the industrial gases via the rains known as “wet deposition” and
“Occult precipitation” was also recorded in England (Dollard et al. 1983). Scientists
found iron and sulfur compounds which were released into the atmosphere during
the ore-smelting activity, and absorbed by the leaves of trees and transported to
other parts. The absorption of atmospheric NH3 and SO2 by plant leaves is also
known (Aneja et al. 1986). While the uptake of N and S serve as nutrients, the
absorption of pollutants like lead and cadmium released from the burning of fossil
fuel is harmful. The most recent report shows how fast an element can enter the leaf
and become toxic more quickly than if supplied through the roots. It relates to
very rapid absorption of boron from boron-containing water by vegetable leaves,
while boron through soil took a long time to reach the plant parts (Ben-Gal 2007).
13
Foliar Fertilization for Sustainable Crop Production
375
There was an interesting study regarding the question which forms of N, i.e., NH4
or NO3 is taken up, as also whether the roots or the fronds of the aquatic plant
Landoltia punctata are capable of greater absorption (Fang et al. 2007). It was
found that both fronds and roots absorbed both forms of N, and the overall capacity
of roots and the fronds to take up ions was similar. The above findings provide
enough evidence about the capacity of the leaf to take up nutrients.
13.1.2 Foliar Supply of Micronutrients: Influence of Growth
Substances
One area where foliar application is most effective is in the control of micronutrient
deficiencies. Foliar application was practiced for the supply of B, Cu, Mg, Mn, and
Zn in many crops for timely control. Swietlik and Faust (1984) have summarized
the results of the experiments with micronutrient sprays on fruit trees. There have
been many reports which appeared over several years. Some of the recent findings
are given here (Table 13.1).
Certain additives and growth substances increased the effectiveness of foliar
uptake. Studies were made with radioisotopes and growth regulators on various
plants and a few nutrient elements and some of these are presented here
(Table 13.2).
A large number of studies were made to measure the rate of mobility of foliarapplied nutrients, and radioisotopes were widely employed for the experiments.
Basically, the nutrient element supplied to the leaf would move in either direction,
i.e., toward the tip or base of the leaf. While the root-absorbed nutrients would
reach the leaf and other aboveground parts through the xylem under the transpiration
pull, the foliar-applied elements can move out of the leaf or be transported to the
base of the plant. To describe a few, there were three experiments conducted by
Table 13.1 Foliar application of micronutrients in different crops
Nutrient elements
Crops
References
Iron
Sorghum, vegetables, ornamental
Ritter 1980
plants, fruit trees
Manganese
Fruit trees, vegetables, soybean
Gettier et al. 1985; Young 1983
Manganese
Lupin
Hannam et al. 1984
Zinc
Apple, grapevine
Peryea 2006
Zinc
Pistachio and walnut fruit crops
Zhang and Brown 1999,
Swietlik 2002
Boron
Tomato, turnip
Williams et al. 1983
Copper
Citrus, onion
Young 1983
Molybdenum
Poinsettia
Cox 1992
Calciuma
Tomato, strawberry
Drake and Bramlage 1983
Blueberry
Stückrath et al. 2008
a
Is not classified as a micronutrient
376
Table 13.2 Foliar uptake of nutrients and influence of growth substances
Element
Plants
Uptake
N, P,+K with
Milk thistle
Yield increased
With Dropp/TIBA/Pix.
(see text)
59
Fe+ABA/kinetin
Bean
Increased absorption
Zn-chelate + GA3
Washington Navel
Orange in Egypt
S. Kannan
Authors
Geneva et al. 2008
Kannan 1986
Eman et al. 2007
GA = gibberellic acid, ABA = abscisic acid
scientists. In one experiment, the movement from the site of application to the
rest of the leaf was followed. Ringoet et al. (1971) developed a technique to measure the rate of movement of 45Ca placed on the middle of an oat leaf by in vivo
counting with b-sensitive semiconductor detectors. They found that Ca migrated
in the acropetal direction at low concentrations, but moved down to the base of
the leaf at concentrations above 0.02 M. They concluded that Ca was fairly
mobile and the downward transport was through the phloem while it moved
upward in the xylem. There are some nutrient elements for which stable isotopes
were not available and a new technique was developed for tracking the movement
of boron (Chamel and Eloy 1983). They used 11B/12B and measured the ratio of
the two in plant samples with a highly sensitive spark-source mass spectrometry
and microanlytical method using a laser-probe mass spectrograph. They found
that the largest fraction of foliar-applied B remained in the applied leaf itself.
However, it entered the leaf surface and remained bound as polysaccharide
complexes. It was concluded that B is partially mobile, like Fe, Mn, or Zn.
Relative mobility of various elements in the leaves was reported in several studies
(Kannan 1990).
Thus there is enough evidence that leaf is capable of absorbing inorganic nutrients
supplied in aqueous forms and then transporting to both the shoots as also the roots.
Elements like Ca were found in the xylem and phloem too.
13.2 Responses to Foliar Supply of Nutrients – Studies
with N, P, and K
13.2.1 Response to N
The application of nutrients like N, P, and K to the leaf during the autumn, i.e., prior
to the leaf fall, is considered beneficial to fruit trees on the hypothesis that these
will be remobilized during the spring growth from the stored organs. Oland (1960)
was the first to report that urea sprayed to apple trees prior to leaf fall was most
effective to supply N for use in spring growth. This is good for another reason in
13
Foliar Fertilization for Sustainable Crop Production
377
that high concentrations of urea can be given with the least damage. The effectiveness
of spraying foliage of 1-year-old nectarine trees with urea to provide nitrogen to
augment the seasonal internal cycling of N was examined (Tagliavini et al. 1998).
The tree was sprayed with a 2% urea solution labeled with 15N just before leaf
senescence. Remobilization of both labeled and unlabeled N for leaf growth the
following spring was quantified. During leaf senescence, the majority of 15N was
withdrawn from the leaves into the shoot and roots. About 38–46% of 15N in the
trees was recovered in the new growth. However, more N taken up by the roots was
mobilized for leaf growth in the spring than was withdrawn from the senescent
leaves receiving N through sprays. They concluded that the foliar-supplied N had
to be supplemented by soil application for new growth. In the case of apple trees,
3% urea sprays given twice a week increased the whole-plant N content which also
enhanced the utilization of reserve carbohydrates for new growth (Cheng et al.
1999).
Nitrogen management for orchard trees is very important and the growers are
keen on increasing productivity and fruit quality without affecting the environment.
They find foliar sprays of N as an alternative to soil feeding. Experiments have been
carried out to ascertain the time for foliar sprays suitable for greatest response.
Using 15N labeled Ca(NO3)2, the uptake, partition of N, and its remobilization in
pear (Pyrus communis L) after 1 year of foliar application were assessed (Quartieri
et al. 2002). The young trees were divided into three groups, viz., (A) received 3 g
of labeled N from mid-March to mid-June, trees of group (B) received 3 g of
labeled N from late June to fruit harvest (August 20). Both A and B also received
unlabeled N at 3 g/tree from late June to fruit harvest and from mid-March to
mid-June respectively. A third set (C) received N at 6 g/tree throughout the season.
Fruits and leaves were analyzed for N and were found to contain similar amounts
of N derived from remobilization of stored N and from spring uptake (March–June,
treatment A); only about 10% of N was derived from N taken up after June (B).
Although abscised leaves contained ten times higher amounts of N taken up early
(A) than late (B) treatments, similar amounts of labeled N were recovered in the
whole tree framework, in winter in trees of group A and B. Remobilization of N in
the following spring accounted for 23–24% of the labeled N in the tree, regardless
of the timing of N uptake. They found that a limited amount of N given before fruit
harvest did not increase the fruit N content, but increased its storage in the roots
during winter, which was remobilized the following spring. Similar findings were
also recorded by Dong et al. (2002) from experiments with urea sprays on apple
trees.
Improvement of the grain protein in high-yielding cereals has been the most
important goal in recent times because of the high premium it fetches the farmers,
and studies have clearly shown that foliar sprays of N increased in grain protein in
wheat. Optimal timing for N sprays on wheat was examined (Bly and Woodard
2003) and the results showed that postpollination foliar N gave the highest grain
protein. Likewise there was significant increase in total grain N and protein content
from the postflowering sprays of urea-ammonium nitrate (Wuest and Cassman
1992; Woolfolk et al. 2002).
378
S. Kannan
The absorption and utilization of N and its influence on the carbon metabolism
in Ricinus communis L. were examined (Peuke et al. 1998). N was taken up more
readily from (NH4)2SO4 than from KNO3, and more evenly distributed between the
shoot and the root while nitrate-N was transported largely to the roots. The sprays
increased both organic and inorganic particles on the surface of the leaf thus
increasing its wettability and absorption. Furthermore, the presence of the nutrient
particles on the leaf surface and in the stomata indicated that the entry of nutrients
in the thin water films entered through the stomata and the cuticles.
Various factors influence the absorption by the leaf and the leaf age and form of
nutrients are important in influencing the uptake. Urea-N has been employed for
such studies. However, for comparison between N from urea and N from KNO3
leaves of citrus were dipped into a solution of 11.2 g N/l and the uptake was measured for several hours (Lea-cox and Syvertsen 1995). It was found that uptake of
N per unit leaf area was 1.6- to sixfold greater for 2-month old leaves than for older
leaves. In another experiment, it was found that 24% and 54% of applied N were
taken up after 1 and 48 h respectively from N-urea and under similar durations,
only 3% and 8% of N from KNO3 were taken up. Urea increased the leaf N much
more than the KNO3 form of N.
Though urea sprays have been used for several crops over many years, this could
not supply the entire N requirement of the crop. Nevertheless, experiments were
conducted to study if foliar-applied urea can be sufficient to increase the fruit growth
and yield of peach [Prunus persica L. Batsch (Peach Group)] cultivar, Early
Maycrest (Johnson et al. 2001). In a 3-year experiment, the authors compared a total
foliar urea to an equivalent amount of N through the soil. Though foliar treatment
supplied adequate amounts of N to the various organs viz., the roots, shoots, and fruit
buds, the mean fruit weights were lower than those fertilized through the soil.
However, when a 50:50 combination treatment of soil-applied N in late summer with
foliar-applied N in October was given, the fruit yields and fruit weights equaled the
soil-fertilized ones. It was concluded that some soil-application of N is necessary for
optimum fruit growth and this is needed in order to have good root proliferation
which would in turn facilitate an increased soil uptake. This combination of fertilization also reduces excessive vegetative growth and offers as a viable alternative for
maintaining tree productivity and reducing soil pollution at the same time.
Foliar supply of urea to citrus trees for N fertilization has been particularly useful
in reducing groundwater pollution with nitrates. The seasonal absorption characteristics of three urea compounds, viz., triazone-urea, liquid urea, and spray grade urea
by citrus leaves were examined (Bondada et al. 2001). Factors like the age and the
N status of the leaves influenced the rate of absorption. In the field grown plants,
leaf N was increased equally in all the three formulations of N. Young leaves from
1-week to 1-month old, absorbed greater amounts of N than the older leaves
(3–6 months).With the increasing epicuticular wax concentrations. 15N uptake
was decreased. Triazone-urea increased the N concentration more than urea sprays.
In the plants grown in the greenhouse, 15N absorption was greater through abaxial
leaf surfaces than through adaxial surfaces, in general. Applying foliar 15N-urea
during night (2,000–2,200 h) resulted in greater absorption of N than in the mornings
13
Foliar Fertilization for Sustainable Crop Production
379
(0800–1,000 h) or afternoons (1,200–1,400 h). Triazone-urea acted as a slow-release
N source that could be exploited for foliar application to be effective over an
extended period of time.
Foliar supply of nutrients assumes importance under various conditions, important one being the inability of the roots to absorb the soil nutrients. Such a situation
prevails when the plant roots are submerged under water or when the plants are
grown in hypoxic nutrient solutions, causing marked inhibition of uptake of major
nutrient elements by the roots. Under hypoxic conditions in particular, the reserve
metabolic energy of root cells is considerably reduced. The foliar application is an
accepted practice to supply nutrients to shoots under such conditions. Nitrogen,
phosphorus and potassium in soluble forms are readily absorbed by aerial plant
parts, often much more efficiently than from supplementary soil treatments (Xie
and Zhang 2004), Foliar sprays of nitrogen fertilizers caused appreciable yield
improvement in waterlogged cotton (Hodgson 1982) and rape (Zhou et al. 1997).
Although application of fertilizers to waterlogged soil has been found to improve
plant growth, the excess water in the soil causes dilution of the nutrients in the root
medium. In addition, waterlogging reduces the ability of plant roots to take up and
transport mineral nutrients to the shoot (Ashraf and Rehman 1999; Malik et al.
2001). Foliar spraying of nutrients serves as an efficient way to improve the nutrient
status of the waterlogged plants. Pang et al. (2007) studied the waterlogging effects
on nutrient uptake from foliar sprays in six barley cultivars with contrasting tolerance to waterlogging. It was found that the adverse effects of waterlogging were
greatly reduced by the foliar sprays of nutrients, in all cultivars in general. The
sprayed plants had better shoot and root growth and reduced leaf senescence. Auxin
was found to be accumulated at the shoot base of the sprayed plants. It is explained
that the better growth was primarily due to increase in the synthesis of growthpromoting substances like auxin. Many of the issues relating to foliar fertilization
by plants have been reviewed by Wojcik (2004). He emphasizes that this mode
should be included in the integrated plant production scheme because it is environment-friendly with prospects of the increasing crop productivity and good-quality
yields. Foliar feeding is profitable for perennial fruit crops with deep-rooting systems since soil surface application of most fertilizers is slow in response. One such
condition prevails in Australia where passion fruit is cultivated. Passion fruit
(Passiflora edulis Sims) is cultivated extensively in Australia and the growers face
the problem of fertilizing the plants through soil since the shorter photoperiod in
winter reduces the vegetative growth and the low temperature prevents soil N
uptake. Commercial growers resort to foliar sprays of urea during winter for providing adequate N (Menzel et al. 1986).
Foliar supply is effective under conditions of decreased nutrient availability
in soil, dry topsoil, and decreased root activity during the reproductive stage.
Ca sprays are beneficial to increase the calcium content of fruits and cereal grain.
For nutrients which are phloem-mobile this method is particularly more effective.
Recently, foliar application of some products, like seaweed extracts, hydrolyzed
proteins, and amino acids is being popularized. But their influence on crop production
is not fully established. Wojcik has presented the findings of several workers, on the
380
S. Kannan
mechanisms of penetration of nutrient ions through cuticles, entry into the leaf cells
through the plasma membrane, and the factors influencing the foliar absorption.
13.2.2 Response to N, P, K, Ca
Foliar sprays could be given for supplying not only N but also other major nutrients.
The results of a few experiments are given here. Early experiments on response to
foliar application were reported in USA and England. Barley, Brussels sprout,
French bean, tomato, and sugar-beet plants grown in soil in pots and sprayed with
nutrient solutions containing nitrogen, phosphorus, potassium, and a spreader, had
higher nutrient content and dry weights than control plants sprayed with water and
spreader only. Increase in nutrient content occurred with high or low levels of nutrient
supply to the roots and was approximately proportional to the concentration of
spray and to the frequency of spraying. There was no difference in N uptake in
sugar beet, from ammonium sulfate, calcium nitrate, or urea in equivalent concentrations. Furthermore, nutrient uptake from solutions sprayed on leaves influenced
root uptake of nutrients (Thorne 1954).
Foliar sprays of N and P on wheat were given at different stages of the crop and
the response with respect to the soil water content was also examined (Alston
1979). Nitrogen sprays given after ear emergence, as a supplement to soil application
of ammonium sulfate resulted in increased grain yield when the soil moisture was
adequate. When phosphorus was also included in the spray liquid containing N the
yield was increased much higher. Liquid foliar fertilizer (“Agroleaf” Scotts Co.,
OH, USA contains NPK at 20:20:20) at 0.3% was sprayed twice a week on pea
plants (Hristozkova et al. 2006) which increased the nitrate reductase and glutamine
synthetase in the shoots especially when Mo was supplied.
The effectiveness of foliar sprays at certain critical growth period has been
discussed (Kannan 1990). Experimental results with maize to find out whether
foliar N, P, K, and S at the grain development stage would be beneficial were not
supportive of the hypothesis (Below et al. 1984). Soybean is classified as a “selfdestructive” crop requiring large amounts of N during the “seed-fill” period.
Experiments with foliar sprays of N, P, K, and S during the R-5 and R-7 stages of
soybean showed positive results (Syverud et al. 1980). Several studies have been
made recently on the effectiveness of foliar sprays at specific growth periods. One
such study was to find out the effectiveness of foliar sprays of nutrients for increasing
the duration of the flowering stage of milk thistle (Silbum marianum L.) so that seed
yield and the silymarin content could be increased (Geneva et al. 2008) Soil and
foliar application of fertilizers and growth regulators together were compared
and it was found that yields could be increased when nutrients and the growth substances Pix and Regalis were given as foliar sprays, while soil application of nutrients
with Pix alone and not Regalis, produced greater yields. Pix is mepiquat chloride,
BASF; and Regalis is Prohexadione-Ca, BASF. However, plant growth regulators
with either soil or foliar application increased the total silymarin content equally.
13
Foliar Fertilization for Sustainable Crop Production
381
In another experiment, Stancheva et al. (2008) examined the effects of Agroleaf, (1)
“Agroleaf total” (N:P:K = 20:20:20 + microelements), twice during the vegetative
growth stage on 20-days interval until the rosette phase; (2) “Agroleaf with high P”
(N:P:K = 12:52:5 + microelements), before the blooming stage; and (3) “Agroleaf
with high K” (N:P:K = 15:10:31 + microelements), after the blooming stage. Their
study included the effects of growth regulator thidazuron on foliar versus soil fertilization, on the seed yield and silymarin content. Combined application of the fertilizers with thidazuron affected the growth, accumulation of nutrients (N, P, and K),
nitrate reductase activity, reducing sugars and free amino acids content significantly. These changes were associated with altered flowering rate, enhanced seed
ripening, and increased yield. Treatment of milk thistle plants with thidazuron in
combination with foliar fertilizer increased seed yield due to an increase in the
number of lateral stems, the number of flower heads and the seed fresh weight per
flower head. Silymarin content in the seeds was also positively increased by using
thidazuron. These results show that foliar fertilization is beneficial, when given at a
given growth stage.
An interesting case relates to K application to cotton. K deficiency is widespread
across the US cotton Belt over several years and it is noticed in the latter half of the
season in a wide range of soils and amongst many cultivars. This deficiency is largely
a result of increased use of N and also the introduction of high-yielding and fasterfruiting cultivars, which need large amounts of K and the roots do not cope with this
demand. Potassium deficiency is also due to a low K status of many soils. Cotton is
more sensitive to low K availability than most other major field crops. Foliar application
of K is very effective for countering late-season K deficiency quickly and efficiently.
Significant yield increases from foliar-applied K were obtained in 40% of field trials
with an average increase of about 75 kg lint/ha. KNO3 was preferred to K2SO4. Cotton
plants respond very well for K sprays in Egypt. Three to four foliar sprays of K to be
given during the first 5 weeks of boll development at 7–10 days intervals starting at
the commencement of flowering are recommended. K given as KNO3 or K2SO4 was
equally effective (Eid et al. 1997). A comparative study of foliar versus soil application
of K to “French” prune trees was made (Southwick et al. 1996). Their trials over 3
years revealed that four sprays of KNO3 (20–22 L/tree were as effective as single
annual soil application of KNO3 at 1.4–2.3 kg/tree. It was also found that foliar KNO3
sprays given four times throughout the growing season corrected incipient K
deficiency and gave same or higher yields than soil application.
K requirement has increased recently in many regions because of periodic
drought conditions resulting in soil compaction and poor soil availability. Soil K
availability is very much reduced in the states of Missouri, Illinois, and Kansas,
where the subsoils are highly clayey. Lesser amount of K was applied as fertilizer
by the farmers, due to low commodity prices. Nelson et al. (2005) studied the
response to foliar-applied K at several growth stages and the cost-effectiveness, for
soybean in claypan soils. K as K2SO4 was given as a pre-plant soil at 140, 280, and
560 kg ha−1, or foliar supply at 9, 18, and 36 kg ha−1 at V4, Rl-R2, and R3-R4 stages
of development. The results showed significant increase in grain yield from 727 to
834 kg ha−1 when K spray was given at 36 kg ha−1 at the V4 and R1-R2 stage, but
382
S. Kannan
when given at the R3-R4 stage, grain yield increased but not as high as at V4 or
R1-R2. It was also revealed that foliar K could only be a supplemental option when
the climatic and soil conditions are unfavorable to root uptake.
Muskmelon (Cucumis melo L. Reticulatus group) responds very well to foliar
supply of K (Lester et al. 2005). In this crop, the fruit sugar content is directly related
to K-mediated phloem transport of sucrose into the fruit. During the muskmelon fruit
growth, soil fertilization was inadequate due to poor root absorption capacity. Under such
conditions K supplement as potassium metalosate (24% K) through foliar sprays was
very effective in improving fruit quality. Their conclusion was that carefully timed foliar
K nutrition can alleviate the K deficiency effects on fruit quality and marketability.
Furthermore, there were many additional benefits from the foliar spray of K. Fruits from
plants, given the foliar K matured 2 days earlier, were firmer with higher K, soluble
solids, total sugars, vitamin C, and beta carotene than those of control plants.
Calcium sprays are very effective on improving the quality of fruits (Kadir
2004). Trees (apple Malus domestica graft) were given one to eight sprays at 8.971
kg ha−1. More than six sprays improved fruit quality, increase in fruit weight, size,
appearance, redness, and less scald incidents. The ratio of soluble solids to titratable
acidity was also increased. Fruit skin redness was the most significant effect and
related to a linear increase in amount of Ca in fruit and leaf tissues. There was also
an increase in K, Mg, P, and N in the fruit.
13.2.3 Response to N, P, K with Micronutrients
Foliar application of N, P, and K can include micronutrients also with good results
on yield and quality of crops. The effects of foliar application of N–P–K mixtures
with or without S, B, Fe, and Zn at V5-V8 stages on the oil and protein content in
soybean were examined (Haq and Mallarino 2005). But the results were not consistent.
In one trial increase in the oil and protein content was obtained, but in another, it
resulted in decrease in protein content. By this combination of major and minor
elements, there was no saving in the cost, which is likely to accrue when herbicide
is included with the nutrients.
There are specific instances where a single major nutrient is combined with
a micronutrient and again the results were not supportive of this combination.
The effects of N and B sprays together were examined on soybean yield in the
soybean production region of Mid-Atlantic Coastal Plain (Freeborn et al. 2001). In
their experiments a few factors were examined, viz., the effects of (i) application rate
and reproductive stage timing of N or B on seed yield; and (ii) cultivar, row spacing,
or planting date on the response to N and B application at R3 stage. N was supplied
to the soil at 0, 14, 28, 56, 84, 112, or 168 kg ha−1. B was given to the foliage at 0,
0.14, 0.28, or 0.56 kg ha−1 to either R3 or R5 stage. It was found that though the N
and B concentrations in the leaf tissues were above the minimum required, maximum
yield was not influenced by N or B. The results were disappointing, since foliar B was
not needed when the soil supply was adequate for higher yields.
13
Foliar Fertilization for Sustainable Crop Production
383
In contrast to the results with N and B, the sprays of both K and B were beneficial.
In Arkansas, research showed that the K requirement of the fast-fruiting and highyielding cultivars of cotton far exceeded the uptake capacity of the plants from the
soil. Furthermore, the root activity of these cultivars actually decreases during
flowering and boll development. Various K compounds viz., KNO3, K2SO4, K2S2O3,
and KCl, and buffers for the spray solution, including addition of B were evaluated
(Howard et al. 1998). In another study, KNO3, or K2SO4 solution, unbuffered, or
buffered to pH 6 and 4 were sprayed at 4.1 kg K ha−1. A third study had combination
of soil-applied and foliar-applied B and K. Foliar sprays were given as 93.5 L ha−1
with water at early flower or 2 weeks after flowering and repeated four times at
fortnightly intervals. Yields from the 4 K sources were 10% higher than the control
or unbuffered solution. Addition of surfactant (ethoxylated alkylaryl phosphate
esters) to KNO3 gave 5% more yields. Foliar application of 0.11 kg B ha−1 plus 4.1
kg K ha−1 increased the yield by 13%. Foliar K solution either buffered or combined
with B was a relatively inexpensive way to increase cotton yield. These treatments
in various combinations brought about returns eight to ten times the cost of the
chemicals used.
13.2.4 Response to Micronutrients
In Egypt, surveys were undertaken to identify crop nutritional problems during
1977–1995 and it showed that the crops in general suffered from micronutrient
deficiencies and responded very well to foliar supply of the nutrients resulting in
higher yields (Fawzi and El-Fouly 1998). The results of experiments with foliar
application of nutrients in cotton in Egypt and other countries were presented in an
interregional symposium (Oosterhuis 1997).
Iron is one of important micronutrients and foliar sprays of iron as chelates are
effective in correcting chlorosis. In a recent study, the interaction of FeHEDTA
given along with post-emergence broadleaf herbicides was examined (Franzen
et al. 2003). Three herbicides, acifluorfen, imazamox, and lactofen were applied
with or without FeHEDTA. At one location, Fe amendment lowered the yields with
acifluorfen and lactofen. But yields were higher with Fe in the imazamox combination,
although weed control was less effective. Therefore, the combination with herbicides
is not recommended, and the chelate alone is beneficial.
Recently there has been some renewed interest in foliar application of Zn
especially in view of increasing yield when given with bacterial fertilizers. Ebrahim
and Aly (2004) studied the effects of Zn foliar application along with soil biofertilization on wheat (Triticum aestvum cv. Sakha 155) plants grown for 70 days
in greenhouse under controlled conditions. Zn sprays were at 0, 25, 50, 100, 200
mg L−1 as ZnSO4.7H2O and the soil was inoculated with Azotobacter chroococcum
(Ar) and/or Azosporillum brasilense (Am) isolates. All test attributes namely,
mineral content, photosynthesis, metabolites, and dry matter accumulation, were
enhanced by Zn at 25 and 50 mg L−1, but at higher levels of 100 and 200 mg L−1
384
S. Kannan
these were reduced. The bio-fertilizers influenced the growth attributes, especially
more so when Ar and Am, than either Ar or Am were used, with the higher levels
of Zn. N, Mg, Mn, carbohydrates, and total soluble proteins were also increased in
the shoot. These treatments enhanced Chla+Chlb, photosynthetic activity, and IAA
concentration in the shoot. Spraying a by-product of olive oil on rice Oryza sativa
cv. Puntal increased the concentration of Fe, Cu, Zn, and Mn as well as the chlorophyll content, the grain yield, and grain protein content. The sprays enhanced the
uptake of N and K by the plants from the soil (Tejada and Gonzalez 2004). This
was because the by-product was not only rich in humic substances but also in both
macro and micronutrients.
A combination of two or more micronutrients in the spray has also been beneficial. In a pot trial, one-year-old apple trees were given a foliar spray containing
MnSO4, ZnO, “Solubar,” copper oxichloride and urea at rates respectively, of 1.0,
0.5, 1.0, 0.25, and 2.5 g L−1 water, and soil-applied fritted trace elements (FTE).
The carrier used (FTE-504Fe®) contained the micronutrients Mn, Zn, Cu, and
boron, and mixed with the growing medium of sand before planting, and was given
at 0, 100, and 200 g m−3 of sand. Where foliar sprays were given with soil FTE
at 100 g m−3, the total dry weight of the tree and that of the rootstock were significantly increased by 16% and 29% respectively over the control (Wooldridge
2002).
Response to foliar sprays of nutrient elements given at an appropriate time has
been recorded in a few crops. B and Zn sprays given during the “prebloom” stage
in apple yielded a very good crop (Stover et al. 1999). The treatments were given
on the basis of a hypothesis that the sprays may accelerate recovery of the vascular
tissue damaged by the cold winter. The following were the treatments: (1) sprays
of B (22.8 mM), (2) Zn-EDTA (0.75 mM), (3) B + Zn-EDTA, (4) Zn-EDTA + urea
(59.4 mM), (5) B + Zn-EDTA, (6) B, Zn-EDTA and urea. The treatments 1–5 were
given at prebloom at 0.5 in. green stage, and the sixth one at the pink stage. In all
treatments with B and Zn sprays, the yield was higher by 22–35% than the control.
The authors attributed the high yield to greater retention of flower buds which
would have abscised before anthesis but for the treatments.
There has been limited study on the spraying of elements which are not nutrients
per se. One such is titanium. The effect of foliar sprays of titanium (Ti) on vigor,
fruiting, and quality and the storage life of apple (Malus domestica Borkh) was examined (Wojcik and Klamkowski 2004). The experiment was carried out in 2000–2001
on mature “Szampion” apple trees. The trees were sprayed with TiCl4 solution at the
rate of 2.5 g ha−1: (1) before blooming at the stage of green and pink bud; (2) during
blooming, at the beginning of flowering and the petal fall; (3) after blooming, 1 and
3 weeks after petal fall; and (4) before fruit picking, 4 and 2 weeks before commercial harvest. However, the sprays did not affect the vigor, fruit set, yield, and
appearance. But it increased the leaf Ti, when given 30, 60, and 90 days after full
bloom. Ti sprays given before harvest and 90 days after bloom enhanced Ti content
in the leaf and fruit tissues. They did not get the desired anticipated effect of Ti
spray under conditions of optimum nutrition. When Ca was included in the spray
with Ti+4 ascorbate, the quality of plum was improved (Alcarez-Lopez et al. 2004).
13
Foliar Fertilization for Sustainable Crop Production
385
These authors sprayed soluble calcium (Ca) on plum trees in combination with two
bio-activators containing Ti+4 ascorbate alone or with marine algae extract, and
examined the commercial quality of fruits, with respect to their resistance to postharvest handling damage. They found that all the treatments containing Ti increased
tree development and fruit size. At harvest, the fruits from the Ti-sprayed trees
showed increased resistance to compression and penetration, but decreased the
weight loss during post-harvest storage. Furthermore, the external red color was
improved and the color parameters remained more stable during storage than in the
control. Ti significantly increased Ca, Fe, Cu, and Zn concentrations in both the
peel and the flesh. It was concluded that Ti facilitated greater absorption and translocation of minerals and the assimilation processes. Both the experiments gave
different effects of Ti sprays, which was due to the fruit trees tested, i.e., one is
apple and the other is plum.
13.2.5 Varietal Differences in Response to Foliar Application
The response of crop plants to foliar supply of nutrients has been different amongst
crop species as well as cultivars within the same species and has been well-documented
(for review see Kannan 1990). Here only a few are described. The differences in
poinsettia for Mo deficiency stress within cultivars were observed (Cox 1992). Of
the six cultivars studied, “Gross Supjibi” “Peace Regal Velvet” and “Peace Noel”
showed no deficiency symptoms when grown in minus-Mo nutrient medium and
thus are Mo deficiency-stress-tolerant. Similarly, there were varietal differences in
soybean for Zn-deficiency tolerance and they also responded to foliar Zn application
differently (Rose et al. 1981). Soybean crop was sprayed with ZnSO4 before flowering
and at one site, Narrabri, a single spray at 4 kg ha−1 gave 13% yield increase while
at another two sites Trangie and Breeza, two sprays increased the yield by 57% and
208% respectively. One of the varieties, Forrest was the most responsive to the
sprays. Results further revealed the differential sensitivity to Zn deficiency and
there was good response in crops even though they did not show any deficiency
symptoms.
The results of work described in this section provide evidence that the foliar
supply is effective in crop yield and also smaller amounts of nutrients can be given
instead of large amounts given to soil. A few of the conclusions are that N, P, and K
foliar sprays are effective especially when given at the appropriate time. Urea is transported and stored when given before the onset of fall in fruit trees. Foliar application
of N as post-pollination sprays of urea gave very good grain yield and highest grain
protein in cereals. However, it is not possible to supply the entire N requirement of a
crop through sprays. A 50:50 combination of soil and foliar fertilization has been
found to maintain tree productivity as also reduce soil pollution. Age of the leaf is
important; the younger leaves are capable of greater absorption than a mature leaf.
Results of foliar sprays of N, P, K, and S during the grain development stage in
soybean have been not uniform. Excessive soil supply of N induces deficiency of
386
S. Kannan
elements like K as obtained in cotton. Significant yield increases were obtained from
foliar sprays of K in such conditions. In many regions where there is periodic drought
which reduces K availability in the soil, foliar K has given significant increase in
grain yield in soybean. Sprays are effective in crops grown in clay soils where k is
bound by the clay complex. The case of muskmelon is interesting. During the fruit
growth soil fertilization of K was inadequate and K supplement through foliar sprays
was very effective in improving fruit quality. Foliar spraying of micronutrients has
been very effective in correcting deficiency, especially in Fe. There are differences
amongst crop cultivars in their response to foliar application of micronutrients.
13.3 Mechanisms of Foliar Absorption of Inorganic Nutrients
13.3.1 Leaf Components and Foliar Uptake: The Cuticle
The outer surface of the leaf is covered by a cuticle which envelopes the entire leaf
including the stomatal pores, epidermal hairs, or trichomes. In the periods of the
1960s, not much was understood on the nature of cuticle, and also in relation to its
function for solute transport. Much later, Wattendorff and Holloway (1980) studied
the structure of the cuticle of Agave americana L. and identified six layers: first, the
epicuticluar wax, then the cuticle proper embedded within an external and an internal
layer, and also an exterior and an interior cellin wall. But none of these layers have
distinct identities, since their boundaries merged with one another. The properties of
the cuticle are important for the nutrient uptake by the leaves. The formation
and development of the cuticle are continuous with the growth of the leaf or fruit.
The property of the cuticle is modified during ontogenesis. The cuticular wax of the
adaxial surface of apple leaves was analyzed for the chemical composition, micromorphology, and hydrophobicity just as the leaf unfolded (Bringe et al. 2006). With the
increasing age of the leaf, the hydrophobicity of the adaxial leaf surface decreased
significantly. The contact angle that is made between the leaf surface and the solute
droplets also decreased, thus facilitating greater absorption of solutes placed on the
leaf. It was also seen that the amount of apolar cuticular wax per unit area was lower
in the old leaf, 0.9 µg cm−2, while the young ones had higher amounts (1.5 µg cm−2).
This also indicates that older leaf will be less resistant to solute absorption assuming
that more wax would offer greater resistance to solute entry. The authors have
obtained evidence for the first time that the epicuticular wax contained tocopherol.
13.3.2 The Trichomes
The cuticular surface has structures referred to as “trichomes” which are uni-or
multicellular projections of different shapes. Trichomes and stomata occur between
ordinary epidermal cells which are also covered by cuticle.
13
Foliar Fertilization for Sustainable Crop Production
387
The thickness of the cuticular membrane varies with its location. It is thinner
over the periclinal walls and thicker between the anticlinal walls of the epidermal
cells. The cuticle undergoes changes in shape and structure and the deposition of
epicuticular wax continues with the growth of the organs (Miller 1986). Furthermore,
the cuticle remains hydrophilic in the early growth, but becomes hydrophobic with
maturity, and there is no further change when the growth ceases. The permeability
of the cuticle to solutes also varies with the development of these properties The
presence of an inner cuticle which forms a uniform layer on the inner periclinal
walls bordering substomatal cavities was observed (Pesacreta and Hasenstein
1999). This cuticle is continuous with the external one through the stomatal pores.
“Abaxial internal cuticle” refers to the cuticle surrounding the substomatal cavities
of the abaxial epidermis. Their observations showed that the internal and external
cuticles formed a continuous hydrophobic envelope around the epidermis excepting
the regions where it is connected to the underlying mesophyll parenchyma cells and
also over the midvein. The authors claim this as the first report on the existence of
an extensive internal cuticle. The physiological role of the internal cuticle may
perhaps be to prevent water loss. They also found that the epidermal cells secreted
cuticular material on their anticlinal and periclinal walls and the noncuticularized
region of the wall could function as the region for transmitting information on the
water potential of the leaf. In species with large islands of epidermal cells covered
by the internal cuticle, information to reach the guard cells would take a longer
time. Leaf internal cuticle has not previously been studied in detail, and yet its
existence has profound implications for the path of water movement. The cuticle
also plays an important physiological role during the development of fruit from the
time of fertilization. While it prevents water loss, it provides the barrier for any
infection by microorganisms. The development of the cuticle follows the same
pattern as that of the leaf. Dominguez et al. (2008) studied the tomato fruit cuticle
at the microscopic level during its growth and ripening and recorded the differences
in cuticle thickness and composition from the time of epidermal differentiation,
changes in the distribution of the lipid, pectin, and cellulose within, appearance of
pegs and cuticular invaginations, the thickness of the cuticle, and the polysaccharide
components. The amount of cuticle per surface area increased with the fruit development, reached its maximum in about 15 days after anthesis, and then remained
constant till the fruit ripening. There was also loss of polysaccharides from the
cuticle, beginning with the ripening of the fruit till the development of red color.
The chemical composition of the cuticle would greatly influence its permeability to
solutes.
The cuticular composition plays an important role in its permeability properties.
However, it is redundant to discuss the cuticular composition studied by several
workers recently. A brief mention is made here. Wen et al. (2006) examined the
leaves of Taxus baccata L., which comprised needles covered with tubular epicuticular waxes which varied in diameters and lengths. The cuticular wax was a
mixture of long chain fatty acids, phenyl esters, alkanes, and tocopeherols. While
the epicuticular layer had aldehydes and alkanes, the intracuticular wax had higher
amounts of cyclic constituents. These could help explain the differences in the rates
of permeability of polar and nonpolar solutes. The formation of the tubular crystals
388
S. Kannan
on the cuticles as a spontaneous physico-chemical process may be relevant with
respect to the establishment of gradients between the epi- and intracuticular wax
layers and local phase separation of solutes.
Several features of the trichomes have been recorded (Grauke et al. 1987).
The bulbous base of the trichome extends over the entire thickness of the epidermal
cells, with the basal accessory cells bulging around the trichome. The cuticle development at the base of the trichomes is less than in the rest of the regions of the
trichomes, and greater absorption of solutes is likely through these basal regions, a
feature favorable for better foliar uptake by the leaves. It is found that in the leaf of
Cannabis, new initials of trichomes arise regularly, maintaining a nearly constant
density. The presence of four morphologically and ontogenetically different
glandular and non-glandular trichome types and a bristle hair type have been
established recently (Kolb and Müller 2004). They found that all these four types
secreted lipids, flavones, and terpenes and some cell wall components. The changes
in the trichomes during leaf development, especially the number of trichomes and
the composition of the exudates have also been investigated (Valkama et al. 2004).
Density of both glandular and non-glandular trichomes decreased drastically with
leaf expansion, although their numbers per leaf remained constant, showing that the
final number in a mature leaf is established early in time. However, the functional
role of trichomes are likely most important at the early stages of leaf development.
Perhaps this property may explain the differences in foliar uptake of different ages
of the plant leaves.
13.3.3 Pores and Ectoteichodes
The existence of wax-exuding pores and channels in the cuticle was postulated long
ago and even the existence of anastomosing microchannels for the extrusion of wax.
The presence of pores and canals in the dewaxed leaf stem and fruit cuticles was
revealed through photomicrographs (Miller 1986). The transcuticular canals are
found oriented perpendicular to the outer and inner membrane surfaces and terminate
as discrete pores, in the adaxial leaf cuticles of Hoya carmosa. The presence of giant
pores in the cuticles has been recently identified in certain plants found in Australian
Wet Tropics (Carpenter et al. 2007). The pores are large in diameter and ubiquitous,
not previously recorded in leaf cuticles. Such structures have been found in Eidothea
zoexylocarya, about 1 mm in diameter that extend perpendicular to most of the way
through the cuticle from inside. They also observed that these occurred on both sides
of the leaf, but were significantly absent in the cuticle associated with stomatal
complexes on the abaxial surface. The pores on both the abaxial and adaxial inner
cuticular surfaces were present on all specimens of E. zoexylocarya, although their
positions could not be discerned on the outer cuticle surface using SEM. The pores
were abundant (1.2 × 105 mm−2) in the cuticle associated with the normal epidermal
cells. On the abaxial surface these were absent from the cuticle associated with the
guard cells and the subsidiary cells, as also in the cuticle overlying the cell immediately
13
Foliar Fertilization for Sustainable Crop Production
389
Fig. 13.1 Adaxial transverse leaf section of Eidothea zoexylocarya showing the pores extending
perpendicularly down through the cuticle (Reproduced with the kind permission of the authors
(Carpenter et al. 2007) and the editor American Journal of Botany)
lateral to the subsidiary cells. In the surface view through the light microscope, the
pores appeared as canals penetrating across the cuticle. Transverse view of the
cuticle showed the pores reaching nearly all the way through the 4–8-µm thick
cuticles from the inside. Pore diameters were nearly uniform in diameter, and were
mostly perpendicular to the leaf surface. The conductance of the astomatous cuticular
leaf surface was measured to find if they are more leaky to water vapor, and it was
however very low, suggesting no role in the conductance of water vapor. Their studies
did not provide any role for these cuticular pores, either in the transport of water or
solutes, however (Fig. 13.1).
Structures in the cell wall of wheat leaves, named “Ectoteichodes” were identified
and considered as pathways for solute transport across the cell walls, and the permeability of ions through the cuticle is also considered to be facilitated by these
structures which were visible microscopically (Franke 1971). Ectodesmata or
ectoteichodes were demonstrated in epidermal walls of mesophytic plant species
using methods of fixation with Gilson solution (Schönherr and Bukovac 1970).
Whole leaves or leaf segments were fixed for 12 h at 38°C and the epidermis was
stripped off, washed in 30% ethanol to remove HgCl2, treated with potassium
iodide for 5–10 min, and then stained with pyoktanin and the tissue was then
examined microscopically. After this procedure, ectodesmata appeared as dark
bands from the cuticle toward the protoplast of the epidermal cells. If potassium
iodide and pyoktanin were omitted from the treatment, ectodesmata appeared
crystalline and birefringent, in polarized light. Cuticles over anticlinal walls form
plenty of ectodesmata, while they are rarely found over periclinal walls. The effect
of removing waxes on the distribution pattern of ectodesmata indicated that waxy
domains are impermeable to HgCl2 even though it dissolved in benzene. Perhaps
crystalline wax domains are impermeable to HgCl2 while amorphous lipids are not.
This would imply that ectodesmata are formed in the cell wall wherever cuticular
waxes are in the amorphous state and crystalline waxes are scarce. The authors are
not fully convinced that ectoteichodes are discrete entities in the cuticles but could
form under the influence of some treatments.
390
S. Kannan
13.3.4 Cuticular Permeability of Nutrients
Perhaps the most important function of the cuticle is to protect the plant from desiccation by preventing the loss of moisture from the leaf surface. However, it is not
impermeable to water and water is lost to some extent through cuticular transpiration.
The sorption and retention of water is an important property of the cuticle. Chamel
et al. (2006) measured the sorption of water by cuticular membranes isolated from
leaves over a wide range of relative humidity using a “magnetic suspension
microbalance.” The sorption isotherms were not linear but increased more rapidly
at higher values of relative humidity. The water content was measured for a
few species at 80–99% and it ranged from 1.1% to 7.7% of the dehydrated weight.
The sorption did not decrease even after extracting the soluble cuticular lipids from
the cuticle. This may partially explain how the humidity favors foliar absorption of
aqueous solutions.
The permeability properties have been studied with the help of radioisotopes
using cuticular membranes isolated enzymically from the leaves and fruits in
several laboratories in the early 1960s and later in the 1980s. Penetration studies
and ion-binding properties of enzymically isolated cuticular membranes were
carried out using special apparatus and radioisotopes in the 1960s. Cuticles from
the adaxial surfaces of grapefruit leaves were isolated (Orbovic et al. 2001) and the
movement of 14C-labeled urea was measured for several hours, using a “dose diffusion”
system developed by them. It was found that within the first 4–6 h of application,
the rate of penetration increased with the increase in temperatures from 19°C upto
28°C, and other factors, viz., relative humidity, cuticle thickness, and the contact
angle of the droplets placed on the cuticle surface all influenced the penetration.
The same group (Bondada et al. 2006) made further studies on penetration of
14
C-labeled urea from the upper cuticular surface to the inner side and it was found
to follow asymptotic curve, with an initial lag phase of about 10 min, and a quasilinear phase reaching a rate of 2% h−1, then a plateau at 144 h. The total
amount penetrated was 35%, and the rate decreased with the thickness of the
cuticle. They found the epicuticular wax appeared as platelets which increased with
the leaf age. Furthermore, dewaxing the cuticles increased the rates of penetration
of urea with the maximum of 64%. The findings on the citrus leaf cuticles are
important with respect to determining the time of foliar fertilization.
The permeability of the astomatous cuticular membranes of Populus canescens
leaves to nutrient ions has been investigated in detail (Schönherr and Schreiber
2004). These leaves have trichomes when very young, but these are shed with the
growth of leaves to full size. Cuticles enzymically isolated from the adaxial
surfaces of fully expanded leaves were used. The ionized Ca salts with anhydrous
molecular weights ranging from 111 to 755 g mol−1 were employed. The penetration
was found to be a first-order process with the rate constants (k) decreasing
exponentially with mol. wt. They concluded that there were differences between
the diffusion of large ionic species through the aqueous pores (polar pathway) and that
for neutral solutes diffusing through cutin and waxes (lipophylic pathway), and
recommended the formulation of large solutes as ionic species for effective sprays.
13
Foliar Fertilization for Sustainable Crop Production
391
Further research on the polar paths of diffusion of ions revealed that ions penetrated
cuticles via water-filled pores and the cuticle covering the stomata and trichomes
served as preferential sites for ion entry (Schreiber 2005). They have given a future
direction of research in entry of solutes through cuticles. The chemical nature of
these polar domains have yet to be characterized, as it is important in agriculture,
since polar diffusion is the most important and faster route for the entry into the leaf
and later translocation of the nutrients. The study relating to cuticular entry has
great significance now more than ever before, since many compounds which are
used for developing the transgenic plants are ionic, and should be suitable for
penetrating through the cuticle. Plants in the field are in several places exposed to
acid precipitation with the pH of the pollutant reaching to values of 4 and below.
However, the leaf tissues are affected only when the leaf cuticle permits the entry
of the ions.
The information about the cuticles and their permeability properties as revealed
by several studies made earlier have been summarized recently (Kerstiens 2006).
There have been major advances on the quantification of cuticular permeability to
water and its dependence on leaf temperature. The roles of epicuticular and intracuticular waxes as also the aqueous pores have been examined. But the differences in
permeability properties of cuticles amongst the plants remain a big challenge. The
water transport in lipophilic pathways and the aqueous pores depend on the humidity
and temperature. Cuticles are considered to act as solution-diffusion membranes for
the entry of water. Kerstiens concludes that many ecophysiologically relevant
questions remain unanswered. Some of these are: What influences the composition
and formation of different forms wax, and how does it affect the cuticular permeability? “What is the temperature dependence of ‘P’ in situ? How large is lateral
variability in P at the cellular and subcellular levels, and how does it affect stomatal
behavior?” A new term is introduced as P which is the cuticular permeability to
water characterized by the variable permeance (P), and is the ratio of water flow
rate density to driving force, the latter being expressed as a concentration difference.
Schönherr and his group had carried out extensive research on the permeability
properties of cuticles over 3 decades. In one such study, the penetration of 54Ca
labeled CaCl2 by the upper and lower surfaces of apple, pear, bean, and corn leaves
was measured using the leaf disks of these plants (Schlegel and Schönherr 2002).
Very significant observations were made. It was found that the penetration of ions
was slower across astomatous leaf surface than through the stomatous one, and the
half-time for penetration through the latter ranged from 0.5 to 9 h. This and other
findings led them to conclude that initial entry of solutes was through stomata, but
further penetration was across the cuticle serving as the major pathway. The appearance
of black silver precipitates in the cuticle present inside and over the guard cells, as
also in the trichomes and the cuticle surrounding their base, proved that the ionic
species essentially entered into the leaf via the same route, i.e., the cuticle present
all over the leaf. Schönherr (2002) examined permeability of salts of Ca and K
which have hydration shells and found that both cations and anions entered the
cuticles in equivalent amounts by diffusion through the aqueous pores and is influenced by humidity and the hygroscopicity of the salts. The point of deliquescence
of the salts is important for the diffusion. Nitrates and chlorides of Ca and Mg,
392
S. Kannan
and K2CO3 have greater permeability but not salts like nitrates and phosphates of
K. The driving force for the diffusion is the concentration difference across the
cuticular membrane and most of the nutrient salts excepting MgCl2 have high
aqueous solubility and thus have greater permeability. Humidity is very important
which increases the solubility and therefore spraying is most effective if given in
the evenings.
Schreiber and Kerstiens (2006) described the work of Schönherr and his group
and about the papers presented in a week-long symposium held near Izmir in
Turkey on the occasion of his 65th birthday and retirement in March 2005. Former
students and colleagues are now working in Germany, Switzerland, and the UK, on
various aspects of transport across cutinized and suberized barriers present in the
cuticles. “One person who has immensely improved our understanding of such
transport barriers is Professor Jörg Schönherr. Since the 1970s he has been investigating the transport properties of cutinized and suberized barriers at the plant/air
interface from 1970s. His group focused initially on ecophysiological questions,
dealing with water permeability, and then turned on to the ecotoxicological and
agronomic questions of the uptake of xenobiotics and agrochemicals into leaves. In
the last few years, Schőnherr’s contribution to our knowledge on the cuticular components, and their permeability to agrochemicals have been remarkable and have
been acknowledged by several workers, particularly Schreiber and Kerstiens.
Schőnherr’s research group have been investigating the transport across the cutinized and suberized barriers at the plant-air interface from 1970s and have greatly
enhanced our understanding of foliar uptake of polar compounds, viz., ions and
hydrophilic organic molecules state Schreiber and Kerstiens. It has been shown that
the cuticle over the trichomes and guard cells differs in structure and permeability
over the rest of that covering the leaf. Ions are lipid-insoluble and therefore enter
through an aqueous pathway present in the cuticles. Aqueous pores are largely present
in the cuticular ledges, at the base of trichomes, and also in the cuticles present over
anticlinal walls. Permeability of cuticles to ions depends on humidity and reaches
the maximum at 100% humidity. Wetting agents increased the rates of penetration,
indicating that the pore openings are surrounded by waxes. The pores in cuticular
ledges of Helxine soleirolii allowed the entry of high molecular weight compounds,
viz., berberine sulfate (MW 769 g mol−1). And finally, Schreiber and Kerstiens suggest a method for the future quantification of changes in leaf or stem surface barrier
properties of transgenic plants with modified cutin and/or wax biosynthesis. The set
of papers presented in the meeting and published in the journal of botany documents the advances in understanding barrier properties of cutinized and suberized
barriers of plants that have been achieved within the last couple of decades.
Recently the biochemistry of cuticular wax formation by the epidermal cells mainly
studied in Arabidopsis thaliana and complemented with those obtained from other
plant species, has been reviewed by Samuels et al. (2008). The plant cuticle
is described as a hydrophobic layer covering the epidermis and forming a continuous
seal over the outer walls of the epidermal pavement, guard, and trichome cells.
The ultrastructure of the cuticle varies widely among plant species, organ types,
and the developmental states. It ranges from a procuticle on emerging organs to a
mature one that gets completed after tissue expansion has ceased. All cuticles fall
13
Foliar Fertilization for Sustainable Crop Production
393
into two types of highly lipophilic substances, viz., (1) cutin and (2) cuticular wax.
Because of the covalent linkages between its monomers, cutin offers resistance to
mechanical damage, for example, the leaf itself. The cuticular wax is monomeric
and can be extracted by organic solvents. Its main function is to prevent nonstomatal water loss, one of the key adaptations in the evolution of land plants.
This chapter discusses leaf components such as cuticular membranes, trichomes,
cuticular pores, the presence of Ectoteichodes, and their properties and their role in
nutrient transport into the plant leaf. Cuticles are permeable to nutrient ions present
in aqueous forms and it is not known if the cuticular pores facilitate easy entry into
the leaf cells. The trichomes increase the amount transported into the leaf by
providing more area for absorption. All cuticles have two types of lipophilic
substances, the cutin and the cuticular wax, which influence the permeability of the
cuticles to nutrient ions to varying degrees.
13.4 Pathways of Nutrients Following Foliar Uptake
Foliar absorption of inorganic nutrients involves a number of steps. The ions after
passing through the cuticular membranes gain entry into the leaf cells. This process
is mediated by energy and is similar to the absorption by root cells. Many micronutrients which are easily supplied to the plants through foliage for correction of
the deficiency, behave differently with regard to the absorption compared to the
major nutrients like N, P, and K. Some are easily mobile and others less so. Zinc
comes under the less freely mobile element. The uptake pattern of Zn was measured
using 65Zn, in both intact and detached leaves of pistachio and walnut (Zhang and
Brown 1999). They found that the mature leaves of pistachio and walnut retained
8% and 12% of the amount applied on the leaves and about half of these moved into
the leaves and translocated out of the applied area. There were differences in the
absorption amongst the age of the leaves especially in pistachio, in which the
immature (young) leaves absorbed more than the older ones. Such differences were
not obtained in walnut leaves. The uptake was higher at pH 3.5 and decreased with
rise in pH in pistachio, while no significant difference was noticed with walnut.
Furthermore, the uptake was not influenced either by light or by the metabolic
inhibitors, suggesting that the process is a passive one. These are significant findings
on the mechanism of foliar uptake of Zn.
13.4.1 Transport of Nutrients in and out of the Leaf
After passing through the cuticular membranes, the nutrient ions enter the epidermal
cells and the mesophylls beneath. The space between the leaf cells forms a
continuum, thus providing the “free space” or apoplast. The free space is relatively
small and varies for different plant leaves. This accounts for about 3–5% of the total
volume in the leaf tissue of wheat (Crowdy and Tanton 1970). The apoplastic
concentrations of K and Ca in the regions adjoining the guard cells of Commelina
394
S. Kannan
communis were high, ranging from 50 to 75 mol m−3 for K+ and 0·05–4 mol.m−3 for
Ca2+ (DeSilva et al. 2006). These two cations play an important role and contribute
significantly to the intracellular signaling and response of the guard cells toward the
changes in stomatal aperture.
The ions after passing through the cuticular membranes gain entry into the leaf
cells. This process is mediated by energy and is similar to the absorption by root
cells. It is necessary to understand therefore the steps involved in the foliar uptake
of nutrient elements which are reviewed in the following sections. While the major
nutrient elements are taken up readily and transported to other parts, the micronutrients behave differently. Some are easily mobile and others less so. Zinc comes
under the less freely mobile element. The uptake pattern of Zn was measured using
65
Zn, in both intact and detached leaves of pistachio and walnut (Zhang and Brown
1999). They found that the mature leaves of pistachio and walnut retained 8%
and 12% of the amount applied on the leaves and about half of these moved into
the leaves and translocated out of the applied area. There were differences in
the absorption amongst the age of the leaves and also plant species. In pistachio,
the immature (young) leaves absorbed more than the older ones. But such differences
were not obtained in walnut leaves. The uptake was higher at pH 3.5 and decreased
with rise in pH in pistachio, while it was not influenced either by light or by the
metabolic inhibitors, suggesting that the process is a passive one. However, no
significant difference was noticed with walnut with respect to the pH.
The nutrients take two routes to reach the vascular tissues for transport to other
parts and one is the apoplast as mentioned earlier. The second route is the transport
through the symplast, which takes place between the cells through the cytoplasmic
continuum. The mechanisms of apoplastic and symplastic transport of ions are not
fully understood, and our knowledge is largely a conjecture and assumed to be
similar to the transport of assimilates from the leaf cells. Structures like “plasmatubule”
in the transfer cells of leaf minor veins of Pisum sativum L. have been associated
with the transfer of solutes between the leaf cells and then to vascular systems
(Harris and Chaffey 1985). Plasmatubules were found in the transfer cells and the
specific distribution of the plasmatubules reflected further membrane amplification
within the transfer cells for the movement of solute from apoplast to symplast.
Plasmatubules appeared as tubular evaginations of the plasmalemma and are
found in the regions of high solute flux between apoplast and symplast (Chaffey
and Harris 1985). Franceschi and Giaquinta (1983) also identified a highly specialized
layer, called the paraveinal mesophyll (PVM) in the leaves of some legumes.
The PVM is a one-cell layer forming a network in the phloem region, and are nonphotosynthetic tissues interspersed between the palisade and spongy mesophylls.
It is positioned in such a way that the photosynthates produced passed through this
region before reaching the phloem.
The cell-to-cell communication in leaves was studied using fluorescent probes,
e.g., 6-carboxyfluoroscein and Lucifer yellow CH, which do not pass through
plasmalemma and are thus ideal to reveal the nonplasmatic connections (Erwee et al.
1985). The dye moved freely in the epidermal cells of Commelina cyanea, showing
that they are symplastically linked, as are those between the mesophylls cells.
13
Foliar Fertilization for Sustainable Crop Production
395
Fig. 13.2 Diagrammatic presentation of the epidermal cells with stomata, guard cells, and the
plasmadesmatic connections between them and guard cells. Thus, ions like K absorbed by guard
cells move between the guard cells but not into the epidermal cells. Note the lack of symplastic
connections between the epidermal cells (Drawn after Erwee et al. 1985)
But injection of the dye into the epidermal cells of the leaves of Vicia faba and
Anthephora pubescens showed poor symplastic connection between the guard cells
and epidermal cells. Mesophyll cells are well linked by plasmadesmata (Ringoet
et al. 1971). Erwee et al. (1985) made an important finding that the guard cells
themselves are isolated from cell-to-cell communication with the epidermal cells
in the leaves. Thus, ions such as K absorbed by guard cells move between the
guard cells, but not the epidermal cells, due to the lack of sympastic connections
(Fig. 13.2).
Similar study on the movement of Lucifer Yellow introduced into the leaf was
followed by fluorescence microscopy (Farrar et al. 1992). They found that dye
transfer from mesophyll cells into the parenchymatous bundle sheath (PBS) and
from PBS to mesophyll sheath occurred readily. In another experiment when fluorescent peptides and dextrans were injected into the cytoplasm and cortical endomembrane network of the epidermal cells of Nicotiana tabacum and Torenia
fournieri, the endomembrane network was similar to the endoplasmic reticulum
and no cell-to-cell movement of dextrans injected into the cytoplasm was obtained
(Cantrill et al. 1999). Thus it was concluded that the endoplasmic reticulum acted
as a pathway for intercellular communication through the desmotubule and plasmadesmata. In another experiment, “thin cell layer explants” of tobacco were
cultured to produce adventitious vegetative shoots and a fluorescein isothiocyanatelabeled peptide (F(Glu)3 MW 799) was microinjected on the epidermal cells to
assess the permeability of the symplast during the adventitious shoot regeneration.
A period of increased symplastic movement of the dye was detected and was
greater in the regenerating layers than in the nonregenerating TCLs. This led to the
conclusion that the symplastic linkage was reinitiated with the first line of cell
divisions (Cantrill et al. 2001). From the point of view of the ion movement within
the leaf tissues, symplastic transport is established.
396
S. Kannan
13.4.2 Transport of Foliar Applied Nutrients to Other Plant
Parts
The nutrients reach the apoplasts after penetrating the cuticular membranes of the
leaf surface and are absorbed by the leaf cells. The apoplasts and the symplasts are
common to the ions absorbed either from the foliar sprays or by the roots and transported to the leaf in the normal course. It is therefore likely that the apoplast plays
a major role in the various intercellular processes, viz., water as well as nutrient
distribution. There have been a few studies on the long-distance transport of nutrients
from the sprayed leaves to other parts. The transport of micronutrients, viz., Fe, Mn,
and Zn is generally much slower than N, P, or K. These in chelated forms are transported more readily to other parts. Bukovac and Wittwer (1957) used radioisotopes
and classified the rates of mobility of the elements in the following order: Freely
mobile K, Na, P, Cl, and S; partially mobile are Fe, Mn, Zn, Cu, and Mo; and
immobile are Ca and Mg. Ca is very important for the development of fruits.
However, it is absorbed directly by the fruits, and foliar spraying on the plants to
cover the fruit surfaces is the best method for correcting Ca deficiency. There have
been two significant contributions to transport of foliar-applied nutrients. One is the
movement of anion 36Cl which was applied to a leaf of Tradescantia viridis and
transport to the leaves above and below as well as the stem portions between the
leaves was followed (Penot and Gallou 1977). They found large amount transported
to the new leaf (bud leaf No.1) and to the stem No.1. However, larger amount was
still found in the applied leaf. The data showed that the anion is rapidly transported
more or less evenly to all leaves and stem above and below the applied leaf and also
to the root, over a period of 3 h (Fig. 13.3). Another finding relates to the transport
of relatively less mobile micronutrient Zn and very little is known about its transport
from leaves to other plant organs. A few forms of Zn for suitability to provide
enough Zn were examined in wheat Triticum aestivum (Haslett et al. 2001). 65Zn
was applied to either leaves or to the root and the transport was followed. The forms
were ZnO, ZnSO4, Zn chelates. Foliar supply of Zn in general increased its content
in shoot. It was translocated to leaves above and below the treated leaf as well as to
the toot tips. Their experiment by girdling the stem proved that Zn was transported
from the leaves to the roots via the phloem.
The most important nutrient given as spray is N which has the advantage of great
mobility in plants. The findings of Okano et al. (1983, 1984) are significant. The
translocation of 13C and 15N from the spray was very similar. N was transferred very
rapidly in the first few hours and continued for 8 days. Both 13C and 15N moved
together in the bulk stream of the phloem of the rice plant. N transport was examined
by Tatsumi and Kono (1981). They found that 25% of N applied was translocated
from the upper leaf to the roots. The study with fruit trees by Zilkah et al. (1987)
revealed that foliar applied urea moved basipetally from the current flush of leaves
to the developing fruits which acted as the “sink” for N.
From the foregoing discussion it is clear that nutrients reach the leaf cells, after
penetrating the cuticle, and are further transported from them to other parts through
13
Foliar Fertilization for Sustainable Crop Production
397
Fig. 13.3 Acropetal transport of 36Cl from the supplied leaf to other leaves above and below in
Tradescantia viridis. The amount of Cl found after 3 h of application, in the leaves are given as %
(Redrawn after Penot and Gallou 1977)
plasmadesmata. Some micronutrients are not as freely mobile as the major nutrient
elements like N, P, or K. The age of the leaf and the pH of the spray liquid are
important for foliar absorption. Significant is the absence of plasmadesmatic
connections between the guard cells and the epidermal cells. One element Cl has
been found to be transported from the applied leaf to other parts rapidly, showing
it is freely mobile. This should be true to many anions.
13.5 Foliar Nutrition and the Law of the Maximum
The resources needed for raising the food production are good soil, adequate water,
and fertilizers. The land is becoming increasingly limited and all efforts should be
made to raise the yield levels on the existing agricultural lands. To meet the food
demands, the average yield of all cereals must be increased by 80%. Furthermore,
using the currently available technologies, yields can be doubled in the Indian subcontinent, Latin America, and East European countries, and by 100–200% in sub-Saharan
Africa, if three conditions, viz., political stability, entrepreneurial freedom, and all the
production inputs are guaranteed. More food can be produced if new lands, i.e., lands
that are hitherto considered unfit for supporting crops, are brought under plough.
398
S. Kannan
Wallace and Wallace (2003) have discussed various methods for increasing crop
production, and introduced the concept of “The Law of the Maximum” for closing
the crop-yield gap. They have extrapolated both the concepts of the Liebig’s Law
of the Minimum and Mitscherlich’s law of the Minimum and discussed them in his
small book. “The greatest response for any one input is obtained when very few
limits remain. Input factors interact to multiply the value of the other when other
limiting factors are corrected. Limiting factors are multiple, and their interactions,
which can be graphed to give Multiple Action Yield Fraction plots, determine final
yields. The MAYF may be used to maximize specific aspects of crop production,
such as per unit of land or per unit of irrigation water.” They have listed salient
points needed for consideration to close the gap to achieve high yields: Increasing
the MAYF by adding N, P, and K may be difficult because the Sufficiently Values
of each may already be near 1.00. Attention to non-NPK factors is probably necessary
for further improvement. Some non-NPK factors are quantity of soil, water,
soil availability; many aspects of crop management are other possible limitations.
The Law of the Maximum also requires attention to non-NPK factors. In this
respect, foliar supply of a nutrient which imposes the limit to yield rise, becomes
relevant. For example, as the yield at one stage reaches the plateau, it implies some
nutrient is needed at that growth stage or fruiting stage. Supplying that by the roots
will not reach the shoot for use in fruiting. Citing a case of cotton, K sprays at boll
formation promptly respond to the timely need, and the yield is increased. Similarly,
during the “seed-filling” period of soybean crop, N supply through sprays has
been effective. Autumn sprays of N for fruit trees provide the nutrient when the
new flush in spring season begins. Soil supply in these cases is less effective.
This causes the yield to rise above the plateau. An interesting case is with regard to
the increase in the atmospheric carbon dioxide, which happens with the burning of
fossil fuel. This can be viewed as an excess of one nutrient, making some essential
nutrient elements insufficient. It was found recently that supplying NO in the
gaseous form increases crop yield and quality especially when atmospheric CO2 is
increased. Jin et al. (2009) grew spinach plant (Spinacia oleracea cv. Huangjia) in
closed growth chamber to investigate the effects of gaseous NO application on
vegetable production in greenhouses. Treatment of low concentration of NO gas
(ambient atmosphere with 200 nL L−1 NO gas) significantly increased the shoot
biomass of the soil-cultivated plants as compared with the control treatment (ambient
atmosphere). In addition, the NO treatment also increased the photosynthetic rate
of leaves, indicating that the enhancement of photosynthesis is an important reason
leading to more biomass accumulation induced by NO gas. Furthermore, the NO
treatment decreased the nitrate concentration and increased the amount of soluble
sugar, protein, antioxidants like vitamin C, glutathione, and flavonoids, and ferricreducing antioxidant power (FRAP) in shoots of the plants grown in soil, suggesting
that the gaseous NO treatment can not only increase vegetable production but also
improve vegetable quality. In addition, the effects of the combined application of
NO and CO2 (NO 200 nL L−1 and CO2 800 mL L−1) on shoot biomass was even
greater than the effects of elevated CO2 (CO2 800 mL L−1) or the NO treatment
alone, implying that gaseous NO treatment can be used in CO2-elevated greenhouses as an effective strategy in improving vegetable production.
13
Foliar Fertilization for Sustainable Crop Production
399
13.6 Foliar Nutrition Through Sprinkler Irrigation
The development of drip-irrigation technology in 1960s opened the doors for the
greatest advancement in fertilizer management especially for vegetables. Early work
for example, in Israel (Bar-Yosef 1977) and later in other countries formed some of
the basis for the water-management technology that is used today. Drip irrigation led
to improvements in water application efficiencies and also reduced the amount of
water used for many vegetables by 50–70% (Clark 1992). Furthermore, the reduction
in water application has positive implications for nutrient efficiencies, especially N
since it is closely related to irrigation efficiency in sandy soil production areas
(Hochmuth 2000). Fertilizer materials could be injected into the drip irrigation system,
a process referred to as “fertigation.” Soluble nutrients such as N and K are supplied
through drip irrigation by injecting small amounts and are also regulated according to
the seasonal crop requirement. Schedules for such injections were developed in
Florida and other southern states (Cook and Sanders 1991). Water conservation technology has also been developed using many advanced technologies and remote
monitoring with computers. One recent advancement is described below.
Writing on the ARS role to help conserve the vital resource for agriculture, Evans
(2007) has presented a new system called “Wireless Watering.” (Fig. 13.4). He states
Fig. 13.4 Wireless Watering: The picture shows in-field sensing stations monitor soil moisture
and soil and air temperatures. All in-field data are sent wirelessly to the base station for determining the precise timing for irrigation. The base station communicates back and forth with the
mobile irrigation cart and the grower, who controls the station. This picture is included in this
review to propose that nutrients could be given through the sprinkler water (Credit: Robert Evans,
USDA-ARS Northern Plains Agricultural Research Laboratory, 1500 North Central Ave.,m
Sidney, MT 433–5038. Picture from Agricultural Research July 2007 page 6)
400
S. Kannan
that worldwide, irrigation is the largest single consumer of freshwater, using up to 60%
of this precious resource, and most of this is for growing food, animal feed, fiber, and
fuel crops. Evans and Kim, who designed and integrated the wireless components, are
still evaluating the full benefit of this system on the water saving, and also conserving
fertilizers. This will help reduce the pollution of the groundwater and soil. They further
state that if irrigation farming is to be profitable in future, such kind of innovations is
important. Evans says: “Before, we were focused on how much productivity we could
extract from a unit of land, now it is time to start thinking about how much we can
wring from each unit of water consumed during the production process.” Evans’ idea
can be further extended for the fertilizer application through foliar sprays.
13.7 Conclusion
The results of several studies discussed above reveal that foliar feeding is a practical
method to provide nutrients to plants. However, there are limitations. The leaf area
needed to accept the foliar sprays is the first requirement. Crops like sugarcane, plantation crops, and fruit trees satisfy this requirement. The absorptive capacity and
effective transport from the leaf to other parts are important. Major nutrients could
be given as sprays for providing the crops during “critical” periods like “grain filling”
when the nutrients are needed the most for grain development. In such cases, soil
application would take a longer time to reach the “sink” regions.
Soil fertilization often results in over-fertilzation. As an example, increased
nitrate content in the soil frequently leads to undesirable changes in the vegetation
compositon, since higher content in the edible plant parts is dangerous to human
health. Foliar sprays are very effective in crops grown on degraded soil. Urea given
as sprays to alfalfa grown in a freshly exposed coal mine spoil have given high
yields. These reports have been discussed in this review.
Ecosystems receiving more nitrogen than is required by the plants are known as
“nitrogen-saturated.” Such a situation contributes to both inorganic and organic
nitrogen to freshwater. The chemical forms of N also cause serious concern with
regard to the eutrophication. This is also the case with increased levels of phosphorus.
Phosphates are less soluble than nitrates, and high amounts of phosphates inhibit the
uptake of other elements. Foliar feeding of agricultural crops is now practicable and
is practiced for N and most of the micronutrients like Fe and Zn which are given for
correction of the deficiency as it is manifested late in the plant growth. As mentioned
earlier, foliar sprays cannot substitute soil fertilization in all cases. But it can supplement
soil application, and can be introduced in sprinkler irrigation system.
References
Bi G, Scagel C (2007) Nitrogen foliar feeding has advantages. Nurs Manage Prod 23(3):43–46
Chamel A, Pineri M, Escoubes M (2006) Quantitative determination of water sorption by plant
cuticles. Plant Cell Environ 14:87–95. DOI: 10.1111/j.1365-3040.1991.tb01374.x
13
Foliar Fertilization for Sustainable Crop Production
401
Dominguez E, López-Casado G, Cuartero J, Heredia A (2008) Development of fruit cuticle in cherry
tomato (Solanum lycopersicum). Functional Plant Biol 35:403–411. doi: 10.1071/FP08018
Ebrahim MKH, Aly MM (2005) Physiological response of wheat to foliar application of zinc and
inoculation with some bacterial fertilizers. J Plant Nutrition 27:1859–1874. DOI: 10.1081/
PLN-200026442
Eid ET, Abel-Al MH, Ismail MS, Wassel OMM (1997) Response of Egyptian cotton to potassium
and micronutrient application. In: Proceedings of FAO-Inter-regional cooperative research
network on cotton (IRCRNC). National Research Centre (NRC), Cairo, Egypt, pp 139–145
Erwee MG, Goodwin PB, Vanbel AJE (2006) Cell-cell communication in the leaves of Commellna
cyanea and other plants. Plant Cell Environ 8(3):173–178. DOI 10.1111/j/1365-3040.1985.
tb01383.x
Evans R (2007) Wireless watering: new irrigation technologies from ARS can help conserve a
vital resource. Agric Res July:6–7
Fawzi FA, El-Fouly MM (1998) Some practical aspects of using foliar micronutrient fertilizers in
Egypt. In: El-Fouly MM, Abdullah FE, Abdel-Maguid AA (eds) Proceedings of symposium
on “foliar fertilization: a technique to improve production and decrease pollution”. NRC,
Cairo, Egypt, pp 17–22, 10–14 Dec 1995
Fernández V, Eichert T (2009) Uptake of hydrophilic solutes through plant leaves: current state of
knowledge and perspectives of foliar fertilization. Crit Rev Plant Sci 28: 36–68. DOI: 10.1080/
07352680902743069
Franceschi VR, Giaquinta RT (1983) The paraveinal mesophyl, of soybean leaves in relation to
assimilate transfer and compartmentation. Planta 157:422–431. DOI: 10.1007/BF00397199
Gilbert GS, Handelsman J, Parke JL (1994) Root camouflage and disease control. Phytopathology
84:222–225. doi: 10.1094/Phyto-84-222
Hristozkova M, Geneva M, Stancheva I (2006) Response of inoculated pea plants (Pisum sativum L.)
to root and foliar fertilizer application with reduced molybdenum concentration. Gen Appl
Plant Physiol XXXII special issue, pp 73–79
Jin CW, Du ST, Zhang YS, Tang C, Lin XY. Atmospheric nitric oxide stimulates plant growth and
improves the quality of spinach (Spinacia oleracea). Ann Appl Biol 155:113–120. DOI:
10.1111/j.1744-7348.2009.00327.x
Kannan S (1990) Role of foliar fertilization on plant nutrition. In: Baligar VC, Duncan RR (eds)
Crops as enhancers of nutrient use. Academic, San Diego, CA, pp 313–348
Nelson KA, Motavalli PP, Nathan M (2005) Response of no-till soybean [Glycine max (l.) Merr.]
to timing of preplant and foliar potassium applications in a claypan soil. Agron J 97:832–838
Okano K, Ito O, Kokubun N, Totsuka T (1983) Determination of 13C in plant materials by infrared absorption spectrometry using a simple calibration method. Soil Sci Plant Nutrition
29:369–374
Okano K, Ito O, Takeba G, Shimizu A, Totsuka T (1984) Alteration of 13C assimilate partitioning
in plants of phaseolus vulgaris exposed to ozone. New Phytologist 97: 155–163. Stable URL
http://www.jstor.org/stable/2432295
Oland K (1960) Nitrogen feeding of apple trees by post-harvest urea sprays. Nature 185:857. doi:
10.1038/185857a0
Oosterhuis DM (1997) Potassium nutrition of cotton in the USA with particular reference to foliar
fertilization. In: Proc. FAO-Inter-regional cooperative research network on cotton (IRCRNC);
Nutrition and growth regulators use in cotton, Part I: Cotton nutrition (Mohamed M. El- Fouly,
ed), Part II: Growth regulators in cotton. Organized by the National Research Centre (NRC),
Cairo-Egypt, 20–23 March 1995, pp 101–124
Pang J, Cuin T, Shabala L, Zhou M, Mendham N, Shabala S (2007) Effect of secondary metabolites associated with anaerobic soil conditions on ion-fluxes and electrophysiology in barley
roots. Plant Physiol 145:266–276. DOI: 10.1104/pp.107.102624
Quartieri M, Millard P, Tagliavini M (2002) Storage and remobilization of nitrogen by pear (Pyrus
communis L.) trees as affected by timing of N supply. Eur J Agron 17:105–110
Ringoet A, Rechenmann RV, Gielink AJ, Wittendorp E (1971) Calcium localization in chloroplasts of the oat leaf by high-resolution tract-autoradiography. Z Pflanzenphysiol 64:80–84.
PMBD, 185507171
402
S. Kannan
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal
cells. Annual Rev Plant Biol 59:683–707. doi: 10.1146/annurev.arplant.59.103006.093219)
Schreiber L, Kerstiens G (2006) Preface to surviving in a hostile environment: barrier properties
of cuticles and periderms. J Exp Bot 57, v–vi, doi:10.1093/jxb/erl031
Schönherr J (2002) A mechanistic analysis of penetration of glyphosate salts across astomatous
cuticular membranes. Pest Management Sci 58:343–351. DOI: 10.1002/ps. 462
Stancheava I, Geneva M, Djonova E, Kaloyanova N, Sichanova M, Boychinova M, Georgiev G
(2008) Response of Alfalfa (Medicago Sativa L) growth at low accessible phosphorus source
to the dual inoculation with mycorrhizal fungi and nitrogen fixing bacteriagen. General Appl
Plant Physiol Special Issue 34(3–4):319–326. http://www.bio21.bas.bg/ipp/gapbfiles/content.
html
Swietlik D, Faust M (1984) Foliar nutrition of fruit crops. Horticultural Rev 287–355. http://www.
pubhort.org/hr/
Tatsumi Y, Kono Y (1981) Translocation of foliar-applied nitrogen to rice roots. Japan. J Crop Sci
50:302–310
Wallace A, Wallace G (2003) Closing the crop yield gap through better soil and better management:
the law of the maximum. Wallace Laboratories, Los Angeles, CA
Wattendorff J, Holloway PJ (1980) Studies on the ultrastructure and Histochemistry of plant
cuticles: The cuticular membrane of agave americana L. in situ. Ann Bot 46:13–28
Wen M, Buschhaus C, Jetter R (2006) Nanotubules on plant surfaces: Chemical composition of
epicuticular wax crystals on needles of Taxus baccata L. Phytochemistry 67:1808–1817. doi:
10.1016/j.phytochem.2006.01.018
Williams RW, Funt RC, Ellis MA, Hall FR (1983) Commercial tree fruit spray guide, Ohio State
University Cooperative Extension Service Bulletin
Wojcik P (2004) Uptake of mineral nutrients from foliar fertilization (Review). J Fruit and
Ornamental Plant Res 12:201–218
Wojcik P, Klamkowski K (2004) “Szampion” apple trees response to foliar titanium application.
J Plant Nutr 27:2033–2046
Woolfolk CW, Raun WR, Johnson GV, Thomason WE, Mullen RW, Wynn KJ, Freeman KW
(2002) Influence of late-season foliar nitrogen in winter wheat. Agron J 94:429–434
Young JO (1983) Spray guide for tree fruits in Eastern Washington. Extension Bulletin 0419
Washington State University Cooperative Extension Service: 46–48
Zilkah S, Klein I, Feigenbaum S, Weinbaum SA (1987) Translocation of foliar-applied urea 15N
to reproductive and vegetative sinks of avocado and its effects on initial fruit set. J Amer Soc
Hort Sci 112:1061–1065. http://www.avocadosource.com/journals/ashs/jashs_toc.htm
Index
A
Abdel-Motaal, H., 108
Abdul-Baki, A.A., 80
Abiotic stress, beneficial microorganisms, 362
Acropetal transport, 396–397
Adam, V., 1
Aery, N.C., 105
Agostini, F., 147
Agricultural crop yields
cereals, 332–334
maize, 334
potatoes, 334
Agroecosystems
arbuscular mycorrhizal fungi, 221, 222
soil microbiological diversity
definition, 219–220
management practices affecting,
221–229
Alkaline soils, cyanobacterial reclamation, 245
Allen, M.B., 248
Aller, M.F., 147
Alum application and treatment, 209–211
Aly, M.M., 383
Amado, T.J.C., 28
Amberger, A., 107
Americas, sustainable agrosystems
cover crop
ecological services, 39
economic benefits, 37–38
food and forage production, 37
historic perspective, 25–27
limitations and challenges
information and technology transfer,
47–48
resource management, 48–49
socioeconomic constraints, 49–50
management
biomass production and residue
quality, 44
cover-crop termination and residue
management, 45
rotation, 43–44
synchronization, 46–47
tillage, 45–46
pest management
diseases, 33–34
insects, 34
nematodes, 34
soil ecology, 32–33
weeds, 35–37
selection
adaptation, 41
functionality and performance,
42–43
screening considerations, 40–41
vigor and reproduction, 42
services and benefits
physical functions, 30–31
primary and secondary effects, 27, 28
soil fertility, 31–32
Ammonia toxicity, 207–208
Anabaena torulosa, 248
Anthony, S., 165
Anuar, A.R., 362
Arbuscular mycorrhizal fungi, 221, 222
beneficial microorganisms, effect of, 358
colonization, 358–259
Armstrong, S.D., 201
Arnon, D.I., 248
Avidin and plant biotechnology
electrochemical methods, 14–16
enzyme-linked immunosorbent assay
(ELISA), 11
fluorescence polarisation (FP), 14
mortality and morbidity assay, 17
polymerase chain reaction (PCR) and
Southern blotting, 10
protect plants against pests
403
404
Arbuscular mycorrhizal fungi (cont.)
pesticidal transgenes, combination
with, 10
pesticide, 4–7
physiological functions and structures,
biotin, 3–4
targeted vacuolar expression, 8–9
transgenic expression, 7–8
SDS-PAGE and Western blotting, 11–13
semiautomatic capillary electrophoresis,
13–14
tissue printing, 15–16
transgenic crops, 3
Avidin physiological functions and structures,
4, 5
Avidin protein, detecting and analysing
methods, 12
Avila, L., 80
B
Bacterial pathogens, control of, 361
Bailey, D.J., 138,
Bajwa, R., 353, 358, 359, 362
Bangar, K.C., 107, 112
Basset-Mens, C., 284
Bastianoni, S., 277
Battilani, A., 164
Baziramakenga, R., 336
Beklova, M., 1
Beneficial microorganisms. See
Microorganisms, sustainable
agriculture
Benincasa, P., 147
Bennett, R.M., 285
Bi, G., 374
Bioavailability PR
co-composting operations, 113
composting conditions
farmyard manure (FYM), 111
organic acid production, 108–110
compost presents P, 111–112
direct application of
total phosphorus contents, 103
triple super phosphate (TSP), 102
phosphorus (P) utilization
availability of, 103–104
Ca and P, equation, 105
composting, 106–108
dissolution rates, 103–104
phosphorus solubilizing microbes
(PSM), 106
utilization evidence, 112
Biochemical oxygen demand (BOD), 206
Index
Biodynamic agricultural systems, 227
Biophysical constraints, 63–64
Biotin physiological functions and structures,
3–4
Blue-green algae. See Cyanobacterial
reclamation, salt-affected soil
BOD. See Biochemical oxygen demand
Boggia, A., 277
Brazil, cover-crop
biophysical production environment, 82
constraints, characterization and diagnosis
of, 83
system analysis and exploration of
alternative systems, 83–85
technology adoption, 85
tillage systems, Santa Catarina, 85–87
Brown, M.T., 287
Bukovac, M.J., 396
Burgess, E.P.J., 1, 10
Burkholder, J.M., 208, 209
Burns, I.G., 151, 152, 158, 169
Businelli, M., 318
C
Calcium sprays, 382
Calegari, A., 44
Campesino-to-campesino approach, 73–74
Cantaloupe, 336
Carbon sequestration, 28, 45
Carton, O.T., 154
Castellini, C., 277, 288
Castro, C.M., 361
Cation exchange capacity (CEC), 312,
317–318
Ca2+ uptake, cyanobacterial reclamation, 249
CEC. See Cation exchange capacity
Chagas, P.R.R., 352, 353
Chamel, A., 390
Cherr, C.M., 23, 29, 44, 59
Chlorophyll meter, 162–163
Christeller, J.T., 11
Chuang, C.C., 108
Clark, M.S., 315
Compost
potential risk
heavy metals, 329–331
hygiene and plant diseases, 332
organic compounds, 31–332
weeds, 332
usage (see Organic farming, compost
usage)
Conventional cropping management, 229–230
Conventional research approaches, 62–63
Index
Corales, R.G., 351
Cornforth, G., 335
Cover crops, 172–173
agrosystems, innovations and applications
biophysical constraints, 63–64
Brazil, 72–87
computer-based exploration and
optimization approaches, 62
exploration of alternative systems,
68–71
Florida, 77–84
information and technology constraints,
65–66
Paraná and Santa Catarina, 89–90
socioeconomic constraints, 64–65
system analysis, 66–67
technology adoption, 76–77
technology development and
adaptation, 71–72
technology transfer, approaches for,
72–76
Uruguay, 87–89
sustainable agrosystems, Americas
diseases, 33–34
ecological services, 39
economic benefits, 37–38
food and forage production, 37
historic perspective, 25–27
insects, 34
management, 43–46
nematodes, 34
physical functions, 30–31
resource management, 48–49
selection, 40–43
socioeconomic constraints, 49–50
soil ecology, 32–33
soil fertility, 31–32
soil organic matter (SOM), 27–30
synchronization, 46–47
transfer, information and technology,
47–48
weeds, 35–37
Creamer, N.G., 40
Crimson clover, 35–36, 41
Cropping systems management
agroecosystems
arbuscular mycorrhizal fungi, 221
soil microbiological diversity,
219–220
interactions and relative importance,
232–234
and microbial communities, 230–231
organic and conventional, 229–230
organic food products, 218
405
practices affecting soil microbiological
diversity
chemical inputs, 227–229
crop choice and rotation, 225–227
flow chart, 222–223
soil properties, 222
tillage, 224
soil biological fertility, 218–219, 234–235
soil microbes, 218
Crop quality, compost use, 336–337
Crop response, cyanobacterial reclamation
residual effect of, 261
saline–alkaline and sodic soils, 259
yield of, 259–260
Crop rotation
design, 84
field crops, 225
genetic engineering, 225–226
mycorrhiza population, 226
soilborne diseases, 123–124
Crop yields, compost use
agricultural
cereals, 332–334
maize, 334
potatoes, 334
vegetable
cruciferous crops, 335–336
Cucurbitaceae, 336
legumes, 336
onions, 336
solanaceous crops, 335
Cruciferous crops, 335–336
Cucurbitaceae, 336
Cultivar nitrogen efficiency, 173
Cuticles, 386
Cyanobacterial reclamation, salt-affected soil
application of
electrical conductivity, 256–257
exchangeable sodium (ES), 257
pH, 256
sodic soils, 256
sodium absorption ratio and, 257
Ca2+ uptake, 249
crop response in
residual effect of, 261
saline–alkaline and sodic soils, 259
yield of, 259–260
distribution of
classification, 246
heterocystous halotolerant, 246–247
non-heterocystous halotolerant,
246–247
halotolerant nitrogen-fixing cyanobacteria,
263
406
Cyanobacterial reclamation, salt-affected soil
(cont.)
mechanisms of
combined nitrogen, 255
compatible solutes and lipids in,
254–255
Na+ in, 252–254
phenomena for, 250
stress-responsive proteins, 251
Na+ uptake, 248–249
saline and alkaline soils, 245
salt stress, 245
soil properties, improvement of
nutrient content, 258–259
structure, 257–258
technology for, 262
thematic areas for, 246
D
Dairy wastewater treatment, 362–363
Daiss, N., 351
Daly, M.J., 351
Decision support system (DSS), 165–166
Devarajan, L., 107
Dhar, D.W., 243
Diez, T., 316
Disease-suppressive mechanisms vs. cropping
systems, 143–144
Dissolution rates, 103–105
Di Stefano, C., 277
Dogliotti, S., 23, 59, 89
Dominguez, E., 387
Douthwaite, B., 72
Drinkwater, L., 320
Drip-irrigation technology, 399
DSS. See Decision support system
E
Eason, W.R., 231
Ebrahim, M.K.H., 383
Ecological footprint analysis, intensive
poultry-rearing system
bio-capacity and, 285
consumption categories, 294
conventional impact assessment, 291
definition, 285, 290
energy and material data, relative
conversion factor, 291, 292
land categories, 293
Ectoteichodes, 388–389
Edwards, A.C., 99
Effective microorganisms (EM). See Micro
organisms, sustainable agriculture
Eichert, T., 374
Index
Eidothea zoexylocarya, 389
Electrochemical methods, 14–16
Emergy evaluation, intensive poultry-rearing
system
in agriculture, 287–288
algebra for, 287
emergy flow density (ED), 287
emergy investment ratio (EIR), 287
environmental loading ratio (ELR), 287
indicators for, 297
raw inputs and, 295–296
transformity, 286
Environmental Protection Agency, 206
Enzyme-linked immunosorbent assay
(ELISA), 11
Erhart, E., 311
Eriksson, I.S., 284
Erwee, M.G., 395
European Union (EU), research and
technology transfer
France, 182–184
Italy, 175–177
Netherlands, 184–186
Spain, 177–182
Eutrophication, 374
Evans, R., 399, 400
Evanylo, G., 327
Exchangeable sodium (ES), 257
F
Farm analysis, consecutive steps, 62
FARMSCAPE approach, 69
Farmyard manure (FYM), 111
Farneselli, M., 147
Faust, M., 375
Fernández, V., 374
Fertigation, 399
Fertigation techniques, 169–171
Fertiliser management, vegetable crops
agronomic options
cover crops, 172–173
cultivar nitrogen efficiency, 173
fertigation techniques, 169–171
intercropping, 171
localised fertilisation, 168–169
mulching, 172
nitrification inhibitors, 171
slow-release fertilisers, 171
water management, 167
high-tech irrigation–fertilization systems,
150
N balance
budgeting approach, 157
Index
irrigation and rainfall, 155
optimum N-fertiliser rate, 151–152
recovery, 155–157
soil N supply, 153–155
total crop N demand, 152
Fließbach, A., 227
Florida, cover-crop
biophysical production environment, 77
constraints, characterization and diagnosis
of, 77–78
system analysis and exploration of
alternative systems, 78–81
technology adoption, 81–82
Fluorescence polarisation (FP), 14
Foliar absorption, inorganic nutrients
cuticle, 386
cuticular permeability
astomatous cuticular membranes, 390
ion diffusion, 391
transport barriers, 392
water sorption, 390
pores and ectoteichodes, 388–389
trichomes
cuticular membrane, 387
features of, 388
Foliar applied beneficial microorganisms,
355–356
Foliar fertilization
application of micronutrients, 375
controlled-release fertilizers, 373
cuticles, 371
foliar-applied nutrients, 371
foliar feeding, 374
foliar nutrition
and law of maximum, 397–398
through sprinkler irrigation, 399–400
inorganic nutrients absorption mechanism
in cuticle, 386
cuticular permeability, 390–393
pores and ectoteichodes, 388–389
trichomes, 386–388
nutrient pathways, foliar uptake
transport, and out of leaf, 393–395
transport, other plant parts, 396–397
nutrients absorption ability, leaf, 374–375
over-fertilization, 373
responses studies
to micronutrients, 383–385
nitrogen, 376–380
to N, P, K, Ca, 380–382
to N, P, K with micronutrients,
382–383
varietal differences, 385–386
407
Ribulose-1, 5-bisphosphate carboxylase/
oxygenase, 372
uptake of nutrients, influence of growth
substances, 375–376
Foliar nutrients supply
nitrogen
absorption and utilization, 378
management, 377
sprays, 378–379
N, P, K, Ca
calcium sprays, 382
critical growth period, 380
effects of Agroleaf, 381
muskmelon, 382
sprays of, 380
N, P, K with micronutrients, 382–383
response to micronutrients
fritted trace elements, 384
iron, 383
titanium sprays, 384–385
Zn application, 383
varietal differences, 385–386
Foliar sprays, 380
Foliar uptake, 375–376
Franceschi, V.R., 394
Frohne, R., 318
Fungal pathogens, control of, 360–361
FYM. See Farmyard manure
G
Gagnon, B., 319, 328
Gallandt, E., 46
Gatehouse, L.N., 13
General stress proteins (GSPs), 251
Genetics, 225–226
Gerbens-Leenes, W., 293
Giaquinta, R.T., 394
Gilbert, G.S., 141
Giusquiani, P., 327
Goenadi, D.H., 112
Goodlass, G., 159
GreenCover, 69, 71
Green manure, vegetable crops, 79–81
Greenwood, D.J., 155, 164
Growth substances, influence of, 375–376
Gu, Y.-H., 140
Guerette, V., 153
H
Haas, G., 284
Haggard, B.E., 210
Halberg, N., 284
408
Halotolerant nitrogen-fixing cyanobacteria, 263
Hammond, G.P., 302
Hammond, J.P., 104
Hartl, W., 311
Hartz, T.K., 162
Heavy metals, 329–331
Hebbar, S.S., 169
Herendeen, R.A., 287
Heterocystous halotolerant cyanobacteria,
246–247
Hiddink, G.A., 119, 141, 144
Higa, T., 352, 354, 357
Hinsinger, P., 105
Holloway, P.J., 386
Hood, E.E., 7, 10, 11, 13, 15
Hoorman, J.J., 205, 207
Hudson, B.D., 28, 327
Hue, N.V., 108
Humus composition, 317
Hussain, T., 351, 355
I
Imai, S., 354
Induced systemic resistance (ISR), 142–143
Information and technology constraints, 65–66
Innovation framework, cover crops
alternative systems, 67–71
Brazil, 82–87
constraints, characterization and
diagnosis of
biophysical constraints, 63–64
information and technology, 65–66
socioeconomic constraints, 64–65
farm analysis, 62
Florida, 77–82
Paraná and Santa Catarina, 89–90
system analysis, 66–67
system, design/selection
approaches for technology transfer,
72–76
technology adoption, sustainability of, 76
technology development and
adaptation, 71–72
Uruguay, 87–89
Inorganic fertilizers, 227–228
Insecticidal mechanism, avidin, 9
Insecticidal properties, avidin, 4–6
Insect pests control, 361–362
Intensive poultry-rearing system,
environmental sustainability
characteristics of, 278, 280
comprehensibility, 303–305
diet composition for, 280
Index
ecological footprint analysis
bio-capacity and, 285
consumption categories, 294
conventional impact assessment, 291
definition, 285, 290
energy and material data, relative
conversion factor, 291, 292
land categories, 293
emergy evaluation
in agriculture, 287–288
algebra for, 287
emergy flow density (ED), 287
emergy investment ratio (EIR), 287
environmental loading ratio (ELR), 287
indicators for, 297
raw inputs and, 295–296
transformity, 286
life cycle assessment (LCA), 281–290
representativeness
indicators denomination and measure
units, 298, 299
resources exploitation and availability
in, 300, 301
reproducibility, 303
verifiability, 302–303
Intercropping, 171–172
ISR. See Induced systemic resistance
Ivanova, R.P., 106
J
Janssen, B.H., 89
Javaid, A., 347, 353, 356–359
Jilani, S., 358
Jin, C.W., 398
Joern, B., 201
Johnsen, K., 228
Johnston, H.W., 107
Jonglaekha, N., 361
Jönsson, H., 107
Joo, Y.H., 352
K
Kannan, S., 371
Karim, M.A., 361
Karlen, D.L., 64
Kerstiens, G., 391, 392
Khaliq, A., 352
Khan, M.S., 106
Kinjo, T., 354
Kizek, R., 1
Klasink, A., 334
Kluge, R., 330
Index
Knox, O.G.G., 99
Kono, Y., 396
Körschens, M., 325
Kpomblekou,-A.K., 103, 105, 106
Kramer, K.J., 1, 5, 7, 11
Kratz, W.A., 248
Krauss, M., 316
Kremen, A., 49, 65
Kremer, R.J., 361
Krizkova, S., 15
K+ uptake, cyanobacterial reclamation,
253–254
L
Lactic acid bacteria, 349
Lactobacillus casei, 349
Lactobacillus plantarum, 349
Leaching, nitrogen, 320–321
Lee, K.H., 355
Lee, K.N., 352
Legumes, 336
Leoni, C., 23, 59
Life cycle assessment (LCA), intensive
poultry-rearing system
characterisation factors, 283–284
Eco-Indicator 99, 288, 290
emissions of, 283, 289
goal and scope definition, 281–283
interpretation, 284–285
inventory, 283
methodological framework for, 282
normalisation, 284
phases of, 289
structure of, 281
Li, J., 170
Linaje, A., 171
Lis, H., 13
Li, W.J., 363
Lord, E.I., 165
Luka-McCafferty, N.J., 210
Lundquist, E.J., 231
Lu, Y., 38, 66
Lynch, D., 328
M
Mäder, P., 227
Mantovani, P., 171
Manure spill remediation methods, 208–209
Manure spills
causes of
chemical analysis, 204
contributing factors, 205–206
409
subsurface tile drainage, 204–205
impact of
algal blooms and eutrophic
conditions, 208
ammonia toxicity, 207–208
water contamination, 207
remediation methods, 208–209
sediment amendments
alum application, 210
fluvarium techniques, 211
Maramble, B., 360
Markwick, N.P., 17
Martin, H., 1
Masarik, M., 1
Maskell, P., 99
MAYF. See Multiple action yield fraction plots
Maynard, A., 335
Mazzola, M., 140
MESMIS, 67
Methemoglobinemia, 203
Meynard, J.M., 166
Microbial antagonism, 124, 127
Microbial antagonists, 140–142
Microbial communities, 230–232
Microclimate, soilborne diseases, 142
Micronutrients, 323–325
foliar applied, 375
foliar uptake of, 375–376
Microorganisms, sustainable agriculture
abiotic stresses, role under, 362
application, 348
biofertilizer, 348
dairy wastewater treatment, 362–363
effect on symbiotic microorganisms
arbuscular mycorrhizal fungi,
357–359
N2−fixing rhizobia, 356–357
foliar application of, 355–356
functions of
lactic acid bacteria, 349
photosynthetic bacteria, 349
yeasts, 349–350
pest management
bacterial pathogens control, 361
fungal pathogens control, 360–361
insect pests control, 361–362
weed management, 359–360
soil application
negative effects, plant growth, 353–354
positive effects, plant growth, 350–353
soil properties, effect on, 354–355
Miller, R.B., 107
Mineral nitrogen, determination method, 160
Mishra, M.M., 112
410
Mixed cropping, soilborne diseases
design of
crop rotation, 121, 123–124
multistorey mix crop, 129–130
single crop successive cultivation, 122
strip mix crop, 127–128
theoretical disease-reducing
mechanisms, 124–126
triticale–clover, 127, 129
various types, 124, 127
disease reduction
allelopathy, 139–140
effect of, 130–137
host dilution, 138–139
ISR and SAR, 142–143
microbial antagonists, 140–142
microclimate, 142
nutrients and disease development, 143
vs. disease-suppressive mechanisms,
143–144
practical feasibility of, 144–145
Mokry, M., 330
Mortality and morbidity assay, 17
Mridha, M.A.U., 359
Mulching, 172
Müller, B., 205
Multiple action yield fraction plots
(MAYF), 398
Murray, C., 7, 13, 16
Mycorrhizal colonization, 231–232
Myers, J., 248
N
Na+, cyanobacterial reclamation
efflux, 252–253
K+ uptake in, 253–254
polysaccharides, 252
uptake, 248–249
Narf, R.P., 211
Nasiruddin, M., 361
N balance
irrigation and rainfall, N supply, 155
nutrient management policy, 156
recovery, 155–156
soil, N supply, 153–155
total crop N demand, 152–153
total N demand of, 151
NDICEA model, 68
Neeteson, J.J., 154
Nelson, K.A., 381
Nelson, A.G., 217
Nematodes, pest management, 34
N fertilisation, methodologies and strategies
Index
crop nutritional status, 161–163
management, agronomic options
cover crops, 172–173
cultivar nitrogen efficiency, 173
fertigation techniques, 169–171
intercropping, 171
localised fertilisation, 168–169
mulching, 172
nitrification inhibitors, 171
slow-release fertilisers, 171
water management, 167
soil mineral N content, 158–161
N2−fixing rhizobia, 356–357
Niccolucci, V., 277
Nitrate leaching, vegetable crops
assessment, 174
fertiliser management, N balance, 151–157
N losses, 149–150
nutrient modelling and system analysis
decision process, different phases, 166
decision support systems (DSS), 165
mechanistic simulation models, 164
precision farming methodology, 167
WELL_N, 164
Nitrification inhibitors, 171
Nitrogen, 203, 207
leaching, 320–321
mineralization, 318–320
Ni, Y., 363
Nonhebel, S., 293
Non-heterocystous halotolerant cyanobacteria,
246–247
Novelli, E., 277
N recovery, 155–157
Nutrient pathways, foliar uptake
to other plant parts, 396–397
in and out of leaf
cell-to-cell communication, 394–395
movement of Lucifer Yellow, 395
O
Oades, J.M., 325
Odum, H.T., 287
Oehmichen, J., 330, 333
Ogdahl, M., 211
Okano, K., 396
Oland, K., 376
Orchard systems, weed suppression, 78–79
Organic cropping management, 229–230
Organic farming, compost usage
beneficial effects
micronutrients, 323–325
nitrogen, 318–321
Index
phosphorus, 321–322
plant-disease suppression, 328–329
potassium, 322–323
soil organic matter, 313–318
soil pH, 318
soil structure, 325–328
biowaste compost, 312
crop quality, 336–337
crop yields
agricultural crops, 332–334
vegetable crops, 334–336
organic pollutants, 338
potential risks
heavy metals, 329–331
hygiene, plant diseases, weeds, 332
organic compounds, 331–332
principles, 311, 313
soil cation exchange capacity, 312
soil organic matter (SOM), 311–312, 337
types, 313
Organic farming, phosphate rock. See
Phosphate rock (PR)
Organic pollutants, 331–332, 338
Osterburg, D., 205
Owens, P.R., 201
P
Pairintra, C., 362
Pakdee, P., 362
Pang, J., 379
Paolotti, L., 277
Paraná and Santa Catarina, 89–90
Park, E.K., 354
Parkinson, R., 334
Paschoal, A.D., 352, 354
Paschold, J., 172
Pelletier, N., 285
Pesticides, 228–229
Pest management
bacterial pathogens control, 361
diseases, 33–34
fungal pathogens control, 360–361
insect pests control, 361–362
insects and nematodes, 34
soil ecology, 32–33
weeds, 35–37, 359–360
Phosphate rock (PR)
co-composting operations, 113
composting conditions
farmyard manure (FYM), 111
organic acid production, 108–110
compost presents P, 111–112
direct application of
411
total phosphorus contents, 103
triple super phosphate (TSP), 102
phosphorus (P) utilization
availability of, 103–104
Ca and P, equation, 105
composting, 106–108
dissolution rates, 103–104
phosphorus solubilizing microbes
(PSM), 106
utilization evidence, 112
Phosphorus, 203, 208–209, 228, 321–322
Phosphorus solubilizing microbes
(PSM), 106
Photosynthetic bacteria, 349
Pizzigallo, A., 277
Plant-disease suppression, 328–239, 328–329
Plant growth, beneficial microorganisms
negative effects, 353–354
positive effects
cereal crops, 351
fruit crops, 352
other crops, 352–353
vegetable crops, 351–352
soil properties, 354–355
Polymerase chain reaction (PCR) and
Southern blotting, 10
Pores, 388–389
Potassium, 322–323
Poultry-rearing system. See Intensive
poultry-rearing system,
environmental sustainability
PR. See Phosphate rock
Priyadi, K., 353
Problem trees, 74–75
Promising technology, 71
PSM. See Phosphorus solubilizing microbes
R
Ramos, C., 179
Rashid, A., 353
Rashid, M.T., 363
Reddy, D.D., 112
Rees, R.M., 99
Reyes, I., 106, 108
Rhodobacter sphaeroides, 349
Rhodopseudomonas palustris, 349
Ringoet, A., 376
Roe, N., 335
Rooting depth, vegetable crops, 159
Ross Breeders-Broiler management manual,
280
Rossing, W.A.H., 23, 59
ROTAT system, 68
412
S
Saccharomyces cerevisiae, 349
Saline soils, cyanobacterial reclamation,
245, 263
Salt-affected soil. See Cyanobacterial
reclamation, salt-affected soil
Samuels, L., 392
Sanchez, J., 320
Sangakkara, U.R., 354, 357, 360
Santa Catarina, tillage systems, 85–87
SAR. See Systemic acquired resistance
Sarrantonio, M., 46
Satisha, G.C., 107
Scagel, C., 374
Schenk, M.K., 173
Scholberg, J.M.S., 23, 59
Schönherr, J., 391
Schreiber, L., 392
SDS-PAGE and Western blotting, 11–13
Seiling, G.H., 107
Semiautomatic capillary electrophoresis,
13–14
Sherony, C., 327
Silgram, M., 147
Simard, R., 319, 336
Sims, J.T., 210
Singandhupe, R.B., 169
Singh, C.P., 107
Singh, N.K., 243
Siswanto, S.Y., 112
Smeltzer, E., 211
Smit, A.B., 167
Smith, D.R., 201, 210
Socioeconomic constraints, 64–65
Soil aggregate, 325–326
Soil biological fertility management, 218–219,
234–235
Soilborne diseases, mixed cropping and
suppression
design of
crop rotation, 121, 123–124
successive cultivation of, 122
disease reduction
allelopathy, 139–140
effect of, 130–137
host dilution, 138–139
ISR and SAR, 142–143
microbial antagonists, 140–142
microclimate, 142
nutrients and disease development, 143
disease-suppressive mechanisms vs.
different cropping systems,
143–144
multistorey mix crop, 129–130
Index
practical feasibility of, 144–145
strip mix crop, 127–128
theoretical disease-reducing mechanisms,
124–126
triticale–clover, 127, 129
various types, 124, 127
Soil degradation and cover crop, field
demonstration, 30–31
Soil erosion, 69, 70
Soil microbiological diversity
in agroecosystems, 219–220
management practices affecting
chemical inputs, 227–229
critical controlling factors, 221–222
crop choice and rotation, 225–227
flow chart, 222–223
soil properties, 222
tillage, 224
Soil N supply
crop residues, 153–154
cultivations and fertilisation history, 154
denitrification losses, 154
mineral soil, 153
soil organic matter mineralisation, 153
Soil organic matter (SOM), 27–30, 69, 70
biochemical decomposition, 314
cation exchange capacity, 317–318
humus composition, 317
humus content
biowaste-compost fertilization,
315–316
DOK-experiment, 316–317
soil organic carbon content, 316
microbiology and fauna, 317
role, 313–314
sustainable agricultural production, 315
Soil pH, 318
Soil porosity, 326–327
Soil structure
aggregate stability, 325–326
attributes, 325
porosity, 326–327
soil water availability, 327–328
soil water infiltration, 328
Soil water availability and infiltration,
327–328
Solanaceous crops, 335
SOM. See Soil organic matter
Southern, E.M., 10
Spaner, D., 217
Spiro, R.G., 13
Sprinkler irrigation, 399–400
Stahr, K., 328
Stamford, N.P., 104
Index
Stancheva, I., 381
Steffens, G., 334
Steinman, A.D., 211
Stewart, D.P.C., 351
Stilwell, D., 324
Stockdale, E.A., 99
Stone, A., 329
Streptococcus lactis, 349
Streptomyces spp., 350
Stress proteins, 251
Strumpf, T., 330
Struthers, P.H., 107
Subsurface tile drainage, 204–205
Sugawara, K., 15
Sundberg, C., 107
Surface water contamination, 204–205
Sustainable crop production. See Foliar
fertilization
Sweeney, D., 172
Swietlik, D., 375
Symbiotic microorganisms. See also
Microorganisms, sustainable
agriculture
arbuscular mycorrhizal fungi, 357–359
N2−fixing rhizobia, 356–357
Synechocystis sp., 253–254
Systemic acquired resistance (SAR),
142–143
T
Tabatabai, M.A., 103, 105, 106
Tatsumi, J., 396
Technical innovations, limited adoption,
72–73
Tei, F., 147
Termorshuizen, A.J., 119
Thompson, R.B., 182
Tillage, 224
Timmermann, F., 315, 332
Tisdall, J.M., 325
Tissue printing methods, 15–16
Tokeshi, H., 352, 361
Transformation and detection methods, avidin
gene, 6–7
Transgenic plants, avidin determine methods
electrochemical methods, 14–16
enzyme-linked immunosorbent assay
(ELISA), 11
fluorescence polarisation (FP), 14
mortality and morbidity assay, 17
polymerase chain reaction (PCR) and
Southern blotting, 10
SDS-PAGE and Western blotting, 11–13
413
semiautomatic capillary electrophoresis,
13–14
tissue printing, 15–16
Tremblay, N., 153, 162
Trichomes
cuticular membrane, 387
features of, 388
Triple super phosphate (TSP), 102
U
Ulgiati, S., 294
Uruguay (Canelones), cover-crop
biophysical environment, 87
constraints, characterization and diagnosis
of, 87–88
system analysis and exploration of
alternative systems, 88–89
V
van Bruggen, A.H.C., 119
van der Werf, H.M.G., 284
Van Straaten, P., 103
Vegetable crops
agronomic options, N-fertilizer
management
cover crops, 172–173
cultivar nitrogen efficiency, 173
fertigation techniques, 169–171
intercropping, 171–172
localised fertilisation, 168–169
mulching, 172
nitrification inhibitors, 171
slow-release fertilisers, 171
European union, research and technology
transfer
France, 182–184
Italy, 175–177
Netherlands, 184–186
Spain, 177–182
fertiliser management, N balance
irrigation and rainfall, N supply, 155
N recovery, 155–156
nutrient management policy, 156
soil, N supply, 153–155
total crop N demand, 152–153
total N demand of, 151
fertiliser N applied vs. nitrate-leaching
losses, 149–150
N fertilisation, methodologies and
strategies
crop nutritional status, 161–163
soil mineral N content, 158–160
414
Index
Vegetable crops (cont.)
N-leaching assessment, 174
nutrient modelling and system analysis,
163–167
yields
cruciferous, 335–336
cucurbitaceae, 336
legumes and onions, 336
solanaceous, 335
Vigor and reproduction, 42
Vogtmann, H., 334, 337
Volterrani, M., 334
Weed management, 359–360
Weil, R., 49, 65
Wen, M., 387
West, J., 363
White, P.J., 104
Wibisono, A., 352
Williams, C., 201
Wireless watering, 399–400
Wittwer, S.H., 396
Wojcik, P., 379
Womack, B.J., 249
Wood, M.T., 362
W
Walker, R.L., 99
Wallace, A., 398
Wallace, G., 398
Wallinga, D., 205
Wastewater treatment, dairy, 362–363
Water quality, manure spills
alternative sediment amendments,
209–211
causes of, 203–206
confined animal farms assessment,
202–203
current remediation methods, 208–209
impact of, 206–208
lagoon breaches, 212
livestock production, 201, 202
methemoglobinemia, 203
nitrogen and phosphorus losses, 201–202
Watson, C.A., 99
Wattendorff, J., 386
X
Xiaohou, S., 355
Xu, H.L., 351, 352
Y
Yang, H.S., 89
Yeasts, 349–350
Yousaf, M., 353
Yousaf, Z., 355
Yoza, K., 5, 7
Z
Zauner, G., 328
Zayed, G., 108
Zewde, T., 140,
Zhao, Q., 354
Zilkah, S., 396
Zotarelli, L., 23, 59