MAJOR ARTICLE
TAPROBANICA, ISSN 1800-427X. April, 2013. Vol. 05, No. 01: 12-18.
© Taprobanica Private Limited, 146, Kendalanda, Homagama, Sri Lanka.
GASTROPOD SHELL UTILIZATION PREFERENCES OF HERMIT
CRAB Clibanarius zebra (DANA, 1852) (DIOGENIDAE, ANOMURA)
Sectional Editor: Michelle Wait
Submitted: 01 November 2012, Accepted: 21 April 2013
J. N. Trivedi1, S. Arya1 and K. D. Vachhrajani1,2
1
Division of Environment and Toxicology, Department of Zoology, Faculty of Science, The M. S. University of
Baroda, Vadodara 390002, Gujarat, India; E-mail: kauresh@gmail.com2
Abstract
The aim of the present study was to characterize the patterns of gastropod shell utilization by the
hermit crab Clibanarius zebra (Dana, 1852) from four different sites along the Saurashtra coast,
Gujarat state, India. A total of 404 individuals of hermit crab were captured (223 males, 147 females
and 34 ovigerous females), occupying 22 species of gastropod shells. Maximum species diversity of
shells occupied by the crab was observed at Veraval. Amongst all the shell species identified,
Cerithium scabridum (36.88 %) was highly occupied by the crab species followed by Astra stellata
(11.39 %), Turbo intercostalis (10.64 %), Cerithidia cingulata (9.16 %) and Lunella coronata (7.43
%). Males of C. zebra utilized a wide range of shell species (21 species), while non ovigerous females
(13 species) and ovigerous females (7 species) use a specific set of gastropod shell species. The
density of live common shell species occupied by C. zebra was also calculated and results revealed
that the density of C. scabridum was very high in the intertidal zone compared to other gastropods.
This indicates that density of shells may influence the utilization of shells by C. Zebra.
Key words: Saurashtra coast, gastropod shell density, shell occupancy, India
Introduction
Benthic fauna show complex patterns in their
bioecological
relationships
and
these
relationships play important roles in the
maintenance of different structural parameters
of benthic communities such as density,
biomass, species richness and spatiotemporal
distribution of species (Tait & Dipper, 1998,
Lawal-Are et al., 2010, Pandya & Vachhrajani,
2010; Trivedi et al., 2012). Hermit crabs
(Anomura: Diogenidae) normally use gastropod
shells as shelter to avoid mechanical damage to
the body as their abdomen lacks calcification
(Barnes, 2003) and to get proper protection
from predators. Hermit crabs obtain empty
gastropod shells from the habitat where
available (Tricarico & Gherardi, 2006). Shell
species and shell morphology have evident
effects on hermit crab’s growth rate (Bertness,
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TAPROBANICA VOL. 05: NO. 01
GASTROPOD SHELL UTILIZATION OF HERMIT CRAB Clibanarius zebra
intertidal areas of Sutrapada and Dhamlej are
flat and rocky in nature with maximum
exposure of 120 to 130 m. The intertidal zone
of both the sites is shallow and presents small
tide pools with sandy or algae-covered
substrata. The intertidal zone at Kodinar is also
flat with numerous small tide pools with
maximum exposure of 120-130 m. The lower
intertidal zone contains large tide pools filled
with zoanthids, while the upper intertidal zone
is made up of sandy shore. Along the coast,
about 1 to 1.5 km of the shore line at all the
study sites was explored.
1981), clutch size and fecundity, (Childress,
1972; Turra & Leite, 2001) and susceptibility to
predation (Mima et al., 2003). In general, the
survival of a hermit crab population in a
particular area is limited by the shell
availability (Kellogg, 1976; Floeter et al.,
2000) and hermit crabs follow particular
patterns of gastropod shell selection, based on
adequacy and availability of gastropod shell
resources (Reese, 1962; Conover, 1978).
The intertidal area of Saurashtra coast, Gujarat,
India is narrow in width and mostly rocky in
nature. The upper intertidal zone is composed
of sandy shore while the lower intertidal zone is
composed of ancient lime stones called
milliolite. The marine biodiversity of the area
includes 120 species of macrofauna recorded so
far (Vaghela, 2010). Two species of hermit
crabs (C. nathii and C. zebra) are commonly
observed in the intertidal area of Saurashtra
coast (Vaghela & Kundu, 2012). Desai &
Mansuri (1989) have studied the different
abiotic and biotic factors, like salinity
fluctuation in sea water, desiccation stress,
substratum preference, temperature, and pH,
that affect density, abundance and spatiotemporal distribution of C. zebra and C. nathii
at various sites on the Saurashtra coast. In the
present study we have studied the distribution,
density and gastropod shell utilization patterns
of the hermit crab Clibanarius zebra.
To study the gastropod species utilization by
hermit crabs, systematic sampling was done
between March 2012 and August 2012. For the
collection of crabs, each of the study sites was
marked with 10 line transects perpendicular to
the coast line and at least 100 m apart where the
length of transects varied with the extent of
exposure during low tide. On each transect four
quadrates of 0.25 m2 were laid randomly. The
C. zebra individuals present in the quadrate
area were collected and brought to the lab. To
calculate the density of the gastropod shells in
the study area, 40 quadrates were laid as
described above. All the gastropod shells
available in the quadrate area were counted and
identified to the species level using
identification key (Apte, 1998). In the
laboratory, the crabs were classified into three
categories on the basis of gender and
reproductive status viz male, non ovigerous
female and ovigerous female. The gastropod
shells occupied by C. zebra were also identified
to the species level.
Materials and Methods
The present study was carried out at four
different sites along the coastal region of
Saurashtra, Gujarat, India viz., Veraval (20 54’
37" N, 70 21’ 04” E), Sutrapada (20 49’ 53" N,
70 29’ 17” E) Dhamlej (20 46’ 29" N, 70 36’
19” E) and Kodinar (20 45’ 29" N, 70 39’ 39”
E). The intertidal area of all the studied sites
shows evident zonation patterns which were
identified based on physiographic features and
dominant species in the community. The
intertidal zone of Veraval is mostly rocky,
while the upper intertidal zone is composed of
sandy shore. The lower intertidal area grades
into a subtidal zone with a steep slope. The
exposure of the intertidal zone is not uniform
and shows a maximum exposure of 60 to 90 m
at different tidal levels. The rocky intertidal
area of Veraval is mostly covered by small tide
pools of varied depth, small boulders, and
crevices, which provide suitable habitat for
gastropods and hermit crab species. The
A Pearson’s χ2 test was used to compare the
shell occupation frequencies by hermit crab
while one way ANOVA was used to compare
the mean density of gastropod shells.
Results
During the study period a total of 404 hermit
crabs were collected; amongst them 223 (55%)
individuals were male, 147 were female (36%)
and 34 (8%) were ovigerous females (Table I).
The hermit crabs were found occupying 22
species of gastropods shells in different
percentages, (Table 1) of which six species of
gastropod shells were most commonly utilized
by the hermit crabs. Cerithium scabridum was
observed to be the most frequently occupied
gastropod shell species ( 37%, χ2 = 6.38, P <
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TAPROBANICA VOL. 05: NO. 01
TRIVEDI ET AL., 2013
Amongst the six species of gastropod shells
utilized by the hermit crab species, Cerithium
scabridum was significantly occupied by males
(24%, χ2 = 26.96, P < 0.05) but in the case of
non ovigerous females (50 %) and ovigerous
females (53 %) significance in occupation was
not observed. The other five species of
gastropod shells significantly occupied by
males were Astrea stellata (13%, χ2 = 52.60, P
< 0.05), Lunella coronata (12%, χ2 = 56.64, P
< 0.05), Cerithidia cingulata (5%, χ2 = 79.14,
P < 0.05), Chicoreus brunneus (9%, χ2 =
77.62, P < 0.05), and Turbo intercostalis (15%,
χ2 = 47.08, P < 0.05) and by non ovigerous
females were Astrea stellata (10%, χ2 = 63.72,
P < 0.05), Lunella coronata (3%, χ2 = 87.40, P
< 0.05), Cerithidia cingulata (15%, χ2 = 47.44,
P < 0.05), Chicoreus brunneus (1%, χ2 =
65.18, P < 0.05), and Turbo intercostalis (4%,
χ2 = 82.12, P < 0.05). For ovigerous females,
Astrea stellata (8%, χ2 = 62.20, P < 0.05),
Cerithidia cingulata (11%, χ2 = 65.18, P <
0.05), and Turbo intercostalis (5%, χ2 = 76.10,
P < 0.05) were significantly occupied while
utilization of Lunella coronata and Chicoreus
brunneus was not observed. Ovigerous females
showed significantly greater usage of Purpura
panama (5%, χ2 = 76.10, P < 0.05) and Thais
lacera (5%, χ2 = 76.10, P < 0.05), which were
not commonly utilized by males or non
ovigerous females (Fig.2-3).
0.05) by the C. zebra population followed by
Astrea stellata (11%, χ2 = 58.1, P < 0.05),
Turbo intercostalis (11 %, χ2 = 60.40, P <
0.05), Cerithidia cingulata (9 %, χ2 = 65.10, P
< 0.05), Lunella coronata (7%, χ2 = 70.80, P <
0.05) and Chicoreus brunneus (5 %, χ2 =
60.40, P < 0.05), which were also significantly
occupied by the hermit crab species (Fig. 1).
The remaining species of gastropod shells
showed variation in percentage of occupation
(0.25 % to 3.47%) and represented 19.05 % of
the total utilization of occupied shell species.
They were assembled in one group and named
as “others”.
Figure 1: Percentage utilization of gastropod shells
by C. zebra
The species diversity of gastropod shells
occupied by hermit crabs was analysed and
revealed that from the total of 22 species of
gastropod shells used by C. zebra, the
maximum species diversity was recorded at
Veraval (20 species) followed by Kodinar (17
species), Sutrapada (13 species), and Dhamlej
(10 species) (Table 2). A difference in the
gastropod species utilization by different sexes
of C. zebra was observed. Males utilized 21
species of gastropod shells while non ovigerous
females utilized 19 species and ovigerous
females utilized 7 species (Table 2). Six species
of gastropod shells; Cerithium scabridum,
Astrea stellata, Lunella coronata, Cerithidia
cingulata, Chicoreus brunneus, and Turbo
intercostalis were commonly utilized by all the
categories where the percentage utilization of
these shells varied considerably. In the case of
ovigerous females, utilization of Lunella
coronata and Chicoreus brunneus was not
observed indicating species preference/
avoidance. Ovigerous females showed greater
usage of Purpura panama and Thais lacera
than males and all females.
A
B
Figure 2: Percentage utilization of gastropod shells
by (A) male (B) female C. zebra
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TAPROBANICA VOL. 05: NO. 01
GASTROPOD SHELL UTILIZATION OF HERMIT CRAB Clibanarius zebra
study, Clibanarius zebra was found to utilize
22 species of gastropod shells and similar
results were obtained for other species of the
same genera.
For example, Clibanarius
erythropus utilizes 19 species of gastropod
shells (Botelho & Costa, 2000), while
Clibanerius virescens was observed to utilize
23 species of gastropod shells (Reddy &
Biseswar, 1993). Fatima (2007) has studied the
gastropod species utilization by hermit crab
species Diogenes planimanus at Karanchi coast
of Pakistan and recorded utilization of 32
gastropod species which is quite higher than the
utilization pattern of gastropod shell by C.
zebra.
Figure 3: Percentage utilization of gastropod shells
by ovigerous female C. zebra
Shell availability in the habitat is the main
factor affecting the shell utilization and survival
of the hermit crab population in a particular
area (Kellogg, 1976; Floeter et al., 2000).
During the study we collected data on the
density of gastropod species which are
commonly utilized by the hermit crab to
determine the shell resources available in the
habitat for hermit crab utilization. The results
revealed that significant variation is observed
for the mean density values of each shell
species (ANOVA: df = 71, F = 17.58, p <
0.05).
Cerithium
scabridum
exhibited
maximum density followed by Lunella
coronata, Turbo intercostalis, Cerithidia
cingulata, Astrea stellata, and Chicoreus
brunneus (Fig. 4).
In the present study, male and non ovigerous
female crabs utilized 21 and 19 species of
gastropod shells respectively but lower
diversity of gastropod shell utilization was
observed in ovigerous females. A total of 7
species of gastropod shells were occupied by
ovigerous females out of 22 species recorded
from the habitat. Similar results have been
recorded in ovigerous female gastropod shell
occupation for two different species, Calcinus
tibicen (Mantelatto & Garcia, 2000) and
Pagarus exilis (Terossi et al., 2006). Present
findings suggest that a specific pattern of shell
selection is observed in case of ovigerous
females.
Further, differences have been
observed for the occupation of common
gastropod species by different sexes of the crab
species. Shells of C. scabridum, A. stellta, C.
cingulata, and T. intercostalis were most
occupied by male, non ovigerous female and
ovigerous females while other species, namely
L. coronata and C. brunneus, were occupied
only by males and non ovigerous females but
not utilized by ovigerous females.
C. Zebra utilizes a wide range of gastropod
shells, and this particular pattern suggests that
the occupation of shells is highly influenced by
shell availability in the area. It was also
observed that in the local population of C.
zebra, specific preference was observed for
Cerithium scabridum which suggests that there
may be a pattern of preference and adaptation
by C. Zebra for this gastropod species. A
similar pattern has been observed for Isocheles
sawayai, which uses the shells of Stramonita
haemastoma (Galindo et al., 2008). In the
present study, C. zebra utilized Cerithium
scabridum maximally (37%), however, it was
Figure 4: Density of gastropod species
Discussion
The population distribution of hermit crabs has
an adequate relationship with the gastropod
species available in the habitat (Mantellato &
Garcia, 2000). The survival of hermit crabs in a
particular area and their gastropod shell
utilization patterns depend on different factors
such as special architecture of the shell
resource, density of shells, and inter- and
intraspecific competition between different crab
species (Reese, 1962, 1969). In the present
1513
TAPROBANICA VOL. 05: NO. 01
TRIVEDI ET AL., 2013
distribution of Cerithium scabridum and C.
zebra is observed on the entire Saurashtra coast
indicating overlapping of geographical
distribution (Apte, 1998, Vaghela & Kundu,
2012). On the basis of this particular
phenomena and shell utilization it is thought
that the shell availability in the habitat is the
main reason for the utilization of Cerithium
scabridum by the hermit crab C. zebra. The
specific selection of gastropod shell species by
the ovigerous females needs further study.
quite lower than the shell utilization pattern
exhibited by hermit crabs C. vittatus (64.7%)
and Isocheles sawayai which utilized the
gastropod Stramonita namastomai shell to the
extent of 64.7 % and 49.87 %, respectively
(Fantucci et al., 2008; Sampaio &Masunari,
2010). A high density of Cerithium scabridum
was recorded (15 animals/m2) as compared to
other shells, which makes it the dominant
gastropod species of the habitat and thus
represents an adequate shell resource for
occupation by hermit crab species. The
Table 1: Percentage of gastropod species utilized by Clibanarius zebra
Total
Gastropod species
Astrea semicostata
Astrea stellata
Bursa granularis
Cantharus spiralis
Cantharus undosus
Cerithidia cingulata
Cerithium rubes
Cerithium scabridum
Chicoreus brunneus
Engina zea
Lunella coronata
Mitra guttata
Mitra scutulata
Nassarius lentigenosus
Nassarius reeveanus
Nassarius sufflatus
Polia rubigenosa
Purpura panama
Thais lacera
Tibia curta
Turbo brunneus
Turbo intercostalis
Total
n
7
46
6
2
12
37
12
149
22
4
30
1
3
1
1
1
2
14
8
1
2
43
404
%
1.73
11.39
1.49
0.50
2.97
9.16
2.97
36.88
5.45
0.99
7.43
0.25
0.74
0.25
0.25
0.25
0.50
3.47
1.98
0.25
0.50
10.64
100
Male
n
6
29
3
1
10
11
4
55
20
1
26
0
2
0
1
1
2
9
5
1
1
35
223
%
2.69
13.00
1.35
0.45
4.48
4.93
1.79
24.66
8.97
0.45
11.66
0.00
0.90
0.00
0.45
0.45
0.90
4.04
2.24
0.45
0.45
15.70
100
Female
n
1
14
3
1
2
22
7
74
2
3
4
1
1
1
0
0
0
3
1
0
1
6
147
%
0.68
9.52
2.04
0.68
1.36
14.97
4.76
50.34
1.36
2.04
2.72
0.68
0.68
0.68
0.00
0.00
0.00
2.04
0.68
0.00
0.68
4.08
100
Ovigerous
female
n
%
0
0
3
8.82
0
0
0
0
0
0
4
11.76
1
2.94
20
58.82
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
2
5.88
2
5.88
0
0
0
0
2
5.88
34
100
Table 2: Gastropod shell diversity at different study sites; V, Veraval; S, Sutrapada; D, Dhamlej; K, Kodinar
Mollusc species
V
S
D
K
Mollusc species
V
S
D
K
Astrea semicostata
√
√
Mitra guttata
√
Astrea stellata
√
√
√
√
Mitra scutulata
√
Bursa granularis
√
√
√
√
Nassarius lentigenosus
√
√
Cantharus spiralis
√
√
Nassarius reeveanus
√
Cantharus undosus
√
√
Nassarius sufflatus
√
Cerithidia cingulata
√
√
√
√
Polia rubigenosa
√
√
√
Cerithium rubes
√
√
Purpura panama
√
√
√
√
Cerithium scabridum
√
√
√
√
Thais lacera
√
√
√
Chicoreus brunneus
√
√
√
Tibia curta
√
√
√
√
Engina zea
√
Turbo brunneus
√
√
√
√
√
Lunella coronata
√
√
√
Turbo intercostalis
√
√
√
√
14
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TAPROBANICA VOL. 05: NO. 01
GASTROPOD SHELL UTILIZATION OF HERMIT CRAB Clibanarius zebra
Table 3: Gastropod shell preferences by different categories of Clibanarius zebra
Mollusc species
Male
Non ovigerous Female
Astrea semicostata
√
√
Astrea stellata
√
√
Bursa granularis
√
√
Cantharus spiralis
√
√
Cantharus undosus
√
√
Cerithidia cingulata
√
√
Cerithium rubes
√
√
Cerithium scabridum
√
√
Chicoreus brunneus
√
√
Engina zea
√
√
Lunella coronata
√
√
Mitra guttata
√
Mitra scutulata
√
√
Nassarius lentigenosus
√
√
Nassarius reeveanus
√
Nassarius sufflatus
√
Polia rubigenosa
√
Purpura panama
√
√
Thais lacera
√
√
Tibia curta
√
√
Turbo brunneus
√
√
Turbo intercostalis
√
√
21
19
Ovigerous
√
√
√
√
√
√
√
7
Childress, J. R., 1972. Behavioral ecology and
fitness theory in a tropical hermit crab. Ecology,
53: 960-964.
Acknowledgements
We are thankful to P. C. Mankodi for his help
in identification of gastropod shell species. We
also thank Trinayan Borgohin, Umang Trivedi,
Vishal Pankhania and Kalpesh Gohel for
support during the field studies. Finally we
would like to Thank Michelle Wait (Nelson
Mandela Metropolitan University – South
Africa) and Johanna Bleecker (McGill
University – Canada) for editing and reviewing
the manuscript.
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Veraval, West coast of India. Indian Journal of
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