Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
Abstract
Two intertidal hermit crabs, Pagurus granosimanus and Pagurus
samuelis, were studied at the Hopkins Marine Station. The two species
demonstrate definite zonation along the intertidal, but intraspecies differences
are not known. Past studies have shown that shell characteristics, such as
damage, fouling, and adequacy have varying influences on the reproductive
success of female.
Ovigerous females, non-ovigerous females, and males were examined at
three different locations.
The study of the distribution and the shell utilization
of each of the hermit crabs revealed that males were more predominant than
females. Non-ovigerous females were more common than males. Shell fouling
had no effect on the shell utilization by ovigerous, non-ovigerous and male
hermit crabs. Ovigerous females were in shells with less damage. Shell
adequacy assignments showed that females were more likely to be ovigerous if
they occupied smaller shells than the preferred size calculated from a shell
adequacy index. Clutch size was minimally correlated to other measurements.
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
Introduction
Ovigerous female hermit crabs must rely on their shell for survival and
for the survival of their egg clutch. Factors such as shell availability and the
habitat in which a female hermit crab lives may affect the success of
reproduction and egg maintenance. Furthermore, reproduction and energy
expenditure may influence the proportions of ovigerous females, non-ovigerous
females, and males located at different lcoations and at different heights along
the intertidal zone.
Shell size affects a hermit crab’s reproductive effort, i.e., how many eggs
are brooded, but the effect varies from species to species. For one species, C.
vittatus, a large shell provides more room for brooding eggs (Fotheringham
1976), but for others, such as the Calcinus obscurus, increased shell size results
in greater energy expenditure in growth rather than reproductive effort,
resulting in fewer eggs (Bertness 1980).
Shell damage can be a variable in the susceptibility to predation for
hermit crabs. One of the local predators, Cancer antennarius, can more easily
eat hermit crabs occupying a damage shell than an intact shell (personal
observation). However it is unclear whether shell damage influences how
shells are distributed among the non-ovigerous, ovigerous and males.
A study of Pagurus longicarpus indicated that shell fouling and shell
damage may have an affect on the clutch size depending on the habitat and the
size of the hermit crab(Wilber 1989).
The distributions of Pagurus granosimanus and Pagurus samuelis have
been identified for the Hopkins Marine Station (Belknap, Robert and John
Markham 1965). P. samuelis occupy the higher portions of the intertidal, and P.
granosimanus occupy the intertidal zone below, with some overlap. However,
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
distribution studies have not reviewed the breakdown of non-ovigerous,
ovigerous, and male hermit crabs. P. granosimanus and P. samuelis are
susceptible to dessication and thermal stress (Taylor 1981), but how those
stresses affect the proportion of non-ovigerous, ovigerous, and males along the
intertidal is uncertain.
The purpose of this study was to determine how a habitat affects the
proportions of females, ovigerous females, and males. Öther elements such as
relative tidal height were examined to indicate if the females, ovigerous females,
and males were more likely to remain in particular parts of the intertidal to
alleviate thermal and dessication stress. Also the type of damage on a shell was
examined for differences between the shell utilization of the non-ovigerous,
ovigerous, and males.
Methods and Materials
Two species of hermit crabs, Pagurus granosimanus and Pagurus samuelis
were collected from the intertidal zone of the Hopkins Marine Station, Pacific
Grove, California. Collection took place during May 11-13, 1994, during low tide.
Three locations were chosen for study: West Beach, an exposed area that
receives direct wave action; Hewett Transect, a semi-protected area; and Agassiz
Beach, a protected area which receives less wave action of the three (Fig 1). At
each location a transect running perpendicular to the shore from the high
intertidal to the lowest exposed position (approximately -0.5 m MLLW) was
sampled. Each transect was divided into five collection sites 2 meters apart
horizontally.
For each site, approximately 0.25 m2, the first fifty (50) hermit crabs were
collected or until thirty (30) minutes had elapsed. If fifty crabs were not
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
collected within the 0.25 m2 area, collection was expanded to the surrounding
area, but did not exceed 1.0 m2. Specimen collection was done while the site was
partially submerged to facilitate locating motile hermit crabs and to reduce the
chances of missing hidden individuals. After collection, crabs were placed in
holding tanks with running sea water. Crabs were fed on a diet of the brown
seaweed Pelvetia.
Hermit crabs were removed from their shells by piercing the whorl of
the shell with the edge of a small, flat screwdriver, and gently proding the
abdomen with a thin piece of magnet wire. Two other methods, heating the
shell with a soldering iron, and placing the crab in mixture of freshwater and
seawater were tried but were not consistently succesful. Out of 400 crabs,
piercing the shells and proding resulted in 5 deaths. Piercing the shell resulted
in loss of a small portion, usually no bigger than 1.5 mm2. Since these
fragments were only a small proportion of the total weight, shell weight
measurements were considered reliable.
After crabs were removed from their shells, they were placed in small,
plastic cylindrical containers with running sea water. Some individuals
burrowed under the shell rubble substrate of the containers.
The following data were recorded for each crab: species, sex, shield
length, wet weight and number of eggs. Sex was determined by locating the
gonopores on the third pereiopods for females and on the fifth pereiopods for
males. Shield length, from the tip of the rostrum to the edge of the hard
carapace, was measured to the nearest 0.1 mm with Venier calipers under a 7X
magnification dissection microscope. Specimens were blotted dry before wet
weight measurements. Eggs were removed from females by clipping the three
pleopods to which eggs are attached, and the eggs were counted under 7X
magnification. Seven clutches were removed and the eggs individually counted
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
and egg weight was measureed. A linear regression determined an egg
number:weight ratio that was later used to determine the number of eggs for
some clutches for which the eggs were not counted.
The following data were recorded for the shells occupied by the hermit
crabs: species, diameter, weight, fouling, and degree of damage. Shell diameter
was measured with Vernier calipers to the nearest 0.1 mm. Shells were dried
before weighing in a microwave for two minutes on the high setting. Shell
weight included weight of any fouling organisms. The gastropods Spirorbis
spp., the polychaetes Cripidula adunca and Cripidula planca, and the non-
geniculate coralline alga Lithothamnion spp. on the underside of the shell and
on the whorl were noted. Damage of the lip, body, and apex was also noted.
A shell adequacy index (SAI) which measures deviation from a calculated
preferred shell size, (Kim 1994) was assigned to each hermit crab and its shell.
The SAI was derived by placing 50 P. samuelis and 57 P. granosimanus
individuals into tanks with an overabundance of shells (1:8 crab to shell ratio).
The crabs were given 5 days to acclimate to their new environment and select
shells. At the end of the five days, it was assumed that the crab was in the shell
size it preferred, and the crab’s wet-weight and the diameter of its shell were
measured. A linear regression was used to analyze the relationship between
crab weight and shell diameter to derive the SAI.
Wet weight of the crab was compared to its shield length and a linear
regression between the two measurements was determined. This regression was
used to determine either the wet-weight or shield length for a few individuals
(«10) whose wet-weight or shield length measurement was not recorded.
Results
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
A total of 136 Pagurus granosimanus and 180 Pagurus samuelis were
collected. Pagurus hirsuiticulus were collected as well but a limited sample size
(n = 36) was not sufficient for a similar study of this species.
The smallest ovigerous P. granosimanus was 4.3 mm in shield length, and
the largest had a shield length of 6.8 mm. The females ranged from 2.3 mm to 5.9
mm, while the males were 1.8 mm to 7.2 mm in shield length.
The smallest ovigerous P. samuelis was 4.0 mm in shield length and the
largest was 5.8 mm. Females ranged from 2.5 mm to 5.6 mm and the males ranged
from 2.2 mm to 6.5 mm.
The different ranges and overlapping of sizes for non-ovigerous,
ovigerous and males indicates that the ovigerous females, non-ovigerous
females and males are not necesssarily competing for the same shells (Fig 2).
Distribution
At West Beach, the Hewett Transect, and Agassiz Beach, 50, 31, and 55 P.
granosimanus were collected, respectively. Of the Pagarus granosimanus
collected, males (avg 64%) were more abundant than the ovigerous and non-
ovigerous. Non-ovigerous females were more common than ovigerous females.
There was a slight increase in males and a decrease in ovigerous females as the
studied area shifted from the exposed area, West Beach, to the protected area,
Agassiz beach (Fig 3). However, there was no statistical difference among the
proportions of non-ovigerous, ovigerous, and male Pagurus granosimanus at the
three transects (p = 0.82). A larger sample size may be needed to accurately
describe a possible trend between the habitats.
At West Beach, the Hewett Transect, and Agassiz Beach, 22, 56, and 102
Pagurus samuelis were collected, respectively. At the three transects, males
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
were more abundant than ovigerous and non-ovigerous crabs (Fig 4). At West
Beach and the Hewett Area, there were more non-ovigerous females than
ovigerous females. But at Agassiz Beach, there was a lower percentage of males
and a higher percentage of ovigerous females than non-ovigerous females.
There was no statistical difference among the proportion of non-ovigerous,
ovigerous and males at the three transects however (p = 0.16).
Trends across the sites (up/down along the intertidal) in a transect were
inconclusive due to some sites having a sparse population of hermit crabs.
Therefore, population distribution analysis focused on trends between the
transects and not the sites within the transects.
Shell Damage
Overall shell damage observations showed that ovigerous P. granosimanus
had shells that were more intact than the shells occupied by the non-ovigerous
and males (Fig 5). At the three transects, ovigerous P. granosimanus were in
shells that had no whorl or apex damage (Fig 6). Among the non-ovigerous,
ovigerous and males, the shells in the Hewett Area had the most damage,
whereas Agassiz Beach had least shell damage. Despite this, damage differences
among the non-ovigerous females, ovigerous females and males were not found
to be significant(p = 0.33).
Shells occupied by P. samuelis in the Hewett Transect were more damaged
than the shells found in the other two transects. The transect with the lowest
amount of shell damage was West Beach. Overall, 86% of ovigerous P. samuelis
were in shells that were intact (Fig 7). Non-ovigerous females were present in
shells that were more damaged than the ovigerous. Males had most of the shells
with lip, whorl and apex damage. The difference between the non-ovigerous
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
and ovigerous’ shell damage was significant (p = 0.01). The difference between
the ovigerous’ and males’ shell damage was significant too (p = 0.04)
Fouling
The predominant fouling organisms were Spirobis spp. and Crepidula
planca , which were commonly found together.
There was no significant difference in the proportion of fouling for
shells occupied by P. granosimanus non-ovigerous, ovigerous, and males (p =
0.93) (Fig 8). The same was true for shells inhabited by P. samuelis (p = 0.60) (Fig
There was a difference in fouling of shells (p = 0.04) between the two
species of hermit crabs (Fig 10), which may be related to the difference in
intertidal heights in which the crabs live and where fouling organisms live
along the intertidal.
Adequacy
Non-ovigerous P. granosimanus were in shells larger than their
preferred size at all three sites (Fig 11). The ovigerous were in shells smaller
than the preferred size. At West Beach, ovigerous females were in shells 25%
smaller than preferred.
For P. samuelis, all were in shells larger than they preferred, except for
males at West Beach (Fig 12). At Agassiz Beach and West Beach, ovigerous
females were in shells smaller than the shells inhabited by the non-ovigerous.
At the Hewett Transect, the situation reversed, and the ovigerous female had a
larger shell than the preferred size shell of the non-ovigerous.
Shell adequacy did have an effect on the reproductive potential of a
female (Fig 13 & 14). To examine this relationship, females below the first
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
observed shield length of an ovigerous female were omitted. The remaining
non-ovigerous and ovigerous females were separated into adequacy bins, and
the percentage of ovigerous females of the total females for each bin was
calculated. For both Pagurus granosimanus and Pagurus samuelis, as shell size
increased from a small fit to a larger fit, the percentage of ovigerous females out
of the total number of females decreased.
Clutch Size
The number of eggs to egg weight ratio was calculated from 7 clutches of
hermit crabs (p = .947) (Fig 15). Note that these weights intermixed the eggs
from both species, and did not take into account any variability in eggs between
the species.
For each species, clutch size was compared to crab wet weight, size, shell
fouling, shell damage, and distribution at each three transects. None of these
variables were correlated to the number of eggs that an ovigerous female
carried. One possible correlation found was with the shell adequacy index for P.
gransimanus. As the shell adequacy index decreased for the ovigerous P
granosimanus, i.e., the hermit crab inhabited a shell smaller than the calculated
preferred shell size, the egg number increased (Fig 16). Although the p-value is
not considered significant (p « .07), more collection of ovigerous females may be
able to reveal a significant trend.
Discussion
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
The proportions of P. granosimanus non-ovigerous, ovigerous, and males
do not appear to be strongly correlated to wave exposure. No trend was
significant but a greater sample size may be needed for a further analysis. The
lack of a significant difference may be that the overall habitat, i.e., the
protected, exposed, and semi-protected areas, are indeed different, but the
micro-habitats of where the hermit crabs live may not make one type of crab,
say an ovigerous female, more or less susceptible to predation, dessication, and
thermal stress. Also, courtship involves two hermit crabs being in close
proximity for sometimes as long as two days (Coffin 1960), while the male goes
through various movements, still holding onto the female’s shell. If an exposed
area really provided significantly higher water turbulence without the
convenience of a micro-habitat, it would be difficult to have courtship for a
long time without the loss of some chelipeds.
At each transect, the difference in relative tidal height did not correlate
with the number of non-ovigerous, ovigerous, and males found. This suggests
that ovigerous females did not seek different habitats than non-ovigerous
females, at least in vertical height. However, more collections at different
transects with higher numbers of hermit crabs would be required to resolve
any subtle patterns, such as high temperatures, which cause eggs to fall from
the pleopods prematurely.
At most of the transects, ovigerous females had shells with less damage
than the non-ovigerous females’ shells. For the avoidance of broken shells by
the ovigerous female, there are at least two possibilities for this trend: (1)
females are more likely to become reproductive when occupying an intact shell,
or (2) ovigerous females prefer to move into intact shells.
Courtship can take between one and two days, and since the male holds on
to the female’s shell during all that time, the lip of the shell must still be
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
grippable. Even though there was a significant amount of lip damage found on
the shells of ovigerous females, none of it seemed so severe as to hamper the
efforts for courtship.
Whorl and apex demage, however, can lead to unsuccessul reproduction.
Since female hermit crabs must hold their eggs in their shell until they become
attached to their pleopods (Coffin 1960), any holes in the shell are possible areas
for eggs to be lost. In terms of shell use, this may imply that females, once
ovigerous, must be in an intact shell to ensure attachment of the eggs to her
pleopods. For these reasons, it appears unlikely that ovigerous females would
ever want to change shells. Furthermore, observations in the lab made it clear
that ovigerous females would have a harder time entering a shell with a clutch
attached.
The fouling data suggests that the fouling of shells does not appear to
influence the choices of shells for non-ovigerous, ovigerous, and male hermit
crabs. Therefore, the visual examination of shells as potential homes may be the
same for ovigerous, non-ovigerous and male hermit crabs.
Although not statiscally significant, shell adequacy appeared to affect the
clutch sizes of P. granosimanus hermit crabs. These results agree with the
findings of Bertness, in which he found that as the shell size adequacy
decreased, the number of eggs increased. As shown by the shell adequacy index
for the three crabs, the ovigerous females are living in shells that are at least
15% smaller than their preferred size. So it is possible that the Pagurus
granosimanus is doing what Bertness described for another species: ovigerous
females change the aim of their energy expenditure from finding a larger
shell, to just producing a larger number of eggs.
This trend was not true for the P. samuelis crabs. Since most of the shells
were slightly larger than predicted, it is difficult to determine how ovigerous
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
females may decide to expend their energy in growth effort or reproductive
effort. However, since the adequacy data suggests that P. samuelis is not shell
stressed, this trend may be irrelevant.
Summary
Examination of the different areas along the intertidal at the Hopkins
Marine Station, Pacific Grove, CA, has shown that the difference in habitats,
from an exposed area to a protected area did not have a strong correlation with
the makeup of non-ovigerous, ovigerous and male hermit crabs of either
species. Differences were noted along each of the sites of the transects but no
definite trend was found to describe the distribution of female hermit crabs.
Damage of shell measurements reflected that ovigerous females were in
shells that were more intact than shells occupied by non-ovigerous females.
This was true for both species. This finding may be of a preference of ovigerous
females or a sign that reproduction may be facilitated when a shell is intact.
The latter seems more probable but additional studies need to be conducted.
Females were more likely to be ovigerous if the shell size was smaller
than the preferred size suggested from a shell adequacy index.
Reproductive effort was only affected by the adequacy of the shell, as no
variables regarding habitat, shell fouling, or tidal height had any correlation.
My findings agree with some other species of hermit crab, i.e., as shell size
becomes smaller than the preferred size, ovigerous females put more effort into
reproduction than growth, rather than expend energy on pursuing a shell that
may be only minimally larger.
Acknowledgements
Martinez, E. The Distribution and Shell Utilization of the Female Hermit Crab
1 would like to thank James Watanabe for his invaluable assistance and patience.
1 would also like to thank Joe Wible for relentlessly tracking down journals.
And thanks to Maggie for getting me off of my butt.
Literature Cited
Belknap, Robert and John Markham. 1965. The intertidal and subtidal
distribution of four species of Pagurus. Unpublished student paper.
Hopkins Marine Station.
Bertness, Mark D. 1980. Pattern and plasticity in tropical hermit crab growth
and reproduction. The American Naturalist 177:754-773.
Coffin
Harold. 1960. The ovulation, embryology, and developmental stages of the
hermit crab Pagurus samuelis. Walla Walla College Publications 25.
Fotheringham, Nick. 1976. Population consequences of shell utlilization by
hermit crabs. Ecology 57: 570-578.
Taylor, Phillip R. 1981. Hermit crab fitness: the effect of shell condition and
behavioral adaptations on environmental resistance. J. exp. mar. Biol.
Ecol. 52: 205-218.
Wilber, T. Payson. 1989. Associations between gastropod shell characteristics and
egg production in the hermit crab Pagurus longicarpus. Oecologia 81: 6-
Figures
Figure 1. Map of the Hopkins Marine Station
Figure 2. Shield length of Pagurus granosimanus
Shield length of Pagurus samuelis
Figure 3. Pagurus granosimanus distribution at each transect
Figure 4. Pagurus samuelis distribution at each transect
Figure 5. Overall damage of shells inhabited by Pagurus granosimanus and
Pagurus samuelis
Figure 6. Shell damage of Pagurus granosimanus at each transect
Figure 7. Shell Damage of Pagurus samuelis at each transect
Figure 8. Fouling of shell inhabited by Pagurus granosimanus
Figure 9. Fouling of shell inhabited by Pagurus samuelis
Figure 10. Overall Shell Fouling
Figure 11. Shell adequacy of Pagurus granosimanus
Figure 12. Shell adequacy of Pagurus samuelis
Figure 13. Affect of shell adequacy on percentage of ovigerous females. Pagurus
granosimanus
Figure 14. Affect of shell adequacy on percentage of ovigerous females. Pagurus
samuelis
Figure 15.
Number of eggs versus clutch weight
Figure 16. Affect of shell adequacy on th reproductive output of Pagurus
granosimanus
5
.

V


1



8




S
G
At

Ju

O


22

3.
27
-
.
8.
o
S
.

S
8 -
8
8
Shield Length (mm)
wAd

Hermit Crabs (%)


18.5
60.5
25.8
12.9
61.3

ENE
8
a
2
Hermit Crabs (%)
22.7
18.2
59

25
61
18.2
30.3
51.5
E
21
1
% intact


% intact
Number
P
25
d avwd
Number
ooON




Number
a
awa
Number
88
PT
5
Number

Number
N08
L
r
awd


number

5

ESE
3
Powpa
number
—


ENE
SESESE

2
5 0
0
n
va
0.745
Adequacy

-
1.009
1.029
1.213
0.94
0.953
0.958
1.037
0.932
ESE
10
9
wa
Adequacy
0.926
1.027
.023
1.068
1.077
.066
1.124
1.148
E
2
+1

w

Ovigerous females %
(out of all females in ovigerous size range)
n
Vud
Ovigerous females %
(out of all females in ovigerous size range)
8 8
id
2pwe
8
Number


31
H
Egg Number
8
L