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.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
is well documented Scully, 1979; McClintock, 1985; Wada et al., 1997. In reality, there are rarely enough shells of the right sizes for all the hermit crabs in a population
e.g., Vance, 1972a; Scully, 1979. Such shell limitation forces many hermit crabs to occupy shells that are the wrong size for them; often the shells are too small.
Shells of inadequate size can increase the risk of both desiccation and predation. Mortality from desiccation at low tide increased for pagurid hermit crabs in shells that
were too small for them Taylor, 1981. The hermit crab Pagurus granosimanus was significantly more vulnerable to predation by the brachyuran crab Cancer gracilis when
the hermit crab was unable to retreat completely into its shell Vance, 1972b. Whether inadequate shell fit increases risk of predation in other pagurid species has not been
examined.
When confined to shells that were too small for them, the temperate hermit crabs Pagurus bernhardus Markham, 1968, Pagurus pollicaris Fotheringham, 1976a,
Pagurus longicarpus Fotheringham, 1976a; Blackstone, 1985, and Clibanarius vittatus Fotheringham, 1976b grew more slowly. Nothing is known of the mechanisms
regulating the reduced growth rate observed in hermit crabs with tight shell fit. Possible mechanisms that could mediate growth rate declines include increased metabolic
activity, decreased feeding activity, or decreased food assimilation efficiency.
While hunting or scavenging food, lobsters and true crabs must often leave shelter and expose themselves to potential predators. In contrast, the hermit crab, a scavenger and
filter feeder, carries shelter with it at all times Hazlett, 1981. However, a hermit crab’s chances of avoiding predation are only as good as its shell protection. This mobile
protection is probably less effective if a hermit crab has outgrown its shell, and is unable to withdraw its body fully inside. Thus, for a hermit crab in a shell-limited environment,
maximal growth best achieved by maximal net energy intake can be at odds with the need for protection. Because there is strong evidence of a behavioral component to the
hermit crab’s assessment and improvement of shell fit Elwood and Neil, 1992; Hazlett, 1996; Wada et al., 1997, it is likely that a quantifiable behavioral change contributes to
any changes in growth rate the hermit crab experiences.
In the summer of 1997, approximately a quarter of the individuals of P . longicarpus at
Nahant occupied tightly fitting shells personal observation, making research of effects of tight shell fit relevant. In this study, it was first determined whether growth rate
decreased for hermit crabs confined to tightly fitting shells. Then, ultimate and proximate mechanisms that might influence growth rate were examined.
2. Methods
2.1. Animals and study site P
. longicarpus, the long-wristed hermit crab, is one of the most common shallow- water decapods along the coast of the Eastern United States and in the Gulf of Mexico
Williams, 1984. Hermit crabs in this study were hand-collected at low tide from the sandflat on the bay side of the peninsula of Nahant, MA, USA.
J .E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
171
2.2. Shell adequacy index The methods used to determine the shell fit preferred by P
. longicarpus at Nahant were pioneered by Vance 1972a. Fifty hermit crabs occupying shells of Littorina
littorea were collected from the field site in June, 1997. Shells of the periwinkle, L .
littorea, are the dominant shell type used by the study population personal observation. The hermit crabs were introduced to an aquarium filled with circulating seawater and
250 empty shells, making a total of 300 shells available for occupation. Empty shells were prepared by collecting live L
. littorea from one rock surface at Nahant, boiling and removing the flesh, rinsing in seawater, and air-drying. The shells ranged in size from 5
to 22 mm in aperture length. The hermit crabs were allowed 48 h to choose new shells. The shells occupied at this time were presumed to be of preferred size since the crabs
had ceased exploring and moving into new shells. Crabs were then removed from their chosen shells. Each crab was blotted of excess water and massed to the nearest 0.1 mg.
The aperture length of the shell occupied by each crab was measured to the nearest 0.1 mm using calipers.
Measurements mass of crab and shell aperture length were log-transformed and plotted. The best fit line describing the relationship between crab mass and preferred
2
shell size was determined using least-squares regression r 5 0.8625, P , 0.0001.
log shell aperture length 5 0.2623log crab mass 1 0.4342
1 Shell adequacy index is defined for any crab-shell combination as the ratio of predicted
crab mass to actual crab mass. Thus, a hermit crab that occupies a shell of preferred size as predicted by Eq. 1 will have a shell adequacy index
51.0. A 500 mg hermit crab that occupies a shell predicted to be the preferred size for a crab half its mass, a 250 mg
crab, has a shell adequacy index of 0.5. Throughout this study, shell fit of experimental hermit crabs was manipulated to yield
a shell adequacy index of either 0.5 tight fit or 1.0 preferred fit. When hermit crabs with a shell adequacy index of 0.5 retreated into the shell, they were unable to withdraw
their chelae behind the shell aperture, allowing predatory crabs to grasp and pull these hermit crabs from the shell. Hermit crabs with a shell adequacy index of 1.0 could
withdraw completely into their shells.
2.3. Growth rate Twenty-eight juvenile hermit crabs were collected in September, 1997, pulled from
the shells occupied at time of collection and massed to the nearest 0.1 mg. The hermit crabs were paired by mass, for a total of 14 pairs, and randomly assigned a shell
treatment either ‘preferred fit’ or ‘tight fit’, as described in Section 2.2. The hermit crabs were maintained individually at 18
8C in 30 ppt salinity seawater. Each hermit crab was held in an 82 mm diameter by 32 mm deep glass dish. Every 2–3 days, the dishes
were cleaned and the seawater was replaced with freshly aerated seawater. Hermit crabs were fed a diet of shrimp pellets Wardley, Secaucus, NJ every 3 days. They were fed
imitation crab meat key ingredient: pollock fish; Star Market, Cambridge, MA on the
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.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
days when feeding rate was measured described in Section 2.5.2. Final wet masses were measured after removing each hermit crab from its assigned shell after 89 days.
Growth rate was calculated as the difference between final and initial wet mass divided by time mg day. One hermit crab died, thus data were available for 13 pairs.
2.4. Predation risk Cancer irroratus Say 1817, a common North Atlantic rock crab family Cancridae
coexists with the population of P . longicarpus at Nahant. C. irroratus is known to prey
on pagurid hermit crabs in the New York Bight Stehlik, 1993 and in kelp beds off Nova Scotia Drummond-Davis et al., 1982.
Individuals of C . irroratus were collected from White Beach, Manchester-by-the-Sea,
MA. Although C . irroratus inhabits the field site at Nahant, it was more abundant and
easier to collect at this site 15 miles north of Nahant. Collections were made on May 29, June 15, and June 19, 1998. Eight males and three non-gravid females were collected.
All predators were maintained in continuously flowing seawater provided via pipeline from surrounding ocean. Temperatures ranged from 9 to 18
8C, reflecting natural increases in field temperatures from late May to late June, 1998, and the salinity
averaged 30 ppt. Predators were fed crushed blue mussel Mytilus edulis every 2–3 days. Prior to use in the predation experiments, the predators were isolated in mesh-walled
plastic containers 320 32303150 mm and starved at least 3 days.
Twenty-two hermit crabs were collected from Nahant. Each hermit crab was pulled from its shell, massed to the nearest 10 mg, and paired by mass with another hermit
crab. The hermit crabs were not sexed, but none was ovigerous. Each member of the pair was randomly assigned to receive one of two shell treatments, ‘preferred fit’ or ‘tight
fit’, as described in Section 2.2.
Each hermit crab was isolated in a 100 ml plastic cup filled with beach sand to a depth of 20 mm and covered with nylon mesh, then submerged in seawater. Like the predators,
they were held in a sea table receiving continuous water flow. All the hermit crabs received a diet of crushed blue mussel and shrimp pellets, and were fed every 2–3 days.
Each pair of hermit crabs adjusted to the shell treatments at least 4 days before being offered to a predator.
Each predator was moved to a glass aquarium 400 32103250 mm receiving
continuous seawater flow. Two to 3 days later, a pair of hermit crabs was introduced into the aquarium. All interactions between predator and hermit crabs were recorded.
Observations were continued until the predator wounded at least one of the hermit crabs; only the eleventh trial was not continuously observed.
The pairs of hermit crabs were left with the predators for two nights trials 1–10 or three nights trial 11. At the end of this time, damage or mortality was assessed. Then,
to be certain that the predator was not satiated, the predator was offered crushed mussel immediately after its use in the predation trial. The predator was considered satiated if it
failed to feed on the mussel within 5 min. Satiation was important to assess, particularly in cases where only one of the two hermit crabs was eaten, in order to eliminate the
possibility that the second hermit crab was spared simply because the predator was no longer hungry after eating the first. However, none of the 11 predators was satiated.
J .E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
173
The dependence of hermit crab mortality on shell adequacy index was analyzed using Fisher’s exact test Ghent, 1996. Each predator was used only once, and surviving
hermit crabs were not used again. 2.5. Feeding rate
2.5.1. Assay development To determine feeding rates in P
. longicarpus, amount of food eaten over time was measured. Imitation crab meat as described in Section 2.3, which neither gained mass
in seawater nor crumbled in seawater, was the food used in the assay. At the end of the feeding period, food fragments not eaten by the hermit crabs were easily collected from
the glass dishes housing the hermit crabs, and then re-massed.
In a preliminary experiment, feeding rates as a function of hermit crab size were measured weekly for 3 weeks. As in the growth rate experiment, hermit crabs were
housed in glass dishes in 30 ppt salinity seawater, this time at 23 8C. Each hermit crab
was starved for 2 days, then given a piece of meat of a mass between 250.0 and 500.0 mg mass was measured to the nearest 0.1 mg after the food soaked 15 min in seawater.
After hermit crabs fed for 5 h, the food was removed and massed. To determine feeding rates mg h, final food mass was subtracted from initial food mass and divided by assay
duration.
Hermit crab size was assessed by measuring the anterior carapace length defined by Markham, 1968 as the length of the ‘hard portion of carapace’ to the nearest 0.1 mm at
12 3 power using a Zeiss dissecting microscope fitted with an ocular micrometer.
Feeding rates varied from barely detectable in the smallest crabs to one record of 35 mg h in the largest crab Fig. 1. The mean feeding rate of three trials increased
2
linearly with crab size r 50.8694, P,0.0001. These results are in agreement with
feeding rates reported for Pagurus acadianus, a larger relative of P . longicarpus. Scarratt
and Godin 1992 reported feeding rates of 160 mg over 8 h, or 20 mg h, for P .
acadianus feeding on haddock. This was for hermit crabs of a mass of approximately 1.5 g, which is about 20–30 larger than the average P
. longicarpus used for assay development.
This preliminary result gave me confidence in my methods. I used this protocol in all subsequent feeding assays.
2.5.2. Feeding rate experiment 1 During the 12 weeks that growth rates were monitored for 14 hermit crab pairs
methods above, feeding rates were measured in weeks 2, 3, and 5 each time after hermit crabs were starved 2 days. Hermit crabs were given pieces of food with initial
wet masses of 600.0–750.0 mg, and were allowed to feed for an average of 5 h. To determine shell treatment effects ‘preferred fit’ and ‘tight fit’ on feeding rate, a t
statistic was calculated.
2.5.3. Feeding rate experiment 2 Thirty-seven large male hermit crabs were collected from Nahant in June, 1997. These
crabs were not massed or otherwise measured; however, none of the hermit crabs could
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.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
Fig. 1. Feeding rate as function of size for hermit crab P . longicarpus. Mean feeding rate
6S.D. is shown as a function of anterior carapace length. Each point represents the mean of three measurements. n
514 hermit crabs.
withdraw their chelae into their shells. Each crab was isolated in a glass dish of 30 ppt salinity seawater at 18
8C, and starved for 2 days before each assay. The hermit crabs were fed only during the assays. For each individual, feeding rates were measured three
to five times in the first 2 weeks of captivity. After 2 weeks, 17 of the crabs were each offered a choice of three larger shells to
move into. All of them switched into larger shells shell switchers. The other 20 crabs were denied the opportunity to switch control. Feeding rates were then re-measured
three to five times for each hermit crab in the two treatments control and shell switchers during the third and fourth weeks of captivity. To determine shell treatment
effects on feeding rate, a t statistic was calculated.
2.6. Activity level Thirty-eight hermit crabs were collected from Nahant in June and July, 1998. Each
hermit crab was pulled from its shell, massed to the nearest 10 mg, and paired with another hermit crab, for a total of 19 pairs. The hermit crabs were not sexed, but none
was ovigerous. Each member of the pair was randomly assigned to receive one of two shell treatments, ‘preferred fit’ or ‘tight fit’, as described in Section 2.2. Each hermit
crab was isolated in a glass dish of 30 ppt salinity seawater at 15.5
8C, and received clean seawater after being fed shrimp pellets every 2–3 days. All the hermit crabs were kept
under the same lighting conditions 12L:12D. After adjusting to their new shells for a minimum of 2 days, each hermit crab and its partner were participants in an activity
assay.
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Activity was monitored for 1 h intervals using a Sony Hi 8 mm video camcorder. The two hermit crabs in each pair were placed on either side assignment to sides was
random of a glass aquarium 400 32103250 mm divided down the middle by a
perforated, opaque plastic tank divider Penn-Plax, New York. A black-on-white paper grid of 25 mm squares was affixed to the outside of the tank’s bottom surface. There
were an equal number of squares marked out on each side of the divider. Seawater 24
8C, 30 ppt covered the crabs, and was replaced for each new pair of crabs observed. The hermit crabs acclimated to their new environment for 1 h.
Each pair of hermit crabs was then recorded for 1 h. The recording room was free of visual and auditory distractions, such as human movement. Both hermit crabs in each
pair received the same light intensity approximately 350 lux from an overhead fluorescent lamp, and because the tank divider was perforated, the paired crabs shared
the same seawater environment.
To analyze the data, the videotape was reviewed at high speed. Activity level was defined as the number of squares on the grid crossed by each hermit crab during the 1 h
of observation. To determine shell treatment effects on activity level, a t statistic was calculated.
3. Results
