178 J
.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
of 19.3 60.9 over the original shell size. However, there was again no significant effect
of shell treatment on mean feeding rate; mean feeding rate 6S.E.M. pre-switch5
16.8 61.1 mg h, and post-switch515.161.4 mg h Fig. 3B, df516, t51.391, P5
0.1832. 3.4. Activity level
Activity levels for the hermit crabs ranged from 6 to 3598 squares crossed in 1 h. In 10 out of 19 pairs, the hermit crab in the smaller shell was more active; in seven cases,
the hermit crab in the shell of preferred fit was more active; in two cases, the hermit crabs were equally active Fig. 4A. The mean activity level
6S.E.M. for hermit crabs in tightly fitting shells was 474
6181 squares crossed h. The mean activity level6S.E.M. for hermit crabs occupying shells of preferred fit was 346
675 squares crossed h. This difference in mean activity level was not significant Fig. 4B; df
518, t50.7885, P
50.4407.
4. Discussion
4.1. Growth rate Forcing P
. longicarpus to occupy shells too small for them significantly decreased their growth rate to near zero. This result is in agreement with laboratory studies of at
least four hermit crab species, including P . longicarpus from populations in Texas
Fotheringham, 1976a, Connecticut, and North Carolina Blackstone, 1985. Zero or negative growth is rare in most crustaceans Hartnoll, 1982, although females may stop
growing during the reproductive season. Females of the Japanese species Diogenes nitidimanus occupied tightly fitting shells in the field shell adequacy index less than
1.0 more often than males, and frequently showed zero or negative growth at molt Asakura, 1992.
4.2. Predation risk Inadequate shell fit for P
. longicarpus from Nahant significantly increased the risk of mortality to a natural predator, C
. irroratus, in the laboratory. This result strengthens the results of Vance 1972b, who studied the mortality of a congener, P
. granosimanus, on the North American west coast, but may have confounded his analysis by using the same
predators in multiple trials. Several shell characteristics have been shown to affect hermit crab mortality in the field and laboratory presence of sea anemones on shell:
Brooks, 1988; size and species of shell, and shell damage: Kuhlmann, 1992; presence of hydroid epibionts: Buckley and Ebersole, 1994. However, none of these studies
assessed hermit crab vulnerability as a function of relative shell fit. Vance’s results have not been replicated until now.
Hermit crabs with tightly fitting shells may generally be at increased risk to dexterous predators. Such dexterous predators would include other hermit crabs, brachyuran crabs
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179
Fig. 4. Activity level as function of shell fit for hermit crab P . longicarpus. A Each bar above the line shows
the activity level for a hermit crab having a shell adequacy index of 0.5; each bar below the line shows the activity level for its partner, a hermit crab having a shell adequacy index of 1.0. n
519 pairs. B Overall mean activity level
6S.E.M. for all hermit crabs having shell adequacy index of 0.5 tight fit, and for all hermit crabs having shell adequacy index of 1.0 preferred fit.
with fine chelae, and octopuses. Some other brachyuran crabs known to prey on P .
longicarpus are the blue crab Callinectes sapidus observed attacking P . longicarpus in
Florida by Kuhlmann, 1992 and the green crab Carcinus maenas gut content analyses by Ropes 1968 and Elner 1981 revealed Pagurus spp.
If the increased mortality observed in the laboratory for hermit crabs in small shells reflects a true survival disadvantage in nature, then a fitness cost to growth for these
crabs is likely in the absence of enough available shells. The slowed growth rates for
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.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
hermit crabs occupying small shells may therefore be advantageous, at least in the short term. However, if hermit crabs cannot recoup this lost growth over the long term, then
shell fit-related decreases in growth rate could reduce individual fecundity. This is because most of the variation in reproductive output can be attributed to differences in
body size Wilber, 1989.
4.3. Feeding rate Manipulations of shell fit for P
. longicarpus did not significantly affect their feeding rates in the first laboratory experiment. The second feeding rate experiment also showed
that allowing the crabs to switch into larger shells did not affect mean feeding rate, yet many of the hermit crabs in this treatment did change their feeding rates substantially
after moving into larger shells. Some fed at faster rates, and some at slower rates. This suggests that feeding rate was affected by the change in shell fit, but not in a consistent
direction. Feeding rates under the experimental conditions, where hermit crabs were fed ad libitum and were exempted from having to find or compete for food, may not reflect
foraging efficiency in the field. However, the decrease in growth rate for hermit crabs in tightly fitting shells shown here and in several previous studies noted above was
documented under laboratory conditions. Therefore, a mechanism hypothesized to affect growth rate, e.g., feeding rate, should be observed under laboratory conditions if it is
truly in effect.
Despite the negative laboratory result, there may still be interesting effects of shell fit on the foraging biology of hermit crabs in the field. Using video surveillance, Ramsay
and Hughes 1997 found intense competition among hermit crabs P . bernhardus in the
Irish Sea when there was a limited food resource i.e., small patches of food. The corresponding reduction in feeding success was related to hermit crab size, with the
smallest crabs suffering the greatest loss of feeding opportunity. Whether shell fit affects competitive success for limited food resources is not known.
Besides the influence of competitive interactions on foraging success and ultimate net energy intake, there is also the question of foraging effort. Foraging effort may be
reduced for hermit crabs occupying suboptimal shells e.g., shells too small if it puts them at greater risk to predators. This risk of predation may be immediate, as shown, or
it may be a future risk that is magnified by continued growth in the current shell. Feeding less, thus growing at a slowed rate until a larger shell is obtained, may result
from reducing foraging effort in the field.
The underlying assumption of optimal foraging theory is that animals increase their fitness by raising their rate of net energy intake Begon et al., 1990; Alexander, 1996.
However, actual foraging patterns do not always meet this prediction; for example, conflicting demands such as increased predation risk may cause maximal net energy
intake to threaten an animal’s survival Sih, 1987. For example, among gastropods, there are whelks that scavenge opportunistically on animals being consumed by sea
stars, even though sea stars will attack whelks, too. However, only larger whelks benefit from this kind of supplemental foraging because the smaller, more vulnerable whelks
avoid associating with sea stars Rochette and Himmelman, 1996. Among decapod crustaceans, juvenile lobsters hide under cobbles and feed on the low energy diet of
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181
suspended organic particles available in their shelters, and only actively forage for higher-energy food as adults Wahle, 1992. Similarly, smaller crayfish, to a greater
extent than larger crayfish, reduce foraging in the presence of predators, and increase defensive behaviors such as displaying chelae and burrowing in the sediment Stein and
Magnuson, 1976. It is therefore apparent that predation threat will affect how some animals forage; when risks of predation are great, maximizing energy intake may be
maladaptive. Further studies are needed to track hermit crab foraging effort in the field as a function of shell fit.
4.4. Activity level Increased activity level is most likely correlated with increased energy expenditure.
Therefore, the growth rate differences observed could be explained if hermit crabs in tightly fitting shells were more active, and expending energy at a faster rate. Assuming
increased activity in the laboratory reflected increased activity in the field, high activity in the field would increase the chances of shell encounters, hence improving the
likelihood that a hermit crab in a tightly fitting shell would be able to secure a better-fitting shell. However, shell fit was not found to significantly affect activity levels
in hermit crabs P
. longicarpus matched by size and observed over the same hour in the laboratory. There was a trend for the hermit crabs in tightly fitting shells to be more
active, but the difference was not significant. Increasing the sample size, or repeatedly observing the same pairs over multiple hours on different days may aid detection of
differences in activity level should they exist.
In fact, there is evidence from other studies that supports the hypothesis that hermit crabs occupying shells too small for them are more active. Elwood et al. 1998
measured the ‘startle response’ of hermit crabs P . bernhardus: the time they spent
withdrawn in their shells after being startled with a standardized stimulus. In each trial of their experiment, two hermit crabs were startled as they fought for possession of a
shell. Those hermit crabs that stood to gain a lot from the fight because they currently occupied shells of tight fit startled for significantly less time than crabs in shells of
preferred fit. This indicates an increased motivation of hermit crabs experiencing tight shell fit to acquire new shells.
In another experiment, the persistence of investigation of a new shell unobtainable because the shell was sealed with dental cement was significantly higher for hermit
crabs currently occupying shells of tight fit than for crabs in shells of preferred fit Elwood, 1995. Both experiments show that, for P
. bernhardus, motivation to obtain a new shell is affected by current shell fit. Energy expenditure was not measured directly,
but increased motivational effort expended in pursuing a shell may indeed require more energy.
Rittschof et al. 1995 used a behavioral assay, rather than the physical relationship of crab and shell size, to define shell adequacy. They showed that hermit crabs C
. vittatus occupying tightly fitting shells were attracted to sites where snails were dying indicating
new shell availability, while hermit crabs in shells of preferred size left these sites, and hermit crabs that were in shells too large for them withdrew into their shells and hid.
Hermit crabs predictably showed one of these three behaviors, consistent with their shell
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.E. Angel J. Exp. Mar. Biol. Ecol. 243 2000 169 –184
fit. If hermit crabs occupying shells too small for them are more agitated in the presence of new shells, they might also be more active in their search for new shells to explore, or
other hermit crabs to fight for possession of a shell. Increased locomotion might aid these hermit crabs in their search for new shells, and also affect growth rates in the field
by raising energy consumption.
4.5. Alternative hypotheses While neither feeding rate nor activity level in the laboratory were significantly
affected by shell fit for hermit crab P . longicarpus, growth rate was significantly reduced
for captive hermit crabs occupying shells that were too small. Increased basal respiration rates or decreased assimilation efficiencies are two alternate mechanisms that might be
influencing growth rate. Respiration rates have been measured in terrestrial hermit crabs put on treadmills Herreid and Full, 1986, but not for aquatic hermit crabs such as P
. longicarpus. Assimilation rates have not been measured in hermit crabs, but probably
could be, given that hermit crab feces are robust in seawater, and could be collected and analyzed. Exploring these alternative hypotheses may shed more light on the explanation
for the growth rate decline observed.
5. Conclusion
