Ecological relations between hermit crabs and their shell-supplying gastropods: Constrained consumers

Journal of Experimental Marine Biology and Ecology 397 (2011) 65–70

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Journal of Experimental Marine Biology and Ecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e

Ecological relations between hermit crabs and their shell-supplying gastropods: Constrained consumers Mark E. Laidre ⁎ Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544, USA

a r t i c l e

i n f o

Article history: Received 7 September 2010 Received in revised form 26 October 2010 Accepted 26 October 2010 Keywords: Biological constraints Crustacea Ecological dependency Gastropod shells Hermit crabs Snails

a b s t r a c t Hermit crabs are critically dependent upon gastropod shells for their survival and reproductive fitness. While anecdotal reports have suggested that hermit crabs may be capable of removing live gastropods from their shells to access the essential shell resource, no systematic experiments have been conducted to investigate this possibility. This paper reports experiments on both marine (Pagurus bernhardus) and terrestrial (Coenobita compressus) hermit crabs in which crabs were paired in the laboratory with the gastropods whose shells they inhabit in the field. Pairings included both shelled and naked crabs and spanned the full range of the gastropod life cycle. Neither marine nor terrestrial hermit crabs were successful at removing live gastropods from their shells. Furthermore, only a small fraction of the crabs (5.7%) were capable of accessing shells in which the gastropod had been killed in advance, with its body left intact inside the shell. Finally, although hermit crabs readily entered empty shells positioned on the surface, few crabs (14.3%) were able to access empty shells that were buried just centimeters beneath them. These results suggest that hermit crabs are constrained consumers, with the shells they seek only being accessible during a narrow time window, which begins following natural gastropod death and bodily decomposition and which typically ends when the gastropod's remnant shell has been buried by tidal forces. Further experiments are needed on more species of hermit crabs as well as fine-grained measurements of (i) the mechanical force required to pull a gastropod body from its shell and (ii) the maximum corresponding force that can be generated by different hermit crab species' chelipeds. © 2010 Elsevier B.V. All rights reserved.

‘Whether the crab had simply appropriated the vacant home of a deceased whelk, or whether it had forcibly ejected the owner of the shell—added “murder to piracy”—was the question to be decided.’ –Jackson (1913, p. 61)

1. Introduction The ecology of most organisms encompasses a set of complex interdependencies in which any given species is generally reliant upon the resources produced by one or more other species. A prime example of such ecological reliance is the case of hermit crabs (Decapoda, Anomura). Rather than building their own fully armored exoskeleton these crustaceans rely on an externally derived form of cover, the shells of gastropods (Hazlett, 1981). Crabs carry around shells effectively as

⁎ Current address: Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA. E-mail address: [email protected]. 0022-0981/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2010.10.024

portable ‘homes’—a behavior which has been classified as a form of animal tool-use (Beck, 1980)—and as a consequence crabs obtain protection for their soft un-calcified abdomens. Indeed, the asymmetrical coiling of a hermit's abdomen is specially fit for shell occupation, and shells seem to fulfill a variety of critical survival and reproductive functions for hermits, including: resistance to desiccation, safeguards against parasites and predators, and shelters from abrasive sand and other environmental stresses (Vance, 1972; Hazlett, 1981; Lancaster, 1988). It has been suggested that shells are a limiting resource for hermit crabs (Fothenngham, 1976; Kellogg, 1976), with crabs in nature often being found in smaller than their preferred size shells (Childress, 1972; Bertness, 1981). Yet because crabs cannot build shells themselves their only possible source of shells is either gastropods, “the original possessors and builders of the house” as Jackson (1913, p. 71) called them, or secondary sources, such as empty shells that have been abandoned or shells that are worn by other crabs. Prior research on the process of shell acquisition by hermit crabs has focused mostly on these secondary sources, examining (1) how crabs ‘negotiate’ shell exchanges with conspecifics (Hazlett, 1978, 1980; Briffa et al., 1998), (2) what preferences crabs have for particular sizes or species of uninhabited shells (Reese, 1963; Elwood and Neil, 1992), and (3) the means by which crabs are attracted to sites of gastropod death or predation, where brand new empty shells have recently

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M.E. Laidre / Journal of Experimental Marine Biology and Ecology 397 (2011) 65–70

become available (McLean, 1974; Rittschof, 1980; Wilber and Herrnkind, 1984). Few studies, in contrast, have examined whether hermit crabs are capable of acquiring shells directly from the primary source, the gastropods themselves. Whether direct shell acquisition from gastropods is possible has both evolutionary and ecological importance. Evolutionarily, the adequacy of crabs' shells can constrain their personal reproductive success, altering their susceptibility to predation (Vance, 1972), their ability to signal and take risks in intraspecific conflicts (Laidre, 2007), and the maximal number of eggs females can carry (Elwood et al., 1995). Also, on a broader ecological scale, the availability of shells can constrain a species' population size, limiting the number of crabs that can thrive in a given area (Kellogg, 1976). If crabs could target shells still occupied by gastropods, then these ecological and evolutionary constraints would be reduced and the raw number of shells and the available range of shells to select from would increase dramatically. Interestingly, some studies have reported that hermit crabs may be capable of removing live gastropods from their shells (e.g., Brightwell, 1951, 1953; Randall, 1964; Rutherford, 1977). For instance, in the common European hermit crab (Pagurus bernhardus), Brightwell (1951) reported that “whelks were invariably set upon by bernhardus, and pulled out of their shells” (p. 283). Aside from such anecdotal reports, however, I am unaware of any published studies systematically testing whether crabs can access the shells of live gastropods, or testing whether crabs can access the shells of dead gastropods whose body still remains intact within the shell. Although Jackson (1913) posed the fundamental question nearly a century ago, there appear to be no experimentally controlled tests of hermit crabs' abilities to remove gastropods from their shells. Authorities on hermit crabs that I consulted (personal communications from: M. Bertness; R. Elwood; B. Hazlett; D. Rittschof; and G. Vermeij) were likewise unaware of any such studies; though I have recently been informed that a pilot study on this topic is in progress on Pagurus longicarpus (personal communication from R. Rotjan). The objective of the present study was to use behavioral experiments in the laboratory and field, in which crabs were paired with gastropods in various situations, to answer a fundamental question about the broader ecology of the hermit clade: how constrained are hermit crabs in their ability to acquire the shells that are so essential to their survival and reproduction? 2. Materials and methods A series of controlled laboratory experiments was carried out to examine the extent to which hermit crabs could access gastropod shells under varying conditions. These conditions included: (i) whether crabs were already housed or were naked; (ii) whether gastropods were living or dead; (iii) for dead gastropods whether the gastropod bodies remained within their shells or had been removed in advance to generate empty shells; and (iv) for empty shells whether the shells were positioned on the surface or buried beneath the sand. By varying these conditions it was possible to demarcate the limitations hermit crabs experience when attempting to acquire shells across the entire gastropod life cycle (from a living gastropod up to a dead gastropod whose body has decomposed completely and whose leftover shell had been buried by tidal action). 2.1. Study species Experiments were carried out on both marine hermit crabs (Pagurus bernhardus) and terrestrial hermit crabs (Coenobita compressus). Both of the chosen study species are abundant, widely distributed hermit crab species. P. bernhardus—the same species that was anecdotally reported to remove living gastropods from their shells (see Introduction)—dominates the intertidal rock pools on the Atlantic coastline of Europe. And C. compressus—one of just twelve known terrestrial hermit crab species

(Briffa and Mowles, 2008)—dominates the tropical beaches on the Pacific coastline of Central America. P. bernhardus was studied off the coast of County Down, Northern Ireland along with the sympatric gastropod species (Buccinum undatum, Gibbula cineraria, Littorina littorea, L. obtusata, and Nucella lapillus) whose shells P. bernhardus commonly inhabits. These five gastropod species occur in the very same tide pools in the littoral zone that P. bernhardus occupies. C. compressus was studied in the Osa Peninsula of Costa Rica along with the sympatric gastropod species (Nerita scabricosta) whose shells C. compressus most commonly inhabits (Abrams, 1978). This gastropod species is found on rocky outcroppings in the same area of the beach that C. compressus regularly traverses. For the experiments, crabs and gastropods were gathered in their zone of overlap, where they were observed interacting naturally, and were then transported less than 1 h away for testing in the laboratory. Experiments on P. bernhardus were carried out during Jul – Sept 2006, May – Sept 2007, Jun – Aug 2008, and Jun – Sept 2009; and experiments on C. compressus were carried out during March – Apr 2008 and Feb – Apr 2010. Further details on the specific study populations and behavior of the two test species can be found in Laidre (2007), Laidre and Elwood (2008), and Laidre (2009) for P. bernhardus and in Laidre (2010) for C. compressus.

2.2. General experimental protocol Marine crabs (P. bernhardus) and their gastropods were maintained in containers filled with natural seawater. Terrestrial crabs (C. compressus) and their gastropods were maintained in containers with natural beach sand as a substrate. While C. compressus could be kept at the surrounding air temperature, given its tropical lifestyle, the temperate zone P. bernhardus required a temperature controlled room (12 ºC), which was set on a 12 h day/12 h night lighting system, with the water aerated using bubblers. In each experiment crabs were given 24 h or more to access gastropod shells. For experiments involving individually isolated crabs, P. bernhardus was kept in glass Pyrex dishes (10 cm diameter, 5 cm height) and the slightly larger C. compressus was kept in empty pickle jars (10 cm diameter, 14 cm height). Only crabs that had all appendages intact and were free of parasites were used in the experiments. Crabs were paired with gastropods whose shell was of the same species as and whose shell diameter was within ± 3 mm of the original shell the crab had inhabited in the field. The gastropod's shell was often chosen to be slightly larger than the crab's original field shell to increase the crab's motivation for shell acquisition. All specimens tested for both hermit crab species occupied shells with diameters between 1 and 3 cm. After being tested crabs were returned to the original spot where they were collected in the field. Below the specific objectives and conditions of each experiment are detailed. Experiments 1, 2, 3, 4, and 6 focused on P. bernhardus and Experiment 5 focused on C. compressus.

2.3. Experiment 1: can shelled crabs remove live gastropods from their shells? This experiment tested whether shelled crabs could acquire shells from live gastropods. In this experiment, crabs (P. bernhardus) occupying their original field shells were group housed in a large plastic tub (45 × 30 cm, 15 cm height). Live gastropods were added to this tub and the state of these gastropods was then assessed after 48 h by gently poking a toothpick into the shell aperture—an act which causes healthy gastropods to retract into the shell and close their opercula. If crabs are able to access the shells of live gastropods, then some of the gastropods would be expected to have been killed or damaged.

M.E. Laidre / Journal of Experimental Marine Biology and Ecology 397 (2011) 65–70

2.4. Experiment 2: can naked crabs remove live gastropods from their shells? This experiment tested whether naked crabs (which are maximally shell-motivated) could acquire shells from live gastropods. In this experiment, crabs (P. bernhardus) were removed from their original field shells and were individually isolated in dishes with live gastropods for 48 h. At 12-h intervals I recorded the positioning of the gastropod, whether the hermit crab was in contact with the gastropod, and what parts of the gastropod it was contacting. At the end of the 48 h the following parameters were assessed: the state of the gastropod (living or dead), whether the crab had injured or eaten the gastropod, and whether the gastropod's body was still intact within the shell. If naked crabs are able to access the shells of live gastropods, then some of the gastropods would be expected to have been killed or damaged. At the end of the 48 h any gastropod that was still alive was removed from its dish and placed in boiling water for 10 min. Boiling killed the gastropods and allowed their bodies to be readily removed from their shells using forceps. After cooling the gastropod's body and its empty shell for 10 min both were then provided to the original crab, which was monitored for 1 h to see if it would now enter the shell and/or eat the gastropod's body. If crabs that had not previously killed their live gastropod now entered its empty shell and consumed its boiled body, it would suggest they had been constrained to access these housing and food resources while the gastropod was living.

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The comparison of how readily live vs. boiled gastropods can be removed from their shells by a human is relevant to the constraints hermit crabs may experience in accessing shells: if live gastropods are substantially more difficult to remove from their shells than boiled gastropods for a human using forceps, and if hermit crabs show little or no ability to remove even boiled gastropods (see Experiment 3), then together these results would underscore how far beyond crabs' abilities it would be for them to remove live gastropods from their shells. 2.7. Experiment 5: can terrestrial crabs remove gastropods from their shells? This experiment tested whether terrestrial crabs that were shelled or naked could acquire shells from live gastropods. In this experiment, crabs (C. compressus) were individually isolated in jars with live gastropods for 48 h. During the first 24 h crabs were left in their original field shells. At the end of this 24 h period if a crab had not accessed the gastropod's shell, then it was removed from its original field shell and left naked with the same gastropod for another 24 h. At the end of this second 24 h period if a crab had still not accessed the gastropod's shell, then the gastropod was removed and boiled for 10 min (killing it), its body was pulled from its shell, and its empty shell was then reintroduced to the crab, which was given another 24 h to access the shell. Altogether, Experiment 5 therefore lasted 72 h. 2.8. Experiment 6: can naked crabs access buried shells?

2.5. Experiment 3: can naked crabs remove boiled gastropods from their shells? This experiment tested whether naked crabs could acquire shells from gastropods that had been boiled. Since boiling kills the gastropod and also eliminates the adhesion of the gastropod's body to the shell apex, boiled gastropods were predicted to be easier for hermit crabs to pull from their shells than live gastropods. In this experiment, crabs (P. bernhardus) were removed from their original field shells and were individually isolated in dishes with gastropods that had been boiled for 10 min. After boiling, the gastropod body was left inside the shell and the entire shell-body complex was submerged in cool water for 10 min before being introduced to the crab. Each naked crab and boiled gastropod were then kept together for 24 h. At the end of the 24 h I assessed whether the crab had removed the gastropod's boiled body from the shell and whether it had entered the shell. If naked crabs are able to access the shells of boiled gastropods, then some of the gastropods would be expected to have been pulled completely out of their shell. As a comparison, to see how readily crabs would enter boiled gastropod shells that were emptied of their contents in advance, I carried out the same steps described above except I pulled out the boiled gastropod body before providing the shell to the crab. 2.6. Experiment 4: how hard is it to remove live gastropods from their shells? This experiment compared how effectively a human with forceps could remove live gastropods vs. boiled gastropods from their shells. In Experiments 2 and 3, the bodies of boiled gastropods were all readily removed from their shells by a human exerting a gentle tug with forceps controlled by the pointer finger and thumb. To test how readily live specimens could be removed from their shells over a hundred live gastropods representing a total of five species (Buccinum undatum, Gibbula cineraria, Littorina littorea, L. obtusata, and Nucella lapillus) were randomly selected in the field. The author then attempted to pull each gastropod out of its shell using the same forceps technique that had been used with boiled specimens.

If the shell of a dead gastropod is not acquired by a hermit crab, then the shell may ultimately become buried beneath the surface of the sand by the tide. Hermit crabs (Pagurus spp.) are known to be capable of digging themselves deeply into the sand (Rebach, 1974). This experiment tested whether naked crabs could acquire empty shells that had been buried. In this experiment, crabs (P. bernhardus) were removed from their original field shells and were individually isolated in dishes with a layer of sand 2–3 cm deep. At the base of each dish a single empty shell was buried. The shell was packed tight with sand and was placed with its aperture facing down. Shells in this experiment had a 1 cm diameter, such that crabs would have to dig through 1–2 cm of sand to access them. The sand was packed to the consistency found in the field and crabs were given 24 h to access the buried shell. For crabs that were unable to access the buried shell after 24 h I brought the shell to the surface (still keeping it packed to the brim with sand) and gave them another 24 h to access the sand-filled shell on the surface. 3. Results 3.1. Experiment 1: can shelled crabs remove live gastropods from their shells? Of the N = 15 live gastropods housed together with N = 100 crabs, all the gastropods remained alive and unharmed after 48 h. Shelled crabs thus appeared unable to access the shells of live gastropods. 3.2. Experiment 2: can naked crabs remove live gastropods from their shells? Although naked crabs contacted gastropods throughout the 48 h period they were housed with them (Table 1), they typically did so in position that would not have enabled them to pry the gastropod from its shell (e.g., chelipeds inserted into aperture). Rather, crabs tended mostly to cling to the outside of the gastropod's shell and occasionally tried to insert their abdomen into the aperture but were blocked by the gastropods' opercula (Video S1). None of the naked crabs were able to access the shells of the gastropods or damage the gastropods in

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Table 1 Percentage of naked Pagurus bernhardus hermit crabs (N = 35) positioned in different ways relative to the live gastropods they were paired with (N = 5 Gibbula cineraria, N = 21 Littorina littorea, and N = 9 L. obtusata). Position of crab relative to gastropod

Overall

Abdomen in aperturea Chelipeds in apertureb Clingingc Not touchingd Gastropod inaccessiblee

8.6% 10.0% 25.7% 30.7% 25.0%

Specific time point 12 h

24 h

36 h

48 h

2.9% 11.4% 22.9% 37.1% 25.7%

5.7% 14.3% 25.7% 31.4% 22.9%

20.0% 8.6% 22.9% 25.7% 22.9%

5.7% 5.7% 31.4% 28.6% 28.6%

a

Crab's abdomen inserted into shell aperture. Crab's cheliped or chelipeds inserted into shell aperture. c Crab clinging to outside of gastropod's shell (no part of crab inserted into shell aperture). d Crab not touching gastropod, though gastropod still accessible beneath waterline. e Gastropod inaccessible to crab, since it was above the waterline. b

any way. At the end of the 48 h when the gastropods were boiled and their bodies were removed from their shells 94.3% (of N = 35 crabs) entered the empty shell and 60% of them fed upon the gastropod's boiled body. 3.3. Experiment 3: can naked crabs remove boiled gastropods from their shells? Few of the N = 53 crabs were able to access the shells of boiled gastropods whose bodies had been left inside their shells. In contrast, all N = 56 crabs that were given a boiled gastropod in which the body had been removed in advance entered the shell (Table 2). Crabs evidently could not easily pull out the bodies of boiled gastropods from their shells. 3.4. Experiment 4: how hard is it to remove live gastropods from their shells? While boiled gastropods presented no difficulty for a human to pull out in Experiments 2 and 3, the same was not true for live gastropods. With boiled gastropods I had been able to remove the body with forceps virtually effortlessly: the entire body would slip out of the shell usually in 3 s or less per gastropod and while employing minimal force. In contrast, with live gastropods despite the application of substantially more force and despite spending up to 5 min per gastropod (two orders of magnitude the time it took to remove each boiled gastropod) I successful removed only a small fraction of live gastropods, all from the genus Littorina (Table 3). Given that the hermit crabs in Experiment 3 showed hardly any capability for removing the easier-to-pull-out boiled gastropods, these results suggested it would be far beyond a hermit crab's abilities to pull live gastropods from their shells. Table 2 Number of naked Pagurus bernhardus crabs able to enter boiled gastropod shells in which the gastropod body had been left inside the shell or had been removed in advance. Experimental condition

No. crabs

Boiled gastropod shell with body left inside shell Boiled gastropod shell with body removed

53a

a

56b

No. (proportion) able to enter shell 3 (5.7%)c

Table 3 Success of a human in pulling live gastropods out of their shells using forceps. Gastropod species

No. live specimens

No. (proportion) that could be pulled out

Buccinum undatum Gibbula cineraria Littorina littorea L. obtusata Nucella lapillus Overall

2 22 35 43 15 117

0 (0%) 0 (0%) 2 (5.7%) 8 (18.6%) 0 (0%) 10 (8.6%)

3.5. Experiment 5: can terrestrial crabs remove gastropods from their shells? None of the N = 44 crabs were able to access the shell of the live gastropod with which they were paired during the first 24 h period (in which crabs were still in their original field shell) or during the second 24 h period (in which crabs were naked). In contrast, nearly all of these N = 44 crabs entered the empty shell provided to them during the third 24 h (in which the gastropod they had been paired with was boiled and its body was removed from its shell beforehand; Table 4). 3.6. Experiment 6: can naked crabs access buried shells? Crabs in this experiment were frequently observed burying their bodies, with only their eyestalks poking above the sand line. Few crabs, however, were able to access the buried shell in their dish within the 24 h period. When the shells were subsequently brought to the surface though nearly all crabs that had previously been unsuccessful now cleaned the sand out from the shell and entered it within 1 h (Table 5). 4. Discussion In his detailed monograph on the common European hermit crab (Pagurus bernhardus), Jackson (1913) speculated about whether crabs might acquire one of their most essential resources, their shell, directly from living gastropods. While some anecdotal reports exist to suggest that hermit crabs might indeed possess this capacity (see Introduction), there have been no systematic tests. The present study attempted to clarify the limits of shell acquisition in hermit crabs by experimentally examining the interaction between the resource suppliers (gastropods) and the resource-users (hermit crabs) under a variety of conditions. The results suggest that both marine and terrestrial hermit crabs (Pagurus bernhardus and Coenobita compressus) are incapable of removing live gastropods from their shells. Although a live gastropod may embody both a home and a meal to hermit crabs (in the form of the gastropod's shell and body, respectively), these resources seem to be completely inaccessible until after a gastropod dies naturally. Even then, hermit crabs are still constrained: additional experiments on Table 4 Percentage of Coenobita compressus crabs entering Nerita scabricosta gastropod shells over a 72 h time period. Experimental conditions for each 24 h block are described below. No. crabs

56 (100%)

The crabs received the following shells: N = 1 Buccinum undatum, N = 12 Gibbula cineraria, N = 11 Littorina littorea, N = 24 L. obtusata, and N = 5 Nucella lapillus. b The crabs received the following shells: N = 12 Gibbula cineraria, N = 15 Littorina littorea, N = 22 L. obtusata, and N = 7 Nucella lapillus. c The crabs entered the following shells: N = 1 Gibbula cineraria, N = 1 L. obtusata, and N = 1 Nucella lapillus.

44 a

Proportion entering shells in each time period 0–24 ha

24–48 hb

48–72 hc

0%

0%

95.5%

During this time period shelled crabs were paired with live gastropods. During this time period naked crabs (their shell having been removed at 24 h) were paired with live gastropods. c During this time period naked crabs were paired with the empty shells of boiled gastropods (the bodies of these boiled gastropods having been removed from the shell after boiling). b

M.E. Laidre / Journal of Experimental Marine Biology and Ecology 397 (2011) 65–70 Table 5 Number of Pagurus bernhardus crabs able to enter buried gastropod shells. Experimental condition

No. crabs

No. (proportion) able to enter shell

Empty gastropod shell packed full of sand and buried beneath the surface

28a

4 (14.3%)b

a The crabs received the following shells: N = 4 Gibbula cineraria, N = 7 Littorina littorea, N = 14 L. obtusata, and N = 3 Nucella lapillus. b The crabs entered the following shells: N = 2 Littorina littorea and N = 2 Nucella lapillus. For the other 24 crabs that were unable to access the buried shell after 24 h I brought the shell to the surface (still keeping it packed to the brim with sand). All but one of these 24 crabs (95.8%) then managed to clean the sand out and enter the shell within 1 h.

P. bernhardus suggested that hermit crabs have severe difficulty accessing the shells of gastropods that have been killed but whose body remains inside the shell. It thus seems that shells with any type of gastropod body (living or dead) remaining inside are significant barriers to hermit crabs: the body must either be removed beforehand by a heterospecific predator (e.g., McLean, 1974; Wilber and Herrnkind, 1984) or the body must decompose naturally. Moreover, once a gastropod's body has decomposed and its empty shell has ultimately been deposited beneath the surface of the sand, this too presents a major hurdle for hermit crabs if they are to acquire the shell. In some habitats though shell deposition may be limited (e.g., by tide pools with solid rock bottoms), and natural ecological processes, such as wind and tides, might also even unearth shells that were previously buried. But these local ecological variables notwithstanding, the experiments herein suggest that hermit crabs are constrained consumers: they are highly dependent on gastropods for their shells but are capable of accessing these shells only in a narrow time window. This time window seems to extend from the point at which a gastropod's body has been consumed by a predator or disintegrated within its shell up to the point at which the leftover empty shell still remains on the surface, not yet having been buried by tidal action. Given the constraints hermit crabs face in acquiring shells directly from gastropods, it is perhaps not surprising that they often target shells already worn by conspecifics (Rotjan et al., 2010). Many hermit crab species have evolved elaborate and ritualized social behaviors specifically for this purpose. For instance, some species perform a variety of visual displays with their chelipeds and ambulatory legs that mediate conflicts over shells (Hazlett, 1972; Laidre, 2007). And many hermit crab species also engage in extended bouts of shell-rapping in which one crab knocks its own shell against that of another crab until the other crab gives up, allowing itself to be evicted (Hazlett, 1978, 1980, 1981; Briffa et al., 1998). These specialized shell-exchange behaviors appear critical to guaranteeing that crabs can move into larger shells as they grow and experience changing size requirements (Sato and Seno, 2006). The experiments in this paper suggest that the population of ‘available’ shells for hermit crabs may, for the most part, be restricted to those that are empty (but still lie on the surface) or those that are occupied by a conspecific. This conclusion, however, should be viewed as preliminary until the experiments reported herein are expanded, both in their taxonomic breadth and in the different experimental design permutations that are possible. With respect to taxonomic breadth, over 800 species of hermit crab exist worldwide (Briffa and Mowles, 2008) and many more times as many gastropods (Vermeij, 1993). The range of test species could therefore be greatly enlarged, especially to encompass sub-tidal hermit crabs whose chelipeds may be stronger and potentially more capable of pulling out gastropod bodies from their shells (Randall, 1964). With respect to experimental design permutations, several features of the above experiments could be altered to test a wider range of behavioral phenomena. First, instead of using only shell-less crabs or crabs in their original field shells, crabs could be allocated to particularly small, low-quality shells before they are paired with a

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gastropod. Crabs in such sub-optimal shells might experience increased motivation for shell-acquisition (compared to normallyshelled crabs) and they also might be able to exert greater leverage while pulling on gastropods (compared to shell-less crabs). A second possible alteration in experimental design concerns the state of the gastropods. In addition to using living gastropods, some of the experiments in the present study used gastropods that had been killed by boiling. Future experiments might try using frozen gastropods after they have thawed, since the proteins would not be denatured—as they are after boiling—and thus gastropod body might be less tough (personal communication from D. Rittschof). Though pilot work that has attempted using frozen gastropods has evidently generated similar initial results to the present study (personal communication from R. Rotjan). Gastropods could also be used that have desiccated in the sun or decomposed for varying durations. Brightwell (1951) reported that “sickly whelks” (p. 283) were readily pulled out of their shells by Pagurus bernhardus. Without a more precise definition of what constituted ‘sickly’, it is unclear how to compare Brightwell's non-quantitative report to what, in the present experiments, was P. bernhardus's minimal effectiveness at pulling out boiled gastropods. In the author's experience, boiled gastropods were by the far the easiest state of gastropod to remove from their shells, and presumably easier than ‘sickly’ gastropods, which would still be physically rooted inside their shell and capable of closing their opercula. Finally, one more possible design alteration would be to allow for the sequential action of several crabs on a single gastropod, giving each crab a specified length of time with the gastropod before pairing that gastropod with a new crab. The accumulated action of several crabs, acting one after the other or in concert, might increase the chance that any later crab could effect an eviction of the gastropod. In addition to widening the taxonomic scope and the variety of behavioral experiments on crab-gastropod relations, it would also be useful to incorporate a greater mechanistic perspective. Particularly useful would be to quantify the mechanical force that different hermit crab species are capable of exerting when they pull materials with their chelipeds (see Wilson et al., 2007 for an example in crayfish). This maximal cheliped pulling force could then be compared to the defensive abilities of gastropods (Hazlett, 1989; see also Vermeij, 2010), especially the force required to eject gastropods at different stages of their life cycle. By taking such a mechanistic approach it might be possible to specifically target behavioral experiments to species that possess the requisite morphological hardware and strength to forcibly remove living gastropods. Supplementary data to this article can be found online at doi:10.1016/ j.jembe.2010.10.024. Acknowledgements I thank Geerat Vermeij for enlightening me about the gastropod perspective during our meeting at UC Davis in fall 2009 and Bob Elwood for useful discussions on hermit crabs when I first began this line of experiments in summer 2006. Bob Elwood and the School of Biological Sciences at Queen's University kindly provided laboratory space in Ireland and the Osa Biodiversity Center kindly provided laboratory space in Costa Rica. Research was supported by grants from the Society for Integrative and Comparative Biology, the American Museum of Natural History, the Department of Ecology and Evolutionary Biology at Princeton, Sigma Xi The Scientific Research Society, the Animal Behavior Society, a Princeton University Graduate School Centennial Fellowship in the Sciences and Engineering, and a National Science Foundation Graduate Research Fellowship. [SS] References Abrams, P., 1978. Shell selection and utilization in a terrestrial hermit crab, Coenobita compressus (H. Milne Edwards). Oecologia 34, 239–253.

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