Shell Exchange in Hawaiian Hermit Crabs1

BRIAN A. HAZLETT 2

ABSTRACT: Shell exchange behavior of intertidal Hawaiian hermit crabs was observed in the laboratory. Outcomes of 255 shell-related interactions were analyzed to test the predictive powers of two models of resource exchange . In the case ofintraspecific interactions, the negotiations model (which predicts that exchanges should occur only when both crabs will gain in shell value) was superior to an aggression model ofresource exchange . In the case of interspecific interactions, the negotiations model accurately predicted outcome of Calcinus Calcinus interactions, but poorly predicted outcome of Calcinus-Clibanarius interactions.

HERMIT CRABSNEED GASTROPOD shells for pro model. Before the development of the negoti tection, and one means of acquiring them is ations idea as an alternative model of resource by exchange of shells with other crabs (Hazlett exchange, an earlier study ofHawaiian species 1966). Shells can be a limiting resource for (Hazlett 1970) emphasized the aggressive/ crabs (Hazlett 1981), and the behavior pat competitive nature ofhennit crab interactions. terns associated with the exchange of this re source have often been viewed as fights (Hazlett 1967, 1972, Bach et al. 1976, Dowds MATERIALS AND METHODS and Elwood 1983, 1985). Indeed, an earlier paper on Hawaiian hermit crabs (Hazlett Crabs used in the study were collected at a 1970) viewed shell fights as a mechanism of variety of locations around the island of ecological competition. Oahu, Hawaii. The crabs were placed in water The idea that exchanges ofshells occur pri tables at the Hawaii Institute of Marine Bio marily when both crabs gain in resource value logy, Coconut Island, Oahu. The crabs were has been termed negotiations (Hazlett 1978), not experimentally treated in any way and and this type of behavioral interaction can were interacting with each other in an envi result in ecological processes that differ quali ronment that was similar to a 0.5 x 1.5 m tide tatively from competition (Hazlett 1987, pool. Observations were made during day Vandermeer et al. 1985). These ecological pro light hours, using natural lighting, during the cesses can occur both intraspecifically months of January through May of 1988. (Abrams 1982a) and interspecifically (Hazlett Crabs were periodically fed with algae and 1983). detritus on rocks placed in the water table. Because most ofthe results that support the Species composition and the relative propor negotiations model of resource exchange were tions of different species changed over the 5 obtained from observations of Caribbean months ofobservation as new specimens were species of hermit crabs, it is of interest to continually added to the water table . Thus no examine the resource exchange patterns of quantitative statements about the relative Pacific species to test the generality of the amounts of inter- versus intraspecific inter actions can be made. The observer sat near the water table and continually scanned the water table for social 1 Contribution no. 807 from the Hawai i Institute of Marin e Biology. Manuscript accepted 31 January 1990. behaviors (the results of reproductive inter 2 Department of Biology, University of Michigan , Ann actions are reported elsewhere [Hazlett 1989]). Arbor, Michigan 48109. A shell-related interaction was recorded when- 401 402 PACIFIC SCIENCE, Volume 44, October 1990 ever shell rapping was seen. This rapid bring gastropod for at least 48 hr. Shell sizes were ing together of shells by an initiating crab chosen to cover the size range possibly used occurs only in the context of shell exchange by the crabs being tested. Each crab had about attempts, and shell exchanges do not occur 201 shells to choose from (its own and 200 without shell rapping. Whenever shell rapping empty ones) since crabs can only occupy one occurred (see Hazlett 1966 for description), shell at a time. After this period, the crabs special attention was paid to that interaction. were removed and the crab and shell para Although attention was focused on the shell meters were measured as outlined above. related interaction, the rest of the water table From these data, a regression line between was also scanned for additional interactions. crab size and shell size for each particular Up to five interactions at a time could be crab-gastropod species combination was cal followed; however, usually only one inter culated. These regressions were obtained only action was in progress at a time. It is import for the more common crab-shell combina ant to remember that these observations were tions. ofcrabs that were not manipulated in any way The data were then analyzed, case by case, other than being collected and placed in a to determine if the outcome of each inter water table.:Crabs that have been experimen action fit one, both, or neither of two models tally manipulated behave differently in shell of resource exchange (Hazlett 1983, 1987). related interactions (Hazlett, unpublished Although the initiating individual was usually data). larger than the noninitiator, either individual Shell-related interactions terminate in one could be the larger crab in a given interaction. of two ways. Either the noninitiator comes In the aggression model, it is predicted that out of its shell and an exchange of shells oc a shell exchange will occur only when the ex curs (exchange) or the initiator stops rapping change will lead to a better shell for the initi behavior and walks away from the shell it was ating crab and the initiator is larger. A parti attempting to obtain (no exchange). Once the cular shell could be better in terms of size of nature of the outcome of the interaction was the shell (closer to the desired shell size as determined by the behavior ofthe crabs, both determined by the free-access experiments) or crabs and their shells were removed from the the species of shell, if there are clear inter water table and set aside for later measure specific preferences. The negotiations model ments. After a period of observations was (Hazlett 1978) predicts that shell exchanges finished, data regarding the interactants were will occur only ifboth participants will obtain recorded. The species, sex, reproductive con a better shell as a result of the exchange. If dition of females (berried or not), and size in only one crab (the initiator) will obtain a bet terms of millimeters of cephalothorax length ter resource, no exchange will occur, accord were recorded. The species ofgastropod shells ing to the negotiations model. Each shell ofthe initiator and noninitiator was recorded, related interaction was scored as to the accu and the shells were placed in a 60° C drying racy of each model in predicting the outcome oven for at least 48 hr. The shells were then of the interaction. The outcome of an inter weighed , first each shell by itself and then action could be correctly predicted by one, when filled with fine sand of known specific both, or neither model. gravity. The latter measurement allowed sub After measurements of its cephalothorax, sequent calculation of the internal volume of each crab was given a new shell and returned the shells. to the intertidal zone , thus limiting its data The desired shell size of several species of input to one interaction. This process was not crab with regard to several species of gastro followed for two species, each represented by pods was determined by free-access experi just one individual. One of these was a single ments (Hazlett 1970). Thirty to 60 crabs of a specimen of Calcinus haigae and the second a particular species were placed with an excess new species of Calcinus currently being des (100-200) ofempty shells ofa given species of cribed by P. A. McLaughlin. Hermit Crab Shell Exchange-c-Hxztrrrr 403

RESULTS either initiator or noninitiator were observed (Table 2). There were two exceptions to this For five crab species (Clibanarius zebra , generality. Individuals of Clibanarius zebra Calcinus laevimanus, Calcinus latens, Calcinus rarely initiated interactions with an individual seuratic, and Calcinus elegans) the relation of any Calcinus species. A few such inter ship between crab size and desired shell vol actions were observed but they were indeed ume was determined for Trochus intextus. not common and none involved individuals of Interestingly, the slope ofthe crab size-desired C. laevimanus. All four Clibanarius-initiated shell size relationship was essentially the same interspecific interactions resulted in no shell for all five species ofcrab (the crab species by exchange. Second, individuals of Calcinus crab size interaction term from an analysis of seurati were rarely the noninitiator in inter variance analyzing variation in shell volume specific interactions. This may be the result chosen with crab size as a covariate; F = 0.667, of the rapid locomotory capabilities of C. P = 0.616). However, both crab size (F = seurati, which allow it to run away from a 307; df = 4, 1; P < 0.001) and crab species potential shell-related interaction initiated (F = 3.2, P = 0.003) significantly affected by slower crabs (i.e., individuals of other shell volume chosen. This indicates that al species). though the slopes are not different for the The outcomes of all of the interspecific in different crab species, the intercepts are dif teractions between individuals in the genus ferent. That is, crabs the same size but of Calcinus were predicted well by the negoti different species selected different-sized shells. ations model. The precentage of cases cor A total of255 shell-related interactions was rectly predicted ranged from 100% (c. observed. Ofthese, 144 were intraspecific and seurati, C. haigae, C. latens, and C. elegans as III were between crabs of different species. noninitiators) to 87% (c. laevimanus as non Overall , the aggression model correctly pre initiator). These interactions are clearly sim dicted the outcome of the interactions 45% ilar in the pattern of their outcomes to the of the time, while the negotiations model was intraspecific interactions observed. However, correct in 71.6% of the cases. where a Calcinus crab was the initiator and an In the intraspecific cases (Table 1), the pat individual of Clibanarius zebra was the non tern ofoutcomes was similar in all the species initiator, the pattern was different. The nego observed.The aggression model was, in every tiations model did not predict the outcomes case, a poorer predictor of the outcome of well (56% correct, n = 52). Individuals of C. interactions (ranging from 25% correct for zebra frequently exchanged shells, especially Calcinus laevimanus to 56% correct for Cal when the initiator was Calcinus laevimanus, cinus seurati). The negotiations model cor when the exchange resulted in occupation of rectly predicted the outcome of interactions a shell that was a poorer fit than the one in between 69% (c. laevimanus) and 78% previously occupied. (Clibanarius zebra) of the intraspecific cases for which reasonable-sized data sets were available. DISCUSSION It should be noted that in the case of Cal cinus seurati a number of cases involved fe The results of these observations and anal males carrying eggs as the initiator (n = 16 yses demonstrate that Pacific hermit crabs out of 99 cases in which a C. seurati was the tend to follow the negotiations model of re initiating crab). Previous studies on other source exchange. Crabs exchange gastropod species (Hazlett 1966) indicated that berried shells when the exchange will result in a gain females rarel y were initiators in shell ex in shell fit for both individuals, and if the non changes. initiator would not gain in shell fit no ex In the case of interspecific interactions, al change occurred. This pattern predominated most all possible combinations of species as in the intraspecific interactions of all species 404 PACIFIC SCIENCE, Volume 44, October 1990

TABLE 1

O UTCOME OFI NTRASPECIFIC SHELL-RELATED I NTERACTIONS AND S UCCESSOF Two MODELS IN P REDICTING THE O UTCOME OF I NTERACTIONS (AN I NTERACTION C OULD FIT THE PREDI CTIONS OF O NE, BOTH , OR N EITHER M ODEL)

% RESULTI NG % CORRECT BY % CORRECT BY CRAB SPECIES n INEXCHANGE AGGRESSION NEGOTIATION

Clibanarius zebra 54 21 39 78 Calcinus seurati 63 29 56 73 Calcinus laevimanus 20 35 25 69 Others* 7 28 42 60 Overall 144 27 42 73

•Calcinus latens and Calcinus elegans.

TABLE 2

O UTCOMES OF I NTERSPECIFIC SHELL-RELATED I NTERACTIONS IN HAWAIIAN H ERMIT C RABS

SPECIES OF NONINlTlA TOR

OTHER C. laevimanu s Calcinus*

n =O n=3 ex = 0 ex = 0 %agg= % agg = 33 % neg = - % neg = 100

n = 21 n = 6 ex = 6 ex = 2 % agg = 38 % agg = 67 % neg = 86 % neg = 100 n = 12 ex = 5 % agg = 50 % neg = 100 n=4 n=6 ex = I ex = 1 % agg = 50 % agg = 50 % neg = 100 % neg = 100 n = 25 n = 27 ex = 7 ex = 8 % agg = 40 % agg = 52 % neg = 87 % neg = 100

N OTE: For each combination of initiating and noniniti ating species the following are given: n = the number of intera ction s observed, ex = the number of exchanges that actually occurred, % agg = the percentage of interacti ons correctly predicted as to outcome by the aggressive model , and % neg = the percentage of interactions correctly predicted as to outcome by the negotiations model. • Calcinus latens, C. elegans, C. haigae, and Calcinus (undescribed sp.). studied. As in studies on both Caribbean and 1987) that this may be the result of inexper European species, the outcome of about 20% ience with particular shell types. of the interactions was not accurately pre The interspecific shell exchanges fell into dicted by either the negotiations or aggression two quite distinct categories. The intrageneric model. I have suggested elsewhere (Hazlett Calcinus interactions were very well predicted Hermit Crab Shell Exchange-HAZLETI 405 by the negotiations model. In almost every seems that the interactions of Clibanarius single case, crabs exchanged only if both par zebra with other intertidal diogenids is more ticipants gained in shell fit. This was the case likely to be of a competitive nature. even for species pairs that do not frequently occur in the same habitat (i.e., Calcinus seurati rarely would interact with other Calcinus ACKNOWLEDGMENTS species because of its supratidal distribution [Reese 1969, Wooster, 1984]. Thanks are given to Ernie Reese for his In contrast, when Clibanarius zebra was the hospitality and assistance, to Linda Baron for noninitiator, the outcomes ofinterspecific in help with some of the observations, and to teractions were poorly predicted. This is con Catherine Bach for comments on the manu sistent with earlier observations (utilizing script. methodologies that could not distinguish be tween the aggression and negotiations mod els) that Calcinus species are dominant over LITERATURE CITED Clibanarius species (Hazlett 1970, Bach et al. 1976, Abrams 1981, 1982b, Bertness 1981). ABRAMS, P. 1981. Competition in an Indo However, the Calcinus-C. zebra result from Pacific hermit crab community. Oecologia the present study contrasts with the results (Berlin) 51 :240-249. from ecologically and behaviorally similar - --. 1982a. Intraspecific shell exchange pairs in the Caribbean (Hazlett 1983). In the in the hermit crab Clibanarius virescens latter cases, Clibanarius species rarely initi (Krauss). J. Exp. Mar. BioI. Ecol. 59:89 ated interactions with individuals of Calcinus, 101. but as noninitiators they exchanged shells - - - . 1982b. Frequencies of interspecific only when it resulted in a gain in shell fit. The shell exchanges between hermit crabs. J. methodological approaches were virtually Exp. Mar. Ecol. 61 :99-209. identical in the two studies. It is not clear why BACH, C., B. A. HAZLETT, and D. RITTSCHOF. C. zebra (in Hawaii) would be so strongly 1976. Effects of interspecific competition dominated by Calcinus species while C. tri on fitness of the hermit crab Clibanarius color and C. antillensis in the Caribbean are tricolor . Ecology 57: 579-586. not so dominated. The extent of ecological BERTNESS, M. D. 1981. Interference, exploita overlap is similarly high in both pairs, and tion, and sexual components of competi both pairs are found together over a wide tion in a tropical hermit crab assemblage. range of the respective oceans. In both loca J. Exp. Mar. BioI. Ecol. 49: 189-202. tion s, the Clibanariu s species is found higher DOWDS, B. M., and R. W. ELWOOD. 1983. in the intertidal and the Calcinus species has Shell wars: Assessment strategies and the much larger chelipeds. Individuals ofCalcinus timing of decisions in hermit crab shell appear to be more aggressive in both locations fights. Behaviour 85 : 1-24. (Dunham 1981), but in the Caribbean inter ---. 1985. Shell wars II: The influence of specific interactions are best predicted by the relative size on decisions made during her negotiations model while they are not in the mit crab shell fights. Anim. Behav . 33 :649 case of the Pacific pair. 656. If the pattern of exchange observed in the DUNHAM, D. W. 1981. Chela efficiency in dis laboratory in Hawaii occurs in the field, it play and feeding by hermit crabs (Deca would at least partially explain the poorer fit poda, Paguridea). Crustaceana (Leiden), ofcrabs to their shells previously reported for 41 :40 -45. C. zebra compared to Calcinus species HAZLETT, B. A. 1966. Social behavior of the (Hazlett 1970). Although Calcinus species Paguridae and Diogenidae of Curacao. could, in theory, interact in either a competi Stud. Fauna Curacao 23: 1-143. tive or mutualistic manner (Hazlett 1987), it - - -. 1967. Interspecific shell fighting be- 406 PACIFIC SCIENCE, Volume 44, October 1990

tween Pagurus bernhardus and Pagurus --- . 1987. Hermit crab shell exchange as cuanensis (Decapoda, Paguridea). Sarsia a model system. Bull. Mar. Sci. 41 :99- 107. 29:215-220. ---. 1989. Mating success of male hermit --- . 1970. Interspecific shell fighting in crabs in shell generalist and shell specialist three sympatric species of hermit crabs in species. Behav. Ecol. Sociobiol. 25: I 19 Hawaii. Pac. Sci. 24 :472-482. 128. --. 1972. Shell fighting and sexual be REESE, E. S. 1969. Behavioral adaptations of havior in the hermit crab genera Paguristes intertidal hermit crabs. Am. Zool. 9 :343 and Calcinus with comments on Pagurus. 355. Bull. Mar. Sci. 22 :806-823. VANDERMEER, J., B. A. HAZLEIT, and B. ---. 1978. Shell exchanges in hermit crabs: RATHCKE. 1985. Indirect facilitation and Aggression, negotiations or both? Anim. mutualism. Pages 326-343 in D. Boucher, Behav. 26 : 1278-1279. ed. The biology of mutualism. Croom Helm ---. 198I. The behavioral ecology of her Publishing, London. mit crabs. Annu. Rev. Ecol. Syst. 12: 1-22. WOOSTER , D. S. 1984. The genus Calcinus 1983. Interspecific negotiations: (Paguridae, Diogenidae) from the Mariana Mutual gain in exchanges of a limiting re Islands including three new species. Mi source. Anim . Behav. 31: 160-163. cronesica (J. Univ. Gu am) 18: 121 - I62.