Hermit crab biocoenoses: a worldwide review of the diversity and natural history of hermit crab associates

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Abstract

The symbiotic associates of hermit crabs (excluding parasites and flora) are reviewed worldwide. The review includes species found on the shells occupied by hermit crabs (epibiotic species), species boring into these shells (endolithic species), species living within the lumen of the shell (either free-living or attached to the shell), species attached to the hermit crabs themselves, and hypersymbionts. In total over 550 invertebrates, from 16 phyla are found associated with over 180 species of hermit crabs. Among these associates, 114 appear to be obligate commensals of hermit crabs, 215 are facultative commensals, and 232 are incidental associates. The taxa exhibiting the highest number of associates are arthropods (126), polychaetes (105), and cnidarians (100). The communities of species associated with Dardanus arrosor, Paguristes eremita, Pagurus bernhardus, Pagurus cuanensis, and Pagurus longicarpus are the best studied and harbor the most diverse assemblages of species. While trends in biodiversity of hermit crab assemblages do not follow predicted patterns (e.g., hermit crabs within the Indo-West Pacific do not harbor more species than those from temperate regions), this is suggested to reflect a lack of sampling rather than a true representation of the number of associates. Hermit crabs date to at least the Cretaceous and provided a niche for a number of groups (e.g., hydractinians, bryozoans, polydorids), which were already associates of living gastropods. Apparently hermit crab shells initially supplied a substrate for settlement and then these symbiotic relationships were reinforced by enhanced feeding of symbionts through the activity of the hosts. Through their use and recycling of gastropods shells, hermit crabs are important allogenic ecosystem engineers in marine habitats from the intertidal to the deep sea. Hermit crabs benefit from some symbionts, particularly cnidarians and bryozoans, through extension of shell apertures (alleviating need to switch into new shells) and by providing protection from predators. However, hermit crabs are also negatively impacted (e.g., decreased reproductive success, increased predation) by some symbionts and a review of egg predators is provided. Thus, the symbiotic relationships between hermit crabs and many associates are difficult to characterize and often exhibit temporal changes depending on environmental and biological factors. Research on the biology of these symbionts and the costs/benefits of their associations with hermit crabs are analyzed. While some associates (e.g., Hydractinia spp.) have been studied in considerable detail, for most associations little is known in terms of the impacts of symbionts on hosts, and future experimental studies on the multitude of relationships are suggested.

Introduction

Hermit crabs are decapod crustaceans most of which have noncalcified abdomens requiring protection from predation. Inhabiting empty gastropod shells serves to protect most of the more than 800 described species of hermit crabs within the Superfamily Paguroidea, nearly all of which are marine McLaughlin, 1983, McLaughlin, 2003. Hermit crabs are best known from intertidal areas where they are conspicuous and ecologically important scavengers and predators (Whitman et al., 2001). A small percentage of hermit crabs use bivalve and scaphopod shells, hollowed cylinders of wood Lemaitre, 1995, McLaughlin and Lemaitre, 1997, Forest, 1987 or hollowed-out fragments of stone Pope, 1953, Mayo, 1973, while others live in immobile domiciles provided by calcareous tubes of polychaetes or vermetid gastropods Markham, 1977, Gherardi and Cassidy, 1994, Gherardi, 1996, Rodrigues et al., 2000, corals (McLaughlin and Lemaitre, 1993), or sponges (Forest, 1987). Some, such as the fully calcified coconut crab, Birgus latro (Linnaeus, 1767), exist without a shell for most of their terrestrial lives, although shells are utilized by megalopae and young crabs Reese, 1968, Greenaway, 2003.

The adaptation of most hermit crabs to a life in empty gastropod shells has been studied in detail. Shell attributes such as type, weight, size, and internal volume affect the reproduction, growth, predator avoidance and behavior of hermit crabs Markham, 1968, Vance, 1972, Fotheringham, 1976, Bertness, 1981a, Bertness, 1981b, Elwood et al., 1995, Angel, 2000, Benvenuto and Gherardi, 2001, Yoshino et al., 2002, Gilchrist, 2003. In addition, shell availability limits hermit crab populations in certain areas Kellogg, 1976, Barnes, 1999 and may account for the coexistence of multiple hermit crab species in intertidal areas Abrams, 1980, Abrams, 1981, Abrams, 1987a, Abrams, 1987b, Gherardi and Nardone, 1997. The biology and behavioral ecology of hermit crabs have been reviewed Hazlett, 1981, Lancaster, 1988, Elwood and Neil, 1992.

In many regions gastropod shells inhabited by hermit crabs provide a substrate for epibiotic and endolithic species to attach and bore into, respectively. In addition, hermit crabs often harbor associates that live within the lumen of the shell (either free-living or attached to the shell) and others that attach to the hermit crabs themselves, both externally and internally. Taxonomic studies of symbiont species are abundant, yet certainly not complete and the ecological relationships between these associates and their hermit crab hosts remain largely unknown. Only a few studies have documented the biocoenosis or complete community of species associated with particular hermit crabs and their shells Samuelsen, 1970, Jensen and Bender, 1973, Cuadras and Pereira, 1977, Stachowitsch, 1977, Stachowitsch, 1980, Karlson and Shenk, 1983, McDermott, 2001, Reiss et al., 2003, although some partial reviews exist Balss, 1924, Gordan, 1956, Lancaster, 1988, Ates, 2003. Gastropod shells and associated species can affect the brood size of hermit crabs and therefore can potentially have significant effects on the fitness of these species (Wilber, 1989). Hermit crab choice of gastropod shells can be affected by epibionts Brooks and Mariscal, 1985a, Brooks and Mariscal, 1985b, Hazlett, 1984, Conover, 1979, McClintock, 1985, Caruso et al., 2003, Turra, 2003. In addition, mating behavior can be influenced by gastropod shells and perhaps attached associates (Hazlett and Baron, 1989).

Through their use of gastropod shells, hermit crabs influence the abundance and distribution of a diverse assemblage of invertebrates and thus provide a good example of ecosystem engineers Jones et al., 1994, Jones et al., 1997. The acquisition of an empty gastropod shell by a hermit crab brings the shell in a sense “back to life” in that it has returned to its original mobile state (in some cases even fossil shells are used; Barnes, 2001; McDermott, unpublished data). This capacity to securely inhabit shells is the result of a long evolutionary process that fashioned a morphological compatibility between hermit crabs and snail shells Cunningham et al., 1991, Schram, 2001. Furthermore, these shells exhibit different characteristics from when they were part of the living gastropod (e.g., shell secretion ceases, periostracum becomes eroded, the lumen is empty). Thus, in many ways the shells become new substrates, usually more conducive to attachment, penetration, and lumen invasion by symbionts. Therein some of these obligate or facultative associates reproduce and complete at least part of their life cycles as a result of hermit crab shell use. These organisms derive a variety of other benefits from hermit crabs and in some cases the symbiotic relationship is mutualistic, with hosts positively affected (e.g., protection from predators).

Ecosystem engineering is a broad, general concept for habitat modification and/or creation by organisms Jones et al., 1994, Jones et al., 1997, Thomas et al., 1998, Coleman and Williams, 2002, Wilby, 2002, Gutiérrez et al., 2003, Berkenbusch and Rowden, 2003 and while hermit crabs are not engineers on the same scale as some other species [e.g., beavers (Wright et al., 2002) and gophers (Reichman and Seabloom, 2002)], hermit crabs on a world-wide basis influence whole communities of associates in a range of habitats from terrestrial to the deep sea. Specifically, hermit crabs are allogenic engineers (i.e., those engineers that transform “living or non-living materials from one physical state to another”; Jones et al., 1997, p. 1949). As ecosystem engineers hermit crabs put discarded gastropod shells that would otherwise likely be buried in the sediments back into circulation (Gutiérrez et al., 2003). Species with analogous roles in marine habitats include the cockle, Austrovenus stutchburyi (Finlay, 1927) that provides a stable substrate along the shores of New Zealand Thomas et al., 1998, Lafferty et al., 2000, Mouritsen and Poulin, 2003. The shell of the cockle is colonized by a variety of invertebrates, thus forming a community of species (obligate and facultative) that would otherwise not be able to persist in this habitat. The cockle provides an example of an autogenic ecosystem engineer (those engineers that “directly transform the environment via endogenous processes”; Jones et al., 1997, p. 1949). Similarly, the bivalve Donax variabilis provides a substrate for the hydroid Lovenella gracilis in wave-swept environments (Manning and Lindquist, 2003). Hermit crabs provide a stable but mobile substrate and thus prevent organisms from being buried and also provide access to positive conditions (e.g., well oxygenated water, food supply, protection from predators). Hermit crab assemblages could also be considered examples of facilitation (Bruno et al., 2003) in which hermit crabs extend the range of associates through these positive interactions.

The purpose of the present study is to provide a review of species associated with hermit crabs. In addition, potential benefits and costs derived by these associates and their impacts on hermit crab hosts are analyzed (including a review of known and suspected egg predators of hermit crabs) based on experimental studies. A discussion of hypersymbiotic relationships and a table of known examples among hermit crabs are provided. Finally, the evolutionary relationships between hermit crabs and their associates are examined.

This review identifies critical aspects of the life history of hermit crab associates that are in need of experimental studies. A wide range of research topics from the initial association of symbionts with hermit crab hosts (e.g., cues for metamorphosis) to their interactions with other symbionts in the hermit crab assemblages (e.g., predation) remain to be explored. The accurate characterization of their symbiotic relationships with hosts requires further studies. The impacts that associates have on hermit crab behavior (e.g., shell choice) are particularly amenable to laboratory and field experiments since extensive background and quantitative models exist (Elwood and Neil, 1992). In addition, this study will serve as a baseline for future field investigations on the diversity patterns of hermit crab assemblages from different geographic regions. Hermit crab biocoenoses would provide an important model system to test hypotheses on the biotic diversity of marine invertebrates associated with hard substrates and their role as ecosystem engineers.

Section snippets

Analysis

The present review, which includes obligate, facultative, and incidental species associated with hermit crabs, was gleaned from the literature since 1864 (inception of the Zoological Record). Symbionts of the atypical “free-living” lithodid paguroids (Lithodidae) are not included in this review. We have used the following definitions in the construction of our list of hermit crab associates: obligate associates are found associated only with hermit crab hosts (although different species of

Results

Presently at least 550 invertebrate species, representing 16 phyla, are found associated with hermit crabs (Table 1). Over 180 hermit crab species act as hosts for these associates. The best-represented groups of symbionts are the arthropods, polychaetes, and cnidarians with 126, 105, and 100 species represented, respectively (Fig. 1A). Of the associates, 114 (20.3%) appear to be obligate commensals of hermit crabs; over 10 of the obligate symbionts are found with a single hermit crab host but

Evolutionary considerations

Debate over the evolutionary history of the Anomura and particularly the origin of hermit and king crabs exists. While morphological evidence indicates that the hermit crabs arose from a fully calcified lithodid ancestor McLaughlin and Lemaitre, 1997, McLaughlin and Lemaitre, 2000, molecular and ontogenetic studies indicate that the lithodids arose from a hermit crab ancestor (Cunningham et al., 1992; Harvey, 1998, Morrison et al., 2002). Regardless of hermit and king crab relationships, it is

Conclusion

The fossil record indicates that hermit crab associations probably first arose in the Jurassic, and multi-species assemblages may have been established by the Cretaceous. In all major phyla examined, symbiotic relationships with hermit crabs have evolved multiple times. It appears that most associations arose initially as a function of hermit crab shells providing a substrate for attachment or for boring. These associations were reinforced by enhanced feeding and protection from predators of

Acknowledgements

We thank Dr. Sandra Shumway (University of Connecticut) for inviting this review. We appreciate the comments of Drs. J. Bret Bennington (Hofstra University), Christopher Boyko (American Museum of Natural History), Randy Brooks (Florida Atlantic University), Daphne Fautin (University of Kansas), Patsy McLaughlin (Western Washington University), and Paul Taylor (Natural History Museum, London) that greatly enhanced this work. We thank Dr. Gregory Pell (Hofstra University) for translation of the

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