Shell use pattern and its effects on hermit crabs

The dependence of hermit crabs on gastropod shells as shelter is fundamental to their survival. Optimum shell selection by hermit crabs is vital as it directly affects growth, reproduction, protection from predators (Fotheringham, 1976; Bertness, 1981a;

Elwood et al., 1995) and reducing risk of desiccation (Bertness 1981b; Bertness &

Cunnigham 1981). A hermit crab constantly moves to a larger gastropod shell as it grows in order to maintain an optimum shelter that adequately protects it from predator.

For the female, the shell must provide a sufficient gap for its brood (Childress, 1972).

Crabs occupying smaller than optimum fit of a shell are more vuInerable to predation than crabs with optimum fit since a higher percentage of their body is exposed or they are unable to retreat further inward (Hazlett, 1981). On the other hand, crabs occupying larger and heavy shells may experience slow growth and their reproduction is affected (Bertness, 1981a; Hazlett & Baron, 1989; Elwood et al., 1995; Osorno et al., 1998) since heavier shells incur higher energy cost for locomotion (Dominciano et al., 2009).

Shell selection patterns have been known to be influenced by shell resources and availability in an ecosystem (Orians & King, 1964; Turra & Leite, 2001; Sant’ Anna et al., 2006). Empty shells are usually scarce in a habitat (Scully, 1979) and thus, it is an important limiting factor for hermit crab population. Increased abundance of shell resources has been shown to increase hermit crab population size (Vance, 1972).

Locating shell supplying sites in a vast habitat may pose a challenge; however, hermit crabs are known to be able to detect chemicals released by tissues of dead gastropods (Rittschof et al., 1990; Kratt & Rittschof, 1991; Rittschof & Cohen, 2004). Hermit crabs often search for new shells by tracing odor from sites where gastropod are being non-destructively predated leaving behind shells with little or no damage; these sites are collectively known as ‘gastropod predation sites’ (McLean, 1974; Tricarico & Gherardi,

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2006). In an environment where empty shells are limiting, intraspecific and interspecific competitions may occur between conspecific or sympatric species (Hazlett, 1966;

Dowds & Elwood, 1983) and between sexes (Briffa & Dallaway, 2007). Shell partitioning between hermit crabs is possible in the presence of different shell species (Kellogg, 1977; Gherardi & Nardone, 1997; Leite et al., 1998; Turra & Leite, 2001, 2002). Sexual dimorphism and size differences between species could be developed to minimize intraspecific competition and to guarantee shell fitness in the population in response to the limiting resources (Garcia & Matellato, 2001).

Hermit crabs are a successful taxon and unique as they choose shelters that they cannot produce themselves (Fotheringham, 1976). Shell selection by hermit crabs is not a random process as suggested by multiple evidences (Grant & Ulmer, 1974). In the selection of appropriate shell types, hermit crabs seem to have the ability to distinguish between different species of shells based on relative weight of shell as well as shell morphology rather than actual species recognition (Scully, 1983). Shells that belong to the same genus may have morphological overlaps or similarity in terms of size, weight and texture (Bertness, 1982) and as well as shape and structures (Shih & Mok, 2000).

The ability to secure shell occupancy compatible to the morphology of both hermit crabs and gastropod shells is an outcome shaped by a long evolutionary process (Cunningham et al., 1991, Schram, 2001).

Hermit crabs choose shells on the basis of how they benefit from them (Garcia

& Mantellato 2001) such as minimal energy cost for locomotion, sufficient protection from predators and water retention (Fotheringham, 1976; Bertness, 1981b; Elwood et al., 1995). However, any advantage in shell use may be compromised by ill-fitting shells that are incompatible with the crab’s biometrics (Blackstone 1985, Turra & Leite

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2003) rendering the animal vulnerable to predators (Hazlett, 1981), reduced reproductive potential (Hazlett & Baron, 1989; Elwood et al., 1995; Osorno et al., 1998) and retarded growth (Fotheringham, 1976, Osorno et al, 2005).

The shell selection process includes gathering of information, assessing shell quality and lastly, making decision accordingly. In an experiment by Imafuku (1984), approximately 80% of hermit crabs changed to new shells that were experimentally provided and abandoned their original shells occupied from the environment.

Knowledge acquired about a shell resource has a profound effect on the motivational state of hermit crab. Tricarico & Gherardi, (2007a) studied the motivation and behaviour of the hermit crab Pagurus longicarpus in deciding whether to retain its original shell or move to a newly found shell following information gathering via investigation. The study revealed that the motivation of P. longicarpus to occupy a new shell is exclusively affected by the worth of the original shell rather than the value or quality of shell resource offered.

The morphometrics of gastropod shells have a direct influence on shell selection patterns of hermit crabs particularly in the context of shell size, weight and shape. These features apparently affect hermit crab reproduction, protection and growth (Fotheringham, 1976; Bertness, 1981c; Elwood et al., 1995). Morphometric data from both hermit crabs and their gastropod shells have been commonly used to quantify shell utilization patterns (Blackstone, 1985; McClintock, 1985; Shih & Mok, 2000; Turra &

Leite, 2004; Barnes & Kuklinski, 2007; Nakin & Somers, 2007; Caruso & Chemello, 2009) and in addition, in-situ and laboratory experiments that were carried out to elucidate the behavioural aspect of shell use (Wilber, 1989; Garcia & Mantellato, 2001;

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Turra & Denadai, 2002; Gherardi, 2004; Tricarico & Gherardi, 2007a; Dominciano et al, 2009; Bach & Hazlett, 2009; Pereira & Goncalves, 2000; Tricarico et al., 2009).

Turra & Leite (2004) carried out a study on crab-shell size relationship of three species of tropical intertidal hermit crabs; Clibanarius antillensis, Clibanarius sclopetarius and Clibanarius vittatus. They found that crab size and weight were significantly related to all morphometric parameters of shells measured. There is also frequent negative allometry between crab and shell variables suggesting that larger crabs utilize lighter shells rather than smaller crabs. In addition, the relationship between crab size and shell length or shell weight is not dependent on species of both crab and shell. The results indicate the role of crab size and crab weight in determining the shell size preference of hermit crabs and that crab-shell size relationship are not species specific.

Caruso & Chemello (2009) employed multivariate analysis to quantify the relative role of shape and size of shells on shell use by hermit crab, Clibanarius erythropus. The result indicated that shell size was more important than shell shape based on the patterns of shell use whereby larger crabs used larger shells. Although shell shape expressed in terms of degree of elongation varied in both males and females, these variations are accounted only towards males as shell shape features have been correlated with male biometrics but not with female biometrics. Caruso & Chemello (2009) further hypothesized that the larger male may have access to larger, heavier and more available shells such as Osilinus turbinatus which cannot be occupied by averaged-sized males or ovigerous females. However, once males reach an adequate size, they are free to choose shells of the desired shape from relatively larger resource of heavy shells.

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Blackstone (1985) investigated experimentally the effects of variations in shell size and shape on growth and cheliped form in the hermit crab, Pagurus longicarpus from two geographic locations on the north and south Atlantic coast. Results showed that crabs occupying small, high-spired shells attained smaller sizes but produced relatively longer claws and greater asymmetry between two claws, while crabs occupying large, low-spired shells, attained larger sizes but produced relatively shorter claws. These results are compatible with the results from field observations made on P.

longicarpus from the two geographic locations whereby the southern crabs occupying small, high-spired shells are smaller and have longer claws compared to the larger and shorter claws of northern crabs that occupy large, low-spired shells. Thus, Blackstone (1985) concluded that size and shape differences between P. longicarpus of these two geographic locations are due to differences in shell occupation.

The energetic cost of carrying a shell as ‘mobile home’ has been demonstrated;

nevertheless the benefit of increase feeding rate and food quality may overpower it (Osorno et al., 2005). When carrying a shell, the terrestrial hermit crab, Coenobita compressus consumes 50% more oxygen than when is ‘naked’ (Herreid & Full, 1986).

Likewise for marine hermit crabs which are fully submerged, they require a lesser effort to carry shells (Briffa & Elwood, 2005). The energy cost could also be expressed in term of increased lactate which causes potential fatigue and consequently affecting general activities of the crabs (Doake et al., 2010). The trade-off between growth and protection can be shown by crabs occupying lighter shells that permit growth due to larger internal volume. As lighter shells are also thinner walled, therefore, the lighter shells which are more brittle may offer less protection from predators and would expose the hermit crabs to higher risk of desiccation. Hermit crabs can compensate higher

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energy expenditure due to carrying heavier shell by increasing food intake (Osorno et al., 2005).

Empty gastropod shells usually are masked by thick epiphytic algae that encrust the shell surface (Reese, 1969) and other symbiotic associates of hermit crabs such as polychaetes, arthropods, bryozoans and cnidarians. There are a total of 550 species of invertebrates found to be associated with 180 species of hermit crabs. These epibionts particularly cnidarians and bryozoans may benefit hermit crabs by reinforcing the extension of shell aperture lip hence lessen the need to change shell and protection (Williams & McDermott, 2004) by enhancing crypsis along with stinging tentacles of cnidarians to deter predators. However, an encrusted shell means additional weight that is likely to impose energetic cost of carrying it particularly shells that are heavily encrusted with barnacles and tubicolous polychaetes (Briffa & Elwood, 2005).

Briffa & Elwood (2005) investigated the effects and preference of hermit crabs towards both encrusted and non-encrusted shells. The results showed that hermit crabs have clear preference towards shells free of epibionts. This outcome is elucidated by the fact that encrusted shells are heavier and have lower internal volume to weight ratio compared to non-encrusted shells and consequently, elevated the haemolymph lactate levels due to increase drag. Effects of increased lactate include potential fatigue impinging on the general activities of the hermit crabs (Doake et al., 2010).

Bertness (1982) carried out an experiment to examine shell selection patterns of two common hermit crabs, Clibanarius antillensis Stimpson and Calcinus tibicen which inhabit hard bottom reef flats on the Carribean coast of Panama in relation to predation pressure and physical stresses. The study revealed that C. antillensis has distinct

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preference towards high-spired shells which would provide protection from thermal stress due to the high water retaining capability of the shells and thus, reducing the risk of desiccation, while C. tibicen has a preference towards low-spired shells which would enhance resistance to predators.