Interpreting odours in hermit crabs: A comparative study

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Abstract

Odours of different sources can indicate to hermit crabs the availability of empty shells, crucial resources for the life cycle of almost all of them. Here, we compared Clibanarius erythropus and Pagurus bernhardus for the intensity of investigative behaviour exhibited towards an empty, well-fitting shell in the presence of (1) plain seawater as control and seawater conditioned by (2) dead and live snails, (3) dead and live conspecifics, (4) live predators, and (5) food. During 10 min of observation, we recorded latency (the time until the first contact with the shell), and the number and duration of shell investigation bouts. The two species behaved similarly when exposed to the odours of food, live snails, and predators, while a more intense shell investigation was induced by dead snail odour in C. erythropus and by dead or live conspecific odour in P. bernhardus. Further studies should investigate the influence of phylogeny and ecology on this interspecific difference.

Research highlights

► Odours of different sources can indicate to hermit crabs the availability of empty shells. ► We compared the hermit crabs Clibanarius erythropus and Pagurus bernhardus for the intensity of investigative behaviour exhibited towards an empty shell in the presence of several odours. ► Their responses to the odours indicating shell availability significantly differed, as a possible reflection of the diverse tactic they adopt to obtain shells. ► The central role played by chemical stimuli for the recruitment of empty shells by hermit crabs is confirmed. ► The relative importance of phylogeny and ecology on such interspecific differences will be explored in other populations and species.

Introduction

Since visibility is most often limited in water, important sources of information to aquatic animals are chemical cues. Aquatic decapods rely on them to avoid predators, to recognize opponents, and to find resources, such as mates and food (Bergman and Moore, 2005). The occupancy of well-fitting gastropod shells is crucial for almost all hermit crab species (for an exception see Gherardi, 1996): their survival, growth, and reproduction depend in fact on both the quality and the availability of empty shells in the habitat (Elwood, 1995). Hermit crabs are indeed unable to directly prey on live snails and so depend upon other causes of snail mortality to generate new shelters (but see Rutheford, 1977). Consequently, they have evolved complex behavioural tactics to obtain empty shells: they can exchange them with con- or heterospecifics through either shell fighting (Hazlett, 1966a, Hazlett, 1966b, Elwood and Glass, 1981) or bargaining (i.e. shell exchanges in which both individuals gain in shell fit; Hazlett, 1978, Hazlett, 1981). They also rely on refined mechanisms of orientation to reach gastropod predation sites, i.e. sites where new empty shells, released by non-destructive predation on snails, are made available (Rittschof, 1980a, Tricarico and Gherardi, 2006, Tricarico et al., 2009). Hermit crabs gather at these sites, interact with each other, and form dominance hierarchies (Winston and Jacobson, 1978). These aggregations may function as “shell markets”, in which most site attendants may take advantage of a vacancy chain process (Chase et al., 1988), thus obtaining a better-quality shell (Rittschof et al., 1992).

Previous studies have shown that shell availability is signalled by the odours released by different sources (Rittschof, 1980a, Rittschof, 1980b, Rittschof et al., 1992), such as calcium ions emanated from the surface of the shell itself (Mesce, 1982), partly digested snail flesh (Katz and Rittschof, 1993), the hemolymph of dying con/heterospecifics, or live conspecifics (Rittschof et al., 1992, Small and Thacker, 1994, Gherardi and Atema, 2005). As shown by Rittschof and Hazlett (1997) and Gherardi and Atema (2005), the intensity of the investigatory acts executed by hermit crabs towards empty, well-fitting shells is an index of their responses to these odours. Previous studies have suggested the existence of an interspecific variability in these behaviours as a possible reflection of both the status of the shells most available in the habitat and the systems adopted to obtain them (Gherardi and Atema, 2005, Tricarico et al., 2009).

To test this hypothesis, in the present laboratory study, we compared two species of hermit crabs (Clibanarius erythropus and Pagurus bernhardus) for the intensity of investigation exhibited towards an empty, well-fitting shell in the presence of different odours. The diogenid C. erythropus (Latreille, 1818) is an intertidal shallow-water species, common in the Mediterranean and European Atlantic rocky shores. Its shell preferences and aggregation formation have been studied by Gherardi and Benvenuto (2001), but little is known about the chemical ecology of this species (except Tricarico et al., 2009). The pagurid P. bernhardus (Linnaeus, 1758) is a common intertidal-subtidal species on the rocky shores of North Sea and European Atlantic coasts. It has been abundantly studied in the laboratory for its refined intraspecific behaviour (e.g. Elwood, 1995, Briffa and Williams, 2006, Briffa et al., 2008) and for its ability to assess shell quality (Elwood et al., 1979, Elwood and Stewart, 1985, Neil and Elwood, 1986, Jackson and Elwood, 1989a, Jackson and Elwood, 1989b), but not for the behavioural tactics used to obtain new shells (except Elwood and Glass, 1981, Briffa and Austin, 2009). We chose these two species because they occupy different habitats, display diverse social behaviour, and have some aspects related to shell recruitment still unexplored, being thus good model systems for investigating the issue of interspecific behavioural differences in hermit crabs.

Section snippets

Subjects, collection, and housing conditions

Clibanarius erythropus (180 individuals, right chela width: 0.5–1.3 mm) and Pagurus bernhardus (180 individuals, major chela width: 2–5.3 mm) were collected during diurnal low tides from the rocky shores of Baia Domiziana (Southern Tuscany, Italy: N 42°26’7’’, E 11°9’10’’) and Robin’s Hood Bay (UK: N 54°26’3”, E 0°32’6’’), respectively, in the summer 2007. We also collected 5 specimens each of the predators of the two species living in the sampled areas (the crabs Eriphia verrucosa in Italy and

Results

A two-way ANOVA shows a significant interaction between the two species for latency only (Table 1a). Investigation bouts were more numerous and longer in Pagurus bernhardus than in Clibanarius erythropus (Table 1a). In the latter species, latency was the shortest and the total duration of shell investigation was the longest in the presence of the dead snail odour (Table 1b; Fig. 1); on the contrary, in P. bernhardus it was the odour of dead and live conspecifics that induced earlier shell

Discussion

Our study shows the existence of significant differences between Clibanarius erythropus and Pagurus bernhardus in the intensity of the target shell investigation when exposed to different odours. While both species showed a similar behaviour in the presence of food odours, live snails, and predators, their responses to the odours indicating shell availability significantly differed: a more intense shell investigation was induced by the odour of dead snails in C. erythropus and by the odour of

Acknowledgements

We thank the HERI (Hull Environment Research Institute) for the financial support of E.T. during her stay in UK and Giuseppe Mazza for his help in collecting hermit crabs in Italy.

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