The influence of some symbionts on the shell-selection behaviour of the hermit crabs, Pagurus pollicarus and Pagurus longicarpus

The influence of some symbionts on the shell-selection by the hermit crabs Pagurus pollicarus and P. longicarpus was examined by placing individual hermit crabs with two similar shells in a choice situation and recording the shell occupied after 12 hr. One shell contained a symbiont species and the other did not. The results indicated that organisms normally found on or in empty shells influence the shell-section by these species of hermit crab. P. pollicarus preferred shells occupied by the sea anemone Calliactis tricolor or by the hydroid Hydractina echinata as opposed to bare shells. P. longicarpus also preferred shells with H. echinata. Both crab species rejected shells with the barnacle Balanus amphitrite. Shells containing the molluscs Crepidula fornicata or C. plana were rejected by the smaller hermit crab P. longicarpus. These molluscs appeared to exert no influence on P. pollicarpus unless they were large or abundant, at which point their weight or occlusion of available space possibly has negative effects on the crab.     

Sex-specific differences and the role of predation in the interaction between the hermit crab, Pagurus longicarpus, and its epibiont, Hydractinia symbiolongicarpus

The interaction between the hermit crab, Pagurus longicarpus, and the shell epibiont, Hydractinia symbiolongicarpus, varies from mutualism to parasitism based on the environmental context. We tested the hypothesis that this interaction also varies as a function of hermit crab sex. Given that recent work showed a negative effect of Hydractinia on female reproduction, we predicted a greater frequency of males in Hydractinia shells in the field and a stronger preference by males than females for shells with Hydractinia. Field collections documented a significantly greater proportion of males than females occupying shells with Hydractinia, and a significantly greater proportion of ovigerous females than non-ovigerous females in shells with Hydractinia. In laboratory shell-switching experiments, a greater proportion of males than females chose to enter shells with Hydractinia, but there was no difference in the proportions of males and females that vacated shells with Hydractinia.We examined whether the presence of Hydractinia influenced predation rates. Blue crabs fed on more than twice as many hermit crabs in shells with Hydractinia as compared to bare shells, but there was no significant difference for stone crabs. Laboratory experiments showed that the force required to crush shells was significantly greater for shells without Hydractinia. Thus, the lower occupancy and preference exhibited by females than males for shells with Hydractinia appears to result both from the decreased reproduction shown in past studies and an increase in predation risk.     

Shell use by juvenile fiddler crabs Uca pugnax and U. pugilator

The present study documents for the first time shell use by juvenile fiddler crabs in the salt marsh. Twenty visits were made to six salt marsh sites at Tybee Island, Georgia between 2007 and 2009. One hundred empty Littorina irrorata shells were collected at each site on each field trip. Juvenile carapace width was measured, crabs sexed, and species identification completed using RFLP analysis. Shell use of up to 79% was observed. Two species of fiddler crabs were found in empty shells, Uca pugnax and U. pugilator. U. pugnax was the dominant species at all sites representing 62-84% of the juvenile fiddler crab population. Juvenile sex ratios were female-biased (1.7:1) at all six sites. Juvenile size did not vary significantly between species but males of both species were significantly larger than females. Size frequency distribution of carapace width revealed that shell use varied with size and sex. In the 3 to 4 mm size class, juvenile females outnumbered juvenile males in empty L. irrorata shells while in the 5 to 6 mm size class and greater, juvenile males outnumbered juvenile females in shells. Significantly more juvenile fiddler crabs were found in empty shells during flood than ebb tide at 3 of the sites. This discovery illuminates the resourcefulness of juvenile fiddler crabs and provides another mechanism that might enhance survival.     

3-Decanol in the haemolymph of the hermit crab Clibanarius vittatus signals shell availability to conspecifics

Hermit crabs with poor fitting shells are chemically attracted to dying gastropods and conspecifics where a shell may become available. For land hermit crabs, the shell cue is a volatile compound found in the haemolymph. Based on this knowledge, we tested the hypothesis that shell investigation behavior in aquatic hermit crabs, the ancestral predecessors of terrestrial hermit crabs, is also triggered by volatile cues. Volatile compounds from haemolymph of Clibanarius vittatus and Pagurus pollicaris and brachyuran decapod crustaceans were purged from a water-haemolymph solution, trapped in seawater and tested for induction of shell investigation behavior with juvenile C. vittatus. Only volatiles from C. vittatus haemolymph stimulated shell investigation. Volatile compounds were isolated from haemolymph by headspace solid-phase microextraction (SPME) and analyzed by coupled gas chromatography-mass spectrometry (GC-MS). Two prominent compounds were identified, 3-decanol, which was unique to C. vittatus haemolymph, and 2-ethyl-1-hexanol, which was present in the haemolymph of all 4 crustacean species. In shell investigation bioassays, 3-decanol from C. vittatus haemolymph stimulated shell investigation behavior, while 2-ethyl-1-hexanol did not. In bioassays with synthetic 1-, 2-, 4-, and 5-decanol, shell investigation behavior was evoked by 1-decanol, 5-decanol and 3-undecanol. There was no response to 2- and 4-decanol. The response of C. vittatus to volatile shell cues supports the hypothesis that volatile cue detection evolved prior to the occupation of terrestrial niches by crustaceans.     

Gastropod shells: A potentially limiting resource for hermit crabs

The availability of gastropod shells to hermit crabs in the Newport River Estuary, Beaufort, N.C. has been assessed by determining the numbers of usuable shells occurring in characteristic subtidal habitats and by measuring shell size adequacy. The proportion of useable shells occupied by hermit crabs ranged from 58–99 % and many of the shells not used by hermit crabs were judged unavailable because they were occupied by sipunculids or only uncovered by the dredge. The shell adequacy index (shell size occupied/shell size preferred) was significantly below 1.0 for the largest species (Pagurus pollicaris Say) in the one location where sufficient numbers were collected and for the next largest species (P. longicarpus Say) in three of the four locations where it was collected. The shell size adequacy index for the smallest species (P. annulipes Stimpson) did not differ significantly from 1.0 in either of the two locations in which it was found. These observations suggest that the availability of gastropod shells plays a significant rôle in limiting the abundance of at least the larger hermit crabs.     

A forced association between the slippersnail Crepidula convexa and the hermit crab Pagurus longicarpus?—possible influence from a third party

The suspension-feeding slippersnail Crepidula convexa is commonly associated with hermit crabs (Pagurus longicarpus) living in periwinkle shells (Littorina littorea) at our study site in Nahant, MA, USA. In 15 field surveys conducted at Nahant in 2000, 2001 and 2003, we found that (1) more than 61.8% of individuals of C. convexa resided on shells occupied by hermit crabs, as opposed to the shells of live periwinkles, empty periwinkle shells or other solid substrates; (2) an average of 8.3% of hermit crabs carried at least one individual of C. convexa; and (3) 39.1-75.0% of hermit crabs carrying C. convexa were carrying “large” individuals (snails with wet weight >10% of the weight of the periwinkle shells they occupied). However, it is unlikely that individuals of C. convexa seek out shells occupied by hermit crabs to colonize, and they showed no preference for empty periwinkle shells over other solid substrates in the laboratory. Moreover, in the laboratory the hermit crabs preferentially occupied intact shells bearing individuals of C. convexa only when the alternatives were shells that had been drilled by naticid snails. Thus, neither party preferentially associates with the other: rather, extensive predation by naticid snails on periwinkles at Nahant appears to limit the availability of suitable shells for the hermit crabs, forcing them to inhabit shells bearing “large” individuals of C. convexa. Individuals of C. convexa may benefit from this inadvertent association with hermit crabs: by facilitating snail dispersal, transport by hermit crabs should reduce the potential for inbreeding, an important consideration for a species that lacks free-living larvae in its life history.     

Biological features of a puzzling symbiotic association between the hermit crab Dardanus insignis and the porcellanid crab Porcellana Sayana (Crustacea)

The symbiotic lifestyle is widespread among porcellanid crabs, which maintain ecological and co-evolutionary associations with annelid polychaetes, poriferans, cnidarians, echinoderms, gastropod mollusks, and other crustaceans such as shrimps and hermit crabs, among others. We investigated the ecological association between the hermit crab Dardanus insignis and the porcellanid Porcellana sayana, in southeastern Brazil. Porcellanid crabs, hermit crabs, and available shells were collected monthly from July 2001 to June 2003, with a shrimp boat equipped with two double-rig trawl nets. The majority of P. sayana specimens were collected in shells occupied by D. insignis (96.6%); a few were found in empty shells (3.4%). The catch of both symbionts and hosts increased with increasing depth, with the highest occurrence at 35 m. The P. sayana crabs of various sizes could be found solitary or forming aggregations of up to 14 individuals per host, showing no sex or size segregation. In spite of the high diversity of shell species occupied by the hermit crabs and also available in the field, only a few of them were also utilized by P. sayana. The majority (93%) of shells utilized by P. sayana also hosted other symbiont species, constituting the basis of extensive symbiotic complexes. Thus, the ecological relationship between D. insignis and P. sayana may be classified as a non-obligate and non-specific symbiosis that may also involve other facultative organisms such as sea anemones.     

Symbiosis of sea anemones and hermit crabs: different resource utilization patterns in the Aegean Sea

The small-scale distribution and resource utilization patterns of hermit crabs living in symbiosis with sea anemones were investigated in the Aegean Sea. Four hermit crab species, occupying shells of nine gastropod species, were found in symbiosis with the sea anemone Calliactis parasitica. Shell resource utilization patterns varied among hermit crabs, with Dardanus species utilizing a wide variety of shells. The size structure of hermit crab populations also affected shell resource utilization, with small-sized individuals inhabiting a larger variety of shells. Sea anemone utilization patterns varied both among hermit crab species and among residence shells, with larger crabs and shells hosting an increased abundance and biomass of C. parasitica. The examined biometric relationships suggested that small-sized crabs carry, proportionally to their weight, heavier shells and increased anemone biomass than larger ones. Exceptions to the above patterns are related either to local resource availability or to other environmental factors.     

Intraspecific competition and aggression for shells in the hermit crab Pagurus samuel1s

Many studies have investigated shell‐related behaviour in hermit crabs. Few studies, however, have focused specifically on the intraspecies aggression associated with shell competition. We examined intraspecies aggression in hermit crab (Pagurus samuelis) pairs as it relates to competition for a limiting resource, gastropod shells. Pairs of hermit crabs were observed in the laboratory in four different treatments that varied the presence or absence of shells for one or both of the crabs. Measurements of the latency to respond, the number of bouts, and the fight durations were recorded. There was a significant difference among treatments for all three measurements, and naked hermit crabs were much more aggressive than housed hermit crabs. There was no significant difference in aggression between males and females in any of the three treatments. The heightened aggression observed in naked P. samuelis is likely in service of acquiring a protective shell.     

The effects of shell size and coil orientation on reproduction in female hermit crabs, Clibanarius vittatus

We investigated the effects of shell coil orientation and shell size on reproduction in field populations of the hermit crab, Clibanarius vittatus. Females were collected in the intertidal in Beaufort, NC. Shell parameters were measured and size (cephalothorax length) and reproductive status were determined for 70 females occupying Busycon shells. Crabs were categorized as berried (eggs on the pleopods), mature ovaries, or non-reproductive (no eggs). For berried females, the number of eggs was recorded. By offering a separate group of females access to empty shells, it was possible to calculate optimal shell size and the deficit in shell size for field-collected animals.Females that were berried were in shells closer to the optimal shell size than females with mature ovaries, both for shell weight and shell volume. And females with mature ovaries were in shells that were closer to the optimal size than females that were non-reproductive. For both categories of females without eggs on the pleopods, the majority of females were in shells that were too big (in weight and internal volume). While the percentage of berried females did not differ between dextral (Busycon carica) and sinistral (Busycon sinistrum) shells, the non-reproductive females had a much smaller deficit in volume in sinistral shells compared to dextral shells. For berried females, there was no relationship between the magnitude of their shell deficit and the number of eggs carried. Our results suggest that reproduction is inhibited when females occupy shells sufficiently greater than the optimal shell size.     

Predator discrimination in the hermit crab Calcinus californiensis: tight for shell breakers,loose for shell peelers

Prey exposed to predators with different hunting and feeding modes are under different selective pressures, therefore it is expected that they should exhibit plastic and adaptive antipredator responses according to current risks. The hermit crab Calcinus californiensis faces two contrasting predators, the shell peeler Arenaeus mexicanus that hunts by active searching and the shell breaker Eriphia squamata that hunts by ambush. In order to discover whether C. californiensis displays plastic responses depending on the type of predatory challenge, we examined the shell size preference, the hiding time, and the escape velocity of hermit crabs in the presence of chemical cues from a shell peeler, a shell breaker, and a control. We also examined the role of shell fit on the escape velocity of the hermit crabs in natural tidal pools. Crabs chose shells with a loose fit (relatively large shells) in the presence of chemical cues from the shell peeler Arenaeus and shells with a tight fit when exposed to cues from the shell breaker Eriphia. The hermit crabs hid for shorter times and moved away faster from Eriphia than from Arenaeus stimulus. The use of a tight shell favours faster movement away from the shell breaker (pre‐capture strategy), but prevents the crab retracting deeper inside the shell, increasing the risk of be eaten by the shell peeler once captured. Hence, the use of loose shells that protect the crab from the shell peeler hinders fast escape. This study shows specific and plastic antipredatory responses to contrasting predators, each bringing adaptive benefits at different levels of the predator sequence.     

Shell recruitment in the Mediterranean hermit crab Clibanarius erythropus

Gastropod shells are vital for the majority of hermit crab species, being essential for their survival, growth, protection, and reproduction. Given their importance, shells are acquired and transferred between crabs through several modalities. We conducted observations and experiments at the Asinara Island (Sardinia, Italy) to investigate the efficacy of the different behavioral tactics adopted by the hermit crab Clibanarius erythropus to acquire shells, such as: (1) locomotion and activity at different tidal phases; (2) attendance at shell-supplying sites (simulated predation sites with five different odors: live and dead gastropods, live and dead crabs, predator); and (3) interactions with conspecifics in aggregations on simulated gastropod predation sites. In each tidal phase, locomotion was slow (0.7 cm min^− 1) and, as a consequence, the probability of encountering empty shells and conspecifics was low. Simulated gastropod predation sites quickly attracted a larger number of hermit crabs than the other sites tested. Aggregations seemed to function as shell exchange markets, as previously suggested for other species: the first attendant took the experimental shell and a chain of shell exchanges among conspecifics followed. Our results show that, in C. erythropus, aggregation is the most efficient tactic for the acquisition of new shells, whereas in other species, such as Pagurus longicarpus, it is associated with exploitation ability due to the intense locomotion. The interspecific plasticity in hermit crabs' behavior is confirmed.     

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

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.     

Why small hermit crabs have large shells

Frequent shell exchanges among hermit crabs imply the enigmatic circumstance that large crabs frequently obtain large shells from smaller crabs. This seeming anomaly is explored as a key to the shell resource system. It is hypothesized to reflect how, where, and how often shells become available to the crabs. Shells become available infrequently, as snails die, and are available to the crabs for only a brief time before they become inaccessible. The standing crop of empty shells is almost always low and is irrelevant to rates of shell turnover in the crab population. Crabs are most likely to encounter shells of the wrong size, and the chance of encountering a shell of the desired size decreases as a crab grows. Snails and crabs are usually found on different portions of the shore; thus, crabs must make “foraging trips” for shells. Under this regime of shell supply, a crab will get a suitable shell the fastest when it accepts any fresh shell that is larger than its initial shell. It can then trade with other crabs to improve its shell fit. This behavior will make small crabs into a regular source of large shells for large crabs, and a shell exchange ritual will be strongly favored because both participants will benefit. Shells are an unusual resource because they are the object of both competitive and mutualistic interactions. This ambiguous quality is revealed in the intraspecific and interspecific responses of crabs to each other and to shells.     

Influence of prior experience on shell selection by the white spotwrist hermit crab Pagurus criniticornis (Crustacea: Paguridae)

Individuals of Pagurus criniticornis in a free-choice situation were experimentally tested under different laboratory conditions. In order to assess the effect of recently occupied shells on the size- and type-preference by hermit crabs, individuals were held for 30 days under one of the following two conditions: (1) excess of shells and (2) absence of shells. The crabs were then allowed to select shells from a wide array of empty gastropod shells of the two most-occupied species, as observed previously in the field: Cerithium atratum and Morula nodulosa. Preferred shell type (species) and size (shell aperture width and length) were correlated with hermit-crab size. The crabs showed a strong (100%) preference for C. atratum shells, demonstrating that recent and past experience did not influence either shell-type or shell-size preferences in this pagurid. Handling editor: K. Martens     

Are the preference and selection patterns of hermit crabs for gastropod shells species- or site-specific?

Experimental analyses of hermit crabs and their preferences for shells are essential to understand the intrinsic relationship of the crabs' dependence on shells, and may be useful to explain their shell use pattern in nature. The aim of this study was to evaluate the effect of crab species and site on the pattern of shell use, selection, and preference in the south-western Atlantic hermit crabs Pagurus brevidactylus and Pagurus criniticornis, comparing sympatric and allopatric populations. Differently from the traditional approach to evaluate shell preference by simply determining the shell selection pattern (i.e., the number of shells of each type selected), preference was defined (according to [Liszka, D., Underwood, A.J., 1990. An experimental design to determine preferences for gastropod shells by a hermit-crab. J. Exp. Mar. Biol. Ecol., 137(1), 47–62]) by the comparison of the number of crabs changing for a particular shell type when three options were given (Cerithium atratum, Morula nodulosa, and Tegula viridula) with the number of crabs changing for this same type when only this type was offered. The effect of crab species was tested at Cabelo Gordo Beach, where P. brevidactylus was found occupying shells of C. atratum, M. nodulosa, and T. viridula in similar frequencies, whereas P. criniticornis occupied predominantly shells of C. atratum. In laboratory experiments the selection patterns of the two hermit-crab species for these three gastropods were different, with P. criniticornis selecting mainly shells of C. atratum, and P. brevidactylus selecting more shells of M. nodulosa. The shell preference was also dependent on crab species, with P. criniticornis showing a clear preference for shells of C. atratum, whereas P. brevidactylus did not show a preference for any of the tested shells. The effect of site was tested for the two species comparing data from Cabelo Gordo to Preta (P. brevidactylus) and Araçá beaches (P. criniticornis). The pattern of shell use, selection, and preference was demonstrated to be dependent on site only for P. brevidactylus. The results also showed that the shell use pattern of P. criniticornis can be explained by its preference at both sites, whereas for P. brevidactylus it occurred only at Cabelo Gordo, where the absence of preference was correlated with the similar use of the three gastropod species studied. Finally, the results showed that the shell selection pattern cannot be considered as a measure of shell preference, since it overestimates crab selectivity.     

Reproductive costs of the symbiotic hydroid Hydractinia symbiolongicarpus (Buss and Yund) to its host hermit crab Pagurus longicarpus (Say)

Studies on the interaction between the hermit crab Pagurus longicarpus and its symbiotic hydroid Hydractinia symbiolongicarpus have focused on positive effects of hydroids on their host hermit crabs (e.g., protection from predators). Yet, these benefits may be balanced with reproductive costs, which are rarely studied. Results from field observations, laboratory trials, and a mesocosm experiment indicate that female hermit crabs in hydroid-colonized shells exhibit depressed ovigery, smaller clutch sizes, and increased clutch failure relative to females in bare shells. Frequent switching between bare and hydroid-colonized shells may alleviate negative effects when the density of hydroids in the environment is low, but at high densities Hydractinia may significantly impact hermit crab reproduction.     

Effects of chemical context on shell investigation behavior in hermit crabs

Specific chemicals in the environment evoke significant changes in the behavior of many aquatic organisms. We studied in the laboratory whether satiated individuals of the hermit crab, Pagurus longicarpus Say 1817, adjust their investigatory behavior towards an empty, optimal gastropod shell according to differences of chemical context. We also explored to what extent shell investigation by a crab in the same hunger state was affected by occupying an inadequately sized shell. Our results confirmed in part previous findings that crabs can discriminate the odor of freshly dead snails from the odor of freshly dead conspecifics. In the presence of the former odor, crabs inhabiting shells of inadequate size were more responsive and active than those in better-fitting shells. To the contrary, regardless of the quality of the inhabited shell, P. longicarpus remained practically motionless when presented with the odor of freshly dead conspecifics, possibly because the risks of incurring in predators would outweigh the benefits of acquiring a new shell. Unexpectedly, we found that crabs in both types of shell quality exhibited nearly the same behavior in control water, while crabs in adequate shells were more responsive in the presence of food odor. Individuals appeared insensitive to the odor of live snails; indeed, only one hermit crab species has been seen removing living snails from their shells. An intriguing result was that water conditioned by the odors of live conspecifics exerted a strong effect on all the individuals by inducing an intense shell investigation. Our study underlines the central role exerted by chemical detection in hermit crabs' behavior and demonstrates the existence of a complex interplay among chemical context, the physiological state of the animal, and the ecological pressures of the habitat.     

Effect of gastropod shell characteristics and hermit crabs on shell Epifauna

The epifauna on gastropod shells occupied by the hermit crabs Pagurus pollicaris (Say) and P. longicarpus (Say) was examined, as was the utilization of shells by these two hermit crabs. In the study area in Tampa Bay, Florida, shells were not a limiting factor to the hermit crab population, and there apparently was little competition for shells. Interspecific competition for shells was limited because the two hermit crab species differed in size and hence occupied shells of different sizes. The total number and density of most epifaunal species were higher on shells occupied by hermit crabs than on unoccupied shells, possibly because hermit crabs prevent their shells from being buried and hence lengthen the time the epifaunal community can grow and develop. The hermit crab species also appeared to affect the epifaunal community, for the total number and density of most epifaunal species were larger on shells occupied by P. pollicaris than P. longicarpus. With increasing shell size, the populations of most epifaunal species, also were larger but not their density. Least influential in affecting the epifaunal community was the species of shells.