Vacancy Chains Provide Aggregate Benefits To Coenobita clypeatus Hermit Crabs

Vacancy chain theory describes a unique mechanism for the sequential distribution of animal resources across multiple individuals. This theory applies to any resources, such as shelters or nest sites, that are discrete, reusable, and limited in use to single individuals or groups at one time. Hermit crabs rely on gastropod shells for shelter, and a single vacant shell can initiate a chain of sequential shell switches that distributes new resources across many individuals. Using the terrestrial hermit crab Coenobita clypeatus , we examined the previously untested theoretical prediction that this process will yield trickle-down resource benefits to vacancy chain participants (aggregate benefits). In laboratory experiments, we measured improvements in shell quality when a single vacant shell was provided to groups of eight crabs. We found that crabs participating in vacancy chains (averaging 3.2 individuals) gained significant reductions in their shell crowding. In addition, vacancy chains terminated early when experimental groups included a single crab occupying a damaged shell, because damaged vacancies always remained unoccupied. Hermit crabs in damaged shells were more likely to win resource contests for high quality shells against size-matched hermit crabs in crowded shells. Finally, field additions of many new shells to an island population of C. clypeatus hermit crabs reduced average shell crowding for crabs of all sizes, possibly from propagation of benefits through vacancy chains. These results provide empirical support for the theoretical prediction that vacancy chains should provide benefits distributed across many vacancy chain participants. Since shelter-based vacancy chains likely occur in other animals, additional studies of vacancy chain processes should provide new insights into resource acquisition behaviors in diverse animal groups.     

The vacancy chain process: a new mechanism of resource distribution in animals with application to hermit crabs

A number of resources important to humans such as jobs in bureaucracies, houses and apartments are allocated through a mechanism known as a vacancy chain. In a vacancy chain process an initial, vacant resource unit entering a population of users is taken by a first individual who leaves his/her previous resource unit behind, which is taken by a second individual, and so on. In this process an initial resource unit works both directly and indirectly to provide opportunities for several individuals to gain new and better resources. Vacancy chains are hypothesized to be important in resource distribution for a variety of non-human animals, and it is documented, in particular, that the hermit crab Pagurus longicarpus gets the gastropod shells in which it lives through this mechanism. The direct and indirect effects of vacancy chains on hermit crabs and the systematic ways in which chains flow through groups of crabs and their resources are indicated. In systems where they occur, it is further hypothesized that vacancy chains have unique implications for the ecology of resource users. Several of these hypotheses are explored using the example of hermit crabs.     

The Influence of Personality on a Group‐Level Process: Shy Hermit Crabs Make Longer Vacancy Chains

Animal personality has been investigated in a variety of contexts but few studies have investigated the effects of individual‐level traits on processes that occur at the group or population level. Vacancy chains describe sequences of linked vacancy moves in systems where individuals use discrete and reuseable resource units. When a new resource unit becomes available, this can cause a cascade of moves between resource units, beyond the first individual that encounters the new unit. Thus, vacancy chains can drive the distribution of resources through a population. Here, I investigate the effect of variation in boldness on movements between vacant gastropod shells in the hermit crab Pagurus bernhardus. Boldness was quantified using the duration of a startle response, which varied consistently between individuals. In groups of five crabs, introduction of a single new shell led to aggregate benefits, in terms of improving shell quality, across all group members. Boldness did not influence the extent of these benefits or the extent to which they were distributed between crabs of different sizes. Initially, vacancy chains were longer, indicating that more individuals moved between shells, for bold groups compared with shy groups. After 24 h, however, the chain length was longer for shy groups. Thus, although participation in a vacancy chain may lead to similar benefits, these could be more widespread for groups comprising shy individuals that show long startle responses, low inquisitiveness and low aggression. Similar effects on resource acquisition could be present in other examples of animals that utilise reusable resource units and show consistent between‐individual differences in behaviour.     

Gastropod shells: A dynamic resource that helps shape benthic community structure

Empty gastropod shells are an important resource for many animals in shallow benthic marine communities. Shells provide shelter for hermit crabs, octopuses, and fishes, provide attachment substratum for hermit crab symbionts, and directly or indirectly modify hermit crab predation. Creation of an empty shell due to predation of one gastropod on another and acquisition of that shell by a hermit crab are two key events in the subsequent use of that shell. Shells of different gastropod species and the species of hermit crab acquiring them affect the symbiont complement that attaches to the shell, which in turn may affect future shell use by other symbionts. Certain shell types worn by the hermit crab, Pagurus pollicaris Say, are positively associated with the symbiotic sea anemone, Calliactis tricolor (Lesueur), which protects the hermit crab from predation by the crab, Calappa flammea (Herbst), and possibly from the octopus, Octopus joubini Robson. Shells of other species of gastropods are resistant to being crushed by the spiny lobster, Panulirusargus (Latreille). The inter-and intraspecific interactions centered on the gastropod shell are termed a “habitat web.” The potential of the shell to limit the size and distribution of animal populations demonstrates how this resource helps shape community structure.     

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.     

Interference and exploitation components in interespecific competition between sympatric intertidal hermit crabs

This study was designed to evaluate the effect of interference and exploitation competition in shell partitioning between two hermit crab species (Pagurus criniticornis and Clibanarius antillensis). Field samples revealed that shells of the gastropod Cerithium atratum were the main resource used by both hermit crab species and that Pagurus used eroded or damaged shells in higher frequency than Clibanarius. The exploitative ability of each species was compared between species in the laboratory using dead gastropod (Cerithium) baits to simulate predation events and signalize newly available shells to hermit crabs. Pagurus reached the baits more rapidly than Clibanarius, but this higher exploitative ability did not explain shell utilization patterns in nature. Another experiment evaluated the dominance hierarchy between these two hermit crab species and revealed that Clibanarius was able to outcompete Pagurus for higher quality shells in agonistic encounters. This higher interference competitive ability of Clibanarius in relation to Pagurus may explain field observations. Nevertheless, Pagurus may be responsible to enhance shell availability to other hermit crab species that have lower ability to find and use newly available shells. Differently, the poorer condition of shells used by Pagurus, the higher ability of this species to attend gastropod predation events and its higher consumption rate by shell-breaking crabs (Menippe nodifrons) may increase its predation risks, thus revealing the disadvantages of such an exploitative competitive strategy for hermit crabs.     

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.     

What makes a good home for hermits? Assessing gastropod shell density and relative strength

The survival and reproductive success of hermit crabs is intrinsically linked to the quality of their domicile shells. Because damaged or eroded shells can result in greater predation, evaluating shell structure may aid our understanding of population dynamics. We assessed the structural attributes of Cerithium atratum shells through assessments of (a) density using a novel approach involving computed tomography and (b) tolerance to compressive force. Our goal was to investigate factors that may influence decision making in hermit crabs, specifically those that balance the degree of protection afforded by a shell (i.e. density and strength) with the energetic costs of carrying such resources. We compared the density and relative strength (i.e. using compression tests) of shells inhabited by live gastropods, hermit crabs (Pagurus criniticornis) and those found empty in the environment. Results failed to show any relationship between density and shell size, but there was a notable effect of shell density among treatment groups (gastropod/empty/hermit crab). There was also a predictable effect of shell size on maximum compressive force, which was consistent among occupants. Our results suggest that hermit crabs integrate multiple sources of information, selecting homes that while less dense (i.e. reducing the energy costs of carrying these resources), still offer sufficient resistance to compressive forces (e.g. such as those inflicted by shell-breaking predators). Lastly, we show that shell size generally reflects shell strength, thus explaining the motivation of hermit crabs to search for and indeed fight over the larger homes.     

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.     

An analysis of competitive interactions between 3 hermit crab species

Summary Competition for empty gastropod shells in a group of three sympatric hermit crabs (Pagurus hirsutiusculus, Pagurus granosimanus, and Pagurus beringanus) was studied in the San Juan Archipelago, Washington State. Estimates of the competitive effects of each species on the others' shell supplies were derived using field data on shell utilization and the results of laboratory experiments to determine rates of acquisition and exchange of shells and preferences for different shell species. Each species experienced approximately an order of magnitude more intraspecific competition than interspecific competition for empty shells. This resulted from differences in preference for shell shapes, shell size use, and habitat use between P. hirsutiusculus and P. granosimanus, and largely from differences in habitat use between P. beringanus and the other two species. Experiments involving the release and recensusing of marked empty shells were used to estimate competitive effects more directly for the interaction between P. hirsutiusculus and P. granosimanus. Results were consistent with the estimates derived from data on resource partitioning. Possible causes of the low levels of interspecific competition are discussed, and results are compared with studies of other organisms that estimated both inter- and intra-specific competition.     

Shell fights in the hermit crabPagurus geminus: Computer simulation and experiment

The shell exchange in the hermit crabPagurus gemiuns was examined by computer simulations and experiments, to learn whether it is based on mutualistic interactions with both participants gaining, or on one-sided interactions with the large crab gaining regardless of loss and gain of the partner. The result of the experiment showed a much better fit to that of the one-sided simulation than the mutualistic simulation, suggesting that competitive interactions in which small crabs lose in the resulting shell exchanges are a part of shell fights of this species. While the shell exchange attempt can be regarded as aggressive, a higher probability of mutualistic encounters and of successful mutualistic shell exchanges in hermit crabs is discussed.     

Land hermit crab (Coenobita clypeatus) densities and patterns of gastropod shell use on small Bahamian islands

Aim To examine patterns of abundance, density, size and shell use in land hermit crabs, Coenobita clypeatus (Herbst), occurring on three groups of small islands, and to determine how these variables change among islands. Location Small islands in the Central Exuma Cays and near Great Exuma, Bahamas. Methods Land hermit crabs were captured in baited pitfall traps and were separately attracted to baits. A mark–recapture technique was used in conjunction with some pitfall traps monitored for three consecutive days. The size of each crab and the type of adopted gastropod shell were recorded, along with physical island variables such as total island area, vegetated area, island perimeter, elevation and distance to the nearest mainland island. Results Relative abundances, densities and sizes of crabs differed significantly among the three island groups. Densities of land hermit crabs were as high as 46 m⁻² of vegetated island area. In simple and multiple linear regressions, the only variable that was a significant predictor of the abundance of hermit crabs was the perimeter to area ratio of the island. Patterns of gastropod shell use varied significantly among the island groups, and the vast majority of adopted shells originated from gastropod species that inhabit the high intertidal and supratidal shorelines of the islands. Main conclusions Although densities of land hermit crabs varied, they were relatively high on many islands, and land hermit crabs may play an important role in these insular food webs. Patterns of shell use may be strongly restricted by island geomorphology: irregular shorelines provide relatively more habitat for the gastropod species that account for the majority of adopted shells and the steep sides of the islands prevent the accumulation of marine gastropod shells. The size of adult hermit crabs appears to be limited by the relatively small gastropod shells available, while the abundance of hermit crabs may be limited by the number of shells available.     

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.     

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.     

Invasive ants compete with and modify the trophic ecology of hermit crabs on tropical islands

Invasive species can dramatically alter trophic interactions. Predation is the predominant trophic interaction generally considered to be responsible for ecological change after invasion. In contrast, how frequently competition from invasive species contributes to the decline of native species remains controversial. Here, we demonstrate how the trophic ecology of the remote atoll nation of Tokelau is changing due to competition between invasive ants (Anoplolepis gracilipes) and native terrestrial hermit crabs (Coenobita spp.) for carrion. A significant negative correlation was observed between A. gracilipes and hermit crab abundance. On islands with A. gracilipes, crabs were generally restricted to the periphery of invaded islands. Very few hermit crabs were found in central areas of these islands where A. gracilipes abundances were highest. Ant exclusion experiments demonstrated that changes in the abundance and distribution of hermit crabs on Tokelau are a result of competition. The ants did not kill the hermit crabs. Rather, when highly abundant, A. gracilipes attacked crabs by spraying acid and drove crabs away from carrion resources. Analysis of naturally occurring N and C isotopes suggests that the ants are effectively lowering the trophic level of crabs. According to δ¹⁵ N values, hermit crabs have a relatively high trophic level on islands where A. gracilipes have not invaded. In contrast, where these ants have invaded we observed a significant decrease in δ¹⁵ N for all crab species. This result concurs with our experiment in suggesting long-term exclusion from carrion resources, driving co-occurring crabs towards a more herbivorous diet. Changes in hermit crab abundance or distribution may have major ramifications for the stability of plant communities. Because A. gracilipes have invaded many tropical islands where the predominant scavengers are hermit crabs, we consider that their competitive effects are likely to be more prominent in structuring communities than predation. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Avoidance of drilled gastropod shells by the hermit crab Pagurus longicarpus at Nahant, Massachusetts

Most hermit crabs depend on empty gastropod shells for shelter; competition for appropriate shells is often severe. This study determined whether shells that have been drilled by naticid gastropods are suitable for occupancy by the hermit crab Pagurus longicarpus. Differences in the characteristics of empty shells and those occupied by hermit crabs were assessed at two adjacent field sites in Nahant, Massachusetts. Drilling damage was far more frequent in empty gastropod shells than in shells occupied by hermit crabs, suggesting that individuals of P. longicarpus avoid drilled shells. They did not appear to avoid shells with other forms of damage. Laboratory experiments confirmed that these hermit crabs preferentially chose intact shells over drilled shells, even when the intact shells offered were most suitable for crabs half the weight of those tested. Final shell choices were generally made within 1 h. The hermit crabs apparently discriminated between intact and drilled shells based on tactile cues, since crabs kept in the dark showed the same preference for intact shells. The hermit crabs strongly avoided, to nearly the same extent, artificially drilled shells, naturally drilled shells, and shells with holes artificially drilled on the opposite side of the shell from where they would normally be located. Possible selective forces causing P. longicarpus to show such strong behavioral avoidance of drilled shells include increased vulnerability of crabs in drilled shells to osmotic stress, predation, and eviction by conspecifics.     

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.     

Feeding and metabolic compensations in response to different foraging costs

How energetic cost of locomotion affects foraging decisions, and its metabolic consequences are poorly understood. In several groups of animals, including hermit crabs, exploratory walking enhances the efficiency of foraging by increasing the probability of finding more and better food items; however, the net gain of energy will only be enhanced if the costs of walking are lower than the benefits of enhanced food acquisition. In hermit crabs, the cost of walking increases with the mass of the shell type occupied. Thus, we expected that hermit crabs should adjust their foraging strategy to the cost of movement in different shells. We assessed the foraging, the quantity and quality of food intake, and the energetic cost of maintenance of hermit crabs paying different costs of foraging in the wild. The exploratory walking negatively correlated with shell mass, showing that hermit crabs use different foraging strategies in response to the expenditure required to move. Hermit crabs deal with high energetic costs of foraging in heavy shells by reduces their exploratory walking and overall metabolic rate, as a strategy to maximize the net energy intake. This study integrates behavioral and metabolic compensations as a response to foraging at different costs in natural conditions.     

How resource quality differentially affects motivation and ability to fight in hermit crabs

Contesting animals typically gather information about the resource value and that information affects fight motivation. However, it is possible that particular resource characteristics alter the ability to fight independently of the motivation. Using hermit crabs, we investigate how the resource in terms of shell quality affects both motivation and ability to fight. These crabs fight for shells, but those shells have to be carried and may impose physiological costs that impede fight vigour. We find that the shell has different effects on motivation and ability. Potential attackers in very small shells were highly motivated to attack but, rather than having enhanced ability, unexpectedly quickly fatigued and subsequently were not more successful in the fights than were crabs in larger shells. We also examined whether defending crabs could gather information about the attacker''s shell from the vigour of the attack. Defending crabs gave up quickly when a potential gain had been assessed, indicating that such information had been gathered. However, there was no indication that this could be owing to the activity of the attacker and the information is probably gathered via visual assessment of the shell.