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.     

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.     

Hermit crabs and their symbionts: Reactions to artificially induced anoxia on a sublittoral sediment bottom

Hermit crabs play an important role in the Northern Adriatic Sea due to their abundance, wide range of symbionts, and function in structuring the benthic community. Small-scale (0.25?m(2)) hypoxia and anoxia were experimentally generated on a sublittoral soft bottom in 24?m depth in the Gulf of Trieste. This approach successfully simulates the seasonal low dissolved oxygen (DO) events here and enabled studying the behaviour and mortality of the hermit crab Paguristes eremita. The crabs exhibited a sequence of predictable stress responses and ultimately mortality, which was correlated with five oxygen thresholds. Among the crustaceans, which are a sensitive group to oxygen depletion, P. eremita is relatively tolerant. Initially, at mild hypoxia (2.0 to 1.0?ml?l(-?1) DO), hermit crabs showed avoidance by moving onto better oxygenated, elevated substrata. This was accompanied by a series of responses including decreased locomotory activity, increased body movements and extension from the shell. During a moribund phase at severe hypoxia (0.5 to 0.01?ml?l(-?1) DO), crabs were mostly immobile in overturned shells and body movements decreased. Anoxia triggered emergence from the shell, with a brief locomotion spurt of shell-less crabs. The activity pattern of normally day-active crabs was altered during hypoxia and anoxia. Atypical interspecific interactions occurred: the crab Pisidia longimana increasingly aggregated on hermit crab shells, and a hermit crab used the emerged infaunal sea urchin Schizaster canaliferus as an elevated substrate. Response patterns varied somewhat according to shell size or symbiont type (the sponge Suberites domuncula). Mortality occurred after extended anoxia (~?1.5?d) and increased hydrogen sulphide levels (H(2)S ~?128?μmol). The relative tolerance of crabs and certain symbionts (e.g. the sea anemone Calliactis parasitica) - as potential survivors and recolonizers of affected areas - may influence and promote community recovery after oxygen crises.     

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.     

Chemical recognition by hermit crabs of their symbiotic sea anemones and a predatory octopus

The ability of the hermit crabs Dardanus venosus and Pagurus pollicaris to recognize chemically their symbiotic sea anemone Calliactis tricolor and a common octopus predator, Octopus joubini, were studied. The crabs were tested for chemoreceptive responses using a Y-trough olfactometer, which prevented visual cues from being used. Choice tests showed that D. venosus could chemically detect Calliactis. If, however, D. venosus had a Calliactis on its shell at the time of the trial, it could not detect the test anemone. P. pollicaris (without a symbiotic anemone) did not locate the test anemone. Both species of crab avoided a water current carrying octopus chemical cues. Chemoreception may play an important role in the interaction of a hermit crab with its symbiotic anemone and an octopus predator.     

The nature of the adhesion of tentacles to shells during shell-climbing in the sea anemone Calliactis parasitica (Couch)

Phase contrast microscopy and scanning electron microscopy show that during the response of the symbiotic sea anemone Calliactis parasitica (Couch) to shells of Buccinum undatum (L.) three times as many spirocysts as nematocysts are discharged. Observations indicate that spirocysts are responsible for the adhesion of tentacles to shells.Discharge levels are not significantly influenced by the nature of the substratum to which the anemones are attached. The reported observation that fewer tentacles adhere to shells when anemones are settled on shells than when they are fixed on a different substratum is re-interpreted in terms of a new model for the control of spirocyst discharge.     

Predation on symbiont sea anemones by their host hermit crab Dardanus pedunculatus

Feeding by host hermit crabs Dardanus pedunculatus on their symbiotic sea anemones Calliactis polypus was investigated using animals collected at Shirahama, Wakayama Prefecture, Japan. In the first experiment, changes in the number of sea anemones on hermit crab shells were recorded in single‐and double‐crab trials without food and single‐crab trials with food. The number of sea anemones significantly decreased under starved conditions. The extent of this decrease per single hermit crab was higher in the double‐crab trials than in the single‐crab trials. Direct observations and video recordings showed that hermit crabs occasionally removed sea anemones from their own shells, and also from partners’ shells in the double‐crab trials, and consumed them. In the second experiment, fed and unfed hermit crabs with or without sea anemones were examined for body weight changes. Fed hermit crabs gained weight whereas unfed hermit crabs lost it. The degree of weight loss in unfed hermit crabs was significantly higher in those without sea anemones, which indicates some value of the latter as food. We offer some speculations on the course of development of this symbiosis, with predation on sea anemones having played an important initial role.     

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.     

The behavior of Dardanus arrosor in association with Cailiactis parasitica in artificial habitat

In the artificial habitat of an aquarium specimens of hermit crabs carrying commensal sea anemones gradually lose their anemones, surprisingly because the crabs frequently damage or eat them.

On the Mediterranean association Dardanus arrosor and Calliactis parasitica, the influence of feeding, of population density, or the activity of Dardanus towards Calliactis, and the presence or absence of a predator, were investigated as possible factors responsible for the disappearance of the anemone and the anomalous behavior of the crabs.

Both lack of food and high population density increased the numbers of anemones that disappeared. It was noted that these artificial conditions probably do not occur in the natural habitat. All freshly collected Dardanus (both sexes), and presumably all Dardanus in their natural habitat, are active in acquiring Calliactis but during 4–5 months in the aquarium most of this activity is lost.

In the presence of a probable predator, the octopus Eledone, these inactive crabs become active again in transferring anemones to their shells. This suggests that predation in the natural habitat is one of the factors responsible for the activity of the crab in acquiring anemones, at least in the association between Dardanus arrosor and Calliactis parasitica.     

Information transfer during shell exchange in the hermit crab Clibanarius antillensis

The shell exchange behaviour of the hermit crab Clibanarius antillensis was examined for evidence that the non-initiating crab used information about the initiator's shell. Manipulation of the internal volume of the initiator's shell altered the outcome of exchanges in a manner consistent with the negotiations model of resource exchange. It is suggested that the fundamental frequency of shells is detected by crabs during rapping behaviour when the initiator raps its shell against that of the non-initiator.     

Crab shell-crushing predation and gastropod architectural defense

The shell-breaking behavior of the crabs Ozius verreauxii Saussure 1853 and Eriphia squamata, Stimpson 1859 from the Bay of Panama is described. The master claws of both these crabs are well designed for breaking shells. Small shells, relative to the size of a crab predator, are crushed by progressively breaking off larger segments of a shell's apex, while larger shells are peeled by inserting a large dactyl molar into the aperture of a shell and progressively chipping away the lip of the shell.

Heavy gastropod shells are shown to be less vulnerable to crab predators than lighter shells, and narrow shell apertures and axial shell sculpture are demonstrated to be architectural features that deter crab predation. The incidence of architectural features which deter crab predation appears to be higher for smaller gastropod species than for larger gastropods which are too large for most crab predators. Large fish predators prey upon both gastropods and shell-crushing crabs. To avoid fish predators, both these prey groups seek refuge under rocks when covered by the tide. Fish predation thus appears to enforce a close sympatry between smaller gastropods and their crab predators.     

Response of hermit crabs to sinistral shells

Shell rotating behavior of the hermit crabPagurus geminus was investigated. In preliminary observations, hermit crabs motivated to change shells rotated presented shells, filled with sand, in a way that dislodged the inside material. In order to determine if this behavior is stereotyped, or flexible and dependent on shell type, hermit crabs were tested with ordinary dextral shells ofLatirulus nagasakiensis and sinistral shells ofAntiplanes contraria. Sinistral shells are not normally encountered by hermit crabs. Their rotation of the dextral shell to the left was adequate for sand discharge. Sinistral shells were rotated in both directions. Analysis of recorded videotapes showed that variation in rotation direction could be attributed to variation in the position of the crab relative to the shell. When the crab faced the shell aperture from the inner lip, it rotated the sinistral shell to the right, and to opposite direction when it faced from the outer lip side. The crab always pushed the upper side of the horizontally laid shell, regardless of shell type or its own position.     

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.     

Agonistic Behaviour and Development of Territoriality During Ontogeny of the Sea Anemone Dwelling Crab Allopetrolisthes Spinifrons (H. Milne Edwards, 1837) (Decapoda: Anomura: Porcellanidae)

Allopetrolisthes spinifrons is an ectosymbiotic crab of the sea anemone Phymactis clematis . As a consequence of low host abundance, these represent a scarce and limited resource for the crab. Additionally, the relatively small size of the sea anemone host suggests that few symbiotic crabs can cohabit on one host individual, forcing crabs to adopt a territorial behaviour. In order to examine the potential presence and ontogenetic development of territoriality, the agonistic behaviour between crabs of various ontogenetic stages (adults, juveniles, and recruits) was studied in the laboratory. Laboratory experiments demonstrated that adult or juvenile crabs aggressively defended their sea anemone hosts against adult or juvenile intruders, respectively, but both adult and juvenile crabs tolerated recruits. Adult crabs behaved indifferently towards juvenile crabs, sometimes tolerating them, sometimes expelling them. Recruits never showed agonistic behaviour among themselves. The agonistic interactions observed in the laboratory and the uniform population distribution pattern on sea anemones recently described for A . spinifrons indicate that this species exhibits territorial behaviour, which develops during ontogeny. Territoriality in this species and other symbiotic decapods may function as a density-dependent mechanism of population regulation, being mediated by the availability of hosts. Resource monopolisation behaviours may be common among other symbiotic and free-living marine invertebrates inhabiting discrete habitats that represent a limiting resource.     

Agonistic Behaviour and Development of Territoriality During Ontogeny of the Sea Anemone Dwelling Crab Allopetrolisthes Spinifrons (H. Milne Edwards, 1837) (Decapoda: Anomura: Porcellanidae)

Allopetrolisthes spinifrons is an ectosymbiotic crab of the sea anemone Phymactis clematis. As a consequence of low host abundance, these represent a scarce and limited resource for the crab. Additionally, the relatively small size of the sea anemone host suggests that few symbiotic crabs can cohabit on one host individual, forcing crabs to adopt a territorial behaviour. In order to examine the potential presence and ontogenetic development of territoriality, the agonistic behaviour between crabs of various ontogenetic stages (adults, juveniles, and recruits) was studied in the laboratory. Laboratory experiments demonstrated that adult or juvenile crabs aggressively defended their sea anemone hosts against adult or juvenile intruders, respectively, but both adult and juvenile crabs tolerated recruits. Adult crabs behaved indifferently towards juvenile crabs, sometimes tolerating them, sometimes expelling them. Recruits never showed agonistic behaviour among themselves. The agonistic interactions observed in the laboratory and the uniform population distribution pattern on sea anemones recently described for A. spinifrons indicate that this species exhibits territorial behaviour, which develops during ontogeny. Territoriality in this species and other symbiotic decapods may function as a density-dependent mechanism of population regulation, being mediated by the availability of hosts. Resource monopolisation behaviours may be common among other symbiotic and free-living marine invertebrates inhabiting discrete habitats that represent a limiting resource.     

The effects of exposure and predation on the shell of two British winkles

Changes in shell size and shell shape of the two British winkles Littorina nigrolineata and L. rudis were studied in relation to exposure and to crab-size. In both species, shells from exposed shores are smaller and more globose than those from sheltered shores. Also, in rudis of exposed shores the mouth is relatively wider. In shores of equally sheltered conditions, shells are bigger at those localities where crabs are large than at those localities where they are small. The largest shells are found in those localities where it is extremely sheltered, and the crabs are very large.
It is argued that on exposed shores, small shells are favoured because they have more possibilities than large ones to shelter in crevices and in barnacle interspaces, from the impact of winds and waves. A globose shell could accommodate more foot muscle and thus enable a stronger adherence to the rock; and an increased mouth diameter would increase the area of foot adherence to the rock. On sheltered shores, on the other hand, large, narrow-mouthed shells are favoured because they discourage crab predation, large crabs being abundant mainly on sheltered shores.
The possible significance of shell size and shape in relation to zonation is discussed, in view of the different predatory and physical conditions which prevail in different zones of the shore, and the different shell specializations which these conditions would require.     

The Social Structure of Inachus phalangium,a Spider Crab Associated with the Sea Anemone

The behaviour of the spider crab Inachus phalangium (Fabricius, 1775), which lives in association with the sea anemone Anemonia sulcata (Pennant), was studied in the field. The crab was found in the littoral zone of the Mediterranean Sea near Banyuls sur Mer, France, in the whole depth range studied (0.5–25 m). The crabs had a long-lasting association with individual Anemonia sulcata, occasionally with Aiptasia mutabilis. Most crabs were found in association with the same anemone for several days, some crabs were found in association with the same anemone for longer than one month. In the areas studied, on average 65 Inachus phalangium were found on 100 anemones. Crabs released in the vicinity of anemones moved towards them and entered them. Inachus phalangium could walk between the tentacles of Anemonia sulcata and Aiptasia mutabilis without eliciting feeding reactions of the anemone. The crabs left the anemones for moulting. After moulting masking material was removed from the exuvia and used again. The animals returned into an anemone while still soft. Material used for masking, usually algae, could be picked off the body and eaten. Masking material may be a food reservoir in addition to providing camouflage. Anemones were left only during night-time. The crabs left their anemone to moult, to feed in the vicinity, fleeing from larger conspecifics, and to migrate to a different anemone. Outside the anemone's protection Inachus was eaten by several species of fish. Individuals appeared to avoid each other. 57% of all animals were found alone on an anemone. Large males and females were more frequently found alone than were small males and females. Fights were observed between members of the same and of the opposite sex. During fights, legs and claws could be torn off. Adult males migrated more often between anemones and moved over larger distances when migrating than did adult females. Adult males probably migrated in search of sexually mature females. Such a roving strategy is evolutionarily stable only when the higher costs (in terms of energy expenditure and mortality) are compensated for by a higher number of offspring than produced in the alternative, pair-bonding strategy.     

Antipredator defence of the hermit crab Pagurus filholi induced by predatory crabs

Hermit crabs have two antipredator tactics: taking refuge in its shell and fleeing. We examined the following two hypotheses using the hermit crab Pagurus filholi : (1) hermit crabs change their preference for shell types that they take refuge in and/or change the timing of fleeing (i.e. the duration of refuge in the shell) when they perceive a predator threat; (2) the type of shell that a hermit crab occupies affects the fleeing tactic of the individual. Under the stimulus of a crushed conspecific, hermit crabs changed neither their preference for shell species nor their refuge duration. On the other hand, under the stimulus of the predatory crab Gaetice depressus , hermit crabs increased their preference for Batillaria cumingi shells, which provide superior protection against predators, and shortened their refuge duration in the shells even when they occupied those effective against predation. Refuge duration was longer in B. cumingi shells than in the more vulnerable shells of Homalopoma sangarense . These results suggest that both antipredator defences (changing shell and timing of fleeing) are induced by the stimulus of a predator, and the timing of fleeing is affected by the shell type occupied.     

Chromatic Patterns of the Hermit Crab Calcinus tubularis Related to the Occupied Shell

Crustacea are known to develop different chromatic patterns due to many factors. Regarding decapods, chromatism was mainly studied in crabs, while very little is known about chromatic patterns in hermit crabs. Calcinus tubularis is a typical infralittoral rocky bottom hermit crab, studied for different aspects of its biology except chromatic variations. This paper aims at describing the different colour morphologies of C. tubularis, discussing hypothesis of why they develop, and testing if in nature the crab prefers a shell with a chromatic pattern similar to that of its body. One hundred and forty crabs were observed and filmed in the laboratory. They were subdivided into two groups, according to their chromatic pattern: 1) light and 2) dark crabs; the shells they occupied were also subdivided into the two groups of 1) light and 2) dark shells on the basis of the epibionts encrusting them. Observations of 129 crabs suggest that the colour depends neither on depth nor on size, intermoult period, diet, reproductive period but it might be connected to genetic factors and might help crab to camouflage. Camouflage is suggested by the fact that 79.3% of the total examined specimens occupy shells with a chromatic pattern resembling that of the crabs themselves. This phenomenon is significantly more recurrent in females than in males and could help the crabs to be cryptic, first with the occupied shell and secondly with the habitat (rocks encrusted by photophylous algae).     

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.