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.     

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.     

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.     

The detachment of the commensal sea anemones,Calliactis polypus and C. tricolor by mechanical and electrical stimulation

Summary 1.Calliactis polypus in Hawaii and C. tricolor in Puerto Rico both respond to mechanical stimuli that resemble the activities of their commensal pagurids, e.g., stroking, tapping, scratching and squeezing of the column, by opening up, relaxing and loosening their pedal discs (Figs. 3–6).2.C. polypus, which does not transfer to crabs unaided, could only be detached by lifting the pedal disc after the anemone had been subjected for some time to tactile stimuli very similar to those applied by Dardanus gemmatus (Figs. 1 and 2). C. tricolor, which can transfer to shells unaided by crabs and which lives on several hosts, can be relaxed and detached quickly by various substitutes, the most effective being gentle brushing around the base (Figs. 7–10).3.Both species of Calliactis, when detached by such substitutes, were expanded and relaxed and retraction responses were inhibited. In this state tentacles and pedal discs adhered strongly to any solid surface and the anemones settled on these quickly (Figs. 11–14).4.Electrical stimuli at low frequencies (maximum 1 pulse per sec at 27–29° C) cause extension and relaxation of the column. Usually after 40–50 stimuli release of the pedal disc occurs. The effective pulse frequencies are close to the frequency of the tactile contacts of crabs or substitutes which evoke the relaxation and release of C. polypus and C. tricolor (Figs. 15–18).5.It is suggested that species with less restricted host relationships, in this case C. tricolor, are less restricted also in the kinds of stimuli that cause detachment. The role of sensory adaptation and the requirements of the neural organization controlling these activities are discussed. The excitation process is frequency-dependent and the response pattern is triggered at an appropriate level by summation. the detachment of C. polypus and C. tricolor is compared with the very slow detachment of C. parasitica in response to shells, and with the very rapid detachment of the swimming sea anemones, Stomphia and Actinostola. All of these anemones use different mechanisms to achieve the same end.We acknowledge the help we received from the following: the Director of the Oceanic Institute, Waimanalo, Hawaii (Dr. John Hendrickson) and the Director of the La Parguera Laboratory of the University of Puerto Rico at Mayagüez (Dr. Maxime Ceramé-Vivas); Dr. Ernst Reese and Mr. John Talis in Hawaii and Dr. Charles Cutress and Dr. Luis Almodovar in Puerto Rico, who arranged for the collection of animals and who assisted us in many other ways; the National Research Council of Canada through Operating Grant A-1445.     

The sea anemone Calliactis tricolor and its association with the Hermit crab Dardanus venosus

The association of certain sea anemones and hermit crabs is established in different ways according to the species involved. The present study shows that the behaviour patterns of the two partners in associations between Calliactis tricolor (Lesueur) and Dardanus venosus (H. M. Edwards) in the Caribbean are similar to those seen in the Mediterranean C. parasitica and D. arrosor .
Although about half the crabs display an active behaviour pattern in laboratory trials, the anemone frequently settles on shells unaided and most C. tricolor respond to molluscan shells by clinging with their tentacles until the pedal disc can be attached. As a rule it is necessary for the anemone to relax and to cling to the shell if the crab is to be successful in transferring the anemone to its shell.
The behaviour patterns of D. venosus include a distinctive tapping of the edge of the base of C. tricolor after which the anemone is pulled or lifted off and transferred to the shell. An experimenter can also cause the anemone to relax and to detach itself by tapping the edge of the base with plastic rods after the manner of the crab.
The mechanisms by which the tentacles of Calliactis cling to, and by which the base settles upon, shells still remain to be elucidated. The participation of nematocysts in these processes could not be demonstrated in this study.
C. tricolor is found on some other pagurid and non-pagurid crabs in various localities. These associations need to be investigated fully in order that the behaviour patterns of C. tricolor may be correctly interpreted and compared with those of other species of Calliactis .     

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.     

The oxygen consumption of Pennatula rubra ellis and some other anthozoans

Summary The oxygen consumption of Pennatula rubra and some other pennatulids, and also of the anemone Calliactis parasitica, has been measured by a reliable method. In general, the oxygen consumption of these coelenterates is proportional to the external oxygen concentration, suggesting that the consumption mechanism relies on simple diffusion of oxygen into the cells.The oxygen consumptions per unit organic dry weight of these species are comparable with typical values for other marine invertebrates, implying that the use of wet weight as a criterion may be misleading and should be discontinued, and that pennatulids respire actively considering the small amount of organic material they contain.It is suggested that the endoderm is the major site of oxygen consumption in these animals. Calliactis parasitica, when under anaerobic conditions, incurs only a partial oxygen debt, as post-anaerobic oxygen consumption is only slightly higher than the normal rate.

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Zusammenfassung Der Sauerstoff-Verbrauch von Pennatula rubra und anderen Pennatuliden und der See-Anemone Calliactis parasitica ist unter Anwendung der Winkler-Methode gemessen worden. Im allgemeinen hängt der Sauerstoffverbrauch dieser Coelenteraten von der O₂-Konzentration im umgebenden Medium ab. Das deutet darauf hin, daß der Mechanismus der O₂-Aufnahme in einer einfachen Diffusion des Sauerstoffes in die Gewebe besteht.Der O₂-Verbrauch, bezogen auf das organische Trockengewicht, ist mit dem anderer wirbelloser Seetiere vergleichbar. Die Verwendung des Frischgewichtes als Bezugsgröße kann demnach irreführend sein; Pennatuliden atmen — in Anbetracht der geringen Menge organischen Materials, die sie enthalten — aktiv.Das Entoderm ist die Gewebeschicht mit dem größten Sauerstoffverbrauch.Unter Bedingungen des Sauerstoffmangels tritt bei Calliactis parasitica nur ein teilweiser Sauerstoffmangel ein, da der anschließende Sauerstoffverbrauch (unter normalen Bedingungen) nur wenig höher ist als der normale.

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We are indebted to the University of London for a grant from the Central Research Fund which made this work possible. We also wish to thank Prof. G. PETIT, Director of the Laboratoire Ar'ago, Banyuls-sur-Mer, for providing facilities and for the interest he showed in the work.     

Predator size interacts with habitat structure to determine the allometric scaling of the functional response

While both predator body size and prey refuge provided by habitat structure have been established as major factors influencing the functional response (per capita consumption rate as a function of prey density), potential interactions between these factors have rarely been explored. Using a crab predator (Panopeus herbstii) – mussel prey (Brachidontes exustus) system, we examined the allometric scaling of the functional response in oyster (Crassostrea virginica) reef habitat, where crevices within oyster clusters provide mussels refuge from predation. A field survey of mussel distribution showed that mussels attach closer to the cluster periphery at high mussel density, indicating the potential for saturation of the refuge. In functional response experiments, the consumption rate of large crabs was depressed at low prey density relative to small crabs, while at high prey density the reverse was true. Specifically, the attack rate coefficient and handling time both decreased non‐linearly with crab size. An additional manipulation revealed that at low prey densities, the ability of large crabs to maneuver their claws and bodies to extract mussels from crevices was inhibited relative to small crabs by the structured habitat, reducing their attack rate. At high prey densities, crevices were saturated, forcing mussels to the edge of clusters where crabs were only limited by handling time. Our study illuminates a potentially general mechanism where the quality of the prey refuge provided by habitat structure is dependent on the relative size of the predator. Thus anthropogenic influences that alter the natural crab size distribution or degrade reef habitat structure could threaten the long‐term stability of the crab –mussel interaction in reefs.     

Ultrastructure of neurons and synapses in the tentacle gastrodermis of the sea anemone Calliactis parasitica

Little is known about gastrodermal neurons and synapses in the tentacles of sea anemones. Using transmission electron microscopy of serial thin sections of Calliactis parasitica, we have identified both a sensory cell and a ganglion cell with granular vesicles originating from the Golgi complex and have identified four types of synapses in the tentacular gastrodermal nerve plexus. The sensory cell has a recessed apical cilium with a basal body and a perpendicularly oriented centriole, below which are several strands of striated rootlets surrounded by mitochondria. The ganglion cell lacks a cilium and resembles a bipolar neuron, with oppositely directed processes lying parallel to the basally located circular smooth muscle. Both one-way and two-way interneuronal synapses are present with 60- to 90-nm granular vesicles of various densities aligned at the paired electron-dense membranes and fine cross filaments in the intervening 13-nm cleft. Two types of neuroeffector synapses have been located. Dense granular vesicles are present at neuromuscular synapses, whereas less dense vesicles are present at neuroglandular synapses. Most of the synaptic vesicles range from 60 to 120 nm in diameter. Two types of nerve cells and a variety of synaptic loci provide morphological substrates for the spontaneous SS2 conduction pulses in the tentacular gastrodermis of C. parasitica. J Morphol 231:217–223, 1997. © 1997 Wiley-Liss, Inc.     

Male reproductive system of the red brocade hermit crab Dardanus insignis (Diogenidae) and its relationship to other family members

The reproductive system of hermit crabs shows species-specific morphology, which can be used in phylogenetic analysis. Here, we describe the male reproductive system of the hermit crab Dardanus insignis, including morphological and biometric analyses of the spermatophore, the gonopore, and sperm ultrastructure. The morphological analyses were based on 15 selected specimens and carried out by means of light and electron microscopy. Our results indicate a reproductive system composed of lobular testes attached to a simple straight vas deferens connected to the exterior via ventral gonopores. The gonopores are ovoid, surrounded by dense serrulate setae, and covered by a membranous operculum. The spermatophores exhibit a tripartite structure, with an elongate ovoid ampulla, a long narrow stalk, and a proximal foot. The spermatozoal ultrastructure shows three main regions: an ovoid-oblong acrosomal vesicle, a nucleus, and cytoplasm with three armlike extensions. Some of these characteristics can also be found in other species of Diogenidae within the genus Dardanus and in members of Coenobitidae, a closely related family. The available information on spermatophore and spermatozoal structure may indicate a closer similarity between the genus Dardanus and the Coenobitidae, compared with other members of Diogenidae.     

Predation risk and competition affect habitat use of adult perch,Perca fluviatilis

The aim of this study was to examine how the presence of a predator and an interspecific competitor influence the habitat use of adult perch (Perca fluviatilis; size: 15.1 ± 0.5 cm) when given the choice between two adjacent habitats. By conducting aquarium experiments, the habitat occupancy of P. fluviatilis was documented in the presence and absence of a predator (pike Esox lucius; size: 25.4 ± 2.1 cm) and a potential competitor (ruffe Gymnocephalus cernuus; size: 14.1 ± 0.3 cm) fish species. Two P. fluviatilis individuals generally shared the same habitat. In the presence of a conspecific, P. fluviatilis favoured the structurally more-complex, artificial macrophyte habitat over the less-structured rock and sand habitat, which in turn were used equally. In the predator- and competitor treatments, P. fluviatilis seemed to adapt their habitat use to the habitat occupancy of E. lucius and G. cernuus in the Macrophyte vs. Rock and, in the predator treatment, also in the Macrophyte vs. Sand habitat combination, by increasingly occupying a habitat that was used less by the predator or competitor species, respectively. This behaviour suggests that P. fluviatilis tried to avoid the other fish species by choosing a, in some cases less preferred, predator- or competitor-free habitat. This study emphasizes the importance of biological interactions illustrated by the potential of predation risk and competition to structure fish communities by influencing habitat use at small spatial scales.     

The presence of α-doradexanthin in crustacea and its possible metabolic fate

α-Doradexanthin has been isolated from the brachyurans Pachygrapsus marmoratus, Eriphia spinifrons and the anomouran Clibanarius erythropus. Small traces of this carotenoid have been also reported in the brachyuran species Potamon edulis and Eriocheir sinensis, but was absent from the anomouran species Dardanus arrosor and Pagurus prideauxi. A transformation pathway of lutein into astaxanthin via α-doradexanthin is suggested.     

Nature and role of newly described symbiotic associations between a sea anemone and gastropods at bathyal depths in the NW Atlantic

The hormathiid sea anemone Allantactis parasitica was found living as an epibiont on numerous species of gastropods at depths of 725-1100 m along the continental slope of eastern Canada. The proportion of bathyal gastropods hosting 1-6 sea anemones reached 72.5% in a single trawl. Although A. parasitica was occasionally found on other substrata (i.e. empty shells, pebbles), laboratory trials confirmed that they preferably associate with living gastropods. Settlement of planula larvae occurred significantly more often on the shells of live bathyal gastropods than on all other substrata present in the tanks. Juvenile sea anemones (∼ 1 mm diameter) readily moved from the mud or other inert substrata onto shells of burrowed bathyal gastropods. Conversely, larvae, juveniles and adults of A. parasitica never associated with any shallow-water gastropods when given the opportunity. Trials exposing predatory sea stars (Leptasterias polaris) from shallow and bathyal depths to bathyal gastropods (Buccinum undatum) with epibiotic A. parasitica, and to asymbiotic bathyal and shallow-water B. undatum, revealed adaptive behaviours in both prey and predator. Shallow-water gastropods (devoid of epibionts) reacted defensively to L. polaris, whereas bathyal gastropods relied mostly on their epibionts to protect them, thus falling prey to L. polaris when the epibionts were removed. L. polaris from bathyal depths typically ignored symbiotic gastropods, but they consistently preyed on asymbiotic ones, while L. polaris from shallow areas initially attempted to prey on all gastropods, but learned to avoid those harbouring sea anemones. Furthermore, living as epibionts afforded sea anemones a means to escape one of their own predators, the sea star Crossaster papposus. The mutualistic relationship between hormathiid sea anemones and bathyal gastropods from the NW Atlantic may have evolved in response to predation pressure.     

Habitat context influences predator interference interactions and the strength of resource partitioning

Despite increasing evidence that habitat structure can shape predator–prey interactions, few studies have examined the impact of habitat context on interactions among multiple predators and the consequences for combined foraging rates. We investigated the individual and combined effects of stone crabs (Menippe mercenaria) and knobbed whelks (Busycon carica) when foraging on two common bivalves, the hard clam (Mercenaria mercenaria) and the ribbed mussel (Geukensia demissa) in oyster reef and sand flat habitats. Because these species co-occur across these and other estuarine habitats of varying physical complexity, this system is ideal for examining how habitat context influences foraging rates and the generality of predator interactions. Consistent with results from previous studies, consumption rates of each predator in isolation from the other were higher in the sand flat than in the more structurally complex oyster reef habitat. However, consumption by the two predators when combined surprisingly did not differ between the two habitats. This counterintuitive result probably stems from the influence of habitat structure on predator–predator interactions. In the sand-flat habitat, whelks significantly reduced their consumption of their less preferred prey when crabs were present. However, the structurally more complex oyster reef habitat appeared to reduce interference interactions among predators, such that consumption rates when the predators co-occurred did not differ from predation rates when alone. In addition, both habitat context and predator–predator interactions increased resource partitioning by strengthening predator dietary selectivity. Thus, an understanding of how habitat characteristics such as physical complexity influence interactions among predators may be critical to predicting the effects of modifying predator populations on their shared prey.     

Individual distance in crustacea: IV. Distance and dominance hierarchies in Pagurus pollicaris

The agonistic acts and distances separating interacting individuals when acts occurred were recorded for specimens of the hermit crab Pagurus pollicaris. Individuals were observed in groups of six under several conditions (during a snail predation, with food in the aquarium, and nothing in the aquarium except the crabs before and after the crabs had access to empty gastropod shells).

The pattern of agonistic interactions within the groups showed a high degree of order, but the lack of changes in behavior over time indicated these crabs have an aggressive order rather than a dominance hierarchy.

The distances separating crabs when acts were executed were significantly affected by (1) the act being executed, (2) the act executed previously by the other crab, (3) the size of the acting crab, (4) the relative size difference of the two interactants, (5) the individual crabs’ identities, and (6) the condition of observation. The individual crab effects on distance were present when crab size was controlled and crabs that reacted at smaller distances tended significantly to elicit reactions at greater distances.     

Habitat partitioning between prey soldier crab Mictyris brevidactylus and predator fiddler crab Uca perplexa

Interaction and habitat partition between the soldier crab Mictyris brevidactylus (prey) and the fiddler crab Uca perplexa (predator) were examined at a sandy tidal flat on Okinawa Island, Japan, where they co-occur. Both live in dense colonies. When the soldier crabs were released in the densely populated habitat of the fiddler crab, male fiddler crabs, which maintain permanent burrows in hard sediment, preyed on small soldier crabs and repelled large ones. Thus, the fiddler crabs prevented the soldier crabs from trespassing. It was also observed whether soldier crabs burrowed successfully when they were released 1) where soldier crab burrows just under the sand were abundant, 2) in a transition area between the two species, 3) an area without either species, and 4) where artificial tunnels simulated soldier crabs' feeding tunnels were made by piling up sand in the area lacking either species. In contrast to the non-habitat area, many soldier crabs burrowed in the sediment near the release point in the tunnel, transition and artificial tunnel areas. This indicates that the feeding tunnels on the surface attracted other crabs after emergence. When the large male fiddler crabs were transplanted into the artificial burrows made in soft sediment of the soldier crab habitat, all left their artificial burrows by 2 days. In the fiddler crab habitat, however, about one-third of the transplanted male fiddler crabs remained in the artificial burrows after 3 days. The soldier crabs regularly disturb the sediment by the up and down movement of their burrow (small air chamber) between tides. This disturbance probably prevents the fiddler crab from making and occupying permanent burrows. Thus, it appears that these crabs divide the sandy intertidal zone by sediment hardness and exclude each other by different means.     

Coelenterate Neuropeptides: Structure, Action and Biosynthesis

Evolutionary "old" nervous systems such as those of coelenteratesare peptidergic: Using various radioimmunoassays we have nowisolated 13 novel neuropeptides from sea anemones and severalothers from hydrozoan polyps and medusae. These peptides areall structurally related and contain the C-terminal sequenceArg-X-NH₂ or Lys-X-NH₂, where X is Ala, Asn, Ile, Phe, Pro orTrp. Three neuropeptides have a novel N-terminal L-3-phenyllactylresidue, which protects against degradation by nonspecific aminopeptidases.The neuropeptides from sea anemones are produced by differentsets of neurones and have excitatory or inhibitory actions onisolated muscle preparations, suggesting that they are neurotransmittersor neuromodulators. We have also cloned the precursor proteinfor the sea-anemone neuropeptide Antho-RFamide (<Glu-Gly-Arg-Phe-NH₂).In Calliactis parasitica this precursor harbours 19 copies ofimmature Antho-RFamide (Gln-Gly-Arg-Phe-Gly) together with 7other, putative neuropeptide sequences. The precursor of Anthopleuraelegantissima contains 14 copies of Antho-RFamide and 19 other,putative neuropeptides. This shows that the biosynthetic machineryfor neuropeptides in coelenterates, the lowest animal grouphaving a nervous system, is already very efficient and similarto that of higher invertebrates, such as molluscs and insects,and vertebrates.     

The effect of raising conditions on behavior of juvenile roach <Emphasis Type="Italic">Rutilus rutilus</Emphasis> (L.) (Cyprinidae)

The behavior of juvenile 4.5-month-old roach Rutilus rutilus (L.) raised (starting on the 12th day after hatching) at different levels of habitat informational diversity (feeding with live and immobilized zooplankton and benthos, the presence of a predator, and a constant water flow in the nursery aquarium) was studied. The fish’s exploratory behavior and locomotor activity were tested in a circular chamber; swimming activity was tested in a hydrodynamic conduit. It was experimentally shown that juvenile roach raised in the presence of a predator differed significantly (p < 0.05) in regards to behavioral characteristics from the fries raised in a water current and in conditions of a high level of environmental deprivation.     

Spontaneous contractions and nerve net activity in the sea anemone calliactis parasitica

Suction electrodes attached to tentacles of the sea anemone Calliactis parasitica record regular bursts of activity associated with the through‐conducting nerve net. Most bursts consist of 10–15 pulses at a frequency of 1 every 4 sec to 1 every 10 sec. The interval between bursts is usually 10–20 min. Regularity in pulse number and frequency in successive bursts suggests that the activity originates from a pacemaker. Bursts are always followed by slow contraction of endodermal longitudinal (parietal) muscles after a short delay, and endo‐dermal circular muscles after a long delay. A simple model for nervous pacemaker control of rhythmic contractions cannot be proposed as slow contractions can also occur in the absence of recorded nerve net activity.     

Habitat quality mediates personality through differences in social context

Assessing the stability of animal personalities has become a major goal of behavioral ecologists. Most personality studies have utilized solitary individuals, but little is known on the extent that individuals retain their personality across ecologically relevant group settings. We conducted a field survey which determined that mud crabs, Panopeus herbstii, remain scattered as isolated individuals on degraded oyster reefs while high quality reefs can sustain high crab densities (>10 m^?2). We examined the impact of these differences in social context on personality by quantifying the boldness of the same individual crabs when in isolation and in natural cohorts. Crabs were also exposed to either a treatment of predator cues or a control of no cue throughout the experiment to assess the strength of this behavioral reaction norm. Crabs were significantly bolder when in groups than as solitary individuals with predator cue treatments exhibiting severally reduced crab activity levels in comparison to corresponding treatments with no predator cues. Behavioral plasticity depended on the individual and was strongest in the presence of predator cues. While bold crabs largely maintained their personality in isolation and group settings, shy crabs would become substantially bolder when among conspecifics. These results imply that the shifts in crab boldness were a response to changes in perceived predation risk, and provide a mechanism for explaining variation in behavioral plasticity. Such findings suggest that habitat degradation may produce subpopulations with different behavioral patterns because of differing social interactions between individual animals.