Predator Inspection Research Articles

Early differences in epithalamic left–right asymmetry influence lateralization and personality of adult zebrafish

The habenulae are part of an evolutionary conserved conduction system that connects the limbic forebrain areas with midbrain structures and is implicated in important functions such as feeding, mating, avoidance learning, and hormonal response to stress. Very early during zebrafish neurogenesis the parapineal organ migrates near to one habenula, commonly the left, inducing wide left–right habenular asymmetries in gene expression and connectivity. It was posited that this initial symmetry-breaking event determines the development of lateralized brain functions and early differences in epithalamic left–right asymmetry give rise to individual variation in coping styles and personality. We tested these two hypotheses by sorting zebrafish with left or right parapineal at birth using a foxD3:GFP marker and by measuring visual and motor laterality and three personality dimensions as they become adults. Significant differences between fish with opposite parapineal position were found in all laterality tests while the influence of asymmetry of the habenulae on personality was more complex. Fish with atypical right parapineal position, tended to be bolder when inspecting a predator, spent less time in the peripheral portion of an open field and covered a shorter distance when released in the dark. Activity in the open field was not associated to anatomical asymmetry but correlated with laterality of predator inspection that in turn was influenced by parapineal position. One personality dimension, sociality, appeared uncorrelated to both anatomical and functional asymmetries and was instead influenced by the sex of the fish, thus suggesting that other factors, i.e. hormonal, may be implicated in its development.

Behavioural trait assortment in a social network: patterns and implications

The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection.

INDIRECT GENETIC EFFECTS INFLUENCE ANTIPREDATOR BEHAVIOR IN GUPPIES: ESTIMATES OF THE COEFFICIENT OF INTERACTIONPSIAND THE INHERITANCE OF RECIPROCITY

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured psi, the coefficient of the interaction, which describes the degree to which an individual's phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.

Senses & Sensibility: Predator-Prey Experiments Reveal How Fish Perceive & Respond to Threats

The predator-prey relationship is one of the most recognizable and well-studied animal relationships. One of the more striking aspects of this relationship is the differential natural selection pressure (Table 1) placed on predators and their prey. This differential pressure results from differing costs of failure, the socalled life-dinner principle (Dawkins & Krebs, 1979). If a predator fails to catch a prey item, it simply goes hungry; if a prey item fails to escape a predator, its life is usually over. This strong selection pressure on prey has led to a diversity of defensive adaptations, such as camouflage, poison, and armoring. Here we describe a two-part laboratory experiment (developed as part of Vassar College's Neuroscience and Behavior program curriculum) designed to examine two putative defensive adaptations in an aquatic predator-prey system: multimodal predator detection systems and the fast-start escape response. Aquatic prey species have multiple senses available to them with which to detect the presence and activity of predators. One of these, the lateral line system, is mechanosensory and allows fish to detect objects moving near them in the water; this system, however, offers limited information about who or what is causing the water to move. Fish have a keen sense of vision that is used in a variety of contexts, including foraging, mating, and predator identification and avoidance; however, vision has limited utility at long distances underwater, due to water's physical properties. Fish also have acute chemosensory abilities. A fish's sense of smell is useful at longer distances than a fish's visual sense and in a wider array of situations, such as murky water or other low-light conditions. By documenting a prey individual's response to threatening stimuli under a variety of contexts, we can explore how fish respond to multiple sensory inputs and which senses take precedence in a given situation. Once a predator has been detected, prey species offer an array of behavior responses. One of the best-studied prey responses is predator inspection. In both wild and laboratory conditions, researchers have observed that, somewhat counter-intuitively, prey fish species tend to move towards predators. The presumption is that individuals are attempting to gain information about potential threats (Magurran & Seghers, 1990; Dugatkin & Godin, 1992). Inspection tendency varies by group size, predator identity, and on geographic location in the wild (e.g., high versus low-predation regions). Another prey response is the fast-start escape response, which is a rapid burst of movement away from a negative or threatening stimulus, such as an attacking predator. The fast start is displayed by an extraordinary diversity of fish species (Hale et al., 2002) and its kinematics, neurophysiology, and biomechanics have been well studied (e.g., Wakeling & Johnston, 1998; Domenici & Blake, 1997). As a consequence, this escape behavior presents an excellent platform for the simultaneous study of many aspects of animal biology. Here we describe a two-part experiment. The first part of the experiment examines three phenomena: * how prey detect the presence of a predator * how prey respond to the presence of a predator * whether prey response to predator presence is dependent on which sensory system the prey uses to detect the predator. The second part of this experiment examines, using highspeed videography: * the importance of the fast-start escape response in escaping threatening stimuli * whether the speed of the fast-start escape response differs with differing levels of threat. Study Organisms & Statistical Context The Trinidadian guppy (Poecilia reticulata) and the pike cichlid (Crenicichla alta) represent an ideal species dyad for classroom or laboratory studies of predator-prey interactions. First, the ecological and evolutionary interactions between the two species are well documented (Reznick & Endler, 1982; Magurran et al. …

Does defection during predator inspection affect social structure in wild shoals of guppies?

Reciprocal altruism has been proposed as a possible mechanism for the evolution of cooperative behaviour. However, very few investigations have tested predictions of reciprocity in wild animal populations. In the current investigation we simulated defection during predator inspection in a wild population of guppies, Poecilia reticulata . Two experiments were run: the first simulating defection during a single exposure to a predator and the second during multiple exposures to a predator. We then compared subsequent social and cooperative interactions with those observed prior to the treatments. From theory and previous experiments on cooperation and reciprocity, we predicted that defection would result in a reduction in social and cooperative interactions during subsequent predator inspections. However, our experiments did not find any effect of simulated defection(s) on the subsequent social structure, or on patterns of predator inspection behaviour. We discuss the potential reasons for the observed results and suggest future directions for research to address mechanisms underpinning the nature of cooperative interactions during predator inspection.

Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks

Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks. PHYSIOL BEHAV 00(0) 000-000, 2006. Here, we compare the behavioral, endocrine and neuroendocrine responses of individual sticklebacks exposed to either an unfamiliar conspecific or to a predator. We found that the two stressors elicited a similar hypothalamic–pituitary–interrenal response as assessed by whole-body concentrations of cortisol, but produced quite different patterns of change in brain monoamine and monoamine metabolite content as assessed by concentrations of serotonin (5-HT), dopamine (DA), norepinephrine (NE) and the monoamine metabolites 5-hydroxyindole acetic acid (5-HIAA), homovanillic acid (HVA) and 3-4-dihydroxyphenylacetic acid (DOPAC). For example, relative to baseline levels, NE levels were elevated in individuals exposed to a predator but were lower in individuals confronted by a challenging conspecific. Levels of monoamine neurotransmitters in specific regions of the brain showed extremely close links with behavioral characteristics. Frequency of attacking a conspecific and inspecting a predator were both positively correlated with concentrations of NE. However, whereas serotonin was negatively correlated with frequency of attacking a conspecific, it was positively associated with predator inspection. The data indicate that the qualitative and quantitative nature of the neuroendocrine stress response of sticklebacks varies according to the nature of the stressor, and that interindividual variation in behavioural responses to challenge are reflected by neuroendocrine differences.

The effects of different predator species on antipredator behavior in the Trinidadian guppy, Poecilia reticulata

Different types of predators often elicit different antipredator responses in a common type of prey. Alternatively, some prey species may adopt a general response, which provides limited protection from many different types of predator. The Trinidadian guppy, Poecilia reticulata, is faced with a wide range of different predators throughout its range and is known to display varying levels of antipredator behavior depending on the predator assemblage. Pike cichlids, Crenicichla frenata, are regarded as the primary aquatic guppy predator in streams in the northern mountain range in Trinidad. As such, they are seen to be responsible for many of the differences in morphology, life history traits, and behavior between guppy populations from areas with few predators and those from areas with many pike cichlids. In this study we investigated how guppies responded when faced with different predator species using three common aquatic predators. We exposed shoals of ten guppies to one out of four treatments: no predator (control), pike cichlid, acara cichlid (Aequidens pulcher), and wolf fish (Hoplias malabaricus); and we made behavioral observations on both focal individuals and the shoal as a whole. Guppies showed significantly greater levels of predator inspection and shoaling behavior, foraged less, spent more time in the surface water, and stayed in significantly larger shoals when faced with pike cichlids than in other treatments. We discuss these results in the context of multiple predator effects.

Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata)

In contrast to the substantial number of theoretical papers that have examined the mechanisms by which cooperation may evolve, very few studies have investigated patterns of co-operation in natural animal populations. In the current study, we use a novel approach, social network analysis, to investigate the structure of co-operative interactions in the context of predator inspection in a wild population of guppies (Poecilia reticulata). Female guppies showed social preferences for stable partners, fulfilling a key assumption made by models of reciprocity. In the laboratory, wild female guppies disproportionately engaged in predator inspection with others with whom they had strong social associations. Furthermore, pairs of fish that frequently engaged in predator inspection did so in a particularly co-operative way, potentially reducing costs associated with predator inspection. Taken together, these results provide evidence for assortative interactions forming the basis of co-operation during predator inspection in a natural fish population. The occurrence of highly interconnected social networks between stable partners suggests the existence of co-operation networks in free-ranging populations of the guppy.

Behavioral left-right asymmetry extends to arthropods

we present behavioral lateralizations of spiders and ants and their probable survival value. they clearly conform to the vertebrate lateralizations reviewed by vallortigara & rogers (v&r) and to earlier arthropod studies. we suggest two complementary reviews: (1) differences in lesion susceptibility and muscle strength between left and right body side, and (2) perceptual biases and predator inspection in invertebrates.

Sticklebacks benefit from closer predator inspection: an experimental test of risk assessment

Small fish often approach and “inspect” a detected predator from a short distance. This apparently paradoxical behaviour has been shown experimentally to incur a risk of death. To have a net benefit predator inspection behaviour must be advantageous. We tested experimentally whether a closer inspection distance per se provides inspecting three-spined sticklebacks (Gasterosteus aculeatus) with more information about a pike's (Esox lucius) hunger state. This prediction was confirmed: test fish that had been assigned to a close inspection distance started foraging earlier after they had inspected a satiated pike compared to those that had inspected a hungry pike. The fish could not assess the pike's hunger state as precisely from a far inspection distance. This was shown by a significant interaction between hunger state of the pike and inspection distance on the time to start foraging. The sticklebacks used the information gained from inspecting the predator because they attacked their own prey more frequently after they had inspected a satiated pike. This effect was most apparent when the fish attacked a high Daphnia density (which impairs vigilance) more frequently after they had seen a satiated pike from a close distance.

Zebrafish (Danio rerio) exhibit individual differences in risk-taking behavior during predator inspection

Risk-taking behavior associated with predator inspection has been described in a number of fish species. As a first step in parsing out the contribution of genes and environment to risk-taking behavior, the predator inspection behavior of zebrafish was examined. Predator inspection behavior of seventy males was measured once a day for five consecutive days and their mean daily inspection score — a measure of risk-taking tendencies — was recorded. Zebrafish did not habituate to the presence of a predator and significant individual differences in risk-taking behavior were uncovered.

Predator scent induces differing responses in two sympatric macropodids

When prey species encounter the scent of a predator they must make a decision on how to respond. This may be either to ignore, flee, hide or alarm call. While many species are able to derive detailed information from the chemical cues associated with predator scent, for some the decision to respond is often made without being able to identify the actual location and intentions of the predator. Depending on the sociality and ecology of the species, it may pay to flee or to engage in predator inspection where knowledge is impure. We tested for this in two sympatric marsupial macropodids, the parma wallaby (Macropus parma) and the red-necked pademelon (Thylogale thetis), as little is known of how these species detect and respond to olfactory cues of predation risk. We observed that, when presented with a synthetic predator scent mimicking dog urine, the social forager, T. thetis, tended to spend more time close to the predator odour, while the solitary forager, M. parma, exhibited an aversive response. The results suggest that social and ecological constraints on the sensory modalities used in predator detection may influence how macropodids respond to olfactory predator cues.

Differences in the pattern of antipredator behaviour between hatchery‐reared and wild European sea bass juveniles

Shoals of hatchery‐reared and wild sea bass juvenilesDicentrarchus labraxwere tested for differences in their antipredator responses towards a potential live predator, the eelAnguilla anguilla. Eight experimental shoals (i.e. replicates), each composed of 15 individuals from the same stock of juveniles (i.e. wild or hatchery), were video recorded for 5 min before and after predator exposure. A set of behavioural variables were measured during the pre‐stimulus and stimulus phases of each test and compared between the two groups of replicates. Results showed that in both hatchery‐reared and wild juveniles predator exposure elicited a significant increase in the mean level of shoal cohesiveness and mean shoal distance from the predator, and a significant decrease in the mean shoal distance from the bottom. Shoals of wild juveniles, however, aggregated more quickly and reached higher shoal cohesiveness within the first 20 s of the stimulus period than shoals of hatchery‐reared fish. During this period, the wild fish also reached the highest peak in shoal cohesiveness, which then decreased gradually towards the levels observed before predator exposure. Another component of the antipredator response, the predator inspection behaviour, was fully developed in both wild and hatchery fish. Wild fish, however, tended to inspect the predator at a closer distance than hatchery fish.

Behavioral responses to a novel predator and competitor of invasive mosquitofish and their non-invasive relatives (Gambusia sp.)

Attributes of the recipient community may affect the invasion success of arriving non-indigenous organisms. In particular, biotic interactions may enhance the resistance of communities to invasion. Invading organisms typically encounter a novel suite of competitors and predators, and thus their invasiveness may be affected by how they cope with these interactions. Behavioral plasticity may help invaders to respond appropriately to novelty. We examined the behavioral responses of highly invasive mosquitofish to representative novel competitors and predators they might encounter as they spread through North America. We compared the behavior of invasive Gambusia holbrooki and G. affinis to that of two close relatives of lower invasive potential (G. geiseri and G. hispaniolae) in order to elucidate whether responses to novelty related to invasiveness. In short-term assays, female Gambusia were paired with a novel competitor, Pimephales promelas, and a novel predator, Micropterus dolomieu. Behavioral responses were measured in terms of foraging success and efficiency, activity, refuge use, predator inspections, and interspecific aggression. Contrary to a priori predictions, invasive and non-invasive responses to novel interactions did not differ consistently. In response to novel competition, both invasive species increased foraging efficiency, but so did G. geiseri. In response to novel predation, only G. holbrooki decreased consumption and activity and increased refuge use. No antipredator response was observed in G. affinis. We found consistent differences, however, between invasives and non-invasives in foraging behavior. Both in the presence and absence of the competitor and the predator, invasives foraged more efficiently and consumed more prey than non-invasives.

Predator inspection behaviour in three-spined sticklebacks ( Gasterosteus aculeatus ): body size, local predation pressure and cooperation

The apparently maladaptive tendency of fish to approach and inspect potential predators has been explained in terms of useful information gathering or as a signal to the predator that it has been seen. We examined this behaviour in 16 populations of wild-caught stickleback (Gasterosteus aculeatus) from ponds with and without predatory perch (Perca fluviatilis). Three large and three small individuals per population were each exposed to three model predators differing in realism. A final cooperative treatment entailed pairing subjects with a second individual from the same population, but of the alternative size class, during predator presentation. As might be expected, predator inspection behaviour was much greater in the predator-sympatric populations, and only these fish increased their level of inspection as the models became incrementally more realistic. This suggests that reductions occur in the level of costly inspection behaviour in populations without predators. Subject body size had no effect on inspection effort, which suggests a limited role for experience (we assumed larger fish to be older than smaller fish), at least over the relative age differences utilized. However, small predator-sympatric fish were the only subjects to increase inspection significantly when in a cooperative context, perhaps reflecting the inherent value of a relatively larger partner in this context. These results confirm that levels of predator inspection are both population- and situation-dependent, suggesting a trade-off in the potential costs and benefits of this behaviour.

Do competing males cooperate? Familiarity and its effect on cooperation during predator inspection in male three‐spined sticklebacks (Gasterosteus aculeatus)

We investigated the trade‐off between conflict and cooperation, using predator inspection behaviour in sticklebacks as a model system. Male three‐spined sticklebacks (Gasterosteus aculeatus) compete for territories during the breeding season and it has been demonstrated that the level of aggression between territorial neighbours declines with time, a phenomenon known as the dear enemy effect. In this experiment we examine whether this increase in familiarity between territorial neighbours can facilitate an increase in cooperation during predator inspection events. This was analyzed using male sticklebacks from four pond populations, two with and two without predatory rainbow trout (Oncorhyncus mykiss). Males were each exposed to five different treatments: (1) the presentation of a live rainbow trout when alone; (2) with a newly revealed territorial neighbour; (3) with this neighbour after two days of familiarization; (4) with another unfamiliar neighbour (termed a ‘floater’); and (5) a second solitary trial (to provide controls at the start and end of the experiment). As predicted, fish from predator‐sympatric populations showed higher levels of predator inspection and lower rates of misdirected territorial aggression towards the predator throughout. However, familiarity between neighbouring males did not facilitate an increase in predator inspection behaviour. Instead, predator inspection behaviour decreased throughout treatments involving the presence of any sort of neighbouring male. Familiarity between neighbours did not influence their ability to cooperatively inspect, but only the nature of any aggressive territorial behaviours, all of which detracted equally from individual inspection effort.

Observational Learning and Predator Inspection in Guppies (Poecilia reticulata)

AbstractPrior work has demonstrated that, following a predator inspection visit of their own, guppies prefer to associate with individuals who inspected a predator most closely. Based on this work, as well as studies of social learning in the context of mate choice, we predicted that male guppies that observed but did not participate in an inspection trial would subsequently choose to associate with the closer of two inspectors. Our experimental protocol consisted of three treatments: a control test in which an observer watched two fish consecutively, only one of which was exposed to a predator, a sequential test in which an observer watched two fish consecutively, both of which were exposed to the predator, and a social test in which an observer watched two fish inspect simultaneously. We found no preferences by the observer for either of the fish in any of the trials. Our results suggest that direct interaction is a critical component to the development of preferences in male guppies. We discuss our findings in light of game theoretical treatments of cooperation.

Predator Inspection Behaviour in a Characin Fish: an Interaction between Chemical and Visual Information?

AbstractRecent evidence suggests that predator inspection behaviour by Ostariophysan prey fishes is regulated by both the chemical and visual cues of potential predators. In laboratory trials, we assessed the relative importance of chemical and visual information during inspection visits by varying both ambient light (visual cues) and predator odour (chemical cues) in a 2 × 2 experimental design. Shoals of glowlight tetras (Hemigrammus erythrozonus) were exposed to a live convict cichlid (Archocentrus nigrofasciatus) predator under low (3 lux) or high (50 lux) light levels and in the presence of the odour of a cichild fed tetras (with an alarm cue) or swordtails (Xiphophorus helleri, with an alarm cue not recognized by tetras). Tetras exhibited threat‐sensitive inspection behaviour (increased latency to inspect, reduced frequency of inspection, smaller inspecting group sizes and increased minimum approach distance) towards a predator paired with a tetra‐fed diet cue, regardless of light levels. Similar threat‐sensitive inspection patterns were observed towards cichlids paired with a swordtail‐fed diet cue only under high light conditions. Our data suggest that chemical cues in the form of prey alarm cues in the diet of the predator, are the primary source of information regarding local predation risk during inspection behaviour, and that visual cues are used when chemical information is unavailable or ambiguous.

Learning about danger: chemical alarm cues and local risk assessment in prey fishes

AbstractAn individual's behaviour patterns can be conceptualized as a series of threat‐sensitive trade‐offs between ambient predation pressure and a suite of fitness‐related activities, such as resource defence, foraging and mating. Individuals that can reliably assess local predation risk could increase their fitness potential by exhibiting predator avoidance behaviours only at appropriate times. However, such learned risk assessment requires reliable information regarding current predation risks.A diverse range of prey fishes are known to possess chemical alarm cues, which when detected by conspecifics and some heterospecifics, elicit a variety of overt and covert responses. These chemical cues, either alone or as a part of a predator's dietary odour, provide reliable information regarding local predation risk. In this review, I describe recent works examining the role of chemosensory information in: (i) acquired predator recognition, (ii) predator inspection behaviour and (iii) the use of conspecific and heterospecific cues as social information sources.

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy (Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.