Predator Inspection Behaviour Research Articles

Evolution of schooling drives changes in neuroanatomy and motion characteristics across predation contexts in guppies

One of the most spectacular displays of social behavior is the synchronized movements that many animal groups perform to travel, forage and escape from predators. However, elucidating the neural mechanisms underlying the evolution of collective behaviors, as well as their fitness effects, remains challenging. Here, we study collective motion patterns with and without predation threat and predator inspection behavior in guppies experimentally selected for divergence in polarization, an important ecological driver of coordinated movement in fish. We find that groups from artificially selected lines remain more polarized than control groups in the presence of a threat. Neuroanatomical measurements of polarization-selected individuals indicate changes in brain regions previously suggested to be important regulators of perception, fear and attention, and motor response. Additional visual acuity and temporal resolution tests performed in polarization-selected and control individuals indicate that observed differences in predator inspection and schooling behavior should not be attributable to changes in visual perception, but rather are more likely the result of the more efficient relay of sensory input in the brain of polarization-selected fish. Our findings highlight that brain morphology may play a fundamental role in the evolution of coordinated movement and anti-predator behavior.

Long-Tailed Pygmy Rice Rats Modify Their Behavioural Response and Faecal Corticosterone Metabolites in Response to Culpeo Fox but Not to Lesser Grison.

Simple SummaryPrey species must fine-tune their antipredator responses to survive, but also to achieve a positive net energy balance which will enhance biological fitness. Given this, we investigated if Oligoryzomys longicaudatus would adapt their behavioural and physiological antipredator responses depending on their relative presence in the predator’s diet. By exposing this rodent species to culpeo fox and lesser grison faeces, we found that O. longicaudatus behavioural and physiological strategies were modulated depending on the predator’s diet. Specifically, rodents would trigger their antipredator responses in the presence of the most dangerous predator, the culpeo, which consumes a higher proportion of O. longicaudatus compared to the lesser grison. Our findings could be of importance for the development of more humane and efficient strategies to control rodent populations.Even though behavioural and physiological reactions to predation risk exhibited by prey species have received considerable attention in scientific journals, there are still many questions still unsolved. Our aim was to broaden the knowledge on one specific question: do long-tailed pygmy rice rats adapt their behavioural and physiological antipredator strategies depending on the predator species? For this question, we live-trapped in a temperate forest in Southern Chile long-tailed pygmy rice rats (Oligoryzomys longicaudatus), which were exposed to three predator odour phases (Phase 0: preliminary, no predator cues; Phase 1: one plot with culpeo fox faeces (Lycalopex culpaeus), one plot with lesser grison (Galictis cuja) faeces and one plot acting as a control with no odour; Phase 2: post treatment, no predator cues). We measured the behavioural response by the capture ratio. To assess the physiological stress response, we collected fresh faecal samples to quantify faecal corticosterone metabolites (FCM). Our results showed that O. longicaudatus increased both the capture ratio and FCM levels in the presence of culpeo cues. Culpeo foxes have higher densities in the study area than G. cuja and exhibit a higher activity pattern overlap with O. longicaudatus. Moreover, it has been also been reported in other regions that L. culpaeus consumption of O. longicaudatus is more frequent compared to G. cuja diet. The increase in capturability could be because traps can be regarded as a shelter in high-risk settings, but it can also be explained by the predator inspection behaviour. The increase in FCM concentrations during culpeo treatment can be linked to the adaptive mobilisation of energy to execute antipredator responses to increase survival chances.

Mate-searching context of prey influences the predator-prey space race.

Predation risk is a strong driver of prey distribution and movement. However, fitness-influencing behaviours, such as mating, can alter risk and influence predator-prey space-use dynamics. In tree crickets, Oecanthus henryi, mate searching involves acoustic signalling by immobile males and phonotactic movement by females. Space-use patterns in tree crickets relative to their primary predators, green lynx spiders (Peucetia viridans), should therefore depend on their current mate-searching state; whether males are calling or non-calling and whether females are phonotactic or non-phonotactic. We first measured the degree of spatial anchoring of crickets to specific bushes in the field and determined whether that influenced the probability of broad-scale spatial overlap with spiders. In the absence of spiders, all crickets, independent of sex or male calling status, were found to be spatially anchored to specific types of bushes and not uniformly distributed on the landscape. At the broad spatial scale, spiders were more likely to be found on bushes with female crickets and, to a lesser degree, calling male crickets. At a finer spatial scale within a bush, movement strategies of crickets not only varied depending on the presence or absence of a spider, but also on their current mate-searching state. Phonotactic females showed clear predator avoidance, whereas calling and non-calling males moved towards the spider instead of away, similar to predator inspection behaviour seen in many taxa. As the strongly selected sex, males are more likely to undertake risky mate-searching activities, which includes inspection of predator positions. Overall, we found that all crickets were predictably anchored at the landscape scale, but their sex and mate-seeking behaviour influenced the degree of overlap with predators and their antipredator movement strategies. Reproductive strategies within a prey species, therefore, can alter predator-prey space race at multiple spatial scales.

Can fiddler crabs detect underwater predators? A laboratory test with Leptuca thayeri

Fiddler crabs are intertidal organisms well known to be highly adapted to low tide activity, thus a number of researches have studied their physiological, behavioral and sensory adaptations to such a tidal phase. However, recent evidences showed that some fiddler crabs are the main food item of fish, suggesting that they could also be active underwater. Based on these preliminary observations, we designed laboratory trials aimed to investigate the ability to detect underwater predators in Leptuca thayeri, across sexes and life stages. We tested a combination of chemical and visual cues, using the predator fish Sphoeroides greeleyi, and, as a control, the non-predator fish Mugil curema. Leptuca thayeri detected the presence of chemical cues coming from the predator fish, although significant differences between adults and juveniles were observed. Adults of L. thayeri remained within their burrows and avoided predator exposition, while juveniles were bold and even increased their activity on the sediment surface. We suggest that juvenile crabs’ boldness could be explained by a predator inspection behavior, which allows them to gather information about the possible risk of different predatory species, while experienced adults reduce predation risk recognizing the predator itself.

Anthropogenic noise compromises the anti-predator behaviour of the European seabass, Dicentrarchus labrax (L.)

Anthropogenic noise is a significant pollutant of the world's oceans, affecting behavioural and physiological traits in a range of species, including anti-predator behaviours. Using the open field test, we investigated the effects of recordings of piling and drilling noise on the anti-predator behaviour of captive juvenile European seabass in response to a visual stimulus (a predatory mimic). The impulsive nature of piling noise triggered a reflexive startle response, which contrasted the behaviour elicited by the continuous drilling noise. When presented with the predatory mimic, fish exposed to both piling and drilling noise explored the experimental arena more extensively than control fish exposed to ambient noise. Fish under drilling and piling conditions also exhibited reduced predator inspection behaviour. Piling and drilling noise induced stress as measured by ventilation rate. This study provides further evidence that the behaviour and physiology of European seabass is significantly affected by exposure to elevated noise levels.

Kinship reinforces cooperative predator inspection in a cichlid fish.

Kin selection theory predicts that cooperation is facilitated between genetic relatives, as by cooperating with kin an individual might increase its inclusive fitness. Although numerous theoretical papers support Hamilton's inclusive fitness theory, experimental evidence is still underrepresented, in particular in noncooperative breeders. Cooperative predator inspection is one of the most intriguing antipredator strategies, as it implies high costs on inspectors. During an inspection event, one or more individuals leave the safety of a group and approach a potential predator to gather information about the current predation risk. We investigated the effect of genetic relatedness on cooperative predator inspection in juveniles of the cichlid fish Pelvicachromis taeniatus, a species in which juveniles live in shoals under natural conditions. We show that relatedness significantly influenced predator inspection behaviour with kin dyads being significantly more cooperative. Thus, our results indicate a higher disposition for cooperative antipredator behaviour among kin as predicted by kin selection theory.

Social deprivation affects cooperative predator inspection in a cichlid fish.

The social environment individuals are exposed to during ontogeny shapes social skills and social competence in group-living animals. Consequently, social deprivation has serious effects on behaviour and development in animals but little is known about its impact on cooperation. In this study, we examined the effect of social environment on cooperative predator inspection. Predator inspection behaviour is a complex behaviour, which is present in a variety of shoaling fish species. Often, two fish leave the safety of the group and inspect a potentially dangerous predator in order to gather information about the current predation risk. As predator inspection is highly risky, it is prone to conflicts and cheating. However, cooperation among individuals may reduce the individual predation risk. We investigated this complex social behaviour in juveniles of the cichlid fish Pelvicachromis taeniatus that were reared in two different social environments throughout development. Fish reared in a group inspected more often than isolation-reared fish and were more likely to cooperate, i.e. they conducted conjoint inspection of a predator. By contrast, isolation-reared fish were more likely to perform a single inspection without a companion. These results suggest an impairment of cooperative behaviour in isolation-reared fish most probably due to lack of social experience and resulting in lowered social skills needed in coordinated behaviour.

Chemically-Mediated Predator Inspection Behavior by Fathead Minnow (Pimephales promelas)

ABSTRACT In the absence of visual cues, information gained from chemically-mediated inspection behavior may serve to reduce predation risk by informing minnow shoals of the proximity of potential predators. Behavioral inspection of predator chemical cues implies that sensory modes other than visual detection may be important for assessing predation risk in shoaling fishes. To assess the potential for inspection behavior by fathead minnow (Pimephales promelas; FHM), we quantified the responses of FHM to chemical cues of a natural predator, northern pike, and chemical cues of conspecifics. The presence of northern pike odor elicited inspection-like behavior among FHM. In control treatments, FHM remained within vegetated cover, and no differences were observed in the number of individuals in open water areas. When northern pike odor was added, significantly more FHM were observed in the open water habitat, although FHM activity was similar to that of controls. This suggests that FHM respond to northern pike chemical cues via directional movement into the open water habitats. These results indicate that FHM acquire information about potential predation risk in the absence of visual cues and engage in seemingly high risk investigating activity.

Predator‐inspection behaviour in female three‐spined sticklebacks Gasterosteus aculeatus is associated with status of gravidity

Differences in predator-inspection behaviour between gravid and non-gravid female as well as between male and female three-spined sticklebacks Gasterosteus aculeatus were investigated. Gravid females confronted with a live rainbow trout Oncorhynchus mykiss showed bolder inspection behaviour than non-gravid ones. The behaviour of gravid females was comparable with that of males, maybe because both face a high risk of predation. The results indicate that antipredator behaviour in female G. aculeatus is not fixed but adjusted to their reproductive state.

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.

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.

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.

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.

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.

Boldness, behavioral inhibition and learning

While many studies have examined both boldness and behavioral inhibition from psychological, psychiatric and physiological perspectives, little in the way of controlled experimental work has examined the costs or benefits of boldness and behavioral inhibition. Predator inspection behavior in fish is a model system for just such an approach. Here, we examined one potential benefit to boldness by examining the relationship between boldness/behavioral inhibition (measured by predator inspection behavior) and associative learning in the guppy (Poecilia reticulata). We found a positive relationship between male boldness and a simple associative learning task, in that males that learned to associate a cue with food were bolder than those that did not.

Predator inspection behaviour and attack cone avoidance in a characin fish: the effects of predator diet and prey experience

Individuals that dare approach predators (predator inspection behaviour) can reduce their overall risk of predation by engaging in attack cone avoidance. Under laboratory conditions, we investigated the interaction between predator diet and prey experience with predators in attack cone avoidance during predator inspection visits by glowlight tetras,Hemigrammus erythrozonus (Characidae, Ostariophysi). Shoals of predator-experienced versus predator-naı̈ve glowlight tetras were exposed to live Jack Dempsey cichlids, Cichlasoma octofaciatum, that had been fed a diet of tetras (possessing an alarm pheromone) or swordtails, Xiphophorus helleri (lacking a recognizable alarm pheromone). Naı̈ve tetras exposed to tetra-fed predators significantly increased their antipredator response (increased shoaling, dashing and freezing) and altered their predator inspection behaviour (increased latency to respond, decreased rate of inspection and decreased inspecting group size) compared with naı̈ve tetras exposed to swordtail-fed predators. In addition, naı̈ve tetras exposed to tetra-fed predators directed significantly greater proportions of their inspection visits towards the tail versus the head of the predator (attack cone avoidance) versus naı̈ve tetras exposed to swordtail-fed predators. Experienced tetras, regardless of predator diet, also significantly increased antipredator responses and altered their inspection behaviour. Experienced tetras also displayed significant attack cone avoidance. These data suggest that both predator diet and prey experience play a significant role in the threat-sensitive mediation of predator inspection behaviour in prey fish. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.