Predator Inspection Research Articles

Amarillo Fish (Girardinichthys multiradiatus) Use Visual Landmarks to Orient in Space

AbstractFish responsiveness to visual stimuli has been studied extensively in contexts such as female mate choice, predator inspection and schooling, yet surprisingly little work has been conducted on visual orientation in space in fish. Here we report on an experiment designed to test whether Amarillo fish can learn to find a goal within a maze more effectively in the presence of local visual landmarks than otherwise. We found that: (a) Amarillo fish can use landmarks to locate a goal, (b) there was no observed difference in the ability to use visual landmarks between two populations and (c) overall navigational performance differed between two populations of Amarillo fish: individuals from a permanently turbid eutrophic pond performed better than those from a pond with clear waters. We hypothesize that fish that inhabit clear waters possess poorer navigational capabilities than fish from turbid waters because they normally rely on goal‐oriented behaviour, which requires neither egocentric nor environmental clues to navigate. This paper adds to the literature on the links between habitat characteristics and population differences in performance.

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.

Association patterns and shoal fidelity in the three-spined stickleback.

We investigated pairwise association patterns and shoal fidelity in free-ranging, individual three-spine sticklebacks (Gasterosteus aculeatus) by capturing entire shoals of sticklebacks and tagging each shoal member with a unique individual mark before releasing the shoal at the point of capture. We recaptured tagged fishes in the study area on five subsequent days, noting their identity, their location and the individuals with which they were associated. Stable partner associations between fishes were observed which might provide the basis for shoal fidelity via social networks. These results suggest the potential for the kinds of inter-individual association patterns assumed by models of predator inspection and 'tit-for-tat' behaviours in free-ranging fishes.

Female behaviour mediates male courtship under predation risk in the guppy ( Poecilia reticulata )

Previous work has shown that under elevated predation risk, male guppies (Poecilia reticulata) switch from courtship to less conspicuous coercive mating at- tempts. This behavioural transition is traditionally inter- preted as a 'risk-sensitive' response that makes males less conspicuous to predators. However, predation risk leads to behavioural changes (such as schooling and predator inspection) in females that may result in coer- cive mating attempts being more profitable in high-risk situations. Here, we tested the hypothesis that the switch to coercive mating by male guppies in high-risk situa- tions is mediated by adjustments in female behaviour, rather than directly by the predator. We used replicate models resembling a known guppy predator to simulate predation risk in wild-caught guppies from a high-preda- tion population in Trinidad. Our results revealed that males performed proportionately more coercive mating attempts when presented with a female that had been ex- posed previously to a model predator compared to when males were paired with non-exposed females. Total mating activity (combined rates of courtship and forced mating attempts) did not differ significantly among the two treatment groups, indicating that overall mating activity is unaffected by predation risk. Importantly, when we subsequently presented both sexes concurrently with a predator model, total mating activity and the pro- portion of forced mating attempts remained unchanged in the high-risk treatment. Taken together, these results indicate that the transition from courtship to forced mating attempts under elevated predation risk is mediated by changes in female behaviour, which we suggest may favour the use of coercive mating under high predation risk.

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.

Chemical Predator Inspection in a Characin Fish (Hemigrammus erythrozonus,Characidae, Ostariophysi): The Effects of Mixed Predator Diets

Many prey organisms will approach (inspect) potential predators, primarily to assess local risk of predation. It has been demonstrated that Ostariphysan prey fishes can detect conspecific alarm pheromones in the diet of potential predators and use this chemical information to reduce their risk of predation while still gaining significant benefits associated with predator inspection. We conducted the current study to examine the possible effects of mixed diets on the use of these chemical predator diet cues during inspection visits. Shoals of four glowlight tetras (Hemigrammus erythrozonus) were exposed to Jack Dempsey cichlids (Cichlasoma octofaciatum) which had been fed diets consisting of: 100% tetras (with alarm pheromone); 75% tetra, 25% swordtail (Xiphophorus helleri, which lack a recognizable alarm pheromone); 25% tetra, 75% swordtail; or 100% swordtails. Tetras significantly increased their anti‐predator behaviour in response to predators fed 100% tetra or the two mixed predator diets, but not when exposed to predators fed a 100% swordtail diet. Likewise, we observed significant differences in inspection behaviour. Tetras took longer to initiate an inspection, inspected in smaller groups and directed a greater proportion of inspection visits towards the tail region of the predator when it had been fed 100% tetra or either of the two mixed prey diets. We found no significant differences in either anti‐predator or inspection behaviour among the three diet treatments containing tetras. These data strongly suggest that glowlight tetras are capable of detecting relatively small amounts of conspecific alarm pheromone in the diet of potential predators and that they modify their behaviour based on the presence or absence of these cues.

Complementary left and right eye use during predator inspection and shoal-mate scrutiny in minnows

Complementary left and right eye use during predator inspection and shoal-mate scrutiny in minnows

Complementary left and right eye use during predator inspection and shoal‐mate scrutiny in minnows

Minnows Phoxinus phoxinus did not show any difference in the average distance from a predator associated with the left or right position of a shoal‐mate. While inspection behaviour of fish tested with a mirror on their left side was indistinguishable from the behaviour of controls tested without a mirror, inspection behaviour of fish tested with the mirror on their right side appeared to be changed and incoherent in both temporal and spatial parameters. These results suggest that, as in mosquitofish Gambusia holbrooki, the condition with the mirror on the left provided the best arrangement of monocular lateral stimulation in which each stimulus fell into the correct lateral visual field. Minnows showed a significant left eye preference during scrutiny of their mirror image when tested in the absence of any predator and a significant right eye preference while monitoring a live predator in the absence of a social partner.

SOCIAL STATUS AND INVESTIGATORY BEHAVIOUR IN THE ANGELFISH (PTEROPHYLLUM SCALARE)

AbstractThe response of juvenile angelfish (Pterophyllum scalare) with different dominance ranks towards a potential predator and a nonthreatening novel stimulus was studied when in a group, to assess the influence of the social status on investigatory behaviour. Dominant fish showed a cautious predator inspection behaviour, often approaching the predator model from a relatively safe distance. In contrast, middle ranking fish inspected the predator model closely and the number and duration of the inspection visits to the area closest to the predator were greater than those of the other group members. Subordinate fish tended to avoid the potential predator, but showed the greatest interest in the novel harmless stimulus, investigating it more readily and for more time from the shortest distance than their companions. Dominant fish displayed a rather weak response towards the nonthreatening stimulus, exhibiting the shortest duration of investigation and the longest latency of approach. The response of intermediate ranking fish was more variable, existing little differences with that showed by any of the other fish categories in the parameters considered. The results indicate that dominance relationships within a group may affect behavioural decisions during investigatory behaviour, and suggest that individuals with different social status use different behavioural strategies dependent on the focal stimulus, possibly reflecting adaptive changes and physiological condition.

Risk assessment in western mosquitofish ( Gambusia affinis ): do multiple cues have additive effects?

The threat-sensitivity hypothesis predicts that prey individuals will increase antipredator behaviors as apparent predator risk increases. An implicit assumption of the threat-sensitivity hypothesis is that predator risk is additive. In other words, all characteristics of a predator that indicate risk should contribute in an additive way to determine the degree of risk-sensitive behavior. We tested this assumption in the laboratory by presenting live predators (green sunfish, Lepomis cyanellus) to groups of western mosquitofish (Gambusia affinis). We examined effects of predator diet, hunger level, and size on predator avoidance and inspection behavior of mosquitofish. Both predator diet and predator hunger level were significant and additive determinants of distance maintained from a predator, resulting in a graded response to combinations of these predator cues. In contrast, whereas predator diet was the most important determinant of general avoidance distances, predator hunger level was more important in determining mosquitofish vertical distribution and inspection behavior. Thus, the relationship between predator cue and the antipredator behavior that it elicits is dependent on which cues and behaviors are examined. Our data suggest that during risky behaviors, such as predator inspection, mosquitofish rely mainly on visual cues (behavior differences between hungry and satiated predators), whereas general avoidance behavior is determined by additive responses from visual and chemical cues.

Mosquitofish display differential left- and right-eye use during mirror image scrutiny and predator inspection responses

Previous work has shown that predator inspection in mosquitofish, Gambusia holbrooki, is more likely to occur when a mirror image of the test fish is visible on its left rather than on its right side. We investigated whether this is due to a preference for using the right eye when fixating the predator or the left eye when fixating the mirror image, or a combination of both eye preferences. We found that mosquitofish preferentially used the left eye during sustained scrutiny of their mirror image when tested in the absence of any predator. On the other hand, when tested in a swimway for predator inspection responses in the absence of any mirror image (or other social stimuli), mosquitofish explored the environment with the left eye when at a distance and the right eye when near the predator.

Attack cone avoidance during predator inspection visits by wild finescale dace (Phoxinus neogaeus): the effects of predator diet.

When confronted by potential predators, many prey fishes engage in predator inspection behavior. Previous authors have argued that by selectively avoiding the predator's head during an inspection visit (attack cone avoidance), individual inspectors may reduce their local risk of predation. In field trials, we investigated the effects of predator diet cues on the presence of 'attack cone avoidance' during predator inspection visits. Wild, free-ranging finescale dace (Phoxinus neogaeus) were exposed to the combined cues of a model predator and a distilled water control or the odor of a yellow perch (Perca flavescens) fed dace (with alarm pheromone), swordtail (Xiphophorus helleri) (lacking Ostariophysan alarm pheromone), or perch that were food deprived for four days. Finescale dace modified their predator inspection behavior following exposure to the odor of a perch fed dace (fewer dace present, reduced frequency of inspections, and an increased per capita inspection rate) compared to those exposed to the odor of a perch fed swordtails, perch that were food deprived, or a distilled water control. In addition, dace inspected the tail region more often only when the model predator was paired with the odor of a perch fed dace. In all other treatments, dace inspected the head region of the model predator more often. These data suggest that attack cone avoidance of inspecting prey fishes may be more likely to occur in high-risk situations, such as in the presence of conspecific alarm pheromones in the diet of potential predators.

CHEMICAL PREDATOR INSPECTION AND ATTACK CONE AVOIDANCE IN A CHARACIN FISH: THE EFFECTS OF PREDATOR DIET

AbstractMany prey organisms will approach (inspect) a potential predator, primarily to assess local risk of predation. It has been argued that by avoiding the head region of predators during inspections, prey can reduce the risks associated with such behaviour (attack cone avoidance). Prior experiments, however, have not incorporated the combined chemical and visual predator cues. We conducted laboratory experiments to determine the effects of combined predator dietary (chemical) and visual cues on the form and location of predator inspection visits by glowlight tetras (Hemigrammus erythrozonus). Tetras were exposed to a live cichlid predator (Cichlasoma octofasciatum) which had been fed tetras (with alarm pheromone), swordtails (Xiphophorus helleri; lacking Ostariophysan alarm pheromones) or food deprived. There was no significant difference in the overall rate of predator inspection by tetras to tetra-fed, swordtail-fed or food deprived cichlids. There was, however, a significant effect of predator diet on the size of inspection shoals and the location of inspections. Tetras inspected a tetrafed predator in significantly smaller groups, more often as singletons and directed a greater proportion of their inspections towards the tail of the predator. Tetras exposed to swordtail-fed or food deprived cichlids inspected in larger groups and directed more inspections towards the head of the predator. When the predator dietary cue contained tetra alarm pheromone, there was a significant increase in the attack latency by predators. Taken together, these data suggest that tetras use both chemical and visual predator cues during inspection visits and will modify their behaviour based on the presence or absence of conspecific alarm pheromone in the diet of a potential predator.

Chemically mediated predator inspection behaviour in the absence of predator visual cues by a characin fish

Animals commonly approach (i.e. ‘inspect’) potential predators. Glowlight tetras,Hemigrammus erythrozonus , have previously been shown to inspect the combined chemical and visual cues originating from novel predators and to modify their inspection (approach) behaviour depending upon the predator's diet. We conducted two experiments to determine whether tetras would inspect the chemical cues of injured prey or the dietary cues of a novel predator in the absence of any visual cues. Shoals of glowlight tetras were exposed to either distilled water (control) or the skin extract of swordtail (lacking ostariophysan alarm pheromones) or the skin extract of tetra (with alarm pheromones). There was no significant difference in the frequency of predator inspection behaviour towards swordtail or tetra skin extract compared to the distilled water controls. In the second experiment, we exposed shoals of tetras to either distilled water or the odour of Jack Dempsey cichlids, Cichlasoma octofasciatum, which had been food deprived, or fed a diet of swordtails or tetras. There was no significant difference in the frequency of predator inspection behaviour towards the odour of the starved cichlids and the odour of the fed cichlids in either of the two diet treatments. However, when tetras were exposed to the odour of cichlids fed tetras, they took significantly longer to initiate an inspection visit, remained further from the source of the chemical cues and inspected in smaller groups, compared with the odour of a starved cichlid or a cichlid fed swordtails. These data strongly suggest that tetras will inspect chemical cues alone, but only if the cue contains information about the predator.

Prior exposure to a predator influences lateralization of cooperative predator inspection in the guppy, Poecilia reticulata

Functional specializations of the right and left side of the brain have been shown to occur in all vertebrate classes and are known to affect various aspects of behaviour. Recent evidence suggests that cerebral lateralization influences cooperative predator inspection in fish. In order to confirm these findings, predator inspection was studied in female guppies (Poecilia reticulata) while a shoalmate (their own mirror image) was visible either on their left or right side. We used laboratory‐reared guppies with no natural experience of predators. One half of the subjects were sensitized to a predator by repeatedly introducing a hungry individual of the species Lepomis gibbosus into their home tank prior to the test, while the other half remained without any experience of predators. Guppies with prior experience of the predator showed a greater tendency to approach a live predator when their shoalmate was visible on their right side.

FORAGING TRADE-OFFS AND PREDATOR INSPECTION IN AN OSTARIOPHYSAN FISH: SWITCHING FROM CHEMICAL TO VISUAL CUES

Abstract Under laboratory conditions, we investigated the presence of a foraging trade-off in the chemical predator inspection behaviour of finescale dace (Chrosomus neogaeus). Dace were fed ad libitum, or food deprived for 24 or 48 hours and allowed to inspect a live yellow perch (Perca flavescens) in the presence of the chemical cues of a perch fed dace (with alarm pheromone) or swordtails (Xiphophorus helleri; without alarm pheromones). Dace exposed to the odour of a perch fed swordtails exhibited no evidence of a trade-off in either anti-predator behaviour or predator inspection behaviour. When fed ad libitum and exposed to the odour of a perch fed dace, individuals exhibited significantly greater anti-predator behaviour (increased shoaling, decreased area use and greater frequency of dashing and freezing behaviour) when compared to the swordtail diet control. Predator inspection behaviour was also significantly affected (increased latency to inspect and minimum distance approached towards the predator and fewer inspectors per visit). However, when food deprived for 24 or 48 hours, dace exhibited no differences in either anti-predator or predator inspection behaviour when exposed to the odour of perch fed dace versus perch fed swordtails. These data demonstrate that predator inspection behaviour based on the chemical cues of a potential predator is subject to foraging trade-offs and that individual prey may reduce their overall risk of predation by increasing the use of visual cues.

Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish

It has recently been reported that predator inspection is more likely to occur when a companion (i.e. the mirror image of the test animal) is visible on the left rather than on the right side of mosquitofish Gambusia holbrooki. This very unexpected outcome could be consistent with the hypothesis of a preferential use of the right eye during sustained fixation of a predator as well as of a preferential use of the left eye during fixation of conspecifics. We measured the time spent in monocular viewing during inspection of their own mirror images in females of six species of fish, belonging to different families— G. holbrooki, Xenotoca eiseni, Phoxinus phoxinus, Pterophyllum scalare, Xenopoecilus sarasinorum, and Trichogaster trichopterus. Results revealed a consistent left-eye preference during sustained fixation in all of the five species. Males of G. holbrooki, which do not normally show any social behaviour, did not exhibit any eye preferences during mirror-image inspection. We found, however, that they could be induced to manifest a left-eye preference, likewise females, if tested soon after capture, when some affiliative tendencies can be observed. These findings add to current evidence in a variety of vertebrate species for preferential involvement of structures located in the right side of the brain in response to the viewing of conspecifics.

Differences in Timidity and Escape Responses between Predator‐naive and Predator‐sympatric Rainbowfish Populations

Responses of rainbowfish (Melanotaenia duboulayi) from two populations towards a) an active and a passive predatory fish and b) a novel trawl apparatus, were compared. Predator‐sympatric fish avoided the fish predators and showed stronger avoidance behaviour in response to the active predator. These fish used predator inspection excursions to rapidly assess the potential risk and their escape responses were consistently effective. In contrast the predator‐naive fish ignored the passive predator but were continually drawn towards the active predator possibly due to generalized curiosity and the absence of significant negative feedback from the predator, which was restrained by a clear Perspex partition. Despite this attraction, the predator‐naive fish did not display typical predator inspection behaviour and showed very poor escape performance when initially confronted by the trawl apparatus. Many of these fish, however, showed rapid improvement in their escape performance through learning. These results suggest that predator‐sympatric rainbowfish have the capacity to assess the level of threat posed by a predator and predator‐naive rainbowfish learn to implement appropriate escape strategies when forced to evade a threat.

Laterality and cooperation: mosquitofish move closer to a predator when the companion is on their left side

Mirror images simulating social partners that cooperated or defected have been used as an experimental method to test the hypothesis that, while inspecting a predator, pairs of fish play a conditional strategy, Tit for Tat, in an iterated version of the Prisoner’s Dilemma game. Using this method, we found that predator inspection was more likely to occur when the mirror image was visible on the left rather than on the right side of mosquitofish,Gambusia holbrooki. The same occurred even when a videorecorded stimulus presentation was used, in which sequences of the predator were mixed with their mirror-image equivalents, thus showing that the asymmetry was not due to behavioural or morphological asymmetries of the predator itself. Moreover, irrespective of whether they were tested with a cooperative (parallel mirror) or a defecting (angled mirror) partner, mosquitofish drew closer to the predator when the mirror was on their left side. These findings suggest that the images seen on the right and left sides by a fish may evoke different types of social behaviour, probably because of differing modes of analysis of perceptual information carried out by the left and right sides of the brain; accurate control and balancing of the side of presentation of visual stimuli during behavioural experiments thus appears to be crucial.

Who dares, learns: chemical inspection behaviour and acquired predator recognition in a characin fish

Individuals that dare approach predators (predator inspection behaviour) may benefit by acquiring information regarding the potential threat of predation. Although information acquisition based on visual cues has been demonstrated for fish, it is unknown whether fish will inspect predators on the basis of chemical cues or whether such inspection behaviour results in information acquisition. Here, we first ascertained whether predator inspection behaviour can be mediated by chemical cues from predators by exposing groups of predator-naive glowlight tetras (Hemigrammus erythrozonus) to the chemical cues of a potential fish predator (convict cichlidCichlasoma nigrofasciatum) that had been fed either tetras (which possess an alarm pheromone) or swordtails (Xiphophorus helleri, which lack Ostariophysan alarm pheromones). Tetras showed a significant increase in antipredator behaviour when exposed to the tetra-diet cue, but not when exposed to the swordtail-diet cue. Chemically mediated predator inspection behaviour was also affected. Both the latency to inspect and the minimum approach distance to the predator significantly increased, and the mean number of inspectors per predator inspection visit significantly decreased when tetras were exposed to the tetra-diet versus the swordtail-diet chemical cues. We then examined a potential benefit associated with chemically mediated predator inspection behaviour. Only tetras that were initially exposed to the tetra-diet cue and that had inspected the predator acquired the visual recognition of a convict cichlid as a predation threat. Our results thus demonstrate that (1) predator inspection behaviour in the glowlight tetra can be initiated by chemical cues, (2) chemically mediated inspection behaviour is affected by the presence of alarm pheromone, and (3) inspectors benefit by acquiring the recognition of novel predators.