The role of vision in the predatory behaviour of natricine snakes

Early workers concluded that ingestively naive garter snakes (Thamnophis) recognize chemical cues from their normal prey, and that such cues are sufficient to elicit prey attack, whereas visual prey cues are not sufficient. In the light of recent observations on how garter and water snakes (Nerodia) forage, new tests were made of the role of visual stimuli in the aquatic predation of several natricine species. Both experienced and ingestively naive snakes oriented to and attacked a fish model in plain water, although they made more orientations and attacks when diffuse fish odour was present in the water. Fish odour in water also elicited increased aquatic searching behaviour. Early views on the role of vision in the predation of newborn natricine snakes require modification, and there is a need for investigation of the properties of effective visual stimuli and the ontogeny of responsiveness to them.     

Predators marked with chemical cues from one prey have increased attack success on another prey species

1. To reduce the risk of being eaten by predators, prey alter their morphology or behaviour. This response can be tuned to the current danger if chemical or other cues associated with predators inform the prey about the risks involved. 2. It is well known that various prey species discriminate between chemical cues from predators that fed on conspecific prey and those that fed on heterospecific prey, and react stronger to the first. It is therefore expected that generalist predators are more successful in capturing a given prey species when they are contaminated with chemical cues from another prey species instead of cues from the same prey species. 3. Here, a generalist predatory mite was studied that feeds on thrips larvae as well as on whitefly eggs and crawlers. Mites were marked with cues (i.e. body fluids) of one of these two prey species and were subsequently offered thrips larva. 4. Predators marked with thrips cues killed significantly fewer thrips than predators marked with whitefly cues, even though the predator's tendency to attack was the same. In addition, more thrips larvae sought refuge in the presence of a predatory mite marked with thrips cues instead of whitefly cues. 5. This suggests that generalist predators may experience improved attack success when switching prey species.     

Predator naïve minnows respond to their conspecific alarm substance but not the odour from a non-native predator

When exposed to predator cues, ostariophysan fishes exhibit short-term anti-predator behavioural responses in order to minimise predation risk. Non-native predator cues are, however, likely to elicit poor behavioural responses in native prey fishes. This study investigated whether chubbyhead barb Enteromius anoplus, a native freshwater minnow in South Africa, had the innate ability to recognise and respond to largemouth bass Micropterus salmoides, a non-native piscivore. This was experimentally evaluated by investigating behavioural responses to both the non-native predator's odour and damage-released conspecific alarm substance (CAS). Chubbyhead barbs did not exhibit any behavioural response to largemouth bass odour both before and after exposure to CAS. This suggests that the chubbyhead barbs likely lacked the innate ability to recognise the non-native largemouth bass predator kairomones. By comparison, exposure to CAS was associated with significant behavioural responses, with chubbyhead barbs shifting from free-swimming to hovering, and frequent use of refugia. This suggests that despite ineffective response to non-native largemouth bass odour, chubbyhead barbs responded to general predator attack. Overall, this study suggests the potential for non-native largemouth bass to induce negative consumptive effects on chubbyhead barbs due to their inability to identify non-native predator's odour. In addition, nonconsumptive effects are likely due to altered activities in response to predator attack.     

Components of predatory behaviour underlying density-dependent prey-size selection by Notiophilus biguttatus F. (Carabidae,Coleoptera)

Summary Prey-size selection by the carabid beetle Notiophilus biguttatus F. was studied, using prey belonging to two-size-classes of the spring-tail species Orchesella cincta (L.) (Collembola). The highest values for attack readiness and success ratio of the attacks were obtained for the smaller prey animals. A model for prey-size selection was constructed in which these two parameters are included, predicting an increasing chance of incorporating large prey in the diet with declining total prey density. This prediction was tested experimentally and qualitatively confirmed. In a quantitative sense, however, the results deviated from the expectation. This was caused by a greater attack readiness of the beetles in a semi-natural environment (in which the prediction was tested) than in the artificial environment in which the parameters had been estimated. General relevance of the results, their bearing on optimal foraging theory and their ecological implications are discussed.     

Underwater Video Reveals Strong Avoidance of Chemical Alarm Cues by Prey Fishes

A diversity of fishes release chemical cues upon being attacked by a predator. These cues, commonly termed alarm cues, act as sources of public information warning conspecifics of predation risk. Species which are members of the same prey guild (i.e. syntopic and share predators) often respond to one another's alarm cues. The purpose of this study was to discriminate avoidance responses of fishes to conspecific alarm cues and cues of other prey guild members from responses to unknown damaged fish odours and novel odours. We used underwater video to measure avoidance responses of freshwater littoral species, namely fathead minnows (Pimephales promelas), finescale dace (Chrosomus neogaeus), and brook stickleback (Culaea inconstans), to both injured fish cues and novel non‐fish odours. The cyprinids (minnows and dace) showed significant avoidance of minnow cues over swordtail cues, morpholine, and the control of distilled water and tended to avoid fathead cues over cues of known prey guild members (stickleback). Cyprinids also significantly avoided cues of stickleback over unknown heterospecific cues (swordtail) and tended to avoid stickleback cues over morpholine and the distilled water control. Stickleback significantly avoided fathead minnow extract over the distilled water and tended to avoid stickleback and swordtail over distilled water. We conclude that fishes in their natural environment can show dramatic changes in behaviour upon exposure to alarm cues from conspecifics and prey guild members. These responses do not represent avoidance of cues of any injured fish or any novel odour.     

Evidence for the Predator Attraction Hypothesis in an amphibian predator–prey system

Many species possess damage-released chemical alarm cues that function in alerting nearby individuals to a predator attack. One hypothesis for the evolution and/or maintenance of such cues is the Predator Attraction Hypothesis, where predators, rather than prey, are the “intended” recipients of these cues. If a predator attack attracts additional predators, these secondary predators might interfere with the predation event, providing the prey with a better chance to escape. In this study, we conducted two experiments to explore this hypothesis in an amphibian predator/prey system. In Experiment 1, we found that tiger salamanders (Ambystoma mavortium) showed a foraging attraction to chemical cues from wood frog (Lithobates sylvaticus) tadpoles. Salamanders that were experienced with tadpole prey, in particular, were strongly attracted to tadpole alarm cues. In Experiment 2, we observed experimental encounters between a tadpole and either one or two salamanders. The presence of the second predator caused salamanders to increase attack speed at the cost of decreased attack accuracy (i.e., increasing the probability that the tadpole would escape attacks). We also found that the mere presence of visual and chemical cues from a second predator did not affect this speed/accuracy trade-off but did cause enough of a distraction to increase tadpole survival. Thus, our findings are consistent with the Predator Attraction Hypothesis for the evolution and/or maintenance of alarm cues.     

Behavioural responses of free‐ranging western grey kangaroos (Macropus fuliginosus) to olfactory cues of historical and recently introduced predators

Predation risk influences foraging decisions and time allocation of prey species, and may result in habitat shifts from potentially dangerous to safer areas. We examined a wild population of western grey kangaroos (Macropus fuliginosus) to test the efficacy of predator faecal odour in influencing time allocated to different behaviours and inducing changes in habitat use. Kangaroos were exposed to fresh faeces of a historical predator, the dingo (Canis lupus dingo), a recently introduced predator, the red fox (Vulpes vulpes), a herbivore (horse, Equus caballus) and an unscented control simultaneously. Kangaroos did not increase vigilance in predator‐scented areas. However, they investigated odour sources by approaching and sniffing; more time was spent investigating fox odour than control odours. Kangaroos then exhibited a clear anti‐predator response to predator odours, modifying their space use by rapidly escaping, then avoiding fox and dingo odour sources. Our results demonstrate that wild western grey kangaroos show behavioural responses to predator faeces, investigating then avoiding these olfactory cues of potential predation risk, rather than increasing general vigilance. This study contributes to our understanding of the impact of introduced mammalian predators on marsupial prey and demonstrates that a native Australian marsupial can recognize and respond to the odour of potential predators, including one that has been recently introduced.     

Negotiating a noisy, information-rich environment in search of cryptic prey: olfactory predators need patchiness in prey cues

1. Olfactory predator search processes differ fundamentally to those based on vision, particularly when odour cues are deposited rather than airborne or emanating from a point source. When searching for visually cryptic prey that may have moved some distance from a deposited odour cue, cue context and spatial variability are the most likely sources of information about prey location available to an olfactory predator. 2. We tested whether the house mouse (Mus domesticus), a model olfactory predator, would use cue context and spatial variability when searching for buried food items; specifically, we tested the effect of varying cue patchiness, odour strength, and cue-prey association on mouse foraging success. 3. Within mouse- and predator-proof enclosures, we created grids of 100 sand-filled Petri dishes and buried peanut pieces in a set number of these patches to represent visually cryptic 'prey'. By adding peanut oil to selected dishes, we varied the spatial distribution of prey odour relative to the distribution of prey patches in each grid, to reflect different levels of cue patchiness (Experiment 1), odour strength (Experiment 2) and cue-prey association (Experiment 3). We measured the overnight foraging success of individual mice (percentage of searched patches containing prey), as well as their foraging activity (percentage of patches searched), and prey survival (percentage of unsearched prey patches). 4. Mouse foraging success was highest where odour cues were patchy rather than uniform (Experiment 1), and where cues were tightly associated with prey location, rather than randomly or uniformly distributed (Experiment 3). However, when cues at prey patches were ten times stronger than a uniformly distributed weak background odour, mice did not improve their foraging success over that experienced when cues were of uniform strength and distribution (Experiment 2). 5. These results suggest that spatial variability and cue context are important means by which olfactory predators can use deposited odour cues to locate visually cryptic prey. They also indicate that chemical crypsis can disrupt these search processes as effectively as background matching in visually based predator-prey systems.     

Habitat and food specificity in aphidophagous predators

Current knowledge of the processes underlying prey location and choice by aphidophagous predators is reviewed by considering the succession of behavioural mechanisms required for the predator to obtain prey. The predator may locate areas where prey are likely to be found by responding to physical aspects of the habitat, or to semiochemicals produced by the host plant. The predator may then respond to visual or olfactory cues to locate the aphid prey. The predator's readiness to attack and consume aphids is influenced by any behavioural or chemical defence strategies, and by the palatability or nutrient value of the aphids. Toxic allelochemicals ingested by aphids from their host plant may have a detrimental effect on predators.     

Variation of prey responses to cues from a mesopredator and an apex predator

Detection and avoidance of predator cues can be costly, so it is important for prey to balance the benefits of gaining food against the costs of avoiding predators. Balancing these factors becomes more complicated when prey are threatened by more than one type of predator. Hence, the ability to recognize species‐specific predator odours and prioritize behaviours according to the level of risk is essential for survival. We investigated how rock rats, Zyzomys spp. modify their foraging behaviour and giving‐up density (GUD) in the presence of an apex predator, the dingo Canis dingo, a mesopredator, the northern quoll Dasyurus hallucatus, a herbivore, the rock wallaby Petrogale brachyotis as a pungency control and water as a procedural control. Both dingoes and quolls consume rock rats, but because quolls can enter small crevices inhabited by rock rats, they pose a greater threat to rock rats than dingoes. Rock rats demonstrated a stronger avoidance to quoll odour than dingo odour, and no avoidance of the pungency control (rock wallaby) and the procedural control (water). GUD values declined significantly over the duration of the study, but did not differ between odour treatments. Our results support the hypothesis that prey vary behaviour according to perceived predator threat, and show stronger responses to potentially more dangerous predators.     

Diel variation in use of cover and feeding activity of a benthic freshwater fish in response to olfactory cues of a diurnal predator

Some fish recognize the threat of predatory fish through chemical cues, which may result in variation in diel activity. However, there is little experimental evidence of diel shifts in activity of prey fish in response to the diel activity of a predator. We compared the total prey consumed and the use of cover by common bullies (Gobiomorphus cotidianus), a native benthic feeding eleotrid, when exposed to the odour of an exotic predator, European perch (Perca fluviatilis), over a 12-h period. Our results showed no significant effect of perch odour on feeding activity, but a significant increase in the use of cover at night and a decrease in the use of cover by day. While common bullies may recognize the presence of a predator through chemical cues, dark conditions may inhibit this and other sensory mechanisms, affecting their ability to recognize the proximity of a predator. For example, during the daytime they may rely on visual cues to initiate cover-seeking behavior, but in the dark, vision is impaired giving them less warning of predators, thus potentially making them more vulnerable.     

Strong behavioural defensive responses of endemic Rana latastei tadpoles induced by a native predator's odour

Prey species must constantly acquire information on predator identity, abundance and dangerousness from the environment. In aquatic habitats, this information is mainly propagated by water-borne chemical signals, either predator-specific odours or prey alarm cues. Anuran larvae innately respond to conspecific alarm cues and are able to associate them to predator cues during their lifetime. In this study, we investigated the anti-predatory responses of endemic Italian agile frog (Rana latastei) tadpoles exposed to either conspecific or heterospecific alarm cues and a native predator's (Anax imperator larvae) odour. Pre-and post-stimulus behaviours of each tadpole were recorded by a digital camera and analysed by a source executable software for image-based tracking. We found that Italian agile frog tadpoles responded to fasted dragonfly odour by strongly reducing their activity, both in terms of the amount of time they spent active and path length covered in comparison to control groups. Contrary to previous studies, predators' diet had a negligible effect on tadpole response and our experiment did not bring any evidence of the phylogenetic-relatedness hypothesis. The innate or early-in-development recognition of dragonfly larvae is clearly adaptive and may increase tadpole survival with relatively low costs, but, at the same time, may increase the risk of ignoring novel potential threats.     

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

Recent 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.     

Detection of substrate-associated odour cues versus prey-associated cues by the oral veil in Tritonia diomedea

Our goal was to test two potential sensory roles for the oral veil in the nudibranch Tritonia diomedea (now synonymous with T. tetraquetra). First, we hypothesized this cephalic sensory organ could detect substrate-associated odours left behind by an odour plume flowing across sediment. In two experiments in a laboratory flow tank, however, T. diomedea did not show consistent crawling headings in response to either prey or predator odours associated with sediment substrate. In one of the experiments, the slugs did significantly decrease crawling speed in response to prey odours. Although slugs could thus detect at least some substrate-associated odours, these results suggest such cues are not used for navigation. We next considered the oral veil’s potential role in behaviours requiring responses to nearby cues. Our observations of animals before and after denervation of the oral veil suggest that, unsurprisingly, predatory bite-strikes do rely on sensory input from the oral veil. Overall, these data, combined with the results of earlier studies, are consistent with the oral veil detecting cues primarily from nearby stimuli (including both chemical and mechanical modalities), while having little or no role in detecting and responding to odour cues originating from distant sources used for navigation behaviour.     

Prey naivety in the behavioural responses of juvenile Chinook salmon (Oncorhynchus tshawytscha) to an invasive predator

1. Non‐native predators might inflict proportionally higher mortality on prey that have no previous experience of them, compared to species that have coexisted with the predator for some time. 2. We tested whether juvenile Chinook salmon (Oncorhynchus tshawytscha) were less able to recognise a non‐native than a native predator, by investigating behavioural responses to the chemical cues of the invasive smallmouth bass (Micropterus dolomieu) and the native northern pikeminnow (Ptychocheilus oregonensis) in both laboratory and field experiments. 3. Laboratory results demonstrated strong innate antipredator responses of individual juvenile Chinook salmon to northern pikeminnow; fish spent 70% of time motionless and exhibited 100% greater panic response than in controls. By contrast, antipredator responses to the chemical cues of smallmouth bass did not differ from controls. 4. These results were supported by similar differences in recognition of these predator odours by groups of juvenile Chinook salmon in fully natural conditions, though responses reflected a greater range of antipredator behaviours by individuals. In field trials, responses to northern pikeminnow odour resulted in increased flight or absence, reductions in swimming and foraging, and increased time spent near the substratum, compared to smallmouth bass odour. 5. Given that survival of juvenile fish is facilitated by predator recognition, our results support the hypothesis that naivety may be an important factor determining the effect of non‐native predators on prey populations. Efforts to manage the effect of native and non‐native predators may benefit by considering complex behavioural interactions, such as these at the individual and group levels.     

Linking Morphological and Behavioural Defences: Prey Fish Detect the Morphology of Conspecifics in the Odour Signature of their Predators

Predation is a strong selective force acting on both morphology and behaviour of prey animals. While morphological defences (e.g. crypsis, presence of armours or spines or specific body morphologies) and antipredator behaviours (e.g. change in foraging or reproductive effort, or hiding and fleeing behaviours) have been widely studied separately, few studies have considered the interplay between the two. The question raised in our study is whether antipredator behaviours of a prey fish to predator odours could be influenced by the morphology of prey conspecifics in the diet of the predator. We used goldfish (Carassius auratus) as our test species; goldfish exposed to predation risk significantly increase their body depth to length ratio, which gives them a survival advantage against gape‐limited predators. We exposed shallow‐bodied and deep‐bodied goldfish to the odour of pike (Esox lucius) fed either form of goldfish. Deep‐bodied goldfish displayed lower intensity antipredator responses than shallow‐bodied ones, consistent with the hypothesis that individuals with morphological defences should exhibit less behavioural modification than those lacking such defences. Moreover, both shallow‐ and deep‐bodied goldfish displayed their strongest antipredator responses when exposed to the odour of pike fed conspecifics of their own morphology, indicating that goldfish are able to differentiate the morphology of conspecifics through predator diet cues. For a given individual, predator threat increases as the prey become more like the individual eaten, revealing a surprising level of sophistication of chemosensory assessment by prey fish.     

Functional responses of five cyprinid species to planktonic prey

Synopsis The functional responses of five species of cyprinids (Chalcalburnus chalcoides, Vimba vimba, Abramis brama, Rutilus rutilus, and Scardinius erythrophthalmus) feeding on four planktonic prey types were measured in the laboratory. Although no alternative prey types were present, the response curves were sigmoid in most cases, because attack rates were not independent of prey density. The findings are explained as being the overt expression of the fishes& foraging tactics. The chief way of maximizing food uptake, according to our interpretation, is accelerating attack rates with increasing prey density. The ability of prey to escape or relative prey size may interfere with this strategy. C. chalcoides, the only obligatory planktivore among the species studied, attacks at higher rates and responds most markedly to changes in prey density.     

Olfactory response of the predator <Emphasis Type="Italic">Zetzellia mali</Emphasis> to a prey patch occupied by a conspecific predator

While searching for food, predators may use volatiles associated with their prey, but also with their competitors for prey. This was tested for the case of Zetzellia mali (Ewing) (Acari: Stigmaeidae), an important predator of the hawthorn spider mite, Amphitetranychus viennensis (Zacher) (Acari: Tetranychidae), in black-cherry orchards in Baraghan, Iran. Using a Y-tube olfactometer, the response of this predatory mite was tested to odour from black-cherry leaves with a conspecific female predatory mite, either with or without a female of the hawthorn spider mite when the alternative odour came from black-cherry leaves with the hawthorn spider mite only. Female predators avoided odours from leaves with both a hawthorn spider mite and a conspecific predator, as well as leaves with a conspecific predator only. We discuss whether avoidance emerges in response to cues from the competitor/predator, the herbivore/prey or the herbivore-damaged plant.     

Visual and olfactory location of biotopes, prey patches, and individual prey by the ladybeetleChilocorus nigritus

Foraging behaviour of the predatorChilocorus nigritus (Fabricius) (Coleoptera: Coccinellidae) at the three spatial levels of biotope, prey patch and individual prey, was studied in the laboratory, and related to behaviour in the field. Vertically oriented parallel lines were more attractive than the same shapes in a horizontal position. A simulated horizon with a tree line was preferred to a simulated flat horizon. They were attracted to a tree image for the first 2 h of exposure, but were less attracted after longer exposure, possibly due to habituation. Leaf shape was recognised, and simple ovate leaves were preferred to compound bipinnate leaves and to squares. These responses were associated with biotope selection for feeding and aggregation at aestivation sites. The location of prey patches by adults involved prey odour but the location of such sites by larvae did not. Adults detected individual prey visually and olfactorily over short distances but physical contact with prey was required for detection by larvae. Location of individual prey and prey patches by adults and larvae was facilitated by alternation between intensive and extensive search. The differences in the ability of larvae and adults to locate prey, stem from the adults being the active locators of biotope and patch, whereas the comparatively immobile larvae depend on their parents’ ability for long-range location of prey. Two hypotheses concerning coccinellid foraging behaviour are proposed. Firstly, the duration of response to a visual cue is related to the distance over which such a cue may be perceived. It follows that habituation to closer range cues occurs more rapidly than to longer range cues. Secondly, visual cues used by adults at the different spatial levels of prey location, and the location of mates and aggregation sites, have the same or similar shape. These results also provide guidelines for orchard management to maximise the biocontrol value of this species.     

Cross‐Modality Effects of Prey Odour During the Intraspecific Interactions of a Mosquito‐Specialist Predator

One of the predictions from evolutionary game theory is that individuals will increase their willingness (i.e. become primed) to escalate aggression when they detect the presence of a limiting resource. Here, we test this prediction in the context of prey odour priming escalation decisions during vision‐based encounters by Evarcha culicivora. This East African jumping spider (Salticidae) feeds indirectly on vertebrate blood by actively choosing blood‐carrying female mosquitoes as preferred prey. Unlike many salticid species, it also expresses pronounced mutual mate choice. As predicted, we show here that, in the presence of odour from their preferred prey, both sexes of E. culicivora escalate during vision‐based same‐sex encounters. This is further evidence that the odour of blood‐carrying mosquitoes is salient to this salticid. For both sexes of E. culicivora, this particular prey may be a resource that matters in the context of intrasexual selection.