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.     

Dynamic Risk Assessment: Prey Rapidly Adjust Flight Initiation Distance to Changes in Predator Approach Speed

The pre‐eminent model of flight initiation distance assumes that the function relating predation risk to distance between predator and prey is constant. However, the risk–distance function can change dramatically during approaches by predators. Changes in predator behavior during approach and in availability of benefits (e.g. food or potential mates) may alter risks and/or costs during encounters. Thus, prey should be able to respond appropriately to changes in cues to risk, such as predator approach speed. Under the assumption that prey assess risk in real time, it was predicted that flight initiation distance (distance between predator and prey when escape begins) decreases when approach speed increases and increases when approach speed decreases during an encounter. Effects of single, abrupt changes from slower to faster approach or the reverse were studied in a lizard, Anolis lineatopus. Flight initiation distances were determined solely by final approach speed, being nearly identical for: (1) continuously fast approaches and approaches initially at the slower and finally at the faster speed and (2) for continuously slower approaches and approaches initially at faster and finally at slower speed. Escape should be adjusted to match changes in risk and cost caused by changes in predator behavior, ability to escape, and costs of escape as attacks unfold. A recent model by Broom and Ruxton [Behavioural Ecology (2004) vol. 16, pp. 534—540] predicts that cryptic prey should stay motionless until detected, then flee immediately. Our results suggest that current escape models can be applied to prey escape strategies when cues to risk change, by assuming that prey base decisions on the current relationship between risk and distance. Empirical studies are needed to test predictions concerning continuous risk assessment.     

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.     

Influence of gaze and directness of approach on the escape responses of the Indian rock lizard, Psammophilus dorsalis (Gray, 1831)

Animals often evaluate the degree of risk posed by a predator and respond accordingly. Since many predators orient their eyes towards prey while attacking, predator gaze and directness of approach could serve as conspicuous indicators of risk to prey. The ability to perceive these cues and discriminate between high and low predation risk should benefit prey species through both higher survival and decreased energy expenditure. We experimentally examined whether Indian rock lizards (Psammophilus dorsalis) can perceive these two indicators of predation risk by measuring the variation in their fleeing behaviour in response to type of gaze and approach by a human predator. Overall, we found that the gaze and approach of the predator influenced flight initiation distance, which also varied with attributes of the prey (i.e. size/sex and tail-raise behaviour). Flight initiation distance (FID) was 43% longer during direct approaches with direct gaze compared with tangential approaches with averted gaze. In further, exploratory, analyses, we found that FID was 23% shorter for adult male lizards than for female or young male (FYM) lizards. In addition, FYM lizards that showed a tail-raise display during approach had a 71% longer FID than those that did not. Our results suggest that multiple factors influence the decision to flee in animals. Further studies are needed to test the generality of these factors and to investigate the proximate mechanisms underlying flight decisions.     

Predator–prey interactions,flight initiation distance and brain size

Prey avoid being eaten by assessing the risk posed by approaching predators and responding accordingly. Such an assessment may result in prey–predator communication and signalling, which entail further monitoring of the predator by prey. An early antipredator response may provide potential prey with a selective advantage, although this benefit comes at the cost of disturbance in terms of lost foraging opportunities and increased energy expenditure. Therefore, it may pay prey to assess approaching predators and determine the likelihood of attack before fleeing. Given that many approaching potential predators are detected visually, we hypothesized that species with relatively large eyes would be able to detect an approaching predator from afar. Furthermore, we hypothesized that monitoring of predators by potential prey relies on evaluation through information processing by the brain. Therefore, species with relatively larger brains for their body size should be better able to monitor the intentions of a predator, delay flight for longer and hence have shorter flight initiation distances than species with smaller brains. Indeed, flight initiation distances increased with relative eye size and decreased with relative brain size in a comparative study of 107 species of birds. In addition, flight initiation distance increased independently with size of the cerebellum, which plays a key role in motor control. These results are consistent with cognitive monitoring as an antipredator behaviour that does not result in the fastest possible, but rather the least expensive escape flights. Therefore, antipredator behaviour may have coevolved with the size of sense organs, brains and compartments of the brain involved in responses to risk of predation.     

Diet quality in a wild grazer declines under the threat of an ambush predator

Predators influence prey populations not only through predation itself, but also indirectly through prompting changes in prey behaviour. The behavioural adjustments of prey to predation risk may carry nutritional costs, but this has seldom been studied in the wild in large mammals. Here, we studied the effects of an ambush predator, the African lion (Panthera leo), on the diet quality of plains zebras (Equus quagga) in Hwange National Park, Zimbabwe. We combined information on movements of both prey and predators, using GPS data, and measurements of faecal crude protein, an index of diet quality in the prey. Zebras which had been in close proximity to lions had a lower quality diet, showing that adjustments in behaviour when lions are within short distance carry nutritional costs. The ultimate fitness cost will depend on the frequency of predator–prey encounters and on whether bottom-up or top-down forces are more important in the prey population. Our finding is the first attempt to our knowledge to assess nutritionally mediated risk effects in a large mammalian prey species under the threat of an ambush predator, and brings support to the hypothesis that the behavioural effects of predation induce important risk effects on prey populations.     

Escape and alerting responses by Balearic lizards (Podarcis lilfordi) to movement and turning direction by nearby predators

Escape theory predicts that prey monitoring an approaching predator delay escape until predation risk outweighs costs of fleeing. However, if a predator is not detected until it is closer than the optimal flight initiation distance (FID = distance between predator and prey when escape begins), escape should begin immediately. Similarly, if a change in a nearby predator’s behavior indicates increased risk, the optimal FID increases, sometimes inducing immediate escape. If a predator that has been standing immobile near a prey suddenly turns toward the prey, greater risk is implied than if the predator turns away. If the immobile predator suddenly moves its foot without turning, it might be launching an attack. Therefore, we predicted that frequency of fleeing and preparation to flee are greater when a predator turns toward than away from prey and that frequency of fleeing when a predator suddenly moves decreases as distance between predator and prey increases. We verified these predictions in the Balearic lizard Podarcis lilfordi in field experiments in which an investigator simulated the predator. Lizards fled and performed alerting responses indicating readiness to flee more frequently when the predator turned toward than away from them, and fled more frequently the nearer the predator.     

The evolution of rates of successful and unsuccessful predation

Summary The question, how will evolutionary change in a predator or in its prey change the ratio of the rate of successful captures to the rate of unsuccessful capture attempts is addressed. I argue that this ratio is not a good index of the predator's adaptation to prey capture, because decreased costs of capture attempts or increased assimilation efficiency (both favored by natural selection in the predator) will usually reduce the ratio. In addition, the evolution of increased ability to capture prey may lead to a reduction in the success/failure ratio. Analysis of several simple models suggests that this result is robust. The presence of unsuccessful predation does have an important influence on the evolution of predator traits that increase its rate of encounter with the prey; the presence of unsuccessful predation may cause the predator to increase its adaptations for prey detection in response to an increase in the prey's ability to avoid detection.     

Effects of adaptive predatory and anti-predator behaviour in a two-prey—one-predator system

Summary Two prey populations that share a common predator can interact indirectly by causing changes in the predator's foraging behaviour. Previous work suggests that adaptive choice of prey by the predator usually has two related consequences: (i) the predation rate on a particular prey species increases with the relative and/or absolute abundance of that prey; and (ii) increases in either prey population produce a short-term increase in the fitness of the other prey (short-term indirect mutualism between prey). This paper investigates how these two consequences are changed if the prey exhibit adaptive anti-predator behaviour. In this case, the predation rate on a particular prey often decreases as the prey's density increases. The predator then usually exhibits negative switching between prey. However, the presence of adaptive antipredator behaviour does not change the short-term mutualism between prey. In this case, as a prey becomes less common, it achieves a larger growth rate by reducing its anti-predator effort. These results imply that observations of the relationship between prey density and predation rate cannot be used to infer the nature of the behavioural indirect effect between prey that share a predator.     

Scale dependent effects of predatory fish on stream benthos

In open predation experiments the effects of predators on prey densities can be influenced by predator consumption and by prey movements in to and out of experimental arenas. A published model predicts that the predator effects observed in such experiments are scale dependent over the scale range where there is a transition from movement control (of prey densities) to consumption control. The scale dependence follows from the assumption that per capita rate of emigration out of an experimental arena decreases with increasing arena size.
To test this model the effects of a small benthic fish ( Cottus gobio ) on densities of stream invertebrates was investigated in instream channels of different length (0.5, 2 and 8 m). The effect of fish predation was scale dependent for four prey taxa. For three of these taxa predator effects increased with experimental scale, which is in agreement with model predictions. However, this proved to be a case of "making the right prediction for the wrong reason" as the basic assumption of scale dependent emigration rate was not upheld. By analyzing the behaviour of the model, parameterized with emigration and consumption rates observed in the experimental channels, it was found that observed scale effects occurred because prey emigration in response to the predator treatment was modified by the experimental scale. Further analysis of the parameterized model suggested that the densities of most prey taxa were controlled by prey movements and not by consumption by the sculpins.     

Interspecific infanticide deters predators

It is well known that young, small predator stages are vulnerable to predation by conspecifics, intra-guild competitors or hyperpredators. It is less known that prey can also kill vulnerable predator stages that present no danger to the prey. Since adult predators are expected to avoid places where their offspring would run a high predation risk, this opens the way for potential prey to deter dangerous predator stages by killing vulnerable predator stages. We present an example of such a complex predator–prey interaction. We show that (1) the vulnerable stage of an omnivorous arthropod prey discriminates between eggs of a harmless predator species and eggs of a dangerous species, killing more eggs of the latter; (2) prey suffer a minor predation risk from newly hatched predators; (3) adult predators avoid ovipositing near killed predator eggs, and (4) vulnerable prey near killed predator eggs experience an almost fourfold reduction of predation. Hence, by attacking the vulnerable stage of their predator, prey deter adult predators and thus reduce their own predation risk. This provides a novel explanation for the killing of vulnerable stages of predators by prey and adds a new dimension to anti-predator behaviour.     

Diet of a polyphagous arthropod predator affects refuge seeking of its thrips prey

Antipredator behaviour of prey costs time and energy, at the expense of other activities. However, not all predators are equally dangerous to all prey; some may have switched to feeding on another prey species, making them effectively harmless. To minimize costs, prey should therefore invest in antipredator behaviour only when dangerous predators are around. To distinguish these from harmless predators, prey may use cues related to predation on conspecifics, such as odours released by a predator that has recently eaten conspecific prey or alarm pheromones released by attacked prey. We studied refuge use by a herbivorous/omnivorous thrips, Frankliniella occidentalis, in response to odours associated with a generalist predatory bug, Orius laevigatus, fed either with conspecific thrips or with other prey. The refuge used by thrips larvae is the web produced by its competitor, the two-spotted spider mite, Tetranychus urticae, where thrips larvae experience lower predation risk because the predatory bug is hindered by the web. Thrips larvae moved into this refuge when odours associated with predatory bugs that had previously fed on thrips were present, whereas odours from predatory bugs that had fed on other prey had less effect. We discuss the consequences of this antipredator behaviour for population dynamics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Risk‐taking and the evolution of mechanisms for rapid escape from predators

Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human. This behavioural measure of risk‐taking reflects the risk of being captured by real predators, and it correlates with a range of life history traits, as expected if flight distance optimizes risk of predation. Given that FID provides information on risk of predation, we should expect that physiological and morphological mechanisms that facilitate flight and escape predict interspecific variation in flight distance. Haematocrit is a measure of packed red blood cell volume and as such indicates the oxygen transport ability and hence the flight muscle contracting reaction of an individual. Therefore, we predicted that species with short flight distances, that allow close proximity between a potential prey individual and a predator, would have high haematocrit. Furthermore, we predicted that species with large wing areas and hence relatively low costs of flight and species with large aspect ratios and hence high manoeuvrability would have evolved long flight speed. Consistent with these predictions, we found in a sample of 63 species of birds that species with long flight distances for their body size had low levels of haematocrit and large wing areas and aspect ratios. These findings provide evidence consistent with the evolution of risk‐taking behaviour being underpinned by physiological and morphological mechanisms that facilitate escape from predators and add to our understanding of predator–prey coevolution.     

Plesiomorphic Escape Decisions in Cryptic Horned Lizards (Phrynosoma) Having Highly Derived Antipredatory Defenses

Escape theory predicts that the probability of fleeing and flight initiation distance (predator–prey distance when escape begins) increase as predation risk increases and decrease as escape cost increases. These factors may apply even to highly cryptic species that sometimes must flee. Horned lizards (Phrynosoma) rely on crypsis because of coloration, flattened body form, and lateral fringe scales that reduce detectability. At close range they sometimes squirt blood‐containing noxious substances and defend themselves with cranial spines. These antipredatory traits are highly derived, but little is known about the escape behavior of horned lizards. Of particular interest is whether their escape decisions bear the same relationships to predation risk and opportunity costs of escaping as in typical prey lacking such derived defenses. We investigated the effects of repeated attack and direction of predator turning on P. cornutum and of opportunity cost of fleeing during a social encounter in P. modestum. Flight initiation distance was greater for the second of two successive approaches and probability of fleeing decreased as distance between the turning predator and prey increased, but was greater when the predator turned toward than away from a lizard. Flight initiation distance was shorter during social encounters than when lizards were solitary. For all variables studied, risk assessment by horned lizards conforms to the predictions of escape theory and is similar to that in other prey despite their specialized defenses. Our findings show that these specialized, derived defenses coexist with a taxonomically widespread, plesiomorphic method of making escape decisions. They suggest that escape theory based on costs and benefits, as intended, applies very generally, even to highly cryptic prey that have specialized defense mechanisms.     

Turbidity amplifies the non‐lethal effects of predation and affects the foraging success of characid fish shoals

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Does prey preference change as a result of prey species being presented together? Analysis of prey selection by the predatory mite Typhlodromus pyri (Acarina: Phytoseiidae)

Summary Prey-selection behaviour of the phytoseiid mite Typhlodromus pyri Scheuten was analysed with a Markovtype model of feeding-state dynamics and feeding-state dependent searching behaviour (Sabelis 1981, 1986, 1989; Metz and Van Batenburg 1985a, b). All behavioural characteristics of the predator which are independent of the feeding state were represented by one parameter. The remaining feeding-state dependent characteristics were represented by a function of the feeding state, with one parameter. The best parameter values to describe a predator-prey interaction were determined by fitting the model to the predation rates in monocultures. Under the assumption that the parameter values are not dependent on the composition of prey species supply, the diet of the predators in mixed cultures was predicted from parameters estimated in monoculture experiments.Two prey types, apple rust mite (Aculus schlechtendali (Nalepa)) adults and European red spider mite (Panonychus ulmi (Koch)) larvae were studied. A large discrepancy was observed between calculated and experimentally determined predation rates of T. pyri in mixed cultures: the predators actually killed 3–7 times more P. ulmi larvae than was predicted by the model.The large difference between observed and predicted predation rates in mixed cultures cannot be explained by changes in the behaviour of the prey species as a result of being together. Therefore, it seems likely that the prey selection behaviour of the predator was different when prey species were presented together than when presented singly. Apparently the predatory mite T. pyri prefers P. ulmi to S. schlechtendali.     

Anti-predator behaviour changes following an aggressive encounter in the lizard Tropidurus hispidus

Avoiding predators may conflict with territorial defence because a hiding territorial resident is unable to monitor its territory or defend it from conspecific intrusions. With persistent intruders, the presence of an intruder in the near past can indicate an increased probability of future intrusions. Therefore, following a conspecific-intrusion, territorial residents should minimize costs from future intrusions at the cost of higher predation risks. I conducted experiments with males of the territorial lizard Tropidurus hispidus recording approach distance (distance between predator and prey when the prey escapes) and time to re-emergence from a refuge after hiding. Past aggressive interactions affected anti-predator behaviour: lizards re-emerged sooner (compared to a control) when the predator attacked 5 min after an aggressive encounter. If the predator attacked while an aggressive encounter was ongoing, there was also a reduction in approach distance. The results are consistent with an economic hypothesis which predicts that T. hispidus incur greater predation risks to minimize future territorial intrusion; additionally they show that the effects of past and ongoing aggressive interactions are different, consistent with the minimization of present intrusion costs. These results are relevant for studies of the changes in aggressive behaviour due to changes in the social environment and for studies of the costs and (co) evolution of aggressive and anti-predator strategies.     

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 cichlid Cichlasoma 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. Copyright 1999 The Association for the Study of Animal Behaviour.     

Intraguild Interactions Between the Predatory Mites Neoseiulus californicus and Phytoseiulus persimilis

Species at the same trophic level may interact through competition for food, but can also interact through intraguild predation. Intraguild predation is widespread at the second and third trophic level and the effects may cascade down to the plant level. The effects of intraguild predation can be modified by antipredator behaviour in the intraguild prey. We studied intraguild predation and antipredator behaviour in two species of predatory mite, Neoseiulus californicus and Phytoseiulus persimilis, which are both used for control of the two-spotted spider mite in greenhouse and outdoor crops. Using a Y-tube olfactometer, we assessed in particular whether each of the two predators avoids odours emanating from prey patches occupied by the heterospecific predator. Furthermore, we measured the occurrence and rate of intraguild predation of different developmental stages of P. persimilis and N. californicus on bean leaves in absence or in presence of the shared prey. Neither of the two predator species avoided prey patches with the heterospecific competitor, both when inexperienced with the other predator and when experienced with prey patches occupied by the heterospecific predator. Intraguild experiments showed that N. californicus is a potential intraguild predator of P. persimilis. However, P. persimilis did not suffer much from intraguild predation as long as the shared prey was present. This is probably because N. californicus prefers to feed on two-spotted spider mites rather than on its intraguild prey.     

Interpopulational differences in the use of the Tit-For-Tat strategy during predator inspection in the guppy,Poecilia reticulata

Summary Prior work (Dugatkin, 1991a) has argued that guppies, originating from an area of high predation pressure, employ the Tit-For-Tat strategy during predator inspection visits. Guppies from the high predation site show all three characteristics associated with Tit-For-Tat; nice, retaliatory and forgiving behaviour. Since predation is the major selective force favouring Tit-For-Tat during predator inspection, we predicted fish from an area of low predation would not display the Tit-For-Tat strategy. Our results confirm this prediction; males display retaliatory, but not nice and forgiving behaviour, while females display none of the three characteristics. Thus as predation pressure changes, so too does the conditional nature of the cooperative strategy used during predator inspection.