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Anthropogenic noise pollution is recognized as a major global stressor of animals. While many studies have assessed the unimodal impacts of noise pollution with a focus on intraspecific acoustic communication, little is known about noise pollution on the perception of visual and chemical information. The 'distracted prey hypothesis' posits that processing noise interferes with processing other information in the brain. Here, we found evidence for such a cross-modal effect of noise on the antipredator behaviour of a freshwater prey fish, the fathead minnow, Pimephales promelas. In laboratory trials, exposure to noise from a motorboat caused the total absence of the classical fright reaction of minnows to conspecific alarm cues, whereas an ambient noise control had no such impact. In natural habitats, the impairment of such antipredator behaviour due to noise pollution could have major fitness consequences. We discuss how our findings translate to animal ecology and the need for future studies that target specific management decisions regarding noise pollution.

Recent studies have documented that exposure to high levels of background risk can induce neophobic predator avoidance in prey animals, whereby they respond to any novel cue with an anti-predator response. Such phenotypically plastic predator avoidance may allow prey to maximize anti-predator benefits in variable risk environments. It remains poorly understood whether risk assessment information from different sensory modalities can be integrated to induce generalized, cross-sensory system neophobic responses. Here, we directly test this hypothesis by exposing juvenile convict cichlids (Amatitlania nigrofasciata) to high- versus low-risk environments using either conspecific alarm cue (chemosensory risk) or a model avian predator (visual/mechanical risk) and testing their response to a novel chemosensory cue (Experiment 1) or visual cue (Experiment 2). Our results suggest that regardless of the sensory modality used to increased perceived risk, cichlids pre-exposed to high-risk conditions exhibited increased predator avoidance in response to any novel visual or chemical cue. As expected, cichlids pre-exposed to low-risk conditions did not display any neophobic responses. Our results suggest that induced neophobia is not cue specific; rather, it may function as a generalized response to perceived predation risk.

Exposure to conditions of elevated predation risk, even for relatively short periods, has been shown to induce neophobic responses to novel predators. Such phenotypically plastic responses should allow prey to exhibit costly anti-predator behaviour to novel cues only in situations where the risk of predation is high. While there is evidence that the level of background risk shapes the strength of induced neophobia, we know little about how long neophobic responses are retained. Here we exposed juvenile convict cichlids (Amatitlania nigrofasciata) to three background levels of short-term background risk and then tested their responses to novel predator odours. Cichlids exposed to low risk did not show neophobic responses, while those exposed to intermediate and high risk did. Using extinction trials, we demonstrate that the retention of neophobic responses is greater among cichlids exposed to high versus intermediate predation risk conditions. Moreover, we found much longer retention of the neophobic responses when cichlids were tested a single time compared to when they were tested repeatedly in the extinction trials. This work supports the prediction that neophobic responses to specific odours are relatively long lasting but can quickly wane if the cues are experienced repeatedly without them being associated with risk. It is clear that background level of risk and the frequency of exposure to novel cues are crucial factors in determining the retention of risk-related information among prey.

Within aquatic ecosystems, chemosensory cues provide valuable public information regarding the form and degree of risk, allowing prey to make informed behavioural decisions. Such cues, however, may vary in both relative concentration detected (i.e. 'quantity') and reliability of the information available (i.e. 'quality'), leading to varying response patterns. Moreover, prey species are also known to exhibit consistent behavioural tactics towards managing risk (i.e. personality), possibly shaping their use of public information. Here, we present two experiments examining the potential interacting effects of personality and the quantity (Experiment 1) or quality (Experiment 2) of public information on the short-term predator avoidance responses of wild-caught Trinidadian guppies under semi-natural conditions. Our first experiment demonstrated that personality shaped responses to a high concentration of alarm cues (high risk), with shyer guppies exhibiting stronger antipredator responses than bolder guppies. When exposed to either low risk or stream water controls, personality had no effect on the intensity of response. Our second experiment demonstrated that personality again shaped the response to high concentrations of alarm cues (a known risk) but not to a novel chemosensory cue (tilapia odour). When exposed to the unknown novel cue, guppies exhibited a relatively high intensity antipredator response, regardless of personality. Combined, our results suggest that individual risk-taking tactics shape the use of public information in a context-dependent fashion.

Due to the high variability in predation risk through space and time, prey have to continuously update information about the risk level posed by predators. Despite numerous studies focusing on temporal risk assessment, we know very little about how individuals deal with information regarding changes in risk level of a given predator through time. In this study, we conditioned tadpoles to recognize a predator as a high or low risk twice 2 weeks apart, in a 2 × 2 design. We tested the responses of the tadpoles 1 and 11 days after each conditioning event. Prey showed responses to the predator 1 day after the first conditioning, but the low-risk group failed to respond to the predator after 11 days. However, we found that information learned during the first conditioning affected the response to the predator after the second conditioning, indicating that prey do not 'forget' old information, but simply ignore it. Moreover, tadpoles were able to assess their change in vulnerability over the 2-week period and further extrapolate the risk level of the predator through time to display adaptive threat-sensitive antipredator responses. Our study highlights the complex decision-making that prey use to assess temporal fluctuation in predation risk.

Due to the highly variable nature of predation risk, prey animals need to continuously collect information regarding the risk posed by predators. One question that ensues is how long to use this information for? An adaptive framework of predator-related information use predicted that certainty should influence the duration for which information regarding the threatening nature of a species is used in decision-making. It predicts that uncertainty contributes to the reduction in the duration of information use, due to the cost of displaying antipredator behaviours towards non-threatening species. Here, we test this prediction using repetition of conditioning events as a way to increase the certainty associated with the predatory nature of a novel salamander for woodfrog tadpoles. Tadpoles were conditioned 1, 2 or 4 times to recognize a novel salamander as a predator and subsequently tested for their response to the salamander 1 day or 11 days post-conditioning. We found that conditioning repetition did not affect the intensity with which tadpoles learned to respond to the salamander after 1 day. However, after 11 days, tadpoles with fewer conditionings responded to the salamander with a weaker intensity than those that received more conditionings. Our results provide support for the model prediction that an increase in the certainty associated with correctly identifying a predator leads to longer retention of the threat.

Predators use a variety of information sources to locate potential prey, and likewise prey animals use numerous sources of information to detect and avoid becoming the meal of a potential predator. In freshwater environments, chemosensory cues often play a crucial role in such predator/prey interactions. The importance of chemosensory information to teleost fish in marine environments is not well understood. Here, we tested whether coral reef fish predators are attracted to damage-released chemical cues from already wounded prey in order to find patches of prey and minimize their own costs of obtaining food. Furthermore, we tested if these chemical cues would convey information about status of the prey. Using y-maze experiments, we found that predatory dottybacks, Pseudochromis fuscus, were more attracted to skin extracts of damselfish, Pomacentrus amboinensis, prey that were in good condition compared to prey in poor body condition. Moreover, in both the laboratory and field, we found that predators could differentiate between skin extracts from prey based on prey size, showing a greater attraction to extracts made from prey that were the appropriate size to consume. This suggests that predators are not attracted to any general substance released from an injured prey fish instead being capable of detecting and distinguishing relatively small differences in the chemical composition of the skin of their prey. These results have implications for understanding predator foraging strategies and highlights that chemical cues play a complex role in predator-prey interactions in marine fish.

Despite the fact that the ability of animals to avoid being consumed by predators is influenced by their behaviour, morphology and life history, very few studies have attempted to integrate prey responses across these adaptation types. Here, our goal was to address the link between life-history traits (size and growth trajectory) of tadpoles and behavioural responses to predators. Specifically, we wanted to determine whether information learned about predators was influenced by prey growth trajectory before and after learning. We manipulated the size/growth trajectory of tadpoles by raising them under different temperatures. Tadpoles raised on a slow-growth trajectory (under cold conditions) and taught to recognize a salamander subsequently showed stronger responses after 2 weeks than tadpoles that were raised on a fast-growth trajectory (under warm conditions). When we account for the effect of size (r (2)=0.22) on the responses of prey to predator cues, we find that the growth trajectory pre-learning but not post-learning influences the learned responses of the tadpoles. The differences in responses to predators may reflect differential memory associated with the predator. To our knowledge, this is the first study that has attempted to link life-history traits (size and growth rate) with learning of predators. In order to gain a comprehensive understanding of antipredator responses of prey animals, we call for additional integrative studies that examine prey anti-predator responses across adaptation types., (© Springer-Verlag 2011)

In communities of high biodiversity, the ability to distinguish predators from non-predators is crucial for prey success. Learning often plays a vital role in the ability to distinguish species that are threatening from those that are not. Many prey animals learn to recognise predators based on a single conditioning event whereby they are exposed to the unknown predator at the same time as alarm cues released from injured conspecifics. The remarkable efficiency of such learning means that recognition mistakes may occur if prey inadvertently learn that a species is a predator when it is not. Latent inhibition is a means by which prey that are pre-exposed to an unknown species in the absence of negative reinforcement can learn that the unknown animal is likely not a threat. Learning through latent inhibition should be conservative because mistakenly identifying predators as non-predators can have fatal consequences. In this study, we demonstrated that a common coral reef fish, lemon damselfish, Pomacentrus moluccensis can learn to recognise a predator as non-threatening through latent inhibition. Furthermore, we showed that we could override the latent inhibition effect by conditioning the prey to recognise the predator numerous times. Our results highlight the ability of prey fish to continually update the information regarding the threat posed by other fishes in their vicinity.

A fundamental prerequisite for prey to avoid being captured is the ability to distinguish dangerous stimuli such as predators and risky habitats from non-dangerous stimuli such as non-predators and safe locations. Most research to date has focused on mechanisms allowing prey to learn to recognize risky stimuli. The paradox of learned predator recognition is that its remarkable efficiency leaves room for potentially costly mistakes if prey inadvertently learn to recognize non-predatory species as dangerous. Here, we pre-exposed embryonic woodfrogs, Rana sylvatica, to the odour of a tiger salamander, Ambystoma tigrinum, without risk reinforcement, and later try to teach the tadpoles to recognize the salamander, a red-bellied newt Cynops pyrrhogaster-a closely related amphibian, or a goldfish, Carassius auratus, as a predator. Tadpoles were then tested for their responses to salamander, newt or fish odour. Pre-exposure to salamander did not affect the ability of tadpoles to learn to recognize goldfish as a predator. However, the embryonic pre-exposure to salamanders inhibited the subsequent learning of salamanders as a potential predator, through a mechanism known as latent inhibition. The embryonic pre-exposure also prevented the learned recognition of novel newts, indicating complete generalization of non-predator recognition. This pattern does not match that of generalization of predator recognition, whereby species learning to recognize a novel predator do respond, but not as strongly, to novel species closely related to the known predator. The current paper discusses the costs of making recognition mistakes within the context of generalization of predators and dangerous habitats versus generalization of non-predators and safe habitats and highlights the asymmetry in which amphibians incorporate information related to safe versus risky cues in their decision-making. Mechanisms such as latent inhibition allow a variety of prey species to collect information about non-threatening stimuli, as early as during their embryonic development, and to use this information later in life to infer the danger level associated with the stimuli.

Larval red-legged frogs (Rana aurora) are known to exhibit antipredator behavior in response to both chemical alarm cues released from injured conspecifics and chemical cues of predators. In some cases, the response to predators is dependent on the predator's diet. In this experiment, we tested whether long-term exposure to predator chemical cues and alarm cues resulted in alteration of life history characteristics of red-legged frogs. We raised groups of tadpoles in the presence of chemical cues of predators that were either fed conspecifics or heterospecific caddis-fly larvae, chemical cues of injured conspecifics, or a no-cue control. Tadpoles raised in the presence of either a predator fed conspecifics or cues of injured conspecifics metamorphosed earlier and at a smaller size than those exposed to predators fed heterospecifics or the no-cue control. The result suggests that red-legged frogs exhibit a life history shift in response to predatory cues and that this response is dependent on the diet of predators.

A wide diversity of aquatic organisms release chemical alarm cues when captured by a predator. For most animals, it is not known whether the specific chemicals that comprise the alarm cue are conserved as prey animals age. In this study, we tested whether brook char (Salvelinus fontinalis) can differentiate alarm cues produced by individuals of different ages/sizes. In separate laboratory experiments we exposed small brook char and large brook char to chemical alarm cues from small brook char, large brook char, and a control of swordtails (Xiphophorus helleri). Both small and large brook char responded with antipredator behavior to chemical alarm cues from both small and large char, but not to those from swordtails. Small char responded with a greater response intensity to cues of small char than to cues of large char. In contrast, large char responded with a greater response intensity to cues of large char than to cues of small char. These results suggest that chemical(s) that act as the alarm cue for fish of different age/size classes may be: (1) identical and that there may be other chemical(s) that allow the test fish to distinguish between cues from fish of different ages/sizes, or (2) the cues are not identical, but similar enough to be recognized.

In this study we conditioned fathead minnows (Pimephales promelas) to recognize the odor of a perch (Perca flavescens) by exposing them to perch odor coupled with minnow alarm cue. We then staged encounters between the predator and prey in order to assess whether the predator odor training had any effect on survival of the prey. We tested for a survival effect in the presence and absence of shelter. Our results indicate that fish trained with alarm signals to recognize predators gained a survival benefit during staged encounters with a predator and that habitat characteristics influenced the survival of conditioned fish.

Brook charr (Salvelinus fontinalis) lay their eggs in gravel nests called redds. The nests are not defended for extended periods and the eggs and young may be subject to predation from predators that travel through the substrate into the redd. In this study we tested whether long-term exposure of brook charr eggs to chemical cues from predatory sculpins (Cottus cognatus) resulted in an adaptive shift in the timing of emergence of charr alevins from artificial redds. We reared brook charr eggs in the presence of chemical cues from sculpins fed brook charr eggs, sculpins fed brine shrimp, and a well water control. Significantly more alevins emerged during the first week of the emergence period when exposed to chemical cues from sculpins fed eggs than from cues from sculpins fed brine shrimp or from well water. Alevins that emerged sooner were smaller and possessed larger yolk sacs than alevins that emerged later in the emergence period. Our results suggest that alevins that emerge sooner may escape predation in the redd, but may pay a cost in being under-developed upon emergence into the open water of the stream or lake.

Bullfrogs (Rana catesbeiana), native to eastern North America, were introduced into Oregon in the 1930's. Bullfrogs are highly efficient predators that are known to eat a variety of prey including other amphibians. In laboratory experiments, we investigated whether juvenile Pacific treefrogs (Hyla regilla) recognize adult bullfrogs as a predatory threat. The ability of prey animals to acquire recognition of an introduced predator has important implications for survival of the prey. We found that treefrogs from a population that co-occurred with bullfrogs showed a strong avoidance of chemical cues of bullfrogs. In contrast, treefrogs from a population that did not co-occur with bullfrogs, did not respond to the bullfrog cues. Additional experiments showed that both populations of treefrogs use chemical cues to mediate predation risk. Treefrogs from both populations avoided chemical alarm cues from injured conspecifics.

A wide diversity of fishes possess chemical alarm signalling systems. However, it is not known whether the specific chemicals that act as alarm signals are conserved within most taxonomic groups. In this study we tested whether cross-species responses to chemical alarm signals occurred within salmonid fishes. In separate laboratory experiments, we exposed brook charr (Salvelinus fontinalis), brown trout (Salmo trutta), and rainbow trout (Oncorhynchus mykiss) to chemical alarm signals from each of the three salmonid species and from swordtails (Xiphophorus helleri). In each case, the test species responded with appropriate antipredator behavior to all three salmonids alarm cues, but did not react to swordtail cues. These data suggest that chemical alarm cues are partially conserved within the Family Salmonidae. For each species tested, the intensity of the response was stronger to conspecific alarm cues, than to heterospecific alarm cues, indicating that salmonids could distinguish between chemical cues of conspecifics versus heterospecifics. These results suggest that the chemical(s) that act as the alarm cues may be: 1) identical and that there may be other chemical(s) that allow the test fish to distinguish between conspecifics and heterospecifics, or 2) that the cues that act as signals are not identical, but are similar enough to be recognized.

Previous studies have examined abiotic and biotic factors that facilitate agonistic behavior. For larval amphibians, food availability and conspecific density have been suggested as important factors influencing intraspecific aggression and cannibalism. In this study, we examined the separate and combined effects of food availability and density on the agonistic behavior and life history of larval long-toed salamanders, Ambystoma macrodactylum. We designed a 2×2 factorial experiment in which larvae were raised with either a high or low density of conspecifics and fed either a high or low level of food. For each treatment, we quantified the amount of group size variation, biting, and cannibalism occurring. Additionally, we examined survival to, time to and size at metamorphosis for all larvae. Results indicated that differences in both density and food level influenced all three life history traits measured. Moreover, differences in food level at which larvae were reared resulted in higher within-group size variation and heightened intraspecific biting while both density and food level contributed to increased cannibalism. We suggest that increased hunger levels and an uneven size structure promoted biting among larvae in the low food treatments. Moreover, these factors combined with a higher encounter rate with conspecifics in the high density treatments may have prompted larger individuals to seek an alternative food source in the form of smaller conspecifics.

Slimy sculpins (Cottus cognatus) are small benthic fish that commonly co-occur with predatory fishes throughout most of their range in North America. In two laboratory experiments we examined the nature and extent of responses of slimy sculpins to chemosensory cues from predatory brook trout (Salvelinus fontinalis) and chemical alarm cues released by conspecific sculpins. Sculpins responded to three different classes of chemical stimuli: (1) cues of predatory brook trout, (2) damage-released alarm cues from conspecific sculpins, and (3) disturbance cues from conspecific sculpins. Sculpins did not distinguish between trout fed different diets; however, the presence of damage-released alarm cues did enhance the intensity of response to the predator chemicals. A histological analysis of the skin of sculpins revealed the presence of large sacciform cells that may act as the source of chemical alarm signals.

We examined the effects of predator diet on the antipredator responses of larval woodfrogs (Rana sylvatica). We found that tadpoles showed stronger responses to fish (Perca flavescens) that were fed tadpoles than those fed invertebrates. Similarly, we found that tadpoles responded more strongly to larval dragonflies (Anax spp.) fed tadpoles than to dragonflies fed invertebrates. The overall intensity of response of tadpoles to fish was much stronger than that to dragonflies. Predator diet effects are not ubiquitous in predator-prey systems. We discuss possible reasons why predator diet effects are seen in some, but not all, predator-prey systems.

Organisms from a wide variety of taxonomic groups possess chemical alarm cues that are important in mediating predator avoidance. However, little is known about the presence of such alarm cues in most amphibians, and in particular terrestrial salamanders. In this study we tested whether adult long-toed salamanders (Ambystoma macrodactylum) showed an avoidance response to stimuli from injured conspecifics. Avoidance of stimuli from injured conspecifics could represent avoidance of a chemical alarm cue or, alternatively, avoidance of a territorial pheromone or conspecific predator odor. Consequently, we also tested whether salamanders avoided stimuli from noninjured conspecifics. Salamanders avoided stimuli from injured but not from noninjured conspecifics. Therefore, we concluded that the response to injured conspecifics represents avoidance of a chemical alarm cue and not avoidance of a territorial pheromone or predator cue. This is the first clear demonstration of chemical alarm signaling by a terrestrial amphibian and the first report of chemical alarm signaling in an ambystomatid salamander. By avoiding an area containing stimuli from injured conspecifics, long-toed salamanders may lower their risk of predation by avoiding areas where predators are foraging.

Fathead minnows (Pimephales promelas) are able to detect conspecific alarm pheromone in the feces of northern pike (Esox lucius) and have been shown to avoid areas labeled with the feces of pike that were fed minnows. The minnows did not avoid areas labeled with the feces of pike that were fed swordtails (Xiphophorous helleri), which lack ostariophysan alarm pheromone. In laboratory experiments, pike fed a diet of minnows localized their defecation away from their foraging area. It has been suggested that in doing so, pike may remove chemical cues that label their foraging area as dangerous to prey species. As yet there has been no conclusive evidence to support this hypothesis. In this experiment, we test the effects of different predator diets on localized defecation by pike. Pike were fed minnows, swordtails, or mice (Mus musculus). Swordtails and mice lack ostariophysan alarm pheromones. Area use and location of feces were recorded. Pike fed minnows spent significantly more time in the home area (i.e., area of the test tank where they were fed) and defecated significantly more often in the opposite end of the tank. Pike fed swordtails also exhibited a significant preference for the home area in area use, while those fed mice showed no such preference. When fed either swordtails or mice, there was no significant difference between the proportion of time spent and proportion of feces in each area of the test tank. These data suggest that pike localize their defecation only when consuming prey items containing alarm pheromone. The current findings support the hypothesis that pike localize their defecation to remove chemical cues from the foraging area of the home range in order to avoid chemically labeling their foraging area as dangerous to prey.

The probability of prey avoiding a predator's attack should increase if the predator's presence is detected at an early stage in the predation sequence. In this study, we tested whether threatened Iowa darters (Etheostoma exile) release disturbance pheromones that warn conspecifics of the presence of predation threat. Pairs of aquaria were visually isolated from one another, but connected chemically by water circulating between them. Darters in one aquarium were observed before and after darters in the other aquarium were chased with a model predator. In control tests, the model was moved in the same manner but there were no darters in the upstream tank. Darters receiving water from threatened fish increased vigilance behavior and decreased movement. Vigilant fish raised their head above the substratum, propping themselves up on their pectoral fins and/or arching their neck dorsally, pointing the snout upward. Exposure to water from disturbed darters suppressed exploratory behavior and resulted in movement by short rapid hops that ended abruptly in a rigid, alert posture. This study suggests that Iowa darters release a disturbance pheromone that can provide conspecifics with an early warning of predation risk.

Brook stickleback (Culaea inconstans) share habitat and predators with cyprinid species, and they exploit the alarm pheromone of fathead minnows (Pimephales promelas) to avoid areas of high predation risk. In this field experiment, we measured the retention and duration of area avoidance by brook stickleback from areas marked with alarm pheromone of fathead minnows. Area avoidance was greatest during the first 2 hr after the source of the alarm pheromone was removed (P<0.05), but after 4 hr, area use was not significantly different from premarking levels. This study shows that brook stickleback: (1) use the alarm pheromone of fathead minnows to avoid high risk areas, (2) continue to avoid locations associated with predation risk after the source of the pheromone has gone, and (3) avoid risky areas temporarily, and resume use of risky areas after 2-4 hr. This behavioral response by stickleback to minnow alarm pheromone could serve to minimize risk of predation.

We conducted a predator bite survey on a population of fathead minnows (Pimephales promelas) considered to be under substantial predation pressure by western plains garter snakes (Thamnophis radix). Scarring, due to failed predation attempts by garter snakes and crayfish (Orconectes virilis), was observed significantly more often in breeding males than in breeding females and nonbreeding minnows. Likely, territorial nest defense under the edges of rocks along the water's edge, a habitat occupied by crayfish and frequented by snakes, caused the breeding males to be differentially vulnerable to predation. Under controlled laboratory conditions, breeding males from this population exhibited an antipredator response to chemical stimuli from live snakes (T. sirtalis andT. radix) significantly more often than breeding female minnows from the same population and breeding minnows of both sexes from a population that was presumed to be under lower predation pressure from snakes.

The detection of a chemical alarm pheromone may allow receivers to avoid areas where a predator has captured the prey's conspecifics. We marked minnow traps with either brook stickleback (Culaea inconstans) skin extract or a control of distilled water and tested whether sticklebacks avoided the skin extract marked traps in a natural habitat. Significantly more sticklebacks were captured in traps marked with control water, thereby demonstrating avoidance of conspecific skin extract. The stickleback captured in traps marked with conspecific extract were significantly smaller than those captured in traps marked with control water, implicating ontogenetic factors (i.e., experience or physiological development) in the development of the response. We also captured significantly fewer finescale dace (Chrosomus neogaeus) and fathead minnows (Pimephales promelas) in traps marked with skin extract. These data suggest that dace and minnows may benefit by avoiding areas where predators have recently captured sticklebacks.

Solitary fathead minnows (Pimephales promelas) were rendered anosmic and exposed to chemical stimuli from a predatory northern pike (Esox lucius) to determine the role of olfaction in the minnow's ability to recognize predators on the basis of chemical stimuli. Anosmic fish did not respond to the pike stimuli with a typical fright reaction, while control fish, with intact olfactory receptors, did. These results demonstrate that the olfactory system is necessary for the ability of fathead minnows to recognize northern pike as a predator and that the gustatory and single-celled chemosensory systems are not sufficient for this recognition in the absence of olfactory input. Olfactory impairment was behaviorally confirmed by exposing minnows to alarm substance (Schreckstoff).