Reehan S. Mirza

Predator Diet Cues and the Assessment of Predation Risk by Aquatic Vertebrates: A Review and Prospectus

Chemosensory assessment of predation risk is widespread in aquatic systems (Chivers and Smith, 1998; Kats and Dill, 1998). Studies completed primarily in the last decade suggest that the level of this assessment is probably much more sophisticated than was previously thought. For example, many prey animals appear to be able to distinguish between predators that are fed different diets. Being able to differentiate that predators are fed different diets means that prey animals can potentially use this information to mediate the intensity of their responses to predators.

Making sense of predator scents: investigating the sophistication of predator assessment abilities of fathead minnows

According to the threat-sensitive predator avoidance hypothesis, selection favors prey that accurately assess the degree of threat posed by a predator and adjust their anti-predator response to match the level of risk. Many species of animals rely on chemical cues to estimate predation risk; however, the information content conveyed in these chemical signatures is not well understood. We tested the threat-sensitive predator avoidance hypothesis by determining the specificity of the information conveyed to prey in the chemical signature of their predator. We found that fathead minnows (Pimephales promelas) could determine the degree of threat posed by northern pike (Esox lucius) based on the concentration of chemical cues used. The proportion of minnows that exhibited an anti-predator response when exposed to a predator cue increased as the concentration of the pike cue used increased. More surprisingly, the prey could also distinguish large pike from small pike based on their odor alone. The minnows responded more intensely to cues of small pike than to cues of large pike. In this predator–prey system small pike likely represent a greater threat than large pike.

Responses of American toad tadpoles to predation cues: behavioural response thresholds, threat-sensitivity and acquired predation recognition

Predation is one of the most important selective forces acting on prey animals. To respond adaptively to predation threats and increase their chances of survival, prey animals have to be able to recognize their potential predators. Even though a few studies demonstrated innate predator recognition, the vast majority of animals have to rely on learning to acquire this information. Often aquatic prey animals can learn to recognize predators when they detect conspecific alarm cues associated with cues from a novel predator. In this study, we exposed American toad (Bufo americanus) tadpoles to varying concentrations of chemical alarm cues (cues from injured conspecifics). We identified a concentration of cues which caused an overt antipredator response (supra-threshold concentration) and a lower concentration for which the prey failed to exhibit a response (sub-threshold concentration). In a second experiment, we attempted to condition the tadpoles to recognize the odour of larval dragonflies (Anax sp.) by pairing the dragonfly odour with either the sub-threshold concentration or the supra-threshold concentration of alarm cues. In both cases, the tadpoles learned to recognize the predator based on this single pairing of alarm cues and predator odour. Moreover, the intensity of the learned response was stronger for tadpoles conditioned with the supra-threshold concentration of alarm cues than the sub-threshold concentration. This is the first documented case of this mode of learning in anuran amphibians. Learned recognition of predators has important implications for survival.

Are Chemical Alarm Cues Conserved Within Salmonid Fishes

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.

LEARNED RECOGNITION OF HETEROSPECIFIC ALARM CUES ENHANCES SURVIVAL DURING ENCOUNTERS WITH PREDATORS

Numerous species of aquatic animals release chemical cues when attacked by a predator. These chemicals serve to warn other conspecifics, and in some cases heterospecifics, of danger, and hence have been termed alarm cues. Responses of animals to alarm cues produced by other species often need to be learned, yet mechanisms of learned recognition of heterospecific cues are not well understood. In this study, we tested whether fathead minnows (Pimephales promelas) could learn to recognize a heterospecific alarm cue when it was combined with conspecific alarm cue in the diet of a predator. We exposed fathead minnows to chemical stimuli collected from rainbow trout, Oncorhynchus mykiss, fed a mixed diet of minnows and brook stickleback, Culaea inconstans, or trout fed a mixed diet of swordtails, Xiphophorous helleri, and stickleback. To test if the minnows had acquired recognition of the heterospecific alarm cues, we exposed them to stickleback alarm cues and introduced an unknown predator, yellow perch (Perca flavescens) or northern pike (Esox lucius). Both perch and pike took longer to initiate an attack on minnows that were previously exposed to trout fed minnows and stickleback than those previously exposed to trout fed swordtails and stickleback. These results demonstrate that minnows can learn to recognize heterospecific alarm cues based on detecting the heterospecific cue in combination with minnow alarm cues in the diet of the predator. Ours is the first study to demonstrate that behavioural responses to heterospecific chemical alarm cues decreases the probability that the prey will be attacked and captured during an encounter with a predator.

Fathead minnows, Pimephales promelas, learn to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans

In four experiments conducted over a 6-year period, we investigated whether fathead minnows, Pimephales promelas, could acquire the ability to recognize chemical alarm cues of introduced brook stickleback, Culaea inconstans. A laboratory experiment documented that stickleback-naïve minnows did not exhibit an anti-predator response when exposed to the chemical alarm cues of stickleback. In a laboratory experiment conducted 5 years after the introduction of stickleback to the pond, minnows exhibited an antipredator response to stickleback cues. Moreover, in a field experiment the minnows exhibited avoidance of areas labelled with stickleback alarm cues. Minnows raised from eggs taken from the test pond did not exhibit an anti-predator response to stickleback cues while minnows from the test pond that had experience with stickleback cues did respond to stickleback cues. Our results provide clear evidence that cross-species responses to chemical alarm cues of fishes can be learned. Learned recognition of alarm cues has important implications for predator/prey interactions.

Juvenile convict cichlids (Archocentrus nigrofasciatus) allocate foraging and antipredator behaviour in response to temporal variation in predation risk

We examined the influence of temporal variation in predation risk on the foraging and antipredator behaviour of juvenile convict cichlids (Archocentrus nigrofasciatus). We exposed fish to one of four treatment regimes: 100% or 20% concentrations of conspecific alarm cue, given once or three times per day, for a period of three days. On the fourth day they were exposed to either 100% conspecific alarm cue or a control of 100% swordtail (Xiphophorus helleri) skin extract. There was no significant effect of concentration of alarm cue, fish previously exposed to the same frequency of risk responded in a similar manner regardless of the concentration of alarm cue previously experienced. Fish that were exposed to predation risk three times per day exhibited moderate intensities of antipredator behaviour during periods of risk and allocated significantly more foraging to periods of safety compared to those exposed to alarm cue once per day. These results demonstrate that temporal variation can influence the trade off between antipredator behaviour and foraging and that prey can use subthreshold cues to assess temporal variability in predation risk.

Brook Char (Salvelinus fontinalis) Can Differentiate Chemical Alarm Cues Produced by Different Age/Size Classes of Conspecifics

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.

Heads up: juvenile convict cichlids switch to threat-sensitive foraging tactics based on chemosensory information

The ability to accurately assess local predation risk is crucial, as it allows prey individuals to maximize trade-offs between predator avoidance and foraging behaviour. Here, we test the hypothesis that juvenile convict cichlids, Archocentrus nigrofasciatus, rely on ambient chemosensory information to make threat-sensitive foraging decisions. In experiment 1, juvenile cichlids were exposed to conspecific chemical alarm cues above or below the threshold required to elicit an overt antipredator response and were allowed to forage on a choice of horizontal (on the substrate) or vertical (perpendicular to the substrate) food patches. Although cichlids exposed to a subthreshold alarm cue did not show an overt antipredator response, they significantly increased their use of the vertical food patch (head-up foraging posture). Cichlids exposed to a suprathreshold alarm cue significantly reduced foraging and aggressive behaviour and shifted to the head-up foraging position. In experiment 2, juvenile cichlids were exposed to the odour of an adult conspecific fed a vegetable diet, or one of two prey fish diets (juvenile cichlids or swordtails, Xiphophorus hellerii), or a distilled water control. Although we found no evidence of an overt antipredator response towards any of the stimuli, cichlids exposed to the odour of predators fed a prey fish diet significantly increased their use of the head-up foraging posture. Our results clearly show that juvenile cichlids are able to adjust their foraging patterns in a threat-sensitive fashion in response to ambient chemosensory information.

Do juvenile yellow perch use diet cues to assess the level of threat posed by intraspecific predators

The mechanisms that drive the evolution of intraspecifc predation (cannibalism) are unclear. Many authors speculate that predators can make substantial gains in nutrition and reproductive output by consuming conspecifics. However, by consuming conspecifics, predators may risk decreasing their inclusive fitness by consuming kin or increasing the chances of pathogen transmission. In fishes intraspecific predation is typically observed when resource levels are low. During these periods it is important for prey fishes to be able to accurately assess their level of predation risk from cannibalistic conspecifics. Prey animals may be able to do this by using chemical cues available in the predators diet. The last meal consumed by the predator may give important information for prey animals to assess predation risk. We exposed juvenile yellow perch, Perca flavescens, to chemical cues of adult perch fed a diet of either juvenile perch, spot tail shiners, Notropis hudsonius, swordtails, Xiphophorus helleri, or a control of distilled water. Spot tail shiners and juvenile perch commonly form mixed species shoals and are vulnerable to the same suite of predators. Swordtails do not co-occur with yellow perch or spot tail shiners. We found that juvenile perch increased shelter use significantly more when exposed to chemical cues of adult perch fed juvenile perch or spot tails, compared to adult perch fed swordtails or those exposed to distilled water. This suggests that the level of chemosensory assessment used by juvenile perch is quite sophisticated and that the antipredator response can be mediated by specific cues in the predators diet. This study is the first to demonstrate a response of a fish to chemical cues from intraspecific predators. Future studies should examine the importance of predator diet cues in responses to chemical cues from intraspecific predators.