Sensory complementation and the acquisition of predator recognition by salmonid fishes

Following disturbance, some aquatic prey species release chemicals that act as a warning cue and increase vigilance in nearby conspecifics. Such disturbance cues evoke consistent low intensity anti-predator responses. In contrast, alarm cues from injured conspecifics often evoke stronger intensity responses in prey animals. In this study, we test the sensory complement hypothesis, which suggests that multiple cues act in an additive or synergistic fashion to provide additional information for risk assessment by prey. In the first experiment, we showed that juvenile rainbow trout pre-exposed to disturbance cues respond to a given concentration of damage-released alarm cues with a higher intensity of response than the trout that were pre-exposed to cues from undisturbed conspecifics. The two cues acted in an additive fashion. In the second experiment, we demonstrated that disturbance cues alone were not enough to elicit a conditioned response to the odour of a novel predator. We also showed that while disturbance cues elicit an increase in the response of trout to alarm cues, this increase does not translate into a stronger learned response to the predator when the predator odour is paired with alarm cues. Future studies should take into account sensory complementation to avoid underestimating the responses of prey to predators.     

Learned recognition of novel predator odour by convict cichlid embryos

Predation exerts tremendous selection pressure on all organisms. In this study, we exposed embryos of convict cichlids (Amatitlania siquia) twice daily to one of the following: (1) chemical alarm cues of damaged conspecifics + odour of a novel predator (Polypterus endlicheri), (2) chemical alarm cues of damaged conspecifics + water or (3) blank water. No chemical cues were presented after the eggs hatched. When the larvae were 9 days old (mean total length?=?5.7 mm), they were exposed to either predator odour or water. Those larvae that had been conditioned as embryos on alarm cues + predator odour showed a significant reduction in activity (i.e. anti-predator behavioural response) to predator odour relative to the other treatments. This is the first demonstration of acquired predator recognition by fish embryos.     

Threat-sensitive learning of predators by larval mosquitoes <Emphasis Type="Italic">Culex restuans</Emphasis>

A prerequisite for prey to show adaptive behavioural responses to predators is that the prey has the ability to recognise predators as threats. While predator recognition can be innate in many situations, learning is often essential. For many aquatic species, one common way to learn about predators is through the pairing of a novel predator odour with alarm cues released from injured conspecifics. One study with fish demonstrated that this mode of learning not only allows the prey to recognise the predatory cues as a threat, but also mediates the level of threat associated with the predator cues (i.e. threat-sensitive learning). When the prey is exposed to the novel predator with a high concentration of alarm cues, they subsequently show a high intensity of antipredator response to the predator cues alone. When exposed to the predator with a low concentration of alarm cues, they subsequently show a low-intensity response to the predator cues. Here, we investigated whether larval mosquitoes Culex restuans have the ability to learn to recognise salamanders as a threat through a single pairing of alarm cues and salamander odour and also whether they would learn to respond to salamander cues in a threat-sensitive manner. We conditioned individual mosquitoes with water or a low, medium or high concentration of crushed conspecific cues (alarm cues) paired with salamander odour. Mosquitoes exposed to salamander odour paired with alarm cues and subsequently exposed to salamander odour alone responded to the salamander as a threat. Moreover, the intensity of antipredator response displayed during the conditioning phase matched the response intensity during the testing phase. This is the first demonstration of threat-sensitive learning in an aquatic invertebrate.     

Disturbance cues in freshwater prey fishes: do juvenile convict cichlids and rainbow trout respond to ammonium as an ‘early warning’ signal?

Summary.  Several freshwater invertebrate and vertebrate prey species rely on chemosensory cues, including non-injury released disturbance cues, to assess and avoid local predation threats. The prevailing hypothesis is that a pulse of ammonia released by disturbed or stressed prey functions as the disturbance cue. Here, we test this hypothesis in two phylogenetically distant freshwater prey fishes, convict cichlids and rainbow trout. In our first experiment, we measured NH₄ ⁺ concentration in tanks containing shoals of cichlid or trout before and after exposure to a realistic model predator (or left undisturbed). We failed to find an increase in ambient NH₄ ⁺ concentration for either cichlids or trout. In our second experiment, we exposed cichlids or trout to NH₄ ⁺ at 0.1 or 0.5 mg L⁻¹ (or a distilled water control) and measured the change in antipredator behaviour (time moving, foraging rate and area use). We found no consistent increase in antipredator behaviour in response to NH₄ ⁺. In our third study, we exposed cichlids and trout to the disturbance cues of cichlids or trout (versus the odour of undisturbed donors). We found significant increases in antipredator behaviour, regardless of donor species, for both cichlids and trout. Thus, the results of our first two experiments do not support the hypothesis that ammonium functions as a disturbance cue in prey fishes. However, the results of our final experiment do confirm the use of disturbance cues in convict cichlids and rainbow trout and support that hypothesis that the disturbance cue is indeed some generalized metabolic byproduct.     

The dynamic nature of antipredator behavior: prey fish integrate threat-sensitive antipredator responses within background levels of predation risk

Prey animals often have to face a dynamic tradeoff between the costs of antipredator behavior and the benefits of other fitness-related activities such as foraging and reproduction. According to the threat-sensitive predator avoidance hypothesis, prey animals should match the intensity of their antipredator behavior to the degree of immediate threat posed by the predator. Moreover, longer-term temporal variability in predation risk (over days to weeks) can shape the intensity of antipredator behavior. According to the risk allocation hypothesis, changing the background level of risk for several days is often enough to change the response intensity of the prey to a given stimulus. As the background level of risk increases, the response intensity of the prey decreases. In this study, we tested for possible interactions between immediate threat-sensitive responses to varying levels of current perceived risk and temporal variability in background risk experienced over the past 3 days. Juvenile convict cichlids were preexposed to either low or high frequencies of predation risk (using conspecific chemical alarm cues) for 3 days and were then tested for a response to one of five concentrations (100, 50, 25, 12.5%, or a distilled water control). According to the threat-sensitive predator avoidance hypothesis, we found greater intensity responses to greater concentrations of alarm cues. Moreover, in accordance with the risk allocation hypothesis, we found that cichlids previously exposed to the high background level of risk exhibited a lower overall intensity response to each alarm cue concentration than those exposed to the low background level of risk. It is interesting to note that we found that the background level of risk over the past 3 days influenced the threshold level of response to varying concentrations of alarm cues. Indeed, the minimum stimulus concentration that evoked a behavioral response was lower for fish exposed to high background levels of predation than those exposed to low background levels of predation. These results illustrate a remarkable interplay between immediate (current) risk and background risk in shaping the intensity of antipredator responses.     

Ontogenetic differences in chemical alarm cue production determine antipredator responses and learned predator recognition

How individuals assess, respond and subsequently learn from alarm cues is crucial to their survival and future fitness. Yet this information is not constant through time; many individuals are exposed to different predators throughout their life as they outgrow some predators or move to habitats containing different predators. To maximise overall fitness, individuals should discriminate between different cues and respond and learn from only those that are relevant to their current ontogenetic stage. We tested whether juvenile spiny chromis, Acanthochromis polyacanthus, could distinguish between chemical alarm cues from conspecific donors of different ontogenetic stages and whether the cue ontogenetic stage of the cue donor affected the efficacy of learning about predators. Juveniles displayed a significant antipredator response when conditioned with juvenile chemical alarm cues paired with predator odour but failed to respond when conditioned with predator odour paired with either adult alarm cues or with saltwater. Subsequently, individuals only recognised the predator odour alone as a threat when conditioned with juvenile alarm cues. This demonstrates that prey may be highly specific in how they use information from conspecific alarm cues, selectively responding to and learning from only those cues that are relevant to their developmental stage.     

A review of predator diet effects on prey defensive responses

Numerous studies have examined how predator diets influence prey responses to predation risk, but the role predator diet plays in modulating prey responses remains equivocal. We reviewed 405 predator–prey studies in 109 published articles that investigated changes in prey responses when predators consumed different prey items. In 54 % of reviewed studies, prey responses were influenced by predator diet. The value of responding based on a predator’s recent diet increased when predators specialized more strongly on particular prey species, which may create patterns in diet cue use among prey depending upon whether they are preyed upon by generalist or specialist predators. Further, prey can alleviate costs or accrue greater benefits using diet cues as secondary sources of information to fine tune responses to predators and to learn novel risk cues from exotic predators or alarm cues from sympatric prey species. However, the ability to draw broad conclusions regarding use of predator diet cues by prey was limited by a lack of research identifying molecular structures of the chemicals that mediate these interactions. Conclusions are also limited by a narrow research focus. Seventy percent of reviewed studies were performed in freshwater systems, with a limited range of model predator–prey systems, and 98 % of reviewed studies were performed in laboratory settings. Besides identifying the molecules prey use to detect predators, future studies should strive to manipulate different aspects of prey responses to predator diet across a broader range of predator–prey species, particularly in marine and terrestrial systems, and to expand studies into the field.     

Learning to recognize novel predators under weakly acidic conditions: the effects of reduced pH on acquired predator recognition by juvenile rainbow trout

Summary. Recent studies have demonstrated that under weakly acidic conditions (pH 6.0), many prey fishes, including juvenile rainbow trout (Onchorhynchus mykiss), do not exhibit overt antipredator responses to conspecific chemical alarm cues. In laboratory trials, we investigated the potential effects of reduced pH on the ability of hatchery reared, predator naïve juvenile rainbow trout to acquire the recognition of a novel predator (yellow perch, Perca flavenscens). Initially, we exposed trout to the odour of a predatory yellow perch, buffered to pH 6.0 (weakly acidic) or pH 7.0 (neutral) paired with conspecific skin extracts (also buffered to pH 6.0 or 7.0) or a distilled water control. Juvenile trout exhibited significant increase in antipredator behaviour when exposed to neutral skin extract (pH 7.0). When retested 48 hours later to perch odour alone (pH 7.0), only trout initially conditioned with neutral skin extracts (pairs with either neutral or acidic perch odour) exhibited a learned recognition of perch odour as a predator risk. Those initially exposed to weakly acidic skin extract or the distilled water control did not show a learned response to predator odour. These results demonstrate that the ability to acquire the recognition of novel predators is impaired under weakly acidic conditions, as would occur in natural waterways affected by acidic precipitation.     

Antipredator responses to invasive lionfish, Pterois volitans: interspecific differences in cue utilization by two coral reef gobies

Understanding prey response to predators and their utilization of sensory cues to assess local predation risk is crucial in determining how predator avoidance strategies affect population demographics. This study examined the antipredator behaviors of two ecologically similar species of Caribbean coral reef fish, Coryphopterus glaucofraenum and Gnatholepis thompsoni, and characterized their responses to different reef predators. In laboratory assays, the two species of gobies were exposed to predator visual cues (native Nassau grouper predator vs. invasive lionfish predator), damage-released chemical cues from gobies, and combinations of these, along with appropriate controls. Behavioral responses indicate that the two prey species differ in their utilization of visual and chemical cues. Visual cues from predators were decisive for both species’ responses, demonstrating their relative importance in the sensory hierarchy, whereas damage-released cues were a source of information only for C. glaucofraenum. Both prey species could distinguish between native and invasive predators and subsequently altered their antipredator responses.     

Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner

Under conditions of spatial and/or temporal variability in predation risk, prey organisms often rely on acquired predator recognition to balance the trade-offs between energy intake and risk avoidance. The question of ‘for how long’ should prey retain this learned information is poorly understood. Here, we test the hypothesis that the growth rate experienced by prey should influence the length of the ‘memory window’. In a series of laboratory experiments, we manipulated growth rate of juvenile rainbow trout and conditioned them to recognize a novel predator cue. We subsequently tested for learned recognition either 24 h or 8 days post-conditioning. Our results suggest that trout with high versus low growth rates did not differ in their response to learned predator cues when tested 24 h post-conditioning. However, trout on a high growth rate exhibited no response to the predator cues after 8 days (i.e. did not retain the recognition of the predator odour), whereas trout on a lower growth rate retained a strong recognition of the predator. Trout that differed in their growth rate only after conditioning did not differ in their patterns of retention, demonstrating growth rate after learning does not influence retention. Trout of different initial sizes fed a similar diet (percent body mass per day) showed no difference in retention of the predator cue. Together, these data suggest that growth rate at the time of conditioning determines the ‘memory window’ of trout. The implications for threat-sensitive predator avoidance models are described.     

Threat-sensitive generalization of predator recognition by larval amphibians

Despite the importance of acquired predator recognition in mediating predator–prey interactions, we know little about the specific characteristics that prey use to distinguish predators from non-predators. Recent experiments with mammals and fish indicate that some prey lacking innate predator recognition have the ability to display anti-predator responses upon their first encounter with those predators if they are similar to predators that the prey has recently learned to recognize. This phenomenon is referred to as generalization of predator recognition. In this experiment, we documented for the first time that larval amphibians (woodfrog, Rana sylvatica) have the ability to generalize the recognition of known predators to closely related novel predators. Moreover, we demonstrated that this ability is dependent on the level of risk associated with the known predator. When red-bellied newt, Cynops pyrrhogaster (known predator), was paired with simulated low risk, tadpoles displayed fright responses to newts and novel tiger salamanders, Ambystoma tigrinum, but not to novel African clawed frogs, Xenopus laevis. However, when the newt was paired with simulated high risk, tadpoles generalized their responses to both tiger salamanders and African clawed frogs. Larval anurans seem to have a wider generalization frame than other animals.     

Risk vs. reward: how predators and prey respond to aging olfactory cues

Many animals use olfaction to find food and avoid predators, and must negotiate environments containing odors of varying compositions, strengths, and ages to distinguish useful cues from background noise. Temporal variation in odor cues (i.e., “freshness”) seems an obvious way that animals could distinguish cues, yet there is little experimental evidence for this phenomenon. Fresh cues provide a more reliable indicator of donor presence than aged cues, but we hypothesize that the benefits of responding to aged cues depend on whether the cue indicates the proximity of a predator or a potential meal. As prey cannot remain eternally risk averse in response to predator odor, we predict that antipredator responses should diminish as predator cues age. In contrast, animals searching for food should investigate aged prey cues if investigation costs are sufficiently low and the potential benefit (a meal) sufficiently high; thus, we predict that predators will maintain interest in aged prey cues. We tested these ideas using free-ranging rats (Rattus spp.) in two separate experiments; firstly assessing giving-up densities in the presence of predator odor, and secondly examining investigation rates of prey odors. As predicted, giving-up densities dropped once predator odor had aged, but investigation rates remained similar for aged and fresh prey odor. Thus, rats used temporal variation in odor cues to evaluate the cost–benefit relationship of responding to predator and prey odors. We suggest that the ecological significance of variable cue age needs more research and should be considered when interpreting behavioral responses to olfactory information.     

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.Communicated by A. Mathis     

Performance level and efficiency of two differing predator-avoidance strategies depend on nutritional state of the prey fish

Animal prey has developed a variety of behavioural strategies to avoid predation. Many fish species form shoals in the open water or seek refuge in structurally complex habitats. Since anti-predator strategies bear costs and are energy-demanding, we hypothesised that the nutritional state of prey should modify the performance level and efficiency of such strategies. In aquaria either containing or lacking a structured refuge habitat, well-fed or food-deprived juvenile roach (Rutilus rutilus) were exposed to an open-water predator (pikeperch, Sander lucioperca). Controls were run without predators. In the presence of the predator, roach enhanced the performance of the anti-predator strategy and increased the use of the refuge habitat whereby food-deprived roach were encountered more often in the structure than well-fed roach. Nonetheless more starved than well-fed roach were fed upon by the predator. In the treatments offering only open-water areas, roach always formed dense shoals in the presence of the predator. The shoal density, however, was lower in starved roach. Starving fish in shoals experienced the highest predation mortality across all experimental treatments. The experiment confirmed the plasticity of the anti-predator behaviour in roach and demonstrated that food deprivation diminished the efficiency of shoaling more strongly than the efficiency of hiding. The findings may be relevant to spatial distribution of prey and predator–prey interactions under natural conditions because when prey are confronted with phases of reduced resource availability, flexible anti-predator strategies may lead to dynamic habitat use patterns.     

Variable predation risk and the dynamic nature of mosquito antipredator responses to chemical alarm cues

Summary. Predation is a pervasive selective agent highly variable in space and time. Due to the costs associated with antipredator responses, prey would be at a selective advantage if they respond to predation threats with an intensitfy matching the threat posed by the predator. Many aquatic organisms have been shown to use chemical alarm cues present in the water to assess the level of risk in their environment. This includes mosquito larvae which show antipredator responses to conspecific alarm cues. In this study, we investigated the nature of the responses of larval mosquitoes Culex restuans to those cues. In our initial observations, we showed pond/population differences in the response intensity of C. restuans to alarm cues. In experiment 1, we showed that the response intensity to alarm cues could be increased by increasing the background level of risk in the mosquitoes’ environment (by adding salamander predators) and once turned on, the response intensity to alarm cues was likely maintained for the remainder of the mosquitoes’ aquatic life. In experiments 2 and 3, we investigated if the increase in response intensity to alarm cues was directly correlated with the level of background risk in the mosquitoes’ environment. When given increasing levels of background risk, mosquito larvae subsequently showed a graded response to conspecific alarm cues. This series of experiments demonstrates that the response intensity of larval mosquitoes to a standard concentration of alarm cues is not fixed, but rather dependent on the background level of risk in the environment. An understanding of the background level of risk is particularly important for comparing antipredator responses of prey between habitats.     

The paradox of risk assessment: comparing responses of fathead minnows to capture-released and diet-released alarm cues from two different predators

Summary. Many aquatic prey are known to use chemical alarm cues to assess their risk of predation. In fishes, such alarm cues can be released either through damage of the epidermis during a predatory attack (capture-released) or through release from the predator feces (diet-released). In our study, we compared the importance of capture- versus diet-released alarm cues in risk assessment by fathead minnows (Pimephales promelas) that were na?ve to fish predators. We utilized two different fish predators: a specialized piscivore, the northern pike (Esox lucius) and a generalist predator, the brook trout (Salvelinus fontinalis). Handling time of pike consuming minnows was much shorter than for trout consuming minnows, likely resulting in less epidermal damage to the minnows during attacks by pike. In accordance with this, minnows showed a less intense antipredator response to capture-released cues from pike than capture-released cues from trout. This represents a paradox in risk assessment for the minnows as they respond to the specialized piscivore, the more dangerous predator, with a less intense antipredator response. In contrast, the minnows showed a stronger antipredator response to the specialized piscivore than to the generalist when given diet cues. This work highlights the need for researchers to carefully consider the nature of the information available to prey in risk assessment.     

Provenance and threat-sensitive predator avoidance patterns in wild-caught Trinidadian guppies

The antipredator behaviour of prey organisms is shaped by a series of threat-sensitive trade-offs between the benefits associated with successful predator avoidance and a suite of other fitness-related behaviours such as foraging, mating and territorial defence. Recent research has shown that the overall intensity of antipredator response and the pattern of threat-sensitive trade-offs are influenced by current conditions, including variability in predation risk over a period of days to weeks. In this study, we tested the hypothesis that long-term predation pressure will likewise have shaped the nature of the threat-sensitive antipredator behaviour of wild-caught Trinidadian guppies (Poecilia reticulata). Female guppies were collected from two populations that have evolved under high- and low-predation pressure, respectively, in the Aripo River, Northern Mountain Range, Trinidad. Under laboratory conditions, we exposed shoals of three guppies to varying concentrations of conspecific damage-released chemical alarm cues. Lower Aripo (high-predation) guppies exhibited the strongest antipredator response when exposed to the highest alarm cue concentration and a graded decline in response intensity with decreasing concentrations of alarm cue. Upper Aripo (low-predation) guppies, however, exhibited a nongraded (hypersensitive) response pattern. Our results suggest that long-term predation pressure shapes not only the overall intensity of antipredator responses of Trinidadian guppies but also their threat-sensitive behavioural response patterns.     

Retention of acquired predator recognition among shy versus bold juvenile rainbow trout

The ability to acquire information about predators allows prey to better balance threat-sensitive tradeoffs by responding only to ecologically relevant predation threats. However, predation risk is highly variable through time and responding to predators that no longer represent a threat would likely prove costly to prey. While a wealth of studies have examined the way in which prey learn, little attention has been paid to retention of acquired information. Recent studies suggest that retention is indeed plastic and shaped by a suite of intrinsic factors such as strength of initial conditioning and individual growth rate. Here, we investigated if the duration of retention of acquired information is influenced by individual behavioral tactics (i.e., ‘personality’). We recorded latency to escape an opaque acclimation chamber of juvenile rainbow trout (Oncorhynchus mykiss) as a measure of behavioral tactic. We then immediately conditioned individual trout to recognize pumpkinseed (Lepomis gibbosus) and tested for recognition 24 h or 8 days postconditioning. Our results demonstrate that while shy versus bold trout exhibited no difference in the strength of conditioned response to pumpkinseed odor during conditioning trials or when tested for recognition 24 h postconditioning, there was a significant effect of individual behavioral tactic on the retention of learned predator recognition. While shy trout continued to exhibit a learned response to pumpkinseed odor when tested 8 days postconditioning, bold trout were not different from our pseudoconditioned controls. These data suggest that the behavioral tactic employed at the time of conditioning influences the ‘memory window’ of acquired information.     

Antipredator responses of koomal (Trichosurus vulpecula hypoleucus) against introduced and native predators

Antipredator behavior studies generally assess prey responses to single predator species although most real systems contain multiple species. In multi-predator environments prey ideally use antipredator responses that are effective against all predator species, although responses may only be effective against one predator and counterproductive for another. Multi-predator systems may also include introduced predators that the prey did not co-evolve with, so the prey may either fail to recognize their threat (level 1 naiveté), use ineffective responses (level 2 naiveté) or succumb to their superior hunting ability (level 3 naiveté). We analyzed microhabitat selection of an Australian marsupial (koomal, Trichosurus vulpecula hypoleucus) when faced with spatiotemporal differences in the activity/density levels of one native (chuditch, Dasyurus geoffroii) and two introduced predators (red fox, Vulpes vulpes; feral cat, Felis catus). From this, we inferred whether koomal recognized introduced predators as a threat, and whether they minimized predation risk by either staying close to trees and/or using open or dense microhabitats. Koomal remained close to escape trees regardless of the predator species present, or activity/density levels, suggesting koomal employ this behavior as a first line of defense. Koomal shifted to dense cover only under high risk scenarios (i.e., with multiple predator species present at high densities). When predation risk was low, koomal used open microhabitats, which likely provided benefits not associated with predator avoidance. Koomal did not exhibit level 1 naiveté, although further studies are required to determine if they exhibit higher levels of naiveté (2–3) against foxes and cats.     

Vivid birds respond more to acoustic signals of predators

Because conspicuous morphology such as colorful plumage may increase predation risk, we aimed to see if variation in plumage coloration could explain variation in avian anti-predator behavior. We included several measures of plumage coloration: human perception of vividness from images in field guides, total intensity from reflectance spectra of museum skins, contrasts calculated from physiological models of these spectra parameterized for both raptors and humans, chroma, and spectral saturation. We investigated how well these measurements predicted risk assessment in ten species of birds in St. John, U.S. Virgin Islands. We quantified how each species responded to playbacks of a predator’s calls and compared this response to that elicited by songs from a non-predatory, sympatric bird. We found that human-determined measures of vividness best predicted anti-predator responses of birds—more vividly colored species responded more to predators than duller species. No spectrophotometric variable explained variation in species reactions to a predator call. Our results suggest that vivid birds may compensate for their conspicuousness by being more responsive to the sound of predators and that more work is needed to better evaluate how animal coloration is quantified in comparative studies.