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.     

Effects of relaxed predation pressure on visual predator recognition in the guppy

Many prey species have a genetic predisposition to recognise and respond to predators and can fine-tune their anti-predator behaviour following appropriate experience. Although the Trinidadian guppy ( Poecilia reticulata) has become a model species for the investigation of adaptive behaviour, the extent to which experience mediates predator recognition remains unclear. In this study, we examined the effects of relaxed predation pressure on patterns of anti-predator behaviour in populations differing in evolutionary history. The anti-predator behaviour of wild- and laboratory-born guppies from high- and low-predation localities in Trinidad were compared using three models resembling Crenicichla alta, a dangerous guppy predator, Aequidens pulcher, a less dangerous piscivore, and a snake. Snakes are not known to prey on guppies in Trinidad. Specifically, the following predictions were tested: (1) wild caught fish from the high-predation localities (where guppies co-occur with C. alta and A. pulcher) would respond to the three models according to their perceived level of threat, whereas guppies from the low-predation site would show a reduced response to all of the predator models; (2) high-predation laboratory-reared fish would display a reduced but qualitatively similar response to their wild counterparts; and (3) there would be no behavioural differences between wild- and laboratory-reared low-predation fish. In accordance with these predictions, the results revealed that wild fish originating from high-predation sites responded more strongly to the models than fish from low-predation sites. When reared in the laboratory, guppies from the high-predation population showed a reduced response compared to their wild-caught counterparts, but there was no difference in the behaviour of wild- and laboratory-reared low-predation fish. Model type affected predator inspection behaviour but not schooling tendency, and both wild- and laboratory-reared guppies were more wary of the fish models than the snake. These results suggest that early experience differentially mediates the anti-predator responses of fish from high-risk localities.     

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.     

The role of learning in the acquisition of threat-sensitive responses to predator odours

The supposition that prey animals respond to a predator with an intensity that matches the risk posed by the predator is known as the threat-sensitive predator avoidance hypothesis. Many studies have provided support for this hypothesis; yet, few studies have attempted to determine how such abilities are acquired by prey species. In this study, we investigated whether fathead minnows (Pimephales promelas) could learn to recognize an unknown predator (northern pike, Esox lucius) in such a way that they could match the intensity of their antipredator response with the threat posed by the predator. We exposed pike-naïve minnows to conspecific alarm cues paired with either a high or low concentration of pike odor. The following day, both groups were tested for a response to either high or low concentration of pike odor alone. We found that minnows conditioned with alarm cues paired with a given concentration of pike odor subsequently responded with a higher intensity to higher concentrations of pike odor, and with a lower intensity to lower concentrations of pike odor. These results demonstrate that during a single conditioning trial, minnows learn the identity of the predator in a threat-sensitive manner. Minnows use predator odor concentrations that they experience in subsequent interactions to adjust the intensity of their antipredator behavior.     

Background level of risk determines the intensity of predator neophobia in juvenile convict cichlids

Behavioural ecology is rife with examples of prey animals that are able to adjust the intensity of their anti-predator response to match background risk levels. Often, preys need experience with predators before they will invest in costly anti-predator responses. This means that prey animals often fail to respond to predators during their first encounter. Recently, we have shown that prey raised under high-risk conditions may exhibit avoidance of potential predation cues independent of experience (neophobia). Such phenotypically plastic neophobic predator responses may reduce the initial costs of learning ecologically relevant threats while maintaining sufficient behavioural plasticity to respond to variation in local conditions. Here, we test if induced neophobia results in threat-sensitive behavioural trade-offs in response to a novel chemosensory cue. Our first experiment shows that while juvenile convict cichlids (Amatitlania nigrofasciata) pre-exposed to high (but not low) risk conditions exhibited predator avoidance to a novel odour (rainbow trout, Oncorhynchus mykiss), the response intensity was not influenced by the concentration of trout odour detected. Our second experiment demonstrated that the intensity of anti-predator response towards a novel predator cue was dependent upon the level of background risk. Convict cichlids pre-exposed to high-risk conditions showed stronger responses than those pre-exposed to low-risk conditions, while cichlids pre-exposed to intermediate-risk conditions exhibited intermediate response intensities. Together, these data demonstrate that background levels of risk and not the concentration of novel cues detected shape the induced neophobic response pattern of juvenile convict cichlids.     

Phylogenetic relatedness and ecological interactions determine antipredator behavior

Interspecific recognition of alarm cues among guild members through "eavesdropping" may allow prey to fine-tune antipredator responses. This process may be linked to taxonomic relatedness but might also be influenced by local adaptation to recognize alarm cues from sympatric species. We tested this hypothesis using antipredator responses of a freshwater gastropod Lymnaea stagnalis (L.) to alarm cues from damaged conspecific and 10 heterospecific gastropod species. As predicted, the magnitude of antipredator response decreased significantly with increasing phylogenetic distance, but increased when species were naturally sympatric (defined as species cohabiting in the same water body) with the source population of L. stagnalis. The responses to sympatric species were higher overall, and the relationship between genetic distance and alarm cue response was stronger when tested with sympatric species. This is the first study to demonstrate that population sympatry influences innate antipredator responses to alarm cues from intraguild members and suggests that responses based on phylogenetic relationships can be modified through local adaptation. Such adaptation to heterospecific alarm cues suggests that species could be at a disadvantage when they encounter novel intraguild members resulting from species invasion or range expansion due to a reduction in the presence of reliable information about predation risk.     

Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata)

Because agonistic behaviour can increase an individual's risk of predation, natural selection should favour individuals that modify their behaviour in the face of predation hazard in ways that maximise fitness. We investigated experimentally the effects of an increase in the apparent risk of predation on male-male competition within mixed-sex shoals of the Trinidadian guppy (Poecilia reticulata). We show that males engaged in significantly fewer aggressive interactions with conspecific males in the presence of a fish predator. However, they continued to court and attempt copulations with females at the same rate irrespective of the level of predation risk. In comparison, under predation hazard, female guppies were less responsive sexually and avoided fewer male copulation attempts. Such predator-mediated changes in male-male agonistic interactions and female sexual responsiveness towards males have important implications for the mode and intensity of sexual selection within populations.     

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     

Are all signals the same? Ontogenetic change in the response to conspecific and heterospecific chemical alarm signals by juvenile green sunfish (<Emphasis Type="Italic">Lepomis cyanellus</Emphasis>)

Within aquatic communities, individuals may gain survival benefits by responding to the chemical alarm signals of heterospecific prey guild members. Piscivorous individuals, however, should be selected to use such chemical signals as foraging cues. A variety of centrarchid species, such as largemouth bass (Micropterus salmoides), undergo an ontogenetic change in their response to the chemical alarm cues of heterospecific guild members, switching from antipredator to foraging responses. This ontogenetic shift should occur when potential foraging benefits outweigh any survival advantage gained from an antipredator response. To test this model, we exposed juvenile green sunfish (Lepomis cyanellus) to the skin extracts of conspecifics, a heterospecific prey guild member (finescale dace, Phoxinus neogeaus) or an allopatric heterospecific (green swordtails, Xiphophorus helleri). Juvenile sunfish exhibited a significant positive relationship between standard length and time spent moving and a significant negative relationship between length and time in a spine-erect posture, when exposed to dace skin extract, but not to either swordtail or conspecific skin extracts. Smaller individuals of less than 90 mm standard length (SL) decreased time moving and increased time with spines erect (indicating an antipredator response) while larger individuals (>90 mm SL) increased time moving and decreased time with spines erect (indicating a foraging response), when exposed to dace skin extract. Conversely, juvenile sunfish, regardless of size tested, always exhibited an antipredator response to conspecific skin extract. Sunfish exhibited no change in behaviour in response to swordtail skin extracts. These data further support our model of a threat sensitive trade-off in the response to chemical alarm signals by juvenile centrarchids.     

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.     

Determinants of vigilance behavior in the ring-tailed coati (Nasua nasua): the importance of within-group spatial position

Individuals living in social groups are predicted to live under unequal predation risk due to their spatial location within the group. Previous work has indicated that individuals located at the edge of groups have higher “domains of danger”, thus are more likely to engage in vigilance or antipredator behavior. We studied the determinants of vigilance behavior in two groups of ring-tailed coatis in Iguazu National Park, Argentina. In addition to the expected pattern that coatis were more vigilant at the edge of the group, we found that individuals were particularly vigilant at the front edge of the group. This pattern conforms to predictions of differing predation risk caused by sit-and-wait predators with respect to mobile animal groups. In addition, coatis exhibited less vigilance when the number of neighbors within 5 m and group size increased. Of the three spatial variables tested, within-group spatial position was the most important predictor variable determining vigilance levels. These results confirm that spatial position has major effects on vigilance behavior, and that group directionality is an important factor which should be taken into account when measuring vigilance behavior. Coatis were more vigilant when juveniles less than 6 months old were in the groups. The presence of these young juveniles also affected the relationship between alarm response and vigilance levels. Coatis were more vigilant after strong alarm reactions, but only when young juveniles were not present in the groups. This may indicate that coatis give differential responses to alarm calls depending on the age of the caller. A comparison of antipredator vigilance between coatis and sympatric capuchin monkeys is consistent with the hypothesis that terrestriality leads to higher perceive predation risk for coatis.     

Can the ratio of aromatic skeletons explain cross-species responses within evolutionarily conserved Ostariophysan alarm cues?: testing the purine-ratio hypothesis

Summary. While the response to damage-released chemical alarm cues within the superorder Ostariophysi appears to be highly conserved across species, it is generally observed that the intensity of response to heterospecific alarm cues decreases with increasing phylogenetic distance. Recent studies have demonstrated that purine-N-oxides function as chemical alarm cues within Ostariophyian fishes and that the nitrogen-oxide functional group is conserved as the chief molecular trigger. According to the purine-ratio hypothesis, these cross-species differences may be due to the relative proportion of different carrier compounds associated with the nitrogen-oxide molecular trigger. To test this hypothesis, we exposed glowlight tetras (Hemigrammus erythrozonus, Characidae, Ostariophysi) to one of five synthetic stimuli (hypoxanthine-3-N-oxide (H3NO), pyridine-N-oxide (PNO) or mixed stimuli of 75 % H3NO-25 % PNO, 50 % H3NO-50 % PNO, or 25 % H3NO-75 % PNO), natural conspecific chemical alarm cue or a distilled water control. We quantified changes in shoal cohesion and vertical area use as species typical indicators of an antipredator response. As predicted, response intensity decreased as the ratio of hypoxanthine-3-N-oxide to pyridine-N-oxide decreased and the strongest response was to natural alarm cue. These results suggest that species-specific carrier compounds may account for the well-documented cross-species differences in the response to heterospecific alarm cues within phylogenetically related taxa.     

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.     

Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata)

Previous work has shown that under elevated predation risk, male guppies (Poecilia reticulata) switch from courtship to less conspicuous coercive mating attempts. This behavioural transition is traditionally interpreted as a 'risk-sensitive' response that makes males less conspicuous to predators. However, predation risk leads to behavioural changes (such as schooling and predator inspection) in females that may result in coercive mating attempts being more profitable in high-risk situations. Here, we tested the hypothesis that the switch to coercive mating by male guppies in high-risk situations is mediated by adjustments in female behaviour, rather than directly by the predator. We used replicate models resembling a known guppy predator to simulate predation risk in wild-caught guppies from a high-predation population in Trinidad. Our results revealed that males performed proportionately more coercive mating attempts when presented with a female that had been exposed previously to a model predator compared to when males were paired with non-exposed females. Total mating activity (combined rates of courtship and forced mating attempts) did not differ significantly among the two treatment groups, indicating that overall mating activity is unaffected by predation risk. Importantly, when we subsequently presented both sexes concurrently with a predator model, total mating activity and the proportion of forced mating attempts remained unchanged in the high-risk treatment. Taken together, these results indicate that the transition from courtship to forced mating attempts under elevated predation risk is mediated by changes in female behaviour, which we suggest may favour the use of coercive mating under high predation risk.     

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.     

Swimming performance trade-offs across a gradient in community composition in Trinidadian killifish (Rivulus hartii)

The impacts of predation and competition on life history, behavioral, and morphological traits are well established for many organisms, but effects on locomotor performance have received relatively little attention. We examined variation in sprint speed and critical swimming speed (U(crit), a measure of stamina) in the Trinidadian killifish (Rivulus hartii) across a gradient of ecological communities. R. hartii are located in (1) "high-predation" sites with large, piscine piscivores, (2) "Rivulus-guppy" sites with guppies, and (3) "Rivulus-only" sites with only R. hartii. R. hartii suffer higher mortality in high-predation sites. In Rivulus-guppy sites, population densities are reduced and growth rates increased compared with Rivulus-only sites, which likely represent indirect effects of guppy predation on young R. hartii. We show a significant negative relationship, suggesting a trade-off, between sprint speed and endurance; Rivulus from high-predation sites were faster sprinters but had reduced critical swimming speeds. This trade-off was also apparent in correlations of the nine population means. At the individual level, the correlation was weaker and only significantly negative when all nine populations (three from each site) were pooled and values were not corrected for body size. Sex had a significant effect on U(crit), with females having a lower U(crit), but sexes did not differ in sprint speed. Fish from high-predation sites also exhibited increased tail lengths and fineness ratios compared to sites without large predators. The two low-predation sites showed no statistical differences in locomotor performance or morphology.     

Novel features of an inducible defense system in larval tree frogs (Hyla chrysoscelis)

Organisms in aquatic ecosystems must often tolerate variable environmental conditions, including an uncertain risk of predation. Individuals that can maintain plastic defenses against predation will increase their survival when predators are present, but will not incur the costs of these defenses when the risk of predation is low and the defense is not induced. Larvae of the pond-breeding anuran Hyla chrysoscelis develop a conspicuous phenotype in the presence of predators consisting of a brightly colored tail and a deeper tail fin. In this study, I attempted to identify the source of the chemical signal that induces this defensive morphology in this species. I tested whether metabolites alone, originating from the prey but passing through the predator, were able to induce the same morphological response as the combination of alarm signals released directly by attacked conspecifics, and metabolites. I used morphometric and tail conspicuousness data to assess tadpole response to the perceived risk of predation by larval odonate predators (Anax junius). I also tested whether this inducing cue could be recognized across species by measuring the morphological response of H. chrysoscelis tadpoles exposed to cues emitted when tadpoles of a closely related genus (Pseudacris crucifer) were consumed. Tadpoles exhibited a clean graded response of both overall shape and tail morphology in response to all cues, corresponding to their relative reliability as indicators of a risk of predation. H. chrysoscelis tadpoles were also able to respond to cues emitted when tadpoles of a closely related genus were consumed by predators. These results illustrate that tadpoles of this species are able to respond to metabolites alone without alarm signals, and that interspecific chemical communication is a primary mechanism for predator avoidance in this inducible defense system.     

Different antipredator behaviour in two anuran tadpoles: effects of predator diet

Recent investigations have indicated that animals are able to use chemical cues of predators to assess the magnitude of predation risk. One possible source of such cues is predator diet. Chemical cues may also be important in the development of antipredator behaviour, especially in animals that possess chemical alarm substances. Tadpoles of the common toad (Bufo bufo) are unpalatable to most vertebrate predators and have an alarm substance. Tadpoles of the common frog (Rana temporaria) lack both these characters. We experimentally studied how predator diet, previous experience of predators and body size affect antipredator behaviour in these two tadpole species. Late-instar larvae of the dragonfly Aeshna juncea were used as predators. The dragonfly larvae were fed a diet exclusively of insects, R. temporaria tadpoles or B. bufo tadpoles. R. temporaria tadpoles modified their behaviour according to the perceived predation risk. Depending on predator diet, the tadpoles responded with weak antipredatory behaviour (triggered by insect-fed predators) or strong behaviour (triggered by tadpole-fed predators) with distinct spatial avoidance and lowered activity level. The behaviour of B. bufo in predator diet treatments was indistinguishable from that in the control treatment. This lack of antipredator behaviour is probably related to the effective post-encounter defenses and more intense competitive regime experienced by B. bufo. The behaviour of both tadpole species was dependent on body size, but this was not related to predator treatments. Our results also indicate that antipredator behaviour is largely innate in tadpoles of both species and is not modified by a brief exposure to predators. Received: 22 August 1996 / Accepted after revision: 31 January 1997     

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.     

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.