Threat-sensitive Predator Avoidance Hypothesis Research Articles

Exploring the threat-sensitive predator avoidance hypothesis on mate competition in two wild populations of Trinidadian guppies

The intensity of mate competition is often influenced by predation pressure. The threat-sensitive predator avoidance hypothesis predicts that prey should precisely adjust their fitness-related activities to the level of perceived acute predation risk and this effect should be stronger under high background risk. Individuals should compensate during periods of moderate risk for lost opportunities during high risk. Our study examined the interaction between acute and background predation risk on mate competition. Under laboratory conditions, we explored the effects of acute risk (low vs. high) using chemical alarm cue (AC; control (results presented in Chuard et al. (2016)) The effects of adult sex ratio on mating competition in male and female guppies (Poecilia reticulata) in two wild populations. Behav Process 129:1−10), 25 % concentration, and 100 % concentration), and population of origin (low vs. high background risk) on mate competition in guppies (Poecilia reticulata). Surprisingly, males favored courtship over forced mating under acute predation risk irrespective of background risk, potentially benefiting from a female preference for bold males. We discuss our results in the context of chemical threat-sensitivity and resource differences in defendability (e.g. mates vs. food).

Do antipredator responses of Euphlyctis cyanophlyctis tadpoles depend on the intensity of predation risk?

Successful coexistence with predators depends on the ability of prey to strike a balance between the costs of predator avoidance and the benefits of foraging and reproducing as there is a trade-off between these activities. Prey animals can balance this trade-off by responding to predation risk in a manner that matches the intensity of risk posed by the predator, which is known as the threat-sensitive predator avoidance hypothesis. To test this hypothesis, we exposed larval Indian skipper frogs (Euphlyctis cyanophlyctis) to different intensities of predation risk by increasing the number of predators and the amount of biomass consumed and recorded their behaviour, morphology, and metamorphic traits. We also quantified the whole-body corticosterone to assess the physiological basis of alterations in morphology, behaviour, and life-history traits. The results indicate that behavioural responses of larval skipper frogs increased with the intensity of risk conforming to the predictions of the threat-sensitivity hypothesis. However, the morphological responses did not vary with the intensity of risk and hence did not support the predictions of the hypothesis. Interestingly, tadpoles facing a higher level of predation risk metamorphosed at the largest size, but with increased larval duration. At the physiological level, corticosterone levels increased with increases in the intensity of risk. Thus, our results suggest that certain antipredator responses may vary with the intensity of risk while others may not. Further, the results of our study also show an association between physiological and behavioural responses of larval E. cyanophlyctis to predation risk. More importantly, we show that larval skipper frogs can assess the intensity of predation risk through threat-sensitive learning by associating conspecific alarm cues with odours of dragonfly nymphs.

To forage or hide? Threat-sensitive foraging behaviour in wild, non-reproductive passerine birds

Abstract Because antipredator behaviours are costly, the threat-sensitive predator avoidance hypothesis predicts that individual animals should express predator-avoidance behaviour proportionally to the perceived threat posed by the predator. Here, we experimentally tested this hypothesis by providing wild passerine birds supplemental food (on a raised feeding platform) at either 1 or 4 m from the edge of forest cover (potential refuge), in either the presence or absence of a nearby simulated predation threat (a sharp-shinned hawk Accipiter striatus model). Compared with the control treatment, we observed proportionally fewer bird visits to the food patch, and the birds took longer to re-emerge from forest refuge and return to feed at the food patch, after the hawk presentation than before it. The observed threat-sensitive latency-to-return response was stronger when the food patch was further away from the nearest refuge. Overall, our results are consistent with the predictions of the threat-sensitive predator avoidance hypothesis in that wild passerine birds (primarily black-capped chickadees Poecile atricapillus) exhibited more intense antipredator behavioural responses with increasing level of apparent threat. The birds were thus sensitive to their local perceived threat of predation and traded-off safety from predation (by refuging) and foraging gains in open habitat in a graded, threat-sensitive manner.

Crabs interpret the threat of predator body size and biomass via cue concentration and diet

Greater predator body size is often associated with greater predation risk. According to the threat-sensitive predator avoidance hypothesis, prey should display graded responses to increasing predator body size; in turn, these differences in behaviour should also cause differing indirect effects. Yet, in aquatic systems, where prey often use chemical cues to judge predator threats, the role of chemically mediated perception of predator body size and the propagation of indirect effects are still unclear. To differentiate intraspecific predator size via chemical cues, prey must judge predator threat quantitatively (i.e. via concentration) or qualitatively (i.e. via differing cues and/or diets). We investigated the role of individual and aggregate predator body size (i.e. biomass, cue concentration) and qualitative diet cues in antipredator behaviour and indirect interactions by examining the behavioural responses of the mud crab Panopeus herbstii and the survival of oyster prey (Crassostrea virginica) in response to various blue crab, Callinectes sapidus, biomass and diet treatments. Mud crabs increased their refuge use and decreased foraging in response to chemical cues from large, but not small, individual blue crabs. The perception of predator size appeared to be related to predator biomass as multiple small blue crabs and large crabs elicited similar foraging responses in mud crabs. However, multiple small blue crabs failed to affect mud crab refuge use, indicating that some measures of behaviour may not always be predictive of indirect effects. Predator diet also influenced mud crab behaviour and foraging: predators fed mud crabs elicited a greater antipredator response than crushed conspecifics or predators fed oyster diets, suggesting that qualitative cues also influence intraspecific threat perception and indirect interactions. These experiments demonstrate that we cannot successfully predict indirect interactions without considering predator population size structure and measuring indirect effects.

From repulsion to attraction: species- and spatial context-dependent threat sensitive response of the spider mite Tetranychus urticae to predatory mite cues

Prey perceiving predation risk commonly change their behavior to avoid predation. However, antipredator strategies are costly. Therefore, according to the threat-sensitive predator avoidance hypothesis, prey should match the intensity of their antipredator behaviors to the degree of threat, which may depend on the predator species and the spatial context. We assessed threat sensitivity of the two-spotted spider mite, Tetranychus urticae, to the cues of three predatory mites, Phytoseiulus persimilis, Neoseiulus californicus, and Amblyseius andersoni, posing different degrees of risk in two spatial contexts. We first conducted a no-choice test measuring oviposition and activity of T. urticae exposed to chemical traces of predators or traces plus predator eggs. Then, we tested the site preference of T. urticae in choice tests, using artificial cages and leaves. In the no-choice test, T. urticae deposited their first egg later in the presence of cues of P. persimilis than of the other two predators and cue absence, indicating interspecific threat-sensitivity. T. urticae laid also fewer eggs in the presence of cues of P. persimilis and A. andersoni than of N. californicus and cue absence. In the artificial cage test, the spider mites preferred the site with predator traces, whereas in the leaf test, they preferentially resided on leaves without traces. We argue that in a nonplant environment, chemical predator traces do not indicate a risk for T. urticae, and instead, these traces function as indirect habitat cues. The spider mites were attracted to these cues because they associated them with the existence of a nearby host plant.

Testing the Threat-Sensitive Hypothesis with Predator Familiarity and Dietary Specificity

In a system with multiple predators, the threat-sensitive predator avoidance hypothesis predicts that prey respond differently to predators relative to the risks each poses (e.g., degree of dietary specialization). Aquatic animals often rely heavily on detecting predators via chemical cues (kairomones) and respond with a suite of behaviors including detection and avoidance. However, little is known about how animals respond to kairomones of specialist versus generalist predators. In laboratory experiments, we compared behavioral responses of a poorly studied aquatic salamander, the greater siren (Siren lacertina), to cues from specialist and generalist predator snakes to evaluate threat-sensitive responses. Sirens exhibited a novel behavior (gill-flushing) most often in the presence of specialist predator cues. Avoidance behavior (reversing direction following cue detection) was higher in response to specialist predator and novel animal control cues and lowest in response to generalist predator cues. An intermediate response to the animal control, an unfamiliar amphibian predator, indicated that sirens respond cautiously to a novel cue. The gradient of observed responses to different snake cues indicates that sirens may be evaluating predation potential of animals based on their foraging specificity and familiarity.

Olfactory recognition of predators by nocturnal lizards: safety outweighs thermal benefits

Many prey species are faced with multiple predators that differ in the degree of danger posed. The threat-sensitive predator avoidance hypothesis predicts that prey should assess the degree of threat posed by different predators and match their behavior according to current levels of risk. To test this prediction, we compared the behavioral responses of nocturnal velvet geckos, Oedura lesueurii, to chemicals from 2 snakes that pose different threats: the dangerous broad-headed snake Hoplocephalus bungaroides that eats geckos and the less dangerous small-eyed snake Cryptophis nigrescens that eats skinks (i.e., does not consume geckos). We also tested whether predator avoidance by prey was modulated by thermal costs associated with retreat-site selection. In both the presence and absence of thermal costs, velvet geckos avoided crevices scented by both dangerous and less dangerous snake species. When given the choice between a crevice scented by a broad-headed snake and a crevice scented by a small-eyed snake, most geckos avoided either retreat site. These results suggest that velvet geckos treat both snake predators as equally dangerous. To further explore these results, we quantified patterns of retreat-site selection by free-living velvet geckos on 2 sandstone plateaux. As in the laboratory, velvet geckos avoided thermally suitable rocks previously used by both snake species. Hence, a gecko's choice of retreat site is influenced by the presence of snake chemicals but is independent of thermal costs or the level of danger posed by the predator. To minimize their risk of predation, geckos may use a simple rule of thumb: “all snakes are dangerous.”

Learning, memorizing and apparent forgetting of chemical cues from new predators by Iberian green frog tadpoles

Many antipredator adaptations are induced by the prey's ability to recognize chemical cues from predators. However, predator recognition often requires learning by prey individuals. Iberian green frog tadpoles (Pelophylax perezi) have the ability to learn new potential predators. Here, we tested the memory capabilities of Iberian green frog tadpoles. We conditioned tadpoles with chemicals cues from a non-predatory fish in conjunction with conspecific alarm cues, and examined whether tadpoles retained their conditioned response (reduction of activity level). We found that conditioned tadpoles reduced their activity levels in subsequent exposures to the non-predatory fish cues alone. Tadpoles were able to remember this association and reduced movement rate at least for 9 days after. The ability to learn and memorize potential predators may be especially important for the survivorship of prey species that are likely to find a high variety of predators. However, after those 9 days, there was a lack of response to the non-predatory fish cues alone in the absence of reinforcement. This could be explained if tadpoles behave according to the threat-sensitive predator avoidance hypothesis, and the perceived risk to the learning cue diminished over time, or it could be due to an apparent forgetting process to avoid non-adaptative responses to chemical cues of non-dangerous species that were randomly paired with alarm cues. Thus, this study demonstrates that green frog tadpoles in the absence of reinforcement remember the chemical cues of a learned predator only for a limited time that may be adaptative in a threat-sensitive context.

Differential responses of red knots, Calidris canutus, to perching and flying sparrowhawk, Accipiter nisus, models

According to the threat-sensitive predator avoidance hypothesis, prey should match the intensity of their antipredation response to the degree of threat posed by predators. We used controlled indoor experiments to investigate the ability of red knots to discern between high- and low-threat encounters with a representative predator, the sparrowhawk. The behaviour of knots was compared across three conditions: no predators present (very low predation threat), presentation of a perching sparrowhawk model (low predation threat) and presentation of a gliding sparrowhawk model (high predation threat). In all behavioural parameters measured, red knots showed evidence of discriminating between the different levels of predation risk. Knots responded immediately to the presence of sparrowhawks with escape flights, and the duration of escape flights was longer following the gliding sparrowhawk events than following perching events. Similarly, the proportion of time spent vigilant increased with increasing level of predation threat, while the proportion of time spent feeding decreased. These results show that knots recognize variations in the level of predation threat, and adjust their antipredator responses accordingly. Furthermore, model sparrowhawks were introduced into the experimental arena at similar distances to the knots, which suggests that knots are able to use cues other than distance to predator to gauge the immediate level of threat that a predator poses.

Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits

Predation is a strong selective force with both direct and indirect effects on an animal's fitness. In order to increase the chances of survival, animals have developed different antipredator strategies. However, these strategies have associated costs, so animals should assess their actual risk of predation and shape their antipredator effort accordingly. Under a stressful situation, such as the presence of predators, animals display a physiological stress response that might be proportional to the risk perceived. We tested this hypothesis in wild European rabbits (Oryctolagus cuniculus), subjected to different predator pressures, in Doñana National Park (Spain). We measured the concentrations of fecal corticosterone metabolites (FCM) in 20 rabbit populations. By means of track censuses we obtained indexes of mammalian predator presence for each rabbit population. Other factors that could modify the physiological stress response, such as breeding status, food availability and rabbit density, were also considered. Model selection based on information theory showed that predator pressure was the main factor triggering the glucocorticoid release and that the physiological stress response was positively correlated with the indexes of the presence of mammalian carnivore predators. Other factors, such as food availability and density of rabbits, were considerably less important. We conclude that rabbits are able to assess their actual risk of predation and show a threat-sensitive physiological response.

The nose knows: minnows determine predator proximity and density through detection of predator odours

Prey often face a behavioural trade-off between fitness-related activities and costly predator avoidance. Individuals that are able to assess their level of risk should maximize their fitness by allocating appropriate amounts of time and energy to avoid predators. The threat-sensitive predator avoidance hypothesis states that prey should respond to a given threat with an intensity that matches their level of risk. Prey fish are known to assess predation risk using predator odours. However, the level of sophistication of risk assessment based on predator odours is not well understood. We conducted two experiments to investigate whether fathead minnows, Pimephales promelas, assess proximity and density of pike, Esox lucius, predators based on pike odours. In experiment 1, we exposed pike-experienced minnows to either 60 ml of pike odour from 12 pike (i.e. 5 ml/pike), 60 ml of pike odour from two pike (i.e. 30 ml/pike) or a control of 60 ml of water. Minnows exposed to odours from two pike showed a more intense antipredator response than did minnows exposed to odours from 12 pike, demonstrating that minnows can detect individual pike in a mixture of odours from several pike. The fact that minnows responded with a greater intensity as the per-pike concentration increased while the overall concentration of pike odour remained constant, indicates that minnows can use odours to determine their relative proximity to predators. In experiment 2, we exposed pike-experienced minnows to either 5 ml/pike from each of 12 pike, 5 ml/pike from each of two pike or a water control. Minnows in the 12-pike treatment showed a stronger antipredator response than did minnows in the two-pike treatment, demonstrating that minnows can assess the relative density of predators using predator odours. These results demonstrate an amazing level of sophistication of predator odour assessment; they are the first to show that prey fish can use odours to determine predator proximity and relative density to respond to predators in a threat-sensitive manner.

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.

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-naive 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.

Learning threat-sensitive predator avoidance: how do fathead minnows incorporate conflicting information?

For prey species, the costs associated with antipredator behaviours should drive the development of efficient risk assessment systems. According to the threat-sensitive predator avoidance hypothesis, prey match the intensity of their antipredator responses with the degree of threat posed. Evidence of threat sensitivity exists for a variety of taxa, but little is known about how such responses develop. We investigated the effect of multiple conditioning events on the development of threat-sensitive antipredator responses of fathead minnows, Pimephales promelas . In experiment 1, we conditioned predator-naive minnows with brook charr, Salvelinus fontinalis , odour paired with either a high or low concentration of conspecific alarm cues. Fish were conditioned twice (low/low, low/high, high/low, high/high), then tested for learned recognition of charr odour alone. Results suggest that minnows learn the relative risk associated with the predator based on the highest alarm cue concentration experienced during the conditioning trials. In experiment 2, predator-naive minnows were conditioned six times with charr odour paired with either a high or low concentration of alarm cues (6 low, 5 low/1 high, 1 high/5 low, 6 high). The intensity of the minnows' antipredator response to charr odour was not an averaging of the intensity of responses during the six conditioning trials. Instead, they used their last conditioning experience to adjust the intensity of their response to the predation cues. Predation fluctuates in space and time. Thus, the best way to adaptively respond to predator cues is to constantly update information regarding the relative risk associated with a given predator.

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.

Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas.

Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.

Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information

The supposition that prey animals assess and behave flexibly in response to different degrees of predation threat is known as the threat-sensitive predator avoidance hypothesis. We completed a series of field and laboratory experiments to examine whether slimy sculpins (Cottus cognatus) exhibit threat-sensitive predator avoidance when exposed to sympatric predatory brook trout (Salvelinus fontinalis). In a field experiment we caged small and large trout in similar habitats and found that sculpins avoided areas containing trout that were large enough to pose a threat to them, but did not avoid areas containing trout that were small and hence not a threat. In a series of laboratory experiments we found that sculpins showed threat-sensitive predator avoidance when they could assess the predator visually. However, when only chemical cues from the predator were presented, sculpins responded to the predator regardless of its size. Chemical cues seem to function to warn the sculpin that the predator is in the vicinity, but visual cues are needed in order to accurately assess the risk posed by the predator.

Threat-sensitive foraging by larval threespine sticklebacks (Gasterosteus aculeatus)

The threat-sensitive predator avoidance hypothesis predicts that prey can assess the relative threat posed by a predator and adjust their behaviour to reflect the magnitude of the threat. We tested the ability of larval threespine sticklebacks to adjust their foraging in the presence of predators by exposing them to conspecific predators of various sizes and recording their foraging and predator avoidance behaviours. Larvae (<30 days post-hatch) displayed predator escape behaviours only towards attacking predators. At 3 weeks post-hatch larvae approached the predator after fleeing, a behaviour which may be the precursor to predator inspection. Larvae reduced foraging and spent less time in the proximity of large and medium-sized predators compared to small predators. The reduction in foraging was negatively correlated to the predator/larva size ratio, indicating that larvae increased their foraging as they increased in size relative to the predator. We conclude that larval sticklebacks can assess the threat of predation early in their ontogeny and adjust their behaviour accordingly.