Temporal Variation In Predation Risk Research Articles

Behaviour of a large ungulate reflects temporal patterns of predation risk

Context Many prey species exhibit antipredator behaviours when threatened, yet prey response to temporal variation in predation risk is not well-understood, despite being foundational to predator–prey dynamics and an important consideration among game population managers and recreationalists. Aims To examine white-tailed deer (Odocoileus virginianus) behaviour in response to temporal variation in predation risk imposed by recreational hunters and to assess the effect of deer sex and age on antipredator response. Methods Global positioning system (GPS) collars were used to monitor behaviour of female and male deer in response to diel and weekly patterns of recreational hunting in Alabama, USA. Key results Deer behaviour on weekends (i.e. Friday–Sunday), corresponding to periods of elevated risk, was similar to behaviour on weekdays (i.e. Monday–Thursday). However, when behaviour was examined by individual day of the week, movement rate decreased by 17%, net displacement decreased by 31%, and the probability of activity decreased by 24% during daylight hours on Sundays compared with Fridays. Behavioural changes among days were not detected at night. Daytime behavioural shifts persisted until Wednesdays, despite lower weekday hunting activity. Behavioural variation by deer sex and age was also observed. Conclusions Deer perceive temporal variation in predation risk and modify their behaviour to reduce the likelihood of predation. Variation in response across sex and age classes may be driven by previous experience with hunters and/or survival- and fitness-related trade-offs that affect prey decisions at the individual level. Antipredator response was not initially detectable when examined at a broad temporal scale (i.e. weekend vs weekday); however, a behavioural response was shown with a finer-scale analysis (i.e. individual day of the week), which more closely reflected the pattern of risk fluctuation. Implications Our findings demonstrated the acute awareness of a large ungulate to temporal changes in predation risk and provided insight into ways in which these prey behaviourally respond to reduce the likelihood of predatory encounters. Future studies should consider the temporal scale of risk fluctuation when examining antipredator response to avoid false conclusions. Ungulate hunters and managers can use this information to more efficiently achieve their goals.

Incorporating thermodynamics in predator-prey games predicts the diel foraging patterns of poikilothermic predators.

Models of foraging behaviour typically assume that prey do not adapt to temporal variation in predation risk, such as by avoiding foraging at certain times of the day. When this behavioural plasticity is considered-such as in predator-prey games-the role of abiotic factors is usually ignored. An abiotic factor that exerts strong influence on the physiology and behaviour of many animals is ambient temperature, although it is often ignored from game models as it is implicitly assumed that both predators and prey are homothermic. However, poikilotherms' performance may be reduced in cold conditions due to reduced muscle function, limiting the prey-capture ability of predators and the predator-avoidance and foraging abilities of prey. Here, we use a game-theoretic predator-prey model in which diel temperature changes influence foraging gains and costs to predict the evolutionarily stable diel activity of predators. Our model predicts the range of patterns observed in nature, including nocturnal, diurnal, crepuscular and a previously unexplained post-sunset crepuscular pattern observed in some sharks. In general, smaller predators are predicted to be more diurnal than larger ones. The safety of prey when not foraging is critical, explaining why predators in coral reef systems (with safe refuges) may often have different foraging patterns to pelagic predators. We make a range of testable predictions that will enable the further evaluation of this theoretical framework for understanding diel foraging patterns in poikilotherms.

Food availability and long-term predation risk interactively affect antipredator response.

Food availability and temporal variation in predation risk are both important determinants of the magnitude of antipredator responses, but their effects have rarely been examined simultaneously, particularly in wild prey. Here, we determine how food availability and long-term predation risk affect antipredator responses to acute predation risk by monitoring the foraging response of free-ranging snowshoe hares (Lepus americanus) to an encounter with a Canada lynx (Lynx canadensis) in Yukon, Canada, over four winters (2015-2016 to 2018-2019). We examined how this response was influenced by natural variation in long-term predation risk (2-month mortality rate of hares) while providing some individuals with supplemental food. On average, snowshoe hares reduced foraging time up to 10h after coming into close proximity (≤75m) with lynx, and reduced foraging time an average of 15.28±7.08min per lynx encounter. Hares tended to respond more strongly when the distance to lynx was shorter. More importantly, the magnitude of hares' antipredator response to a lynx encounter was affected by the interaction between food-supplementation and long-term predation risk. Food-supplemented hares reduced foraging time more than control hares after a lynx encounter under low long-term risk, but decreased the magnitude of the response as long-term risk increased. In contrast, control hares increased the magnitude of their response as long-term risk increased. Our findings show that food availability and long-term predation risk interactively drive the magnitude of reactive antipredator response to acute predation risk. Determining the factors driving the magnitude of antipredator responses would contribute to a better understanding of the indirect effects of predators on prey populations.

Correction to: 'How do developmental and parental exposures to predation affect personality and immediate behavioural plasticity in the snail Physa acuta?'

Correction to: 'How do developmental and parental exposures to predation affect personality and immediate behavioural plasticity in the snail Physa acuta?'

Does temporal variation in predation risk affect antipredator responses of larval Indian Skipper Frogs (Euphlyctis cyanophlyctis)?

Predation risk varies on a moment-to-moment basis, through day and night, lunar and seasonal cycles, and over evolutionary time. Hence, it is adaptive for prey animals to exhibit environment-specific behaviour, morphology, and (or) life-history traits. Herein, the effects of temporally varying predation risk on growth, behaviour, morphology, and life-history traits of larval Indian Skipper Frogs (Euphlyctis cyanophlyctis (Schneider, 1799)) were studied by exposing them to no risk, continuous, predictable, and unpredictable risks at different time points. Our results show that larval E. cyanophlyctis could learn the temporal pattern of risk leading to weaker behavioural responses under predictable risk and stronger responses to unpredictable risk. Temporally varying predation risk had a significant impact on tadpole morphology. Tadpoles facing continuous risk had narrow tail muscles. Tadpoles facing predictable risk during the day were heavy with wide and deep tail muscles, whereas those facing predictable risk at night had long tails. Tadpoles facing unpredictable risk were heavy with narrow tail muscles. Metamorphic traits of E. cyanophlyctis were also affected by the temporal variation in predation risk. Tadpoles facing predictable risk during the day emerged at the largest size. However, tadpoles facing predictable risk at night and unpredictable risk metamorphosed earlier, whereas those facing continuous risk metamorphosed later.

Mortality, perception, and scale: Understanding how predation shapes space use in a wild prey population.

Attempts to assess behavioral responses of prey to predation risk are often confounded by depredation of prey. Moreover, the scale at which the response of prey is assessed has important implications for discovering how predation risk alters prey behavior. Herein, we assessed space use of wild Ring-necked Pheasants (Phasianus colchicus) in response to spatial and temporal variation in recreational hunting. We radio-marked pheasants and monitored space use at two spatial scales: short-term seasonal home range, and nightly resting locations. Additionally, we considered temporal variation in predation risk by monitoring space use prior to and during the pheasant hunting season. Although we found no change in nightly resting location, pheasants subjected to predation risk expanded their home range and shifted home range location even when invulnerable to predation. Home range formation was plastic, with home ranges expanding and contracting as risk fluctuated before and during the hunting season. Depredation reduced the measured response within the population, obscuring the potential importance of perceived predation risk in shaping prey communities, particularly when not measured at the appropriate scale. By assessing space use of a wild prey population at multiple scales, considering spatial and temporal variation in predation risk, we show that not only does predation risk affect space use, but that the effects at the population level may be challenging to assess when not measured at the appropriate ecological scale because of the direct effects of differential mortality on the same behaviors.

Spatial distribution of display sites of Grey Peacock-pheasant in relation to micro-habitat and predators during the breeding season

BackgroundThe destruction and fragmentation of forest in Southeast Asia is accelerating biodiversity loss, resulting in a range of management and conservation actions. For some species, a detailed understanding of microhabitat selection is critical for this, especially in the breeding season.MethodsTo understand the factors that explain how specific habitats are used by the Grey Peacock-pheasant (Polyplectron bicalcaratum) in the breeding season, we used camera trapping and microhabitat sampling to assess the microhabitat selection of males. We also looked at their interaction with predators in an area of 1200 m × 1200 m at the Huai Kha Khaeng Wildlife Sanctuary, Thailand, between January and May 2013.ResultsWe show that display scrapes are situated on flatter open areas with small saplings and some vines, typified by low horizontal understory density. We hypothesise that this allows a trade-off between courtship display and the avoidance of predators. Our study showed that the position of Grey Peacock-pheasant display scrapes regularly overlapped with predators within the same microhabitat. We hypothesise that the species’ behavioural responses to temporal variation in predation risk allows them to avoid most predators.ConclusionsParticular microhabitats are required for Grey Peacock-pheasant display. They avoid predators at these places by being active when predators are not.

Re-examining the Causes and Meaning of the Risk Allocation Hypothesis.

The risk allocation hypothesis has inspired numerous studies seeking to understand how temporal variation in predation risk affects prey foraging behavior, but there has been debate about its generality and causes. I examined how imperfect information affects its predictions and sought to clarify the causes of the predicted patterns. I first confirmed that my modeling approach-given a threshold or linear fitness function-produced the risk allocation prediction that prey increase their foraging efforts during low and high risk as the proportion of high-risk periods increases. However, the causes of this result and its robustness differed for the two fitness functions. When prey that had evolved to use perfect information received imperfect information, risk allocation was reduced. However, prey that evolved to use imperfect information in some cases reversed the risk allocation prediction. The model also showed that risk allocation occurs even when prey have no knowledge that the proportions of low- and high-risk periods have changed. I conclude that risk allocation is largely not driven by prey expectations about future states of the environment but rather by the prey's current energetic state and time remaining. I discuss the consequences for experimental design and explanations for empirical results.

Can coyote predation risk induce reproduction suppression in white‐tailed deer?

AbstractPredators can have powerful nonconsumptive effects on their prey by inducing behavioral, physiological, and morphological responses. These nonconsumptive effects may influence prey demography if they decrease birthrates or increase susceptibility to other sources of mortality. The Reproductive Suppression Model suggests that iteroparous species may maximize their lifetime reproductive success by suppressing their reproduction until a future time, when conditions may be more favorable. Coyote (Canis latrans) range expansion in the United States has exposed white‐tailed deer (Odocoileus virginianus) populations to increased predation risk, and coyote predation can have profound effects on white‐tailed deer reproductive success. We evaluated effects of temporal variation in predation risk (i.e., coyote–deer ratios) on fecundity and reproductive success of white‐tailed deer on the Joseph W. Jones Ecological Research Center in southwestern Georgia, United States, by exploiting a rapid decline in coyote abundance to establish a natural experiment. We measured fecundity by examining ovaries for evidence of ovulation, and measured reproductive success using evidence of lactation from deer harvested before and after the decline in coyote abundance. We found that incidence of ovulation and lactation increased following the decline in predation risk. Our results suggest coyotes may be able to influence deer recruitment, independent of direct predation, through interactions that result in reduced fecundity. More broadly, our study suggests that in order to understand the totality of the effect of predators on prey population dynamics, studies should incorporate measures of direct and indirect predator effects.

Behavior of Cape fur seals (Arctocephalus pusillus pusillus) in relation to temporal variation in predation risk by white sharks (Carcharodon carcharias) around a seal rookery in False Bay, South Africa

AbstractThe marked differences in predation risk posed by white sharks (Carcarodon carcarias) at island rookeries of Cape fur seals (Arctocephalus pusillus pusillus) offer a quasi‐experimental design within a natural system for exploring how prey adjust their behavior in response to temporal variation in predation risk. Here we compare movement of juvenile and adult Cape fur seals at a high risk (Seal Island) and low risk (Egg Island) rookery. We further compare juveniles and adults at Seal Island in low and high risk seasons and at low and high risk times of day within those seasons. Adult fur seals at Seal Island avoided traversing the zone of high white shark predation risk during the high risk period (0700–0959) in the season of high risk (winter), but not during the low risk season (summer). By contrast, adult fur seals at Egg Island showed no temporal discretion in either season. Unlike juvenile fur seals at Egg Island, juveniles at Seal Island adjusted their temporal movement patterns to more closely mimic adult seal movement patterns. This suggests that exposure to predators is the primary driver of temporal adjustments to movement by prey species commuting from a central place.

Prey state shapes the effects of temporal variation in predation risk.

The ecological impacts of predation risk are influenced by how prey allocate foraging effort across periods of safety and danger. Foraging decisions depend on current danger, but also on the larger temporal, spatial or energetic context in which prey manage their risks of predation and starvation. Using a rocky intertidal food chain, we examined the responses of starved and fed prey (Nucella lapillus dogwhelks) to different temporal patterns of risk from predatory crabs (Carcinus maenas). Prey foraging activity declined during periods of danger, but as dangerous periods became longer, prey state altered the magnitude of risk effects on prey foraging and growth, with likely consequences for community structure (trait-mediated indirect effects on basal resources, Mytilus edulis mussels), prey fitness and trophic energy transfer. Because risk is inherently variable over time and space, our results suggest that non-consumptive predator effects may be most pronounced in productive systems where prey can build energy reserves during periods of safety and then burn these reserves as 'trophic heat' during extended periods of danger. Understanding the interaction between behavioural (energy gain) and physiological (energy use) responses to risk may illuminate the context dependency of trait-mediated trophic cascades and help explain variation in food chain length.

Phenotypically plastic neophobia: a response to variable predation risk

Prey species possess a variety of morphological, life history and behavioural adaptations to evade predators. While specific evolutionary conditions have led to the expression of permanent, non-plastic anti-predator traits, the vast majority of prey species rely on experience to express adaptive anti-predator defences. While ecologists have identified highly sophisticated means through which naive prey can deal with predation threats, the potential for death upon the first encounter with a predator is still a remarkably important unresolved issue. Here, we used both laboratory and field studies to provide the first evidence for risk-induced neophobia in two taxa (fish and amphibians), and argue that phenotypically plastic neophobia acts as an adaptive anti-predator strategy for vulnerable prey dealing with spatial and temporal variation in predation risk. Our study also illustrates how risk-free maintenance conditions used in laboratory studies may blind researchers to adaptive anti-predator strategies that are only expressed in high-risk conditions.

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

AbstractIn natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Białowieża Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.

Costs and benefits of temporary brood desertion in a Neotropical harvestman (Arachnida: Opiliones)

Brood desertion is a life history strategy that allows parents to minimize costs related to parental care and increase their future fecundity. The harvestman Neosadocus maximus is an interesting model organism to study costs and benefits of temporary brood desertion because females abandon their clutches periodically and keep adding eggs to their clutches for some weeks. In this study, we tested if temporary brood desertion (a) imposes a cost to caring females by increasing the risk of egg predation and (b) offers a benefit to caring females by increasing fecundity as a result of increased foraging opportunities. With intensive field observations followed by a model selection approach, we showed that the proportion of consumed eggs was very low during the day and it was not influenced by the frequency of brood desertion. The proportion of consumed eggs was higher at night and it was negatively related to the frequency of brood desertion. However, frequent brood desertion did not result in higher fecundity, measured both as the number of eggs added to the current clutch and the probability of laying a second clutch over the course of the reproductive season. Considering that harvestmen are sensitive to dehydration, brood desertion during the day may attenuate the physiological stress of remaining exposed on the vegetation. Moreover, since brood desertion is higher during the day, when egg predation pressure is lower, caring females could be adjusting their maternal effort to the temporal variation in predation risk, which is regarded as the main cost of brood desertion in ectotherms.

The effects of variable predation risk on foraging and growth: Less risk is not necessarily better

There is strong evidence that the way prey respond to predation risk can be fundamentally important to the structuring and functioning of natural ecosystems. The majority of work on such nonconsumptive predator effects (NCEs) has examined prey responses under constant risk or constant safety. Hence, the importance of temporal variation in predation risk, which is ubiquitous in natural systems, has received limited empirical attention. In addition, tests of theory (e.g., the risk allocation hypothesis) on how prey allocate risk have relied almost exclusively on the behavioral responses of prey to variation in risk. In this study, we examined how temporal variation in predation risk affected NCEs on prey foraging and growth. We found that high risk, when predictable, was just as energetically favorable to prey as safe environments that are occasionally pulsed by risk. This pattern emerged because even episodic pulses of risk in otherwise safe environments led to strong NCEs on both foraging and growth. However, NCEs more strongly affected growth than foraging, and we suggest that such effects on growth are most important to how prey ultimately allocate risk. Hence, exclusive focus on behavioral responses to risk will likely provide an incomplete understanding of how NCEs shape individual fitness and the dynamics of ecological communities.

Predation risk increases permissiveness for heterospecific advertisement calls in túngara frogs, Physalaemus pustulosus

Factors that influence the strength of sexual selection within a population may have important consequences for the evolution and maintenance of reproductive isolation between populations. Here we examine the role of one such factor, predation risk, in influencing female permissiveness for heterospecific advertisement calls. Specifically, we tested the effect of simulated predation risk on mate choice in female tungara frogs, Physalaemus pustulosus, using variation in ambient light levels, travel time and the presence of auditory cues of local predators. Simulated predation risk increased female permissiveness for advertisement calls along an artificial gradient of calls intermediate between conspecifics and a congener, Physalaemus enesefae. Across the entire gradient, the presence of auditory cues of the predatory frog Leptodactylus pentadactylus in association with the conspecific call dramatically increased the likelihood of females choosing the intermediate call. In addition, higher ambient light levels and simulation of increased travel distances both increased the likelihood that females would choose intermediate calls over conspecific calls. These results suggest that, although mate choice may be important in causing reproductive isolation between allopatric populations, spatial or temporal variation in predation risk may strongly influence the expression of mate choice and thus the outcome of secondary contact.

Reversibility of predator‐induced plasticity and its effect at a life‐history switch point

In natural systems, organisms are frequently exposed to spatial and temporal variation in predation risk. Prey organisms are known to develop a wide array of plastic defences to avoid being eaten. If inducible plastic defences are costly, prey living under fluctuating predation risk should be strongly selected to develop reversible plastic traits and adjust their defences to the current predation risk. Here, we studied the induction and reversibility of antipredator defences in common frog Rana temporaria tadpoles when confronted with a temporal switch in predation risk by dragonfly larvae. We examined the behaviour and morphology of tadpoles in experimental treatments where predators were added or withdrawn at mid larval development, and compared these to treatments with constant absence or presence of predators. As previous studies have overlooked the effects that developing reversible anti‐predator responses could have later in life (e.g. at life history switch points), we also estimated the impact that changes in antipredator responses had on the timing of and size at metamorphosis. In the presence of predators, tadpoles reduced their activity and developed wider bodies, and shorter and wider tails. When predators were removed tadpoles switched their behaviour within one hour to match that found in the constant environments. The morphology matched that in the constant environments in one week after treatment reversal. All these responses were highly symmetrical. Short time lags and symmetrical responses for the induction/reversal of defences suggest that a strategy with fast switches between phenotypes could be favoured in order to maximise growth opportunities even at the potential cost of phenotypic mismatches. We found no costs of developing reversible responses to predators in terms of life‐history traits, but a general cost of the induction of the defences for all the individuals experiencing predation risk during some part of the larval development (delayed metamorphosis). More studies examining the reversibility of plastic defences, including other type of costs (e.g. physiological), are needed to better understand the adaptive value of these flexible strategies.

The responses of prey fish to temporal variation in predation risk: sensory habituation or risk assessment?

Predation is an important selection pressure acting on prey behavior. Although numerous studies have shown that when predation risk is high, prey tend to increase vigilance and reduce foraging effort, until recently, few studies have looked at how temporal patterns of risk influence the trade-off between foraging and antipredator behavior. The risk allocation hypothesis predicts that prey should respond strongly to predators that are usually absent, as they can meet their energy demands during safe periods. In contrast, if predators are almost always present, prey need to forage actively even though predators are present, a counter-intuitive prediction for many behavioral ecologists. This decrease in antipredator behavior on increasing exposure to risk has thus far been attributed to sensory habituation. Using cichlids, we show that sensory habituation is likely not the proximate explanation for the reduction in antipredator behaviors in this system. Such responses may rather be the result of adaptive decision making.

Phenotypic plasticity in response to fine‐grained environmental variation in predation

Summary 1 In nature, organisms experience environmental variability at coarse-grained (inter-generational) and fine-grained (intra-generational) scales and a common response to environmental variation is phenotypic plasticity. The emphasis of most empirical work on plasticity has been on examining coarse-grained variation with the goal of understanding the costs and benefits of plastic responses in response to a particular environment. 2 In this study, we investigated the effects of fine-grained variation in predation on the inducible defences of larval wood frogs (Rana sylvatica) by widely altering the density and feeding schedule of caged predators (Dytiscus spp.) while holding average predation constant. 3 We found that predator cues induced change in tadpole behaviour, morphology, and mass. Surprisingly, however, temporal variation in predation did not cause the tadpoles to alter their activity (compared to a constant predation treatment) or mass. Temporal variation in predation did alter tadpole tail depth, but only when experiencing our most extreme variation treatment in which the predators were fed once every 8 days. Under these conditions, the predator-induced tadpole tail was less extreme compared to environments containing constant predation. 4 While a number of previous studies have examined behavioural responses of prey to temporal variation in predation risk without holding average predation constant, this appears to be the first test of temporal variation per se. As in previous studies of organism responses to temporal variation in resources, our results suggest that fine-grained environmental variability can affect the expression of phenotypically plastic traits, but our tadpoles appear to be generally unresponsive to this fine-grained variation for many of their traits.

Exotic shrubs as ephemeral ecological traps for nesting birds

Certain exotic plants may increase risk of nest predation, and, in this way, may act as ecological traps. We hypothesized that the greater vulnerability to predation was a consequence of either (1) reduced nest height due to architectural differences among plant species or (2) seasonal changes in the distribution of nests among forest strata. To test this, we examined temporal variation in nest survival of 888 nests of Northern Cardinal (Cardinalis cardinalis) in native substrates and two exotic shrubs (Lonicera maackii and Rosa multiflora) in Ohio, USA, 2001–2006. We evaluated evidence for an ecological trap by monitoring the annual reproductive productivity of 245 breeding pairs of cardinals. Only nests in Rosa experienced relatively constant survival rates across the season, whereas probability of survival increased over the season for nests in other substrates. Interestingly, the relative vulnerability of nests in different substrates varied across the season. Most strikingly, nests in Lonicera in early spring showed the lowest survival rates but exceeded survival rates of nests in native substrates late in the season. Nest height failed to explain seasonal changes in nest survival, as only nests in native plants significantly increased in height as the season progressed. Rather, predation risk seemed to be a function of the proportion of nests within each substrate, as illustrated by the decreased predation in Lonicera as the relative proportion of nests in native substrates increased. The patterns of temporal variation in predation risk that we detected show that impacts of Lonicera are not a function of plant architecture alone and may be related to leaf phenology, changes in nest density, nest site location, and/or nest synchrony. Examination of the reproductive productivity of cardinals showed that pairs that made their first nest attempt in Lonicera fledged 20% fewer cardinal young than birds that began the season using other substrates. Thus, we suggest that exotic plants may represent an ephemeral ecological trap for certain nesting birds, where negative effects persist only during certain periods.