Prey Antipredator Behavior Research Articles

Adaptive Vertical Positioning as Anti-Predator Behavior: The Case of a Prey Fish Cohabiting with Multiple Predatory Fish within Temperate Marine Algal Forests.

Simple SummaryFish cohabiting within structurally complex habitats (e.g., coral reefs, seagrass meadows, algal forests) include abundant small-bodied prey fish and specialized piscivorous fish. Habitat structural complexity mediating fish predator–prey interactions has been shown to be an important mechanism sustaining this coexistence. However, the effect of the vertical stratification of habitat structure on predator–prey interactions remains poorly known, especially within a forest-like marine habitat, i.e., a habitat containing three vertical strata (understory, canopy and open-water). We set up tank experiments to test how such habitat vertical stratification affects predator–prey lethal and behavioral interactions, using one prey and two predator model species cohabiting in Mediterranean algal forest. We found that prey anti-predator behavior was predator-specific. When exposed to a sit-and-wait predator, the prey increased its vertical distance from the predator, regardless of the habitat structure. Conversely, when exposed to a stalk-and-attack predator, the prey sought refuge within forest structures. Prey hide motionless within the canopy, the most complex strata, while they avoid and escape from predators within the understory, which is a less complex stratum allowing for fast prey movements but still protected from predators by the canopy above. Our results suggest the crucial role of habitat vertical stratification in influencing predator–prey interactions, which should be studied in three dimensions.Prey fish cohabit with specialized predator fish within structurally complex habitats. How the vertical stratification of the habitat affects lethal and behavioral predator–prey interactions and contributes to explaining these patterns has never been investigated within a forest-like marine habitat, i.e., a habitat containing three vertical strata (understory, canopy, open-water above). We studied this in tank experiments, with a model prey (the wrasse Symphodus ocellatus) and two model predators (the stalk-and-attack comber Serranus cabrilla and the sit-and-wait scorpionfish Scorpaena porcus), which are among the most abundant prey and predators cohabiting in Mediterranean Cystoseira forests. Wrasse anti-predator behavior was predator-specific. When exposed to the scorpionfish, the wrasse increased its vertical distance from the predator, regardless of the habitat structure. Conversely, when exposed to the comber, the wrasse sought refuge within forest structures: (1) the canopy provides more hiding opportunities due to its high complexity, and (2) the understory provides more escape/avoidance opportunities due to (a) its low complexity that allows for fast prey movements, and (b) the presence of the canopy above that limits the comber’s access to the understory. Our results suggest that habitat vertical stratification mediates predator–prey interactions and potentially promotes the co-existence of prey and multiple predators within marine forests.

Antipredator response diminishes during periods of resource deficit for a large herbivore.

The starvation-predation hypothesis predicts that, during resource shortages, prey forego antipredator behavior and forage as much as possible to avoid starvation, even when risk of predation is high. We tested this hypothesis using GPS locations collected simultaneously from moose (Alces alces) and wolves (Canis lupus) in the Greater Yellowstone Ecosystem of North America. We assessed shifts in the speed, displacement, and habitat selection of moose 24h following encounter with wolves (0-1,500m distance). We examined whether the strength of antipredator behaviors would weaken as winter progressed and the nutritional condition of moose declined. Moose responded to wolf encounters by increasing their rate of movement in early winter, but only within 500m distance. Importantly, these responses attenuated as winter progressed. Moose did not avoid their preferred foraging habitat (riparian areas) following encounters with wolves at any distance, and instead they more strongly selected riparian areas, especially in early winter. Our findings support theoretical predictions that resource deficits should dampen prey antipredator behavior, and suggest that nutritional condition of prey may buffer against run-away risk effects in food webs involving large mammalian predators and prey.

Predator and prey functional traits: understanding the adaptive machinery driving predator-prey interactions.

Predator–prey relationships are a central component of community dynamics. Classic approaches have tried to understand and predict these relationships in terms of consumptive interactions between predator and prey species, but characterizing the interaction this way is insufficient to predict the complexity and context dependency inherent in predator–prey relationships. Recent approaches have begun to explore predator–prey relationships in terms of an evolutionary-ecological game in which predator and prey adapt to each other through reciprocal interactions involving context-dependent expression of functional traits that influence their biomechanics. Functional traits are defined as any morphological, behavioral, or physiological trait of an organism associated with a biotic interaction. Such traits include predator and prey body size, predator and prey personality, predator hunting mode, prey mobility, prey anti-predator behavior, and prey physiological stress. Here, I discuss recent advances in this functional trait approach. Evidence shows that the nature and strength of many interactions are dependent upon the relative magnitude of predator and prey functional traits. Moreover, trait responses can be triggered by non-consumptive predator–prey interactions elicited by responses of prey to risk of predation. These interactions in turn can have dynamic feedbacks that can change the context of the predator–prey interaction, causing predator and prey to adapt their traits—through phenotypically plastic or rapid evolutionary responses—and the nature of their interaction. Research shows that examining predator–prey interactions through the lens of an adaptive evolutionary-ecological game offers a foundation to explain variety in the nature and strength of predator–prey interactions observed in different ecological contexts.

Quantifying insect predation with predator exclusion cages: the role of prey antipredator behavior as a source of bias

AbstractThere are limitations imposed by current methodologies to detect and quantify insect predation. However, there has been relatively little effort to experimentally document the sources of biases associated with the various methodologies. In this study, we examined how predation estimates in the field using predator exclusion cages may be biased when one fails to account for antipredator behavioral responses. To do this, we did the usual comparison of the number of insects missing from plants where predators were allowed access to the number missing from plants where predators were excluded, but also determined how many of the missing insects reacted to predators by dropping from plants and how many were actually preyed upon. Our results provide evidence that estimates of insect mortality in the field are significantly reduced if prey antipredator behavior is taken into account. As it is commonly assumed that prey missing in the field are predated, documenting the incidence of predator‐mediated ‘disappearance’ and capturing insect prey before they escape can provide with a relevant estimate of bias.

Moose anti-predator behaviour towards baying dogs in a wolf-free area

Understanding the impact of human activity on prey anti-predator behaviour is becoming increasingly important. For many species, hunting is the dominating mortality cause in areas where predators are functionally extinct. In a controlled field experiment in Northern Sweden devoid of wolves, we exposed adult female moose (Alces alces) to hunting activity using a dog (Canis lupus familiaris) to study individual moose anti-predator behaviour. Moose were more active, had larger 24-h activity ranges and left the area after the disturbance. Our study supports the existence of several anti-predator strategies within a species even when predators are absent. A mixed strategy among individuals may be beneficial when a new predator eventually enters the system. Instead of fronting as expected from other study systems, most individuals fled when confronted. We argue that heavily harvested Scandinavian moose may be more adapted to human and bear predation in contrast to the suggested behavioural maladaption towards wolf predation. We build on two major lines of arguments; first, being less defensive, but fleeing when approached by a baying dog which mimics wolf encounters, is likely to increase moose survival compared with the risk to be shot when being defensive and fronting, held at bay. Secondly, we assume that escaping in a tortuous manner, i.e. in an unpredictable way, may increase the chance to undergo persecution by increasing the chance that chaser switches the target animal, especially in areas of high moose density. We recommend future studies to address individual variation and behavioural plasticity in anti-predator behaviour.

An island-wide predator manipulation reveals immediate and long-lasting matching of risk by prey.

Anti-predator behaviour affects prey population dynamics, mediates cascading effects in food webs and influences the likelihood of rapid extinctions. Predator manipulations in natural settings provide a rare opportunity to understand how prey anti-predator behaviour is affected by large-scale changes in predators. Here, we couple a long-term, island-wide manipulation of an important rodent predator, the island fox (Urocyon littoralis), with nearly 6 years of measurements on foraging by deer mice (Peromyscus maniculatus) to provide unequivocal evidence that prey closely match their foraging behaviour to the number of fox predators present on the island. Peromyscus maniculatus foraging among exposed and sheltered microhabitats (a measure of aversion to predation risk) closely tracked fox density, but the nature of this effect depended upon nightly environmental conditions known to affect rodent susceptibility to predators. These effects could not be explained by changes in density of deer mice over time. Our work reveals that prey in natural settings are cognizant of the dynamic nature of their predators over timescales that span many years, and that predator removals spanning many generations of prey do not result in a loss of anti-predator behaviour.

Size-structured abundance relationships between upper- and mid-trophic level predators on temperate rocky reefs

Top-down control of community structure can manifest as inverse relationships between the abundances of organisms at adjacent trophic levels. Due to the time costs of handling very large prey it may be optimal for gape-limited predatory fishes to select prey with body depths that are ≤ 60% of predator gape width. We tested for inverse relationships between the abundances of different sized rockfish (prey) and of lingcod (predator) large enough to be expected to select that rockfish size. We predicted that these relationships would be stronger when assuming that body depth of selected prey is ≤ 60%, rather than ≤ 100%, of lingcod gape width. Results were consistent with this prediction for small and medium size classes of rockfish. Regardless of prey selection assumptions there were no negative relationships between lingcod and large size classes of rockfish, possibly because only 2.3% of observed lingcod were large enough to select large rockfish when assuming prey body depth selection of ≤ 60% of predator gape width. Large rockfish, therefore, may have occupied a size refuge from lingcod risk. Our results, however, are characterized by large statistical uncertainty. We suggest that prey antipredator behaviour, which has the cost of reducing access to resources and the benefit of lowering mortality rates, might explain much of this uncertainty. Quillback and copper rockfish are long-lived species with late maturity. As such, they are expected to maximize fitness by investing heavily in antipredator behaviour, and this investment may have weakened numerical relationships between lingcod and small and medium size classes.

Behavioral refuges and predator–prey coexistence

The effects of a behavioral refuge caused either by the predator optimal foraging or prey adaptive antipredator behavior on the Gause predator–prey model are studied. It is shown that both of these mechanisms promote predator–prey coexistence either at an equilibrium, or along a limit cycle. Adaptive prey refuge use leads to hysteresis in prey antipredator behavior which allows predator–prey coexistence along a limit cycle. Similarly, optimal predator foraging leads to sigmoidal functional responses with a potential to stabilize predator–prey population dynamics at an equilibrium, or along a limit cycle.

Effects of Predator Hunting Mode on Grassland Ecosystem Function

The way predators control their prey populations is determined by the interplay between predator hunting mode and prey antipredator behavior. It is uncertain, however, how the effects of such interplay control ecosystem function. A 3-year experiment in grassland mesocosms revealed that actively hunting spiders reduced plant species diversity and enhanced aboveground net primary production and nitrogen mineralization rate, whereas sit-and-wait ambush spiders had opposite effects. These effects arise from the different responses to the two different predators by their grasshopper prey-the dominant herbivore species that controls plant species composition and accordingly ecosystem functioning. Predator hunting mode is thus a key functional trait that can help to explain variation in the nature of top-down control of ecosystems.

Prey choice by predators: effect of prey vulnerability

We examined the effect of prey vulnerability on the prey choice behaviour of the turtle Phrynops gibbus in a series of laboratory experiments using two sizes and states (mobile and immobile) of prey. Our results suggest that prey vulnerability (ease of capture) alters the apparent choice of prey by these turtles. When vulnerability was low, turtles consumed significantly more small prey and when vulnerability was high they consumed significantly more large prey exhibiting what has been respectively referred to in the foraging literature as passive and active prey choice. We suggest that the distinction between passive and active prey choice may be misleading and that the interaction between forager behaviour and prey antipredator behaviour should be considered in studies of nonrandom predator diets.

Predator Foraging Capabilities and Prey Antipredator Behaviours: Pre- versus Postcapture Constraints on Size-Dependent Predator-Prey Interactions

In order to understand patterns of predator diets and foraging efficiency relative to predator and prey size, it is essential to determine which particular suite of constraints determines the outcome of predator prey interactions. Feeding experiments were carried out with differently-sized piscivorous Eurasian perch (13-24 cm total length) and prey fish, roach (3.4-11.6 cm total length), at two different spatial scales, tanks and wading pools. The tank experiments focused on morphological constraints in the predation process, as the spatial scale of the tanks (0.4 m 3 ) restricted antipredator behaviour. The pool experiments focused on prey anti-predator behaviour, such as schooling capacity, evasive behaviours, predator and prey swimming capacities, and predator reaction times, as the spatial scale of tanks (2.5 m 3 ) allowed prey to express antipredator behaviours. In the tanks, for a given predator size, the number of attacks and the manipulation time after prey had been caught increased with prey size. The maximum size of prey caught appeared to be related mainly to predator gape limitation. In the pools the maximum size at which prey were captured by predators generally was smaller than in the tanks, indicating that prey evasive behaviour was important in determining predator success. The scaling of prey schooling, positioning in the water column and evading by jumping out of the water with prey size did not indicate that these behaviours were determining the maximum size of prey consumed in pools. Rather, the relation between predator and prey mobility seemed to be the most important factor determining the maximum size of prey consumed in the pools. This suggests that foraging models using handling time as currency may be poor predictors'of active predator active prey foraging patterns.

Strong Preferences for Apparently Dangerous Habitats? A Consequence of Differential Escape from Predators

Predators may affect prey populations not only through the direct removal of individual prey (e.g., Taylor 1984), but also through their prey's anti-predator behavior (e.g., Abrams 1984, Sih 1987, Kotler and Brown 1988). Several recent studies (see Lima and Dill 1990) demonstrate that these behaviorally-mediated effects are particularly important in determining the spatial distribution of prey in the environment: animals avoid habitats with abundant predators and correspondingly high risk of attack. This is a reasonable result, and ruling-out between-habitat differences in food abundance, mating prospects, etc., it might appear entirely general. However, consider the fact that habitat choice may be influenced by the probability of escape as well as the probability of attack itself. Studies of habitat use under the risk of predation have focused almost exclusively on habitat-specific attack rates, predator abundance, etc. (see Lima and Dill 1990), whereas habitatspecific escape has rarely been considered (or essentially held constant between habitats). When considering both attack and escape simultaneously, the above avoidance of habitats with high risks of predatory attack may no longer hold in general. This paper explores some simple ideas on why animals may not only prefer apparently dangerous habitats, but also exhibit such strong preferences for them that a very high risk of attack may not drive them away. Consider a generic animal with a choice between two habitats, designated 1 and 2. Let ai and ej represent the probability of attack in habitat i, and probability of escape given attack in habitat i, respectively. The probability of being killed by a predator in habitat i (Pi) is thus Pi = ai(1-ei). For simplicity, assume that the habitats differ only in Pi values, thus habitat 1 will be chosen when Pi<P2, or ai(1-ej)<a2(1-e2), which rearranges to