Dangerous prey and daring predators: a review

How foragers balance risks during foraging is a central focus of optimal foraging studies. While diverse theoretical and empirical work has revealed how foragers should and do manage food and safety from predators, little attention has been given to the risks posed by dangerous prey. This is a potentially important oversight because risk of injury can give rise to foraging costs similar to those arising from the risk of predation, and with similar consequences. Here, we synthesize the literature on how foragers manage risks associated with dangerous prey and adapt previous theory to make the first steps towards a framework for future studies. Though rarely documented, it appears that in some systems predators are frequently injured while hunting and risk of injury can be an important foraging cost. Fitness costs of foraging injuries, which can be fatal, likely vary widely but have rarely been studied and should be the subject of future research. Like other types of risk‐taking behaviour, it appears that there is individual variation in the willingness to take risks, which can be driven by social factors, experience and foraging abilities, or differences in body condition. Because of ongoing modifications to natural communities, including changes in prey availability and relative abundance as well as the introduction of potentially dangerous prey to numerous ecosystems, understanding the prevalence and consequences of hunting dangerous prey should be a priority for behavioural ecologists.     

The effect of habitat structure on prey mortality depends on predator and prey microhabitat use

Structurally complex habitats provide cover and may hinder the movement of animals. In predator–prey relationships, habitat structure can decrease predation risk when it provides refuges for prey or hinders foraging activity of predators. However, it may also provide shelter, supporting structures and perches for sit-and-wait predators and hence increase their predation rates. We tested the effect of habitat structure on prey mortality in aquatic invertebrates in short-term laboratory predation trials that differed in the presence or absence of artificial vegetation. The effect of habitat structure on prey mortality was context dependent as it changed with predator and prey microhabitat use. Specifically, we observed an ‘anti-refuge’ effect of added vegetation: phytophilous predators that perched on the plants imposed higher predation pressure on planktonic prey, while mortality of benthic prey decreased. Predation by benthic and planktonic predators on either type of prey remained unaffected by the presence of vegetation. Our results show that the effects of habitat structure on predator–prey interactions are more complex than simply providing prey refuges or cover for predators. Such context-specific effects of habitat complexity may alter the coupling of different parts of the ecosystem, such as pelagic and benthic habitats, and ultimately affect food web stability through cascading effects on individual life histories and trophic link strengths.     

Juvenile prey induce antipredator behaviour in adult predators

It is generally assumed that the choice of oviposition sites in arthropods is affected by the presence of food for the offspring on the one hand and by predation risk on the other hand. But where should females oviposit when the food itself poses a predation risk for their offspring? Here, we address this question by studying the oviposition behaviour of the predatory mite Amblyseius swirskii in reaction to the presence of its counterattacking prey, the western flower thrips Frankliniella occidentalis. We offered the mites a choice between two potential oviposition sites, one with and one without food. We used two types of food: thrips larvae, which are predators of eggs of predatory mite but are consumed by older predator stages, and pollen, a food source that poses no risk to the predators. With pollen as food, the predators preferred ovipositing on the site with food. This might facilitate the foraging for food by the immature offspring that will emerge from the eggs. With thrips as food, female predators preferred ovipositing on the site without thrips. Predators that oviposited more on the site with thrips larvae killed more thrips larvae than females that oviposited on the site without food, but this did not result in higher oviposition. This suggests that the females killed thrips to protect their offspring. Our results show that predators display complex anti-predator behaviour in response to the presence of counter-attacking prey.     

Predation cues rather than resource availability promote cryptic behaviour in a habitat-forming sea urchin

It is well known that predators often influence the foraging behaviour of prey through the so-called “fear effect”. However, it is also possible that predators could change prey behaviour indirectly by altering the prey’s food supply through a trophic cascade. The predator–sea urchin–kelp trophic cascade is widely assumed to be driven by the removal of sea urchins by predators, but changes in sea urchin behaviour in response to predators or increased food availability could also play an important role. We tested whether increased crevice occupancy by herbivorous sea urchins in the presence of abundant predatory fishes and lobsters is a response to the increased risk of predation, or an indirect response to higher kelp abundances. Inside two New Zealand marine reserves with abundant predators and kelp, individuals of the sea urchin Evechinus chloroticus were rarer and remained cryptic (i.e. found in crevices) to larger sizes than on adjacent fished coasts where predators and kelp are rare. In a mesocosm experiment, cryptic behaviour was induced by simulated predation (the addition of crushed conspecifics), but the addition of food in the form of drift kelp did not induce cryptic behaviour. These findings demonstrate that the ‘fear’ of predators is more important than food availability in promoting sea urchin cryptic behaviour and suggest that both density- and behaviourally mediated interactions are important in the predator–sea urchin–kelp trophic cascade.     

Habitat selection by predators and prey in communities with asymmetrical intraguild predation

Competition and predation have broad ecological consequences as they may influence individual behavior and community structure. In some cases, they are linked and predator and prey are also competitors (intraguild predation). I present a game theoretic model of habitat use by predators and prey under conditions of asymmetrical intraguild predation. This model predicts that when the diet of intraguild predators is restricted to intraguild prey and the resource for which predators and prey compete (the basal resource), co-occurrence is only stable when dietary overlap is low and productivity of the basal resource is not high. The addition of alternative resources for predators results in co-occurrence under all conditions. Variation in alternative resource productivity produces a continuum of intraguild prey distributions from matching relative habitat safety, to one that reflects both food and predation risk. When there is a substantial alternative resource for predators, the distribution of predators matches that of alternative resource availability while the distribution of prey is influenced by both habitat riskiness and food availability. The density and distribution of the predator's alternative resource thus influence habitat selection by the intraguild prey. This stresses the importance of indirect interactions in structuring habitat use in communities and the need to view habitat selection in a community context.     

Interspecific differences in drift behaviour between the native <Emphasis Type="Italic">Gammarus pulex</Emphasis> and the exotic <Emphasis Type="Italic">Gammarus roeseli</Emphasis> and possible implications for the invader’s success

“Drifting” is known to subject aquatic invertebrates to intense predation by drift feeding fish. Consequently, interspecific variations in drifting behaviour could lead to differences in predation pressure between coexisting prey species. Predation being an important factor determining the success of invaders, differences in drift patterns could advantage either native or exotic invertebrates through differential predation by native fish predators. The exotic freshwater amphipod (Gammarus roeseli) has now largely colonized Western Europe where it is often found in sympatry with a native species (Gammarus pulex). Here we documented interspecific differences in drifting behaviour that might have favored the invader’s success through differential predation. Benthic and drifting amphipods were sampled three times at the same site to compare the proportion of each species within and between sample types (benthos or drift) across time. Compared with the benthos, where the invader (G. roeseli) was significantly less abundant than the native (G. pulex), G. roeseli was proportionally overrepresented in the drift but displayed a very different drifting pattern. While G. pulex drift rates remained roughly constant over a 24 h period, G. roeseli showed a marked diel periodicity with low diurnal and high nocturnal drift rates. Such drifting behaviour could procure this species with a competitive advantage regarding predation as most drift feeding fish are diurnal. As a result, the native appears more disadvantaged with respect to drift. This may partly explain the ability of G. roeseli to coexist with G. pulex in a habitat more suitable to the native.     

Prey abundance vs diet breadth in a spider test system

Summary Decisions made as to what prey types to include in the diet were analysed for two populations of the spider,Agelenopsis aperta existing under markedly different prey availability and predation levels. Potential prey types were ranked as to their relative profitabilities with respect to energy gain per handling effort and predation risk. Members of the population experiencing limited prey availability but low risk of predation to visually hunting predators exhibited a significantly higher capture attempt rate towards all prey encountered than the population for which prey were abundant but for which predation was a significant problem. Neither spider population preferentially attacked prey that exhibited higher profitability rankings. An experiment was completed that indicates thatA. aperta can discriminate between more and less profitable prey. Suggestions are made as to why the population experiencing abundant food did not exhibit a narrower diet when compared to the population existing under limited food.     

Naïve,bold, or just hungry? An invasive exotic prey species recognises but does not respond to its predators

Alien species experience both costs and benefits in invaded environments, through naiveté of potential prey species, but also predation pressure from native predators. The question of whether alien prey recognise and respond to native predators has been relatively understudied, despite the hypothesised potential for native predators to provide biotic resistance to invasion. There are two main hypotheses about whether exotic prey should recognise native and exotic predators in their new ranges: (1) naiveté—predicting recognition of evolutionarily familiar predators only, and (2) pre-adaptation—predicting recognition of all predators through a generalist recognition template. With regards to antipredator responses, (3) naïveté theory presumes that exotic prey will respond to the predators they recognise, but we suggest that (4) a bold behavioural syndrome, and/or a high marginal value of food in invaded environments might result in weak or absent responses, even to recognised predators. Here we combine the giving-up density framework with behavioural analysis of remote camera footage to experimentally test these ideas in a disturbed, peri-urban, Australian ecosystem, where alien black rats are predated on by alien dogs, foxes, cats, and native quolls. Black rats recognised dogs and foxes, but appear naïve towards quolls. However, they showed no antipredator responses at all, consistent with a bold behavioural syndrome, elevated predation risk, and/or a high marginal value of food in invaded environments.     

Diagnosing predation risk effects on demography: can measuring physiology provide the means?

Predators kill prey thereby affecting prey survival and, in the traditional top-down view of predator limitation, that is their sole effect. Bottom-up food limitation alters the physiological condition of individuals affecting both fecundity and survival. Predators of course also scare prey inducing anti-predator defences that may carry physiological costs powerful enough to reduce prey fecundity and survival. Here, we consider whether measuring physiology can be used as a tool to unambiguously diagnose predation risk effects. We begin by providing a review of recent papers reporting physiological effects of predation risk. We then present a conceptual framework describing the pathways by which predators and food can affect prey populations and give an overview of predation risk effects on demography in various taxa. Because scared prey typically eat less the principal challenge we see will be to identify measures that permit us to avoid mistaking predator-induced reductions in food intake for absolute food shortage. To construct an effective diagnostic toolkit we advocate collecting multiple physiological measures and utilizing multivariate statistical procedures. We recommend conducting two-factor predation risk × food manipulations to identify those physiological effects least likely to be mistaken for responses to bottom-up food limitation. We suggest there is a critical need to develop a diagnostic tool that can be used when it is infeasible to experimentally test for predation risk effects on demography, as may often be the case in wildlife conservation, since failing to consider predation risk effects may cause the total impact of predators to be dramatically underestimated.     

Loss of body mass under predation risk: cost of antipredatory behaviour or adaptive fit-for-escape?

Predation risk may compromise the ability of animals to acquire and maintain body reserves by hindering foraging efficiency and increasing physiological stress. Locomotor performance may depend on body mass, so losing mass under predation risk could be an adaptive response of prey to improve escape ability. We studied individual variation in antipredatory behaviour, feeding rate, body mass and escape performance in the lacertid lizard Psammodromus algirus. Individuals were experimentally exposed to different levels of food availability (limited or abundant) and predation risk, represented by reduced refuge availability and simulated predator attacks. Predation risk induced lizards to reduce conspicuousness behaviourally and to avoid feeding in the presence of predators. If food was abundant, alarmed lizards reduced feeding rate, losing mass. Lizards supplied with limited food fed at near-maximum rates independently of predation risk but lost more mass when alarmed; thus, mass losses experienced under predation risk were higher than those expected from feeding interruption alone. Although body mass of lizards varied between treatments, no component of escape performance measured during predator attacks (endurance, speed, escape strategy) was affected by treatments or by variations in body mass. Thus, the body mass changes were consistent with a trade-off between gaining resources and avoiding predators, mediated by hampered foraging efficiency and physiological stress. However, improved escape efficiency is not required to explain mass reduction upon predator encounters beyond that expected from feeding interruption or predation-related stress. Therefore, the idea that animals may regulate body reserves in relation to performance demands should be reconsidered.     

Predator-prey shell games: large-scale movement and its implications for decision-making by prey

Many classical models of food patch use under predation risk assume that predators impose patch-specific predation risks independent of prey behavior. These models predict that prey should leave a chosen patch only if and when the food depletes below some critical level. In nature, however, prey individuals may regularly move among food patches, even in the apparent absence of food depletion. We suggest that such prey movement is part of a predator-prey "shell game", in which predators attempt to learn prey location, and the prey attempt to be unpredictable in space. We investigate this shell game using an individual-based model that allows predators to update information about prey location, and permits prey to move with some random component among patches, but with reduced energy intake. Our results show the best prey strategy depends on what the predator does. A non-learning (randomly moving) predator favors non-moving prey – moving prey suffer higher starvation and predation. However, a learning predator favors prey movement. In general, the best prey strategy involves movement biased toward, but not completely committed to, the richer food patch. The strategy of prey movement remains beneficial even in combination with other anti-predator defenses, such as prey vigilance.     

Effects of Predation Risk on Habitat Selection by Water Column Fish, Benthic Fish and Crayfish in Stream Pools

Predation risk can affect habitat selection by water column stream fish and crayfish, but little is known regarding effects of predation risk on habitat selection by benthic fish or assemblages of fish and crayfish. I used comparative studies and manipulative field experiments to determine whether, (1) habitat selection by stream fish and crayfish is affected by predation risk, and (2) benthic fish, water column fish, and crayfish differ in their habitat selection and response to predation risk. Snorkeling was used to observe fish and crayfish in, (1) unmanipulated stream pools with and without large smallmouth bass predators (Micropterus dolomieui >200 mm total length, TL) and (2) manipulated stream pools before and after addition of a single large smallmouth bass, to determine if prey size and presence of large fish predators affected habitat selection. Observations of microhabitat use were compared with microhabitat availability to determine microhabitat selection. Small fish (60–100 mm TL, except darters that were 30–100 mm TL) and crayfish (40–100 mm rostrum to telson length; TL) had significantly reduced densities in pools with large bass, whereas densities of large fish and crayfish (> 100 mm TL) did not differ significantly between pools with and without large bass. Small orangethroat darters (Etheostoma spectabile), northern crayfish (Orconectes virilis), and creek chubs (Semotilus atromaculatus) showed significantly greater densities in pools without large bass. The presence of large smallmouth bass did not significantly affect depths selected by fish and crayfish, except minnows, which were found significantly more often at medium depths when bass were present. Small minnows and large and small crayfish showed the greatest response to additions of bass to stream pools by moving away from bass locations and into shallow water. Small darters and sunfish showed an intermediate response, whereas large minnows showed no significant response to bass additions. Response to predation risk was dependent on prey size and species, with preferred prey, crayfish and small minnows, showing the greatest response. Small benthic fish, such as darters, are intermediate between small water column fish and crayfish and large water column fish in their risk of predation from large smallmouth bass.     

Relationships between direct predation and risk effects

Risk effects arise when prey alter their behavior in response to predators, and these responses carry costs. Empirical studies have found that risk effects can be large. Nonetheless, studies of predation in vertebrate conservation and management usually consider only direct predation. Given the ubiquity and strength of behavioral responses to predators by vertebrate prey, it is not safe to assume that risk effects on dynamics can be ignored. Risk effects can be larger than direct effects. Risk effects can exist even when the direct rate of predation is zero. Risk effects and direct effects do not necessarily change in parallel. When risk effects reduce reproduction rather than survival, they are easily mistaken for limitation by food supply.     

Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail

Predators can alter the outcome of ecological interactions among other members of the food web through their effects on prey behavior. While it is well known that animals often alter their behavior with the imposition of predation risk, we know less about how other features of predators may affect prey behavior. For example, relatively few studies have addressed the effects of predator identity on prey behavior, but such knowledge is crucial to understanding food web interactions. This study contrasts the behavioral responses of the freshwater snail Physellagyrina to fish and crayfish predators. Snails were placed in experimental mesocosms containing caged fish and crayfish, so the only communication between experimental snails and their predators was via non-visual cues. The caged fish and crayfish were fed an equal number of snails, thereby simulating equal prey mortality rates. In the presence of fish, the experimental snails moved under cover, which confers safety from fish predators. However, in the presence of crayfish, snails avoided benthic cover and moved to the water surface. Thus, two species of predators, exerting the same level of mortality on prey, induced very different behavioral responses. We predict that these contrasting behavioral responses to predation risk have important consequences for the interactions between snails and their periphyton resources. Received: 1 June 1998 / Accepted: 12 October 1998     

Unidirectional prey-predator facilitation: apparent prey enhance predators' foraging success on cryptic prey

Food availability can strongly affect predator-prey dynamics. When change in habitat condition reduces the availability of one prey type, predators often search for other prey, perhaps in a different habitat. Interactions between behavioural and morphological traits of different prey may influence foraging success of visual predators through trait-mediated indirect interactions (TMIIs), such as prey activity and body coloration. We tested the hypothesis that foraging success of stream-dwelling cutthroat trout (Onchorhyncus clarki) on cryptically coloured, less-active benthic prey (larval mayfly; Paraleptophebia sp.) can be enhanced by the presence of distinctly coloured, active prey (larval stonefly shredder; Despaxia augusta). Cutthroat trout preyed on benthic insects when drifting invertebrates were unavailable. When stonefly larvae were present, the trout ate most of the stoneflies and also consumed a higher proportion of mayflies than under mayfly only treatment. The putative mechanism is that active stonefly larvae supplied visual cues to the predator that alerted trout to the mayfly larvae. Foraging success of visual predators on cryptic prey can be enhanced by distinctly coloured, active benthic taxa through unidirectional facilitation to the predators, which is a functional change of interspecific interaction caused by a third species. This study suggests that prey-predator facilitation through TMIIs can modify species interactions, affecting community dynamics.     

Foraging decisions in risk-uniform landscapes

Behaviour is shaped by evolution as to maximise fitness by balancing gains and risks. Models on decision making in biology, psychology or economy have investigated choices among options which differ in gain and/or risk. Meanwhile, there are decision contexts with uniform risk distributions where options are not differing in risk while the overall risk level may be high. Adequate predictions for the emerging investment patterns in risk uniformity are missing. Here we use foraging behaviour as a model for decision making. While foraging, animals often titrate food and safety from predation and prefer safer foraging options over riskier ones. Risk uniformity can occur when habitat structures are uniform, when predators are omnipresent or when predators are ideal-free distributed in relation to prey availability. However, models and empirical investigations on optimal foraging have mainly investigated choices among options with different predation risks. Based on the existing models on local decision making in risk-heterogeneity we test predictions extrapolated to a landscape level with uniform risk distribution. We compare among landscapes with different risk levels. If the uniform risk is low, local decisions on the marginal value of an option should lead to an equal distribution of foraging effort. If the uniform risk is high, foraging should be concentrated on few options, due to a landscape-wide reduction of the value of missed opportunity costs of activities other than foraging. We provide experimental support for these predictions using foraging small mammals in artificial, risk uniform landscapes. In high risk uniform landscapes animals invested their foraging time in fewer options and accepted lower total returns, compared to their behaviour in low risk-uniform landscapes. The observed trade off between gain and risk, demonstrated here for food reduction and safety increase, may possibly apply also to other contexts of economic decision making.     

Patch use in time and space for a meso-predator in a risky world

Predator–prey studies often assume a three trophic level system where predators forage free from any risk of predation. Since meso-predators themselves are also prospective prey, they too need to trade-off between food and safety. We applied foraging theory to study patch use and habitat selection by a meso-predator, the red fox. We present evidence that foxes use a quitting harvest rate rule when deciding whether or not to abandon a foraging patch, and experience diminishing returns when foraging from a depletable food patch. Furthermore, our data suggest that patch use decisions of red foxes are influenced not just by the availability of food, but also by their perceived risk of predation. Fox behavior was affected by moonlight, with foxes depleting food resources more thoroughly (lower giving-up density) on darker nights compared to moonlit nights. Foxes reduced risk from hyenas by being more active where and when hyena activity was low. While hyenas were least active during moon, and most active during full moon nights, the reverse was true for foxes. Foxes showed twice as much activity during new moon compared to full moon nights, suggesting different costs of predation. Interestingly, resources in patches with cues of another predator (scat of wolf) were depleted to significantly lower levels compared to patches without. Our results emphasize the need for considering risk of predation for intermediate predators, and also shows how patch use theory and experimental food patches can be used for a predator. Taken together, these results may help us better understand trophic interactions.     

Living and dying in a multi‐predator landscape of fear: roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans

The theory of predation risk effects predicts behavioral responses in prey when risk of predation is not homogenous in space and time. Prey species are often faced with a tradeoff between food and safety in situations where food availability and predation risk peak in the same habitat type. Determining the optimal strategy becomes more complex if predators with different hunting mode create contrasting landscapes of risk, but this has rarely been documented in vertebrates. Roe deer in southeastern Norway face predation risk from lynx, as well as hunting by humans. These two predators differ greatly in their hunting methods. The predation risk from lynx, an efficient stalk‐and‐ambush predator is expected to be higher in areas with dense understory vegetation, while predation risk from human hunters is expected to be higher where visual sight lines are longer. Based on field observations and airborne LiDAR data from 71 lynx predation sites, 53 human hunting sites, 132 locations from 15 GPS‐marked roe deer, and 36 roe deer pellet locations from a regional survey, we investigated how predation risk was related to terrain attributes and vegetation classes/structure. As predicted, we found that increasing cover resulted in a contrasting lower predation risk from humans and higher predation risk from lynx. Greater terrain ruggedness increased the predation risk from both predators. Hence, multiple predators may create areas of contrasting risk as well as double risk in the same landscape. Our study highlights the complexity of predator–prey relationship in a multiple predator setting. Synthesis In this study of risk effects in a multi‐predator context, LiDAR data were used to quantify cover in the habitat and relate it to vulnerability to predation in a boreal forest. We found that lynx and human hunters superimpose generally contrasting landscapes of fear on a common prey species, but also identified double‐risk zones. Since the benefit of anti‐predator responses depends on the combined risk from all predators, it is necessary to consider complete predator assemblages to understand the potential for and occurrence of risk effects across study systems.     

Investment into Defensive Traits by Anuran Prey (Lithobates pipiens) Is Mediated by the Starvation-Predation Risk Trade-Off

Prey can invest in a variety of defensive traits when balancing risk of predation against that of starvation. What remains unknown is the relative costs of different defensive traits and how prey reconcile investment into these traits when energetically limited. We tested the simple allocation model of prey defense, which predicts an additive effect of increasing predation risk and resource availability, resulting in the full deployment of defensive traits under conditions of high risk and resource saturation. We collected morphometric, developmental, and behavioural data in an experiment using dragonfly larvae (predator) and Northern leopard frog tadpoles (prey) subject to variable levels of food availability and predation risk. Larvae exposed to food restriction showed limited response to predation risk; larvae at food saturation altered behaviour, development, and growth in response to predation risk. Responses to risk varied through time, suggesting ontogeny may affect the deployment of particular defensive traits. The observed negative correlation between body size and activity level for food-restricted prey – and the absence of a similar response among adequately-fed prey – suggests that a trade-off exists between behavioural and growth responses when energy budgets are limited. Our research is the first to demonstrate how investment into these defensive traits is mediated along gradients of both predation risk and resource availability over time. The interactions we demonstrate between resource availability and risk level on deployment of inducible defenses provide evidence that both internal condition and extrinsic risk factors play a critical role in the production of inducible defenses over time.     

Effect of Predator-Prey Phylogenetic Similarity on the Fitness Consequences of Predation: A Trade-off between Nutrition and Disease?

A largely neglected aspect of foraging behavior is whether the costs and benefits of predation vary as a function of phylogenetic (i.e., genetic) similarity between predator and prey. Prey of varying phylogenetic similarities to predators might differ in value because both the risk of pathogen transmission and the nutritional quality of prey typically decline with decreasing phylogenetic similarity between predator and prey. I experimentally evaluated this hypothesis by feeding omnivorous spadefoot toad tadpoles (Spea bombifrons, Spea multiplicata, and Scaphiopus couchii) either conspecific tadpoles or an equal mass of three different species of heterospecific prey, all of which contained naturally occurring bacteria. I also examined which prey species Spea tadpoles preferred. I found that all three species of tadpoles performed best on, and preferred to eat, prey that were of intermediate phylogenetic similarity to the predators. Prey of intermediate phylogenetic similarity may provide the greatest fitness benefits to predators because such prey balance the nutritional benefits of closely related prey with the cost of parasite transmission between closely related individuals.