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.     

Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments

Summary Predator-prey studies in semi-arid eastern Australia demonstrated that populations of rabbits (Oryctolagus cuniculus) could be regulated by predators. The functional, numerical and total responses of foxes (Vulpes vulpes) to rabbits and the numerical response of feral cats (Felis catus) to rabbits, are described. Measurement of the rabbit component of foxes' stomach contents indicates a Type III functional response. The size of the fox population in summer was dependent on the availability of rabbits over the immediately preceding rabbit breeding season but there appeared to be no density-dependent aggregation of young foxes in areas of surplus food. The total response of foxes, estimated using the short-term numerical response of dispersing foxes, was directly density-dependent for low rabbit densities and inversely density-dependent for high rabbit densities. Two states are possible with this form of total response: a state with low rabbit densities regulated by predators and a state with high rabbit densities which occurs when rabbits escape predator regulation. The boundary between regulation and non-regulation by predators was demonstrated by a predator-removal experiment. In the treated areas, predators were initially culled and rabbits increased to higher densities than in an untreated area where predators were always present. When predators were allowed back into the treated areas, rabbit populations continued to increase and did not decline to the density in the untreated area. This is the critical evidence for a two-state system. When predators were present, rabbits could be maintained at low densities which were in the density-dependent part of the total response curve for foxes. Exceptionally high rabbit recruitment, or artificially reduced predation, could result in rabbits escaping predator-regulation. Under these circumstances, rabbits could move into the inversely density-dependent region of the total response curve for foxes.     

Predator‐Naïve Brown Trout (Salmo trutta) Show Antipredator Behaviours to Scent from an Introduced Piscivorous Mammalian Predator Fed Conspecifics

Introduced mammalian predators may pose a high risk for native and naïve prey populations, but little is known about how native fish species may recognize and respond to scents from introduced mammalian predators. We investigated the role of diet‐released chemical cues in facilitating predator recognition, hypothesizing that native brown trout (Salmo trutta) would exhibit antipredator behaviours to faeces scents from the introduced American mink (Neovision vison) fed conspecifics, but not to non‐trout diets. In treatments‐control and replicate stream tank experiments, brown trout showed significant antipredator responses to faeces scent from mink fed conspecifics, but not to faeces scent from mink fed a non‐trout diet (chicken), or the non‐predator food control, Eurasian beaver (Castor fiber). We conclude that native and naïve brown trout show relevant antipredator behaviours to an introduced mammalian predator, presumably based on diet‐released conspecific alarm cues and thereby estimate the predation risk.     

Nest predation in forest birds: influence of predator type and predator's habitat quality

We used the introduction of a generalist nest predator, the red squirrel Tamiasciurus hudsonicus, and of a large herbivore, the Sitka black-tailed deer Odocoileus hemionus sitkensis, to the islands of Haida Gwaii (Queen Charlotte Islands, British Columbia, Canada) to study how predator assemblage and habitat quality and structure influenced nest predation in forest birds. We compared losses of natural nests to predators on islands with and without squirrels. We selected nine islands with or without squirrel or deer and used 506 artificial nests put on the ground or in shrubs to further analyse variation of nest predation with predator assemblage and habitat quality for the predators. For both natural and artificial nests predation risk was higher in presence of squirrels. But predation risk varied within island categories. In presence of squirrels it was highest in stands with mature conifers where it fluctuated from year to year, in response to fluctuations in squirrel abundance. Vegetation cover around the nest had little effect on nest predation by squirrels. Where squirrels were absent, nest predation concentrated near predictable food sources for corvids, the main native predators, and increased with decreasing vegetation cover, suggesting that removal of the vegetation by deer increased the risk of predation by native avian nest predators that use visual cues. Predation risk in these forests therefore varies in space and time with predator composition and with quality of the habitat from the predators' perspective. This temporal and spatial variation in predation risk should promote trade-offs in the response of birds to nest predation, rather than fine-tuned adaptations to a given predation pattern.     

The effect of predator and prey density on the induced defence of a ciliate

1. The level of antipredator defence should be proportional to the actual attack probability to minimize the cost of defence and maximize the net benefit.
2. The hypothesis that the induced antipredator morphology of Euplotes octocarinatus is a graded response to the actual risk of predation by Stylonychia mytilus was tested by manipulating the density of both prey and predator populations.
3. The magnitude of the response was graded according to both predator and prey density. A dense prey population may be protective since a prey is more exposed to a predator's attack as a solitary individual.
4. The results suggest that Euplotes is able to 'estimate' the real risk of predation and respond appropriately, without mobilizing more resources than needed.
5. Separation of the prey and predator with a nylon net revealed that the response was not induced by a water-transmitted factor but that direct cell-to-cell contacts were important. This finding departs from those of other studies.     

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.     

Interactions between the information content of different chemical cues affect induced defences in tadpoles

Animals often alter their behaviour, morphology and physiology in the presence of predators. These induced defences can be fine‐tuned by a variety of environmental factors such as predator species, acute predation risk or food availability. It has, however, remained unclear what cues influence the extent and quality of induced defences and how the information content of these cues interact to determine the development of antipredator defences. We performed an experiment to study the significance of direct chemical cues, originating from the predators themselves, and indirect cues, released by attacked or consumed prey, for phenotypic responses in Rana dalmatina tadpoles. We reared tadpoles in the presence of caged predators (Triturus vulgaris, Aeshna cyanea) fed either one or three tadpoles every other day outside the tadpole‐rearing tanks. Fifteen hours after food provisioning, predators were put back into the tanks containing focal tadpoles either after washing (direct + digestion‐released cues) or with the water containing remnants of the prey (direct + all types of indirect cues). Our results suggest that direct cues together with digestion‐released cues can be sufficient to induce strong antipredator responses. Induced defences depended on both direct cues, affecting predator‐specific responses, and the quantity of indirect cues, resulting in graded responses to differences in predation threat. Moreover, direct and indirect cues interacted in behaviour, resulting in predator‐specific graded responses. We also observed a decrease in the extent of predator‐induced responses in large tadpoles as compared to small ones. Our results, thus, suggest that prey integrate multiple cues about predators to optimize induced defences and that this process changes during ontogeny.     

Phenotypic plasticity in anti-intraguild predator strategies: mite larvae adjust their behaviours according to vulnerability and predation risk

Interspecific threat-sensitivity allows prey to maximize the net benefit of antipredator strategies by adjusting the type and intensity of their response to the level of predation risk. This is well documented for classical prey-predator interactions but less so for intraguild predation (IGP). We examined threat-sensitivity in antipredator behaviour of larvae in a predatory mite guild sharing spider mites as prey. The guild consisted of the highly vulnerable intraguild (IG) prey and weak IG predator Phytoseiulus persimilis, the moderately vulnerable IG prey and moderate IG predator Neoseiulus californicus and the little vulnerable IG prey and strong IG predator Amblyseius andersoni. We videotaped the behaviour of the IG prey larvae of the three species in presence of either a low- or a high-risk IG predator female or predator absence and analysed time, distance, path shape and interaction parameters of predators and prey. The least vulnerable IG prey A. andersoni was insensitive to differing IGP risks but the moderately vulnerable IG prey N. californicus and the highly vulnerable IG prey P. persimilis responded in a threat-sensitive manner. Predator presence triggered threat-sensitive behavioural changes in one out of ten measured traits in N. californicus larvae but in four traits in P. persimilis larvae. Low-risk IG predator presence induced a typical escape response in P. persimilis larvae, whereas they reduced their activity in the high-risk IG predator presence. We argue that interspecific threat-sensitivity may promote co-existence of IG predators and IG prey and should be common in predator guilds with long co-evolutionary history.     

Referential calls signal predator behavior in a group-living bird species

Predation is a powerful agent of natural selection, driving the evolution of antipredator calls [1]. These calls have been shown to communicate predator category [2-4] and/or predator distance to conspecifics [5-7]. However, the risk posed by predators depends also on predator behavior [8], and the ability of prey to communicate predator behavior to conspecifics would be a selective advantage reducing their predation risk. I tested this idea in Siberian jays (Perisoreus infaustus), a group-living bird species. Predation by hawks, and to a lesser extent by owls, is substantial and the sole cause of mortality in adult jays [9]. By using field data and predator-exposure experiments, I show here that jays used antipredator calls for hawks depending on predator behavior. A playback experiment demonstrated that these prey-to-prey calls were specific to hawk behavior (perch, prey search, attack) and elicited distinct, situation-specific escape responses. This is the first study to demonstrate that prey signals convey information about predator behavior to conspecifics. Given that antipredator calls in jays aim at protecting kin group members [10, 11], consequently lowering their mortality [9], kin-selected benefits could be an important factor for the evolution of predator-behavior-specific antipredator calls in such systems.     

Assessing resource and predator effects on habitat use of tropical small carnivores

Habitat use of animals is influenced by a combination of factors including food abundance and interactions with other species. Animals typically must forage while simultaneously avoiding predation from multiple potential predators, but habitat use in tropical forest ecosystems that assesses effects of both predation risk and resources has rarely been conducted. We used camera traps and occupancy analyses to document small mammalian carnivore occurrence in relation to food abundance and interactions with large predators. We hypothesized that habitat use of six small mammalian carnivores (≤15 kg) would be influenced by (1) abundance of resources (fruit, rodents, and streams) and/or (2) large predators. Predictions regarding food and habitat resources were only supported for one species (crab-eating mongoose, Urva urva), which was positively associated with rodents and streams. Three small carnivores (masked palm civet Paguma larvata, common palm civet Paradoxurus hermaphroditus, yellow-throated marten Martes flavigula) were affected negatively by leopard and mesopredators as predicted. Counter to our predictions, two species (masked palm civet and yellow-throated marten) showed spatial avoidance of tiger suggesting that an apex predator might also pose predation risk to small carnivores. The focal small carnivores and large predators of this study appeared to have moderately to highly overlapping temporal activity indicating no temporal avoidance. In conclusion, food resources appeared to have minimal effects for six small carnivores in this ecosystem probably due to continuous resource availability. Predation risk appeared to affect some species in terms of spatial occupancy but not in temporal activity, indicating perhaps complex, but not entirely negative interactions between larger carnivores and this guild of small carnivores. The mechanisms which facilitate co-occurrence between small carnivores and large predators may, however, operate at finer spatiotemporal scales than we investigated here.     

Do anuran larvae respond behaviourally to chemical cues from an invasive crayfish predator? A community-wide study

Antipredator behaviour is an important fitness component in most animals. A co-evolutionary history between predator and prey is important for prey to respond adaptively to predation threats. When non-native predator species invade new areas, native prey may not recognise them or may lack effective antipredator defences. However, responses to novel predators can be facilitated by chemical cues from the predators’ diet. The red swamp crayfish Procambarus clarkii is a widespread invasive predator in the Southwest of the Iberian Peninsula, where it preys upon native anuran tadpoles. In a laboratory experiment we studied behavioural antipredator defences (alterations in activity level and spatial avoidance of predator) of nine anurans in response to P. clarkii chemical cues, and compared them with the defences towards a native predator, the larval dragonfly Aeshna sp. To investigate how chemical cues from consumed conspecifics shape the responses, we raised tadpoles with either a tadpole-fed or starved crayfish, or dragonfly larva, or in the absence of a predator. Five species significantly altered their behaviour in the presence of crayfish, and this was largely mediated by chemical cues from consumed conspecifics. In the presence of dragonflies, most species exhibited behavioural defences and often these did not require the presence of cues from predation events. Responding to cues from consumed conspecifics seems to be a critical factor in facilitating certain behavioural responses to novel exotic predators. This finding can be useful for predicting antipredator responses to invasive predators and help directing conservation efforts to the species at highest risk.     

Shifting the balance between foraging and predator avoidance: the importance of food distribution for a schooling pelagic forager

It is widely held that when predator avoidance conflicts with other activities, such as feeding, avoidance of predators often takes precedence. In this study, we examine how predation risk and food distribution interact to influence the schooling behavior and swimming speed of foraging juvenile walleye pollock, Theragra chalcogramma. Fish were acclimated to either spatially and temporally clumped, or spatially and temporally dispersed food for 3 weeks. Fish were then monitored while feeding in the absence and presence of predatory sablefish, Anoplopoma fimbria. Fish foraging for clumped food swam rapidly in a loose school when predators were absent, but swam more slowly and adopted more cohesive schooling in the presence of predators, trading-off foraging opportunity for decreased vulnerability to predators. Fish foraging for dispersed food swam about slowly and did not engage in cohesive schooling in either the absence or presence of predators. These fish accepted greater predation risk in order to continue foraging, suggesting that the cost of schooling, in terms of decreased foraging opportunity, was greater when food was dispersed than when it was clumped. This lower responsiveness to predators among fish receiving dispersed food demonstrates that predator avoidance does not always take precedence over other activities, but rather, that a balance is maintained between predator avoidance and feeding, which shifts as food distribution changes.     

Threat‐sensitive predator avoidance by pike larvae

The threat‐sensitive predator avoidance (TSPA) hypothesis was tested on hatchery‐reared pike Esox lucius larvae. Larval swimming activity, food attacks upon zooplankton, escapes, immobility behaviour, vigilance, as well as time in vegetation under different predation risk were measured. Single larvae were video‐filmed in aquaria allowing them to have visual contact with a small or a large perch Perca fluviatilis as predator. The odds of fleeing increased significantly if the larvae were exposed to a large predator instead of a small one. Swimming activity and foraging decreased significantly in the presence of a predator compared to the control. On the other hand, no significant effect was detected in time spent in the vegetation, and in vigilance of larvae, measured as time intervals between food attacks. The findings suggest that pike larvae primarily flee in the presence of a large predator, whereas they remain immobile, and forage, when possible, in the presence of a small predator. Sometimes a lack of response between the large and the small predator treatments was detected, which suggests that the antipredator response has a threshold, and when increasing the threat, the prey response does not increase. In the present paper it is demonstrated that hatchery‐reared pike larvae respond to the level of threat, and thereby seem to be risk adjusting as predicted.     

The interaction between predation risk and food ration on behavior and morphology of Eurasian perch

The risk of both predation and food level has been shown to affect phenotypic development of organisms. However, these two factors also influence animal behavior that in turn may influence phenotypic development. Hence, it might be difficult to disentangle the behavioral effect from the predator or resource‐level effects. This is because the presence of predators and high resource levels usually results in a lower activity, which in turn affects energy expenditure that is used for development and growth. It is therefore necessary to study how behavior interacts with changes in body shape with regard to resource density and predators. Here, we use the classic predator‐induced morphological defense in fish to study the interaction between predator cues, resource availability, and behavioral activity with the aim to determine their relative contribution to changes in body shape. We show that all three variables, the presence of a predator, food level, and activity, both additively and interactively, affected the body shape of perch. In general, the presence of predators, lower swimming activity, and higher food levels induced a deep body shape, with predation and behavior having similar effect and food treatment the smallest effect. The shape changes seemed to be mediated by changes in growth rate as body condition showed a similar effect as shape with regard to food‐level and predator treatments. Our results suggests that shape changes in animals to one environmental factor, for example, predation risk, can be context dependent, and depend on food levels or behavioral responses. Theoretical and empirical studies should further explore how this context dependence affects fitness components such as resource gain and mortality and their implications for population dynamics.     

Dynamic switching in predator attack and maternal defence of prey

Predator and prey relationships are dynamic and interrelated. Thus, any offensive behaviour will vary according to differing defensive behaviours, or vice versa, within each species in any predator–prey system. However, most studies are one‐sided as they focus on just one behaviour, that of either the predator or prey. Here, we examine both predatory behaviour of an oophagus katydid and antipredator behaviour by a frog with egg‐stage parental care. Katydid offensive behaviour and predation success was greater in females and increased with predator maturity and size. Frog defensive behaviour was sex specific, probably because only mothers provide parental care. Defensive behaviour could be active, such as charging predators, or passive, such as sheltering eggs, with greater active defence against larger predators; neither was influenced by offspring age. These results are contrary to existing theory, which argues parental investment ought to be negatively correlated with parental predation risks and affected by offspring age. This study highlights the use of antipredator behaviour to test predictions of parental investment theories in amphibians. In addition, it illustrates the need to consider factors that influence both species concurrently when examining the complex interaction between predators and parents.     

Role of prey and intraspecific density dependence on the population growth of an avian top predator

Exploring predator–prey systems in diverse ecosystems increases our knowledge about ecological processes. Predator population growth may be positive when conspecific density is low but predators also need areas with prey availability, associated with competition, which increases the risk of suffering losses but stabilises populations. We studied relationships between European rabbits Oryctolagus cuniculus (prey) and adult eagle owls Bubo bubo (predators) in south-western Europe. We assessed models explaining the predator population growth and stability. We estimated the abundance of rabbits and adult eagle owls during three years in eight localities of central-southern Spain. We explored models including rabbit and adult eagle owl abundance, accounting for yearly variations and including the locality as a random variable. We found that population growth of adult eagle owls was positive in situations with low conspecific abundance and tended to be negative but approaching equilibrium in situations of higher conspecific abundance. Population growth was also positively related to previous summer rabbit density when taking into account eagle owl conspecific abundance, possibly indicating that rabbits may support recruitment. Furthermore, abundance stability of adult eagle owls was positively related to previous winter–spring rabbit density, which could suggest predator population stabilisation through quick territory occupation in high-quality areas. These results exemplify the trade-off between prey availability and abundance of adult predators related to population growth and abundance stability in the eagle owl–rabbit system in south-western Europe. Despite rabbits have greatly declined during the last decades and eagle owls locally specialise on them, eagle owls currently have a favourable conservation status. As eagle owls are the only nocturnal raptor with such dependence on rabbits, this could point out that predators may overcome prey decreases in areas with favourable climate and prey in the absence of superior competitors with similar foraging mode.     

The control of risk hypothesis: reactive vs. proactive antipredator responses and stress‐mediated vs. food‐mediated costs of response

Inducible defences against predators evolve because they reduce the rate of direct predation, but this benefit is offset by the cost (if any) of defence. If antipredator responses carry costs, the effect of predators on their prey is partitioned into two components, direct killing and risk effects. There is considerable uncertainty about the strength of risk effects, the factors that affect their strength, and the mechanisms that underlie them. In some cases, antipredator responses are associated with a glucocorticoid stress response, and in other cases they are associated with trade‐offs between food and safety, but there is no general theory to explain this variation. Here, I develop the control of risk (COR) hypothesis, predicting that proactive responses to predictable and controllable aspects of risk will generally have food‐mediated costs, while reactive responses to unpredictable or uncontrollable aspects of predation risk will generally have stress‐mediated costs. The hypothesis is grounded in laboratory studies of neuroendocrine stressors and field studies of food‐safety trade‐offs. Strong tests of the COR hypothesis will require more studies of responses to natural variation in predation risk and the physiological consequences of these responses, but its explanatory power can be illustrated with existing case studies.     

Adaptive flexibility in the behaviour of juvenile Atlantic salmon: short-term responses to food availability and threat from predation

Juvenile Atlantic salmon Salmo salar were shown experimentally to make adaptive behavioural decisions as a short-term response to changes in food availability and predation risk. Restricted food availability caused an increase in activity, whereas activity was decreased under predation threat. Although changes in activity were not more pronounced among the hunger-motivated fish, suggesting that they were not balancing risk and hunger, hungrier fish spent less time in refuges in the presence of a predator, indicating that they were more willing to take risks than satiated fish. Aggressive interactions among juvenile Atlantic salmon were decreased by predation threat, but were highest when predators were absent and food was abundant.     

Diet of a polyphagous arthropod predator affects refuge seeking of its thrips prey

Antipredator behaviour of prey costs time and energy, at the expense of other activities. However, not all predators are equally dangerous to all prey; some may have switched to feeding on another prey species, making them effectively harmless. To minimize costs, prey should therefore invest in antipredator behaviour only when dangerous predators are around. To distinguish these from harmless predators, prey may use cues related to predation on conspecifics, such as odours released by a predator that has recently eaten conspecific prey or alarm pheromones released by attacked prey. We studied refuge use by a herbivorous/omnivorous thrips, Frankliniella occidentalis, in response to odours associated with a generalist predatory bug, Orius laevigatus, fed either with conspecific thrips or with other prey. The refuge used by thrips larvae is the web produced by its competitor, the two-spotted spider mite, Tetranychus urticae, where thrips larvae experience lower predation risk because the predatory bug is hindered by the web. Thrips larvae moved into this refuge when odours associated with predatory bugs that had previously fed on thrips were present, whereas odours from predatory bugs that had fed on other prey had less effect. We discuss the consequences of this antipredator behaviour for population dynamics. Copyright 2000 The Association for the Study of Animal Behaviour.     

Predator–prey naïveté, antipredator behavior,and the ecology of predator invasions

We present a framework for explaining variation in predator invasion success and predator impacts on native prey that integrates information about predator–prey naïveté, predator and prey behavioral responses to each other, consumptive and non‐consumptive effects of predators on prey, and interacting effects of multiple species interactions. We begin with the ‘naïve prey’ hypothesis that posits that naïve, native prey that lack evolutionary history with non‐native predators suffer heavy predation because they exhibit ineffective antipredator responses to novel predators. Not all naïve prey, however, show ineffective antipredator responses to novel predators. To explain variation in prey response to novel predators, we focus on the interaction between prey use of general versus specific cues and responses, and the functional similarity of non‐native and native predators. Effective antipredator responses reduce predation rates (reduce consumptive effects of predators, CEs), but often also carry costs that result in non‐consumptive effects (NCEs) of predators. We contrast expected CEs versus NCEs for non‐native versus native predators, and discuss how differences in the relative magnitudes of CEs and NCEs might influence invasion dynamics. Going beyond the effects of naïve prey, we discuss how the ‘naïve prey’, ‘enemy release’ and ‘evolution of increased competitive ability’ (EICA) hypotheses are inter‐related, and how the importance of all three might be mediated by prey and predator naïveté. These ideas hinge on the notion that non‐native predators enjoy a ‘novelty advantage’ associated with the naïveté of native prey and top predators. However, non‐native predators could instead suffer from a novelty disadvantage because they are also naïve to their new prey and potential predators. We hypothesize that patterns of community similarity and evolution might explain the variation in novelty advantage that can underlie variation in invasion outcomes. Finally, we discuss management implications of our framework, including suggestions for managing invasive predators, predator reintroductions and biological control.