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.     

Wall lizards combine chemical and visual cues of ambush snake predators to avoid overestimating risk inside refuges

The threat sensitivity hypothesis assumes that multiple cues from a predator should contribute in an additive way to determine the degree of risk-sensitive behaviour. The ability to use multiple cues in assessing the current level of predation risk should be especially important to prey exposed to multiple predators. Wall lizards, Podarcis muralis, respond to predatory attacks from birds or mammals by hiding inside rock crevices, where they may encounter another predator, the smooth snake, Coronella austriaca. We investigated in the laboratory whether chemical cues may be important to wall lizards for detection of snakes. The greater tongue-flick rate and shorter latency to first tongue-flick in response to predator scents indicated that lizards were able to detect the snakes' chemical cues. We also investigated the use of different predatory cues by lizards when detecting the presence of snakes within refuges. We simulated successive predator attacks and compared the propensity of lizards to enter the refuge and time spent within it for predator-free refuges, refuges containing either only visual or chemical cues of a snake, or a combination of these. The antipredatory response of lizards was greater when they were exposed to both visual and chemical cues than when only one cue was presented, supporting the threat sensitivity hypothesis. This ability may improve the accuracy of assessments of the current level of predation risk inside the refuge. It could be especially important in allowing lizards to cope with threats posed by two types of predators requiring conflicting prey defences.     

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

Summary In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.     

Variability in the Assessment of Snake Predation Risk by Liolaemus Lizards

The ability to assess and respond to predation risk is a strong selective force. Detection of predators is carried out by one or more sensory modalities, but the use of chemoreception has significant advantages. This study examines the chemosensorial assessment of snake predation risk and corresponding behaviours in different species and populations of Liolaemus lizards naturally exposed to different levels of snake predation pressure. The species studied were sympatric (Liolaemus lemniscatus), parapatric (L. nigroviridis) and allopatric (L. fitzgeraldi) to the saurophagous snake, Philodryas chamissonis. Additionally, two populations of L. lemniscatus from areas differing in snake densities were compared. Chemo‐assessment of predation risk was determined by comparing the number of tongue‐flicks (TF) and the behavioural responses of lizards submitted to three treatments (with semiochemicals of snake, conspecifics, and without semiochemicals – control). The results suggest that Liolaemus lizards can chemo‐assess snake predation risk, but this was modulated by the predation pressure experienced by lizards in their natural habitats. When exposed to snake semiochemicals, the sympatric prey showed less chemical exploratory behaviour (i.e. lower number of TF), a higher frequency of antipredator behaviours that would reduce its detection by a predator, and did not show the behaviour triggered by conspecific semiochemicals. The parapatric prey showed similar number of TF across different treatments, suggesting an absence of recognition of snake semiochemicals; however, it did show antipredatory behaviours when confronted with snake semiochemicals. The allopatric prey showed similar behaviour in all treatments. Both populations of the sympatric species, L. lemniscatus, showed a similar ability to detect predation risk when confronted with snake semiochemicals (i.e. similar number of TF), but antipredatory behaviours were diminished, and marking behaviours were present in the population subject to lower predation pressure. Relaxed predation pressure from a predator that releases and detects semiochemicals had similar consequences at species and population levels.     

Influence of gaze and directness of approach on the escape responses of the Indian rock lizard, Psammophilus dorsalis (Gray, 1831)

Animals often evaluate the degree of risk posed by a predator and respond accordingly. Since many predators orient their eyes towards prey while attacking, predator gaze and directness of approach could serve as conspicuous indicators of risk to prey. The ability to perceive these cues and discriminate between high and low predation risk should benefit prey species through both higher survival and decreased energy expenditure. We experimentally examined whether Indian rock lizards (Psammophilus dorsalis) can perceive these two indicators of predation risk by measuring the variation in their fleeing behaviour in response to type of gaze and approach by a human predator. Overall, we found that the gaze and approach of the predator influenced flight initiation distance, which also varied with attributes of the prey (i.e. size/sex and tail-raise behaviour). Flight initiation distance (FID) was 43% longer during direct approaches with direct gaze compared with tangential approaches with averted gaze. In further, exploratory, analyses, we found that FID was 23% shorter for adult male lizards than for female or young male (FYM) lizards. In addition, FYM lizards that showed a tail-raise display during approach had a 71% longer FID than those that did not. Our results suggest that multiple factors influence the decision to flee in animals. Further studies are needed to test the generality of these factors and to investigate the proximate mechanisms underlying flight decisions.     

Vole cycles and antipredatory behaviour

During recent years the role of predation as a simple mechanism to produce cyclical population fluctuations in microtine rodent populations has gained stronger empirical and theoretical support. Predation by several generalist species produces non-cyclicity, and predation by resident specialists, such as small mustelids, produces a synchronous cyclic pattern of population fluctuations in several vole species. At the same time, behavioural ecological studies have shown that the same group of specialist predators crucial for cyclicity causes the strongest antipredatory responses in vole behaviour. Recently, breeding suppression in cyclic microtines under risk of mustelid predation has been documented both in the laboratory and in the field. This review links the new population ecological studies and modelling of cyclic microtines and their predators with recent findings on antipredatory adaptations of voles.     

Increased predation risk while mate guarding as a cost of reproduction for male broad-headed skinks (Eumeces laticeps)

We investigated antipredatory costs associated with mate guarding as potential costs of reproduction for male broad-headed skinks. Mate guarding by male lizards may increase fitness by preventing loss of fertilizations of the guarded female's eggs to other males, but it may have several costs. In addition to lost opportunities to search for additional females, risk of injury while fighting other males, and energetic expenditures while following females and fighting, guarding males might suffer increased risk of predation and reduction of opportunities to forage. We studied potential antipredatory costs of mate guarding by simulating predators searching for and approaching pairs of lizards in the field. Among pairs of lizards in close proximity to each other, males were detected before females 10 times more frequently than females were detected before males, and females fled before males much more frequently than males fled before females when pairs were approached, leaving the males exposed to the predator. After one or both lizards fled, males frequently followed females by scanning visually and scent trailing, exposing themselves to the predator while the female hid. Females never followed males. The implications of these findings for antipredatory costs of mate guarding are discussed. Electronic Publication     

Balancing the dilution and oddity effects: decisions depend on body size

Background

Grouping behaviour, common across the animal kingdom, is known to reduce an individual''s risk of predation; particularly through dilution of individual risk and predator confusion (predator inability to single out an individual for attack). Theory predicts greater risk of predation to individuals more conspicuous to predators by difference in appearance from the group (the ‘oddity’ effect). Thus, animals should choose group mates close in appearance to themselves (eg. similar size), whilst also choosing a large group.

Methodology and Principal Findings

We used the Trinidadian guppy (Poecilia reticulata), a well known model species of group-living freshwater fish, in a series of binary choice trials investigating the outcome of conflict between preferences for large and phenotypically matched groups along a predation risk gradient. We found body-size dependent differences in the resultant social decisions. Large fish preferred shoaling with size-matched individuals, while small fish demonstrated no preference. There was a trend towards reduced preferences for the matched shoal under increased predation risk. Small fish were more active than large fish, moving between shoals more frequently. Activity levels increased as predation risk decreased. We found no effect of unmatched shoal size on preferences or activity.

Conclusions and Significance

Our results suggest that predation risk and individual body size act together to influence shoaling decisions. Oddity was more important for large than small fish, reducing in importance at higher predation risks. Dilution was potentially of limited importance at these shoal sizes. Activity levels may relate to how much sampling of each shoal was needed by the test fish during decision making. Predation pressure may select for better decision makers to survive to larger size, or that older, larger fish have learned to make shoaling decisions more efficiently, and this, combined with their size relative to shoal-mates, and attractiveness as prey items influences shoaling decisions.     

Does risk of predation by mammalian predators affect the spacing behaviour of rodents? Two large-scale experiments

Predator-prey interactions between small mammals and their avian and mammalian predators have attracted much attention. However, large-scale field experiments examining small-mammal antipredatory responses under the risk of predation by mammals are rare. As recently pointed out, the scale of experiments may cause misleading results in studies of decision-making under predation risk. We studied the effect of small mustelid predators on the spacing behaviour of the gray-tailed vole (Microtus canicaudus) and the bank vole (Clethrionomys glareolus) in two separate field enclosure experiments. The experiments were conducted during the breeding season in North America and northern Europe, where small mustelids have been suggested to be important mammalian predators of voles. As in most of the earlier laboratory studies, predation risk was simulated using fresh mustelid faeces and urine. This made it possible to compare the results from experiments at different spatial scales. We did not find any effect of increased predation risk on spacing behaviour (mean and/or maximum distance moved and home range size) or trappability in either vole species. Simulated predation risk did not affect the breeding of females in gray-tailed voles, as has previously been shown in bank voles. The results disagree with most of the studies conducted in laboratory conditions with small mammals. We discuss whether this discrepancy could be caused by differences in the scale of the experiments. Received: 12 April 1999 / Accepted: 7 October 1999     

Party size and early detection of predators in sumatran forest primates

Theoretical considerations suggest that the ability to detect the presence or approach of a predator when there is still enough time to flee (early detection) should improve with group size, if group living is to be advantageous for individual non-human primates. The hypothesis that the distance at which forest primates detect predators increases with the size of their party was confirmed by observation. It was found that in addition to party size height (vegetation density) could also influence detection distance. Because height relates not only to visibility but also to the number of potential predators, one would predict that small parties are found higher in the canopy to compensate for the increased risk of predation. This prediction was confirmed using data on long-tailed macaques (Macaca fascicularis). The correlation found between party size and predation risk demonstrates that forest monkeys can adjust their behaviour in response to changes in predation risk, and hence support the hypothesis that predation risk has been an important, perhaps even the only, selective force responsible for the evolution of group living in non-human primates.     

Introduced mammalian predators induce behavioural changes in parental care in an endemic New Zealand bird

The introduction of predatory mammals to oceanic islands has led to the extinction of many endemic birds. Although introduced predators should favour changes that reduce predation risk in surviving bird species, the ability of island birds to respond to such novel changes remains unstudied. We tested whether novel predation risk imposed by introduced mammalian predators has altered the parental behaviour of the endemic New Zealand bellbird (Anthornis melanura). We examined parental behaviour of bellbirds at three woodland sites in New Zealand that differed in predation risk: 1) a mainland site with exotic predators present (high predation risk), 2) a mainland site with exotic predators experimentally removed (low risk recently) and, 3) an off-shore island where exotic predators were never introduced (low risk always). We also compared parental behaviour of bellbirds with two closely related Tasmanian honeyeaters (Phylidonyris spp.) that evolved with native nest predators (high risk always). Increased nest predation risk has been postulated to favour reduced parental activity, and we tested whether island bellbirds responded to variation in predation risk. We found that females spent more time on the nest per incubating bout with increased risk of predation, a strategy that minimised activity at the nest during incubation. Parental activity during the nestling period, measured as number of feeding visits/hr, also decreased with increasing nest predation risk across sites, and was lowest among the honeyeaters in Tasmania that evolved with native predators. These results demonstrate that some island birds are able to respond to increased risk of predation by novel predators in ways that appear adaptive. We suggest that conservation efforts may be more effective if they take advantage of the ability of island birds to respond to novel predators, especially when the elimination of exotic predators is not possible.     

Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics?

Many animals benefit from the presence of conspecifics by reducing their rate of scanning for predators while increasing their time spent foraging. This group size effect could arise from a decreased perception of individual risk (dilution hypothesis) and/or an increased ability to detect predators (detection hypothesis). We compared individual and group vigilance of Rocky Mountain elk, Cervus elaphus, in three regions of Yellowstone National Park, Wyoming, U.S.A. that varied in their encounter frequency with coyote, Canis latrans, grizzly bear, Ursus arctos, and grey wolf,Canis lupus , predators. Adult females without calves increased scanning and decreased foraging with high encounter risk and small herd size. Adult females with calves increased scanning and decreased foraging with high encounter risk, but showed no decrease in scanning with large herd size. Yearlings increased scanning and decreased feeding with small herd size, but not with high encounter risk. Adult males were least vigilant, fed most and were not influenced by encounter risk or herd size. These age-sex class differences led to significant differences in group vigilance depending on the composition of the herd. Herds with a majority of mothers were significantly more vigilant than herds with a majority of adult males. However, these differences in group vigilance had no influence on the individual scanning of females without calves. Thus, the decrease in individual scanning with herd size may depend more on changes in individual risk than on cooperative detection of predators. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Frequency-dependent predation and maintenance of prey polymorphism

In positive frequency-dependent predation, predation risk of an individual prey correlates positively with the frequency of that prey type. In a number of small-scale experiments individual predators have shown frequency-dependent behaviour, often leading to the conclusion that a population of such predators could maintain prey polymorphism. Using simulations, I studied the dynamics of frequency-dependent predation and prey polymorphism. The model suggests that persistence of prey polymorphism decreases with increasing number of predators that show frequency-dependent behaviour, questioning conclusions about polymorphism based on experiments with few predators. In addition, prey population size, prey crypsis, difference in crypsis between prey morphs and the way the behaviour was adjusted affected the persistence of polymorphism. Under some circumstances prey population remained polymorphic for a shorter time under frequency-dependent than under frequency-independent predation. This suggests that although positive frequency-dependent predator behaviour may maintain prey polymorphism, it is not a sufficient condition for persistent prey polymorphism.     

Egg concealment is an antipredatory strategy in a cavity‐nesting bird

Birds have developed different behavioural strategies to reduce the risk of predation during the breeding period. Bird species that nest in the open often cover their eggs to decrease the risk of predators detecting the clutches. However, in cavity nesters, the potential functions of egg covering have not been explored despite some bird species that nest in cavities also covering their eggs as open nesters do. We analysed whether egg covering is an antipredatory behaviour in the blue tit (Cyanistes caeruleus). We simulated an increase in the perceived risk of predation at experimental nests by adding predator scent inside the nest boxes during the egg‐laying period, whilst adding lemon essence or water to control nest boxes. Birds exposed to predator chemical cues in the nest of experimental pairs more frequently covered their eggs than birds exposed to an odorous control. These results suggest that egg covering may have evolved as an antipredatory behaviour also in cavity nesters to reduce the risk of egg predation and thus increase reproductive success in birds.     

Pregnant female lizards Iberolacerta cyreni adjust refuge use to decrease thermal costs for their body condition and cell-mediated immune response

Lizards often respond to increased predation risk by increasing refuge use, but this strategy may entail a loss of thermoregulatory opportunities, which may lead to a loss of body condition. This may be especially important for pregnant oviparous female lizards, because they need to maintain optimal body temperatures as long as possible to maximize developmental embryos rate until laying. However, little is known about how increased time spent at low temperatures in refuges affects body condition and health state of pregnant female lizards. Furthermore, it is not clear how initial body condition affects refuge use. Female Iberian rock lizards forced to increase time spent at low temperatures showed lower body condition and tended to show lower cell-mediated immune responses than control females. Therefore, the loss of thermoregulatory opportunities seems to be an important cost for pregnant females. Nevertheless, thereafter, when we simulated two repeated predatory attacks, females modified refuge use in relation to their body condition, with females with worse condition decreasing time hidden after attacks. In conclusion, female lizards seemed able to compensate increased predation risk with flexible antipredatory strategies, thus minimizing costs for body condition and health state.     

Vigilance and Collective Detection of Predators in Degus (Octodon degus)

Individuals of social and partially social species typically reduce their vigilance activity when foraging in groups. As a result, per capita risk of predation decreases and individuals allocate more time to foraging and other fitness rewarding activities. Reduction of per capita risk is hypothesized to occur because there are more individuals to detect potential predators. If so, collective (i.e. total) vigilance is expected to increase with foraging group size. Increased surveillance during group foraging may occur if group members scan independently of one another, or sequentially to avoid the overlapping of their vigilance bouts. Intriguingly, such coordinated vigilance assumes that individuals monitor not only the presence, but the vigilance behaviour of group mates. We used seasonal records on time budget and grouping patterns of individually marked degus (Octodon degus), a social rodent, to examine if (a) individual vigilance decreases and/or foraging increases with group size, (b) collective vigilance increases with group size and (c) foraging degus coordinate their vigilance. When foraging, degus decreased their individual vigilance and increased their foraging time when in larger groups. Despite this, degus in larger groups increased their collective vigilance, supporting the hypothesis that socially foraging degus decrease predation risk through an improved ability to detect and escape potential predators. Additionally, patterns of collective vigilance suggested that degus scan independently of each other and so, they do not coordinate their vigilance to prevent its temporal overlapping. This finding does not support that foraging degus monitor the vigilance activity of group mates.     

Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts

Given limited food, prey fishes in a temperate climate must take risks to acquire sufficient reserves for winter and/or to outgrow vulnerability to predation. However, how can we distinguish which selective pressure promotes risk-taking when larger body size is always beneficial? To address this question, we examined patterns of energy allocation in populations of age-0 trout to determine if greater risk-taking corresponds with energy allocation to lipids or to somatic growth. Trout achieved maximum growth rates in all lakes and allocated nearly all of their acquired energy to somatic growth when small in early summer. However, trout in low-food lakes took greater risks to achieve this maximal growth, and therefore incurred high mortality. By late summer, age-0 trout allocated considerable energy to lipids and used previously risky habitats in all lakes. These results indicate that: (i) the size-dependent risk of predation (which is independent of behaviour) promotes risk-taking behaviour of age-0 trout to increase growth and minimize time spent in vulnerable sizes; and (ii) the physiology of energy allocation and behaviour interact to mediate growth/mortality trade-offs for young animals at risk of predation and starvation.     

Conspecific alarm cues, but not predator cues alone, determine antipredator behavior of larval southern marbled newts, Triturus pygmaeus

Predation imposes selection on the ability of prey to recognize and respond to potential threats. Many prey species detect predators via chemoreception, particularly in aquatic environments. Also, chemical cues from injured prey are often perceived as an indication of predation risk. However, because antipredatory behavior can be costly, prey responses should depend on the current level of risk that each predator poses, which may depend on the type of chemical cues detected. We exposed larval newts, Triturus pygmaeus, to chemical cues from predator larval beetles or to alarm cues from conspecific larval newts and examined the behavioral changes of larval newts. Results showed that larval newts reduced activity levels when conspecific alarm cues were present but not when the predator cues alone were present. These results might suggest that larval newts are unable to recognize predator chemicals. To avoid costs of unnecessary antipredatory behaviors, larval newts may benefit by avoiding only predators that represent a current high level of threat, showing only antipredatory responses when they detect conspecific alarm cues indicating that an actual predatory attack has occurred.     

High Antipredatory Efficiency of Insular Lizards: A Warning Signal of Excessive Specimen Collection?

We live-captured lizards on islands in the Gulf of California and the Baja California peninsula mainland, and compared their ability to escape predation. Contrary to expectations, endemic lizard species from uninhabited islands fled from humans earlier and more efficiently than those from peninsular mainland areas. In fact, 58.2% (n=146) of the lizards we tried to capture on the various islands escaped successfully, while this percentage was only 14.4% (n=160) on the peninsular mainland. Separate evidence (e.g., proportion of regenerated tails, low human population at the collection areas, etc.) challenges several potential explanations for the higher antipredatory efficiency of insular lizards (e.g., more predation pressure on islands, habituation to humans on the peninsula, etc.). Instead, we suggest that the ability of insular lizards to avoid predators may be related to harvesting by humans, perhaps due to the value of endemic species as rare taxonomic entities. If this hypothesis is correct, predation-related behavioral changes in rare species could provide early warning signals of their over-exploitation, thus encouraging the adoption of conservation measures.     

Effects of Microhabitat‐Dependent Predation Risk on Vigilance during Intermittent Locomotion in Psammodromus algirus Lizards

Animals should be able to adjust their behavior by tracking changes in predation risk level continuously. Many animals show a pattern of intermittent locomotion with short pauses that may increase detection and vigilance of predators. These locomotor patterns may depend on the microhabitat structure, which affect predation risk levels. We examined in detail in the laboratory the characteristics of spontaneous locomotion, scanning behavior, and the escape performance of Psammodromus algirus lizards moving in two different microhabitats (leaf litter patches and open sand areas). Results showed that in leaf litter, lizards moved at slower speed and had shorter bursts of locomotion both in distance and duration, than in sand substrates. This locomotor pattern allowed lizards to increase scanning rate and total time spent in vigilance behavior. When lizards were forced to flee, they escaped to longer distances and during more time in open sand areas, but lizards were able to attain similar escape speed in the two substrates. Lizards may be able to compensate the cost of moving between different microhabitats with different predation risk by behaviorally changing their locomotor and vigilance patterns. However, complex interactions between the visibility of lizards to predators and the ability of lizards to detect predators, together with the need of attending simultaneously to other conflicting demands, may lead to apparently non‐intuitive solutions in locomotor patterns and the rate of vigilance behavior.