Optimal escape theory predicts escape behaviors beyond flight initiation distance： risk assessment and escape by striped plateau lizards Sceloporus virgatus

Escape theory predicts that flight initiation distance (FID=distance between predator and prey when escape begins) is longer when risk is greater and shorter when escape is more costly. A few tests suggest that escape theory applies to distance fled. Escape models have not addressed stochastic variables, such as probability of fleeing and of entering refuge, but their economic logic might be applicable. Experiments on several risk factors in the lizard Sceloporus virgatus confirmed all predictions for the above escape variables. FID was greater when approach was faster and more direct, for lizards on ground than on trees, for lizards rarely exposed to humans, for the second of two approaches, and when the predator turned toward lizards rather than away. Lizards fled further during rapid and second consecutive approaches. They were more likely to flee when approached directly, when a predator turned toward them, and during second approaches. They were more likely to enter refuge when approached rapidly. A novel finding is that perch height in trees was unrelated to FID because lizards escaped by moving out of sight, then moving up or down unpredictably. These findings add to a growing body of evidence supporting predictions of escape theory for FID and distance fled. They show that two probabilistic aspects of escape are predictable based on relative predation risk levels. Because individuals differ in boldness, the assessed optimal FID and threshold risks for fleeing and entering refuge are exceeded for an increasing proportion of individuals as risk increases[Current Zoology 55(2):123-131,2009].     

Predation Risk and Opportunity Cost of Fleeing While Foraging on Plants Influence Escape Decisions of an Insular Lizard

Cost‐benefit models of escape behaviour predict how close a prey allows a predator to approach [flight initiation distance (FID)] based on cost of not fleeing (predation risk) and cost of fleeing (loss of opportunities). Models for FID have been used with some success to predict distance fled (DF). We studied effects of foraging opportunity cost of fleeing and examined differences between age‐sex groups in the omnivorous Balearic Lizard, Podarcis lilfordi. Balearic lizards forage on the ground for invertebrate prey and climb the thistle Carlina corymbosa to forage on its inflorescences. We studied escape behaviour in three experimental groups, with human beings as simulated predators: lizard foraging above ground on C. corymbosa, foraging on the ground away from thistles and on the ground with cut inflorescences. Flight initiation distance was shorter for lizards with cut inflorescences than for (1) lizards above ground due to the greater risk above ground due to conspicuousness of black lizards on yellow flowers; and (2) lizards on ground away from flowers due to the cost of leaving while feeding. The only age‐sex difference was slightly greater FID for adult males than subadults, presumably because larger adult males are more likely to be attacked by predators. Other potential factors affecting this difference are discussed. Experimental group and age‐sex group did not interact for FID or DF. Because lizards foraging on inflorescences above ground fled to the base of the plants to refuge provided by spiny thistle leaves, their DF was shorter than in the other groups, which fled across the ground, usually without entering refuge. DF did not differ between groups on the ground or among age‐sex groups. The predicted shorter DF for lizards with cut inflorescences than on ground without inflorescences did not occur. We hypothesize that the opportunity cost was small due to the abundance of blooming thistles and that DF may be less sensitive to opportunity cost than FID.     

Ecological factors affecting flight initiation distance in Daurian ground squirrels (Spermophilus dauricus)

More often than not, animals forage under predation risk. Foragers, therefore, face a challenge to balance between two conflicting tasks, namely energy intake and safety. Flight initiation distance (FID, defined as the distance between a prey and a predator when the prey starts to flee) has been widely measured in many taxa to study such economic trade‐offs. However, FID may also be affected by limitations on the prey's ability to detect predators, especially when there is visual obstruction caused by surrounding vegetation. Although both vegetation cover and vegetation height may contribute to such obstruction, the effect of vegetation height on FID has not been well studied. In this study, we explored the effects of vegetation height, vegetation cover and distance to refuge on FID in free‐living Daurian ground squirrels (Spermophilus dauricus) inhabiting a grassland in Inner Mongolia, China. Multiple linear regressions suggested that both vegetation height and distance to refuge significantly affected FID in S. dauricus. Ground squirrels fled earlier when vegetation was low or when foraging farther away from a refuge. No significant effect of vegetation cover on FID was detected. Our results have implications for ecologically based pest control, and FID may be used as an effective and easy‐to‐use behavioral indicator in wildlife management.     

Tail flicking in the black redstart (<Emphasis Type="Italic">Phoenicurus ochruros</Emphasis>) and distance to cover

Tail flicking is a common behavior in many bird species, but its function is often unknown. Apart from intraspecific communication, tail flicking could be used during predator–prey communication, e.g., as a signal of prey vigilance or quality. We studied this behavior in the black redstart (Phoenicurus ochruros), a species that frequently shows tail flicking and is prone to attacks by ambushing predators that hide in cover. Hence, cover might be perceived as dangerous by this species. We hypothesized that flicking should increase with decreasing distance to cover. We counted the number of tail flicks of individuals and measured their distance to the nearest cover for an ambushing predator. We found that distance to cover had a significant effect on tail flicking behavior, as flicking increased with decreasing distance, but found no difference in flicking frequency between adults and juveniles or between sexes. Consequently, tail flicking is unlikely to signal submission or to be sexually selected in the black redstart. Since tail flicking also occurred in the absence of predators, we consider tail flicking in black redstarts to display vigilance and to be directed towards ambushing predators.     

鸟类惊飞距离及其影响因素

惊飞距离(FID)是指捕食者(包括人类)接近目标个体并导致其逃避时,捕食者与目标个体之间的距离。惊飞距离能很好地衡量动物个体在特定环境下的恐惧反应和风险权衡,是研究动物逃避行为的常用指标,并为物种保护提供科学依据。鸟类是研究逃避行为的理想对象,本文综述了影响鸟类惊飞距离的各种因素,可分为3类:栖息地因素(距隐蔽处的距离和生境开阔度等)、鸟类自身因素(生活史、体型和群体大小等)以及与捕食者相关的因素(捕食者的接近方向和速度等)。城市化也会影响鸟类的惊飞距离,导致城市中的鸟类通常比乡村生境的同种鸟类拥有更短的惊飞距离。习惯化、适应和生境选择是解释惊飞距离城乡差异的3种假说。研究鸟类的惊飞距离及其影响因素,有助于理解鸟类的逃避行为及其风险权衡机制,为物种保护中设立合理的缓冲区域及制定有效的保护管理措施提供科学依据。目前国内有关鸟类惊飞距离的研究多为行为观察和单一因素的影响,有待从不同因素的交互作用角度探讨鸟类的逃避行为并用于物种保护。     

Complex Relationships amongst Parasite Load and Escape Behaviour in an Insular Lizard

Economic escape models predict escape decisions of prey which are approached by predators. Flight initiation distance (FID, predator–prey distance when prey begins to flee) and distance fled (DF) are major variables used to characterize escape responses. In optimal escape theory, FID increases as cost of not fleeing also increases. Moreover, FID decreases as cost of fleeing increases, due to lost opportunities to perform activities that may increase fitness. Finally, FID further increases as the prey's fitness increases. Some factors, including parasitism, may affect more than one of these predictors of FID. Initially, parasitized prey may have lower fitness as well as impaired locomotor ability, which would avoid predation and/or reduce their foraging ability, further decreasing the opportunity of fleeing. For example, if parasites decrease body condition, prey fitness is reduced and escape ability may be impaired. Hence, the overall influence of parasitism on FID is difficult to predict. We examined relationships between escape decisions and different traits: parasite load, body size and body condition in the Balearic lizard, Podarcis lilfordi. Lizards that showed higher haemogregarines load had longer FID and shorter DF. Although results did not confirm our initial predictions made on the basis of optimal escape theory, our findings suggest that parasites can alter several aspects of escape behaviour in a complex way.     

Choosing among alternative refuges: Distances and directions

Many prey flee to refuges to escape from approaching predators, but little is known about how they select one among many refuges available. The problem of choice among alternative refuges has not been modeled previously, but a recent model that predicts flight initiation distance (FID = predator–prey distance when escape starts) for a prey fleeing to a refuge provides a basis for predicting which refuge should be chosen. Because fleeing is costly, prey should choose to flee to the refuge permitting the shortest FID. The model predicts that the more distant of two refuges can be favored if it is not too far and if the prey's trajectory to the farther refuge is more away from the predator than the direction to the nearer refuge. The difference in predicted FID between the farther and nearer refuges increases curvilinearly as the interpath angle for the farther refuge increases. The difference in predicted FID between the farther and nearer refuges increases linearly as the distance to the farther refuge increases. An isocline describing where nearer and farther refuges are equally favored shows a negative curvilinear relationship between interpath angle and prey distance to the farther refuge. In the region below the isocline, the farther refuge is favored, whereas above the isocline the prey should flee to the nearer refuge.     

Universal Optimization of Flight Initiation Distance and Habitat-Driven Variation in Escape Tactics in a Namibian Lizard Assemblage

Some aspects of escape predicted by theoretical models are intended to apply universally. For example, flight initiation distance (distance between an approaching predator and prey when escape begins) is predicted from predation risk and the costs of escaping. Escape tactics and refuge selection are not currently predicted by theoretical models, but are expected to vary with structural features of the habitat. One way of studying such variation is to compare aspects of antipredatory behavior among sympatric species that differ in habitat or microhabitat use. In an assemblage of lizards in northwestern Namibia, we conducted experiments to test predictions of escape theory for three risk factors in representatives of three families and observed escape tactics in additional species. As predicted by escape theory, flight initiation distance increased with directness of a predator's approach and predator speed in Agama planiceps, Mabuya acutilabris, and Rhotropus boultoni, and with distance from refuge in M. acutilabris. As predicted by theory, the probability of entering refuge increased with risk in R. boultoni. All available data indicate that flight initiation distance and refuge entry by lizards conform to theoretical predictions. Escape tactics varied greatly as a function of habitat type: (1) arboreal species fled up and around trees and sometimes entered tree holes; (2) saxicolous species used rock crevices as refuges, but differed in tactics prior to entering refuges; and (3) terrestrial species fled into bushes or other vegetation, often to the far sides of them. Some M. acutilabris entered small animal burrows or buried themselves in sand beneath bushes. Escape tactics varied even among congeners in Mabuya, highlighting the important effect of habitat structure on them. Although habitat partitioning has traditionally been viewed as favoring species coexistence, an interesting by‐product appears to be structuring of escape tactics in lizard communities.     

Managing human disturbance: factors influencing flight-initiation distance of birds in a West African nature reserve

Escape behaviour in response to perceived predators can be employed as a guide when designating protected areas around sensitive bird species to minimise the impact of human disturbance. A key measure of escape response is flight-initiation distance (FID), the distance at which a prey animal initiates its escape when approached by a potential predator. We tested the predictions of optimal escape theory by determining the factors that influence FID of bird species in a Nigerian reserved area and its surrounding habitats, and so the potential utility of FID in managing human disturbance on birds, for the first time within a West African context. We tested how FID varied with group size, proximity to vegetation acting as protective cover, levels of human use, and survival rate, and whether these relationships varied by species. We collected 504 FIDs for seven bird species in Amurum Forest Reserve and its surrounding habitats (Jos, Nigeria). The FID was lower in larger groups and when species were closer to protective cover. The FID was lower outside of the protected area because animals in sites with higher levels of human presence and use may become habituated. The FID was higher for species with higher survival, being consistent with predictions from life history theory. Overall, birds perceived humans as a potential threat and responded in accordance to the predictions of optimal escape theory, with FID increasing with increased cost of staying. Reserve managers in Africa could use species- and context-specific FIDs to designate buffer distances for the protection of wildlife from human disturbance.     

When to Run and When to Hide: The Influence of Concealment,Visibility, and Proximity to Refugia on Perceptions of Risk

An animal's ability to avoid predation likely depends on its ability to detect approaching predators, conceal itself, and seek refuge or protection from predators. Habitat, especially vegetation structure, can influence all of these factors concurrently. Binary categorical assessments of habitat as ‘open’ or ‘closed’, however, confound at least two functions of habitat structure that could influence the perceived risk of predation: concealment, which functions to hide an individual, and visibility, which enhances detection of a potential predator. Both can influence predation risk independently and s imultaneously. In this study, we decoupled these functional properties of vegetation and studied the effects of concealment, visibility, and proximity to a refuge on the distance at which pygmy rabbits (Brachylagus idahoensis) fled from an approaching threat (flight initiation distance; FID). Concealment by vegetation decreased perceptions of risk; however, pygmy rabbits exhibited elevated risk at high levels of visibility, regardless of the amount of concealment. Proximity to burrow entrances also influenced perceptions of risk, such that risk was significantly lower when rabbits were on or near burrow systems. Disentangling the functional properties of habitat can provide a more comprehensive understanding of the factors that influence perceived risk and escape behaviors of prey and provide insight into how habitat structure mechanistically relates to predation risk.     

Determinants of sexual differences in escape behavior in lizards of the genus Anolis: a comparative approach

Males and females are known to differ in a whole suite of characteristics,such as morphology, physiology, ecology, and behavior. Intersexualdifferences are generally believed to arise because of differencesin selective pressures on either sex. In this study, we investigatedwhether intersexual differences in escape behavior exist inlizards of the genus Anolis, and whether these could be explainedby intersexual differences in body size and/or microhabitatuse. To do so, we compared the behavioral response to an approachinghuman predator in the field in males and females of 12 Anolisspecies. We found that ecomorphs and sexes differ greatly withrespect to escape behavior. Twig anoles have the shortest approachdistance (i.e., distance between the observer and the lizardwhen it starts fleeing) and final distance (i.e., distance betweenthe observer and the lizard when it stops moving), comparedwith the other ecomorphs. The distance fled, on the contrary,is greatest in twig anoles. Also, females flee less soon andrun over shorter distances than do males. Since twig anolesare considered the most cryptic anoles, and females may be lessconspicuous than males, these results corroborate the idea thatwell camouflaged animals allow predators to come closer. Theinterspecific variation in sexual dimorphism in escape behavior,however, cannot be explained by the interspecific variationin sexual size dimorphism or sexual dimorphism in microhabitatuse. Thus, escape behavior appears determined by different factorsin males and females.     

To run or hide? Age-dependent escape behaviour in the common flat lizard (Platysaurus intermedius wilhelmi)

Flat lizards Platysaurus intermedius wilhelmi occur on small discrete rock outcrops in Mpumalanga Province, South Africa. These rock outcrops are structurally simple and this, combined with the lizard's behaviour (ambush foraging in the open), make them ideal for field studies of anti-predatory behaviour. Lizards were approached in the field and how escape behaviour was influenced by habitat and age-sex class was recorded. Juveniles ( c. 4 months of age) responded quite differently to an approaching human 'predator' compared with adult males and females (which responded similarly). Compared to adults, juveniles allowed a closer approach by the investigator; took longer to find a refuge and therefore fled further; were more likely to remain visible in the open and maintain visual contact with the investigator; and more likely to flee into vegetation when given the opportunity to take refuge in a crevice. We suggest that because a greater suite of predators (including arthropods living in rock crevices) feed on small juvenile lizards, this may affect their choice of refuge and result in the avoidance of crevices when chased. Finally, because juveniles were frequently found on small rock outcrops, the influence of rock outcrop area on anti-predatory behaviour was tested. Escape behaviour (time to refuge) was independent of rock outcrop area.     

Risk Assessment and Withdrawal Behavior by Two Species of Aposematic Poison Frogs, Dendrobates auratus and Oophaga pumilio, on Forest Trails

Many chemically defended prey advertize toxicity to predators by aposematic coloration. When aposematic prey are approached, they often move slowly or not at all, allowing predators to evaluate their unprofitability. Poison frogs (Dendrobatidae) are toxic, aposematically colored, forage openly and diurnally, and are much easier to capture than many palatable frogs. Although protected against diverse predators, they are sometimes attacked and are subjected to injury by large animals without predatory intent. We predicted that they have limited escape behavior, but retain ability to assess and respond to risk. When we approached Dendrobates auratus and Oophaga pumilio on forest trails, both species hopped by the shortest route to the nearer forest edge and stopped there. When approached, D. auratus moved after shorter latency at an angle closer to perpendicular to the forest edge, were more likely to leave the trail, and left the trail sooner with fewer changes in direction after moving a shorter distance than when not approached. In agreement with predictions of optimal escape theory based on risk, flight initiation distance by D. auratus was greater when approached directly than indirectly and rapidly than slowly, and was greater when frogs were in the open than partially concealed. Frogs neither attempted rapid escape nor entered refuges. Both species hopped leisurely and remained visible after stopping. They exhibit the diminished escape behavior of aposematic prey, yet retain the capacity to assess risk and adjust behavior accordingly. Their behavior demonstrates continued need for escape behavior by highly toxic aposematic prey.     

Contagious fear: Escape behavior increases with flock size in European gregarious birds

Flight initiation distance (FID), the distance at which individuals take flight when approached by a potential (human) predator, is a tool for understanding predator–prey interactions. Among the factors affecting FID, tests of effects of group size (i.e., number of potential prey) on FID have yielded contrasting results. Group size or flock size could either affect FID negatively (i.e., the dilution effect caused by the presence of many individuals) or positively (i.e., increased vigilance due to more eyes scanning for predators). These effects may be associated with gregarious species, because such species should be better adapted to exploiting information from other individuals in the group than nongregarious species. Sociality may explain why earlier findings on group size versus FID have yielded different conclusions. Here, we analyzed how flock size affected bird FID in eight European countries. A phylogenetic generalized least square regression model was used to investigate changes in escape behavior of bird species in relation to number of individuals in the flock, starting distance, diet, latitude, and type of habitat. Flock size of different bird species influenced how species responded to perceived threats. We found that gregarious birds reacted to a potential predator earlier (longer FID) when aggregated in large flocks. These results support a higher vigilance arising from many eyes scanning in birds, suggesting that sociality may be a key factor in the evolution of antipredator behavior both in urban and rural areas. Finally, future studies comparing FID must pay explicit attention to the number of individuals in flocks of gregarious species.     

Distance from Water,Sex and Approach Direction Influence Flight Distances Among Habituated Black Swans

In many animals, response to predators occurs at greater distances the further an individual is from a refuge, but this has rarely been investigated in birds. Here, we test the hypothesis that the further from refuge (i.e. water) a foraging black swan Cygnus atratus is situated, the longer its flight initiation distance (FID) in response to a pedestrian approach on land. As predicted, swans situated farther from water exhibited longer FIDs compared with those closer to the shore. In addition, there was the possibility of an interesting interaction effect (p < 0.061) of sex and direction of approach on FID. Whilst males tended to not alter their response in relation to the angle of approach relative to the water, females tended to respond at longer distances, when approached from the shore than when approached from the land or parallel to the shore. This is one of the first reports of sex differences in FIDs for birds, with sex differences only manifesting themselves under certain approach types. Group size, the order of repeated approaches, and time of day did not influence responses, although starting distance of approach was positively related to FID.     

Escape and alerting responses by Balearic lizards (Podarcis lilfordi) to movement and turning direction by nearby predators

Escape theory predicts that prey monitoring an approaching predator delay escape until predation risk outweighs costs of fleeing. However, if a predator is not detected until it is closer than the optimal flight initiation distance (FID = distance between predator and prey when escape begins), escape should begin immediately. Similarly, if a change in a nearby predator’s behavior indicates increased risk, the optimal FID increases, sometimes inducing immediate escape. If a predator that has been standing immobile near a prey suddenly turns toward the prey, greater risk is implied than if the predator turns away. If the immobile predator suddenly moves its foot without turning, it might be launching an attack. Therefore, we predicted that frequency of fleeing and preparation to flee are greater when a predator turns toward than away from prey and that frequency of fleeing when a predator suddenly moves decreases as distance between predator and prey increases. We verified these predictions in the Balearic lizard Podarcis lilfordi in field experiments in which an investigator simulated the predator. Lizards fled and performed alerting responses indicating readiness to flee more frequently when the predator turned toward than away from them, and fled more frequently the nearer the predator.     

Hybridization between two insectivorous bird species and the effect on prey-handling efficiency

Gene flow between closely related species is not always impeded by hybrid inviability or sterility but may be limited by behavioural or ecological factors. European common redstarts, Phoenicurus phoenicurus, and black redstarts, P. ochruros, are insectivorous passerine bird species which regularly interbreed in the wild and produce viable and fertile progeny. Yet, the isolation barriers, which prevent extensive gene flow between these distinct species, are unknown. I studied prey-handling time and efficiency in both species and the F₁-hybrids in captivity. All birds changed prey-handling mode from a single pick to more complex behaviour with increasing prey length and their handling time was a positive function of prey length. Common redstarts tended to handle their prey quicker than black redstarts. Hybrids appeared to be intermediate. However, individual differences were significant, but group membership was not. Handling efficiency decreased with increasing prey length and was determined by individual and family effects. Hybrid females handled their prey as efficient as hybrid males. Small differences in beak morphology could not explain individual differences in prey-handling behaviour. The results of this study suggest that prey-handling in F₁-hybrids is not a postzygotic barrier which prevent gene flow between common and black redstarts in the wild.     

Island tameness: living on islands reduces flight initiation distance

One of Darwin''s most widely known conjectures is that prey are tame on remote islands, where mammalian predators are absent. Many species appear to permit close approach on such islands, but no comparative studies have demonstrated reduced wariness quantified as flight initiation distance (FID; i.e. predator–prey distance when the prey begins to flee) in comparison with mainland relatives. We used the phylogenetic comparative method to assess influence of distance from the mainland and island area on FID of 66 lizard species. Because body size and predator approach speed affect predation risk, we included these as independent variables. Multiple regression showed that FID decreases as distance from mainland increases and is shorter in island than mainland populations. Although FID increased as area increased in some models, collinearity made it difficult to separate effects of area from distance and island occupancy. FID increases as SVL increases and approach speed increases; these effects are statistically independent of effects of distance to mainland and island occupancy. Ordinary least-squares models fit the data better than phylogenetic regressions, indicating little or no phylogenetic signal in residual FID after accounting for the independent variables. Our results demonstrate that island tameness is a real phenomenon in lizards.     

Escape behavior of the green lizard (Lacerta viridis) in the Slovak Karst

The escape behavior of the green lizard (Lacerta viridis) was investigated in natural conditions of the Slovak Karst, Slovakia. The seasonal changes of approach distances and types of escape behavior were monitored for both sexes, also in relation to differences in anthropogenic influence. In our study, the escape behavior of green lizard changed significantly during the season, and differ significantly between localities and in respect to human disturbance. At the beginning of the season, females stayed in close proximity to a refuge and hid immediately after being disturbed. Among males, the distance to and from a refuge was longer and any accessible protrusions were used to hide. The approach distance was greater among males. During the mating period, approach distance for females and males was similar and both sexes hid in a refuge. However, after the mating period, the approach distance for females was decreasing, whereas that of males begun to increase.     

Risk-taking behavior of bull-headed shrikes that recently colonized islands

Individuals which have invaded urbanized environments are reported to engage in riskier behaviors, possibly influenced by the scarcity of predators in urbanized areas. Here, we studied the risk-taking behavior of birds which had invaded a new natural environment, rather than an artificial urban environment, using recently established populations of the bull-headed shrike Lanius bucephalus, which naturally colonized three subtropical islands in Japan. We compared flight initiation distance (FID), the distance at which an individual approached by a human initiates flight, between the islands and the temperate mainland. FID was longer for the insular shrikes compared with the mainland shrikes after controlling for other factors, indicating that the individuals which had invaded a new natural environment had a lower propensity for risk-taking. A possible explanation for these results is that low risk-taking behavior might be adaptive on the islands due to predation by the black rat Rattus rattus, an unfamiliar predator not found in shrike habitats on the temperate mainland. Further studies are needed to examine the nest predation rate, predator species, and nest site selection of these insular shrike populations.