Effects of risk assessment, predator behavior, and habitat on escape behavior in Columbian black-tailed deer

The relationship between preflight risk assessment by prey andthe escape behaviors they perform while fleeing from predatorsis relatively unexplored. To examine this relationship, a humanobserver approached groups of Columbian black-tailed deer (Odocoileushemionus columbianus), varying his behavior to simulate moreor less threatening behavior. We measured the focal deer's angleof escape, distance moved during flight, duration of trottingand stotting behavior, and change in elevation during flight.Analyses revealed positive relationships between the distancemoved during flight and the distance at which they fled. Whenflight was initiated when the approacher was close, deer fledrelatively shorter distances and took flight paths at more acuteangles, a property that would force a real predator to changedirection suddenly. Our results indicate that deer do not compensatefor allowing the observer to approach more closely by fleeinggreater distances. Rather, distance moved and flight initiationdistance are linked by level of reactivity and habituation:more reactive or less habituated deer both flee at a greaterdistance and move away to a greater distance during flight.More threatening behavior by the approacher led to longer durationsof rapid flight behavior (e.g., trotting and stotting), anddeer tended to flee uphill and into taller vegetation, usingthese landscape features as refuge from danger. Finally, weprovide the first evidence for Pitcher's untested "antiambush"hypothesis for the function of stotting and discuss its significance.In general, both preflight predator behavior and habitat featuresinfluence both duration and direction of escape.     

Effects of risk, cost, and their interaction on optimal escape by nonrefuging Bonaire whiptail lizards, Cnemidophorus murinus

Optimal escape theory seeks to explain variation in the distanceto an approaching predator at which the prey initiates escape(flight initiation distance). Flight initiation distance increaseswhen predators pose a greater threat and decreases when escapecosts increase. Although optimal escape theory has been highlysuccessful, its predictions have been tested primarily for speciesthat escape to discrete refuges, and most studies have focusedon single risk or cost factors. We present data from two experimentsin which two risks or a risk and a cost varied in Bonaire whiptaillizards (Cnemidophorus murinus) that escaped without enteringrefuges. Our data verify several predictions about optimal escapefor nonrefuging lizard prey. Two risk factors, speed and directnessof approach by the predator, interacted. Directly approachedlizards had greater flight initiation distances than did indirectlyapproached lizards when approached rapidly, but shorter flightinitiation distances when approached slowly. Flight initiationdistance was shorter in the presence of food and during slowversus rapid approaches, but contrary to expectation, food presenceand approach speed did not interact. This would be explainedif cost curves are nonlinear or if they are parallel ratherthan intersecting when the predator reaches the prey. More empiricalwork is needed to determine which risk and cost factors actadditively and which act synergistically. The absence of interactionbetween the risk and cost factors suggests that cost curveswere nonlinear.     

Factors affecting the escape behaviour of juvenile chinstrap penguins, <Emphasis Type="Italic">Pygoscelis antarctica</Emphasis>, in response to human disturbance

Human disturbance can be considered to have similar effects as predation risk for animals. Thus, when disturbed, animal responses are likely to follow the same economic principles used by prey when encountering predators. We simulated predator attacks with different characteristics and in different situations to study the factors that determine the escape response of 1-year-old chinstrap penguins. The results indicate that 1-year-old penguins adjusted their escape behaviour according to the level of risk posed by the researcher acting as a potential predator. When 1-year-old penguins were close to a breeding subcolony, they started to escape later, and fled shorter distances, at lower speeds, and not fleeing directly into the subcolony. This contrasts with their fleeing behaviour far from subcolonies, when penguins fled sooner, for longer, and faster, and in a direction that maximized the distance between themselves and the experimenter, by fleeing directly away from the experimenter. This might suggest the existence of a trade-off between fleeing from the predator and avoiding entering the subcolony where 1-year-old penguins will receive aggressive responses from breeding adults. The type of approach was not important in deciding when to flee. However, penguins did escape for longer distances and faster when approached directly, showing that penguins were able to assess risk level based on predator behaviour. Our findings may have implications for management of penguin colonies visited by tourists. The delimitation of buffer areas and advice on how tourists should behave when approaching penguins might arise from studies of the factors that affect risk assessment of penguins.     

Predator–prey interactions,flight initiation distance and brain size

Prey avoid being eaten by assessing the risk posed by approaching predators and responding accordingly. Such an assessment may result in prey–predator communication and signalling, which entail further monitoring of the predator by prey. An early antipredator response may provide potential prey with a selective advantage, although this benefit comes at the cost of disturbance in terms of lost foraging opportunities and increased energy expenditure. Therefore, it may pay prey to assess approaching predators and determine the likelihood of attack before fleeing. Given that many approaching potential predators are detected visually, we hypothesized that species with relatively large eyes would be able to detect an approaching predator from afar. Furthermore, we hypothesized that monitoring of predators by potential prey relies on evaluation through information processing by the brain. Therefore, species with relatively larger brains for their body size should be better able to monitor the intentions of a predator, delay flight for longer and hence have shorter flight initiation distances than species with smaller brains. Indeed, flight initiation distances increased with relative eye size and decreased with relative brain size in a comparative study of 107 species of birds. In addition, flight initiation distance increased independently with size of the cerebellum, which plays a key role in motor control. These results are consistent with cognitive monitoring as an antipredator behaviour that does not result in the fastest possible, but rather the least expensive escape flights. Therefore, antipredator behaviour may have coevolved with the size of sense organs, brains and compartments of the brain involved in responses to risk of predation.     

Flush early and avoid the rush? It may depend on where you stand

Optimal escape theory predicts that animals should flee at an optimal distance from the approaching predator (flight initiation distance, FID). However, FID usually increases with increasing alert distance (AD) or starting distance (SD). As an explanation for this pattern, the “flush early and avoid the rush” (FEAR) hypothesis states that prey should escape soon after detecting an approaching predator due to the cost of continuously monitoring risk. However, the positive relationship observed may also result from a mathematical artefact. Meanwhile, it is unknown whether animals would consistently follow this rule in different environmental contexts. We explored escape behaviours in light-vented bulbuls (Pycnonotus sinensis) perched at different heights. FID generally increased with increasing AD and decreasing perch height. The positive relationships between AD and FID were outside the 95% confidence levels of simulated slopes from Monte Carlo simulations, suggesting that the relationships observed reflect biological effects rather than merely a mathematical artefact. Increasing perch height was also associated with longer buffer distance (defined as FID minus AD or SD), suggesting that the birds tend to delay their flush after detecting an approaching predator when perched high. The effects of environmental contexts (and the associated predation risk) on the AD-FID relationship should be considered when performing inter-specific comparisons or meta-analyses.     

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].     

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.     

Risks Associated with Predator Immobility,Movement Direction,and Turn Direction Similarly Affect Pursuit‐Deterrent Signaling and Escape by Zebra‐Tailed Lizards (Callisaurus draconoides)

Some prey may signal to deter pursuit by predators. Because deterrence is not needed when risk is low or useful when capture is imminent, most signaling should occur at intermediate risk. Probability of fleeing increases with risk for various risk factors. At low–intermediate risk, more frequent signaling should occur as assessed risk associated with risk factors increases. I examined the effects of three risk factors related to immobility and movement by a predator: standing distance (distance from prey to immobile predator), directions of walking, and turning by the predator. Risk is greater when the predator stands nearer, walks toward prey vs. retreating, and turns toward prey vs. away. In the lizard Callisaurus draconoides, which signals by elevating and waving its tail, signaling was more frequent before fleeing when I stood immobile at the shorter of two distances. All the lizards fled when I walked toward them, regardless of standing distance. Fewer fled when I moved away and only at the shorter standing distance. At the shorter standing distance, signal probability was high and did not differ between movement directions. At the longer standing distance, fewer lizards signaled and only when I moved toward them. Patterns of response of signaling and escape to combinations of standing distance and turn direction were qualitatively identical. When I turned away from lizards, none displayed or fled at the longer standing distance. At the shorter standing distance, probabilities of displaying and fleeing were higher when I turned toward than away from lizards. Standing distance affected signaling interactively with directions of movement and turning in manners readily interpretable from risk. Signaling was affected by risk associated with all factors, being absent or infrequent at both high‐ and low‐risk levels but frequent at intermediate risk, strengthening evidence for pursuit‐deterrent signaling.     

Effects of Single‐ and Mixed‐Species Group Composition on the Flight Initiation Distances of Plains and Grevy's Zebras

Zebras, as prey species, attend to the behavior of nearby conspecifics and heterospecifics when making decisions to flee from predators. Plains zebras (Equus quagga) and Grevy's zebras (E. grevyi) frequently form mixed‐species groups in zones where their ranges overlap in Kenya. Although anecdotal observations suggest that Plains zebras are more flighty around humans than Grevy's zebras are, this has not been empirically confirmed, and relatively little is known about how they may influence each other's flight behavior. We addressed these questions by examining the flight initiation distances (FIDs) of Plains and Grevy's zebras in single‐species and mixed‐species groups from an approaching human. One target individual per group was approached steadily on foot, with start distance, alert distance, and FID recorded from this target. Using start distance and alert distance separately as covariates, 22 Plains zebras in single‐species groups exhibited a significantly longer mean FID than 15 Grevy's zebras in single‐species groups. The FIDs of 7 Plains zebras and 5 Grevy's zebras tested in mixed‐species groups were virtually equivalent and intermediate to those of Plains and Grevy's zebras in single‐species groups, suggesting a bidirectional moderating influence of heterospecifics on risk assessment. This effect was most pronounced for Plains zebras in mixed‐species groups that exhibited an FID that was significantly shorter than that of Plains zebras in single‐species groups. Our findings underscore the importance of recognizing that related equids may be differently impacted by anthropogenic stress.     

Flight initiation distance and escape behavior in the black redstart (Phoenicurus ochruros)

There are many anti‐predatory escape strategies in animals. A well‐established method to assess escape behavior is the flight initiation distance (FID), which is the distance between prey and predator at which an animal flees. Previous studies in various species throughout the animal kingdom have shown that group size, urbanization, and distance to refuge and body mass affect FID. In most species, FID increases if body mass, group size or distance to refuge decreases. However, how age and sexual dimorphism affect FID is rather unknown. Here, we assess the escape behavior and FID of the black redstart (Phoenicurus ochruros), a small turdid passerine. When approached by a human, males initiated flights later, that is allowing a closer approach than females. Males of this species are more conspicuous, and therefore, may exhibit aposematism to deter potential predators or are less fearful than females. Additionally, juveniles fled at shorter distances and fled to lower heights than adults. Lastly, concerning escape strategy, black redstarts, unless other passerine birds, fled less often into cover, but rather onto open or elevated spots. Black redstarts are especially prone to predation by ambushing predators that might hide in cover. Hence, this species most likely has a higher chance of escaping by fleeing to an open spot rather than to a potentially risky cover.     

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.     

Magnitude of food reward affects escape behavior and acceptable risk in Balearic lizards, Podarcis lilfordi

During encounters with predators, prey must balance the degreeof risk against the loss of fitness-enhancing benefits suchas feeding and social activities. Most studies of tradeoffsbetween risk and cost of escaping have measured flight initiationdistance and time to emerge from refuge, for which theory providesrobustly supported predictions. Tradeoffs involving other aspectsof encounters, including distance fled and time between escapeand return to a food source, have received little theoreticalor empirical attention. By adapting models of flight initiationdistance and time between entry into refuge and emergence, wepredict effects of predation risk and cost on distance fledand time to return to a source of benefit after fleeing. Actingas simulated predators that approached at a fixed speed, weconducted an experimental field study to test the hypothesesthat flight initiation distance, distance fled, and time toreturn to food by Balearic lizards (Podarcis lilfordi) decreasewith the presence and amount of insect food. Predictions ofthe models were strongly supported, including those for distancefled and return time, but predictions for other cost factorsand predation risk factors remain to be tested.     

Detection and Avoidance of Predators in White-Tailed Deer (Odocoileus virginianus) and Mule Deer (O. hemionus)

In this paper, we investigate the relationship between early detection of predators and predator avoidance in white-tailed deer ( Odocoileus virginianus ) and mule deer ( O. hemionus ), two closely related species that differ in their habitat preferences and in their anti-predator behavior. We used observations of coyotes ( Canis latrans ) hunting deer to test whether the distance at which white-tails and mule deer alerted to coyotes was related to their vulnerability to predation. Coyote encounters with both species were more likely to escalate when deer alerted at shorter distances. However, coyote encounters with mule deer progressed further than encounters with white-tails that alerted at the same distance, and this was not due to species differences in group size or habitat. We then conducted an experiment in which a person approached groups of deer to compare the detection abilities and the form of alert response for white-tails and mule deer, and for age groups within each species. Mule deer alerted to the approacher at longer distances than white-tails, even after controlling for variables that were potentially confounding. Adult females of both species alerted sooner than conspecific juveniles. Mule deer almost always looked directly at the approacher as their initial response, whereas white-tails were more likely to flee or to look in another direction with no indication that they pinpointed the approacher during the trial. Mule deer may have evolved the ability to detect predators earlier than white-tails as an adaptation to their more open habitats, or because they need more time to coordinate subsequent anti-predator defenses.     

Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.     

Distance-to-cover and the escape decisions of an African cichlid fish,Melanochromis chipokae

Synopsis The risk to a prey individual in an encounter with a predator increases as the distance to protective cover increases. Prey should therefore initiate their flight to cover at longer distances from an approaching predator (i.e., sooner) and/or flee at greater velocities, as the distance to cover increases. These predictions were tested with an African cichlid fish, Melanochromis chipokae presented with a looming stimulus simulating an attacking predator. The fish varied their flight initiation distance as predicted, but there was no significant effect of distance-to-cover on escape velocity. Nevertheless, the cichlids appeared to choose a combination of flight initiation distance and escape velocity which ensured they reached cover with a constant temporal margin of safety.     

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.     

Influence of predation pressure on the escape behaviour of Podarcis muralis lizards

Relationships between predator avoidance behaviour and predation pressure were investigated in the wall lizard, Podarcis muralis. The wariness of lizards belonging to high (1185m) and low elevation (308m) populations under two different predation pressure levels was compared. Wall lizards belonging to the lowland population experienced greater predation pressure than those belonging to the highland population. Lizards belonging to the population under higher predation pressure had higher frequency of refuge use, and had longer flight initiation distances (i.e. the distance lizards allowed the observer to approach before fleeing). In contrast, neither the distance fled (i.e. the total distance they fled in one continuous movement from the lizard's initial position until hiding or stopping at a safe distance) nor the distance to the nearest refuge were significantly different between populations. Escape responses were independent of ambient temperature in the lowland population, but animals belonging to the highland population had longer flight initiation distances when the ambient temperatures were higher. These findings suggest that predator avoidance behaviour may vary with predation pressure.     

Influence of Some Potential Predation Risk Factors and Interaction between Predation Risk and Cost of Fleeing on Escape by the Lizard Sceloporus virgatus

Escape theory predicts that flight initiation distance (predator–prey distance when escape begins) increases as predation risk increases and decreases as cost of fleeing increases. Scant information is available about the effects of some putative predation risk factors and about interaction between simultaneously operating risk and cost of fleeing factors on flight initiation distance and distance fled. By simulating an approaching predator, I studied the effects of body temperature (BT), distance to nearest refuge, and eye contact with a predator, as well as simultaneous effects of predator approach speed and female presence/absence on escape behavior by a small ectothermic vertebrate, the lizard Sceloporus virgatus. Flight initiation distance decreased as BT increased, presumably because running speed increases as BT increases, facilitating escape. Distance to nearest refuge was unrelated to BT or flight initiation distance. Substrate temperature was only marginally related, and air temperature was not related to flight initiation distance. Eye contact did not affect flight initiation during indirect approaches that bypassed lizards by a minimum of 1 m, but an effect of eye contact found in other studies during direct approach might occur. Predator approach speed and presence of a female interactively affected flight initiation distance, which increased as speed increased and decreased when a female was present. In the presence of a female, flight initiation distance was far shorter than when no female was present. The high cost of forgoing a mating opportunity accounts for the interaction because the difference between female presence and absence is greater when risk is greater.     

Fear in animals: a meta-analysis and review of risk assessment

The amount of risk animals perceive in a given circumstance (i.e. their degree of 'fear') is a difficult motivational state to study. While many studies have used flight initiation distance as a proxy for fearfulness and examined the factors influencing the decision to flee, there is no general understanding of the relative importance of these factors. By identifying factors with large effect sizes, we can determine whether anti-predator strategies reduce fear, and we gain a unique perspective on the coevolution of predator and anti-predator behaviour. Based on an extensive review and formal meta-analysis, we found that predator traits that were associated with greater risk (speed, size, directness of approach), increased prey distance to refuge and experience with predators consistently amplified the perception of risk (in terms of flight initiation distance). While fish tolerated closer approach when in larger schools, other taxa had greater flight initiation distances when in larger groups. The presence of armoured and cryptic morphologies decreased perception of risk, but body temperature in lizards had no robust effect on flight initiation distance. We find that selection generally acts on prey to be sensitive to predator behaviour, as well as on prey to modify their behaviour and morphology.     

Flight Distance and Eye Size in Birds

Larger eyes capture more information from the environment than small eyes, but also require more brain space for information processing. Therefore, individuals have to optimize the size of their eyes, leading to the prediction that larger eyes should have evolved in species with greater benefits from large eyes, such as species subject to intense predation risk. In a comparative analysis of 97 bird species, we found that species that fled at longer distances from an approaching potential predator indeed had relatively large eyes for their body size. In contrast, there was no indication that large eyes had evolved in species living in secluded habitats, or in species eating mobile prey. These findings are consistent with the assumption that eye size is labile and can evolve in response to changing predator environments. They also suggest that eye size may act as a constraint on optimal anti‐predator behavior, if the predator community changes as a consequence of introductions or invasions.