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.     

Phi Index: A New Metric to Test the Flush Early and Avoid the Rush Hypothesis

Optimal escape theory states that animals should counterbalance the costs and benefits of flight when escaping from a potential predator. However, in apparent contradiction with this well-established optimality model, birds and mammals generally initiate escape soon after beginning to monitor an approaching threat, a phenomena codified as the “Flush Early and Avoid the Rush” (FEAR) hypothesis. Typically, the FEAR hypothesis is tested using correlational statistics and is supported when there is a strong relationship between the distance at which an individual first responds behaviorally to an approaching predator (alert distance, AD), and its flight initiation distance (the distance at which it flees the approaching predator, FID). However, such correlational statistics are both inadequate to analyze relationships constrained by an envelope (such as that in the AD-FID relationship) and are sensitive to outliers with high leverage, which can lead one to erroneous conclusions. To overcome these statistical concerns we develop the phi index (Φ), a distribution-free metric to evaluate the goodness of fit of a 1∶1 relationship in a constraint envelope (the prediction of the FEAR hypothesis). Using both simulation and empirical data, we conclude that Φ is superior to traditional correlational analyses because it explicitly tests the FEAR prediction, is robust to outliers, and it controls for the disproportionate influence of observations from large predictor values (caused by the constrained envelope in AD-FID relationship). Importantly, by analyzing the empirical data we corroborate the strong effect that alertness has on flight as stated by the FEAR hypothesis.     

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.     

Danger Comes from All Fronts: Predator-Dependent Escape Tactics of Túngara Frogs

The escape response of an organism is generally its last line of defense against a predator. Because the effectiveness of an escape varies with the approach behaviour of the predator, it should be advantageous for prey to alter their escape trajectories depending on the mode of predator attack. To test this hypothesis we examined the escape responses of a single prey species, the ground-dwelling túngara frog (Engystomops pustulosus), to disparate predators approaching from different spatial planes: a terrestrial predator (snake) and an aerial predator (bat). Túngara frogs showed consistently distinct escape responses when attacked by terrestrial versus aerial predators. The frogs fled away from the snake models (Median: 131°). In stark contrast, the frogs moved toward the bat models (Median: 27°); effectively undercutting the bat’s flight path. Our results reveal that prey escape trajectories reflect the specificity of their predators’ attacks. This study emphasizes the flexibility of strategies performed by prey to outcompete predators with diverse modes of attack.     

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.     

Effect of Risk on Aspects of Escape Behavior by a Lizard, Holbrookia propinqua, in Relation to Optimal Escape Theory

Prey must balance gains from activities such as foraging and social behavior with predation risk. Optimal escape theory has been successful in predicting escape behavior of prey under a range of risk and cost factors. The optimal approach distance, the distance from the predator at which prey should begin to flee, occurs when risk equals cost. Optimal escape theory predicts that for a fixed cost, the approach distance increases as risk increases. It makes no predictions about approach distance for prey in refuges that provide only partial protection or about escape variables other than approach distance, such as the likelihood of stopping before entering refuge and escape speed. By experimentally simulating a predator approaching keeled earless lizards, Holbrookia propinqua, the predictions of optimal escape theory for two risk factors, predator approach speed and directness of approach were tested. In addition, predictions that the likelihood of fleeing into refuge without stopping and the speed of escape runs increase with risk, in this case predator approach speed, and that lizards in incompletely protective refuges permit closer approach than lizards not in refuges were also tested. Approach distance increased with predator approach speed and directness of approach, confirming predictions of optimal escape theory. Lizards were more likely to enter refuge and ran faster when approached rapidly, verifying that predation risk affects escape decisions by the lizards for escape variables not included in optimal escape theory. They allowed closer approach when in incompletely protective refuges than when in the open, confirming the prediction that risk affects escape decisions while in refuge. Optimal escape theory has been highly successful, but testing it has led to relative neglect of important aspects of escape other than approach distance.     

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.     

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.     

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].     

The influence of distance to burrow on flight initiation distance in the woodchuck, Marmota monax

We used woodchucks (Marmota monax) to test predictions of acost-benefit model of antipredator behavior that flight initiationdistance would increase with distance to refuge and with predatorapproach velocity. We also examined the effects of distanceto refuge and predator approach velocity on escape velocityand on both temporal and spatial margin of safety (expectedtime and distance between predator and burrow at the time ofthe woodchuck's arrival). The observer, assumed to be perceivedas a potential predator, approached juvenile woodchucks fromthe direction opposite to the burrow at a slow (1.24 m/s) orfast (1.79 m/s) walking pace. When the woodchuck started toflee, the observer recorded the woodchuck's distance from theobserver and from its burrow, the time spent running, and whetherthe woodchuck stopped before reaching its burrow. Flight initiationdistance increased consistendy with distance to the burrow overthe entire observed range (0–25 m) but was not significantlyaffected by observer approach velocity. Escape velocity wasnot significantly influenced by the observer approach velocityand was approximately constant over the range of 2–25m, but was slower for woodchucks less than 2 m from their burrows.Both temporal and spatial margins of safety increased with distancefrom the burrow. The temporal margin of safety increased withdistance from the burrow more rapidly for slow than for fastobserver approach velocity. Woodchucks fleeing from greaterthan 2 m usually stopped near the burrow before entering, butthose from closer distances usually entered directly. Theseresults support the assumption that antipredator behavior issensitive to the costs and benefits of alternative escape decisions.     

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.     

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.     

An alternative theoretical approach to escape decision-making: the role of visual cues

Escape enables prey to avoid an approaching predator. The escape decision-making process has traditionally been interpreted using theoretical models that consider ultimate explanations based on the cost/benefit paradigm. Ultimate approaches, however, suffer from inseparable extra-assumptions due to an inability to accurately parameterize the model's variables and their interactive relationships. In this study, we propose a mathematical model that uses intensity of predator-mediated visual stimuli as a basic cue for the escape response. We consider looming stimuli (i.e. expanding retinal image of the moving predator) as a cue to flight initiation distance (FID; distance at which escape begins) of incubating Mallards (Anas platyrhynchos). We then examine the relationship between FID, vegetation cover and directness of predator trajectory, and fit the resultant model to experimental data. As predicted by the model, vegetation concealment and directness of predator trajectory interact, with FID decreasing with increased concealment during a direct approach toward prey, but not during a tangential approach. Thus, we show that a simple proximate expectation, which involves only visual processing of a moving predator, may explain interactive effects of environmental and predator-induced variables on an escape response. We assume that our proximate approach, which offers a plausible and parsimonious explanation for variation in FID, may serve as an evolutionary background for traditional, ultimate explanations and should be incorporated into interpretation of escape behavior.     

Optimal flight initiation distance

Decisions regarding flight initiation distance have received scant theoretical attention. A graphical model by Ydenberg and Dill (1986. The economics of fleeing from predators. Adv. Stud. Behav. 16, 229-249) that has guided research for the past 20 years specifies when escape begins. In the model, a prey detects a predator, monitors its approach until costs of escape and of remaining are equal, and then flees. The distance between predator and prey when escape is initiated (approach distance = flight initiation distance) occurs where decreasing cost of remaining and increasing cost of fleeing intersect. We argue that prey fleeing as predicted cannot maximize fitness because the best prey can do is break even during an encounter. We develop two optimality models, one applying when all expected future contribution to fitness (residual reproductive value) is lost if the prey dies, the other when any fitness gained (increase in expected RRV) during the encounter is retained after death. Both models predict optimal flight initiation distance from initial expected fitness, benefits obtainable during encounters, costs of escaping, and probability of being killed. Predictions match extensively verified predictions of Ydenberg and Dill's (1986) model. Our main conclusion is that optimality models are preferable to break-even models because they permit fitness maximization, offer many new testable predictions, and allow assessment of prey decisions in many naturally occurring situations through modification of benefit, escape cost, and risk functions.     

Does Locomotor Ability Influence Flight Initiation Distance in Yellow‐Bellied Marmots?

Flight initiation distance (FID) is the distance between a potential threat and the point at which a potential prey flees. Animals may modify their FID to compensate for increased risk generated by external/extrinsic factors such as habitat type, visibility, group size, time of year, predator‐approach velocity, and distance to burrow, as well as internal/intrinsic factors such as physical condition, body temperature, crypsis, and morphological antipredator defenses. The intrinsic speed at which an animal can escape a predator is a factor that should influence FID. We studied the relationship between an individual's intrinsic escape speed and FID in yellow‐bellied marmots (Marmota flaviventris) to determine whether marmots compensated for slower escape speeds by fleeing at greater distances. We found no evidence of risk compensation. Rather, we found that slower marmots tolerated closer approaches. This behavioral syndrome may be explained by a coevolution of FID and escape speed in determining an individual's antipredator behavior, an idea upon which we expand.     

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.     

Direct Look from a Predator Shortens the Risk-Assessment Time by Prey

Decision making process is an important component of information use by animals and has already been studied in natural situations. Decision making takes time, which is expressed as a cost in evolutionary explanations of decision making abilities of animals. However, the duration of information assessment and decision making process has not been measured in a natural situation. Here, we use responses of wild magpies (Pica pica) to predictably approaching humans to demonstrate that, regardless of whether the bird perceived high (decided to fly away) or low (resumed foraging) threat level, the bird assessed the situation faster when approaching humans looked directly at it than when the humans were not directly looking at it. This indicates that prey is able to extract more information about the predator’s intentions and to respond sooner when the predator is continuously (“intently”) looking at the prey. The results generally illustrate how an increase of information available to an individual leads to a shorter assessment and decision making process, confirming one of central tenets of psychology of information use in a wild bird species in its natural habitat.     

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.     

Hunted Woolly Monkeys (Lagothrix poeppigii) Show Threat-Sensitive Responses to Human Presence

Responding only to individuals of a predator species which display threatening behaviour allows prey species to minimise energy expenditure and other costs of predator avoidance, such as disruption of feeding. The threat sensitivity hypothesis predicts such behaviour in prey species. If hunted animals are unable to distinguish dangerous humans from non-dangerous humans, human hunting is likely to have a greater effect on prey populations as all human encounters should lead to predator avoidance, increasing stress and creating opportunity costs for exploited populations. We test the threat sensitivity hypothesis in wild Poeppigi''s woolly monkeys (Lagothrix poeppigii) in Yasuní National Park, Ecuador, by presenting human models engaging in one of three behaviours “hunting”, “gathering” or “researching”. These experiments were conducted at two sites with differing hunting pressures. Visibility, movement and vocalisations were recorded and results from two sites showed that groups changed their behaviours after being exposed to humans, and did so in different ways depending on the behaviour of the human model. Results at the site with higher hunting pressure were consistent with predictions based on the threat sensitivity hypothesis. Although results at the site with lower hunting pressure were not consistent with the results at the site with higher hunting pressure, groups at this site also showed differential responses to different human behaviours. These results provide evidence of threat-sensitive predator avoidance in hunted primates, which may allow them to conserve both time and energy when encountering humans which pose no threat.