Anti-Predator Benefits of Mixed-Species Groups of Cowtail Stingrays (Pastinachus sephen) and Whiprays (Himantura uarnak) at Rest

Heterospecific grouping can sometimes provide greater antipredator benefits to individuals than grouping with conspecifics. We explored the potential benefits of mixed‐species group resting in the cowtail stingray, Pastinachus sephen, and the reticulate whipray, Himantura uarnak, in Shark Bay, Western Australia. From focal follow data on individual resting choice, we first ascertained that cowtails preferred to rest with heterospecifics, as they chose to settle next to whiprays more often than to pass them (with the opposite trend observed for conspecifics). In addition, we determined from filmed boat transects that cowtails formed larger hetero‐ than monospecific groups despite the low density of whiprays. Possible benefits accrued by the cowtail were investigated in terms of predator protection. Whiprays responded earlier than cowtails to a mock predator (boat), and were most frequently the first to respond when in a mixed group. Thus, cowtails may benefit from grouping with heterospecifics by receiving earlier warning of a predator's approach. A decoy experiment using model whiprays demonstrated that cowtails were more willing to rest with models with relatively longer tails (controlled for body size). Ray tails, which are equipped with a mechanoreceptor capable of detecting predators, may constitute an important secondary means of predator detection aside from early warning. This contention is supported by the observation that stingrays mainly form resting groups when their visual ability is likely to be impaired by environmental conditions, and that tail length is negatively allometric with body size, suggesting its importance in vulnerable early life stages. If the efficacy of the mechanoreceptor increases with tail length, then cowtails may have further improved their likelihood of detecting predators by grouping with longer‐tailed heterospecifics.     

Sex and social costs of escaping in the striped plateau lizard Sceloporus virgatus

As a predator approaches, prey base decisions about when toflee on a balance between degree of predation risk and costsof escaping. Lost opportunities to perform activities that mayincrease fitness are major escape costs. Paramount among theseare chances to increase fitness by courting and mating and bydriving away sexual rivals. Because sexual selection imposesdifferent social demands on the sexes, social opportunitiescan have different consequences for males and females, but effectsof sex differences in social opportunity costs on escape behaviorare unknown. We conducted a field experiment showing that malestriped plateau lizards (Sceloporus virgatus) given the opportunityto court or perform aggressive behavior permit closer approachbefore fleeing, but females do not. Males allowed a simulatedpredator to approach closer before initiating escape if a tetheredmale or female rather than a control stimulus was introducedto them, but females initiated escape at similar distances inall conditions. For males, a trade-off between the greater predationrisk accepted before fleeing due to the likelihood of enhancingfitness by sexual or aggressive behavior accounts for closerapproach allowed in the presence of conspecifics. Mating opportunitiesare not limiting for females in most species and females oftenhave little to gain by interacting aggressively with other females.Therefore, presence of a conspecific male or female may notjustify taking greater risk. Results confirm the predictionof optimal escape theory that flight initiation decreases ascost of escaping increases. The sex difference in effect ofpresence of conspecifics on flight initiation distance is aconsequence of the sex difference in costs of escaping.     

Costs of Refuge Use Affect Escape Decisions of Iberian Rock Lizards Lacerta monticola

Theoretical models of anti-predator escape behaviour suggest that prey may adjust their escape response such that the optimal flight distance is the point at which the costs of staying exceed the costs of fleeing. Anti-predatory decisions should be made based also on consequences for long-term expected fitness, such as the costs of refuge use. For example, in lizards, the maintenance of an optimal body temperature is essential to maximize physiological processes. However, if unfavourable thermal conditions of refuges can decrease the body temperature of lizards, their escape decision should be influenced by refuge conditions. Analyses of the variation in flight distances and emergence latency from a refuge for the lizard Lacerta monticola under two different predation risk levels, and their relationship with the thermal environment, supported these predictions. When risk increased, lizards had longer emergence latencies, and thus costs of refuge use increased (a greater loss of time and body temperature). In the low-risk situation, lizards that were farther from the refuge had longer flight distances, whereas thermal conditions were less important. When risk increased, lizards had longer flight distances when refuges were farther off, but also when the external heating rate and the refuge cooling rate were lower. The results suggest that, in addition to the risk of predation, expected long-term fitness costs of refuges can also affect escape decisions.     

Risk taking by singing males

The distance at which an individual flees from a potential predatorrepresents a measure of risk taking. If individuals are engagedin another activity that might affect fitness, trade-offs betweenthe fitness benefits of flight and the other activity shoulddetermine the nearest distance of approach by a predator. Ina comparative analysis of birds, flight distance representeda reliable measure of risk of predation by the sparrowhawk Accipiternisus that increased with decreasing flight distance acrossspecies. To test the hypothesis that singing males adjustedtheir risk taking to the costs and benefits of early flight,we compared the flight distance of singing and nonsinging birdsto an approaching human observing with a binocular. Singingbirds on average fled at a greater distance than nonsingingbirds, implying that singing birds took small risks. We useda standardized measure of difference in flight distance betweensinging and nonsinging individuals to investigate factors affectinginterspecific variation in risk taking. Species that used moreexposed song posts (sites used for singing) took smaller risksthan species with less exposed song posts. Species that sufferedfrom higher levels of parasitism as reflected by the prevalenceof Plasmodium, but not by 3 other genera of blood parasites,took greater risks during singing compared with nonsinging activities.Likewise, species with high circulating levels of natural antibodies,and hence a history of natural selection caused by bacteriatook relatively greater risks during singing than species withfew natural antibodies. These findings suggest that risks takenby singing birds have been molded by natural and sexual selection,and that risk taking represents a compromise between the costsand benefits of flight from a potential predator.     

Plesiomorphic Escape Decisions in Cryptic Horned Lizards (Phrynosoma) Having Highly Derived Antipredatory Defenses

Escape theory predicts that the probability of fleeing and flight initiation distance (predator–prey distance when escape begins) increase as predation risk increases and decrease as escape cost increases. These factors may apply even to highly cryptic species that sometimes must flee. Horned lizards (Phrynosoma) rely on crypsis because of coloration, flattened body form, and lateral fringe scales that reduce detectability. At close range they sometimes squirt blood‐containing noxious substances and defend themselves with cranial spines. These antipredatory traits are highly derived, but little is known about the escape behavior of horned lizards. Of particular interest is whether their escape decisions bear the same relationships to predation risk and opportunity costs of escaping as in typical prey lacking such derived defenses. We investigated the effects of repeated attack and direction of predator turning on P. cornutum and of opportunity cost of fleeing during a social encounter in P. modestum. Flight initiation distance was greater for the second of two successive approaches and probability of fleeing decreased as distance between the turning predator and prey increased, but was greater when the predator turned toward than away from a lizard. Flight initiation distance was shorter during social encounters than when lizards were solitary. For all variables studied, risk assessment by horned lizards conforms to the predictions of escape theory and is similar to that in other prey despite their specialized defenses. Our findings show that these specialized, derived defenses coexist with a taxonomically widespread, plesiomorphic method of making escape decisions. They suggest that escape theory based on costs and benefits, as intended, applies very generally, even to highly cryptic prey that have specialized defense mechanisms.     

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.     

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.     

Dynamic Risk Assessment: Prey Rapidly Adjust Flight Initiation Distance to Changes in Predator Approach Speed

The pre‐eminent model of flight initiation distance assumes that the function relating predation risk to distance between predator and prey is constant. However, the risk–distance function can change dramatically during approaches by predators. Changes in predator behavior during approach and in availability of benefits (e.g. food or potential mates) may alter risks and/or costs during encounters. Thus, prey should be able to respond appropriately to changes in cues to risk, such as predator approach speed. Under the assumption that prey assess risk in real time, it was predicted that flight initiation distance (distance between predator and prey when escape begins) decreases when approach speed increases and increases when approach speed decreases during an encounter. Effects of single, abrupt changes from slower to faster approach or the reverse were studied in a lizard, Anolis lineatopus. Flight initiation distances were determined solely by final approach speed, being nearly identical for: (1) continuously fast approaches and approaches initially at the slower and finally at the faster speed and (2) for continuously slower approaches and approaches initially at faster and finally at slower speed. Escape should be adjusted to match changes in risk and cost caused by changes in predator behavior, ability to escape, and costs of escape as attacks unfold. A recent model by Broom and Ruxton [Behavioural Ecology (2004) vol. 16, pp. 534—540] predicts that cryptic prey should stay motionless until detected, then flee immediately. Our results suggest that current escape models can be applied to prey escape strategies when cues to risk change, by assuming that prey base decisions on the current relationship between risk and distance. Empirical studies are needed to test predictions concerning continuous risk assessment.     

Risk‐taking and the evolution of mechanisms for rapid escape from predators

Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human. This behavioural measure of risk‐taking reflects the risk of being captured by real predators, and it correlates with a range of life history traits, as expected if flight distance optimizes risk of predation. Given that FID provides information on risk of predation, we should expect that physiological and morphological mechanisms that facilitate flight and escape predict interspecific variation in flight distance. Haematocrit is a measure of packed red blood cell volume and as such indicates the oxygen transport ability and hence the flight muscle contracting reaction of an individual. Therefore, we predicted that species with short flight distances, that allow close proximity between a potential prey individual and a predator, would have high haematocrit. Furthermore, we predicted that species with large wing areas and hence relatively low costs of flight and species with large aspect ratios and hence high manoeuvrability would have evolved long flight speed. Consistent with these predictions, we found in a sample of 63 species of birds that species with long flight distances for their body size had low levels of haematocrit and large wing areas and aspect ratios. These findings provide evidence consistent with the evolution of risk‐taking behaviour being underpinned by physiological and morphological mechanisms that facilitate escape from predators and add to our understanding of predator–prey coevolution.     

Aerodynamics and Energetics of Intermittent Flight in Birds

Hypotheses explaining the use of intermittent bounding and undulatingflight modes in birds are considered. Existing theoretical modelsof intermittent flight have assumed that the animal flies ata constant speed throughout. They predict that mean mechanicalpower in undulating (flap-gliding) flight is reduced comparedto steady flight over a broad range of speeds, but is reducedin bounding flight only at very high flight speeds. Lift generatedby the bird's body or tail has a small effect on power, butis insufficient to explain observations of bounding at intermediateflight speeds. Measurements on starlings Sturnus vulgaris inundulating flight in a wind tunnel show that flight speed variesby around ±1 m/sec during a flap-glide cycle. Dynamicenergy is used to quantify flight performance, and reveals thatthe geometry of the flight path depends upon wingbeat kinematics,and that neither flapping nor gliding phases are at constantspeed and angle to the horizontal. The bird gains both kineticand potential energy during the flapping phases. A new theoreticalmodel indicates that such speed variation can give significantsavings in mechanical power in both bounding and undulatingflight. Alternative hypotheses for intermittent flight includea gearing mechanism, based on duty factor, mediating musclepower or force output against aerodynamic requirements. Thiscould explain the use of bounding flight in hovering and climbingin small passerines. Both bounding and undulating confer otheradaptive benefits; undulating may be primitive in birds, butbounding may have evolved in response to flight performanceoptimization, or to factors such as unpredictability in responseto predation.     

The ontogeny of escape behavior,locomotor performance,and the hind limb in Sceloporus woodi

Flight initiation distance describes the distance at which an animal flees during the approach of a predator. This distance presumably reflects the tradeoff between the benefits of fleeing versus the benefits of remaining stationary. Throughout ontogeny, the costs and benefits of flight may change substantially due to growth-related changes in sprint speed; thus ontogenetic variation in flight initiation distance may be substantial. If escape velocity is essential for surviving predator encounters, then juveniles should either tolerate short flight initiation distances and rely on crypsis, or should have high flight initiation distances to remain far away from their predators. We examined this hypothesis in a small, short-lived lizard (Sceloporus woodi). Flight initiation distance and escape velocity were recorded on an ontogenetic series of lizards in the field. Maximal running velocity was also quantified in a laboratory raceway to establish if escape velocities in the field compared with maximal velocities as measured in the lab. Finally a subset of individuals was used to quantify how muscle and limb size scale with body size throughout ontogeny. Flight initiation distance increased with body size; larger animals had higher flight initiation distances. Small lizards had short flight initiation distances and remained immobile longer, thus relying on crypsis for concealment. Escape velocity in the field did not vary with body size, yet maximum velocity in the lab did increase with size. Hind limb morphology scaled isometrically with body size. Isometric scaling of the hind limb elements and its musculature, coupled with similarities in sprint and escape velocity across ontogeny, demonstrate that smaller S. woodi must rely on crypsis to avoid predator encounters, whereas adults alter their behavior via larger flight initiation distance and lower (presumably less expensive) escape velocities.     

Historical influence of predation pressure on escape by Podarcis lizards in the Balearic Islands

Island tameness (reduced escape behaviour on islands where prey have experienced prolonged relaxation of predation pressure) is known in several taxa, although the relationships between recent predation pressure and escape on islands are poorly known. We investigated escape by numerous populations exposed to differing predation pressure of two sister species of Podarcis lizards in the Balearic Islands. Our main findings are that flight initiation distance was greater in Podarcis pityusensis than Podarcis lilfordi and increased as predation pressure increased in P. pityusensis. Island tameness led to extinction of P. lilfordi on Menorca and Mallorca following anthropogenic introduction of predators; this species is extant only on nearby islets. The lack of relationship between recent predation pressure and flight initiation distance in P. lilfordi indicates that the historically acquired deficit in the ability to adjust escape behaviour to predation pressure still exists. Podarcis pityusensis, which was exposed to greater natural predation pressure before human introduction of predators, survives on Ibiza and Formentera, as well as on islets. Retention of the ability to respond to predation pressure is consistent with our finding that flight initiation distance increases as predation pressure increases among current populations. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Nuptial Coloration and Mate Guarding Affect Escape Decisions of Male Lizards Psammodromus algirus

Males of many species show conspicuous breeding colours that are important for status signalling, but that may decrease crypsis and increase predation risk. However, prey may adjust their escape response, such that the optimal distance at which an animal starts to flee (approach distance) would be the point where the costs of staying exceed the cost of fleeing. We examined in the field the escape response of Psammodromus algirus lizards, to test the hypothesis that more conspicuous old males, showing orange nuptial coloration on most of the head, which presumably have a higher probability of being detected (i.e. increased costs of staying), have longer approach distances, independent of other environmental variables. As predicted, old brightly coloured males had significantly longer approach and flight distances than young dull males, and young males had longer ones than females. In contrast, neither the distance to the nearest refuge nor the air temperature when the lizards escaped were significantly different. In addition, although male and female lizards differed in their use of microhabitats, old and young males did not differ. We also found that old males guarding a female (i.e. increased costs of fleeing) had shorter approach distances than old males that were found alone.     

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.     

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.     

Up,up, and away: relative importance of horizontal and vertical escape from predators for survival and senescence

Animals fleeing a potential predator can escape horizontally or vertically, although vertical flight is more expensive than horizontal flight. The ability to escape in three dimensions by flying animals has been hypothesized to result in greater survival and eventually slower senescence than in animals only fleeing in two dimensions. In a comparative study of flight initiation distance in 69 species of birds when approached by a human, I found that the amount of variance explained by flight initiation distance was more than four times as large for the horizontal than the vertical component of perch height when taking flight. The slope of the relationship between horizontal distance and flight initiation distance (horizontal slope) increased with increasing body mass across species, whereas the slope of the relationship between vertical distance and flight initiation distance (vertical slope) decreased with increasing body mass. Therefore, there was a negative relationship between horizontal and vertical slope, although this negative relationship was significantly less steep than expected for a perfect trade‐off. The horizontal slope decreased with increasing density of the habitat from grassland over shrub to forest, whereas that was not the case for the vertical slope. Adult survival rate increased and rate of senescence (longevity adjusted for survival rate, body mass and sampling effort) decreased with increasing vertical, but not with horizontal slope, consistent with the prediction that vertical escape indeed provides a means of reducing the impact of predation.     

Habitat affects escape behaviour and alarm calling in Common Starlings Sturnus vulgaris

Animals should adapt their escape behaviour to both physical and social surroundings in order to maximize their probability of survival. Cover can be both obstructive, reducing the visibility of the surroundings and hindering escape, and protective, providing refuge. We investigated how the provision of cover (long grass) affected (1) the escape behaviour and (2) the alarm call behaviour of Common Starlings Sturnus vulgaris responding to a model hawk during a simulated attack. Starlings always retreated away from the predator and sometimes alarm-called. Their escape trajectory was close to the ground when escaping in long grass, which could be explained by either tall swards hindering take-off or such swards being used as protective cover. On short grass their escape trajectory was much steeper (> 45°). We also investigated the use of alarm calls in Starlings according to predictions arising from the costs and benefits to callers and receivers. Callers could benefit from using alarm calls through dilution or confusion if their use initiates flock departures, thus reducing their probability of being targeted. If there is no cost to the producer of alarm calls we predicted that detectors should call at all times to gain these benefits (i.e. irrespective of grass length), but if their use is costly we predicted that they would be used only when the benefits outstrip the costs. In this case we would predict that alarm calls would be given when other (visual) signals were impaired on long grass but not when they were effective on short grass. Starlings used alarm calls on long grass when visibility was reduced more frequently than on short grass, suggesting that calling has a cost to the producer. The contrasting escape strategies of Starlings in relation to a relatively small (10 cm) change in grass height demonstrates the potential importance of habitat structure in determining predation risk.     

Continuous cycling of grouped vs. solitary strategy frequencies in a predator-prey model

We present a model of predator and prey grouping strategies using game theory. As predators respond strategically to prey behavior and vice versa, the model is based on a co-evolution approach. Focusing on the "many eyes-many mouths" trade-off, this model considers the benefits and costs of being in a group for hunting predators and foraging prey: predators in a group have more hunting success than solitary predators but they have to share the prey captured; prey in a group face a lower risk of predation but greater competition for resources than lone prey. The analysis of the model shows that the intersections of four curves define distinct areas in the parameter space, corresponding to different strategies used by predators and prey at equilibrium. The model predictions are in accordance with empirical evidence that an open habitat encourages group living, and that low risks of predation favor lone prey. Under some conditions, continuous cycling of the relative frequencies of the different strategies may occur. In this situation, the proportions of grouped vs. solitary predators and prey oscillate over time.     

The effect of human disturbance and flock composition on the flight distances of waterfowl species

Flocking bird species tolerate an approaching human up to a certain distance. We measured this distance, i.e., flight distance, to an approaching small boat for 11 waterfowl species. The flight distances correlated positively with flock size and species diversity (Shannon index H′) in species that showed relatively short flight distances when they were in a single-species flock. However, we did not observe such a correlation for single-species flocks that showed relatively long flight distances. Only pochards (Aythya ferina), a species with large individual variation in flight distances, showed a positive correlation between flight distance and flock size in both single- and multispecies flocks. Flight distance seemed to be affected by usage of the water area: flight distances tended to be longer for waterfowl species that use a water area for foraging than for those that use it primarily for resting. Thus, the behavior of actively foraging species may be more affected by human disturbances than that of resting species. Received: March 10, 2001 / Accepted: May 22, 2001