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.     

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.     

Avian Risk Assessment: Effects of Perching Height and Detectability

We studied two components of predator risk assessment in birds. While many species are limited to seeking safety under cover or under ground, some birds can fly away from their predators and escape to trees. If birds in fact ‘feel’ safer (e.g. perceive less risk) in trees, we would expect them to tolerate closer approach by a potential terrestrial predator. Another component of safety is at which point the animal detects an approaching threat, which we expected to increase with eye size, assuming eye size is a surrogate for visual acuity. We used the distance birds moved away from an approaching human [flight initiation distance (FID)] as a metric to determine whether birds associated a lower risk of predation by being in trees, and we used the distance at which birds first displayed alert behaviors from an approaching human (alert distance) to determine if birds with larger eyes had higher detection distances. Although some species were affected by tree height, we found no clear pattern that birds assessed themselves to be at a lower risk of predation when they were ≥3 m above the ground compared with being <3 m above ground. In the 10 species for which height had any significant effect on FID, birds ≥3 m off the ground had greater FIDs in six species, but the remaining three species had the opposite response. While we found a significant positive relationship between eye size and alert distance in 23 species, the relationship was not present in a phylogenetic analysis using independent contrasts, which suggests that the apparent relationship was influenced strongly by the association between the studied species. Together, these results suggest that birds do not obviously associate being in a tree with safety, and that variations in visual acuity, per se, cannot be used as a general indicator of differences in alert distances, as previously suggested in the literature.     

Escape from predators and genetic variance in birds

Predation is a common cause of death in numerous organisms, and a host of antipredator defences have evolved. Such defences often have a genetic background as shown by significant heritability and microevolutionary responses towards weaker defences in the absence of predators. Flight initiation distance (FID) is the distance at which an individual animal takes flight when approached by a human, and hence, it reflects the life‐history compromise between risk of predation and the benefits of foraging. Here, we analysed FID in 128 species of birds in relation to three measures of genetic variation, band sharing coefficient for minisatellites, observed heterozygosity and inbreeding coefficient for microsatellites in order to test whether FID was positively correlated with genetic variation. We found consistently shorter FID for a given body size in the presence of high band sharing coefficients, low heterozygosity and high inbreeding coefficients in phylogenetic analyses after controlling statistically for potentially confounding variables. These findings imply that antipredator behaviour is related to genetic variance. We predict that many threatened species with low genetic variability will show reduced antipredator behaviour and that subsequent predator‐induced reductions in abundance may contribute to unfavourable population trends for such species.     

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.     

Empirical studies of escape behavior find mixed support for the race for life model

Escape theory has been exceptionally successful in conceptualizing and accurately predicting effects of numerous factors that affect predation risk and explaining variation in flight initiation distance (FID; predator–prey distance when escape begins). Less explored is the relative orientation of an approaching predator, prey, and its eventual refuge. The relationship between an approaching threat and its refuge can be expressed as an angle we call the “interpath angle” or “Φ,” which describes the angle between the paths of predator and prey to the prey’s refuge and thus expresses the degree to which prey must run toward an approaching predator. In general, we might expect that prey would escape at greater distances if they must flee toward a predator to reach its burrow. The “race for life” model makes formal predictions about how Φ should affect FID. We evaluated the model by studying escape decisions in yellow-bellied marmots Marmota flaviventer, a species which flees to burrows. We found support for some of the model’s predictions, yet the relationship between Φ and FID was less clear. Marmots may not assess Φ in a continuous fashion; but we found that binning angle into 4 45° bins explained a similar amount of variation as models that analyzed angle continuously. Future studies of Φ, especially those that focus on how different species perceive relative orientation, will likely enhance our understanding of its importance in flight decisions.     

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.     

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

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

Cost/benefit analysis of group and solitary resting in the cowtail stingray, Pastinachus sephen

Unless a safe refuge is found where predation threats are negligible,resting poses risks for many animals, necessitating risk managementstrategies. The adult cowtail stingray (Pastinachus sephen)of Shark Bay, Western Australia, is a solitarily foraging animalthat facultatively groups when resting on shallow, inshore sandflats. We hypothesized that environmental conditions influencethe propensity of cowtails to group due to the limited abilityto detect predators visually in certain conditions. We thenexplored the possible benefits of grouping, such as bodily protection,early warning, and predator confusion, in conjunction with potentialgrouping costs, such as increased interference when initiatingflight and decreased escape speeds. Our study revealed thatin poor underwater visibility (due to turbidity and/or low ambientlight levels), cowtails primarily rest in small groups (threerays). Tests of flight initiation distance to a mock predatordemonstrated that solitary cowtail escape distances are significantlyshorter in poor than in good underwater visibility conditions.As to grouping benefits, filmed boat transects revealed thatcowtails most often arrange themselves in a rosette position,possibly as a means to protect their bodies and expose theirtails. The first cowtail in a group initiates flight to a mockpredator at a significantly greater distance than a solitarycowtail, and grouped cowtails escape an approaching boat ina significantly more cohesive manner than a simulated groupof escaping individual rays. Grouped cowtails exhibit behaviorsthat would impede immediate flight after detection. As a result,grouped rays escape a boat at significantly slower speeds thansolitary cowtails. Results from this study demonstrate thatthe interplay between costs and benefits of grouped and solitaryresting under differing environmental conditions is driven bydifferences in perceived predation risk and ultimately reflectedin the facultative grouping behavior of this species.     

Persistence of antipredator behavior in an island population of California quail

Island populations may provide unique insights into the evolution and persistence of antipredator behavior. If antipredator behavior is costly and islands have reduced predation risk, then we expect the reduction or loss of antipredator behavior on islands. However, if even a single predator remains, the multipredator hypothesis predicts that antipredator behaviors will be conserved. We compared the flight initiation distances (FID) of California quail (Callipepla californica) on Santa Catalina Island (a location with reduced predation pressure) with quail on the mainland. We found no differences in FID between mainland and island quail. However, despite employing consistent testing methods, the starting distance from which quail were approached was significantly reduced for quail studied on the island when compared with quail studied on the mainland. Our results are consistent with the multipredator hypothesis because, while the island population had substantially fewer predators, some predators remained and some antipredator behavior persisted.     

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

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

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

Island tameness: living on islands reduces flight initiation distance

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

Behavioral and physiological adjustments to new predators in an endemic island species,the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.     

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].     

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.     

Basal metabolic rate and risk‐taking behaviour in birds

Basal metabolic rate (BMR) constitutes the minimal metabolic rate in the zone of thermo‐neutrality, where heat production is not elevated for temperature regulation. BMR thus constitutes the minimum metabolic rate that is required for maintenance. Interspecific variation in BMR in birds is correlated with food habits, climate, habitat, flight activity, torpor, altitude, and migration, although the selective forces involved in the evolution of these presumed adaptations are not always obvious. I suggest that BMR constitutes the minimum level required for maintenance, and that variation in this minimum level reflects the fitness costs and benefits in terms of ability to respond to selective agents like predators, implying that an elevated level of BMR is a cost of wariness towards predators. This hypothesis predicts a positive relationship between BMR and measures of risk taking such as flight initiation distance (FID) of individuals approached by a potential predator. Consistent with this suggestion, I show in a comparative analysis of 76 bird species that species with higher BMR for their body mass have longer FID when approached by a potential predator. This effect was independent of potentially confounding variables and similarity among species due to common phylogenetic descent. These results imply that BMR is positively related to risk‐taking behaviour, and that predation constitutes a neglected factor in the evolution of BMR.     

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.     

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.     

Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana

For the past 5 to 15 million years, marine iguanas (Amblyrhynchus cristatus), endemic to the Galápagos archipelago, experienced relaxed predation pressure and consequently show negligible anti-predator behavior. However, over the past few decades introduced feral cats and dogs started to prey on iguanas on some of the islands. We investigated experimentally whether behavioral and endocrine anti-predator responses changed in response to predator introduction. We hypothesized that flight initiation distances (FID) and corticosterone (CORT) concentrations should increase in affected populations to cope with the novel predators. Populations of marine iguanas reacted differentially to simulated predator approach depending on whether or not they were previously naturally exposed to introduced predators. FIDs were larger at sites with predation than at sites without predation. Furthermore, the occurrence of new predators was associated with increased stress-induced CORT levels in marine iguanas. In addition, age was a strong predictor of variation in FID and CORT levels. Juveniles, which are generally more threatened by predators compared to adults, showed larger FIDs and higher CORT baseline levels as well as higher stress-induced levels than adults. The results demonstrate that this naive island species shows behavioral and physiological plasticity associated with actual predation pressure, a trait that is presumably adaptive. However, the adjustments in FID are not sufficient to cope with the novel predators. We suggest that low behavioral plasticity in the face of introduced predators may drive many island species to extinction.