Antipredator Vigilance Research Articles

The evolution of different forms of sociality: behavioral mechanisms and eco-evolutionary feedback.

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from “leader-follower” societies to “fission-fusion” societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.

Innovative problem solving in nonhuman animals: the effects of group size revisited

Sociality is associated with a variety of costs and benefits, one of which can be to increase the likelihood of individuals solving novel problems. Several hypotheses explaining why groups show higher innovative problem-solving efficiencies than individuals alone have been proposed including the sharing of antipredator vigilance and the pool-of-competence effect, whereby larger groups containing a more diverse range of individuals are more likely to contain individuals with the skills necessary to solve the particular problem at hand. Interference between group members may cause groups to have lower problem solving abilities, however. Using a simulation approach, we model the shape of the relationship between group-level problem-solving probability and group size across a range of facilitation and inhibition scenarios, various population distributions of problem solving, and a task requiring 1 action or 2 actions to be solved. Simulations showed that both sharing of antipredator vigilance and the addition of competent individuals to an existing group lead to positive relationships between group-level problem solving and group size that reach 100% solving probability, whereas interference effects generate group-solving probabilities that rise to a maximum and decrease again, generating a group size for which problem solving is maximized. In contrast, both inhibition and facilitation scenarios generate identical patterns of individual efficiencies. Our results have important implications for our ability to understand the mechanisms that underpin group-size effects on problem solving in nonhumans.

Predators, food and social context shape the types of vigilance exhibited by kangaroos

Vigilance in prey species can serve many purposes, including predator detection and monitoring other group members, and is generally thought to impose a cost due to reduced food intake. However, previous studies have shown that herbivores are able to reduce the foraging cost of vigilance by chewing their food during vigilance bouts (‘vigilance with chewing’, as compared to ‘vigilance without chewing’). How predation risk, food availability and competition affect both the functions and the foraging costs of vigilance remains an open question. We studied female eastern grey kangaroos, Macropus giganteus, during winter and summer, when available food supplies were poor and rich, respectively, to investigate how group size, distance to cover, proximity between foragers and food patch quality affected decisions of foraging female kangaroos to exhibit antipredator or social vigilance, distinguishing vigilance with and without chewing. The use of antipredator vigilance was mainly driven by the perception of predation risk, and antipredator vigilance without chewing decreased with increased group size whereas antipredator vigilance with chewing increased nonlinearly with group size in winter. Distance to cover affected both forms of antipredator vigilance in summer only but there was no effect of nearest-neighbour distance. Social vigilance was affected positively by group size, and distance between foragers affected social vigilance without chewing positively, particularly in winter, and social vigilance with chewing negatively. Finally, patch quality increased the use of social vigilance with chewing in both seasons and decreased the use of antipredator vigilance with chewing in winter. This study provides new information on how animals make decisions about the functions and foraging costs of vigilance and allows a better understanding of how social foragers respond to an ever-changing environment.

Antipredator vigilance decreases with food density in staging flocks of Semipalmated Sandpipers (Calidris pusilla)

When animals face time constraints, antipredator vigilance is expected to decrease in patches with higher food density. Indeed, sacrifices in safety are worthwhile in rich food patches that allow substantial foraging gains in response to a decrease in vigilance. This prediction has received little empirical attention. I tested this prediction in fall-staging Semipalmated Sandpipers (Calidris pusilla (L., 1766)) using the frequency of looks while foraging as a proxy for vigilance. Fall-staging sandpipers face time constraints, as individuals must accumulate fat rapidly before undertaking their long migration south. Controlling for known correlates of vigilance, such as distance to obstructive cover, bird density, and position in the flock, the frequency of looks decreased as predicted when the density of food in a patch was higher. That vigilance can vary with food density is relevant for observational studies of vigilance. When food density is positively correlated with group size, food density can become a confounding factor in the well-known negative relationship between vigilance and group size.

Intra-sexual variability in feeding behaviour of a mountain ungulate: size matters

Many studies comparing the behaviour of individuals of different genders or species showed that animal body mass and forage quality/quantity are key elements of the foraging ecology of herbivores. Since body mass could also influence the animal’s sensitivity to predation risk, its vigilance behaviour should consequently be affected. Alpine ibex (Capra ibex) is characterised by a strong dimorphism among males of different ages, thus representing an ideal case study for testing the Jarman-Bell principle, avoiding possibly misleading effects resulting from the comparison between different species or genders. We analysed the fine-scale foraging behaviour of male ibex in order to assess the effect of body mass and the effects of vegetation quality/quantity on both foraging and vigilance behaviour. Our results showed that smaller males were more selective than larger ones, on account of their lower capability of digesting plant. Smaller males scanned the environment more frequently than larger ones. Male ibex grazed more selectively in sites with high quality forage and their bite rate increased as forage biomass decreased. Vigilance frequency increased with increasing forage biomass as, under these circumstances, ibex are able to prolong anti-predator vigilance while chewing bites that have already been cropped. Our findings highlight the effects of body mass per se on both foraging and anti-predator behaviours in herbivores, thus supporting the Jarman-Bell principle. Foraging can arguably be considered a very flexible behaviour with high evolutionary relevance as it enables herbivores to optimally adjust their total energy intake under varying conditions of food resources.

Sex-related differences in the trade-off between foraging and vigilance in a granivorous forager.

The relationship between intake rate and food density can provide the foundation for models that predict the spatiotemporal distribution of organisms across a range of resource densities. The functional response, describing the relationship between resource density and intake rate is often interpreted mechanistically as the relationships between times spend searching and handling. While several functional response models incorporate anti-predator vigilance (defined here as an interruption of feeding or some other activity to visually scan the environment, directed mainly towards detecting potential predators), the impacts of environmental factors influencing directly anti-predator vigilance remains unclear. We examined the combined effects of different scenarios of predation risk and food density on time allocation between foraging and anti-predator vigilance in a granivorous species. We experimentally exposed Skylarks to various cover heights and seed densities, and measured individual time budget and pecking and intake rates. Our results indicated that time devoted to different activities varied as a function of both seed density and cover height. Foraging time increased with seed density for all cover heights. Conversely, an increased cover height resulted in a decreased foraging time. Contrary to males, the decreased proportion of time spent foraging did not translate into a foraging disadvantage for females. When vegetation height was higher, females maintained similar pecking and intake rates compared to intermediate levels, while males consistently decreased their energy gain. This difference in anti-predator responses suggests a sexually mediated strategy in the food-safety trade-off: when resource density is high a females would adopt a camouflage strategy while an escape strategy would be adopted by males. In other words, males would leave risky-areas, whereas females would stay when resource density is high. Our results suggest that increased predation risk might generate sexually mediated behavioural responses that functional response models should perhaps better consider in the future.

Tolerance of human approaches by Common Mynas along an urban-rural gradient

Successful urban colonisation by birds requires tolerance of many disturbances and avoidance of chronic stress and major disruption to critical activities. Habituation may be involved in acquiring tolerance of human proximity, in which case tolerance should vary with the degree of opportunity to learn that most humans do not present a threat and should therefore vary with human population density. We studied Common Mynas (Acridotheres tristis) in the urban, suburban, peri-urban and surrounding rural zones of Melbourne, Australia, to determine whether flight-initiation distance (FID) and time allocated to anti-predator vigilance increased along this gradient from the urban to the rural zone. This gradient encompassed a 143-fold variation in average human population density during daylight hours. Urban and suburban Mynas had a 2.3-5.7 times shorter FID, were 1.6-2.5 times less likely to retreat by flying and were 1.9-3.1 times more likely to flee >5 m than their peri-urban and rural conspecifics. Fleeing behaviour was not strongly correlated with estimated human population density, but exhibited an apparent ‘step’ in response at the suburban-peri-urban divide. Vigilance effort did not vary significantly between zones. This suggested that habituation did not occur with respect to surveillance for people, although surveillance presumably encompassed other predators too. Similar foraging effort and rates of food acquisition among zones could suggest that food abundance per individual was similar in urban and rural environments for Common Mynas, although this requires direct measurement.

Determinants of vigilance in a reintroduced population of Père David’s deer

Abstract After being kept in captivity and isolated from natural predators for more than 1,200 years, Père David’s deer has been reintroduced in China and now occurs in a reserve where human activity is the only potential threat. Antipredator vigilance is an important component of survival for many prey animals in their natural habitat. Do deer still adjust vigilance as a function of risk after such a long period of relaxed predation pressure? Here, we examined vigilance levels in Père David’s deer groups as a function of group size, sex and level of human disturbance. The results showed that individual vigilance significantly decreased with group size in all-female groups but not in all-males or mixed-sex groups. In rutting season, males compete with one another and harass females, and we argue that vigilance is partly aimed at threatening males and that such vigilance increases with group size. This explains why overall vigilance did not vary with group size for males in general and for females in mixed-sex groups. Vigilance increased in more disturbed areas but in in male deer only. The results indicate that despite relaxed predation pressure over centuries, Père David’s deer can still adjust antipredator responses as a function of perceived risk. Such information may become useful in the rewilding programme now under way for this species in China.

Individual variation in vigilance in female eastern grey kangaroos

For herbivores, vigilance usually involves a trade-off with foraging, and a further trade-off between antipredator and social vigilance. Thus individual variation in vigilance may result in significant fitness consequences. We used mixed-effects models to document individual variation in vigilance in wild adult female eastern grey kangaroos (Macropus giganteus) in Queensland, Australia. We tested the effects of group size, presence of adult males and wind on vigilance patterns and variation by analysing 399 five-minute samples on 31 individually identified females who were foraging on the periphery of groups. We determined the proportion of time that individuals spent vigilant, and the proportions of vigilance time spent in social versus antipredator vigilance and in low- versus high-intensity vigilance postures. The proportion of time females spent vigilant decreased with increasing group size but was not affected by wind speed or male presence, while the amount of their vigilance time spent in social vigilance was affected by interactions among the variables. After controlling for these effects, 13 females’ vigilance patterns were significantly different from the population mean. Individual variation was also found in vigilance postures used and the effect of male presence. Understanding individual variation in vigilance is important for understanding individuals’ antipredator and social strategies.

Social Familiarity Reduces Reaction Times and Enhances Survival of Group-Living Predatory Mites under the Risk of Predation

BackgroundSocial familiarity, which is based on the ability to recognise familiar conspecific individuals following prior association, may affect all major life activities of group-living animals such as foraging, reproduction and anti-predator behaviours. A scarcely experimentally tested explanation why social familiarity is beneficial for group-living animals is provided by limited attention theory. Limited attention theory postulates that focusing on a given task, such as inspection and assessment of unfamiliar group members, has cognitive and associated physiological and behavioural costs with respect to the attention paid to other tasks, such as anti-predator vigilance and response. Accordingly, we hypothesised that social familiarity enhances the anti-predator success of group-living predatory mites, Phytoseiulus persimilis, confronted with an intraguild predator, the predatory mite Amblyseius andersoni.Methodology/Principal FindingsWe videotaped and analysed the response of two P. persimilis larvae, held in familiar or unfamiliar pairs, to attacks by a gravid A. andersoni female, using the behavioural analyses software EthoVision Pro®. Familiar larvae were more frequently close together, reacted more quickly to predator attacks, survived more predator encounters and survived longer than unfamiliar larvae.SignificanceIn line with the predictions of limited attention theory, we suggest that social familiarity improves anti-predator behaviours because it allows prey to shift attention to other tasks rather than group member assessment.

The Effects of Group Size and Reproductive Status on Vigilance in Captive Callithrix jacchus

Previous work on mammals and birds has often demonstrated a negative relationship between group size and individual vigilance. However, this relationship has received only weak support in nonhuman primates. This result may be due to the failure to distinguish different forms of vigilance such as antipredatory vigilance and social monitoring. Here, we tested the effects of group size, reproductive status (breeding vs. nonbreeding), and sex on antipredatory vigilance and social monitoring in captive common marmosets (Callithrix jacchus). Behavioral observations using one-zero sampling were conducted on adult members of three captive groups of small, medium, and large size. Data were analyzed using a series of general linear models (GLMs) analyses of covariance (ANCOVAs). We found an overall negative group size effect on antipredatory vigilance and that breeders, especially breeding males, were significantly more vigilant than nonbreeders. Conversely, we found that social monitoring increased with group size. Unlike the results for antipredatory vigilance, neither breeders and nonbreeders nor males and females differed in their amounts of social monitoring. However, the effect of group size appeared to differ for nonbreeding males compared to all other adults. Our results generally support the idea that individuals in larger groups are safer with breeding males likely playing a prominent role in protection from predation. The increase in social monitoring may be related to increased reproductive competition with the presence of adult offspring, but future studies need to clarify the target of social monitoring in both breeders and nonbreeders. Overall, the study underlines the importance of distinguishing different forms of vigilance and other factors as they may confound the effects of group size on antipredatory vigilance.

Foraging success in a wild species of bird varies depending on which eye is used for anti-predator vigilance

Brain lateralisation in animals with laterally placed eyes often leads to preferential eye use for ecologically relevant tasks such as monitoring predators and companions. Few studies of preferential eye use have been conducted in the wild and it is not clear if such preferences in the wild are widespread, how individuals can benefit from them, and which ecological factors influence their evolution. In a wild species of bird the extent to which foraging success varied depending on which eye is used during concomitant anti-predator vigilance was examined. When foraging in open mudflats, semipalmated sandpipers (Calidris pusilla) are frequently exposed to predation attempts by falcons (Falco spp) that originate from the tree cover bordering mudflats. Sandpipers spread along the receding tideline and can face the riskier side of their habitat primarily with the left or the right eye as they forage. If foraging is mostly incompatible with vigilance, the rate at which prey items are collected should decrease when birds use their less-preferred eye to scan cover. If foraging and vigilance can be carried out simultaneously, time spent foraging should not be affected but the efficiency with which their burrowing amphipod prey are located may be reduced, thus leading to decreased capture rate. Birds facing the riskier side of the habitat with their right eye captured significantly more prey than those scanning the same side with their left eye. Specialised eye use in sandpipers may allow individuals to perform simultaneous tasks, such as foraging and vigilance, more efficiently.

Behavioural transition probabilities in dugongs change with habitat and predator presence: implications for sirenian conservation

Although not widely appreciated, prey can manage predation risk by modifying the sequence of their behavioural states. We explored this phenomenon in dugongs (Dugong dugon) subject to spatially and temporally variable risk of tiger shark (Galeocerdo cuvier) predation in Shark Bay, Australia. Dugong behaviour was assayed using focal follows and organised into sequences of foraging, resting, and travelling bouts. We used log-linear analysis to test for sequence differences in relation to habitat (deep, shallow) and predation danger (sharks present, largely absent). Dugongs modified their behavioural sequences between periods of high and low shark abundance: those at risk alternated more frequently between foraging, which constrains anti-predator vigilance, and travelling, which facilitates predator detection. Dugongs also avoided continuous series of resting bouts, during which awareness is reduced, when sharks were present. These changes were only observed in relatively dangerous shallow habitat, which is hunted disproportionately by tiger sharks; behavioural responses to sharks in deep habitat were modest. We conclude that dugongs in risky habitat resort to safer behavioural sequences in response to sharks. Given that human disturbance and predators are perceived similarly by many species, some forms of vessel interaction could compromise the fitness of sirenians by eliciting similar behavioural adjustment.

Understanding selection for long necks in different taxa

There has been recent discussion about the evolutionary pressures underlying the long necks of extant giraffes and extinct sauropod dinosaurs. Here we summarise these debates and place them in a wider taxonomic context. We consider the evolution of long necks across a wide range of (both living and extinct) taxa and ask whether there has been a common selective factor or whether each case has a separate explanation. We conclude that in most cases long necks can be explained in terms of foraging requirements, and that alternative explanations in terms of sexual selection, thermoregulation and predation pressure are not as well supported. Specifically, in giraffe, tortoises, and perhaps sauropods there is likely to have been selection for high browsing. It the last case there may also have been selection for reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing. For camels, wading birds and ratites, original selection was likely for increased leg length, with correlated selection for a longer neck to allow feeding and drinking at or near substrate level. For fish-eating long-necked birds and plesiosaurs a small head at the end of a long neck allows fast acceleration of the mouth to allow capture of elusive prey. A swan's long neck allows access to benthic vegetation, for vultures the long neck allows reaching deep into a carcass. Geese may be an unusual case where anti-predator vigilance is important, but so may be energetically efficient low browsing. The one group for which we feel unable to draw firm conclusions are the pterosaurs, this is in keeping with the current uncertainty about the biology of this group. Despite foraging emerging as a dominant theme in selection for long necks, for almost every taxonomic group we have identified useful empirical work that would increase understanding of the selective costs and benefits of a long neck.

Consistent waves of collective vigilance in groups using public information about predation risk

Consistent waves of collective vigilance in prey groups using public information about predation risk. Antipredator vigilance models have long assumed that individuals in groups monitor threats independently from one another. This assumption has been challenged recently, both theoretically and empirically. In particular, recent models predict that individuals should pay attention to the vigilance state of their neighbors and become increasingly vigilant when the proportion of vigilant neighbors is higher. Such copying can lead to temporal waves of collective vigilance in groups rather than random fluctuations. Here, we investigated the robustness of these predicted waves under varying ecological situations. Using an individual-based modeling approach, we show that such waves are predicted to occur in small and large groups, when copying only involves the nearest neighbor or the radius of copying is small or large or when the shape of the group is square or rectangular. However, when the influence of neighbors was restricted (e.g., by reducing the radius of influence, by only considering the nearest neighbor, or in more elongated groups), waves involved a smaller proportion of the group. In general, collective patterns were more organized when the copying tendency was strong and the frequency at which individuals can switch state was not too high. Our results show that collective waves of vigilance are a robust phenomenon emerging from the individual social behavior of group members, thus encouraging empirical scrutiny of the connection between individual and group vigilance. Key words: antipredator vigilance, collective pattern, copying, group size, predation risk. (Behav Ecol)

Changes in antipredator vigilance over time caused by a war of attrition between predator and prey

Prey animals often move from patch to patch in search of food and must evaluate the likelihood that a predator is present in each patch to adjust their antipredator behavior. This is important because a prey animal might have inadvertently arrived at a patch on which a sit-and-wait predator is lurking, a common situation in many species of animals. In a simulation model, we explore how long the ambushing predator should wait before attacking the prey animal and how the prey animal can adjust its vigilance in response. We adopted a war-of-attrition framework where the predator selects randomly an attack time from a distribution to keep the prey guessing and where the prey also keep the predator guessing by selecting randomly a time at which to switch from high to low vigilance. We found that an evolutionarily stable solution can emerge in this game and has the following form under a broad range of ecological conditions: the predator attacks early and the prey adopts a high vigilance early and then switches later to a lower vigilance. The results indicate that antipredator vigilance may change as a function of time rather than being a constant value as assumed in most vigilance models. We conclude that the uncertainty that ambushing predators and their prey must plant in the minds of the other can have important consequences for the evolution of predator and prey tactics.

Making heads turn: association between head movements during vigilance and perceived predation risk in brown-headed cowbird flocks

Models of antipredator vigilance show that animals should be more vigilant when in smaller groups, when neighbours are farther away, and when they occur at the edge rather than at the centre of a group. However, models fail to specify how animals are expected to look out for threats while actually scanning. We suggest that head movements during scanning may represent a way that animals can control the value of scanning while in groups. Head movements can be used to increase visual coverage (visual search) as well as bring features of the environment to more sensitive parts of the eyes (visual fixation). We conducted a seminatural experiment with brown-headed cowbirds, Molothrus ater , in which we manipulated group size and neighbour distance, and recorded vigilance for peripheral and central individuals. During scanning, the rate of head movements by peripheral individuals increased, probably to enhance visual coverage due to their higher perceived risk of predation. However, individuals that were farther apart and in smaller groups used a different scanning strategy by reducing their rate of head movements (e.g. increased the averaged time they spent holding a given head position steady), probably to fixate their gaze longer on neighbours. Visual fixation may be useful for obtaining social information about predation threats from the behaviour of groupmates. We show that (1) a vigilance metric associated with head movement behaviour, which is attuned to the visual system of a species, can provide novel information about vigilance in groups, and that (2) birds have different head movement strategies, probably associated with different visual targets, when the risk of predation is higher.

On the perception of targeting by predators during attacks on socially feeding birds

We examined the spatial perception of predator targeting by prey during simulated hawk attacks on house finch, Carpodacus mexicanus, flocks, with an overall goal of gaining insight into the targeting process itself. Predator targeting of specific prey during attacks determines how danger is distributed among group members, and thereby determines key aspects of the safety of feeding in groups, such as risk dilution and its relationship to antipredator vigilance. During the main experiment, a model hawk suddenly appeared at either 3 m or 9 m from finches feeding near protective cover. The 9 m attacks always caused nearly all birds to flee to cover. During 3 m attacks, only birds directly in the line of attack fled to cover; the other birds instead consistently flew nearly perpendicular to the attack and away from cover. These results suggest that most finches did not perceive themselves to be targeted for attack when the hawk appeared at close range; otherwise, all birds appeared to perceive themselves as potential targets. A second experiment demonstrated that information about predator targeting is derived from observation of the predator itself rather than the behaviour of flockmates in the direct line of attack. A third experiment demonstrated that distance to cover also influenced the birds’ response to targeting; thus, reactions to apparent nontargeting were not simply a matter of moving away from the line of attack. The differential perception of targeting during an attack is probably a widespread phenomenon in social birds and other animals.

MODELING SELECTION AND EXTINCTION MECHANISMS OF BIOLOGICAL SYSTEMS

In this paper, the behavior of a genetic algorithm is modeled to enhance its applicability as a modeling tool of biological systems. A new description model for selection mechanism is introduced which operates on a portion of individuals of population. The extinction and recolonization mechanism is modeled, and solving the dynamics analytically shows that the genetic drift in the population with extinction/recolonization is doubled. The mathematical analysis of the interaction between selection and extinction/recolonization processes is carried out to assess the dynamics of motion of the macroscopic statistical properties of population. Computer simulations confirm that the theoretical predictions of described models are in good approximations. A mathematical model of GA dynamics was also examined, which describes the anti-predator vigilance in an animal group with respect to a known analytical solution of the problem, and showed a good agreement between them to find the evolutionarily stable strategies.

Zebra finches are bolder in an asocial, rather than social, context

Despite an expanding interest in animal personalities, the influence of social interactions and sex differences on individual differences in behaviour remains poorly understood. Using the social zebra finch (Taeniopygia guttata), we tested for behavioural differences in exploration of a novel environment and objects, between individuals of both sexes in relation to a social context; the presence of three male companions, three female companions or no companion birds. We predicted that the presence of conspecific companions should result in focal birds reacting to novelty by exploring more extensively because the companion birds contribute to anti-predator vigilance behaviour and because social isolation often causes behavioural inhibition in social species. We found that exploratory behaviour of focal individuals was significantly reduced in the presence of conspecific companions, irrespective of the companion's sex. Moreover, we found a weak trend towards females being more exploratory than males, irrespective of the social context. These results demonstrate the importance of considering the social context in animal personality studies and of exploring sex differences in personalities.