European Roe Deer Increase Vigilance When Faced with Immediate Predation Risk by Eurasian Lynx

Prey animals must balance antipredatory behaviour with foraging behaviour. According to the risk allocation hypothesis, prey increase antipredatory behaviour and reduce foraging activity during pulses of high risk, but with continuous risk, other activities must continue and antipredatory behaviour decreases despite the risk. We studied the impact of lynx presence on the vigilance behaviour of wild roe deer under conditions of (i) a pulsed elevated risk by experimentally spreading lynx urine as an olfactory cue, and (ii) continuous risk by comparing an area where lynx was eradicated 160 years ago to an area where lynx has been re‐introduced 30 years ago. Roe deer were extremely vigilant in response to the predator olfactory cue; however, roe deer vigilance did not differ measurably among areas with or without potential lynx presence. Deer were more vigilant before sunset than during the night at both study areas, probably due to long‐term adaptation of roe deer to human hunting during daytime. Vigilance decreased from August to September even though activity of lynx increases in autumn, which may be a result either of increased foraging due to decrease in food quality in autumn, or of changes in social organization of the deer. Our results suggested that the degree of vigilance depends on environmental cues. We found that roe deer respond to lynx urine despite a long absence of lynx in the ecosystem. Our results support the risk allocation hypothesis for responses to pulses of high risk but not for responses to continuous elevated levels of risk.     

Vigilance and grouping in the southern African ground squirrel (Xerus inauris)

Animals may form groups in response to the foraging–vigilance trade‐off, through enhanced predator detection (collective detection hypothesis) or reduced predation risk to the individual (dilution hypothesis), allowing individuals to decrease vigilance levels. Both hypotheses predict decreasing individual vigilance levels with increasing group size; however, the collective detection hypothesis also predicts increasing overall group vigilance with increasing group size. However, in species in which vigilance and foraging are not mutually exclusive, where vigilance may not be as costly, neither of these hypotheses may apply. Here, we examine the relationship between group size and vigilance in the social Cape ground squirrel (Xerus inauris), a species that can combine foraging and vigilance behaviours. Ten groups were observed using scan sampling, measuring both group and individual vigilance and group size. A negative relationship existed between individual vigilance and group size and a positive relationship between group vigilance and group size. Therefore, in Cape ground squirrels, vigilance seems to be costly even though it can be combined with foraging behaviours. Furthermore, group vigilance behaviour gives support to the collective detection hypothesis, whilst individual vigilance gives support to both hypotheses.     

Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance

Many studies of social species have reported variation in the anti-predator vigilance behaviour of foraging individuals depending on the presence and relative position of other group members. However, little attention has focused on how foragers assess these variables. It is commonly assumed that they do so visually, but many social species produce frequent calls while foraging, and these 'close' calls might provide valuable spatial information. Here, we show that foraging pied babblers (Turdoides bicolor) are less vigilant when in larger groups, in the centre of a group and in closer proximity to another group member. We then show that foragers are less vigilant during playbacks of close calling by more individuals and individuals on either side of them when compared with calls of fewer individuals and calls on one side of them. These results suggest that foragers can use vocal cues to gain information on group size and their spatial position within a group. Future studies of anti-predator vigilance should consider the relative importance of both visual and vocal monitoring of group members.     

Costs and benefits of flocking in foraging white-fronted geese (Anser albifrons): effects of resource depletion

This study investigated the costs and benefits of flocking in white-fronted geese Anser albifrons foraging on rice grains in Japan. The time budgets of focal geese were recorded, and the effects of flock size on the proportions of time spent in vigilant and agonistic behaviour were tested. The results showed that the decline in vigilance level and consequent increase in foraging time were beneficial results of flocking whereas agonistic interactions, a potential cost of flocking, did not increase with increasing flock size. However, seasonal variation in flock size suggested that exploitative competition could be a cost of flocking; the sizes of flocks in spring, when resource depletion had progressed, were significantly reduced compared with those in autumn. An experimental increase in rice density resulted in a significant increase in flock size. We conclude that the flock size of foraging white-fronted geese is a result of compromise between a constant benefit of flocking (i.e. decline in vigilance level) and a cost of flocking varying with food abundance (i.e. exploitative competition).     

Inter‐individual variation in honey bee dance intensity correlates with expression of the foraging gene

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Amongst honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter‐individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined, for these foragers, the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR‐2. As expected, foragers showed large inter‐individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co‐opting behavioural modules involved in food search and foraging in solitary insects.     

Relatedness does not predict vigilance in a population of the social rodent Octodon degus

The possibility that social foragers adjust and coordinate their scanning activity when in the presence of close relatives to attain inclusive fitness benefits remains controversial and scarcely examined. To this aim, we first tested the null hypothesis of no association between foraging individuals of the diurnal rodent, Octodon degus and their pairwise relatedness (six microsatellite loci), under natural conditions. Secondly, we examined the influence of relatedness on scan effort (percent overlapping) and temporal distribution of scanning using linear regression. Finally, we evaluated whether temporal distributions of scanning were significantly lower (coordination) or higher (synchrony) than random expectations using bootstrapping. We found that pairwise relatedness between focal degus and their foraging partner did not influence the scan effort or the temporal distribution of scanning. These original, field-based findings imply that vigilance behavior in socially foraging degus is unlikely to be kin-selected and adds to results from previous lab studies in that kinship remains a poor predictor of social behavior in these animals. Overall, our study adds to others revealing that kin selection may not have had an impact on aspects of social behavior such as vigilance during social foraging.     

Are the Costs of Site Unfamiliarity Compensated With Vigilance? A Field Test in Eurasian Siskins

Determination of fitness differentials between individuals adopting different migratory and dispersal strategies is basic to understand the evolution of migration. In the Eurasian siskin Carduelis spinus, both resident and transient birds forage within the same wintering area, providing the rare opportunity to compare their foraging behaviour in the same area and habitat. The aim of this study was to test the predictions associated to the different hypothesized costs of transience by studying the vigilance and foraging behaviour of wild wintering siskins foraging at three bird tables with different predation risk and interference competition levels. Transient siskins showed longer scan durations than residents, either because of site unfamiliarity or subordination (i.e. prior‐occupancy effect). However, residents and transients did not differ in aggression rates, contrary to the dear‐enemy effect. Transient siskins did not show a higher allocation of time to vigilance, contrary to the hypothesis of compensation vigilance to reduce predation risk by dispersing animals. Moreover, transients increased pecking rate with increasing predation risk, showed lower scan rates, longer foraging bouts and, in males, presented marginally higher proportions far from cover. Altogether these results strongly support the hypothesis that transients incur a predation cost due to a less efficient vigilance and foraging system.     

Relationships between densities of previous and simultaneous foragers and the foraging behaviour of three bumblebee species

1. The local insect composition may be as important as the local floral composition for bumblebees' foraging behaviour. However, little is known about how the local abundance of insects affects the foraging patterns of individuals. 2. Using field observations, we studied the relationships between the local density of previous and simultaneous foragers and the local foraging behaviour of Bombus pascuorum, Bombus lucorum/B. terrestris and Bombus lapidarius while pollinating Centaurea jacea. 3. The number of bumblebees foraging in the plots was positively related to the number of new individuals arriving at these plots. The number of inflorescences contacted and the duration of visits were negatively related to the number of simultaneous foragers, but only in B. lucorum/B. terrestris. The effects of previous foragers on the behaviour of other bumblebees were species‐specific and variable in their direction. Such contrasting effects can be explained in terms of bumblebee species' abundances and functional similarity. In some cases, the effect of previous foragers increased with Centaurea density. 4. The local abundance of previous and simultaneous foragers affected the foraging behaviour of particular bumblebee individuals in complex ways. Future studies on local foraging behaviour might benefit from including the abundance of co‐foragers.     

Behavioural Responses of European Roe Deer to Temporal Variation in Predation Risk

In natural environments, predation risk varies over time. The risk allocation hypothesis predicts that prey is expected to adjust key anti‐predator behaviours such as vigilance to temporal variation in risk. We tested the predictions of the risk allocation hypothesis in a natural environment where both a species‐rich natural predator community and human hunters are abundant and where the differences in seasonal and circadian activity between natural and anthropogenic predators provided a unique opportunity to quantify the contributions of different predator classes to anti‐predator behaviour. Whereas natural predators were expected to show similar levels of activity throughout the seasons, hunter activity was high during the daytime during a clearly defined hunting season. According to the risk allocation hypothesis, vigilance should then be higher during the hunting season and during daytime hours than during the non‐hunting season and night‐time hours. Roe deer (Capreolus capreolus) on the edge of Bia?owie?a Primeval Forest in Eastern Poland displayed vigilance behaviour consistent with these predictions. The behavioural response of roe deer to temporarily varying predation risks emphasises the behavioural plasticity of this species and suggests that future studies of anti‐predator behaviour need to incorporate circadian variation in predation pressure as well as risk gradients of both natural and anthropogenic predators.     

Vigilance and Collective Detection of Predators in Degus (Octodon degus)

Individuals of social and partially social species typically reduce their vigilance activity when foraging in groups. As a result, per capita risk of predation decreases and individuals allocate more time to foraging and other fitness rewarding activities. Reduction of per capita risk is hypothesized to occur because there are more individuals to detect potential predators. If so, collective (i.e. total) vigilance is expected to increase with foraging group size. Increased surveillance during group foraging may occur if group members scan independently of one another, or sequentially to avoid the overlapping of their vigilance bouts. Intriguingly, such coordinated vigilance assumes that individuals monitor not only the presence, but the vigilance behaviour of group mates. We used seasonal records on time budget and grouping patterns of individually marked degus (Octodon degus), a social rodent, to examine if (a) individual vigilance decreases and/or foraging increases with group size, (b) collective vigilance increases with group size and (c) foraging degus coordinate their vigilance. When foraging, degus decreased their individual vigilance and increased their foraging time when in larger groups. Despite this, degus in larger groups increased their collective vigilance, supporting the hypothesis that socially foraging degus decrease predation risk through an improved ability to detect and escape potential predators. Additionally, patterns of collective vigilance suggested that degus scan independently of each other and so, they do not coordinate their vigilance to prevent its temporal overlapping. This finding does not support that foraging degus monitor the vigilance activity of group mates.     

Good foragers can also be good at detecting predators

The degree to which foraging and vigilance are mutually exclusive is crucial to understanding the management of the predation and starvation risk trade-off in animals. We tested whether wild-caught captive chaffinches that feed at a higher rate do so at the expense of their speed in responding to a model sparrowhawk flying nearby, and whether consistently good foragers will therefore tend to respond more slowly on average. First, we confirmed that the time taken to respond to the approaching predator depended on the rate of scanning: as head-up rate increased so chaffinches responded more quickly. However, against predictions, as peck rate increased so head-up rate increased and mean length of head-up and head-down periods decreased. Head-up rate was probably dependent on peck rate because almost every time a seed was found, a bird raised its head to handle it. Therefore chaffinches with higher peck rates responded more quickly. Individual chaffinches showed consistent durations of both their head-down and head-up periods and, therefore, individuals that were good foragers were also good detectors of predators. In relation to the broad range of species that have a similar foraging mode to chaffinches, our results have two major implications for predation/starvation risk trade-offs: (i) feeding rate can determine vigilance scanning patterns; and (ii) the best foragers can also be the best at detecting predators. We discuss how our results can be explained in mechanistic terms relating to fundamental differences in how the probabilities of detecting food rather than a predator are affected by time. In addition, our results offer a plausible explanation for the widely observed effect that vigilance continues to decline with group size even when there is no further benefit to reducing vigilance.     

The effect of group size on vigilance in Ruddy Turnstones Arenaria interpres varies with foraging habitat

Foraging birds can manage time spent vigilant for predators by forming groups of various sizes. However, group size alone will not always reliably determine the optimal level of vigilance. For example, variation in predation risk or food quality between patches may also be influential. In a field setting, we assessed how simultaneous variation in predation risk and intake rate affects the relationship between vigilance and group size in foraging Ruddy Turnstones Arenaria interpres. We compared vigilance, measured as the number of ‘head‐ups’ per unit time, in habitat types that differed greatly in prey energy content and proximity to cover from which predators could launch surprise attacks. Habitats closer to predator cover provided foragers with much higher potential net energy intake rates than habitats further from cover. Foragers formed larger and denser flocks on habitats closer to cover. Individual vigilance of foragers in all habitats declined with increasing flock size and increased with flock density. However, vigilance by foragers on habitats closer to cover was always higher for a given flock size than vigilance by foragers on habitats further from cover, and habitat remained an important predictor of vigilance in models including a range of potential confounding variables. Our results suggest that foraging Ruddy Turnstones can simultaneously assess information on group size and the general likelihood of predator attack when determining their vigilance contribution.     

The visual fields of Common Guillemots Uria aalge and Atlantic Puffins Fratercula arctica: foraging,vigilance and collision vulnerability

Significant differences in avian visual fields are found between closely related species that differ in their foraging technique. We report marked differences in the visual fields of two auk species. In air, Common Guillemots Uria aalge have relatively narrow binocular fields typical of those found in non‐passerine predatory birds. Atlantic Puffins Fratercula arctica have much broader binocular fields similar to those that have hitherto been recorded in passerines and in a penguin. In water, visual fields narrow considerably and binocularity in the direction of the bill is probably abolished in both auk species. Although perceptual challenges associated with foraging are similar in both species during the breeding season, when they are piscivorous, Puffins (but not Guillemots) face more exacting perceptual challenges when foraging at other times, when they take a high proportion of small invertebrate prey. Capturing this prey probably requires more accurate, visually guided bill placement and we argue that this is met by the Puffin's broader binocular field, which is retained upon immersion; its upward orientation may enable prey to be seen in silhouette. These visual field configurations have potentially important consequences that render these birds vulnerable to collision with human artefacts underwater, but not in air. They also have consequences for vigilance behaviour.     

The value of constant surveillance in a risky environment

In risky environments, where threats are unpredictable and the quality of information about threats is variable, all individuals face two fundamental challenges: balancing vigilance against other activities, and determining when to respond to warning signals. The solution to both is to obtain continuous estimates of background risk, enabling vigilance to be concentrated during the riskiest periods and informing about the likely cost of ignoring warnings. Human surveillance organizations routinely produce such estimates, frequently derived from indirect cues. Here we show that vigilant individuals in an animal society (the pied babbler, Turdoides bicolor) perform a similar role. We ask (i) whether, in the absence of direct predator threats, pied babbler sentinels react to indirect information associated with increased risk and whether they communicate this information to group mates; (ii) whether group mates use this information to adjust their own vigilance, and whether this influences foraging success; and (iii) whether information provided by sentinels reduces the likelihood of inappropriate responses to alarm calls. Using playback experiments, we show that: (i) sentinels reacted to indirect predator cues (in the form of heterospecific alarm calls) by giving graded surveillance calls; (ii) foragers adjusted their vigilance in reaction to changes in surveillance calls, with substantial effects on foraging success; and (iii) foragers reduced their probability of responding to alarm calls when surveillance calls indicated lowered risk. These results demonstrate that identifying attacks as they occur is only part of vigilance: equally important is continuous surveillance providing information necessary for individuals to make decisions about their own vigilance and evasive action. Moreover, they suggest that a major benefit of group living is not only the increased likelihood of detecting threats, but a marked improvement in the quality of information available to each individual.     

The Context and Quality of Social Relationships Affect Vigilance Behaviour in Wild Chimpanzees

Previous studies of vigilance behaviour have focused mainly on the influence of predation threat, whereas the influences of conspecific factors, such as within‐group threats, are relatively unstudied. To elucidate the influences of conspecific factors, this study examined vigilance behaviour in wild chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania. Vigilance level was lower during foraging than during resting, which indicated a conflict between vigilance and foraging activity. In addition, vigilance level was higher when chimpanzees were on the ground where an encounter with leopards (Panthera pardus) is likely than when the chimpanzees were in trees. Males, but not females, increased their level of vigilance as the number of individuals within 3 m increased. In both males and females, daily party size – an index of group cohesion – did not affect the vigilance level. The level of maternal vigilance was higher when a dependent infant was separated from its mother than when the offspring was in contact with its mother. Both males and females increased their vigilance when a less‐associated group member was nearby, when compared with when there was no less‐associated group member nearby. This finding suggests that variation in relationship quality influences the vigilance level and that individuals need to increase their level of vigilance when the level of within‐group threats is high. This study indicated that variation in vigilance cannot be understood unless conspecific factors, such as variation in the relationship quality with associates, are considered.     

Coordination and synchronisation of anti-predation vigilance in two crane species

Much of the previous research on anti-predation vigilance in groups has assumed independent scanning for threats among group members. Alternative patterns that are based on monitoring the vigilance levels of companions can also be adaptive. Coordination of vigilance, in which foragers avoid scanning at the same time as others, should decrease the odds that no group member is alert. Synchronisation of vigilance implies that individuals are more likely to be vigilant when companions are already vigilant. While synchronisation will increase the odds that no one is vigilant, it may allow a better assessment of potential threats. We investigated temporal sequences of vigilance in family flocks consisting of two parents and at most two juveniles in two species of cranes in coastal China. We established whether the observed probability that at least one parent is alert was greater (coordination) or lower (synchronisation) than that predicted under the null hypothesis of independent vigilance. We documented coordination of vigilance in common cranes (Grus grus) foraging in an area with high potential for disturbance by people. We documented synchronisation of vigilance in red-crowned cranes (Grus japonensis) in the less but not in the more disturbed area. Coordination in small flocks leads to high collective vigilance but low foraging rates that may not be suitable in areas with low disturbance. We also argue that synchronisation should break down in areas with high disturbance because periods with low vigilance are riskier. Results highlight the view that temporal patterns of vigilance can take many forms depending on ecological factors.     

Influence of environmental and colony factors on the initial commodity choice of foragers of the stingless bee Plebeia tobagoensis (Hymenoptera, Meliponini)

Novice foragers of social bees have to decide what food commodity to collect when they start foraging for the first time. In this decision making process two types of factors are involved: internal factors (the response threshold) and external factors (environmental and colony conditions). In this study we will focus on the importance of two external factors, pollen storage level and information from experienced foragers about food availability in the field, on the initial commodity choice of foragers of the stingless bee species Plebeia tobagoensis. We also studied the effect of the initial choice of individuals on their subsequent foraging career. This study was performed in a closed greenhouse compartment, where food availability and colony condition could be controlled. Information on food availability in the field from experienced foragers and pollen storage level both greatly influenced the initial commodity choice of individuals, with more choices for the commodity communicated by experienced foragers or lacking in storage. The initial choice of foragers is of importance for their future foraging career, although a substantial proportion of foragers did switch between food commodities. Because of the ability of novice foragers to become flexibly distributed over foraging tasks, social bees are able to react to changes in their environment without directly having to decrease foraging effort devoted to other foraging tasks. This, in combination with individual flexibility during foraging careers makes it possible for colonies of P. tobagoensis to forage efficiently in an ever-changing environment. Received 7 November 2005; revised 12 January 2006; accepted 16 February 2006.     

Vision and touch in relation to foraging and predator detection: insightful contrasts between a plover and a sandpiper

Visual fields were determined in two species of shorebirds (Charadriiformes) whose foraging is guided primarily by different sources of information: red knots (Calidris canutus, tactile foragers) and European golden plovers (Pluvialis apricaria, visual foragers). The visual fields of both species showed features that are found in a wide range of birds whose foraging involves precision pecking or lunging at food items. Surprisingly, red knots did not show comprehensive panoramic vision as found in some other tactile feeders; they have a binocular field surrounding the bill and a substantial blind area behind the head. We argue that this is because knots switch to more visually guided foraging on their breeding grounds. However, this visual field topography leaves them vulnerable to predation, especially when using tactile foraging in non-breeding locations where predation by falcons is an important selection factor. Golden plovers use visually guided foraging throughout the year, and so it is not surprising that they have precision-pecking frontal visual fields. However, they often feed at night and this is associated with relatively large eyes. These are anchored in the skull by a wing of bone extending from the dorsal perimeter of each orbit; a skeletal structure previously unreported in birds and which we have named 'supraorbital aliform bone', Os supraorbitale aliforme. The larger eyes and their associated supraorbital wings result in a wide blind area above the head, which may leave these plovers particularly vulnerable to predation. Thus, in these two shorebirds, we see clear examples of the trade-off between the two key functions of visual fields: (i) the detection of predators remote from the animal and (ii) the control of accurate behaviours, such as the procurement of food items, at close quarters.     

Task‐Dependent Differences in Learning by Subordinate and Dominant Wild Arabian Babblers

Learning and innovation abilities have been studied extensively in flocking birds, but their importance and relevance in cooperatively breeding birds have been relatively unexplored. We studied the acquisition of novel foraging skills in 14 groups of wild, cooperatively breeding Arabian babblers (Turdoides squamiceps). While in a previous study we found that subordinate individuals were usually the first to learn to remove black rubber lids from a foraging grid, here we show that dominant individuals were the first to succeed in shifting from these black rubber lids to newly introduced white rubber lids. We also found that in all groups where one forager learned to shift to the white lids, the rest of the foragers also learned to do so, suggesting that this behaviour may be transmitted among group members. Although dominant individuals were almost always the first to remove white lids, once starting to remove white lids, dominants and subordinates learned equally well to prefer white over black lids based on differential reinforcement (food was provided only under white lids). Together with our previous study, our results suggest that differences in learning between dominants and subordinates may be task‐specific, which may represent different cognitive strategies: subordinates may explore a more diverse range of foraging opportunities, while dominants may be better at generalizing from familiar tasks to similar ones.     

Does vigilance always covary negatively with group size? Effects of foraging strategy

The possible effects of foraging strategy on the relationship between vigilance and group size were studied in three species of waders with different foraging strategies. I predict that (1) pause–travel species should show no relationship between scanning and group size, because these species scan for prey as well as for predators; (2) continuous-tactile foraging species should show a positive relationship between flock size and vigilance level, because in their large groups vigilance towards other birds could be used to avoid interference and aggression; and (3) continuous-visual searching species should show the general pattern of decreasing vigilance when group size increases as predicted by both the 'many eyes' and the 'predatory risk' hypotheses. Results support the predictions for the influence of foraging strategy on the relationship between vigilance level and group size. The mutual exclusion of foraging and scanning can determine the importance of the 'many eyes' hypothesis. Such exclusion seems to be determined by foraging strategy. The influence of foraging on scanning must be taken into account in future studies on the group-size effect. Electronic Publication