Unpredictability of vigilance in two sympatric Tibetan ungulates

Vigilance is important for anti-predation, and different animals adopt different vigilance strategies. Instantaneous and sequential randomness in vigilance behavior are two main principles for the classic Pulliam model (1973). Given this context, we studied the vigilance behaviors in two wild cloven-hoofed animals, the Tibetan antelope (Pantholops hodgsonii) and the Tibetan gazelle (Procapra picticaudata) on Qinghai–Tibet Plateau, to explore if the two randomness principles work across species. The results showed that the distribution of inter-scan intervals of both Tibetan antelope and Tibetan gazelle followed the negative exponential distribution; inter-scans of both Tibetan antelope and Tibetan gazelle were unrelated with their previous scan, and most sequences of inter-scan intervals could be considered as random organized or unpredictable. In conclusion, the vigilance patterns of Tibetan antelope and Tibetan gazelle followed instantaneous randomness and sequential randomness of Pulliam model. A random vigilance strategy might be the best choice for Tibetan ungulates, and how to distinguish the social vigilance from anti-predator vigilance is an important issue for future research.     

Vigilance and scanning patterns in birds

We present a new approach to the analysis of scanning patterns in feeding birds. We estimate the probability of a bird detecting a predator from the frequency distribution of inter-scan intervals and the proportion of time spent scanning. This method avoids, several unrealistic assumptions implied in earlier analyses of vigilance data, and can accommodate predators attacking randomly or using prey behaviour to time an attack. The practical application of this approach is illustrated using data for feeding and vigilance in the ostrich (Struthio camelus). The analysis is discussed with reference to the hunting tactics of predators and Pulliam's (1973) model of feeding and vigilance in birds.     

西藏拉萨越冬黑颈鹤家庭群的警戒同步性

以往关于动物警戒行为的研究多以经典随机独立模型为基础,然而,近期一些理论和实证研究则向该模型发出了挑战。根据警戒行为同步性程度的不同,集体警戒可能存在基于模仿的同步警戒和避免重复的协调警戒两种模式。研究了中国雅鲁藏布江自然保护区越冬黑颈鹤家庭群的警戒行为,通过独立样本t检验验证由于年龄和是否携幼所导致的个体警戒水平的差异,通过单因素方差分析比较不同类型家庭群的集体警戒水平,通过配对t检验比较集体警戒的实际观测值和独立假设下的预期值从而确定越冬黑颈鹤家庭群的警戒同步性。结果表明家庭群中的幼年黑颈鹤警戒行为时间显著低于成年黑颈鹤,但幼鹤的存在对成鹤的警戒水平没有显著影响。不同类型黑颈鹤家庭群的集体警戒水平没有差异,但并未如预期表现为同步警戒。警戒行为模式是动物在特定环境中的适应性表现,越冬黑颈鹤生境中不存在落后目标策略的捕食者和高强度的捕食风险,因而可能不足以诱发以降低捕食风险为主要功能的高强度的警戒行为同步性;同时,在资源匮乏的冬季对食物获取的优先性可能也削弱了对同步警戒的需求。     

The group size effect and synchronization of vigilance in the Tibetan wild ass

Vigilance behavior is considered as an effective strategy for prey species to detect predators.An individual benefits from living in a group by reducing the time spent being vigilant without affecting the probability of detecting a predator.However,the mechanism producing a decrease in vigilance with increasing group size is unclear.Many models of vigilance assume that group members scan independently of one another.Yet in recent studies,the other 2 patterns of vigilance,coordination and synchronization,were reported in some species.In 2 summers(2018 and 2019),we studied the group-size effect on vigilance and foraging of Tibetan wild ass in Chang Tang Nature Reserve of Tibet.We also tested whether individuals scan the environment independently,tend to coordinate their scans,or tend to synchronize their vigilance.The results showed that individuals decreased the time spent on vigilance with increasing group size,while increased the time spent foraging.Group members scanned the environment at the same time more frequently and there was a positive correlation between group members'behaviors,indicating that Tibetan wild asses tend to synchronize their vigilance.     

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.     

Disturbance and predation risk influence vigilance synchrony of black‐necked cranes Grus nigricollis,but not as strongly as expected

Animals monitor surrounding dangers independently or cooperatively (synchronized and coordinated vigilance), with independent and synchronized scanning being prevalent. Coordinated vigilance, including unique sentinel behavior, is rare in nature, since it is time‐consuming and limited in terms of benefits. No evidence showed animals adopt alternative vigilance strategies during antipredation scanning yet. Considering the nonindependent nature of both synchronization and coordination, we assessed whether group members could keep alert synchronously or in a coordinated fashion under different circumstance. We studied how human behavior and species‐specific variables impacted individual and collective vigilance of globally threatened black‐necked cranes (Grus nigricollis) and explored behavior‐based wildlife management. We tested both predation risk (number of juveniles in group) and human disturbance (level and distance) effects on individual and collective antipredation vigilance of black‐necked crane families. Adults spent significantly more time (proportion and duration) on scanning than juveniles, and parents with juveniles behaved more vigilant. Both adults and juveniles increased time allocation and duration on vigilance with observer proximity. Deviation between observed and expected collective vigilance varied with disturbance and predation risk from zero, but not significantly so, indicating that an independent vigilance strategy was adopted by black‐necked crane couples. The birds showed synchronized vigilance in low disturbance areas, with fewer juveniles and far from observers; otherwise, they scanned in coordinated fashion. The collective vigilance, from synchronized to coordinated pattern, varied as a function of observer distance that helped us determine a safe distance of 403.75 m for the most vulnerable family groups with two juveniles. We argue that vigilance could constitute a prime indicator in behavior‐based species conservation, and we suggesting a safe distance of at least 400 m should be considered in future tourist management.     

Group size elicits specific physiological response in herbivores

With increasing group size, individuals commonly spend less time standing head-up (scanning) and more time feeding. In small groups, a higher predation risk is likely to increase stress, which will be reflected by behavioural and endocrine responses. However, without any predator cues, we ask how the predation risk is actually processed by animals as group size decreases. We hypothesize that group size on its own acts as a stressor. We studied undisturbed groups of sheep under controlled pasture conditions, and measured in situ the cortisol and vigilance responses of identified individuals in groups ranging from 2 to 100 sheep. Both vigilance and average cortisol concentration decreased as group size increased. However, the cortisol response varied markedly among individuals in small groups, resulting in a lack of correlation between cortisol and vigilance responses. Further experiments are required to explore the mechanisms that underlie both the decay and the convergence of individual stress in larger groups, and whether these mechanisms promote adaptive anti-predator responses.     

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.     

Prey synchronize their vigilant behaviour with other group members

It is generally assumed that an individual of a prey species can benefit from an increase in the number of its group''s members by reducing its own investment in vigilance. But what behaviour should group members adopt in relation to both the risk of being preyed upon and the individual investment in vigilance? Most models assume that individuals scan independently of one another. It is generally argued that it is more profitable for each group member owing to the cost that coordination of individual scans in non-overlapping bouts of vigilance would require. We studied the relationships between both individual and collective vigilance and group size in Defassa waterbuck, Kobus ellipsiprymnus defassa, in a population living under a predation risk. Our results confirmed that the proportion of time an individual spent in vigilance decreased with group size. However, the time during which at least one individual in the group scanned the environment (collective vigilance) increased. Analyses showed that individuals neither coordinated their scanning in an asynchronous way nor scanned independently of one another. On the contrary, scanning and non-scanning bouts were synchronized between group members, producing waves of collective vigilance. We claim that these waves are triggered by allelomimetic effects i.e. they are a phenomenon produced by an individual copying its neighbour''s behaviour.     

Dilution games: use of protective cover can cause a reduction in vigilance for prey in groups

Antipredatory vigilance usually decreases in groups. The generallyaccepted "collective detection" explanation implies that becausethere are more eyes to scan the surroundings for predators,individuals in a group can lower their personal investment invigilance without increasing their predation risk. The roleof other factors, such as numerical risk dilution caused bythe mere presence of companions, has been neglected. In a model,we explore a dilution game when foragers in groups have accessto protective cover. We show that foragers can take advantageof risk dilution and that this leads to changes in vigilancewith group size without the need to invoke collective detection.We identify a cost to maintaining high levels of vigilance asless vigilant foragers gather food faster and so depart thegroup sooner (to reach cover) leaving more vulnerable stragglersbehind. In groups, there is a scramble to reach safe sites thatcan induce a reduction in vigilance levels. Such a mechanismoperates less forcefully in large groups because individualsin these groups are less vulnerable to the departure of an individual.We also demonstrate that individuals should adopt lower levelsof vigilance, to reach safe sites sooner, when predator evasionis compromised or when the rate of food intake is high. Themodel provides new insights into the mechanisms underlying changesin vigilance with group size in animals.     

Does an opportunistic predator preferentially attack nonvigilant prey?

The dilution effect as an antipredation behaviour is the main theoretical reason for grouping in animals and states that all individuals in a group have an equal risk of being predated if equally spaced from each other and the predator. Stalking predators, however, increase their chance of attack success by preferentially targeting nonvigilant individuals, potentially making relative vigilance rates in a group relatively important in determining predation compared with the dilution effect. Many predators, however, attack opportunistically without stalking, when targeting of nonvigilant individuals may be less likely, so that the dilution effect will then be a relatively more important antipredation reason for grouping. We tested whether an opportunistically hunting predator, the sparrowhawk, Accipiter nisus, preferentially attacked vigilant or feeding prey models presented in pairs. We found that sparrowhawks attacked vigilant and feeding mounts at similar frequencies. Our results suggest that individuals should prioritize maximizing group size or individual vigilance dependent on the type of predator from which they are at risk. When the most likely predator is a stalker, individuals should aim to have the highest vigilance levels in a group, and there may be relatively little selective advantage to being in the largest group. In contrast, if the most likely predator is an opportunist, then individuals should simply aim to be in the largest group and can also spend more time foraging without compromising predation risk. For most natural systems this will mean a trade-off between the two strategies dependent on the frequency of attack of each predator type. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.     

Prey scan at random to evade observant predators

Anti-predator scans by animals occur with very irregular timing, so that the initiation of scans resembles a random, Poisson-like, process. At first sight, this seems both dangerous (predators could exploit the long intervals) and wastefull (scans after very short intervals are relatively uninformative). We explored vigilance timing using a new model that allows both predators and prey to vary their behaviour. Given predators that attack at random with respect to prey behaviour, constant inter-scan intervals minimize predation risk. However, if prey scan regularly to minimize their risk from randomly attacking predators, they become more vulnerable to predators that initiate attacks when the inter-scan intervals begin. If, in order to defeat this tactic, prey choose extremely variable inter-scan intervals, they become more vulnerable to predators who wait for long intervals before launching attacks. Only if predators can monitor the variability of inter-scan intervals and either attack immediately (if variability is too low) or wait for long intervals to attack (if variability is too high) does the empirically observed pattern of Poisson-like scanning become the optimal prey strategy.     

Collective Vigilance in the Wintering Hooded Crane: The Role of Flock Size and Anthropogenic Disturbances in a Human‐Dominated Landscape

Vigilance achieved at the group level, known as collective vigilance, can enhance the ability to assess threats and confer benefits to gregarious prey species. Examining the factors that influence collective vigilance and exploring how individual vigilance is organized at the group level can help to understand how prey groups respond to potential threats. We quantified collective vigilance and determined its temporal pattern in a natural wintering population of the hooded crane Grus monacha in the Shengjin Lake reserve in China. We examined the role of flock size and anthropogenic disturbances in the human‐dominated landscape on collective vigilance and level of synchronization. The proportion of time during which at least one individual scanned the surroundings (collective vigilance) increased with flock size and was higher in the more disturbed buffer zone of the lake. Synchronization of vigilance occurred more frequently in the smaller flocks but was not related to the risk of disturbance. Synchronization implies that individuals tend to monitor and copy the vigilance of neighbors. In the degraded wetlands, the wintering hooded crane benefits from foraging in groups and synchronizing their vigilance in response to human disturbances.     

Habitat but not group size or recent predator activity affect corvid collective vigilance at carcasses

Vigilance is an important anti-predator behaviour that can be an indicator of the predation risk faced by potential prey animals. Here, we assess the collective vigilance, or the vigilance level of an entire group, of corvids (Family: Corvidae) at experimentally placed carcasses in a desert environment in Australia. Specifically, we explore the relationship between collective vigilance levels and the habitat in which the carcass was placed, the time since a potential predator (dingo Canis dingo, wedge-tailed eagle Aquila audax or red fox Vulpes vulpes) was present at a carcass, and the group size of corvids around the carcass. We found that corvids are more vigilant in open habitat, but that group size and the recent presence of a potential predator does not affect the collective vigilance behaviour of corvids. The results demonstrate the important link between habitat and vigilance, and that animals may adopt anti-predator behaviours irrespective of the size of the group in which they occur or the recent presence of a potential predator.     

东方田鼠家族群对成员个体觅食行为的影响

植食性哺乳动物在分享社群觅食带来好处的同时,是否因个体间的相互干扰而影响其摄入率。在新鲜马唐叶片构建的均质密集食物斑块上,测定东方田鼠家族群成员个体在食物斑块上的觅食行为序列过程及行为参数,检验家族群存在对成员个体觅食行为的影响。结果发现,东方田鼠家族群雌、雄成员个体的觅食行为参数均无显著差异。然而,与单只个体相比,家族群觅食尽管能显著地缩短成员个体的觅食决定时间,但却显著地降低了成员个体的摄入率。分析觅食行为参数觅食中断时间发现,相较于单只个体,家族群成员个体间因相互干扰而引起的觅食中断时间的增加,不但增大了收获每口食物的时间,而且导致其摄入率下降。检测家族群成员个体各警觉行为动作参数,发现,成员个体间的相互干扰能引致个体的一般扫视、盯视及嗅闻动作时间比例显著增大,尽管直立扫视和静听动作时间比例减少显著,但并未使个体的觅食中断时间减小。结果充分说明,东方田鼠家族群成员个体间的相互干扰能使个体觅食行为参数发生变异,导致觅食中断时间增加,摄入率降低。     

Number of neighbors instead of group size significantly affects individual vigilance levels in large animal aggregations

The group size effect states that animals living in groups gain anti‐predator benefits through reducing vigilance levels as group size increases. A basic assumption of group size effect is that all individuals are equally important for a focal individual, who may adjust its vigilance levels according to social information acquired from them. However, some studies have indicated that neighbors pose greater influences on an individual's vigilance decisions than other group members, especially in large aggregations. Vigilance has also been found to be directed to both predators (anti‐predation vigilance) and conspecifics (social vigilance). Central individuals might rely more on social vigilance than peripheral individuals. To test these hypotheses, we examined the effects of flock size, number of neighbors and position within a flock on vigilance and competition of greater white‐fronted goose Anser albifrons that form large foraging flocks in winter, controlling the effects of other variables (group identity, winter period and site). We found that individual vigilance levels were significantly affected by number of neighbors and position within a flock, whereas flock size showed no effect. Individuals devoted a large component of vigilance to nearby flock mates. Central individuals directed a relatively larger proportion of vigilance to monitor neighbors than peripheral ones, indicating that central individuals more relied on social information acquired from neighbors, possibly caused by the more blocked visual field of central individuals. Moreover, some social vigilance may function as conducting or preventing agonistic interactions since competition intensity was positively correlated with number of neighbors. Our study therefore demonstrate that the number of neighbors is more important than group size in determining individual vigilance in large animal groups. Further studies are still needed to unravel which neighbors pose greater influence on individual vigilance, and the factors that influence individuals to acquire information from their neighbors to adjust vigilance behaviors.     

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.     

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.     

Vigilance in Single- and Mixed-Species Groups of Tamarins (Saguinus labiatus and Saguinus fuscicollis)

By forming larger sizes of groups, individuals benefit from a decrease in vigilance, but the collective vigilance of the group as a whole is not compromised. We examined whether this group size effect is apparent in mixed-species groups of red-bellied tamarins (S. labiatus) and saddleback tamarins (S. fuscicollis) which form stable and permanent associations in the wild. We studied general vigilance and responses to hidden threatening stimuli in five captive groups of each species, while they were housed in single- and mixed-species groups. For vigilance, the individual rate was lower in the larger mixed-species groups than in the smaller single-species groups. In addition, the amount of time when at least one individual was vigilant was higher in mixed-species groups. This suggests that the tamarins alter their vigilance behavior in the presence of the other species. In response to hidden threats, both species performed brief vigilance checks and frequencies of checking did not differ in single- and mixed-species groups. However, both species had a significant reduction in the mean duration per check, and there was a reduced total amount of time spent vigilance checking in the mixed-species groups compared to the single-species groups, demonstrating the group size effect. Overall the mixed-species groups had a higher number and mean duration of checking than the smaller single-species groups. Given that the two species share a common set of predators, and respond to each other's alarm calls, these findings provide strong evidence that individuals of both tamarin species may be able to benefit from forming mixed-species groups via improved vigilance and monitoring of threats.     

Noise, predation risk compensation and vigilance in the chaffinch Fringilla coelebs

Background noise should in theory hinder detection of auditory cues associated with approaching danger. We tested whether foraging chaffinches Fringilla coelebs responded to background noise by increasing vigilance, and examined whether this was explained by predation risk compensation or by a novel stimulus hypothesis. The former predicts that only inter-scan interval should be modified in the presence of background noise, not vigilance levels generally. This is because noise hampers auditory cue detection and increases perceived predation risk primarily when in the head-down position, and also because previous tests have shown that only interscan interval is correlated with predator detection ability in this system. Chaffinches only modified interscan interval supporting this hypothesis. At the same time they made significantly fewer pecks when feeding during the background noise treatment and so the increased vigilance led to a reduction in intake rate, suggesting that compensating for the increased predation risk could indirectly lead to a fitness cost. Finally, the novel stimulus hypothesis predicts that chaffinches should habituate to the noise, which did not occur within a trial or over 5 subsequent trials. We conclude that auditory cues may be an important component of the trade-off between vigilance and feeding, and discuss possible implications for anti-predation theory and ecological processes.