Predator-driven fragmentation of fiddler crab droves into selfish miniherds of biased composition

An explanation for animal groups is the selfish herd, characterized by aggregation as each member tries to shield itself from a predator by moving into a tight gap between other members. We test the hypotheses that: (1) droves, the large feeding groups of fiddler crabs, are selfish herds; (2) the miniherds that form when droves fragment on approach of a large predator are selfish herds; (3) selfish herds form when refugia are unlikely to be reached before an approaching predator arrives; and (4) the composition of selfish miniherds is biased toward individuals most vulnerable to predation. The study was conducted in South Carolina (USA) by videotaping the movements of sand fiddler crabs Uca pugilator when approached by a human predator. In both droves and miniherds, interindividual distance decreases with predator approach, consistent with behavior in a selfish herd. However, two other expectations for selfish herds—herd cohesion and sacrificing distance from the predator in order to get closer to other herders—are only met in miniherds. Crabs farther from refugia are more likely to form and remain in miniherds, indicating that selfish herding is only favored when refugia cannot be quickly reached. The composition of the smallest miniherds, consisting of 2-18 crabs, is biased toward females and small males. These individuals may be more vulnerable to predation because they lack the enlarged claw of large males that deters some predators. The small miniherds are relatively homogeneous with respect to the size and sex of their members, which may enhance cohesion and effectiveness as selfish herds. Miniherds will be effective selfish groups when predator attack has a significant vertical component and when the strike distance is large relative to both the size of the prey and the distance between group members. Droves are not selfish herds but permit crabs to flee feeding grounds as members of selfish miniherds.     

Within‐group vigilance in red colobus and redtail monkeys

In theory, animals are expected to relax vigilance in the safety of large groups. Four controlled studies of primates have failed to detect relaxed vigilance as group size increases. The counter‐intuitive behavior of primates might arise if another component of vigilance increases with group size, masking any decrease in outward, anti‐predator vigilance. Surveillance of associates is a major component of primate vigilance and might be expected to increase with group size due to an increase in competitive interactions. The present analysis uses data on glances toward associates to determine if within‐group surveillance is related to group size in wild red colobus and redtail monkeys of Uganda. Although males glance at associates more frequently during mating periods and females glance at associates more often when infants are young or out of contact, there was no evidence of a group‐size effect on within‐group surveillance. As with previous studies, primate vigilance patterns reflect reproductive strategies such as infant protection and mate defense. This study joins several others that indicate that primate vigilance is unresponsive to group size. New models that take into account association patterns below the level of the group may be needed. Am. J. Primatol. 48:113–126, 1999. © 1999 Wiley‐Liss, Inc.     

Selfish altruism,fierce cooperation and the predator*

This paper suggests a new way to think about a famous question: what explains cooperation in nature and in particular in humans? I argue that, for an evolutionary biologist as well as a quantitative social scientist, the triangle of two ‘teammates’ in the presence of a predator (passing and shooting in two-on-one situations) is one of the fundamental conceptual building-blocks for understanding these phenomena because in such a situation the fact that life is packaged in many distinct enclosures (and not in one big monolithic blob) can unfold its comparative advantage. I show how, in the presence of a predator, cooperative equilibria emerge among entirely selfish teammates if we infinitesimally bias the lead player in the selfish direction or assign a computational burden on the predator due to the presence of a teammate. I argue that ‘predators’ are common in the biological jungle but also in everyday human settings. Intuitively, this paper builds on the simple idea – a familiar one to a biologist observing the natural world but perhaps less so to social scientists – that everybody has enemies.     

Evolution of anti-predator traits in response to a flexible targeting strategy by predators

Anti-predator benefits increase with vigilance rate and group size in many species of animal, while simultaneously resource intake rates usually decrease. This implies that there is an optimal group size and vigilance rate that will maximize individual fitness. While this basic theory of vigilance has been modelled and tested extensively, it has often been assumed that the predator represents a 'fixed-risk' such that groups of prey are essentially independent entities that exert little or no effect on one another either directly or indirectly. We argue that this is an over-simplification, and propose that the behaviour of one group of prey will likely affect the fitness of another local group of prey if the predator preferentially attacks the most vulnerable group-rather than attack both with constant rates. Using a numerical simulation model, we make the first examination of this game and allow the prey to dynamically evolve both optimal group size distributions between two habitats and vigilance rates in response to a predator with a preference for whichever group is the more vulnerable. We show that the density of prey in the population and the sensitivity of a predator to differences in prey vulnerability are likely to drive the dynamics of such a game. This novel approach to vigilance theory opens the door to several challenging lines of future research, both experimental and theoretical.     

Visual obstruction and vigilance: a natural experiment

Visual obstructions can cause an increase in antipredator vigilance in prey animals by making predator detection more difficult. However, visual obstructions can also skew the perception of group size and inter‐individual distances and impair the detection of alarm signals by conspecifics. These changes within the group alone can cause an increase in vigilance. To disentangle the contribution of these various factors to changes in vigilance, I documented vigilance in a gregarious species, the semipalmated sandpiper Calidris pusilla, foraging in a habitat where a naturally‐occurring visual barrier partially prevented predator detection without altering the transfer of information about predation risk within the group. I used a matched sampling design to collect vigilance data for birds using adjacent areas with and without the visual barrier. In the visually‐obstructed area, sandpipers maintained a higher level of vigilance, occurred farther away from cover and in smaller flocks, and preferentially scanned the area of danger with one eye in particular. All these changes suggest that visual obstruction increased perceived predation risk. I conclude that it is the inability to get a good view of any approaching predator, rather than changes in intra‐group communication that caused the increase in vigilance in the visually‐obstructed area.     

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.     

Facultative response to a kleptoparasite by the cooperatively breeding pied babbler

In many cases of interspecific kleptoparasitism, hosts developdefensive behaviors to minimize the impact of kleptoparasites.Because vigilance and defensive behaviors are often costly,selection should favor hosts that adjust the amount of investmentneeded to minimize losses to kleptoparasitism. However, examplesof such facultative responses are rare. Here, we investigatethe response of cooperatively breeding pied babblers (Turdoidesbicolor) to the drongo (Dicrurus adsimilis), an avian kleptoparasitethat regularly follows pied babbler groups, often giving alarmcalls to alert the group to predators but also occasionallygiving false alarm calls in order to steal food items. We showthat pied babbler response to drongos varies markedly accordingto babbler group size. In small groups, where there are fewindividuals available to act as sentinels, babblers sentinelless when a drongo is present and respond strongly to drongoalarm calls. However, in large groups, where there are manyindividuals available to participate in predator vigilance,babblers sentinel more often when a drongo is present, rarelyrespond to drongo alarm calls, and aggressively displace drongos,with a consequent decline in the number of successful kleptoparasitismevents. This behavior represent a facultative response to akleptoparasite according to the costs versus benefits of toleratingtheir presence.     

Many eyes or many ewes: vigilance tactics in female bighorn sheep Ovis canadensis vary according to reproductive status

In gregarious animals, there is usually a negative relationship between individual vigilance and group size. This effect of group size is generally explained by increasing probability of predator detection (the many-eyes hypothesis) and by the dilution of risk occurring in larger groups. Few studies have attempted to examine the specific implications of either hypothesis on the expected vigilance pattern of an animal. Here we examine whether reproductive status affects vigilance patterns in bighorn sheep Ovis canadensis ewes. We also test whether the observed vigilance patterns are consistent with predictions from dilution or detection models of vigilance. Although vigilance decreased with increasing group size, vigilance tactics differed between barren and lactating females. Lactating ewes relied solely on predator detection. In contrast, barren ewes benefited from both detection and dilution effects when group size increased and adjusted vigilance effort according to the proportion of lactating ewes in their group. It is generally assumed that gregariousness increases safety. Here we further show that reproductive status influenced how animals reduce predation risk and that some individuals take advantage of the vigilance effort provided by others.     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

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.     

Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation

Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.     

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.     

Persistence of Alarm-Call Behaviour in the Absence of Predators: A Comparison Between Wild and Captive-Born Meerkats (Suricata Suricatta)

Performing correct anti‐predator behaviour is crucial for prey to survive. But, are such abilities lost in species or populations living in predator‐free environments? How individuals respond to the loss of predators has been shown to depend on factors such as the degree to which anti‐predator behaviour relies on experience, the type of cues evoking the behaviour, the cost of expressing the behaviour and the number of generations under which relaxed selection has taken place. Here we investigated whether captive‐born populations of meerkats (Suricata suricatta) used the same repertoire of alarm calls previously documented in wild populations and whether captive animals, as wild ones, could recognize potential predators through olfactory cues. We found that all alarm calls that have been documented in the wild also occurred in captivity and were given in broadly similar contexts. Furthermore, without prior experience of odours from predators, captive meerkats seemed to distinguish between faeces of potential predators (carnivores) and non‐predators (herbivores). Despite slight structural differences, the alarm calls given in response to the faeces largely resembled those recorded in similar contexts in the wild. These results from captive populations suggest that direct, physical interaction with predators is not necessary for meerkats to perform correct anti‐predator behaviour in terms of alarm‐call usage and olfactory predator recognition. Such behaviour may have been retained in captivity because relatively little experience seems necessary for correct performance in the wild and/or because of the recency of relaxed selection on these populations.     

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

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

Vigilance behavior of Pyrenean chamois Rupicapra pyrenaica pyrenaica: Effect of sex and position in the herd

The Pyrenean chamois Rupicapra pyrenaica pyrenaica is a mountain-dwelling ungulate with an extensive presence in open areas. Optimal group size results from the trade off between advantages (a reduction in the risk of predation) and disadvantages (competition between members of the herd) of group living. In addition, advantages and disadvantages of group living may vary depending on the position of each individual within the herd. Our objective was to study the effect of central vs. Peripheral position in the herd on feeding and vigilance behavior in male and female Pyrenean chamois and to ascertain if a group size effect existed. We used focal animal sampling and recorded social interactions when a focal animal was involved. With males, vigilance rate was higher in the central part of the group than at the periphery, probably due to a higher density of animals in the central part of the herd and a higher probability of being disturbed by conspecifics. With females, vigilance rate did not differ according to position in the herd. Females spent more time feeding than males, and males showed a higher frequency of the vigilance behavior than females. We did not observe a clear relationship between group size and vigilance behavior. The differences in vigilance behavior might be due to social interactions.     

Species-level selection reduces selfishness through competitive exclusion

Adaptation does not necessarily lead to traits which are optimal for the population. This is because selection is often the strongest at the individual or gene level. The evolution of selfishness can lead to a 'tragedy of the commons', where traits such as aggression or social cheating reduce population size and may lead to extinction. This suggests that species-level selection will result whenever species differ in the incentive to be selfish. We explore this idea in a simple model that combines individual-level selection with ecology in two interacting species. Our model is not influenced by kin or trait-group selection. We find that individual selection in combination with competitive exclusion greatly increases the likelihood that selfish species go extinct. A simple example of this would be a vertebrate species that invests heavily into squabbles over breeding sites, which is then excluded by a species that invests more into direct reproduction. A multispecies simulation shows that these extinctions result in communities containing species that are much less selfish. Our results suggest that species-level selection and community dynamics play an important role in regulating the intensity of conflicts in natural populations.     

Investigating Differences in Vigilance Tactic Use within and between the Sexes in Eastern Grey Kangaroos

Aggregation is thought to enhance an animal’s security through effective predator detection and the dilution of risk. A decline in individual vigilance as group size increases is commonly reported in the literature and called the group size effect. However, to date, most of the research has only been directed toward examining whether this effect occurs at the population level. Few studies have explored the specific contributions of predator detection and risk dilution and the basis of individual differences in the use of vigilance tactics. We tested whether male and female (non-reproductive or with young) eastern grey kangaroos (Macropus giganteus) adopted different vigilance tactics when in mixed-sex groups and varied in their reliance on predator detection and/or risk dilution as group size changed. This species exhibits pronounced sexual dimorphism with females being much smaller than males, making them differentially vulnerable toward predators. We combined field observations with vigilance models describing the effects of detection and dilution on scanning rates as group size increased. We found that females with and without juveniles relied on predator detection and risk dilution, but the latter adjusted their vigilance to the proportion of females with juveniles within their group. Two models appeared to equally support the data for males suggesting that males, similarly to females, relied on predator detection and risk dilution but may also have adjusted their vigilance according to the proportion of mothers within their group. Differential vulnerability may cause sex differences in vigilance tactic use in this species. The presence of males within a group that do not, or only partially, contribute to predator detection and are less at risk may cause additional security costs to females. Our results call for reexamination of the classical view of the safety advantages of grouping to provide a more detailed functional interpretation of gregariousness.     

Costs and Benefits of Sociality Differ Between Female Guanacos Living in Contrasting Ecological Conditions

According to current theory, anti‐predator benefits promote group formation in open‐dwelling ungulates. An inverse relationship between vigilance effort and group size has been documented frequently and thought to reflect the consequent decrease in perceived predation risk as group size increases. In contrast, competition costs are supposed to set the upper limit to the number of individuals that can forage together. As anti‐predator behavior is no longer functional in the absence of predation and competition costs might be affected by resource distribution, the net benefit of aggregation will depend on the particular combination of predation risk and habitat structure experienced by the individual. To test this hypothesis, group‐size effects on female time allocation and within‐group aggression rate were compared between two guanaco populations exposed to contrasting levels of puma predation. Habitat structure within both sites consisted of mosaics of shrublands and grasslands, and group‐size effects were also compared between these habitat types. Females under predation risk showed a strong reduction in vigilance as the number of adults in the group increased, whereas females from the predator‐free population showed overall low levels of vigilance, regardless of group size. These results emphasize the anti‐predator significance of the group‐size effect on female vigilance, as well as guanaco plasticity to adjust time allocation to local conditions. On the other hand, within‐group aggression rate increased with the number of adults in the group. Aggression rate was almost null within groups located in grasslands but was significantly higher in shrublands, regardless of predation risk, suggesting that the more heterogeneous distribution of shrubs increases the interference competition level. These results strengthen the notion of predation pressure and habitat structure as major determinants of the balance between costs and benefits of group living, and highlight the potential of individual behavioral patterns to make qualitative predictions about group‐size variation within territorial ungulates.     

Predator occurrence and perceived predation risk determine grouping behavior in guanaco (Lama guanicoe)

Grouping behavior of social ungulates may depend on both predator occurrence and perceived predation risk associated with habitat structure, reproductive state, and density of conspecifics. Over 3 years, we studied grouping behavior of guanaco (Lama guanicoe) families in Chilean Patagonia during the birthing season and determined their response to variation in predator occurrence and perceived predation risk (habitat structure, calf/adult rate, and density of conspecifics). We considered the effect of two predators, puma (Puma concolor) and culpeo fox (Lycalopex culpaeus). We measured two common (family group size and vigilance) and one novel (family group cohesion) behavioral responses of guanaco. Our results show that guanaco family groups adapted their grouping behavior to both predator occurrence and perceived predation risk. Larger family groups were found in open habitats and areas with high puma occurrence, while guanacos stayed in small family groups in areas with high shrub cover or low visibility. Group cohesion increased in areas with higher occurrence of pumas and culpeo foxes, and also increased in smaller family groups and in areas with low guanaco density. Vigilance (number of vigilant adults) was mainly related to group size and visibility, increasing in areas with low visibility, while residual vigilance (vigilance after removing the group‐size effect) did not vary with the explanatory variables examined. Our results suggest that a mix of predator occurrence and perceived predation risk influences guanaco grouping behavior and highlights the importance of evaluating different antipredator responses together and considering all predator species in studies aimed at understanding ungulate behavior.     

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.