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.     

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.     

Vigilance behavior during the birth and lactation season in naturally occurring ring-tailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

I examined the vigilance behavior of adult males and females in two groups of ring-tailed lemurs(Lemur catta)during the birth and lactation season at the Beza-Mahafaly Reserve, southwestern Madagascar. I found no sex difference with respect to the rates of overall vigilance, rates of vigilance toward a potential predator or unfamiliar sound, or rates of vigilance toward conspecifics from other social groups, nor were there sex differences in the percentage of time spent vigilant in any of the above categories. Higher-ranking females were vigilant significantly more often toward predators or potential predators than lower-ranking females were. I detected no relationship between vigilance behavior and dominance rank among adult males. The alpha female in each group exhibited significantly more vigilance behavior than all other members of her group. It was predicted that males should exhibit more vigilance behavior than females do, particularly during the birth and lactation season, when predator pressure is high, if they are benefiting females in this respect. I discuss the results in the context of this prediction and in terms of how ring-tailed lemur males benefit females, and why they may be tolerated in social groups.     

Influence of Different Individual Traits on Vigilance Behaviour in European Rabbits

An animal's level of vigilance depends on various environmental factors such as predator presence or the proximity of conspecific competitors. In addition, several individual traits may influence vigilance. We investigated the effects of body condition, social rank and the state of pregnancy on individual vigilance (scanning) rates in individually marked European rabbits ( Oryctolagus cuniculus ) of a field enclosure population. We found lower rates in young rabbits than in adult females, but male and female juveniles did not differ. Vigilance of juveniles was positively correlated with their age-dependent body mass (used as a measure of body condition), i.e. young rabbits with lower body condition scanned less. We suggest that juveniles with low body condition were trading off vigilance against feeding to maximise their growth. In contrast, there was no significant correlation between body mass and vigilance in adult females. Adult females increased scanning rates during late pregnancy, which might constitute a behavioural compensation because of their lower capacity to escape predator attacks. In addition, adult females with low social ranks scanned more than high ranking individuals, likely because of their higher risk of attacks by conspecifics. In summary, our results highlight various individual characteristics that influence vigilance behaviour in European rabbits.     

Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics?

Many animals benefit from the presence of conspecifics by reducing their rate of scanning for predators while increasing their time spent foraging. This group size effect could arise from a decreased perception of individual risk (dilution hypothesis) and/or an increased ability to detect predators (detection hypothesis). We compared individual and group vigilance of Rocky Mountain elk, Cervus elaphus, in three regions of Yellowstone National Park, Wyoming, U.S.A. that varied in their encounter frequency with coyote, Canis latrans, grizzly bear, Ursus arctos, and grey wolf,Canis lupus , predators. Adult females without calves increased scanning and decreased foraging with high encounter risk and small herd size. Adult females with calves increased scanning and decreased foraging with high encounter risk, but showed no decrease in scanning with large herd size. Yearlings increased scanning and decreased feeding with small herd size, but not with high encounter risk. Adult males were least vigilant, fed most and were not influenced by encounter risk or herd size. These age-sex class differences led to significant differences in group vigilance depending on the composition of the herd. Herds with a majority of mothers were significantly more vigilant than herds with a majority of adult males. However, these differences in group vigilance had no influence on the individual scanning of females without calves. Thus, the decrease in individual scanning with herd size may depend more on changes in individual risk than on cooperative detection of predators. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

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.     

Human Disturbances,Habitat Characteristics and Social Environment Generate Sex-Specific Responses in Vigilance of Mediterranean Mouflon

In prey species, vigilance is an important part of the decision making process related to predation risk effects. Therefore, understanding the mechanisms shaping vigilance behavior provides relevant insights on factors influencing individual fitness. We investigated the role of extrinsic and intrinsic factors on vigilance behavior in Mediterranean mouflon (Ovis gmelini musimon×Ovis sp.) in a study site spatially and temporally contrasted in human pressures. Both sexes were less vigilant in the wildlife reserve compared to surrounding unprotected areas, except for males during the hunting period. During this period, males tended to be less strictly restricted to the reserve than females what might lead to a pervasive effect of hunting within the protected area, resulting in an increase in male vigilance. It might also be a rutting effect that did not occur in unprotected areas because males vigilance was already maximal in response to human disturbances. In both sexes, yearlings were less vigilant than adults, probably because they traded off vigilance for learning and energy acquisition and/or because they relied on adult experience present in the group. Similarly, non-reproductive females benefited of the vigilance effort provided by reproductive females when belonging to the same group. However, in the absence of reproductive females, non-reproductive females were as vigilant as reproductive females. Increasing group size was only found to reduce vigilance in females (up to 17.5%), not in males. We also showed sex-specific responses to habitat characteristics. Females increased their vigilance when habitat visibility decreased (up to 13.8%) whereas males increased their vigilance when feeding on low quality sites, i.e., when concomitant increase in chewing time can be devoted to vigilance with limited costs. Our global approach was able to disentangle the sex-specific sources of variation in mouflon vigilance and stressed the importance of reserves in managing and conserving wild sheep populations.     

Vigilance Patterns of Territorial Guanacos (Lama guanicoe): The Role of Reproductive Interests and Predation Risk

We conducted focal observations of territorial guanacos, a highly polygynous and social mammal, to compare time budgets between sexes and test the hypothesis that the differences in reproductive interests are associated with differential group size effects on male and female time allocation patterns. In addition, we used group instantaneous sampling to test the hypothesis that grouping improves detection capacity through increased collective vigilance. We fit GLM to assess how group size and group composition (i.e., presence or absence of calves) affected individual time allocation of males and females, and collective vigilance. As expected from differences in reproductive interests, males in family groups devoted more time to scan the surroundings and less to feeding activities compared to females. Both sexes benefited from grouping by reducing the time invested in vigilance and increased foraging effort, according to predation risk theory, but the factors affecting time allocation differed between males and females. Group size effects were significant when females were at less than five body‐lengths from their nearest neighbour, suggesting that grouping benefits arise when females are close to each other. Female time budgets were also affected by season, topography and vegetation structure. In contrast to our expectation, males reduced the time invested in vigilance as the number of females in the group increased, supporting the predation risk theory rather the intrasexual competition hypothesis. The presence of calves was associated with an increase in male individual vigilance; and vegetation type also affected the intensity of the group size effect over male time allocation. In closed habitats, collective vigilance increased with the number of adults but decreased with the number of calves present. Although male and female guanacos differed in their time allocation patterns, our results support the hypothesis that both sexes perceive significant antipredator benefits of group living.     

Vigilance in Przewalski's gazelle: effects of sex, predation risk and group size

Vigilance in social animals is often aimed at detecting predators. Many social and environmental factors influence vigilance, including sex, predation risk and group size. During the summer of 2007, we studied Przewalski's gazelle Procapra przewalskii , an endemic ungulate to the Qinghai-Tibet Plateau, to test whether and how these three factors affect vigilance. We distinguished groups consisting of males, mothers with lambs and females without lambs making observations on groups in the presence or absence of nearby predators. We assessed the group-size effect on vigilance and how this varied with levels of predation risk and sex. Males and mothers scanned longer and with a higher frequency than females without lambs. Individuals were more vigilant under direct predation threat. Although vigilance generally decreased with group size, the extent of the decrease was independent of predation risk and was not significant in males. The results suggest that mothers are more vigilant suggesting greater vulnerability and that males may have increased their vigilance to compete for higher social ranks. The positive correlation between vigilance and predation risk and the negative correlation between vigilance and group size are consistent with earlier findings, but we failed to find an interaction between group size and predation risk on vigilance perhaps because vigilance levels are low even in small groups, thus making similar vigilant upward adjustments in both small and large groups.     

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.     

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.     

Vigilance and group size in ostriches

Wild ostriches were observed while feeding alone or in groups of up to four birds, and their vigilance (proportion of time with the head up) recorded. Individual vigilance declined as group size increased, mainly through a decrease in the frequency with which the head was raised. Males were more vigilant than females, mainly because they kept their heads up for longer. Vigilance was influenced more by the presence than by the vigilance of a companion. When a head would stay down for a long time was impossible for a predator to predict. It is concluded that grouping by ostriches when feeding results in only a slight reduction in the group's vulnerability to successful predator attack, but in a considerable decrease in individual vulnerability.     

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.     

Why are scanning patterns so variable? An overlooked question in the study of anti‐predator vigilance

Anti-predator vigilance describes how animals scan their environments for predators. For mathematical simplicity, theories of anti-predator vigilance have generally assumed that animals initiate scans with a constant probability for each unit of time spent feeding. Initiating scans in such a fashion would produce a wide distribution of intervals between scans. Because so much variation was assumed by theory, observations of variation have received little consideration. We show that the original theories of vigilance contain a conceptual discrepancy between the assumed predator and anti-predator tactics. Modified versions of the theory allow variation only under restrictive circumstances that seem unlikely to apply in nature. Plausible reasons for the observed variation in interscan interval are that theories of vigilance assume the wrong predator tactics or the wrong details of predator detection. These possibilities lead to testable predictions about how distributions of interscan intervals should change under different threat and detection conditions.     

Effects of reproductive status, social rank, sex and group size on vigilance patterns in Przewalski's gazelle

Background

Quantifying vigilance and exploring the underlying mechanisms has been the subject of numerous studies. Less attention has focused on the complex interplay between contributing factors such as reproductive status, social rank, sex and group size. Reproductive status and social rank are of particular interest due to their association with mating behavior. Mating activities in rutting season may interfere with typical patterns of vigilance and possibly interact with social rank. In addition, balancing the tradeoff between vigilance and life maintenance may represent a challenge for gregarious ungulate species rutting under harsh winter conditions. We studied vigilance patterns in the endangered Przewalski''s gazelle (Procapra przewalskii) during both the rutting and non-rutting seasons to examine these issues.

Methodology/Principal Findings

Field observations were carried out with focal sampling during rutting and non-rutting season in 2008–2009. Results indicated a complex interplay between reproductive status, social rank, sex and group size in determining vigilance in this species. Vigilance decreased with group size in female but not in male gazelles. Males scanned more frequently and thus spent more time vigilant than females. Compared to non-rutting season, gazelles increased time spent scanning at the expense of bedding in rutting season. During the rutting season, territorial males spent a large proportion of time on rutting activities and were less vigilant than non-territorial males. Although territorial males may share collective risk detection with harem females, we suggest that they are probably more vulnerable to predation because they seemed reluctant to leave rut stands under threats.

Conclusions/Significance

Vigilance behavior in Przewalski''s gazelle was significantly affected by reproductive status, social rank, sex, group size and their complex interactions. These findings shed light on the mechanisms underlying vigilance patterns and the tradeoff between vigilance and other crucial activities.     

Effect of Group Size on Individual and Collective Vigilance in Greater Rheas

We studied the effect of group size on the proportion of time that greater rheas, Rhea americana, allocated to vigilance and feeding during the non‐breeding season. We tested whether: (1) the proportion of time that one bird allocates to vigilance (individual vigilance) decreases with group size, and (2) the proportion of time that at least one bird of the group is vigilant (collective vigilance) increases with group size. We analyzed video‐recordings of birds that were foraging alone or in groups from two to 12 birds. The proportion of time allocated to individual vigilance decreased and the proportion of time spent feeding increased with group size. In both cases the main significant difference was between birds foraging alone and in groups. Collective vigilance did not vary with group size and it was lower than expected if vigilance bouts were random or sequential. Our results indicate that rheas foraging in large groups would not receive the benefit of an increase in collective vigilance, although they could still benefit from a reduction of predation risk by the dilution effect.     

Social grooming in assamese macaques (Macaca assamensis)

Reciprocity and social bonding hypotheses were evaluated as explanations for observed patterns of social grooming in assamese macaques (Macaca assamensis). In accordance with social bonding, females, as the long-term residents of this matrifocal group, groomed each other and juveniles more often than males groomed one another or juveniles. On the other hand, males groomed females more often and for longer durations than females groomed males and, whereas both males and females groomed juveniles more often than juveniles groomed them, juveniles groomed their elders for longer durations. Male grooming of females did not seem directly related to matings as males are single mount ejaculators and use coercive mating tactics. Male grooming of females could not be accounted for in terms of reciprocity; it was not a simple function of dominance. Although both sexes groomed subordinate females more than vice versa, males groomed dominant males more and females groomed subordinate males more than they received grooming from them. Grooming was concluded to function to establish and maintain affiliative social bonds rather than as a specific mechanism to obtain matings or any other specific reciprocation in terms of services or favors.     

The Consequences of Predation Risk on the Male Territorial Behavior in a Solitary Bee

Territorial males may adopt a mating tactic that yields greater reproductive success but that at the same time increases the risk of predation. Plasticity in reproductive behavior can reflect a balance between sexual selection and natural selection. In this study, we sought to verify the effect of predation risk on territorial behavior of males of the solitary bee Ptilothrix fructifera (Apidae). Males of the species employ alternative mating tactics and can be territorial in defense of larval food sources. By manipulating predator models in the field, we tested whether (1) males avoid perch flowers containing predator models; (2) males alternate between mating tactics when their territory is associated with a predation risk; and (3) female foraging on flowers in a territory is altered in the presence of a predator model. We measured the responses of males and females in flowers containing and not containing a model of a spider or a stuffed bird. The results show that territorial males of P. fructifera alter their territorial behavior when faced with a high risk of predation. They do not abandon their territory or change to a non‐territorial mating tactic, but instead change the use of their territory, avoiding flowers containing predator models or perching on other flowers when the previous flower presented a potential predation risk. Female P. fructifera decreases the frequency of their visits to flowers and the length of time spent there in the presence of a spider model. In short, in the face of predation risk, females and males alter their behaviors at the cost of less efficient foraging and searching for partners, respectively.     

On how risk and group size interact to influence vigilance

Vigilance allows animals to monitor their surroundings for signs of danger associated with predators or rivals. As vigilance is costly, models predict that it should increase when the risk posed by predators or rivals increases. In addition, vigilance is expected to decrease in larger groups that provide more safety against predators. Risk and group size are thus two key determinants of vigilance. Together, they could have additive or interactive effects. If risk and group size interacted, the magnitude of the group‐size effect on vigilance would vary depending on the level of risk experienced, implying that the benefits of sociality in terms of vigilance vary with risk. Depending on the model, vigilance is predicted to decrease more rapidly with group size at low risk or at high risk. Little work has focused directly on the interaction between risk and group size, making it difficult to understand under which conditions particular interactive effects arise and whether interactive effects are common in natural systems. I review the vast literature on vigilance in birds and mammals to assess whether interactive effects between risk and group size are common, and if present, which pattern occurs more frequently. In studies involving predation risk, the greatest proportion reported no statistically significant interactive effects. In other cases, vigilance decreased with group size more rapidly at low or high risk in a similar proportion of studies. In studies involving risk posed by rivals (social risk), most documented a more rapid decrease in vigilance with group size at low than at high risk, as predicted if the need to monitor rivals increases in larger groups. Low statistical power to detect interactive effects might have been an issue in several studies. The absence of interactive effects, on the other hand, might suggest constraints or limits on the ability of animals to adjust vigilance to current risk or group sizes. Interactive effects on vigilance have implications for the evolution of sociality and for our understanding of the phenotypic plasticity of predator‐ and competitor‐induced defences and deserve more attention in future studies.     

Behavioral response of 12 ungulate species in captivity to the presence of humans

Twelve species of captive ungulates were studied to determine behavioral responses to the presence of a zookeeper within the exhibit and in front of the exhibit, with and without zoo visitors present. Significant differences in behavior occurred between species for nearly all behaviors observed. A significantly greater occurrence of vigilance and approach behavior was directed toward the zookeeper while within the exhibit relative to when the zookeeper stood in front of the exhibit. A significantly lower occurrence of eating or drinking occurred when the zookeeper was inside the exhibit. Significant differences occurred across size categories in the occurrence of approaching the zookeeper. The most frequently scored behavior was visual orientation. Statistically significant differences in the occurrence of visual orientation directed by females toward the zookeeper existed across size category, with more vigilance by species with larger body size. A statistically higher occurrence of vigilance toward the zookeeper was directed by female ungulates but not by males when the zoo was closed to the public. Although no statistical significance was found regarding the intraspecific vigilance of males, data on females revealed significant differences across species and across size categories. When data regarding vigilance toward the public were analyzed, statistically significant differences existed between species for females only. Likewise, when data regarding interspecific vigilance were examined, statistically significant differences were found across size categories for females, but not for males. The potential roles of vigilance in the wild are discussed in reference to its role in captivity.