Mutualism among safe, selfish sentinels: a dynamic game

Sentinels are group members that watch from prominent positions. Sentinel interchanges often appear orderly, and groups with sentinels rarely have zero or many sentinels. A dynamic game was constructed to examine if these observations about sentinels could be based on selfish actions by individual group members. In this game, each group member chose to forage or be a sentinel based on its own energetic state and the actions of others. Sentinels received a selfish antipredator benefit if their ability to detect approaching predators more than compensated for their increased exposure to undetected predators. Provided sentinels were relatively safe and that detection information spread to other group members when sentinels detected predators, sentinels appeared highly coordinated for all combinations of parameters. This apparent coordination was based on mutualism because each individual gained by being a sentinel when other group members were not (and foraging when other group members were being sentinels). The model was very robust, but exact level of sentinel behavior varied somewhat with changes in foraging and predation parameters. This model could best be tested by testing its assumptions about sentinel safety, foraging-predation trade-offs, and information transfer in groups.     

Florida Scrub-Jays (Aphelocoma coerulescens) are Sentinels More When Well-Fed (Even with no Kin Nearby)

Sentinels occupy high, exposed positions while other group members forage nearby. If sentinel behavior involves a foraging–predation risk trade‐off, animals should be sentinels more when fed supplemental food. When individual Florida scrub‐jays (Aphelocoma coerulescens) were fed fragments of peanuts, during the following 30 min they shifted 30% of their time from foraging to sentinel behavior. In a follow‐up experiment, we fed either one or two members in each group. As before, the jays reduced their foraging and spent much more time as sentinels when given supplemental food. In each treatment, pairs were sentinels simultaneously considerably less often than expected by chance. The dramatic shift from foraging to sentinel behavior suggests that for Florida scrub‐jays sentinel behavior brings substantial benefits for no greater cost than that of lost opportunities to forage. Because the results held for simple mated pairs of scrub‐jays, we argue that kin selection and social prestige are not necessary to explain sentinel behavior.     

Calling by Concluding Sentinels: Coordinating Cooperation or Revealing Risk?

Efficient cooperation requires effective coordination of individual contributions to the cooperative behaviour. Most social birds and mammals involved in cooperation produce a range of vocalisations, which may be important in regulating both individual contributions and the combined group effort. Here we investigate the role of a specific call in regulating cooperative sentinel behaviour in pied babblers (Turdoides bicolor). 'Fast-rate chuck' calls are often given by sentinels as they finish guard bouts and may potentially coordinate the rotation of individuals as sentinels, minimising time without a sentinel, or may signal the presence or absence of predators, regulating the onset of the subsequent sentinel bout. We ask (i) when fast-rate chuck calls are given and (ii) what effect they have on the interval between sentinel bouts. Contrary to expectation, we find little evidence that these calls are involved in regulating the pied babbler sentinel system: observations revealed that their utterance is influenced only marginally by wind conditions and not at all by habitat, while observations and experimental playback showed that the giving of these calls has no effect on inter-bout interval. We conclude that pied babblers do not seem to call at the end of a sentinel bout to maximise the efficiency of this cooperative act, but may use vocalisations at this stage to influence more individually driven behaviours.     

Cooperative sentinel calling? Foragers gain increased biomass intake

Many foraging animals face a fundamental tradeoff between predation and starvation. In a range of social species, this tradeoff has probably driven the evolution of sentinel behavior, where individuals adopt prominent positions to watch for predators while groupmates forage. Although there has been much debate about whether acting as a sentinel is a selfish or cooperative behavior, far less attention has focused on why sentinels often produce quiet vocalizations (hereafter known as "sentinel calls") to announce their presence. We use observational and experimental data to provide the first evidence that group members gain an increase in foraging success by responding to these vocal cues given by sentinels. Foraging pied babblers (Turdoides bicolor) spread out more, use more exposed patches, look up less often, and spend less time vigilant in response to sentinel calling. Crucially, we demonstrate that these behavioral alterations lead to an increase in biomass intake by foragers, which is likely to enhance survival. We argue that this benefit may be the reason for sentinel calling, making it a truly cooperative behavior.     

Do Conversational Gutturals Help Florida Scrub‐Jays Coordinate Their Sentinel Behavior?

Florida scrub‐jays, Aphelocoma coerulescens, perform sentinel behavior in which individuals alternate bouts of watchfulness with little overlap. We examined how calls might facilitate sentinel coordination. Small soft calls labeled conversational gutturals were heard more often from sentinels than from foraging birds. Calls occurred infrequently throughout sentinel bouts but were more common later in bouts. The pattern of calling does not match predictions for a ‘watchman’s song’ at regular intervals nor for a signal at the end of a sentinel bout. Thus, our quantitative assessment of calling by sentinels did not find support for either standard hypothesis. Although Florida scrub‐jays clearly have information on each other’s sentinel behavior, our results suggest that calls provide perhaps a fraction of this information.     

Interspecific signalling between mutualists: food-thieving drongos use a cooperative sentinel call to manipulate foraging partners

Interspecific communication is common in nature, particularly between mutualists. However, whether signals evolved for communication with other species, or are in fact conspecific signals eavesdropped upon by partners, is often unclear. Fork-tailed drongos (Dicrurus adsimilis) associate with mixed-species groups and often produce true alarms at predators, whereupon associating species flee to cover, but also false alarms to steal associating species'' food (kleptoparasitism). Despite such deception, associating species respond to drongo non-alarm calls by increasing their foraging and decreasing vigilance. Yet, whether these calls represent interspecific sentinel signals remains unknown. We show that drongos produced a specific sentinel call when foraging with a common associate, the sociable weaver (Philetairus socius), but not when alone. Weavers increased their foraging and decreased vigilance when naturally associating with drongos, and in response to sentinel call playback. Further, drongos sentinel-called more often when weavers were moving, and weavers approached sentinel calls, suggesting a recruitment function. Finally, drongos sentinel-called when weavers fled following false alarms, thereby reducing disruption to weaver foraging time. Results therefore provide evidence of an ‘all clear’ signal that mitigates the cost of inaccurate communication. Our results suggest that drongos enhance exploitation of a foraging mutualist through coevolution of interspecific sentinel signals.     

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.     

Moving calls: a vocal mechanism underlying quorum decisions in cohesive groups

Members of social groups need to coordinate their behaviour when choosing between alternative activities. Consensus decisions enable group members to maintain group cohesion and one way to reach consensus is to rely on quorums. A quorum response is where the probability of an activity change sharply increases with the number of individuals supporting the new activity. Here, we investigated how meerkats (Suricata suricatta) use vocalizations in the context of movement decisions. Moving calls emitted by meerkats increased the speed of the group, with a sharp increase in the probability of changing foraging patch when the number of group members joining the chorus increased from two up to three. These calls had no apparent effect on the group's movement direction. When dominant individuals were involved in the chorus, the group's reaction was not stronger than when only subordinates called. Groups only increased speed in response to playbacks of moving calls from one individual when other group members emitted moving calls as well. The voting mechanism linked to a quorum probably allows meerkat groups to change foraging patches cohesively with increased speed. Such vocal coordination may reflect an aggregation rule linking individual assessment of foraging patch quality to group travel route.     

The higher the better: sentinel height influences foraging success in a social bird

In all social species, information relevant to survival and reproduction can be obtained in two main ways: through personal interaction with the environment (i.e. ‘personal’ information) and from the performance of others (i.e. ‘public’ information). While public information is less costly to obtain than personal information, it may be inappropriate or inaccurate. When deciding how much to rely on public information, individuals should therefore assess its potential quality, but this possibility requires empirical testing in animals. Here, we use the sentinel system of cooperatively breeding pied babblers (Turdoides bicolor) to investigate how behavioural decisions of foragers are influenced by potential variation in the quality of anti-predator information from a vigilant groupmate. When sentinels moved to a higher position, from where their probability of detecting predators is likely to be greater, foragers reduced their vigilance, spread out more widely and were more likely to venture into the open. Consequently, they spent more time foraging and increased their foraging efficiency, resulting in a profound increase in biomass intake rate. The opposite behavioural changes, and consequent foraging outcomes, were found when sentinels moved lower. A playback experiment demonstrated that foragers can use vocal cues alone to assess sentinel height. This is the first study to link explicitly a measure of the potential quality of public information with a fitness measure from those relying on the information, and our results emphasize that a full understanding of the evolution of communication in complex societies requires consideration of the reliability of information.     

Risky foraging leads to cost-free mate guarding in male teal Anas crecca

Mate guarding by males is common in species with long-lasting pair bonds. We tested if the need to guard females affected foraging depth in male teal (Anas crecca), and if they were more vigilant than females when foraging with submerged eyes (preventing monitoring of competing males and predators). These predictions were not supported, suggesting that foraging depth selection is primarily driven by other factors, presumably food related. A likely reason why deeply foraging males did not increase vigilance is that 37.5% of the foraging time was already dedicated to it. The apparent lack of guarding costs in foraging male teal may explain why such small ducks can maintain pair bonds for up to 7 months.     

The guard honey bee: ontogeny and behavioural variability of workers performing a specialized task

Guarding is a relatively unstudied aspect of honey bee, Apis mellifera L., worker behaviour. The aim of this study was to characterize quantitatively the ontogeny and individual variability of guarding behaviour, the allocation of workers to the guard population in a colony, and the intercolonial variability of guarding behaviour. Guarding is a discrete task performed by a distinct group of workers that are younger than foragers and older than house bees. Workers that guarded initiated the behaviour between the ages of 7 and 22 days. The mean age of the onset of guarding varied; the minimum mean age of guards for a colony was 13·6 days and the maximum was 16·0 days. Workers varied in the length of time they spent as a guard. Most bees guarded for less than 1 days; however, some guarded up to 6 consecutive days. The more time a bee spent guarding during a day the more likely that bee was to guard for more than 1 day. Bees that guarded for more than 1 day also had longer and more frequent individual guarding bouts. All colonies that were studied had guard populations, but not all workers guarded. A relatively small proportion of any age cohort was observed to guard. The percentage of an age cohort that guarded varied among colonies, as did the size of the guard population. Guarding is a specialized task in that few bees guard, but guarding does not appear to require experience because so few bees remained as guards for very long. There was intercolonial variation in all aspects of the ontogeny of guarding and in allocation of workers to guarding. This variation is discussed in the light of other studies of variation in worker behaviour.     

Predation risk affects trade-off between nest guarding and foraging in Seychelles warblers

The fitness costs of egg loss for Seychelles warblers (Acrocephalus sechellensis)on Cousin Island are considerable because warblers have a single-eggclutch and no time to lay a successful replacement clutch. Onthe islands of Cousin and Cousine, with equal densities of Seychellesfodies (Foudia sechellarum), nearly 75% of artificial eggs placedin artificial nests were predated by fodies after 3 days. OnAride Island with no fodies present, loss of artificial eggswas not observed. Female warblers incubate the clutch, and malewarblers guard the clutch when females are absent. Deterrenceof fodies by male warblers is efficient: loss rate of eggs fromunattended warbler nests was seven times as high as from attendednests, and the more nest guarding, the lower the egg loss andthe higher the hatching success. Egg loss is independent ofthe amount of incubation by females. There is no trade-off betweenincubating and foraging by females. Nest guarding competes withforaging by males, and this trade-off has a more pronounced effecton egg loss when food availability is low. The transfer of breeding pairsfrom Cousin to either Cousine with egg-predating fodies or toAride without fodies allowed us to experimentally investigatethe presumed trade-off between nest guarding and foraging. OnCousine, individual males spent the same amount of time nestguarding and foraging as on Cousin, and egg loss was similarand inversely related to time spent nest guarding as on Cousin.Males that guarded their clutch on Cousin did not guard theclutch on Aride but allocated significantly more time to foragingand gained better body condition. Loss of warbler eggs on Aridewas not observed. Time allocation to incubating and foragingby individual females before and after both translocations remainedthe same.     

Florida Scrub-Jays Compensate for the Sentinel Behavior of Flockmates

Sentinel coordination requires that individuals react to the sentinel behavior of others. Previous work showed that Florida scrub‐jays are sentinels more often when given supplemental food. Here we measured how birds in pairs reacted when their mates were fed. Scrub‐jays were sentinels less when their mates were fed, demonstrating compensation. Indirect evidence suggests that this compensatory decrease in sentinel behavior was smaller than the increase in sentinel behavior by their mates. In addition, males in newly established groups were sentinels less often.     

Social foragers adopt a riskier foraging mode in the centre of their groups

Foraging in groups provides many benefits that are not necessarily experienced the same way by all individuals. I explore the possibility that foraging mode, the way individuals exploit resources, varies as a function of spatial position in the group, reflecting commonly occurring spatial differences in predation risk. I show that semipalmated sandpipers (Calidris pusilla), a social foraging avian species, tended to adopt a riskier foraging mode in the central, more protected areas of their groups. Central birds effectively used the more peripheral group members as sentinels, allowing them to exploit a wider range of resources within the same group at the same time. This finding provides a novel benefit of living in groups, which may have a broad relevance given that social foraging species often exploit a large array of resources.     

Effects of proximity and activity on visual and auditory monitoring in wild Japanese macaques

Group-living primates monitor group members to maintain the spatial cohesiveness of the group. We examined the possibility that visual scanning (turning the head for more than 3 sec) and contact calls (coo calls) function as visual and auditory monitoring behaviors to avoid separation from group members in wild Japanese macaques. The rate of visual scanning increased as proximity to group members decreased and as mobile activities (foraging and moving) increased, compared with immobile activities (resting and grooming). However, the rate of contact calls varied differently with proximity and activities. During resting and moving, the rate of contact calls increased as proximity decreased. In contrast, the rate increased with closer proximity during feeding. Visual scanning during all activities and contact calls during resting and moving increased when the group members were likely to spread over a larger area, suggesting that these behaviors functioned as monitoring of group members to avoid separation from the group. Contact calls also increased when the group members stayed in close proximity during foraging, suggesting that this behavior was also associated with competitive situations. Contact calls may also function to ease tension or maintain distance to avoid conflict in competitive situations.     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

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

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

Raptors and "campo-cerrado" bird mixed flock LED BY Cypsnagra hirundinacea (Emberizidae:Thraupinae)

Bird mixed flocks including Cypsnagra hirundinacea and Neothraupis fasciata as species with sentinels were studied in "campo-cerrado" in order to investigate the possible relationship between alertness and the mixed flock leadership. This study was conducted from March to September 1996 and mixed flocks were observed on average for 2:30h. The time with sentinels were recorded for C. hirundinacea and N. fasciata. The sentinels of Cypsnagra hirundinacea performed most of the vigilance (time with sentinel was on average 42 +/- 17%, 41 +/- 17% of which by C. hirundinacea, whereas only 1.2% by N. fasciata) and gave all the alarm calls recorded (54% of the encounters with raptors stimulated alarm calls). A relationship was verified between time with sentinel and the rate of encounters with raptor (ANOVA, F = 3.0. P < 0.05). The results of this study are an evidence for the anti-predatory function of mixed flocks, in campo-cerrado, and the alertness as a major feature of a leader species, since C. hirundinacea always led those flocks.     

A sentinel system in the Florida scrub jay

One postulated advantage of living in groups is increased protection from predators. Living in small, permanent groups of stable composition allows for the formation of a sentinel system, in which individuals coordinate their vigilance. Florida scrub jays, Aphelocoma coerulescens coerulescens, live in family groups, and coordinate their vigilance into a sentinel system. Observed vigilance behaviour was compared with models generating similar behaviour patterns at random. The occurrence of one jay terminating vigilance in the same minute that another initiated vigilance was greater than expected by chance, and the occurrence of more than one vigilant jay at one time was less frequent than expected by chance. The seasonal pattern of scrub jay sentinel behaviour suggests that it functions primarily for predator detection, especially of raptors. Most aerial predator alarm calls were given by sentinels, and a sentinel was most likely to give the alarm call first.