Kinship, dear enemies, and costly combat: The effects of relatedness on territorial overlap and aggression in a cooperative breeder.

Many species maintain territories, but the degree of overlap between territories and the level of aggression displayed in territorial conflicts can vary widely, even within species. Greater territorial overlap may occur when neighboring territory holders are close relatives. Animals may also differentiate neighbors from strangers, with more familiar neighbors eliciting less-aggressive responses during territorial conflicts (the "dear enemy" effect). However, research is lacking in how both kinship and overlap affect territorial conflicts, especially in group-living species. Here, we investigate kinship, territorial overlap, and territorial conflict in a habituated wild population of group-living cooperatively breeding birds, the southern pied babbler Turdoides bicolor. We find that close kin neighbors are beneficial. Territories overlap more when neighboring groups are close kin, and these larger overlaps with kin confer larger territories (an effect not seen for overlaps with unrelated groups). Overall, territorial conflict is costly, causing significant decreases in body mass, but conflicts with kin are shorter than those conducted with nonkin. Conflicts with more familiar unrelated neighbors are also shorter, indicating these neighbors are "dear enemies." However, kinship modulates the "dear enemy" effect; even when kin are encountered less frequently, kin elicit less-aggressive responses, similar to the "dear enemy" effect. Kin selection appears to be a main influence on territorial behavior in this species. Groups derive kin-selected benefits from decreased conflicts and maintain larger territories when overlapping with kin, though not when overlapping with nonkin. More generally, it is possible that kinship extends the "dear enemy" effect in animal societies.

Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder.

Kin selection theory predicts that animals should direct costly care where inclusive fitness gains are highest. Individuals may achieve this by directing care at closer relatives, yet evidence for such discrimination in vertebrates is equivocal. We investigated patterns of cooperative care in banded mongooses, where communal litters are raised by adult 'escorts' who form exclusive caring relationships with individual pups. We found no evidence that escorts and pups assort by parentage or relatedness. However, the time males spent escorting increased with increasing relatedness to the other group members, and to the pup they had paired with. Thus, we found no effect of relatedness in partner choice, but (in males) increasing helping effort with relatedness once partner choices had been made. Unexpectedly, the results showed clear assortment by sex, with female carers being more likely to tend to female pups, and male carers to male pups. This sex-specific assortment in helping behaviour has potential lifelong impacts on individual development and may impact the future size and composition of natal groups and dispersing cohorts. Where relatedness between helpers and recipients is already high, individuals may be better off choosing partners using other predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination.

Explaining negative kin discrimination in a cooperative mammal society.

Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

Calling Where It Counts: Subordinate Pied Babblers Target the Audience of Their Vocal Advertisements.

For territorial group-living species, opportunities to reproduce on the natal territory can be limited by a number of factors including the availability of resources within a territory, access to unrelated individuals, and monopolies on reproduction by dominant group members. Individuals looking to reproduce are therefore faced with the options of either waiting for a breeding opportunity to arise in the natal territory, or searching for reproductive opportunities in non-natal groups. In the cooperatively breeding Southern pied babbler, Turdoides bicolor, most individuals who achieve reproductive success do so through taking up dominant breeding positions within non-natal groups. For subordinate pied babblers therefore, searching for breeding opportunities in non-natal groups is of primary importance as this represents the major route to reproductive success. However, prospecting (where individuals leave the group to search for reproductive opportunities within other groups) is costly and individuals rapidly lose weight when not part of a group. Here we demonstrate that subordinate pied babblers adopt an alternative strategy for mate attraction by vocal advertisement from within their natal territories. We show that subordinates focus their calling efforts on the edges of their territory, and specifically near boundaries with neighbouring groups that have potential breeding partners (unrelated individuals of the opposite sex). In contrast to prospecting, calling individuals showed no body mass loss associated with this behaviour, suggesting that calling from within the group may provide a 'cheap' advertisement strategy. Additionally, we show that subordinates use information regarding the composition of neighbouring groups to target the greatest number of potential mating partners.

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.

Singing for your supper: sentinel calling by kleptoparasites can mitigate the cost to victims.

Parasitism generally imposes costs on victims, yet many victims appear to tolerate their parasites. We suggest that in some cases this may be because parasites provide victims with mitigating benefits, paradoxically giving rise to selection for advertisement rather than concealment by parasites. We investigate this possibility using the interaction between an avian kleptoparasite, the fork-tailed drongo (Dicrurus adsimilis), and one of its victims, the pied babbler (Turdoides bicolor). Combining field observations and a playback experiment, we demonstrate that a conspicuous vocal signal broadcast by drongos perched waiting to steal food from foraging babblers allows the latter to improve their own foraging efficiency, although not to the same extent as that experienced in response to conspecific sentinel calling. We argue that "sentinel" calling by drongos may originally have arisen as a means of manipulating babblers: because babblers find more food items and venture into the open more in response to these vocalizations, drongos are presented with more kleptoparasitism opportunities. However, the resulting benefit to babblers could be sufficient to reduce selection for the evolution of defenses against drongos, and the current situation may represent a rare example of an interspecific relationship in transition from a parasitism to a mutualism.

Reproductive control via eviction (but not the threat of eviction) in banded mongooses.

Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the 'restraint' model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive 'transaction' to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each other's reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.

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.

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.

Strategic adjustment of begging effort by banded mongoose pups.

Variation in the intensity of conspicuous displays raises three basic questions: (i) the relationship between internal state and display intensity, (ii) the relationship between display intensity and receiver response, and (iii) the effect of variation in receiver responsiveness on signaller behaviour. Here, I investigate the interaction between pups and helpers in the communally breeding banded mongoose (Mungos mungo), where each pup forms an exclusive relationship with a single adult helper (termed its 'escort'). By experimentally manipulating pup need, I demonstrate that changes in begging rate correspond to changes in short-term need. The data then suggest that escorts in good condition may be more responsive to increased begging and that pups associating with them increase their begging more than do pups paired with escorts in poor condition. Escorts also appear more responsive to increased begging by female pups, and female pups increase their begging more than do male pups. These results suggest that banded mongoose pups may strategically adjust their investment in begging in relation to variation in the expected pay-off. I argue that such adjustment is likely to be a general phenomenon: wherever there is variation in responsiveness to signals, signallers will be selected to identify different categories of receiver and adjust their signals in order to maximize the pay-offs. Therefore, differences in signal intensity may be as much a product of context as an indication of variation in individual phenotypic or genotypic state.

Interspecific audience effects on the alarm-calling behaviour of a kleptoparasitic bird.

Audience effects are increasingly recognized as an important aspect of intraspecific communication. Yet despite the common occurrence of interspecific interactions and considerable evidence that individuals respond to the calls of heterospecifics, empirical evidence for interspecific audience effects on signalling behaviour is lacking. Here we present evidence of an interspecific audience effect on the alarm-calling behaviour of the kleptoparasitic fork-tailed drongo (Dicrurus adsimilis). When foraging solitarily, drongos regularly alarm at aerial predators, but rarely alarm at terrestrial predators. In contrast, when drongos are following terrestrially foraging pied babblers (Turdoides bicolor) for kleptoparasitic opportunities, they consistently give alarm calls to both aerial and terrestrial predators. This change occurs despite no difference in the amount of time that drongos spend foraging terrestrially. Babblers respond to drongo alarm calls by fleeing to cover, providing drongos with opportunities to steal babbler food items by occasionally giving false alarm calls. This provides an example of an interspecific audience effect on alarm-calling behaviour that may be explained by the benefits received from audience response.

Cooperative begging in banded mongoose pups.

Vivid begging displays are common in species with parental care [1, 2]. They are usually seen as the way that rival offspring selfishly compete over parental investment [3], and individuals are expected to respond to the begging of rivals by increasing their own begging intensity [4, 5]. Here I show the opposite - that potential rivals gain direct benefits from begging by littermates, so that begging behavior becomes a collective enterprise, similar to other cooperative activities. I investigate begging in communally breeding banded mongooses (Mungos mungo), where each pup forms an exclusive relationship with a single helper (its "escort"), minimizing competition over food allocation. Escorts were influenced by the total signal emanating from a litter, so that pups who begged at low rates received more food as litter size increased. Focal pups increased their begging when litters were experimentally reduced or littermates were induced to beg at low rates, but they received food at similar rates and showed reduced weight gain - indicating that they were paying a higher cost for a similar reward. These results suggest that offspring can benefit from companions despite conflicts over the allocation of parental investment [6, 7]. Such benefits provide an explanation for observed variation in the expression of parent-offspring conflict.