Fighting force and experience combine to determine contest success in a warlike mammal.

Conflicts between social groups or "intergroup contests" are proposed to play a major role in the evolution of cooperation and social organization in humans and some nonhuman animal societies. In humans, success in warfare and other collective conflicts depends on both fighting group size and the presence and actions of key individuals, such as leaders or talismanic warriors. Understanding the determinants of intergroup contest success in other warlike animals may help to reveal the role of these contests in social evolution. Using 19 y of data on intergroup encounters in a particularly violent social mammal, the banded mongoose (Mungos mungo), we show that two factors, the number of adult males and the age of the oldest male (the "senior" male), have the strongest impacts on the probability of group victory. The advantage conferred by senior males appears to stem from their fighting experience. However, the galvanizing effect of senior males declines as they grow old until, at very advanced ages, senior males become a liability rather than an asset and can be evicted. As in human conflict, strength in numbers and the experience of key individuals combine to determine intergroup contest success in this animal society. We discuss how selection arising from intergroup contests may explain a suite of features of individual life history and social organization, including male eviction, sex-assortative alloparental care, and adult sex ratio.

Exploitative leaders incite intergroup warfare in a social mammal.

Collective conflicts among humans are widespread, although often highly destructive. A classic explanation for the prevalence of such warfare in some human societies is leadership by self-serving individuals that reap the benefits of conflict while other members of society pay the costs. Here, we show that leadership of this kind can also explain the evolution of collective violence in certain animal societies. We first extend the classic hawk-dove model of the evolution of animal aggression to consider cases in which a subset of individuals within each group may initiate fights in which all group members become involved. We show that leadership of this kind, when combined with inequalities in the payoffs of fighting, can lead to the evolution of severe intergroup aggression, with negative consequences for population mean fitness. We test our model using long-term data from wild banded mongooses, a species characterized by frequent intergroup conflicts that have very different fitness consequences for male and female group members. The data show that aggressive encounters between groups are initiated by females, who gain fitness benefits from mating with extragroup males in the midst of battle, whereas the costs of fighting are borne chiefly by males. In line with the model predictions, the result is unusually severe levels of intergroup violence. Our findings suggest that the decoupling of leaders from the costs that they incite amplifies the destructive nature of intergroup conflict.

Call order within vocal sequences of meerkats contains temporary contextual and individual information.

BACKGROUND: The ability to recombine smaller units to produce infinite structures of higher-order phrases is unique to human language, yet evidence of animals to combine multiple acoustic units into meaningful combinations increases constantly. Despite increasing evidence for meaningful call combinations across contexts, little attention has been paid to the potential role of temporal variation of call type composition in longer vocal sequences in conveying information about subtle changes in the environment or individual differences. Here, we investigated the composition and information content of sentinel call sequences in meerkats (Suricata suricatta). While being on sentinel guard, a coordinated vigilance behaviour, meerkats produce long sequences composed of six distinct sentinel call types and alarm calls. We analysed recordings of sentinels to test if the order of the call types is graded and whether they contain additional group-, individual-, age- or sex-specific vocal signatures. RESULTS: Our results confirmed that the six distinct types of sentinel calls in addition to alarm calls were produced in a highly graded way, likely referring to changes in the perceived predation risk. Transitions between call types one step up or down the a priory assumed gradation were over-represented, while transitions over two or three steps were significantly under-represented. Analysing sequence similarity within and between groups and individuals demonstrated that sequences composed of the most commonly emitted sentinel call types showed high within-individual consistency whereby adults and females had higher consistency scores than subadults and males respectively. CONCLUSIONS: We present a novel type of combinatoriality where the order of the call types contains temporary contextual information, and also relates to the identity of the caller. By combining different call types in a graded way over long periods, meerkats constantly convey meaningful information about subtle changes in the external environment, while at the same time the temporal pattern of the distinct call types contains stable information about caller identity. Our study demonstrates how complex animal call sequences can be described by simple rules, in this case gradation across acoustically distinct, but functionally related call types, combined with individual-specific call patterns.

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.

Meerkats (Suricata suricatta) fail to prosocially donate food in an experimental set-up.

Although humans are usually believed to be prosocial, the evolutionary origins of prosociality are largely debated. One hypothesis is that cooperative breeding has been one major precursor to the emergence of prosociality. In vertebrates, however, experimental evidence of prosociality has been mainly gathered in non-human primates. In this study, we tested the cooperative breeding hypothesis in cooperative breeding meerkats (Suricata suricatta). In particular, we tested whether meerkats take into account partners' benefits when distributing food rewards. Nine individuals were presented with two platforms baited with different food distributions (providing food to themselves, to a partner or both). In all conditions, the decision to operate the apparatus was based on the presence of food on the subject's side, and not on the possible benefits to partners. Despite being cooperative breeders, meerkats in this study failed to be prosocial, suggesting that prosociality in this species may be limited to specific contexts.

Social-bond strength influences vocally mediated recruitment to mobbing.

Strong social bonds form between individuals in many group-living species, and these relationships can have important fitness benefits. When responding to vocalizations produced by groupmates, receivers are expected to adjust their behaviour depending on the nature of the bond they share with the signaller. Here we investigate whether the strength of the signaller-receiver social bond affects response to calls that attract others to help mob a predator. Using field-based playback experiments on a habituated population of wild dwarf mongooses (Helogale parvula), we first demonstrate that a particular vocalization given on detecting predatory snakes does act as a recruitment call; receivers were more likely to look, approach and engage in mobbing behaviour than in response to control close calls. We then show that individuals respond more strongly to these recruitment calls if they are from groupmates with whom they are more strongly bonded (those with whom they preferentially groom and forage). Our study, therefore, provides novel evidence about the anti-predator benefits of close bonds within social groups.

Cooperative personalities and social niche specialization in female meerkats.

The social niche specialization hypothesis predicts that group-living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life-history strategies for different roles. Social niche specialization, coupled with role-specific life-history trade-offs, should thus generate between-individual differences in behaviour that persist through time, or distinct personalities, as individuals specialize in particular nonoverlapping social roles. We tested for support for the social niche specialization hypothesis in cooperative personality traits in wild female meerkats (Suricata suricatta) that compete for access to dominant social roles. As cooperation is costly and dominance is acquired by heavier females, we predicted that females that ultimately acquired dominant roles would show noncooperative personality types early in life and before and after role acquisition. Although we found large individual differences in repeatable cooperative behaviours, there was no indication that individuals that ultimately acquired dominance differed from unsuccessful individuals in their cooperative behaviour. Early-life behaviour did not predict social role acquisition later in life, nor was cooperative behaviour before and after role acquisition correlated in the same individuals. We suggest that female meerkats do not show social niche specialization resulting in cooperative personalities, but that they exhibit an adaptive response in personality at role acquisition.

Experimental evidence for delayed post-conflict management behaviour in wild dwarf mongooses.

In many species, within-group conflict leads to immediate avoidance of potential aggressors or increases in affiliation, but no studies have investigated delayed post-conflict management behaviour. Here, we experimentally test that possibility using a wild but habituated population of dwarf mongooses (Helogale parvula). First, we used natural and playback-simulated foraging displacements to demonstrate that bystanders take notice of the vocalisations produced during such within-group conflict events but that they do not engage in any immediate post-conflict affiliative behaviour with the protagonists or other bystanders. We then used another playback experiment to assess delayed effects of within-group conflict on grooming interactions: we examined affiliative behaviour at the evening sleeping burrow, 30-60 min after the most recent simulated foraging displacement. Overall, fewer individuals groomed on evenings following an afternoon of simulated conflict, but those that did groomed more than on control evenings. Subordinate bystanders groomed with the simulated aggressor significantly less, and groomed more with one another, on conflict compared to control evenings. Our study provides experimental evidence that dwarf mongooses acoustically obtain information about within-group contests (including protagonist identity), retain that information, and use it to inform conflict-management decisions with a temporal delay.

Social animals that live in groups often have disagreements over access to mates and food. Even fleeting in-group disputes can be costly, disrupting relationships, wasting time and energy, or causing injury if aggression escalates. So, much like humans, many social animals, including primates, birds and dogs, have evolved conflict management strategies to prevent and resolve in-group disagreements. In the immediate aftermath of a conflict, this usually involves changes in the interactions between those involved in the disagreement, or between bystander groupmates and either the victim or aggressor. Less is known about whether social animals can recall past disputes and if they can use conflict management strategies some time after a quarrel has occurred. That is, do aggressive interactions between groupmates influence later social decisions of bystanders in the group? To investigate, Morris-Drake et al. studied groups of wild dwarf mongooses (Helogale parvula) that have become accustomed to living alongside humans in Limpopo Province, South Africa. Dwarf mongooses live in groups of up to 30 individuals, with one dominant breeding pair and lower-ranked helpers. When disagreements arise over food, an aggressor growls deeply and hip-slams the victim away from their foraging patch, stealing the victim's prey in the process. Victims often produce high-pitched squeals in retreat. Using recordings of these calls, Morris-Drake et al. devised a field experiment to investigate how mongooses responded to nearby conflicts between other group members. Recordings simulating a conflict over food were played to groups of foraging mongooses over the course of an afternoon, so that group members effectively heard what sounded like repeated squabbles between two out-of-sight individuals. Similar to natural conflicts, the mongooses did not engage in any obvious conflict management behaviour immediately after hearing these disputes. But when the group returned to their sleeping burrow that evening, subordinate group members shunned the perceived aggressors from grooming, a key social activity. This work provides evidence that dwarf mongooses keep tabs on conflicts that occur between groupmates. It shows these animals can extract information about conflicts from vocal cues alone and that bystanders use this information when making later social decisions impacting group dynamics. It also adds to growing evidence from baboons, monkeys and chimpanzees that social animals can remember past events and take these into account when interacting with groupmates.

Do anvil-using banded mongooses understand means-end relationships? A field experiment.

Tool use and the associated need to choose appropriate objects for a particular task are thought to have selected for specialized cognitive abilities such as means-end comprehension. Several studies on large-brained tool-using primates and birds have demonstrated understanding of causal relationships to some extent. However, a comprehensive appraisal of this hypothesis requires testing for means-end comprehension also in non-tool-users as well as in small-brained tool users. Moreover, the results of captive studies do not answer the question whether such cognitive abilities are relevant to an animal in its natural environment. Here I presented wild banded mongooses Mungos mungo, small-brained carnivores that regularly use anvils to open food items with a hard shell, with a transfer test involving novel anvil objects. I found no evidence for means-end comprehension or a heuristic strategy used for anvil choice in this species. Instead, recognition of suitable anvils appears to be learned by trial and error separately for different categories of anvils. These data suggest that, at least for the anvil-choice task investigated here, the need to choose suitable objects has not selected for specialized cognitive abilities in banded mongooses, a finding that may extend to a large range of proto-tool users. Furthermore, this study adds to growing evidence that animals subjected to the selection pressures and trade-offs of their natural environment may get by with cognitively more simple strategies than sometimes suggested by captive studies or plausibility arguments.

The vocal repertoire in a solitary foraging carnivore, Cynictis penicillata, may reflect facultative sociality.

We describe the vocal repertoire of a facultatively social carnivore, the yellow mongoose, Cynictis penicillata. Using a combination of close-range observations, recordings and experiments with simulated predators, we were able to obtain clear descriptions of call structure and function for a wide range of calls used by this herpestid. The vocal repertoire of the yellow mongooses comprised ten call types, half of which were used in appeasing or fearful contexts and half in aggressive interactions. Data from this study suggest that the yellow mongoose uses an urgency-based alarm calling system, indicating high and low urgency through two distinct call types. Compared to solitary mongooses, the yellow mongoose has a large proportion of 'friendly' vocalisations that enhance group cohesion, but its vocal repertoire is smaller and less context-specific than those of obligate social species. This study of the vocal repertoire of the yellow mongoose is, to our knowledge, the most complete to have been conducted on a facultatively social species in its natural habitat.

Meerkats (Suricata suricatta) are able to detect hidden food using olfactory cues alone.

Meerkats (Suricata suricatta) are known to strongly rely on chemical signals for social communication. However, little is known about their use of the sense of smell in foraging and food detection. The aim of the present study was therefore to assess whether captive meerkats are able to (1) detect hidden food using olfactory cues alone, (2) discriminate between the odor of real food and a single food odor component, and (3) build an association between the odor of real food and a novel odor. We employed the buried food test, widely used with rodents to assess basic olfactory abilities and designed to take advantage of the propensity of certain species to dig. We found that the meerkats were clearly able to find all four food types tested (mouse, chicken, mealworm, banana) using olfactory cues alone and that they successfully discriminated between the odor of real food (banana) and a food odor component (iso-pentyl acetate). In both tasks, the animals dug in the food-bearing corner of the test arena as the first one significantly more often than in the other three corners. No significant association-building between a food odor and a novel odor was found within the 60 trials performed per animal. We conclude that meerkats are able to use olfactory cues when foraging for hidden food. Further, we conclude that the buried food test, employed for the first time with a non-rodent species, is a useful means of assessing basic olfactory capabilities in meerkats.

The number of subordinates moderates intrasexual competition among males in cooperatively breeding meerkats.

For dominant individuals in cooperatively breeding species, the presence of subordinates is associated with both benefits (i.e. increased reproductive output and other group-living benefits) and costs (i.e. intrasexual competition on reproduction). The biological market theory predicts that dominant individuals are tolerant to same-sex group members when there are only a few subordinates, so as to maximize their own reproductive success. We investigated factors affecting aggression by dominant males and submission by subordinate males for a cooperatively breeding mammal, meerkats, Suricata suricatta. In this species, reproductive conflict occurs between the dominant male and the non-offspring males. As predicted, the number of subordinates in a group was positively associated with the aggression frequency by the dominant male and with the submission frequency by the subordinate males. Relative to the aggression frequency against male offspring, the frequency of aggression against non-offspring males was comparable in small groups, but was higher in large groups. These results indicate that reproductive conflict is present between the dominant male and the non-offspring males but is moderated in groups with small numbers of subordinates. This study provides an empirical data agreeing with the biological market theory in the context of intrasexual competition in cooperatively breeding species.

Experience of the signaller explains the use of social versus personal information in the context of sentinel behaviour in meerkats.

To maximise foraging opportunities while simultaneously avoiding predation, group-living animals can obtain personal information on food availability and predation risk and/or rely on social information provided by group members. Although mainly associated with low costs of information acquisition, social information has the potential to be irrelevant or inaccurate. In this study we use playbacks of individually distinct sentinel calming calls produced during sentinel behaviour, a form of coordinated vigilance behaviour, to show that meerkats (Suricata suricatta) discriminate between social information provided by different sentinels and adjust their personal vigilance behaviour according to the individual that is played back. We found that foraging group members acquired the lowest amounts of personal information when hearing social information provided by experienced individuals that act as sentinels most often in their group and littermates. Our study shows that social information can be flexibly used in the context of sentinel behaviour in order to optimize the trade-off between foraging and vigilance behaviours dependent on discrimination among signallers. We also provide novel evidence that the experience of sentinels rather than their age or dominance status is the main factor affecting the extent to which individuals use social information.

Decoupling of Genetic and Cultural Inheritance in a Wild Mammal.

Cultural inheritance, the transmission of socially learned information across generations, is a non-genetic, "second inheritance system" capable of shaping phenotypic variation in humans and many non-human animals [1-3]. Studies of wild animals show that conformity [4, 5] and biases toward copying particular individuals [6, 7] can result in the rapid spread of culturally transmitted behavioral traits and a consequent increase in behavioral homogeneity within groups and populations [8, 9]. These findings support classic models of cultural evolution [10, 11], which predict that many-to-one or one-to-many transmission erodes within-group variance in culturally inherited traits. However, classic theory [10, 11] also predicts that within-group heterogeneity is preserved when offspring each learn from an exclusive role model. We tested this prediction in a wild mammal, the banded mongoose (Mungos mungo), in which offspring are reared by specific adult carers that are not their parents, providing an opportunity to disentangle genetic and cultural inheritance of behavior. We show using stable isotope analysis that young mongooses inherit their adult foraging niche from cultural role models, not from their genetic parents. As predicted by theory, one-to-one cultural transmission prevented blending inheritance and allowed the stable coexistence of distinct behavioral traditions within the same social groups. Our results confirm that cultural inheritance via role models can promote rather than erode behavioral heterogeneity in natural populations.

Motivation before meaning: motivational information encoded in meerkat alarm calls develops earlier than referential information.

In contrast to historical assumptions about the affective nature of animal vocalizations, it is now clear that many vertebrates are capable of producing specific alarm calls in response to different predators, calls that provide information that goes beyond the motivational state of a caller. However, although these calls function referentially, it does not mean that they are devoid of motivational content. Studies on meerkats (Suricata suricatta) directly support this conclusion. The acoustic structure of their alarm calls simultaneously encodes information that is both motivational (level of urgency) and referential (predator specific). In this study, we investigated whether alarm calls of young meerkats undergo developmental modification and whether the motivational or the referential aspect of calls changes more over time. We found that, based on their acoustic structure, calls of young showed a high correct assignment to low- and high-urgency contexts but, in contrast to adults, low assignment to specific predator types. However, the discrimination among predator types was better in high-urgency than in low-urgency contexts. Our results suggest that acoustic features related to level of urgency are expressed earlier than those related to predator-specific information and may support the idea that referential calls evolve from motivational signals.

Reduced social-information provision by immigrants and use by residents following dispersal.

Greater access to social information is a proposed benefit of group living [1]. However, individuals vary in the quantity and quality of information they provide [2], and prior knowledge about signaller reliability is likely important when receivers decide how to respond [3]. While dispersal causes regular changes in group membership [4], no experimental work has investigated social-information provision and use in this context. We studied sentinel behaviour following immigration in a habituated population of wild dwarf mongooses (Helogale parvula) [5]; sentinels (raised guards) use various vocalisations to provide social information [5,6]. Recent immigrants acted as sentinels rarely and significantly less often than residents, limiting their role as social-information providers. Even when recent immigrants acted as social-information providers, foragers responded to them less than they did to residents. Several months after arrival, immigrants had increased sentinel contributions, and foragers no longer responded differently to sentinel activity by former immigrants and residents. Our results raise questions about the assumed social-information benefits associated with increased group size.

Discrete call types referring to predation risk enhance the efficiency of the meerkat sentinel system.

Sentinel behaviour, a form of coordinated vigilance, occurs in a limited range of species, mostly in cooperative breeders. In some species sentinels confirm their presence vocally by giving a single sentinel call type, whereby the rate and subtle acoustic changes provide graded information on the variation of perceived predation risk. In contrast, meerkat (Suricata suricatta) sentinels produce six different sentinel call types. Here we show that manipulation of perception of danger has different effects on the likelihood of emitting these different call types, and that these call types affect foraging individuals differently. Increasing the perceived predation risk by playing back alarm calls decreased the production rate of the common short note calls and increased the production rate of the rare long calls. Playbacks of short note calls increased foraging behaviour and decreased vigilance in the rest of the group, whereas the opposite was observed when playing long calls. This suggests that the common call types act as all-clear signals, while the rare call types have a warning function. Therefore, meerkats increase the efficiency of their sentinel system by producing several discrete call types that represent changes in predation risk and lead to adjustments of the group's vigilance behaviour.

The causes of physiological suppression among female meerkats: a role for subordinate restraint due to the threat of infanticide?

In many animal societies, subordinates exhibit down-regulated reproductive endocrine axes relative to those of dominants, but whether this 'physiological suppression' arises from active interference by dominants or subordinate self-restraint is a matter of debate. Here we investigate the roles that these processes play in precipitating physiological suppression among subordinate female meerkats, Suricata suricatta. We show that, while subordinate females are known to suffer stress-related physiological suppression during periodic temporary evictions by the dominant female, their low estrogen levels while within their groups cannot be readily attributed to chronic stress, as their fecal glucocorticoid metabolite levels during this time are comparable to those of dominants. The low estrogen levels of subordinate females also cannot be explained simply by self-restraint due to factors that could reduce their payoff from maintaining their fertility regardless of the presence of the dominant female (young age, a lack of unrelated mates, poor body condition and limited breeding experience), as substantial rank-related differences in fecal total-estrogen metabolite levels remain when such factors are controlled. We suggest that this residual difference in estrogen levels may reflect a degree of subordinate restraint due in part to the dominant female's ability to kill their young. Accordingly, subordinate female estrogen levels vary in association with temporal variation in the likelihood of infanticide by the dominant. Attempts to identify the causes of physiological suppression should be cautious if rejecting any role for dominant interference in favor of subordinate restraint, as the dominant's capacity to interfere may often be the reason why subordinates exercise restraint.

Teaching in wild meerkats.

Despite the obvious benefits of directed mechanisms that facilitate the efficient transfer of skills, there is little critical evidence for teaching in nonhuman animals. Using observational and experimental data, we show that wild meerkats (Suricata suricatta) teach pups prey-handling skills by providing them with opportunities to interact with live prey. In response to changing pup begging calls, helpers alter their prey-provisioning methods as pups grow older, thus accelerating learning without the use of complex cognition. The lack of evidence for teaching in species other than humans may reflect problems in producing unequivocal support for the occurrence of teaching, rather than the absence of teaching.

Cost minimization by helpers in cooperative vertebrates.

When parents invest heavily in reproduction they commonly suffer significant energetic costs. Parents reduce the long-term fitness implications of these costs through increased foraging and reduced reproductive investment in the future. Similar behavioral modifications might be expected among helpers in societies of cooperative vertebrates, in which helping is associated with energetic costs. By using multivariate analyses and experiments, we show that in cooperative meerkats, Suricata suricatta, helping is associated with substantial short-term growth costs but limited long-term fitness costs. This association forms because individual contributions to cooperation are initially condition dependent, and, because when helpers invest heavily in cooperation, they increase their foraging rate during the subsequent nonbreeding period and reduce their level of cooperative investment in the subsequent reproductive period. These results provide a unique demonstration that despite significant short-term costs, helpers, like breeders, are able to reduce the fitness consequences of these costs through behavioral modifications.