The fermentation hypothesis for animal signalling posits that bacteria dwelling in an animal’s scent glands metabolize the glands' primary products into odorous compounds used by the host to communicate with conspecifics. There is, however, little evidence of the predicted covariation between an animal’s olfactory cues and its glandular bacterial communities. Using gas chromatography-mass spectrometry, we first identified the volatile compounds present in ‘pure’ versus ‘mixed’ anal-gland secretions (‘paste’) of adult meerkats (Suricata suricatta) living in the wild. Low-molecular-weight chemicals that likely derive from bacterial metabolism were more prominent in mixed than pure secretions. Focusing thereafter on mixed secretions, we showed that chemical composition varied by sex and was more similar between members of the same group than between members of different groups. Subsequently, using next-generation sequencing, we identified the bacterial assemblages present in meerkat paste and documented relationships between these assemblages and the host’s sex, social status and group membership. Lastly, we found significant covariation between the volatile compounds and bacterial assemblages in meerkat paste, particularly in males. Together, these results are consistent with a role for bacteria in the production of sex- and group-specific scents, and with the evolution of mutualism between meerkats and their glandular microbiota.
In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight and slow-growing animals may lose their place in breeding queues to younger ‘challengers’ that grow faster. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish and mammals, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.
In many animal societies, a small proportion of dominant females monopolize reproduction by actively suppressing subordinates. Theory assumes that this is because subordinate reproduction depresses the fitness of dominants, yet the effect of subordinate reproduction on dominant behaviour and reproductive success has never been directly assessed. Here, we describe the consequences of experimentally preventing subordinate breeding in 12 groups of wild meerkats (Suricata suricatta) for three breeding attempts, using contraceptive injections. When subordinates are prevented from breeding, dominants are less aggressive towards subordinates and evict them less often, leading to a higher ratio of helpers to dependent pups, and increased provisioning of the dominant’s pups by subordinate females. When subordinate breeding is suppressed, dominants also show improved foraging efficiency, gain more weight during pregnancy and produce heavier pups, which grow faster. These results confirm the benefits of suppression to dominants, and help explain the evolution of singular breeding in vertebrate societies.
Risk-sensitive adaptive spatial organisation during group movement has been shown to efficiently minimise the risks associated with external ecological threats. Whether animals can draw on such behaviours when confronted with man-made threats is generally less clear. We studied road-crossing in a wild, but habituated, population of meerkats living in the Kalahari Desert, South Africa. We found that dominant females, the core member in meerkat social systems, led groups to the road significantly more often than subordinates, yet were consistently less likely to cross first. Our results suggest that a reshuffling occurs in progression order when meerkat groups reach the road. By employing a simple model of collective movement, we have shown that risk aversion alone may be sufficient to explain this reshuffling, but that the risk aversion of dominant females toward road crossing is significantly higher than that of subordinates. It seems that by not crossing first, dominant females avoid occupying the most risky, exposed locations, such as at the front of the group - a potential selfish strategy that also promotes the long-term stability and hence reproductive output of their family groups. We argue that our findings support the idea that animals can flexibly apply phylogenetically-old behavioural strategies to deal with emerging modern-day problems.
It is well established that animal vocalizations can encode information regarding a sender’s identity, sex, age, body size, social rank and group membership. However, the association between physiological parameters, particularly stress hormone levels, and vocal behavior is still not well understood. The cooperatively breeding African meerkats (Suricata suricatta) live in family groups with despotic social hierarchies. During foraging, individuals emit close calls that help maintain group cohesion. These contact calls are acoustically distinctive and variable in rate across individuals, yet, information on which factors influence close calling behavior is missing. The aim of this study was to identify proximate factors that influence variation in call rate and acoustic structure of meerkat close calls. Specifically, we investigated whether close calling behavior is associated with sex, age and rank, or stress hormone output (i.e., measured as fecal glucocorticoid metabolite (fGCM) concentrations) as individual traits of the caller, as well as with environmental conditions (weather) and reproductive seasonality. To disentangle the effects of these factors on vocal behavior, we analyzed sound recordings and assessed fGCM concentrations in 64 wild but habituated meerkats from 9 groups during the reproductive and non-reproductive seasons. Dominant females and one-year old males called at significantly higher rates compared to other social categories during the reproductive season. Additionally, dominant females produced close calls with the lowest mean fundamental frequencies (F0) and the longest mean pulse durations. Windy conditions were associated with significantly higher call rates during the non-reproductive season. Fecal GCM concentrations were unrelated to close calling behavior. Our findings suggest that meerkat close calling behavior conveys information regarding the sex and social category of the caller, but shows no association with fGCM concentrations. The change in call rate in response to variation in the social and ecological environments individuals experience indicates some degree of flexibility in vocal production.
1.Dispersal is a key process governing the dynamics of socially and spatially structured populations, and involves three distinct stages: emigration, transience, and settlement. At each stage, individuals have to make movement decisions, which are influenced by social, environmental, and individual factors. Yet, a comprehensive understanding of the drivers that influence such decisions is still lacking, particularly for the transient stage during which free-living individuals are inherently difficult to follow. 2.Social circumstances such as the likelihood of encountering conspecifics can be expected to strongly affects decision making during dispersal, particularly in territorial species where encounters with resident conspecifics are antagonistic. Here we analyzed the movement trajectories of 47 dispersing coalitions of Kalahari meerkats (Suricata suricatta) through a landscape occupied by constantly monitored resident groups, while simultaneously taking into account environmental and individual characteristics. 3.We used GPS locations collected on resident groups to create a geo-referenced social landscape representing the likelihood of encountering resident groups. We used a step-selection function to infer the effect of social, environmental and individual covariates on habitat selection during dispersal. Lastly, we created a temporal mismatch between the social landscape and the dispersal event of interest to identify the temporal scale at which dispersers perceive the social landscape. 4.Including information about the social landscape considerably improved our representation of the dispersal trajectory, compared to analyses that only accounted for environmental variables. The latter were only marginally selected or avoided by dispersers. Before leaving their natal territory, dispersers selected areas frequently used by their natal group. In contrast, after leaving their natal territory, they selectively used areas where they were less likely to encounter unrelated groups. This pattern was particularly marked in larger dispersing coalitions and when unrelated males were part of the dispersing coalition. 5.Our results suggest that, in socially and spatially structured species, dispersers gather and process social information during dispersal, and that reducing risk of aggression from unrelated resident groups outweighs benefits derived from conspecific attraction. Finally, our work underlines the intimate link between the social structure of a population and dispersal, which affect each other reciprocally. This article is protected by copyright. All rights reserved.
In group-living mammals, the eviction of subordinate females from breeding groups by dominants may serve to reduce feeding competition or to reduce breeding competition. Here, we combined both correlational and experimental approaches to investigate whether increases in food intake by dominant females reduces their tendency to evict subordinate females in wild meerkats (Suricata suricatta). We used 20 years of long-term data to examine the association between foraging success and eviction rate, and provisioned dominant females during the second half of their pregnancy, when they most commonly evict subordinates. We show that rather than reducing the tendency for dominants to evict subordinates, foraging success of dominant females is positively associated with the probability that pregnant dominant females will evict subordinate females and that experimental feeding increased their rates of eviction. Our results suggest that it is unlikely that the eviction of subordinate females serves to reduce feeding competition and that its principal function may be to reduce reproductive competition. The increase in eviction rates following experimental feeding also suggests that rather than feeding competition, energetic constraints may normally constrain eviction rates.
Vigorous debates as to the evolutionary origins of culture remain unresolved due to an absence of methods for identifying learning mechanisms in natural populations. While laboratory experiments on captive animals have revealed evidence for a number of mechanisms, these may not necessarily reflect the processes typically operating in nature. We developed a novel method that allows social and asocial learning mechanisms to be determined in animal groups from the patterns of interaction with, and solving of, a task. We deployed it to analyse learning in groups of wild meerkats (Suricata suricatta) presented with a novel foraging apparatus. We identify nine separate learning processes underlying the meerkats' foraging behaviour, in each case precisely quantifying their strength and duration, including local enhancement, emulation, and a hitherto unrecognized form of social learning, which we term ‘observational perseverance’. Our analysis suggests a key factor underlying the stability of behavioural traditions is a high ratio of specific to generalized social learning effects. The approach has widespread potential as an ecologically valid tool to investigate learning mechanisms in natural groups of animals, including humans.
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.
Group coordination, when ‘on the move’ or when visibility is low, is a challenge faced by many social living animals. While some animals manage to maintain cohesion solely through visual contact, the mechanism of group cohesion through other modes of communication, a necessity when visual contact is reduced, is not yet understood. Meerkats (Suricata suricatta), a small, social carnivore, forage as a cohesive group while moving continuously. While foraging, they frequently emit ‘close calls’, soft close-range contact calls. Variations in their call rates based on their local environment, coupled with individual movement, produce a dynamic acoustic landscape with a moving ‘vocal hotspot’ of the highest calling activity. We investigated whether meerkats follow such a vocal hotspot by playing back close calls of multiple individuals to foraging meerkats from the front and back edge of the group simultaneously. These two artificially induced vocal hotspots caused the group to spatially elongate and split into two subgroups. We conclude that meerkats use the emergent dynamic call pattern of the group to adjust their movement direction and maintain cohesion. Our study describes a highly flexible mechanism for the maintenance of group cohesion through vocal communication, for mobile species in habitats with low visibility and where movement decisions need to be adjusted continuously to changing environmental conditions.