Group-living Species Research Articles

Sex differences in cooperative coalitions: a mammalian perspective.

In group-living species, cooperative tactics can offset asymmetries in resource-holding potential between individuals and alter the outcome of intragroup conflicts. Differences in the kinds of competitive pressures that males and females face might influence the benefits they gain from forming intragroup coalitions. We predicted that there would be a female bias in intragroup coalitions because females (1) are more like to live with kin than males are, and (2) compete over resources that are more readily shared than resources males compete over. We tested this main prediction using information about coalition formation across mammalian species and phylogenetic comparative analyses. We found that for nearly all species in which intragroup coalitions occur, members of both sexes participate, making this the typical mammalian pattern. The presence and frequency of female or male coalitions were not strongly associated with key socio-ecological factors like resource defensibility, sexual dimorphism or philopatry. This suggests that once the ability to form intragroup coalitions emerges in one sex, it is likely to emerge in the other sex as well and that there is no strong phylogenetic legacy of sex differences in this form of cooperation. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

The evolution of marsupial social organization.

It is generally believed that marsupials are more primitive than placentals mammals and mainly solitary living, representing the ancestral form of social organization of all mammals. However, field studies have observed pair and group-living in marsupial species, but no comparative study about their social evolution was ever done. Here, we describe the results of primary literature research on marsupial social organization which indicates that most species can live in pairs or groups and many show intra-specific variation in social organization. Using Bayesian phylogenetic mixed-effects models with a weak phylogenetic signal of 0.18, we found that solitary living was the most likely ancestral form (35% posterior probability), but had high uncertainty, and the combined probability of a partly sociable marsupial ancestor (65%) should not be overlooked. For Australian marsupials, group-living species were less likely to be found in tropical rainforest, and species with a variable social organization were associated with low and unpredictable precipitation representing deserts. Our results suggest that modern marsupials are more sociable than previously believed and that there is no strong support that their ancestral state was strictly solitary living, such that the assumption of a solitary ancestral state of all mammals may also need reconsideration.

The Yellow-breasted Barbet (Trachyphonus margaritatus) introduces vocal duets and choruses with a specific multimodal signal, during territorial advertisement

Cooperative behaviour is a prominent feature among many group-living species and continues to pose challenges to our understanding about the evolution of social relationships and task coordination between members of the same social group. Individuals who are willing to cooperate to achieve a joined action need to communicate their intentions and somehow make a common agreement. We investigated how a coordinated chorus song is initiated in a cooperative-breeding bird species, The Yellow-Breasted Barbet (Trachyphonus margaritatus). A chorus can be defined as an interactive vocal display involving several individuals who are synchronizing their behaviour to sing in a time coordinated manner. Synchronizing behaviour to sing in chorus might become quite challenging when several individuals are involved. Thus, group members could use a specific signal to induce such collective action. Yet, few studies have investigated the mechanisms of communal display initiation in chorusing bird species. We conducted playback experiments to induce and record territorial defensive reactions from birds with a video camera. We recorded 26 different groups from distinct wild populations in Djibouti which belonged to 17 sites. We found that barbets use a specific vocalization named chewp note to introduce their duet and chorus. Moreover, we found that the individual that initiates such communal displays may broadcast a multimodal signal by combining chewp note series with a typical body posture with the tail raised and fanned. We suggest that the multimodal signal could serve to attract attention and elicit a response from other group members or could enhance the song coordination.

Coevolution of social and communicative complexity in lemurs.

The endemic lemurs of Madagascar (Lemuriformes: Primates) exhibit great social and communicative diversity. Given their independent evolutionary history, lemurs provide an excellent opportunity to identify fundamental principles in the coevolution of social and communicative traits. We conducted comparative phylogenetic analyses to examine patterns of interspecific variation among measures of social complexity and repertoire sizes in the vocal, olfactory and visual modality, while controlling for environmental factors such as habitat and number of sympatric species. We also examined potential trade-offs in signal evolution as well as coevolution between body mass or brain size and communicative complexity. Repertoire sizes in the vocal, olfactory and visual modality correlated positively with group size, but not with environmental factors. Evolutionary changes in social complexity presumably antedated corresponding changes in communicative complexity. There was no trade-off in the evolution of signals in different modalities and neither body mass nor brain size correlated with any repertoire size. Hence, communicative complexity coevolved with social complexity across different modalities, possibly to service social relationships flexibly and effectively in pair- and group-living species. Our analyses shed light on the requirements and adaptive possibilities in the coevolution of core elements of social organization and social structure in a basal primate lineage. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Special Feature: Linking capture-recapture and movement.

Special Feature: Linking capture-recapture and movement.

Not just females: the socio-ecology of social interactions between spider monkey males.

Male-male relationships are mostly characterized by competition. However, males also cooperate with one another if socio-ecological conditions are suitable. Due to their male philopatry, the need for cooperation in home range defence and high degree of fission-fusion dynamics, spider monkeys provide an opportunity to investigate how male-male interactions are associated with socio-ecological factors, such as the presence of potentially receptive females, the degree of food availability and the likelihood of home range defence. We tested predictions about changes in social interactions between wild spider monkey males in relation to these factors. First, males did not change their interaction patterns when potentially receptive females were in the subgroup compared to when they were absent. Second, males tended to be less tolerant of one another when feeding, but spent more time grooming, in contact and proximity with one another when food availability was lower than when it was higher. Third, males exchanged fewer embraces, spent less time grooming, in proximity and in contact with one another, and spent more time vigilant at the home range boundary area than at other locations. Our findings contribute to the understanding of social flexibility and the importance of considering males in socio-ecological models of any group-living species.

Intraspecific variation in audience effects during outgroup conflict in a cooperatively breeding fish

Conspecific audiences have frequently been shown to affect behaviour during competitive interactions. However, research on audience effects has focused almost exclusively on how individual observers influence dyadic contests. Few studies have investigated more complex social scenarios, such as when groups defending a collective territory against outsiders can be monitored by neighbours. We used groups of the cooperatively breeding cichlid fish Neolamprologus pulcher to test experimentally how the presence of neighbours influences group and individual level defence behaviour towards a female intruder, as well as associated within-group interactions. In the presence of neighbours, groups performed more defensive acts and spent more time defending their territory, but the nature of the response to neighbour presence differed between group members. Dominant females attacked intruders more, while subordinate females produced aggressive displays of longer mean duration; dominant males also tended to increase mean display duration. Despite the significant audience effects on defence behaviour, neighbour presence did not lead to any discernible changes in within-group aggression, affiliation or submission during the intrusions. Our study expands the small current literature on audience effects in group-living species and thus contributes to a fuller understanding of within- and between-group social dynamics. • We assessed audience effects on collective defence and within-group interactions. • Groups increased their defensive efforts in the presence of neighbours. • The type of defensive behaviour that increased differed between group members. • Within-group behaviour during the intrusion was not affected by neighbour presence.

Expanding the frame around social dynamics and glucocorticoids: From hierarchies within the nest to competitive interactions among species

The effect of the social environment on individual state or condition has largely focused on glucocorticoid levels (GCs). As metabolic hormones whose production can be influenced by nutritional, physical, or psychosocial stressors, GCs are a valuable (though singular) measure that may reflect the degree of “stress” experienced by an individual. Most work to date has focused on how social rank influences GCs in group-living species or how predation risk influences GCs in prey. This work has been revealing, but a more comprehensive assessment of the social environment is needed to fully understand how different features of the social environment influence GCs in both group living and non-group living species and across life history stages. Just as there can be intense within-group competition among adult conspecifics, it bears appreciating there can also be competition among siblings from the same brood, among adult conspecifics that do not live in groups, or among heterospecifics. In these situations, dominance hierarchies typically emerge, albeit, do dominants or subordinate individuals or species have higher GCs? We examine the degree of support for hypotheses derived from group-living species about whether differential GCs between dominants and subordinates reflect the “stress of subordination” or “costs of dominance” in these other social contexts. By doing so, we aim to test the generality of these two hypotheses and propose new research directions to broaden the lens that focuses on social hierarchies and GCs.

Olfactory Strategies in the Defensive Behaviour of Insects.

Simple SummaryInsects have several methods to protect themselves and their resources from danger. One of them is to use their sense of smell. In this review, we describe how insects use smell to detect threats and perform behaviours of ‘flight or fight’ such as avoidance, escape or attack, in order to protect themselves. We also discuss how group-living insects share the information of danger through semiochemicals called alarm pheromones, to act as a collective. In the second section of this paper, we review how these odours are processed in insect brains. We discuss how the two kinds of neural architectures observed in olfactory areas, labelled-lines and across-fiber patterns, support the processing of alarm pheromones. Finally, we give an outlook on potential future studies that will help us understand this field better. Most animals must defend themselves in order to survive. Defensive behaviour includes detecting predators or intruders, avoiding them by staying low-key or escaping or deterring them away by means of aggressive behaviour, i.e., attacking them. Responses vary across insect species, ranging from individual responses to coordinated group attacks in group-living species. Among different modalities of sensory perception, insects predominantly use the sense of smell to detect predators, intruders, and other threats. Furthermore, social insects, such as honeybees and ants, communicate about danger by means of alarm pheromones. In this review, we focus on how olfaction is put to use by insects in defensive behaviour. We review the knowledge of how chemical signals such as the alarm pheromone are processed in the insect brain. We further discuss future studies for understanding defensive behaviour and the role of olfaction.

Intergroup conflict: origins, dynamics and consequences across taxa.

Although uniquely destructive and wasteful, intergroup conflict and warfare are not confined to humans. They are seen across a range of group-living species, from social insects, fishes and birds to mammals, including nonhuman primates. With its unique collection of theory, research and review contributions from biology, anthropology and economics, this theme issue provides novel insights into intergroup conflict across taxa. Here, we introduce and organize this theme issue on the origins and consequences of intergroup conflict. We provide a coherent framework by modelling intergroup conflicts as multi-level games of strategy in which individuals within groups cooperate to compete with (individuals in) other groups for scarce resources, such as territory, food, mating opportunities, power and influence. Within this framework, we identify cross-species mechanisms and consequences of (participating in) intergroup conflict. We conclude by highlighting crosscutting innovations in the study of intergroup conflict set forth by individual contributions. These include, among others, insights on how within-group heterogeneities and leadership relate to group conflict, how intergroup conflict shapes social organization and how climate change and environmental degradation transition intergroup relations from peaceful coexistence to violent conflict.This article is part of the theme issue ‘Intergroup conflict across taxa’.

Sex, not social behavior, predicts fecal glucocorticoid metabolite concentrations in a facultatively social rodent, the highland tuco-tuco (Ctenomys opimus)

Social relationships may influence circulating glucocorticoid levels, particularly in group-living species in which individuals regularly engage in interactions with conspecifics. The effects of such interactions appear to vary, with greater social contact being associated with increased glucocorticoid concentrations in some species but decreased concentrations in others. These distinct responses raise intriguing questions regarding relationships among social behavior, individual phenotypes, and glucocorticoid physiology. To explore such relationships in a free-living mammal with a dynamic social organization, we quantified variation in baseline glucocorticoids in a population of highland tuco-tucos (Ctenomys opimus) from Jujuy Province, Argentina. These subterranean rodents are facultatively social, with lone and group-living individuals regularly occurring within the same population. To assess potential endocrine correlates of this behavioral variability, we examined differences in baseline fecal glucocorticoid metabolite (fGCm) concentrations as a function of social group size and composition as well as several metrics of social behavior derived from social network analyses. Despite marked variability in social relationships among the 37 (12 male, 25 female) free-living tuco-tucos sampled, none of the measures of social behavior examined were significant predictors of variation in fGCm concentrations. In contrast, individual variation in glucocorticoid metabolites was best explained by sex, with males having higher fGCm concentrations than females. These analyses provide the first characterization of the glucocorticoid physiology of highland tuco-tucos and underscore the potential importance of intrinsic phenotypic factors (e.g., sex) in shaping glucocorticoid variation in free-living mammals.

Do immigrant female bonobos prefer older resident females as important partners when integrating into a new group?

Intergroup transfer is a critical part of the life history of group-living species, with considerable variation in its timings and patterns among species. Immigrant female bonobos are documented to smoothly integrate into a new group through forming affiliative relationships with old, high-ranking resident females (Idani, Folia Primatol 57:83-95, 1991). However, only a few studies are available on immigration costs and strategies for female bonobos. Here, we compared social relationships of natal females (known to be 4.5-7.2years old) and immigrant females (estimated to be 6.8-12.3years old) from one bonobo group at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo. Similar to previous studies, resident females did not appear to spatially isolate immigrant females or act aggressively toward them. However, resident males were more frequently aggressive toward immigrant females than toward natal females. Both natal and immigrant females tended to groom high-ranking females more than middle- and low-ranking females, although immigrant females spent more time grooming unrelated females than natal females. Immigrant females did not exhibit rank-related partner preference for genito-genital rubbing and copulation. Although we did not control for age differences because of the small sample size, our results provide partial support for the hypothesis that old female bonobos are important partners for the successful integration of young females into an unfamiliar group. This strategy could explain why female bonobos disperse before reaching sexual maturity, which contrasts with the need for female chimpanzees to display sexual swellings and draw male interest as protection against aggression from resident females.

Simulated poaching affects global connectivity and efficiency in social networks of African savanna elephants-An exemplar of how human disturbance impacts group-living species.

Selective harvest, such as poaching, impacts group-living animals directly through mortality of individuals with desirable traits, and indirectly by altering the structure of their social networks. Understanding the relationship between disturbance-induced, structural network changes and group performance in wild animals remains an outstanding problem. To address this problem, we evaluated the immediate effect of disturbance on group sociality in African savanna elephants-an example, group-living species threatened by poaching. Drawing on static association data from ten free-ranging groups, we constructed one empirically based, population-wide network and 100 virtual networks; performed a series of experiments 'poaching' the oldest, socially central or random individuals; and quantified the immediate change in the theoretical indices of network connectivity and efficiency of social diffusion. Although the social networks never broke down, targeted elimination of the socially central conspecifics, regardless of age, decreased network connectivity and efficiency. These findings hint at the need to further study resilience by modeling network reorganization and interaction-mediated socioecological learning, empirical data permitting. The main contribution of our work is in quantifying connectivity together with global efficiency in multiple social networks that feature the sociodemographic diversity likely found in wild elephant populations. The basic design of our simulation makes it adaptable for hypothesis testing about the consequences of anthropogenic disturbance or lethal management on social interactions in a variety of group-living species with limited, real-world data.

A spatial capture-recapture model for group-living species.

Group living in species can have complex consequences for individuals, populations, and ecosystems. Therefore, estimating group density and size is often essential for understanding population dynamics, interspecific interactions, and conservation needs of group-living species. Spatial capture-recapture (SCR) has been used to model both individual and group density in group-living species, but modeling either individual-level or group-level detection results in different biases due to common characteristics of group-living species, such as highly cohesive movement or variation in group size. Furthermore, no SCR method currently estimates group density, individual density, and group size jointly. Using clustered point processes, we developed a cluster SCR model to estimate group density, individual density, and group size. We compared the model to standard SCR models using both a simulation study and a data set of detections of African wild dogs (Lycaon pictus), a group-living carnivore, on camera traps in northern Botswana. We then tested the model's performance under various scenarios of group movement in a separate simulation study. We found that the cluster SCR model outperformed a standard group-level SCR model when fitted to data generated with varying group sizes, and mostly recovered previous estimates of wild dog group density, individual density, and group size. We also found that the cluster SCR model performs better as individuals' movements become more correlated with their groups' movements. The cluster SCR model offers opportunities to investigate ecological hypotheses relating group size to population dynamics while accounting for cohesive movement behaviors in group-living species.

Cooperative Behaviors in Group-Living Spider Mites

Cooperative behaviors are evolutionary stable if the direct and/or indirect fitness benefits exceed the costs of helping. Here we discuss cooperation and behaviors akin to cooperation in subsocial group-living species of two genera of herbivorous spider mites (Tetranychidae), i.e., the largely polyphagous Tetranychus spp. and the nest-building Stigmaeopsis spp., which are specialized on grasses, such as bamboo. These spider mites are distributed in patches on various spatial scales, that is, within and among leaves of individual host plants and among individual hosts of single or multiple plant species. Group-living of spider mites is brought about by plant-colonizing foundresses ovipositing at local feeding sites and natal site fidelity, and by multiple individuals aggregating in the same site in response to direct and/or indirect cues, many of which are associated with webbing. In the case of the former, emerging patches are often composed of genetically closely related individuals, while in the case of the latter, local patches may consist of kin of various degrees and/or non-kin and even heterospecific spider mites. We describe and discuss ultimate and proximate aspects of cooperation by spider mites in host plant colonization and exploitation, dispersal, anti-predator behavior, and nesting-associated behaviors and conclude with theoretical and practical considerations of future research on cooperation in these highly rewarding model animals.

Association networks and social temporal dynamics in ewes and lambs

Sheep are highly social domesticated animals that evolved to live in large and structured groups. As in other group-living species, individuals differ in the level of association they have with others, and these associations often result in lasting and stable social bonds. However, there are substantial gaps in our knowledge of the temporal social dynamics in sheep, and how their social bonds vary in relation to environmental changes. Here, we aimed to assess the social relationships between ewes and lambs, collecting dyadic associations data of 41 ewes and 55 lambs through the use of proximity loggers on a commercial farm. We computed association indices between each pair of animals to estimate the proportion of time any two individuals associated. We first generated an aggregated network of the whole 13-day observation period, and we compared the values of association indices between different types of dyads (i.e., lamb-mother, lamb-ewe non-mother, lambs littermates, lambs non-littermates, ewe-ewe). We generated aggregated contact networks on a daily scale to compare the ego-networks of individuals obtained in successive time windows to determine how stable social associations were over time. As would be expected, the highest values of association indices were found in dyads formed by dams and lambs (0.17 ± 0.11) and by lambs of the same litter (0.32 ± 0.09). Both single-born and twin-born lambs showed high association values with their dams (single-born: 0.24 ± 0.11; twin-born: 0.1 ± 0.05), although twin-born lambs had stronger associations with their littermates compared with those with their mothers (p-value < 0.001). At a temporal level, the flock exhibited periods of high network stability at the beginning and at the end of the study period. However, periods of social instability occurred one-two days after management interventions, such as changes in field size. These transitory periods of social instability were driven by changes in the association patterns of ewes and single born lambs. In contrast, the ego-networks of twin-born lambs remained relatively stable, supported by strong association levels between twins. Thus, the social instability of the social network was not a global one, but some parts of the network remained stable while others underwent important changes. Our study represents a first step to track social associations within an ewe-lamb group using proximity tags and advances our understanding of the social organisation of sheep. We highlight the importance of detecting social network instability as a consequence of different types of perturbations in order to identify the presence of social rearrangements.

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.

Economies of scale shape energetics of solitary and group-living spiders and their webs.

Metabolic scaling, whereby larger individuals use less energy per unit mass than smaller ones, may apply to the combined metabolic rate of group-living organisms as group size increases. Spiders that form groups in high disturbance environments can serve to test the hypothesis that economies of scale benefit social groups. Using solitary and group-living spiders, we tested the hypothesis that spiders exhibit negative allometry between body or colony mass and the standing mass of their webs and whether, and how, such a relationship may contribute to group-living benefits in a cooperative spider. Given the diverse architecture of spider webs-orb, tangle and sheet-and-tangle, and associated differences in silk content, we first assessed how standing web mass scales with spider mass as a function of web architecture and whether investment in silk differs among web types. As group-living spiders are predominantly found in clades that build the presumably costlier sheet-and-tangle webs, we then asked whether cost-sharing through cooperative web maintenance contributes to a positive energy budget in a social species. We found that larger spiders had a relatively smaller investment in silk per unit mass than smaller ones, but more complex sheet-and-tangle webs contained orders of magnitude more silk than simpler orb or tangle ones. In the group-living species, standing web mass per unit spider mass continued to decline as colony size increased with a similar slope as for unitary spiders. When web maintenance activities were considered, colonies also experienced reduced mass-specific energy expenditure with increasing colony size. Activity savings contributed to a net positive energy balance for medium and large colonies after inputs from the cooperative capture of large prey were accounted for. Economies of scale have been previously demonstrated in animal societies characterized by reproductive and worker castes, but not in relatively egalitarian societies as those of social spiders. Our findings illustrate the universality of scaling laws and how economies of scale may transcend hunting strategies and levels of organization.

Vocal repertoire, micro-geographical variation and within-species acoustic partitioning in a highly colonial pinniped, the Cape fur seal.

Communication is fundamental for the survival of animal species as signals are involved in many social interactions (mate selection, parental care, collective behaviours). The acoustic channel is an important modality used by birds and mammals to reliably exchange information among individuals. In group-living species, the propagation of vocal signals is limited due to the density of individuals and the background noise. Vocal exchanges are, therefore, challenging. This study is the first investigation into the acoustic communication system of the Cape fur seal (CFS), one of the most colonial mammals with breeding colonies of hundreds of thousands of individuals. We described the acoustic features and social function of five in-air call types from data collected at two colonies. Intra-species variations in these vocalizations highlight a potential ability to convey information about the age and/or sex of the emitter. Using two classification methods, we found that the five call types have distinguishable frequency features and occupy distinct acoustic niches indicating acoustic partitioning in the repertoire. The CFS vocalizations appear to contain characteristics advantageous for discrimination among individuals, which could enhance social interactions in their noisy and confusing acoustic environment. This study provides a basis for our understanding of the CFS acoustic communication system.

Location probing by males complicates sexual dynamics and successful mate‐guarding in squid groups

Reproductive fitness is defined by the successful passing of an individual's genes to the next generation. Cephalopods that mate in groups, in particular coastal squid and cuttlefish species, have evolved complex sexual tactics in order to maximize reproductive success (Morse and Huffard 2019). Through dynamic skin patterning accompanied by typical body postures, individuals send visual signals in the form of displays to potential mates and rival competitors, often engaging in escalating conflicts (Moynihan and Rodaniche 1982, Mather 2016).