Fission-fusion Societies Research Articles

Resource seasonality and reproduction predict fission-fusion dynamics in black-and-white ruffed lemurs (Varecia variegata).

Ruffed lemurs (genus Varecia) are often described as having a flexible social organization, such that both cohesive (low fission-fusion dynamics) and fluid (high fission-fusion dynamics) grouping patterns have been observed. In ruffed lemur communities with high fission-fusion dynamics, group members vary in their temporal and spatial dispersion throughout a communally defended territory. These patterns have been likened to those observed in several haplorrhine species that exhibit the most fluid types of fission-fusion social organization (e.g., Pan and Ateles). To substantiate and further refine these claims, we describe the fission-fusion dynamics of a black-and-white ruffed lemur (Varecia variegata) community at Mangevo, an undisturbed primary rainforest site in Ranomafana National Park, Madagascar. We collected instantaneous group scan samples from August 2007-December 2008 (4,044 observation hours) to study and characterize patterns of subgroup size, composition, cohesion, and social association. In 16 consecutive months, we never found all members of the community together. In fact, individuals spent nearly half of their time alone. Subgroups were small, cohesive, and typically of mixed-sex composition. Mixed-sex subgroups were significantly larger, less cohesive, and more common than either male-only or female-only subgroups. Subgroup dynamics were related to shifts in climate, phenology of preferred fruit species, and female reproductive state. On average, association indices were low. Males and females were equally gregarious; however, adult male-male associations were significantly weaker than any other association type. Results presented herein document striking differences in fission-fusion dynamics between black-and-white ruffed lemurs and haplorrhines, while also demonstrating many broad-scale similarities to haplorrhine taxa that possess the most fluid fission-fusion societies.

Dyadic associations and individual sociality in bighorn ewes

Sociality presumably evolved because it leads to fitness benefits; yet we know little about what drives individual variability in sociality, particularly with respect to hierarchical levels of social organization. Social network architecture is based upon dyadic interactions, but the factors affecting pairwise relationships are not necessarily those affecting higher-level network-derived measures of social behavior. We examined the influence of relatedness, age, dominance, and reproductive status on proximal associations and social network centrality of individuals in the fission–fusion society of bighorn ewes (Ovis canadensis) at Ram Mountain, Canada. From 2011 to 2013, 63–81% of adult ewes were equipped with proximity loggers, recording when they were within 1.5 m of one another. Ewe social structure was not random and individuals exhibited a tendency to have proximal associations that were consistent across years. Age and reproductive status appeared to have a weak effect on network centrality, but this effect was largely absent for frequency of proximal association. Furthermore, we found no effect of dominance rank on either proximal associations or network centrality. We speculate that interannual variation in these relationships may be indicative of predation affecting social dynamics. The disconnect between determinants that affect the costs and benefits of dyadic associations and those that emerge from network-derived behaviors highlights the importance of testing effects at multiple levels of social organization in animal societies.

Similar but Different: Dynamic Social Network Analysis Highlights Fundamental Differences between the Fission-Fusion Societies of Two Equid Species, the Onager and Grevy's Zebra.

Understanding why animal societies take on the form that they do has benefited from insights gained by applying social network analysis to patterns of individual associations. Such analyses typically aggregate data over long time periods even though most selective forces that shape sociality have strong temporal elements. By explicitly incorporating the temporal signal in social interaction data we re-examine the network dynamics of the social systems of the evolutionarily closely-related Grevy’s zebras and wild asses that show broadly similar social organizations. By identifying dynamic communities, previously hidden differences emerge: Grevy’s zebras show more modularity than wild asses and in wild asses most communities consist of solitary individuals; and in Grevy’s zebras, lactating females show a greater propensity to switch communities than non-lactating females and males. Both patterns were missed by static network analyses and in general, adding a temporal dimension provides insights into differences associated with the size and persistence of communities as well as the frequency and synchrony of their formation. Dynamic network analysis provides insights into the functional significance of these social differences and highlights the way dynamic community analysis can be applied to other species.

Extreme vocal plasticity in adult budgerigars: Analytical challenges, social significance, and underlying neurogenetic mechanisms

Vocal learning is a complex trait that is expressed differently across different taxa. While many of the best-studied species exhibit close-ended learning, in which vocal signals are learned from adult tutors during juvenile critical learning periods, other species have open-ended learning in which new signals are learned throughout life. Budgerigars (Melopsittacus undulatus) are an extreme example of an open-ended learner, in which both sexes have a repertoire of multiple contact calls types that continually change through adulthood to match the call types of social associates. We discuss the analytical challenges posed by the rapid plasticity of the budgerigar vocal repertoire and compare results from several different approaches to characterizing call variation. We then consider the social implications and benefits of contact call matching in fission–fusion groups. Finally, we examine the mechanisms underlying this plasticity, with a special focus on the role of the gene FoxP2. We find downregulation of FoxP2 mRNA and protein in the primary parrot vocal learning center, MMSt, across a variety of social conditions in which birds also show vocal plasticity. The results support the hypothesis that FoxP2 is a key gene regulating the neural plasticity that underlies the persistent vocal plasticity exhibited by budgerigars.

Preliminary evidence for signature and copied whistles among spinner dolphins in the Southwest Atlantic Ocean: Beacon purpose?

In order to evaluate strategies of cohesion in a fission-fusion society, the occurrence of signature and copied whistles were investigated in free-ranging spinner dolphins, Stenella longirostris. Through an one-element hydrophone array towed over the Brazilian continental shelf break, a group of approximate 400 dolphins were recorded at 96 kHz/24 bits while navigating. The preliminary results demonstrated 218 similar signals that fit into previous definitions of signature or copied whistles. These whistles were produced in bouts with an inter-whistle interval of 0.066—11.56 s (mean ± SD: 2.66 ± 2.72) that varied from 2 to 32 repetitions comprising six different contour shapes. Thus, these data support previous hypothesis that these signals are important units in the dolphin’s repertoire. It may also suggests a potential use on individual direction and localization, where repeated contours could be acting as a beacon to direct and locate the animals within the group. Additional research to ascertain the natural function of these vocalizations may clarify the basis for acoustic badges of membership and group organization of this cosmopolitan species.

Measuring variation in the frequency of group fission and fusion from continuous monitoring of group sizes

The frequency of group fission and fusion is critical for understanding the evolution of sociality, as it measures group cohesiveness, which can confer a high fitness value on individuals who practice it. Variations in the frequency of fission and fusion can also reveal an individual's response to environmental changes. As fission—fusion group dynamics influence the risk of disease transmission, measuring it accurately may have implications for population management. Here, we extend a method to assess the frequency of fission and fusion from continuous monitoring of group composition. The former method was based on the variation in group size (i.e., party/subgroup size) within which marked individuals were successively recorded. Upon validation of the method here, we propose a correction, using the coefficient of variation in group size instead of the variation in group size. We performed our study on an enclosed herd of reindeer, Rangifer tarandus. All reindeer were tracked using Global Positioning Syste...

Collective movements, leadership and consensus costs at reunions in spotted hyaenas

Because collective movements have fitness consequences for all participants, group travel can impose conflicts of interest when group-mates vary. Challenges associated with coordinating activities of group-mates, such as during travel, may potentially be mitigated through the use of simple rules governing leadership and other behaviours to minimize conflict. Although individuals living in groups with fission–fusion dynamics may temporarily separate, leadership determination at subsequent reunions, and events occurring during reunions, are poorly understood. Here we investigate leadership during travel prior to reunions of spotted hyaenas, Crocuta crocuta , living in one large social group in the Masai Mara National Reserve, Kenya. Whereas individuals often arrived at dens or joined hunting parties alone, those joining others to participate in group defence of shared resources typically did so when accompanied by group-mates. Although most hyaenas led processions, the attributes of members within each travelling party consistently predicted leadership roles. The highest-ranking adult within each travelling subgroup, often a lactating female, typically assumed the vanguard position prior to reunions. Reunions promoted conflict, particularly at kills. However, as predicted by the conflict mitigation hypothesis, individuals that greeted conspecifics were significantly less likely to fight at reunions than were hyaenas that failed to greet at reunions. Thus, whereas temporary separations may reduce immediate conflicts of interest in fission–fusion societies, hyaenas pay consensus costs at subsequent reunions, particularly in the context of feeding competition, and greetings appear to reduce such costs. Finally, we propose a novel scheme for leadership categorization in which leadership depends on whether or not leadership is based on specific attributes of individual group members. We apply this attribute-based framework to quantify the patterns and mechanisms of leadership during group travel for 52 species of mammals, including the spotted hyaenas studied here, and place findings in a broad evolutionary context. • Individuals may separate to reduce group conflicts, but reunions are poorly understood. • We investigated leadership at reunions in fission–fusion societies of spotted hyaenas. • Leaders at reunions varied, but higher-ranking lactating females led most often. • Reunions promoted conflict, particularly at kills, and greetings mitigated these costs. • Our novel, attribute-based scheme characterizes patterns of leadership across mammals.

Mother-offspring distances reflect sex differences in fine-scale genetic structure of eastern grey kangaroos.

Natal dispersal affects life history and population biology and causes gene flow. In mammals, dispersal is usually male-biased so that females tend to be philopatric and surrounded by matrilineal kin, which may lead to preferential associations among female kin. Here we combine genetic analyses and behavioral observations to investigate spatial genetic structure and sex-biased dispersal patterns in a high-density population of mammals showing fission–fusion group dynamics. We studied eastern grey kangaroos (Macropus giganteus) over 2 years at Wilsons Promontory National Park, Australia, and found weak fine-scale genetic structure among adult females in both years but no structure among adult males. Immature male kangaroos moved away from their mothers at 18–25 months of age, while immature females remained near their mothers until older. A higher proportion of male (34%) than female (6%) subadults and young adults were observed to disperse, although median distances of detected dispersals were similar for both sexes. Adult females had overlapping ranges that were far wider than the maximum extent of spatial genetic structure found. Female kangaroos, although weakly philopatric, mostly encounter nonrelatives in fission–fusion groups at high density, and therefore kinship is unlikely to strongly affect sociality.

Rupture in long-term vocal recognition of past social partners in bonobos

Bonobos live in dense forest habitats where visual communication is often limited rendering vocal signals important to regulate their social interactions. Moreover their fluid fission-fusion society requires contact over long distances, suggesting that vocal signals of group members are recognised individually. To this end, individual signatures should be reliably encoded in vocal interactions and memorised by recipients over long periods. In this study we investigated individual vocal recognition of group members that had been separated for long periods of time (two to nine years) with varying relationships. In the wild, long-term separation happens regularly, usually in relation to female migration. In captivity, the same process takes place during the transfer of individuals between zoos, mimicking wild migration. We simulated bonobo transfers by broadcasting contact calls of familiar or unfamiliar individuals to our subjects, thus imitating the arrival of new group members. In total, we tested 15 bonobos (> 10 years old) from three European zoos and compared their behavioural responses. We found that bonobos responded differently to familiar voices than to stranger voices, even after prolonged separation. However, the recognition of past partners appears to diminish after being separated for 6-8 years. This interesting result will be discussed regarding to the social needs in bonobos.

Network analysis reveals cryptic seasonal patterns of association in Gould’s wattled bats (Chalinolobus gouldii) roosting in bat-boxes

Tree-roosting bats are highly social mammals, which often form fission–fusion societies. However, extensive, fine scale data is required to detect and interpret these patterns. We investigated the social structure of Gould’s wattled bats,Chalinolobus gouldii, roosting in artificial roosts (bat-boxes) over a continuous 18-month period. Network analyses revealed non-random associations among individuals in the roosting population consistent with a temperate zone fission–fusion social structure. Females generally showed stronger associations with roost-mates than did males. Two distinct sub-groups within the larger roosting population were detected. There was also evidence of smaller subunits within these larger roosting groups in spring and summer, with broader mixing at other times of the year. The extensive roost occupancy data collected across all seasons was critical in defining this fine scale, and otherwise cryptic, social structure, and in particular indicating that associations observed during peak activity periods may not be maintained across the year.

Within-group vocal differentiation of individuals in the cooperatively breeding apostlebird

The ability of animals to discriminate between individuals or groups of individuals (e.g., kin or nonkin) is an important component of many hypotheses proposed to explain the evolution of cooperation and benefits of group living. Previous studies in mammalian systems have demonstrated the use of vocal cues in individual recognition and discrimination. However, there are few such studies in birds. Previous avian studies have largely examined discrimination between different categories of individuals (e.g., mate vs. nonmate, offspring vs. non-offspring) while discrimination between individuals of the same category remain largely unexplored. Previous work has demonstrated that the contact calls of free-living apostlebirds (Struthidea cinerea) are individually distinct. Here, we demonstrate that apostlebirds can differentiate between the calls of other individuals of the same social group using vocal cues alone. These findings are biologically relevant as apostlebirds live in complex fission–fusion societies where social groups vary in size, sex ratio, number of breeders, and composition of related and unrelated members.

Roosting behavior and group decision making in 2 syntopic bat species with fission-fusion societies

In many social species, individuals make group decisions to coordinate their actions. Despite the importance of group decisions for successful group living, few studies investigated how wild animals make group decisions in situations where group members have conflicting interests. This lack of empirical data is most evident for animal groups that regularly split into subgroups for some time. In groups with high fission–fusion dynamics, individuals can avoid group decisions that are not in their interest without foregoing benefits from being social. Here, we compare group decision making about communal day roosts in 2 syntopic bat species with a similar ecology and life history but a different fission–fusion behavior of their colonies. Daily roost monitoring during 3 breeding seasons showed that Bechstein’s bats formed subgroups 5 times more often than brown long-eared bats although both species occupied a similar number of bat boxes per colony and year. Bechstein’s bats were also significantly faster in discovering newly installed boxes and explored them further away from their established roosting areas compared with brown long-eared bats. In a field experiment where we created a conflict of interests among colony members where to roost, brown long-eared bats always achieved a colony-wide consensus about communal roosts. On the contrary, in Bechstein’s bats, individuals with conflicting interests often formed subgroups in different roosts according to their individual interests instead of reaching a consensus on a single communal roost. Our findings show that even ecologically similar species can use different group decision-making rules for solving an identical coordination problem.

Unraveling fission-fusion dynamics: how subgroup properties and dyadic interactions influence individual decisions

Many species show fission-fusion group dynamics because it has clear advantages for flexibly exploiting heterogeneous environments. However, the mechanisms by which these dynamics arise are not well known. We used a hierarchical Bayesian model to disentangle the different influences on spider monkey (Ateles geoffroyi) individual fissions and fusions, including the three dimensions of fission-fusion dynamics (subgroup size, dispersion, and composition). Furthermore, we considered the influences of other individuals also leaving or joining a subgroup at the same time. We found that the most important influence on individual fissions and fusions is whether other individuals are also doing the same. Subgroup size and dispersion did not have clear effects on the probability that an individual fissioned or fusioned, while individuals tended to leave subgroups that were biased toward the opposite sex and to join subgroups that were biased toward their own sex. The networks constructed by the inter-individual influences during fissions and fusions were cohesive and did not show assortativity by sex or by degree. Individuals had a similar degree in both networks and each was influenced by a different set of individuals, suggesting a high fluidity in the social networks. We suggest that these networks reflect the way in which information about the environment flows as individuals follow one another during fissions and fusions.

Fission-fusion group dynamics in reindeer reveal an increase of cohesiveness at the beginning of the peak rut

Knowledge of the processes of group formation is important to understand the evolution of animal societies. Ungulates typically aggregate during the breeding season. According to the self-organization theory, proximal processes such as mating tactics should explain variation in average group size through their influences on group dynamics. Here, we tested whether variation of the fusion rate or fission rate led to an increase of average group size at the beginning of the peak rut. We followed the movement of marked animals within an enclosed herd of reindeer Rangifer tarandus during two breeding seasons (2009 and 2011). We used synchronized GPS collars that fixed the animals’ position every hour (2009) and every 15 min (2011). Group dynamics occurred in three steps as follows: (1) a continuous aggregation of groups, (2) a continuous departure of single females from these groups, and (3) the aggregation of these solitary females to form new groups. We attributed the increase in average group size mainly to a decrease in the number of groups due to a decrease in the group and individual splitting propensities, rather than to an increase of their merging propensities. A decrease in the splitting propensity at the beginning of the peak rut may be due to males herding females, female mate choice, or female harassment avoidance. Further research on fission-fusion group dynamics should calculate merging and splitting propensities by controlling for variables such as group size, group density, or habitat characteristics.

Highly competitive reindeer males control female behavior during the rut.

During the rut, female ungulates move among harems or territories, either to sample mates or to avoid harassment. Females may be herded by a male, may stay with a preferred male, or aggregate near a dominant male to avoid harassment from other males. In fission-fusion group dynamics, female movement is best described by the group’s fission probability, instead of inter-harem movement. In this study, we tested whether male herding ability, female mate choice or harassment avoidance influence fission probability. We recorded group dynamics in a herd of reindeer Rangifer tarandus equipped with GPS collars with activity sensors. We found no evidence that the harassment level in the group affected fission probability, or that females sought high rank (i.e. highly competitive and hence successful) males. However, the behavior of high ranked males decreased fission probability. Male herding activity was synchronous with the decrease of fission probability observed during the rut. We concluded that male herding behavior stabilized groups, thereby increasing average group size and consequently the opportunity for sexual selection.

Goats excel at learning and remembering a highly novel cognitive task

IntroductionThe computational demands of sociality (maintaining group cohesion, reducing conflict) and ecological problems (extractive foraging, memorizing resource locations) are the main drivers proposed to explain the evolution cognition. Different predictions follow, about whether animals would preferentially learn new tasks socially or not, but the prevalent view today is that intelligent species should excel at social learning. However, the predictions were originally used to explain primate cognition, and studies of species with relatively smaller brains are rare. By contrast, domestication has often led to a decrease in brain size, which could affect cognition. In domestic animals, the relaxed selection pressures compared to a wild environment could have led to reduced social and physical cognition. Goats possess several features commonly associated with advanced cognition, such as successful colonization of new environments and complex fission-fusion societies. Here, we assessed goat social and physical cognition as well as long-term memory of a complex two-step foraging task (food box cognitive challenge), in order to investigate some of the main selection pressures thought to affect the evolution of ungulate cognition.ResultsThe majority of trained goats (9/12) successfully learned the task quickly; on average, within 12 trials. After intervals of up to 10 months, they solved the task within two minutes, indicating excellent long-term memory. The goats did not learn the task faster after observing a demonstrator than if they did not have that opportunity. This indicates that they learned through individual rather than social learning.ConclusionsThe individual learning abilities and long-term memory of goats highlighted in our study suggest that domestication has not affected goat physical cognition. However, these cognitive abilities contrast with the apparent lack of social learning, suggesting that relatively intelligent species do not always preferentially learn socially. We propose that goat cognition, and maybe more generally ungulate cognition, is mainly driven by the need to forage efficiently in harsh environments and feed on plants that are difficult to access and to process, more than by the computational demands of sociality. Our results could also explain why goats are so successful at colonizing new environments.

Female competition in chimpanzees.

Female chimpanzees exhibit exceptionally slow rates of reproduction and raise their offspring without direct paternal care. Therefore, their reproductive success depends critically on long-term access to high-quality food resources over a long lifespan. Chimpanzee communities contain multiple adult males, multiple adult females and their offspring. Because males are philopatric and jointly defend the community range while most females transfer to new communities before breeding, adult females are typically surrounded by unrelated competitors. Communities are fission-fusion societies in which individuals spend time alone or in fluid subgroups, whose size depends mostly on the abundance and distribution of food. To varying extents in different populations, females avoid direct competition by foraging alone or in small groups in distinct, but overlapping core areas within the community range to which they show high fidelity. Although rates of aggression are low, females compete for space and access to food. High rank correlates with high reproductive success, and high-ranking females win direct contests for food and gain preferential access to resource-rich sites. Females are aggressive to immigrant females and even kill the newborn infants of community members. The intensity of such aggression correlates with population density. These patterns are compared to those in other species, including humans.

Ovarian cycle activity varies with respect to age and social status in free-ranging elephants in Addo Elephant National Park, South Africa.

Free-ranging African elephants live in a fission-fusion society, at the centre of which is the matriarch. Matriarchs are generally older females that guide their families to resources and co-ordinate group defense. While much is known about elephant society, knowledge is generally lacking about how age affects the physiology of wild elephants. Investigation of the ovarian activity of free-ranging elephants could provide insight into the reproductive ageing process, with implications for population management. Faecal samples were collected from 46 individuals ranging in age from 14 to 60 years for a 2-year period, and progestagen metabolite analyses were used to examine relationships between social status, age, season, and ovarian activity in female elephants in Addo Elephant National Park, South Africa. Social status was the strongest predictor of faecal progestagen metabolite concentrations in non-pregnant elephants, with grand matriarchs (n = 6) having the lowest values compared with matriarchs (n = 21) and non-matriarch females (n = 19). Likewise, social status and age were the strongest predictors of faecal progestagen metabolite concentrations in pregnant elephants (n = 27). The number of years since a non-pregnant female gave birth to her last calf (post-partum duration) was longer for older females with a higher social status, as well as during the dry season. Our results indicate that social standing and age of elephants are related to reproductive function, and that older females exhibit reductions in ovarian capacity. These results expand our understanding of reproduction and fertility throughout an elephant's lifespan, and the factors that impact gonadal function in free-ranging females. Given that possible over-abundance of elephants in areas such as Addo Elephant National Park is fuelling the debate over how best to manage these populations, knowledge about the reproductive potential of high-ranking females can provide managers with biological data to identify the best candidates for controlling growth through translocation or contraception.

Pant hoot chorusing and social bonds in male chimpanzees

Vocal interactions, such as call exchanges or chorusing, are common behaviours in many animal species and their function has often been attributed to social bonding. However, few studies have investigated the effectiveness of vocalizations as bonding signals in comparison to other affiliative behaviours. We tested the hypothesis that male chimpanzee, Pan troglodytes schweinfurthii, pant hoot chorusing, a common behaviour in these primates, is a reliable but also flexible signal of affiliative relationships. The results of our study, conducted on the Kanyawara community of chimpanzees in Uganda, show that males were more likely to join in with the pant hoot of preferred long-term social partners to form a chorus. This supports the hypothesis that this behaviour is a good indicator of strong or long-term social bonds between male chimpanzees. However, our results also show that pant hoot chorusing reliably reflects short-term affiliations between males. For instance, male dyads were more likely to be involved in affiliative behaviours, such as reciprocated grooming, joint nonvocal displays and coalitions, on days when they chorused together, compared to days when they did not. This pattern applied to both preferred and neutral social partners. Moreover, on a short-term basis chorusing was a better indicator of other affiliative behaviours than grooming. We suggest that in male chimpanzees pant hoot choruses are efficient signals of short-term affiliative relationships. We conclude that potentially low-cost bonding behaviours such as coordinated vocal displays might be especially adaptive in highly fluid fission–fusion societies where grouping patterns are often unpredictable.

A leopard ate a chimpanzee: First evidence from East Africa

Fission-fusion societies are social systems in which individuals belonging to the same community are rarely all together but rather spend most of their time in temporary parties. This flexible social organization is assumed to be an adaptation that balances advantages and costs of group living in a fluid way as resources and constraints shift through space and time. It has been argued that this flexibility freed hominins from the foraging constraints caused by living in large groups. Given their close genetic relationship to humans and because they represent the classic case of a fission-fusion society, chimpanzees have often been used as referential models to understand human social evolution. Determinants of chimpanzee party size have been widely studied for decades across several communities. However, we lack data from open and dry sites—which closely resemble those reconstructed for Plio-Pleistocene hominins—on communities that potentially face similar environmental constraints as early hominins did. We investigated chimpanzee (Pan troglodytes schweinfurthii) grouping patterns on a recently habituated community living in the savanna-woodland mosaic landscape of the Issa Valley, western Tanzania, by following chimpanzees daily and recording party size every hour. Our results revealed that party size at Issa 1) followed seasonal fluctuations in food availability, 2) increased in the presence of swollen females, and 3) was higher in open vegetation, which potentially presents a high predation risk. Furthermore, we found the Issa community to be highly cohesive compared with the majority of other communities, possibly due to a combination of its small size and potential threats characterizing its home range. Our study fills a gap in our knowledge of chimpanzee sociality by exploring grouping pattern determinants in an East African understudied biome and highlights what elements of early hominin social behavior may have evolved in Late Pliocene landscapes.