Collective decision‐making and fission–fusion dynamics: a conceptual framework

Sociality exists in an extraordinary range of ecological settings. For individuals to accrue the benefits associated with social interactions, they are required to maintain a degree of spatial and temporal coordination in their activities, and make collective decisions. Such coordination and decision‐making has been the focus of much recent research. However, efforts largely have been directed toward understanding patterns of collective behaviour in relatively stable and cohesive groups. Less well understood is how fission–fusion dynamics mediate the process and outcome of collective decisions making. Here, we aim to apply established concepts and knowledge to highlight the implications of fission–fusion dynamics for collective decisions, presenting a conceptual framework based on the outcome of a small‐group discussion INCORE meeting (funded by the European Community's Sixth Framework Programme). First, we discuss how the degree of uncertainty in the environment shapes social flexibility and therefore the types of decisions individuals make in different social settings. Second, we propose that the quality of social relationships and the energetic needs of each individual influence fission decisions. Third, we explore how these factors affect the probability of individuals to fuse. Fourth, we discuss how group size and fission–fusion dynamics may affect communication processes between individuals at a local or global scale to reach a consensus or to fission. Finally, we offer a number of suggestions for future research, capturing emerging ideas and concepts on the interaction between collective decisions and fission–fusion dynamics.     

The influence of size-dependent life-history traits on the structure and dynamics of populations and communities

Individual organisms often show pronounced changes in body size throughout life with concomitant changes in ecological performance. We synthesize recent insight into the relationship between size dependence in individual life history and population dynamics. Most studies have focused on size‐dependent life‐history traits and population size‐structure in the highest trophic level, which generally leads to population cycles with a period equal to the juvenile delay. These cycles are driven by differences in competitiveness of differently sized individuals. In multi‐trophic systems, size dependence in life‐history traits at lower trophic levels may have consequences for both the dynamics and structure of communities, as size‐selective predation may lead to the occurrence of emergent Allee effects and the stabilization of predator–prey cycles. These consequences are linked to that individual development is density dependent. We conjecture that especially this population feedback on individual development may lead to new theoretical insight compared to theory based on unstructured or age‐dependent models. Density‐dependent individual development may also cause individuals to realize radically different life histories, dependent on the state and dynamics of the population during their life and may therefore have consequences for individual behaviour or the evolution of life‐history traits as well.     

Applying the resource dispersion hypothesis to a fission–fusion society: A case study of the African lion (Panthera leo)

The relationship between the spatiotemporal distribution of resources and patterns of sociality is widely discussed. While the resource dispersion hypothesis (RDH) was formulated to explain why animals sometimes live in groups from which they derive no obvious benefits, it has also been successfully applied to species that benefit from group living. Some empirical tests have supported the RDH, but others have not, so conclusions remain equivocal and further research is required to determine the extent to which RDH predictions hold in natural systems. Here, we test four predictions of the RDH in an African lion population in the context of their fission–fusion society. We analyzed data on group composition of GPS‐collared lions and patterns of prey availability. Our results supported the first and second predictions of the RDH: Home range size (a) was independent of group size and (b) increased with distance between encounters with prey herds. Nonetheless, the third and fourth RDH predictions were not supported: (c) The measure of resource heterogeneity and (d) resource patch richness measured through prey herd size and body size had no significant effect on lion group size. However, regarding the fourth prediction, we added an adaptation to account for dynamics of fission–fusion society and found that the frequency of pride fission increased as group size increased. Our data set restricted us from going on to explore the effect of fission–fusion dynamics on the relationship between group size and patch richness. However, this should be investigated in future studies as including fission–fusion dynamics provides a more nuanced, realistic appreciation of lion society. Our study emphasizes the importance of understanding the complexity of a species' behavioral ecology within the framework of resource dispersion. Whatever larger theoretical framework may emerge to explain lion society, incorporating fission–fusion dynamics should allow the RDH to be refined and improved.     

Social and spatial effects on genetic variation between foraging flocks in a wild bird population

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co‐occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission–fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission–fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%–45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space‐independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.     

To follow or not? How animals in fusion–fission societies handle conflicting information during group decision‐making

When group members possess differing information about the environment, they may disagree on the best movement decision. Such conflicts result in group break‐ups, and are therefore a fundamental driver of fusion–fission group dynamics. Yet, a paucity of empirical work hampers our understanding of how adaptive evolution has shaped plasticity in collective behaviours that promote and maintain fusion–fission dynamics. Using movement data from GPS‐collared bison, we found that individuals constantly associated with other animals possessing different spatial knowledge, and both personal and conspecific information influenced an individual's patch choice decisions. During conflict situations, bison used group familiarity coupled with their knowledge of local foraging options and recently sampled resource quality when deciding to follow or leave a group – a tactic that led to energy‐rewarding movements. Natural selection has shaped collective behaviours for coping with social conflicts and resource heterogeneity, which maintain fusion–fission dynamics and play an essential role in animal distribution.     

Fission‐fusion dynamics of Guiana dolphin (Sotalia guianensis) groups at Pipa Bay,Rio Grande do Norte,Brazil

Fission‐fusion dynamics seem to reflect individual decisions as well as temporal and spatial variations in the organization of groups of the same species. To understand the group dynamics of the Guiana dolphin, Sotalia guianensis, at Pipa Bay, Brazil, we investigated the three dimensions of a fission‐fusion social system: (1) variation in spatial cohesion, (2) variation in party size, and (3) variation in party composition. Sampling took place from December 2007 to February 2009 over 176 d and we analyzed the behavioral patterns of 658 groups. Within subgroups, animals remained cohesive, particularly in groups of adults and calves. Greater cohesion was also observed during resting and fission‐fusion rates were higher during milling and feeding. Groups composed of adults and juveniles showed a higher dynamics index (group size variation as a function of time) than groups composed only of adults and the fission‐fusion rate was higher during dry periods. Guiana dolphin groups frequently changed their group size and composition every 20 min on average. Taking these factors into consideration, we suggest that the Guiana dolphin demonstrates fission‐fusion dynamics, a pattern of behavior similar to what has been observed in other coastal odontocete species, such as Tursiops spp. and Lagenorhynchus obscurus.     

Herd composition,kinship and fission–fusion social dynamics among wild giraffe

A variety of social systems have evolved as a consequence of competition and cooperation among individuals. Giraffe (Giraffa camelopardalis sp.) societies are an anomaly because the dearth of long‐term data has produced two polar perspectives: a loose amalgamation of non‐bonded individuals that sometimes coalesce into a herd and a structured social system with a fission–fusion process modifying herd composition within a community. We analysed 34 years of data collected from a population of Thornicroft's giraffe (G. c. thornicrofti, Lydekker 1911) residing in South Luangwa, Zambia, to establish the nature of giraffe society. Our sample consisted of 52 individually recognized animals. We found that giraffe herd composition is based upon long‐term social associations that often reflect kinship, with close relatives significantly more likely than non‐relatives to establish herds. Mother/offspring dyads had the strongest associations, which persisted for years. Giraffe live in a complex society characterized by marked flexibility in herd size, with about 25% of the variance in herd composition owing to kinship and sex. We suggest that giraffe herds share many characteristics of fission–fusion social systems and propose that sophisticated communication systems are a crucial component regulating subgroup dynamics.     

Organellar vs cellular control of mitochondrial dynamics

Mitochondrial dynamics, the fusion and fission of individual mitochondrial units, is critical to the exchange of the metabolic, genetic and proteomic contents of individual mitochondria. In this regard, fusion and fission events have been shown to modulate mitochondrial bioenergetics, as well as several cellular processes including fuel sensing, ATP production, autophagy, apoptosis, and the cell cycle. Regulation of the dynamic events of fusion and fission occur at two redundant and interactive levels. Locally, the microenvironment of the individual mitochondrion can alter its ability to fuse, divide or move through the cell. Globally, nuclear-encoded processes and cellular ionic and second messenger systems can alter or activate mitochondrial proteins, regulate mitochondrial dynamics and concomitantly change the condition of the mitochondrial population. In this review we investigate the different global and local signals that control mitochondrial biology. This discussion is carried out to clarify the different signals that impact the status of the mitochondrial population.     

Modelling Animal Group Fission Using Social Network Dynamics

Group life involves both advantages and disadvantages, meaning that individuals have to compromise between their nutritional needs and their social links. When a compromise is impossible, the group splits in order to reduce conflict of interests and favour positive social interactions between its members. In this study we built a dynamic model of social networks to represent a succession of temporary fissions involving a change in social relations that could potentially lead to irreversible group fission (i.e. no more group fusion). This is the first study that assesses how a social network changes according to group fission-fusion dynamics. We built a model that was based on different parameters: the group size, the influence of nutritional needs compared to social needs, and the changes in the social network after a temporary fission. The results obtained from this theoretical data indicate how the percentage of social relation transfer, the number of individuals and the relative importance of nutritional requirements and social links influence the average number of days before irreversible fission occurs. The greater the nutritional needs and the higher the transfer of social relations during temporary fission, the fewer days will be observed before an irreversible fission. It is crucial to bridge the gap between the individual and the population level if we hope to understand how simple, local interactions may drive ecological systems.     

Loner or socializer? Ravens' adrenocortical response to individual separation depends on social integration

Non-breeding common ravens (Corvus corax) live in complex social groups with a high degree of fission–fusion dynamics. They form valuable relationships and alliances with some conspecifics, while taking coordinated action against others. In ravens, affiliates reconcile their conflicts, console each other after conflicts with a third party, and provide each other with social support — all behaviors that presumably reduce corticosterone levels and alleviate stress. However, how well an individual is socially integrated in a (sub)group might vary substantially. This raises the question whether the social integration of a raven affects its stress responses to fission–fusion dynamics. The present study aims to investigate this effect experimentally by separating single ravens (n = 16) individually from their group for four days and subsequently reintroducing them. To determine stress response patterns in the separated individuals we measured the amounts of immunoreactive corticosterone metabolites (CM) in droppings. We compared two enzyme immunoassays, which we validated by conducting an ACTH challenge, and finally decided to apply an 11-oxoetiocholanolone enzyme immunoassay. Additionally, we determined levels of social integration using focal observations. Our findings suggest that a strong social integration is related to low CM levels when the individuals are within the group and high levels during separations, implying that separation leads to stress in these birds. In contrast, poorly socially integrated ravens seem to exhibit the opposite pattern, indicating that to them group living is more stressful than being temporarily separated. We, therefore, conclude that the birds' adrenocortical activity is modulated by their social integration.     

Dusky dolphin group dynamics and association patterns in Península Valdés,Argentina

We inspected dusky dolphin (Lagenorhynchus obscurus) group dynamics in Golfo Nuevo and found differences in social organization between cold and warm seasons. Surveys were conducted onboard a research vessel, from which we collected behavioral observations and group fission‐fusion data from 2001 to 2008; we also collected photo‐identification data from 2004 to 2012. To analyze association patterns, we calculated half‐weight association index (HWI) and social differentiation (S). We conducted a Monte Carlo permutation test to determine whether observed association patterns were significantly different from random association using a compiled version of SOCPROG 2.7. Group fission and fusion dynamics depended on group behavior, the main activity after the groups' fusion was feeding, and they never fission before socializing. The social structure of dusky dolphins included long‐term preferred companions in the cold season; during the warm season, there were no preferred companions. This seasonal difference in social structure could be related to an accompanying shift in foraging behaviors that appears to be driven by changes in prey availability. If so, then a loosening of bonds among individuals during the warm season, when prey is more available, would reflect these social structure changes.     

Collective decision‐making promotes fitness loss in a fusion‐fission society

While collective decision‐making is recognised as a significant contributor to fitness in social species, the opposite outcome is also logically possible. We show that collective movement decisions guided by individual bison sharing faulty information about habitat quality promoted the use of ecological traps. The frequent, but short‐lived, associations of bison with different spatial knowledge led to a population‐wide shift from avoidance to selection of agricultural patches over 9 years in and around Prince Albert National Park, Canada. Bison were more likely to travel to an agricultural patch for the first time by following conspecifics already familiar with agricultural patches. Annual adult mortality increased by 12% due to hunting of bison on agricultural lands. Maladaptive social behaviour accordingly was a major force that contributed to a ~50% population decline in less than a decade. In human‐altered landscapes, social learning by group‐living species can lead to fitness losses, particularly in fusion‐fission societies.     

Non-lethal effects of predation in birds

Predators can affect individual fitness and population and community processes through lethal effects (direct consumption or ‘density’ effects), where prey is consumed, or through non‐lethal effects (trait‐mediated effects or interactions), where behavioural compensation to predation risk occurs, such as animals avoiding areas of high predation risk. Studies of invertebrates, fish and amphibians have shown that non‐lethal effects may be larger than lethal effects in determining the behaviour, condition, density and distribution of animals over a range of trophic levels. Although non‐lethal effects have been well described in the behavioural ecology of birds (and also mammals) within the context of anti‐predation behaviour, their role relative to lethal effects is probably underestimated. Birds show many behavioural and physiological changes to reduce direct mortality from predation and these are likely to have negative effects on other aspects of their fitness and population dynamics, as well as affecting the ecology of their own prey and their predators. As a consequence, the effects of predation in birds are best measured by trade‐offs between maximizing instantaneous survival in the presence of predators and acquiring or maintaining resources for long‐term survival or reproduction. Because avoiding predation imposes foraging costs, and foraging behaviour is relatively easy to measure in birds, the foraging–predation risk trade‐off is probably an effective framework for understanding the importance of non‐lethal effects, and so the population and community effects of predation risk in birds and other animals. Using a trade‐off approach allows us to predict better how changes in predator density will impact on population and community dynamics, and how animals perceive and respond to predation risk, when non‐lethal effects decouple the relationship between predator density and direct mortality rate. The trade‐off approach also allows us to identify where predation risk is structuring communities because of avoidance of predators, even when this results in no observable direct mortality rate.     

Site fidelity in temporally correlated environments enhances population persistence

Site fidelity, the phenomenon of remaining faithful to sites, often where an individual has bred successfully in the past, has important consequences for population dynamics. Previous results have shown that site fidelity results in a positive correlation between population density and fitness. Here, I build on this theme by incorporating site fidelity using the win‐stay : lose‐switch rule often seen among birds, i.e. individuals return to sites were they bred successfully in the past and vacate those where they have not. Results demonstrate that the combination of site fidelity and temporal autocorrelation in site quality can enhance the persistence of population networks, whereas either factor acting alone has little or no influence. Moreover, there is an abrupt threshold at moderate levels of temporal autocorrelation, ρ_time > 0.35–0.4, beyond which persistence time and the probability of surviving >500 years is greatly accelerated. These results suggest that temporal autocorrelation combined with appropriate behavioural responses may enhance population persistence.     

How can social network analysis improve the study of primate behavior?

When living in a group, individuals have to make trade-offs, and compromise, in order to balance the advantages and disadvantages of group life. Strategies that enable individuals to achieve this typically affect inter-individual interactions resulting in nonrandom associations. Studying the patterns of this assortativity using social network analyses can allow us to explore how individual behavior influences what happens at the group, or population level. Understanding the consequences of these interactions at multiple scales may allow us to better understand the fitness implications for individuals. Social network analyses offer the tools to achieve this. This special issue aims to highlight the benefits of social network analysis for the study of primate behaviour, assessing it's suitability for analyzing individual social characteristics as well as group/population patterns. In this introduction to the special issue, we first introduce social network theory, then demonstrate with examples how social networks can influence individual and collective behaviors, and finally conclude with some outstanding questions for future primatological research.     

Are fission–fusion dynamics consistent among populations? A large‐scale study with Cape buffalo

Fission–fusion dynamics allow animals to manage costs and benefits of group living by adjusting group size. The degree of intraspecific variation in fission–fusion dynamics across the geographical range is poorly known. During 2008–2016, 38 adult female Cape buffalo were equipped with GPS collars in three populations located in different protected areas (Gonarezhou National Park and Hwange National Park, Zimbabwe; Kruger National Park, South Africa) to investigate the patterns and environmental drivers of fission–fusion dynamics among populations. We estimated home range overlap and fission and fusion events between Cape buffalo dyads. We investigated the temporal dynamics of both events at daily and seasonal scales and examined the influence of habitat and distance to water on event location. Fission–fusion dynamics were generally consistent across populations: Fission and fusion periods lasted on average between less than one day and three days. However, we found seasonal differences in the underlying patterns of fission and fusion, which point out the likely influence of resource availability and distribution in time on group dynamics: During the wet season, Cape buffalo split and associated more frequently and were in the same or in a different subgroup for shorter periods. Cape buffalo subgroups were more likely to merge than to split in open areas located near water, but overall vegetation and distance to water were very poor predictors of where fission and fusion events occurred. This study is one of the first to quantify fission–fusion dynamics in a single species across several populations with a common methodology, thus robustly questioning the behavioral flexibility of fission–fusion dynamics among environments.     

Mitochondrial fusion and fission in cell life and death

Mitochondria are dynamic organelles that constantly fuse and divide. These processes (collectively termed mitochondrial dynamics) are important for mitochondrial inheritance and for the maintenance of mitochondrial functions. The core components of the evolutionarily conserved fusion and fission machineries have now been identified, and mechanistic studies have revealed the first secrets of the complex processes that govern fusion and fission of a double membrane-bound organelle. Mitochondrial dynamics was recently recognized as an important constituent of cellular quality control. Defects have detrimental consequences on bioenergetic supply and contribute to the pathogenesis of neurodegenerative diseases. These findings open exciting new directions to explore mitochondrial biology.     

Testing the Cognition of the Forgotten Colobines: A First Look at Golden Snub-Nosed Monkeys (Rhinopithecus roxellana)

Although our understanding of primate cognition is growing rapidly, little is known about the cognition of colobines. Here we report the results of a set of 5 experiments on colobine cognition using 17 golden snub-nosed monkeys (Rhinopithecus roxellana). These monkeys are folivores that form multilevel societies with groups of hundreds of individuals and relatively high fission–fusion dynamics. We investigated their sensitivity to human social cues and ability to inhibit impulsive behavioral responses. In three sociocognitive experiments we found that, like most other primates, they follow the gaze direction of a human demonstrator but there is no evidence that they use others’ social cues in a cooperative task to locate hidden food or in a competitive task to steal forbidden food. In two inhibitory control experiments, we found that the monkeys showed a low level of inhibitory control, comparable to that of other folivorous primates. These results suggest that phylogeny and folivory might have been important in shaping the cognition of golden snub-nosed monkeys. Moreover, this species’ large group size and relatively high fission–fusion dynamics may not have imposed a significant social challenge to their cognition, as social interactions occur mainly within basic social units.     

Dyadic associations reveal clan size and social network structure in the fission–fusion society of spotted hyaenas

Estimating the size and dynamics of populations is of paramount importance in ecology. In species with uniquely marked individuals, capture–recapture methods can be used to establish population size and to explore associations between individuals. However, very few studies have used cameras traps to focus on group composition in social carnivores, despite being of particular interest in species characterised by “fission–fusion” formation of sub-groups. Here, we provide estimates of (a) population size, (b) density, (c) clan size, (d) association patterns and (e) social network structure in spotted hyaenas (Crocuta crocuta) based on images from camera traps deployed at waterholes on Ongava Game Reserve (northern Namibia). In a 15 week study period, we identified 32 individuals. Dyadic associations and the resulting social network showed that all but two hyaenas associated directly or indirectly with each other, indicating the presence of one clan of at least 30 individuals, resulting in a density of 8.1 hyaenas/100 km². We found a very high variability in the tendency of individuals to associate with others. This study confirms a highly dynamic fission–fusion society in spotted hyaenas. We argue that camera traps can provide relevant insights into large carnivore social network structure where associations between individuals are difficult to observe directly.