Fission‐Fusion Dynamics: New Research Frameworks Author(S): Filippo Aureli, Colleen M

Fission‐Fusion Dynamics: New Research Frameworks Author(s): Filippo Aureli, Colleen M. Schaffner, Christophe Boesch, Simon K. Bearder, Josep Call, Colin A. Chapman, Richard Connor, Anthony Di Fiore, Robin I. M. Dunbar, S. Peter Henzi, Kay Holekamp, Amanda H. Korstjens, Robert Layton, Phyllis Lee, Julia Lehmann, Joseph H. Manson, Gabriel Ramos‐Fernandez, Karen B. Strier, and Carel P. van Schaik Source: Current Anthropology, Vol. 49, No. 4 (August 2008), pp. 627-654 Published by: The University of Chicago Press on behalf of Wenner-Gren Foundation for Anthropological Research Stable URL: http://www.jstor.org/stable/10.1086/586708 . Accessed: 12/11/2015 08:47

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Fission-Fusion Dynamics New Research Frameworks

by Filippo Aureli, Colleen M. Schaffner, Christophe Boesch, Simon K. Bearder, Josep Call, Colin A. Chapman, Richard Connor, Anthony Di Fiore, Robin I. M. Dunbar, S. Peter Henzi, Kay Holekamp, Amanda H. Korstjens, Robert Layton, Phyllis Lee, Julia Lehmann, Joseph H. Manson, Gabriel Ramos-Fernandez, Karen B. Strier, and Carel P. van Schaik

CAϩ Online-Only Material: Supplements A–I

Renewed interest in fission-fusion dynamics is due to the recognition that such dynamics may create unique challenges for social interaction and distinctive selective pressures acting on underlying communicative and cognitive abilities. New frameworks for integrating current knowledge on fission- fusion dynamics emerge from a fundamental rethinking of the term “fission-fusion” away from its current general use as a label for a particular modal type of social system (i.e., “fission-fusion societies”). Specifically, because the degree of spatial and temporal cohesion of group members varies both within and across taxa, any social system can be described in terms of the extent to which it expresses fission-fusion dynamics. This perspective has implications for socioecology, communication, cognitive demands, and human social evolution.

The term “fission-fusion” was first used by Hans Kummer and distribution of resources.1 Social systems characterized (1971) to describe the social system of a few taxa of non- by such fission-fusion dynamics are considered rare among human primates, such as chimpanzees, geladas, and hama- mammals, but they are typical of some primate (Smuts et al. dryas baboons, that change the size of their groups by means 1987) and other mammalian species (e.g., some bats [Kerth of the fission and fusion of subunits (called parties or sub- and Ko¨nig 1999], dolphins [Connor et al. 2000], elephants groups) according to both their activity and the availability

Human Origins, New York University. Robin I. M. Dunbar is Pro- Filippo Aureli is Professor and Codirector of the Research Centre fessor of Evolutionary Anthropology, University of Oxford, and Co- in Evolutionary Anthropology and Palaeoecology at Liverpool John director of the British Academy’s Centenary Project “Lucy to Lan- Moores University (School of Biological and Earth Sciences, James guage.” S. Peter Henzi is Professor of Psychology, University of Parsons Building, Byrom Street, Liverpool L3 AF3, United Kingdom Lethbridge. Kay Holekamp is Professor of Zoology, Michigan State [[email protected]]). Colleen M. Schaffner is Professor of Be- University. Amanda H. Korstjens is a senior lecturer in biological havioral Biology in the Department of Psychology, University of anthropology, Bournemouth University. Robert Layton is Professor Chester. Christophe Boesch is Professor at the University of Leipzig of Anthropology, University of Durham. Phyllis Lee is Professor of and a director of the Max Planck Institute of Evolutionary Anthro- Psychology, University of Stirling. Julia Lehmann is a senior lec- pology. Aureli, Schaffner, and Boesch organized the workshop that turer in biological anthropology, University of Roehampton. Joseph led to this collaborative effort. The remaining contributors are listed H. Manson is Professor of Anthropology, University of California alphabetically. Simon K. Bearder is Professor of Biological An- at Los Angeles. Gabriel Ramos-Fernandez is Professor of Biology, thropology, Oxford Brookes University. Josep Call is Codirector of Instituto Polite´cnico Nacional, Mexico. Karen B. Strier is Professor the Wolfgang Ko¨hler Primate Research Center, Max Planck Institute of Anthropology, University of Wisconsin–Madison. Carel P. Van for Evolutionary Anthropology. Colin A. Chapman is Canada Re- Schaik is Professor and Director of the Anthropological Institute and search Chair and Professor of Anthropology at McGill School of Museum, University of Zu¨rich. This paper was submitted 9 VI 06 Environment, McGill University. Richard Connor is Professor of and accepted 28 I 08. Biology, University of Massachusetts–Dartmouth. Anthony Di Fiore 1. Filippo Aureli, Colleen M. Schaffner, and Christophe Boesch have is Associate Professor of Anthropology, Center for the Study of principal responsibility for this section.

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[Moss and Lee n.d.; Wittemyer, Douglas-Hamilton, and Getz This perspective on the use of the term “fission-fusion” fits 2005], and spotted hyenas [Holekamp et al. 1997]). Among well with Kappeler and van Schaik’s (2002) definition of social primates most studies on fission-fusion dynamics have fo- organization, which explicitly incorporates the degree of spa- cused on chimpanzees (Boesch and Boesch-Achermann 2000; tiotemporal cohesion of a social system. In particular, this Mitani, Watts, and Muller 2002; Nishida and Hiraiwa- perspective emphasizes that simple dichotomous distinctions Hasegawa 1987) and spider monkeys (Chapman, Wrangham, of social organizations as cohesive versus flexible are neither and Chapman 1995; Symington 1990). Similar patterns also realistic nor accurate (Strier 1989). Moreover, it highlights seem to occur in bonobos (Hohmann and Fruth 2002; that flexible spatiotemporal grouping patterns in primates and Nishida and Hiraiwa-Hasegawa 1987; Stumpf 2007) and some other vertebrates are more common—and more complex— populations of muriquis (Milton 1984). Fission-fusion dy- than generally recognized (Kinzey and Cunningham 1994; namics are likewise typical of modern humans, including Struhsaker and Leland 1979; Sussman and Garber 2007). The hunter-gatherers (Marlowe 2005), although they are not often critical issue is that spatiotemporal variation in grouping pat- explicitly recognized. The following quote captures this ap- terns influences the opportunities for group members to in- parent anomaly: “Fission-fusion sociality seems so natural and teract with one another and, ultimately, the resulting social necessary to humans—including anthropologists—that it system. hardly demands explanation, if it is noticed at all” (Rodseth This modification of the use of the term “fission-fusion” et al. 1991, 238). The sharing of this flexible social nature requires the development of new conceptual frameworks for with our closest living relatives suggests that fission-fusion studying the implications of variation in fission-fusion dy- dynamics were characteristic of the social system of the last namics across groups and species for their socioecological, common ancestor of chimpanzees, bonobos, and modern communicatory, and cognitive aspects. As a start, it is nec- humans. essary to develop basic heuristics for describing the degree of Given the potential role of fission-fusion dynamics in hu- fission-fusion dynamics seen in a group or species and thus man social evolution, we organized a symposium at the Twen- the opportunities that individuals have for close-range social tieth Congress of the International Primatological Society and interaction. Any such conceptual framework will, of course, a postcongress workshop to explore from a broad comparative be multidimensional. Here we propose a framework involving perspective whether fission-fusion dynamics create unique three dimensions that together capture potential temporal challenges for social interactions or distinct selective pressures variation in spatial cohesion and membership in a given en- for specific underlying communicative and cognitive abilities. vironment: (1) the temporal variation in spatial cohesion In this section, we emphasize that the variation in fission- among group members, (2) the temporal variation in party fusion dynamics goes beyond the modal types of societies that size, and (3) the temporal variation in party composition (fig. have traditionally been described as “fission-fusion.” We 1; for detail on the three dimensions, see CAϩ online sup- therefore suggest a revision of the way the term “fission- plement C). fusion” is used to reflect such variation, and we propose a The accumulation of data for the dimensions of the pro- new framework to stimulate the quantification of the relative posed framework or other variants will permit the relative degrees of fission-fusion dynamics in different taxa in order placement of species and populations of the same species to facilitate future comparative research. within a complex multidimensional fission-fusion space (e.g., Although the distinctions among modal types of “fission- fig. 1), which is an essential first step toward the systematic fusion societies” (for a brief review, see CAϩ online supple- investigation of whether social systems characterized by dif- ment A) are useful for describing the degree of flexibility in ferent degrees of fission-fusion dynamics are quantitatively or the social system of certain species, many other systems char- qualitatively different from one another in terms of socio- acterized by fission-fusion dynamics do not fit within these ecological conditions, social interaction, and cognitive abili- modal types. In fact, there is pronounced variation in the ties. However, because the relative positions of most species degree of fission-fusion dynamics both across and within spe- and populations within this multidimensional space have yet cies (for examples, see CAϩ online supplement B), and this to be empirically determined, a simplified terminology is used poses a difficulty in using the modal terminology. Given this throughout the following sections for ease of notation in com- variation, we propose a fundamental rethinking of that ter- paring social systems characterized by a higher degree of minology. We suggest that the term “fission-fusion” be aban- fission-fusion dynamics (hereafter “higher-FF” groups or doned as a label for a particular modal type of social system taxa) and those characterized by relatively higher temporal (i.e., “fission-fusion societies”) and that the term “fission- stability in group cohesion and membership (hereafter fusion dynamics” be used to refer to the extent of variation “lower-FF” groups or taxa). The terms “higher-FF” and in spatial cohesion and individual membership in a group over “lower-FF” represent relative points within multidimensional time. This will allow any animal society to be characterized fission-fusion space and therefore need to be interpreted in by its degree of fission-fusion dynamics, which can vary from terms of different degrees of fission-fusion dynamics (i.e., highly cohesive with stable group membership to highly fluid higher and lower in at least one of the three dimensions); in with either relatively stable or flexible subgroup membership. other words, they do not reflect an actual dichotomy.

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ecological theory, whose principal goal is to explain grouping patterns, range use, mating behavior, dispersal tendencies, and inter- and intrasexual social relationships as adaptive responses to features of the ecological and social environment. Primate socioecology historically has taken a reductionist perspective, recognizing a discrete set of modal social systems and seeking to explain, for example, the “nepotistic” female social relationships of many cercopithecines as a consequence of the competitive regime engendered by food resource distribution. The discipline has come a long way using this categorical framework, but the framework plays down the fact that many aspects of social systems (e.g., the spatiotemporal variation in the association patterns of individuals) can vary dramatically both among populations of a given taxon and within the same population over time. Primate socioecology is currently at an important juncture (Janson 2000). If primatologists are to continue to contribute to the development of socioecological theory, it is crucial for us to reevaluate past Figure 1. A three-dimensional conceptual framework to represent assumptions about how ecological variables influence social the degree of fission-fusion dynamics of groups and taxa. The systems and to expand our efforts to understand the first X-axis represents the temporal variation in spatial cohesion principles that shape movement and grouping patterns. In among group members, the Y-axis represents the temporal var- the past, the study of higher-FF taxa has offered a useful tool iation in party size, and the Z-axis represents the temporal var- for exploring such issues, since their responses to ecological iation in party composition. Region A illustrates cases that are changes take place over very short timescales. Here we return low in all three dimensions, such as very cohesive groups or to the example of higher-FF taxa and suggest a new framework constantly dispersed situations (e.g., territorial, solitary species). Region B would include cases that are highly variable in spatial that derives more explicit null models of association by using cohesion and party size but not in party composition, such as spatially explicit agent-based simulations that begin from as- the multilevel societies of hamadryas baboons, which are based sumptions about the state of resources in the environment. on relatively stable one-male units. Region C represents cases The modeling approach that we advocate will accomplish that are high in all three dimensions, such as the highly fluid several goals. First, it will allow us to assess the validity of communities of chimpanzees, spider monkeys, and spotted hy- currently recognized modal types of primate social systems, enas, characterized by highly variable party membership. Groups particularly the so-called fission-fusion societies of chimpan- of modern humans, bottlenose dolphins, and elephants would likely be located between regions B and C. Comparative data for zees and spider monkeys. Second, it will let us explore, in each dimension are needed for the accurate relative placement silico, new metrics for describing patterns of sociospatial as- of species and populations. sociation that might then be applied across taxa and be used for quantifying the fission-fusion space discussed above; using these metrics, we can begin to evaluate the importance of The three-dimensional framework proposed here is a useful observed deviations from expected null models. Finally, first step, but additional frameworks are needed depending through this approach we expect to be able to explore whether on which aspects of fission-fusion dynamics are being con- apparently similar social systems might arise for very different sidered. The following sections propose several new frame- reasons and by different evolutionary routes (Lee 1994). works that are relevant to exploring and understanding variation in fission-fusion dynamics in terms of socioecology, communication, and cognitive demands. The concluding sec- Are Higher-FF Taxa “Special”? tion explores the implications of fission-fusion dynamics for Because higher-FF taxa are relatively uncommon among pri- human evolution. mates and other mammals, researchers tend to imagine that the socioecological pressures they face may be somehow dif- The Socioecology of Fission-Fusion ferent in form or degree from those faced by lower-FF taxa. 2 Dynamics Some higher-FF groups (e.g., those falling into region C of fig. 1) have historically been incorporated into the general Over the past 25 years, studies of primate behavior and ecol- socioecological model as follows. First, the flexible association ogy have contributed greatly to the development of socio- patterns of these higher-FF groups are commonly interpreted 2. Anthony Di Fiore, Colin A. Chapman, S. Peter Henzi, Phyllis Lee, as a solution by large-bodied primates—who face a relatively Julia Lehmann, and Gabriel Ramos-Fernandez have principal responsi- low risk of predation—for coping more efficiently with patch- bility for this section. ily distributed and temporally varying food sources (Dunbar

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1988; Klein and Klein 1977; Milton 1984; Strier 1992; Sy- any one set of ecological conditions determines superficially mington 1988; van Schaik 1989; Wrangham 1977, 1980). Un- similar fission-fusion dynamics in these disparate taxa. Having der these circumstances, females are suggested to spread out identified a number of limitations to current socioecological from one another when resources are scarce to reduce feeding models (see CAϩ online supplement D), we outline a research competition and possibly to aggregate and forage together framework that may help us to address these limitations. when resources are plentiful. More recently, fission-fusion dynamics in these taxa have been viewed as affording flexible A Way Forward? Deriving an Inclusive Spatial Null Model responses for optimal solutions to the usually contrasting pressures of avoiding predators and minimizing feeding com- Our proposition is to develop a new set of null models of petition when there is temporal or spatial fluctuation association and sociality that begin from first principles to in predation pressure and food availability (Boesch and explore links between ecological, social, and demographic var- Boesch-Achermann 2000). For some higher-FF taxa (e.g., iables, on the one hand, and sociospatial relationships, on the chimpanzees, spider monkeys), males are or are presumed to other. Given that there is a great complexity in the environ- be philopatric and cooperate with male relatives to defend ments in which grouping takes place, producing null expec- access to the ranges of several females against males from tations of grouping patterns should take as a starting point neighboring groups (Ghiglieri 1984; Strier 1994; Wrangham a spatially explicit description of the environment inhabited 1979), which in turn is thought to force the dispersal of by a species. Spatial analysis is a mature field that offers many maturing females (Pusey 1979; Pusey and Packer 1987). Ad- tools useful to socioecologists for describing how resources ditional social and demographic factors (e.g., overall com- (e.g., food, watering holes, sleeping sites) or predation risk munity size, presence of cycling females) have been shown to vary in space and time (Dale et al. 2002; Fortin, Dale, and affect fission-fusion dynamics and party size (Lehmann and van Hoef 2002). From this description of the environmental Boesch 2004). For other higher-FF taxa (e.g., geladas and some complexity faced by animals, null models can be produced baboons, which live in multilevel societies; region B of fig. 1) that predict what grouping patterns may arise simply as a the risk posed by nocturnal predators is seen as the selective consequence of the environment. One possible null model pressure favoring the aggregation of large numbers of animals might be summarized as follows: at communal sleeping sites, while competition drives fission- Within a primate social group, patterns of association across ing of these large groups into smaller, cohesive foraging parties time are a consequence solely of individual decisions that during the day (Dunbar 1988; Kummer 1968) and the risk maximize access to resources (i.e., they are not influenced of infanticide prompts the consistent association of particular by social factors, such as individuals’ relative dominance males with particular females (Henzi and Barrett 2003). rank or their relatedness to other group members). The There are a number of problems inherent in the notion temporal variation in spatial cohesion and membership that higher-FF groups face “special” ecological pressures. First, characteristic of higher-FF groups emerges in response to a past socioecological models of higher-FF groups in primates specific subset of all possible patterns of resource dispersion. offer only post hoc and incomplete explanations for observed patterns of association and kinds of social relationships. For Subsequently, deviation from what is predicted from these example, the existence of a positive relationship between first principles can be analyzed to understand the factors that, habitat-wide fruit availability and foraging party size in both in addition to environmental variation, influence grouping spider monkeys and chimpanzees is taken as evidence that patterns and social relationships. Some of these deviations resource distribution constrains grouping patterns, and yet will not lead too far (e.g., sleeping sites may physically con- resource patch density and distribution explain less than half strain spatial dispersion), while others may be fascinating (e.g., the variance in party size in these taxa (Chapman, Wrangham, quantitative descriptions of how alternative social strategies, and Chapman 1995). In addition, long-term primate studies such as infanticide avoidance, might influence grouping). are increasingly revealing that considerable flexibility in One way to develop null models of movement and group- grouping patterns and within-group social relationships may ing patterns against which empirical data can be compared exist both between populations and within the same popu- is through the use of spatially explicit agent-based simulations. lation of higher-FF taxa over time (Strier 2003; supplement Throughout the history of primate socioecological research, B). Thus, models of the way ecological conditions shape even these kinds of models have been used by various researchers such basic aspects of social systems as group or party size are (Boyer et al. 2004, 2006; Ramos-Fernandez, Boyer, and Go´mez less than straightforward. 2006; Rodman and Di Fiore 1993; te Boekhorst and Hogeweg Moreover, as primatologists pay more attention to work 1994; reviewed by Dunbar 2002), but they have yet to gain on nonprimate taxa, we are coming to appreciate that a wide widespread acceptance (Bryson, Ando, and Lehmann 2007). variety of other vertebrates are also characterized by fission- We stress that these are null models that need to be used as fusion dynamics (see supplement B). The extent to which tools to begin to understand the behavior of real animals rather socioecological models developed from primate studies can than as actual descriptions of an animal’s behavior (Peck be applied across taxa is unknown, but it is very unlikely that 2004).

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The central elements of a spatially explicit agent-based sim- run for a number of steps. The model is then iterated many ulation model include a habitat in which various kinds of times, and the resulting grouping patterns of the agents are resources (e.g., depleting food patches, sleeping sites) and recorded for different values of the environmental parameters, agents (e.g., individual model animals, predators) occupy par- generating a surface that reflects what association patterns are ticular locations (fig. 2). The construction of such a model predicted to be associated with what combinations of envi- will begin by explicitly designating the distribution of food ronmental variables. Observed field data can then be exam- resources because food necessarily drives travel patterns— ined for concordance with this model surface. If we start with even if every other factor were missing from the environment, realistic values for meaningful environmental parameters and animals would still need to move to feed. On the basis of the notice that the particular grouping patterns arise only in cer- spatially explicit descriptions of environmental variation, a set tain environments, we obtain testable predictions about the of model parameters or dimensions that capture this variation effect of the environment on grouping, and this provides a is developed. Multiple agents within the simulation are then means of understanding deviations from a purely ecological given simple foraging rules (e.g., “move to the next available explanation. For examples of the use of spatially explicit patch” or “move to the largest patch within a certain dis- agent-based simulations see CAϩ online supplement E. tance”), and the emergent spatial structuring of those indi- As with traditional socioecological models, accurate em- viduals (association patterns) is assessed after the model is pirical measures of environmental variables of interest (e.g.,

Figure 2. Hypothetical components of a spatially explicit agent-based simulation model. On the left is a photograph of the landscape being simulated. The top layer on the right side of the ﬁgure (A) shows “baboon” agents distributed across the landscape at one point in time and varying degrees of spatial association (e.g., four “parties” containing two to six independently moving animals). The bottom two layers on the right represent the spatial distribution of two key resources presumed to be important to baboons at that same point in time, where B represents the gradient of food resource availability across the landscape, with the degree of shading proportional to average energy return rate (e.g., calories per unit time) that “baboons” could receive by foraging at that location and C represents the locations of possible sleeping sites (e.g., cliffs) where predation risk is lower (i.e., the degree of shading is inversely proportional to the degree of predation risk experienced at that site). In running a simple simulation, individual “baboons” are given a foraging rule that moves them across the landscape (e.g., “move to an adjacent location where the return rate is higher”). At each step, the positions of all “baboons” and the details of each resource layer are updated, and various measures of association (e.g., average interindividual distance, average party size, etc.) can be calculated.

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 632 Current Anthropology Volume 49, Number 4, August 2008 food distribution) are desirable to lend “realism” to a sim- Implications of Fission-Fusion Dynamics ulation, but one important advantage of a simulation-based for Communication3 approach is that it is possible to explore the effect of a range of values for any model parameter, even one that is very Within primate groups, social signals may perform functions difficult to measure because of observational limitations or as simple as coordinating group movement (Boinski 1996) the time frame needed for accurate measures (e.g., predation or as intricate as conveying and negotiating relationship qual- pressure or infanticide risk). Moreover, once a simple model ities and processes such as formal submission and dominance has been constructed, additional environmental variables can (Flack and de Waal 2004, 2007), reconciliation (Aureli and be added or removed to explore their effect on the emergent de Waal 2000), and trust in the context of coalition formation spatial structuring. In sophisticated models, the various re- (Smuts and Watanabe 1990). The kinds of signals and the sources and agents in the simulation might themselves show size of signal repertoires selected to fulfill these functions are temporal variation in their size (e.g., growing and shrinking expected to be affected by fission-fusion dynamics (Kummer to simulate food patches such as fruiting trees with ripening 2002; Milton 2000). Members of lower-FF groups must re- and then diminishing crops), location (e.g., moving in space solve the conflicts generated by relatively high levels of as- according to behavioral rules to simulate mobile prey or pred- sociation and avoid social disintegration. Members of higher- ators), or state (e.g., cycling through varying stages of “re- FF groups must have ways to reestablish relationships and ceptivity” to simulate female reproductive state). resolve uncertainties (e.g., concerning alliances, dominance The power of the agent-based modeling approach lies in status, and each individual’s relationship to third parties), its versatility and potential for expansion in ways that are depending on the frequency and patterns of spatial and tem- informed by observational studies. For example, although ini- poral separations (Barrett, Henzi, and Dunbar 2003). The tial null models might not explicitly incorporate social factors interacting effects of the spatiotemporal variation in grouping (e.g., dominance or kinship relationships among different patterns and social dynamics determine whether communi- agents) or demographic factors (e.g., group size, population cation functions to solve primarily the problems posed by sex ratio, number of simultaneously receptive females) that relatively high levels of association or those posed by extended are known to influence the degree of spatial cohesion among or frequent spatial separations, independent of the sensory animals (Lehmann and Boesch 2004), the modeling approach anatomy and physiology that different modes of communi- is sufficiently versatile to accommodate the inclusion of these cation (e.g., visual, olfactory, auditory) require. kinds of variables. This can be done, for example, by altering Differences in communication patterns may reflect distinct the behavioral rules that agents follow when they encounter evolutionary routes that could have led to both higher- and one another (e.g., “retreat” when the other agent is more lower-FF groups, and we begin our consideration of com- dominant, “follow” when the other agent is in estrus) or by munication with a description of two possible routes. We then making the behavior of agents contingent on accumulated present a framework for the evolution of social signaling that information about the set of agents previously encountered illustrates the relative importance of signals for maintaining (e.g., “do X” when the sex ratio of encountered agents is male spatial cohesion, separating from other group members, re- biased and “do Y” when it is female biased). Indeed, research solving uncertainty due to low spatial cohesion when indi- on other mammalian taxa suggests that broadening our per- viduals reunite, and negotiating social interactions depending spective from purely resource-based models to more socio- on the degree of fission-fusion dynamics and the evolutionary reproductively based ones may have considerable application route. We finish by showing the utility of the framework for to the study of primate spatial and social associations. For generating testable hypotheses about the way communicatory example, it is clear that various social factors are key deter- signals might vary depending on the social complexity and minants of grouping patterns in other social mammals; the level of cohesion underlying fission-fusion dynamics. Our risk of infanticide influences grouping in lions (Grinnell and framework for the evolution of social signaling is heuristic. McComb 1996; Packer and Pusey 1983), allomaternal care It is meant to stimulate research that investigates the extent shapes the social associations of elephants (Lee 1987), and to which variation in fission-fusion dynamics influences com- reproductive competition over females shapes male alliances munication because few such data exist at present. among dolphins (Connor et al. 2000). The potential influence of these kinds of variables on primate associations and sociality could be explored by integrating them into agent-based The Phylogeny of Fission-Fusion Dynamics simulations, which in turn could be used to develop new Figure 3 depicts two hypothetical evolutionary routes by predictions that could then be tested with field data. We be- which higher-FF groups can arise and yield a variety of social lieve that this integration of theory, modeling, and observation systems (supplement B). On route A, social relationships be- will be a profitable way to understand the causes and con- came increasingly valuable as the fitness gained through long- sequences of higher-FF dynamics in primate and nonprimate taxa and to help identify the range of socioecological con- 3. Karen B. Strier, Colleen M. Schaffner, Joseph H. Manson, and Simon ditions under which lower-FF groups are likely to arise. K. Bearder have principal responsibility for this section.

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Figure 3. Alternative routes to higher degree of fission-fusion dynamics. The ecological conditions that require fissioning of cohesive groups along route A may also make cohesiveness detrimental for higher-FF groups along route B. In this scenario, extended associations may impose ecological costs that will need to be offset by other advantages, such as increased survival of offspring or reproductive success among mates, to achieve the neutrality required for the social transitions along route B. term associations—beginning between mates and/or between while together, signaling departures, and reassessing their re- mothers and their adult offspring—increased. Along route A, lationships following separation (Barrett, Henzi, and Dunbar then, the driving force behind increasing gregariousness was 2003; Dunbar 2003). The particular signals employed by the increasing value of social relationships for mutual advan- higher-FF groups need not be more cognitively demanding, tages, which over time and with expanding scope could have but their repertoires may be more extensive than those of resulted in lower-FF groups such as those of macaques and lower-FF groups. capuchin monkeys. The high value of social relationships By contrast, species on route B in our scenario would move (Cords 1997; Kummer 1978) selected for increasingly so- to higher-FF groups from a solitary rather than a group-living phisticated relationship negotiation skills, thus permitting condition (Mu¨ller and Thalmann 2000; Sterling, Nguyen, and group members to remain together unless ecological pressures Fashing 2000; fig. 3). Route B does not require that differ- imposed high levels of resource competition that necessitate entiated social relationships become increasingly valuable as fissioning. On route A we can envision two main ways in gregariousness intensifies, and associations may have been which higher-FF groups could have evolved: (1) by large short-lived and random or opportunistic. In some galagos, groups fissioning into temporary smaller parties such as those for example, it may be thermally advantageous or safer with observed in the communities of chimpanzees and spider mon- respect to predators to sleep with conspecifics than to sleep keys (Nishida and Hiraiwa-Hasegawa 1987; Symington 1990), alone, but it is the number of conspecifics (as opposed to or (2) by small groups temporarily fusing into larger bands/ differences in their individual value as social partners) that clans and then aggregating with other bands/clans to exploit leads them to fusion. However, it may also be easier or more limited safe sleeping locations, with the basic subunits having a relatively fixed composition, as is the case with the multilevel efficient to associate with familiar conspecifics than with societies of hamadryas baboons (Stammbach 1987). On route strangers, and the resulting higher-FF groups may shift into A, then, higher-FF groups would have emerged among taxa facultatively lower-FF groups if ecological conditions permit in which sophisticated relationship negotiation skills formed (Bearder 1999; fig. 3). Along route B, the transition from the background from which the additional skills necessary for solitary to higher-FF groups could have required some en- resolving relationship uncertainties in the face of periodic hancement of the minimal social skills (i.e., for distinguishing separations evolved. This scenario also conforms to the per- familiar individuals from strangers) and signals for resolving ception of higher-FF taxa evolving along route A having relationship uncertainties over distance and time, though not greater social complexity because their communication rep- to the level attained by lineages traversing route A. Similarly, ertoire requires adeptness at negotiating social relationships lower-FF groups that emerge through route B are expected

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 634 Current Anthropology Volume 49, Number 4, August 2008 to lack the range of relationship negotiation signals found in ships. Examples include schooling fish that execute sophis- both lower-FF and higher-FF groups on route A. ticated antipredator maneuvers (Pitcher and Wyche 1983). In the upper half of figure 4 we find animals that live in complex societies, defined by de Waal and Tyack (2003b)as Mapping the Social Landscape societies that are individualized, longitudinally stable, and The different evolutionary trajectories by which higher-FF probably characterized by strong learning effects on social groups could have arisen have implications for the evolution behavior and survival strategies. It is only in these societies of social signaling. Figure 4 illustrates our framework by de- that we expect to find signals by which individuals can convey picting a two-dimensional landscape for mapping social sys- the relationship qualities and processes described at the be- tems along two intersecting continua to consider the range ginning of this section. We expect the evolution of com- and types of signaling mechanisms required to regulate spatial municative abilities to differ among taxa that fall in quadrants cohesion and social relationships. The X-axis in our landscape III and IV mainly because of differences in the degree to which represents the degree of cohesiveness, operationalized here as individuals need to negotiate conflicts of interest immediately the percentage of conspecifics within a given individual’s so- when extended separation is not a common option (quadrant cial group that it can communicate with at any given time III) or the degree to which they need to resolve uncertainties (which depends on the temporal variation in spatial cohesion, about relationships in the face of frequent separations (quad- party size, and composition; supplement C). We hypothesize rant IV). We suggest that when fissioning is a viable ecological that different kinds of signals are needed, depending on option, conflicts can be avoided instead of deliberately re- whether they function primarily to resolve relationship un- solved. Prolonged, elaborate displays may be warranted dur- certainties that arise without constant contact and to convey ing reunions when fissioning is rare (quadrant III), whereas information about fission events or to maintain coordination simple greeting interactions of shorter duration may suffice within relatively cohesive groups. The Y-axis of the landscape when fission-fusion dynamics are common (quadrant IV) represents the complexity and differentiation of dyadic social (Aureli and Schaffner 2007). Finally, different degrees of social relationships (sensu Hinde 1979), measurable by criteria such complexity and sophistication in signaling should occur de- as high between-dyad variation and low within-dyad variation pending on whether species arrived in quadrant IV via route A or route B. Individuals from route B (e.g., lesser galagos) in rates and intensities of friendly and antagonistic behavior. will have a more limited range of signals than individuals At one extreme of our Y-axis dimension, adults will regard from route A (e.g., chimpanzees). adult conspecifics of the same sex, reproductive condition, and possibly degree of relatedness as interchangeable; at the other extreme, each dyadic relationship will be highly distinct Additional Factors along several dimensions (e.g., agonistic asymmetry, tolerance Local ecological conditions can result in interspecific variation of close proximity, services provided). The X-axis demarcates that affects the relative placement of taxa within quadrants a critical threshold for distinguishing between social environ- III or IV. We identify two parallel gradients in our qualitative ments that either do (upper) or do not (lower) require com- assessment of primates (dotted lines in fig. 4), each of which munication signals for the long-term maintenance of differ- reflects the range spanned by taxa with evolutionarily distinct entiated social relationships. Individuals of species that fall life histories. The upper gradient represents taxa with com- below this threshold may be able to recognize one another paratively slow life histories, such as the atelins, apes, capuchin and may have signals for mediating their social interactions monkeys, and several Old World monkeys, while the lower and coordinating their movements, but it is only among spe- gradient represents taxa with comparatively fast life histories, cies that fall above this threshold that we expect to find signals such as galagos and callitrichids. Taxa with slower life histories that allow for the establishment and maintenance of long- tend to have more complex and differentiated social rela- term, differentiated social relationships. tionships, based on their slower rates of development and The intersection of the two axes in figure 4 divides the longer life spans (Charnov 1991), than those with faster life social landscape into four quadrants. Species in quadrant I histories when their degree of cohesiveness is similar. are low in spatial cohesion and social complexity. Examples Our landscape accounts for the differences in the employ- include solitary mammals in which adults associate only to ment of signals by populations of the same or closely related mate and to contest access to resources (e.g., shrews [Cantoni species whose cohesion and quality of social relationships 1993], giant mouse lemurs [Schu¨lke and Ostner 2005]). affect their respective positions in any of the quadrants. For Courtship and assessment signals are used in these contexts, example, the specialized reconciliation gestures observed in but they communicate only about the current interaction. some captive chimpanzees (de Waal and Roosmalen 1979) Among species in quadrant II, signals serve to coordinate are apparently absent in wild populations (Arnold and Whiten activities and maintain cohesive spatial associations, but social 2001), possibly because the increased spatial cohesion im- interactions are not based on differentiated social relation- posed by captivity necessitates more explicit, unambiguous

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Figure 4. Social landscape and its implications for social signals. The X- axis represents the degree of cohesiveness, while the Y-axis represents the degree of differentiation of social relationships. The type and frequency of signals required to maintain the corresponding range of social associations emerges as an interaction of the two axes within the social landscape space. The position of species on the landscape is meant to be relative and not absolute. To illustrate the variation that is captured by our framework, several primate species have been placed within the landscape. The utility of the landscape is further demonstrated by the placement of several carnivore species. Polar bears are largely solitary and fall within quadrant I. Dwarf mongooses, wolves, and spotted hyenas fall above the X-axis because they are group-living species with highly individualized relationships but differ in the extent of cohesiveness (Hole- kamp, Boydston, and Smale 2000). Intraspecific variation may also be illustrated within the landscape. For example, female and male African elephants are positioned along the X-axis to reflect the sex difference in cohesiveness (see CAϩ online supplement B). reconciliation signals than in the wild, where spatial separa- communication. We have focused on the functions rather tion through fission is an option. The gradients, which express than the forms of social signals. However, consideration of the interacting effects of ecology and phylogeny, provide an the ways in which different modes of communication permit additional basis for predictions about the way intraspecific individuals to keep track of one another without maintaining variation in signals might vary with a taxon’s life-history pat- spatial cohesion is a critical next step (Kummer 2002; see tern. An additional factor affecting signaling is an individual’s CAϩ online supplement G for examples). The parallel gra- range of social opportunities (see CAϩ online supplement dients that distinguish species according to their life-history F). patterns, the impact of variation in social opportunities (sup- This framework for the evolution of social signaling gen- plement F), the evolutionary route followed to reach their erates a suite of testable hypotheses about the minimum re- position in the multidimensional fission-fusion space, and the quirements that different kinds of social patterns impose on different abilities to coordinate their activities over space and

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 636 Current Anthropology Volume 49, Number 4, August 2008 time provide additional variables around which future com- namics automatically endows all species with the same cog- parative studies on the role of communication in regulating nitive abilities. Rather, given that a high degree of fission- social relationships can be designed. fusion dynamics evolved multiple times in a wide range of taxa (from fish to birds to mammals), we should expect that Cognitive Demands of Fission-Fusion cognitive adaptations to such dynamics are both variable and 4 strongly influenced by the species’ evolutionary history, in Dynamics addition to the nature of fission-fusion dynamics (supplement Chimpanzees, elephants, and dolphins—all taxa characterized B) and the degree of differentiation of social relationships by a high degree of fission-fusion dynamics—are renowned (from simple aggregations to complex societies; fig. 4). Com- for having relatively large brains and advanced cognitive abil- parative studies of cognitive adaptations to different degrees ities. One might argue that possessing these characteristics of fission-fusion dynamics should therefore use appropriate and living in higher-FF groups fit together in a causal manner, phylogenetic methods (e.g., Pagel and Harvey 1991; Nunn but this is not necessarily true. Here we explore this issue and and Barton 2001). propose a framework for identifying some of the cognitive abilities we expect to find enhanced among animals living in The Demands of Sociospatial Flexibility higher-FF groups. Another important issue is whether species living in higher- The Role of Evolutionary History FF groups have greater cognitive abilities than species that share an evolutionary history but live in lower-FF groups. We Chimpanzees, elephants, and dolphins are special in that they focus here on taxa that derive from group-living ancestors display an array of cognitive abilities that are not found in (route A in fig. 3). When comparing species living in higher- many other animals, one of which is the apparently sophis- and lower-FF groups, we must recognize that each kind of ticated manner in which they manage their social relationships group offers opportunities for new skills to develop but also over both space and time (de Waal and Tyack 2003a). They for certain selection pressures to be relaxed. We should there- each have particular evolutionary histories and share a num- fore not assume that one kind of group necessarily produces ber of characteristics (e.g., slow life histories and long devel- greater cognitive abilities or “social intelligence” than another. opmental periods), any and all of which may have influenced With this in mind, we can formulate a framework regarding their cognitive abilities. Living in higher-FF groups, therefore, the cognitive demands that the sociospatial flexibility of dif- may be not a causal factor but simply a correlate of enhanced ferent fission-fusion dynamics may impose and use this to brain power. develop testable hypotheses. Even if living in higher-FF groups has evolutionarily con- The degree of fission-fusion dynamics experienced may sequences, its effects may well be contingent on what evo- make different demands on the various cognitive processes lution was given to work with in the first place. When con- involved in the acquisition, storage, processing, and use of sidering the whole array of species living in higher-FF groups, social information. At present, it is not clear whether any as in the case of communication discussed above, we need to cognitive abilities are unique to higher-FF taxa, although var- recognize the variation in cognitive abilities among these spe- ious suggestions have been made (Barrett, Henzi, and Dunbar cies, which is strongly dependent on the phylogenetic route 2003; Boesch and Boesch-Achermann 2000; Dunbar 2003; by which a social organization with a higher degree of fission- Milton 2000; Skoyles and Sagan 2002), and it seems most fusion dynamics was achieved. For example, the ancestors of parsimonious to assume that we are dealing with relative en- modern chimpanzees were likely group-living primates with hancement of certain cognitive abilities rather than a suite of the cognitive abilities to weigh the costs and benefits of in- new skills. teracting with multiple group members in ways dependent Living in lower-FF groups may impose greater demands on on current circumstances (route A in fig. 3). This capacity information acquisition than living in higher-FF groups be- could then be used in the fission-fusion context characterized cause normally there are more group members present (and by broader temporal and spatial scales. In this respect, chim- for longer periods) in the former than in the latter. Thus, panzees stand in contrast to some other primates, like galagos, members of lower-FF groups are constantly bombarded with which have moved during their evolutionary histories from social information that often involves multiple partners en- a solitary state toward a more social state in higher-FF groups gaged in fast-paced interactions. It is even possible that mem- (route B in fig. 3; Bearder 1999). In these cases, it is a matter bers of lower-FF groups cope with such massive amounts of not of employing an already existing set of social skills in a social information by paying selective attention to certain new context but of developing them de novo. We should not stimuli and filtering out redundant or unnecessary infor- assume, therefore, that a higher degree of fission-fusion dy- mation. By contrast, individuals living in higher-FF groups may display an enhanced ability to pick up subtle social cues 4. Filippo Aureli, Josep Call, Richard Connor, and Kay Holekamp (in and to use behaviors designed to probe others and extract alphabetical order) have principal responsibility for this section. relevant information from them (e.g., behaviors designed to

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 637 test bonds; Zahavi 1977). These enhanced information ac- such information “off-line” may be reduced by the increased quisition skills may allow individuals to detect altered rela- likelihood of witnessing interactions between dyads. Further- tionships among individuals who have temporarily been in a more, in taxa in which fission-fusion dynamics involve parties different party (Connor 2007). Among higher-FF taxa, these of mostly fixed composition (e.g., the joining and splitting of abilities are likely more important where party composition stable one-male units of hamadryas baboons), cognitive de- is highly variable (e.g., chimpanzees) than where the majority mands can be reduced by forming equivalence classes (cf. of social interactions take place within parties with mostly Schusterman, Reichmuth Kastak, and Kastak 2003). For ex- fixed composition, although such parties fission and fuse with ample, it would be easier to remember that “party X” was others to form multilevel societies (e.g., hamadryas baboons). present during an interaction than to remember the presence The storage and processing of information appear more of individuals A, B, C, D, and E. demanding in higher-FF than in lower-FF groups. This is a Cognitive demands can also be reduced if assessment and direct consequence of the patchier information gathered by updating of social relationships with various partners are individuals in the former. At the most basic level, these in- achieved via emotional mediation, which is based on the emo- dividuals must remember the members of their own group tion experienced when partners interact and the role of part- for longer periods because they are not exposed to them con- ner-dependent emotional experience in guiding future inter- tinuously. Moreover, because of changing party composition, actions (Aureli and Schaffner 2002). Under this scenario, these individuals have to keep track not only of who was individuals’ behavior toward other animals may reflect an involved in a particular interaction but also of who else was emotional response akin to Damasio’s (2004) “somatic mark- present (or absent) at the event. There is some evidence sug- ers,” which guide current action by producing a positive or gesting that chimpanzees can encode who witnessed an event, negative “gut feeling” about another individual based on both such as a particular food-baiting episode (Hare, Call, and experienced and observed interactions involving that individ- Tomasello 2001), but comparative systematic data are needed ual. This emotional response reflects the nature of past infor appropriate testing of this hypothesis (and the other hy- teractions but does not require any active recollection of them potheses below). or indeed any conscious cognitive response at all, merely a The dispersed nature of higher-FF groups in space and time linking of a particular individual and situation with a partic- may have favored an ability to encode information concerning ular emotional experience. Compared with lower-FF taxa, who was involved in what interaction and to remember such emotional mediation in higher-FF taxa should be based on a knowledge over longer periods than would be needed in lower sample size of direct observations (because they do not lower-FF groups. Renegotiating important long-standing re- witness all interactions of others) and on more indirect evi- lationships (sensu Kummer 1978) because individuals have dence (e.g., detectable changes in the behavior of others to- forgotten where they stand with respect to each other is waste- ward a particular individual after fusion). ful of both time and energy. Selection should therefore favor Finally, information should be put to good use, and we can individuals living in higher-FF groups who are able to retain also hypothesize possible differences in this regard between knowledge about partners (and their relationships with oth- higher-FF and lower-FF taxa. Owing to the changing oppor- ers, i.e., third-party relationships) over a long period, even in tunities of social partners in higher-FF taxa, individuals may the absence of those partners, so that they can “pick up where possess an enhanced capacity to inhibit and control their they left off” when they meet again. responses. For example, given that the appropriate response The patchy nature of information gathered by members of higher-FF groups may also promote enhancement of various to a situation may vary depending on party composition, the information-processing skills. Inferential skills may enable an- capacity to inhibit responses under less favorable conditions imals to extract information about relationships among others should prove selectively advantageous. Thus, inhibiting pre- from cues based on limited dyadic and triadic observations, potent responses, assessing a situation before acting, and pos- which may be particularly important when not all interactions sibly concealing changed relationships at reunions would all can be witnessed. For example, spotted hyenas use transitive be expected to be enhanced in taxa experiencing a higher inference very effectively in social situations (Engh et al. 2005). degree of fission-fusion dynamics. Japanese macaques provide Thus, although transitive inference is not exclusive to higher- an illustrative example of how members of lower-FF groups FF taxa (e.g., pinyon jays; Paz-y-Minõ et al. 2004), we predict may react to sudden changes in group composition without its enhancement in higher-FF taxa. showing appropriate behavioral inhibition. High-ranking ju- It is also possible that, for some higher-FF taxa, the ability venile macaques whose relatives have been removed from the to understand relations between relations (analogical reason- group invariably continued to challenge subordinate animals ing) will be enhanced. This can act as a way of reducing with intact matrilines (Chapais 1992). This led to the high- cognitive demands while enhancing cognitive capacity (e.g., ranking juveniles losing their dominance rank as a result of by storing information on particular kinds of relationships the lack of support from their absent relatives. Chimpanzees, rather than retaining knowledge of many specific individual in contrast, seem to be able to inhibit aggressive behavior interactions; Call 2001). In lower-FF taxa, the need to store under challenging conditions (Aureli and de Waal 1997). As

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 638 Current Anthropology Volume 49, Number 4, August 2008 mentioned above, comparative systematic data are needed for questions at present; our intention, rather, is to develop a appropriate testing of this and other hypotheses. framework that identifies issues that need to be explored in The particularly fluid nature of higher-FF groups also may order to provide those answers. allow individuals to model the future and optimize social outcomes in many situations. For these individuals enhanced Human and Ape Social Systems Compared planning skills could be especially beneficial by enabling them to “engineer” party composition and associate with the most The social systems of great apes and humans share a low level profitable partners. Chimpanzees seem to display such plan- of spatial cohesiveness but strongly developed social relation- ning skills during boundary patrols, territorial incursions, and ships (quadrant IV in fig. 4). Orangutans are clearly the least cooperative hunting (Boesch and Boesch-Achermann 2000; cohesive of the apes, but they are known to aggregate more Wrangham 1999). There is also some indication of planning when ecological conditions are favorable, and there appears for future needs from tool use experiments in bonobos and to be some form of a community (Delgado and van Schaik orangutans (Mulcahy and Call 2006) and from the selection 2000). Even the generally cohesive gorilla groups may be part of the most helpful partners in a cooperative task in chim- of some form of multilevel society (Bradley et al. 2004). Our panzees (Melis, Hare, and Tomasello 2006). In addition, fur- closest relatives, chimpanzees and bonobos, whose physiology ther cognitive demands can be encountered when individuals and food choice are more comparable to those of humans, are in parties of varying size and composition because of a have a social system with a high degree of fission-fusion dy- biological market of exchanges (Barrett, Henzi, and Dunbar namics but also a very high level of cooperation and affiliation 2003; see CAϩ online supplement H). within communities. Bonobos differ from chimpanzees In conclusion, if different degrees of fission-fusion dynam- mainly in having slightly larger party sizes and a generally ics make characteristic cognitive demands on animals, then higher level of spatial cohesion. In addition, while male al- we should expect to see enhanced abilities of the kind de- liances are important in chimpanzees, female alliances and scribed above in higher-FF taxa compared with closely related male-female alliances are more important in bonobos (Hoh- taxa living in lower-FF groups. Empirical evidence for such mann and Fruth 2002; Parish and de Waal 2000). For sim- a difference in demands and enhanced abilities is clearly plicity, we limit our framework mainly to a comparison be- needed. Our framework provides guidance on how to gather tween early humans and chimpanzees (including bonobos, such evidence and how to carry out “fair” tests to probe these unless stated otherwise). abilities. In other words, species-appropriate tests should be Humans and chimpanzees share a number of features (see implemented to reflect the potentially different phylogenetic also Layton and Barton 2001; Moore 1996; Nishida and routes to fission-fusion dynamics and their different under- Hiraiwa-Hasegawa 1987): an omnivorous diet associated with lying brain substrates. cooperative hunting, tool use (though cooperative hunting and tool use may not apply to bonobos), large community Implications of Fission-Fusion Dynamics size, and higher-FF groups within the context of a multimale/ for the Evolution of Complex multifemale social organization. There are also a number of 5 shared features that are expressed differently in the two taxa: Human Societies sexual division of labor (only in humans does this entail a Modern humans (and particularly modern foraging peoples; form of mutual dependence), hunting (meat sharing occurs Marlowe 2005) offer what is in many ways an archetypal in both chimpanzees and humans, but only in humans do example of a higher-FF taxon. We therefore build on issues we see prey killed elsewhere and brought back to a camp for raised in the preceding sections to investigate how human distribution), and flexible territoriality. To compare chim- society—characterized by well-structured social relationships panzees and modern humans regarding territorial tendencies, but with a low level of spatial cohesiveness during the day— we first need to understand the phylogenetic connection be- may have evolved. In trying to understand the origins and tween human and chimpanzee grouping patterns. If the hu- evolution of human society, we can usefully ask four ques- man band (i.e., overnight camp) corresponds to the chim- tions: (1) To what extent does human society differ from that panzee community, then the territoriality is more relaxed in seen in other anthropoid primates (in particular, in chim- modern humans than in chimpanzees. In many hunter- panzees)? (2) By what evolutionary route did modern human gatherer societies, adult humans of both sexes can readily social systems evolve? (3) What function(s) do higher-FF move (temporarily or permanently) between bands (e.g., Lee groups have for hominids? (4) What cognitive demands do 1979, 42; Turnbull 1965, 96; Woodburn 1982, 435). However, higher-FF groups impose on humans? We do not believe that if the regional hunter-gatherer community (commonly as- it is possible to provide definitive answers to any of these sociated with a unique dialect) corresponds to the chimpanzee community, then territoriality of modern hunter-gatherers is 5. Amanda H. Korstjens, Robert Layton, Carel P. van Schaik, Chris- more comparable to that of chimpanzees. Relations between tophe Boesch, and Robin I. M. Dunbar have principal responsibility for regional communities are more constrained (e.g., Andrews this section. 1996), although exchange across community boundaries does

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 639 occasionally take place (e.g., McBryde 1978). When we as- path in which a chimpanzee-like hominid ancestor, with a sume that chimpanzee communities should be compared to low degree of spatial cohesiveness but highly structured social regional communities (and the cognitive evidence suggests relationships, started to exploit not just forests but also more that this is the correct equivalence; Dunbar 1993), then hu- open savannah/woodland environments. In such environ- man social evolution has moved toward longer-term associ- ments, daytime food-searching demands required individuals ation in subunits (i.e., subunits have become more stable). to forage in small parties, as do contemporary chimpanzees Finally, human societies differ from those of apes in a num- in forested habitats and baboons in dry savanna habitats ber of respects: the recurrent assembly of subunits at an over- (Nishida and Hiraiwa-Hasegawa 1987; Stammbach 1987). night base camp, the presence of social and economic pair However, some variable—most likely the rarity of essential bonds, significant alloparental inputs in child rearing, ex- resources such as safe refuges at night (with an increased risk change of goods as tokens of social relations, and, perhaps of predation in the more open habitat) or waterholes (scarce rather obviously, the use of language in regulating relation- in savannah habitats but less so in forests)—forced individuals ships (see also Dunbar 1993; Marlowe 2005; Rodseth et al. to aggregate once a day in large groups that contained the 1991). These differences are numerically and qualitatively suf- entire band or community, as happens in hamadryas baboons ficiently large that they are unlikely to have arisen at the same (Stammbach 1987) but not in contemporary woodland and time, which raises the second issue of our framework: how forest chimpanzees (Nishida and Hiraiwa-Hasegawa 1987). were these differences acquired in the hominid lineage? Coming together at night and at waterholes is not the only difference in fission-fusion dynamics between chimpanzees and baboons: they also differ in the types of parties that are Phylogeny and Function for Human Higher-FF Groups commonly formed. As discussed earlier, in hamadryas ba- At present, we can say little about the sequence of specific boons large night aggregations split into smaller foraging par- events that occurred in the hominid lineage, but it is likely ties based on one-male units during the course of the day, that human higher-FF groups derived from group-living spe- whereas in chimpanzees community members are very rarely cies that depended on cooperation and had various social all together and form parties rather independently. This dif- skills (e.g., conflict resolution [Aureli and de Waal 2000] and ference can have a major impact on the level of cooperation alliance formation [Harcourt and de Waal 1992]) useful for among community members. A chimpanzee-like system may maintaining social relationships in spite of low spatial co- be more conducive to cooperation (as seen among chimpan- hesion (route A in fig. 3). The best we can do is to assume zee males during hunting of difficult prey and border patrols) that whatever chimpanzee and bonobo societies have in com- than a hamadryas baboonlike system because all members of mon with those of modern humans resembles those of their a chimpanzee community may regularly interact affiliatively common ancestor (Moore 1996) and then ask what changes when they meet in different parties. In a baboonlike system had to be made and in what sequence in order for the dif- individuals always remain in the same party (at the smallest ferences to develop. Because these changes are inevitably unit level), and there is little affiliative interaction between linked to the function of fission and fusion, the third question members of different parties. of our framework is embedded in the discussion below. We do not know what kind of aggregation or dispersal Most of the differences we have listed between chimpanzee behavior may have occurred among australopithecines, but and human societies are unique features of humans and prob- most paleoanthropologists agree that australopithecines were ably evolved fairly recently in human evolutionary history. highly sexually dimorphic (similar to baboons) and that, The use of sites where the community aggregates at night (i.e., therefore, neither a chimpanzee-like social system nor one a possible precursor of home bases), however, is common in approximating that of modern hunter-gatherers was found many primates (although not in chimpanzees or bonobos). among them. Rather, intermale competition may have been The use of a limited number of sleeping sites is driven by as strong as it is in baboons (Foley and Lee 1989; Plavcan predation pressure and the availability of safe refuges that are and van Schaik 1997), which tends to reduce levels of co- large enough for the group (Anderson 2000). If the society operation among males. Indeed, what was once thought to has a relatively low level of spatial cohesiveness, a lack of safe be evidence for “home bases” among early Palaeolithic hom- sleeping sites or extreme predation risk may force the group inids is now discounted because the accumulations of tools members to come together at night. Such a situation is es- and bones are considered to have been caused by transport pecially obvious in hamadryas baboons (Kummer 1995), in streams or flash floods (Binford 1987; Stern 1993). All we though similar patterns may be seen in all Papio baboons. can say at this stage is that the typical chimpanzee strategy The fact that baboons live in as large a variety of habitats as of building nests wherever individuals happen to find them- our earliest ancestors did (from rain forests to open savannah selves at nightfall would have been constrained by the areas), including more open and drier habitats than those occurrence of fewer suitable sites in more open savannah/ where modern chimpanzees occur, seems relevant, given that woodland environments. We stress nonetheless that this hy- Papio and our earliest ancestors emerged at about the same pothetical formation of large groups at least once a day at a time (Jolly 2001; Moore 1996). We envisage an evolutionary safe location would, in a society in which cooperation is com-

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 640 Current Anthropology Volume 49, Number 4, August 2008 mon, offer a whole new set of opportunities, especially for a each individual’s behavior while the group is dispersed. Com- large-brained primate like our ancestor. Some of the benefits ing together daily not only allows individuals to reinforce of aggregating once a day do not require anything as advanced bonds but also provides opportunities to observe the social as a home base—only that individuals spend a relatively long interactions taking place among other individuals (and thus period of social time in each other’s presence while not en- update reputations) and additionally forces individuals to re- gaged in activities such as foraging, hunting, or patrolling solve conflicts in order to reduce tensions in the group instead their boundaries. of simply avoiding one another. In combination with the As the daily aggregation at a safe limiting resource evolved cognitive abilities of great apes and their tendency toward into a home base in later Homo species, fusing at nighttime complex social relationships, this could have been the point may have offered the opportunity for sexual division of labor, of departure for the high level of cooperation and the evo- whereby gatherers and hunters shared their spoils at the end lution of complex symbols to indicate intentions that we ob- of the day (Key and Aiello 2000). Some degree of resource serve in hominids. Social learning and information exchange redistribution would have been allowed by alloparenting at these daily gatherings are likely to have increased the de- (Kennedy 2003), costly signaling by males, and perhaps pair velopment of a society with highly structured social relation- bonding; the latter could have allowed pooling of resources ships and elaborate signals. Even though the original need for within a domestic unit in a context in which confidence in fusing on a daily basis may have disappeared as hominids reciprocity of food transfers was maximized (a feature that came to occupy various environments, the other benefits of may have been reinforced or actively selected for by the pa- doing so may have been the evolutionary adaptation that rental investment demands of increasing brain size; Key and allowed our ancestors to become a highly adaptable species, Aiello 2000). Because the weakest individuals no longer had capable of spreading across the world. to leave the safety of the home base to forage, the home base would presumably have increased the survival chances of the Conclusions weakest individuals (e.g., young children, older people, women with newborns, and heavily pregnant women), who The five interlinked sections of this article propose several could nonetheless have performed essential tasks there such new frameworks within which to pursue research on a range as child care. At this stage, the sharing of spoils means that of topics that we believe are particularly relevant to fission- individuals in the community could distribute themselves op- fusion dynamics. In the years since the term “fission-fusion” timally over the area to increase efficient use of resources. was first introduced (Kummer 1971), research in this area Eventually, this could have given rise to the multilayered so- has been rather patchy and has focused on only a limited ciety of modern hunter-gatherers, in which survival risks were number of topics. For example, significant methodological further reduced through cooperation between different bands improvement for the recognition of nonrandom association in the form of trading and allowing some trespassing onto patterns has been made (supplement A), and several socio- each other’s territory (Klein 1999; Layton and Barton 2001). ecological factors influencing party size have been identified Many of these latter changes imply significant demands in (e.g., Chapman, Wrangham, and Chapman 1995; Lehmann terms of social skills and may have selected for the evolution and Boesch 2004; Mitani, Watts, and Lwanga 2002). Less at- of larger brains (see CAϩ online supplement I for archeo- tention has been paid to other aspects of fission-fusion dy- logical evidence). namics, such as the rate of change in party size or the extent to which parties, when they do form, are composed of the same set of individuals. Cognitive Demands of Human Higher-FF Groups A possible reason for the lack of more systematic investi- This leads us to the last of the four questions of our frame- gation of fission-fusion dynamics is the tendency for re- work, because the scale of human social groups (and, in par- searchers to adhere to a dichotomous perspective on flexible ticular, the size and dispersion of forager communities,in versus cohesive organizations and to focus on the so-called combination with a gathering at home bases) must inevitably fission-fusion societies of chimpanzees and spider monkeys. impose considerable demands on human cognition (Aiello We believe that much progress can be achieved by acknowl- and Dunbar 1993). We would simply stress that a high degree edging that this is a false dichotomy and by recognizing that of fission-fusion dynamics may be cognitively taxing and, fission-fusion dynamics occur to some extent in most social without the gathering of individuals at night, may undermine systems (cf. Kinzey and Cunningham 1994; Strier 1989; high degrees of cooperation for two reasons. First, fission- Struhsaker and Leland 1979; Sussman and Garber 2007). We fusion dynamics do not allow for regular updating of infor- reiterate, therefore, that a starting point for a renewed research mation about social relationships in the community, and this input is the adoption of a relativistic approach that places makes it more difficult for individuals to depend on a rela- species—and even populations of the same species—within tionship when individuals are spatially dispersed. Second, reg- a complex, multidimensional fission-fusion space of the sort ular fission and fusion creates opportunities for free riders illustrated in figure 1. Higher- and lower-FF groups refer to (Enquist and Leimar 1993) because it is impossible to monitor relative positions within such a space, and comparisons be-

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 641 tween taxa and populations need to be interpreted within this cognitive abilities, depending on their degree of fission-fusion framework. dynamics. Because higher-FF groups occur in a wide variety A second critical point we have stressed is the pressing need of taxa, a broad comparative perspective, not limited to pri- for primatologists—and other researchers interested in the mates, should help elucidate underlying principles and also evolution of flexible patterns of social organization—to de- highlight fundamental differences due to evolutionary history. velop new null models against which the associations of in- This perspective could also be highly beneficial in increasing dividuals can be compared. The generalized modeling frame- our understanding of the causes of the variability in human work of spatially explicit agent-based simulation is a powerful fission-fusion dynamics and the evolution of our complex tool that can be applied to many different taxa. Another crit- societies. ical point emphasized in our frameworks is that the evolutionary route followed to reach a given degree of fission-fusion Acknowledgments dynamics has fundamental implications for the types of social and cognitive skills the organism may possess. This means The Wenner-Gren Foundation for Anthropological Research that two species that lie relatively close to one another in the and Ethoikos financially supported the organization of the multidimensional fission-fusion space may nonetheless differ workshop where most of the ideas for the paper were dis- in important respects depending on their phylogenetic back- cussed and developed. We are especially grateful to Roberto ground. Thus, interspecific comparisons need to take evo- Cozzolino and his team for the smooth running of the work- lutionary history into account (Pagel and Harvey 1991; Nunn shop at the Convento dell’Osservanza, Radicondoli, Italy. We and Barton 2001). also thank ten anonymous reviewers for comments. During The relativistic approach based on the degree of fission- the writing of this paper, F.A. was supported by a Higher fusion dynamics within such an evolutionary framework pro- Education Funding Council for England Promising Research vides an effective way to evaluate patterns of communication Fellowship and R.I.M.D. by a British Academy Research across taxa. Given similar differentiation of social relation- Professorship. ships, we expect that communication in lower-FF groups will be focused on coordinating movement, resolving conflicts, and promoting cooperation, whereas the communication systems of higher-FF groups must accommodate the additional Comments requirements of routinely negotiating separations, reestablish- ing relationships, and reducing tension at reunions. In ad- Christopher Boehm dition, while carrying out comparative analyses, we need to Departments of Anthropology and Biological Sciences, be aware that higher-FF groups may have evolved either from University of Southern California, Jane Goodall Research rather solitary species with limited social skills or from rel- Center, Social Science 154, Los Angeles, CA 90089–0032, atively cohesive groups that already possessed effective means U.S.A. ([email protected]). 15 IV 08 for maintaining differentiated relationships. Furthermore, despite the fact that many animals living in higher-FF groups Customarily, anthropologists describe the social organization have large brains and sophisticated cognitive abilities, we sug- of extant mobile foragers with fission-fusion “bands” as the gest that a higher degree of fission-fusion dynamics does not main focus, noting that bands may dissolve into families (see necessarily impose selection pressures that promote the evo- Gould 1982). Multifamily bands form because of human gre- lution of novel forms of “social intelligence.” However, evo- gariousness and cooperation around large game (Kelly 1995), lutionary enhancement of existing cognitive skills may in- with frequent interchange of personnel between bands. Re- crease fitness in higher-FF taxa and thus promote cognitive gional networks (Wobst 1978), which Aureli et al. compare attributes such as long-term memory about who did what to to chimpanzee territorial communities, are relatively ne- whom and the inferential abilities necessary to put together glected. I believe this analogy is somewhat oversimplified. patchy social information. Finally, the nature of fission-fusion The most basic unit in these regional networks is not the dynamics of early hominids, in particular the suggested com- multifamily band but a pair-bonded family, which is lacking bination of both a high degree of interaction among com- in great apes. Such networks are readily describable (Schweit- munity members due to frequent changes in party compo- zer and White 1998); for example, Wiessner’s (2002) analysis sition and a tendency to reunite on a daily basis, may have of Xharo exchange deals with regional personal trading net- strongly influenced the evolution of the highly adaptable and works that enable families to seek refuge with related or un- cognitively sophisticated species that we are today. related families in distant bands in times of localized scarcity. Given these premises, the proposed frameworks we ad- This applies to a !Kung “territorial structure,” which seems vocate here are expected to stimulate new momentum in the far less xenophobically driven than that of chimpanzees or investigation of whether qualitative or quantitative differences even bonobos. Similar patterns are documented in less detail in fact exist between species or populations in the underlying for Australia (see Lourandos 1997). In contrast, Burch’s socioecological conditions, communication skills, or required (2005) analysis of the In˜upiaq in northwestern Alaska de-

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 642 Current Anthropology Volume 49, Number 4, August 2008 scribes a similar regional safe-haven network in which territorial tendencies are expressed much more strongly than in Patrıćia Izar chimpanzees: local groups make genocidal attacks against en- Institute of Psychology, Department of Experimental emy bands, yet widespread familial networks based on mar- Psychology, University of Saõ Paulo, Avenida Professor riage alliances and trading partnerships exist. Mello Moraes 1721, Cidade Universitaria, Saõ Paulo CEP Aside from the transfer of females, chimpanzee commu- 05508-030, Brazil ([email protected]). 31 III 08 nities have only hostile relations with neighbors. In contrast, Since the 1960s, primate socioecologists have repeatedly at- the genocidally warlike In˜upiaq have developed a special fu- tempted to classify the diversity of primate social systems into sion process that allows friendly and hostile bands alike to discrete categories or modal types according to features of unite temporarily: annual trade fairs permit exchange on a social organization, mating system, and social structure (Kap- wide regional basis and can involve more than 1,000 people. peler and van Schaik 2002). Each new classification system is This is enabled through three-week truces that suspend the eventually challenged by the information arising from long- ongoing genocidal fighting between bands. term field studies (Boinski 1999; Isbell and Young 2002) that Thus, we may need a more flexible and complicated notion is at variance with key components of the model. For instance, of social “fissioning and fusion” when it comes to mobile Crook and Gartlan (1966) proposed the first classification of foragers. While not all Holocene foragers face the Kalahari primate social systems into nocturnal solitary species, forest or In˜upiaq type of microecological unpredictability that stim- diurnal species with small social groups, savanna species with ulates their safe-haven networking, such challenges were prob- large permanent groups, and desert species with large mul- ably much more pervasive and threatening in the Pleistocene. tilevel societies. In addition to other flaws, this scheme did Another, universal challenge is the need for political safe ha- not contemplate the diurnal forest species of New World mon- vens. The cause is homicidal quarrels, and they predictably keys that may live in very large groups (Janson 2000). In the cause the killers’ families to fission from one band and fuse same way, Wrangham’s (1980) proposed dichotomous cate- with another. Protracted visits with relatives and in-laws are gorization of primates into female-bonded and non-female- another candidate for universality. bonded species did not accommodate data from several newly The chimpanzee/bonobo model lacks families with paren- studied species; it subsequently gave place to a model pre- tally investing fathers even though matricentric social units dicting four types of social systems (Sterck, Watts, and van exist, and in chimpanzees they sometimes can transfer to the Schaik 1997). Ten years later, the time is now ripe for Aureli mother’s natal group. In studies of the evolution of fission- and collaborators’ claim that, at least for the social organi- fusion groupings in humans, the basic family units are based zation component of social systems (Kappeler and van Schaik on long-term bonding and parenting by both parents, and 2002), we must abandon fixed labels for describing the ob- such families are free to associate with other congenial families served social organization of different primate species or even within the same cultural region. This is a major difference. populations. Politically, chimpanzee communities never form alliances In the first part of their work, the authors expanded the against other communities even though within their groups idea of a continuum of sociality proposed by Lee (1994), ranging from solitary species to four types of group-living coalition behavior is normal. Likewise, mobile hunter- species characterized by the frequency of association between gatherers are not at all prone to form political alliances be- the same individuals. One of the major contributions of Aureli tween territorial units—even though after the Holocene began et al.’s conceptual framework is the proposal that specific tribal humans with agriculture regularly did this, as do mod- dimensions of spatiotemporal associations among individuals ern nations. Thus, factors such as demographics, subsistence, vary in a scalar rather than a categorical manner. This frame- and cultural lifestyle would appear to influence the expression work would be useful for understanding the recently reported of our capacity for political fission and fusion. variability in group cohesion of two wild populations of tufted The authors of this article have proposed a processual ap- capuchin monkeys Cebus nigritus (Izar and Nakai 2006; proach that looks to fission-fusion dynamics, and overall this Lynch-Alfaro 2007). First, we could abandon tentative labels approach does seem potent for humans. I would add that for describing the variability in spatiotemporal association multiple analytical perspectives may be needed for humans among group members, such as subgrouping behavior in particular, because not only individuals but also male- (Lynch-Alfaro 2007) or fission and formation of new groups female nuclear families are basic units, because we engage in (Izar 2004), and assume that we are observing the fission- trade and offer safe havens, and because even hostile territorial fusion dynamics of these populations. This is not just a matter communities are capable of fusion, whether in trade fairs or of semantics; it is the realization that these populations express through expedient political alliances between groups. Needed the same behavioral phenomena in variable degrees rather to explain these phenomena are both “group” and “network” than presenting unusual types of social organization. In a brief approaches that, as the authors imply, should look at least as attempt to compare published data on these two populations much to processes as to structures. (Lynch-Alfaro 2007; Izar et al. n.d.) with respect to the tem-

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 643 poral variation in spatial cohesion, party size, and party com- animals are available for only a handful of species, including position, as proposed by Aureli et al., it was possible to identify a few primates. a difference between the two populations in the degree of Aureli et al. report the outcome of a workshop on fission- temporal variation in party composition, although they fusion dynamics in primates. Their paper provides us with seemed to be similar with respect to temporal variation in new ideas about the potential evolutionary routes leading to spatial cohesion. groups with fission-fusion behavior, suggests a new termi- The second part of Aureli et al.’s work can be helpful in nology, and outlines research areas (communication, cogni- answering questions about why these particular populations tion) in which the study of fission-fusion behavior can add of C. nigritus show a higher degree of fission-fusion dynamics to our understanding of complex societies. They focus on than the majority of Cebus species studied so far (Fragaszy, humans and nonhuman primates, but their ideas also apply Visalberghi, and Fedigan 2004; see Aureli et al.’s section on to other animals that exhibit fission-fusion behavior. I will the implications of fission-fusion dynamics for communica- therefore comment on their paper from the perspective of a tion), including other populations of C. nigritus (e.g., Di Bi- behavioral ecologist whose research deals with the causes and tetti 2001). I agree with the authors that it is time to reevaluate consequences of sociality in bats, a group of mammals in post hoc assumptions of traditional socioecological models. which fission-fusion behavior is particularly common (Kerth It will be fruitful to develop computer models that can be 2008). run repeatedly (in simulations) to test how often the actual One of the most exciting questions in the context of fission- observed behavior would result as a function of the param- fusion dynamics is whether fission-fusion behavior requires eters included. Their suggestion of using agent-based simu- special communication, decision-making, and cognitive skills lation models seems promising and echoes the recommen- (Conradt and Roper 2005; Kerth, Ebert, and Schmidtke 2006). dations of several other researchers of primate behavior (e.g., Aureli et al. do not deal with group decision making, but they Hemelrijk 2002; Bryson, Ando, and Lehmann 2007; Sellers, address the question of whether species that live in groups Hill, and Logan 2007). with frequent fission-fusion events require communication In the last three sections Aureli et al. hypothesize about and cognition skills different from (and possibly more ad- possible consequences of fission-fusion dynamics in the evo- vanced than) those of species that live in more cohesive lution of communication and cognition in primates as well groups. Aureli and coauthors identify a variety of potential differences but also remind us that the evolutionary route as in human evolution. It is worth emphasizing that the au- that has led to groups with particular fission-fusion dynamics thors circumvent a flaw of past socioecological models in that may be as important as the current social organization of a they do not underplay the influence of phylogeny on primate species. Their remark that the relative importance of phylo- behavioral features (Di Fiore and Rendall 1994; Janson 2000). genetic constraints and recent fission-fusion dynamics can be The validity of hypotheses will be evaluated through future addressed only with comparative studies that correct for phy- research, but, as pointed out by the authors, these sections logenetic inertia is on the mark. It also needs to be stressed have heuristic value and may stimulate new studies on primate that, owing to the limited data available for primates, such behavior. an approach can be successful only if it includes nonprimate mammals that show fission-fusion dynamics, such as bats, ungulates, and whales. The widespread occurrence of fission- Gerald Kerth fusion behavior in mammals (Kerth 2008) suggests that Department of Ecology and Evolution, University of this behavior has evolved independently many times. This Lausanne–Biophore, CH-1015 Lausanne, Switzerland allows for studying the evolutionary relationship between ([email protected]). 27 III 08 fission-fusion behavior and cognitive/communication ability. Whereas communication can be studied directly in the field, Fission-fusion behavior, which describes the temporary split- neocortex and total brain size may be used as correlates for ting and reformation of groups, is widespread among animals, cognitive abilities (Deaner et al. 2007). If fission-fusion be- occurring in social insects, fish, birds, and mammals, includ- havior requires special cognitive skills, species that differ in ing humans. Understanding the fission-fusion dynamics of their extent of fission-fusion behavior may also differ in their groups is important because the extent to which groups can brain morphology. temporarily split into smaller social units has far-reaching Species with fission-fusion behavior also provide us with consequences for the social organizations, mating systems, opportunities to study the effect of fission-fusion dynamics and social interactions of species. Consequently, increasing on group decisions, which are central elements of human and numbers of evolutionary anthropologists, behavioral ecolo- nonhuman societies (Kerth, Ebert, and Schmidtke 2006; Kerth gists, and sociobiologists interested in the functioning of com- 2008). For individuals that disagree about an action, one al- plex societies have started to study the causes and conse- ternative is to avoid a consensus and temporarily split into quences of fission-fusion behavior. At present, however, subgroups that better represent their preferences. This option detailed data on the fission-fusion dynamics of free-ranging has largely been neglected in studies on group decision making

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 644 Current Anthropology Volume 49, Number 4, August 2008 or has been treated as a nonadaptive outcome. However, the point? Such questions obviously are best answered by exper- ability or inability of members to temporarily avoid group iments. The article does not treat these questions in any detail, decisions that are not in their favor should strongly affect the possibly because the authors found only marginal attention way group decisions are made (Conradt and Roper 2005; among primatologists in the past, in contrast to the outstand- Kerth, Ebert, and Schmidtke 2006). ing research on social foraging in hymenopterans. The ab- Aureli and coauthors do an excellent job of advocating the stract states that “any social system can be described in terms importance of studying fission-fusion dynamics and outlining of the extent to which it expresses fission-fusion dynamics” interesting research avenues, even without covering all im- (emphasis added). This is true, but in my assessment the plications in detail (mating systems, group decision making). “extent” or any similar quantification reflects a trivial con- However, their paper makes clear the need for more long- sequence of far more interesting social and cognitive abilities. term field studies on fission-fusion dynamics that combine Because the hamadryas study is probably one of the most detailed behavioral observations with knowledge on the de- thorough investigations of group decisions in primates, I shall mography and kinship of the studied individuals. Quantifying refer to some of their complexities. individual associations in fission-fusion groups with classical The question is how social motives of many individuals association indices (Whitehead 1999) and modern network interfere with the formation of ecologically adaptive parties. analyses (Krause, Croft, and James 2007; Wey et al. 2008) will Socioecological models analyze the interacting influences of tell us to what degree relatedness and shared interests (e.g., both factors. The model of Ramos-Fernandez, Boyer, and resulting from the same reproductive status, sex, age, or rank) Go´mez (2006) assumes that individuals may join and separate explain the fission-fusion dynamics and hence the social or- freely. It correctly describes the group sizes of spider monkeys. ganization of species (e.g., Kerth and Ko¨nig 1999; Connor Although the model allows social bonds, they do not seem and Whitehead 2005; Archie, Moss, and Alberts 2006; Smith, to prevent the free recombination of individuals. Memenis, and Holekamp 2007; Sundareasan et al. 2007). The stable subunits of hamadryas do not allow free vari- Studying fission-fusion dynamics in wild populations has im- ation of party compositions. Fine-grained observation de- portant implications for our understanding of how complex tected the social constraints, and experiments excluding eco- societies work in primates and other animals. logical influences identified their underlying mechanisms. At the lowest level, females of one-male units cannot leave and join another unit or move independently because they are Hans Kummer guarded by their males. A lactating female needing water can Grundrebenstrasse 119, CH-8932 Mettmenstetten, turn aside to a pool only if the male in front has noticed her Switzerland ([email protected]). 2 IV 08 intention movements and follows. Clans and bands cannot join bands of a foreign troop without risking extended fights This comment tries to bridge the 40 years since my colleagues (Kummer 1968, 1995). Bands of the same herd can fuse only and I analyzed the daily regrouping cycle of hamadryas ba- thanks to a triadic inhibition of rivalry over females (Kummer, boons and termed it a fusion-fission society. Methods and Go¨tz, and Angst 1974). emphases have changed since then (Kummer 2002). We were Leadership in hamadryas does not have to be concentrated not anthropologists but ethologists relying on fine-grained in one individual moving in front, nor is it always linked to observations and testing hypotheses by experiment. I welcome dominance. In a band or clan young dominant males take the comprehensive revival of the topic but also have some initiatives by sitting a few meters ahead of the group, often doubts. in diverging directions. One direction is eventually followed. Aureli et al. propose “the quantification of the relative de- Sometimes, old males who have already lost their females and grees of fission-fusion dynamics” by describing the degree of rank low in dominance do not agree, occasionally for reasons variation in party size, cohesion, and composition. Such de- even the observer understands. One of them then walks in a scriptive terms are of comparative interest, but they miss the new direction and is always and immediately followed by the core aspect of “dynamics.” Merging and splitting result from entire band, including the dominant males. movements of individuals following social and ecological mo- Sigg (1980) did a close study of free-ranging one-male units tives. These motives may conflict with each other, and they with only two females. The older and lower-ranking female will often conflict among individuals. While fusion and fission walks significantly farther from the male and is first to ap- are relatively simple processes, the transfers of leadership they proach and look beyond a horizon. The male observes her require can be very complex, as the hamadryas example taught more closely than he does his younger female. In enclosure us. We were soon involved in searching for the individuals tests these older females learned much faster than the younger that made decisions in this or the other process, by what ones which color of nails in the sand indicated buried food. actions they promoted their decisions, and who prevailed in In bands, as in one-male units, the baboons thus recognize the end. We began to ask: Can members of a party guess and follow competence rather than dominance. How they where others are or where they intend to go? Can they learn assess competence is not known. They may pool positive for- who is a competent leader? Can parties agree on a meeting aging experiences in a leader’s company or follow an indi-

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 645 vidual who strides with great determination to a resource it among field sites that would contribute to interspecific dif- has recently discovered. The latter could be experimentally ferences within and across taxa. Modeling strategies tend to tested with artificial water holes that are opened only in the assume that any data are better than none, even with a small presence of certain individuals. There is no obvious reason sample size. The latter can result from limited sampling of a that other primates with more flexible societies should not variety of taxa. For example, one small, mixed-sex feeding have equally interesting decision systems. party of a given species is randomly sampled and taken as representative of the whole taxon within the model’s framework and generated predictions. These predictions about the Mauricio Talebi taxon may persist in the scientific literature for years or even Animal Reproduction Department, Veterinary Medicine decades. In the meantime, underrepresented/unrepresented Faculty, University of Saõ Paulo, and Pro´-Muriqui taxa behave differently than predicted by the model. Conservation Research Society, Saõ Paulo, Brazil The feasibility of applying carefully designed frameworks, ([email protected]). 7 IV 08 such as those presented here, is indeed extraordinary but largely dependent on the large-scale collection of standardized Aureli et al.’s original and thoughtful contribution to both data on the full range of multiphyletic communities on small primatology and anthropology explores a broad range of phe- spatial scales. This is a mandatory first step for assessing the nomena underlying the complexity of fission-fusion dynam- robustness of the predictions generated by the proposed ics, a rare kind of vertebrate social system. The article proposes frameworks. Moreover, representative data collection through the use of new and integrative research frameworks for en- carefully designed and standardized protocols would avoid abling a more comprehensive and precise characterization of generating unrealistic patterns in taxa that inhabit remote/ fission-fusion dynamics in human and nonhuman-primate less studied/unstudied regions where field research is difficult societies. These frameworks combine methodological, theo- or complex to conduct. retical, and observational aspects of primate socioecology, Although seemingly obvious, the need for larger sample communication, and cognition. The article’s proposal of the sizes and greater taxon representation is critical in the study term “fission-fusion dynamics” is of wider significance be- of fission-fusion dynamics. Nonetheless, as these researchers cause this represents the complexity of both obtaining relevant state, the power of the modeling approach lies in its versatility, data and characterizing the precise contribution of variables/ because variables can be included or excluded and parameters events that underlie the observed social grouping patterns can be changed. Given the modeling premises, it seems rea- within/across vertebrate taxa. In addition, the proposal of new sonable to suggest that understanding of the principles that frameworks is an attempt to go beyond the lack of data for shape movement and grouping patterns in primates is de- advancing our knowledge of vertebrate social systems. Ade- pendent on the completion of comparative research specifi- quate paradigms to describe fission-fusion dynamics, in turn, cally designed for different taxa in the frameworks presented can be realistically established only through the use of inte- and the study of all of the species inhabiting different sub- grative and standardized research frameworks of data collec- environments, thus avoiding broad generalizations about taxa tion and analysis. Consequently, the current lack of adequate and their habitats. paradigms substantiates the authors’ provocative claims for a multidimensional integrative scenario in terms of socioecology, communication, and cognition. Furthermore, it repre- Juichi Yamagiwa sents the first combined approach to research on the puzzling Laboratory of Human Evolution Studies, Faculty of and complex fission-fusion social system. Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan The revaluation of past assumptions about the way eco- ([email protected]). 29 III 08 logical variables influence social systems through the use of agent-based modeling, communication signs, and quantifi- Aureli et al.’s paper attempts to move beyond the dichoto- cation of cognitive complexity is a fascinating and powerful mous distinctions between cohesive and flexible primate approach. These models aim for the construction of a fission- social organizations to propose a new conceptual framework. fusion continuum space in which species can be plotted and I agree with most of the authors’ arguments and proposals eventually ranked according to levels of responses to ecolog- for understanding the variation in fission-fusion dynamics of ical change, what I call “taxon dynamicity.” It is also impor- primate social evolution. Earlier concepts of primate socio- tant to ask how much information can be achieved from ecology have been criticized for their reductionist perspec- observing fission-fusion complexity through the use of a few tives, and sexual conflict or phylogeny, rather than ecological (even nondichotomous) variables while ensuring the internal constraints, is considered responsible for some patterns of and external cohesiveness of comparative data for supporting primate sociality. The authors of this paper take these debates the proposed frameworks. For example, a given tropical hab- into account in the new framework. My comments are con- itat comprises several ecologically differentiated habitats in cerned only with the adequacy of their discussions. which latitude differences produce ecological differences First, although the new set of null models proposed in this

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions 646 Current Anthropology Volume 49, Number 4, August 2008 paper succeeds in positioning the type of fission-fusion of families as its substructure. Such a multilevel society is more each primate species in three dimensions without using so- likely to have evolved from lower-FF groups with the pro- cioecological predictions, such classification does not ade- longed pair bond than from the chimpanzee-like community quately explain the relationships between types. The social characterized by promiscuous mating. The most notable fea- systems of groups having the same position are not necessarily ture of the human band is its high degree of fission-fusion affected by the same factors. It is unclear whether the con- at both individual and group levels, which is not found in tinuum of the three dimensions is reversible. As the authors the multilevel society of hamadryas baboons. The authors stress, these models should be used as tools for understanding regard australopithecines as highly sexually dimorphic (sim- the behavior of real animals rather than as actual descriptions. ilar to baboons), but recent findings suggest that they were It is important to incorporate various factors into these mod- similar to modern humans (Reno et al. 2003). In order to els in order to explain the degree of fission-fusion of each resolve the question how such a multilevel fission-fusion so- species exhibited in figure 1. ciety has evolved in the less sexually dimorphic hominin, Second, the authors simply reconstruct two evolutionary possibly with a prolonged pair bond, it is important to use scenarios of fission-fusion dynamics in primates (fig. 3), but phylogenetic reconstructions appropriate to the fossil evi- these scenarios need reliable explanations of the factors pro- dence at each phase of human evolution. moting each variable. As the authors hypothesize, the most primitive lifestyle of primates is a solitary one. Yet, primate groups always include both sexes even outside mating season, and, in contrast to the situation in most other mammals, neither solitary females nor all-female groups are found in Reply group-living primates. This may reflect contrasting strategies between sexes that are unique to primates. Figure 4 also lacks Our main aim was to propose new frameworks for the study sex-biased dispersal patterns of primates. There are two kinds of fission-fusion dynamics. We are pleased to have Kummer’s of dispersal in primate aggregation: (1) spatiotemporal dis- welcoming words for a comprehensive revival of the topic. persal and (2) prolonged dispersal from natal groups. This We recognized that important starting points for a renewed paper considers only the former, but the latter is also im- research impetus are the rejection of the false dichotomy be- portant because it may affect diachronic social changes. Bi- tween flexible and cohesive organizations and the adoption sexual groups of primates are classified into female philopatry of a relativistic approach. Fission-fusion dynamics occur to and female dispersal, either of which is highly conservative some extent in most social systems. in most lineages of primate phylogeny. Both gorillas and Ha- We are grateful to the commentators for their stimulating numan langurs form polygynous and cohesive groups, but comments showing how our proposed frameworks may be female gorillas emigrate from their natal groups, while female expanded in various directions. We find Izar’s enthusiasm for Hanuman langurs remain in them after maturity. This ex- applying our conceptual framework of spatiotemporal vari- ample shows that similar social structures can be supported ation and multidimensional fission-fusion space to the social by different types of dispersal and different strategies. In this dynamics of wild populations of tufted capuchin monkeys respect, behavioral comparison between lower-FF groups very encouraging. We hope that others will find our frame- and higher-FF groups should be made between closely related works useful for explaining the grouping patterns of their species with similar dispersal patterns. The authors should study species and integrating them with those observed in compare chimpanzees (female dispersal) not with Japanese different populations and different taxa. macaques (female philopatry) but with gorillas (female We are pleased to receive Izar’s and Talebi’s comments dispersal). supporting our proposal of reevaluating the assumptions of Third, the perspectives on fission-fusion dynamics for hu- traditional socioecological models by using spatially explicit man evolution in Aureli et al.’s paper are based on invalid agent-based simulations, and we agree wholeheartedly with debates from the past. Although humans and chimpanzees Yamagiwa’s remark that we need to incorporate multiple fac- share many features, chimpanzees have mating patterns that tors into null models of association. That is a point we tried are very different (apomorphic) from those of other great to make in our article. In fact, the flexibility of the agent- apes and humans. Conspicuous swelling of sexual skin, based approach makes it an especially powerful tool for ex- unique to Pan, is strongly linked with their promiscuous mat- ploring, in a controlled way, the influence of a range of factors, ing and fission-fusion features. This feature has evolved in at both individually and simultaneously. Yamagiwa remarks that least four different phylogenetic lineages of primates (Dixon the same position of different taxa in the three-dimensional 1983), and the common ancestor of hominids may not have fission-fusion space (fig. 1) does not mean that the same had it (Silleń-Tullberg and Møller 1993). Aureli et al. hy- exogenous factors are affecting the fission-fusion dynamics of pothesize that the human band assumed from the hunter- those taxa. We are perfectly comfortable with this position, gatherer community corresponds to the chimpanzee com- as different taxa may show the same quantification of fission- munity. However, the human band always consists of plural fusion dynamics for different reasons. This emphasizes that

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Figure 5. One frame in the running of a simple agent-based simulation model of association patterns among hamadryas baboons (A. Di Fiore, unpublished data). In this model, 20 females move randomly but also follow a simple flocking algorithm, moving in coordination with other females when they get close to them. When females get close to a male “leader,” they preferentially follow the male. The four males in this run of the model also move randomly, but they are intolerant of one another and turn away from one another when they get close. With these two different classes of behavioral rules—one for females and one for males— “harem” subgroups of female agents form around male “leaders.” At this point in the run, for example, harem sizes for the four males are nine, four, four, and three females. Harem compositions remain generally stable, but some interactions between males, depending on the spatial details of those interactions, can result in the transfer of particular females between harems. in addition to being able to describe and compare the actual The agent-based models can help us explore relevant social fission-fusion dynamics across taxa, we need to study why interactions or social roles just as easily as we can evaluate those dynamics take the form that they do. The various sec- the influence of the environment on association patterns—a tions of our article propose frameworks to address that point we do make explicitly in the article. For example, figure question. 5 shows the output of a simple simulation model with “male” Kummer’s commentary raises a very good point that we and “female” agents that follow different behavioral rules. In did not discuss: the roles that certain key individuals or classes this model females move randomly but also follow a simple of individuals can play in structuring subgroups (e.g., via flocking algorithm and coordinate their movement with con- mutual attraction of animals to a particular leader). This as- specifics when close to them; when they are close to a male, pect, however, can easily be incorporated into agent-based they preferentially follow the male. Males also move randomly models by ascribing characteristics to particular agents. For but do not follow a flocking algorithm, and they are intolerant example, one might add the behavioral rule “agents follow of one another; when males get close to another male, both animal A” when they get close to it or set a measure of turn away. With these simple rules, subgroups of female agents “intolerance” between animals A and B to be high, such that form around “leader males.” when they get near each other, they (and their followers) split. Kerth and Kummer both correctly point out that observed

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fission-fusion patterns derive from individual decisions that, typical in the following contexts. First, victims of aggression in turn, are products of evolved goals and motives that may separate from former opponents to reduce the immediate differ among individuals. Both cite experimental studies that costs of escalated aggression. Second, mothers reduce infan- have elucidated the links between ecological variables, indi- ticide risk by avoiding conspecifics during early lactation. vidual psychology, and the collective decisions that produce Third, individuals benefit from temporarily departing from fission and fusion events. We agree that experimental ap- group members to hunt alone because lone hunters gain more proaches, which we did not discuss in our article, can yield energy from feeding from ungulate carcasses that they acquire important data with which to address the questions we have before competitors arrive. Therefore, we suggest that future raised. For example, Meunier et al. (2006) have shown that research must focus on the communication and cognitive captive white-faced capuchins differed in their tendency to demands regarding not only fusion decisions (e.g., Aureli and follow group members when choosing a travel direction in Schaffner 2007; Smith, Memenis, and Holekamp 2007) but search of food. Subordinate females were least likely to con- also fission decisions. Both types of decisions should theo- form to majority decisions, as would be expected if they had retically have large fitness consequences for individuals and, learned to expect exclusion from food while accompanied by consequently, should strongly affect the way group decisions dominants. We anticipate and encourage similar research that are made in species from a variety of taxa. can be incorporated with our relativistic approach on fission- Boehm and Yamagiwa both draw attention to the impor- fusion dynamics. tance of pair bonding in human social evolution. Boehm is The social constraints on party size and composition dis- correct to argue that the most basic unit in hunter-gatherer cussed by Kummer are perfectly compatible with the frame- regional networks is the pair-bonded family, which is lacking works presented in our article. As we mentioned, agent-based in great apes. We acknowledge this in our article, and the models can include rules instantiating socially differentiated evolutionary context of pair bonding has been modeled before agents. Negotiating travel routes and meeting points, as ham- (e.g., Foley and Lee 1989). We do not dispute the importance adryas baboons accomplish in the fascinating and intricate ways of this aspect of human evolution but wish to draw attention documented years ago by Kummer and his colleagues, are to another level of human social organization that we (and among the social tasks that drew our attention in “Implications Boehm) consider as having received less attention. Social an- of Fission-Fusion Dynamics for Communication,” though thropology equated hunter-gatherer society with the band, space limitations precluded specific discussion of them. Kum- but early authors (Radcliffe-Brown 1931; Steward 1936) sup- mer’s lead in this area needs to be followed seriously. posed that men remained in the same band all their lives Yamagiwa asks us to consider generally the evolutionary while women transferred from one band to another at mar- origins and functions of primate sociality. Other authors riage. Pace Yamagiwa (and in contrast to many previous au- (Dunbar 1988; Isbell 1991; Sterck, Watts, and van Schaik 1997; thors) we do not assume such an equivalence; indeed, we van Schaik 1989; Wrangham 1980) have tackled these ques- suggest rather that it may well be the hunter-gatherer com- tions, and they remain unsettled. Our point in figure 3 was munity (or regional grouping) that is the analogue of the not to rehash these debates but to draw a distinction between chimpanzee community, and that changes what is in need of the hypothesized effects on fission-fusion dynamics of two explanation. As Boehm points out, the band is a much more general evolutionary routes to group living that differ in the fluid and permeable grouping than Radcliffe-Brown and importance of differentiated social relationships. Yamagiwa Steward appreciated. Despite the advantages of band life, such also draws attention to sex-differentiated dispersal and its as developing trust in reciprocal exchange, human adults of implications for comparative analyses. Clearly, philopatric in- both sexes often freely change band membership. Recognizing dividuals are more likely than dispersing individuals to be the evolutionary importance of this aspect, we propose that more closely related to—and possibly more familiar with— if the human band is the analogue of the fusion phases in potential social partners. This variation could influence sex chimpanzee community interaction, then crucial elements in differences in the costs and benefits of gregariousness and the evolution of human behavior, such as band exogamy and therefore could affect fission-fusion dynamics in situations in gift exchange, can be explained as responses to the problem which party composition is flexible. of sustaining relationships in a community that is far more We agree with Kerth that more research must be done to dispersed (temporally and spatially) than that of chimpanzees, test the theoretical prediction that group members should hence enabling the kind of movement to which Boehm refers. temporarily leave subgroups to avoid group-level decisions In analyzing these relationships we need to distinguish be- that are not in their favor (Conradt and Roper 2005). Fission- tween function (meat sharing, dispute avoidance) and con- fusion dynamics offer opportunities to deal with group-level sequence (gregariousness, long-term kinship relations). The decisions. For example, and consistent with Kerth, Ebert, and differences in mating strategies between chimpanzees (pro- Schmidtke’s (2006) findings in bats, the high degree of fission- miscuity with strong female sexual signals) and humans (small fusion dynamics permits another nonprimate species, the family units with a strong tendency of pair bonding) that spotted hyena, to directly benefit the interests of the departing Yamagiwa highlights are most likely elements that evolved individuals (Smith et al. 2008). Departing from subgroups is after humans and chimpanzees diverged from the shared

This content downloaded from 23.235.32.0 on Thu, 12 Nov 2015 08:47:44 AM All use subject to JSTOR Terms and Conditions Aureli et al. Fission-Fusion Dynamics 649 common ancestor. Humans, indeed, are distinguished by their Aureli, F., and C. M. Schaffner. 2002. Relationship assessment ability to extend pair-bonded-like relationships beyond breed- through emotional mediation. Behaviour 139:393–420. ing couples to enduring relationships in wider social networks. ———. 2007. Aggression and conflict management at fusion Finally, as pointed out by most commentators and stressed in spider monkeys. Biology Letters 3:147–49. in our article, a broad approach is needed to achieve our main Barrett, L., P. Henzi, and R. Dunbar. 2003. Primate cognition: goals. First, we need to populate the multidimensional fission- From “what now?” to “what if?” Trends in Cognitive Science fusion space with taxa and populations. To do so, we need 7:494–97. data from multiple sites for the same species belonging to a Bearder, S. K. 1999. Physical and social diversity among noc- large number of primate and nonprimate taxa. With this da- turnal primates: A new view based on long-term research. tabase comparative analysis of the relation between the extent Primates 40:267–82. of fission-fusion dynamics and factors related to socioecology, Binford, L. R. 1987. Searching for camps and missing the communication, and cognitive abilities can be carried out evidence? Another look at the Lower Palaeolithic. In The taking evolutionary history into account. To understand such Pleistocene Old World, ed. O. Soffer, 17–32. New York: Ac- dynamics we need long-term field studies, which can be in- ademic Press. formed by the findings of agent-based simulations and which Boesch, C., and H. Boesch-Achermann. 2000. The chimpan- can, in turn, provide essential data for the implementation zees of the Taı¨ forest. Oxford: Oxford University Press. of further simulations and generate hypotheses for testing on Boinski, S. 1996. Vocal coordination of troop movement in actual animals. A comparative experimental approach, along squirrel monkeys (Saimiri oerstedi and S. sciureus)and with better knowledge of comparative brain structures and white-faced capuchins (Cebus capucinus). In Adaptive ra- functioning, not limited to primates and possibly beyond diations of Neotropical primates, ed. M. A. Norconk, A. L. mammals, complements the endeavor to understand the im- Rosenberger, and P. A. Garber, 251–69. New York: Plenum pact of fission-fusion dynamics on communication and cog- Press. nitive abilities. We believe that this broad comparative per- ———. 1999. The social organizations of squirrel monkeys: spective can identify common underlying principles and Implications for ecological models of social evolution. 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