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W2795782618 abstract "Much has changed in our understanding of primate social behavior since the pioneering naturalistic field study conducted by Clarence Ray Carpenter (1934) on the behavior and social relations of mantled howler monkeys in Panama. These changes reflect a combination of interacting factors, including: (i) shifts in disciplinary perspectives; (ii) advances in theory, methods, and analytical (including computational) power; and (iii) a dramatic increase in the diversity of primate taxa that have been studied across space and over time. Together, these changes have broadened our comparative perspectives about primates, and challenged basic longstanding concepts such as those about the stability of group size and composition, and the role of kinship in structuring primate social relationships. They have also stimulated new considerations of behavioral adaptation, variation, and flexibility (Strier, 2017a). After a remarkable expansion in primate behavioral and ecological studies over the past half-century, we have reached an exciting new threshold of understanding about the range of flexible behavioral patterns that primates exhibit in response to local ecological and demographic conditions. This understanding is poised to lead to the development of new dynamic comparative models that encompass both interspecific and intraspecific variation in primate behavioral ecology, and thus will provide insights into primate social evolution and adaptive potential (Strier, 2017b). At the same time, however, we are facing an impending crisis. Some 60% of primate taxa are already threatened with extinction, and 75% of primate populations are experiencing dangerous declines (Estrada et al., 2017). Accelerating anthropogenic pressures from habitat loss and hunting, coupled with irreversible climate change, extreme weather events, and the spread of zoonotic diseases, are now escalating the risks to primates at local, regional, and global scales. Urgent concerns about the long-term prospects for the survival of primates cast a formidable shadow over what would otherwise be an unguarded optimism about the future of the field. The realities of anthropogenic impacts on primate populations and their habitats, though cause for alarm, have nonetheless led to new insights into the inconsistencies between predictions about behavioral adaptations derived from socioecological theory and the actual behavior patterns we observe (Janson, 2000; Strier, 2003a, 2003b; Thierry, 2008; Koenig & Borries, 2009). Indeed, a major challenge in contemporary primate behavioral ecology revolves around identifying whether the behavior patterns that presumably evolved under very different ecological and demographic conditions in the past still continue to be adaptive today. Increasing sensitivities to the altered conditions under which the majority of primates now live and to the high level of behavioral flexibility that many species exhibit are stimulating us to think about social evolution over ecological time. At the same time, we are becoming increasingly more reflective about how well our knowledge of primates might be usefully applied toward conservation measures on their behalf (Lee, 2010; Riley, 2013). I have divided the body of this Perspective into three sections corresponding to the past, the present, and what I envision to be the greatest challenges for the future of primate behavioral ecology. The historical context of primate behavioral studies has been thoroughly reviewed elsewhere (e.g., Strum & Fedigan, 2000; Kelley & Sussman, 2007), so my aim here is mainly to establish a framework for interpreting how we reached our present state of knowledge about primate social behavior. Unfortunately, space constraints prevent mention of more than a very small subset of the many important discoveries that have been influential in expanding our knowledge base and in shaping the field (from my perspective as a U.S.-trained biological anthropologist and primatologist). I then draw on both historical and contemporary perspectives and achievements to anticipate the next major new directives. It will be immediately apparent that my own research interests are biased toward observational studies of wild primates. However, it is also the case that both experimental field studies and studies of provisioned and captive primates have played significant roles in shaping our understanding of primates and I suspect that these approaches may have yet even greater roles to play as the status of so many of the world's wild primates becomes increasingly uncertain. Over the late twentieth century, the study of primate social behavior shifted from natural history-like narratives to become increasingly focused on the hypotheses-driven systematic collection of quantifiable data, which are now also commonly supplemented with non-invasive hormonal, physiological, genetic, or microbial samples to gain insights into the underlying mechanisms and consequences of behavior. Nonetheless, the early original descriptions of the behaviors of wild primates at the time they were first observed scientifically afford vitally important documentation, and many of these reports are now also of tremendous (but perhaps not yet fully recognized) value for the historical perspectives they offer into primates whose populations and habitats have undergone dramatic changes in the intervening years. One such example comes from Carpenter's mantled howler monkey data, which provided not only the first scientific descriptions of the behavior of these monkeys in the wild, but also the baseline for documenting a 48% decline in the population between 1933 and 1951, with yellow fever considered to be a possible cause (Collias & Southwick, 1952). This early quantitative account of yellow fever's potentially devastating impact on howler monkeys is now providing essential historical context and comparative perspectives for interpreting the impact of more recent yellow fever outbreaks, such as those that have been responsible for the deaths of thousands of brown howler monkeys in southeastern Brazil in 2008–2009 and 2016–2017 (Bicca-Marques et al., 2017). Demographic variables such as group and population size, composition, and density are known to directly affect individual social and reproductive options, so changes in numbers on the order of magnitude induced by outbreaks of yellow fever (and other zoonotic diseases) have obvious important implications for interpretations of the inter- and intraspecifc variation in behavior patterns we observe today. Moreover, these impacts from zoonotic diseases are expected to increase with climate change and further human encroachment into primate habitats (Estrada et al., 2017). Carpenter's (1934) first monograph stands as a landmark achievement for other reasons in addition to its historical value. Unlike his contemporaries, Harold C. Bingham and Henry Nissen, who were also then working with Robert Yerkes at Yale, Carpenter spent an initial 6 months in the field actually observing wild howler monkeys, and returned again to Panama for another 2 months, making a total of 8 months in all. Apparently, Bingham rarely saw the mountain gorillas he sought to study during his two months in the Belgian Congo in 1929 (Peterson, 2006), and Nissen's (1931) initial 3-month effort to study chimpanzees in French Guinea (now Guinea) continued with his subsequent more extensive behavioral observations of the 18 chimpanzees he brought back with him from the field (Carmichael, 1965). In contrast to his colleagues, Carpenter continued to focus on what he referred to as “naturalistic” studies of wild primates. He conducted a second significant field study on lar gibbons in Siam (now Thailand) in the late 1930s (Carpenter, 1940), which Margaret Mead (1942) recommended as a model of the observational field method, and therefore essential reading for anthropologists in her glowing review of the monograph for the American Anthropologist. Carpenter traveled widely to other primate habitat countries, and although he returned from a visit to India in 1938 with more than 400 rhesus macaques, which became the founders of the colony at Cayo Santiago, Puerto Rico, he remained committed to the behavioral study of wild primates. Carpenter was internationally recognized for his influential role in establishing the foundations of contemporary field primatology (Teleki, 1981). He also became an important colleague to Kinji Imanishi, who is known as “the father of Japanese primatology” and who, like Carpenter, appreciated the merits of studying behavior in the primate's naturalistic social context (Matsuzawa & McGrew, 2008). I have dwelled on Carpenter in part to highlight some of the historical connections that link naturalistic, free-ranging, and provisioned studies of primates. These connections are important to acknowledge because what we now know about primate social behavior comes from a combination of these contexts. Indeed, Carpenter's gibbon study was initiated while he was on the Asiatic Primate Expedition led by zoologist Harold J. Coolidge, Jr., who was a curator of mammals at the Harvard Museum of Comparative Zoology, and also an able primatologist who helped to describe Pan paniscus from the drawers of museums (Coolidge, 1933). Other members of the expedition included anatomist Adolph H. Schultz and anthropology student Sherwood Washburn (Marks, 2000). It is hard to reconcile these early expeditions, which relied more heavily on the collection and description of dead primates than on the observations of the behavior of live ones, with the urgent conservation concerns of contemporary primate behavioral ecology. Yet, Coolidge was also a leading conservationist, who later became a founding director and president of the International Union for the Conservation of Nature, or IUCN and a founder of the World Wildlife Fund (Sullivan, 1985), and Washburn was influential in bringing behavioral studies of wild primates into American physical anthropology (Washburn 1951, 1973). Thus, these collecting expeditions merge with the deep roots that trace back to psychologists from the U.S., the U.K., and elsewhere in Europe, who worked at the interface between field and captive behavioral studies (Bernstein, 1964; de Waal, 2005; Kelley & Sussman, 2007). In the late 1940s, when Imanishi (an ecologist and anthropologist) and his colleagues launched their long-term studies of Japanese macaques, they had the insight to distinguish their study subjects as individuals (Hirata et al., 2001), and to recognize the social and anthropological relevance of nonhuman primate “cultural” continuities with humans (Kawamura, 1959; Imanishi, 1960). Roughly a decade later came Washburn and DeVore's (1961) study of the social behavior of baboons in their “natural environment” of the East African savanna, where it was thought our ancestors had evolved. Complementary to Imanishi's considerations of the social environment and contemporaneous with Washburn and DeVore's considerations of the ecological context, was paleontologist Louis Leakey's interest in the phylogenetic continuities that the extant great apes represented with humans. Leakey sent his first recruit, Jane Goodall, to Tanzania to study chimpanzees in 1960. In 1962, he had arranged for Goodall to write up her observations about the Gombe chimpanzees for her PhD under the supervision of British ethologist, Robert Hinde, who trained as an ornithologist at Oxford but who had just established a colony of rhesus macaques at Cambridge in order to understand human relationships (Goodall, 2017). After Goodall, Hinde trained many other distinguished field primatologists, extending the links from ethology and psychology to primatology that recurred within other European academic lineages, including that of Jan van Hooff (Kelley & Sussman, 2007). By the early 1960s, all four of the principal explanatory foundations for comparative primate behavioral studies (e.g., demographic, social, ecological, and phylogenetic) had been established. It was also around this time that the American Journal of Physical Anthropology, for which Sherwood Washburn had been editor from 1955–1957, became a resource for primate behavior research, although initially this was primarily as a result of the publication of informative Book Reviews on the monographs and especially, edited volumes, about primate social and ecological behavior that were starting to proliferate. Curiously (and in contrast to the American Anthropologist), Carpenter's work was only reviewed in the AJPA in the 1970s for a film he made on Japanese macaque behavior, and then later in the context of the two obituaries written about him (Buettner-Janusch, 1976; Teleki, 1981). A key unifying theme of early behavioral field studies was the ecological context in which the observations were made relative to those reported by others elsewhere. Researchers were careful to compare the ecological conditions of their studies to those of others on similar species to such an extent that even Washburn and DeVore's pioneering behavioral descriptions were considered to be in need of a “social” or “human adjustment factor” because the observations were made on baboons living in a game reserve, where their behavior may have been affected by the presence of humans, instead of on baboons living more remotely in “the wild state” (Maxim & Buettner-Janusch, 1963). The different behavior patterns exhibited by conspecifics living under different ecological and demographic conditions continued to figure prominently in debates over how to identify the normative behavior patterns for a species. One of these early debates focused on behavioral differences between savanna and forest baboons (DeVore & Hall, 1965; Rowell, 1966, 2000). Another emerged in the 1970s over the variation observed in the occurrence of male infanticidal behavior in Hanuman langurs (Hrdy, 1977; Dolhinow, 1977), which was ultimately explained as an effective male reproductive strategy under some, but not all, demographic conditions (Moore 1999). Even the seemingly invariant rule of “youngest daughter ascendency,” whereby the youngest daughters displace their older sisters to attain a dominance rank immediately below their mothers, in the matrilocal societies of Japanese macaques (Kawai, 1958, Kawamura, 1958), turned out to be more relaxed in small, unprovisioned groups (Hill & Okayasu, 1995). The quest for species-typical behavior patterns that fueled these debates may make little sense today, but back then, in the historical context of an anthropocentric, anthropological rationale for primate behavioral studies that was focused on gaining comparative insights into human social evolution, the primary comparisons of interest were, by definition, being made at the species level. At that comparative scale, it was about the similarities and differences in the behavioral traits ubiquitous to humans versus those of other species. Other primatological traditions, such as that of Latin American primatology, were less concerned with direct behavioral comparisons between nonhuman and human primates, focusing instead on broader ecological questions and on the evidence of intraspecific behavioral variation that the anthropocentric primatological perspectives tended to ignore (Strier, 2016). These perspectives began to shift, however. As psychologist Irwin Bernstein (1964:236) wrote in an early comparative paper in the AJPA, “…the study of primates should not be directed exclusively at determining the origins of one particular primate, Homo sapiens, and/or the understanding of his behavior. Instead, we ought to direct our efforts at understanding the many forces which work to shape behavior and the organization of societies, and the many possible solutions which will satisfy the requirements of any particular situation.” Bernstein's first point, about understanding the many forces that shape social behavior, was consistent with the underlying premises of Tinbergen's (1963) four “rules” for understanding behavior (proximate, ultimate, phylogenetic, and ontogenetic), and anticipated the direction of the earliest synthetic models of the evolution and ecology of primate societies (Crook & Gartlan, 1966). Bernstein's second point, about there being alternative solutions to the same problems, also resonated with what some other leading primatologists, such as Imanishi (1967) and Phyllis Jay (1968) were also saying about the importance of recognizing behavioral variation (reviewed in Strier, 2017b). The early comparative models of primate sociality (e.g., Crook & Gartlan, 1966; Eisenberg et al., 1972) were impressive in their success at identifying patterns of interspecific variation while also characterizing intraspecific variation in social behavior. However, they were also quite limited because of the lack of standardized methods for collecting behavioral data, the absence of explicit theoretical formulations that could generate testable hypotheses, and the narrow taxonomic breadth of species that had been studied. Major advances were made as each of these limitations was addressed. The lack of a standardized methodology made it difficult to compare findings from one study with those from another. This problem was appreciated by many early fieldworkers (reviewed in Kelley & Sussman, 2007), but not fully resolved until Jeanne Altmann's (1974) pivotal paper, “Observational Study of Behavior: Sampling Methods.” This article rapidly became the gold standard for recording behaviors and interactions based on pre-determined sampling protocols that were tailored to the kinds of questions being asked, and that maintained the independence needed for statistical comparisons of frequencies and rates of behavior across studies. The standardization of behavioral sampling methods also stimulated increasingly fine-grained behavioral analyses. One example of these kinds of analyses focused on the nuanced interactions reflecting subtle shifts in the individual affiliations and alliances that Frans de Waal (1982) described in Chimpanzee Politics. Other examples focused on components of primate social dynamics, such as the variants of reconciliation (e.g., de Waal, 1989; reviewed by Silk, 2002), and the diverse indicators of valued relationships and partner value, which could be understood in terms of “biological markets” (e.g., Noë & Hammerstein, 1994, 1995). During the 1980s and 1990s, systematic methods of behavioral sampling were also complemented with new assays for quantifying the proximate hormonal mechanisms underlying behavior in ways that could be compared across studies of the same and different species and across contexts ranging from captivity to the field. Many insights on topics ranging from the social and reproductive correlates of sexual behavior (e.g., Whitten et al., 1998) to the social and biological relationships involved in cooperative breeding and paternal care (e.g Snowdon & Ziegler, 2007; Snowdon, 2017) have come from the merging of observational and hormonal data obtained noninvasively from urine or more commonly, dung (Strier & Ziegler, 2005). The incorporation of testable hypotheses based on the evolutionary theories of natural selection, kin selection, and sexual selection into primate behavioral ecology was also a relatively rapid process (Richard, 1981). The initial framework for many of the key evolutionary and ecological principles had already been outlined by Darwin, and by the 1970s these were well on their way to being synthesized into comparative analyses of organisms ranging from birds, to bats, to ungulates and other mammals, including primates, (e.g., Trivers, 1971, 1972; Eisenberg et al., 1972; Jarman, 1974; Wilson, 1975; Emlen & Oring, 1977; Bradbury & Vehrencamp, 1977). The idea that individual behavioral traits, similar to morphological and physiological traits, are shaped by evolutionary selection pressures because of the differential fitness benefits they confer on individuals meant that behavioral traits could vary among individuals and across spatial and temporal scales, including those of individual lifespans. Behavioral variants were described in terms of individual social and reproductive strategies, although whether these were inherently competitive and aggressive, versus cooperative and affiliative, has remained controversial because of the implications that these alternative assumptions held about the origins of our own social natures as well as those of other primates (Sussman et al., 2005; Koenig et al., 2006). More acute controversies about evolutionary theories of behavior emerged in response to what critics perceived as genetic determinism, reminiscent of eugenics (e.g., Lewontin, 1979), at least as they were being synthesized and disseminated by the critics following the publication of E.O. Wilson's (1975) Sociobiology. The idea that elements of human social behavior had been shaped by selection pressures favoring fitness also contributed to divisions between sociocultural and biological anthropologists (e.g., Sahlins, 1976). Even among primatologists, the initial controversy over the variable expression of infanticidal behavior across populations of langurs was essentially a critique of what was perceived by some as an uncritical adaptationist paradigm (Sussman et al., 1994; Hrdy et al., 1994; reviewed in Rees, 2009). Concurrent with these debates, however, were complementary evolutionary insights into topics such as parental and allo-parental infant care, the influence of female mate choice, and the capacity of females to confuse paternity. Discussions around such topics figured prominently in parallel efforts to consider the importance of females, and feminist perspectives, in evolutionary theory in general and in primate behavioral ecology more specifically (e.g., Altmann, 1980; Hrdy, 1981; Small, 1989; Fedigan, 1994; Strum & Fedigan, 2000). The underlying assumptions of evolutionary and ecological models of behavioral adaption put an even greater premium on studying the social behavior of primates in their “natural” habitats and social groups than before (e.g., Richard, 1978). However, observational field studies of wild populations could still only address a limited number of evolutionary questions. One response to these limitations was the enhancement of experimental field methods; another response was the development of noninvasive methods for obtaining genetic data. Field play-back experiments involve monitoring the behavioral responses of wild subjects to controlled recordings of vocalizations that can then be quantitatively assessed. Among the earliest and most effective uses of field playback experiments were those employed to evaluate how vervet monkeys responded to recordings of alarm calls to different types of predators, which demonstrated their referential cognitive abilities, and to distress calls from group members, which provided cues into their perceptions of kinship, relative dominance rankings, and the influence of affiliative interactions such as grooming on their subsequent social interactions (Cheney & Seyfarth, 1990). Predictions about nepotistic behavior derived from kin selection theory could only be evaluated along maternal lines with observational data (e.g. Kurland 1977; Packer 1977), and even then, only in species in which females remained in their natal groups with extended maternally-related female kin, where both the strength of female social partners and the number of close maternal kin are positively related to female fitness (Silk et al., 2009, 2010). Indeed, comparative analyses suggest that female kin groups are more resistant to change under variable demographic conditions than other kinds of groups (Strier et al., 2014). However, similar predictions about nepotism among paternally-related female kin in these societies, or among male kin in patrilocal societies were not accessible from observational data because of uncertainties about paternity and the relationships among patrilineal kin. Thus, although males in patrilocal societies could be assumed to be more closely related to one another, on average, than males that dispersed from their natal groups into matrilocal societies, genetic paternity data were still needed to test hypotheses about the social relationships of particular males within and among these patrilines. The development of noninvasive methods for extracting and replicating DNA from the dung of wild primates was essential to advances in our understanding of the genetic structuring of primate groups and communities (e.g., Morin et al., 1994; Bradley et al, 2004; Langergraber et al., 2014). Noninvasive methods of obtaining genetic paternity data were also necessary for evaluating predictions about reproductive strategies and nepotism in a wider range of primates (Di Fiore, 2003). These studies have provided insights into topics such as the effects of social stability and instability on male paternity success (e.g., Altmann et al., 1996), and the potential role of mothers and other maternal kin on paternity success in patrilocal societies (e.g., Strier et al., 2011). At the same time, however, there is now increasing evidence from both behavioral and genetic studies that kinship is not essential for the development and maintenance of long-term affiliative social bonds (e.g., Langergraber et al., 2007, 2017). In contrast to the rapidity of methodological and theoretical advances, the expansion of the diversity of species and populations studied has been a much slower process. Between 1931 and 1982, only 10 primate genera accounted for more than 60% of published field studies, with only one New World monkey genus (Alouatta) and one prosimian genus (Lemur) among them (Southwick & Smith, 1986). This is not to say that comparative studies of other primates, including even distantly-related, nocturnal prosimians, did not exist, because they did (e.g., Charles-Dominique, 1977). However, despite even Carpenter's pioneering success with New World howler monkeys, subsequent naturalistic research on wild primates was strongly biased toward the Old World and a few genera of African and Asian monkeys, most of which were semi-terrestrial, and the African apes. These biases made it difficult to distinguish whether differences and similarities in behavior patterns were shaped by ecological conditions or phylogeny. The only way to evaluate these alternatives was with new data from a greater diversity of taxa. Richard Wrangham's (1980) paper, “An Ecological Model of Female-Bonded Primates,” provided a blueprint for a new generation of comparative studies on the behavioral ecology of primates about which little or nothing was yet known. Following his predecessors studying other organisms (e.g., Jarman, 1974; Emlen & Oring, 1977), Wrangham's model focused on the ways in which variation in the distribution and availability of food shaped female behavior, which consequently shaped male behavior, and ultimately the species’ social organization. Similar to many others in my graduate cohort in the 1980s, I framed my dissertation research around testing alternative predictions about social behavior based on these food-related variables. My study subjects were the elusive and endangered muriquis (Brachyteles arachnoides). They are now classified as critically endangered and since 2000 have been recognized as a separate species, the northern muriqui (B. hypoxanthus), distinct from the southern muriqui (B. arachnoides). Others in my cohort focused on other primate species about which little was known and on different subsets of predictions about the effects of ecology on social behavior. Pooling these comparative findings has led to many refinements in subsequent iterations of what has become known as the socioecological model (e.g., van Schaik, 1983, 1989; Isbell, 1991; Sterck et al., 1997; Kappeler & van Schaik, 2002). The application of methods of comparative analyses to control for the effects of phylogeny on behavior also became an essential tool for testing hypotheses about the evolution of behavioral adaptations (Harvey & Pagel 1991; Harvey & Purvis, 1991). Even with the limited comparative perspectives at the time, it became increasingly clear that the female-bonded cercopthecines that featured so prominently in Wrangham's model were not “typical” of the majority of primates (Strier, 1994). Instead of being widespread, the matrilocality required for extended matrilineal kin to co-reside and maintain the differentiated relationships that defined female-bonded primates turned out to be much less common across the Primates than Wrangham's model assumed (Moore, 1984). Analyses of the phylogenetic distribution of the suite of behavioral traits attributed to female-bonded primates provided early statistical support for the evolutionary distinctiveness of this clade (Di Fiore & Rendall, 1994). Similar to the use of systematic methods of behavioral sampling and its focus on testing hypotheses generated from evolutionary and ecological theory, the use of phylogenetic controls is now standard practice in comparative analyses of primate behavioral ecology. Refinements in our knowledge of the phylogenetic patterning of behavior can be attributed, in part, to advances in our understanding of primate phylogenetic relationships as a result of developments in molecular biology. The expansion of accessible computational power (from advances in computer technology) has also contributed to the widespread use of comparative analyses to identify behavior patterns that can be attributed to shared ancestry as opposed to those that reflect evolutionary adaptations (Nunn & Barton, 2001). Yet despite their value, it is important to remember that these are analytical methods, not ends in themselves, and their utility for understanding patterns of social evolution is determined as" @default.
W2795782618 created "2018-04-13" @default.
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W2795782618 date "2018-03-25" @default.
W2795782618 modified "2023-10-04" @default.
W2795782618 title "Primate social behavior" @default.
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