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Izar Et Al. 2011B American Journal of Primatology.Pdf American Journal of Primatology 73:1–17 (2011) RESEARCH ARTICLE Flexible and Conservative Features of Social Systems in Tufted Capuchin Monkeys: Comparing the Socioecology of Sapajus libidinosus and Sapajus nigritus PATRI´CIA IZAR1Ã, MICHELE P. VERDERANE1, LUCAS PETERNELLI-DOS-SANTOS1,OLI´VIA MENDONC-A-FURTADO1, 1 1 2 3 ANDRE´APRESOTTO, MARCOS TOKUDA ,ELISABETTAVISALBERGHI, AND DOROTHY FRAGASZY 1Department of Experimental Psychology, Institute of Psychology, University of Sa˜o Paulo, Sa˜o Paulo, Brazil 2Istituto di Scienze e Tecnologie della Cognizione, Consiglio Nazionale delle Ricerche, Rome, Italy 3Psychology Department, University of Georgia, Athens, Greece Socioecological models assume that primates adapt their social behavior to ecological conditions, and predict that food availability and distribution, predation risk and risk of infanticide by males affect patterns of social organization, social structure and mating system of primates. However, adaptability and variation of social behavior may be constrained by conservative adaptations and by phylogenetic inertia. The comparative study of closely related species can help to identify the relative contribution of ecological and of genetic determinants to primate social systems. We compared ecological features and social behavior of two species of the genus Sapajus, S. nigritus in Carlos Botelho State Park, an area of Atlantic Forest in Sa˜o Paulo state, and S. libidinosus in Fazenda Boa Vista, a semi-arid habitat in Piauı´ state, Brazil. S. libidinosus perceived higher predation risk and fed on clumped, high quality, and usurpable resources (fruits) all year round, whereas S. nigritus perceived lower predation risk and relied on evenly distributed, low-quality food sources (leaves) during periods of fruit shortage. As predicted by socioecology models, S. libidinosus females were philopatric and established linear and stable dominance hierarchies, coalitions, and grooming relationships. S. nigritus females competed less often, and could transfer between groups, which might explain the lack of coalitions and grooming bonds among them. Both populations presented similar group size and composition and the same polygynous mating system. The species differed from each other in accordance with differences in the characteristics of their main food sources, as predicted by socioecological models, suggesting that phylogenetic inertia does not constrain social relationships established among female Sapajus. The similarity in mating systems indicates that this element of the social system is not affected by ecological variables and thus, is a more conservative behavioral feature of the genus Sapajus. Am. J. Primatol. 73:1–17, 2011. r 2011 Wiley-Liss, Inc. Key words: food competition; predation risk; phylogenetic inertia; adaptability; Cebus; Sapajus INTRODUCTION aspects of primate social systems. As female repro- ductive success is limited by food intake (due to the Primate socioecology comprehends primate so- costs of high parental investment [Trivers, 1972]), cial systems as evolved species-specific traits, the the number of females in a group is expected to be adaptive outcome of individual behavioral decisions limited by food competition [Isbell, 1991; Sterck to deal with selective pressures such as the distri- et al., 1997; van Schaik, 1989; Wrangham, 1980]. bution of risks and of limiting resources [reviewed In contrast, male reproductive success is limited by in Janson, 2000]. By means of hypothetic deductive access to sexually receptive females, so the number of models derived from evolutionary theory, different causal factors have been associated with three fundamental elements of social systems: the social Contract grant sponsor: FAPESP; Contract grant numbers: organization (the number, sex ratio, and spatial 06/51577-2; 06/56059-0; 08/55684-3; Contract grant sponsor: cohesion of conspecific individuals that typically live CNPq; Contract grant number: 420038/2005-1; Contract grant sponsors: National Geographic Society; Leakey Foundation; together), the social structure (the set of non- IBAMA; CNPq. reproductive social relationships among these indi- ÃCorrespondence to: Patrı´cia Izar, Av. Prof. Mello Moraes, 1721, viduals), and the mating system (the pattern of CEP: 05508-030, Sa˜o Paulo, SP, Brazil. E-mail: [email protected] mating relationships) [reviewed in Kappeler & van Received 15 November 2010; revised 28 March 2011; revision Schaik, 2002]. accepted 23 April 2011 In socioecological models, food competition DOI 10.1002/ajp.20968 among females plays a central role in all the above Published online in Wiley Online Library (wileyonlinelibrary.com). r 2011 Wiley-Liss, Inc. 2 / Izar et al. males in a group is expected to be a function of the observed in field studies, and because most field spatial (number) and temporal (estrous synchrony) tests were based on Old World species [e.g. Chapman distribution of reproductive females [Clutton-Brock, & Rothman, 2009; Strier, 1994, 2003, 2009; Thierry, 2004; Lindenfors et al., 2004]. Thus, food competi- 2008], indicating that more studies are necessary to tion limits group size, because larger groups deplete improve the models, especially incorporating the less food sources faster and need to travel to find other investigated New World primate species [Janson, sources, increasing daily travel costs [e.g. Chapman 2000; Kappeler & van Schaik, 2002; Strier, 1994]. & Chapman, 2000; Isbell, 1991; Izar, 2004; Snaith & More research is also necessary to address the Chapman, 2007; Strier, 1989; Teichroeb & Sicotte, question of how flexible and how conservative 2008], and decreasing female reproductive success primate social systems are. The focus of behavioral [e.g. Borries et al., 2008; Ryan et al., 2008; van Belle ecology is on adaptation, but it is assumed that & Estrada, 2008]. Besides affecting social organiza- selection act(ed) on individual strategies, or decision tion, food competition affects mating systems rules, so that organisms behave as fitness maximi- because the capacity of individual males to mono- zers. Indeed, tests of the models are based ‘‘on the polize sexually receptive females is correlated with current fit of an organism’s behavior to local the size and degree of overlap of females’ range environmental conditions’’ [Rendall & Di Fiore, [Komers & Brotherton, 1997] and with the number 2007, p 509] and thus behavior should vary according of males in a group [Kutsukake & Nunn, 2006]. Food to local and current environment conditions, within competition also affects female social relationships. the limits of social trajectories or behavioral syn- Females might compete directly for patchy usurpable dromes [Cahan et al., 2002; Sih et al., 2004]. One foods, and indirectly for evenly distributed foods, method to identify what behavioral features vary within group and between groups [reviewed in Isbell along with variation in ecological factors is to & Young, 2002]. According to the most recent model study behavioral variation among populations or [Sterck et al., 1997], the combination of the level of sister species, on the assumption that there is little the four types of food competition leads to four or no biological difference among them [e.g. Barton behavioral syndromes of female social relationships, et al., 1996]. in regards to their tendency to remain in the natal Tufted capuchin monkeys are particularly group, and to establish dominance relationships and suitable for this kind of study. According to kin-biased affiliative relationships. recent reviews based on morphological [Oliveira & Predation risk is considered the ultimate cause Langguth, 2006; Silva, 2001] and molecular evidence of group living in diurnal primates [van Schaik, 1983; [Lynch-Alfaro et al., submitted], this is a group but see Rasoloarison et al., 1995]. At the proximate of eight species of the Neotropical genus Sapajus level, it is expected to affect social organization and (S. apella, S. macrocephalus, S. libidinosus, S. cay, mating system, by limiting minimum group size S. nigritus, S. robustus, S. xanthosternos, and [Dunbar, 1996; but see Boinski et al., 2003; McGraw S. flavius), formerly classified as the robust forms & Zuberbu¨hler, 2008] and increasing group cohesion of the Neotropical genus Cebus (that now, according [Boesch & Boesch-Achermann, 2000; Sterck et al., to these reviews, includes only the gracile forms 1997], and there is evidence that the extra-number of C. albifrons, C. olivaceus, and C. capucinus). The males in a group (expected by number of females) is genus Sapajus has a wide distribution, occupying correlated with predation risk [Hill & Lee, 1998; very different habitats, including evergreen tropical Stanford, 2002; van Schaik & Ho¨rstermann, 1994]. forests, mangrove forests, the semi-arid Caatinga Sexual conflict is also expected to affect primate and Cerrado in northeast and central Brazil, and dry social systems. In this view, mating patterns might seasonal forests [Fragaszy et al., 2004a]. These reflect female strategies to confound (e.g. promiscuous habitats vary widely in ecological features, including mating) or to concentrate paternity, counteracting food availability and predation risk. It has been male strategies like harassment and infanticide argued that capuchins’ capacity to adapt to these [Nunn & van Schaik, 2000]. As a consequence, species different environments is related to their great showing the same social organization might present behavioral flexibility, particularly with respect to different mating systems
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