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Cacajao, Chiropotes, and Pithecia) American Journal of Primatology 00:1–22 (2012) RESEARCH ARTICLE Terrestrial Activity in Pitheciins (Cacajao, Chiropotes, and Pithecia) ADRIAN A. BARNETT1,2∗, SARAH A. BOYLE3,4, MARILYN M. NORCONK5, SUZANNE PALMINTERI6, RICARDO R. SANTOS7, LIZA M. VEIGA8,9, THIAGO H.G. ALVIM10, MARK BOWLER11, JANICE CHISM12, ANTHONY DI FIORE13, EDUARDO FERNANDEZ-DUQUE14, ANA C. P. GUIMARAES˜ 8, AMY HARRISON-LEVINE15, TORBJØRN HAUGAASEN16, SHAWN LEHMAN17, KATHERINE C. MACKINNON18, FABIANO R. DE MELO10, LEANDRO S. MOREIRA10, VIVIANE S. MOURA10, CARSON R. PHILLIPS19, LILIAM P. PINTO20,21, MARCIO PORT-CARVALHO22, ELEONORE Z. F. SETZ23, CHRISTOPHER SHAFFER24,LIVIA´ RODRIGUES DA SILVA25, SULEIMA DO S. B. DA SILVA26, RAFAELA F. SOARES8, CYNTHIA L. THOMPSON27, TATIANA M. VIEIRA8, ARIOENE VREEDZAAM28, SUZANNE E. WALKER-PACHECO29, WILSON R. SPIRONELLO2, ANN MACLARNON1, AND STEPHEN F. FERRARI30 1Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London, England 2Biodiversity Unit, National Institute for Amazonian Research, Manaus, Amazonas, Brazil 3Department of Biology, Rhodes College, Memphis, Tennessee 4Biological Dynamics of Forest Fragments Project, National Institute for Amazonian Research and Smithsonian Tropical Research Institute, Manaus, Amazonas, Brazil 5Department of Anthropology, Kent State University, Kent, Ohio 6Centre for Evolution, Ecology and Conservation, School of Environmental Sciences, University of East Anglia, Norwich, Norfolk, United Kingdom 7Centre of Agrarian and Environmental Sciences, Federal University of Maranh˜ao, Chapadinha, Maranh˜ao, Brazil 8Post-graduate Program in Zoology, Museu Paraense Emilio Goeldi, Bel´em, Par´a, Brazil 9Department of Zoology, Museu Paraense Emilio Goeldi, Bel´em, Par´a, Brazil 10Research-Aid Foundation, Federal University of Goi´as, Goiˆania, Brazil 11Department of Psychology, University of St. Andrews, St. Andrews, Scotland 12Department of Biology, Winthrop University, Rock Hill, South Carolina 13Department of Anthropology, University of Texas at Austin, Austin, Texas 14Department of Anthropology, University of Pennsylvania, Philadelphia, Pennsylvania and Centre for Applied Litoral Ecology (Conicet), Argentina 15Department of Anthropology, University of Colorado – Boulder, Boulder, Colorado 16Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Norway 17Department of Anthropology, University of Toronto, Toronto, Ontario, Canada 18Department of Sociology and Criminal Justice, Saint Louis University, St. Louis, Missouri 19School of Natural Resources and Environment, Florida Museum of Natural History, University of Florida, Gainesville, Florida 20Postgraduate Ecology Course, Institute of Biology, Campinas State University, Campinas, S˜ao Paulo, Brazil 21National Center for Amazonian Biodiversity Research and Conservation, Chico Institute for Biodiversity Conservation, Manaus, Amazonas, Brazil 22S˜ao Paulo Forestry Institute, Bauru Experimental Station, S˜ao Paulo, Brazil 23Animal Biology Dept., State University of Campinas, Campinas, S˜ao Paulo, Brazil 24Department of Anthropology, Washington University in St. Louis, St. Louis, Missouri 25Post-graduate School, Biology Department, Federal University of Amazonas, Manaus, Amazonas, Brazil 26Wild Animal Reproduction Laboratory Institute of Biological Sciences, Federal University of Par´a, Par´a, Brazil 27Department of Anatomy & Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio 28Advanced Teachers Training Institute of Suriname, Leysweg 5, University of Suriname Campus, Paramaribo, Suriname and Green Heritage Fund, Suriname 29Department of Sociology and Anthropology, Missouri State University, Springfield, Missouri 30Department of Biology, Federal University of Sergipe, S˜ao Crist´ov˜ao, Sergipe, Brazil Neotropical monkeys of the genera Cacajao, Chiropotes,andPithecia (Pitheciidae) are considered to be highly arboreal, spending most of their time feeding and traveling in the upper canopy. Until now, the use of terrestrial substrates has not been analyzed in detail in this group. Here, we review the frequency of terrestrial use among pitheciin taxa to determine the ecological and social conditions that might lead to such behavior. We collated published and unpublished data from 14 taxa in the three genera. Data were gleaned from 53 published studies (including five on multiple pitheciin genera) and personal communications of unpublished data distributed across 31 localities. Terrestrial activity was reported in 61% of Pithecia field studies (11 of 18), in 34% of Chiropotes studies (10 of 29), and 36% of Cacajao studies (4 of 11). Within Pithecia, terrestrial behavior was more frequently reported ∗ Correspondence to: Adrian A. Barnett, Roehampton University–CREEA, Holybourne Avenue, London SW15 4JD, United Kingdom. E-mail: [email protected] Received 6 November 2011; revised 27 June 2012; revision accepted 2 July 2012 DOI 10.1002/ajp.22068 Published online xx XXXX xxxx in Wiley Online Library(wileyonlinelibrary.com). C 2012 Wiley Periodicals, Inc. 2 / Barnett et al. in smaller species (e.g. P. pithecia) that are vertical clingers and leapers and make extensive use of the understory than in in the larger bodied canopy dwellers of the western Amazon (e.g. P. irrorata). Terrestrial behavior in Pithecia also occurred more frequently and lasted longer than in Cacajao or Chiropotes. An apparent association was found between flooded habitats and terrestrial activity and there is evidence of the development of a “local pattern” of terrestrial use in some populations. Seasonal fruit availability also may stimulate terrestrial behavior. Individuals also descended to the ground when visiting mineral licks, escaping predators, and responding to accidents such as a dropped infant. Overall, the results of this review emphasize that terrestrial use is rare among the pitheciins in general and is usually associated with the exploitation of specific resources or habitat types. Am. J. Primatol. 00:1–22, 2012. C 2012 Wiley Periodicals, Inc. Key words: behavior; pitheciids; primates; terrestrial INTRODUCTION weight range 2–4.5 kg). Collectively known as While some extinct New World primates may “pitheciins,” these primates are extremely (Cacajao have been exclusively, predominantly, or partially and Chiropotes), or quite strongly (Pithecia), special- terrestrial [Rosenberger et al., 2009], all living ized dentally for the predation of immature seeds Neotropical species are highly adapted for an arbo- [Kinzey, 1992; Norconk et al., 2009; Rosenberger, real lifestyle [Heymann, 1998]. Nevertheless, there 1992; Teaford & Runestad, 1992]. The larger-bodied are examples of terrestrial use among several genera, Cacajao (uacaris) and Chiropotes (bearded platyrrhines suggesting that coming to the ground is sakis or cuxius,´ hereafter “cuxius”´ giving preference a response to specific local environmental factors. Po- to the local common name throughout much of the tential causes for such interpopulational differences geographic range of this genus: Barnett et al., in include habitat fragmentation [Cebus olivaceus: press-a), tend to inhabit the middle to upper strata of Fragaszy, 1986], specialized foraging adaptations the forest, through which they move using a mixture [Cebus apella: Haugaasen & Peres, 2009; Cebus li- of quadrupedal climbing and leaping along horizon- bidinosus: Spagnoletti et al., 2009], use of mineral tal substrates [Walker, 1996, 2005]. A key difference licks [e.g. Ateles belzebuth: Link et al., 2011a,b], co- between the genera is the occupation of flooded for- foraging with other (primarily terrestrial) mammals est ecosystems by many uacari populations, which [e.g. Cebus apella and Nasua nasua: Haugaasen & may place additional limitations on the potential Peres, 2008], and the relaxation of predation pres- for terrestrial behavior. The smallest sakis (Pithecia sure [Brachyteles hypoxanthus:Mourthe´ et al., 2007; pithecia) typically use lower to middle strata when Ateles spp.: Campbell et al., 2005]. traveling, which may be related to their morpholog- In other Neotropical primate populations, terres- ical specializations for vertical clinging and leaping trial activity may be an established, but infrequent [Walker, 2005]. Other Pithecia species (e.g. P. albi- element of the behavioral repertoire, and is almost cans, P. irrorata, P. monachus) occupy higher forest invariably related to the execution of three main canopy levels, are more quadrupedal, and more often activities—the retrieval of food items [Cebus apella leap and land horizontally (Janice Chism, unpub- and Saimiri sciureus, Silva & Ferrari, 2009], move- lished data vide Swanson-Ward and Chism, 2003; ment between discontinuous substrates [Alouatta Anthony Di Fiore and Eduardo Fernandez-Duque, caraya, Bicca-Marques & Calegaro-Marques, 1995; unpublished data vide Di Fiore et al., 2007). With the Brachyteles arachnoides: Dib et al., 1997], and spe- possible exception of P. irrorata, which may feed pre- cific social behaviors, such as play and resting dominantly on hard fruits [Palminteri, 2010], sakis [Brachyteles hypoxanthus: Tabacow et al., 2009]. The tend to have a more diverse diet that includes a use of terrestrial mineral licks is a characteristic of higher proportion of ripe fruit and young leaves than the behavior of many Amazonian atelids, for exam- uacaris and cuxius´ [Norconk, 2011]. ple [Campbell et al., 2005; Link et al., 2011a,b], and In addition to their tendency to occupy the mid- the
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