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Neotropical primates
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Permanent Link: http://ufdc.ufl.edu/UF00098814/00061
 Material Information
Title: Neotropical primates a newsletter of the Neotropical Section of the IUCNSSC Primate Specialist Group
Abbreviated Title: Neotrop. primates
Physical Description: v. : ill. ; 27 cm.
Language: English
Creator: IUCN/SSC Primate Specialist Group -- Neotropical Section
IUCN/SSC Primate Specialist Group -- Neotropical Section
Conservation International
Center for Applied Biodiversity Science
Publisher: Conservation International
Place of Publication: Belo Horizonte Minas Gerais Brazil
Belo Horizonte Minas Gerais Brazil
Publication Date: 12-2011
Frequency: quarterly
regular
 Subjects
Subjects / Keywords: Primates -- Periodicals -- Latin America   ( lcsh )
Primates -- Periodicals   ( lcsh )
Wildlife conservation -- Periodicals   ( lcsh )
Genre: review   ( marcgt )
periodical   ( marcgt )
serial   ( sobekcm )
Spatial Coverage: Brazil
 Notes
Additional Physical Form: Also issued online.
Language: English, Portuguese, and Spanish.
Dates or Sequential Designation: Vol. 1, no. 1 (Mar. 1993)-
Issuing Body: Issued jointly with Center for Applied Biodiversity Science, <Dec. 2004->
General Note: Published in Washington, D.C., Dec. 1999-Apr. 2005 , Arlington, VA, Aug. 2005-
General Note: Latest issue consulted: Vol. 13, no. 1 (Apr. 2005).
 Record Information
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: oclc - 28561619
lccn - 96648813
issn - 1413-4705
System ID: UF00098814:00063

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Neotropical Primates A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group Conservation International 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA ISSN 1413-4703 Abbreviation: Neotrop. Primates Editors Erwin Palacios, Conservacin Internacional Colombia, Bogot DC, Colombia Liliana Corts Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA Jlio Csar Bicca-Marques, Pontifcia Universidade Catlica do Rio Grande do Sul, Porto Alegre, Brasil Eckhard Heymann, Deutsches Primatenzentrum, Gttingen, Germany Jessica Lynch Alfaro, Institute for Society and Genetics, University of California-Los Angeles, Los Angeles, CA, USA Liza Veiga, Museu Paraense Emlio Goeldi, Belm, Brazil New s and Books Reviews Brenda Solrzano, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Founding Editors Anthony B. Rylands, Center for Applied Biodiversity Science Conservation International, Arlington VA, USA Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Editorial Board Bruna Bezerra, University of Louisville, Louisville, KY, USA Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK Adelmar F. Coimbra-Filho, Academia Brasileira de Cincias, Rio de Janeiro, Brazil Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA Stephen F. Ferrari, Universidade Federal do Sergipe, Aracaj, Brazil Russell A. Mittermeier, Conservation International, Arlington, VA, USA Marta D. Mudry, Universidad de Buenos Aires, Argentina Horcio Schneider, Universidade Federal do Par, Campus Universitrio de Bragana, Brazil Karen B. Strier, University of Wisconsin, Madison, WI, USA Maria Emlia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil Primate Specialist Group Chairman, Russell A. Mittermeier Deputy Chair, Anthony B. Rylands Coordinator, Special Section on Great Apes, Liz Williamson Regional Coordinators Neotropics Mesoamerica, Liliana Corts -Ortiz Andean Countries, Erwin Palacios and Eckhard W. Heymann Brazil and the Guianas, M. Ceclia M. Kierul, Mauricio Talebi and Fabiano R. de Melo Regional Coordinators Africa West Africa John F. Oates East Africa, David Mbora Regional Coordinator Madagascar Jrg U. Ganzhorn Regional Coordinators Asia China, Long Yongcheng Southeast Asia, Jatna Supriatna and Christian Roos South Asia, Sally Walker Layout: Kim Meek, Washington, DC IUCN/SSC Primate Specialist Grou p logo courtesy of Stephen D. Nash, 2002. Front cover: Wieds black-tufted-ear marmoset ( Callithrix kuhlii ), Una, Bahia, Brazil, 1985. Photo by Russell A. Mittermeier. is issue of Neotropical Primates was kindly sponsored by the Margot Marsh Biodiversity Foundation, 432 Walker Road, Great Falls, Virginia 22066, USA, and the Los Angeles Zoo, Director John R. Lewis 5333 Zoo Drive, Los Angeles, California 90027, USA.

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39 A HOWLER AND CAPUCHIN MONKEY DENSITIES IN RIPARIAN FORESTS ON ISLANDS AND ADJACENT SHORES ON THE UPPER PARAN RIVER, SOUTHERN BRAZIL Lucas M. Aguiar 1 Gabriela Ludwig 2 James J. Roper 3 Walfrido K. Svoboda 3 Italmar T. Navarro 4 Fernando C. Passos 3 1 Universidade Federal da Integrao Latino-Americana (UNILA), Foz do Iguau, Brasil. Email: lucas.aguiar@unila.edu.br; 2 Instituto Chico Mendes de Conservao da Biodiversidade (ICMBio), Centro Nacional de Pesquisa e Conservao de Primatas Brasileiros, Fundao Flora de Apoio a Botnica, Joo Pessoa, Brasil. 3 Universidade Federal do Paran (UFPR), Curitiba, Brasil; 4 Universidade Estadual de Londrina (UEL), Londrina, Brasil. Abstract ree primates ( Alouatta caraya Sapajus nigritus and Sapajus cay ) are found in riparian areas of the Upper Paran River in southern Brazil. Population densities of these three species were estimated from October 2004 through September 2005 by counts on linear transects in riparian forests on two riverine islands and adjacent shores in the states of Mato Grosso do Sul and Paran. A total of 397 sightings of these species were accumulated in 188 km of traversed transects. Alouatta caraya was the most abundant species on the large island (2.56 ind ha-1) and on the Mato Grosso do Sul side (0.84 ind ha -1 ). is den sity was greater than twice that of the sympatric S. cay (0.31 ind ha -1 ). Sapajus nigritus was the most abundant species on the Paran side (0.51 ind ha -1 ) followed by A. caraya (0.40 ind ha -1 ). e folivorous A. caraya was the most abundant in ooded forests, while the omnivorous Sapajus species were less so. Dierences in forests, conservation status, dispersal restrictions and autecology of the primates help explain dierences in primate abundance. Keywords: Alouatta caraya Sapajus cay Sapajus nigritus habitat fragmentation, population survey, primate conservation. Resumo Trs espcies de primatas ( Alouatta caraya Sapajus nigritus e Sapajus cay ) podem ser encontradas nas matas ciliares do Alto Rio Paran, sul do Brasil. Suas densidades populacionais foram estimadas atravs do mtodo das transeces lineares em matas ciliares de duas ilhas uviais e das margens opostas do rio, no limite entre os estados do Mato Grosso do Sul e Paran, durante outubro de 2004 a setembro de 2005. Obteve-se um total de 397 avistamentos de primatas ao longo de 188 km percorridos. Alouatta caraya foi a espcie mais abundante na maior ilha (2.56 ind ha -1 ) e na margem do Mato Grosso do Sul (0.84 ind ha -1 ). A densidade da espcie neste local foi maior que o dobro da densidade da espcie simptrica, S. cay (0.31 ind ha -1 ). Sapajus nigritus foi a espcie mais abundante na margem do Paran (0.51 ind ha -1 ), seguido de A. caraya (0.40 ind ha -1 ). A espcie folvora, A. caraya foi mais abundante na oresta de inundao, mais conservada, enquanto que Sapajus onvoro, foi mais abundante na oresta de terra rme. Diferenas entre a estrutura das orestas, grau de conservao, restries para disperso e autoecologia dos primatas ajudam a explicar as diferenas entre as abundncias encontradas. Palavras-chaves: Alouatta caraya Sapajus cay Sapajus nigritus fragmentao orestal, levantamento populacional, conser vao de primatas. Introduction Fragmentation may result in rapid population growth in mammal species whose population sizes, in other more di verse communities, would have been controlled by com petition or predation (Redford, 1992; Peres and Dolman 2000; Terborgh et al ., 2001; Link et al ., 2010). At least three hypotheses may explain these increased densities: (1) absence of predators, (2) ecological plasticity and (3) density compensation, in which the eects of isolation result in the elimination of some species (Redford, 1992; Glanz, 1996; Gonzlez-Sols et al ., 2001; Terborgh et al ., 2001). For example, in the Amazon, small and mediumsized primate species increase in abundance where larger

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40 species of the family Atelidae are preferentially hunted (Peres and Dolman, 2000). Also, greater densities in Al ouatta and Sapajus species may be found in degraded com munities in fragments and islands (Chiarello and Galetti 1994; Gonzlez-Sols et al ., 2001; Ludwig et al ., 2005; Martins, 2005; Almeida-Silva et al ., 2005; Link et al ., 2010). Islands may serve as natural experiments to examine the eects of isolation on mammal populations (Glanz, 1996; Terborgh et al ., 2001). For example, abundance of Alouatta seniculus increased in the absence of predators as well as with simplication of forests on articial islands (Terborgh et al ., 2001). Similarly, black-and-gold howler monkey ( Al ouatta caraya ) densities are greater on an island than the nearby shores of the Paran River in Argentina (Rumiz, 1990; Zunino et al ., 2001). However, islands in the Paran River are natural and have primate predators, such as large cats (Aguiar et al ., 2007; Ludwig et al ., 2007). On the is lands of the Paran River, with rich alluvial soils, two im portant factors may contribute to high howler population densities: (1) greater productivity of high-quality resources, such as fruits and young leaves, and (2) year-round re source availability (Janzen, 1974; Rumiz, 1990; Zunino et al ., 2001; Bravo and Sallenave, 2003). Although A. caraya population studies have taken place in the system of islands of the Middle Paran River (Rumiz, 1990; Zunino et al ., 2001), few studies include other pri mates in this area (Brown and Zunino, 1994) and in others portions of this river. Given the importance of understand ing local variation in primate abundances, the main goal of this study was to examine and compare densities of A. caraya Sapajus nigritus and Sapajus cay on forested islands and along the adjacent margins of the Upper Paran River in southern Brazil. Methods Study area Primates were studied in the Upper Paran River Protect ed Area in the southern Brazilian Atlantic Forest. Primate abundances were estimated on two islands and along the margins of the river near the city of Porto Rico in Paran, and near the city of Taquarussu in Mato Grosso do Sul (22'60"S and 53'18"W; Fig. 1). e region is sub tropical, with an average rainfall between 1,2001,300 mm (Romagnolo and Souza, 2000). Human impact has de graded the forests, although today the area is in process of recovery (Campos and Souza, 2002). e study area comprises two main forest types: alluvial, or ooded forests ( vrzeas ), that are found in the islands and ood plains on the Mato Grosso do Sul side of the river; and submontane (higher than 250 m above sea level) on the Paran side of the river. Alluvial forests ood annually and have low tree diversity and are dominated by pioneer species (Romagnolo and Souza, 2000; Campos and Souza, 2002). e canopy is open and low (1015 m, emergent to 25 m). Productivity is high due to the rich alluvial soils and so high-quality forage (leaves) is abundant and relatively constant for folivorous howler monkeys (Rumiz, 1990). Cecropia pachystachya is the dominant tree and the main food source for howler monkeys here (Ludwig et al ., 2008). Submontane forests are the most diverse and mature forests in the region in areas that do not ood (M. C. Souza, unpublished). How ever, productivity of resources used by folivorous primates is relatively lower and more seasonal (Rumiz, 1990). e canopy is more closed with trees of 15 m. Today, the submontane forest is nearly extinct in this region with only a few fragments remaining (Campos and Souza, 1997). Primates were counted on two islands and both margins of the river (Fig. 1). Mutum Island is the largest island (1,050 ha), near the river center (1,000 m from Paran, 700 m from Mato Grosso do Sul) and comprises a mosaic of alluvial forests, swamps, and patches of more preserved forests, and is dominated by the pioneer tree C. pachys tachya Carioca Island is smaller (360 ha), 600 m from Paran, 800 m from Mutum Island, and comprises a mosaic of degraded alluvial forests with few trees and dis continuous canopy with many vines. Humans and feral domestic pigs ( Sus scrofa ) have impacted the island. e shores of Mato Grosso do Sul comprise alluvial forests that are naturally narrow corridors above the dikes formed by the river. Today, they are fragmented and poorly preserved due to an increasing pressure from agriculture, cattle, re, and human settlements. Farther from the dikes, the forests are rapidly being replaced by pasture and marshes. Finally, the Paran shore has submontane forests and, despite some anthropic inuence, has continuous, wider stretches that retain most of the original forest structure (M. C. Souza, unpublished). Abundant palms ( Acrocomia aculleata and Syagrus romanzoanum ), and agriculture, including corn and cassava, are only on the Parana side of the river (L. M. Aguiar, personal observation). Figure 1. Location of the study area on the Upper Paran River, southern Brazil. X marks the transect locations on the river shore; MI: Mutum Island; CI: Carioca Island. Porto Rico: nearby city.

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41 Study animals ree species of primates are found in the region (Aguiar et al ., 2007). e black-and-gold howler monkey is found on both shores of the river, and is the only monkey on the islands. e black-horned capuchin ( S. nigritus ) is found on the Paran side of the river, and Azaras capuchin ( S cay ) on the Mato Grosso do Sul side of the river. e Paran river is a barrier for dispersal of both capuchins (Aguiar et al ., 2007). Monkeys are seldom hunted in the region and so populations are not responses to hunting pressure (Aguiar et al ., 2007). Capuchin taxonomy follows Alfaro et al (2011). Density estimates Linear transects with multiple counts (Buckland et al ., 1993; Ferrari, 2002) were used to estimate primate den sity. Due to the narrow riparian forests in various degrees of perturbation, transects were established to accompany the forest habitat and had to vary in length to t within these patches. Transect lengths were 1500 m on Mutum Island, 560 and 1260 m on Carioca Island, 1000 and 1010 m on the Mato Grosso do Sul shore, and 1000 and 1180 m on the Paran shore. Transects were walked once or twice each week from October 2004 through September 2005. Transects were walked at an average speed of 0.5 km h -1 between 06:0012:00 h, and between 14:0019:00 h. No transect was walked twice in the same day. At each sight ing, the perpendicular distance to the trail was measured (Bushnell distance meter or tape), and time, species and numbers of visible individuals were noted (measurable in dividuals following Marshall et al ., 2008). e distance to the most distant individual in each group was measured. e program Distance version 4.1 was used to estimate abundance using the size-biased sampling method, using a probability of 0.15 for signicance of regressions between clusters sizes and sighting distances to the clusters (Buck land et al ., 1993). Results A total of 397 sightings were recorded during about 500 h of walking over 188 km (Table 1). Howler monkey density varied between 0.402.56 ind ha -1 with the lowest den sities on the Paran side and on Carioca Island, and the greatest on the Mato Grosso do Sul side and Mutum Island. Capuchin monkey density varied between 0.31 ind ha -1 for S. cay in Mato Grosso do Sul and 0.51 ind ha -1 for S. nigritus in Paran. Discussion e ooded, and more conserved forests on Mutum Island are apparently the most favorable local habitats for A caraya such that their density is more than ve times that of the other locations. Primate density is similar in the other locations, although capuchin density was greater in more mature and conserved forests ( e.g. S. nigritus in Paran) and greater than the density of sympatric howlers. Indeed, howler density was lower than that of the capu chins in mature forests of Paran and in the most disturbed habitat of Carioca Island. Howler abundance, therefore, may be strongly inuenced by productivity (such as ood ed forests), while the more generalist capuchins do better in mature forests and more conserved habitats. We suggest that the ooded habitat in Mutum Island is important to maintain the extremely abundant C. pachystachya as a very important resource that allows greater population sizes in A. caraya In contrast, while often ooded, Carioca Island apparently cannot support similar population sizes there due to environmental degradation. A similar relationship of abundance, productivity and degradation has been found in the Middle Paran River (Rumiz, 1990; Brown and Zunino, 1994; Zunino et al ., 2001). Other factors may also inuence densities in this study area: 1) low predation and hunting pressure, 2) density compensation (Redford, 1992; Glanz, 1996; GonzlezSols et al ., 2001; Terborgh et al ., 2001) and 3) crowding (Lovejoy et al ., 1986). First, hunting pressure by humans is low and natural primate predators are less abundant in this region, probably due to the presence of humans. While predation is an important component of primate life his tories, predation as a constraint on primate population size has not been clearly demonstrated in most species (Isbell, Table 1. Sampling eort (distance walked in km), number of sightings, sighting rate (sightings km-1), average group (cluster) size, and density estimate (individuals ha-1) at four sampling locations on the Upper Paran River, in southern Brazil. Estimates-statistics Mutum Is. Carioca Is. Paran Mato Grosso do Sul A. caraya A. caraya S. nigritus A. caraya S. cay Distance 21 49 57 57 61 61 Sightings 99 42 45 52 111 48 Sighting rate 13.2 1.6 1.1 1.59 2.6 0.43 Group sizea 3.1 3.3 3.2 2.8 2.1 1.6 Density 2.56 0.63 0.40 0.51 0.84 0.31 Function Uni/Cos Hazard rate Uni Uni/Cos Half-normal Half-normal/Cos a Group size (average) was counted on the islands and estimated on the mainland using the program Distance. Coecient of variation (CV) varied between 15%. Eective width varied between 20 m ( S. cay ) and 32 m ( A. caraya in Paran).

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42 1994). Density compensation may also allow greater abun dance. Since the local primate community is depauperate, with never more than two co-occurring species in any one place, it is possible that reduced competition for resources and isolation due to fragmentation combine to favor in creased density. Also, other potential competitors for howl ers, such as capuchins and coatis are absent from the islands (Aguiar et al ., 2007). is distribution raises the question of why there are not three primate species, and coatis, at any given site, since they are all locally available?. Perhaps the river is an eective barrier for dispersal of capuchins and coatis, or ooded forests may not provide the addi tional resources (prey, fruit) that these omnivorous species require (Haugaasen and Peres, 2005; Aguiar et al ., 2011). e crowding eect (Lovejoy et al ., 1986) may also be im portant, since these primates are opportunists and general ists, and may have overlapping ranges. ey may coexist at relatively high densities in environmentally degraded areas due to dispersal limitation, such as on the islands. is is an important possibility, because it suggests that degraded areas may still provide resources to maintain large or dense populations. Usually, capuchins are more frugivorous and more resource generalists than howlers (Freese and Oppen heimer, 1981; Link et al. 2010). However, S. cay is not very abundant (in contrast to howlers), apparently because the ooded forest is not ideal habitat for capuchin species (Peres, 1989; Haugaasen and Peres, 2005). Riparian forest along the river in Mato Grosso do Sul is a narrow corridor and with a relatively small area for foraging. In contrast, S nigritus is more abundant on the Paran side of the river than is typical (Ludwig et al ., 2005; Martins, 2005; Almei da-Silva et al ., 2005). On the Paran side, the riparian forest corridor is wider, with more mature and better-preserved forest including many palm trees where they forage, as well has having cultivated crops that they may also consume (Ludwig et al ., 2005). ese complex interactions require autecological studies that examine the importance of each resource to better understand how these resources inuence abundance patterns. erefore, here, the abundance patterns of these three pri mate species suggest that forest structure and conservation status may be the main inuences regulating population size. Greater abundance may be explained by both, immi gration and reproduction (Begon et al ., 2006). Since howl ers can swim (Aguiar et al ., 2007) and then nd abundant resources, their populations will grow as long as resources are not limiting. If riparian areas are well protected, they can maintain populations of primates and other animals. We suggest that the interactions of density compensation, crowding, low hunting and predation pressures, and the extremely abundant Cecropia (for howlers) probably allow the unusually high densities. Although humans have frag mented the habitat, primates are still relatively abundant, which suggests that these are important populations for conservation, in contrast with the lower abundances of these species elsewhere (Ludwig et al ., 2005; Moura, 2007). us, populations along the Paran River are potentially important sources for regional maintenance of these spe cies. We recommend further study to specically tests the hypotheses presented here and thereby assure conservation of these primates. Acknowledgments We thank CNPq for scholarships to L. M. Aguiar, G. Ludwig and F. C. Passos, SESA-PR for their nancial support, and the ICMBio for a license provision. e man uscript beneted from the comments of A. G. Chiarello, Z. M. B. Hirano, E. L. A. Monteiro-Filho, J. E. SilvaPereira, R. F. Moro-Rios and two reviewers. References Aguiar, L. M., Ludwig, G., Svoboda, W. K., Hilst, C. L. S., Navarro, I. T. and Passos, F. C. 2007. Occurrence, local extinction and conservation of primates in the corridor of the Upper Paran River, with notes on other mammals. Rev. Bras. Zool. 24: 898906. Aguiar, L. M., Moro-Rios, R. F., Silvestre, T., Silva-Pereira J. E., Bilski, D. R., Passos, F. C., Sekiama, L. M. and Rocha, V. J. 2011. Diet of brown nosed coatis and cr ab-eating raccoons from a mosaic landscape with exotic plantations in southern Brazil. Stud. Neotrop. Fauna En vironm. 46: 153161. Alfaro, J. W., Boubli, J. P., Olson, L. E., Di Fiore, A., Wilson, B., Gutirrez-Espeleta, G. A., Chiou, K. L., Schulte, M., Neitzel, S., Ross, V., Schwochow, D., Nguyen, M. T. T., Farias, I., Janson, C. H. and Alfaro, M. E. 2011. Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys. J. Biogeogr 39: 272288. Almeida-Silva, B., Cunha, A. A., Boubli, J. P., Mendes, S. L. and Strier, K. B. 2005. Population density and verti cal stratication of four primate species at the Estao Bi olgica de Caratinga/RPPN-FMA, Minas Gerais, Brazil. Neotrop. Primates 13: 2529. Asensio, N., Arroyo-Rodrguez, V. and Cristbal-Azkarate, J. 2007. Feeding encounters between a group of a howler monkeys and white-nosed coatis in a small forest fragment in Los Tuxtlas, Mxico. J. Tropical Ecol. 23: 253255. Begon, M., Townsend, C. R., Harper, J. L. 2006. Ecol ogy: from individuals to ecosystems Blackwell Publishing, Malden. Bravo, S. P. and Sallenave, A. 2003. Foraging behavior and activity patterns of Alouatta caraya in the northeastern ar gentinean ooded Forest. Int. J. Primatol. 24: 825846. Brown, A. D. and Zunino, G. E. 1994. Hbitat, densidad y problemas de conservacin de los primates de Argentina. Vida Silvestre Neotropical 3: 3040. Buckland, S. T., Anderson, D. R., Burnham, K. P. and Laake, J. L. 1993. Distance sampling: estimating abun dance of biological populations Chapman and Hall, London.

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43 Campos, J. B. and Souza, M. C. 1997. Vegetao. In: A Plancie de Inundao do Alto Rio Paran: Aspectos fsicos, biolgicos e socioeconmicos A. E. A. M. Vazzoler, A. A. Agostinho and N. S. Hahn (eds.), pp.331342. EDUEM, Maring. Campos, J. B. and Souza, M. C. 2002. Arboreous vegeta tion of an Alluvial Riparian Forest and their soil relations: Porto Rico Island, Paran River, Brazil. Braz. Arch. Biol. Technol. 45: 137149. Chiarello, A. G. and Galetti, M. 1994. Conservation of the brown howler monkey in South-east Brazil. Oryx 28: 3742. Ferrari, S. F. 2002. Multiple transects or multiple walks? A response to Magnusson (2001). Neotrop. Primates 10: 131132. Freese, C. H. and Oppenheimer, J. R. 1981. e capu chin monkeys, Genus Sapajus In: Ecology and Behavior of Neotropical Primates A. F. Coimbra-Filho and R. A. Mittermeier (eds.), pp.331389. Academia Brasileira de Cincias, Rio de Janeiro. Glanz, W. E. 1996. e terrestrial mammal fauna of Barro Colorado Island: censuses and long-term changes. In: e Ecology of a tropical forest: seasonal rhythms and longterm changes E. G. Leigh, A. S. Rand and D. M. Wind sor (eds.), pp.455468. Smithsonian Institution Press, Washington. Gonzlez-Sols, J., Guix, J. C., Mateos, E. and Llorens, L. 2001. Population density of primates in a large fragment of the Brazilian Atlantic Rainforest. Biodiversity Conserv. 10: 12671282. Haugaasen, T. and Peres, C. A. 2005. Primate assemblage structure in amazonian ooded and unooded forests. Am. J. Primatol. 67: 243258. Isbell, L. A. 1994. Predation on primates: ecological pat terns and evolutionary consequences. Evol. Anthropol. 3: 6171. Janzen, D. H. 1974. Tropical Blackwater rivers, animals, and mast fruiting by Dipterocarpaceae. Biotropica 6: 69103. Link, A., Luna, A. G., Alfonso, F., Giraldo-Beltran, P. and Ramrez, F. 2010. Initial eects of fragmentation on the density of three Neotropical primates species in two low land forests of Colombia. Endang. Species Res. 13: 4150. Lovejoy, T. E., Bierregaard, R. O., Rylands, A. B., Mal colm, J. R., Quintela, C. E., Harper, L. H., Brown Jr., K. S., Powell, A. H., Powell, G. V. N., Schubart, H. O. R. and Hays, M. B. 1986. Edge and other eects of isolation on Amazon forest fragments In: Conservation Biology, the science of scarcity and diversity M. E. Soul (ed.), pp.257 285. Sinauer Associates Inc Publishers, Massachusetts. Ludwig, G., Aguiar, L. M. and Rocha, V. J. 2005. Uma avaliao da dieta, da rea de vida e das estimativas pop ulacionais de Sapajus nigritus (Goldfuss, 1809) em um fragmento no Norte do Estado do Paran. Neotrop. Pri mates 13: 1218. Ludwig, G., Aguiar, L. M., Miranda, J. M. D., Teixeira, G. M., Svoboda, W. K., Malanski, L. S., Shiozawa, M. M., Hilst, C. L. S., Navarro, I. T. and Passos, F. C. 2007. Cougar predation on Black-and-gold howlers on Mutum Island, Southern Brazil. Int. J. Primatol. 28: 3946. Ludwig, G., Aguiar, L. M., Svoboda, W. K., Hilst, C. L. S., Navarro, I. T., Vitule, J. R. S. and Passos, F. C. 2008. Comparison of the diet of Alouatta caraya (Primates, Atelidae) between a riparian island and mainland on the Upper Paran River, southern Brazil. Rev. Bras. Zool. 25: 419426. Marshall, A. R., Lovett, J. C. and White, P. C. L. 2008. Selection of Line-transect methods of estimating the den sity of group-living animals: lessons from the primates. Am. J. Primatol. 70: 452462. Martins, M. M. 2005. Density of primates in four semideciduous forest fragments of So Paulo, Brazil. Biodiver sity Conserv. 14: 23212329. Moura, A. C. A. 2007. Primate group size and abundance in the Caatinga Dry Forest, northeastern Brazil. Int. J. Primatol. 28: 12791297. Peres, C. A. and Dolman, P. M. 2000. Density compensa tion in Neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forests of varying productivity. Oecologia 122: 175189. Redford, K. H. 1992. e empty Forest. BioScience 42: 412422. Romagnolo, M. B. and Souza, M. C. 2000. Anlise o rstica e estrutural de orestas riprias do alto rio Paran, Taquaruu, MS. Acta Botanica Brasilica 14: 163174. Rumiz, D. I. 1990. Alouatta caraya : Population density and demography in northern Argentina. Am. J. Primatol. 21: 279294. Terborgh, J., Lopez, L., Nuez, P. V., Rao, M., Shahabud din, G., Orihuela, G., Riveros, M., Ascanio, R., Adler, G. H., Lambert, T. D. and Balbas, L. 2001. Ecological meltdown in predator-free Forest fragments. Science 294: 19231926. Zunino, G. A., Gonzlez, V., Kowalewski, M. M. and Bravo, S. P. 2001. Alouatta caraya : relations among habi tat, density and social organization. Primate Report 61: 3746.

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44 S A UM CASO DE USO ESPONTNEO DE FERRA MENTA POR UM MACACOPREGO CEBUS APELLA MANTIDO EM CATIVEIRO Miguel Angelo Monteiro Lessa Olavo de Faria Galvo Paulo Elias Gotardelo Audebert Delage Introduo Os macacos-prego so macacos do Novo Mundo que com pem o gnero Cebus (Rylands et al ., 2000). Eles so en contrados a partir de Honduras na Amrica Central at o nordeste da Argentina na Amrica do Sul (Fragaszy et al ., 2004b). Seu repertrio manipulativo bastante diversi cado. Logo nos primeiros meses de vida j manipulam e combinam objetos com superfcies e outros objetos (Fra gaszy et al ., 2004b). O desenvolvimento dessas aes ainda na infncia fator importante para o surgimento do uso de ferramentas no nal da juventude e incio da fase adulta (Resende et al ., 2008). O comportamento de usar ferra mentas ocorre quando um animal altera as propriedades fsicas de um objeto, substncia, superfcie ou qualquer outro alvo por meio da manipulao de outro objeto ex terno (St. Amant e Horton, 2008; Bentley-Condit e Smith, 2010). Episdios de uso espontneo de ferramentas por macacos do gnero Cebus so registrados em diferentes es pcies, sistemas ecolgicos e objetivos. Em cativeiro (zoolgicos e laboratrios) um macaco-prego adulto da espcie Cebus apella fatuellus utilizou um pedao de madeira para se defender dos ataques de outros membros do grupo (Cooper e Harlow, 1961). Um macho da espcie Cebus apella foi visto utilizando pedaos de alimentos, como batata, tomate ou banana como iscas para atrair os peixes para a margem e captur-los (Mendes et al ., 2000). Manipu lando as iscas na margem do rio ou arremessando dentro da gua foram as maneiras que os macacos desenvolveram para atrair os peixes. Em um estudo descritivo do comportamen to de Cebus apella mantidos em cativeiro foi observado dois tipos diferentes de uso de ferramentas (Serbena e Monteiro -Filho, 2002). No primeiro, o macaco-prego posicionava pedaos de laranja ou mamo em uma pedra grande e com uma pedra menor ele golpeava os alimentos. No segundo, a extremidade de um instrumento oco de madeira foi utilizada para cavar a terra em busca de formigas. Macacos da espcie Cebus paraguayanus foram observados usando galhos e folhas para buscar alimentos fora do alcance das mos e pernas (Giudice e Pav, 2007). E uma fmea adulta supostamente da espcie Cebus nigritus foi observada fabricando e usando um graveto para sondar um buraco provavelmente em busca de gua, e tambm utilizando pedras para quebrar frutos de casca dura e cubos de gelo contendo alimentos (Bortolini e Bicca-Marques, 2007). As primeiras observaes sistemticas de uso espontneo de ferramentas no gnero Cebus fora do ambiente de cativei ro foram feitas por Mannu e Ottoni (1996) e Rocha et al (1998). Nestes estudos, macacos da espcie Cebus apella usaram espontaneamente pedras como martelos para quebrar cocos ( Syagrus cf. romanzoanum ) apoiados em substratos planos. Ottoni e Mannu (2001), em um estudo mais siste mtico sobre este tipo de uso de ferramentas observaram que os macacos mais jovens (entre 2 e 5 anos de idade) eram os que mais quebravam cocos usando ferramentas em compa rao aos adultos. Para os autores, esta diferena pode estar relacionada ao monoplio de alimentos mais desejveis pelos dominantes e, tambm, pelo fato dos cocos estarem mais dis persos no ambiente o que restringe o controle de acesso pelos dominantes. No ambiente de vida livre diversas publicaes tambm tm mostrado as habilidades do gnero Cebus no uso de ferramentas. Na oresta tropical da Costa Rica um grupo de Cebus capucinus utilizou pedaos de madeira para atacar e matar uma cobra venenosa ( Bothrops asper ) (Boinski, 1988). Na regio de manguezal do Nordeste brasileiro, um macho adulto da espcie Cebus apella utilizou pedaos de conchas de ostras ( Crassostrea rhizophorae) para bater insistentemente na concha de outra ostra at quebr-la e se alimentar do molusco (Fernandes, 1991). Mas nas regies brasileiras do Cerrado e Caatinga onde h a maior concentrao de uso de ferramentas por populaes de macacos-prego em vida livre (Ottoni e Izar, 2008). A utilizao de pedras (martelos) para quebrar cocos ( Attalea spp ., Astrocaryum sp .) previamente posicionados em cima de uma superfcie slida (bigorna) constitui uma ati vidade comum entre os macacos da espcie Cebus libidinosus que habitam essas regies (Langguth e Alonso, 1997; Fragaszy et al ., 2004a; Moura e Lee, 2004). Alm de martelos as pedras desempenham outras funes na vida diria desses macacos. Podem funcionar como enxadas para cavar a terra ou espa lhar folhas secas do cho, como machados para cortar partes de galhos e piles para amolecer a terra facilitando o ato de cavar (Mannu e Ottoni, 2009). A utilizao de pedras e pedaos de madeira so os materiais mais comuns que os macacos-prego usam como ferramentas para alcanar alimentos que no podem ser alcanados direta mente. Registros de outros tipos de materiais como ferramentas so escassos na literatura primatolgica. O uso de gua como ferramenta, por exemplo, somente tem sido descrito at o mo mento em orangotangos ( Pongo abelii e Pongo pygmaeus ), chim panzs ( Pan troglodytes ) e humanos ( Homo sapiens ). Mendes et al (2007) investigaram o uso de gua como ferramenta em cinco fmeas de orangotangos ( Pongo abelii ) que viviam em um zoolgico. Apresentaram s fmeas um recipiente (26 5 cm) de acrlico transparente preenchido com um quarto de gua. Dentro do recipiente colocaram um gro de amendoim de modo que mesmo boiando na gua o alimento no podia ser alcanado diretamente pelos sujeitos da pesquisa. Para resolver o problema, ento, todos os sujeitos se dirigiram ao bebedouro, armazenaram a gua dentro da boca e cuspiram de volta dentro do tubo. Essa ao era repetida at aumentar o nvel da gua sucientemente para pegar o alimento com os dedos, por volta de trs a cinco vezes.

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45 Para comparar os desempenhos dos orangotangos no estudo de Mendes et al (2007), Hanus et al (2011) apresentaram a mesma tarefa para orangotangos ( Pongo pygmaeus ), chim panzs ( Pan troglodytes ), gorilas ( Gorilla gorilla ) e crianas humanas ( Homo sapiens ). No caso das crianas ao invs do bebedouro foi usada uma jarra contendo gua que deveria ser usada para conseguir pegar o amendoim. No geral apenas os gorilas no conseguiram resolver a tarefa, alguns chimpan zs e orangotangos conseguiram resolver e somente crianas a partir de seis anos de idade derramaram a gua no tubo para pegar o prmio. Neste artigo apresentamos um caso de uso espontneo de ferramenta por um macaco-prego ( Cebus apella ) mantido em cativeiro no qual freqente o forneci mento de material para manipulao. O macaco-prego uti lizou a gua do bebedouro para conseguir um alimento que no podia ser alcanado diretamente. Trata-se do primeiro registro em macacos (i.e. que possuem rabo) da utilizao deste tipo de material como ferramenta para conseguir um alimento de difcil acesso, sem que o animal tivesse algum tipo de treino para resolver tal problema. Materiais e mtodos O sujeito focal foi um macaco-prego chamado Nego com aproximadamente quatro anos de idade no dia da obser vao. Nego chegou Escola Experimental de Primatas (http://www.ufpa.br/eep/) no ano de 2005 oriundo do Ins tituto Brasileiro do Meio Ambiente e dos Recursos Natu rais Renovveis (IBAMA). Na poca da lmagem o animal pesava cerca de 2 kg e media aproximadamente 40 cm de corpo e 40 cm de cauda (hoje j est maior inclusive prestes a se tornar o dominante do grupo). O Nego e todos outros macacos da Escola Experimental de Primatas (EEP) partici pam diariamente de sesses experimentais. Ao todo a EEP contava com 16 macacos-prego. Suas tarefas so realizadas em monitores LCD de 17 sensvel ao toque (Elo Entuiti ve) voltadas aos estudos de aprendizagem e desenvolvimento de pr-requisitos de comportamentos cognitivos (Galvo et al ., 2002). O sujeito focal vivia em companhia de mais dois macacos machos adultos da mesma espcie em uma gaiola -viveiro de 2,50 2,50 2,50 m., construda de tubos e tela metlica galvanizada, e cava sobre uma base de alvenaria. Mais trs gaiolas-viveiro semelhantes estavam lateralmente posicionadas uma do lado da outra. A aproximadamente 1m de distncia do topo das gaiolas havia uma cobertura de telha de barro que media 20,0 3,0 m. No interior de todas as gaiolas, inclusive a do sujeito focal, havia plataformas de madeira a 1 m e a 2 m do solo. Sobre a plataforma mais alta na parte coberta cava uma caixa de madeira medindo 0,47 0,49 0,47 m, com vrias entrada e sadas. Em todas as gaiolas havia bebedouros de bico de ao posicionados a 2 m do solo que eram acionados por presso. Anexas a uma das laterais de cada gaiola se encontravam quatro gaiolas de conteno (0,60 0,50 0,50 m), com portas de correr que davam acesso ao interior da gaiola e um suporte (0,24 0,33 0,24 m) utilizado para colocar uma bandeja com alimen to. Os macacos eram alimentados uma vez ao dia no pero do da tarde. A dieta era composta por rao para primatas (Megazoo P18), frutos variados (banana, ma, melo, me lancia, laranja, manga, abacate, milho verde), legumes e verduras (pepino, cenoura, beterraba, batata doce), ovos, e bolachas tipo cream-cracker. Para suplementar a dieta, os macacos recebem semanalmente um suplemento vitamnico (Revitam Jnior BIOLAB). A EEP conta com uma mdica veterinria que avalia perio dicamente a sade dos animais, coleta fezes e sangue para exames laboratoriais, e efetua as medidas prolticas reco mendadas. No prprio ambulatrio veterinrio da EEP ela atende prontamente aos casos de urgncia como ferimen tos, diagnostica e trata eventuais doenas. Sua participao tambm essencial no planejamento da dieta normal para os macacos saudveis e dieta especial para os em tratamen to. A EEP tambm conta com um prossional responsvel pela manuteno do biotrio, que envolve principalmente a higiene do ambiente e a alimentao dos animais. As condi es de alojamento, manejo, alimentao, cuidados veteri nrios e os procedimentos experimentais que so adotados na EEP foram aprovados junto ao IBAMA (Inscrio no IBAMA 207419; Cdigo Unidade/Convnio 381.201-4) e junto ao Comit de tica em Pesquisa com Animais da Universidade Federal o Par (CEPAE), mediante o docu mento CEPAE-UFPA: PS001/2005. O ambiente do sujei to era enriquecido diariamente com objetos manipulveis (p. ex., garrafas plsticas, papelo, correntes de ao e tubos de PVC). A garrafa pet utilizada nas lmagens foi uma garrafa de gua mineral de 500 ml sem tampa, medindo aproximadamente 17 cm de altura, 6,5 cm de dimetro do corpo e 3 cm de dimetro do bocal. Procedimento Uma observao casual de utilizao espontnea de ferra menta para alcanar alimento de difcil acesso foi lmada pelo primeiro autor. O sujeito experimental utilizou a gua do bebedouro para obter farelo de bolacha do tipo gua e sal grudado no fundo de uma garrafa pet. A partir dessa ob servao seguiu-se uma segunda observao na qual foram mantidas as mesmas condies em que a utilizao da fer ramenta ocorreu anteriormente. Na segunda observao, o primeiro autor prendeu os dois membros do grupo nas gaiolas de conteno, deixando apenas o sujeito experimen tal solto na gaiola-viveiro. Antes de entregar a garrafa pet ao macaco, o primeiro autor colocou alguns farelos de bolacha dentro da garrafa e pingou algumas gostas de gua mineral dentro da garrafa para xar o farelo no fundo. Tanto a gar rafa quanto a bolacha foram semelhante observao ante rior. Com o material pronto, o primeiro autor entregou a garrafa ao macaco e logo em seguida realizou a lmagem da utilizao de ferramenta. Resultados Na observao casual, aps um dos membros do grupo (o dominante) ter se desinteressado de uma garrafa de plstico anteriormente depositada na gaiola pelo tratador, o sujeito

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46 experimental (Nego) se aproximou dela, agarrou-a com as mos e lambeu algumas vezes na parte de dentro do bocal. Em seguida, o sujeito experimental prendeu o bocal da gar rafa entre as mandbulas e transportou-a at o bebedouro. Um deslocamento de aproximadamente 3 metros de dis tncia. Chegando ao lado do bebedouro, o sujeito sentou -se na plataforma e com uma das mos segurou a garrafa pelo bocal posicionando-o em direo ao bebedouro. Com a outra mo pressionou o dispositivo do bebedouro para a liberao da gua. O sujeito pressionou o dispositivo do bebedouro por aproximadamente dois segundos, introdu zindo apenas uma pequena quantidade de gua dentro da garrafa. Em seguida, segurou a garrafa com as duas mos, bateu levemente o fundo da garrafa na plataforma e lambeu o interior do bocal. Na sequncia ergueu a garrafa com as mos (a garrafa formava um ngulo de aproximadamente 30 com o poleiro), posicionando o gargalo em frente a sua boca e, ento, bebeu o lquido que fora depositado dentro do objeto (Fig. 1). Como ainda restavam alguns farelos no fundo da garrafa, o sujeito repetiu a ao. Mas, desta vez Figura 1. Observao casual do macaco-prego ( Cebus apella ) macho sub-adulto utilizando a gua do bebedouro como ferramenta. Filma gem do primeiro autor, em 02 de agosto de 2007.

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47 alm de bater levemente o fundo da garrafa na platafor ma, ele balanou a garrafa presa nas mandbulas pelo bocal antes de beber o lquido. A durao deste episdio, isto a partir do momento em que o sujeito se aproxima da garrafa at o momento em que ele bebe o lquido pela segunda vez, foi de 2 minutos e 17 segundos. Na segunda observao, aps receber do primeiro autor a garrafa com farelo de bolacha grudado no fundo, o su jeito prontamente se deslocou em direo ao bebedouro. Ele exibiu um repertrio comportamental semelhante ao que fora realizado na primeira observao: (a) sentou-se ao lado do bebedouro, (b) posicionou o gargalo da garrafa em frente ao bebedouro, (c) colocou apenas uma pequena quantidade de gua dentro da garrafa e (d) bebeu o lquido (Fig. 2). Porm, desta vez ele no bateu com a garrafa na plataforma nem a balanou como fez na observao ante rior. A durao deste episdio, isto do momento em que ele recebe a garrafa do primeiro autor at o momento em que bebe o lquido, foi de 16 segundos. Figura 2. Replicao da primeira observao do macaco-prego utilizando a gua do bebedouro como ferramenta. Filmagem do primei ro autor, em 17 de Agosto de 2008. As lmagens das duas observaes podem ser vistas atravs dos sites: http://www.youtube.com/ watch?v=EP1BaKRHZTw http://www.youtube.com/watch?v=dFJ0rGtqyPU

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48 Discusso Observaes do uso espontneo de ferramentas por dife rentes espcies de macacos-prego mostram o quanto este comportamento caracterstico do gnero Cebus Fatores comportamentais e ambientais contribuem para o surgi mento do comportamento de usar ferramentas. A habilida de que os macacos-prego possuem de manipular e combi nar objetos juntamente com algum nvel de terrestrialidade representam os fatores comportamentais (Fragaszy et al ., 2004b). Entre os fatores ambientais destacam-se o grau de provisionamento, o baixo risco de predao (Ottoni e Izar, 2008), e a presena de objetos adequados que possam assu mir a funo de ferramenta (Rocha et al ., 1998). No entanto, a maioria dos relatos de uso de ferramentas no gnero Cebus incluem pedras e pedaos de madeira como os materiais mais comuns. A utilizao de outros tipos de materiais como ferramenta escasso entre os macacos deste gnero e tambm entre os grandes primatas. Embora haja relatos de que orangotangos ( Pongo abelii e Pongo pyg maeus ), chimpanzs ( Pan troglodytes ) e crianas humanas ( Homo sapiens ) utilizem a gua como ferramenta para al canar determinado objetivo (Mendes et al ., 2007; Hanus et al ., 2011). O presente estudo o primeiro entre os macacos (i.e., pri matas com rabo) a registrar o uso espontneo de gua do bebedouro como ferramenta para conseguir um alimento de difcil acesso. Com o alimento preso no fundo da gar rafa plstica, o sujeito experimental no tinha ao seu redor nenhum outro tipo de ferramenta disponvel a no ser uti lizar a gua para destacar o alimento do fundo. De acordo com a classicao dos nveis de uso de ferramentas propos ta por Fragaszy et al (2004b), o sujeito experimental exibiu uma relao com o objeto no nvel de Primeira-Ordem/ Esttico, pois combinou um objeto (garrafa plstica) com outro objeto xo (bebedouro) para conseguir o alimento. Na primeira observao, o macaco-prego levou pouco mais de dois segundos para resolver a tarefa, mas na segunda observao esse tempo caiu para apenas 16 segundos. Essa diferena na latncia entre tentativas tambm foi observada nos estudos de Mendes et al (2007) e Hanus et al (2011) com grandes primatas. O episdio de uso espontneo de ferramenta tratado aqui uma demonstrao da variedade de atividades manuais e da exibilidade cognitiva que so caractersticas marcantes entre os macacos do gnero Cebus (Fragaszy et al ., 2004b). Westergaard e Fragaszy (1985) observaram algo semelhan te ao que registrado aqui. Aps fornecer diversos tipos de objetos manipulveis aos macacos-prego ( Cebus apella ) cativos, os autores zeram o primeiro registro do uso de uma colher de plstico para coletar gua e levar boca em macacos do Novo Mundo. Portanto, tanto o trabalho de Westergaard e Fragaszy (1985) como a observao trata da aqui demonstram a importncia da presena de obje tos manipulveis dentro dos recintos dos macacos-prego. Fortalece, tambm, a ideia de que a manuteno de animais em um ambiente que crie oportunidades para a emisso de comportamentos tpicos para aquela espcie um fator essencial quando se leva em conta a melhoria da qualidade de vida desses animais (Celli et al ., 2003; Bortolini e Bicca -Marques, 2007). O registro de uso de ferramentas feito aqui juntamente com o registro feito por Westergaard e Fragaszy (1985) chamam a ateno no somente para o uso de objetos manipulveis como parte de um programa de enriquecimento ambiental. Alm de proporcionar um padro comportamental tpico do gnero, os objetos manipulveis criam oportunidades para que comportamentos criativos e inditos sejam desco bertos no cativeiro. Agradecimentos Agradecemos ao CNPQ pela bolsa de mestrado cedida ao primeiro autor, ao Olavo de Faria Galvo e Romariz da Silva Barros pela dedicao ao cuidado dos macacos-prego mantidos na Escola Experimental de Primatas e ao Edilson Pastana (tratador dos animais). Miguel Angelo Monteiro Lessa Mestre em Teoria e Pes quisa do Comportamento pela Universidade Federal do Par, R. Augusto Corra, 1, Laboratrio de Psicologia Ex perimental, Belm PA, CEP: 66075110, e-mail: , Olavo de Faria Galvo Professor Titular do Programa de Pos-graduao em Teoria e Pes quisa do Comportamento, Universidade Federal do Par, , Paulo Elias Gotardelo Au debert Delage Doutor em Teoria e Pesquisa do Compor tamento pela Universidade Federal do Par, . Referncias Bentley-Condit, V. e Smith, E. O. 2010. Animal tool use: current denitions and an updated comprehensive cata log. Behaviour 147: 188221. Boinski, S. 1988. Use of a club by a wild White-faced ca puchin to attack a venomous snake. Am J Primatol 14: 177180. Bortolini, T. S. e Bicca-Marques, J. C. 2007. A case of spontaneous tool-making by a captive capuchin monkey. Neotrop Primates 14(2): 7476. Celli, M. L., Tomonaga M., Udono T., Teramoto M. e Nagano K. 2003. Tool use task as environmental enri chment for captive chimpanzees. Appl. Anim. Behav. Sci 81: 171182. Cooper, L. R. e Harlow, H. F. 1961. Note on a Cebus monkeys use of a stick as a weapon. Psychos Rep 8: 418. Fernandes, M. E. B. (1991). Tool use and predation of oysters ( Crassostrea rhizophorae ) by the tufted capuchin, Cebus apella apella in brackish water mangrove swamp. Primates 32(4): 529531.

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49 Fragaszy, D. M. e Adams-Curtis, L. E. 1991. Generative aspects of manipulation in tufted capuchin monkeys ( Cebus apella ). J Comp Psychol 105(4): 387397. Fragaszy, D. M, Izar, P., Visalberghi, E., Ottoni, E. B. e Oliveira, M. G. 2004a. Wild capuchin monkeys ( Cebus libidinosus ) use anvils and stone pounding tools. Am J Primatol 64: 359366. Fragaszy, D. M., Visalberghi, E. e Fedigan, L. M. 2004b. e Complete Capuchin: e Biology of the Genus Cebus Cambridge University Press, Cambridge. Galvo, O. F., Barros, R. S., Goulart, P. R. K., Mendona, M. B. e Rocha, A. C. 2002. Escola experimental de pri matas. Estud Psicol 7: 361370. Giudice, A. M. e Pav, R. 2007. Cebus paraguayanus in zoos: the spontaneous expression of species-specic beha viors. Neotrop Primates 14(2):6571. Hanus, D., Mendes, N., Tennie, C. e Call, J. (2011). Com paring the performances of apes ( Gorilla gorilla Pan tro glodytes Pongo pygmaeus ) and human children ( Homo sa piens ) in the oating peanut task. Plos One 6(6): e19555. Langguth, A. e Alonso, C. 1997. Capuchin monkeys in the Caatinga: tool use and food habits during drought. Neotrop Primates 5(3):7778. Mannu, M. e Ottoni, E. 1996. Observaes preliminares das tcnicas de forrageamento e uso espontneo de fer ramentas por um grupo de macacos-prego ( Cebus apella Primates -Cebidae) em condies de semi-cativeiro. Anais de Etol 14: 384. Mannu, M. & Ottoni, E. B. 2009 e enhanced tool-kit of two groups of wild bearded capuchin monkeys in the ca atinga: tool making, associative use, and secondary tools. Am J Primatol 71: 242251. Mendes, F. D. C., Martins, L. B. R., Pereira, J. A. e Marque zan, R. F. 2000. Fishing with a bait: a note on behavioral exibility in Cebus apella. Folia Primatol 71:350352. Mendes, N., Hanus, D. e Call, J. 2007. Raising the level: orangutans use water as a tool. Biol Lett 3: 453455 Moura, A. C. A. e Lee, P. 2004. Capuchin stone tool use in caatinga dry forest. Science 306: 1909. Novak, M. A. e Suomi, S. 1988. Psychological well-being of primates in captivity. Am Psychol 43:765773. Ottoni, E. B. e Mannu, M. 2001. Semi-free ranging tufted capuchin monkeys ( Cebus apella ) spontaneously use tools to crack open nuts. Int J Primatol ., 22 (3): 347358. Ottoni, E. B. e Izar, P. 2008. Capuchin monkey tool use: overview and implications. Evo Anthropol 17:171178. Resende, B. D., Ottoni, E. B. e Fragaszy, D. M. 2008. Ontogeny of manipulative behavior and nut-cracking in young tufted capuchin monkeys ( Cebus apella ): a percep tionaction perspective. Dev Sci 11:812824. Rocha, V. J., Reis, N. R. e Sekiama, M. L. 1998. Uso de ferramentas por Cebus apella (Linnaeus) (Primates, Cebi dae) para a obteno de larvas de Coleoptera que parasi tam sementes de Syagrus romanzoanum Rev Bras Zool 15: 945950. Rylands, A. B., Schneider, H., Langguth, A., Mittermeier, R. A., Groves, C. P., e Rodriguez-Luna, E. 2000. An assessment of the diversity of New World Primates. Neo trop Primates 8: 6193. Serbena, A. L. e Monteiro-Filho, E. L. A. 2002. A behavio ral description of captive young capuchin monkey ( Cebus apella ). Rev Etol 4(2): 109116. St. Amant, R. e Horton, T. E. 2008. Revisiting the deni tion of animal tool-use. Anim. Behav 75: 11991208. Westergaard, G. C., e Fragaszy, D. M. 1985. Eects of ma nipulatable objects on the activity of captive capuchin monkeys ( Cebus apella ). Zoo. Biology 4: 317 FIRST OBSERVATIONS OF TERRESTRIAL TRAVEL FOR OLALLAS TITI MONKEY ( CALLICEBUS OLALLA E ) Jess Martnez Robert B. Wallace Introduction Primates are characterized by a morphology and anatomy that clearly shows adaptations for an arboreal life includ ing climbing, brachiating and swinging abilities (Chivers, 1991). Marked terrestrial habits are present in some Catar rhini members such as Mandrillus, Papio and Macaca in the Old World. Observations of terrestrial behaviors were also reported for some essentially arboreal Neotropical primate species such as Alouatta, Cebus, Ateles and Brachyteles to obtain some food, water or minerals and/or for geographic dispersion (Dib et al. 1997; Emmons, 1999; Mandujano et al. 2004; Almeida Silva et al. 2005; Campbell et al 2005; Mourthe et al. 2007; Pozo-Montuy & Serio-Silva, 2007). is last point is very important in fragmented forest habitats where monkeys move on the ground to reach new patches of forest but in so doing expose them selves to increased predation risks. As such, increases in forest fragmentation may aect primate conservation and survival beyond just the immediate eects of habitat loss. Olalla brothers titi monkey ( Callicebus olallae ) has one of the most restricted distribution ranges of Neotropical primate species inhabiting a small naturally fragmented forest-savanna area in the southwestern portion of the Beni department in Bolivia, almost exclusively within the river ine forest of Yacuma River. Initial work on this species con centrated on their distribution, demography and taxonomy (Barreta et al. 2007; Felton et al ., 2006; Lopez-Strauss & Wallace, in prep; Martinez & Wallace, 2007). To better un derstand the ecological requirements of this primate a be havioral ecology survey was initiated in 2007. In this note we present a series of observations concerning terrestrial movements of these monkeys obtained during this study.

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50 Methods e study site was at La Asunta, a cattle ranch located along the Yacuma River where, according to previous distribu tional knowledge, a number of C. olallae groups occurred (Figure 1). Two general types of forest habitats are present: gallery and fragmented forest, with the latter more evident at greater distances from the river. In July 2007 two groups inhabiting gallery forest and fragmented forest respectively, were chosen for study. Primate observations were made from 06:30 to 18:00 h, searching for study groups at sun rise and then attempting to follow them all day. We reg istered places visited frequently by the groups in order to record resting, feeding and sleeping sites. Results Observations 1 and 2 Early on in the habituation phase, the original fragmented forest group of ve individuals (Quinteto, Fig. 1) aban doned their territory when two groups one of squirrel monkeys ( Saimiri boliviensis ) and another of night mon keys ( Aotus azarae ) arrived in the forest patch. Individu als of this group were observed travelling to and between several of the forest patches adjacent to their original site, covering distances by ground of 5 to 20 m. During these displacements, the titi monkeys remained some time at the edge of the forest before jumping to the ground and jump ing quickly with arms and legs moving together and the tail lifted. Upon reaching the adjacent forest patch the leading titi monkey, usually the adult male, waited for the rest of the group in a tree on the edge of the patch before together moving o in the forest. Similar observations were recorded for gallery forest group (Rio group, Fig. 1) following the burning of a grassland area next to the forest, which forced the two adult individu als of the group to search for a new territory. e two mon keys were observed travelling along the ground between forest patches covering greater distances than in the previ ous case (around 40 m) due the isolation of forest islands although they looked for forest connections to avoid the ground whenever possible. Observation 3 As the original groups mentioned in observations 1 and 2 were not yet habituated, other groups were selected for study in fragmented and gallery forests, Pistero and Figure 1. Location of La Asunta and observed Callicebus olallae groups.

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51 Ribereo, respectively. e Pistero group inhabited a highly fragmented forest area consisting of several forest islands lo cated near each other including three larger islands. Initial ly, this group was observed in the largest forest patch with the highest trees and this was assumed to be the groups entire home range. However, during the course of the study we observed the group in neighboring and isolated forest islands accessible only by ground displacements (Figure 2). Terrestrial displacements were rst conrmed when the group was spotted moving along a wire fence located in the middle of the group territory dividing two cattle camps. When terrestrial the monkeys showed the same jump ing style of movements previously described. In total, we obtained 100 observations of these terrestrial movements from September 2007 to March 2008. e mean distance covered was 10 m (DS=4; range 5 m), and although these displacements represent a low proportion of the total movement records (7 %), it is signicant for a Neotropical primate. Finally, of 11 sites where terrestrial movements were reported in the Pistero group territory, in all except three cases the movements were in both directions (see white arrows in Fig. 2). Conclusions Titi monkeys are arboreal and previous studies on the di verse Callicebus genus show very low percentages of activi ties made at ground level related principally to individuals playing, falling and casual predation of insects (1%, Kinzey, 1981). According to their distribution, most of the Calli cebus species inhabit continuous forest areas with high veg etation density (Anderson, 1997; Hershkovitz 1990; Mar tinez & Wallace, 2010; Van Roosmalen et al. 2002). e naturally fragmented forest-savanna inhabited by C. olallae (Martinez & Wallace, 2007) clearly necessitates frequent terrestrial travel during ranging behavior, as was previously suggested by Felton and colleagues (2006) and conrmed by our observations. Even if individuals inhabit large con tinuous forest areas, eventually they may need to travel terrestrially to look for new areas when they reach sexual maturity and form new groups (Kinzey, 1981; Wright, 1986). In all cases the monkeys travelled the shortest terres trial route between neighboring forested areas showing an evident eort to reduce the predation risks associated with terrestrial travel. e rst two observations where longer distances were covered must represent extreme risks given the small size of these primates and the diverse carnivore community associated with these forests. Indeed, when iso lated small trees are on pathways to large forest areas, the monkeys climb them making their displacement in stages instead of passing directly from one forest patch to another. In naturally fragmented habitats, terrestrial movements of monkeys may not always be related to terrestrial-based feeding or drinking behavior but also due to ranging re quirements. As the worlds forests become more fragment ed due to human intervention these terrestrial movements may become more commonplace in primate species that normally occur in more continuous forests increasing ex position to predation risks. Jess Martnez Wildlife Conservation Society, Casilla 3 35181 SM, La Paz, Bolivia, e-mail: , and Robert B. Wallace Wildlife Conservation Society, 185th & Southern Boulevard, Bronx, NY 10460, USA, e-mail: References Almeida Silva B., P.G. Guedes, J.P. Boubli, K.B. Strier. 2005. Deslocamento terrestre e o comportamento de beber em um grupo de barbados ( Alouatta guariba clami tans ) em Minas Gerais, Brasil. Neotrop. Primates 13:13. Anderson S. 1997. Mammals of Bolivia: taxonomy and distribution. Bull. Am. Mus. Nat. His New York. Barreta J. 2007. Caracterizacin gentica de dos especies de monos tit Callicebus olallae y Callicebus modestus del departamento del Beni. Informe Tcnico. Wildlife Con servation Society & Instituto de Biologa Molecular y Biotecnologa, La Paz, Bolivia. 15 pp. Campbell C. J., F. Aureli, C. A. Chapman, G. RamosFernndez, K. Mathews, S. E. Russo, S. Suarez, L. Vick. 2005. Terrestrial behavior of Ateles spp. Int. J. Primatol 26(5): 10391051. Chivers D. J. 1991. Species dierences in tolerance to envi ronmental change. In: Primate responses to environmental changes Box, H. O. (Ed.). pp. 537. Chapman and Hall. London. Dib L. R. T., A. S. Oliva, K. B. Strier. 1997. Terrestrial travel in muriquis ( Brachyteles arachnoides ) across a forest clearing at the Estacao Biologica de Caratinga, Minas Gerais, Brazil. Neotrop. Primates 5(1): 89. Emmons, L., F. Feer. 1990. Neotropical Rainforest Mam mals Chicago and London: e University of Chicago Press, USA. Figure 2. Map of the Pistero groups territory including reported terrestrial travel routes between forest fragments.

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52 Felton A., A. M. Felton, R. B. Wallace, H. Gmez. 2006. Identication, distribution and behavioral observations of the titi monkeys Callicebus modestus Lnnberg 1939, and Callicebus olallae Lnnberg 1939. Primate Cons 20: 4046. Hershkovitz P. 1990. Titis, new world monkeys of the genus Callicebus (Cebidae, Platyrrhini): A preliminary taxonomic review. Fieldiana Zool ., New Series 55: 1109. Kinzey W. G. 1981. e titi monkeys, genus Callicebus In: Ecology and behavior of Neotropical primates CoimbraFilho A.F., Mittermeier R.A. (eds.).Vol 1. pp. 241276. Academia Brasileira de Ciencias. Rio de Janeiro. Lpez-Strauss H., R. B. Wallace. Submitted. Density esti mates of two Bolivian primate endemics, Callicebus olallae and C. modestus Submitted to Mastozoologia Neotropical Mandujano S., L. A. Escobedo-Morales, R. Palacios-Silva. 2004. Movements of Alouatta palliata among forest frag ments in Los Tuxtlas, Mexico. Neotrop. Primates 12(3): 126131. Martinez J., R. B. Wallace. 2007. Further notes on the distribution of endemic Bolivian titi monkeys, Callice bus modestus and Callicebus olallae Neotrop. Primates 14: 4754. Martnez J., R. B. Wallace. 2010. Pitheciidae. In: Mamferos medianos y grandes de Bolivia : distribucin, ecologa y con servacin Wallace R.B., D. Rumiz & H. Gomez (eds.). pp. 305330. Editorial: Centro de Ecologa y Difusin Simn I. Patio, Santa Cruz, Bolivia. Mourthe I. M., D. Guedes, J. Fidelis, J. P. Boubli, S. L. Mendes, K. B. Strier. 2007. Ground use by northern muriquis ( Brachyteles hypoxanthus ). Am. J. Primatol 69:706712. Pozo Montuy G., J. C. Serio-Silva. 2007. Movement and resource use by a group of Alouatta pigra in a forest frag ment in Balancn, Mxico. Primates 48: 102107. Van Roosmalen M. G. M., T. van Roosmalen, R. A. Mit termeier. 2002. A taxonomic review of the titi monkeys, genus Callicebus omas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus ste phennashi from Brazilian Amazonia. Neotrop. Primates 10: 152. Wright P. C. 1986. Ecological correlates of monogamy in Aotus and Callicebus Pp. 159167. In: Primate ecology and conservation. Else J. & P. C. Lee (eds.). Cambridge University. New York. EXTRAGROUP COPULATIONS IN ALOUATTA GUARIBA CLAMITANS Karine Galisteo Diemer Lopes Jlio Csar Bicca-Marques Howler monkeys often live in unimale-multifemale or multimale-multifemale cohesive groups in which the alpha male may monopolize estrus females, although females may mate promiscuously with subordinate and extragroup males (Kowalewski and Garber, 2010; Di Fiore et al., 2011). Extragroup copulations (EGCs) have been reported for A. arctoidea (Agoramoorthy and Hsu, 2000), A caraya (Kowalewski and Garber, 2010), A. guariba clamitans (Fialho and Setz, 2007), A. palliata (Glander, 1992), and A. pigra (Van Belle et al., 2008). EGCs in Alouatta spp. have been related to a female strategy to increase paternity confusion (both inside and outside the group) and decrease the risk of infanticide following alpha male takeover (Kow alewski and Garber, 2010) and to female choice of higher quality or unfamiliar males (Fialho and Setz, 2007). Con sidering that fertility and compatibility may vary among males, EGCs may also maximize the reproductive success of promiscuous females (Reeder, 2003). ese hypotheses are not mutually exclusive. Here we report seven EGCs between an adult male brown howler monkey ( Alouatta guariba clamitans ) from a group monitored from dawn to dusk during 26 days from Janu ary to July 2011 in a ca. 1-ha forest fragment (30S, 51W; ca. 45 m a.n.s.l.) in Itapu District, Viamo, state of Rio Grande do Sul, Brazil, with an adult female from a neighboring group. In January, our study group was composed of six individuals: an adult male (Jorge), two adult females, one juvenile, and two infants. An adult female died electrocuted in a power line in March. In May, a birth increased group size to six individuals again. Also, the juvenile was classied as subadult and the infants as juveniles beginning this month. e neighboring group was composed of, at least, four individuals, including two adult males, an adult female (Jane), and a subadult male. We have no information about the degree of relatedness between individuals both within and between groups. e forest fragments that they inhabited are separated by a 20 m-wide dirty road. Intergroup interactions were witnessed between April and July. ese are described in chronological order below. When Jorge reached the canopy, the neighboring adult males chased him back to the post. Jorge rubbed his chin at the post and was supplanted by a male. en, the male also rubbed his chin in the same place, while Jorge observed him from the electric wire. When the adult male left the pole and returned to a place behind Jane in the canopy, Jorge attempted to approach her again and was once more chased by her male mates. Finally, Jorge went back to the other side of the road and his group left the border of the fragment. June 22 nd : At noon, all members of the study group ran to a strip of forest near the road. At 12:15, Jorge and the three males were howling at their home range borders. Jorge moved to the electric post at the other side using the cables and came back without trying to get closer to Jane. At 13:00, Jane crossed the road using the cable. Jorge unsuccessfully attempted to mate with her on the cable and they almost fell to the ground. After that, the couple

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53 moved to an electric post and mated. Jorges group was rest ing in a nearby tree. ere was no attempt of copulation interruption by his groups adult female or her adult male group mates, who remained at the other side of the road. At 13:15, the couple mated again and Jane returned to her group. Jorge vocalized while she crossed the road via the cable. July 19 th : Jorge, the adult female, and the subadult vocal ized at 16:15 when Jane arrived at the border of her home range. She crossed the road as usual at 16:30, reaching a tree within the home range of Jorges group. e couple mated four times near his group while her male group members howled at the other side of the road. At 16:45, Jorge began to slowly moving away from the border of the road, only stopping to rub his chin on tree trunks. He was followed by Jane. An adult male from Janes group (appar ently slightly larger than Jorge) also crossed the road using the electric cable, reaching the trees. e last EGC was recorded at 17:15. After that, Jane returned to her home range, whereas Jorge remained with his group. We dont know whether the adult male from Janes group left the area prior or together with her. In sum, both Jorge and Jane sought EGCs, but only her attempts were successful. When Jorge moved to her home range, he was chased away by her adult male group mates. On the other hand, his adult female group mate appeared to ignore his sexual interactions with Jane. We have no data on the occurrence and frequency of EGCs during the days we were not monitoring our study group and whether Jane mated within her group during our study. We also do not know whether Jane got pregnant as a result of these EGCs because our study ended only ve weeks after the record of the rst event. erefore, our data do not allow excluding any of the aforementioned hypotheses for explaining the EGCs between Jorge and Jane. is was the second report on EGC in Alouatta guariba clamitans Acknowledgements We thank Silvia Beatriz Saint-Martin Ribeiro, Vera Lcia dos Santos, Celso dos Santos, and Mr. Ari for logistical sup port, and Jonas da Rosa Gonalves for helping in the eld at the beginning of the study. is study was approved by the Scientic Committee of the Faculdade de Biocincias/ Pontifcia Universidade Catlica do Rio Grande do Sul (project #3477). KGDL was supported by a FAPERGS PROBIC grant and JCBM by a CNPq PQ-1D grant (# 303154/20098). Karine Galisteo Diemer Lopes and Jlio Csar BiccaMarques Laboratrio de Primatologia Faculdade de Bio cincias Pontifcia Universidade Catlica do Rio Grande do Sul, Porto Alegre, RS 90619900, Brasil. E-mails: and . References Agoramoorthy, G. and Hsu, M. J. 2000. Extragroup cop ulation among wild red howler monkeys in Venezuela. Folia Primatol. 71: 147151. Di Fiore, A., Link, A. and Campbell, C. J. 2011. e atelines: behavioral and socioecological diversity in a New World monkey radiation. In: Primates in Perspective C. J. Campbell, A. Fuentes, M. C. MacKinnon, S. K. Bearder and R. M. Stumpf (eds.), pp. 155188. Oxford University Press, New York. Fialho, M. S. and Setz, E. Z. F. 2007. Extragroup copula tions among brown howler monkeys in southern Brazil. Neotrop. Primates 14: 2830. Glander, K. E. 1992. Dispersal patterns in Costa Rican mantled howling monkeys. Int. J. Primatol. 13: 415436. Kowalewski, M. M. and Garber, P. A. 2010. Mating pro miscuity and reproductive tactics in female black and gold howler monkeys ( Alouatta caraya ) inhabiting an island in the Parana river, Argentina. Am. J. Primatol. 72: 734748. Reeder, D. M. 2003. e potential for cryptic female choice in primates: behavioral, anatomical, and physio logical considerations. In: Sexual Selection and Reproduc tive Competition in Primates: New Perspectives and Direc tions C. B. Jones (ed.), pp. 255303. American Society of Primatologists, Norman. Van Belle, S., Estrada, A. and Strier, K. B. 2008. Social relationships among male Alouatta pigra Int. J. Primatol. 29: 14811498. THE SOUTHERNMOST RECORD OF MICO EMILIAE (THOMAS, 1920) FOR THE STATE OF MATO GROSSO, NORTHERN BRAZIL Guilherme Siniciato Terra Garbino e marmoset genus Mico comprises 14 species, 13 of which are endemic to Brazil (Rylands et al. 2009; Ferrari et al. 2010). Mico emiliae was described by omas (1920) based on two specimens collected by Emilia Snethlage in the Rio Curu, a tributary of the Rio Iriri, that is an auent of the Rio Xingu (omas, 1920; Vivo, 1985). Mico emiliae is restricted to the region between the Rio Curu and Rio Iriri to the north, reaching the Rio Teles Pires to the west (Pimenta and Silva Jr., 2005; Fialho, 2010). e southern limit of the distribution remains unconrmed but has been proposed by Roosmalen et al. (2000) to lie between the Xing headwaters region and the eastern (or right) margin of the Upper Rio Teles Pires. Besides the aforementioned distribution, M. emiliae was believed to occur westwards, in the Madeira/Aripuan interuvium (Alperin, 1993; Fer rari and Lopes, 1992; Vivo, 1985, 1991). e form from this region, however, has now been described as a new spe cies, M. rondoni (Ferrari et al. 2010). In this note, I report the rst record of M. emiliae south of the Rio Teles Pires

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54 and Rio Iriri interuvium, in the Xing headwaters region, and provide an updated map of the known occurrence re cords of M. emiliae After reviewing the published records of M. emiliae and analyzing 12 museum specimens housed in the Museu de Zoologia da Universidade de So Paulo, So Paulo (MZUSP) and Museu Paraense Emlio Goeldi, Belm (MPEG) zoological collections, a total of seven locality re cords of M. emiliae were found (Figure 1). Pimenta and Silva Jr. (2005) cited the record from Vieira (1955) as dis tinct from omas (1920), but both publications refer to the type locality of M. emiliae e new record is based on a stued skin, with separated skull and postcranial skeleton (eld number PEV 11941195, voucher number MZUSP 35106), collected in the municipality of Cludia (10'S, 54' W, 345m) (Figure 1) by Marilia Kerr in 24.vii.1997. e determination of the species was based on diagnostic characters described in the literature (Vivo, 1991; Ferrari et al. 2010). According to the eld notes made by the collec tor, the animal was run over by a vehicle while crossing the MT-423 highway (the label identies it as MT-427, but since this road does not exist, and MT-423 passes through the municipality of Cludia, I assume that the collector was referring to this highway) and was previously identied as Callithrix melanura e collecting locality lies on a par ticular region, on the southeastern limit of the Brazilian Amazon Forest that can be classied phytogeographically as Evergreen Seasonal Forest (Ivanauskas et al. 2008). e observed characters agree with the analyzed series from Alta Floresta (MPEG 24595, 24596), Ourolndia, Alta Floresta (MPEG 24606, 24608, 24609, 24610, 24611), Serra do Cachimbo (MPEG 38104, 38105, 38106) and also with the paratype (MPEG 170). e specimen showed the typical black crown, white patch at the brow, unpig mented face, pigmented naked ears, light gray dorsum and black tail. e specimen diers slightly from the other ana lyzed specimens in its darker pelage (dark gray) of the dorsal sacral region and by having a tail with signs of annulations, caused by the presence of a dark brown basal band and a black distal band on the tail fur. e external measurements were taken from the label and are as follow: weight = 330 g, total body length = 539 mm, tail length = 333 mm, foot length = 65 mm, ear length = 25 mm. is record conrms the occurrence of the species 165 km south of its previous southernmost locality, in the Xing headwaters region, as predicted by Roosmalen et al. (2000) and is an important conrmation of the species presence Figure 1. Map showing the known records of Mico emiliae e grey area indicates the putative distribution of the species according to Rylands et al. (2009). 1. Cludia (11'S, 54'W) (new record); *2. Fazenda So Jos, Peixoto de Azevedo (10'S, 55'W) (vilaPires, 1986); 3. Alta Floresta (09'S, 56'W) (Ferrari et al. 2010); 4. Ourolndia, Alta Floresta (09'S, 56'W) (Ferrari et al. 2010); 5. Serra do Cachimbo (09'S, 55'W) (Pimenta and Silva Jr., 2005); **6. Rio So Benedito, left margin (09'S, 56'W) (Fialho, 2010, Fialho pers. comm.); 7. Maloca, Upper Rio Curu (type locality) (07'S, 54'W) (omas, 1920). *Specimen housed in private collection; **Observational record

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55 in the area. e possibility that the animal was kept in captivity by the local human population cannot be ruled out, as the collector did not state whether the single col lected specimen belonged to a larger group of individuals or was found alone. As more specimens become available, a more comprehensive study about geographical variation in pelage among distinct populations of M. emiliae would be important for understanding whether the variation found within the species warrants its division into separate spe cic taxa or not. Acknowledgements I am grateful to Dr. Jos de Souza e Silva Jnior and Dr. Suely Marques-Aguiar at MPEG. M. Fialho, for the correct in formation about his locality of M. emiliae Dr. Mario de Vivo for the advising and Juliana Gualda Barros, collection manager at MZUSP. Rafael S. Marcondes, for critically reading the manuscript. Research was funded by CAPES. Guilherme Siniciato Terra Garbino Museu de Zoolo gia da Universidade de So Paulo, Seo de Mastozoolo gia, Caixa Postal 42694. CEP 04299970. So Paulo, SP, Brasil. E-mail: References Alperin, R. 1993. Callithrix argentata (Linnaeus, 1771): consideraes taxonmicas e descrio de subespcie nova. Bol. Mus. Para. Emlio Goeldi, Sr. Zool 9(2):317328. vila-Pires, F.D. de. 1986. On the validity of and geograph ical distribution of Callithrix argentata emiliae omas, 1920 (Primates, Callithricidae). In: A primatologia no Brasil M.T. de Mello (ed.), pp. 319322. Sociedade Brasileira de Primatologia, Braslia. Ferrari, S.F. and Lopes, M.A. 1992. A New species of mar moset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates) from western Brazilian Amazonia. Goeldiana Zoologia 12:113. Ferrari, S.F., Sena, L., Schneider, M.P.C. and Silva Jnior, J.S. 2010. Rondons marmoset, Mico rondoni sp. n., from southwestern Brazilian Amazonia. Int. J. Primatol. 31: 693714. Fialho, M.S. 2010. Contribuio distribuio do gnero Mico (Callitrichidae, Primates) no Mdio Teles Pires, Jacareacanga, Par. Neotrop. Primates 17(1): 31. Ivanauskas, N.M., Monteiro, R. and Rodrigues, R.R. 2008. Classicao togeogrca das orestas do Alto Rio Xingu. Acta Amazonica 38(3): 387402. Pimenta, F.E. and Silva Jnior, J.S. 2005. An Update on the Distribution of Primates of the Tapajs-Xingu In teruvium, Central Amazonia. Neotrop. Primates 13(2): 2328. Roosmalen, M.G.M. van, Roosmalen, T. van, Mittermeier, R.A. and Rylands, A.B. 2000. Two new species of mar moset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates), from the Tapajs/Madeira interuvium, South Central Amazonia, Brazil. Neotrop. Primates 8(1): 218. Rylands, A. B., Coimbra-Filho, A. F. and Mittermeier, R. A. 2009. e systematics and distributions of the mar mosets ( Callithrix, Callibella, Cebuella and Mico ) and callimico ( Callimico ) (Callitrichidae, Primates). In: e smallest anthropoids: the marmoset/callimico radiation S.M. Ford, L. Porter and L.C. Davis (eds.), pp. 2561. Springer, New York. omas, O. 1920. On mammals from the lower Rio Ama zonas in the Goeldi Museum, Par. Ann. Mag. Nat. Hist. 9(6):266283. Vieira, C.O. da C. 1955. Lista remissiva dos Mamferos do Brasil. Arq. Zool. 8(11): 354374. Vivo, M. de. 1985. On some monkeys from Rondnia, Brasil (Primates: Callitrichidae, Cebidae). Papis Avulsos de Zoologia, So Paulo 4: 131. Vivo, M. de. 1991. Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Fundao Biodiversitas, Belo Horizonte. OBSERVATIONS OF TERRESTRIAL BEHAVIOR IN THE PERUVIAN NIGHT MONKEY ( AOTUS MICONAX ) IN AN ANTHROPOGENIC LANDSCAPE, LA ESPERANZA, PERU Sam Shanee Noga Shanee Introduction e Peruvian night monkey ( Aotus miconax ) is one of the least studied of all Neotropical primate taxa. A. miconax is endemic to northeastern Peru (Aquino and Encarnacion 1994) and its entire range lies within the tropical Andes biodiversity hotspot, an area characterized by its high levels of species endemism and threats to conservation (Myres et al. 2000). is species has not been the focus of previous behavioral studies and is only known from ad libitum ob servations and collection localities in the departments of Amazonas, Hunuco and San Martin (omas 1927a; 1927b; Butchart et al. 1995; Cornejo et al. 2008). ese same departments have some of the highest rates of defor estation in Peru (Elgregen 2005; INEI 2007). Deforesta tion in the area is fuelled by immigration of people from the central and northern highlands looking for land for small scale agriculture, cattle ranching and timber extrac tion (Garland 1995; Schjellerup 2000; Shanee 2010). In many areas this has caused the complete loss of large areas of forested land (Shanee et al. 2007; Shanee 2010). In other areas patterns of land use and ownership have caused the isolation of many small patches of forest forming an an thropogenic landscape mosaic (Shanee 2010). A. miconax is listed as Vulnerable by the IUCN (Red List categories A2c) and Endangered under Peruvian law (Decreto Supre mo 342004-AG). A. miconax lives in small family groups of 26 individuals (personal observation). Like other night monkey species these groups generally comprise a hetero sexual pair and their o-spring. e diet of night monkeys

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56 is primarily frugivorous although leaves, buds and insects also gure in their diet (Ganzhorn and Wright 1994; Fer nandez-Duque 2003). Fruiting gs ( Ficus spp. ) are a pre ferred food source in all studied Aotus species (FernandezDuque 2007). Terrestriality has been recorded in other species of neo tropical primates. Most commonly terrestriality has been observed in populations of Cebus spp. using stone tools to open hard shelled fruit (Fleagle 1999; Waga et al. 2006) and at dry season waterholes (Freese 1978). Terrestriality has also been observed in populations of Ateles spp. (Camp bell et al. 2005) at dry season water holes as well as to access salt-licks and other scarce resources. A similarly wide range of terrestrial behaviors has been observed in Brachyteles spp. (Mourthe et al. 2007). We aimed to gather basic ecological data on this little known species. We conducted night follows and ad libitum data collection to monitor the behavior of a group of A mi conax in a mosaic landscape of forest patches and cultivated land, to better understand the interactions between night monkeys and their habitat in an anthropogenic environ ment. e work will aid ongoing conservation eorts for A. miconax and other endangered primates in the northeast of Peru. Methods Study site Our observations took place in the Centro Poblado La Espe ranza (S 05'46", W 77'32"), Amazonas department, Peru. Habitat in the area is comprised of disturbed primary and regenerating secondary montane and pre-montane cloud forests interspersed with pasture and plantations. In areas closer to human settlements this landscape becomes decreasingly forested with isolated forest patches ranging in size from ~ 0.5 ha to ~ 10 ha surrounded by cattle pas ture and small cultivated plots of corn, potatoes, beans and other vegetables for local sale or local consumption. e area lies on the eastern slopes of the Andes with elevations between 1800 and 2400 meters above sea level. Terrain is very rugged with steep valleys separated by high moun tain ridges. Temperatures uctuate between approximately 25 C in the day and can reach as low as 6 C before dawn. Rainfall is heavy year round with a drier season during June November. Average monthly rainfall is 1500 mm. Habituation We conducted group follows on a habituated group of A miconax. When the group was identied it was already well habituated to the presence of humans due to the prox imity of the village of La Esperanza and nearby houses (three houses bordered the patch). Local residents fre quently pass through the forest patch on their way to their elds and many use the patch as a source of rewood for their homes. We furthered the habituation process between January 2008 and the start of the study period while testing methodologies and preparing transects for the study. No dedicated habituation program was implemented as this was deemed unnecessary. Study group At the start of the study period the group consisted of 5 in dividuals (2 adults, 2 sub-adults/juveniles and one infant). One individual was born in April 2010, for a group of 6 in dividuals (3 adults, 2 sub-adults/juveniles and one infant) at the end of the study period. Data collection Observations took place between 18:0022:00 hours and 03:0006:30 hours for ve nights each month between December 2009 and November 2010. Our night follows were conducted on the days preceding, during and after the full moon. Group follows were made by one to three trained observers using red light LED headlamps (Silva) as well as conventional light ashlights. e focal group lives in a small ~ 1.4 ha isolated forest patch (S 05'17", W 77'14"). Trails were cut in a 10 10 meter grid; all intersections were tagged with high visibility agging tape. We also recorded ad libitum data from observations of A. miconax while conducting other research in the same area, since the initiation of the project in October 2007. Results We observed terrestrial behavior during a four day period whilst carrying out group follows; we also inferred terres trial behavior from two ad libitum observations. e rst ad libitum observation was made on the 27 th February 2008. A lone adult female was found in a patch of euca lyptus trees ( Eucalyptus globulus ) just outside the village of La Esperanza. e trees, located next to a house on the edge of the main highway ( Carretera Fernando Belaunde Tierry ), were over 100 meters from the nearest forest patch and ~20 meters from the next nearest trees. In the morn ing the patch of trees was surrounded by dogs trapping the individual until we were able to remove her from the tree and release her in a nearby forest patch. e second ad libitum observation was made on the 11 th August 2010. Again a lone adult female was found behind a house in the village of La Esperanza. e individual was heard vocalizing continuously for 15 minutes. e trees where this individual was observed were >300 meters from the nearest forest patch. A discontinuous line of trees runs from this forest patch almost to the village but is broken in places, with one gap of >15 meters and one gap of ~6 meters, where the individual had to descend to the ground to cross. Other less substantial gaps also exist in this line but were probably crossed by leaping from one tree to another. During group follows on the nights of 20 th 21 st 22 nd and 23 rd of November 2010 we observed a group of 6 individu als leaving the forest patch where they live to gain access to

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57 a fruiting g tree ( Ficus spp.). On all occasions the group left the forest in the undergrowth and crossed ~5 meters of open ground before climbing a neighboring tree to gain access to the g. On each occasion the group stayed in the tree for 1525 minutes before returning to the forest by leaping from neighboring trees into the undergrowth on the border area of the home patch, thus avoiding crossing open ground again. On one occasion the group returned to the same tree, crossing open ground, twice in the same night. Discussion We found no published records of terrestrial behavior in any Aotus species although similar behavior has been re ported for A. a. azarai in Argentina (M. Svensson & E. Fer nandez-Duque pers. comm.), and probably exists in other areas where habitat is similarly fragmented. e highly disturbed and fragmented habitat of A. miconax at La Es peranza is representative of forests in much of this species range where anthropogenic pressures on remaining forests are increasing. e ability of primates to cope in anthro pogenic landscapes is becoming more and more important to their survival as human populations continue to grow, particularly for those with restricted ranges and in areas of high human population density (Marsh 2003). Our rst two observations were probably individuals dispersing from their natal groups, although solitary individuals are reported to be common in populations of A a. azarai in Argentina (Fernandez-Duque 2004) and Aotus spp. in Co lombia (Villavicencio-Galindo 2003). Our observations on Aotus diet at this site show a relatively high reliance on buds and leaves, accounting for 30% of their diet (Shanee and Shanee in prep). is is more than for most other night monkey species (Fernadez-Duque 2007). High consumption of leaves has also been observed in the cathemeral A. a. azarai (Fernadez-Duque 2007). In creased leaf consumption could be a strategy developed to cope with reduced availability of fruiting species in smaller patches or less productive forest types. e home patch of the focal group contains other fruiting trees, including gs. However, only two other food species were seen to be fruiting at the time, Styrax sp. and one unidentied species. Both of these have smaller, less eshy fruits then gs and so are probably less desirable to A. miconax. e forests of La Esperanza are home to three other primate species: Oreonax avicauda, Ateles belzebuth and Cebus al bifrons (Shanee and Shanee 2010), however only Aotus mi conax has been observed so close to villages or in such small forest patches (> 50 ha). In part this is probably because of their smaller body size, nocturnal habits and undesirability to hunters. ere are however reports from local people of O. avicauda crossing open ground between forests and in one incident an individual of this species was captured by a local man in a semi-isolated patch of ~30 ha when it tried to enter a coee plantation (A. Mego-Rodriguez, pers. comm.). Terrestrial behavior in primarily arboreal primates such as Aotus may leave individuals at greater risk to predation (Isbell 1994; Mourthe 2007). e risk of attack or preda tion by domestic animals such as dogs and possible oppor tunistic capture by hunters will be especially great in areas with relatively high human population densities such as La Esperanza. Even with these increased risks many species of neotropical primate demonstrate occasional terrestriality (Freese 1978; Dib et al. 1997; Fleagle 1999; Campbell et al. 2005; Waga et al. 2006; Mourthe 2007). Several popu lations of Cebus spp. regularly descend to the ground to open dry or hard shelled fruits (Waga et al. 2006), a re source that would be unavailable without access to stone tools. Similarly, Cebus spp., Ateles spp. and Brachyteles spp. have all been observed descending to the ground to access dry season waterholes and otherwise un-available resourc es (Freese 1978; Port-Carvalho et al. 2004; Campbell et al. 2005; Mourthe et al. 2007). In the 12 months of our study the focal group was only observed descending to the ground during a single four-day period to access an other wise un-available resource. is occurred during the dry season when fruit is scarce. In one study Dib et al. (1997) reported that groups of northern muriqui ( Brachyteles hypoxanthus ) descend to the ground to cross areas of pasture between isolated forest patches. Terrestriality in dispersing females has also been observed in Brachyteles (Lemos de Sa 1988 cited by Dib et al. 1997). If individuals need to disperse from groups in isolated patches then occasional terrestriality becomes a necessary behavior to avoid inbreeding and intragroup con icts. e solitary Aotus females we observed were probably dispersing from their natal groups. Our observations sug gest that conservation of A. miconax and other primates in similar landscapes can be aided by the preservation of con nectivity between forest patches. rough better planning when converting forest to pasture or plantations, arboreal food sources close to forest habitat could be conserved. Understanding the reasons for, and risks and benets in volved in, terrestrial behaviors in Aotus spp. will greatly aid in conservation assessments and planning for this and other species. Acknowledgments We wish to thank Alejandro Mego-Rodriguez, Nestor Allgas-Marchena, iago Pereira and Julio Cachay for their help in the eld and INRENA/DGFFS for permis sion to work in Peru (Permits: N 1222008-INRENAIFFS-DCB; N 1022009-AG-DGFFS-DGEFFS and N 3842010-AG-DGFFS-DGEFFS). is work was funded by Primate Conservation, Apenhuel Primate Conservation Trust, La Vallee des Singes/Le conservatoire pour la pro tection des primates and Wild Futures/e Monkey Sanc tuary Trust. We also wish to thank all the authorities and

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58 members of the Comunidad Campesina Yambrasbamba for their help and permission to work in the area. Sam Shanee Neotropical Primate Conservation, 203 Cal lington Road, Saltash, Cornwall, PL12 6LL. , Noga Shanee Neotropical Primate Conser vation, 203 Callington Road, Saltash, Cornwall, PL12 6LL and Durrell Institute of Conservation and Ecology, University of Kent, Canterbury, Kent CT2 7NS, UK. References Aquino, R. and Encarnacin, F. 1994. Primates of Peru. Primate Report 40: 1127. Butchart, S.H.M., Barnes, R., Davies, C.W.N., Fernandez, M, and Seddon, N. 1995. Observations of two threat ened primates in the Peruvian Andes. Primate Cons 16: 15. Campbell, C. J., Aureli, F., Chapman, C. A., Ramos-Fer nandez, G., Matthews, K., Russo, S. E., Surez, S. and Vick, L. 2005. Terrestrial behavior of Ateles spp. Int. J. Primatol. 26: 10391051. Cornejo, F. M., Aquino, R. and Jimenez, C. 2008. Notes on the natural history, distribution and conservation status of the Andean night monkey, Aotus miconax omas, 1927. Primate Cons. 23: 1. Dib, L. R. T, Oliva, A. S. and Strier, K. B. 1997. Terrestrial travel in muriquis ( Brachyteles arachnoides ) across a forest clearing at the Estao Biolgica de Caratinga, Minas Gerais, Brazil. Netrop Primates 5: 89. Elgegren, J. J. 2005. La Deforestacin en el Per. [Online] retrieved on 1 August 2008 www.conam. gob.pe/documentos/Taller-Analisis_Ambiental/La_ Deforestacion_en_el _Peru.pdf Fernndez-Duque, E. 2003. Inuences of moonlight, am bient temperature and food availability on the diurnal and nocturnal activity of owl monkeys ( Aotus azarai ). Behav. Ecol. Sociobiol. 54: 431. Fernndez-Duque, E. 2004. High levels of intrasexual competition in sexually monomorphic owl monkeys. Folia Primatol 75(suppl. 1): 260. Fernndez-Duque, E. 2007. Aotinae: Social monogamy in the only nocturnal haplorhines. In: Primates in per spective C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger and S. K. Bearder (eds), pp.139154. Oxford University Press. Oxford, UK. Fleagle, C. H. 1999. Primate adaptation and evolution. Aca demic Press, London. Freese, C. H. 1978. e behaviour of white faced capu chins (Cebus capucinus) at a dry-season waterhole. Pri mates 19: 275286. Ganzhorn, J. U. and Wright, P. C. 1994. Temporal patterns in primate leaf eating: the possible role of leaf chemistry. Folia Primatol. 63: 203208. Garland, E. B. 1995. e social and economic causes of deforestation in the Peruvian Amazon basin: Natives and colonists. In: e social causes of environmental destruction in Latin America. M. Painter and W. H. Durham (eds.), pp 217246. University of Michigan Press, Michigan. INEI, Instituto Nacional de Estadstica e Informtica. 2006. [Online] Retrieved on 1 August 2007 from: // www.inei.gob.pe/ Isbell, L. A. 1994. Predation on primates: ecological pat terns and evolutionary consequences. Evol Anthrop. 3: 6171. Marsh, L. K. 2003. e nature of fragmentation. In: Pri mates in Fragments, L. K. Marsh (ed.), pp.110. Kluwer Academic, New York. Mourthe, I. M. C., Guades, D., Fidelis, J., Boubli, J.P., Mendes, S.L. and Strier, K.B. 2007. Ground use by northern muriquis (Brachyteles hypoxanthus). Am. J. Pri matol. 69: 706712. Myers, N., Mittermeier, R. A., Mittermeier, C. G., daFon seca G. A. B. and Kent. J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853858. Port-Carvalho, M., Ferrari, S. T. and Magalhaes, C. 2004. Predation of crabs by tufted capuchins ( Cebus apella ) in eastern Amazonia. Folia Primatol 75: 154156. Schjellerup, I. (2000), La Morada. A case study on the impact of human pressure on the environment in the Ceja de Selva, northeastern Peru, AMBIO. 29: 45154. Shanee, N., Shanee, S. and Maldonado, A. M. 2007. Con servation assessment and planning for the yellow tailed woolly monkey ( Oreonax avicauda ) in Peru. Wildlife Biol. Practice 3: 7382 Shanee, S. 2010. Distribution survey and threat assessment of the yellow tailed woolly monkey ( Oreonax avicauda ; Humboldt 1812), North Eastern Peru. Int. J. Primatol DOI 10.1007/s10764-0119507-x Shanee, S. and Shanee, N. 2010. Population density esti mates for the critically endangered yellow tailed woolly monkey ( Oreonax avicauda ) at La Esperanza, northeastern Peru. Int. J. Primatol 32: 691707. omas, O. 1927a. e Godman-omas expedition to Peru. On mammals collected by Mr. R. W. Hendee in the province of San Martin, N. Peru, mostly at Yurac Yacu. Ann. Mag. Nat. Hist ., Ser. 9, 19: 361375. omas, O. 1927b. e Godman-omas expedition to Peru. On mammals from the upper Huallaga and neigh bouring highlands. Ann. Mag. Nat. Hist ., Ser. 9, 20: 594608. Villavicencio-Galindo, J. M. 2003. Distribucin geograph ica de los primates del gnero Aotus el departamento Norte de Santander, Colombia. In: Primatologia de Nuevo Mundo. V. Pereira-Bengoa., F. Nassar-Montoya. and A. Savage (eds). Centro de Primatologia Araguatos, Bogota. Waga, I. C., Dacier, A. K., Pinha, P. S. and Tavares, M. C. H. 2006. Spontaneous tool use by wild capuchin mon keys ( Cebus libidinosus ) in the Cerrado. Folia Primatol 77: 337344.

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59 A WILD TAMARIN WITHOUT A FOOT SURVIVAL DESPITE A HANDICAP Eckhard W. Heymann Ney Shahuano Tello Oda Hlscher Introduction One might suspect that for arboreal animals like most pri mates, full functionality of the locomotor apparatus is an essential condition for survival. Nevertheless, the presence of healed fractures and of (congenital) malformations of the extremities reported from several wild primate popula tions suggest that aected individuals are capable of com pensating impairments and thus to survive and even repro duce (Schultz 1939, 1956; Stokes & Byrne 2006; Arlet et al. 2009, Ferrari et al. 2010). Fractures (and perhaps other impairments) occurring at an early phase of life are sug gested to be less fatal than those obtained during adult hood (Bulstrode et al. 1986). Here we report the case of a wild moustached tamarin, Saguinus mystax who lacked one foot, probably from birth or shortly after birth on. Methods e observations reported here were made at the Estacin Biolgica Quebrada Blanco (EBQB) in north-eastern Pe ruvian Amazonia (4'S 73'W). Groups of S. mystax and its congener, the black-fronted tamarin, Saguinus nigrifrons 1 are observed at EBQB during behavioural and ecological projects by researchers, students and local eld assistants or routinely in-between projects by local eld assistants. Apart from project-specic data, we also record unusual and rare events in the life of the tamarins. Results and discussion On 12 September 2008, we detected that one juvenile in our S. mystax study group 2 (by that time consisting of two adult males, one adult female, and two juvenile males born around 20 September 2007) lacked the right foot. e juve niles right leg ended in a round and naked stump with skin slightly lighter than the palms of the hands and the other foot (see video at http://www.soziobio.uni-goettingen.de/ Peru/patita.html). It is unknown whether the foot was al ready missing at birth, lost soon after birth or later through an accident or a bite. We suspect the rst or second alterna tive: during observations of that group between 24 and 26 September 2007 we recorded one infant in an unusual po sition on the lower back of the carrier, and also falling from the back of the carrier, suggesting that the infant could not 1 A recent phylogenetic analysis by Matauschek et al. (2011) concluded that most subspecies of Saguinus fuscicollis like Saguinus fuscicollis nigrifrons should be elevated to species rank. hold normally to the carrier and that the foot was already missing at that time. At rst glance, the locomotion of the juvenile male ( Patita ) was inconspicuous. Only when looking very scrupulously did it become evident that Patita was occasionally slipping from the substrate with his right leg. When travelling on large branches, Patita simply touched the substrate with the stump; when travelling on small branches, this could not be unequivocally observed. Patita used the same routes for travelling than the other group members, but some times seemed to be more hesitative when a large leap had to be made. During foraging, Patita employed all manoeu vres typical for S. mystax i.e. rapid grasping, lunging and pouncing (see Peres 1993). He was also feeding and forag ing on thin terminal branches, and clinging vertically to the trunks of Parkia trees to consume exudates. Patita was not seen falling from a tree more often than other tamarins with fully functional extremities. Only on very smooth sur faces did Patita have obvious problems with locomotion. When trying to reach the infructescences of Wettinia may nensis (Arecaceae), he was sliding down the basal part of the fronds rather than climbing down headrst, and also climbed up with diculty compared to other S. mystax Patita was regularly seen in rough-and-tumble and chase playing with his slightly larger twin brother, although we had the impression that his playing was less vigorous than in non-handicapped tamarins. He participated in carrying twins born in January 2009 only very sporadically, while his twin brother did almost two-thirds of all infant carry ing. He was last seen with his natal group on 7 December 2009. On 9 December 2009, Patita participated in an in tergroup encounter as member of a neighbouring group to which he obviously had immigrated. While healed fractures of the extremities and congenital malformations of hands and feet are known from callit richids in captivity and in the wild (Schultz 1956; French 1986; Ferrari et al. 2010), the complete lack of a cheiridi um has not been reported. While we do not know the cause of the lack of a foot in Patita our observations indicate that despite some handicap during locomotion on smooth sur faces, this tamarin compensated the impairment and per formed most behaviour normally, as also reported for wild Mico argentatus with a congenital lack of the big toe (Fer rari et al. 2010). However, Patita was clearly handicapped with regard to infant carrying. is is not surprising, given the constraints that the heavy load represented by callitri chid infants imposes on locomotion and foraging, even in captive callitrichids (Schradin & Anzenberger 2001; Cape ros et al. 2012). Tamarin societies are highly cooperative, and S. mystax may modify their behaviour in response to an injured group member (Tirado Herrera & Heymann 2004). In the ab sence of quantitative data, we do not know whether Patitas group also had modied its behaviour, particularly in the

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60 critical transitional phase between infant dependency and locomotor independence. Primates with impairments are obviously also capable of surviving without any assistance from conspecics (Struhsaker et al. 2011), but cooperation by group members would certainly be conducive to com pensate impairments and thus to increase the likelihood of survival. Eckhard W. Heymann Abteilung Verhaltenskologie & Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Gttingen, Germany, e-mail: eheyman@gwdg. de. Ney Shahuano Tello Estacin Biolgica Quebrada Blanco, Ro Tahuayo, Loreto, Per, shahuano@hotmail. com. Oda Hlscher Abteilung Verhaltenskologie & Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Gttingen, Germany, e-mail: oda_hoelscher@ gmx.de. References Arlet, M. E., Carey, J. R. and Molleman, F. 2009. Species, age and sex dierences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park, Uganda. Primates 50:6573. Bulstrode, C., King, J. and Roper, B. 1986. What happens to wild animals with broken bones? Lancet (8471):2931. Caperos, J. M., Morcillo, A., Pelez, F., Fidalgo, A. and Snchez, S. 2012. e eect of infant body mass on car rier travel speed in cotton-top tamarins ( Saguinus oedi pus ). Int. J. Primatol. 33:447459. Ferrari, S. F., Coutinho, P. E. G. and Corra, H. K. M. 2010. Congenital digital aplasia in a free-ranging group of silvery marmosets, Mico argentatus J. Med. Primatol. 39:166169. French, J. M. 1986. Ectrodactyly and syndactyly in a common marmoset ( Callithrix jacchus ). Lab. Anim. 20:4950. Matauschek, C., Roos, C. and Heymann, E. W. 2011. Mitochondrial phylogeny of tamarins ( Saguinus Ho mannsegg 1807) with taxonomic and biogeographic im plications for the S. nigricollis species group. Am. J. Phys. Anthropol. 144:564574. Peres, C. A. 1993. Diet and feeding ecology of saddleback ( Saguinus fuscicollis ) and moustached ( S. mystax ) tamarins in Amazonian terra rme forest. J. Zool. Lond. 230:567592. Schradin, C. and Anzenberger, G. 2001. Costs of infant carrying in common marmosets, Callithrix jachus : an ex perimental analysis. Anim. Behav. 62:289295. Schultz, A. H. 1939. Notes on diseases and healed fractures of wild apes. B. Hist. Med. 7:571582. Schultz, A. H. 1956. e occurrence and frequency of pathological and teratological conditions and of twinning among non-human primates. In: Hofer, H., Schultz, A.H. and Starck, D., editors. Primatologia, vol. 1 Basel: S. Karger. p. 9651014. Stokes, E. J. and Byrne R. W. 2006. Eect of snare in juries on the g-feeding behavior of chimpanzees of the Budongo Forest, Uganda: behavioral adaptations and long-term implications. In: Newton-Fisher, N. E., Notman, H., Paterson, J. D. and Reynolds, V., editors. Primates of Western Uganda New York: Springer. p. 281297. Struhsaker, T. T., Chapman, C. A., Pope, T. R. and Marcus, J. R. 2011. Healthy baboon with no upper jaw or nose: an extreme case of adaptability in the Kibale National Park, Uganda. Primates 52:1518. Tirado Herrera, E. R. and Heymann, E. W. 2004. Behav ioural changes in response to an injured group member in a group of wild moustached tamarins ( Saguinus mystax ). Neotrop. Primates 12:1315. OBSERVAO DE COMPORTAMENTO AGONS TICO DE CEBUELLA PYGMAEA SOBRE SCIURUS SPADICEUS EM UM FRAGMENTO FLORESTAL NO ESTADO DO ACRE, BRASIL Rodrigo Otvio Almeida Canizo Armando Muniz Calouro O leozinho, Cebuella pygmaea Spix, 1824 (Primates, Cebi dae: Callitrichinae) a menor espcie de primata neotropi cal, medindo cerca de 23 cm do focinho a ponta da cauda e pesando de 120 a 190 g quando adulto (Ankel-Simons, 2007). Ocorre na regio amaznica, abrangendo o Brasil (nos estados do Acre, parte de Rondnia e sul do Amazo nas), Colmbia, Equador, Peru e norte da Bolvia (Bicca -Marques e Calegaro-Marques, 1995; van Roosmalen e van Roosmalen, 1997; Buchanan-Smith et al ., 2000; Rylands et al ., 2009). Embora normalmente viva em orestas pri mrias no perturbadas, tambm pode ocorrer em orestas secundrias e habitats degradados (Soini, 1988; Reis et al ., 2008). O esquilo-vermelho, Sciurus spadiceus Olfers, 1818 (Rodentia, Sciuridae: Sciurinae) conhecido popularmente em vrios locais na Amaznia como quatipuru-vermelho, uma espcie neotropical, medindo pouco mais de 30 cm do focinho a ponta da cauda e pesando de 225 a 240 g quando adulto (Reis et al ., 2006; Bonvicino et al ., 2008), podendo ser encontrada no Peru, Equador, Bolvia e Brasil (sul do rio Amazonas e oeste do rio Tapajs) (Emmons & Feer, 1997). Segundo Patton et al. (2000), o quatipuru -vermelho somente encontrado em orestas primrias ou secundrias de terra rme, nunca em orestas de vrzea. A observao registrada aqui parte de um estudo em an damento com um grupo de oito indivduos de C. pygmaea (um macho e uma fmea adultos, um subadulto macho, dois subadultos, dois juvenis e um lhote cujos sexos no foram identicados), ocorrendo durante a segunda semana de habituao do mesmo, no qual se pretende estudar sua ecologia e padres comportamentais em um fragmento urbano de aproximadamente 150 ha (Parque Zoobot nico, 9'30" 67'08" S, 9'19" 67'00" W). O Parque Zoobotnico um fragmento orestal urbano

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61 pertencente Universidade Federal do Acre (UFAC). O parque foi criado em 1979, sendo uma rea de oresta se cundria em diferentes estgios de regenerao, fruto da retirada de madeira e da agricultura de subsistncia que ocorreu na rea a mais de 40 anos (Meneses-Filho et al. 1995). Alm disso, ocorre uma dinmica orestal provoca da pela mortandade simultnea do bambu Guadua weber baueri a cada 32 anos (Silveira, 1999), espcie comum na rea (Calouro et al ., 2010). O clima considerado tropical mido, com uma estao seca compreendendo os meses de maio a outubro e uma estao chuvosa de novembro a abril. Para se identicar individualmente os indivduos do grupo foram utilizadas duas caractersticas, a colorao e o tamanho corporal. O perodo de habituao teve incio no dia 1 de agosto de 2010, onde o grupo era acompanhado principalmente pela parte da manh (6 horas dirias), du rante todos os dias. No dia 11 de agosto de 2010, s 09:15 da manh, a oito metros do observador, foi registrado o encontro de um in divduo macho adulto de leozinho com um quatipuru -vermelho. O lezinho estava forrageando insetos em uma rvore ( Cedrela sp.) sem ores, frutos ou sementes (poste riormente a rvore foi conrmada como local de alimenta o de C. pygmaea ) quando o quatipuru-vermelho adulto apareceu na mesma rvore, mas em direo oposta a tra jetria realizada pelo leozinho (o qual estava subindo). Ao se encontrarem, ambos demonstraram comportamento agonstico de ploereo durante grande parte do tempo (aproximadamente trs minutos) em que foram observa dos. Logo em seguida, se agrediram sicamente com r pidas mordidas, voltando a apresentar ploereo, at que o leozinho expulsou o quatipuru-vermelho para fora da rvore onde estavam. O tempo total da observao foi de aproximadamente quatro minutos. Durante o compor tamento apresentando por ambas as espcies, outros dois indivduos de C. pygmaea (o macho subadulto e a fmea adulta) se encontravam prximos da rvore do acontecido, a cerca de dois metros de distncia, apresentando compor tamento de fuga ao incio do comportamento agonstico. Somente um estudo relatou esse tipo de comportamento contra Sciurus sp. (Soini, 1988), mas o mesmo no fornece maiores detalhes sobre como ocorreu esse comportamento. Nesse estudo, Soini (1988) arma que o comportamento se deu principalmente porque C. pygmaea estava protegendo suas rvores de alimentao, os quais so utilizadas eventual mente por Sciurus sp. para se alimentar, embora o exsudato contribua minimamente para sua dieta (Soini, 1988), a qual composta principalmente por sementes de Astrocaryum sp., Attalea sp., Dipteryx panamensis e Syagrus romanzoana (Emmons, 1984; Forget, 1993; Galetti et al ., 1992; Paschoal & Galetti, 1995; Miranda, 2005). Cebuella pygmaea classi cado como sendo exsudatvoro-insetvoro, baseado em es tudos ecolgicos no Peru, Colmbia e Equador (Moynihan, 1976; Soini, 1982; Ypez et al ., 2005), enquanto que Sciurus spadiceus considerado frugvoro, predando principalmente sementes de palmeiras (Emmons, 1984). Em seu ambiente natural, o leozinho simptrico com outros calitriquneos (e.g. Saguinus sp. e Callimico goeldii ) (Dalton e Buchanan -Smith, 2005; Ferrari, 1993) e outras espcies de primatas (e.g. Callicebus sp.). Apesar de ser simptrico com estas es pcies, C. pygmaea no forma grupos mistos nem associaes poliespeccas com as mesmas. Uma possvel explicao para o comportamento observa do por C. pygmaea que, alm de apresentar uma baixa tolerncia presena de outras espcies em seus locais de alimentao, a presena constante do observador na rea de vida da espcie pode ter de alguma forma, estressado o animal, fazendo-o apresentar tal comportamento perante um invasor. Comportamentos agonsticos devido presen a humana foram descritos para Alouatta caraya (Humbol dt, 1812) por Aguiar et al (2005) e para Cebus libidinosus (Spix, 1823) e Callithrix penicillata (Hershkovitz, 1977) por Vilela (2007). Entretanto, no existem informaes disponveis para Cebuella pygmaea Rodrigo Otvio Almeida Canizo Programa de Ps -Graduao em Ecologia e Manejo de Recursos Naturais, Universidade Federal do Acre, Rio Branco, Acre, Brasil, 69915900; e-mail: rodrigo.canizo@gmail.com e Arman do Muniz Calouro Centro de Cincias Biolgicas e da Natureza, Universidade Federal do Acre, Rio Branco, Acre, Brasil, 69915900. Referncias Aguiar, L. M.; Ludwig, G.; Hilst, C. L. S.; Malanski, L. S. e Passos, F. C. 2005. Tentativa de infanticdio por um macho dominante de Alouatta caraya (Humboldt) (Primates, Ateli dae) em um infante extra-grupo devido a inuncia do ob servador. Revista Brasileira de Zoologia 22: 12011203. Ankel-Simons, F. 2007. Primate Anatomy: an introduction. ird edition. Duke University, North Carolina. Bicca-Marques, J. C. e Calegaro-Marques, C. 1995. Up dating the known distribution of the pygmy marmoset ( Cebuella pygmaea ) in the State of Acre, Brazil. Neotrop. Primates 3: 4849. Bonvicino, C. R.; Oliveira, J. A. e DAndrea, P. S. Guia dos roedores do Brasil, com chaves para gneros baseadas em car acteres externos Centro Pan-Americano de Febre Aftosa OPAS/OMS, Rio de Janeiro. Buchanan-Smith, H. M.; Hardie, S. M.; Caceres, C. e Prescott, M. J. Distribution and forest utilization of Sa guinus and other primates of the Pando Department, Northern Bolivia. Int. J. Primatol. 21: 353379. Calouro, A. M.; Santos, F. G. A.; Faustino, C. L. Souza, S. F.; Lague, B. M.; Marciente, R.; Santos, G. J. L. e Cunha, A. O. 2010. Riqueza e abundncia de morcegos captura dos na borda e no interior de um fragmento orestal do estado do Acre, Brasil. Biotemas 23: 109117. Dalton, R. e Buchanan-Smith, H. M. 2005. A mixed-spe cies exhibit for Goeldis monkeys and pygmy marmosets Callimico goeldii and Callithrix pygmaea at Edinburgh Zoo. International Zoo Yearbook 39: 176184.

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62 Eisenberg, J. F. e Redford, K. H. 1999. Mammals of the Neotropics e University of Chicago Press, Chicago. Emmons, L. H. 1984. Geographic variation in densities and diversities of non-ying mammals in Amazonia. Bio tropica 16: 210222. Ferrari, S. F. 1993. Ecological dierentiation in the Cal litrichidae. Em: Marmosets and tamarins: systematics, be haviour, and ecology A. B. Rylands (ed.), pp.314374, Oxford University Press, Oxford. Forget, P. M. 1993. Post-dispersal predation and scatter hoarding of Dipteryx panamensis (Papilionaceae) seeds by rodents in Panama. Oecologia 94: 255261. Galetti, M.; Paschoal, M. e Pedroni, F. 1992. Predation on palm nuts ( Syagrus romanzoana ) by squirrels ( Sciurus ingrami ) in south-east Brazil. J. Trop. Ecol. 8: 121123. Meneses-Filho, L. C. L.; Ferraz, P. A.; Ferraz, J. M. M. & Ferreira, L. A. 1995. Comportamento de 25 espcies arbreas tropicais frutferas introduzidas no Parque Zoobotnico, Rio Branco Acre Volume 3. Rio Branco: UFAC / PZ. Miranda, J. M. D. 2005. Dieta de Sciurus ingrami omas (Rodentia, Sciuridae) em um remanescente de Floresta com Araucria, Paran, Brasil. Revista Brasileira de Zoolo gia 22: 11411145. Moynihan, M. 1976. Notes on the ecology and behavior of the pygmy marmoset ( Cebuella pygmaea ) in Amazo nian Colombia. Em: Neotropical primates: eld studies and conservation R. W. orington Jr. e P. G. Heltne (eds.), pp.7984. National Academy of Sciences, Washington. Paschoal, M. e Galetti, M. Seasonal food use by the squir rel Sciurus ingrami in Southeastern Brazil. Biotropica 27: 268273. Patton, J. L.; Silva, M. N. F. e Malcolm, J. R. 2000. Mam mals of the Rio Juru and the evolutionary and ecologi cal diversication of Amazonia. Bull. Am. Mus. Nat. His. 244: 8590. Reis, N. R.; Almeida, I. G. e Lapenta, M. G. 2008. Gnero Cebuella Gray 1886. Em: Primatas Brasileiros N. R. Reis; A. L. Peracchi e F. R. Andrade (eds.), pp.7375, Techni cal Books Editora, Londrina. Rylands, A. B.; Coimbra-Filho, A. F. e Mittermeier, R. A. 2009. e systematics and distributions of the marmo sets ( Callithrix Callibella Cebuella and Mico ) and Cal limico ( Callimico ) (Callitrichidae, Primates). Em: e smallest anthropoids: the marmoset/Callimico radiation S. M. Ford; L. M. Porter e L. C. Davis (eds.), pp.2561. Springer, New York. Silveira, M. 1999. Ecological aspects of bamboo-dominat ed forest in southwestern Amazonia: an ethnoscience per spective. Ecotropica 5: 213216. Soini, P. 1982. Ecology and population dynamics of the pygmy marmoset, Cebuella pygmaea Folia Primatol. 39: 121. Soini, P. 1988. e Pygmy Marmoset, Genus Cebuella Em: Ecology and behavior of Neotropical primates volume 2 R. A. Mittermeier; A. B. Rylands; A. F. Coimbra-Filho e G. A. B. Fonseca (eds.), pp.79. World Wildlife Fund, Washington. van Roosmalen, M. G. M. e van Roosmalen, T. 1997. An eastern extension of the geographical range of the pygmy marmoset, Cebuella pygmaea Neotrop. Primates 5: 36. Vilela, S. L. 2007. Simpatria e dieta de Callithrix penicillata (Hershkovitz) (Callitrichidae) e Cebus libidinosus (Spix) (Cebidae) em matas de galeria do Distrito Federal, Brasil. Rev. Bras. Zool. 24: 601607. Wilson, D. E. e Reeder, D. M. 2005. Mammal species of the world: A taxonomic and geographic reference. e Johns Hopkins University Press, Baltimore. Ypez, P.; de La Torre, S. e Snowdon, C. T. 2005. Inter population dierences in exudate feeding of pygmy mar mosets in Ecuadorian Amazonia. Am. J. Primatol. 66: 145158. FURTHER INFORMATION ON NEOTROPICAL MONKEYS IN THE XVI CENTURY: PART 3 Bernardo Urbani Here, I report on further descriptions and mentions of Neotropical monkeys when Europe rst began its coloniza tion of the New World. In 1498, Christopher Columbus (hereafter referred to as C. Coln) landed on the island of Trinidad, four days before stepping foot on continen tal America in Paria, Venezuela. Hernando Coln (1488 1539), son of the admiral of Genoa, wrote a chronicle about the travels of his father, including the day he rst visited Trinidad. H. Coln indicated in his posthumous work (1571) that in the point named Galea [currently known as Galeota Point, southeastern Trinidad] ey found many animal footprints that looked like goats, and also bones from one, but, since the head did not have horns, they believed it was a gato pal or monkey, later they knew that it was, since they saw many gatos pales in Paria. at same day, August rst [1498], sailing between Cape Galea and Cape Playa, to starboard, to the South, we saw Tierra Firme (H. Coln 1932: 132). As in the report of C. Coln about primates in Paria (Coln 1996, Urbani 1999), this mention not only refers to the rst ob servation of remains alleged to be a monkey on the island of Trinidad (probably Cebus albifrons trinitati s or Alouatta macconelli ), but also remarks on monkeys on the continent ( A. arctoidea or C. olivaceus ) seen by C. Coln a few days later in northeastern Venezuela. Regarding the rst report about monkeys on terra rma written by C. Coln in 1498 (Coln 1996, Urbani 1999), Pedro Martir de Anglera (14571526) added further in formation in 1500 indicating that Another very singular thing the Admiral [C. Coln] has told me, and which is conrmed by his companions (all worthy of credence and whom I carefully questioned concerning the details of the voyage), is that he sailed twenty-six leagues, that is to say, one hundred and forty-eight miles, in fresh water; and the farther he advanced to the west, the fresher the water

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63 became. Finally, he saw a very lofty mountain, of which the eastern part was inhabited only by a multitude of mon keys with very long tails. All this side of the mountain is very steep, which explains why no people live there It was learned by signs that that country was called Paria, that it was very extensive (Anglera 1912: 75). P. M. de Anglera also indicated that in the regions of Curiana and Cauchieta, in todays Venezuela where the Peninsula of Paria is located, e Spaniards brought away some very pretty monkeys and a number of parrots of varied colors, from that country (Anglera 1912: 85). is seems to be the rst report of primate tracking from the Neotropics. e monkeys were probably wedge-capped capuchins ( C olivaceus ) or howler monkeys ( A. arctoidea ). In 1504, Angelo Trevisan, assistant to the Venetian ambas sador to the Spanish Crown, provided information on the primates encountered in continental America (Vannini de Gerulewicz 1989). He narrated part of the story of Pedro Alonso-Nio (15691502), who in 1499 directed an expe dition to the region of Paria. Trevisan (1989: 151) wrote that Entering the island [refers to terra rme = Paria], they saw forests with the tallest dense trees, from where voices of animals lled the country with strange howls. But they saw that there were no dangerous animals, because the local in habitants of those forests walked quietly, without fear, with their bows and spears. Considering the particular tenden cy of reporting primates in the earliest XV century chroni cles (Urbani 1999, this study), it is quite probable that the above mentioned animals with their particular vocalization were almost certainly howler monkeys ( A. arctoidea ). Few illustrations have been found that show primates from Brazil during the XVIth century. In 1557, the German trav eler Hans Staden (15251579) provided an illustration of a primate together with Amerindians and a European (Fig. 1). In 1558, the French traveler and cleric Andr de evet (15021590) published his Les singularitez de la France Ant arctique is book has illustrations of three primates with humans (Fig. 2). evet visited the region of Rio de Janeiro, and it seems he was recording how Tupi Amerindians inter acted with monkeys (see also Urbani 1999). In 1585, Jean de Lrys Histoire dun voyage faict en la terre du Bresil, published not only descriptions of primates from the Brazil ian coast but also an illustration. De Lry (15361613), a French explorer, visited the land of the Tupi in eastern Brazil. In this book, he presented an illustration of Tupinamba Am erindians with a monkey (Fig. 3). In 1592, the publisher eodore de Bry (15271598) printed a scene in the Brazil ian coast of an indigenous community with Europeans and mythological entities, where a monkey was included (Fig. 3). ese primates seem to be similar in term of the style with those illustrated Old World primates represented in the in cunable books produced during the rst century of printing (B. Urbani, unpublished). By 1558, the renowned Swiss naturalist Konrad Gessner (15161565) already published his Histori animalium is work included a review of the primates known in Europe by the rst half of the XVIth century. In 1560, Gessner published his Icones animalium where the preLinnean zoologist published what seems to be the rst sci entic representation of a Neotropical monkey. e author showed dierent Old World monkeys such as a baboon and a macaque, primates from the Medieval imaginary, as well as the sagoin as an illustrated primate from the Americas (Fig. 1). A brief prole of this monkey, a marmoset (Calli thrix sp.), is also presented. He noticed morpho-behavioral characteristics such as its small size, and its agile and elusive nature. Gessner used the term Galeopithecum for referring to this primate. Acknowledgments anks to the Rare Book and Manuscript Library of the Uni versity of Illinois at Urbana-Champaign and its personnel for their great support while visiting it on numerous occasions as well as the Library of Congress. e author would appreciate any comments and references for future updates. Figure 1. e monkey of Hans Staden (1557, left), and the sagoin of C. Gessner (1558, right). Figure 2. e monkeys of Andr de evets Les singularitez de la France Antarctique. Figure 3. e monkey of the Tupinamba in Jean de Lry (1585)s chronicle (left), and eodore de Bry (1592, right).

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64 Bernardo Urbani, Centro de Antropologa, Instituto Vene zolano de Investigaciones Cientcas, Apartado 66.755, Caracas 1061-A, Venezuela E-mail: . References Anglera P. M. de. 1912. De Orbo Novo the eight decades of Peter Martyr DAnghera Vol. 1 Putnam, New York. (Translated from the Latin with notes and introduction by Francis Augustus MacNutt). Bry, T. de. 1592. America tertia pars. Memorabile provinci Brasili Historiam Ocina eodori de Bry, Frankfurt. Coln, C. 1996. Los cuatro viajes. Testamento Alianza Edi torial, Madrid. Coln, H. 1932. Historia del almirante don Cristbal Coln por su hijo don Hernando. Tomo Primero. Librera General de Victoriano Surez, Madrid. Gessner, C. 1560. Icones animalium quadrupedum vivip arorum et oviparorum, quae in historiae animalium Con radi Gesneri libro I et II Describuntur, cum nomenclaturis singulorum latinis, graecis, italicis, gallicis, et germanicus plerunque, et aliarum quoque linguarum, certis ordinibus digestae Excudebat C. Froschoverus, Tiguri. Lry, J. de 1585. Histoire dun voyage faict en la terre du Bresil, autre ment dite Amerique. Antoine Chuppin, Geneva. Staden, H. 1557. Warhaftige Historia und beschreibung eyner landtschat der Wilnen Nacketen Grimmigen Men schfresser Leuthen in der Newenwelt America. Andre Kolben, Marburg. evet, A de 1558. Les singularitez de la France Antarctique Imprimerie de Christophe Plantin, Antwerp. Trevisan, A. 1989. Libretto de tutta la nauigationes de Re de Spagna de le isole et terreni nuouamente trouati. In: Vannini de Gerulewicz M. (ed.), El Mar de los Descu bridores Fundacin de Promocin Cultural de Venezuela. Coleccin Viajes y Descripciones, Caracas. pp. 111158. Urbani, B. 1999. Nuevo mundo, nuevos monos: sobre primates neotropicales en los siglos XV y XVI. Neotrop. Primates 7(4): 121125. POPULATION DENSITY OF THE RED HOWLER MONKEY ( ALOUATTA SENICULU S ) IN A TROPICAL DRY FOREST FRAGMENT IN NORTHWESTERN COLOMBIA Juan Carlos Meja Flrez Jorge Andrs Lpez Delgado Introduction e tropical dry forest is one of the most endangered habi tats in Colombia. is habitat has been reduced to 1.5% of its original range due to anthropogenic eects (Murphy and Lugo 1986; Ramrez and Tesillo 2001). New World primates are dependent on arboreal habitats, so habitat loss in this region has caused primates to be restricted to the remaining forest fragments. Although habitat destruction continues to threaten Neotropical primates (Deer 2003; Michalski and Peres 2005), there are some species that can persist in these disturbed ecosystems (Crockett 1998; Hor wich 1998). e red howler monkey ( Alouatta seniculus ) is the primate with the largest range of distribution in Colom bia (dwelling in habitats from 0 to 3200 meters above sea level) and seems to be the most adaptable of these primates, occurring in habitats with a minimal amount of forest where other species of primates have disappeared (Crockett 1998; Horwich 1998; Deer 2003). Although A. seniculus is not considered endangered in Colombia (it is categorized as Low Concern for this country) (Deer 2003), popula tions of this species inhabiting tropical dry forest could be threatened with extirpation due to habitat loss and frag mentation. Although A. seniculus is one of the most studied Neotropical primates, few studies have reported the status of its populations in tropical dry forest fragments (Green 1978; Salazar 2000; Avila and Padilla 2005). is study reports a survey of A. seniculus in a conserved remnant of tropical dry forest at Hacienda El Ceibal, Municipio de Santa Catalina, Bolvar, Colombia with the aim of estimat ing density and evaluating population structure of this spe cies in the area. At the study site the Fundacin Proyecto Tit (FPT) has carried out long-term investigations on the cotton-top tamarin, Saguinus oedipus, and led conservation activities including community-based programs. Methods Study area Data were collected from the remnant of tropical dry forest (300 ha) at Hacienda El Ceibal (10'36" N; 75'50"W) located in northwestern Colombia (Figure 1). is forest fragment is located in the northern part of the Hacienda El Ceibal and is surrounded by pasture for cattle ranching. e study area has a maximum elevation of 34 m.a.s.l. and tem perature ranges from 24 to 38 C. Rainfall (1200 mm/yr) varies seasonally with two dry seasons, one from January to March and one in December. Ramrez and Tesillo (2001) report that 7580% of the trees lose their leaves during the dry season of January to March. Although this forest fragment is not a national park or sanctuary, it is under protection for conservation by the Fundacin Proyecto Tit since the establishment of biological station in 1999. ree species of primates inhabit this forest fragment: S. oedipus, A. seniculus and Cebus capucinus. However, of these three primate species, only S. oedipus had been subject of studies in this area. Data collection We estimated the density of red howler monkeys follow ing the protocol presented by Peres (1999). From Novem ber 28 to December 1, 2005, ve transects ranging from 800 to 1200 m were prepared from south to north in the forest fragment (Fig. 1). ese ve transects were walked from December 2005 to February 2006. Transects were

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65 walked during 24 days by two observers with an aver age speed of 1.25.5 km/h. At every encounter with red howler monkeys we collected the following data: perpen dicular distance (distance between the rst animal seen and the transect), group size and location along the transect. Since surveys oer data from brief contact spans (no more than 15 minutes), which can lead to an underestimation of individual density of red howler monkeys (Pruetz and Leasor 2002; Gmez-Posada et al. 2005), we followed three groups in addition to the transect surveys to obtain a more reliable composition and size of groups (only three groups were followed because of time limitations). During these direct counts the following data were collected: 1) group size, 2) sex of adult individuals, and 3) age of individuals. We followed the characteristics used by Deer (1981) to determine the sex and age of individuals, and divided age into three categories: adults (the sum of adults and sub adults), juveniles and infants. Data analysis To estimate the density of howler monkeys in the fragment, we initially estimated the group ecological density for each transect, using the following formula: L ESW N D ) ( 2 In which: D = density (groups/km 2 ); N = number of sightings in each transect. ESW = Eective Strip Width, in m, calculated by the DIS TANCE 5.0 software release (omas et al. 2005). L = total transect length, in km (the total length walked in each transect). e formula above was used given that the sample size was not large enough to estimate density accurately with the DISTANCE software (Chiarello and Melo 2001; Palacios and Peres 2005). e total group density was obtained as the average of ecological density for the ve transects. We also estimated the individual density using data from groups followed out of surveys. Individual density was ob tained as the product of total group density and average group size of groups followed out of surveys. We calculated the adult sex ratio (adult male:adult female) and the adult female:immature ratio. For the later we used immature as the sum of the juvenile and infant categories. Results Density A total of 98.9 km was walked and 42 encounters with A. seniculus were recorded at the study area. ree of these encounters were with isolated males and, given that living as solitary individuals is a temporary condition (GmezPosada et al. 2005), we did not include these encounters in the analyses to estimate density. With an ESW of 0.016 km we estimated the following ecological densities for each transect: T1: 11.04, T2: 9.70, T3: 1.83, T4: 17.2 and T5: 10.51 groups/km 2 e total group density estimated for the study site was 10.37 4.43 groups/km. From the three groups followed, we obtained an average group size of 11 5 individuals per group and estimated an individual densi ty of 114.07 22.15 individuals per km 2 With these den sity values we estimated a population size of 343 66.45 howlers in 31 13.29 groups in the tropical dry forest at Hacienda El Ceibal. Group composition Group composition of the three howler monkey groups followed is presented in Table 1. We calculated a ratio of 1:1 for both the adult sex ratio and the adult female to im mature ratio. Table 1. Group composition of three groups of red howler mon keys at Hacienda El Ceibal, Bolvar, Colombia. Group Males Females Juveniles Infants Total of individuals G1 3 4 2 2 11 G2 6 5 3 2 16 G3 2 2 1 1 6 TOTAL 11 11 6 5 33 Average 3.66 3.66 2 1.66 11 % 33.33 33.33 18.18 15.15 Figure 1. Location of Hacienda El Ceibal, Bolvar, Colombia. Dotted lines refer to the position of transects used for the estima tion of population density of Alouatta seniculus in the forest frag ment at Hacienda El Ceibal (FPT, Fundacin Proyecto Tit).

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66 Discussion Population density is study provides the rst estimate for population density of A. seniculus in a conserved remnant of tropical dry forest at Hacienda El Ceibal, Bolivar, Colombia. e Colombian tropical dry forest is one of the most endangered habitats in the country, and few red howler monkey populations remain in these forests (Salazar 2000; Deer 2003). e tropical dry forest at Hacienda El Ceibal is one of the few remnant fragments in the northwestern coast of Colombia, encompassing approximately 300 hectares of forest under conservation. Population density of A. seniculus at Hacienda El Ceibal is within the wide range reported for the species, but among the highest densities reported (Table 2). ese reports show that higher densities of red howler monkeys, and other spe cies of the genus Alouatta are found in forest fragments than in continuous forest (Chapman and Balcomb 1998; Deer 2003; Gmez-Posada et al. 2005, 2007, 2009, 2010; Link et al 2010; Londoo and Gmez-Posada 2010). After isolation, forest fragments can act as refuges for primate species that can persist within these disturbed habitats (Deer 1981; Chapman and Balcomb 1998; Gmez-Posa da et al. 2005, 2007, 2009, 2010). Folivorous primates, such as red howler monkeys, are expected to adapt better to habitat loss and fragmentation than other primate spe cies (Chapman 1988; Crockett 1996; Deer 2003). is ability to survive in small fragments may be due to the fact that red howler monkeys can rely on a limited set of plant species, minimizing energy expenditure (Strier 1992). Gmez-Posada and collaborators (2005) reported the highest population density (254 ind/km) of red howler monkeys at Vereda Montegrande in Caicedonia, Colom bia. ese authors attributed this value to the high number of individuals inhabiting a small isolated fragment of forest (154 individuals in 60.4 ha). In the present study we esti mated a total of 343 66.45 individuals inhabiting 300 ha of isolated forest. In addition to fragmentation, the protection of the area is another main factor that may be inuencing the popula tion density of red howler monkeys at Hacienda El Ceibal. We suggest that population density of A. seniculus is prob ably positively inuenced by the conservation activities conducted by the Fundacin Proyecto Tit at the study site. Although these activities are conducted for the protection of S. oedipus they have indirectly led to the conservation of the other two primate species, and of all the ora and fauna associated with this forest fragment. Even when conser vation eorts are not specically directed towards howler monkey populations, conservation areas may allow the recovery and conservation of howler monkey populations (Horwich 1998). For example, Fedigan and Jack (2001) documented the recovery of the mantled howler monkey ( Alouatta palliata ) population in the 28 years after the es tablishment of the Santa Rosa National Park in Costa Rica. However, because of lack of data available on population density for A. seniculus before the establishment of the bio logical station of the Fundacin Proyecto Tit we cannot be certain that the howler monkey population inhabit ing Hacienda El Ceibal has increased due to conservation activities. Group composition We report an adult sex ratio of 1:1 at Hacienda El Ceibal, a value unexpected for this species (Deer 1981; Chapman and Balcomb 1998; Deer 2003). In red howler monkeys there usually are slightly more adult females than adult males (Deer 1981; Jones 2004). e data on group com position obtained from the three followed groups included Table 2. Population density of Alouatta seniculus reported in the literature. Study site Density (ind/km 2 ) Average Group Size Author Colombia, Vereda Montegrande* 254 8.11 Gmez-Posada et al. 2005 Colombia, Yotoco 191 8.2 Gmez-Posada et al. 2005 Colombia, vereda Maravlez* 163.4 9.0 Gmez -Posada et al. 2009 Bolivia 120 7.4 Freese et al 1982 Venezuela, Hato Masaguaral 83118 8.46 Neville 1972; Crockett and Eisenberg 1987 Colombia, Hacienda El Ceibal* 114.1 11 Present study Colombia, Otn Quimbaya 72.6 7.3 Gmez-Posada et al. 2007 Colombia, Ro Barbas* 72.2 11.3 Londoo and Gmez-Posada 2010 Venezuela, Hato El Frio 54 6.3 Braza et al. 1981 Colombia, Nana Luisa* 51.5 5 Gmez-Posada et al. 2005 Venezuela, Hato Masaguaral 50 8.3 Crockett and Eisenberg 1987 Colombia, Cuenca del Ro Nima 22.6 6 Gmez-Posada et al. 2005 Colombia, Reserva Patasola 18.6 8.5 Gmez-Posada et al. 2010 Colombia, La Macarena 10 7.5 Stevenson et al. 1991 = Fragmented forests.

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67 a group containing six males and ve female adults. is high number of reproductive individuals of both sexes is not common for the species (Deer 1981; Soini 1992; Chapman and Balcomb 1998). Crockett (1996) argued that the success of subordinate males in beginning a new group might be restricted by the lack of habitat availability to migrate. us, the isolation of the forest fragment may cause howler monkeys to remain in their natal group or to disperse to another established group, which may lead to a crowded population and to a change in the sex ratio. Similar variations in red howler monkey group composi tion had been found in other forest fragments in Colom bia (Gmez-Posada et al 2010). However, because of the small sample of groups followed in this study we cannot be certain that fragmentation is the cause of altered group structure of red howler monkeys at Hacienda El Ceibal. It is argued that the ratio of adult female to immature may be used to measure population health (Heltne et al. 1976; Deer 1981). In red howler monkeys, populations with less than 0.75 immatures for each adult female are ex pected to be in diculty; on the contrary, populations with higher number of immature individuals per adult female are expected to be stable or expanding (Heltne et al. 1976; Deer 1981). In this study we found a ratio (adult female: immature) of 1:1 which does not seem to indicate a de creasing population. In conclusion, the population density of red howler mon keys at Hacienda El Ceibal is high compared to other densities reported in the literature, but is consistent with densities reported in fragmented habitats. is value might be a result of the capacity of the species to inhabit in an thropogenic habitats in conjunction with the protection of the area. However, at this site, there is a need to conduct long-term studies to assess the impact of fragmentation and protection of this area on the existing populations of A. seniculus Acknowledgments e authors thank Carolina Gmez Posada for sharing all her knowledge with us and for her advice to conduct this project in the best possible way. We also thank Dr. Anne Savage and the Fundacin Proyecto Tit eld team (Luis Soto Rojas, Jaime Causado and Flix Mdina) for allow ing us the use of their eld equipment and for welcom ing us into their biological station. We appreciate the help given by our advisor, Juan Carlos Narvaez Barandica, who believed in us in moments of diculty. And last, but not least, we appreciate the care and partnership given by Jos Gregorio Olivares El diablo and Antonio Rojano Oliva res during the surveys. Juan Carlos Meja Flrez and Jorge Andrs Lpez Del gado. Departamento de Biologa, Universidad del Atln tico, Km 7 antigua va a Puerto Colombia, Barranquilla, Colombia. E-mail: and jorg_ and@yahoo.es. References Avila, F. and Padilla, O. 2005. Variacin estacional del uso de recursos alimenticios del mono aullador rojo Alouatta seniculus (Linnaeus 1766) en un fragmento de bosque seco tropical (Bs-t) en el norte del departamento del At lntico, Colombia. Tesis de biologa. Universidad del At lntico, Colombia. Braza, F., lvarez F., and Azcarate, T. 1981. Behavior of the red howler monkey ( Alouatta seniculus ) in the llanos of Venezuela. Primates 22: 45973. Chapman, C. 1988. Patterns of foraging and range use by three species of neotropical primates. Primates 29: 177194. Chapman, C. and Balcomb, S. 1998. Population character istics of howlers: ecological conditions or group history. Int. J. Primatol 19 (3): 385403. Chiarello, A and De Melo, F. 2001. Primate population densities and sizes in Atlantic forest remnants of northern Espirito Santo. Brazil. Int J Primatol 22 (3): 379376. Crockett, C. and Eisenberg, J. 1987. Howlers: variation in group size and demography. In: Primate Societies Smuts, B., Seyfarth, R., Wrangham, R. and Struhsaker, T (eds.), pp. 5468. University of Chicago Press. Crockett, C. 1996. e relation between red howler monkey ( Alouatta seniculus ) troop size and population growth in two habitats. In: Adaptive radiations of Neotropical pri mates M. A. Norconk, A. L. Rosenberg & P. A. Garber (eds.), pp. 489510. Plenum Press, New York. Crockett, C. 1998. Conservation biology of the genus Al ouatta Inter. J. of Primatol 19 (3): 549579. Deer, T. 1981. e density of Alouatta seniculus in the eastern Llanos of Colombia. Primates 22: 564569. Deer, T. R. 2003. Primates de Colombia. Serie de guas tropicales 4. Conservacin Internacional. Bogot D.C. Fedigan, L. and Jack, K. 2001. Neotropical primates in a regenerating Costa Rican dry forest: a comparison of howler and capuchin population patterns. Int. J. Prima tol 22 (5): 689. Freese, C., Heltne, P., Castro, R. and Whitesides, H. 1982. Patterns and determinants of monkey densities in Peru and Bolivia, with notes on distribution. Int. J. Primatol 3: 5390. Gmez-Posada, C., Roncancio, N. and Hincapi, P. 2005. Evaluacin de las poblaciones de mono aullador rojo ( Alouatta seniculus ) en fragmentos de bosque en el Valle del Cauca. Informe tcnico presentado a la Corporacin Autnoma Regional del Valle del Cauca. Fundacin Ecoandina /WCS Colombia. Cali. Gmez-Posada, C., Martnez, J., Giraldo, P. and Kattan, G. 2007. Density, hbitat use, and ranging patterns of red howler monkeys in a Colombian Andean forest. Neotrop. Primates 14 (1): 210. Gmez-Posada, C., lvarez, Z. and Giraldo-Chavarria ga, P. 2009. Densidad y estatus poblacional de monos

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68 aulladores rojos en un guadual, fragmento aislado, La Talebaida, Quindo, Colombia. Universitas Scientiarum 14 (1): 815. Gmez-Posada, C., Giraldo, P. and valrez, Z. 2010. Eval uacin de las poblaciones del mono aullador ( Alouatta seniculus ) en dos localidades en Quindo y Risaralda, Co lombia. In: Primatologa en Colombia: Avances al principio del milenio V. Pereira-Bengoa, P. R. Stevenson, M. L. Bueno and F. Nassar-Montoya (eds.), pp.3755. Grcas San Martin. Bogot D. C. Green, K. 1978. Primate censusing in Northern Colom bia: A comparison of two techniques. Primates 19 (3): 537550. Heltne, P., Turner, D., and Scott, N. 1976. Comparison of census data on Alouatta palliata from Costa Rica and Panam. In: orington, R and Heltne, P. (eds.), pp. 1019. National Academy of Sciences, Washington D.C. Horwich, R. H. 1998. Eective solutions for howler con servation Int. J. Primatol 19 (3): 679598. Jones, C. B. 2004. e number of adult females in groups of polygynous howling monkeys ( Alouatta spp.): theo retical inferences. Primate Report 68: 725. Link, A., Luna, A., Alfonso, F., Giraldo-Beltran, P., Ramirez and Ramirez, F. 2010. Initial eects of fragmentation on the density of three neotropical primate species in two lowland forests of Colombia. Endang. Species Res 13: 4150. Londoo, J. and Gmez-Posada, C. 2010. Estatus de la po blacin de monos aulladores rojos en el can del Barbas, fragmento montano, Cordillera Central, Colombia. Acta Biol. Colomb. 15 (1): 2536. Michalski, F. and Peres, C. 2005. Anthropogenic determi nants of primate and carnivore local extinctions in a frag mented forest landscape of southern Amazonia. Biological Conservation. 124: 383396. Murphy, P. and Lugo, A. 1986. Ecology of tropical dry forest. Ecologic Systems 17: 6788. Neville, N. 1972. e population structure of red howler monkeys ( Alouatta seniculus ) in Trinidad and Venezuela Folia Primatol 18: 4777. Palacios, E. and Peres, C. 2005. Primate population densi ties in three nutrient-poor Amazonian terra rme forests of south-eastern Colombia. Folia Primatol 76 : 135145. Peres, C. A. 1999. General guidelines for standardizing line-transect surveys of tropical forest primates. Neotrop. Primates 7:1116. Pruetz, L. and Leasor, J. 2002. Survey of three primate spe cies in forest fragments at La Suerte biological Field Sta tion, Costa Rica. Neotrop. Primates. 10: 4. Ramrez, D. and Tesillo, A. 2001. Estructura, diversidad y produccin de hojarasca en un remanente de bosque seco tropical en el departamento de Bolvar, Colombia. Tesis de Biologa. Universidad del Atlntico, Colombia. Salazar, W. 2000. Variacin de la estructura grupal y rea de dominio vital del mono aullador rojo Alouatta seniculus (Linnaeus, 1766) a causa de la perturbacin humana del bosque Santuario de Fauna y Flora los Colorados, San Juan de Nepomuceno, Bolvar. Tesis de Biologa. Univer sidad del Atlntico, Colombia. Soini, P. 1992. Ecologa del coto mono ( Alouatta seniculus CEBIDAE) en el ro Pacaya, reserva Pacaya Saimiria, Per. Folia Amazonica 4: 103118. Stevenson, P. R., Quiones, M. J. and Ahumada, J. 1991. Relacin entre la abundancia de frutos y las estrategias alimenticias de cuatro especies de primates en el ro Duda, Macarena. Informe nal presentado al Banco de la Repblica, Bogot. Strier, K. 1992. Atelinae adaptations: Behavioral strate gies and ecological constraints. Am J Phys. Anthrop 88: 515524. omas, L., Laake, J.L., Strindberg, S., Marques, F.F.C., Buckland, S.T., Borchers,D.L., Anderson, D. R., Burn ham, K.P., Hedley, S. L., Pollard, J.H., BishoP, J.R.B. and Marques, T. A. 2005. Distance 5.0. Release Re search Unit For Wildlife Population Assessment, Univer sity of St. Andrews, UK. http://www.ruwpa.stand.ac.uk/ distance/ REGISTRO OCASIONAL DA PREDAO DA POMBADEBANDO ZENAIDA AURICULATA DES MURS, 1847 PELO SAGIDOCERRADO CALLITHRIX PENICILLATA GEOFFROY, 1812 NO INTERIOR DE SO PAULO, SP Felipe Bittioli R. Gomes Renata C. de Lima-Gomes O sagui-do-cerrado, Callithrix penicillata (Primates: Calli thrichidae), a menor espcie dentre os primatas do Brasil Central, pesando entre 350 e 500 gramas (Stevenson e Rylands, 1988), primitivamente uma espcie de Cerrado, ocupando matas de galeria, cerrades e cerrado strictu sensu (Bicca-Marques et al. 2006). Sua dieta baseada em ar trpodos, frutos, nctar e, principalmente, exsudatos de plantas, sendo a espcie considerada gomvora-insetvora (Stevenson e Rylands, 1988). Primatas do gnero Calli trhix tambm so conhecidos por eventualmente forragear em ninhos de aves (Miranda e Faria, 2001; Lyra-Neves et al. 2007). Por exemplo, Mendes Pontes e Soares (2005) citam a predao por C. jacchus em ninhegos de pombo -domstico ( Columba livia domestica Columbidae) e sabi -laranjeira ( Turdus ruventris Turdidae); Silva et al. (2008) relatam a predao de C. penicillata em uma rolinha-roxa ( Columbina talpacoti Columbidae); Begotti e Landes mann (2008), relatam algumas tentativas e predaes de um grupo hbrido de C. jacchus e C. peniccilata em ovos da pomba-de-bando ( Zenaida auriculata, Columbidae) do sabi-barranco ( Turdus leucomelas, Turdidae ) e do sabi do campo ( Mimus saturninus Mimidae). Nosso objetivo relatar a predao de dois ninhegos da pomba-de-bando, Z. auriculata por um grupo de C. penicillata na regio no roeste do estado de So Paulo, onde a sagi-do-cerrado uma espcie introduzida.

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69 Ao dia 08 de Agosto de 2008, por volta da 09:50 h. da manh, ouvimos a agitao de um grupo de C. penicilla ta no jardim do estacionamento da Universidade Estadu al Paulista-UNESP (20 47'09.82 S, 49 21'31.69" O), Campus de So Jos do Rio Preto, interior de So Paulo. Ao nos aproximarmos, observamos um grupo de trs in divduos adultos em uma palmeira (Arecaceae). O grupo emitia guinchos e estava bastante agitado. Registramos em fotograa, um dos indivduos, aparentemente um macho, com uma pequena ave morta nas mos, a cerca de trs metros de altura (Fig. 1). O sagi se afastou dos demais, carregando a presa com a boca e, subiu para um galho mais elevado, a aproximadamente quatro metros do solo, consumindo-a sem dividi-la com os demais. Os outros membros do grupo caram guinchando e observando sua movimentao. Longe destes, o sagi manipulou a peque na ave, observando-a sob as asas e patas, como se estivesse buscando ectoparasitas; mordeu a cabea e pescoo e, em seguida soltou-a ao cho. O grupo de C. penicillata ento desceu da palmeira, correndo pelo cho at outra rvore, distante aproximadamente 8 metros, no sendo possvel observ-los por mais tempo. Toda observao foi ocasio nal, no sendo parte de outro estudo e durou em torno de 10 minutos. Aps o grupo de C. penicilata se afastar do local, nos aproximamos da palmeira e vericamos que se tratava de um ninhego de Z. auriculata Na base da rvore observamos um segundo indivduo morto e, assim como o primeiro, encontrava-se parcialmente predado, com apenas a regio da cabea consumida, sendo que todo o restante do corpo da ave encontrava-se inteiro e sem ferimentos. As aves apresentavam penugem juvenil, com muitas penas em desenvolvimento, sendo a primeira ave observada, menor que a segunda (120 mm. e 140 mm. de comprimento total, sem a cabea, respectivamente). Vericamos um ninho na mesma rvore, possivelmente de onde os ninhegos foram obtidos. Adultos da ave no foram observados nas proxi midades, mas a espcie bastante comum na rea, como pudemos constatar em observaes anteriores. Espcimes de C. penicillata foram introduzidos por meio do trco ilegal para serem utilizados com animais de es timao (Begotti e Landesmann, 2008), nos estados do Rio de Janeiro e poro centro-sul de So Paulo (Olmos e Martuscelli, 1995; Bicca-Marques et al. 2006). Introduo de espcies no-nativas pode gerar competio interespec ca e transmisso de doenas fauna nativa (Costa et al. 2005; Ruiz-Miranda et al. 2006; Mendes Pontes et al. 2007). O hbito de forrageio em ninhos de aves conhe cido para Callithrix porm mais habitualmente sobre os ovos (Stevenson e Rylands, 1988, Miranda e Faria, 2001; Lyra-Neves et al. 2007). Argel de Oliveira (1995) cita que a predao de ninhos pode reduzir a riqueza e diversidade da avifauna local, e nossa observao corrobora a interferncia negativa de espcies introduzidas na avifauna nativa. O fato observado pode ter sido um comportamento oportunista, no sendo necessariamente relacionado a limitaes de re cursos, visto que os indivduos residentes na universidade j foram observados se alimentando de exsudatos, frutos ou sendo alimentados por seres-humanos. Nossa observa o evidencia a importncia destes pequenos mamferos em uma srie de importantes processos ecolgicos (De Esteven e Putz, 1984; Fragoso, 1994), como a predao de espcies nativas e a competio com espcies sinantrpicas. Agradecimentos FBRG grato a FAPESP (Mestrado proc. #07/529731) e ao CNPq (Doutorado proc. #145304/20094). RCLG grata ao CNPq (Bolsa de Desenvolvimento Tecnolgico Industrial do CNPq Nvel 7F, proc. #383268/20109) e (Mestrado proc. #134785/20118). Ambos agradecem a Empresa ATEND Ltda., pelo patrocnio e conana em seus trabalhos. Felipe Bittioli R. Gomes, Programa de Ps-graduao em Ecologia, Instituto Nacional de Pesquisas da Amaz nia, PPG-ECO/INPA, Manaus, Amazonas, 69060001, Brasil. E-mail: , Renata C. de Lima-Gomes, Programa de Ps-graduao em Biologia de gua Doce e Pesca Interior, Instituto Nacional de Pes quisas da Amaznia, PPG-BADPI/INPA, Manaus, Amazo nas, 69011970, Brasil. Referncias Argel de Oliveira, M. M. 1995. Aves e vegetao em um bairro residencial da cidade de So Paulo (So Paulo, Brasil). Rev. Brasil. Zool. 12(1): 8192. Begotti, R. A. e Landesmann, L. F. 2008. Predao de ninhos por um grupo hbrido de sagis ( Callithrix Jac chus / Penicillata ) introduzidos em rea urbana: implica es para a estrutura da comunidade. Neotrop. Primates 15(1): 2829. Bicca-Marques, J. C., Silva, V. M. e Gomes, D. F. 2006. Ordem Primates. Em: Mamferos do Brasil N. R. Reis, A. L. Peracchi, W. A. Pedro e I. P. Lima, (eds.), pp. 101 148. Imprensa da UEL, Londrina-PR. Figura 1. Indivduo de Callithrix penicillata durante a predao do ninhego de Zenaida auriculata em So Jos do Rio Preto, noro este de So Paulo, Brasil.

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70 Costa, L. P., Leite, Y. L., Mendes, S. L. and Ditcheld, A. D. 2005. Mammal conservation in Brazil. Cons. Biol 19(3): 672679. De Esteven, D. and Putz F. E. 1984. Impacts of mammals on early recruitment of a tropical canopy tree, Dipteryx panamensis in Panama. Oikos 43: 207216. Fragoso, J. M. V. 1994. Large mammals and the dynamics of an Amazonian rain forest. PhD. thesis, University of Florida, Gainesville, FL. Lyra-Neves, R. M., Oliveira, M. A., Telino-Jnior, W. R. e Santos, E. M. 2007. Comportamentos interespeccos entre Callithrix jacchus (Linnaeus) (Primates, Callitri chidae) e algumas aves de Mata Atlntica, Pernambuco, Brasil. Rev. Brasil. Zool. 24(3): 709716. Mendes Pontes, A. R. and Soares, M. L. 2005. Sleeping sites of common marmosets ( Callithrix jacchus ) in defau nated urban forest fragments: a strategy to maximize food intake. J. Zool. 266: 5563. Mendes Pontes, A. R., Normande, I. C., Fernandes, A. C., Ribeiro, P. F. and Soares, M. L. 2007. Fragmentation causes rarity in common marmosets in the Atlantic Forest of northeastern Brazil. Biodiv Conserv 16(4): 11751182. Miranda, G. H. B. and Faria, D. S. 2001. Ecological as pects of black-pincelled marmoset ( Callithrix penicillata ) in the cerrado and dense cerrado of the Brazilian Central Plateau. Braz. J. Biol. 61(3): 397404. Olmos, F. and Martuscelli, P. 1995. Habitat and distribu tion of the buy-tufted-ear marmoset Callithrix aurita in So Paulo State, Brazil, with notes on its natural history. Neotrop. Primates 3(3): 7579. Ruiz-Miranda, C. R., Aonso, A. G., Morais, M. M., Verona, C. E., Martins, A. and Beck, B. 2006. Behavioral and ecological interactions between reintroduced golden lion tamarins ( Leontopithecus rosalia Linnaeus, 1766) and introduced marmosets ( Callithrix spp Linnaeus, 1758) in Brazils Atlantic coast forest fragments. Brazilian Archives of Biology and Technology 49(1): 99109. Silva, I. O., Alvarenga, A. B. B. and Boere, V. 2008. Occa sional eld observations of the predation on mice, dove and ants by black-tufted-ear marmosets ( Callithrix peni cillata ). Neotrop. Primates 15(2): 5962. Stevenson, M. F. and Rylands, A. B. 1988. e marmosets, genus Callithrix In: Ecology and Behavior of Neotropical Primates Mittermeier, R. A., Rylands, A. B., Coimbra -Filho, A. F. and Fonseca, G. A. B. (eds.), pp. 131222. World Wildlife Fund, Washington, D. C. NEWS SIMPOSIO PRIMATOLOGA EN EL PER: HISTORIA, ESTADO ACTUAL Y PERSPECTIVAS Per es uno de los pases con la mayor diversidad de pri mates, tanto a nivel de la regin Neotropical como a nivel mundial (IUCN 2010). No obstante esta diversidad, las actividades primatolgicas en el Per parecen bastante limitadas, realizadas por unas pocas instituciones/cient cos y poco coordinadas; en consecuencia, la informacin disponible es bastante escasa y dispersa. Para analizar estos problemas y fomentar la primatologa en el Per, era necesaria una evaluacin de la situacin actual de la pri matologa en el Per, su historia, y desarrollar perspectivas para el futuro de la primatologa en el pas. Con estos nes, se realiz el simposio Primatologa en el Per: Historia, Estado Actual y Perspectivas, entre el 17 y 22 de octu bre 2011, en Lima (Per). Las instituciones organizadoras fueron Yunkawasi (Lima), el Museo de Historia Natural de la Universidad Nacional Mayor de San Marcos (UNMSM, Lima) y el Deutsches Primatenzentrum (DPZ, Gttingen, Alemania). Este simposio convoc a 105 cientcos y estu diantes, mayormente del Per, pero tambin de Alemania, Bolivia, Colombia, Ecuador, EE.UU., Espaa, Francia, In glaterra y Mxico. Se realiz en las instalaciones del Museo de Historia Natural, UNMSM y la Facultad de Biologa, Universidad Ricardo Palma (Lima). La inauguracin ocial del evento tuvo lugar en el Museo de Historia Natural UNMSM, el 18 de octubre, y cont con la presencia del decano de la Facultad de Ciencias Biolgi cas de la Universidad Ricardo Palma, Dr. Toms Agurto, de la directora del Museo de Historia Natural UNMSM, Dra. Betty Milln y del Secretario General del Servicio Na cional de reas Naturales Protegidas por el Estado SER NANP, Dr. Carlos A. M. Soria DallOrso. Durante la in auguracin, se celebr tambin la presentacin del lbum Filatlico Primates del Per y la carta del primer da de emisin (Fig. 1), en un lbum latlico conmemorativo. Se manifest la esperanza que la emisin de estas estampillas aumente el conocimiento y el orgullo del pblico en gen eral sobre los primates peruanos. El simposio incluy las siguientes actividades: Conferencias magistrales (Bertha Alvarado, Per; Mark Bowler, Inglaterra; Fanny M. Cornejo, Per; Xyomara Carretero-Pinzn, Colombia; Liliana Cor ts-Ortz, EE.UU y Mxico; Csar Flores, Per; Fer nando Guerra, Per; Eckhard W. Heymann, Alema nia; Christian Matauschek, Alemania; Dirk Meyer, Alemania; Pablo Puertas, Per; Jennifer A. Rehg, EE.UU.; Stella de la Torre, Ecuador.; Robert B. Wal lace, Bolivia.) Presentaciones orales y posters

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71 Mesa redonda: Estudios primatolgicos en Latinoamrica Taller de especialistas: Vacos de informacin y prio ridades de investigacin primatolgica y de conserva cin de primates en el Per Adems, se realizaron los siguientes talleres metodolgicos: Tpicos bsicos en primatologa (Fanny M. Cornejo y Mark Bowler) Herramientas moleculares para el estudio y conser vacin de primates (Liliana Corts-Ortz, Christian Matauschek y Dirk Meyer) Estudios poblacionales y uso de DISTANCE para es timados de densidad (Miguel Antnez) Herramientos botnicas para primatologa (Ricardo Zarate) Mtodos de observacin de comportamiento y ecologa de primates (Eckhard W. Heymann) Bioacstica (Dirk Meyer) Uso de GPS y Sistemas de Informacin Geogrca (Yvan Lledo-Ferrer) Ser un primatlogo en Per: claves y tips (Fanny M. Cornejo y Mark Bowler) Envolviendo al pblico: educacin en ciencia para la conservacin (Mark Bowler y Fanny Fernndez) En la mesa redonda Estudios primatolgicos en Lati noamrica, representantes de los pases vecinos Bolivia (Robert B. Wallace), Colombia (Xyomara CarreteroPinzn), Ecuador (Stella de la Torre) presentarn infor macin sobre el estado de la primatologa de dichos pases. Como los dos primatlogos peruanos de mayor prestigio internacional, Rolando Aquino y Filomeno Encarnacin (autores del libro Primates of Peru Los Primates del Per) infelizmente no pudieron atender al evento, la situacin en el Per fue presentada por Eckhard W. Heymann, quien realiza estudios primatolgicos en el Per desde 1982. Se identicaron los problemas comunes y los problemas espe ccos y se concluy que, tanto desde el aspecto cientco como desde el aspecto de conservacin ser necesario la formacin de nexos entre los primatlogos de estos pases. La misma conclusin se dio en el taller de especialistas sobre Vacos de informacin y prioridades de investigacin pri matolgica y de conservacin de primates en el Per. En este taller se revis el estado taxonmico de los primates peruanos, el conocimiento sobre su distribucin geogrca y el estado de las poblaciones. En el taller se concluy que como consecuencia de las ltimas revisiones taxonmicas del gnero Saguinus por Matauschek et al. (2011) y del gnero Pithecia Laura Marsh (en preparacin), el nmero de especies de primates que existen en el Per ahora es de por lo menos 45, seis ms que la lista previa de Pacheco et al. (2009). Futuras revisiones taxonmicas (p. e. de los Figura 1. Carta del primer da de emisin y estampillas con primates del Per, emitida el 18 Octubre 2011, en el marco de la inauguracin del simposio Primatologa en el Per.

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72 gneros Callicebus y Cebus ) posiblemente aumentaran esta cifra. Como los limites de distribucin lgicamente no co inciden con los lmites nacionales, la integracin de cono cimientos y trabajos a ambos lados de las fronteras es de gran importancia para llenar los vacos que todava existen sobre la distribucin geogrca. Por ejemplo, la presencia de Alouatta sara en Bolivia, en la zona fronteriza con el Per (Wallace et al. 2010), hace muy probable su presencia en el extremo sur del Per, pero no existen estudios que lo conrmen. Slo con la integracin de conocimientos y la formacin de nexos se puede llenar este y otros vacos. Adems de los primatlogos, el taller de especialistas cont con la participacin de guardaparques y profesionales de diferentes reas naturales protegidas del Per, gracias a la colaboracin del Servicio Nacional de reas Naturales Protegidas por el Estado (SERNANP). Esto fue de gran importancia, ya que el personal del SERNANP, por su casi continua presencia en estas reas, acumula bastante infor macin y conocimientos que de otra manera no llegan a ser divulgados. Las presentaciones orales (11) y los posters (25) de los estu diantes y cientcos jvenes fueron juzgados por un comit de evaluacin. Las cinco mejores presentaciones orales y los ocho mejores posters fueron premiados con los libros Pri mate conservation biology de Guy Cowlishaw y Robin Dunbar y Field and laboratory methods in primatology por Joanna Setchell y Deborah Curtis respectivamente, do nados por University of Chicago Press y Cambridge Uni versity Press. Los autores y ttulos de los premiados se en cuentran en http://www.monosperu.org/ganadores.html. En una plenaria hacia el nal del simposio, los participantes acordaron por unanimidad la formacin de un grupo de primatologa dentro de la Sociedad Peruana de Mastozo ologa. Esperamos que con este grupo las actividades pri matolgicas en el Per sigan creciendo, tanto en el nmero de investigaciones primatolgicas como en las acciones de conservacin de los primates peruanos que estas promue van y soporten. El simposio ha sido un primer e importante paso hacia esta direccin. Agradecimientos Agradecemos a las siguientes organizaciones e instituciones por su aporte nanciero y administrativo: Universidad Ri cardo Palma Facultad de Biologa; SERNANP (Servicio Nacional de reas Naturales Protegidas, Per); Conserva tion International; Margot Marsh Biodiversity Founda tion; Frderkreis des Deutschen Primatenzentrums e.V.; PERAC (Peruvian Agency of Cooperation); e Mohamed bin Zayed Species Conservation Fund; Sociedad Peruana de Mastozoologa; GenLab del Per SAC; Wildlife Con servation Society; San Diego Zoo Institute for Conserva tion Research; Estacin Biolgica Cocha Cashu, University of Michigan Museum of Zoology; Cambridge University Press; University of Chicago Press; y SERPOST (Servicios Postales del Per). Tambin agradecemos a Laura Marsh por proporcionar los resultados inditos de su revisin tax onmica del gnero Pithecia Finalmente, agradecemos a Fanny Fernndez, Presidenta de Yunkawasi, por su inapre ciable labor a fondo en todos los aspectos administrati vos, logsticos y tcnicos de la organizacin. Fanny Cornejo Fernndez, Departamento de Mastozo ologa, Museo de Historia Natural, Universidad Nacional Mayor San Marcos, Av. Arenales 1256, Lima 11, Per, y Yunkawasi ; Vctor Pacheco Torres Departamento de Mastozoologa, Museo de His toria Natural, Universidad Nacional Mayor San Marcos, Av. Arenales 1256, Lima 11, Per, ; Eckhard W. Heymann Abt. Verhaltenskologie & Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Gttingen, Alemania, . Referencias IUCN. 2010. Global primate diversity. http://www.pri mate-sg.org/diversity.htm (accedido 28/10/2011). Matauschek, C., Roos, C., y Heymann EW. 2011. Mi tochondrial phylogeny of tamarins ( Saguinus Ho mannsegg 1807) with taxonomic implications for the S. nigricollis species group. Am. J. Phys. Anthropol. 144:564574. Pacheco, V., Cadenillas, R., Salas, E., Tello, C., y Zeballos, H. 2009. Diversidad y endemismo de los mamferos del Per. Rev. Per. Biol 16:005032. Wallace, R. B., Gmez, H., Porcel, Z. R., y Rumiz, D. I. 2010. Distribucin, ecologa y conservacin de los mamferos medianos y grandes de Bolivia. Centro de Ecologa Difusin Simn I. Patio, Santa Cruz, Bolivia. Figura 1. Carta del primer da de emisin y estampillas con pri mates del Per, emitida el 18 Octubre 2011, en el marco de la inauguracin del simposio Primatologa en el Per GOLDEN-HEADED LION TAMARIN RESEARCH IN THE 21 ST CENTURY: RECENT ADVANCES AND POTENTIAL AREAS OF FUTURE RESEARCH On 7 and 8 December 2011, students, researchers, and conservationists with a vested interest in golden-headed lion tamarins ( Leontopithecus chrysomelas; GHLTs) gath ered at the State University of Santa Cruz (UESC; Ilhus, Bahia, Brazil) for the symposium `Golden-Headed Lion Tamarin Research in the 21st Century: Recent Advances and Potential Areas of Future Research with the aim of sharing recent work and discussing potential future avenues for research. Within the last 5 years, several doctoral disserta tions and masters theses were completed that focused on the biology, ecology, and/or conservation of GHLTs in ad dition to the ongoing work of established scientists who have devoted their professional lives to the study of this

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73 species and the Atlantic Forest. However, language barriers and the fact that many members of the GHLT community are based at institutions throughout the world have compli cated widespread access to these results and collaborations among researchers. e primary goals of this symposium were to (1) promote the exchange of existing information, (2) contribute towards a better synchronization of research eorts, and (3) identify important steps for more ecient/ collaborative conservation eorts for GHLTs and their habitat. is symposium brought together 30 participants from 12 institutions in Brazil, Belgium and the USA and allowed for the dissemination of information to the global GHLT community, compilation of recent advances in re search, and identication of gaps in knowledge of GHLT biology, ecology and conservation, which ultimately fos tered discussions on how attendees could collaborate to ll knowledge gaps. Golden-headed lion tamarins GHLTs are small arboreal primates threatened by extreme habitat fragmentation and loss of the Atlantic Forest in southern Bahia, Brazil (Pinto and Rylands 1997; IUCN 2012). ey are frugi-faunivores that live in small groups (57 individuals on average) and maintain home ranges that can be quite large (20200 ha; Raboy and Dietz 2004; Oliveira et al 2011). In addition to mature and secondary forest, the species uses shade-cocoa plantations known lo cally as cabruca (Raboy et al 2004, Oliveira 2010). e spe cies geographic range is characterized by two distinct veg etation types: coastal humid forest in the east, where cocoa production is the predominant agricultural activity, and semi-deciduous mesophytic forest in the west, where cattle ranching is widely practiced (Pinto and Rylands 1997). Because shade-cocoa production in this region utilizes a canopy of native trees, large swaths of forested habitat are still available for GHLTs throughout the east compared to the small, fragmented forest cover interspersed by open cattle ranches in the west. However, forest throughout the species range was lost at a rate of 13% over the last 20 years, and this deforestation rate is projected to increase as shade cocoa plantations are converted to cattle pastures fol lowing declines in cocoa prices and fungal epidemics that devastated the cocoa industry beginning in the early 1990s ( Schroth & Harvey, 2007 ). Additionally, planned changes to Brazils Forest Act will eliminate enforced protection of certain areas of existing forest ( Calmon et al., 2011 ). Be cause the majority of native vegetation within the GHLT range is found on private land where extreme pressure for agricultural expansion is highest ( Sparovek et al., 2010 ; Ferreira et al., 2012 ), a better understanding of the needs of GHLTs and the protection of their habitat is becoming increasingly critical for the survival of this species. Overview of existing knowledge relevant to the in situ conservation of the species e two-day symposium was structured to allow for a day of research presentations and a day of discussion. rough 16 presentations, participants presented the major results of their recently concluded or ongoing research programs. Topics included ecology and behavior of GHLTs in vari ous habitat types, genetic structure and health of GHLT populations, the impacts of forest fragmentation/connec tivity and climate change on the species, and updates on the activities of NGOs and the status of protected areas within the species distribution range. Following presenta tions, participants summarized existing knowledge on in situ GHLT biology, ecology and conservation based on past research programs/publications and on the information presented at the symposium (Tables 1 & 2). Additional information (e.g. population surveys, extensive GIS work, population and landscape modelling, genetic sampling, and health assessments) not listed in Table 2 is available at the level of the entire distribution range. Dening priorities for future research and conservation Following the summation of existing knowledge, partici pants worked in break-out groups to identify what they deemed the top ve most signicant research gaps in GHLT research and knowledge. Working group results were presented and discussed in a plenary session. e topics identied as highest priority research areas included: 1. Ecology, biology, health status, and genetic dierentiation of western populations : Demographic and landscape model ing have demonstrated that without protective measures, all western populations are in immediate danger of extinc tion in the short term (Zeigler, unpubl. data). Despite this urgency, basic scientic information (i.e. ecology, basic bi ology, genetic dierentiation, and health status) needed to develop sound conservation measures is still unavailable for these populations. Such information will improve our un derstanding of the species management needs throughout its range. 2. GHLTs and cabruca agroforest : Cabruca plantations can range from heavily managed monocultures to highly natu ral mosaics of cacao trees and endemic tree species, and not all forms are suitable as GHLT habitat. Research focusing on the presence/absence of GHLTs and their comparative demography and ecology along the full spectrum of ca bruca agroforest is essential to understanding the species habitat and management needs and balancing regional so cioeconomics with conservation. 3. GHLT dispersal and survival in fragmented landscapes : Very little is known about how GHLTs move and survive in fragmented forest; how often individuals leave forest boundaries and move through non-forest matrix, how far

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74 individuals travel through non-forest matrix, what land scape elements individuals are willing to travel through and which elements act as barriers to dispersal, the probability that dispersing individuals will survive the journey, and whether other characteristics (such as patch occupancy by GHLTs) inuence dispersal and settlement. is informa tion is critical for landscape-level conservation planning. 4. A new census of the current GHLT distribution : Given con tinuing threats across the species distributional range, the size and locations of populations are likely to still change/ decline. Knowing how many individuals/populations exist and where they are located is of vital importance to man aging and protecting the species in addition to improving our understanding of population trends and gauging the eectiveness of conservation eorts. 5. GHLT use and behavior in unknown habitat types : Re search has thus far focused on GHLTs in primary forest, degraded forest, and cabruca agroforest. Little is known re garding if and how GHLTs use other habitat types such as restinga high altitude forest, or other agroforestry systems. 6. reat impact analysis : reats to GHLT survival have been identied and include broad processes like forest loss and fragmentation and climate change. Information on the specic nature of these threats and their impacts on GHLT survival, however, is limited. A better understanding of these threats is necessary for protecting GHLT populations from negative impacts. 7. Environmental services provided by GHLTs : GHLTs are hypothesized to have an important role in ecosystem func tioning. Research is needed to better understand the im portance of the species in maintaining the structure and viability of the Atlantic Forest through, for example, seed dispersal. Since a major part of Brazils economy relies on Atlantic Forest resources, demonstrating that GHLTs themselves play a critical role in the functionality of the forest may be an alternative approach to securing conserva tion of the species and its habitat. 8. Environmental education : Research into the perceptions of local people towards GHLTs and conservation in gen eral is important for improving our understanding of their attitudes and oers important information for developing sound, ecient and viable education and outreach pro grams that involve all relevant stakeholders. Table 1. Denitions used to categorize the scope of available knowledge, sample size and duration of available studies on which the as sessment in Table 2 is based. Scope of information Denition of scope Sample on which knowledge is based Duration of study Homogeneous habitat Principally composed of relatively continuous mature forest, with only smaller patches of secondary forest. Maruim-REBIO Una, 17 groups (one study-site) 11 years Heterogeneous habitat Composed of a mixture of small and large patches of a wide variety of habitat types. Types of habitats include selectively logged and secondary forest in dierent stages of regeneration interspersed with abandoned agricultural elds and pastures in the process of regeneration (e.g. cocoa, rubber and jackfruit stands) as well as a mosaic of primary and secondary forest with cabruca agroforest. Piedade-REBIO Una, 5 groups (one study-site); 4 groups in the municipalities of Camacan, Jussari, Una and Arataca 8 years for Piedade-REBIOUna, 1 year for other groups Cabruca agroforest Cacao agroforest where the understory is replaced by cacao trees and around 10% of native canopy trees are left to provide shade for understory. e suitability of cabruca for GHLTs varies depending on the diversity and density of shade trees. 3 groups concentrated in the municipality of Ilhus 4 years and on-going Semi-deciduous forest Seasonal forested habitat in the western portion of the species range. 1 fragment, 2 groups 1 year Restinga Vegetation adapted to sandy soil; normally distributed along the coast and on soils under marine inuence. Currently no studies Currently no studies High altitude forest Areas of the GHLT range above 400m. Limited information from survey work across the species range and from two groups using a mosaic forest that were monitored for a few months in the cabruca study 1 season

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75 e symposium was concluded with a discussion of how we can ll these major research gaps and how communica tion between researchers and stakeholders can be improved in order to disseminate the results of research and improve the eciency of conservation eorts of the species. Conclusion We considered this meeting a very signicant event because it brought together the majority of researchers involved with the in situ conservation of GHLTs to discuss research and exchange ideas. e resulting overview of existing knowl edge and the list of knowledge gaps can serve as guidelines for the development of future research projects that wish to ultimately contribute to the development of conservation actions for the species. With this information, next steps will include reaching out to stakeholders involved with ac tivities relevant to the conservation of the Atlantic Forest in general and GHLTs in particular. It is important that research results presented during this symposium become available to the wider public, particularly to federal and non-governmental institutions and civil society. e format of the distributed information should allow stakeholders to see how their respective activities might aect GHLTs and the landscape in which they reside while suggesting the kind of alterations that may be required to make those activities more compatible with GHLT conservation. Ultimately, to maximize the long-term persistence of GHLTs, we need to conserve a functionally connected Table 2. Overview of key research topics relevant for the in-situ conservation of golden-headed lion tamarins and the current level of available knowledge (both published and unpublished) for those topics. Information is categorized per habitat/landscape or as global knowledge using the following scale: (0) No Information, (1) Little Information (i.e. information based on a single eld season and/or on only a few GHLT groups/individuals), (2) Moderate Information, (3) High Amount of Information (i.e. information based on multiple eld seasons and GHLT groups/individuals). Asterisks (*) indicate that data have been collected but not yet analyzed. Category of knowledge Scope of knowledge Homogeneous Heterogeneous Cabruca Semideciduous Restinga Altitude Mortality 3 2 1 0 0 Reproduction 3 2 2 1 0 0 Diet 2 2 2 1 0 0 Activity budget 3 3 2 1 0 0 Tree use 3 3 1 0 0 Predation 3* 3 3 0 0 0 Space use 3 3 2 1 0 0 Density 3 2 2 1 0 0 Group size 3 2 2 1 0 1 Home range size 3 2* 2 1 0 0 Health (parasites) 1 1 1 0 0 0 Associations with C. kuhlii 3* 2 2 1 0 0 Genetic diversity 3 1 1 0 0 Movement within fragments 3 3* 3* 1 0 0 Movement between fragments 0 0 0 0 0 0 Anthropic pressure 1 1 1 2 0 0 Community ecology 2 1 0 0 0 0 Environmental education 3 0 0 0 0 0 Mortality within matrix 0 0 0 0 0 0 Migration/emigration/immigration 2 1 0 0 0 0 Ethnozoology 0 0 0 0 0 0 Environmental quality 2 2 0 1 0 0 Extinction 3 3 2 0 0 Extinction rate 3 2 0 0 0 0

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76 landscape that oers adequate resources and allows GHLTs to move and breed successfully within the exceptionally heterogeneous environment of southern Bahia. Partly, this includes a much better understanding of the anthropogen ic pressures on GHLTs and their habitat. Of equal impor tance is the consideration of GHLTs within their broader ecological network and the Atlantic Forest ecosystem. Studying GHLTs as an integral part of the ecological net work of which they are a part will improve our understand ing of the species needs as well as its role within the ecosys tem, contributing to more ecient conservation actions in the long-term. To get to this point, critical research is still needed at both broader and narrower scales as described in this document. Broadening our focus to the entire Atlantic Forest while continuing to study essential aspects of the species biology, is likely the most ecient conservation strategy over the long-term. ere is an increasing demand for large-scale projects that focus on regions, their ecologi cal functionality, and the species within those regions. We hope that this document serves as a guideline for how to develop new projects and partnerships that incorporate this demand and contribute to the long-term persistence of GHLTs and the Atlantic Forest. Acknowledgments is symposium was made possible with nancial and structural support of the Centre for Research and Con servation of the Royal Zoological Society of Antwerp and logistical support from UESC. We thank Paula Reis and Juliana Monteiro for note-taking during the symposium, and Deborah Faria, Vanessa Nogueira, and Josinei da Silva Santos for advertising and logistical support. Funding to the CRC is provided by the Flemish Ministry of Economy, Science and Innovation (Belgium). Kristel De Vleeschouwer Centre for Research and Con servation-Royal Zoological Society of Antwerp, Antwerp, Belgium and Instituto de Estudos Socioambientais do Sul da Bahia, Ilhus, BA, Brasil, Leonardo Oliveira In stituto de Estudos Socioambientais do Sul da Bahia and Ps Graduao em Ecologia-Universidade Federal do Rio de Janeiro, RJ, Brasil, Becky Raboy Instituto de Estudos Socioambientais do Sul da Bahia and Smithsonian Con servation Biology Institute, Washington DC, USA, Nima Raghunathan Science and Environmental Management/ Behavioural Biology and Animal Psychology, University of Liege, Belgium, and Sara Zeigler Department of Biologi cal Sciences, Virginia Tech, Blacksburg VA, USA. References Calmon, M., Brancalion, P. H. S, Paese, A., Aronson, J., Castro, P., da Silva S. C. and Rodrigues R. R. 2011. Emerging threats and opportunities for large-scale eco logical restoration in the Atlantic Forest of Brazil. Restor. Ecol. 19(2): 154158. Ferreira, J., Pardini, R., Metzger, J. P., Fonseca, C. R., Pompeu, P. S., Sparovek, G., and Louzada, J. 2012. To wards environmentally sustainable agriculture in Brazil: challenges and opportunities for applied ecological re search. J. Appl. Ecol 49(3): 535541. IUCN, 2012. IUCN Red List of reatened Species, ver sion 2010.3. In IUCN (ed.), Gland, Switzerland. Oliveira, L. 2010. Ecology and demography of goldenheaded lion tamarins ( Leontopithecus chrysomelas ) in Cabruca agroforest, Bahia state, Brazil. Doctoral thesis, University of Maryland, USA. Oliveira, L. C., Neves, L. G., Raboy, B. E. and Dietz, J. M. 2011. Abundance of jackfruit ( Artocarpus heterophyllus ) aects group characteristics and use of space by goldenheaded lion tamarins ( Leontopithecus chrysomelas ) in Ca bruca agroforest. Environ. Manage 48: 248262. Pinto, L., and Rylands A. 1997. Geographic distribution of the golden-headed lion tamarin, Leontopithecus chrysome las : Implications for its management and conservation. Folia Primatol 68:161180. Raboy, B. E., Christman M. C., and Dietz J. M.,. 2004. e use of degraded and shade cocoa forests by endan gered golden-headed lion tamarins Leontopithecus chrys omelas Oryx 38:7583. Raboy, B. E. and Dietz, J. M. 2004. Diet, foraging, and use of space in wild golden-headed lion tamarins. Am. J. Primatol 63:115. Schroth, G., and Harvey, C.A. 2007. Biodiversity conser vation in cocoa production landscapes: an overview. Bio divers. Conserv 16:22372244. Sparovek, G., Berndes, G., Klug, I. L. F. and Barretto, A. G. O. P. 2010. Brazilian agriculture and environmental legislation: status and future challenges. Environ. Sci. Technol 44: 60466053. Zeigler, S., Fagan, W. F., Defries, R. and Raboy, B. E. 2010. Identifying important forest patches for the long-term persistence of the endangered golden-headed lion tama rin ( Leontopithecus chrysomelas ). Tropical Conservation Science 3:6377. Recent Publications BOOKS Field and Laboratory Methods in Primatology: A Practical Guide edited by Joanna M. Setchell & Deborah J. Curtis. 2011. Cambridge University Press. 456 pp. ISBN: 978 052114213. e second edition of this guide to research on wild primates covers the latest advances in the eld, in cluding new information on eld experiments and measur ing behavior. It provides essential advice on the technical and practical aspects of both eld and laboratory methods. Contents: 1. An ethno primatological approach to interac tions between human and non-human primates JonesEngel L, Engel GA & Fuentes A; 2. Habituating primates:

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77 processes, techniques, variables and ethics Williamson EA & Feistner ATC; 3. Habitat description and phenology Ganzhorn JU, Rakotondranary SJ. & Rakotondranary YR; 4. Geographical information systems and remote sens ing Osborne PE & Glew L; 5. Monitoring local weather and climate Mayes JC & Pepin N; 6. Survey and census methods: population distribution and density Ross C & Reeve N; 7. Trapping primates Jolly CJ, Phillips-Conroy JE & Mller AE; 8. Handling, anaesthesia, heatlh evalu ation and biological sampling Unwin S, Ancrecaz M & Bailey W; 9. Morphology, morphometrics and taxonomy Groves C & Harding J; 10. Marking and radio-tracking primates Honess PE & Macdonald DW; 11. Field experi ments with non-human primates: a tutorial Zuberbhler K & Wittig RM; 12. Feeding ecology, frugivory and seed dispersal Dew JL; 13. Dietary analysis I: food physics Lucas PW, Osorio D, Yamashita N, Prinz JF, Dominy NJ & Darvell BW; 14. Dietary analysis II: food chemistry Lucas PW, Corlett RT, Dominy NJ, Essackjee HC, RibaHernandez P, Ramsden L, Stoner KE & Yamashita N; 15. Collecting arthropods and arthropod remains for primate studies Ozanne CMP, Bell JR & Weaver DG; 16. Record ing primate vocalizations Geissmann T & Parsons S; 17. Photography and video for eld researchers Rowe N & Myers M; 18. Chronobiological aspects of primate research Erket HG; 19. ermoregulation and energetics Schmid J; 20. Field endocrinology: monitoring hormonal changes in free-ranging primates Hodges JK & Heistermann M; 21. Collection, storage and analysis of non-invasive genetic material in primate biology Goossens B, Anthony N, Jef fery K, Johnson-Bawe M & Bruford MW; 22. Tips from the bush: an A-Z of suggestions for successful eld work Bearder SK & Nekaris AI. ARTICLES Azevedo E, Miranda M, de Campos M, Moreira AP, Rios M, Magalhes F, Guimares F, Ecco R, Resende M. 2011. Outbreak of Human Herpesvirus Type 1 Infection in Nonhuman Primates ( Callithrix penincillata ). J. Wildlife Disease 47 (3):690693. Babb PL, Fernndez-Duque E, Baiduc CA, Gagneux P, Evans S, Schurr TG. 2011. mtDNA diversity in azaras owl monkeys ( Aotus azarai azarai ) of the Argentinean Chaco. Am. J. Phys. Anthropol. 146(2): 209224. Babb PL, McIntosh AM, Fernndez-Duque E, Di Fiore A, Schurr TG. 2011. An Optimized Microsatellite Geno typing Strategy for Assessing Genetic Identity and Kin ship in Azaras Owl Monkeys (Aotus azarai) Folia Prima tol. 82(2): 107117. Barbosa Caselli C, Setz EZF. 2011. Feeding ecology and activity pattern of black-fronted titi monkeys ( Callicebus nigrifrons ) in a semideciduous tropical forest of southern Brazil. Primates 52(4): 351359 Bashaw MJ, McIntyre C, Salenetri ND. 2011. Social or ganization of a stable natal group of captive Guyanese squirrel monkeys ( Saimiri sciureus sciureus ). Primates 52(4): 361. Boubli JP, Couto-Santos FR, Strier KB. 2011. Structure and oristic composition of one of the last forest frag ments containing the critically endangered northern muriqui ( Brachyteles hypoxanthus primates). Ecotropica 17 (2) Bowler M, Bodmer RE. 2011. Diet and food choice in Peruvian red uakaris ( Cacajao calvus ucayalii ): selective or opportunistic seed predation? Int. J. Primatol. 32(5): 11091122 Bunce JA, Isbell LA, Grote MN, Jacobs GH. 2011. Color vision variation and foraging behavior in wild Neotropical titi monkeys ( Callicebus brunneus ): possible mediating roles for spatial memory and reproductive status. Int. J. Primatol. 32(5): 10581075 Caperos JM, Snchez S, Pelez F, Fidalgo A, Morcillo A. 2011. e eect of crowding on the social behavior of the cooperatively breeding Cotton-top tamarins ( Sagui nus oedipus ). Int. J. Primatol. 32(5): 11791189 Carnegie SD, Fedigan LM, Melin AD. 2011. Reproduc tive seasonality in female capuchins ( Cebus capucinus ) in Santa Rosa (Area de Conservacin Guanacaste), Costa Rica. Int. J. Primatol. 32(5): 10761090 Carnegie SD, Fedigan LM, Ziegler TE. 2011. Social and environmental factors aecting fecal glucocorticoids in wild, female white-faced capuchins ( Cebus capucinus ). Am. J. Primatol. 73 (9): 861869. Cedillo-Pelez C, Rico-Torres CP, Salas-Garrido CG, Correa D. 2011. Acute toxoplasmosis in squirrel monkeys ( Saimiri sciureus ) in Mexico. Vet parasitol 180: 368371 Chaves OM, Stoner KE, Arroyo-Rodrguez V. 2011. Sea sonal dierences in activity patterns of georoyis spider monkeys ( Ateles georoyi ) living in continuous and frag mented forests in southern Mexico. Int. J. Primatol. 32(4): 960973 Coutinho LN, Monteiro FOB, Takeshita RSC, de Miranda Lins e Lins FL, da Silva GA, Faturi C, de Castro PHG, Muniz JAPC, Kugelmeier T, Whiteman CW, Vicente WRR. 2011. Eect of age and number of parturitions on uterine and ovarian variables in owl monkeys. J. Med. Prim. 40(5): 310316. Crofoot MC, Rubenstein DI, Maiya AS, Berger-Wolf TY. 2011. Aggression, grooming and group-level cooperation in white-faced capuchins ( Cebus capucinus ): insights from social networks. Am. J. Primatol. 73 (8): 821833. Culot L, Lledo-Ferrer Y, Hoelscher O, Muoz Lazo FJJ, Huynen M-C, Heymann EW. 2011. Reproductive fail ure, maternal infanticide and cannibalism in wild mous tached tamarins, Saguinus mystax. Primates 52:179186. da Cunha DB, Monteiro E, Vallinoto M, Sampaio I, Fer rari SF, Schneider H. 2011. A molecular phylogeny of the tamarins (genus Saguinus ) based on ve nuclear sequence data from regions containing Alu insertions. Am. J. Phys. Anthropol. 146(3): 385391. Dufour V, Sueur C, Whiten A, Buchanan-Smith HM. 2011. e impact of moving to a novel environment on

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78 social networks, activity and wellbeing in two new world primates. Am. J. Primatol. 73 (8): 802811. Fernndez-Duque E. 2011. Renschs rule, Bergmanns eect and adult sexual dimorphism in wild monogamous owl monkeys ( Aotus azarai ) of Argentina. Am. J. Phys. Anthropol. 146 (1): 3848. Fernndez-Duque E, Burke K, Schoenrock K, Wolovich CK, Valeggia CR. 2011. Hormonal Monitoring of Re productive Status in Monogamous Wild Female Owl Monkeys (Aotus azarai) of the Argentinean Chaco. Folia Primatol. 82(3): 143153. Ferrari SF, Beltro-Mendes R. 2011. Do snakes represent the principal predatory threat to callitrichids? Fatal attack of a viper ( Bothrops leucurus ) on a common marmoset ( Callithrix jacchus ) in the Atlantic Forest of the Brazilian Northeast. Primates 52(3): 207209 Fragaszy DM, Deputte B, Cooper EJ, Colbert-White EN, Hmery C. 2011. When and how well can human-social ized capuchins match actions demonstrated by a familiar human? Am. J. Primatol. 73 (7): 643654. Fragaszy DM, Stone BW, Scott NM, Menzel C. 2011. How tufted capuchin monkeys ( Cebus apella spp) and common chimpanzees ( Pan troglodytes ) align objects to surfaces: insights into spatial reasoning and implications for tool use. Am. J. Primatol. 73 (10): 10121030. Gonzlez-Hernndez M, Dias PAD, Romero-Salas D, Ca nales-Espinosa D. 2011. Does home range use explain the relationship between group size and parasitism? A test with two sympatric species of howler monkeys. Primates 52(3): 211216 Gonzlez-Zamora A, Arroyo-Rodrguez V, Chaves OM, Snchez-Lpez S, Aureli F, Stoner KE. 2011. Inuence of climatic variables, forest type, and condition on activity patterns of georoyis spider monkeys throughout Meso america. Am. J. Primatol. 73 (12): 11891198. Heymann EW. 2011. Florivory, nectarivory and pollina tion a review of primate-ower interactions. Ecotropica 17: 4152. Heymann EW. 2011. Coordination in primate mixed-spe cies troops. In: Coordination in human and non-human primate groups Boos M, Kolbe M, Ellwart T, Kappeler PM (eds.). Heidelberg: Springer, p 263281. Huck M, Rotundo M, Fernndez-Duque E. 2011. Growth and Development in Wild Owl Monkeys ( Aotus azarai ) of Argentina. Int. J. Primatol. 32(5): 11331152 Jaeggi AV, Van Schaik CP. 2011. e evolution of food sharing in primates. Behav. Ecol. Sociobiol. 65 (11): 21252140. Kelaita M, Dias PAD, Aguilar-Cucurachi MS, CanalesEspinosa D, Corts-Ortiz L. 2011. Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. Am. J. Phys. Anthropol. 146 (2): 179187. Lampert RMS, de Azevedo CVM, Menezes AAL. 2011. Inuence of dierent light intensities on the daily groom ing distribution of common marmosets Callithrix jac chus. Folia Primatol. 82(3): 131142. Lledo-Ferrer Y, Pelez F, Heymann EW. 2011. e equivo cal relationship between territoriality and scent marking in wild saddleback tamarins ( Saguinus fuscicollis ). Int. J. Primatol. 32(4): 974991 Mndez-Carvajal P. 2011. Population size, distribution and conservation status of howler monkeys ( Alouatta coibensis trabeata ) and spider monkeys ( Ateles georoyi azuerensis ) on the Azuero peninsula, Panama. Prim. Cons. 26. Mohanasundaram D, Drogemuller C, Brealey J, Jessup CF, Milner C, Murgia C, Lang CJ, Milton A, Zalewski PD, Russ GR, Coates PT. 2011. Ultrastructural analysis, zinc transporters, glucose transporters and hormones ex pression in New World primate ( Callithrix jacchus ) and human pancreatic islets. Gen. Comp. Endocrinol. 174 (2): 7179. Morimoto Y, Fujita K. 2011. Capuchin monkeys ( Cebus apella ) modify their own behaviors according to a con specics emotional expressions. Primates 52(3): 279286 Nakamura N, Amato KR, Garber P, Estrada A, Mackie RI, Gaskins HR 2011. Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys ( Alouatta pigra ) in Palenque national park, Mexico. Am. J. Primatol. 73 (9): 909919. Nascimento ATA, Schmidlin LAJ, Valladares-Padua CB, Matushima ER, Verdade LM. 2011. A comparison of the home range sizes of mainland and island populations of black-faced lion tamarins ( Leontopithecus caissara ) using dierent spatial analysis. Am. J. Primatol. 73 (11): 11141126. Norris D, Rocha-Mendes F, Marques R, de Almeida R, Galetti M. 2011. Density and spatial distribution of buy-tufted-ear marmosets ( Callithrix aurita ) in a con tinuous Atlantic Forest. Int. J. Primatol. 32(4): 811829 Obaldia III N, Otero W, Marin C, Aparicio J, Cisneros G. 2011. Long-term eect of a simple nest-box on the reproductive eciency and other life traits of an Aotus lemurinus lemurinus monkey colony: an animal model for malaria research. J. Med. Primatol. 40(6): 383391. Oliveira LC, Dietz JM. 2011. Predation risk and the in terspecic association of two Brazilian Atlantic forest primates in Cabruca agroforest. Am. J. Primatol. 73 (9): 852860. Palma AC, Vlez A, Gmez-Posada C, Lpez H, Zrate DA, Stevenson PR. 2011. Use of space, activity patterns, and foraging behavior of red howler monkeys ( Alouatta seniculus ) in an Andean forest fragment in Colombia. Am. J. Primatol. 73 (10): 10621071. Pinheiro T, Ferrari SF, Lopes MA. 2011. Polyspecic asso ciations between squirrel monkeys ( Saimiri sciureus ) and other primates in eastern Amazonia. Am. J. Primatol. 73 (11):11451151. Printes RC, Rylands AB, Bicca-Marques JC. 2011. Distri bution and status of the Critically Endangered blond titi monkey Callicebus barbarabrownae of north-east Brazil. Oryx 45(3): 439 Raboy BE, Neves LG, Zeigler SL, Oliveira, LC. 2011. Occurrences of the golden-headed lion tamarin ( Leonto pithecus chrysomelas ) above 500 meters in southern Bahia,

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79 Brazil and implications for conservation planning. Prim. Cons. 26. Ramos-Fernndez G, Pinacho-Guendulain B, MirandaPrez A, Boyer D. 2011. No evidence of coordination between dierent subgroups in the ssionfusion soci ety of spider monkeys ( Ateles georoyi ). Int. J. Primatol. 32(6): 13671382 Rein TR. 2011. e correspondence between proximal phalanx morphology and locomotion: Implications for inferring the locomotor behavior of fossil catarrhines Am. J. Phys. Anthropol. 146(3): 435445. Rovirosa-Hernndez MJ, Garca-Ordua F, Caba M, Canales-Espinosa D, Hermida-Lagunes J, Torres-Pelayo VR. 2011. Blood parameters are little aected by time of sampling after the application of ketamine in black howler monkeys ( Alouatta pigra ). J. Med. Primatol. 40(5): 294299. Ruiz-Garca M, Vsquez C, Camargo E, Leguizamn N, Glvez H et al. 2011. Molecular Phylogenetics of Aotus (Platyrrhini, Cebidae). Int. J. Primatol. 32(5): 12181241 Russo GA, Young JW. 2011. Tail growth tracks the ontog eny of prehensile tail use in capuchin monkeys ( Cebus albifrons and C. apella ). Am. J. Phys. Anthropol. 146(3): 465473. Schino G, Palumbo M, Visalberghi E. 2011. Factors Af fecting Urine Washing Behavior in Tufted Capuchins ( Cebus apella ). Int. J. Primatol. 32(4): 80181. Serra Rego B, Spyrides MHC, Cordeiro de Sousa MB.2011. Possible organizational eect of sex steroids on the stabili zation of manual preference in female common marmo sets ( Callithrix jacchus ). Primates 52(4): 343349 Shanee S, Shanee N. 2011. Population density estimates of the Critically Endangered yellow-tailed woolly monkeys ( Oreonax avicauda ) at La Esperanza, Northeastern Peru. Int. J. Primatol. 32(4):878888 Smith HM, ompson CL. 2011. Observations of hand preference in wild groups of white-faced sakis ( Pithecia pithecia ) in Suriname. Am. J. Primatol. 73 (7): 655664. Souza-Alves JP, Fontes IP, Chagas RRD, Ferrari SF. 2011. Seasonal versatility in the feeding ecology of a group of titis ( Callicebus coimbrai ) in the northern Brazilian Atlan tic Forest. Am. J. Primatol. 73 (12):11991209. Stevenson PR. 2011. e abundance of large ateline mon keys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica 43 (4): 512519. ompson CL, Donley EM, Stimpson CD, Horne WI, Vinyard CJ. 2011. e inuence of experimental ma nipulations on chewing speed during in vivo laboratory research in tufted capuchins ( Cebus apella ). Am. J. Phys. Anthropol. 145 (3): 402414. ompson CL, Norconk MA. 2011. Within-group social bonds in white-faced saki monkeys ( Pithecia pithecia ) display malefemale pair preference. Am. J. Primatol. 73 (10): 10511061. Tiddi B, Aureli F, Schino G, Voelkl B. 2011. Social rela tionships between adult females and the alpha male in wild tufted capuchin monkeys. Am. J. Primatol. 73 (8): 812820. Vermeer J, Tello-Alvarado JC, Moreno-Moreno S, GuerraVsquez F. 2011. Extension of the Geographical Range of White-browed Titi Monkeys ( Callicebus discolor ) and Evidence for Sympatry with San Martin Titi Monkeys ( Callicebus oenanthe ). Int. J. Primatol. 32(4): 924930 Vidal-Garca F, Serio-Silva JC. 2011. Potential distribu tion of Mexican primates: modeling the ecological niche with the maximum entropy algorithm. Primates 52(3): 261270 Wedi E, Nayudu PL, Michelmann HW. 2011. A case report of spontaneous opening of congenitally fused labia in a female common marmoset ( Callithrix jacchus ) fol lowed by pregnancy and birth of twins. J. Med. Primatol. 40(5): 351353. Yamasaki T, Duarte AMRC, Curado I, Summa MEL, Neves DVDA, Wunderlich G, Malafronte RS. 2011. De tection of etiological agents of malaria in howler monkeys from Atlantic Forests, rescued in regions of So Paulo city, Brazil. J. Med. Primatol. 40(6): 392400. Zimbler-DeLorenzo HS, Dobson FS. 2011. Demography of squirrel monkeys ( Saimiri sciureus ) in captive environ ments and its eect on population growth. Am. J. Prima tol. 73 (10): 10411050. Zimbler-DeLorenzo HS, Stone AI. 2011. Integration of eld and captive studies for understanding the behavioral ecology of the squirrel monkey ( Saimiri sp.). Am. J. Pri matol. 73 (7): 607622. ABSTRACTS Selected abstracts relating with neotropical primates from the 34 rd Meeting of the American Society of Primatologists, Austin, Texas, USA, September 16 to 19, 2011 Adams DB, Rehg J, Watsa M. 2011. Observations of ter mitarium geophagy by bald-faced saki monkeys ( Pithecia irrorata ) in Madre De Dios, Peru. Alvarado Villalobos M, Serio-Silva JC, Gatica-Colima AB, Garca-Hernndez J. 2011. Prevalence and intensity of intestinal parasites of Alouatta pigra in forest fragments in playas de Catazaj, Chiapas. Amato KR, Yeoman CJ, RighiniN, Kent A, Estrada A, Stumpf RM, Nelson KE, Torralba M, Gillis M, Leigh SR. 2011. e inuence of habitat on Mexican black howler ( Alouatta pigra ) gut microbial community composition. Barahona P, Campbell C, Ramirez S. 2011. An assessment of black-handed spider monkey ( Ateles georoyi ) mobility using GPS data, Barro Colorado Island, Panama. Behie A, Pavelka M. 2011. Why do primates in disturbed habitats show increased parasitism? a new mechanism proposed. Brenskelle LM, Rapaport L. 2011. Caretaker contributions to foraging behavior in young wild golden lion tamarins ( Leontopithecus rosalia ) in the Uniao Reserve, Brazil.

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80 Chism J, Kieran T. 2011. Vocalizations of Peruvian Equa torial sakis ( Pithecia aequatorialis ). Corewyn LC, Clarke MR, Glander KE. 2011. Variation in male dominance relationships in two multimale groups of mantled howlers ( Alouatta palliata ) at La Pacica, Costa Rica. Di Fiore A, Link A. 2011. Male mating strategies and pa ternity in white-bellied spider monkeys ( Ateles belzebuth ) of Amazonian Ecuador. Eadie EC. 2011. Age of achievement of maximum foraging return rates in wild capuchin monkeys ( Cebus capucinus ): a test of the ecological complexity model for long juvenile periods. Eshchar Y, Crast J, Fragaszy D. 2011. Visual attention to social partners in capuchin monkeys. Evans KJ, Pavelka MS, Hartwel KSl, Notman H. 2011. Is infant handling a mechanism for male bond formation in Ateles georoyi ?. Evans TA, Beran MJ, Paglieri F, Addessi E. 2011. Delay of gratication for accumulating tokens and rewards in capuchin monkeys ( Cebus apella ). Fernndez-Duque E, Evans S, Emery-ompson M. 2011. A lab-eld approach to estimating the energetic costs of biparental care in owl monkeys. Fisher-Phelps M, Gothberg JM, Mendoza SP, Mason WA, Bales KL. 2011. Temperament testing in coppery titi monkeys ( Callicebus cupreus ). French JA. 2011. Reproductive steroids across the lifespan in male marmoset monkeys. Gonzles Valentin E, Scarry CJ. 2011. Eects of female re productive status on activity budget, ingestion rates and energy intake in tufted capuchin monkeys ( Cebus apella ). Hinde KJ, Maninger N, Mendoza SP, Mason WA, Wang GB, Cherry SL, Bales KL. 2011. Neurobiological chang es in the reward circuit following pair-bond formation in monogamous titi monkeys ( Callicebus cupreus ). Jack KM, Schoof VA, Sheller CR, Rich CI, Klingelhofer PP. 2011. e inuence of age and dominance status on fecal testosterone, dihydrotestosterone, and cortisol ex cretion in male white-faced capuchin monkeys ( Cebus capucinus ) in Santa Rosa National Park, Costa Rica. Jarcho M, Mendoza SP, Bales KL. 2011. e eects of social condition and experience on physiological reactiv ity in a monogamous primate ( Callicebus cupreus ). Kloc B, Rapaport LG, Warneke M, Ballou J, Mickelberg J. 2011. Mothers prefer helpers: birth sex ratio adjustment in captive Callitrichids. Lam K, Cortez N, Ratnam R. 2011. Antiphonal calling in single-housed, free-behaving marmosets ( Callithrix jacchus ). Link A, Di Fiore A. 2011. Intergroup competition and ag gression in wild spider monkeys ( Ateles belzebuth ). Maninger N, Hinde K, Mendoza SP, Mason WA, Cherry SR, Bales KL. 2011. Functional imaging of pair-bond formation in the coppery titi monkey ( Callicebus cupreus ). Massaro L, Liu Q, Visalberghi E, Fragaszy D. 2011. Wild bearded capuchins ( Cebus libidinosus ) select tools to min imize transport distance. Meno WE, Coss R, Perry S. 2011. e impact of the social environment on the development of antipredator behav ior in white-faced capuchin monkeys ( Cebus capucinu s). Notman H, Hartwell K, Pavelka MS. 2011. Seasonal varia tion in sexual segregation in spider monkeys ( Ateles geof froyi yucatanensis ) at Runaway Creek Nature Preserve, Belize. Parrish AE, Brosnan SF. 2011. Active tool transfer in a co operative task by capuchin monkeys ( Cebus apella ). Paukner A, Suomi SJ. 2011. Fur rubbing aects sub sequent social behavior in captive capuchin monkeys ( Cebus apella ). Perry SE, Godoy I, Lammers W. 2011. Alpha male tenures and male reproductive success in wild white-faced capu chin monkeys, C. capucinus at Lomas Barbudal, Costa Rica. Petracca MM, Caine NG. 2011. Individually distinct alarm calls in Georoys marmosets. Phillips KA, Wey H, Holder N, Kochunov P. 2011. Rest ing-state functional connectivity in capuchin monkeys ( Cebus apella ). Porter LM, Garber PA. 2011. Decision-making and spa tial memory in wild saddleback tamarins ( Saguinus fuscicollis). Ragen BJ, Maninger N, Mendoza SP, Jarcho MR, Bales KL. 2011. Mu opioid receptor involvement in social and non-social behaviors in titi monkeys ( Callicebus cupreus ). Reagan NA, Campbell CJ, Essiambre D. 2011. Distribu tion of the Azuero spider monkey in forest fragments. Rogge JR, Sherenco KD, Malling R, iele E, Schapiro SJ, Lambeth SP, Williams LE. 2011. Establishing a positive reinforcement training program in Neotropical primates: a comparison of squirrel and owl monkeys. Rubin TL, de Waal F. 2011. Discrimination of conspecic emotional facial expressions in captive tufted capuchins ( Cebus apella ). Rutherford JN, Ross CS, Tardif SD. 2011. Early life pro gramming of stillbirths in adult female common marmo sets ( Callithrix jacchus ). Scarry CJ. 2011. Between-group contest competition in tufted capuchin monkeys ( Cebus apella). Sharpe D, Vratanina T, Cudmore B, Markham K. 2011. Parasite prevalence in free-ranging mantled howler mon keys ( Alouatta palliata ), La Suerte Biological Field Sta tion, Costa Rica. Sherenco KD, Freeman H, Schapiro SJ, Lambeth SP, Wil liams LE. 2011. Behavioral and physiological impacts of shifting light periods in a captive Aotus colony. Simon RH, Mendoza SP, Lindsay KA, Bales KL. 2011. Validation of an open eld test as a measure of anxietylike and exploratory behavior in infant titi monkeys ( Cal licebus cupreus ). Slack A, Rapaport LG. 2011. Coforaging in wild golden lion tamarins ( Leontopithecus rosalia ) in the Uniao Re serve, Brazil. Smith AS, Birnie AK, French JA. 2011. Social isolation af fects partner-directed social behavior and cortisol during

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81 pair formation in male and female white-faced marmo sets, Callithrix georoyis Stollenmaier S, Leavens DA. 2011. Captive, common squirrel monkeys ( Saimiri sciureus ) select ve visual arbi trary symbols in accordance with food preferences. Sullivan JM, Freeman HD, Schultz-Darken N, Brosnan S. 2011. Responses to inequitable outcomes in a coopera tive breeder, the common marmosets ( Callithrix jaccus ). Talbot CF, Freeman HD, Williams LE, Brosnan SF. 2011. Squirrel monkeys response to inequitable outcomes indi cates a behavioral convergence within the primates. Valencia L, Link A, Cadena CD, di Fiore A. 2011. Phylo geography of brown spider monkeys ( Ateles hybridus ) in Colombia: testing the riverine barrier hypothesis. Valero MD, Pasanen EG, McFadden D, Ratnam R. 2011. Distortion-product otoacoustic emissions in the common marmoset ( Callithrix jacchus ): parameter optimization and repeatability. Van Belle S, Estrada A, Garber PA. 2011. Collective group movement and leadership in black howler monkeys ( Al ouatta pigra ). Vidal-Garcia F, Argello-Snchez LE, Corona-Callejas NE, Serio-Silva JC. 2011. Environmental education activities: a tool for primates conservation in Mexico. Vidal-Garcia F, Serio-Silva JC. 2011. Validation of poten tial distribution models of howler monkeys ( Alouatta pigra and Alouatta palliata ) in Tabasco, Mexico. Ziegler TE. 2011. Social eects via sensory stimuli on re productive function & dysfunction in cooperative breed ing marmosets and tamarins. Meetings 2012 III Congreso Colombiano de Primatologa La Asociacin Primatolgica Colombiana junto con la Universidad del Norte y la Fundacin Proyecto Tit, or ganizarn el III Congreso Colombiano de Primatologa dentro del marco del evento Biodiversidad: Recurso Estrat gico el cual se llevar a cabo en Abril de 2012, en la ciudad de Barranquilla Colombia. XXVI Congress of the International Primatological Society e XXVI congress of the International Primatological Society will be held at the Cancn Convention Center, Cancn, Mexico, from August 1217, 2012. For more in formation visit http://www.ips2012.org.mx/ 5 th Conference of the International Society for Gesture Studies: the communicative body in development e conference, sponsored by the International Society for Gesture Studies (ISGS) will be held from July 2427 at Lund, Sweden. For more information visit http://www. gesturestudies.com/isgs2012/ International Symposium on Primate Research e symposium will be held at Kunming, Yunnan, China P.R. from August 1921, 2012, and is sponsored by the Yunnan Key Laboratory of Primate Biomedical Research. For more information visit http://www.lpbr.cn/symposium

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Scope e journal/newsletter aims to provide a basis for conservation information relating to the primates of the Neotropics. We welcome texts on any aspect of primate conservation, including articles, thesis abstracts, news items, recent events, recent publications, primatological society information and suchlike. Submissions Please send all English and Spanish contributions to: Erwin Palacios, Conservacin Internacional Colombia, Carrera 13 # 71-41 Bogot D.C., Colombia, Tel: (571) 345-2852/54, Fax: (571) 3452852/54, e-mail: , and all Portuguese contributions to: Jlio Csar Bicca-Marques, Departamento de Biodiversidade e Ecologia, Pontifcia Universidade Catlica do Rio Grande do Sul, Av. Ipiranga, 6681 Prdio 12A, Porto Alegre, RS 90619-900, Brasil, Tel: (55) (51) 3320-3545 ext. 4742, Fax: (55) (51) 3320-3612, e-mail: . Contributions Manuscripts may be in English, Spanish or Portuguese, and should be double-spaced and accompanied by the text on CD for PC compatible text-editors (MS-Word, WordPerfect, Excel, and Access), and/or e-mailed to (English, Spanish) or (Portuguese). Hard copies should be supplied for all gures (illustrations and maps) and tables. e full name and address for each author should be included. Please avoid abbreviations and acronyms without the name in full. Authors whose rst language is not English should please have their English manuscripts carefully reviewed by a native English speaker. Articles. Each issue of Neotropical Primates will include up to three full articles, limited to the following topics: Taxonomy, Systematics, Genetics (when relevant for systematics and conservation), Bioge ography, Ecology and Conservation. Text for full articles should be typewritten, double-spaced with no less than 12 cpi font (preferably Times New Roman) and 3-cm margins throughout, and should not exceed 25 pages in length (including references). Please include an abstract in the same language as the rest of the text (English, Spanish or Portuguese) and (optional) one in Portuguese or Spanish (if the text is written in English) or English (if the text is written in Spanish or Portuguese). Tables and illustrations should be limited to six, except in cases where they are fundamental for the text (as in species descrip tions, for example). Full articles will be sent out for peer-review. For articles that include protein or nucleic acid sequences, authors must deposit data in a publicly available database such as GenBank/EMBL/ DNA Data Bank of Japan, Brookhaven, or Swiss-Prot, and provide an accession number for inclusion in the published paper. Short articles. ese manuscripts are usually reviewed only by the editors. A broader range of topics is encouraged, including such as behavioral research, in the interests of informing on general research activities that contribute to our understanding of platyrrhines. We encourage reports on projects and conservation and research programs (who, what, where, when, why, etc.) and most particularly information on geographical distributions, locality records, and protected areas and the primates that occur in them. Text should be typewritten, doublespaced with no less than 12 cpi (preferably Times New Roman) font and 3-cm margins throughout, and should not exceed 12 pages in length (including references). Figures and maps. Articles may include small black-andwhite photographs, high-quality gures, and high-quality maps. (Resolution: 300 dpi. Column widths: one-column = 8-cm wide; two-columns = 17-cm wide). Please keep these to a minimum. We stress the importance of providing maps that are publishable. Tables. Tables should be double-spaced, using font size 10, and prepared with MS Word. Each table should have a brief title. News items. Please send us information on projects, eld sites, courses, esis or Dissertations recently defended, recent publications, awards, events, activities of Primate Societies, etc. References. Examples of house style may be found throughout this journal. In-text citations should be rst ordered chronologically and then in alphabetical order. For example, (Fritz, 1970; Albert, 1980, 2004; Oates, 1981; Roberts, 2000; Smith, 2000; Albert et al. 2001) In the list of references, the title of the article, name of the journal, and editorial should be written in the same language as they were published. All conjunctions and prepositions (i.e., and, In) should be written in the same language as rest of the manuscript (i.e., y or e, En or Em). is also applies for other text in references (such as PhD thesis, accessed see below). Please refer to these examples when listing references: Journal article Stallings, J. D. and Mittermeier, R. A. 1983. e black-tailed marmoset ( Callithrix argentata melanura ) recorded from Paraguay. Am. J. Primatol. 4: 159. Chapter in book Brockelman, W. Y. and Ali, R. 1987. Methods of surveying and sampling forest primate populations. In: Primate Conservation in the Tropical Rain Forest, C. W. Marsh and R. A. Mittermeier (eds.), pp.23. Alan R. Liss, New York. Book Napier, P. H. 1976. Catalogue of Primates in the British Museum (Natural History). Part 1: Families Callitrichidae and Cebidae. British Museum (Natural History), London. esis/Dissertation Wallace, R. B. 1998. e behavioural ecology of black spider monkeys in north-eastern Bolivia. Doctoral thesis, University of Liverpool, Liverpool, UK. Report Muckenhirn, N. A., Mortensen, B. K., Vessey, S., Fraser, C. E. O. and Singh, B. 1975. Report on a primate survey in Guyana. Unpublished report, Pan American Health Organization, Washington, DC. Website UNESCO. 2005. UNESCO Man and the Biosphere Programme. United Nations Educational, Scientic, and Cultural Organisation (UNESCO), Paris. Website: http://www.unesco.org/mab/index.htm. Accessed 25 April 2005. (Acessada em 25 de abril de 2005 and Consultado el 25 de abril de 2005 for articles in Portuguese and Spanish respectively). For references in Portuguese and Spanish: and changes to e and y for articles in Portuguese and Spanish respectively. In changes to Em and En for articles in Portuguese and Spanish respectively. Doctoral thesis changes to Tese de Doutoramento and Tesis de Doctorado for articles in Portuguese and Spanish respectively. MSc esis changes to Dissertao de Mestrado and Tesis de Maestra for articles in Portuguese and Spanish respectively. Unpublished report changes to Relatrio Tcnico and Reporte no publicado for articles in Portuguese and Spanish respectively. Notes to Contributors

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Neotropical Primates A Journal and Newsletter of the IUCN/SSC Primate Specialist Group Vol. 18(2), December 2011 Contents Articles Howler and Capuchin Monkey Densities in Riparian Forests on Islands and Adjacent Shores On the Upper Paran River, Southern Brazil Lucas M. Aguiar, Gabriela Ludwig, James J. Roper, Walfrido K. Svoboda, Italmar T. Navarro and Fernando C. Passos ....................... 39 Short Articles Um Caso de Uso Espontneo de Ferramenta por Um Macaco-Prego ( Ce bus apella ) Mantido em Cativeiro Miguel Angelo Monteiro Lessa Olavo de Faria Galvo Paulo Elias Gotardelo Audebert Delage ........................................................... 4 4 First Observations of Terrestrial Travel for Olallas Titi Monkey ( C allicebus olallae ) Jess Martnez and Robert B. Wallace ............................................................................................................................................... 49 Extragroup Copulations in Alouatta guariba clamitans Karine Galisteo Diemer Lopes and Jlio Csar Bicca-Marque s ........................................................................................................... 5 2 e Southernmost Record of Mico emiliae (omas, 1920) for the State of Mato Grosso, Northern Brazil Guilherme Siniciato Terra Garbino ................................................................................................................................................... 5 3 Observations of Terrestrial Behavior in the Peruvian Night Monkey ( Aotus miconax ) in an Anthropogenic Landscape, La Esperanza, Peru Sam Shanee and Noga Shanee .......................................................................................................................................................... 5 5 A Wild Tamarin Without a Foot Survival Despite a Handicap Eckhard W. Heymann Ney Shahuano Tello and Oda Hlscher ........................................................................................................... 59 Observao de Comportamento Agonstico de Cebuella pygmaea Sobre Sciurus spadiceus em um Fragmento Florestal No Estado Do Acre, Brasil Rodrigo Otvio Almeida Canizo e Armando Muniz Calouro ............................................................................................................. 6 0 Further Information on Neotropical Monkeys in the XVI Century: Part 3 Bernardo Urbani ............................................................................................................................................................................. 6 2 Population Density of the Red Howler Monkey ( Alouatta seniculus ) in a Tropical Dry Forest Fragment in Northwestern Colombia Juan Carlos Meja Flrez and Jorge Andrs Lpez Delgado ................................................................................................................ 6 4 Registro Ocasional da Predao da Pomba-De-Bando ( Zenaida auriculata Des Murs, 1847) Pelo Sagi-Do-Cerrado ( Callithrix penicillata Georoy, 1812) No Interior De So Paulo, SP Felipe Bittioli R. Gomes e Renata C. de Lima-Gomes ......................................................................................................................... 68 News ...................................................................................................................................................................... 70 Recent Publications ................................................................................................................................................ 76 Meetings ................................................................................................................................................................ 81