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pt-BRNeotropical Primatespt-BRA Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group pt-BRConservation Internationalpt-BR 2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA ISSN 1413-4703 pt-BRAbbreviation:pt-BR Neotrop. Primatespt-BREditorspt-BR Erwin Palacios,pt-BR Conservacin Internacional Colombia, Bogot DC, Colombiapt-BR Liliana Corts Ortiz,pt-BR Museum of Zoology, University of Michigan, Ann Arbor, MI, USApt-BR Jlio Csar Bicca-Marques,pt-BR Pontifcia Universidade Catlica do Rio Grande do Sul, Porto Alegre, Brasilpt-BR Eckhard Heymann,pt-BR Deutsches Primatenzentrum, Gttingen, Germanypt-BR Jessica Lynch Alfaro,pt-BR Institute for Society and Genetics,pt-BR University of California-Los Angeles, Los Angeles, CA, USApt-BR Liza Veiga,pt-BR Museu Paraense Emlio Goeldi, Belm, Brazil New s and Books Reviewses-MX Brenda Solrzano, Instituto de Neuroetologa, Universidad Veracruzana,es-MX Xalapa, Mxicoes-MX Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, es-MX Xalapa, Mxico Founding Editorses-MX Anthony B. Rylands, Center for Applied Biodiversity Science Conservation International, Arlington VA, USAes-MX Ernesto Rodrguez-Luna, Instituto de Neuroetologa, Universidad Veracruzana, Xalapa, Mxico Editorial Boardpt-BR Bruna Bezerra, University of Louisville, Louisville, KY, USA pt-BR Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UKpt-BR Adelmar F. Coimbra-Filho, Academia Brasileira de Cincias, Rio de Janeiro, Brazilpt-BR Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USApt-BR Stephen F. Ferrari, Universidade Federal do Sergipe, Aracaj, Brazilpt-BR Russell A. Mittermeier, Conservation International, Arlington, VA, USApt-BR Marta D. Mudry, Universidad de Buenos Aires, Argentinapt-BR Horcio Schneider, Universidade Federal do Par, Campus Universitrio de Bragana, Brazilpt-BR Karen B. Strier, University of Wisconsin, Madison, WI, USApt-BR Maria Emlia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil Primate Specialist Grouppt-BR Chairman, pt-BRRussell A. Mittermeierpt-BR Deputy Chair, pt-BRAnthony B. Rylands pt-BR Coordinator, Special Section on Great Apes,pt-BR Liz Williamsonpt-BR Regional Coordinators Neotropicspt-BR pt-BR Mesoamerica,pt-BR Liliana Corts -Ortizpt-BR Andean Countries,pt-BR Erwin Palacios and Eckhard W. Heymannpt-BR Brazil and the Guianas,pt-BR M. Ceclia M. Kierul, Mauricio Talebi and Fabiano R. de Melopt-BR Regional Coordinators Africapt-BR West Africapt-BR, John F. Oatespt-BR East Africa, pt-BRDavid Mbora pt-BR Regional Coordinator Madagascarpt-BR Jrg U. Ganzhorn pt-BR Regional Coordinators Asiapt-BR China,pt-BR Long Yongchengpt-BR Southeast Asia,pt-BR Jatna Supriatna and Christian Roospt-BR South Asia,pt-BR Sally Walkerpt-BR Layout:pt-BR Kim Meek, Washington, DC
1 A SEARCHING FOR ALOUATTA PALLIATA IN NORTHERN COLOMBIA: CONSIDERATIONS FOR THE SPECIES DETECTION, MONITORING AND CONSERVATION IN THE DRY FORESTS OF BOLVAR, COLOMBIA Andrea Dechner 1 1 Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI. 48824, U.S.A. firstname.lastname@example.org Abstract e conservation status of A. palliata commonly referred to as black mantled howler monkey, is vulnerable in Colombia because of its decline in population. e distributional limit in the northeast of the country is not well dened and the dry forests of the north of the country are being destroyed at alarming rates. In the municipality of El Guamo (Bolvar) less than 20% of the landscape is composed of forests. e two largest remnants of forests in the municipality have extensions of 3,544.7 and 879.6 ha each. From interviews with the community, I concluded that habitat loss is the main threat to pri mate populations. 37.6 % of the community of inhabitants said they had seen the monkey in the municipality of Guamo, however, I found no A. palliata during a short transect sampling. Individuals of the species Alouatta seniculus and Saguinus oedipus were detected during these walks. Conservation actions such as reforestation, establishment of agroforestry systems and corridors designed to improve the habitat of A. palliata should encourage the participation of the human communities. Key Words: Black mantled howler monkey, primate conservation, dry forests, Colombia, El Guamo. Resumen El estatus de conservacin de A. palliata mico aullador negro, en Colombia es vulnerable debido al decremento en las po blaciones. El lmite de distribucin hacia el noreste del pas no es bien denido y los bosques secos del norte del pas estn desapareciendo rpidamente. En El Guamo (Bolvar) menos del 20% del paisaje esta compuesto por bosque. Los dos rema nentes de bosque mas grandes tienen extensiones de 3,544.7 y 879.6 ha respectivamente. De entrevistas con la comunidad se concluy que la perdida de hbitat es la mayor amenaza para las poblaciones de primates. 37.6% de la comunidad de habitantes de El Guamo arm haber visto la especie en el rea del municipio, sin embargo ningn individuo de A. palliata fue encontrado durante el recorrido de un transecto piloto. Individuos de las especies Alouatta seniculus y Saguinus oedipus fueron encontrados durante las caminatas. Las acciones de conservacin en conjunto con las comunidades rurales deben ser una prioridad en la propuesta de actividades como la reforestacin, el establecimiento de corredores y de sistemas agrofores tales con el objetivo de mejorar las condiciones de hbitat para poblaciones de A. palliata Palabras Clave: Mico aullador negro, conservacin de primates, bosques secos, Colombia, El Guamo. Introduction Although A. palliata is one of the best studied neotropical species (Neville et al ., 1988; Deer, 2004), little is known about the state of its populations, its ecology and its geo graphic distribution in Colombia. A. palliata is listed in CITES in Appendix I and by the IUCN as Low Concern (LC), because its populations are considered abundant and stable. However in Colombia, the loss of habitat and the pressure of hunting have aected populations negatively, and presently the species is classied as vulnerable (VU) in the red lists of the IUCN for Colombia (Cuarn et al ., 2003). A. palliata is distributed throughout southern Mexico as well as much of Central America to the west coast of Co lombia and Ecuador. In Colombia, the range of A. pal liata includes the entire pacic coastal lowlands, except in ooded areas (Hernndez-Camacho and Cooper, 1975; Deer, 2004) ; the distribution of A. palliata in the North of the country is poorly dened (Deer, 2004). A speci men of the species collected by Carriker in the Cartagena region during the early 1900s (and information provided by Dugand during the 1950s about the presence of the species in a locality close to the study site of this research), suggests that the distribution of the species to the northeast
2 could be greater than indicated in some distribution maps (Deer, 2004). However, the few studies carried out in the Montes de Maria (Mountains of Mary), in the departments of Sucre and northern Bolivar, including Cartagena region, have not reported A. palliata. e research I conducted was carried out in 2005 under the regional conservation strategy for threatened species of the Corporacion Autonoma Regional del Canal del Dique (CARDIQUE), a governmental organization with jurisdic tion in the northern and central parts of the department of El Bolivar. e interest of this organization in the popula tions of A. palliata are due to a variety of reasons: the con servation status of the species in Colombia, the unknown distribution of the species in the north of the country, the lack of knowledge about the ecology of the species in dry forests of the country and lastly the repeated sightings of the species in the area. Methods Study Area El Guamo is located in the department of Bolivar in north ern Colombia, west side of the Magdalena River between the municipalities of Calamar and San Juan de Nepo muceno. It is located between 10 08' and 9' N, and 75'74 47' W. Its altitude lies between 25 and 100 m above sea level. Mean annual rainfall in this region is about 1185 mm. e area presents a dry period between Decem ber and April, and a rainy season between May and No vember, with a decrease in rainfall during June and July. e annual average for temperature is 28C, with insigni cant uctuations through the year, and the annual average for relative humidity is 77% (IDEAM, 2005). e total municipality area is about 39,000 ha. is research was divided into 4 phases: 1) identication and description of the forested landscape patterns using remote sensing 2) meetings and interviews with the com munity 3) pilot study and 4) description of the habitat. Description of the forested landscape patterns using remote sensing e description of forested areas in El Guamo was done through analysis of an ASTER satellite image taken in May of 2004 during the rainy season for a better estima tion of vegetation. e analysis was done using ARC GIS. Vegetation was identied by using the Normalized Dier ence Vegetation Index ratio (NDVI) (NASA, 2010). e description of the landscape pattern, applied only to the patches of forests, followed the methodology for numerical and spatial data processing in landscape ecology, (Forman and Gordon, 1986; Farina, 1998), including: a) dimen sions of individual elements, b) landscape composition, and c) spatial arrangements of elements. Overall analysis was focused on the identication of potential areas for monitoring and conservation of A. palliata with consider ation of the habitat requirements of the species. Focus groups and interviews I conducted focus groups and interviews with the com munity members of El Guamo in each of the main vil lages in order to determine the presence of A. palliata in the municipality. During the focus groups I presented visual material such as pictures, only after the community described the species they allegedly saw, in order to con rm the accuracy of the information. e questions asked during the focus groups and interviews were: have you seen the black howler monkey in the forests of this area? if yes, where have you seen it?, how long ago did you see it?, are monkeys frequently hunted for bushmeat?. I asked these questions in order to conrm the presence of the species in the region and also, to determine possible locations, as well as main threats. Participation was voluntary, all responses were anonymous and no incentives were oered to survey responders. I asked the questions to each participant and the information was collated using a questionnaire during the focus groups and interviews. Pilot census of Alouatta palliata In 2005 I conducted a pilot census in order to determine the presence of the species in the area. e site was selected taking into account information provided by inhabitants of the region, accessibility and security. However, the presence of illegal armed groups in the area (paramilitares and guer rillas) did not allow the application of probabilities sam pling. erefore the selection of a survey site was biased by external factors. I conducted the census of A. palliata using the line transect method. A transect of 2000 m was cut in a fragment of forest called La Reserva (28.7 ha) (Figure 1). e pilot census were conducted in the morning starting at 6:00 am (during the maximum time spent by A palliata in howling and traveling (Muoz et al ., 2001)), and nishing Figure 1. Land Cover map of the study area. Minimum mapping unit: 10 ha. Elaborated by Andrea Dechner.
3 at 12:00m, due to rainy afternoons. e speed of the walks was 1 km/h, with stops of 5 minutes each 100 m for visual or auditory indications of the presence of animals. Description of the habitat In order to characterize the oristic composition and struc ture of the vegetation of the area, a single quadrant of 1,000 m 2 was established in the area selected for the census of A palliata All trees in the quadrant with a diameter at breast height (DBH) greater than or equal to 10 cm were identied. I measured variables such as tree height, DBH, and cover, as well as altitude, presence of erosion processes and terrain inclination. Taxonomic identication of collected samples relied on Gentry (1993) and Mahecha (1997), as well as by comparison with specimens from the MOBOTMissouri Botanical Garden. Results Description of the Forested Landscape Patterns Using Remote Sensing e municipality of El Guamo consists of 38,270 ha mainly covered by grasslands or croplands (17,166 ha), followed by low forests or shrublands (8,281 ha) and well developed forests (6,834 ha) (Table 1). Forested areas represent 17.9% of the total study area and are mainly located to the south towards the border with the municipality of San Juan de Nepomuceno. ere are 31 fragments of forest, presenting an average size of 220 ha. e fragment sizes vary between 10 ha (the MMU or minimum mapping unit) and 3544 ha (Table 2). e largest fragment of forest is the fragment N 7. It is located to the south of the capital and has an extension of 3,544 ha (Figure 1). It represents 53% of the total area of forests. However, this fragment presents small perforations which were not mapped due to their small size (i.e. under the assigned MMU). In addition it has a very irregular shape (CPA Corrected Perimeter Area Ratio = 4.6). Frag ments N 10 and 3 present the second and third largest extensions with 880 and 266 ha respectively. e nearest neighbor observed mean distance between for ests was 1,956 meters and the nearest neighbor ratio based on feature centroids had a value of 0.94. is indicates that the spatial pattern of the fragments of forests is random, neither clustered or dispersed. According to the directional distribution of the fragments of forests, the largest frag ments of forests are located to the south and are connected with other forests located outside El Guamo. Focus groups and interviews I conducted 141 interviews in 7 dierent localities of the municipality of El Guamo during July-August 2005. ese localities include El Guamo (capital of the municipality, 58 interviews), Nerviti (27 interviews), Tasajera (21 inter views), El Totumo (12 interviews), La Enea (5 interviews), Robles (10 interviews), and El Acueducto (8 interviews). About 62% of the participants interviewed said they have never seen A. palliata while 38% said they have seen the species. Participants from localities such as La Enea and Robles armed they have never seen a black howler monkey, while more than the 40% of the interviewers in localities such as El Guamo, Nerviti and Tasajera said they have seen the species in nearby areas. Approximately 30% of the interviewees said they have seen the monkey in Lata, followed by El Totumo (29%), Casa blanca (12%), San Luis (9%) and La Reserva (9%). Loca tions where the sightings had been less included Descon solado, Cerro de Maco, El Yucal and La Venta. e people who have seen the species more recently (i.e. between July 2004 and July 2005) said they have seen it between April and July 2005 in El Totumo, between January and April 2005 in La Reserva and Lata, and between July 2004 and January 2005 in localities such as San Luis and La Venta. Localities where it had not been seen recently include Casablanca. Table 1. Area and relative abundance of cover types in the study area. e mixed vegetation category was given to those areas with 2 or more types of cover, where each cover had less than 10 ha (MMU). Cover type Total area (ha) Relative abundance (%) Forest 6,834.0 17.9 Low forest or shrubland 8,281.0 21.6 Mixed vegetation 2,212.0 5.8 Grassland or cropland 17,165.5 44.9 Water Bodies 2,310.8 6.0 Bare Ground 1,112.9 2.9 Built up areas 189.2 0.5 No Information 165.2 0.4 Total 38,270.7 100.0 Table 2. Characteristics of patches of forest in the study area. Table shows the details of the 3 largest fragments. Fragment # Area (ha) Perimeter (m) Patch shape Relative abundance (%) 7 3,544.7 99,806 4.7 51.9 10 879.6 33,259 3.2 12.9 3 266.1 16,367 2.8 3.9 Following 28 fragments 2,143.8 167,779 55.8 31.3 Minimum 10.1 1373 1.2 0.1 Maximum 3544.7 99806 4.7 51.9 Average 220.5 10233.3 2.1 3.2 Total 6834 317231 66.5 100
4 Only 2.8% of the total participants said monkeys are frequently hunted for bushmeat. Hunted species includ ed Alouatta seniculus (red howler monkey) and Cebus ca pucinus (white throated capuchin monkey). In addition, visits to places in El Guamo, La Enea and Robles, where the presence of monkeys in captivity was conrmed, uncovered no individuals of A. palliata in captivity. However some inhabitants said they had a black howler monkey in captivity in the past. Individuals of the spe cies Cebus capucinus (white throated capuchin monkey) and Saguinus oedipus (cotton top tamarin), were found in captivity. Census of Alouatta palliata e area selected for the census of the species was La Reserva which has an extension of 28.7 ha (Fragment N 15) (Figure 1). Although a small percentage of the in terviewees said they have seen the species there, the selec tion of the area was made based on a convenience (nonprobability) sampling due to the presence of illegal armed groups (paramilitares and guerrillas). In total I walked a distance of 22 km and no individuals of A. palliata were found. Troops of other primates such as Alouatta senicu lus and Saguinus oedipus were observed during the census (Table 3). In addition, during informal walks, a troop of 9 individu als of the species Saguinus oedipus was observed on a single tree in a semi-open area in a place called El Acueducto (10'53.18" N, 74'41.25" W). Description of habitat e total tree species richness with DBH 10cm was 14 spe cies (32 individuals) in a total area of 1,000m 2 (0.1 ha). e Shannon-Weaver species diversity index was 2.2, and the Simpson diversity index was 0.8. e families with higher number of species were Leguminosae with 4 spe cies, followed by Bignoniaceae with 2 species. Only one species was found for the rest of the families (Table 4). e most abundant species were Astronium graveolens (Anacar diaceae) with 34.4% of the individuals found, followed by Bursera simaruba (Burseraceae) and Caesalpinia sp. (Legu minosae), each with 12.5% of the species found. e mean tree height was 9.4 m; the tallest trees measured were a Girocarpus americanus and Caesalpinia sp., with a total height of 16 m each; whereas the minimum height registered was for a Cordia sp. with 4 meters of height. e average tree diameter at breast height was 20.8 cm with a maximum diameter of 59.5 cm. e total basal area of all the tree species was 10.1m 2 /ha Caesalpinia sp. makes the greatest contribution to this value with 26% of the total Table 4. Floristic composition of 0.1 ha vegetation plot in the study area. Family # sp. % Species # ind % Anacardiaceae 1 7.1 Astronium graveolens 11 34.4 Apocynaceae 1 7.1 Aspidosperma polyneuron 1 3.1 Bignoniaceae 2 14.3 Tabebuia bilbergii 1 3.1 Tabebuia rosea 1 3.1 Boraginaceae 1 7.1 Cordia sp. 2 6.3 Burseraceae 1 7.1 Bursera simaruba 4 12.5 Capparidaceae 1 7.1 Capparis odoratisima 1 3.1 Euphorbiaceae 1 7.1 Hura crepitans 1 3.1 Hernandiaceae 1 7.1 Girocarpus americanus 2 6.3 Leguminosae 4 28.6 sp 1 1 3.1 Caesalpinia sp. 4 12.5 Acacia sp. 1 3.1 sp 2 1 3.1 Rubiaceae 1 7.1 Alseis sp. 1 3.1 Total 14 100 32 100 Table 3. Information on the individuals of the species Alouatta seniculus and Saguinus oedipus found during the census in La Reserva. Species # of individuals observed Location (Coordinates) Alouatta seniculus 2 10'24.00"N, 74'34.49"W Saguinus oedipus 5 10'24.73"N, 74'29.80"W
5 basal area, followed by Astronium graveolens with 21% of the total basal area. Caesalpinia sp. is dominating in the upper canopy with 53% of the crown cover, followed by Astronium graveolens (14%) and Bursera simaruba (6%). Discussion Dry forests, such as those in El Guamo, Bolivar, are consid ered the most endangered major tropical ecosystem because their original area has been reduced by more than 90%, and less than 2% of what remains is protected (Janzen, 1986). By 1997 only 1.5% of the original cover of the dry forests remained in Colombia (IAVH, 1997). In comparison to other ecosystems, dry forests are more exposed to human disturbances due to a variety of reasons: 1) the climate, 2) the forest structure, which make easier to cut them down for agriculture, 3) the soils, which are more fertile than the soils of rainforests, and 4) in many areas like in El Guamo, the geomorphology, which is highly suitable for livestock. Consequently, tropical dry forests are under increasing pressure and the status of conservation of this ecosystem is critical for large areas of South America (Janzen, 1986). In El Guamo, grassland or cropland compose the matrix of the landscape being the most extensive and contiguous ele ment in the landscape. Forests in the study area were highly fragmented, under increasing threat of being replaced for agricultural or cattle grazing lands, reducing the areas with potential value for the monitoring and conservation of bio diversity. e fragments of forests presented an irregular shape which increases signicantly the amount of habitat aected by the edge eect, consequently altering plant composition, structure and the functionality of the forests (Laurance et al 1997). Considering that the habitat availability depends on the extension of the area, and that largest fragments would contain sucient habitat to meet the needs of the spe cies (Saunders et al ., 1991; leigh et al ., 1993), the largest remaining fragments should be rst in consideration for monitoring and conservation actions for A. palliata e average size of the fragments of forests is 220 ha, which is a favorable number considering that A. palliata presents a home range that varies between 10 and 60 ha (Chiv ers, 1969) and that the average daily path ranges between 123 and 443 m (Milton, 1980; Estrada, 1982, 1984). e nearest neighbor ratio indicates that the forest fragments are not clustered, which may have negative implications on the movement of the species that inhabit these areas. Actions toward increasing connectivity of the fragments should be considered in order to reduce the impact of the fragmentation. Although only 37.6% of the stakeholders interviewed said they have seen the monkey, the fact that the physical de scriptions of the species provided by them were so accurate (i.e. black face, body not completely black, with brown fur in the back) reinforce the idea that although in very low densities, A. palliata may be in the area. Also, as expressed by some farmers, the species is living sympatrically with Alouatta seniculus as reported by Hernandez-Camacho and Cooper (1975) in the west of the Atrato River of Colombia. Localities such as Lata and El Totumo, should be priorities in selecting sampling areas for monitoring because results from the interviews with the community suggest the pres ence of the monkey in these areas (Figure 1). From the in terviews it can be concluded that hunting is not currently the main threat for populations of the species. Instead, the continuing loss of forested areas to cattle grazing and crop cultivation is the main threat to species in the region. e absence of sightings of the species during the pilot study may have been due to the low density or absence of the spe cies in the sampled area (La Reserva) and the short length of the transect (22 km). In addition, the likely absence of the species in the sampled area may have been due to habi tat degradation and isolation. e forests of the sampled area are secondary forests, and the tree species richness (14 spp.) is lower than the aver age richness registered in other dry forests (24.7 spp.) (Gentry, 1995). is low tree species richness value may be explained as the result of the dierent levels of human disturbance and selective logging. Also, the dierence be tween species richness values may be due to the sampling size and to the fact that I sampled 0.1 ha using a single quadrant (20 50 m) and not 10 2 50 m transects like in the studies reported by Gentry (1995). Results of the most important families in number of species showed that as reported for other dry forests (Gentry, 1995; Mendoza, 1999), Leguminosae was the most speciose family (4 spp.). e second most speciose family was Bignoniaceae (2 spp.), which is described by Gentry (1995) as the undisputed number two family of woody plants of neotropical dry forests. Results of this study showed that by comparison with the diet of A. palliata in other dry forests, the potential spe cies to be used as a source of food by A. palliata in the area of El Guamo include Astronium graveolens (Glander, 1981) with 30% of relative abundance in the study area, Bursera simaruba (Serio-Silva et al ., 2002) with 13% of relative abundance, and several species of the genera Cordia (Estrada, 1984) also with 13% of relative abundance in the study area. Being folivore and because of their wide diet that includes mature leaves, young leaves, owers and fruits (Glander, 1981), A. palliata has more food available to them in comparison with non-folivore primates. How ever, the food supply of the species can be aected by the phenology of the species they feed on. e relationship be tween the seasonality, availability of resources and the be havior in primates has been widely studied (Hladik, 1977; Overdor, 1993; Gursky, 2000). In tropical dry forests, which are characterized by 4 months of drought, sea sonal climate and tree phenology are not highly correlated. Phenology varies widely among plant species with shoot
6 growth and owering occurring either after the leaves are dropped during the dry season or during the beginning of the rainy season (Borchert 1994, 1996). According to the climatic information, the area of El Guamo presents a dry period between December and April, and a rainy season between May and November, with a de crease in rainfall during June and July. Plant species such as Astronium graveolens and Bursera simaruba being abun dant in the study area may provide an important amount of food to the populations of A. palliata almost all year round. Astronium graveolens has been classied as droughtdeciduous species with young leaves that appear together with the owers immediately after leaf shedding during the dry season. is species can also be used for reforestation activities due to its ability to grow under full light (Marin and Flores, 2002). Similarly, Bursera simaruba has been described as a deciduous species, with owering of leaess trees during the dry season and fruits almost year round. Bursera simaruba grows well in either poor or rich soils and adapts to severe drought periods. It has a fast germination with 80% of germination reaching maturity after 15 years (Navarrete-Tindall and Orellana Nunez, 2002). In regard to the structural development of the sampled forests, results showed that the canopy height and basal area registered are lower than those registered in other dry forests. In such forests, the average canopy height varies between 10 and 40 m and the basal area varies between 17 and 40 m2/ha (Murphy and Lugo, 1986). ese dier ences in structural terms may be the result of disturbance activities in the area. Selected areas for censusing and con servation activities should include structurally well devel oped forests. Fedigan et al (1998) suggested that as struc tural requirements, A. palliata only feed and rest in trees that are suciently large to support their weight (with a minimum DBH of 20 cm and a preferred DBH of 63 cm). en, although the habitat of the sampled area can meet the structural requirements of the species, its relatively low structural development may be the cause of the low densi ties or absence of the A. palliata in some areas and of the restricted presence of the species in other areas with greater structural development. erefore, it is necessary to consid er conservation actions in order to enhance the suitability of all the fragments of forests in the area. Considerations for the conservation of Alouatta pal liata in the dry forests of northern Colombia Dry forests of El Guamo are under increasing pressure to be turned into areas for agricultural use and cattle grazing. is implies that most of primates that live in these for ested areas and require relatively well developed forests are threatened, and the conservation of their habitats should be a priority in proposing strategies of conservation in the region. Conservation strategies should include actions di rected to the restoration of some fragments and of the con nectivity between them in order to increase the suitability of the habitat. Towards these actions, working with farmers and land owners to reduce habitat destruction is very im portant. Encouraging forest corridors through the cut areas will improve their habitat by allowing howlers monkeys to move between fragments of forests (Horwich, 1998). Agro ecosystems with cacao, coee and mixed plantations have proved to have a positive eect on enhancing forest habitat for primates (Estrada, 2006) In agricultural areas, it is essential to encourage actions such as: (1) promoting the planting of food species for howlers and (2) establishing corridors to enhance the con nection between isolated forests (Horwich, 1998). Choos ing species that are used by A. palliata as resource of food could radically improve their habitat. Although species of the genus Ficus are an important food source for A. palliata (Horwich, 1998; Ramrez-Orjuela and Snchez-Dueas, 2005), species of this genus were not considered in this study because of their preference for humid areas. Restoration actions should be done by planting fast to medium growing native species of trees encountered in the dry forests of the area preferred as a resource of food by A. palliata. Trees to be planted include Brosimum ali castrum and Anacardium excelsum Brosimum alicastrum remains green during the dry season, thus being a res ervoir of food for many species (Rocas, 2002). Anacar dium excelsum drops its leaves for a short period of time (Fournier, 2002). Additionally, other species of the genera Brosimum and Anacardium excelsum were reported as food resource for A. palliata in the Choc region in Colombia (Ramrez-Orjuela and Snchez-Dueas, 2005). Other po tential species to be used in restoration activies are: Spon dias mombin Muntingia calabura, Guazuma ulmifolia and Gliricidia sepium Spondias mombin produces fruits that are consumed by livestock and by humans, also its fruits and both young and mature leaves are consumed by A. palliata (Serio-Silva et al ., 2002). Muntingia calabura is a very fastgrowing evergreen tree characterized for being droughtresistant (Morton, J. 1987). Guazuma ulmifolia and Gliri cidia sepium are fast growing medium trees that may also be used as living fence (Suttie, 2000). Additionally, Guazuma ulmifolia may be a source of food for livestock (Little and Wadsworth, 1964). All these tree species may play an im portant role in the establishment of activities to improve the suitability of habitat of populations of A. palliata by providing food resources to the species, services to the rural community, and by allowing and encouraging the forest regeneration. One of the main limitations to any monitoring and con servation action in the area is the presence of illegal groups, although such topic is out of the scope of this paper, it is important for governmental and non-governmental or ganizations to set realistic objectives and conservation ac tions, as well as to make constant presence in these areas to be recognized by the dierent actors of the conict as neutral in order to reach desired conservation objectives.
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9 DENSIDADE E TAMANHO POPULACIONAL DE PRIMATAS EM UMA REA DE TERRA FIRME NA AMAZNIA CENTRAL Lilian Figueiredo Rodrigues 1 e Marcelo Derzi Vidal 2 1 Instituto Nacional de Pesquisas da Amaznia INPA, Coordenao de Pesquisa em Ecologia, CP 478, CEP 69.011, Manaus-AM, Brasil, email@example.com 2 Instituto Chico Mendes de Conservao da Biodiversidade ICMBio. Centro Nacional de Pesquisa e Conservao da Biodiversidade Amaznica CEPAM, CEP 69.041, Manaus-AM, Brasil, firstname.lastname@example.org Abstract Brazil contains 1/3 of the worlds remaining tropical forests and is recognized as one of the worlds most important store houses of biodiversity. With regard to primate species richness, it is especially prominent. ere are 133 species and subspe cies in Brazil of these 80 occur in the Brazilian Amazon and 11 are in danger of extinction. In spite of these impressive numbers, there is little ecological or population data available for many of these species, especially those that occur in the Amazon. To address this lack, the objectives of this study were to: 1) record occurring primate species; 2) estimate their population densities; and 3) characterize their distributions in the Adolpho Ducke Forest Reserve. is reserve, situated on north of Manaus in the state of Amazonas, Brazil, contains 10,000 hectares of primary forest. e data were collected using linear transects, covering the entire system of trails within the reserve. In a total of 720 km of trails walked, 58 sightings were registered of Saguinus bicolor 29 of Cebus apella 20 of Alouatta seniculus 13 of Pithecia pithecia and 10 of Chiropotes sagulatus Sightings occurred in all types of environments (plateau, slope, and lowland). S. bicolor had the greatest density (1.00 group/km 2 ), followed by C. apella (0.67), A. seniculus (0.66), P. pithecia (0.64) and C. sagulatus (0.30). e resulting estimate of groups present in the total reserve area, not considering possible gaps, natural habitat variation, or resource avail ability, is 100 groups of S. bicolor 67 of C. apella, 66 of A. seniculus 64 of P. pithecia and 30 of C. sagulatus. ese results demonstrate the importance of the Adolpho Ducke Forest Reserve for the maintenance of biodiversity and emphasize the need for targeted conservation policies to contain anthropogenic disturbances in the region. Keywords: Ducke reserve, Amazon forest, linear transect, Manaus Resumo O Brasil apresenta 1/3 das orestas tropicais remanescentes do mundo e reconhecidamente um dos mais importantes repositrios da diversidade biolgica mundial. Quanto riqueza de espcies de primatas, ocorrem em seu territrio 133 es pcies e subespcies, sendo que 80 ocorrem em territrio amaznico e 11 esto ameaadas de extino. Apesar dos nmeros expressivos, boa parte das espcies, principalmente as que ocorrem na regio amaznica, apresenta carncia de informaes ecolgicas e populacionais. Diante disto, os objetivos deste estudo foram (1) registrar as espcies de primatas, (2) estimar suas densidades e (3) caracterizar suas distribuies na Reserva Florestal Adolpho Ducke, uma rea de oresta primria de 10.000 hectares situada na regio de crescimento urbano norte da cidade de Manaus-AM. Os dados foram coletados por meio do mtodo de transeco linear, cobrindo todo o sistema de trilhas da reserva. Foram percorridos 720 km e registrados 58 avistamentos de Saguinus bicolor 29 de Cebus apella 20 de Alouatta seniculus 13 de Pithecia pithecia e 10 de Chiropotes sagulatus distribudos em todos os tipos de ambientes (plat, vertente e baixio). A maior densidade registrada foi de S. bicolor (1.00 Gr/Km 2 ), seguida por C. apella (0.67), A. seniculus (0.66), P. pithecia (0.64) e C. sagulatus (0.30). Assim, a estimativa de grupos presentes na rea total da reserva, desconsiderando-se a possvel presena de lacunas, as variaes naturais do habitat ou a disponibilidade dos recursos, de 100 grupos de S. bicolor 67 de C. apella, 66 de A. seniculus 64 de P. pithecia e 30 de C sagulatus. Esses resultados demonstram a importncia da Reserva Florestal Adolpho Ducke na manuteno da biodiversi dade e impem a necessidade de polticas conservacionistas para sua rea. Palavras-chaves: Reserva Ducke, Floresta Amaznica, transecto Linear, Manaus.
10 Introduo O Brasil apresenta 1/3 das orestas tropicais remanescentes do mundo e reconhecidamente um dos mais importantes repositrios da diversidade biolgica mundial (Ayres et al., 2005). Embora seja considerada a maior do planeta, a di versidade de mamferos do Brasil ainda pouco conhecida (Voss e Emmons, 1996). Quanto riqueza de espcies de primatas, o Brasil apresenta um lugar de maior destaque: dos 624 taxa de primatas existentes no mundo, 133 esp cies e subespcies vivem em territrio brasileiro (Machado et al. 2005), sendo que 80 ocorrem em territrio amazni co e 11 esto ameaadas de extino (Gordo et al ., 2008). Apesar dos nmeros expressivos, boa parte das espcies, principalmente as que ocorrem na regio Amaznica, apre senta carncia de informaes ecolgicas e populacionais (Machado et al ., 2005). O comprometimento da diversidade biolgica est relacio nado no somente ao acelerado ritmo do desmatamento, mas tambm a presso de caa e ao corte seletivo de orestas (e.g. Robinson et al ., 1999), fatores que atuam como princi pais ameaas para os mamferos, principalmente os de mdio e grande porte, que necessitam de grandes reas de vida e esto sujeitos a caa (Pardini et al ., 2003). A perda de ha bitat ainda um dos principais responsveis por declnios de 83% dos pssaros e 85% dos mamferos ameaados no mundo (BirdLifeInternational, 2000; Hilton-Taylor, 2000). Nos neotrpicos, os primatas apresentam um elevado inte resse para estudos de fragmentao orestal. Geralmente as espcies com grande massa corprea, portanto com grandes exigncias espaciais, tendem a ter suas densidades reduzidas signicativamente ou sofrem extines locais quando as o restas so reduzidas a pequenos fragmentos orestais (Peres, 1990). Dependendo da distncia entre orestas, as reas abertas entre fragmentos frequentemente constituem barrei ras a disperso e a colonizao, impedindo o uxo gnico entre populaes (Ferrari e Diego, 1995). Diversos estudos em reas orestais fragmentadas na Ama znia relacionaram a abundncia, densidade, ocorrncia e riqueza das espcies com o tamanho do fragmento ores tal, presso de caa, estrutura da vegetao e qualidade de habitat (Schwarzkopf e Rylands, 1989; Peres, 1997; Vidal e Cintra, 2006). Muitos estudos, entre eles os de Peres (1990; 2000) e Peres e Dolmann (2000), reportam a forte presso de caa de subsistncia e comercial, especialmente sobre primatas de maior biomassa, como guaribas ( Alouat ta spp.), macacos-aranha ( Ateles spp.) e macacos-barrigudo ( Lagothrix spp.). O pequeno tamanho e isolamento da maioria dos fragmentos de orestas comprometem a ma nuteno em longo prazo de populaes mnimas viveis de primatas (Chiarello e Melo, 2001). Assim, reas como a Reserva Florestal Adolpho Ducke (RFAD), que possuem importante funo na manuteno da biodiversidade local, e que podem ser destinadas conservao de metapopula es, merecem grande ateno para serem evitadas extin es locais de espcies (Kierul e Rylands, 2003). At o momento, escassas so as pesquisas abrangendo toda a extenso da RFAD, principalmente aquelas relacionadas a grandes mamferos. O nico estudo com primatas desen volvido em toda a rea da Reserva foi realizado por Vidal e Cintra (2006), mas foi direcionado para o uso do hbi tat por uma nica espcie. Este o primeiro trabalho que envolve informaes sobre todas as espcies de primatas que utilizam a RFAD. Assim, de modo a contribuir com a gerao de conhecimentos e explicitar a importncia da RFAD para a manuteno da biodiversidade, este estudo teve como objetivos (1) registrar as espcies de primatas que ocorrem no interior da reserva, (2) estimar as densidades populacionais de cada espcie e (3) caracterizar suas distri buies espaciais nos ambientes de plat, baixio e vertente, presentes na reserva. Material e mtodos rea de estudo A Reserva Florestal Adolpho Ducke (Fig. 1), localizada no Km 26 da Rodovia Estadual AM 010 (02'-03'S, 59'-59' W), possui uma rea de 10,000 ha, com to pograa acidentada e altitude variando entre 39 e 109 m acima do nvel do mar. Nas reas altas predomina o latos solo amarelo alico (oxisol) de textura muito argilosa, e nas reas baixas o solo constitudo de podzis (de textura are nosa). A vegetao do tipo oresta ombrla densa de terra rme. O dossel bastante fechado e o sub-bosque tem pouca luminosidade, caracterizado pela abundncia de pal meiras acaules (Guillaumet e Kahn, 1982). A altura mdia das rvores ca entre 35 e 40 m, com indivduos emergentes que atingem os 50 m (Ribeiro et al. 1999). Por estar muito prxima a cidade, tendo somente o seu limite leste conec tado a oresta contnua, a reserva apresenta considervel perturbao antrpica, sendo comuns os registros de reti rada de madeira e a caa comercial e de subsistncia, aes ilegais praticadas pelas populaes do entorno. A expanso urbana da zona leste de Manaus poder contribuir para o seu completo isolamento, transformando a reserva em um grande fragmento orestal urbano (Ribeiro et al ., 1999). A precipitao anual na rea varia de 1,900 a 2,500 mm, com estao chuvosa de dezembro a maio e estao seca de junho a novembro (Gascon e Bierregard, 2001). Segundo a classicao de Keppen, a RFAD apresenta um clima do tipo Af (Equatorial mido) com temperatura mdia em torno de 26C (mnima de 19C e mxima de 39C). A umidade relativa varia de 77 a 88%, com mdia anual de 84% (Leopoldo et al., 1987). Mtodos O sistema de trilhas da RFAD formado por 18 trilhas de 8 km, sendo que nove esto dispostas no sentido norte -sul e nove no sentido leste-oeste, formando um sistema regular de quadrantes de 1000 m 1,000 m. As trilhas esto marcadas com tubos de PVC a intervalos regulares de 100 m. Os censos foram conduzidos de acordo com a metodologia de transeco linear (Burnham et al. 1980; Buckland et al. 1993), cobrindo todo o sistema de trilhas
11 da RFAD e realizados durante oito dias por ms, de novem bro de 2002 a julho de 2003. Os censos foram realizados no perodo de 06:30 s 17:00 horas. Este perodo abrange os ciclos dirios de atividades de vrias espcies de primatas (Terborgh, 1983; Egler, 1986; Menezes et al ., 1993; Vidal e Cintra, 2006). Durante o perodo do censo foram feitas caminhadas pelo sistema de trilhas numa velocidade em torno de 1.5 km/h. A cada 50 m parava-se por cerca de 30 s para fazer uma varredura visual e auditiva para cada lado da trilha, maximizando assim a chance de visualizao dos pri matas (Peres, 1997). A cada avistamento foram registradas as seguintes informaes: 1) espcie observada; 2) tamanho do grupo, feito por contagem direta do nmero de indiv duos avistados, 3) dia e hora do avistamento; 4) nmero da trilha e posio do grupo na mesma; e 5) distncia perpendicular do avistamento em relao trilha (com o uso de trena de 50 m). Para estimar a distribuio espa cial dos grupos registrados, os ambientes disponveis foram classicados de acordo com as seguintes cotas altimtricas: 100, plat; 70, vertente; e, 40, baixio. As densidades dos grupos de primatas presentes no inte rior da RFAD foram estimadas dividindo-se o nmero de grupos avistados (n) pela rea amostrada, onde l o comprimento total da trilha e w a distncia perpendicular mxima de avistamento (NRC, 1981). D = n/2lw As abundncias foram estimadas dividindo-se o nmero de grupos avistados (n) pelo comprimento total da trilha (l). A = n/l Para estimar diferenas entre taxas de avistamentos nos di ferentes horrios do dia, os registros foram divididos nas seguintes classes de horrios: 06:30:00, 08:01:30, 09:31:00, 11:01:30, 12:31:00, 14:01:30, 15:31:00. Qui-quadrados foram realizados para es timar diferenas nas taxas de avistamentos nas diferentes classes de horas. Resultados Durante os nove meses de coleta de dados foram per corridos 720 km de trilhas e registradas cinco espcies de primatas: Saguinus bicolor (sauim-de-coleira), Cebus apella (macaco-prego), Alouatta seniculus (guariba), Pi thecia pithecia (parauacu) e Chiropotes sagulatus (cuxi). O sauim-de-coleira foi a espcie de primata mais avistada (n=58 avistamentos), seguida pelo macaco-prego (n=29), guariba (n=20), parauacu (n=13) e cuxi (n=10), totali zando 130 diferentes avistamentos, distribudos nas dife rentes cotas altitudinais mensuradas e, consequentemente, em todos os tipos de ambientes plat, vertente e baixio (Fig. 2). Apenas Saguinus bicolor ( 2 =14.89, gl=6, p<0.02) e Chiropotes sagulatus ( 2 =19.40, gl=6, p<0.03) apresenta ram diferenas signicativas no nmero de grupos avista dos nas diferentes classes de horrios (Fig. 3). O nmero de indivduos por grupo variou de um (para A. seniculus, C apella e P. pithecia ) a 15 (para C. sagulatus ), sendo que a mdia dos grupos variou de 2,5 (para P. pithecia ) a 7,7 (para C. sagulatus ). A maior densidade foi registrada para S. bi color (1.00 Gr/km 2 ), seguida por C. apella (0.67 Gr/km 2 ), A. seniculus (0.66 Gr/km 2 ), P. pithecia (0.64 Gr/km 2 ) e C. sagulatus (0.30 Gr/km 2 ). Esse mesmo padro encon trado quando calculamos a abundncia relativa das espcies (Tabela 1). Figura 1. Imagem de satlite destacando a cidade de Manaus, os rios Negro e Amazonas, e a Reserva Florestal Adolpho Ducke (RFAD) (Fonte: ppbio.inpa.gov.br/Port/inventarios/ducke /). Tabela 1. Informaes sobre os parmetros populacionais das espcies de primatas encontradas na RFAD. Espcie N de avistamentos Tamanho populacional* Densidade ( Gr/Km 2 ) Abundncia (Gr /l ) Alouatta seniculus 20 2,95 (1-6) 0,66 0,28 Cebus apella 29 5,90 (1-13) 0,67 0,40 Chiropotes sagulatus 10 7,70 (3-15) 0,30 0,14 Pithecia pithecia 13 2,54 (1-4) 0,64 0,18 Saguinus bicolor 58 5,26 (2-11) 1,00 0,80 Entre parnteses se encontram os valores mnimos e mximos de indivduos
12 Se levarmos em conta que a RFAD abrange uma rea de 10,000 ha de oresta, podemos armar que a estimativa de grupos presentes em sua rea total, desconsiderando-se a possvel presena de lacunas, as variaes naturais do ha bitat ou a disponibilidade dos recursos, de 100 grupos de S. bicolor 67 grupos de C. apella, 66 grupos de A. seniculus 64 grupos de P. pithecia e 30 grupos de C. sagulatus. Discusso Nossos resultados, registrando cinco espcies de primatas no interior da RFAD, demonstram que esta rea abriga uma considervel representatividade de espcies quando comparada com outras reas nas proximidades de Manaus. Na rea de relevante interesse ecolgico do Projeto Dinmi ca Biolgica de Fragmentos Florestais (PDBFF), unidade de conservao situada a cerca de 60 km da RFAD, a fauna de primatas representada por seis espcies (Gilbert e Setz, 2001; Boyle, 2008). Enquanto que nas matas ciliares do rio Cuieiras, inseridas no Parque Estadual do Rio Negro Setor Sul, distante cerca de 70 km da rea urbana de Manaus, a primatofauna um pouco mais diversa, tendo sido registra das oito espcies (Spironello, 2000). Das cinco espcies registradas em nosso estudo, Saguinus bicolor o nico calitriqudeo encontrado na rea classi cado como Ameaado na Lista Vermelha da IUCN (IUCN, 2010) e Criticamente Ameaado segundo a Lista Brasilei ra de Espcies Ameaadas (Gordo, 2008). De acordo com Rylands e Mittermeier (1983), as espcies mais ameaadas de extino so aquelas que apresentam distribuio geo grca restrita e se encontram nas reas mais urbanizadas, caractersticas plenamente identicveis em Saguinus bico lor Quando comparamos a densidade de grupos de sauim -de-coleira encontrada em nosso estudo com as obtidas por Subir (1998) e Rosas-Ribeiro et al (2006) (Tabela 2), podemos observar que a de nosso estudo situa-se em nvel intermedirio. Estas diferenas para densidade podem ser explicadas por dois motivos relacionados metodologia aplicada: (1) os dois ltimos estudos citados trabalharam somente em uma parcela da RFAD e (2) apesar das tcnicas de censo utilizadas terem sido semelhantes nos trs estudos, o fato das anlises considerarem ou no a probabilidade di ferenciada de avistamento de um animal pelo observador em relao distncia entre eles e a distncia entre o animal detectado e a trilha, pode ter contribudo para subestimar os resultados ou o inverso. importante salientar que va riaes intraespeccas no tamanho das reas de uso e na densidade dos primatas podem estar relacionadas com mu danas espaciais e temporais de recursos como alimento, gua ou habitats adequados em termos de proteo contra predadores (Rylands, 1986), bem como com o grau de con servao de suas reas. Em nosso estudo, Cebus apella apresentou densidade um pouco maior que as reportadas por Rylands e Keuroghlian (1988) em uma rea de oresta contnua na Amaznia Cen tral e por Rosas-Ribeiro et al. (2006) em trs reas de ores ta de terra rme da Amaznia Central, incluindo a RFAD (Tabela 2). Cebus apella um primata que possui uma dieta generalista e apresenta grandes reas de vida na Amaznia Central (Spironello, 1991). Reporta-se que, em fragmen tos menores, estes primatas possuem densidades relativa mente altas. Isto deve estar ligado ao fato destes animais apresentarem uma larga plasticidade ecolgica (Robinson e Redford, 1986). Nossos resultados sugerem que, apesar da RFAD ainda estar se tornando um grande fragmento orestal dentro da cidade de Manaus, populaes como as de macaco-prego j esto respondendo a essas mudanas da paisagem. Dos primatas Neotropicais com grande massa corprea os guaribas so as nicas espcies capazes de so breviver em fragmentos de oresta com menos de 10 ha (Rylands e Keuroghlian, 1988). Isto se deve ao fato de que as populaes desses primatas apresentam uma dieta mais baseada em folhas nos meses de escassez de frutos na ores ta (Crockett, 1998; Santamara-Gmez, 1999). Apesar de apresentarem essa alta exibilidade alimentar e siolgica, Figura 2. Nmero de avistamentos de primatas na RFAD em re lao variao altitudinal. Figura 3. Nmero de grupos avistados nas diferentes classes de horrios registrados na RFAD.
13 a densidade dessa espcie parece ser bastante comprometida pela presso de caa (Peres, 1997). Em nosso estudo esti mamos uma densidade bem inferior quelas encontradas em outros estudos em orestas de terra rme (Tabela 2). Essa diferena pode estar relacionada ao fato da RFAD estar imersa em uma rea de franca expanso urbana e a frequen te presena de caadores em seu interior, fazendo assim com que as populaes destes grandes ateldeos respondam de maneira negativa. Quando comparamos as densidades de Chiropotes sagulatus e Pithecia pithecia encontradas por Rylands e Keuroghlian (1988) e por Rosas-Ribeiro et al. (2006) com os resultados que obtivemos, nota-se que houve diferena entre os trs estudos. O presente estudo estimou uma densidade inter mediria entre os dois anteriores (Tabela 2). Estes resulta dos podem ser explicados pelo fato destes estudos terem utilizado diferentes metodologias de censo para a estima tiva de densidades, fazendo com que subestimem e/ou su perestimem as populaes estudadas. Da a necessidade de uma padronizao de metodologias para que as estimativas possam ser mais conveis e comparveis. O pequeno ta manho populacional das espcies de primatas encontradas na RFAD sugere que a sobrevivncia das mesmas na rea pode estar ameaada em longo prazo, visto que necessrio um valor muito maior de indivduos/oresta para que esta seja vivel e no sofra com os efeitos demogrcos, genti cos e estocsticos (Reed et al. 2003). As cinco espcies de primatas reportadas em nosso estudo tiveram uma ampla distribuio nos ambientes de plat, vertente e baixio. Vidal e Cintra (2006), em um estudo com Saguinus bicolor mostram que essa espcie teve uma ampla distribuio na RFAD, incluindo reas de plat, vertente e baixio. Essa ampla distribuio nos ambientes foi tambm documentada para outras espcies de Sagui nus na Amaznia (Terborgh, 1983; Peres, 1994). Alouat ta seniculus se encontra amplamente distribudo na regio Amaznica, mas pode tambm ocupar outros tipos de hbitat como os bosques secos, com nvoas, de galeria e mangues (Rylands et al ., 1996/1997; Crockett 1998). Se gundo Crockett (1998) as espcies do gnero Alouatta esto catalogadas entre os maiores primatas e os mais folvoros do Neotrpico, o que deve explicar em parte essa ampla distribuio na oresta. Cebus apella tambm um pri mata generalista de habitats, sendo encontrado em dife rentes extratos da oresta e em diferentes tosionomias (Mittermeier e Coimbra-Filho, 1977; Mittermeier e van Roosmalen, 1981; Terborgh, 1983; Peres, 1994; Mendes -Pontes, 1997). Os primatas do gnero Chiropotes habitam os estratos mdio e superior de orestas, acima de 20 m de altura (van Roosmalen et al. 1981; Ayres, 1989) e parecem ter uma forte preferncia por orestas de terra rme com pouca perturbao. Pithecia um gnero pouco estudado, e o que se sabe desta espcie est relacionado a estudos sobre a comunidade de primatas (Mittermeier e van Roosmalen, 1981; Rylands e Keuroghlian, 1988; Trolle, 2003). Paraua cus so muito silenciosos, fugidios e rpidos, alm de raros (Setz, 1993). No entanto vale ressaltar que indivduos dos gneros Chiropotes e Pithecia tm preferncia pelas orestas de terra rme (Ayres, 1981; van Roosmalen et al. 1981; Frazo, 1992; Peres, 1993; Ferrari et al ., 2003). Essas in formaes corroboram com os dados obtidos neste estudo, que evidenciam o maior encontro destas duas espcies em ambientes de terra rme. Apesar de nosso estudo evidenciar diferenas obtidas nas visualizaes de grupos em diferentes classes de horrios, para duas das cinco espcies registradas h escassez de tra balhos que reportam estas caractersticas. Vrias espcies de primatas neotropicais apresentam um padro comum de atividade, concentrando suas atividades de forragea mento/alimentao e deslocamento de manh e a tarde, e descansando nas horas mais quentes do dia (Egler, 1986; Santamara-Gomez, 1999; Vidal e Cintra, 2006). Este padro parece determinado parcialmente pela necessidade de satisfazer os requerimentos energticos depois de longos perodos de inatividade noturna, e por facilitar a termorre gulao durante as horas mais quentes do dia (van Roos malen, 1985; Stevenson et al. 1994). Uma das espcies que apresentou diferena nos avistamentos ao longo do dia foi Chiropotes sagulatus Segundo Frazo (1992), no perodo seco os cuxis apresentam os maiores picos de atividades no perodo da manh, onde a temperatura se apresenta mais amena. Em nosso estudo este primata foi mais vi sualizado neste perodo dirio, no entanto nossa pesquisa Tabela 2. Densidades de primatas registradas em diferentes estudos na Amaznia. Autores Local Densidade (Gr/Km 2 )/Espcies Alouatta seniculus Cebus apella Chiropotes sagulatus Pithecia pithecia Saguinus bicolor Nosso estudo RFAD* 0.66 0.67 0.3 0.64 1 Subir, 1998 RFAD 0.4 Rylands e Keuroghlian, 1998 BDFFP** 2 0.4 0.4 0.2 Peres e Nascimento, 2000 PNJ*** 1.3 3.4 1.2 Rosas-Ribeiro et al. 2006 RFAD/LBA****/BDFFP 2.15 0.54 0.99 1.28 1.63 *RFAD Reserva Florestal Adolpho Ducke; ** Projeto Dinmica Biolgica de Fragmentos Florestais; *** Parque Nacional do Ja; **** Programa de Grande Escala da Biosfera-Atmosfera na Amaznia
14 foi desenvolvida nos meses de novembro a julho, perodo que abrange o denominado inverno na Amaznia. Neste perodo, segundo Frazo (1992) eles substituem as ativi dades de forrageamento/alimentao por descanso. Essa ltima atividade poderia inuenciar a deteco destes pri matas na oresta, no entanto isso no pode ser observado neste estudo, visto que no realizamos censos durante o perodo seco. Tal como em outras pesquisas relacionadas com calitriquneos (Terborgh, 1983; Egler, 1986; Vidal e Cintra, 2006), nossos avistamentos de S. bicolor sugerem um padro tpico de atividades mais intensas nas horas ini ciais e nais do dia, com um perodo de descanso durante as horas mais quentes. Implicaes conservacionistas Localizada na zona leste de Manaus, a RFAD representa um dos recursos ambientais mais valiosos da cidade, pois abriga uma diversidade de fauna e ora de extrema impor tncia. Ela foi criada para preservar parte da oresta prim ria com toda a sua diversidade de fauna e ora para estudos cientcos. No entanto, no ano 2000, foi necessrio criar o Jardim Botnico de Manaus, que ocupa uma rea de 5 km da poro sul da reserva, de modo a conter o avano das ocupaes humanas nesta regio. Mesmo com a construo do Jardim Botnico, em vrios pontos da reserva podemos notar a destruio das cercas que demarcam os seus limites e a execuo em seu interior de atividades ilegais como caa de animais silvestres, extrao de madeira, retirada de frutos e queimadas. No grupo dos primatas, espcies com baixas taxas repro dutivas, longos perodos de gestao e baixa fecundidade, como os representantes da famlia Atelidae, so mais sens veis caa que espcies com taxas reprodutivas mais altas, longevidade mais curta e menor tempo de gestao, como os ungulados e roedores (Peres, 1990; 2000). Em nosso estudo no foi conrmada a presena de macaco-aranha ( Ateles paniscus ) no interior da reserva. No entanto, segun do observao pessoal de Rodrigues, L.F., fora dos censos desse estudo, foi registrada vocalizao deste primata dentro da reserva. A equipe do Protocolo de Primatas do Projeto TEAM tambm registrou a presena desta espcie na rea (dados no publicados). Estes dados so extremamente im portantes visto que a espcie h muito tempo no era visu alizada na reserva. Provavelmente, estas visualizaes espo rdicas devem-se ao fato da RFAD possuir uma conexo, ainda que pequena, com a mata contnua, fazendo com que animais como o macaco-aranha, que possui grande rea de vida (1.50 a 4.00 km 2 Siemmen e Sabatier, 1996), saia da mata contnua e use eventualmente a rea da reserva. Mit termeier et al. (1998) ressaltaram a necessidade de medidas emergenciais e de denies de prioridades para a conserva o de reas sob forte impacto de fragmentao, com con sequente perda rpida de hbitat e de biodiversidade, em todas as escalas (global, regional e local). Ao avaliarmos o acelerado processo de fragmentao que a RFAD sofreu ao longo dos ltimos anos, vericamos que as concluses de Mittermeier et al (1998) tomam uma proporo de urgn cia ainda maior, principalmente para espcies que reque rem grandes reas de vida e aquelas ameaadas de extino. A RFAD est inserida neste contexto e necessita de medidas que impeam o avano das queimadas e caa ilegal dentro da rea, comprometendo assim o mais estudado fragmento orestal urbano da cidade de Manaus e as espcies que l ocorrem. Neste sentido, torna-se necessrio enfatizar a im portncia da criao de corredores ecolgicos que liguem a RFAD a outros fragmentos orestais urbanos ou a oresta contnua, garantindo assim a sobrevivncia das espcies que necessitam de extensas reas de vida. Em nosso estudo, a variabilidade na densidade dos prima tas encontrados na RFAD, era esperada e pode estar as sociada s caractersticas biolgicas das espcies, tais como mobilidade entre habitats, tamanho da rea de uso, riqueza de recursos alimentares, entre outros. Os resultados suge rem a importncia da RFAD na manuteno da biodiversi dade e impem a necessidade de polticas conservacionistas direcionadas para a conteno das perturbaes antrpicas em sua rea. Agradecimentos Gostaramos de agradecer a Gernimo Ferreira Leite (Gera) e Lucas Mergulho pela competente ajuda em campo. A Marcelo Gordo por compartilhar seus conhecimentos sobre primatas. A Renato Cintra pelo apoio no desenvol ver do estudo. Ao Conselho Nacional de Desenvolvimen to Cientco e Tecnolgico (CNPq) e a Coordenao de Aperfeioamento de Pessoal de Nvel Superior (CAPES) pela bolsa de estudos a Marcelo Derzi Vidal. 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Valladares-Padua (eds.), pp.181, Editora da Universidade Federal do Paran, Paran. Peres, C. A. 1990. Eects of hunting on western Amazo nian primate communities. Biol. Conserv. 54 : 47. Peres, C. A. 1993. Notes on the Ecology of Buy Saki Monkeys ( Pithecia albicans Gray, 1860): A Canopy Seed-Predator. Am. J. Primatol 31: 129. Peres, C. A. 1994. Primate responses to phonological changes in an Amazonian Terra Firme forest Biotropica 26(1): 98. Peres, C. A. 1997. Primate community structure at twenty western Amazonian ooded and unooded forests. J. Trop. Ecol. 13: 381. Peres C. A. 2000. Eects of subsistence hunting on verte brate community structure in Amazonian forests. Con serv. Biol. 14: 240. Peres, C. A. e Dolman, P. M. 2000. Density compensa tion in neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forests of varying productivity. Oecologia 122: 175.
16 Reed, D. H., OGrady, J. J., Brook, B. W., Ballou, J. D. e Frankham, R. 2003. Estimates of minimum viable popu lation sizes for vertebrates and factors inuencing those estimates. Biol. Conserv. 113: 23. Ribeiro, J. E. L. S., Hopkins, M. G., Vicentini, A., Sothers, C. A., Costa, M. A. S., Brito, J. M., Souza, M. A. D., Martins, L. H. P., Lohmann, L. G., Assuno, P. A. C. L., Pereira, E. C., Silva, C. F., Mesquita, M. R. e Procpio, L. 1999. Flora da Reserva Ducke: guia de identicao das plantas vasculares de uma oresta de terra-rme na Amaz nia Central Instituto Nacional de Pesquisas da Amaz nia, Manaus. Rylands, A. B. e Mittermeier, R. A. 1983. Parks, reserves and primate conservation in Brazilian Amazonia. Oryx 17(2): 78. Rylands, A. B. 1986. Ranging behavior and habitat pref erence of a wild marmoset group, Callithrix humeralifer (Callitrichidae, Primates). J. Zool. Lond 210: 489. Rylands, A. B. e Keuroghlian, A. 1988. Primate popula tions in continuous forest and forest fragments in Central Amazonia. Acta Amaz. 18(3): 291. Rylands, A. B., Rodriguez-Luna, E. e Cortez-Ortiz, L. 1996/1997. Neotropical conservation the species and the UICN/SSC primate specialist group network. Pri mate Conserv. 17: 46. Robinson, J. G. e Redford, K. H. 1986. Body size, diet, and population density of neotropical forest mammals. Am. Natural. 128: 665. Robinson, J. G., Redford, K. H. e Bennett, E. L. 1999. Wildlife harvest in logged tropical forests. Science 284: 595. Rosas-Ribeiro, P. F., Rodrigues, L. F. e Spironello, W. R. 2006. Density of primates in the Central Amazonian Terra Firme forests: Two years results of the Tropical Ecology Assesment and Monitoring Program (TEAM). Dados no publicados, Tropical Ecology Assesment and Monitoring Program (TEAM), Manaus. Santamara-Gmez, A. M. 1999. Ecologia e comporta mento de Alouatta seniculus em uma mata de terra rma na Amaznia Central. Dissertao de mestrado, Univer sidade Federal de Minas Gerais, Belo Horizonte, Brasil. Schwarzkopf, L. e Rylands. A. B. 1989. Primates species richness in relation to habitat structure in Amazonian rainforest fragments. Biol. Conserv. 48: 1. Setz, E. Z. F. 1993. Ecologia alimentar de um grupo de parauacus ( Pithecia pithecia chrysocephala ) em um frag mento orestal na Amaznia Central. Tese de doutorado, Universidade Estadual de Campinas, Campinas, Brasil. Siemmen, B. e Sabatier. D. 1996. Diets of some French Guianan primates: food composition and food choices. Inter. J. Primatol 17 (5): 661. Spironello, W. R. 1991. Importncia dos frutos de pal meiras (Palmae) na dieta de um grupo de Cebus apella (Cebidae, Primates) na Amaznia Central. Em: A pri matologia no Brasil 3 A. B. Rylands e A. T. Bernardes (Eds.), pp.285, Sociedade Brasileira de Primatolo gia, Braslia. Spironello, W. R. 2000. Levantamento preliminar de ma cacos: Alto rio Cuieiras. Website: http://www.viverde. com.br/cuieiras_macacos.html Acessada em 15 de abril de 2010. Stevenson, P. R., Quiones, M. J. e Ahumada, J. A. 1994. Ecological strategies of woolly monkeys ( Lagothrix lagothricha ) at Tinigua National Park, Colombia. Am. J. Primatol. 32: 123. Subir, R. J. 1998. Avaliao da situao atual das popula es do sauim-de-coleira, Saguinus bicolor bicolor (Spix, 1823). Dissertao de mestrado, Universidade de Bras lia, Braslia, Brasil. Terborgh, J. 1983. Five New World Primates: a Study in Comparative Ecology Princeton University Press, Princeton. Trolle, M. 2003. Mammal survey in the Rio Jauaperi region, Rio Negro Basin, the Amazon, Brazil. Mammalia 67(1): 75. van Roosmalen, M. G. M., Mittermeier, R. A. e Milton, K. 1981. e bearded sakis, genus Chiropotes Em: Ecol ogy and Behavior of Netropical Primates Coimbra-Filho, A. F. e Mittermeier, R. A. (eds.), pp.419, Academia Brasileira de Cincias, Rio de Janeiro. van Roosmalen, M. G. M. 1985. Habitat preferences, diet, feeding strategy and social organization of black spider monkey ( Ateles paniscus Linnaeus, 1758) in Surinam. Acta. Amaz. 19: 1. Vidal, M. D. e Cintra, R. 2006. Eects of forest structure components on the occurrence, group size and density of groups of bare-face tamarin ( Saguinus bicolor Primates: Callitrichinae) in Central Amazonia. Acta Amaz. 36 (2): 237. Voss, R. S. e Emmons, L. H. 1996. Mammalian diversity in neotropical lowland rainforest: a preliminary assess ment. B. Am. Mus. Nat. His. 230: 1.
17 POPULATION DENSITY OF BLACK-FACED LION TAMARIN ( LEONTOPITHECUS CAISSARA ) Alexandre T. Amaral Nascimento 1 *, Fabiana Prado 2 Claudio B. Valladares-Padua 1 and Paulo de Marco Jnior 1 IP Instituto de Pesquisas Ecolgicas, So Paulo, Brasil, e-mail: email@example.com Author for correspondence, cpadua@ ipe.org.br 2 Fabiana Prado, ICMBio Instituto Chico Mendes de Conservao da Biodiversidade,Brasilia, DF, Brasil, e-mail: pradof@uol. com.br 3 Paulo De Marco Jnior, Universidade Federal de Gois, Instituto de Cincias Biolgicas, Departamento de Biologia Geral. Goinia, GO, Brasil, e-mail: firstname.lastname@example.org Abstract Here we present the results of a population survey of the black-faced lion tamarin, Leontopithecus caissara on Superagi Island, and we extrapolate this estimation to the entire population. We used the linear transect method for surveys of the area from November 2000 to January 2002. When lion tamarins were seen in transects, we noted the perpendicular distance from the path and the number of individuals sighted in a cluster. Using the software Distance 4.0 we estimated a density of 1.79 individuals/km and a population of 205 individuals (95% CI: 79 537 ind/km) on the Superagi Island. e extrap olation of these results to populations on the mainland gave us an estimate of 187 individuals (95% CI: 72 489 ind/km). Our estimate for the total population is 392 individuals (95% CI: 218 1,026 ind/km). e lower population density of L caissara compared to other species of the genus, in combination with its very small geographic range, indicate that it is critically endangered. We also discuss some aspects of the limitations of the linear transect method when densities are extremely low. e Distance 4.0 software suggested a minimum of 30 sightings for a density estimate; but from the sighting frequency in our study this would require 2,489 hours and 883 surveys, not logistically viable. Key words: Black-faced lion tamarin, Leontopithecus caissara population density, line transect methodology. Resumo Apresentamos a estimativa populacional do mico-leo-da-cara-preta, Leontopithecus caissara na Ilha do Superagi e a ex trapolao desses resultados para a populao continental. Amostramos 12 trilhas por transeco linear entre os meses de Novembro de 2000 a Janeiro de 2002. Quando avistvamos micos-lees-da-cara-preta anotvamos a distncia perpendicular ao transecto e o nmero de indivduos presentes no grupo avistado. Utilizando o software Distance 4.0 estimamos uma den sidade de 1.79 indivduos/km e uma populao de 205 (IC 95% 79 537) indivduos na Ilha do Superagi. A extrapolao desses resultados para a poro continental de distribuio da espcie resulta em uma estimativa de 187 indivduos (IC 95% 72 489). A estimativa para a populao total de 392 indivduos (IC 95% 218 1,026). Estes resultados indicam uma baixa densidade de L. caissara comparada com as demais espcies do gnero, o que somado a sua restrita distribuio geogr ca resulta em seu estatus de espcie criticamente ameaada. Tambm discutimos alguns aspectos da limitao do mtodo de transeco linear na estimativa de espcies com densidade muito baixas. O software Distance 4.0 sugere um mnimo de 30 avistamentos para a estimativa de densidade, mas com a freqncia de avistamentos desse estudo seriam necessrias 2489 horas e 883 amostragens em transectos, o que se torna invivel em termos operacionais e econmicos. Palavras-chaves : Mico-Leo-da-Cara-Preta, Leontopithecus caissara, densidade populacional, mtodo de transectos lineares. Introduction e black-faced lion tamarin, Leontopithecus caissara was described in 1990, from Superagi, an island just o the coast in the north of the state of Paran, Brazil. It was later also found to occur in a small area of the continent, in Paran and the extreme south of the state of So Paulo, Brazil (Lorini & Persson 1990, 1994). Lorini & Persson (1994) found the population of L. caissara to be very small. From their surveys by the linear transect method, they estimated an overall density of 0.3 groups/km or 1.5 in dividuals/km, and a total population of 260 individuals in three separate subpopulations. e largest of these sub populations, with 121 individuals, was that on the Island of Superagi, with two mainland subpopulations in the states of Paran (Guaraqueaba) and So Paulo (Canania). Population density was found to be lower, and the total population and geographic range smaller (approximately
18 300 km), than any of the other lion tamarins. As a result, L caissara is ranked as Critically Endangered on the IUCN Red List of reatened Species (IUCN, 2011). Superagi Island is part of the Superagui National Park, de creed in 1989 with an area of 24,500 ha. e initial surveys were carried out in the early 1990s, and the objective of the present study was to verify the current population size of L. caissara on Superagi Island. We used the linear transect method and carried out some analyses concerning about the use of this methodology in the censusing of rare species. e fact that Superagi is the stronghold for this species has considerably inuenced investment in the management of the park. As a result of ndings concerning the distribution of lion tamarin groups on Superagi, the size of the park was increased in 1997 to 33,928 ha. Basic quantitative in formation on the population of this species on the Superagi Island is crucial to our understanding of its status and viabil ity, and for the future management of the park. Study area and methodology Superagi Island (25'40 S, 48'09 W) has a total area of 114.59 km 2 and altitudes ranging from sea level to some small isolated hills reaching 245 m. e vegetation includes low coastal scrub and tall forest on sandy soils ( restinga and oresta de restinga ), some mangroves, and dense large-leafed tropical lowland and submontane forest (Prado, 1999; Schmidlin, 2004). e surveys were carried out between November 2000 and January 2002. e linear transect method (Burnham et al ., 1980; Buckland et al ., 1993; omas et al ., 2002) was used along 12 trails totaling 37.43 km, the mean length was 3.12 km, and transects ranged from 2.25 to 4.15 km in length. In order to sample all the study area, transects were distributed along the whole island of Superagi (Figure 1). Figure 1. Location of transects on the island of Superagi; Superagui National Park. e points indicate the locations of sightings of L caissara groups.
19 All trails were marked at 50 m intervals to take the geo graphical coordinates using a GPS. e trails were censused an average of 15 times each (SE = 3.56); all between 07:00 and 16:00 h. e walking speed along the trails was ap proximately 1 km/hour. In order to make each census an independent sample, we use a minimum of 30 minutes to separate censuses along a trail when going out and return ing, as suggested by the linear transect method (Buckland et al. 1993). On sighting a lion tamarin group, we took note of the time, the perpendicular distance from the trail of the rst animal seen, the number of individuals, age/sex composition of the group where possible, and the name, height and geographical coordinates of the tree in which the individual or group was sighted. No more than 10 min utes were spent collecting the data for each group sighted. Unhabituated animals move away quickly after they per ceive the presence of researchers. Population size and density of individuals were calculated using the software DISTANCE 4.0 (Buckland et al ., 1993, omas et al ., 2001, 2002). e detection function for L. caissara was tted by the model Half Normal Simple Polynomial, based on the smallest value of AIC (Aikaikes Information Criterion) and the larger value of GOF (Goodness of t) (Cullen & Rudran, 2003). e estimates for the island were extrapolated to the mainland as well, in order to present an estimate of the overall population of L. caissara omas et al (2001) suggested that a minimum of 30 sightings are necessary for the survey method using linear transects. We estimated the number of surveys and hours spent in the eld necessary to attain this number of sightings from the sighting rate we achieved, using the ac cumulated number of sightings, the distance censused and the time taken in censusing. A power function was tted to the relationship between number of sightings and distance censused using a non-linear procedure with minimum squares as loss function and in a Quasi-Newton estimation process (Zar, 1999). Results Lion tamarins were sighted 13 times during 575,512 km of censusing (mean = 44.27 km per sighting). e density of black-faced lion tamarins was estimated at 1.79 indi viduals/km (95% CI 0.69 4.69 ind/km), and the total population for the island (114.59 km) at 205 (95% CI 79 537 ind/km) with a coecient of variation (CV) of 48.2%. Extrapolating the same population density to the mainland occurrence area (104.28 km including the Paran and So Paulo populations) results in an estimate of 187 mainland individuals (95% CI 71.95 489.07 ind/km). e estimate for the total population size was 392 individuals (95% CI 151 1,026.5 ind/km). e mean number of individuals per group observed on the island was 4.5 (95% CI 3.64 5.56 ind.). e relation between the accumulated time spent cen susing (in hours) and the number of sightings showed a progressive correlation (Figure 2). According to the equa tion of the line estimated from the data in Figure 2, time spent surveying would have to be 7.56 times greater than was done on this study (2,489 hours) in order to obtain 30 sightings of L. caissara as suggested by omas et al (2001). We conducted 182 independent censuses (including those on the same trail going up the trail and then back after an interval of a half-hour or more) on the 12 transects. When the number of surveys increased, there was a non-exponen tial increase in the number of sightings, and, according to the equation of the curve in Figure 3, it would be necessary to carry out 883 censuses to obtain 30 sightings of lion tamarin groups. Figure 2. Time accumulated on the survey in hours in relation to the number of sightings. e equation of the line y = 0.84 x 0.45 explains 94.67% of variation. Figure 3. Correlation between the accumulation in the number of surveys and the number of sightings. e graph indicates that 95.78% of the variation displayed by the non-linear regression is explained by the equation of the line y = 0.78 x 0.53
20 Discussion e estimate of 205 black-faced lion tamarins on the island of Superagi, and our extrapolation of an estimated 187 individuals on the mainland and a total population of 392 wild individuals, has a relatively wide margin of error due to the small number of sightings (n=13) during the cen suses. e coecient of variation (48.2) of the population size estimate reects the variation between transects (n=12) (Magnusson, 2001), resulting from such as: i) variation in the structure of the vegetation, ii) seasonality and availabil ity of food resources, and iii) presence or absence of the capuchin monkey ( Sapajus nigritus ), a possible competi tor. e two species were frequently seen eating the same fruits, and the lion tamarins seemed to avoid the capuchin monkeys. e surveys illustrate a problem with regard to repeat transect censusing as a method for estimating popula tion densities of rare species such as the black-faced lion tamarin. As indicated by DISTANCE 4.0, 2,489 hours of survey (Figure 2) and 883 censuses (Figure 3) would be necessary to achieve the 30 sightings necessary to reduce the condence interval and the standard error to a more acceptable level. It would not be logistically viable. e question is whether 30 sightings are really necessary. We believe additional eorts must focus on research design and event counts, both factors aecting the error of Distance Sampling (Buckland et al., 2001). e methods accuracy would also benet from alternative estimations of popula tion density and the incorporation of ecological parameters into models. In this study, we propose novel strategies for population density estimates, including the use of con dence intervals and the use of home-range and home-ran ge-overlap in association with group size. A mean home range of 250 ha with an overlap of approxi mately 19%, based in data from four groups studied on Su peragi Island (F. Prado, unpublished data), and an average group size of 4.5 individuals, provides an approximate pop ulation of 244 individuals for the 11,459 ha of the island. is estimate represents the environmental carrying capaci ty (K) of the black-faced lion tamarins on Superagi Island, and is within the condence interval of the estimate from the censuses. As such it reduces the maximum value of the population of L. caissara in Superagi to 244 individuals. e only previous estimate for the Superagi population, reported by Lorini & Persson (1994), indicated 121 indi viduals. Ours, seven years on, is 40.98% higher, and 121 is within the condence interval for our estimate. It im portant to highlight that it may also reect a real increase in the numbers of lion tamarins due to protection in the park and the environmental education program, initiated in 1996 (Padua et al ., 2002). e population density we estimate for L. caissara on Su peragi is lower than those found for the other lion tama rins. An understanding of density and population size is, of course, a key factor, in future contingencies for the genetic management of the three sub-populations as a metapopu lation. However, further research is needed to understand the habitat requirements of L. caissara and what may well be signicant dierences in the population dynamics in the subtly diverse vegetation types they occupy in terms of structure and oristic composition, both on the island and on the mainland. Small populations with restricted geographical distributions and low population densities, as it is the case for L. caissara are more susceptible to ex tinction, genetic problems, environmental uctuations and extreme environmental conditions (Gilpin & Soul, 1986; Soul, 1987; Lacy, 1987, Ralls et al ., 1988, Purvis et al ., 2000). e small population and low population density conrm that the black-faced lion tamarin should be con sidered Critically Endangered and given top priority for conservation programs. Acknowledgments We thank the following institutions and people for their help and support: e Margot Marsh Biodiversity Foun dation, Wildinvest, the Lion Tamarins of Brazil Fund, Primate Conservation, Inc., the American Society of Pri matologists, the Zoological Society of London, the Dur rell Wildlife Conservation Trust, the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renovveis (IBAMA), Anthony B. Rylands, Fabiano R. Melo, Karla M. Paranhos, Laury Cullen Jr., Leandro Scoss and Lucia Agathe J. Schmidlin. Special thanks at IP Instituto de Pesquisas Ecolgicas and the sta, professors and students of the II Curso Latino Americano de Biologia da Conser vao (2001). References Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L. 1993. Distance Sampling, Estimating Abundance of Biological Populations Chapman and Hall, London. Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borches, D. L., omas, L. 2001. Introdution to Distance Sampling Oxford University Press, Oxford. Burnham, K.P., Anderson, D. R., Laake, J. L. 1980. Esti mation of density from line transect sampling of biologi cal population. Wildl. Monog. 72: 1. Cullen Jr., L. and Rudran, R. 2003. Transectos lineares na estimativa de densidade de mamferos e aves de mdio e grande porte. In Mtodos de Estudos em Biologia da Con servao & Manejo da Vida Silvestre (Cullen Jr. L, Rudran R, Valladares-Padua C, editors), pp 169. Editora UFPR, Curitiba, Paran, Brasil. Gilpin ME, Soul ME. 1986. Minimum viable popula tions: processes of species extinction. In Conservation
21 Biology: e Science of Scarcity and Diversity (Soul ME, editor), pp 19. Sinauer Associates, Sunderland, Massachusetts. IUCN 2011. IUCN Red List of reatened Species. Ver sion 2011.1. < www.iucnredlist.org >. Downloaded on 14 October 2011. Lacy, R. C. 1987. Loss of genetic diversity from managed populations: interacting eects of drift, mutation, im migration, selection and population subdivision. Conserv Biol 1: 143. Lorini, M. L. and Persson, V. G. 1990. Nova espcie de Leontopithecus Lesson 1840 do sul do Brasil (Primates, Callitrichidae). Bol Mus Nac Rio de Janeiro 338: 1. Lorini, M. L. and Persson, V. G. 1994. Status and eld research on Leontopithecus caissara : e Black-faced Lion Tamarin Project. Neotrop Primates 2(Suppl): 52. Magnusson, W. E. 2001. Standard errors of surveys esti mates: What do they mean? Neotrop Primates 9: 53. Padua, S. M., Deitz, L. A., Rambaldi, D. M., Souza M das G de, Santos, G. R dos. 2002. In situ conservartion education and the lion tamarins. In Lion Tamarins: Biol ogy and Conservation (Kleiman DG, Rylands AB, eds.), pp 315. Smithsonian Institution Press, Washington, DC. Prado, F. 1999. Ecologia, comportamento e conservao do mico-leo-da-cara-preta (Leontopithecus caissara) no Parque Nacional do Superagi, Guaraqueaba, Paran Masters thesis, Universidade Estadual Paulista, Botucatu, Brasil. Purvis, A., Gittleman, J. L., Cowlishaw, G., Mace, G. M. 2000. Predicting extinction risk in declining species. Proc R Soc Lond, B 267: 1947. Ralls, K., Ballou, J. D., Templeton, A. 1988. Estimates of lethal equivalents and the cost of inbreeding in mam mals. Conserv Biol 2: 185. Schmidlin, L. A. J. 2004. Anlise da disponibilidade de habitat para o mico-leo-da-cara-preta ( Leontopithecus caissara Lorini & Persson, 1990) e identicao de reas preferenciais para o manejo da espcie por tcnicas de geoprocessamento. Masters thesis. Universidade Federal do Paran, Curitiba, Brazil. Soul, M. E. 1987. Viable Populations for Conservation Cambridge University Press, Cambridge, UK. omas, L., Laake, J. L., Strindberg, S., Marques, F., Borch ers, D. L., Buckland, S. T., Anderson, D. R., Burnham, K. P., Hedley, S. L., Pollard, J. H. 2001. Distance 4.0, Beta 2 Research unit for Wildlife Population Assessment. University of St. Andrews, St. Andrews, UK. http://www. ruwpa.st-and.ac.uk/distance / omas, L., Buckland, S. T., Burnham, K. P., Ander son, D. R., Laake, J. L., Borches, D. L., Strindberg, S. 2002. Distance sampling. In Encyclopedia of Environmet rics (El-Shaarawi AH, Piegorsch WW, eds.), Volume 1, pp 544. John Wiley & Sons, Ltd, Chichester. Zar, J. H. 1999. Biostatistical Analysis (4th ed.), New Jersey, Prentice Hall.
22 S A MALE CARE IN MANTLED HOWLER MONKEYS ( ALOUATTA PALLIATA PALLIATA ) Eugenia Zandon Introduction Adult male-immature interactions in non-human primates range from aggressive displays their extreme expression being infanticide (Bartlett et al., 1993) agonistic bu ering (Taub, 1980), tolerance or indierence (Baldwin & Baldwin, 1973) to aliative and caretaking (Riedman, 1982; Buchan et al., 2003). In some monogamous spe cies such as tamarins and marmosets (reviewed in Ried man, 1982), males participate in parental care almost as frequently as mothers. Indeed in these species, the adult males reproductive eorts include parental care (mainly expressed in infant transportation)and not just mating costs as in polygamous species (Key & Aiello, 2000). Some forms of paternal care, particularly protection from danger, are also seen in polygamous species (e.g. savannah baboons, Papio cynocephalus ; Buchan et al., 2003). In the genus Alouatta cases of infanticide by males have been reported following group take-overs (Clarke, 1983; Agoramoorthy & Rudran, 1995; Knop et al., 2004). Nevertheless, tolerant, playful, and protective behaviors toward infants and juveniles are more common than ago nistic activities (Baldwin & Baldwin, 1973; Clarke, 1986). In this paper I report on male care of an immature mantled howler monkey ( Alouatta palliata palliata ) orphan, and dis cuss whether it can be viewed in terms of paternal care or adoption. Methods e observations reported here were recorded during a study of the behavioral ecology of four groups of mantled howler monkeys in the Sectr Santa Rosa of the Area de Conservacin Guanacaste (ACG) in Costa Rica (Fig. 1). e study area is a tropical dry forest with patches of semievergreen forest at various stages of succession, character ized by distinct wet and dry seasons (Janzen, 1986), with an annual rainfall of ~1,500. e study group was observed during a more extensive behavioral research project cover ing three eld periods over a total of 15 months: 1) from September to November 2003, the infants mother was still in the group; 2) from April to August 2004, interactions occurred between the immature orphan and the immatureadult male and 3) from April to October 2005, when the immature was already independent. Rare behaviors and un usual social interactions, such as those described here, were recorded ad libitum and all occurrences recording (sensu Martin and Bateson 1993), thus an exact and detailed Figure 1. Map of the study site, the Area de Conservacin Guanacaste (ACG) in Costa Rica. (Map credit Waldy Medina, ACG).
23 account of the behavior was recorded. Group composition and details of the sampling and recording methods for data collection during the three eld periods are presented in Table 1. It was possible to identify all group individuals via unique physical features such as light spots underneath their feet, scars, or clitoris shape. At the beginning of the study, the group comprised 2 adult males, 4 adult females and 3 immature, however the two key individuals in this study were an adult male, CH, and a female infant, EV. CH was probably the e lder of the two adult males, he had numerous facial wrinkles. EVs birth is estimated to have taken place in March or April 2003; so at the start of the study she was approximately 5 months old. When group observations resumed in 2004, EV was an orphan and her mother had disappeared from the group. Here I report on interactions between EV and CH during 2004. As the group was not the main focus of the overall research project during this year, it was fol lowed for a shorter period (4 and 7 hours per day over 13 days) when compared to 2003 and 2005. Data reported here were collected ad libitum and recorded continuously (Altmann, 1974). Results During 2003, EV was still nursing and spending a large amount of time in proximity or in body-contact with her mother. In particular, while resting and sleeping, they were frequently in the mother-ospring resting (MOR) posi tion, typical for an infant of EVs age. MOR is when the mother sits on her haunches on a support and the imma ture maintains ventral contact. In 2003, no interactions were recorded between CH and EV. By April 2004, EV was approximately 12 months old and an orphan, at this time she was observed interacting habitually with CH. During each of the 13 observation days, EV and CH were frequently seen resting in close proximity. On 17 occasions EV and CH were observed assuming the MOR posture, six times at sunrise, three at sunset and seven times during the day and once during a heavy rainfall event. In the majority of cases, EV solicited that CH assume the MOR position, vocalizing, approaching him and crawl ing on to his body. In general, CH was passive during these interactions, simply allowing EV to attain body contact. However, on two occasions CH actively invited EV to assume the MOR posture, reaching out and pull ing her gently towards him. e rst event (30 Jun 2004) occurred when it was raining heavily, EV approached CH and started to emit distress calls; CH oered her protec tion, enabling her to position herself in ventral contact with him. e second time (23 Aug 2004), CH and EV were already in the MOR position, but after a few min utes CH removed EV, after which the infant started to produce distress calls and moved closer to CH, who then gently lifted her towards him, allowing her to return to the MOR posture. On several occasions, EV was observed following CH during travel, and feeding in close proxim ity to him. Play sessions were also recorded between these two individuals. No other adult was observed giving EV maternal/paternal care. When the group was observed again in 2005, EV was 24 months old, she was completely independent and appeared to be healthy. She was never seen assuming the MOR posture with CH, however, aliative interactions between the two individuals continued, mainly expressed through play (three records). EV was also seen playing with other juveniles and adult females. During the three years of observations (634 hours), EV was never observed interacting with the other adult male member of the group. Discussion Adult male howler monkeys are generally tolerant of infants and immatures, and have been recorded playing with them and allowing them to crawl on their bodies (Bolin 1981; Clarke, 1986). Males also occasionally ba by-sit immatures when the mother moves away for short periods of time and they may also protect them in situ ations of potential danger (Clarke et al., 1998). Bolin Table 1. Description of the sampling methods, group and orphan characteristics during the three years of observations for the study group. Sampling methods refer to all data collection for the study group during the larger behavioral project. EV: orphan; CH: adult male; M: adult male; F: adult female; I: immature; Fs: subadult female; MOR: mother-ospring resting posture Year Sampling methods Observation time Group composition EVs estimated age (months) EVs condition Interactions between EV and CH 2003 All occurrences, focal animal and ad libitum 33 days, 5 hr/d (Total=290 hrs) 2 M, 4 F, 3 I (Total=9) ~5 EV was still nursing and dependent on her mother No interactions recorded 2004 All occurrences, ad libitum 13 days, 4 hr/d (Total=70 hrs) 2 M, 3 F, 3 I (Total=8) ~12 EV was an orphan Numerous aliative interactions were recorded, including MOR 2005 All occurrences, scan and ad libitum 30 days, 8 hr/d (Total=274 hrs) 2 M, 5 F, 2 Fs, 4 I (Total=13) ~24 EV was healthy and completely independent Observed playing on 3 separate occasions
24 (1981) reported an increase in adult male-infant inter actions with increased age of the infant in Alouatta pal liata pigra documenting that older infants (12 months or more, moderately independent of their mother) fol lowed males during travel and foraged next to them. In 2004, EV and CH were observed both foraging and trav eling in close proximity and playing together. However, the interactions between EV and CH were not limited to these contexts, CH undertook a role as paternal care giver over longer periods. At night, and even during the day, they repeatedly assumed the MOR posture, which is normally restricted to the mother and infant. As in fants mature (approximately 2 years in Alouatta p. pallia ta ), this type of physical contact with the mother occurs less frequently, only during nighttime sleeping or heavy rainfall (pers. obs.). During these moments, older infants are still dependent on their mother for thermoregula tion and protection from predators (Bicca-Marques & Calegaro-Marques, 1998). EV was orphaned at around 8 months, an age when she probably still needed the protection of an adult and required parental care, espe cially at night. Without the care of another individual of the group, she may have died. CH provided exclusive care to EV and probably contributed to her survival. In Alouatta palliata likely fathers show dierent forms of paternal care, such as carrying, cuddling, watching, and sit ting in proximity, and have never been observed showing aggressive behavior towards their probable ospring, but they can be violent towards non-related infants (Clarke 1986; Clarke et al., 1998). During the observation period (2003), CH and another individual were the only two adult males in the group. In stark contrast to the close relationship shared by EV and CH, no interactions were ever observed between EV and the other male. Although the genetic relatedness of EV and CH was never tested, it is possible that CH was EVs father. It has been demonstrated that in some non-human primate species males can recognize their ospring and provide them with paternal care (e.g. Papio cynocephalus ; Buchan et al., 2003). CH may have recognized EV as his daughter and taken care of her when she became an orphan, thereby substituting her mother and providing her with atypical paternal care for the species. Guaranteeing the survival of EV would thereby optimize CVs reproductive eort and increase his tness. Infant adoption is often dependent upon the persistence of the immature in soliciting adult care, the tenacity of the infant can aect its chances of sur vival (Clarke & Glander, 1981; Dolhinow & Ta, 1993; Gould, 2000). In the case reported here, the female infant was often observed closely following the adult male, and more importantly, actively soliciting body contact and adoption by the male of the MOR posture. EVs insistence appeared to have paid o and she was able to secure the parental care she needed. Biedzicki de Marquez and Ades (2000) described the only known case of male adoption in the genus Alouatta where infant persistence seems also to have played a considerable role in the positive outcome of the adoption. Nevertheless, the adoption they described followed the kidnapping of the infant from another group and was undertaken by an adult female and adult male (the only two mature individuals of the group). is is somewhat dierent to the case described here. e orphans survival was probably due largely to the care and protection given by the adult male, promoted by the orphans persistence and the possible paternity of the adult male, thus this can be viewed as a case of paternal care rather than adoption. Acknowledgments e research was mainly funded by the Fondazione Ing. Aldo Gini. I am grateful to the rea de Conservacin Gua nacaste, particularly R. Blanco, the Costa Rican MINAE (Ministerio del Medio Ambiente y Energia) for issuing the permits (2003: licencia #30242; 2004: licencia #36792; 2005: scientic passport #0436), to N. Asensio for his sup port and insightful suggestions, to A. Sieg, S. Ansaloni, M. Weksler, and L. Guidolin for comments on this manu script, to L. Rebecchini and E. Murillo-Chacn for help in the eld. A Brazilian CNPq-PDJ scholarship supported the writing of this manuscript. Eugenia Zandon Dipartimento di Biologia, Universit degli Studi di Padova, Italy. Departamento de Ecologia IBRAG, Universidade do Estado do Rio de Janeiro, Rua So Francisco Xavier, 524, Maracan, Rio de Janeiro, RJ, CEP 20550, Brasil, e-mail: < eugenia.zandona@gmail. com > References Agoramoorthy, G. and Rudran, R. (1995) Infanticide by adult and subadult males in free-ranging red howler monkeys, Alouatta seniculus in Venezuela. Ethology 99: 75. Altmann, J. (1974) Observational study of behavior: sam pling methods. Behaviour 49: 227. Baldwin, J. D. and Baldwin, J. I. (1973) Interactions be tween adult female and infant howling monkeys ( Alouat ta palliata ). Folia Primatol. 20: 27. Bartlett, T. Q., Sussman, R. W. and Cheverud, J. M. (1993) Infant killing in primates: a review of observed cases with specic reference to the sexual selection hypothesis. Am. Anthropol. 95: 958. Bicca-Marques, J. C. and Calegaro-Marques, C. (1998) Behavioral thermoregulation in a sexually and develop mentally dichromatic Neotropical primate, the blackand-gold howling monkey ( Alouatta caraya ). Am. J. Phys. Anthropol 106: 533.
25 Biedzicki de Marquez, A. A. and Ades, C. (2000) Male care in a group of wild Alouatta fusca clamitans in southern Brazil. Folia Primatol. 71: 409. Bolin, I. (1981) Male parental behavior in black howler monkeys ( Alouatta palliata pigra ) in Belize and Guate mala. Primates 22: 349. Buchan, J. C., Alberts, S. C., Silk, J. B. and Altmann, J. (2003) True paternal care in a multi-male primate society. Nature 425, 179. Clarke, M. R. (1983) Infant-killing and infant disappear ance following male takeovers in a group of free-ranging howling monkeys ( Alouatta palliata ) in Costa Rica. Am. J. Primatol. 5:241. Clarke, M. R. (1986) Interactions of adult male howling monkeys ( Alouatta palliata ) with immatures in a freeranging social group. Am. J. Phys. Anthropol. 69:188. Clarke, M. R. and Glander, K. E. (1981) Adoption of infant howling monkeys ( Alouatta palliata ). Am. J. Pri matol. 1: 469. Clarke, M. R., Glander, K. E. and Zucker, E. L. (1998) Infant-non mother interactions of freeranging mantled howlers ( Alouatta palliata ) in Costa Rica. Int. J. Primatol. 19: 451. Dolhinow, P. and Ta, M. A. (1993) Immature and adult langur monkey ( Presbytis entellus ) males: infant-initiated adoption in a colony group. Int. J. Primatol. 14: 919. Gould, L. (2000) Adoption of a wild orphaned ringtailed lemur infant by natal group members: adaptive explana tions. Primates 41: 413. Janzen, D. H. (1986) Guanacaste Natural Park: tropical ecology and cultural restoration. Fundacin de Parques Nacionales, Editorial Universidad Estatal Distancia, San Jos, Costa Rica. Key, C. and Aiello, L. C. (2000) A prisoners dilemma model of the evolution of paternal care. Folia Primatol. 71:77. Knop, K. H., Knop, A. R. A. and Pavelka, M. S. M. (2004) Observed case of infanticide committed by a resi dent male Central American black howler monkey ( Al ouatta pigra ). Am. J. Primatol. 63: 239. Martin, P. and P. Bateson. 1993. Measuring behavior. An introductory guide. 2nd Edition. Cambridge University Press, Cambridge, UK. Riedman, M. L. (1982) e evolution of alloparental care and adoption in mammals and birds. Q. Rev. Biol. 57: 405. Taub, D. M. (1980) Testing the agonistic buering hy pothesis. I: e dynamics of participation in the triadic interactions. Behav. Ecol. Sociobiol. 6: 187. A PRELIMINARY STUDY OF THE GENETIC DIVERSITY OF PYGMY MARMOSET CALLITHRIX PYGMAEA (PRIMATES: CEBIDAE: CALLITHRICHINAE) USING SHORT SEQUENCE REPEATS (SSR) Diego Alejandro Nieto Monteros Stella de la Torre Venancio Arahana Mara de Lourdes Torres Ana Mara Troya Zuleta Introduction Genetic diversity is a major concern in conservation biol ogy, the loss of genetic diversity is often associated with a reduction in reproductive tness and a population decrease. Genetic diversity is required for populations to evolve and adapt to environmental changes that in present times are more frequent and more rapid due to anthropogenic factors (Frankham et al. 2003). Primates play a fundamental role in the dynamics of tropical ecosystems. e pygmy marmoset Callithrix pygmaea is the smallest primate species in Ecuador and shows a high degree of specialization in habitat and diet (de la Torre et al. 2009). is specialization combined with the increase of human ac tivities in tropical rainforests could drive pygmy marmoset populations to genetic bottle necks with the subsequent loss of genetic diversity. Almost nothing, however, is known about the genetic diversity of this species so we began a pilot study to evaluate the genetic diversity of 3 wild groups of pygmy marmosets in one population located on the margins of the Aguarico River, in northeastern Ecuador. We developed a non-invasive protocol to obtain DNA samples from feces to characterize the genetic diversity of the groups as a rst and necessary step in the implementation of a program to evaluate human impact on the genetic diversity of pygmy marmosets and other Ecuadorian primate species. Study area and subjects e San Pablo population is located at the margins of the Aguari co river (0'27"S, 76'29"W) (Fig 1). is area has varzea forest and is seasonally ooded by white-waters rivers. ree groups (P1, P2, P4), in this population have been monitored since the year 2000 and were the study subjects (de la Torre et al. 2009). Group size varied from 5 to 7 individuals during the sampling period. Groups P1 (5 individuals) and P2 (6 individu als) had the most distant home ranges, separated by open areas, houses and several plantations (closest linear distance between P1 and P2 home ranges: 250 m). Groups P1 and P4 (7 individuals) had a disturbed, secondary forest connecting their home range areas (closest linear distance between P1 and P4 home ranges: 165 m). Finally, between the home range areas of groups P2 and P4 there are open areas with some trees but no houses (closest linear distance between P2 and P4 home ranges: 200 m).
26 Methods Collection of fecal samples Fecal samples were collected from September 2008 through February 2009 from these three groups. Large leaves of banana ( Musa paradisiaca ) and heliconia ( Heliconia spp.) were placed very early in the morning under the feeding tree of a group before the marmosets began their daily activities. Animals were observed by one eld worker in periods of 3 hours from 0600 to 0900 and from 1500 to 1800 (local time). e leaves were checked continuously during the observation periods. Due to the collection methods, we could not accurately address a particular fecal sample to a given animal in a group; however, based on our observations, we are condent that the collected feces belonged to at least 3 dierent animals in each group. Col lected feces were stored on lter paper and placed in a ask with a desiccant (silica gel). e closed asks with the sam ples were dried with controlled sunlight (avoiding drastic rises of temperature) during one or two days to reduce the probability of contamination of the feces with fungi. e samples were later transported to Quito and placed in a freezer at C. Genetic analyses DNA from the samples was obtained using the QIAamp DNA Stool Mini Kit ( QIAGE N ). Polymerase chain reac tion technique was used to amplify nDNA microsatel lites; we tested primers established by Nievergelt et al. (1998) for Callithrix jacchus e PCR amplication was performed in a 25 L reaction volume which include buer 1X, 1.5mM of MgCl 2 0.2M of dNTP`s, 0.24M of each primer, 0.5U of Taq polymerase (Invitrogen) and 5ng of sampled DNA. e amplication program consisted of an initial denaturation of 3 min at 95 C; 40 cycles of denatur ation for 1 min at 94 C, annealing for 1 min at optimum temperature (Table 1) and an elongation during 1 min at 72 C; and a nal elongation at 72 C during 5 min. Polyacrylamide 6% and urea 5M gels were used to separate DNA bands. Results Forty two fecal samples were collected from the three groups; 23 samples from group P4, 12 samples from group P2 and 7 samples from group P1. Five of the nine loci tested (CJ-1, CJ-7, CJ-11, CJ-12, and CJ-15) showed a higher number of amplied samples (>10 amplied sam ples per primer) (Table 1) and were used for a preliminary analysis of the number of alleles in each loci. DNA sam ples from group P4 showed various alleles at the ve loci tested, samples from group P2 showed alleles at 3 loci, and samples from group P1 showed alleles at four loci (samples from this group showed xed alleles at 2 loci) (Fig 2). Discussion Although the number of samples for each group was small (P1 n = 7; P2 n = 12; and P4 n = 23) and the number of loci analyzed was also low (5 loci), the results evidence the Figure 1. Location of the San Pablo population in Ecuadorian Amazonia
27 feasibility of inter-specic use of microsatellite primers to evaluate genetic variability of related primate species (Clisson et al. 2000, Nievergelt et al. 1998). e results also allow us to dierentiate several alleles in some of the tested loci. e xed alleles found in groups P1 and P2 could be an artefact of the collection methods (we could not address fecal sam ples to particular individuals) and the small sample sizes for these groups, making it possible that more than one sample belonged to the same individual. However, they could also suggest a reduced genetic variability in groups aected by strong habitat fragmentation (Frankham et al. 2003). We are now collecting more samples to identify dierent genotypes in each group to be able to assess genetic variability in this and other populations of pygmy marmosets. e conservation of biodiversity is critical in tropical for ests of the Amazon. e annual deforestation rate in Ecua dor is estimated at around 200,000 ha and most of it takes place in the Amazon region, which is also aected by oil exploitation and mining (Ministerio del Ambiente et al. 2001, SENPLADES 2007). Molecular genetics is a tool to evaluate the impact of human activities on the popula tions of species inhabiting these areas, such as the pygmy marmoset. Sensitive genetic markers, such as microsatel lites, have the power to detect reductions in heterozygosity and allelic diversity in small and fragmented populations (Frankham et al. 2003) and provide useful information for conservation planning. is is the rst study of this type for pygmy marmosets in Ecuador and elsewhere; our re sults suggest that non-invasive methods to collect DNA for the evaluation of the genetic diversity can be used even for small species such as pygmy marmosets. Our next steps in this research will be to improve the collection methods in the eld (to reduce DNA damage, increase sample size and identify genotypes) and include more populations in the genetic analyses. Acknowledgments We are grateful to the Small Grants Scholarship Program of the Universidad San Francisco de Quito, to the VIHOMA foundation and the University of Wisconsin, Madison, USA for their nancial support. We thank Hernn Pay aguaje and Pablo Ypez for the valuable help in the samples collection, Charles T. Snowdon for his donation of labora tory supplies and his valuable comments on the manuscript, and the team of the Laboratorio de Biologa Molecular of the Universidad San Francisco de Quito, for their help and guidance in the laboratory analyses. is research was car ried out with the permit 014-IC-FAU-DRSO-MA2008 of the Ecuadorian Ministry of the Environment. Diego Alejandro Nieto Monteros, Stella de la Torre*, Ana Mara Troya Zuleta, Venancio Arahana, Mara de Lourdes Torres Colegio de Ciencias Biolgicas y Ambien tales (COCIBA), Universidad San Francisco de Quito, Va Interocenica S/N, Cumbay, Ecuador. *Corresponding author email: < email@example.com > References Clisson, M., Lathuilliere, M., Crouau-Roy, B. 2000. Con servation and Evolution of Microsatellite Loci in Primate Taxa. Am. J. Primatol 50:205 214 de la Torre, S., Ypez, P., Snowdon, CT. 2009. pp. 451 463. Ecology and conservation of pygmy marmosets in Amazonian Ecuador. In: e Smallest Anthropoids: e Marmoset/Callimico Radiation. L.C. Davis S.M. Ford, L. Porter (eds.). Springer, New York Frankham, R., Ballou, J., Briscoe, D. 2003. Introduction to Conservation Genetics Cambridge University Press. United Kingdom. Ministerio del Ambiente, EcoCiencia, UICN. 2001. La biodiversidad del Ecuador ; Informe 2000. Ministerio del Ambiente/EcoCiencia/UICN. Quito. Nievergelt, C., Mundy, N. Woodru, D. 1998. Micro satellite primers for genotyping common marmoset ( Callithrix jacchus ) and other callitrichids. Mol. Ecol. 7: 1432. SENPLADES. 2007. Plan Nacional de Desarrollo. Quito. Figure 2. Allele frequencies at the ve loci in the pygmy marmoset groups P1, P2, and P4 (numbers in the X axis correspond to the base pairs) Table 1. Annealing temperature, number of amplied samples and product size range in base pairs (bp) for the nine loci analyzed in Callithrix pygmaea Primer Annealing temperature (C) # Amplied samples Product size range in base pairs (bp) CJ-1 58 11 128 176 CJ-6 58 0 CJ-7 50 13 119 127 CJ-10 50 4 217 243 CJ-11 50 14 106 142 CJ-12 58.4 27 132 168 CJ-13 50 0 CJ-14 56.2 9 156 184 CJ-15 50 15 124 138
28 REACTIONS OF WHITE-BELLIED SPIDER MONKEYS TO A PREDATION ATTEMPT BY A COUGAR talo Mourth An increasing body of evidence suggests that large felids are one of the main predators of large arboreal primates (e.g., Peetz et al. 1992 ; Matsuda and Izawa, 2008 ). Preda tors employ highly specic hunting techniques in order to successfully capture their prey, and prey species may evolve elaborate defense behaviors in order to avoid been killed ( Zuberbhler and Jenny, 2002 ). However, just as there are a scarce number of predation records in the wild, there are also relatively few accounts of behavioral responses by primates facing their predators ( Stelzner and Strier, 1981 ; Heymann, 1990 ; Nunes et al. 1998 ; Asensio and GmezMartn, 2002 ; Miranda et al. 2006 ). Here, I describe the reactions of white-bellied spider monkeys ( Ateles belze buth ) facing a large potential predator, the cougar (Puma concolor) at Marac Ecological Station (MES; 3'44" N, 61'01" W), a large riverine tropical rainforest island in the state of Roraima, Brazil. On June 22, 2010, I witnessed the furtive approach of a cougar while following a mixed-sex troop of approximately 7 spider monkeys in a relatively low terra-rme forest. e cougar was observed at 0704h moving quickly and silently, and it appeared to be pursuing the spider mon keys. During the few seconds the cougar was observed, it crouched with its head slightly raised, its ears up and facing forward, and its face oriented toward the moving monkeys. en, it resumed tracking the monkeys route and I did not see it again. e cougar apparently did not perceive or ignored my presence nearby. e spider monkeys reacted instantly when they detected the cougar. Intense and loud barking calls were emitted and they quickly climbed as high as possible in the canopy ( ca. 18 m). However, monkeys did not shake branches or throw sticks down as observed when they are disturbed by predators ( e.g., Matsuda and Izawa, 2008 )Colombia
29 challenges, and directions for the future
30 SOUTHERN EXTENSION OF THE GEOGRAPHICAL RANGE OF THE PYGMY MARMOSET CEBUELLA PYGMAEA NIVEIVENTRIS (LNNBERG, 1940) IN THE SOUTHWESTERN AMAZON BASIN, STATE OF RONDNIA, BRAZIL Mariluce Rezende Messias Juliano Tupan Coragem Ivonete Santa Rosa Gomes Marcela Alvares Oliveira Paulo Henrique Bonavigo Samuel dos Santos Nienow Eduardo Santos de Souza In this paper we identify a southern extension of Cebuella pygmaea niveiventris in the upper reaches of the Rio Ma deira basin, State of Rondnia, located in the Southwest ern Amazon Biome, Brazil is includes the rst registered sighting of Cebuella pygmaea niveiventris within the State of Rondnia. We adopt the taxonomic guidelines of Ln nberg (1940) and consider the Cebuella pygmaea specimen collected from Lago Ipixuna (on the southern banks of the Rio Solimes) with a white chest, belly, inner surface of forelegs and hindlegs, as a subspecies ( C. p. niveiventris ). Hershkovitz (1977), on the other hand, argues that the color of the underparts in this specimen is an individual characteristic and varies locally in the C. pygmaea popula tion, and so does not justify the status of subspecies. Cebuella pygmaea niveiventris was previously thought to occur in the following locations: in Eastern Peru south of the Rio Maraon and east of the Rio Huallaga, and in the Brazilian state of Amazonas, south of the Rio Solimes and west of the Rio Purus. Its geographical distribution was later found to include the interuvium Purus-Madeira to the southern limits of the Rio Ipixuna (or Paranapixuna) by Roosmalen and Roosmalen (1997). e presence of C. p. niveiventris in northern Bolivia reported by Heltne et al. (1976), Izawa (1979), Izawa and Bejarano (1981) and Brown and Rumiz (1986) suggests its occurrence in the upper Rio Madeira basin, as well as the eastern part of the State of Acre including the upper reaches of the Rio Abun, a tributary of the Rio Madeira, as argued by Rylands et al. (1993). Ferrari (1993, 1996) also suggested that it was likely to occur along the upper reaches of the Rio Madeira basin, as local residents had reported its presence near to the Serra dos Trs Irmos Ecological Station in northwest ern Rondnia. In addition, according to Messias (2002, 2004), a total of 18 out of 66 interviewees living between the Santo Antnio rapids and the convergence of the Rio Abun with the Rio Madeira conrmed the presence of Cebuella pygmaea niveiventris when shown a selection of photos of various neotropical mammal species. Sightings by riverine communities indicate that the ocur rence of Cebuella pygmaea niveiventris is always found in terra rme (non-ooded) riparian forests of the Rio Madeira and those of its major tributaries near to their conuence (Messias, 2004) e upper reaches, with high, steep banks have terra rme forest right up to the edge of the riverbank along almost all of its length. Interviewees ex plained that Cebuella pygmaea niveiventris visits fruit trees at the height of the rainy season, however the number of sightings has drastically decreased over the last ten years. In these interviews, the occurrence of Cebuella pygmaea was particularly high among the Jatuarana and Cachoeira do Macaco riverside communities, where pygmy marmosets were frequently observed eating the Inga edulis fruits (Mes sias, 2004) and associated ants (M. A. Oliveira personal observation). Cebuella pygmaea niveiventris has never been sighted by re searchers in the upper reaches of the Rio Madeira before, although several groups have been registered at the con struction site of the Santo Antnio hydroelectric dam near the Santo Antnio rapids, located approximately 9 km upstream from the city of Porto Velho, Rondonias State capital, and the rst of 16 rapids that present a major ob stacle to navigation of the upper reaches of the river. Here we report a specimen that was rescued during the clear ing of the Santo Antnio hydroelectric dam construction site (08 o 46.4 S; 63 o 58.0 W) and deposited at the scientic collection of the Federal University of Rondnia (UNIR), in the Reference Mammal Collection (CRMRO) (museum catalogue: UFROM 175, adult male, skull, skin and skeleton, collected by Juliano Coragem and Ivonete Santa Rosa Gomes, October 10, 2009). e specimen is yellowish grey with a white chest, belly and inner surface of forelegs and hindlegs, and is similar to the Lnnberg description of the subspecies Cebuella pygmaea niveiventris We also report that two Cebuella groups were observed after the Santo Antnio hydroelectric dam construction site had been cleared; both groups were in a very small forest patch with a high density of Cecropia sp. trees (two individuals at 08'53.9" S; 63'11.9" W and four at 08'05.3" S; 63'11.9" W, J. Coragem, personal ob servation). is corroborates the ecological data from Ce buella pygmaea niveiventris from the lower reaches of the Rio Madeira basin, where locals reported C. p. niveiventris to be common but conned to terra rme forest (van Roos malen and van Roosmalen, 1997). e newly registered sightings and the collected sample conrm the southern extension of the geographical range of Cebuella pygmaea niveiventris to the upper reaches of the Rio Madeira basin (an area that has been highly impact ed by the recent construction of two hydroelectric dams: Santo Antnio and Jirau). e preferred habitat of Cebuella in this region the riparian forest of the Rio Madeira and major tributaries is directly aected by the dams res ervoirs, and although information is lacking in terms of the distribution and density of groups in this area, reports by local people indicate a sharp population decrease in the last 10 years. is, together with the synergetic impact of
31 deforestation of the reservoir areas, merit further research and monitoring in order to establish the consequences for Cebuella pygmaea niveiventris in the upper reaches of the Rio Madeira basin. Acknowledgments We are grateful to Nick Richardson for the English revision and to Santo Antnio Energia Sustentvel Consortium (SAE) for the logistic and nancial support. Mariluce Rezende Messias, Universidade Federal de Rondnia UNIR Mastozoology Laboratory. BR 364, Km 9,5. CEP 76900. Porto Velho, Rondnia, Brazil, e-mail: firstname.lastname@example.org Juliano Tupan Coragem, Ivonete Santa Rosa Gomes, Marcela Alvares Oliveira, Paulo Henrique Bonavigo, Samuel dos Santos Nienow and Eduardo Santos de Souza, Environment Basic Program (PBA) of Faunal observation and rescue from the construction site (dry areas) of the Santo Antnio hydroe lectric dam Santo Antnio Energia Sustentvel Consor tium (SAE). References Brown, A. D. and Rumiz, D. I. 1986. Distribucin y con servacin de los primates em Bolivia estado actual de conocimiento. In: Primatologia no Brasil vol. 2, M. T. de Mello (ed.), pp. 335. Sociedade Brasileira de Prima tologia, Braslia. Ferrari, S. F. 1993. e adaptive radiation of Amazonian callitrichids (Primates, Platyrrhini). Evolucin Biolgica 7:81. Ferrari, S. F., Cruz Neto, E. H., Iwanaga, S., Corra, H. K. M. and Ramos, P. C. S. 1996. An unusual pri mate community at the Estao Ecolgica Serra dos Trs Irmos, Rondnia, Brazil. Neotrop. Primates 4(2): 55. Heltne, P. G., Freese, C. H. and Whitesides, G. 1976. Field survey of nonhuman primates in Bolivia. Unpublished report, Panamerican Health Organization (PAHO), Washington, D.C. Izawa, K. 1979. Studies on the peculiar distribution pat tern of Callimico Kyoto University Primate Research Institute, Reports of New World Monkeys (1979): 23. Izawa, K. and Bejarano, G. 1981. Distribution ranges and patterns of nonhuman primates in western Pando, Boliv ia. Kyoto University Overseas Research Reports of New World Monkeys (1981): 1. Lnnberg, E. 1940. Notes on marmosets. Ark. Zool. 32A (10):1. Messias, M. R. 2002. Levantamento de mastofauna da Avaliao Ecolgica Rpida da Estao Ecolgica Estadual Antnio Mujica Nava/ RO, fevereiro de 2002. Unpub lished report, Programa das Naes Unidas para o Desen volvimento PNUD Projeto BRA/00/004, technical co operation with PLANAFLORO, Porto Velho/RO. Messias, M. R. 2004. Diagnstico Ambiental da rea de Inuncia Direta dos AHEs de Jirau e Santo Antnio considerando-se mamferos de mdio e grande porte como grupo indicador. Unpublished report., Furnas Centrais Eltricas S.A. Napier, P. H. 1976. Catalogue of Primates in the British Museum (Natural History), Part 1: Families Callitrichidae and Cebidae. British Museum (Natural History), London. Rylands, A. B., Coimbra-Filho, A. F. and Mittermeier, R. A. 1993. Systematics, distributions and some notes on the conservation status of the Callitrichidae. In: Mar mosets and Tamarins: Systematics, Behaviour and Ecology A.B. Rylands (ed.), pp.11. Oxford University Press, Oxford. Roosmalen, M. G. M. van and T. van Roosmalen. 1997. An Eastern Extension of the Geographical Range of the Pygmy Marmoset, Cebuella pygmaea Neotrop. Primates 5(1), pp: 3. OBSERVATIONS OF A FIGHT BETWEEN TWO ADULT MALE MANTLED HOWLER MONKEYS ( ALOUATTA PALLIATA ) Christopher Meyer Orrey P. Young Introduction e mantled howler monkey ( Alouatta palliatta ), in the initial studies by Carpenter (1934), was considered to have very low social interaction rates and very rare aggressive behaviors. Forty years later, Klein (1974) was still able to claim that howlers exhibited the lowest levels of conspecic aggression among social primates. More recently, reports of male-male ghts (Glander, 1992) and chases (Young, 1981), female-female ghts (Zucker & Clarke, 1998), male-female ghts leading to death of the female (MendezCarvajal et al., 2005), and infanticide by males (Clarke, 1983), have changed that perception. e actual observa tion of these aggressive interactions, however, continues to be a rare event, and has led to various indirect measures documenting aggression, such as bodily injuries of live animals in the eld (Cristobal-Azkarate et al., 2004) and skeletal pathologies of collected skulls from one location (DeGusta & Milton, 1998). Considering just potential aggressive interactions between males, individuals within the same troop may ght over access to an estrous female (Jones, 1980), or a solitary male may ght the alpha male of a troop either for control of the troop (Glander, 1992) or just to become a troop member (Estrada, 1982). If the relationship of the two males had been father-son, there probably would not have been a ght, with the displaced father either leaving or becoming a subordinate (Glander, 1992). Numerous observers have in dicated the take-over of mantled howler troops by solitary males (e.g. Young, 1982). Only one publication, involving
32 a long-term study, indicates that a possible take-over ght was actually seen (3 times); unfortunately, descriptions of the actual ghts were not included (Glander, 1992). Shortterm observations, obtained due merely to chance, can sometimes provide records of rarely-occurring behavior not typically documented in long-term observations. An exam ple of such a phenomenon is the following observations of a ght between two male mantled howler monkeys. Observations On 15 March 2002 on the west side of the Osa Peninsula of Costa Rica, at Drake Bay in the vicinity of the Punta Rio Clara Wildlife Refuge, a group of howlers were at a beach area with low forest canopy (height 25 ft) com posed of the trees Manchineel ( Hippomane mancinella ) and Beach Almond ( Terminalia catappa ). Observations began 0900 h, with clear skies. e howler group was composed of 12 individuals (3 males, 6 females, 1 juvenile, 2 infants) spread out amongst several adjacent trees. All was quiet for the rst hour of observation with no obvious feeding by adults and immatures. e two infants were active and separated from adults, with several adults grooming them selves or adjacent animals. At about 1000 h, an adult male (henceforth A), at the periphery of the group and adjacent to several females, began howling and making other vocal izations, began jumping from one branch to another, and in general seemed quite agitated. After several minutes of this activity, another adult male in the group (henceforth B), slightly smaller and in apparent prime condition, also became agitated. is male had been quietly reposing well within the group area, adjacent to other members of both sexes. Male B began jumping and running from limb to limb, circling male A while continuing to vocalize. Male A stayed in place but kept moving so as to continually face male B. Actual physical contact was initiated by male B, with subsequent screaming, yipping, wrestling, and biting, with blood becoming visible on both monkeys. About 20 seconds after the initial contact, both monkeys fell together approximately 20 ft to the ground. Within an approxi mately 6m 2 area, the two male monkeys continued vocal izing and ghting, with blood now visible on the sand as well as on bodies. e ghting involved standing upright on the rear legs and grabbing and biting of face, neck, back, arms, and legs, (but not tails); close face-to-face contact with associated body punching and scratching; all of which continued for approximately 90 seconds. Finally male B began chasing male A on the ground; when male A went up into a tree, male B followed, but when male A contin ued into an adjacent tree, male B did not follow. Male A continued moving through the trees, away from male B, until out of sight of the observers. Male B stayed quietly in the tree for about 10 minutes, then moved back to the trees where the other group members resided. ere were no obvious sounds or movements of group members when male B arrived. All members remained quiet and inactive for the next hour, when the observations were terminated. In departing the area, the observers searched for male A in the direction that it had ed, but it was not detected. When the ghting began, the 2 infants of the group had quickly moved to adjacent adult females. e group members then vacated the tree in which the ght was occurring, moved to the surrounding trees, and faced the combat area. Discussion One of several unusual aspects of these observations is that both males appeared to be within the group structure group initially quiet, the two males resting close to other group members and within the apparent borders of the spread-out group suggesting that neither male was a solitary male trying to gain access to the troop and that both may actually have been resident males. ere did not appear to be an estrous female being guarded by either male, which if that had been the case, could have led to a ght (Jones, 1980). e ght also suggests that their re lationship was not of father-son. Male A was the slightly larger monkey, but male B was in prime condition (no ob vious scars or other damage or deformities) with a shiny coat and quite vigorous, whereas male A had several neck and facial scars, a dull coat, and seemed to be less vigorous. e very placid response of the other members of the group to the ght was also not anticipated, the minimal response suggesting that the ght was something that was expected by group members or at least was not unusual and was not something that should have led to group agitation. e two most probable alternative interpretations of these observations are as follows: 1) Male A was the alpha male of the group, male B was a subordinate male within the group (both males had all white and fully descended scrotums) who successfully changed his position in the dominance hierar chy by defeating and chasing the alpha male from the group. e fact that male A was the rst to become agitated (issuing a challenge?) suggests that there was some tension between these monkeys, and that as alpha male he was looking for a resolution, for him the removal of B from the group. Being the larger male, with some probable battle scars, would not be unusual for an alpha male (Carpenter, 1934), or, 2) Male B was the alpha male of the group, defending successfully his position from the attack by the subordinate male A. e fact that male B initiated the physical contact indicates that he was willing to actually ght, rather than merely postur ing. His prime physical condition suggests that he had been well fed and cared for, also not unusual for an alpha male (Carpenter, 1934). Additional factors that seem to favor this interpretation of male B as the alpha male include his be havior once male A became agitated. Male B was the sub sequent aggressor, circling male A before nally attacking, suggesting willingness for physical combat expected from an alpha male defending his status. A subordinate male would likely attempt to intimidate an alpha male by threatening behaviors but be less likely to actually ght, given that in general the possessor of resources is usually successful in de fending those resources (e.g. Silk, 1987). Perhaps the most signicant indication that male B was the initial alpha male
33 was the apparent lack of response of the group to his victory. If the subordinate male A had been the victor, immediate and considerable activity of the other group members would have been expected, particularly from the females (Young, pers. obs.). Unfortunately, it was not possible to obtain observations of this group on the days immediately before or after the ght, observations that could have indicated the previous relationship of these two males and the subsequent fate of the defeated male and the group infants. Acknowledgments A discussion with K. E. Glander was particularly important in interpreting the observations and is greatly appreciated. Christopher Meyer Avenida cinco, calle cinco, San Jos, Costa Rica and Orrey P. Young 9496 Good Lion Rd, Co lumbia, MD 21045, E-mail: < email@example.com > References Carpenter, C. R. 1934. A eld study of the behavior and social relations of howling monkeys. Comp. Psychol. Monogr 10: 1. Clarke, M. R. 1983. Infant-killing and infant disappear ance following male takeovers in a group of free-ranging howling monkeys ( Alouatta palliatta ) in Costa Rica. Am. J. Primatol 5: 241-247. Cristobal-Azkarate, J., Dias, P. A. D., and Vea, J. J. 2004. Causes of intraspecic aggression in Alouatta palliatta mexicana : evidence from injuries, demography, and habi tat. Int. J. Primatol 25: 939. DeGusta, D., and Milton, K. 1998. Skeletal pathologies in a population of Alouatta palliatta : behavioral, ecologi cal, and evolutionary implications Int. J. Primatol 19: 615. Estrada, A. 1982. Survey and census of howler monkeys ( Alouatta palliatta ) in the rainforest of Los Tuxtlas, Ve racruz, Mexico. Am. J. Primatol 2: 363. Glander, K. E. 1992. Dispersal patterns in Costa Rican mantled howling monkeys. Int. J. Primatol 13: 415. Jones, C. B. 1980. e functions of status in the mantled howler monkey, Alouatta palliatta Grey: intraspecic competition for group membership in a folivorous neo tropical primate. Primates 21: 389. Klein, L. L. 1974. Agonistic behavior in neotropical pri mates. In: Primate aggression, territoriality, and xenopho bia R. L. Holloway (ed.), pp. 77. Academic Press, New York. Mendez-Carvajal, P. G., Santamaria, M., and Moreno, R. A. 2005. An observation of agonistic behavior in howler monkeys ( Alouatta palliata ) on Barro Colorado Island, Panama. Neotrop. Primates 13: 30. Silk, J. B. 1987. Social behavior in evolutionary per spective. In: Primate societies B. B. Smuts et al. (eds.), pp. 318. University of Chicago Press, Chicago. Young, O. P. 1981. Chasing behavior between males within a howler monkey troop. Primates 22: 424. Young, O. P. 1982. Tree-rubbing behavior of a solitary male howler monkey. Primates 23: 303. Zucker, E. L. and Clarke, M. R. 1998. Agonistic and ali ative relationships of adult female howlers ( Alouatta pal liatta ) in Costa Rica over a 4-year period. Int. J. Primatol 19:433. R P rf BOOKS Behavioral Flexibility in Primates: Causes and Consequenc es (Developments in Primatology: Progress and Prospects), by Clara B. Jones. 2011. Springer. 208pp. ISBN: 978 1441936028. With numerous gures, illustrations, and tables; this book emphasizes upon both behavioral and cognitive mechanisms, conceptually unifying primatology and the other evolutionary sciences, developing novel per spectives, and integrating new literature and concepts into primatology. Contents: 1. Introduction to intraindividual variation of primate behavior; 2. e costs and benets of behavioral exibility to inclusive tness: dispersal as an option in heterogeneous regimes; 3. Primate signatures and behavioral exibility in heterogeneous regimes; 4. Social cognition and behavioral exibility: categorical decisionmaking as a primate signature; 5. Female primates as ener gy-maximizers in heterogeneous regimes; 6. Male primates time-minimizers in heterogeneous regimes; 7. Intersexual interactions in heterogeneous regimes: potential eects of antagonistic coevolution in primate groups; 8. Sociosexual organization and the expression of behavioral exibility; 9. Behavioral exibility: interpretations and prospects. Primate Biogeography: Progress and Prospects (Developments in Primatology: Progress and Prospects), edited by S. M. Lehman & J. G. Fleagle. 2010. Springer. 546pp. ISBN: 978. is book highlights the many fac tors that may inuence the distribution of primates, and reveals the wide range of approaches that are available to understanding the distribution of this order. e bioge ography of primates in the past is a major component of our understanding of their evolutionary history and is an essential component of conservation biology. Contents: 1. Biogeography and primates: A review S. M. Lehman & J. G. Fleagle; 2. Nested distribution patterns and the historical biogeography of the primates of Guyana S. M. Lehman; 3. Genetic evidence pn historical biogeography of Central American howler monkeys J. A. Ellsworth & G. A. Hoelzer; 4. Ecological biogeography of primates in Guyana S. M. Lehman, R. W. Sussman, J. PhilipsConroy & W. Prince; 5. Contrasting phylogeographic his tories of chimpanzees in Nigeria and Cameroon: A multilocus genetic analysis M. K. Gonder & T. R. Disotell;
34 6. Geographic variation in savanna baboon ( Papio) ecology and its taxonomy and evolutionary implications J. M. Kamilar; 7. Biogeography and evolution of the Cercocebus-. Mandrillus clade: Evidence from the face W. S. McGraw & J. G. Fleagle; 8. Lemur biogeography J. U. Ganzhorn, S. M. Goodman, S. Nash & U. almann; 9. Mouse lemur phylogeography revises a model of ecogeographic con straint in Madagascar A. D. Yoder & K. L. Heckman; 10. Abiotic and biotic factors as predictors of species rich ness on Madagascar N. J. Stevens & P. M. OConnor; 11. e geography of mammals and rivers in mainland southeast Asia E. Meijaard & C. P. Groves; 12. Primate biogeography and ecology on the Sunda Shelf Islands: A paleontological and zooarcheological perspective T. Har rison, J. Krigbaum & J. Manser; 13. e Biogeography on primate evolution: e role of the plate tectonics, climate and chance J. G. Fleagle & C. C. Gilbert; 14. Biogeo graphic origins of primate higher taxa C. P. Heesy, N. J. Stevens & K. E. Samonds; 15. Mammalian biogeography and anthropoid origins K. C. Beard; 16. Continental pa leobiogeography as phylogenetic evidence J. B. Rosie & E. R. Seiert. Conservation Refugees: e Hundred-Year Conict between Global Conservation and Native Peoples, by M. Dowie. 2011. e MIT Press. 371pp. ISBN: 978-0262516006. is book describes how native peoples have been displaced from their lands in the name of nature conservation. It also discusses issues as diering denitions of nature and wilderness, the need for Western scientists to respect and honor traditional lifeways, and the need for native peoples to blend their traditional knowledge with the knowledge of modern ecology. ARTICLES Addessi E, Mancini A, Crescimbene L, Visalberghi E. 2011. How social context, token value, and time course aect token exchange in capuchin monkeys ( Cebus apella ). Int. J. Primatol. 32(1):83. Anzures-Dadda A, Andersen E, Martinez ML, Manson RH. 2011. Absence of howlers ( Alouatta palliata ) inuences tree seedling densities in tropical rain forest fragments in southern Mexico. Int. J. Primatol. 32(3):634. Bezerra BM, Barnett AA, Souto A, Jones G. 2011. Etho gram and natural history of golden-backed uakaris ( Ca cajao melanocephalus ). Int. J. Primatol. 32(1):46. Birnie AK, Smith AS, Nali C, French JA. 2011. Social and developmental inuences on urinary androgen levels in young male white-faced marmosets ( Callithrix georoyi ) Am. J. Primatol. 73(4):378. Bunce JA, Isbell LA, Neitz M, Bonci D, Surridge AK, Jacobs GH, Smith DG. 2011. Characterization of opsin gene alleles aecting color vision in a wild population of titi monkeys ( Callicebus brunneus ). Am. J. Primatol. 73(2):189. Chaves OM, Stoner KE, Arroyo-Rodrguez V, Estrada A. 2011. Eectiveness of spider monkeys ( Ateles georoyi vellerosus ) as seed dispersers in continuous and frag mented rain forests in southern Mexico. Int. J. Primatol. 32(1):177. Culot L, Lledo-Ferrer Y, Hoelscher O, Muoz-Lazo FJJ, Claude-Huynen M. 2011. Reproductive failure, possible maternal infanticide, and cannibalism in wild moustached tamarins, Saguinus mystax. Primates 52(2):179. De Mello F, Gifalli-Lughetti C, Priszkulnik C, Harris EE. 2011. Coalescent analysis of mtDNA indicates Pleisto cene divergence among three species of howler monkey ( Alouatta spp.) and population subdivision within the At lantic Coastal Forest species, A. guariba. Primates 52(1): 77. Dias PAD, Rangel-Negrin A, Canales-Espinosa D. 2011. Eects of lactation on the time-budgets and foraging patterns of female black howlers ( Alouatta pigra ). Am. J. Phys. Antrhopol. 145(1):137. Duarte MHL, Young RJ. 2011. Sleeping site selection by urban marmosets ( Callithrix penicillata ) under condi tions of exceptionally high predator density. Int. J. Pri matol. 32(2):329. Hopkins ME. 2011. Mantled howler ( Alouatta palliata ) arboreal pathway networks: relative impacts of re source availability and forest structure. Int. J. Primatol. 32(1):238. Jackson CP. 2011. e positional behavior of pygmy mar mosets ( Cebuella pygmaea ) in northwestern Bolivia. Pri mates 52(2):171. Juarez CP, Rotundo MA, Berg W, Fernandez-Duque E. 2011. Costs and benets of radio-collaring on the be havior, demography, and conservation of owl monkeys ( Aotus azarai ) in Formosa, Argentina. Int. J. Primatol. 32(1):69. Kowalewski MM, Salzer JS, Deutsch JC, Rao M, Kuhlen schimdt MS, Gillespie TR. 2011. Black and gold howler monkeys ( Alouatta caraya ) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of humanprimate contact. Am. J. Primatol. 73(1):75. Kugelmeier T, Rio do Valle R, de Barros MA, Pereira JA, Barros-Monteiro FO. 2011. Tracking the ovarian cycle in black-and-gold howlers ( Alouatta caraya ) by measur ing fecal steroids and observing vaginal bleeding. Int. J. Primatol. 32(3):605. Larson SG, Demes B. 2011. Weight support distribution during quadrupedal walking in Ateles and Cebus. Am. J. Phys. Anthropol. 144(4):633. Link A, Galvis N, Fleming E, Di Fiore A. 2011. Patterns of mineral lick visitation by spider monkeys and howler monkeys in Amazonia: are licks perceived as risky areas? Am. J. Primatol. 73 (4):386. Link A, de Luna AG, Arango R, Diaz M C. 2011. Ge ophagy in Brown Spider Monkeys ( Ateles hybridus ) in a Lowland Tropical Rainforest in Colombia. Folia Prima tol 83(1):25.
35 Long CT, Pacharinsak C, Jampachaisri K, McKeon GP,Howard AM, Albertelli MA, Felt SA. 2011. Compar ison of rectal and tympanic core body temperature mea surement in adult Guyanese squirrel monkeys ( Saimiri sciureus sciureus ). J. Med. Prim. 40(2):135. Matauschek C, Roos C, Heymann EW. 2011. Mitochon drial phylogeny of tamarins ( Saguinus Homannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. Am. J. Phys. Anthropol. 144(4): 564. McKinney T. 2011. e eects of provisioning and cropraiding on the diet and foraging activities of human-com mensal white-faced Capuchins ( Cebus capucinus ). Am. J. Primatol. 73(5):439. Mller T, Hupfeld T, Roessler J, Simoni M, Gromoll J, Behr R. 2011. Molecular cloning and functional char acterization of endogenous recombinant common mar moset monkey ( Callithrix jacchus ) follicle-stimulating hormone. J. Med. Prim. 40(2):111. Muoz-Lazo FJJ, Culot L, Huynen MC, Heymann EW. 2011. Eect of resting patterns of tamarins ( Saguinus fuscicollis and Saguinus mystax ) on the spatial distribu tion of seeds and seedling recruitment. Int. J. Primatol. 32(1):223. Nascimento ATA, Schmidlin LAJ. 2011. Habitat selection by, and carrying capacity for, the Critically Endangered black-faced lion tamarin Leontopithecus caissara (Pri mates: Callitrichidae). Oryx 45(2): 288. Palminteri S, Powell G, Endo W, Kirby C, Yu D, Peres CA. 2011. Usefulness of species range polygons for predict ing local primate occurrences in southeastern Peru. Am. J. Primatol. 73(1):53. Peck M, orn J, Mariscal A, Baird A, Tirira D. 2011. Fo cusing conservation eorts for the critically endangered brown-headed spider monkey ( Ateles fusciceps ) using remote sensing, modeling, and playback survey methods. Int. J. Primatol. 32(1):134. Pele M, Micheletta J, Uhlrich P, ierry B, Dufour V. 2011. Delay maintenance in Tonkean macaques ( macaca tonkeana ) and brown capuchin monkeys ( Cebus apella ). Int. J. Primatol. 32(1):149. Pena HFJ, Marvulo MFV, Horta MC, Silva MA, Silva JCR, Siqueira DB, Lima PACP, Vitaliano SN, Gennari SM. 2011. Isolation and genetic characterisation of Toxo plasma gondii from a red-handed howler monkey ( Al ouatta belzebul ), a jaguarundi ( Puma yagouaroundi ), and a black-eared opossum ( Didelphis aurita ) from Brazil. Vet. Parasitol. 175:377. Pozo-Montuy G, Serio-Silva JC, Bonilla-Sanchez YM. 2011. Inuence of the landscape matrix on the abun dance of arboreal primates in fragmented landscapes. Pri mates 52(2): 139. Rylands AB, Matauschek C, Aquino R, Encarnacion F, Heymann EW, de la Torre S, Mittermeier RA. 2011. e range of the golden-mantle tamarin, Saguinus tripartitus (Milne Edwards, 1878): distributions and sympatry of four tamarin species in Colombia, Ecuador, and northern Peru. Primates 52(1): 25. Saito A, Izumi A, Nakamura K. 2011. Development of infant common marmosets ( Callithrix jacchus ) prefer ence for their parents over adults from another group. Primates 52(1): 43. Santos SV, Strefezzi RDF, Pissinatti A, Catao-Dias JL. 2011. Liver iron overloading in captive muriquis ( Brachyteles spp.). J. Med. Prim. 40(2):129. Shanee S. 2011. Distribution survey and threat assessment of the yellow-tailed woolly monkey ( Oreonax avicauda ; Humboldt 1812), northeastern Peru. Int. J. Primatol. 32(3):691. Smith TD, Rossie JB, Cooper GM, Schmieg RM, Bonar CJ, Mooney MP, Siegel MI. 2011. Comparative mi crocomputed tomography and histological study of maxillary pneumatization in four species of new world monkeys: the perinatal period. Am. J. Phys. Anthropol. 144(3):392. Souza-Alves JP, Fontes IP, Ferrari SF. 2011. Use of sleeping sites by a titi group ( Callicebus coimbrai ) in the Brazilian Atlantic Forest. Primates 52(2):155. Takeshita RSC, Monteiro FOB, de Miranda FL, da Silva GA, Faturi C, Coutinho LN, Monteiro MVB, Kugelmei er T, Castro PHG, Muniz JAPC. 2011. Hematological, hepatic, and renal evaluation in Aotus azarai infulatus. J. Med. Prim. 40(2):104. Vogel ER, Janson CH. 2011. Quantifying primate food distribution and abundance for socioecological studies: an objective consumer-centered method. Int. J. Primatol. 32(3):737. Wimsatt A, Withrow SJ, Danner D, Powers B, Hagler T, Pritzker KPH. 2011. Multicystic bone disease (Gorham Stout Syndrome) in a spider monkey ( Ateles georoyi ). J. Med. Prim. 40(2):61. 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):607. ABSTRACTS Selected abstracts of oral presentations relating with neo tropical primates from the 80 th Meeting of the American Association of Physical Anthropologists, Minneapolis, Minnesota, USA, April 12 to 16, 2011 Amato KR, Yeoman CJ, Righini N, Kent A, Estrada A, Munoz D, Stumpf RM, White B, Nelson KE, Torralba M, Gillis M, Leigh SR. 2011. Gastrointestinal microbial community composition and habitat structure in howler monkeys ( Alouatta pigra ). Arnedo LF, Ahumada JA, Boughman JW, Snowdon CT, Mendes FDC, Strier KB. 2011. Variation in vocal struc ture reects group history in primates. Babb P, Fernandez-Duque E, Schurr T. 2011. Monoga mous owl monkeys dier in the structure of OXTR from other non-monogamous primates.
36 Benitez M, Anestis S, Santos L, Brisiesca R, Beehner J. 2011. A non-invasive method for collecting salivary tes tosterone in socially-housed captive monkeys. Beznson M, Watts SM. 2011. Tree truthing: How accurate are substrate estimates in primate eld studies? Chalki J, Wright BW, Lucas PW, Richmond BG, Fragaszy D, Visalberghi E, Izar P, Ottoni EB. 2011. Feeding be haviors and food mechanics during Cebus libidinosu s ontogeny. Coleman MN, Boyer DM. 2011. e evolution of hearing sensitivity and vocal communication in primates. Clink D, Huck M, Fernandez-Duque E. 2011. Betweengroup variation in the activity patterns of cathemeral owl monkeys ( Aotus azarai ) under similar temperature and light conditions. Coles J, Hurst D. 2011. White-faced saki ( Pithecia pithe cia ) vocalizations in relation to ambient noise at Browns burg Natuurpark in Suriname. Connour JR. 2011. Comparison of Ateline limb bone bio mechanical properties. de la Cuetara JM, Fiorenza L, Bruner E. 2011. A structural approach to cranial variation in the genus Alouatta (Pri mates, Atelidae). Delson E, Ford E, Friess M, Frost SR, Harcourtsmith W. 2011.Organizing administering, and sustaining an open-access database, examples learned from PRIMO. Di Fiore A, Fernandez-Duque. 2011. Interbirth interval, age at dispersal, and sexual dimorphism in wild titis ( Cal licebus discolor ) and sakis ( Pithecia aequatorialis ). Dingess KA. 2011. Duet type description and matching in the Bolivian gray titi monkey, Callicebus donacophilus. Eadie E. 2011. Tolerated scrounging a foraging strategy for young juvenile capuchin Cebus capucinus monkeys. Evans KJE, Hartwell KS, Pavelka MSM, Notman H. 2011. e eect of infant age on infant attraction, tolerance and handling in Ateles georoyi Fernandez-Duque E, Babb P, Schurr T. 2011. Group struc ture and dispersal patterns of the socially monogamous owl monkey as revealed by mtDNA data. Gabe AK, Dingess KA. 2011. Neighbor-stranger dis crimination in the Bolivian gray titi monkey Callicebus donacophilus. Gladman JT. 2011. Linear enamel hypoplasias and the di etary adaptations of Cebus Glander KE, Vinyar CJ, Williams S. 2011. ermal im aging and iButtons: a novel use of two technologies to quantify the daily thermal proles of wild howlers ( Al ouatta palliata ) and their habitats at La Pacica, Costa Rica. Graves J, Kirk EC, Lewis RJ. 2011. Eects of social co hesion, pairbonding and monogamy on primate brain evolution. Gregory T, Norconk M. 2011. Behavioral responses to sea sonal changes in Guianan bearded sakis ( Chiropotes sagu latus ): Brownsberg Nature Park, Suriname. Hale V, Tan C, Lin TL, Wu CC. 2011. Evaluation of meth ods for preserving fecal microbial DNA from the spider monkey. Halloran AR, Milini AB, Huettmann F. 2011. Monkey census by vocalization: an eective approach. Hartwelli KS, Notman H, Pavelka MSM. 2011. Seasonal variation in sexual segregation in spider monkeys ( Ateles georoyi yucatanensis). Herrera JP, Taylor LL, Evans S. 2011. Use of auditory and olfactory signals in night monkeys ( Aotus nancymaae). Huck M, Fernandez-Duque E. 2011. Children of divorce: eects of adult replacements on survival and dispersal of young owl monkeys in the Argentinean Chaco. Ingraham J, Schreier AL. 2011. Path analysis of vocallymediated intergroup spacing strategies in mantled howl ing monkeys. Jaeggi AV, Van Schaik CP. 2011. e evolution of food sharing in primates. Jarrell H. Association between locomotor tendencies, habi tat use and skeletal trauma in nonhuman primates. Kauman L. 2011. Creating sustainable primate-based tourism: a view from the Central Suriname Nature Reserve. Klukkert ZS, Rosenberger AL. 2011. A new angle on the anterior dentition of Platyrrhines: a preliminary report. Kohn LAP. 2011. Morphological integration in Primate limb morphology. Ledogar JA, Bunn JM, Clair EST, Boyer DM. 2011. Dental topographic analysis of pitheciine (Pithecia, Chi ropotes, Cacajao) second mandibular molars. Machnicki AL, Haile-Selassie Y, Spurlock L, Mendes S, Strier KB, McCollum MA, Lovejoy C. 2011. Paral lel lumbar and pelvic morphology in Atelines and early hominids: clues to the earliest hominid adaptations to upright walking? Matthews LJ, Nun CJ. 2011. Using phylogenies and social networks to detect the modality of disease transmission in wild primate social groups. Middleton ER, Schmitt CA, Di Fiore A. 2011. Ontoge netic changes in prehensile tail use by lowland woolly monkeys (Lagothrix poeppigii) in Yasunn National Park, Ecuador. Miller CE; Schmitt D. 2011. Primate tail function: balanc ing the variables. Muchlinski MN, Paesani SM. 2011. 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37 Porter L, Garber P. 2011. Foraging and spatial memory in saddleback tamarins ( Saguinus fuscicollis ). Reever NM, Sylvester AD, Auerbach BM. 2011. Behav ioral laterality and skeletal directional asymmetry in cot tontop tamarins. Russo G, Young JW, Matthews LJ. 2011. Ontogeny of caudal vertebral structure in capuchin monkeys ( Cebus albifrons and C. apella ). Rutherford J, Ross C, Tardi S. 2011. Energetics and life history plasticity in Callitrichine primates: a view within and across generations. Scarry CJ. 2011. Experimental analyses of intergroup en counters among tufted capuchin monkeys: eects of re source quality and female sexual behavior. Shaer C. 2011. Diet and ranging behavior of bearded sakis ( Chiropotes sagulatus ) in the Upper Essequibo Con servation Concession, Guyana. Smith TD, Garrett EC, Bhatnagar KP, Bonar CJ, Bruening AE, Dennis JC, Morrison EE. 2011. New ndings on the vomeronasal complex of Platyrrhine primates. Snowdon CT, de la Torre S. 2011. Adaptations to noisy environments: structure and usage of acoustic signals in Callitrichid primates. Spence-Aizenberg A, Di Fiore A, Fernandez-Duque E. 2011. Pairbonded adult titi monkeys of Ecuador ( Cal licebus discolor ) change their aliative relationships in the presence of infants. Strier KB, Chaves PB, Mendes S, Fagundes V, Di Fiore A. 2011. Molecular paternity analyses conrm inbreeding avoidance and low reproductive skew in the northern muriqui, Brachyteles hypoxanthus. Suarez SA, Karro J, Kiper J, Farler D, McElroy B, Stockwell B, Young T. 2011. e use of a repeated-route system im proves foraging eciency in simulated spider monkeys. ompson CL, Norconk M. 2011. Social bonds in wild white-faced saki monkeys reect male/female pair prefer ence, despite lacking behavior and physical traits typical of primate monogamy. Tujague MP, Scarry CJ. 2011. Consequences of changing numerical asymmetries on intergroup relations among tufted capuchins: a case study. Valencia LN, Link A, Di Fiore A. 2011. Phylogeography of brown spider monkeys ( Ateles hybridus ) in Colombia: testing the riverine hypothesis. Westin JL, Kauman L. 2011. Tourism in Suriname: do monkeys view tourists as predators or conspecics? Zichello J, Steiper M. 2011. Comparison of intraspecic genetic and morphological diversity among primate s. Mt 2011 Joint Meeting opf the International Ethological Confer ence and the Animal Behavior Society e International Ethological Conference and the Animal Behavior Society will have a joint meeting this year at the Indiana University, Bloomington, Indiana, USA, from July 25, 2011. For more information and registration go to: http://www.indiana.edu /~behav11 45th Congress of the International Society for Applied Ethology e 45 th congress of the International Society for Applied Ethology will take place in Indianapolis, USA, from July 31 to August 4, 2011. e general theme will be Scien tic evaluation of behavior, welfare and enrichment; and some of the specic topics: Zoo animal behavior, Labora tory animal behavior, Engineering environments & mea surement technologies for science and welfare Pain, distress & humane end-points. Abstract submission closes Febru ary 14 th For more information visit http://www.appliedethology.org/isaemeetings.htm 34th Meeting of the American Society of Primatologists e meeting of the American Society of Primatologist will be held in Austin, Texas, USA, fro, August 13, 2011. Preliminary abstracts for symposia and workshops should be submitted by January 15, 2011. General abstracts dead line March 12, 2011. For more information go to http:// www.asp.org/asp2011/index.htm Simposio La Primatologa en el Per La Fundacin Yunkawasi organiza el Simposio La Prima tologa en el Per: Historia, Estado Actual y Perspectivas, el cual se llevar a cabo en Lima del 17 22 de Octubre de 2011. Para ms informacin consulte http://www.yunka wasiperu.org/evento-primates.html 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 12, 2012. For more in formation visit http://www.ips2012.org.mx /
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:
Neotropical Primates A Journal and Newsletter of the IUCN/SSC Primate Specialist Group Vol. 18(1), June 2011ContentsArticlesSearching for Alouatta palliata in Northern Colombia: Considerations for the Species Detection, Monitoring and Conservation in the Dry Forests of Bolvar, Colombia Andrea Dechner . ................................................................................................................................................................................. 1 Densidade e Tamanho Populacional de Primatas em uma rea De Terra Firme Na Amaznia Central Lilian Figueiredo Rodrigues e Marcelo Derzi Vidal . .............................................................................................................................. 9 Population Density of Black-Faced Lion Tamarin (Leontopithecus caissara) Alexandre T. Amaral Nascimento, Fabiana Prado, Claudio B. Valladares-Padua and Paulo de Marco Jnior . ........................................ 17Short ArticlesMale Care in Mantled Howler Monkeys (Alouatta palliata palliata) Eugenia Zandon . ............................................................................................................................................................................ 22 A Preliminary Study of the Genetic Diversity of Pygmy Marmoset Callithrix pygmaea (Primates: Cebidae: Callithrichinae) Using Short Sequence Repeats (SSR) Diego Alejandro Nieto Monteros, Stella de la Torre, Venancio Arahana, Mara de Lourdes Torres and Ana Mara Troya Zuleta . .............. 25 Reactions of White-Bellied Spider Monkeys to a Predation Attempt by a Cougar talo Mourth . .................................................................................................................................................................................. 28 Southern Extension of the Geo graphical Range of the P ygmy Marmoset Cebuella pygmaea niveiventris (Lnnberg, 1940) in the Southwestern Amazon Basin, State of Rondnia, Brazil Mariluce Rezende Messias, Juliano Tupan Coragem, Ivonete Santa Rosa Gomes, Marcela Alvares Oliveira, Paulo Henrique Bonavigo Samuel dos Santos Nienow and Eduardo Santos de Souza . .......................................................................... 30 Observations of a Fight Between Two Adult Male Mantled Howler Monkeys (Alouatta palliata) Christopher Meyer and Orrey P. Young . .............................................................................................................................................. 31Recent Publications . ................................................................................................................................................ 33 Meetings . ................................................................................................................................................................ 37
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