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NEOTROPICAL PRIMATES rfnnftbnfbrfn bfntnbbft n n nnn Editorsbb bbffb bbn n nbr bnb News and Book Reviewsn nfnPSG ChairmannbffnnbnPSG Deputy Chairmanf SPECIES SURVIVAL COMMISSION
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 Washington State University, Pullman, WA, 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 Ernesto Rodriguez Lunapt-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
37 THE CONSERVATION STATUS OF enCALLICEBUS CAQUETENSISen (PITHECIIDAE): A NEW SPECIES en IN SOUTHERN CAQUET DEPARTMENT, COLOMBIAenJavier Garcaen1,2en, Thomas R. Defleren2en, Marta L. Buenoen2en1enFundacin Herencia Natural, Bogot D. C., Colombiaen2enDepartamento de Biologa, Universidad Nacional de Colombia, Bogot D. C., ColombiaAbstractMoynihan (1976) mentioned an undescribed species of Callicebus between the ros Caquet and Orteguaza, Caquet Department, Colombia. In August 2008, we conrmed the new species, which is phylogenetically related to C. ornatus and C discolor to the north and south of the type locality respectively. We described this species as Callicebus caquetensis Deer et al., 2010 establishing its distribution through direct observations and information from local communities. Eighty-two animals were seen, including the holotype and paratype, which were collected. A review of historical archives of aerial pho tographs and satellite maps was carried out to assess the loss of the original vegetation of the area, and we found the habitat in an advanced state of fragmentation caused by extensive ranching and illegal crop cultivation. Existing coverage is now limited to small fragments of the original primary forest and secondary vegetation. We analyzed a Google Earth image of 75 km2 of this primates habitat and found only 32% of forest and secondary forest vegetation remaining in 2002, the year the image was captured. We propose this Colombian endemic species should be considered as Critically Endangered (CR), (based upon the criteria A3c,d,e, C2 of the IUCN). We suggest that the Colombian and Caquet governments and private individuals give special attention to this endemic primate, most importantly in the creation of reserves and in environmental education initiatives. is is probably the most endangered of Colombias primates. Key words: Callicebus caquetensis, endangered primates, endemics, ColombiaResumenes-ESMartin Moynihan (1976) fue el primero en mencionar la existencia de una nueva especie de es-ES Callicebuses-ES en el Departamento es-ES del Caquet, Colombia. En Agosto del 2008 conrmamos la presencia de esta nueva especie, relacionada logenticamenes-ES -es-ES te con es-ESCallicebus ornatuses-ES yes-ES Callicebus discolores-ES al norte y al sur de su localidad tipo (entre los ros Orteguaza y Caquet) y es-ES describimos la especie como es-ES Callicebus caquetensises-ES Deer es-ES et ales-ES., 2010. La distribucin de la especie fue establecida a travs es-ES de entrevistas con la comunidad local y observaciones directas. Un total de 82 animales fueron observados, incluyendo el es-ES holotipo y el paratipo que fueron colectados. Una revisin histrica de fotografas areas y mapas satelitales fue llevada a es-ES cabo para evaluar la disminucin de la cobertura vegetal original en el rea; encontramos el hbitat en un avanzado estado de es-ES fragmentacin causado por la ganadera extensiva y cultivos ilcitos. La cobertura existente esta relegada a pequeos bosques es-ES primarios y vegetacin secundaria. Analizamos imgenes de Google Earth de 100 kmes-ES2es-ES del hbitat de este primate y encontraes-ES -es-ES mos solo 32% de bosque original y bosque secundario en el 2002, ao de captura de la imagen. Proponemos que esta especie es-ES debe ser considerada como Crticamente Amenazada (CR), (basados en los criterios A3c,d,e,C2 de la UICN). Sugerimos es-ES al gobierno nacional y del Caquet que presten especial atencin a este primate endmico, estabilizando reservas en la zona, es-ES estableciendo programas de ganadera sostenible, proyectos REDD y un programa de educacin ambiental regional. Esta es es-ES probablemente la especie de primate ms amenazada de Colombia. Palabras Claves: Callicebus caquetensis, primates amenazados, endmico, Colombia. A
38 IntroductionIn 2010, we described a new species of titi monkey, Callicebus caquetensis Deer et al., 2010, from southern Caquet Department, Colombia. To date it has been found only in forest patches on agricultural land that has been estab lished in the region over past 5060 years. is primate was mentioned by Moynihan (1976) from his travels in the piedmont of Colombia in 1969, although Hershkovitz (1990) made no mention of it. In 2008, the rst author, a native of Caquet, agreed to attempt eld work where the titi monkey had been rst observed by Moynihan (1976). e completely fragmented state of the forest was known to us from satellite images. An analysis of Colombian Amazonian forest cover by Deer (1992) indicated that about 70% of the forest had been lost in southern Caquet by 1985. A further analysis was carried out with satellite images available to us from 2003. Caquet is one of the principal colonization fronts in the Colombian Amazon, and in 1985 it was considered to be the Amazonian depart ment that had suered the most forest loss, with only about 29.4% left, and 79.6% under varying stages of conversion (Deer, 1992). An assessment of the status of this species was evidently a matter of urgency. Field work in the area was made dicult by the fact that for past 50 years or so, the area where Moynihan (1976) described this primate has been a continual zone of conict, with the presence of various insurgent groups on both ends of the political spectrum. Data collection in this region demanded careful preparation for all forays into the coun tryside, involving prior conversations with all possible con tacts about the advisability of working in particular zones, and by carefully following the advice given. Despite this, it remained impossible to survey one of the most promising forest fragments for a possible reserve (described below). Field work was facilitated by the fact that the rst author was a native of the nearby capital of Caquet Department, Florencia, and was able to establish some local contacts through his family. Cattle-raising and illicit cultivars are the main agricultural activities in the region. While cattle-raising has been supported in the past by the Colombian government and by the World Bank (Andrade & Ruiz, 1988), in the last three decades ocial support for colonization and cattle ranch ing has been reduced (Myers, 1980; Repblica de Colom bia, 1982; Jimeno, 1987; Jaramillo et al., 1989).Methodse rst author spent 22 days in April, 2008, 21 days in May, 2008 and 39 days in JuneJuly 2010 for a total of 82 days of eld work (Garca, 2008, 2010; Garca & Deer, 2009). Garcas eld work involved contacting landowners using his family contacts to visit farms where small, forest patches remained. It is necessary to be connected to, and vouched for by, locals to guarantee personal security in this part of Colombia. e local people are very mistrustful of strangers. e study began at the village of Valparaso, Ca quet, where Moynihan rst observed the monkeys in 1969. In the 2010 survey, Garca concentrated on the region to the west of the previous observations of 2008 and 2009, as well as the municipalities ( municipios) of Albania, San Jos del Fragua and Curillo (see Garca, 2008; Garca & Deer, 2009 for details; in Colombia a municipio is more compa rable to a county and often contains several dierent towns or cities; the term is not limited to one town as in the United States). Six additional groups were located (Fig. 1). Google Earth allowed an overall view of the study area; it depicts the region using two dierent scales or resolutions for southern Caquet. A baseline resolution of 15 m was used for the majority of the area, but it is not a scale easily analyzed for fragment sizes. A smaller percentage of area is depicted in a ner-grained resolution of 1 m, allowing analysis of forest condition and fragment area. Using a ner resolution, in an area centered around the coordinates 1'27.8"N, 75'57.6"W, 220 m altitude, we analyzed an image captured on 30 November, 2003 (10.7 km 7.5 km or 75 km, and the latest image available to us) for the extent of fragmentation. With the results of the eld work, and using the Google images, we identied six pos sible reserves for C. caquetensis.Results and DiscussionDuring the 82 days of surveys, we detected 82 (includ ing the holotype and paratype) animals with an average of four animals per group. Table 1 shows the breakdown per group for the 13 groups found, and the coordinates of where they were seen. e animals were detected at an alti tudinal range of 190270 m. Figure 1 shows the locations of the sightings made during 2008, 2009, and 2010. e point on the map marked Callicebus torquatus identies a sighting of a C. torquatus group, suggesting that originally, when the forest was intact, C. torquatus and C. caquetensis were sympatric. All observations were made in forest fragments, some of which were severely degraded. Moynihan (1976) reported seeing a group in a medium-sized patch of vegetation mostly less than 7 m in height, and he made a number of observations from low second growth forest, except for land between a broad river on one side and patches of bamboo and abandoned crop elds on the other (p.76). We delineated a square of land (Fig. 2) from the most re cently available Google World image (30 November, 2003) of 11 km 7.5 km (75 km) and calculated the percentage of remaining forest there. Existing Callicebus habitat was in the form of fragments and tree-lined streams, and rep resented about 32% of the total area (about 26.4 km of the total area) (1'45.74"N, 75'37.28"W, center of the rectangle) of vegetation that could sustain Callicebus at that time.
39 Figure 3 shows a group of interconnected fragments on the William Cuartas farm (1'17.9"N, 75'28.5"W) totaling about 2.5 km of forest. Only one group of C caquetensis was found there, even though this large fragment could evidently harbor more, since groups of the closely re lated C. ornatus have been observed in territories of 3.29 ha, 4.18 ha, and 3.5 ha in gallery forests in Meta and 14.2 ha in closed canopy forest (Deer, 2004; Mason, 1965, 1966). Robinson (1977) estimated densities for C. ornatus at about 5 individuals/km, which would suggest that this fragment could hold at least 12.5 animals (34 groups) of C. caquetensis. Although there are no large blocks of forest in the area con rmed as the range of C. caquetensis, there are still possibili ties for small reserves for this species and we suggest several here. An advantage of declaring several small reserves is the insurance against any large disaster in any one of them, since other small reserves will continue to protect the spe cies. Presuming that C. caquetensis groups defend territory similar in size to those defended by C. ornatus, we believe that a fair population could be preserved in some of the larger available fragments between the Rios Orteguaza and Caquet. Part of our future work will involve the develop ment of proposals for the establishment of biological corri dors to connect some of these reserves. Below are some sug gestions for small reserves to protect Callicebus caquetensis. 1. El Dorado ( municipio of Albania) contains Mauritia exuosa palm forests combined with gallery forest close to a school (Institucin Educativa Rural El Dorado) in El Dorado where environmental work could be carried out with the added advantage of security. e forest has easy access for the development of basic ecology or behavior projects. ese forests might provide connections to forests along the Ro Pescado, although they are Figure 1. Map of observations of Callicebus caquetensis 20082010.
40 Table 1. Size, composition and location of Callicebus caquetensis and Callicebus torquatus groups observed in 20082009. M F Subad. Juv. Inf. Total Place Coordinates 1 1 1 1 1 0 4 Nilson Barragn farm 01'38.3"N 75'00.4"W 2 1 1 0 2 1 5 Nilson Barragn farm 01'40.8"N 75'43.0"W 3 1 1 0 1 0 3 Alirio Santanilla farm 01 08'09.4"N 75'51.4"W 4 1 1 0 1 1 4 Hacienda William Cuartas 01'17.90"N 75'28.5"W 5 1 1 1 0 1 4 Resbaln Creek 01'30.4"N 75'42.8"W 6 1 1 2 0 1 5 Hacienda Moiss Cruz 01' 54.4"N 75'27.3"W 7 1 1 0 1 1 4 Fidelino Pea farm 01 07'11.0"N 75'01.1"W 8 1 1 2 1 1 6 Vereda la Florida* 01'07.92"N 75'43.86"W 9 1 1 1 0 1 4 La Solita Creek 0'57.42"N 75'15.76"W 10 1 1 1 0 0 3 La Solita Creek 0'05.2"N 75'00.6"W 11 1 1 0 0 1 3 Yaneth Soto farm 0'12.6"N 75'31.22"W 12 1 1 0 0 1 3 Doa Amparo farm 0'15.4"N 75'34.9"W 13 1 1 1 2 1 6 Edilberto Surez farm 0 54'47.8"N 75'36.3"W 14 1 1 1 1 1 5 Libardo Rojas farm 01'24.35"N 75'10.82"W 15 1 1 1 1 4 Libardo Rojas farm 01'12.27"N 75'58.80"W 16 1 1 2 Bello Diamante farm 01'13.09"N 75'5.26"W 17 1 1 1 2 LOCATION 01'06.87"N 75'1.02"W 18 1 1 1 3 Road along a creek, 4 km from Albania to Valparaiso 01'23.55"N 75'16.16"W 19 1 1 1 1 4 Forest road to Valparaiso 01'00.43"N 75'29.97"W 20 1 1 1 3 Hacienda Don Flix 01'39.84"N 75'27.34"W Total observed 80 Altitudes 190270 m Average group size 4 Holotype captured by locals LOCATION 01'24.61"N 75'34.04"W Paratype captured by locals LOCATION 01'23.10"N 75'32.5"W Callicebus torquatus group LOCATION 01'11.49"N 75'28.71"WM: Adult male F: Adult female
41 extremely fragmented. Local people conrm that C. caquetensis eats Mauritia exuosa fruits, just as has been observed for Callicebus torquatus lugens by Palacios et al. (1997) and Callicebus t. lucifer by TRD (unpubl. data). 2. Both C. torquatus and C. caquetensis occur in the for ests of Canelo Creek From the north it is easy to enter the area, although there are some security issues at this time. Canelo Creek ows into the Ro Caquet and would be important as a protective zone for that part of the river. 3. Aguas Negras Creek ( municipios of Miln and Valpara iso) is a corridor that has sizeable forests along most of its length and may serve as habitat for C. caquetensis. South of it is a small forest of 90 ha, but it is being logged and will soon be ruined, although secondary vegetation probably would be attractive for this pri mate. Access to this forest is via the Ro Orteguaza and Valparaso. 4. One of the largest fragments that probably protects C. caquetensis is immediately east of the town of La Solita. Because of local security concerns it has not yet been possible to survey the fragment to determine if the species is there, although it has been conrmed nearby to the north. is fragment, about 17 km in length and 14 km wide, lies alongside the Ro Ca quet. e species complex C. ornatus, C. caquetensis, C. discolor, and C. cupreus is particularly attracted to low-lying land alongside rivers, so the forest could be prime habitat for this small monkey (Deer, 2010). We have detected Pithecia monachus, Lagothrix lagothricha lugens, Saimiri sciureus, Saguinus nigricollis hernandezi, and Cebus apella in other, nearby fragments, and this large fragment might well protect small populations of C. caquetensis as well (Garca, 2008; Garca & Deer, 2009). e forest is probably scrubby, since lumbering in the region has long ago harvested the largest trees. Callicebus from this species group are also known to do well in scrubby and secondary vegetation, so we can surmise that this would be adequate habitat for C caquetensis (Moynihan, 1976; Deer, 1994; Van Roosmalen et al., 2002). is fragment is a prime choice for further evaluation in the future when the security situation improves. 5. Another possible r eserve for this species could be es tablished along La Solita Creek to the west of La Solita. Callicebus caquetensis has been registered there and, al though the forest is not as extensive as to the east of La Solita, there is adequate vegetation along this creek for at least 6 km, and at its mouth the vegetation (probably seasonally ooded and attractive to this titi monkey) extends to a width of 5 km. To the north C. ornatus is very common in riparian (gallery) forests or forests along creeks and this preference is probably shared with C. caquetensis. e advantage of reserves being estab lished in these two patches of large fragments is that they could be administered in part from the village of La Solita, situated between the two. 6. Other large fragments of forest still persist to the east, towards the mouth of the Ro Orteguaza, where it ows into the Ro Caquet. e largest fragment (6 km 4 km) is across the river from Tres Esquinas, the Colombian air force base Ernesto Esguerra and village, where security might be stronger due to the mil itary presence and where a reserve might be more easily protected. However, presently it is conjecture whether it contains C. caquetensis, since this part of the inter uvium of the Orteguaza and Caquet has not been surveyed. e species might be present in some other large fragments in this part of the interuvium, but the fragments have not been surveyed, and they are isolated in terms of transportation and security. Forests along the right bank of the Ro Orteguaza seem promising, since these are wide frag ments and the forest following the right bank is continuous from just below Valparaso. If this forest has not been cut Figure 2. 75-km2 quadrate analyzed for fragmentation and per cent of forest cover (Image Google Earth, 2003). Figure 3. Area around the Hacienda William Quartas (4 km 2.75 km) showing ongoing fragmentation. (Image Google Earth, 2003).
42 because it is low-lying and seasonally ooded, it is a good possibility for establishing reserves for C. caquetensis. Reynaldo Ruz (a colonist of the area) mentioned the his toric presence of C. caquetensis in the oodplain of the Ro Fragua (see Fig. 1), but it seems to be locally extinct there due to intense agricultural activities. is would be the westernmost point of its distribution and the point closest to the Cordillera de los Andes. Field work in 2010 con rmed the absence of the species west of the Ro Pescado ( veredas [= a subdivision of a municipio in Colombia], La Esperalda and Rochela, in the municipio of Morelia). We suppose that the western range extension of the species might prove to be more extensive than we have been able to demonstrate to date and this has important implications. Unfortunately the Agencia Nacional de Hidrocarburos of Colombia is planning extensive oil exploration in this western part of Colombia, but it is unclear whether such development will include safeguards for the conservation of the ora and fauna (
43 Eighty-nine percent of La Solita had been converted by 2001; 98% of the municipality of Albania. Like other species of Callicebus, from this complex, C. caquetensis seems tolerant of human activities, and habituated animals read ily move and probably disperse using very scarce vegetation or none at all. We saw a number of groups that seemed unconcerned by our presence. One animal was seen to pass over barbed wire from one patch of vegetation to another (Fig. 5). Another animal ate unconcernedly while being photographed (Fig. 6). Since primates are mostly ignored in this part of Colombia, the major pressure is forest con version, although poor, broken-up, isolated patches, bamboo thickets, dense vegetation, crowded and rela tively low forests, thickets, and tangles and secondary veg etation is sometimes used by this primate and by closely related species (Mason, 1965, 1966; Moynihan, 1976; Kinzey, 1981; Deer, 2004). We believe that alternatives need to be supported that allow for a change in the mentality in this part of Colombia so heavily given to cattle ranching. But even though the low prices of milk and meat do not support successful cattle production, the frontier mentality in rural Colombia places a high premium on this activity, just as it does in so many other nations. Part of the solution in the area between the Ros Orteguaza and Caquet must be inclusion into national strategies such as the Project Sustainable Colombian Cattle-ranching supported by the Federacin Colombi ana de Ganaderos (FEDEGAN), see
44 been evaluated in terms of its damage to arboreal fauna such as titi monkeys. Genotoxic, hormonal, and enzymatic eects of glyphosate in mammals have been reported, nev ertheless (Lioi et al., 1998; Peluso et al., 1998; Daruich et al., 2001). In rats, glyphosate has been found to decrease the activity of some detoxifying enzymes, cytochrome P-450, and monooxygenase activities and the intestinal activity of aryl hydrocarbon hydroxylase when injected into the abdomen (Hietanen et al., 1983). e fact that this primate depends on vegetation that may often be sprayed with glyphosate around coca elds means that the animals are subjected to yet another environmental assault, which has never been evaluateddie-back of a part of their habitat due to spraying, the ingestion of aected fruits, or even being directly coated by the herbicide. General poverty in southern Caquet means that any con servation eort needs to be seen to provide economic advan tages to the local communities. Socioeconomic conditions in southern Caquet are dicult, and the rural population suers from the lack of basic necessities (for example, inad equate housing with overcrowding, poor sanitation, poor structural integrity, and poor school attendance). e last national census of the Departamento Administrativo Na cional de Estadstica (DANE) (2005:
45 Acknowledgments We are grateful for the company in the eld of the biolo gists Victor Luna, Gabriel Beltrn and Juan Pablo Parra and the kind hospitality and advice of the families in this part of southern Caquet. We thank the biologist John Fredy Jimnez for help drawing the map. Without this support it would have been very dicult to gather the information included here. We are grateful to the Fondo para la Accin Ambiental y la Niez, Programa de Becas Jorge Ignacio Hernndez-Camacho Iniciativa de Especies Amenazadas of Conservacin Internacional Colombia, to the Primate Action Fund of Conservation International, to the Universidad Nacional de Colombia, Idea Wild, and the Conservation Leadership Programme for supporting the rst conservation initiatives for Callicebus caquetensis in the area. Google Earth images of southern Caquet enabled us to calculate areas of fragments and condition of the forest (Garca, 2008, 2010). We thank an anonymous editor for many helpful suggestions for the text of this article.ReferencesAndrade, G. I. and Ruiz, J. P. 1988. Amazonia Colombiana: Aproximacin Ecolgica y Social de la Colonizacin del Bosque Tropical. FESCOL, Bogot. Chivian, E. and Bernstein, A. 2008. reatened groups of organisms valuable to medicine. In: Sustaining Life: How Human Health Depends on Biodiversity E. Chivian and A. Bernstein (eds.), p.209. Oxford University Press, New York. Daruich, J., Zirulnik, F. and Gimenez, M. S. 2001. Eect of the herbicide glyphosate on enzymatic activity in preg nant rats and their fetuses. Environ. Res. 85: 226231. Deer, T. R. 1992. Un anlisis del estado de la cobertura de bosque en la Amazonia colombiana. Unpublished. Deer, T. R. 1994. Callicebus torquatus is not a white-sand specialist. Am. J. Primatol. 33: 149154. Deer, T. R. 2010. Historia Natural de los Primates Co lombianos. Universidad Nacional de Colombia, Bogot. 614pp. Deer, T. R., Bueno, M. L. and Garca, J. 2010. Callicebus caquetensis: a new and critically endangered titi monkey from southern Caquet, Colombia. Primate Conserv. (25): 19. Garca, J. 2008. Evaluacin del Hbitat y de una Poblacin del Primate Callicebus sp. nov. del Sur del Caquet: Espe cie Nueva y Crticamente Amenazada. Informe Tcnico para la Fundacin Omacha y Conservacin Internacio nal, Fondo de Accin Ambiental, Programa de Becas Jorge Ignacio Hernndez-Camacho, Iniciativa de Espe cies Amenazadas. Garca, J. 2010. From the eld: discovery and conservation in Caquet, Colombia. Website:
46 Palacios, E., Rodrguez A. and Deer, T. R. 1997. Diet of a group of Callicebus torquatus lugens during the annual resource bottleneck. Int. J. Primatol. 18: 503522. Peluso, M., Munnia, A., Bolognesi, C. and Parodi. S. 1998. P32-Postlabeling detection of DNA adducts in mice treated with the herbicide Roundup. Environ. Mol. Mut. 31:5559. PRORADAM. 1979. La Amazonia Colombiana y sus Re cursos. Vol. 1. Proyecto Radargrametrico del Amazonas (PRORADAM), Repblica de Colombia, Bogot. 590pp. Proyecto SIMCI II: Cultivos de Coca estadsticas municipales censo 31 de Diciembre del 2009. Bogot, Colombia. Agosto del 2010. ONODC, Ocina de las Naciones Unidas Contra la Droga y el Delito Colombia, Bogot DC Repblica de Colombia 1992. Colombia: Informe Nacional para CNUMAD (Conferencia de Naciones Unidas sobre el Medio Ambiente y el Desarrollo). Bogot. Robinson, J. G. 1977. e vocal regulation of spacing in titi monkey Callicebus moloch. PhD thesis, University of North Carolina, Chapel Hill. Ruiz, S. L., Snchez, E., Tabares, E., Prieto, A., Arias, J. C., Gmez, R., Castellanos, D., Garca P. and Rodrguez, L. (eds.). 2007. Diversidad Biolgica y Cultural del Sur de la Amazonia ColombianaDiagnstico. Corpoamazonia, Instituto Humboldt, Instituto SINCHI, UAESPNN, Bogot DC, Colombia. 636pp. Rylands, A. B., Huber, O. and Brown, K. S., Jr. 1991. Workshop : B iological Priorities for Conservation in Amazonia. Map scale 1:5,000,000. Instituto Brasileiro do Meio-Ambiente e dos Recursos Naturais Renovveis (Ibama), Braslia, Instituto Nacional de Pesquisas da Amaznia (INPA), Manaus, and Conservation Interna tional, Washington, DC. SIMCI. 2010. Proyecto SIMCI II: Cultivos de Coca: Estadsticas Municipales. Censo 31 de Diciembre del 2009 Bogot DC, Colombia. August 2010. ONODC, O cina de las Naciones Unidas contra la Droga y el Delito, Colombia. SINCHI. 2007. Balance Anual sobre el Estado de los Eco sistemas y el Ambiente de la Amazonia Colombiana 2006. Instituto Amazonico de Investigaciones Cientcas (SINCHI), Bogot, DC. Van Roosmalen, M. G. M., van Roosmalen, T. and Mit termeier, R. A. 2002. A taxonomic review of the titi monkeys, genus Callicebus omas, 1903, with the description of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neo trop. Primates 10(suppl.): 213221.
47 A MORPHOLOGICAL ANALYSIS OF SOME SPECIES OF enCALLICEBUS, en THOMAS, 1903 en (PITHECIIDAE CALLICEBINAE)enPaulo Auricchioen1en1 enDepartamento de Biologia, Campus Cinobelina Elvas, Universidade Federal do Piau, Rodovia BR-135, km 03, Planalto en Horizonte 64900-000 Bom Jesus PI, email:. firstname.lastname@example.orgAbstractA chromogenetic eld analysis was performed with 25 of 29 of the known species of the genus Callicebus. Some species pre sented polymorphism, such as C. moloch, C. homansii and C. cupreus. C. bernhardi presents the same distribution of color in chromogenetic elds as C. moloch, diering only in pigment amount, mainly in ventral surfaces, suggesting C. bernhardi is a junior synonym of C. moloch. C. homansii presents two distinct phenotypes, but without a geographic barrier between them. Callicebus cupreus, C. dubius and C. caligatus are distinct species. Key Words: Callicebus, taxonomy, phenotypical polymorphism Resumopt-BRUma reviso taxonmica baseada nos campos cromogenticos foi procedida em 25 das 29 espcies conhecidas do gnero pt-BR Callicebuspt-BR. Algumas espcies apresentaram polimorsmo como pt-BR C. moloch, C. homansii e C. cupreus. Callicebus bernhardi pt-BR apresenta o mesmo padro de distribuio de campos cromogenticos de pt-BR C. molochpt-BR, divergindo somente na quantidade pt-BR de pigmentos, principalmente na face ventral da pelagem. Assim, pt-BR C.pt-BR pt-BR bernhardipt-BR deve ser considerado sinnimo jnior de pt-BR C. moloch. C. homansii pt-BR apresenta dois fentipos distintos, porm no h uma barreira geogrca entre eles. pt-BR C. cupreus, pt-BR Cpt-BR pt-BR dubius pt-BR e pt-BR C. caligatuspt-BR so espcies distintas. Palabras Clave: Callicebus, taxonomia, polimorsmo fenotpico IntroductionAlthough new species of Callicebus have been described from Brazil and Bolivia during the last decade, few taxo nomic studies had been made on this genus during the same period. e rst taxonomic review was performed by Elliot (1913), who recognized 22 monotypic species. is arrangement has been modied by several researchers, such as Tate (1939), omas (1927), Lnnberg (1939), CruzLima (1945), Vieira (1955) and Cabrera (1958), who proposed more detailed taxonomic arrangements, dened geographical distributions and suggested phylogenetic re lationships within the taxon. Hill (1960), inuenced by those authors, proposed a more complete taxonomic ar rangement. More recently, only Hershkovitz (1990), Ko bayashi (1995) and Anselmo (1997) performed taxonomic studies of Callicebus. Hershkovitz (1990) based in skull, skeleton morphology and pelage color, recognized 13 spe cies with 25 subspecic taxa, divided among four groups, as listed in Table 1. Kobayashi (1995) carried a phenetic analysis based on metric skull characters, besides cariotype, pelage color ation and geographic distribution of 23 species and sub species (C oenanthe, C. aureipalatti and C. coimbrai were not included; the last two had not been described at that time). He recognized ve species groups (Table 1) and stated these groups are independent lineages since the rates of character dierentiation were not signicantly dierent among the nearest related groups. Among these groups, Kobayashi (1995) pointed out a great dierentiation rate between personatus and torquatus, while donacophilus, cupreus, moloch appear more closely related. Concerning the pelage color pattern of the moloch group, Kobayashi con sidered donacophilus and personatus groups as no contrast ing pattern, burnt yellow for donacophilus and blackish to yellowish for personatus; the cupreus group was dened as weakly contrasting and moloch and torquatus groups as contrasting ventral surfaces and throat with white band, respectively. Roosmalen et al. (2002) described two new species (C. stephennashi and C. bernhardi ), and considered ve species groups: 1. torquatus, 2. personatus, 3. moloch, 4. cupreus, 5. donacophilus. e great individual and population color variation in Callicebus raises several doubts and, sometimes, misun derstanding about the taxonomy of this genus. Aquino et al. (2008) found two distinctive populations of Callicebus torquatus in northeast Peru. Although several characteristics such as the shape of the hair tuft on the throat
48 (a characteristic of torquatus group), color tones on hands and the width of frontal band, seems to be dierent among those populations, the authors were not condent whether the two populations could be considered as dierent taxa or not. Heymann et al. (2002) also found problems with Callicebus phenotypical characterization, notably on the color of the hands. Moore (2009) tested the use of pelage color characters as diagnostic taxonomic markers across the geographic distribution of the Callicebus cupreus-group as an example. He found both a clinal variation along a geo graphic transect, as well as a localized intra-populational variation. He emphasizes that systematists should be careful while considering the relationship between intrapopulational variation and geographic distribution. In this Table 1. Taxonomic status synopsis of Callicebus as presented by some authors and this work (modied from Roosmalen, 2002). Hershkovitz (1963) Hershkovitz (1988, 1990) Kobayashi (1995) Groves (2001) Roosmalen et al, 2002 Auricchio (2005) Group modestus Group modestus C. modestus C. modestus Group donacophilus Group donacophilus Group donacophilus Group donacophilus Group donacophilus C. moloch donacophilus C. donacophilus donacophilus C. donacophilus donacophilus C. donacophilus C. donacophilus C. donacophilus C. d. pallescens C. d. pallescens C. pallescens C. pallescens C. pallescens C. oenanthe C. oenanthe C. oenanthe C. oenanthe C. modestus C. modestus C. modestus C. olallae C. ollalae C. olallae C. olallae C. olallae C. m. moloch Group moloch Group moloch Group moloch Group moloch Group moloch C. moloch C. moloch C. moloch C. moloch C. moloch C. cinerascens C. cinerascens C. cinerascens C. cinerascens C. cinerascens C. m. homannsi C. h. homannsi C. h. homannsi C. homannsi C. homannsi C. homannsi C. h. baptista C. h. baptista C. baptista C. baptista C. baptista C. m. brunneus C. brunneus C. brunneus C. brunneus C. brunneus C. brunneus C. caligatus C. bernhardi C. dubius Group cupreus Group cupreus Group cupreus C. m. cupreus C. cupreus cupreus C. cupreus cupreus C. cupreus cupreus C. cupreus C. cupreus C m. discolor C. c. discolor C. c. discolor C. c. discolor C. discolor C. discolor C. m. ornatus C. c. ornatus C. c. ornatus C. c. ornatus C. ornatus C. ornatus C. personatus personatus C. personatus personatus C. caligatus C. caligatus C. coimbrai C. p. melanochir C. p. melanochir C. dubius C. dubius C. p. nigrifrons C. p. nigrifrons C. stephennashi C. stephennashi C. p. barbarabrownae C. p. barbarabrownae C. aureipalatti Group torquatus Group torquatus Group torquatus Group torquatus Group torquatus C. torquatus torquatus C. torquatus torquatus C. torquatus torquatus C. torquatus torquatus C. torquatus C. torquatus C. t. lugens C. t. lugens C. t. lugens C. t. lugens C. lugens C. lugens C. t. lucifer C. t. lucifer C. t. lucifer C. lucifer C. lucifer C. t. purinus C. t. purinus C .t. purinus C. purinus C. purinus C. t. regulus C .t. regulus C. t. regulus C. regulus C. regulus C. t. medemi C. t. medemi C. t. medemi C. medemi C. medemi C. medemi Group personatus Group personatus Group personatus C. personatus C. personatus C. personatus C. melanochir C. melanochir C. melanochir C. nigrifrons C. nigrifrons C. nigrifrons C. barbarabrownae C. barbarabrownae C. barbarabrownae C. coimbrai C. coimbrai C. coimbrai
49 article I present an analysis of the color pattern of all Cal licebus specimens from the main Brazilian collections, in order to evaluate phenotypical polymorphism and the va lidity of these species using the color pattern of fur and hair as diagnosable characters. Material and methodsI examined 455 dry skins of 25 species from 136 localities belonging to the following collections: Museu de Zoologia da Universidade de So Paulo (MZUSP 194 specimens); Museu Nacional do Rio de Janeiro (MNRJ 97); Museu Paraense Emlio Goeldi (MPEG 130); Instituto Nacional de Pesquisas da Amaznia (INPA 10); Instituto Pau Brasil de Histria Natural (IPBHN 10; Universidade de Braslia (UnB 1) and Centro de Primatologia do Rio de Janeiro (CPRJ 4). Appendix I lists the specimens together with geographic coordinates, label identication and a review of identication as found after this analysis. One specimen of C. pallescens and one of C. caligatus were studied alive in captivity. Material of Callicebus medemi, C. oenanthe, C ollalae, C. modestus and C. auriepallati were not available so these were excluded from this study. Characters were chosen based on the pelage color of body parts or chromogenetic elds. Following Hershkovitz (1977), these are dened as any part of the pelage showing a particular color pattern from nearby areas, (for instance, the forearm, the back, one sub-apical band in a hair, etc), as shown in Figure 1. I could nd chromogenetic elds char acters only in pelage, not in hair, so the analysis focused on those. Each specimen was morphologically analyzed and Table 2. Distinctive characters among C. cupreus, C. caligatus and C. dubius. C. cupreus phenotype 1 (most common) C. caligatus C. dubius Face Reddish-cream Dark reddish brown Sideburns, sides of head and beard deep red Forehead reddish-cream (agouti hair banded with light stripes longer than dark ones) Frontal Black stripe with no abrupt division with nape transversal frontal band whitish, with a ne black line of superciliar vibrissae which connects the blackish ears Crown reddish-cream (agouti hair banded with light stripes longer than dark ones). Black (rostral part) brownish agouti; hairs with 4 pheomelanic bands, each alternated with eumelanic band. Nape reddish-cream (agouti hair banded with light stripes longer than dark ones). Dark reddish brown -agouti. Each hair reddish brown with black tip brownish agouti; hairs with 4 pheomelanic bands, each alternated with eumelanic band. Back reddish-cream (agouti hair banded with light stripes longer than dark ones). Black Brownish agouti. brownish agouti; hairs with 4 pheomelanic bands, each alternated with eumelanic band. Lower back reddish-cream (agouti hair banded with light stripes longer than dark ones), but washed with brown. Dark reddish brown -agouti. Each hair reddish brown with black tip Reddish -brown -agouti brownish agouti; hairs with 4 pheomelanic bands, each alternated with eumelanic band External surface of fore legs and forearms intense redish brown which can vary to orangish. Dark reddish brown -agouti. Each hair reddish brown with black tip Reddish Back of Hands Brown, not agouti Black Blackish agouti, Fingers Brown, not agouti Black Contrasting white Back of Feet Brown, not agouti Black Contrasting white Base of tail Reddish-cream (agouti hair banded with light stripes longer than dark ones), but washed with brown. Black (20%) Reddish-brown -agouti Middle tail Reddish-cream (agouti hair banded with light stripes longer than dark ones), but washed with brown. Greyish, black/beige or burnt yellow (blackish hairs with 0.7 cm of whitish tip) Blackish. Tip of tail Reddish-cream (agouti hair banded with light stripes longer than dark ones), but washed with brown. Burnt yellow/ beige brush (INPA 4032) Contrasting white brush Ventral surface Intense reddish brown which can vary to orangish. Deep reddish-brown agouti. Each hair reddish-brown with black tip; Hairs of throat blackish agouti; chest, belly and ventral surface of legs and arms reddish or reddishbrown; not banded.
50 assigned to dierent chromogenetic pattern groups by com paring the color pattern of 14 regions (shown in Figure 1, plus chest, belly and ventral surface of limbs), considering color tone variation as character states. is variation is due to the pigment present in hairs. Hershkovitz (1977) points out pheomelanin as the pigment responsible for yellows, browns and reds, depending on the amount of it depos ited in the hair. Melanin is the pigment which gives black and gray colors to the hair. e analyses were performed by simple visual inspection, for example: when the character was crown with melanin pigment, states could be gray or black. Characters used in this study are listed in Table 2. Collecting sites were plotted (Fig. 2) and compared with bibliography. Although almost all Callicebus species were in cluded in this analysis (25 of 29 species), only the ones with taxonomic problems are discussed in this paper. Table 3 lists these species and the number of specimens analyzed.Results and DiscussionenMorphological Analysis 1. C. moloch/ C. bernhardi Pelage chromogenetic analysis shows C. moloch has great color tone variation on several chromogenetic elds, espe cially on the ventral surface, which ranges from yellow to reddish-brown. I could split the specimens into three phe notypes: normal phenotype, red phenotype and light phe notype. e normal phenotype is the commonest (84% of the sample) and has a cream forehead, crown (banded Figure 1. Pelage chromogenetic elds considered for this analysis. Figure 2. Map of collecting sites of Callicebus ( C. bernhardi, C. moloch (3 forms), C. brunneus, C. homannsi (2 forms) and C. cinerascens). Black arrow indicates a locality where all 3 phenotypes of C. moloch appear sympatric. Numbers refer to Appendix I localities.
51 hair showing light bands broader than dark ones) anks, dorsal surface of limbs, feet and hands; lower-back light brown with a slight brown stripe along the middle back, slightly darker than the anks, not washed with brown or it has very little amount of this pigment. e middle portion of tail is very dark (from dark brown to black) and the tip lightening to very light brown or dirty white. Beard, chest, belly and ventral surface of limbs are light orange-brown, more pigmented at the tip of hairs. e general color pattern of all specimens follows the de scription above, but specimens IPBHN 207, 208, 209 (loc. 52, Ig Almas, Rio Juruena, extreme north of Apiacs, MT); MZUSP 18956 (loc.53 RO, Nova Colina Polonoroeste); MZUSP 18964, 20253, 20255, 20058, 20067 (loc.54 RO, Nova Braslia Polonoroeste); MPEG 21972 (loc. 112 PA, Ig. do Patau, Municpio de Itaituba); MPEG 22000 (loc. 113 PA, Apui, BR-230 Humait-Itaituba km 17) have the ventral pelage extremely pheomelanized of a live reddish-brown. ese represent what I called red phenotype. A third phenotype, called here light phenotype has ventral parts much lighter, sort of a lime-yellow (specimens MZUSP 5198 and 5200 from loc. 82 AM, Bom Jardim, right margin of Amazonas River); MPEG 22014, 22015, 22016, 22017 (loc. 109 PA, UHE Tucuru, Tocantins River); MPEG 245 (loc. 95 PA, So Joo do Araguaia); MPEG 246 (loc. 94 PA, Alto Iriri River, Xingu). Roosmalen et al. (2002) described C. bernhardi and identied specimens MPEG 22996, 22997 (locality 50 BR km 150 Apis-Humait, right margin of Marmelos River, AM); MPEG 24590 and 24591 (locality 55 Alta Floresta, MT) as belonging to this taxon. Paratypes of C. bernhardi (INPA 4029 and 4033; locality 57 AM River Mariepau left a. River Madeira) show the same chromogenetic pattern as C moloch, with identical chromogenetic elds. ese specimens dier only in color tone and pigment amount on the ventral surface, exactly as seen in the red phenotype. In Roosmalen et al. ( op. cit.), diagnostic characters that distinguish C. bernhardi of C. moloch are described as fol lows: ...by grayish forehead and crown, white ear tufts, and blackish tail with a distinct white pencil . Actually, there is wide variation in forehead and crown color tone among all 183 specimens of the 3 phenotypes, from grayish to light red-brown, and the description above agrees perfectly with most specimens analyzed of normal phenotype as well. Concerning the auricular tufts, none of 183 specimens of C. moloch (3 phenotypes) and those identied as C. bernhardi in INPA and MPEG that I could analyze, presented white auricular tufts (including C. bernhardi paratypes). Tails of all red phenotype specimens as well as C. bernhardi specimens are identical to C. moloch: black with a lighter tip. Drawings of C. moloch in Roosmalen et al. (2002) do not show a black tail and the whitish back of the hands, not matching all specimens analyzed. us, all specimens of the normal phenotype, red phenotype, light phenotype and those described as C. bernhardi show the same chro mogenetic eld pattern, diering, as mentioned, only in the amount of pigment (color tone) of the ventral surface. Concerning the geographic distribution of C. moloch (all phenotypes), it is the broadest among all Callicebus species, occurring south of the Amazonas River, between the right margin of Madeira/Ji-Paran Rivers to the left margin of Tocantins River. C. moloch is not found between the right margin of Aripuan River and the left margin of Aba caxis River, where C. cinerascens is found (Noronha, et al. 2007). Callicebus moloch is found in Rondnia on both margins of the medium/upper Ji-Paran River (Ferrari, et al. 2000), what is conrmed by specimens MZUSP 18956 (RO, Nova Colina Polonoroeste, right margin of Ji-Paran River 10'S61'W, red phenotype; MZUSP 18964, 20253, 20255, 20058, 20067 (RO, Nova Braslia Polonoroeste, right margin of Ji-Paran River 10'S61'W red phenotype, and MPEG 19709, 19710, 19712, 19713 (Alvorada dOeste, BR 429 linha 64 km 87, left margin of Ji-Paran River 11'S62'W normal phenotype. Mono et. al. (2008) also assigned specimens they called C. bernhardi (here, red phenotype) to 90 km west of Alto Alegre dos Parecis (Chapada dos Parecis, Rondonia). Roosmalen (2002) states that there is a gap in the range of Callicebus at the southern portion of this region, between Sucunduri/Juruena River and Tapajs River. I could not nd any specimens in Brazilian museums from this region. Wide rivers such as the Juruena / Teles Pires / Tapajs are no barriers isolating the three phenotypes of C. moloch. Gascon et al. (2000) observed that wide rivers are not always obstacles to put apart small mammals and frogs as well. Localities for C. bernhardi indicated by Roosmalen et al. (2002) are: 51 (AM, Comunidade de Nova Olinda, right margin of Aripuan River, Novo Aripuan holotype INPA 3929 only skeleton) and 57 (AM, Mariepau River, right tributary of Madeira River paratypes of C bernhardi) Specimens MNRJ 2480 and 2481 (from AM, right margin of So Joo do Aripuan River) presents light phenotype and this locality is only 30 km straight line from locality 51 and 60 km from locality 57, mentioned Table 3. Material used for this study. Species Skins Alive C. moloch normal phenotype 154 C. moloch red phenotype / C. bernhardi* 20 C. moloch light phenotype 9 C. homannsi 27 C. brunneus 56 C. dubius 1 C. cupreus 70 C. caligatus 2 1 TOTAL 339 1
52 above, on the same bank of Aripuan River. In the local ity 109 (PA, UHE Tucuru rio Tocantins) it is possible to nd both light and normal phenotype as can be seen in specimens MPEG 21442, 21443, 22014, 22015, 22016, 22017, 22016 (normal phenotype) MPEG 22018 (light phenotype), one evidence of polymorphism. Red phenotype can be found far to the east from known localities of C. bernhardi. Specimens MPEG 21972 (locality 112Ig. Patau, Itaituba, PA), MPEG 22000 (BR 230 Itaituba, PA) and IPBHN 207, 208, 209 (locality 52Ig. Almas, Juruena River, Apiacs, MT) are red phenotype (see Appendix I for coordinates). ese localities are among others where phenotype can be normal phenotype or light phenotype, one more evidence of polymorphism. One specimen from Alta Floresta (locality 55) MPEG 24590, label identicated as C. bernhardi, had its DNAmt sequenced and it is more similar to the sequence of IPBHN 207 (from Apiacs, MT), both red phenotypes. A phylo genetic analysis for Callicebus carried by me (to be pub lished elsewhere) shows strong evidence for the three phe notypes of C. moloch to be considered a polymorphism of the same taxon. Also, C. bernhardi appears as sister group of C. moloch. It is possible to recognize a trend to a clinal variation along a east-west transect through the range of the species, with specimens from western localities showing more pigmented ventral parts (phenotype red) and speci mens with lighter ventral parts (phenotype light) to the east. Normal phenotype is found throughout the range. Moore (2009) found similar results in C. cupreus. C. homannsi showed similar south-north dierences in ventral amount of pigments as can be seen bellow. Based on this, I suggest here C. bernhardi, Roosmalen et al. (2002), to be considered as a junior synonym of C. moloch. 2. C. homannsi Analysis of chromogenetic elds of C. homannsi found two phenotypes diering only in the color tones of the ventral parts: homannsi 1, yellow similar to that observed in typical C. moloch ; and homannsi 2 which looks a very light lime-yellow. Pattern homannsi 2 is found north of pattern 1, the boundary between them set approximately by latitude 4oS (Itaituba, Para) (Fig. 2). Despite color dif ferences and non-overlapping ranges, I could not nd any geographic barrier or an ecological feature supporting the possibility that C. homannsi should be split into two taxa. So, I consider these two phenotypes as polymorphisms of the same species until other evidence of speciation arises. 3. C. cupreus Callicebus cupreus also shows three phenotypes: Phenotype 1: forehead and crown reddish-cream (agouti hair banded with light stripes broader than the dark ones). Back and nape almost concolor with crown. Lower back similar, but washed with brown. Tail as back; arms, legs, chest, belly and ventral surface of an intense reddish brown, sometimes orangish. Back of hands and feet are brown, not agouti. Phenotype 2: specimens MZUSP11831 and 11832 from Pauini, AM, have arms, legs, chest and ventral surfaces orangish. Phenotype 3 C. cupreus MZUSP7332 from Iquiri River, AM, holotype of C. cupreus acreanus and MZUSP5067 and 5068 from Santa Cruz do Eiru River have forehead and crown agouti-brown with black and cream, lighter than described for the phenotype 1, back as moloch and lower-back more brownish. Tail is dark-brown, gradually getting lighter to the tip, which is cream. Arms, legs, ventral surfaces and beard are dark reddish-brown, almost dark red. Six specimens (MPEG 1587, 1588, 1605, 1608, 1609 and 1845) from Amazonas (Rio Javari, Estiro do Equador) are darker than the phenotype 3, described here. Phenotypes are distributed in four localities (Figure 2) that are inside the known distribution of C. cupreus and do not show a geographic pattern that could suggest an existence of more than one only taxon. As it was not possible to identify geo graphical limits that could indicate segregation among taxa, and it was not possible to perform a DNA analysis, denite considerations about the taxonomic status of C. cupreus must await, intra-specic color polymorphism being the best explanation for the observed pattern. 4. C. cupreus, C. caligatus and C. dubius Grooves (2001) follows Hershkovitz (1990) in Callicebus taxonomy, but doubts him concerning some propositions. One of them considers C. caligatus, C. dubius and C. cupreus as synonyms. Roosmalen et al. (2002) described differences among these three species, considering all of them valid, a view I agree based on morphological grounds. All three show several distinctive characters, as pointed out by Roosmalen (2002) and revised here (shown in Table 2), such as the presence or absence of chromogenetic elds, e.g. frontal white and black stripes, tip of tail and white ngers. ConclusionsC. bernhardi must be considered as a junior synonym of C. moloch, since the only dierence between them is the amount of pigment in the hairs and it occurs in sympatry with C. moloch in several localityes. C. homannsii shows two phenotypes with parapatric ranges, but without any dened geographic barrier that could support their assign ment as two dierent taxa. Phenotype variation in C. cupreus is polymorphic, and do not show a geographic pattern that could support the idea of splitting it in more than one taxon; Callicebus cupreus, C. dubius e C. caligatus are dis tinct species since they present several distinctive characters and allopatric ranges.AcknowledgementsI would like to thank Dr. Paulo Nogueira Neto, my super visor, for making all these analyses possible; to Dr. Renato
53 Caparroz, Maraisa Lopes, Dr. Fbio Olmos, MSc. Cludia Renata Madella, Dr. Erwin Palacios and other two anonymous reviewers who provided many valuable comments and constructive criticisms on this manuscript. Also, I thank all institutions which allowed me to access their col lections, in the name of their very kind curators. I am very proud and thankful to Departamento de Zoologia da Uni versidade de So Paulo for accepting me for my doctorate thesis. I also thank to CAPES for nancing my scholarship and trips which were necessary for the development of this project.References Anselmo, N. P. 1997. Estudo das relaes intragenricas em Callicebus (Primates) usando a subunidade II do gene mi tocondrial do Citocromo c Oxidase (COII) Dissertao de Mestrado. Belm, Universidade Federal do Par. Aquino, R; Terrones, W; Cornejo, F. and Heymann, E. W. 2008. Geographic distribution and possible taxonomic distinction of Callicebus torquatus populations (Pitheci idae: Primates) in Peruvian Amazonia. Am. J. Primatol. 70:11811186. Cabrera, A. 1958. Catlogo de mamferos de amrica de sur. Revista Museo Argentino Ciencias Naturales, Bernardi no Rivadavia 4 (1): 1307. Cruz-Lima, E. 1945. Mammals of Amazonia. General In troduction and Primates. Belm, Museu Paraense Emlio Goeldi. 274 p. Elliot, D. G. 1913. A review of the primates New York, American Museum of Natural History. v.1. Gascon, C., Malcolm, J. R., Patton, J. L., Silva, M. N. F. da, Bogart, J. P., Lougheed, S. C., Peres, C. A., Neckel, S. and Boag, P. 2000. Riverine barriers in the geographic distribution of Amazonian species. P. Natl. Acad. Sci. 97 (25): 1367213677. Grooves, C. P. 2001. Primate Taxonomy. Washington, Smithsonian Institution. 350p. Hershkovitz, P. 1990. Titis New World monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zool., 55: 1109. Heymann E. W., Encarnacin F. C. and Soini, P. 2002. On the diagnostic characters and geographic distribution of the yellow handed titi monkey, Callicebus lucifer in Peru. Neotrop. Primates 10:124126. Hill, W. C. O. 1960. Primates, comparative anatomy and taxonomy. IV Cebidae, Part A New York, Wiley Inter cience. vii+523p. Kobayashi, S. 1995. A phylogenetic study of titi monkeys, genus Callicebus, based on cranial mesurements, I: Phy letic groups of Callicebus. Primates, 36(1): 101. Moore, 2009. Levels of resolution in the geographic distribution of pelage color characters as diagnostic taxonomic markers. Am. J. Phys. Anthropol. Suppl 120. Lnnberg, E. 1939. Notes on some members of the genus Callicebus. Arkiv fur Zoologi, 31A (13):118. Mono, G. R.; Selhorst, V. and Soares-Filho, J. A. R. 2008. Expanso da distribuio geogrca de Callicebus bernhardi a oeste do Rio Ji-Paran, Estado de Rondnia, Brasil. Neotrop. Primates 15: 6768. Moore, W. D. 2009. Levels of resolution in the geographic distribution of pelage color characters as diagnostic taxo nomic markers. Am. J. Phys. Anthropol. Suppl 48: 193. Noronha, M. A., Spironello, W. R. and Ferreira, D. C. 2007. New occurrence records and eastern extension to the range of Callicebus cinerascens (Primates, Pitheciidae). Neotrop. Primates 14: 137139. Roosmalen, M. G. M., Roosmalen, T. and Mittermeier, R. A. 2002. A taxonomic Review of the titi monkeys, Genus Callicebus, omas, 1903, with description of two new species, Callicebus bernhardi and Callicebus stephennashi, from brazilian amazonia. Neotrop. Primates, 10: 152. Schneider, H.; Schneider, M.P.; Sampaio, I.; Montoya, E.; Tapia, J.; Encarnacin, F.; Anselmo, N. P. & Salzano, F. M. 1993a. Divergence beetween biochemical and ci togenetic dierences in three species of the Callicebus moloch group. Am. J. Phys. Anthropol. 90: 345350. Tate, G. H. H. 1939. e mammals of Guines region. B Am. Mus. Nat. His. 76: 151229. omas, O. 1927. On further monkeys of the Callicebus torquatus group. Annals and Magazine of Natural History Srie 9, 20: 287. Vieira, C. O. C. 1955. Lista remissiva dos mamferos do Brasil. Arquivos de Zoologia, So Paulo, 8 (11): 341474.
54 Appendix I Collecting sites of all specimens analyzed. Label: Taxon indicated in label; Analysis = identication b y the author of this article; Specimens = specimens Number at collection; Listing numbers in bold are those cited in the map of Figure 2. No Collecting Locality Coordinates Label Analysis SPECIMENS1Colombia (loctip regio de Vil lavicencio Rio Meta) 04'N 73'W C. ornatus C. ornatus MNRJ 24862Ecuador, Rio Anaray 00'S 76'W C. discolor C. discolor MNRJ 39173AM Ig. I Pq. Nac. Pico da Neblina 00'N 66'W C. lugens C. lugens MNRJ 596574AM, Barcelos, Rio Arac Ig Jauari 00'S 63'W C. lugens C. lugens MNRJ 670715AM Ig. Japomeri, Rio Padauiri 00'S 64'W C. lugens C. lugens CRB 2570 MNRJ 270706RR Lago da Cobra dir. Rio Mucaja 01'N 60'W C. torquatus C. lugens MZ 9689, 96907AM So Gabriel da Cacheira 00'S 67'W C. lugens C. lugens INPA 40668AM Rio Tootobi af.dir. rio Demini 01'N 63'W C. lugens C. lugens MPEG 100189AM Rio Mucaja 02'N 62'W C. torquatus C. lugens MPEG 1928, 1929, 1931,1932, 2637410PA 54 km S 150 km W de Altamira Gleba 61 lote 02 03'N 52'W C. torquatus C. lugens MPEG20181 near Rio Uruar 11AM, Rio Juru 06'S 68'W C. regulus C. regulus MZUSP 911; MZ911mounted12AM, Fonte Boa 02'S 66'W C. regulus C. regulus MNRJ 2465, 21047, 25 89914AM Lg. Taoaria Grande, Rio Purus 6'S 64'W C. purinus C. purinus MNRJ 246115AM Lg. Ayapu, R. Purus 04'S 62'W C. purinus C. purinus MNRJ 2464, 2466, 247016AM Porangaba mg.dir. rio Juru Porto Walter 8'S 72'W C. cupreus C. cupreus MPEG 22998 (black tail), 2300017AM Barro Vermelho mg.esq. rio Juru Eirunep 06'S 68'W C. cupreus C. cupreus MPEG 2300118AM So Luiz do Mamori rio Purus 07'S 66'W C. cupreus C. cupreus MPEG 270 (light colored)19Peru Iquitos Parque do MPEG 03'S 73'W C. cupreus C. cupreus MPEG 253 (leucometopa), 672, 6874, 6875, 25920Peru Rio Maraons Iquitos 04'S 73'W C. cupreus C. cupreus MPEG 677 21AM Rio Javari Estiro do Equador 04'S 71'W C. cupreus C. cupreus 2 MPEG 1587, 1588, 1605, 1608,1609,184522AC Rio Branco 9'S 67'W C. cupreus C. cupreus MPEG 7102, 710323AM Rio Jaquirana (Cach Jaquirana) 8'S 66'W C. cupreus C. cupreus MPEG 890324AM Lago Tef Porto da Castanha 3'S 64'W C. cupreus C. cupreus MPEG 13207, 13208, 1321125AM Santo Antonio do R. Eiru 07'S 70'W C. cupreus C. cupreus MZUSP 4798,480526AM Santa Cruz do R. Eiru 07'S 70'W C. cupreus C. cupreus MZUSP 5054, 5057, 5062, 5064, 5066, 5067, 5068, 5069, 5070, 5071, 5072, 5073, 5076, 5077, 5081, 5082, 5085, 5086, 5087, 5088, 5089, 509027AM Eirunep 06'S 69'W C. cupreus C. cupreus MZUSP 5052, 5055, 5056, 5058, 5059, 5060, 5061, 5063, 5065, 5074, 5075, 5078, 5079, 5080, 5083, 5084, 1153428AC Manoel Urbano 08'S 69'W C. cupreus C. cupreus MZUSP 11237, 19542
55 No Collecting Locality Coordinates Label Analysis SPECIMENS29AC Sena Madureira 09'S 68'W C. cupreus C. cupreus IPBHN 82030AM, So Paulo de Olivena -Mata Juratuba 03'S 68' W C. cupreus C. cupreus MNRJ 2104931AM Pauini 07'S 66'W C. cupreus C. cupreus 2 MZUSP 11831,1183232AC Iquiri 09'S 67'W C. cupreus C. cupreus 2 MZUSP 733233RO EE Antonio Mugica Nava, Porto Velho esq Rio Madeira 09'S 64'W C. dubius C. dubius MZ (no number sat at time)35AM Ig. Bacana marg. Oeste lago Jar marg dir baixo Purus 04'S 61'W C. caligatus C. caligatus INPA 4032; MZUSP 11722(unknown locality)36AM Humait Lbrea BR 230 km 41 mg.dir rio Ipixuna 07'S 63'W C. cupreus C. caligatus MPEG 22011, 2201237AM Interuvio R. Ipixuna e Mucuim no Purus 06'S 64'W C. stephennashi C. stephennashi INPA 4030, 403138AM mdio e alto rio Purus 05'S 63'W C. stephennashi C. stephennashi INPA (no number sat at time)39Bolivia Sta Cruz de la Sierra Provincia de Cercado 17'S 63'W C. donacophilus C. donacophilus MNRJ 5537, 21059, 2106040MS Corumb 19'S 57'W C. donacophilus C. donacophilus MZUSP 3355, 3356, 3358, 3359, 337141RO Alto Paraso. Polonoroeste 09'S 63'W ? C. brunneus MZUSP 2007542RO Porto Velho 08'S 63'W C. brunneus C. brunneus MZUSP 7798, 779943RO Santa Brbara 09'S 63'W C. brunneus C. brunneus MZUSP 2014144RO Rio Machado Cach Nazar 08'S 62'W C. brunneus C. brunneus MZUSP 20432, 20433, 20434,20435; MPEG 22993, 22994, 2299545RO Pedra Branca 10'S 62'W C. brunneus C. brunneus MZUSP 2289746RO Faz. Rio Candeias municpio Porto Velho 08'S 63'W C. brunneus C. brunneus MPEG 10941,1094247RO UHE Samuel rio Jamari a.dir. rio Madeira 08'S 63'W C. brunneus C. brunneus MPEG 21686,21687, 21688, 21689, 21690, 21691, 21692, 21693, 21694,21695, 21696, 21697, 21698, 21699, 21700, 21701, 21702, 21703, 21704, 21705, 21706, 21707, 21710, 21711, 21748, 21795, 21943, 21944, 21945, 21946, 21947, 21948, 21949, 21954, 21955, 21956, 23035, MNRJ 28487, 28488, 2848948RO Calama margem direita Rio Ji-paran 08'S 62'W C. moloch C. brunneus MPEG 2200649PA Ig. Mundo novo margem direita do mdio Rio Iriri 05'S 54'W C. moloch C. moloch MPEG2183650AM BR-230 Humait-Apis km 150 mg.dir. rio Marmelos 07'S 61'W C. bernhardi C. moloch red phenotype MPEG 22996, 2299751AM Com. Nova Olinda dir. R. Aripuan Novo Aripuana 05'S 60'W C. bernhardi C. moloch red phenotype INPA 3929 (holotype only skeleton)52MT Apiacs Ig. Almas Rio Juruena 07'S 58'W C. moloch red phenotype IPBHN 207, 208, 209,53RO Nova Colina Polonoroeste 10'S 61'W C. moloch C. moloch red phenotype MZUSP 1895654RO Nova Braslia Polonoroeste 10'S 61'W C. moloch C. moloch red phenotype MZUSP 18964, 20253, 20255, 20058, 2006755MT Alta Floresta 09'S 56'W C. bernhardi C. moloch red phenotype MPEG 24590, 2459156AM Com. Nova Olinda Rio Aripuan 05'S 60'W C. bernhardi C. moloch red phenotype INPA 3929
56 No Collecting Locality Coordinates Label Analysis SPECIMENS57AM Rio Mariepau a. esq. Madeira 05'S 60'W C. bernhardi C. moloch red phenotype INPA 4033 (paratype), 4029 (paratype)58AM Prainha Rio Aripuan 07'S 59'W ? C. cinerascens MZUSP 11806, 11807, 11808, 11809, 11810, 11811, 1181259AM Prainha perto de Cipotuba m dir Rio Aripuan. 07'S 60'W ? C. cinerascens INPA 408560AM Lago do Batista marg dir R. Amazonas I. Tupinambarana 03'S 58'W C. baptista C. baptista MZUSP 4802, 4957, 5141, 5145, 5161, 5162, 5163, 5164, 5168, 5170, 7168, 7169, 7173, 7174, MNRJ 5923, 5903, 600361AM Tapaiuna marg dir R. Amazonas I. Tupinambarana 03'S 58'W C. baptista C. baptista MZUSP 7166,7167,717162Ura Curap 03'S 58' W C. baptista no visto MGMvanR50 63AM Parintins 02'S 56'W C. moloch C. homannsi MPEG 69064PA Fordlandia 03'S 55'W C. homannsi C. homannsi 1 MZUSP 11731, 1183965PA Itaituba marg esq R. Tapajs 04'S 56'W C. homannsi C. homannsi 1 MZUSP 3574, 3575, 357666PA Brasilia Legal marg esq R. Tapajs 03'S 55'W C. homannsi C. homannsi 1 MZUSP 11715, 11721, 1172667PA Vila Braga Tapajs 04'S 56'W C. homannsi C. homannsi 1 MPEG 251, MNRJ 247268PA Jacareacanga 17km Rod. Transamaznica 06'S 58'W C. homannsi C. homannsi 1 IPBHN 44469PA Samauma R Tapajs 03'S 55'W C. homannsi C. homannsi 2 MZUSP 11741, 1174570PA Aru Rio Arapiuns marg esq R. Tapajs 02'S 55'W C. homannsi C. homannsi 2 MZUSP 509171PA Urucurituba marg esq Rio Tapajs 03'S 55'W C. homannsi C. homannsi 2 MZUSP 10154, 10155, 11743, 11815, 11833, 1953472PA Santa Rosa Ilha de Urucurituba 03'S 56'W C. homannsi C. homannsi 2 MZUSP 11834, 11835, 1183673PA Rio Arapiuns Santarm Tapajs 02'S 55'W C. homannsi C. homannsi 2 MPEG 58774PA Vila Marip, marg dir R Tapajs 02'S 55'W C. homannsi C. homannsi 2 MPEG 2144475PA Itaituba-Jacareacanga km 19 04'S 56'W C. homannsi only skull MPEG 8499, 8500, 8501, 850276PA Monte Cristo marg dir R. Tapajs 04'S 55'W C. moloch C. moloch MZUSP 3567, 3568, 3569, 1181777PA Taperinha 02'S 54'W C. moloch C. moloch MZUSP 3570; MPEG 4733, 4734, 4735, 4736, 4737, 4738, 4739, 4740, 4743, 4744, 4745, 4746, 4747, 4748, 4749, 4750, 4751, 4752, 4753, 4754, 4755, 4756, 4757, 4758, 4759, 4760, 4761, 4762, 4763, 4764, 4765, 4766, 4767, 4768,4769, 4770, 477878PA Santarm Faz Maru 02'S 54'W C. moloch C. moloch MZUSP 3571, 357279PA Piquiatuba 03'S 55'W C. moloch C. moloch MZUSP 5142,5153, 5155, 5156,5158, 5160, MNRJ 5981, 5979, 598080PA Caxiricatuba R. Tapajs 02'S 54'W C. moloch C. moloch MZUSP 5143, 5144, 5146, 5147, 5148, 5149, 5150, 5151, 5152, 5157, 5159, 5165, 5166, 5167, 5169, 2473581PA Foz do Curu 02'S 54'W ? C. moloch MZUSP 5196, 5197, 520282PA Bom Jardim dir Rio Amazonas 02'S 54'W C. moloch C. moloch MZUSP 5198, 5200
57 No Collecting Locality Coordinates Label Analysis SPECIMENS83Pa Cachimbo 09'S 54'W C. moloch C. moloch MZUSP 806284PA Fordlandia 03'S 55'W C. moloch C. moloch MZUSP 10151, 10153,11716, 11717, 11718, 11719, 11720, 11723, 11724, 11725, 11727, 11728, 11729, 11730, 11732, 11733, 11734, 11735, 11736, 11737, 11738, 11739, 11740, 11742, 11744, 11813, 11814, 11816, 11837, 11838, 11840, 11841, 1969085PA Itapoama R. Tapajs 03'S 55'W C. moloch C. moloch MZUSP 1015286PA Sto Antonio R. Tocantins 02'S 49'W C. moloch C. moloch MZUSP 13472 (~= IPBHN 444 breast redish)87PA dir Rio Tapajs esq R. Mutuns 06'S 57'W C. moloch C. moloch IPBHN 20388MT R. Arinos, a dir R. Juruena 10'S 58 o00'W C. moloch C. moloch MZUSP 11244 (SP Zoo), MNRJ 2915, 292389PA Largo do Souza Rio Iriri 04'S 53'W ? C. moloch MZUSP 25441, 25442, 2544390PA Boca do rio Bacaj 03'S 51'W ? C. moloch MZUSP 25444, 2544591PA, Santarm, Rio Curuatinga, A Rio Curuauna 02'S 54'W C. moloch C. moloch MNRJ 11590, 1159392PA, Alto Cururu 07'S 57'W C. moloch C. moloch MNRJ 2386793PA, Rio Xingu 07'S 53'W C. moloch C. moloch MNRJ 54834, 54835, 5483694PA Alto rio Iriri Xingu 08'S 53'W C. moloch C. moloch light phenotype MPEG 24695PA So Joo rio Araguaia 06'S 48'W C. moloch C. moloch light phenotype MPEG 24596PA Igarap Joo Ribeiro mg.esq. rio Iriri 03'S 53'W C. homannsi C. moloch MPEG 21837, 2188397Luzilndia rio Araguaia Prox. Itaipava 06'S 48'W C. moloch C. moloch MPEG 1093298PA Luzilndia rio Araguaia Xinguara 06'S 49'W C. moloch C. moloch MPEG 10933, 1093999PA Serra Norte Carajs N1 06'S 50'W C. moloch C. moloch MPEG 10943, 10944,11843100PA Serra Norte Carajs N2 rea de mangans 06'S 50'W C. moloch C. moloch MPEG 11832101PA 170 km S de Tucuru Sade mg.esquerda rio Tocantins 05'S 49'W C. moloch C. moloch MPEG 12175, 12176102PA Santarm-Cuiab Itaituba BR 165 zona Sul 04'S 54'W C. moloch C. moloch MPEG 12627103PA Santarm Rod BR-163 km125 Flora do Tapajs. =78 03'S 55'W C. moloch C. moloch MPEG 26406104MT Apiacs 09'S 57'W C. moloch C. moloch IPBHN 208, 209105Alvorada dOeste BR 429 linha 64 km 87 11'S 62'W C. moloch C. moloch MPEG 19709, 19710, 19712, 19713106AM, So Joo, R. Aripuan 05'S 60'W C. moloch C. moloch MNRJ 2480, 2481107PA, Santarm, Belterra = 80 02'S 54'W C. moloch C. moloch MNRJ 5494108AM, Foz do Rio Castanho ( R Roosevelt) 07'S 60'W C. moloch C. moloch MNRJ 2482, 2484, 2485109PA UHE Tucuru rio Tocantins 03'S 49'W C. moloch C. moloch MPEG21442, 21443, 22014, 22015, 22016, 22017, 22016109aPA UHE Tucuru rio Tocantins 03'S 49'W C. moloch C. moloch light phenotype MPEG 22018
58 No Collecting Locality Coordinates Label Analysis SPECIMENS110PA Mun Tucuru Stio Calandri acima da barragem mg esq Rio Tocantins 03'S 49'W C. moloch C. moloch light phenotype MPEG 22015, 22016111PA, Ipanema, beira da Rodagem esquerda Santarm = 78 02'S 54'W C. moloch C. moloch MNRJ 11588, 11591, 11592112PA Ig. do Patau af. esq. Rio ?? Municpio de Itaituba 04'S 55'W C. moloch C. moloch red phenotype MPEG 21972113PA, Apui, BR-230 HumaitItaituba km 17 07'S 62'W C. moloch C. moloch red phenotype MPEG 22000114(loctip 30 milles north Concepcin, Paraguai) 22'S 57'W C. pallescens Criad. Velho Jatob115Ba, Mirors Faz Conceio 11'S 42'W C. barbarabrownae C. barbarabrownae UNB 1510116SE, Cristinapolis, Faz. Cruzeiro 11'S 37'W C. personatus C. coimbrai MNRJ 30550117BA, (loctip Morro Drara ou Faz Arara) 14'S 40'W C. melanochir C. melanochir MZUSP 3884118MG Telo Otoni 17'S 41'W C. personatus C. personatus MZUSP 2712, 2713, 2714119MG Baixo R. Suaui 18'S 41'W C. personatus C. personatus MZUSP 5839, 5931, 5932120ES Colatina 19'S 40'W C. personatus C. personatus MZUSP 2219, 2220, 2221, 2222, 2223, 2224, 2225, 2226, 2227121ES Rio Doce 19'S 40'W C. personatus C. personatus MZUSP 2409, 2410, 2411, 2412, 2413122ES Sooretama 19'S 40'W C. personatus C. personatus MZUSP 11142, 11148, 111152, 111164, 11711, 11712, 11713, 11714, 11803, 11804, 11805123MG, Passos, Foz do Brejo, So Joo da Glria 20'S 46'W C. personatus C. personatus MNRJ 21065, 21066, 25898124ES, So Domingos, Mata 10 de Agosto, Faz 10 de Agosto 19'S 40'W C. personatus C. personatus MNRJ 21054, 21052, 21053125ES, Lagoa Juparaua, Santanna 19'S 40'W C. personatus C. personatus MNRJ 2478126ES, Estrada Linhares, So Matheus km 54 19'S 40'W C. personatus C. personatus MNRJ 21051127ES, Rio So Jos, Brao do Sul 19'S 40'W C. personatus C. personatus MNRJ 54782, 54788128MG, Ituete, Rio Poo 19'S 41'W C. personatus C. personatus MNRJ 11986129RJ Itatiaia 22'S 44'W C. nigrifrons C. nigrifrons MZUSP 7426, 7427, 7428, 7429, 7430,19548130SP Serra da Cantareira 23'S 46'W C. nigrifrons C. nigrifrons IPBHN 318131SP Itatiba 23'S 46'W C. nigrifrons C. nigrifrons IPBHN 605, IPBHN 1016, IPBHN 1017132RJ, Itatiaia, Chevap Funil 22'S 44' W C. personatus C. nigrifrons MNRJ 25897133Cabeceiras do Paranatinga C. personatus C. personatus MNRJ 3008134C. personatus C. personatus MNRJ 2479135C. melanochir C. melanochir MNRJ 11049136C. purinus C. purinus CPRJ 005
59 SEED DISPERSAL PATTERNS IN TWO CLOSELY RELATED HOWLER MONKEY SPECIES en(en ALOUATTA PALLIATAen AND en A. PIGRAen): A PRELIMINARY REPORT OF DIFFERENCES IN FRUIT en CONSUMPTION, TRAVELING BEHAVIOR, AND ASSOCIATED DUNG BEETLE ASSEMBLAGESenKatherine R. Amatoen1*en, Alejandro Estradaen2en1 enProgram in Ecology, Evolution, and Conservation Biology, University of Illinois Urbana/Champaign, email: email@example.com edu, Author for correspondenceen2 enLaboratorio de Primatologa, Estacin de Biologa Tropical Los Tuxtlas, Instituto de Biologa, Universidad Nacional en Autnoma de Mxico, email: firstname.lastname@example.orgAbstractTwo-phased seed dispersal by primates and dung beetles is crucial for tropical rainforest regeneration. Two species of howler monkey exist in the tropical rainforests of southern Mexico: the mantled howler monkey ( Alouatta palliata), and the black howler monkey (A. pigra) Dierences between these species in foraging and traveling behavior, as well as associated dung beetle assemblages, may inuence seed dispersal patterns. In this paper we present the results of a preliminary four-month study comparing the above aspects between a group of A. palliata (N = 15) in Los Tuxtlas, Veracruz and a group of A. pigra (N = 7) in Palenque National Park, Chiapas, Mexico. We observed each group in alternating months using focal sampling, fecal examination, and trapping of dung beetles. Results showed that the A. palliata group consumed more mature fruit, but both groups dispersed similar numbers of seeds over the study period (ca. 13,000 seeds). e total number of seed species collected from the feces of the A. palliata group was lower than for the A. pigra group (13 vs. 31 species). e A palliata group had a larger home range (33 vs. 6.25 ha) and average day range (202 vs. 126 m). More dung beetles from more spe cies were associated with the A. palliata group (357 v. 99 beetles, 16 v. 8 species). e A. palliata group attracted more ballrolling dung beetles (75.1% of total), while the A. pigra group attracted more burrowers (80.8% of total). Our results suggest important dierences between black and mantled howler monkeys of southern Mexico as seed dispersers and highlight the need to consider foraging and ranging patterns, as well as associated secondary dispersers, when assessing seed dispersal by primates. Key Words: howler monkeys, seed dispersal, A. palliata, A. pigra, dung beetles, Mexico Resumenes-ESLa dispersin por primates y cucarrones estercoleros es crucial para la regeneracin del bosque tropical. Dos especies de es-ES monos aulladores existen en los bosques lluviosos del sur de Mexico: el mono aullador de manto (es-ES Alouatta palliata)es-ES, y el es-ES mono aullador negro (es-ES A. pigra). es-ESLas diferencias entre estas dos especies en el comportamiento de forrajeo y desplazamiento, es-ES as como los ensamblajes de cucarrones estercoleros asociados, pueden inuenciar los patrones de dispersin de semillas. En es-ES este artculo presentamos los resultados de un estudio preliminar de cuatro meses, comparando estos aspectos entre un grupo es-ES de es-ES A. palliata (N = 15) es-ES es-ES en Los Tuxtlas, Veracruz, y un grupo de es-ESA. pigra (N = 7) en el P arque Nacional Palenque, Chiapas, es-ESMexico. Observamos cada grupo durante meses alternos utilizando el muestreo focal, examinando muestras de heces, y es-ES coleccionando cucarrones estercoleros. Los resultados mostraron que el grupo de es-ES A. palliata es-ES consumi ms frutos maduros, es-ES pero los grupos de ambas especies dispersaron un nmero similar de semillas durante el perodo de estudio (ca. 13,000 sees-ES -es-ES millas). El nmero total de especies de semillas coleccionadas de las heces del grupo de es-ES A. palliata es-ESfue ms bajo que aquel es-ES para el grupo de es-ESA. pigra es-ES(13 vs. 31 especies). El grupo de es-ES A. palliata es-EStuvo un rea de rango vital ms grande (33 vs. 6.25 ha) es-ES as como un recorrido diario promedio mayor (202 vs. 126 m). Ms cucarrones estercoleros de ms especies estuvieron es-ES asociados con el grupo de es-ES A. palliata es-ES (357 v. 99 cucarrones, 16 v. 8 especies). El grupo de es-ES A. palliata es-ESatrajo ms cucarrones es-ES estercoleros peloteros (75.1% del total), mientras que el grupo de es-ESA. pigra es-ESatrajo ms estercoleros cavadores (80.8% del total). es-ES Nuestros resultados sugieren importantes diferencias entre los aulladores negros y aulladores de manto del sur de Mexico es-ES como dispersores de semillas y resaltan la necesidad de considerar el forrajeo y los patrones de movimiento, as como los es-ES dispersores secundarios asociados, cuando se evala la dispersin de semillas por parte de primates. Palabras Clave: monos aulladores, dispersin de semillas, A. palliata, A. pigra, cucarrones estercoleros, Mexico
60 IntroductionLarge frugivorous primates are important seed dispersers for many tropical tree species (Link and Di Fiore 2006). Although birds disperse a larger number of seeds, primates disperse the seeds of twice as many plant species as birds via endozoochory (Clark et al. 2001), and their ecological services are critical for recruitment of many mediumand large-seeded plant species (Ponce-Santizo and Andresen 2006; Stevenson and Aldana 2008; Stoner et al. 2007). Additionally, many seeds ingested by primates undergo twophase dispersal. Dung beetles attracted to primate feces act as secondary dispersal agents by accidentally burying seeds along with feces at the deposition site or, if the beetles are ball-rollers, a short distance away (Vander Wall and Long land 2004; Vulinec et al. 2006). is behavior may allow some seeds to escape post-dispersal predation and may pro vide ideal microclimatic conditions, increasing the prob ability of seed germination and establishment (Nichols et al. 2008; Vander Wall and Longland 2004; Vulinec and Lambert 2009; Vulinec et al. 2006). Two species of howler monkeys exist in the tropical forests of southern Mexico. e mantled howler monkey ( Alouatta palliata), which is found throughout Central America and into western South America, and the black howler monkey ( A. pigra), which is endemic to the area shared by Mexico, Belize, and Guatemala (Ford 2006; Rylands et al. 2006). Behavioral studies generally report similar resource use and activity budgets for A. palliata and A. pigra (Estrada 1984; Pavelka and Knop 2004), and the reported values of spe cies richness for dung beetle populations associated with each primate species (A. palliata: 33 sp.; A. pigra: 29 sp.) are also similar (Estrada and Coates-Estrada 2002; PonceSantizo and Andresen 2006). Many seed dispersal studies assume that all primates dis perse seeds similarly (Gross-Camp et al. 2009; NunezIturri et al. 2008), and only a few studies compare seed dispersal by closely related primate species in similar habi tats (Knogge and Heymann 2003; Stevenson et al. 2002). However, based on dierences in average body size (A palliata, males: 4.5.8 kg, females: 3.1.6 kg; A. pigra, males: 11.1.6 kg, females: 6.2.6 kg, (Ford and Davis 1992) and group size ( A. palliata, 5 indiv., average: 8 indiv.; A. pigra, 2 12 indiv., average: 4 individuals, (Di Fiore and Campbell 2007; Van Belle and Estrada 2008), A. palliata and A. pigra may dier in seed dispersal patterns. In this paper, we report results from a short comparative study of A. palliata and A. pigra aimed at documenting daily travel patterns, seed species dispersed, and dung beetle species as sociated with howler monkey feces.MethodsenData collection e mantled howler monkey (A. palliata) was studied in a 2000 ha segment of the Los Tuxtlas Biosphere Reserve in the region of Los Tuxtlas, Veracruz (18'08.63"N, 95'26.99"W), and the black howler monkey ( A. pigra) was studied in Palenque National Park (PNP) (~1800 ha; 17'12.02"N, 92'01.05"W), Chiapas, both in southeast Mexico (Fig. 1). At both sites vegetation is classied as tall, tropical rainforest, and the altitudinal gradient ranges from 150m to 500m above sea level (Estrada 1984; Estrada et al. 2002). Sampling was conducted in areas of continu ous forest at both sites. Focal samples were collected for one group of A. palliata (N = 15) in Los Tuxtlas during March and May 2008, and for one group of A. pigra (N = 7) in PNP during February and April 2008 for eighteen days each month. We collected 135 and 120 hrs of continu ous focal samples on the A. palliata group and A. pigra group, respectively. To control for dierences in group size and observation time, all focal data for each species were pooled across individuals and an average focal observation for each species was calculated. We assumed that by alter nating monthly observations for each howler group/species during the dry season (Estrada et al. 2002; Estrada and Coates-Estrada 2002) at both sites that, to a certain extent, we compensated for seasonal eects in the data. Additionally, sampling took place during the high-fruit season in both forests. In Los Tuxtlas, A. palliata consumes the most mature fruit between March and October (Estrada 1984; Estrada and Coates-Estrada 1991), and in PNP, A. pigra consumes the most mature fruit between March and July (Estrada and Muoz, unpublished data). Studies of dung beetles in Los Tuxtlas have demonstrated that dung beetle populations during the same months (Estrada et al. 1993). No previous studies have examined the dung beetle popula tion at PNP, but because the annual rainfall prole generally matches that observed at Los Tuxtlas (Estrada and Muoz, unpublished data), seasonal uctuations in the dung beetle population are likely similar to those in Los Tuxtlas. Figure 1. Location of study sites in southeast Mexico.
61 Focal samples were completed between 06:00 and 15:00 hrs each day to allow time for fecal sample processing. Each sample lasted between ve and 15 min (avg.: 14 min 3). Focal individuals were chosen in a random order, and sampling was rotated until all individuals in the group were sampled. For each sample, the occurrence and duration of feeding (ingestion of plant material) and travel (group movement from one tree to another) activity was recorded. During feeding observations, the type of plant part ingest ed was recorded and identied to the species level. A scaled topographic map was used to estimate the distances tra versed by the howlers. Total group biomass was estimated using the median body weight for each species (Ford and Davis 1992), and group biomass per hectare was calculated using the home range estimate from each map. Both groups were known to have only one neighboring group, and home range overlap was negligible. Only two A. palliata and three A. pigra intergroup interactions were observed during the study period. Fecal samples were collected each day and examined for seeds. Seeds collected from the fecal samples were counted and, when possible, identied to species by comparison to the seed collection at the Los Tuxtlas eld station and the National Herbarium housed at the Institute of Biology of the Universidad Nacional Autnoma de Mxico. In the case of seeds < 1 mm in length occurring at high densities, the number of seeds in the sample was estimated by sample volume (seeds/30 mL feces). Sampling of dung beetles was conducted at each site within the home range of the study groups using 10 pit-fall traps (15 cm in height 5 cm width) baited with 60 g of feces from the howler species present. Traps were placed at 50 m intervals along a 500 m sinuous transect (Larsen and For syth 2005) and remained there for 24 hr. e traps were located about 1 m o of the main trail in ecologically similar locations at each site. Sampling was repeated three times per months at each site, and three distinct transects were used each month in an eort to fully represent each groups home range. Dung beetles encountered in the traps were counted and, when possible, identied to species by comparison of specimens with the dung beetle collection at the Los Tuxtlas eld station. en Data analysis Because individuals were sampled randomly, and no individual was sampled two times consecutively, focal samples were assumed to be independent. e proportion of time spent traveling and feeding on each resource during a given focal sample were compared between groups using a Krus kal-Wallis test with a Bonferroni correction (R Software). e amount of time dedicated to feeding on each mature fruit species was expressed as a percent of total maturefruit consumption time. Total average distance traveled per day during the observation period was compared be tween howler monkey groups using a two-tailed, one-way ANOVA, after log-transformation (JMP 7.0). Since tree crowns as large as 50 m have been measured in the tropical forests of southeastern Mexico (Estrada and Coates-Estra da 1984), only daily movements of 50 m or more were considered as contributions to seed dispersal. Home range was calculated by using a gridded topographic map (50 50 m) of the study site to count the number of quadrants in which the group was present during monthly observations. e number of seeds dispersed per day and the number of seeds per milliliter of fecal sample were compared using a two-tailed, one-way ANOVA (JMP 7.0). A chi-squared test was used to compare the total number of seeds dispersed, the number of large and small seeds dispersed, the total volume of feces produced, and the estimated biomass of each group. Shannons diversity index (H') and Sorensons similarity quotient were calculated to compare the dung beetle populations collected at each study site (Estrada and Coates-Estrada 2002). Results On average, both howler groups spent a similar percent age of time feeding on fruit during a focal sample (A. palliata: 9.27 % 5.05, A. pigra: 11.21 % 4.76; 2 = 0.81, df = 1, p = 0.37; Table 1). Consumption of mature fruit ac counted for 8.54 % 4.94 of an average focal sample for the A. palliata group and 5.28 % 2.96 for the A. pigra Table 1. Average percent time individuals from the A. palliata and A. pigra groups spent consuming fruit and leaves during any given focal sample (N = 584 and 547 focal samples, r espectively). Comparisons between groups were performed using a Kruskal-Wallis test with Bonferroni correction. Asterisks indicate signicant p values. All medians = 0%. Alouatta palliata Alouatta pigra Kruskal-Wallis Average SD Average SD 2df p Fruit 9.27 5.056 11.21 4.76 0.80 1 0.37 Mature fruit 8.54 4.94 5.28 2.96 2.69 1 0.10 Young fruit 0.73 1.29 5.93 3.28 11.53 1 0.00069* Leaves 2.66 2.06 10.24 4.89 11.31 1 <0.00077* Mature leaves 0.46 0.72 1.86 2.30 2.75 1 0.097 Young leaves 2.21 1.81 8.38 2.96 11.35 1 <0.00076*
62 group (Table 1). During the study period the A. palliata group consumed the mature fruits of a total of nine species (Table 2), while the A. pigra group consumed the mature fruits of four species (Table 3). A. palliata group was ob served consuming mostly Ficus species (Moraceae) ( F. pertusa: 17.33% of mature-fruit feeding time, F. colubrinae: 15.30%, F. insipida: 15.65 %) (Table 2), and A. pigra group mostly P. armata (Moraceae) (43.04%) (Table 3). Overall, fewer fecal samples were collected from the A palliata group (156 samples = 3230 mL) than fr om the A pigra group (167 samples = 4800 ml, 2 = 307.0, df = 1, p = 0.0001). M ore seeds were collected from the fecal samples of the A. palliata group (13,756 seeds) than the A pigra group (13,162 seeds; 2 = 13.1, df = 1, p = 0.0003), and fecal samples contained seeds from 13 and 31 species, respectively (Tables 2 and 3). Based on both focal and fecal sample data, the A. palliata group utilized 18 fruit species during the study period, and the A. pigra group utilized 33. e majority of seeds recovered from both groups were from Ficus species (A. palliata, F. eugeniafolia: 43.7 % of Ficus seeds, A. pigra, F. sp. 1: 43.9 %; Table 2, 3). How ever, the seeds collected from the two groups varied in size. e largest seed found in fecal samples of A. palliata was 21 mm in length (unknown sp. 10) (Table 2), and the largest seed found in fecal samples of A. pigra was 40 mm in length (Inga sp. 1) (Table 3). Most seeds measuring < 3 mm belonged to the Ficus genus, and both howler groups ex pelled more seeds measuring < 3 mm than seeds measur ing > 3 mm ( A. palliata: 2 = 13022.2, df = 1, p < 0.0001; A. pigra: 2 = 10831.2, df = 1, p < 0.0001). However, the percent of total seeds deposited that were greater than 3 mm was smaller for the A. palliata group (1.3%) than for the A. pigra group (4.6%). ese seeds belonged to four and 11 plant species, respectively. Feces from A. palliata contained slightly more seeds/ml than those from A pigra (4 4 seeds/ml and 2 3 seeds/ml respectively; F 1, 64 = 7.63, p = 0.007). However, both groups deposited similar num bers of seeds per day ( A. palliata: 458 643 ( SD), A. pigra: 376 1030 (SD); F 1, 64 = 0.15, p = 0.70). e A. palliata group used a larger home range (12.5 ha) than the A. pigra group (6.25 ha) during the study period. erefore, despite dierences in group size, both groups ac counted for similar howler monkey biomass/ha ( A. palliata: 6.1 kg/ha, A. pigra: 7.7 kg/ha, 2 = 0.185, df =1, p = 0.33). Table 2. List of seed species collected from howler fecal samples and mature fruit species howlers were observed consuming in Los Tuxtlas ( A. palliata). Quantity of seeds from each plant species is reported using the absolute number and the percent of total seeds collected in each site. Also shown is the percent of mature-fruit feeding time howlers devoted to consuming a particular species. Species recorded from focal samples only are highlighted in bold. Values for seed size marked with an asterisk were estimated in the eld. Values without an asterisk were obtained from Croat (1978). Species/Morphotype Family Lifeform Type of Fruit Percent Feeding Time Number Seeds Percent Total Seeds Seed Size (mm) Brosimum alicastrum Moraceae Tree drupe 10.96 15 Coussapoa purpusii Moraceae Tree drupe drupe Ficus pertusa Moraceae Tree syconium 17.33 <1* Ficus sp. Moraceae Tree syconium 2.65 <1* Ficus tecolutensis Moraceae tree syconium 7.07 <1* sp. 1 0.53 Ficus eugeniaefolia Moraceae tree syconium 5679 43.70 <1* Ficus colubrinae Moraceae tree (strangler) syconium 15.30 3925 30.20 1* Ficus insipida Moraceae tree syconium 15.65 1647 12.67 2* Ficus petenensis Moraceae tree (strangler) syconium 1462 11.25 1* Cecropia obstusifolia Cecropiaceae tree drupe 0.88 808 6.22 2* Poulsenia armata Moraceae tree aggregate 15.83 116 0.89 4, 10* sp. 10 37 0.28 21* sp. 5 33 0.25 sp. 11 26 0.20 3* Cynometra vetusa Fabaceae tree drupe 8.66 16 0.12 13* Smilax sp.1 Smilicaceae vine berry 4 0.03 8* sp. 13 2 0.02 3* sp. 12 1 0.01 Total Species = 18 Total Seed 13,756
63 e average proportion of time spent traveling also did not dier between groups ( A. palliata: 0.058 0.055, A pigra: 0.069 0.018; 2 = 2.23, df = 1, p = 0.13). During the study period, the A. palliata group traveled less than 50 m on 12 of the 34 days during which it was followed. e A pigra group traveled less than 50 m on 15 of 34 days. Excluding these days, the A. palliata group had a margin ally signicantly larger day range (202 149 m, range: 50630 m) than the A. pigra group (127 66 m, range 50m; F1, 40 = 4.15, p = 0.048). At Los Tuxtlas, pit-fall traps captured 357 beetles belonging to 16 species (avg beetles/session = 59.50 78.69), while in Palenque they captured 99 beetles belonging to eight species (avg. beetles/session = 16.50 12.68) ( Table 4). ere was some evidence for higher dung beetle species Table 3. List of seed species collected from howler fecal samples and mature fruit species howlers were observed consuming in Palenque ( A. pigra). Quantity of seeds from each plant species is reported using the absolute number and the percent of total seeds collected in each site. Also shown is the percent of mature-fruit feeding time howlers devoted to consuming a particular species. Species recorded from focal samples only are highlighted in bold. Values for seed size marked with an asterisk were estimated in the eld. Values without an asterisk were obtained from Croat (1978). Species/Morphotype Family Lifeform Type of Fruit Percent Feeding Time Number Seeds Percent Total Seeds Seed size (mm) Brosimum alicastrum Moraceae tree drupe 13.92 15 Ficus sp. 1 Moraceae syconium 5599 43.87 <1* Ficus sp. 9 Moraceae syconium 3152 24.70 <1* Ficus colubrinae Moraceae tree (strangler) syconium 30.87 2670 20.92 1* Poulsenia armata Moraceae tree aggregate 43.04 459 3.60 4, 10* Ficus pertusa Moraceae tree (strangler) syconium 425 3.33 <1* Ficus insipid Moraceae tree syconium 379 2.97 2* sp. 2 140 1.10 Ficus sp. 3 Moraceae syconium 69 0.54 1* Ficus sp. 2 Moraceae syconium 40 0.31 1* Ficus petenensis Moraceae tree (strangler) syconium 38 0.30 1* Cecropia obstusifolia 36 0.28 sp. 6 33 0.26 8* sp. 3 17 0.13 Ficus eugeniaefolia Moraceae tree syconium 15 0.12 <1* Ficus sp. 4 Moraceae syconium 14 0.11 <1* sp. 1 13 0.10 15*, 34* Cynometra vetusa Fabaceae tree drupe 12.15 11 0.09 13* Ficus sp. 7 Moraceae syconium 10 0.08 1* Pseudolmedia oxyphyllaria Moraceae tree drupe 10 0.08 10* Dendropanax arboreus Araliaceae tree berry 5 0.04 7, 5* Ficus sp. 6 Moraceae syconium 5 0.04 <1* sp. 8 4 0.03 Cissus sp. 1 Vitaceae vine berry 3 0.02 9* Ficus sp. 8 Moraceae syconium 3 0.02 4* sp. 4 3 0.02 Ocotea sp. 1 Lauraceae tree drupe 2 0.02 15* sp. 5 2 0.02 Coussapoa purpusii Cercropiaceae epiphyte aggregate 1 0.01 2* Ficus sp. 5 Moraceae syconium 1 0.01 2* Inga sp. 1 Fabaceae tree legume 1 0.01 40 sp. 7 1 0.01 2* Trichostigma octandrum Phytolaccaceae vine drupe 1 0.01 5* Total Species = 33 Total Seeds 13,162
64 diversity at Los Tuxtlas (H' = 1.59, E H = 0.57) than in Palenque (H' = 1.30, E H = 0.63). Six dung beetle species were associated with both howler monkey groups, and Sorensons quotient for dung beetles was 0.50. e most common beetle species associated with howler feces at Los Tuxtlas was Canthon femoralis (58.3 %; Table 4), and at PNP it was Copris laeviceps (56.6 %; Table 4). At Los Tuxt las, most of the beetles captured were ball-rollers (75.1 %), while at PNP most were burrowers (80.8 %; Table 4). Also, at Los Tuxtlas 21.3 % of the beetles collected were noctur nal and 78.7 % were diurnal, while at PNP 62.6 % were nocturnal and 37.4% were diurnal (Table 4).Discussion Our behavioral and fecal samples data suggest that A. palliata and A. pigra dier somewhat in seed dispersal patterns despite being closely related. Previous studies report that A palliata can incorporate between nine and 35 fruit spe cies into its diet depending on the location, and in Los Tux tlas, a year-long study documented 28 seed species in A. palliata feces (Estrada and Coates-Estrada 1991; Whencke et al. 2004). A. pigra utilizes 25 fruit species in fragmented forests in Belize, and a ve-month study reported ten seed species in A. pigra feces in Guatemala (Marsh and Loiselle 2003; Ponce-Santizo and Andresen 2006). ese data sug gest that A. palliata is capable of consuming more seed species than the 18 documented in this study and that A pigra consumes more seed species in PNP than in other locations. However, because this study directly compares the two spe cies in similar forests during the same period of the year, the dierences detected between A. palliata and A. pigra may indicate a potential distinction in plant-primate dynamics. Specically, A. palliata appears to consume more mature fruit and disperse more total seeds while A. pigra appears to disperse a greater diversity of seeds. Table 4. Dung beetle species collected in Los Tuxtlas ( A. palliata) and Palenque (A. pigra). 60 traps were set in each site for 24 hours for a total of 1,440 trap hours at each site. Quantity of each beetle species is reported using the absolute number and the percent of total beetles collected in each site. Activity describes the time of day at which each species is active, and behavior describes fecal treatment. Alouatta palliata Species Activity Behavior Number Percent Canthon femoralis diurnal ball-roller 208 58.3 Copris laeviceps nocturnal burrower 52 14.6 Canthon euryscelis diurnal ball-roller 19 5.3 Deltochilum pseudoparile nocturnal ball-roller 12 3.4 Onthophagus batesi diurnal burrower 12 3.4 Canthon viridis vazquezi diurnal ball-roller 11 3.1 Dichotomius satanis nocturnal burrower 11 3.1 Neocanthidium martinezi diurnal ball-roller 7 2.0 Onthophagus rhinolophus diurnal burrower 7 1.0 Pseudocanthos perplexus diurnal ball-roller 5 1.4 Canthidium a ardens Bates diurnal burrower 4 1.1 Canthon subhyalinus diurnal ball-roller 3 0.8 Canthidium perceptible diurnal burrower 2 0.6 Phanaeus chryseicollis diurnal ball-roller 2 0.6 Canthon sp. diurnal ball-roller 1 0.3 Copris lubgris nocturnal burrower 1 0.3 Total 357 Alouatta pigra Species Activity Behavior Number Percent Copris laeviceps nocturnal burrower 56 56.6 Onthophagus vatesi diurnal burrower 19 19.2 Canthon euryscelis diurnal ball-roller 15 15.2 Dichotomius satanis nocturnal burrower 4 4.0 Canthon femoralis diurnal ball-roller 2 2.0 Copris lubgris nocturnal burrower 1 1.0 Deltochilum gibbosum nocturnal ball-roller 1 1.0 Phanaeus endymion diurnal ball-roller 1 1.0 Total 99
65 Dierences in patterns of range-use and daily travel be tween the two howler groups also likely result in the pro duction of dierent seed shadows (sensu Clark et al. 2005). Since both groups dispersed similar amounts of seeds per day, but the A. palliata group utilized a larger home range and day range than the A. pigra group, the seed shadow produced by the A. palliata group is likely less dense than that produced by the A. pigra group. ese behavioral differences are unlikely to be a result of group size since group size in these species appears to be dictated by social con straints and not by food availability (Chapman and Pavelka 2005; Cowlishaw and Dunbar 2000; Van Belle and Estrada 2008). Similarly, because territory overlap among groups was minimal, these patterns are likely to remain constant across the entire territory. During the high-fruit season, seed dispersal patterns also appear to dier between howler species with regard to associated secondary dispersers. Pre vious research in the continuous forest of Los Tuxtlas de scribed 20 dung beetle species associated with A. palliata, and a study of A. pigra in Guatemala documented 29 dung beetle species (Estrada and Coates-Estrada 1991; PonceSantizo and Andresen 2006). However, our data reveal a larger and more diverse dung beetle population associated with the A. palliata group than the A. pigra group, which may indicate a higher probability of secondary dispersal for seeds dispersed in A. palliata feces between February and May. Furthermore, most seeds dispersed by ball-rollers are less than 3 mm in length (Estrada et al. 1993; Vulinec et al. 2006). e A. palliata group was associated with more ball-rollers and dispersed fewer large seeds than the A. pigra group, and the A. pigra group was associated with more burrowers and dispersed more large seeds than the A. palliata group. erefore, the eectiveness of seed dispersal by each howler species may depend on the interaction of seed size and secondary dispersal by dung beetles. e as sociation of more diurnal dung beetles with the A. palliata group and more nocturnal dung beetles with the A. pigra group likely also inuences patterns of secondary seed dispersal since a large proportion of diurnal dung beetles are ball-rollers which may move seeds up to 5 m from the ini tial deposit site while a large proportion of nocturnal dung beetles are burrowers which bury seeds on-site (Slade et al. 2007; Vulinec and Lambert 2009). e subtle dierences in howler seed dispersal behavior and associated dung beetle assemblages described in this study suggest an important distinction between black and mantled howler monkeys as seed dispersers. Further inves tigation of these dierences in more groups of each species may broaden our understanding of how closely related pri mate species diering in associated secondary seed disper sal agents, among other features (e.g. body size and group size), may also dier in their contribution to the mainte nance of plant diversity in their habitats. e participa tion of distinct dung beetle communities in processing the feces produced by each howler group during the high-fruit season also highlights the importance of dung beetles as secondary dispersers (Nichols et al. 2008). Recent studies have shown that the stability of this interface is altered by human-induced forest fragmentation and habitat isolation, which cause local declines in size or extinctions of primate and dung beetle populations (Andresen 2002; Estrada and Coates-Estrada 2002; Nichols et al. 2008; Ponce-Santizo and Andresen 2006). Such changes may result in signi cant modications in patterns of recovery and distribution for many forest plant species. ese modications will have a strong impact on the persistence of primates in fragment ed landscapes and on human livelihood and merit further investigation. AcknowledgmentsK.R.A. acknowledges the Institute for International Educa tion and the Comisin Mxico-Estados Unidos para el In tercambio Educativo y Cultural (COMEXUS) (Fulbright Garcia-Robles), the National Geographic Conservation Trust (Young Explorers Grants), and Dartmouth College (Reynolds Fellowship) for their support of this project. We are grateful to the Universidad Nacional Autnoma de Mexico (UNAM), specically the Instituto de Biologa, for its logistical support in both Palenque and Los Tux tlas, and to the Comisin Nacional de Areas Naturales Protegidas (CONANP-PALENQUE) and the Secretaria del Medio Ambiente y Recursos Naturales (SEMARNAT) for granting access to our eld sites in Mexico. 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Neutral and niche perspectives and the role of primates as seed dispersers: a case study from Rio Paratari, Brazil. In: Garber, P. A., Estrada, A. E., Bicca-Marques, J. C., Heymann, E. W., and Strier, K. B., editors. South American Primates, Devel opments in Primatology: Progress and Prospects New York: Springer. p 321340. Vulinec, K., Lambert, J. E., and Mellow, D. J. 2006. Pri mate and dung beetle communities in secondary growth rain forests: implications for conservation of seed disper sal systems. Int. J. Primatol. 27(3):855879. Whencke, E. V., Valdez, C. N., and Dominguez, C. A. 2004. Seed dispersal and defecation patterns of Cebus capucinus and Alouatta palliata: consequences for seed dispersal eectiveness. J. Trop. Ecol. 20(5):535543.
67 S A O P N P E I E, E M G, BenDenize Fontes Nogueiraen Daniel da Silva Ferraz.en Aquila Fialho Oliveiraen Fernanda Pedreira Tabacowen Sara Machado de Souza Amncioen Fabiano Rodrigues de Melopt-BRIntroduopt-BRA Mata Atlntica est sendo fortemente afetada pelos efeipt-BR -pt-BR tos de fragmentao semelhana das demais orestas pt-BR tropicais do planeta. Depois da Amaznia, a Mata Atlnpt-BR -pt-BR tica o bioma neotropical que apresenta a maior riqueza pt-BR de espcies. Das cerca de 260 espcies de mamferos que pt-BR ocorrem no bioma (Mittermeier pt-BR et alpt-BR. 1998; Myers pt-BRet alpt-BR. pt-BR 2000), 24 so primatas, sendo 17 endmicas (Rylands pt-BR et pt-BR alpt-BR. 1996; Mendes pt-BR et al.pt-BR 2003). Devido ao hbito arborcola, pt-BR a destruio e a fragmentao da oresta, em alguns casos pt-BR aliadas caa, levaram cerca de 70% das espcies de primapt-BR -pt-BR tas da Mata Atlntica beira da extino (Machado pt-BR et alpt-BR. pt-BR 2008). Para agravar a situao, somente das reas protept-BR -pt-BR gidas da Mata Atlntica tem rea suciente para sustentar pt-BR populaes viveis de primatas (Chiarello 2000). O Estado pt-BR de Minas Gerais, outrora amplamente coberto por orespt-BR-pt-BR tas, tem registrado altos nveis estveis de desmatamento na pt-BR ltima dcada, resultando na reduo da cobertura orespt-BR -pt-BR tal de 47% para 33% de sua rea total (Instituto Estadual pt-BR de Florestas 2008). Embora esse cenrio seja desfavorvel pt-BR para as espcies que dependem de orestas, levantamentos pt-BR recentes tm localizado grupos remanescentes de primatas pt-BR em vrias reas. A estimativa da populao selvagem do pt-BR muriqui-do-norte (pt-BRBrachyteles hypoxanthuspt-BR), espcie Critipt-BR -pt-BR camente Em Perigo, por exemplo, aumentou de 500 para pt-BR mais de 900 indivduos (Mendes pt-BR et alpt-BR. 2005). No entanpt-BR-pt-BR to, a maioria de suas populaes sobrevive em pequenos pt-BR fragmentos orestais (Mittermeier pt-BR et al. pt-BR1987; Strier 2000; pt-BR Dias pt-BR et alpt-BR. 2005).pt-BR O Parque Estadual do Ibitipoca (PEIb) um bom exemplo pt-BR dessa paisagem fragmentada. A Floresta Ombrla Densa pt-BR Altimontana (Fontes pt-BRet alpt-BR. 1996) desta Unidade de Conserpt-BR-pt-BR vao (UC) e de seu entorno habitada por cinco espcies pt-BR de primatas: pt-BRCallicebus nigrifronspt-BR (sau), pt-BRCallithrix penipt-BR-pt-BR cillatapt-BR (mico-estrela), pt-BR Alouatta guariba clamitanspt-BR (barbado), pt-BR Cebus nigrituspt-BR (macaco-prego) e pt-BRBrachyteles hypoxanthuspt-BR pt-BR (muriqui-do-norte) (Hirsch pt-BRet alpt-BR. 1994; Fontes pt-BRet alpt-BR. 1996). pt-BR Devido carncia de dados acerca da densidade e estado pt-BR de conservao dos primatas no PEIb e nos fragmentos pt-BR orestais de seu entorno, este trabalho visou descobrir pt-BR novas populaes remanescentes de muriquis, determinar pt-BR parmetros populacionais a m de avaliar a necessidade de pt-BR ampliao da rea do PEIb ou de estabelecimento de um pt-BR mosaico de UCs no seu entorno.Metodologiaenrea de estudopt-BR O estudo foi realizado no Parque Estadual de Ibitipopt-BR -pt-BR ca (Fig. 1) que administrado pelo Instituto Estadual de pt-BR Florestas-IEF, Estado de Minas Gerais, e em 22 fragmentos pt-BR orestais localizados em propriedades particulares de seu pt-BR entorno. O PEIb est localizado no municpio de Lima pt-BR Duarte e faz divisa com os municpios de Bias Fortes a pt-BR leste e nordeste e Santa Rita do Ibitipoca a noroeste. Os pt-BR 22 fragmentos esto distribudos em trs regies distintas: pt-BR Mata do Patu, Mata dos Luna e Mata Grande. A rea dos pt-BR fragmentos variou de 32 a 1600 ha. pt-BR O PEIb (21'32,3"S, 43'45,3"O; 1100-1782 pt-BR m.a.n.m.; 1488 ha) faz parte do complexo da Serra da Manpt-BR -pt-BR tiqueira situada nos municpios de Lima Duarte e Santa Rita pt-BR de Ibitipoca, numa zona de transio entre a Mata Atlntica pt-BR e o Cerrado (Hermann 2007). considerada uma UC de pt-BR alta importncia biolgica para a conservao de mamferos pt-BR da Mata Atlntica (Oliveira 2004; Biodiversitas 2005). A pt-BR Mata Grande possui 70 ha (Rodela 1998) e compreende pt-BR aproximadamente 47% da rea total de Floresta Ombrla Figura 1. Cobertura vegetal na regio do Parque Estadual do Ibiti -pt-BR poca, Lima Duarte, Estado de Minas Gerais, Brasil.
68 pt-BRdo PEIb (Oliveira 2003), representando um importante rept-BR -pt-BR fgio para espcies endmicas e raras da fauna. A Mata do pt-BR Patu (21'26,4"S, 43'39,4"O) est localizada na base pt-BR do morro do Gavio, paredo grantico que faz divisa com pt-BR o PEIb, no municpio de Lima Duarte. O tipo sionmico pt-BR predominante a Floresta Estacional Semidecidual Monpt-BR -pt-BR tana, na sua maior parte em estgio secundrio de desenpt-BR -pt-BR volvimento devido a um intenso processo de corte seletivo. pt-BR Prximos a este bloco de oresta, existem fragmentos em dipt-BR -pt-BR versos estgios de regenerao, alguns dos quais encontrampt-BR-pt-BR -se interligados nas cumeeiras dos morros por corredores pt-BR de mata. A Mata dos Luna (21'42,5"S, 43'45,1"O) pt-BR possui cerca de 32 ha e caracterizada por Floresta Estapt-BR -pt-BR cional Semidecidual Montana, a qual foi alterada por corte pt-BR seletivo, embora possua reas com rvores de grande porte pt-BR (Arajo 2003). Est localizada a noroeste do PEIb no mupt-BR -pt-BR nicpio de Santa Rita do Ibitipoca onde encontra-se isolada pt-BR por reas de atividade agropecuria.pt-BR As reas de mata visitadas foram identicadas atravs da pt-BR base cartogrca do IBGE (escala 1:50000), de imagens pt-BR de satlite IKONOS e da indicao de proprietrios e pt-BR moradores. Treze campanhas de censo com durao de pt-BR 5 a 7 dias (totalizando 60 dias de campo) foram realizapt-BR -pt-BR das no perodo de julho de 2004 a junho de 2006. Para pt-BR localizao dos grupos de primatas, foram percorridos pt-BR transectos pr-existentes em bordas de mata, trilhas e espt-BR -pt-BR tradas no interior do PEIb e nos fragmentos do entorno, a pt-BR uma velocidade aproximada de 1,0 km/h conforme sugept-BR -pt-BR rido para o Mtodo do Transecto Linear (Buckland pt-BRet alpt-BR. pt-BR 1993). De forma oportunstica foram registrados todos os pt-BR avistamentos, vocalizaes e fezes obtidos a p ou a cavalo pt-BR durante os deslocamentos entre os fragmentos. A utilizao pt-BR de pt-BR playbackpt-BR tambm foi realizada durante as caminhadas. pt-BR Entrevistas elaboradas na forma de roteiro tambm foram pt-BR realizadas com a apresentao de fotograas das espcies da pt-BR fauna com ocorrncia comprovada para a rea de estudo e pt-BR a utilizao de CD com gravao das vocalizaes caractept-BR -pt-BR rsticas de pt-BR B. hypoxanthuspt-BR, pt-BR C. nigrifronspt-BR, pt-BR C. penicillatapt-BR e pt-BR Apt-BR pt-BR g. pt-BR clamitanspt-BR. A densidade de pt-BR B. hypoxanthuspt-BR foi calculada com pt-BR base no nmero de indivduos avistados dividido pela rea pt-BR total da Mata dos Luna (mapeamento total). Devido ao pt-BR baixo nmero de avistamentos das demais espcies, foi calpt-BR -pt-BR culado o ndice de abundncia relativa (taxa de encontro), pt-BR expresso em nmero de indivduos avistados por 10 km pt-BR percorridos.Resultados e DiscussoForampt-BR obtidos 50 registros de primatas (13 no PEIb, 30 na pt-BR Mata dos Luna e 7 na Mata do Patu) distribudos em cinco pt-BR espcies: pt-BR C. nigrifronspt-BR (18), pt-BRB. hypoxanthuspt-BR (17), pt-BRCpt-BR pt-BR penipt-BR-pt-BR cillatapt-BR (8), pt-BR A. g. clamitanspt-BR (6) e pt-BR C. nigrituspt-BR (1) (Tabela 1). pt-BR Brachyteles hypoxanthuspt-BR teve sua densidade estimada em pt-BR 0,15 ind./ha, enquanto a taxa de encontro das demais esppt-BR -pt-BR cies foi de 7,1 ind./10 km para pt-BR C nigrifronspt-BR, 3,1 ind./10 km pt-BR para pt-BR C. penicillatapt-BR, 2,4 ind./10 km para pt-BR A. g. clamitanspt-BR e pt-BR 0,4 ind./10 km parapt-BR C. nigrituspt-BR A riqueza de espcies pt-BR encontrada est de acordo com o citado por vrios autores pt-BR (Hirsch pt-BR et al.pt-BR 1994; Fontes pt-BRet al.pt-BR 1996; Melo pt-BR et al.pt-BR 2002; pt-BR Oliveira 2004; Hermann 2007). semelhana de Melo pt-BRet pt-BR al.pt-BR (2002) e Oliveira (2004), pt-BRB. hypoxanthuspt-BR foi registrado pt-BR somente na Mata dos Luna, observao compatvel com a pt-BR hiptese de Oliveira (2004) e Hermann (2007) de que a pt-BR espcie est extinta no PEIb. Alm disso, o presente estudo pt-BR constatou um declnio no tamanho populacional da esppt-BR-pt-BR cie nesta localidade. Enquanto Oliveira (2003) relata a prept-BR -pt-BR sena de um grupo composto por 10 indivduos, Melo pt-BR et al.pt-BR pt-BR (2004) registraram apenas sete indivduos adultos (quatro pt-BR machos e trs fmeas) no mesmo grupo. No levantamento pt-BR de 2005 vericou-se que as fmeas haviam desaparecido, pt-BRpermanecendo at 2009 apenas os quatro machos adultos pt-BR (F. R. Melo, obs. pess.). Este resultado compatvel com pt-BR o sistema social de pt-BR Brachytelespt-BR spp., no qual as fmeas supt-BR -pt-BR badultas dispersam de seus grupos natais e os machos so pt-BR loptricos (Strier 1992; Printes & Strier 1999). Devido pt-BR provvel ausncia da espcie nos fragmentos orestais do pt-BR entorno da Mata dos Luna, o que inviabiliza a imigrao de pt-BR fmeas para essa rea, apenas estratgias de manejo visanpt-BR -pt-BR do a suplementao dessa populao podero evitar a sua pt-BR extino (Melo pt-BRet alpt-BR. 2004). A recente extino da populapt-BR -pt-BR o do fragmento orestal de 44 ha da Fazenda Esmeralda, pt-BR Rio Casca, um testemunho dessa realidade. Inicialmente pt-BR composto por 15 a 16 indivduos, o grupo estudado por pt-BR Fonseca (1985) e Lemos de S (1991) foi extinto em 2008 pt-BR aps a transferncia do ltimo indivduo para o cativeiro pt-BR (F. R. Melo, obs. pess.). Tabela 1. Espcies de primatas encontradas nas trs regies de estudo e seus respectivos mtodos de amostragem, Lima Duarte, Minas Gerais. rea Selecionada Espcies Mtodos de Amostragem Total Mata Grande (PEIb) A. g. clamitans Avistamento 3 C. nigrifrons Avistamento 5 C. penicillata Avistamento 4 C. nigritus Avistamento 1 Mata dos Luna B.hypoxanthus Avistamento Vocalizao (playback) 17 1 C. penicillata Avistamento Vocalizao (playback) Entrevista 3 9 2 C. nigrifrons Avistamento Vocalizao (playback) 10 36 A. g. clamitans Vocalizao espontnea 1* Patu C. penicillata Avistamento Entrevista 1 1 A. g. clamitans Entrevista Avistamento 1 3 C. nigrifrons Entrevista Avistamento 1 3
69 O registro de apenas trs indivduos de pt-BRC. nigrituspt-BR na rea pt-BR do PEIb tambm requer ateno, pois segundo Chiarello pt-BR (2000) essa espcie pouco discreta e possui alta taxa de pt-BR encontro. Essa caracterstica, por sua vez, pode tornar a pt-BR espcie mais vulnervel caa (Johns & Skorupa, 1987). pt-BR Embora a espcie no esteja sob ameaa de extino, ela pt-BR encontrada em baixas densidades na regio e no foi citada pt-BR para a rea do PEIb nas entrevistas com os funcionrios pt-BR do Parque e os moradores da comunidade de Conceio pt-BR do Ibitipoca. Registros semelhantes da espcie na Mata pt-BR Grande, localizada no interior do PEIb, por Drumond pt-BR (1989), Oliveira (2004) e Hermann (2007) reforam as pt-BR observaes desta pesquisa. pt-BR Por m, o pequeno tamanho populacional dessas espcies pt-BR vivendo em fragmentos isolados compromete sua sobrevipt-BR -pt-BR vncia (Bernardo & Galetti 2004). Neste sentido, Chiarello pt-BR & Melo (2001) sugerem que apenas fragmentos orestais > 20000 ha so capaz es de manter populaes viveis de pt-BRprimatas em longo prazo. Portanto, os 32 ha da Mata dos pt-BR Luna esto muito aqum do necessrio para a manuteno pt-BR de uma populao mnima de 50 indivduos. Consequenpt-BR -pt-BR temente, os limites do PEIb so insatisfatrios para garanpt-BR -pt-BR tir a sobrevivncia das espcies na regio, o que refora a pt-BR necessidade de implantao de um mosaico de Unidades pt-BR de Conservao no seu entorno. Desta forma, o incentivo pt-BR criao de Reservas Particulares do Patrimnio Natural pt-BR (RPPNs) e Refgios de Vida Silvestre Estaduais pode viapt-BR -pt-BR bilizar o estabelecimento desse mosaico. Tambm possvel pt-BR aumentar a conectividade estrutural entre os fragmentos pt-BR por corredores de mata ciliar, a qual se encontra constituda pt-BR por vegetao em estgio avanado de recuperao (D. F. pt-BR Nogueira, obs. pess.). Corredores ecolgicos entre a Mata pt-BR do Luna e outros fragmentos com a mata do PEIb ampliapt-BR -pt-BR riam a rea de habitat disponvel e poderiam restabelecer pt-BR o uxo gnico entre as populaes isoladas, mitigando os pt-BR efeitos da fragmentao orestal.pt-BR Denize Fontes Nogueira,pt-BR Instituto Estadual de Florestas pt-BR (IEF/MG). Rua Esprito Santo,495 Centro Belo Hoript-BR -pt-BR zonte, Minas Gerais Brasil. CEP: 30166-030, e-mail: pt-BR
70 pt-BRInstituto Estadual de Florestas. 2008. Cobertura vegetal pt-BR de Minas Gerais. Website: http://www.ief.meioambiente.pt-BR mg.gov.br. Acessada em 07 de novembro de 2008.pt-BR Johns, A. D. and Skorupa, J. P. 1987. Responses of rainpt-BR -pt-BR -forest primates to habitat disturbance: a review. pt-BR Int. J. pt-BR Primatolpt-BR. 8 (2): 157191.pt-BR Lemos de S, R. M. 1991. A populao de pt-BR Brachyteles arapt-BR-pt-BR chnoides pt-BR (Primates: Cebidae) da Fazenda Esmeralda, Rio pt-BR Casca, Minas Gerais. Em: Rylands, AB. e Bernardes, AT, pt-BR editores. pt-BR A primatologia no Brasil 3pt-BR. Fundao Biodiverpt-BR-pt-BR sitas para a Conservao da Diversidade Biolgica, Belo pt-BR Horizonte, Minas Gerais. pp. 235238.pt-BR Machado, A., Drummond, G. M. and Paglia, A. P. 2008. pt-BR Livro Vermelho da Fauna Brasileira Ameaada de Extino. pt-BR 1a. Ed. 2 vols. Braslia, DF, Belo Horizonte, MG: MMA pt-BR e Fundao Biodiversitas. 1420pp.pt-BR Melo, F. R, Nogueira, D. F. and Rylands, A. B. 2002. Pript-BR -pt-BR matas do vale Jequitinhonha, Minas Gerais. Em: pt-BR Livro de pt-BR Resumos. X Congresso Brasileiro de Primatologia, Sociedade pt-BR Brasileira de Primatologiapt-BR. Universidade Federal do Par, pt-BR Belm, Par p.56.pt-BR Melo, F. R., Moreira, L. S. and Ferraz, D. S. 2004. pt-BR Invenpt-BR-pt-BR trio da populao de muriquis-do-norte (Brachyteles hypt-BR-pt-BR poxanthus) da Reserva do Ibitipoca, Lima Duarte MGpt-BR. pt-BR [Relatrio Tcnico no publicado]. U&M, Santa Rita do pt-BR Ibitipoca, MG.pt-BR Mendes, S. L., Coutinho, B. R. and Moreira, D. O. 2003. pt-BR Efetividade das unidades de conservao da Mata Atlnpt-BR-pt-BR tica para a proteo dos primatas ameaados de extino. pt-BR Em: pt-BR VI Congresso de Ecologia do Brasil Anais de Trabapt-BR -pt-BR lhos Completospt-BR, Editora da UFCE, Fortaleza. pp.286287.pt-BR Mendes, S. L., Melo, F. R., Boubli, J. P., Dias, L. G., Strier, pt-BR K. B., Pinto, L. P. S., Fagundes, V., Cosenza, B. A. P. and pt-BR De Marco Jr., P. 2005. Directives for the consertavation pt-BR of the northern muriqui pt-BRBrachyteles hypoxanthuspt-BR (Primapt-BR-pt-BR tes, Atelidae). pt-BRNeotrop. Primatespt-BR 13:718.pt-BR Mittermeier, R. A., Valle, C. M. C., Alves, M. C., Santos, pt-BR I. B., Pinto, C. A. M., Strier, K. B., Young, A. L., Veado, pt-BR E. M., Constable, I. D., Paccagnella, S. G. and Lemos de pt-BR S, R. M. 1987. Current distribution of the muriqui in pt-BR the Atlantic forest region of Eastern Brazil. pt-BR Primate Conspt-BR. pt-BR 8:143149.pt-BR Mittermeier, R. A., Myers, N., omsen, J. B., Fonseca, pt-BR G. A. B. and Olivieri, S. 1998. Biodiversity hotspots and pt-BR major tropical wilderness areas: approaches to setting pt-BR conservation priorities. pt-BRConserv. Biolpt-BR.pt-BR pt-BR 12 (3): 516520.pt-BR Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonsept-BR -pt-BR ca, G. A. B. & Kent, J. 2000. Biodiversity hotspots for pt-BR conservation priorities. pt-BRNaturept-BR 403: 853858.pt-BR Printes, R. C. and Strier, K. B. 1999. Behavioral correlates pt-BR of dispersal in female muriquis (pt-BRBrachyteles arachnoidespt-BR). pt-BR Int. J. Primatolpt-BR. 20: 941960.pt-BR Oliveira, E. G. R. 2003. Ocorrncia de muriqui (pt-BR Brachytept-BR-pt-BR les hypoxanthuspt-BR) no entorno do Parque Estadual do Ibitipt-BR-pt-BR poca, MG. Em: pt-BR Sociedade Brasileira de Mastozoologia. II pt-BR Congresso Brasileiro de Mastozoologiapt-BR PUC-Minas, Belo pt-BR Horizonte. p.228. pt-BROliveira, E. G. R. 2004. Levantamento de mamferos de pt-BR mdio e grande porte e estimativa de tamanho populaciopt-BR -pt-BR nal de duas espcies de primatas no Parque Estadual do pt-BR Ibitipoca, MG. [Dissertao de Mestrado]. Programa de pt-BR Ps Graduao em Ecologia da Universidade Federal do pt-BR Rio de Janeiro, Rio de Janeiro, Brasil. 84 p.pt-BR Rodela, L. G. 1998. pt-BR Mapa de Vegetao e Uso do Solo pt-BR Parque Estadual do Ibitipoca MGpt-BR [Relatrio Tcnico pt-BR no publicado]. IEF/DPB, Belo Horizonte, MG.pt-BR Rylands, A. B., Fonseca, G. A. B., Leite, Y. L. and Mitterpt-BR -pt-BR meier, R. A. 1996. Primates of the Atlantic Forest, origin, pt-BR distributions, endemism, and communities. Em: Norpt-BR -pt-BR conk, P., editor. pt-BR Adaptive Radiations of Neotropical Primapt-BR -pt-BR tespt-BR. Plenum Press, New York. pp. 2151.pt-BR Strier, K. B. 1992. Faces in the forest: pt-BRept-BR pt-BR endangered Mupt-BR-pt-BR riqui monkey of Brazilpt-BR Oxford University Press, Oxford. pt-BR 138 p.pt-BR Strier, K. B. pt-BR 2000. Population viabilities and conservapt-BR -pt-BR tion implications for Muriquis (pt-BRBrachyteles aracnoidespt-BR) in pt-BR Brazils Atlantic Forest. pt-BRBiotropicapt-BR 32: 903. r ffr ( CEBUS NIGRITUS ) n enCarlos Rodrigo Brocardo en Henrique Santos Gonalves en Valesca Bononi Zipparroen Mauro GalettiIntroductionNeotropical primates aect plant population through mutualistic interactions, such as seed dispersal, and antagonist interactions such as seed predation and herbivory (Peres, 1993; Russo and Augspurger, 2004; Mourth et al ., 2008). Primates killing trees through herbivory is rarely documented (Rocha, 2000; Santos et al., 2007). e genus Cebus (Erxleben, 1777) is considered as having the widest diet plasticity among neotropical primates, eating leaves, seeds, fruits, invertebrates and even vertebrates (Fedigan, 1990; Galetti and Pedroni, 1994; Susan and Rose, 1994; Rose, 1996; Ludwig et al., 2005; Carretero-Pinzn et al., 2008; Freitas et al., 2008). In this paper, we documented the predation of two palm species through the consump tion of palm heart (apical meristem) by black-capuchin monkey ( C ebus nigritus Goldfuss, 1809). Materials and methodsOur observations were carried out between June 2009 and June 2010 in Carlos Botelho State Park (CBSP) (24' and 24'S; 47' and 48'W), in So Paulo State, Brazil. e CBSP has an area of 37,644 ha of Atlantic Forest, and it is located in the Forest Continuum of Pa ranapiacaba massif. e annual average temperature varied
71 from 15 to 19 C, and the annual precipitation varied from 1700 to 2400 mm (Instituto Florestal, 2008). e densi ty of black-capuchin monkeys in this site is estimated at 10.5 ( 2.4 SE) individuals/km, and the av erage group size is 5.16 ( 0.55 SE) individuals (G aletti et al., unpub. data). e records of palm heart predation (directly and indi rectly) were taken during line transects of mammal survey (430 km, approach 500 hours) and during the displace ments to line transects in the forest (about 200 eld hours). Despite that the C. nigritus groups were not accompa nied directly, the animals are relatively habituated to ob servers. e line transects surveys were carried monthly (10 days per month), when we encounter predation events, ad libitum observations were made (with binocu lars or naked eye), each predation event was recorded by a single observer. We sampled adult trees through random ized 15 0.04-ha plots, and juvenile trees through 15 0.01ha plots to estimate the capuchin-monkey palm predation (sampling tree adapted from Durigan, 2003). Chi-square analysis was used to estimate dierences in predation in tensity between seasons.ResultsWe observed capuchin-monkeys preying upon palm hearts of Euterpe edulis Mart. in 14 occasions, being 12 times in the Winter (May A ugust), once in the Summer (November F ebruary), and once in the Autumn (February M ay). We recorded from one to four capuchinmonkeys (sub-adult and adult) feeding simultaneously on apical meristem, but each animal on a dierent palm. e group size in these events varied from 3 to 12 blackcapuchin monkeys. Capuchin monkeys spend between 10 to 40 minutes (mean 25 4 SE) to open the palm heart, varying principally with palm diameter. Initially, the monkeys bite the outer leaves, forcing them down using both hands, remaining supported with tail and posterior mem bers on the palm stipe, then they repeat this process until liberate the apex of most leaves. After that, the animals bite the apex basis, to release it from the stipe, and consumed the apical meristem on other tree. We found other 44 E. edulis killed by capuchins along the forest trails, of which 38 palms were killed in the Winter, four in the Summer, and two in the Autumn. e pres ence of recently signals permitted the identication of predation period (recently withdrawn leaves on the ground, recently destroyed apices and remains of consumed meri stems; Fig. 1A and 1B). Other 12 palms were too old to determine the season of the predation (resting only the old destroyed apices). Considering direct and indirect observa tions of palms predation (only events where was possible determining the period of predation), the consumption of E. edulis diered signicantly between seasons ( = 73.0, df = 2, p < 0.001), being 10 times higher in the Winter than Summer, and 18 times greater than in the Autumn. e E. edulis palms killed had diameter at breast height from 8.6 to 15.4 cm (mean 12.8 0.55 SE) and height fr om 7 to 20 m (mean 12.2 0.94 SE). E. edulis is the most abundant arboreal plant in the study area, with a mean density of 93.3 ( 22.8 SE) adults/ha and 706.6 ( 90.7 SE) juveniles/ha. We estimated E edulis adult mortality by ca puchin monkeys at 1.7 ( 1.6 SE) individuals/ha per y ear (1.8 % of adult population). Moreover, for the rst time, we observed the predation of palm heart of Geonoma gamiova Barb. Rodr., an understory palm species, with height up to 4 m. Two adults G gamiova were upon preyed by two adult capuchin monkeys (in the Winter). e process is similar to E. edulis, but beyond the animals supported on the palm, they supported in near lianas, taking for predation 8 minutes for a palm and 9 minutes for other. Figure 1. A) Remains of consumed apical meristem by C. nigritus in CBSP. B) Recently withdrawn leaves of E. edulis on the ground.
72 Discussione distribution of E. edulis and C. nigritus overlaps in most part of their occurrence in the Brazilian Atlantic Forest (Vilanova et al., 2005; Herderson, 2000) (Fig. 2A). But, the palm heart predation by capuchin monkeys has been reported in a few places (Fig. 2B). In others areas we have worked, as the Iguau National Park (Araucaria Forest and Semidecidual Atlantic Forest, 185,262 ha continuous area, Paran state, Brazil) and Semidecidual Atlantic Forest fragments in So Paulo state (Mata So Jos and Mata Santa Genebra, both approximately 250 ha), this behav ior or predation signals were never recorded. It is possible that the use of this resource may be related to the group cultural inheritance, such as tool use and food-processing (Antinucci and Visalberghi, 1986; Rocha et al., 1998; Fra gaszy et al., 2004; OMalley and Fedigan, 2005; Canale et al., 2009). e group cultural inheritance in Cebus species, as well as other primate species, involves social learning, when the animals observe and interact with other group members, acquiring behaviors (Panger et al., 2002; Dindo et al., 2008; Dindo et al., 2009). e removal of the apical meristem demands dexterity and physical eort, being not accomplished by all members of a group, commonly this is done by some adults and sub-adults, and is observed for young animals. Except humans, C. nigritus seems to be one of the only vertebrate able to prey upon apical meristem of adults E edulis, since white-lipped peccaries ( Tayassu pecari Link, 1795) prey upon apical meristem of saplings (F. RochaMendes unp. data), and one of the few primates killing an arboreal plant (see Santos et al., 2007; Rocha, 2000). E. edulis is a palm with single stipe (dierently of Euterpe oleracea), and removal of apical meristem leads to the death of individual. In forest fragments the main cause of mor tality of E. edulis and Geonoma brevispetha (adult and juve nile palms) is the impact of meristem predation by blackcapuchin monkeys (Souza and Martins, 2006; Santos et al., 2007; Portela, 2008; Portela et al., 2010). In areas where this behavior occurs, the capuchin monkeys may be help ing to modeling the forest structure, similar to observed for ungulates (Silman et al., 2003; Wyatt and Silman, 2004; Beck, 2007). e palm heart predation by capuchins may have consequences for other species, especially birds, ro dents and ungulates that depend on E. edulis fruits during the Winter (Galetti et al., 1999; Mikich, 2002). Neverthe less, this impact is much smaller than the one caused by human extraction, which may extirpate locally entire adult populations, being the higher threat to conservation of E. edulis (Galetti and Aleixo, 1998; Galetti and Fernadez, 1998; Pizo and Vieira, 2004). Taira (2007) suggests that the consumption of palm heart in the Winter is an alternative source to insect scarcity, but not to fruit scarcity, which also occurs in the Winter at CBSP (Nakai, 2007). On the other hand, several papers concerning the diet of C. nigritus and congeners reported the use of alternative food resource in period of scarcity of fruits which normally constitute the main part of Cebus diet (Galetti and Pedroni, 1994; Peres, 1994; Freitas et al., 2008). erefore, we suggest that palm heart of E. edulis and, at a lesser extent, of G. gamiova, might be considered as a fallback food of C. nigritus. Indeed, fallback foods are dened as foods consumed during seasons when pre ferred foods are unavailable (Altman, 1998) or as foods Figure 2. A) Distribution of Cebus nigritus (triangles) and Euterpe edulis (circles) in Brazil (adapted from Vilanova et al., 2005 and Herderson, 2000); B) Areas with records of apical meristem predation of E. edulis by C. nigritus: 1 Poos das Antas Biological Reserve, fragment (Portela, 2008; Portela et al., 2010); 2 Caetetus Ecological Station, fragment (R. Lzara pers. com.); 3 CBSP, continuous (this paper, Taira, 2007); 4 Intervales State Park, continuous (Zipparro and Galetti pers. ob.); 5 Juria-Itatins Ecological Station continuous (P. Rubim pers. com.); 6 Mata Doralice, fragment (Ludwig et al., 2005); 7 Vila Rica do Esprito Santo State Park, fragment (Santos et al., 2007).
73 whose use is negatively correlated with the availability of preferred foods (Marshall and Wrangham, 2007; reviewed in Lambert, 2009). E. edulis is known as a keystone-species, providing fruits and seeds for several animal species during the time of greatest shortage (Galetti et al., 1999; Mikich, 2002). e consumption of meristem apical by C. nigritus, especially in the Winter, highlights another aspect of im portance of this palm.AcknowledgementsWe thank the direction of CBSP and Fundao Florest al do Estado de So Paulo for allowing to carry out this study. We thank F. Rocha-Mendes, P. Rubim and R. Lzara for sharing their data with us. is work was supported by Fundao de Amparo Pesquisa do Estado de So Paulo (FAPESP) through the process BIOTA FAPESP 2007/03392-6. C. R. B. and M. G. receives a CNPq fel lowship (Conselho Nacional para o Desenvolvimento Cientco e Tecnolgico). V. B. Z. and H. S. G. received a FAPESP fellowship. We thank L. Culot and R. S. B. Gavira for improving the revision of manuscript. We thank refer ees for their comments and suggestions. Carlos Rodrigo Brocardo*, Valesca Bononi Zipparro and Mauro Galetti, Laboratrio de Biologia da Conservao, Universidade Estadual Paulista (UNESP), CEP 13.506900. Av. 24 A, n 1515, Rio Claro, So Paulo, Brazil, Hen rique Santos Gonalves, Laboratrio de Biologia da Conservao, Universidade Estadual Paulista (UNESP) and Instituto Chico Mendes de Conservao da Biodiversidade (ICMBio) RESEX Mdio Purus, Lbrea, Amazonas, Brazil. *Author for correspondence. E-mail:
74 northern muriquis (Brachyteles hypoxanthus). Neotrop. Primates 15 (2): 4045. Nakai, S. 2007. Fisso-fuso em Cebus nigritus: Flexibi lidade social como estratgia de ocupao de ambientes limitantes. MSc thesis. Instituto de Psicologia. Universi dade de So Paulo, So Paulo. OMalley, R. C. and Fedigan, L. 2005. Variability in foodprocessing behavior among white-faced capuchins ( Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am. J. Phys. Anthropol. 128: 6373. Panger, M. A.; Perry, S.; Rose, L.; Gros-Louis, J.; Vogel, E.; Mackinnon, K. C. and Baker, M. 2002. Cross-site dif ferences in foraging behavior of whitefaced capuchins ( Cebus capucinus). Am. J. Phys. Anthropol. 119:5266. Peres, C. A. 1994. Primates responses to phenological changes in an Amazonian Terra Firme Forest. Biotropica 26 (1): 98112. Peres, C. A. 1993. Notes on the ecology of buy saki mon keys (Pithecia albicans, Gray 1860): A canopy seed-pred ator. Am. J. Primatol. 31:129140. Pizo, M. A. and Vieira, E. M. 2004. Palm harvesting aects seed predation of Euterpe edulis, a threatened palm of the Brazilian Atlantic Forest. Braz. J. Biol. 64(3B): 669676. Portela, R. C. Q. 2008. Ecologia populacional de trs es pcies de palmeiras em uma paisagem fragmentada no domnio Mata Atlntica, RJ. Doctoral thesis. Universi dade Estadual de Campinas, Campinas. Portela, R. C. Q., Bruna, E. M. and Santos, F. A. M. 2010. Demography of palm species in Brazils Atlantic forest: a comparison of harvested and unharvested species using matrix models. Biodivers. Conserv. 19: 23892403. Rocha, V. J. 2000. Macaco-prego, como controlar esta nova praga orestal? Floresta 30 (1/2): 9599. Rocha, V. J., Reis, N. R. and Sekiama, M. L. 1998. Uso de ferramentas por Cebus apella (Linnaeus) (Primates, Cebidae) para obteno de larvas de Coleoptera que parasitam sementes de Syagrus romanzoanum (Cham.) Glassm. (Arecaceae). Rev. Bras. Zool. 15 (4): 945950. Rose, L. M. 1997. Vertebrate predation and food-sharing in Cebus and Pan Int. J. Primatol. 18 (5): 727765. Russo, S. E. and Augspurger, C. K. 2004. Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecol. Lett. 7: 10581067. Santos, C. V., Morais Jr, M. M., Oliveira, M. M., Mikich, S. B., Ruiz-Miranda, C. R. and Moore, K. P. da L. 2007. Ecologia, comportamento e manejo de primatas invaso res e populaes-problema. In: A Primatologia no Brasil. Bicca-Marques, J. (Ed.), Vol. 10, Sociedade de Brasileira Primatologia, Porto Alegre. Pp. 101108. Souza, A. F. and Martins, F. R. 2006. Demography of the clonal palm Geonoma brevispatha in a Neotropical swamp. Austral Ecol., 31: 869881. Silman, M. R., Terborgh, J. W. and Kiltie R. A. 2003. Population regulation of a dominant rain forest tree by a major seed predator. Ecology 84 (2): 431438. Susan, P. and Rose, L. 1994. Begging and transfer of coati meat by white-faced capuchin monkeys, Cebus capucinus. Primates 35(4): 409415. Taira, J. T. 2007. Consumo de palmito-juara ( Euterpe edulis Mart.) por macacos-pregos ( Cebus nigritus): Estratgia de forrageamento timo ou requinte de um goumert? MSc esis. Instituto de Psicologia. Universi dade de So Paulo, So Paulo. Vilanova, R., Silva Jnior, J. S., Grelle, C. E. V., Marroig, G. and Cerqueira, R. 2005. Limites climticos e vegetacio nais das distribuies de C ebus nigritus e Cebus robustus (Cebinae, Platyrrhini). Neotrop. Primates 13 (1): 1419. Wyatt, J. L. and Silman, M. R. 2004. Distance-dependence in two Amazonian palms: eects of spatial and temporal variation in seed predator communities. Oecologia 140: 2635.tr f t fr ( ALOUATTA CARAYA ) r brenAnthony J. Giordanoen Warren B. Ballard Howler monkeys (Alouatta) comprise a diverse genus of neotropical primates that range from southern Mexico ( A. palliata, A. pigra) to northern Argentina and southeastern Brazil ( A. guariba, A. caraya) (Corts-Ortiz et al., 2003). Howler monkeys are the most folivorous of the Neotropical primates (Terborgh, 1983), and thus must forage for long periods to meet their high energetic de mands. e southernmost distributed of the howler spe cies, the South American black howler ( A. caraya) has been reported to occur at the highest densities (Zunino and Rumiz, 1986; Bicca-Marques, 1990; Rumiz, 1990; Crock ett, 1998). Considered principally an inhabitant of tropical lowland deciduous and semideciduous forests, black howl ers are also known to frequent the gallery forests of the Rio Paraguay and Rio Paran, as well as the seasonally in undated Pantanal in Brazil (Redford and Eisenberg, 1992; Crockett, 1998). In Paraguay, black howlers are mostly associated with inland Atlantic forest fragments in the east and gallery for ests of high rainfall in the Chaco (Stallings, 1985; Crock ett, 1998). However, they have not been reported from the more xeric regions of the Chaco Boreal far from a major drainage system. Stallings and Mittermeier (1983: 161) found that A. caraya was recorded from the higher forest [of the Chaco Boreal] but seemed to be rare in the region. However, they made no specic reference to geographic location, as howlers were not the primary subject of their discussion. Furthermore, they did not reference the time of year their primate observations were made. In conduct ing primate transects at Chaco Defensores National Park, Stallings et al. (1989) failed to record an observation of
75 A caraya during the austral winter. Neither of these claims is surprising given that xeric regions of deciduous and semideciduous scrub forest likely act as barriers to the sea sonal movements of a species that depends entirely on a low-quality, leafy forage. is is particularly true during the austral winter, when most such deciduous trees are devoid of leaves. Here we describe an encounter with a solitary adult male black howler monkey of unknown age in the north-central Chaco of Paraguay. e encounter took place on a cool, overcast morning between 10:00 and 11:00 hours on 7 August, 2007. e solitary male was observed on private property approximately 130 km south of Chaco Defensores National Park (21 41.176 South, 060 09.234 West). e property is approximately 45,000 ha in expanse, > 80% of which contains natural vegetation. In contrast, the majority of the surrounding properties have converted most of the natural vegetation into rangeland for livestock, and there is little opportunity for far-reaching habitat connectivity. e howler was at the top of a short canopy tree (< 12 15 m) completely devoid of foliage. e tree was at the edge of a new clearing that had been opened up to create a cattle pasture and was isolated from other neighboring trees (i.e., the only access into the tree would have been from the base). We were able to observe it unobstructed, aided by binoculars, for approximately 20 minutes, while stand ing < 23 meters from the trunk. During this time, the animal appeared completely undisturbed, and made no at tempt to ee. On the contrary, it appeared indierent to our presence and more concerned with that mornings cold temperature as it huddled over its extremities and moved very little. is observation occurred before the onset of a prolonged drought in the Paraguayan Chaco, and at the time when few trees were bearing leaves. Furthermore, the property owner, who observed the animal as well and had owned and managed the property for more than 20 years at the time of the observation, had never before seen the spe cies on his property or anywhere else in the north-central Chaco. It was unclear where the animal had come from and what was sustaining it. We left to pursue other unrelat ed activities and returned less than 1 hour later to nd the monkey gone, with no evidence as to where it had gone to. A subsequent, albeit anecdotal, inquiry among landowners found few to be familiar with this species. It would not be unreasonable to conclude that this male did not exist in isolation amidst such a sizeable region in the dry Chaco. Horwich (1998) remarked on the general adaptability of all Alouatta species, and we agree that A. caraya must be particularly adaptable to persist in such an ecosystem during a time of year when its limiting resources must be considered very scarce at best. Anthony J. Giordano* and Warren B. Ballard, Department of Natural Resources Management, Texas Tech University, Box 42125, Lubbock, TX 79409 (AJG) and (WBB), A uthor for correspondence:
76 the only primate sighted during the survey and although troops were not habituated every attempt was made to gather data. Tamarins were followed for anywhere from 15 minutes to up to ve hours. Tamarins used all levels of the forest, from the ground to the canopy (0m) and were seen foraging in both primary and secondary forest as well as along the main road that runs through the re serve (even crossing the road on the ground). Our pre liminary data indicate that there are at least three troops, but there may be up to six. Average troop size was four individuals. Several intertroop encounters were observed and consisted of continuous loud chattering vocalizations lasting over 30 minutes in one instance. A number of calls were recorded and will be analyzed in the future. Forag ing data gathered indicate that like most other tamarins, the individuals at this site have a mixed diet. Individuals were seen foraging on the owers of Inga sp. and Mucuna elliptica, fruit of Pourouma cecropiifolia and an unkown liana, and palm exudates. During the study period a dead juvenile male was discovered with few marks. e speci men was measured (HB = 23 cm, T = 32.5 cm, HF = 6.5 cm, E = 2.4 cm) and deposited at P onticia Universidad Catli ca del Ecuador in Quito. Although cause of death could not be determined, potential predators at the site include margays, tayras and several raptor species. In addition to the tamarins, four other species of primates have been observed in the reserve: Aotus vociferans, Ateles belzebuth, Cebus albifrons, and Alouatta seniculus Although not in the reserve Woolly monkeys ( Lagothrix lagotricha) do reside in the nearby Sumaco Galeras National Park. Researchers will continue to monitor primates at the site and more behav ioral data will be collected in the future. e Wildsumaco Biological Field Station, a joint venture between the pre serve, Francis Marion University and University of North Carolina Wilmington, will open in July 2011 and facilitate future primate studies in the area. For more information on primate studies at Wildsumaco please contact Natasha Vanderho (email@example.com) or visit the website (http:// www.riopucunofoundation.org/). E. Natasha Vanderho Department of Biology and Marine Science, Jacksonville University 2800 University Blvd N., Jacksonville, FL 32211. Jonas Nillson, Wildsumaco Wildlife Sanctuary S.A., Pacto Sumaco, Ecuador. es-ESNC M C r Eb Ces-ESLa Asociacin Colombiana de Primatologa en coordinaes-ES -es-ES cin con la Universidad de Los Andes y el Laboratorio de es-ES Ecologa de Bosques Tropicales y Primatologa, los invitan es-ES a participar en el Primer Curso de Mtodos de Campo es-ES y Estrategias de Conservacin en Primatologa del 10 al es-ES 22 dees-ES es-ES Julio de 2011, en el Parque Nacional Natural Cueva es-ES de Los Gucharos, Colombia. Para mayores informes es-ES entrar a http://cursoprimatologia2011.webs.com/ P Ebr A Be Institute of Tropical Ecology and Conservation oers the eld course Primate ethology and animal behavior at the Bocas del Toro Biological Station, Panama. e pur pose of this course is to give the student a foundation in primate ecology, primate behavior, eld techniques and analytical tools in a tropical setting. e material covered is equivalent to a university upper level course in primate ecology. e course is available to college students, post bachs, graduate students or faculty. Registration deadline: November 20th, 2011. For more information go to: http:// www.itec-edu.org/index.html MP C Le MPhil in Conservation Leadership at University of Cambridges Department of Geography, is a full-time, one-year, masters course, aimed at graduates of lead ership potential with at least three to ve years of rel evant experience. e unique features of this course are its delivery by a partnership between several univer sity departments and conservation organizations based around Cambridge, and its focus on issues of man agement and leadership. A key aim of the course is to build the capacity of conservation leaders from tropical countries. For more information visit: http://www.geog. cam.ac.uk/graduate/mphil/conservation/
77 R es-ESPes-ES rBfAtlas of Biodivesity Risk, edited by J. Settele, L. Peney, T. Georgiev, R. Grabaum & V. Grobelnik. 2010. Pen soft Publishers. 300pp. ISBN: 978-9546424464. is is the rst book to describe and summarise the major pres sures, impacts and risks of biodiversity loss at a global level. It identies the main risks as global climate and land use change, environmental pollution, loss of pollinators and biological invasions. It also analyzes the impacts and consequences of biodiversity loss, with a strong focus on socio-economic drivers and their eects on society. Contents: 1. Biodiversity baseline information; 2. Research approaches for biodiversity and impacting factors; 3. Climate change impacts on biodiversity; 4. Land use change and their impacts; 5. Environmental chemicals and biodiver sity; 6. Biological invasions; 7. Decline of pollinators and its impact; 8. Socio-economy and its role in biodiversity loss; 9. Combined biodiversity eects of major drivers and pressures; 10. e future of biodiversity and biodiversity research. Primate Anti-Predator Strategies, edited by S. Gursky & K. A. I. Nekaris. 2010. Springer. 396pp. ISBN: 9781441941909. is volume details the dierent ways that nocturnal primates avoid predators. It is a rst of its kind within primatology, and is therefore the only work giving a broad overview of predation. Contents: 1. Predation and primate congnitive evolution K. Z uberbhler; 2. Predation on primates: a biogeographical analysis D. H art; 3. Primates and other prey in the seasonally variable diet of Cryptoprocta ferox in western Madagascar L. D ollar, J. U. Ganzhorn & S. M. Goodman; 4. Predation on lemurs in the rainforest of Madagascar by multiple predator species S. M. Karpanty & P C. Wright; 5. Predation, communication and cognition in lemurs M. Scheumann, A. Rabesandratana & E. Zimmermann; 6. A consideration of leaping locomotion as a means of predator avoidance in prosimian primates R. H. Crompton & W. I. Sellers; 7. Anti-predator strategies of cathemeral primates I. C. Colquhoun; 8. M oonlight and behavior in nocturnal and cathemeral primates L. T. Nash; 9. A comparison of calling patterns in two nocturnal primates, Otolemur crassicaudatus and Galago moholi as guide to predation risk S. K. B earder; 10. Predator defense by slender Lorises ans Pottos K. A. I. N ekaris, E. R. Pimley & K. M. Albard; 11. e response of spectral trasiers toward avian and terrestrial predators S. L. Gursky; 12. Talking defensively a dual use for brachial and gland exudates of slow and pygmy lorises L. R. H agey, B. G. Fry & H. F. Snyder; 13. Anti-predator strategies in diurnal prosimian L. G ould & M. L. Sarther; 14. Howler monkeys and harpy eagles: a communication arms race R. Gil-da-Costa; 15. Eects of habitat structure on perceived risk of predation and anti-predator behavior of vervet and patas monkeys K. L. E nstam; 16. Predation risk and habitat use in Chacma baboons R. A. H ill & T. Weingrill; 17. Reconstructing hominin interactions with mammalian carnivores A. Treves & P. Palmqvist. Primate Locomotion: Linking Field and Laboratory Research, edited by K. DAot & E. E. Vereecke. 2010. Springer. 364pp. ISBN: 978-1441914194. is book brings togeth er the two aspects of primate locomotion studies: labora tory studies based on biomechanics and energetics, and the eld studies focused on behavior and ecology. Contents: 1. Introduction: primate locomotion, towards a synergy of in situ and ex situ research V ereecke et al.; 2. Experimental and computational studies of bipedal locomo tion in the bipedally-trained Japanese monkey O gihara et al.; 3. Scapula movements and their contribution to the three dimensional forelimb excursions in quadruped primates Schmidt & Krause; 4. e kinematics of load carrying in great apes, implications for the evolution of human bipedalism Watson et al.; 5. Field and experimen tal approaches to the study of locomotor ontogeny in Pro pithecus verreauxi Wunderlinch et al.; 6. Comparisons of limb structural properties in habituated chimpanzees from Kibale, Gombe, Mahale and Ta communities Carlson et al.; 7. Gait and kinematics of arboreal quadrupedal walk of free-ranging red howlers ( Alouatta seniculus) in French Guiana Youlatos & Gasc; 8. Implications of chimpanzee bipedal feeding for the evolution of hominid posture and locomotion S tanford; 9. Linking in situ and ex situ ap proaches for studying primate locomotor responses to sup port stability S tevens; 10. Leaping, body size, predation and energetic eciency of locomotion Blanchard et al.; 11. Translating primate locomotor biomechanical variables from the laboratory to the eld Schmitt. Mfb S I EReview of: Seeds of Amazonian Plants, by Fernando Cornejo and John Janovec, 2010. Princeton, Princeton University Press. ISBN 978-0-691-14647-8 (Paperback), 978-0-691-11929-8 (Hardcover). 155 pages, 750 colour illustrations, 2 b/w plates. Price: US-$ 35.00 (Pbk.), US-$ 75.00 (Hard.).
78 the descriptive part. Since many plant families possess specic seed characteristics that are easily recognized, the arrangement of families in alphabetic order makes it also possible to go strait to a family and then search for the correct genus. When I browsed through this book for the rst time, I immediately recognized many seeds that my students and I had recovered from tamarin faeces and feed ing residuals during eld work in north-eastern Per. is book will be useful to every primatologist working on the feeding ecology of or on seed dispersal and seed predation by New World monkeys and who needs to get a decent taxonomic identication of plants consumed, dispersed or preyed by their study subjects. Given the huge diversity of Neotropical plants, this guide cannot be comprehen sive. e range of families and genera is certainly biased towards western Amazonia, where the eld work was performed upon which this book is based. But many fami lies and genera dealt with in this book have a very broad distribution, even ranging into Mesoamerica, so the book will be useful over a wider geographic area. As with van Roosmalens Fruits of the Guianan Flora (which is also restricted to a specic area) Seeds of Amazonian Plants will at least help to get a rst identication in the eld in many if not in most cases. In sum, I highly recommend this book to Neotropical primatologists. Seeds of Amazonian Plants will make ecological eld work on New World monkeys a bit easier. Eckhard W. Heymann Abteilung Verhaltenskologie & Soziobiologie, Deutsches Primatenzentrum, Kellnerweg 4, D-37077 Gttingen, e-mail:
79 dos Santos Neves N, Feer F, Salmon S, Chateil C, Ponge JF. 2010. e impact of red howler monkey latrines on the distribution of main nutrients and on topsoil proles in a tropical rain forest. Austral Ecol. 35(5): 549559. Fernandez-Duque E, de la Iglesia H, Erkert HG. 2010. Moonstruck primates: owl monkeys ( Aotus) need moon light for nocturnal activity in their natural environment. Plos One. 5(9): Article No.: e12572. Ferrari SF, Coutinho PEG, Correa HK. 2010. Congenital digital aplasia in a free-ranging group of silvery marmo sets, Mico argentatus. J. Med. Prim. 39(3): 166169. Ferrari SF, Sena L, Schneider MPC, Silva JS Jr. 2010. Ron dons marmoset, Mico rondoni sp., from southwestern Brazilian Amazonia. Int. J. Primatol. 31(5): 693714. Ferrari SF, Chagas RRD, Souza-Alves JP. 2010. Line tran sect surveying of arboreal monkeys: problems of group size and spread in a highly fragmented landscape. Am. J. Primatol. 72(12): 11001107. 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Examining the linkages between community benets, place-based meanings, and conser vation program involvement: a study within the Community Baboon Sanctuary, Belize. Soc. & Nat. Resources 23(6): 542556.ASelected abstracts of oral presentations relating with neo tropical primates from the XXIII International Primatological Society congress, Kyoto, Japan, 1218 September 2010. Abbott DH, Tannenbaum PL, Schultz-Darken NJ, Saltzman W, Woller MJ. 2010. In vivo and in vitro approaches to direct assessment of hypothalamic release of gonadotropin releasing hormone in marmosets. Addessi A, Paglieri F, Focaroli V, Visalberghi E. 2010. An egg today? Or a hen tomorrow? Delay discounting for primary and secondary rewards in capuchin monkeys. Ameca y Juarez E, Rodriguez-Luna E, Mace G. 2010. Vi ability assessment for a population of the Mexican howler monkey: potential threats and performance of dierent management interventions. Amici F, Aureli F, Capellini I, Call J. 2010. 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81 Biondi L, Wright K, Fragaszy DM, Izar P. 2010. Bipedal posture and terrestriality in bearded capuchin monkeys. Blair ME, Melnick DJ. 2010. Landscape heterogeneity inuences gene ow in the Central American squirrel monkey. Boubli JP, Alfaro JL, Farias I. 2010. Capuchins of the pan tepuy biogeographic region: Cebus apella, C. olivaceus and C. albifrons. Campos FA, Jack KM. Distribution and abundance of the critically endangered Ecuadorian white-fronted capuchin ( Cebus albifrons aequatorialis) in western Ecuador. Csar C, Young R, Byrne R, Zuberbhler Z. 2010. Vocal communication in Callicebus: new perspectives for the study of human language evolution. Chikhi L, Sousa BDV, Luisi P, Goossens B, Beaumont MA. 2010. e eect of the demographic history and sam pling sheme on the detection of spurious bottlenecks in fragmented and structured populations. Cornejo FM, Tello C, Chocce M, Vega N. 2010. Geo graphical distribution and state of conservation of the yellow tailed woolly monkey Oreonax avicauda in northeastern Peru. Cortes-Ortiz L. 2010. Hybridization and gene introgres sion in Mexican howler monkeys. Cristobal-Azkarate UJ, Dunn JC, Garcia J, Osorio D, Vea JJ. 2010. Levels of parasitisation on howler monkeys: inter and intra annual variations between two groups living in forest fragments in Mexico. Cronin KA, Schroder KKE, Snowdon CT. 2010. Prosocial behavior emerges independent of reciprocity in cotton tamarins (Saguinus oedipus). DeLuycker AM. 2010. Observations on a daytime birth in the wild of titi monkey (Callicebus oenanthe) and subsequent male paternal care. Ferrari SF, Santos EM, Freitas EB, Souza-Alves JP, Jerusa linsky L, Mendes RB, Chagas RRD. 2010. Living on the edge: habitat fragmentation at the interface of the semiarid zone of the Brazilian northeast. Ferreira GR, Enidio RA. 2010. Capuchins in northeastern Brazil caatinga: limits of occurrence, area of use and diet. Fruteau C, Perry S, Petit O. 2010. Comparing the manipu lative abilities of Cebus apella and Cebus capucinus: insights into their cognitive skills? Fuchs E, Plassmann K. 2010. Remote registration of eeg and core body temperature in marmoset monkeys. Fuchs E, Schlumbohm C. 2010. Programming obesity in marmoset monkeys. Fujita K. 2010. Memory awareness in tufted capuchin monkeys. Garber PA, Kowalewski MK. 2010. Why leave feeding patch: patch choice, patch depletion and nutrient mixing in Peruvian tamarin monkeys ( Saguinus mystax and S. fuscicollis). Goncalves Da Silva A, Perez-Sweeney B, Martins CS, Medici EP, Nava A, Valladares-Pauda CB, Melnick DJ, 2010. Landscape connectivity dierences in black lion tamarins (Leontopithecus crysopygus) and ungulates across the fragmented landscape of the Pontal region, brazil. Gunhold T, Bugnyar T. 2010. Transmission of experi mentally-seeded information in free-living common marmosets. Hiramatsu C, Melin AD, Aureli F, Schaner CM, Vo robyev M, Kawamura S. 2010. Challenging advantange of trichromacy in fruit foraging behavior of wild spider monkeys. Hopkins ME. 2010. e importance of location: evaluat ing mantled howler monkeys spatial foraging decisions for neighborhood eects. Isler K, van Schaik CP. 2010. Energetic eects of coopera tive breeding on brain size and fertility. Izar P, Verderance MP, Mendoca-Furtado O. 2010. So ciecology of two species of tufted capuchin monkeys: Cebus libidinosus and C. nigritus. Jerusalinsky L. 2010. Strategic planning for Brazilian pri mates conservation: advances and priorities. Kap YS, Jagessar SA, Heijmans N, van Driel N, Laman JD, t Hart BA. 2010. Unreaveling the key pathogenic mechanisms in a marmoset model of multiple sclerosis. Kawamura S, Hiwatashi T, Okabe Y, Tsutsui T, Hira matsu C, Melin AD, Oota H, Schaner CM, Aureli F, Fedigan LM, Innan H. 2010. A population genetic test of balancing selection for color vision variation in new world monkeys. Kitchen DM, Bergman TJ, Cortes-Ortiz L. 2010. Acoustic variation among hybrid and purebred black and mantled howler monkeys ( Alouatta spp.) within and outside a Mexican hybrid zone. Kuroshima H, Paukner A, Kaiser I, Suomi SJ, Fragaszy DM, Fujita K. 2010. Perception of others actions: eect of ones own actions in capuchin monkeys. Lynch-Alfaro J, Schwochow D, Santini F, Alfaro ME. 2010. Capuchin phylogenetics and statistical phylogeography: implications for behavioral evolution. MacKinnon KC. 2010. Home range use and patterns of social interactions for Cebus apella at Brownsberg, Suriname. Madden M, Jordan T, Hinlev AJ, Bernardes S, TavaresRochas Y, Izar P. 2010. Geospatial modeling of factors predicting bearded capuchin tool use in Boa Vista and across e Cerrado of Brazil. Maldonado AM, Nijman V, Breader SK. 2010. Trade in night monkeys in the Brazil-Colombia-Peru tri-border area: international wildlife trade regulations are ineec tively enforced. Mano S. 2010. Polymorphism and migration rate dier ence in fragmented habitat. Massarotto VM, Carvalho FM, Arakaki PR, Calvi TS, Nichi M, Guimaraes MABV, Miglino MA, Valle RR. 2010. Collection and analysis of semen from Callithrix penicillata. Matsunami H, Adipietro KA, Zhuang H. 2010. Function al evolution of primate odorant receptors. Matsuno T, Fujita K. 2010. Body perception in tufted capuchin monkeys (Cebus apella).
82 Melin AD, Fedigan LM, Parr N, Kawamura S. 2010. Di etary selectivity by white-faced capuchins: how impor tant are colorful fruits? Melo FR. 2010. Conservation of the northern muriqui, Brazil. Mendoca-Furtado O, de Sousa MBC, Izar P. 2010. Cor tisol levels in three species of tufted capuchin monkeys living in dierent habitats. Montague MJ, Di Fiore A. 2010. e implications of color vision on prey capture trategies for wild squirrel monkeys ( Saimiri sciureus). Morimoto Y, Fujita K. 2010. Capuchin monkeys reason about emotional valence of an object which elicits con specic expressions. Muehlenbein MP. 2010. Do the benets of primate tour ism outweigh the costs of potential anthropozoonoses and stressed animals. Mundy NI. 2010. Polymorphic colour vision compared among lemurs and new world monkeys. Nakamura K, Takemoto A, Koba R, Izumi A. 2010. PC-based automated apparatus to test cognitive abilities of marmoset monkeys. Notman HGW, Pavelka MSM. 2010. Demography, diet and range size in a population of black-handed spider monkeys (Ateles georoyi yucatanensis) from Belize. Papworth SK, Milner-Gulland EJ, Slocombe K. 2010. Changes in dusty titi monkey ( Callicebus cupreus discol or) dawn choruses with hunting pressure from human hunters. Paukner A, Ferrari P, Visalberghi E, Suomi SJ. 2010. Imitation and social bonding in tufted capuchin monkeys. PerezRuiz AL, Mondragon R. 2010. Feeding party size and party composition in relation to food availability in free-ranging spider monkeys. Pessoa DMA, Pessoa VF. 2010. e visual ecology of neo tropical primate: food selection, predation avoidance and reproduction. Polizzi di Sorrentino E, Schino G, Visalberghi E; Aureli F. 2010. Reconciliation reduces post-conict anxiety in capuchin monkeys. Pozzi L, Hodgson JA, Bergey C, Disotell TR. 2010. Dating the primate tree: new insights on primate origins from complete mitochondrial genomes. Presotto A, Biondi LM, Verderance MP, Izar P. 2010. Ca puchin monkeys (Cebus libidinosus) navigation system in a semi-arid habitat, Boa Vista, Piaui-Brazil. Ramos-Fernandez G. 2010. Using social network metrics to explore the ecological determinants of grouping pat terns in spider monkeys (Ateles spp.) Rapaport L. 2010. Allocation of maternal and allomaternal foraging assistance in wild golden lion tamarins. Rodriguez-Luna E, Shedden A, Solorzano B. 2010. A re gion-wide review of Mesoamerican primates and prioritizing for conservation. Sabbatini G, Truppa V, Gambetta B, Hribar A, Call J, Visalberghi E. 2010. Do capuchin monkeys ( Cebus apella) and chimpanzees (Pan troglodytes) show analogical rea soning when using tools? Sato Y, Fujimori Y, Hayashi M. 2010. Laterality of manual actions in substrate use by captive tufted capuchin mon keys ( Ce bus apella). Shedden A, Ellis EA, Rodriguez-Luna E. 2010. Spatial use and route selection of translocated howler group: conser vation implications. Smith AC, Surridge AK, Prescott MJ, Osorio D, Mundy MI, Buchanan-Smith HM. 2010. e eect of sex and colour vision status on insect prey capture eciency by captive and wild tamarins ( Saguinus spp.). Solorzano-Garcia B, Ellis EA, Rodriguez-Luna E. 2010. Comparative study of primate populations in fragmens of Los Tuxtlas Biosphere Reserve, Mexico: Landscape dy namics and habitat availability (19862007). Spagniletti N, Visalberghi E, Presotto A, Izar P. 2010. Spatial distribution of resources for the occurrence of nut cracking with tools in wild bearded capuchins ( C ebus libidinosus). Spehar SN, Di Fiore A, Link A, Aureli F, Ramos-Fernan dez G, Schaner CM, Shimooka Y, Vick L, Wallace RB: 2010.Why scarcity: how does the number of males in a group inuence spider monkey society? Stone BW, Jeyaraj T, Fragaszy D. 2010. How do capuchins stack up against chimpanzees and humans? Assessing combinatory manipulation in a block stacking task. Takimoto A, Fujita K. 2010. Do capuchin monkeys behave prosocially to others at a small expense of their reward in an experimental food sharing situation? Talbot CF, Williams LE, Brosnan SF. 2010. Responses to inequity in squirrel monkeys, Saimiri spp. Talebi MG, Melo FR, Martinez R. 2010. Building capac ity in primatology: a new series of primat eld courses in Brazil. Tatsuta I, Kutsukaka N, Kawasaki A, Yokoyama C, Onoe H, Hasegawa M. 2010. Paternal changes in body weight during paternal care period in cooperatively breeding common marmosets. Tomioka I, Sasaki E. 2010. Recent progress in reproductive technologies based on the common marmoset ( Callithrix jacchus): application of ES and iPS cells. Truppa V, Garofoli D, Piano E, Gastorina G, Natale F, Visalberghi E. 2010. Same/dierent concept learning in matching-to-sample tasks by capuchin monkeys. Urbani B, Garber PA. 2010. Spatial mapping in wild whitefaced capuchin monkeys (Cebus capucinus). Watson CFI, Morris K, Caldwell CA. 2010. Social conta gion as a potential mechanism for transmission of social culture in common marmosets. Williams LE, Schapiro SJ, Nehete PN, Behete B, Lambeth S. 2010. Eects of relocation on immunological and physiological measures in two captive non-human primate species: squirrel and owl monkeys. Winandy MM, Izar P. 2010. Juvenile capuchin monkeys ( Cebus apella) dier from adults on foraging behavior. Wright K, Wright B, Fragaszy D, Izar P, Norconk M. 2010. Is a xed or plastic response to ecological variation the key to capuchin adaptability? Yokoyama C, Onoe H. 2010. Molecular brain of personal ity traits in common marmosets.
83 Mf 2011Joint Meeting of 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 -30, 2011. For more information and registration go to: http://www.indiana.edu/~behav11 45th Congress of the International Society for Applied Ethology e 45th 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 scientic evaluation of behavior, welfare and enrichment; and some of the specic topics: Zoo animal behavior, Labo ratory animal behavior, Engineering environments & measurement technologies for science and welfare pain, distress & humane end-points. Abstract submission closes February 14th. For more information visit http://www. applied-ethology.org/isaemeetings.htm 10th International Conference on Environmental Enrichment e 10th International Conference on Environmental En richment will take place in the Benson Hotel, Portland, Oregon, USA from August 14 to 19, 2011. e conference is sponsored by the Oregon National Primate Research Center and the Oregon Zoo. For more information go to http://bit.ly/icee2011 AP Summer Course Husbandry of Rescued Primates e AP Summer Course, sponsored by the AAP, Sanctuary for Exotic Animals, will be held in the AAP Sanctuary for Exotic Animals at Almere, e Netherlands from August 21 to 26, 2011. For more information please visit http:// www.aap.nl/english/aap-summer-course.html 2011 AAZK Conference e AAZK Conference, sponsored by the American Asso ciation of Zoo Keepers, will take place in San Diego, Cali fornia, USA, from August 24 to 28, 2011. For more infor mation go to http://sdaazkconf.wordpress.com/ IV Congress of the European Federation for Primatology III Iberian Primatological Conference e IV congress of the European Federation for Primatol ogy and the III Iberian Primatological conference, spon sored by the APP-Associao Portuguesa de Primatologia, will take place in Almada, Portugal from September 14 to 17, 2011. For more information visit http://apprimatologia. com/Actividades/CEP2011.aspx 34th Meeting of the American Society of Primatologists e meeting of the American Society of Primatologists will be held in Austin, Texas, USA, from September 1619, 2011. Preliminary abstracts for symposia and workshops should be submitted by January 15, 2011. General ab stracts deadline March 12, 2011. For more information go to http://www.asp.org/asp2011/index.htm2012III Congreso Colombiano de Primatologaes-ES La Asociacin Primatolgica Colombiana junto con la es-ES Universidad del Norte y la Fundacin Proyecto Tit, ores-ES -es-ES ganizarn el IIIes-ES es-ES Congreso Colombiano de Primatologaes-ES es-ES dentro del marco del evento es-ES Biodiversidad: Recurso Estrates-ES-es-ES gicoes-ES, el cual se llevar a cabo en Abril de 2012, en la ciudad es-ES de Barranquilla Colombia. XXVI Congress of the International Primatological Society e XXVI congress of the International Primatological Society will be held at the World Trade Center, Veracruz, Mexico, from August 1317, 2012. For more information visit http://www.citrouv.edu.mx/ips2012/
pt-BRScope 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.pt-BR Submissions Please send all English and Spanish contributions to: Erwin Palacios, Conservacin Internacional Colombia, Carr era 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. 17(2), December 2010ContentsArticlese Conservation Status of Callicebus caquetensis (Pitheciidae): A New Species in Southern Caquet Department, Colombia Javier Garca, omas R. Deer and Marta L. Bueno . ........................................................................................................................ 37 A Morphological Analysis of Some Species of Callicebus, omas, 1903 (Pitheciidae Callicebinae) Paulo Auricchio . ............................................................................................................................................................................... 47 Seed Dispersal Patterns in Two Closely Related Howler Monkey Species (Alouatta palliata and A. pigra): A Preliminary Report of Dierences in Fruit Consumption, Traveling Behavior, and Associated Dung Beetle Assemblages Katherine R. Amato and Alejandro Estrada . .................................................................................................................. ..................... 59Short ArticlesOccorrncia de Primatas No Parque Estadual do Ibitipoca e Entorno, Estado de Minas Gerais, Brasil Denize Fontes Nogueira, Daniel da Silva Ferraz, Aquila Fialho Oliveira, Fernanda Pedreira Tabacow Sara Machado de Souza Amncio e Fabiano Rodrigues de Melo . ......................................................................................................... 67 Predation of adult palms by black-capuchin monkeys ( Cebus nigritus) in the Brazilian Atlantic Forest Carlos Rodrigo Brocardo Henrique Santos Gonalves, Valesca Bononi Zipparro and Mauro Galetti . ..................................................... 70 Noteworthy record of a black howler monkey (Alouatta caraya) from the central dry Chaco of Paraguay Anthony J. Giordano and Warren B. Ballard . ..................................................................................................................................... 74 Preliminary Observations of Napo Tamarins (Saguinus graellsi ) and Notes on Primates of Wildsumaco Wildlife Sanctuary E. Natasha Vanderho and Jonas Nillson . .......................................................................................................................................... 75News . ............................................................................................................................................................................................ 76Recent Publications . ................................................................................................................................................................... 77Meetings . ..................................................................................................................................................................................... 83
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