Check List 9(1): 113–115, 2013 © 2013 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution
n Primates, Pitheciidae, Callicebus barbarabrownae istributio D Hershkovitz, 1990: New localities for the critically raphic g endangered titi monkey in the São Francisco basin, state of
eo 1,2 1,3* 1,3,4 G
n Sergipe, Brazil o Eduardo La Noce Marques , Raone Beltrão-Mendes and Stephen Francis Ferrari otes 1 Universidade Federal de Sergipe, Programa de Pós-Graduação em Ecologia e Conservação da Caatinga, Av. Marechal Rondon. CEP 49100-000. N São Cristóvão, SE, Brazil. 2 Reserva Biológica do Lago Piratuba (SUPES/ICMBio), Rua Hamilton Silva. CEP 68906-440. Macapá, AP, Brazil. 3 Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Cidade Universitária. CEP 58059-900. [email protected]ão Pessoa, PB, Brazil. 4 Universidade Federal de Sergipe, Departamento de Biologia, Av. Marechal Rondon. CEP 49100-000. São Cristóvão, SE, Brazil. * Corresponding author. E-mail: Abstract: Barbara Brown’s titi monkey, Callicebus barbarabrownae
Hershkovitz, 1990, appears to be endemic to the Caatinga of northern Bahia and western Sergipe, although few data are available for the northernmost portion of its range. The present study presents seven new occurrence records of the species, in the São Francisco basin of northern Sergipe, extending its range in the state over a distance of more than 50 km from west to east. This represents an important extension of the known range and total number of populations of this critically endangered primate species.
Barbara Brown’s titi monkey, Callicebus barbarabrownae Hershkovitz, 1990, was originally recorded from Lamarão in the Brazilian state of Bahia (see Hershkovitz 1990), 550 mm, and a mean temperature of around 26 °C. In the first phase of the survey, forest fragments conducted some 20 years later (Printes et al. 2011), and were selected through the visual interpretation of recent littlealthough was the known first of systematic its distribution geographic in the surveyneighboring was satellite images (LandSat 5 images fromC. 2006) barbarabrownae of the study area,within which the studypermitted area. the Only identification fragments with and amapping minimum of potentialarea of 20 sites hectares for thewere occurrence included in of the analysis, as this state of Sergipe prior to the present study. The species appears to be restricted to semi-aridet al. 2011), arboreal a fact Caatinga that size in Callicebus habitats (Marinho-Filho and Veríssimo 1997; Kobayashi represents the approximate lower limit of home range and Langguth 1999;et al Printes species (Bicca-Marques & Heymann in andcontributes fragmentation, to its classification given that more as critically the 40% endangered of this biome by waspress). indicated During by fieldwork local residents. at some sites, however, smaller the IUCN (Veiga . 2008)et al due. 2003) primarily and less to habitat than 1% loss is fragments were surveyed whenever the presence of titis et al. 2005), which has a direct effect on Callicebus is degraded (Castelletti During the second (field) phase, the presence of protected (Leal recordings at of the the sites territorial identified vocalizations in the first of phase the genus was the number of populations surviving in the wild. evaluated through the use of playback surveys, in which In the present study, the Caatinga of the São Francisco basin in the northern extreme of the state of Sergipe (Figure were broadcast through a megaphone (CSR Hmp 1503; the1) was northern surveyed limit systematically of the genus for Callicebus the identification (personatus of 20w) in order to elicit a response from titi groups within new populations of titis. The São Francisco River forms andauditory advancing range. inTitis the will direction normally of thereact source. incisively Playbacks to the havepotential been presence used successfully of conspecific in intruders a number by ofvocalizing surveys species group) in eastern Brazil (Hershkovitz, 1990). The of Callicebus primary aim was to locate all the populations remaining et al in the Caatinga domain, as defined by IBGE (2004), within et al populations et al. 2011). (Rowe & Martinez 2003; the area demarcated for the study, in order to provide a Jerusalinsky . 2006; Martinez & Wallace 2007; Aldrich database for the estimation of metapopulation parameters. were. 2008; visited Printes and surveyed by carefully walking along The study area comprises the municipalities of Graccho existingIn the trails field, at fragments the edge and identified interior byof localthe forest, residents and Cardoso (10°13’ S, 37°11’ W), in the south,Sertão and Canindé do São Francisco (9°39’ S, 37°47’ W) in the north, and represents the highest part of the state, the plateau, broadcasting the playback at 15-minute intervals. Surveys with altitudes reaching a maximum of 715 m a.s.l. in the were conducted between 06:00-09:00 h et and al . 15:00-2011). Serra da Guia (9°57’ S, 37°52’ W). The region’s climate is 17:00 h, when titis are normally more responsive to the typical of the Caatinga – hot, semi-arid (Köppen’s BSsh’ playbacks (Melo and Mendes 2000; Soares type) – with a mean annual precipitation of approximately When no response was obtained during the initial survey,113 Marques et al. | New localities for Callicebus barbarabrownae in northeastern Brazil
km south of the southernmost C. barbarabrownae locality
Siterecorded 1: Fazenda in the present “Tonho” study (Figure 1).
Very small and highly degraded fragment of arboreal Caatinga habitat surrounded by pasture, and used by the local population as a source of firewood, which poses a Sitegrave 2: threat Fazenda to the João long-term de Lima survival of the forest.
Habitat at an advanced stage of succession, with a Fragment of hyperxerophilous arboreal Caatinga.
relatively tall canopy of up to 10 m in height located within a matrix of pasture. The principal threat is the extraction Siteof firewood. 3: Fazenda Paturi
Fragment of hyperxerophilous arboreal Caatinga at an intermediate stage of succession. The fragment is surrounded by pasture, and the primary threat to the habitat appears to be incursions by cattle, which may be suppressing the recruitment of seedlings in many areas. Evidence was also found of the extraction of firewood, Figure 1. such as recently-cut tree stumps, and hunting (baiting ▲ = Callicebus barbarabrownae Map of the São C. Francisco barbarabrownae basin in not northern found), localities Sergipe, Siteplatforms) 4: Mata within do Enoc the area of the fragment. atshowing which C. the barbarabrownae sites surveyed ( during● the present study ( recorded; + = Callicebus coimbrai ) was recorded in previous studies (Sousa 2003; Jerusalinsky et al. 2006) and the nearest site at which Very small fragment of hyperxerophilous arboreal was recorded in the São Francisco basin ( ) by Beltrão-Mendes Caatinga at an advanced stage of degradation, similar to (2010) and Santos Junior (2010). The sites are numbered as in Table 1. itsthat isolation of site 1.(over The 10fragment km from is thelocated nearest within area a ofmatrix natural of Callicebus was pasture and subsistence plots, and its primary threat is the site was resurveyed on subsequent days following the same procedure until either the presence of Sitehabitat 5: Assentamento with known population Raimundo – site Monteiro 2). confirmed or the site had been surveyed on four separate occasions, when fieldwork was interrupted and the site was recorded as not having a population of titis. When a Relatively large, but poorly-preserved fragment of response was obtained, efforts were made to visualize the arboreal Caatinga. The central portion of the fragment is observationsanimals, and verifyin different the minimum areas of numberthe forest. of groups within thecharacterized forest are by at dense an intermediate undergrowth stage reflecting of succession. intense the area, based on simultaneous responses to playbacks or anthropogenic pressure, although some portions of
A total of 36 localities were visited within the study thusThe fragmentconstituting is the surrounded major threat by pastureto the fragment. and numerous area between October, 2008, and May, 2010. The presence subsistence plots, many of which are expanding illegally, of these titi monkeys sites (1, was 4, and confirmed 5), although at seven their of characteristic these sites Sites 6 and 7: Serra Azul and Serra da Beleza (Table 1). Monkeys were observed directly at only three genus. vocalization is an unmistakable sign of C.the barbarabrownae presence of the Two medium-sized fragments of arboreal Caatinga based onFor the sites fact at that which this isthe the animals only member were not of theobserved genus located close to one another, but in distinct municipalities. directly, the species was identified as These fragments form the forest reserve of the Projeto extensivelyde Assentamento degraded, José even Pedro though Teixeira, the habitat an agricultural is at an that occurs in the Caatinga,et al and that all sites were within settlement. Located on hilltops, the fragments are the general area of the geographic rangeC. coimbrai of the species,, which as is defined by Printes . (2011). The only other member remainingintermediate habitat successional was encroached stage. The bysurrounding an uncontrolled matrix of the genus found in Sergipe is is formed by pastures and subsistence plots. Part of the restricted to the Atlantic Forestet alecosystems in the eastern and southern extremes of the state (Kobayashi and burn-off of agricultural land in 2005. ofLangguth C. barbarabrownae 1999; Jerusalinsky . 2006). The species can criticallyThe present endangered study C. represents barbarabrownae an important in the Brazilian advance be distinguished by the predominantly buffy coloration in our knowledge of the geographic distribution of the , primarily on theet forehead, al crown, nearesttrunk, andknown limbs, record with of palerC. coimbrai subterminal pheomelanic Northeast, but the results also serve to reinforce the banding of the hairs (van et Roosmalen al. ., 2002). The generally precarious circumstances of most of the in the São Francisco remaining populations. While a total area of 955.5 ha basin of Sergipe (Marques in press.) is more than 50 was identified, only three fragments were over 100 ha 114in Marques et al. | New localities for Callicebus barbarabrownae in northeastern Brazil area, all of which are degraded and suffer some form of
the present study, most large fragments are separated by C.ongoing barbarabrownae anthropogenic impact. In addition, only seven of distances of a number of kilometers, which are prohibitive the 36 sites (19.4 %) surveyed contained populations of for the effective dispersal of titis. The most serious threat . As populations were observed in very to all these populations may nevertheless be the lack of thansmall fragment fragments, size of lessper thanse 10 ha, the absence of theCallicebus species official protection, not least because the only officially from a given site appears to be related to factors otheret al. protected areaC. in barbarabrownae northern Sergipe – the Grota do Angico . Given the dynamics of Natural Monument in Poço Redondo – does not contain a populations in fragmented landscapes (Jerusalinsky population of . The long-term survival 2006), the critical factor for the survival of populations of this species will ultimately depend on the development may be the distance between fragments. Within the area of of an effective program of metapopulation management. Table 1. Callicebus barbarabrownae
Details of the sites at which populations were recorded in the Caatinga of the São Francisco basin in northern GEOGRAPHIC ALTITUDE FRAGMENT SIZE DISTANCE TO Sergipe,SITE Brazil. LOCALITY MUNICIPALITY COORDINATES (M) (HA) NEAREST FRAGMENT (KM) 1 228 2.3 0.5 2 253 0.8 Fazenda ‘Tonho” Monte Alegre de Sergipe 10°03’ S, 37°36’ W 3 305 0.5 Fazenda João de Lima Porto da Folha 10°01’ S, 37°28’ W 163.0 4 135 3.0 0.8 Fazenda Paturi Canindé do São Francisco 9°47’ S, 37°57’ W 266.0 5 381.0 3.8 MataMonteiro do Enoc Porto da Folha 10°02’ S, 37°22’ W Assentamento Raimundo Monte Alegre de Sergipe 10°04’ S, 37°42’ W 268330 42.5 1.0 Serra da Beleza 1.0 6 Serra Azul Canindé do São Francisco 9°46’ S, 37°52’ W 7 Poço Redondo 9°45’ S, 37°51’ W 306 97.7 Acknowledgments: Callicebus modestus and We are grateful to FAPITEC/SE and CAPES for Martinez,Callicebus J. and olallae R.B. . Wallace.Neotropical 2007. Primates Further Notes on the Distribution masters stipend to ELNM and RBM, the Brazilian National Research of the Bolivian Endemic Titi Monkeys, Council, CNPq for stipend (process 503122/2010-6) to RBM, CNPq de Callicebus nigrifrons 14(2):playbacks 47-54. In (projects 302747/2008-7 and 303994/2011-8), Doces Matas Project, Melo, F.R. and S.L. Mendes. 2000.A Emissão Primatologia de gritos no Brasil longos 7 por grupos CODEVASF/MMA, SEMARH Sergipe, and the Boticário Foundation e suas reações a ; p. 215-222 C. (Project 0846_20092). We also thank Leandro Jerusalinsky (Brazilian Alonso and A. Langguth (ed.). . João Pessoa: Primate Research and Conservation Center – CPB/ICMBio), Crizanto Editora UFPB/SBPr.Cuadernos de Herpetología Brito,Literature and Evelyn Cited Borges for their help with fieldwork. Montero, R. 1996. Lista de localidades de Amphisbaenia de la República Argentina. Cuadernos de Herpetologia 10(1/2): 25-45. Montero, R. and G.J. Terol. 1999. Los Amphisbaenidae en Paraguay, listado Aldrich,Callicebus B.C., L.oenanthe Molleson and K.A.L. Nekaris. 2008. Vocalizations as a geográfico. 13(1/2): 89-95. conservation tool: an auditoryContributions survey of to the Zoology Andean titi monkey Peters, J.A. and B. Orejas-Miranda.United States 1970. National Catalogue Museum of the Bulletin Neotropical B Thomas, 1924 (Mammalia: Primates: Pitheciidae) Squamata: part II lizards and amphisbaenians – with new material titiat Tarangue, monkeys (genusNorthern Callicebus Peru. In 77(1): 1-6. by P. E. Vanzolini. 297: icca-Marques, J.C. and E.W. Heymann.Evolutionary 2013. Ecology Biology andand behaviourConservation of VIII+25+1-293.status of the critically endangered bold titi monkey Callicebus of the Titis, Sakis, and Uacaris.); p. 1-15 L.M. Veiga, A.A. Barnett, S.F. Printes,barbarabrownae R.C., A.B. Rylands and J.C. Bicca-Marques.. Oryx 2011. Distribution Press.Ferrari and M.A. Norconk (ed.) Callicebus sightings in Bolivia, Peru and Cambridge, Cambridge University2003. Neotropical of north-east Primates Brazil 45(3): 439-443. Rowe, N. and W. Martinez. 2003. Castelletti, C.H.M.,In A.M.M. Santos, M. Tabarelli and J.M.C. Silva.Ecologia e Ecuador. 11(1): 32-35.Callicebus coimbrai e Callithrix ConservaçãoQuanto ainda da restaCaatinga da Caatinga? Uma estimativa preliminar; p. Soares,jacchus N.M., E.M. Santos Jr.,In R. Beltrão-Mendes and S.F. Ferrari. 2011. UsoA 719-734 I.R. Leal, M. Tabarelli and J.M.C Silva (ed.). Primatologiado habitat e reações no Brasil ao 12 playback em . Recife: Editora Universitária da UFPE.Fieldiana ; p. 303-307 J.M.D. MirandaCallicebus and Z.M.B. coimbrai Hirano (ed.). Hershkovitz,Zoology P. 1990. Titis, new world monkeys of the genus Callicebus Neotropical Primates. Curitiba: UFPR/SBPr. (Cebidae,Mapa Platyrrhini): da cobertura a preliminary vegetal dos biomas taxonomic brasileiros review. (shapefile) . Sousa, M.C. 2003. Distribuição do guigó ( ) no Estado 5: 1–109. Mendes.de Sergipe. 2008. Callicebus barbarabrownae 11: 89-91.. In IUCN Red IBGE. 2004. Veiga,List L.M., of Threatened R.C. Printes, Species. A.B. Rylands, V. 2011.2 M.C. Kierulff, M.M. Oliveira and S.L. Downloaded in
In Press. 38: 429-433. Marques, E.L.N., L. Jerusalinsky, J.C.A.G. Rocha, P.M. Santos, R. Beltrão- Received: July 2012 Mendes and S.F. Ferrari. Primates, Pitheciidae,Check List Callicebus. Accepted: November 2012 coimbrai Kobayashi and Langguth 1999: New localities for an Published online: March 2013 endangered titi monkey in eastern Sergipe, Brazil. Editorial responsibility: Fabio Oliveira do Nascimento
115 Check List 9(1): 113–115, 2013 © 2013 Check List and Authors Chec List ISSN 1809-127X (available at www.checklist.org.br) Journal of species lists and distribution
n Primates, Pitheciidae, Callicebus barbarabrownae Hershkovitz, 1990: New localities for the critically
istributio endangered titi monkey in the São Francisco basin, state of D Sergipe, Brazil raphic g
eo Eduardo La Noce Marques 1,2, Raone Beltrão-Mendes 1,3* and Stephen Francis Ferrari 1,3,4 G n o
1 Universidade Federal de Sergipe, Programa de Pós-Graduação em Ecologia e Conservação da Caatinga, Av. Marechal Rondon. CEP 49100-000.
otes São Cristóvão, SE, Brazil.
N 2 Reserva Biológica do Lago Piratuba (SUPES/ICMBio), Rua Hamilton Silva. CEP 68906-440. Macapá, AP, Brazil. 3 Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza, Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Cidade Universitária. CEP 58059-900. João Pessoa, PB, Brazil. 4 Universidade Federal de Sergipe, Departamento de Biologia, Av. Marechal Rondon. CEP 49100-000. São Cristóvão, SE, Brazil. * Corresponding author. E-mail: [email protected]
ERRATUM
In page 114 there is a mistake in the legend of Figure 1, We regret this error. which should be as: The authors,
April 2013
Figure 1. Map of the São Francisco basin in northern Sergipe, showing the sites surveyed during the present study (▲ = Callicebus barbarabrownae recorded; + = C. barbarabrownae not found), localities at which C. barbarabrownae (●) was recorded in previous studies (Sousa 2003; Jerusalinsky et al. 2006) and the nearest site at which Callicebus coimbrai was recorded in the São Francisco basin ( ) by Marques et al. (in press.). The sites are numbered as in Table 1.