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First record of the Peruvian yellow-tailed woolly Lagothrix flavicauda in the Región Junín, Peru

S EAN M. MC H UGH,FANNY M. CORNEJO,JASMINA M C K IBBEN,MELISSA Z ARATE C ARLOS T ELLO,CARLOS F. JIMÉNEZ and C HRISTOPHER A. SCHMITT

Abstract The Critically Endangered Peruvian yellow-tailed Cornejo et al., ). Research on L. flavicauda has focused Lagothrix flavicauda was presumed to only on sparse museum and genetic samples to elucidate its taxo- occur in the tropical montane cloud forests between the nomic placement. Phenetic and morphological analyses had Marañón and Huallaga rivers in northern Peru. Here we placed it in the monospecific genus Oreonax (Thomas, ; report the discovery of a population to the south of its Groves, ), or as a sister species to the other woolly previously known range, in the Región Junín. During monkeys in the genus Lagothrix (Fooden, ; Matthews September–December  we carried out transect surveys & Rosenberger, ; Rosenberger & Matthews, ). to record large present near the village of San Recent molecular genetic analyses support the latter (Ruiz- Antonio in the district of Pampa Hermosa, at ,–, m Garcia et al., ; Di Fiore et al., ). Knowledge of altitude. We recorded five species during transect this species comes mainly from long-term study sites in surveys. Lagothrix flavicauda was seen four times, and remnant high-elevation tropical Andean forests in the appeared phenotypically distinct from populations to the Región Amazonas and Región San Martín in Peru (Graves north, with notable white patches above each eye and a &O’Neil, ; Leo Luna, , ; Butchart et al., ; reduced yellow patch at the end of the . The presence DeLuycker, ; Cornejo, ; Shanee et al., ; of L. flavicauda in Junín extends its known geographical Shanee, ; Shanee et al., a,b; Allgas et al., ). range over  km southwards from the closest previously The last assessment of viable habitat in this area, in , known population in the Huánuco region, and presents a estimated a reduction by almost % since surveys in  unique opportunity for the conservation of this Critically (Buckingham & Shanee, ), leading to an estimated Endangered species. % decline of L. flavicauda numbers in this area (Shanee & Shanee, ). Early estimates of the geographical range Keywords Andean montane forest, distribution, Lagothrix of L. flavicauda placed it in the pre-montane and montane flavicauda, Neotropical , Peru, primate conserva- forests between the Marañón and Huallaga rivers, but recent tion, yellow-tailed woolly monkey research has expanded that range southwards into Región Supplementary material for this article is available at Huánuco and east of the Río Huallaga near the border https://doi.org/./SX with Región Pasco (Shanee et al., a; Aquino et al., a,b; Aquino et al., ; Fig. ). There are also reports of L. flavicauda in areas of Región La Libertad (Parker & he Peruvian yellow-tailed woolly monkey Lagothrix fla- Barkley, ; Shanee et al., b) and Región Loreto Tvicauda is categorized as Critically Endangered both (Patterson & Wong, ), but these potential occurrences nationally in Peru (Heymann, ; MINAGRI, ) and have been neither consistently observed nor studied. Neither internationally (Cornejo et al., ), and is one of the field surveys nor distribution niche modeling have placed most threatened primates (DeLuycker & Heymann, ; L. flavicauda further south than south-east Huánuco (Shanee et al., a;Shaneeetal.,;Aquinoetal.,; Aquino et al., ), although further field surveys of Pasco SEAN M. MCHUGH (Corresponding author, orcid.org/0000-0002-3306-8832) and JASMINA MCKIBBEN Rainforest Partnership, 800 W 34th St Suite #105, and Junín are necessary to assess its presence in these regions Austin, Texas 78705, USA. E-mail [email protected] (Aquino et al., ). Here we report L. flavicauda  km

FANNY M. CORNEJO Interdepartmental Doctoral Program in Anthropological south-east of previous observations in Huánuco. Sciences, Stony Brook University, Stony Brook, New York, USA, and Our study area is the upper and lower montane forest Yunkawasi, Lima, Peru adjacent to the Río Pampa Hermosa, near the village of San MELISSA ZARATE Department of Biology, Boston University, Boston,  Massachusetts, USA Antonio in Región Junín (Fig. ), where accessible forest at lower elevations has been cleared for small-scale cultiva- CARLOS TELLO and CARLOS F. JIMÉNEZ Yunkawasi, Lima, Peru tion of coffee, coca, corn and yucca. Cattle ranching is also CHRISTOPHER A. SCHMITT ( orcid.org/0000-0003-2143-9226) Department of Anthropology and Biology, Boston University, Boston, Massachusetts, USA a contributing factor to this deforestation. Because of the steep slopes and terrain, however, most of the forest remains Received  February . Revision requested  April . Accepted  July . First published online  October . intact, albeit with some selective logging. Our study area has

Oryx, 2020, 54(6), 814–818 © 2019 Fauna & Flora International doi:10.1017/S003060531900084X Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 24 Sep 2021 at 16:32:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531900084X Peruvian yellow-tailed woolly monkey 815

individuals, which comprised one adult male, one subadult male, three adult females, three juveniles and three infants. According to people we spoke with in San Antonio, infants and juveniles can be seen with their mothers during December–January. The size of the infants observed in December suggest that one was a newborn and the other two perhaps  months old, suggesting births in October– December. The yellow-tailed woolly monkeys in San Antonio are phenotypically distinct from those further north. All ob- served individuals had distinct white patches on the brow, one above each eye (Plate ). This trait has been seen among populations in San Martín and Amazonas, but paler in colour and not in all individuals. The eponymous patch of yellow fur that surrounds the callus friction pad at the ventrodistal end of the prehensile tail is smaller in the Junín individuals than in those further north. All other aspects of appearance (mahogany fur, bright yellow scrotal tuft and pubic hair, white muzzle) seem consistent with other members of the species (Aquino et al., ). Despite being accessible from major towns such as Satipo, via road A, the forest in our study area is not heavily frag- mented and still has high connectivity, with large tracts of primary forest on the steep slopes. Closer to San Antonio the forest is disturbed, largely by farming. The forest sur- rounding San Antonio is better preserved and more intact on the northern side of the Río Pampa Hermosa because of the steep terrain, which limits accessibility for farming.  FIG. 1 Known observations of Lagothrix flavicauda From there, the forest is contiguous for km to the border (Supplementary Table ), including the newly discovered of the Bosque de Protección Pui Pui. The area to the south of population in Junín. the river is more degraded, with widespread farming and cattle ranching contributing to fragmentation, creating a a unique primate community (Supplementary Material ) mosaic of habitat types, including pastures and secondary along with terrestrial mammals such as the Andean bear and riparian forests. Tremarctos ornatus, red brocket deer Mazama americana, The greatest threats to the forests around San Antonio collared peccary Pecari tajacu, ocelot Leopardus pardalis are selective logging and clear cutting for agriculture. These and tayra Eira barbara. The University of Central Peru activities particularly affect the forest between Mariposa administers a , ha Área de Concesión de Conservación and the settlement of Calabaza, adjacent to road Aand (Conservation Concession Area) that comprises a portion the Río Pampa Hermosa, with higher rates of deforestation of our study area (Fig. ). eastwards to Satipo. The selective logging of rare and During a camera-trap study of terrestrial large mam- valuable trees, such as Cedrela angustifolia and Prumnopitys mals, we opportunistically observed the primate com- harmsiana, puts L. flavicauda at risk. Increased forest frag- munity. We surveyed .  km of cleared logging trails mentation could limit the species’ access to lower eleva- and Andean bear trails over altitudes of ,–, m. In tion forests and important seasonal fruit resources. As the addition to L. flavicauda, we observed other primate species human population increases, poaching could become a (Supplementary Material ). risk, as at other sites (Shanee, ; Shanee & Shanee, We encountered L. flavicauda four times (Table ), ). Although this does not currently affect L. flavicauda in primary forest. The monkeys did not flee, but rather or the other primates around San Antonio, it is imperative approached and descended to observe us more closely, that intact forests are managed properly, to prevent the de- behaviour consistent with unhabituated lowland woolly gree of forest fragmentation prevalent in San Martín and monkeys Lagothrix lagotricha spp. and yellow-tailed Amazonas (Buckingham & Shanee, ; Shanee, ). woolly monkeys at other sites (FMC & CAS, pers. obs.), Our observations expand the geographical range of L. allowing us to take photographs (Plate ). We were able to flavicauda to central Junín, well beyond the southernmost determine the composition of one of the groups, with  limit of the species proposed by Aquino et al. (b, ).

Oryx, 2020, 54(6), 814–818 © 2019 Fauna & Flora International doi:10.1017/S003060531900084X Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 24 Sep 2021 at 16:32:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531900084X 816 S. M. McHugh et al.

FIG. 2 Location of the new L. flavicauda records (a) in relation to the nearest known records in Región Huánuco and protected areas, and (b) the study area, with Bosque de Protección Pui Pui, the University of Central Peru Conservation Concession Area, nearby towns, Río Pampa Hermosa and Road A.

TABLE 1 The four troops of yellow-tailed woolly monkeys Lagothrix flavicauda observed in the forests around San Antonio (Fig. ; see Supplementary Table  for observations of other primate species in the area).

Date Time Individuals Altitude (m) Latitude (W) Longitude (S) 22 Oct. 2018 11.59 3 1,746 74.7854612 11.4113691 12 Nov. 2018 09.59 1 1,711 74.7846628 11.4126528 28 Dec. 2018 14.31 2+ 1,437 74.7738746 11.4146831 29 Dec. 2018 08.57 11 1,574 74.7776503 11.4135501

This lends urgency to expand the search for L. flavicauda in incentives provided by ecotourism are an effective previously neglected regions of Junín and Pasco (Aquino conservation model in Peruvian forests (Gordillo Jordan et al., ). Non-invasive genetic analyses of this new et al., ; Stronza & Gordillo, ; Stronza & Pegas, population would reveal the extent of its genetic isolation ), with community-run ecotourism being profitable and it is also important that there is further investigation of for local communities and encouraging local conservation the viable habitat between Huánuco and the newly discovered (Kirkby et al., , ). The community conservation population, to examine the degree of isolation between the model has been shown to be effective for conservation of Marañón–Huallaga and Junín populations. the yellow-tailed woolly monkey in north-east Peru, leading The Rainforest Partnership and the regional government to both reduced deforestation and localized population of Junín are working together to create a regional protected increases (Shanee & Shanee, ). Future research on pri- area that would protect remaining L. flavicauda habitat in mates in this area will need to be carried out jointly with Junín (Buckingham & Shanee, ; Aquino et al., a). the community members of San Antonio, to enable them Rainforest Partnership also works with the community of to participate in scientific research and to engage them as San Antonio to develop sustainable incomes via ecotourism, conservation stewards (Horwich et al., ). This integrated which can empower the local community to protect this approach will be essential for the conservation of this new- ecosystem and its rare and threatened species. The economic found population of L. flavicauda.

Oryx, 2020, 54(6), 814–818 © 2019 Fauna & Flora International doi:10.1017/S003060531900084X Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 24 Sep 2021 at 16:32:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531900084X Peruvian yellow-tailed woolly monkey 817

Huallaga: an expansion of its known geographic distribution. Primate Conservation, , –. AQUINO, R., GARCÍA,G.&CHARPENTIER,E.(a) Distribution and current status of the Peruvian yellow-tailed woolly monkey (Lagothrix flavicauda) in montane forests of the Región Huánuco, Peru. Primate Conservation, , –. AQUINO, R., GARCÍA, G., CHARPENTIER,R.&LÓPEZ,L.() Estado de conservación de Lagothrix flavicauda y otros primates en bosques montanos de San Martín y Huánuco, Perú. Revista Peruana de Biología, , –. AQUINO, R., LÓPEZ, L., FALCÓN, R., DÍAZ,S.&GÁLVEZ,H.() First inventory of primates in the montane forests of the Pasco and Ucayali regions, Peruvian Amazon. Primate Conservation, , –. AQUINO, R., ZÁRATE, R., LÓPEZ, L., GARCÍA,G.&CHARPENTIER,E. () Current status and threats to Lagothrix flavicauda and other primates in montane forest of the Región Huánuco. Primate Conservation, , –. BUCKINGHAM,F.&SHANEE,S.() Conservation priorities for the Peruvian yellow-tailed woolly monkey (Oreonax flavicauda): a GIS risk assessment and gap analysis. Primate Conservation, , –. BUTCHART, S.H.M., BARNES, R., DAVIES, C.W.N., FERNANDEZ,M.& SEDDON,N.() Observations of two threatened primates in the Peruvian Andes. Primate Conservation, , –. PLATE 1 Lagothrix flavicauda adult female (a) and adult male CORNEJO, F.M. () Aspects of the Ecology and Behaviour of the (b) observed in San Antonio (corresponding to the first Yellow-Tailed Woolly Monkey Oreonax flavicauda Humboldt, . observation in Table ). Photos: Jasmina McKibben. XXII Congress of the International Primatological Society, Edinburgh, UK, – August . Primate Eye, , Special Issue . CORNEJO, F.M., DELUYCKER, A.M., QUINTANA, H., PACHECO,V.& Acknowledgements We thank Rainforest Partnership for making HEYMANN, E.W. () Peruvian yellow-tailed woolly monkey the survey possible, the community of San Antonio for Oreonax flavicauda (Humboldt, ). In Primates in Peril: their help and knowledge, which led to the discovery of this new the World’s  Most Endangered Primates – (eds R.A. population, Eusebio Alanya Quiñones and Rosendo Ponce Cervantes Mittermeier, J. Wallis, A.B. Rylands, J.U. Ganzhorn, J.F. Oates, for help and support in San Antonio and in the field, Volodymyr E.A. Williamson, E. Palacios, E.W. Heymann, M.C.M. Kierulff, Izerskyy for insight and guidance, the University of Central Peru L. Yongcheng, J. Supriatna, C. Roos, S. Walker, L. Cortés-Ortiz & for allowing us to conduct our mammal survey in their Conservation C. Schwitzer). IUCN/SSC Primate Specialist Group, International Concession Area, Lucas Vega for field support, and Niyanta Spelman, Primatological Society and Conservation International, Arlington, Marshall Huggins and Mariela Palacios for comments on the text. USA. The fieldwork by FMC, CT and CJ was carried under permit RDG CORNEJO, F.M., RYLANDS, A.B., MITTERMEIER, R.A. & HEYMANN,E. 0107-2017-SERFOR-DGGSPFFS provided by Servicio Forestal y de () Lagothrix flavicauda.InThe IUCN Red List of Threatened Fauna Silvestre/Ministerio de Agricultura y Riego. Species : e.TA. Http://dx.doi.org/./IUCN. UK..RLTS.TA.en [accessed  January ]. Author contributions Fieldwork: SMM, FMC, JM, CT, CFJ; writ- DELUYCKER, A.M. () Notes on the yellow-tailed woolly monkey ing: SMM, FMC, CT, CAS, JM; editing: all authors; creation of maps: (Oreonax flavicauda) and its status in the Protected Forest of Alto CAS; photographs: JM. Mayo, northern Peru. Primate Conservation, , –. DELUYCKER, A.M. & HEYMANN, E.W. () Peruvian yellow-tailed Conflicts of interest None. woolly monkey Oreonax flavicauda (Humboldt, ). In Primates in Peril: the World’s  Most Endangered Primates – (eds Ethical standards This research abided by the Oryx guidelines on R.A. Mittermeier, J. Ratsimbazafy, A.B. Rylands, E.A. Williamson, ethical standards and followed the Code of Best Practices for Field J.F. Oates, D. Mbora, J.U. Ganzhorn, E. Rodriguez-Luna, E. Palacios, Primatology recommended by the American Society of Primatologists. E.W. Heymann, M.C.M. Kierulff, L. Yongcheng, J. Supriatna, C. Roos, S. Walker & J.M. Aguiar), Primate Conservation, , –. DI FIORE, A., CHAVES, P., CORNEJO, F.M., SCHMITT, C.A., SHANEE, References S., CORTES-ORTIZ, L. et al. () Rise and fall of a genus: complete mtDNA coding sequences shed light on the phylogenetic ALLGAS, N., SHANEE, S., PERALTA,A.&SHANEE,N.() Yellow- position of yellow-tailed woolly monkeys, Lagothrix (Oreonax) tailed woolly monkey (Oreonax flavicauda: Humboldt ) flavicauda, and on the evolutionary history of the Neotropical primate altitudinal range extension, Uchiza, Perú. Neotropical Primates, family (Platyrrhini). Molecular Phylogenetics and Evolution, , –. , –. AQUINO,R.() Fauna de la Provincia de Tocache. Informe Final. FOODEN,J.() A revision of the woolly monkeys (genus Lagothrix). Proyecto de Zonificación Ecológica y Económica. Convenio entre el Journal of Mammalogy, , –. 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