The Peruvian yellow-tailed woolly monkey Lagothrix flavicauda is categorized as Critically Endangered both nationally in Peru (Heymann, Reference Heymann2004; MINAGRI, 2014) and internationally (Cornejo et al., Reference Cornejo, Rylands, Mittermeier and Heymann2008), and is one of the most threatened primates (DeLuycker & Heymann, Reference DeLuycker, Heymann, Mittermeier, Ratsimbazafy, Rylands, Williamson, Oates, Mbora, Ganzhorn, Rodriguez-Luna, Palacios, Heymann, Kierulff, Yongcheng, Supriatna, Roos, Walker and Aguiar2007; Cornejo et al., Reference Cornejo, DeLuycker, Quintana, Pacheco, Heymann, Mittermeier, Wallis, Rylands, Ganzhorn, Oates, Williamson, Palacios, Heymann, Kierulff, Yongcheng, Supriatna, Roos, Walker, Cortés-Ortiz and Schwitzer2009). Research on L. flavicauda has focused on sparse museum and genetic samples to elucidate its taxonomic placement. Phenetic and morphological analyses had placed it in the monospecific genus Oreonax (Thomas, Reference Thomas1927; Groves, Reference Groves2001), or as a sister species to the other woolly monkeys in the genus Lagothrix (Fooden, Reference Fooden1963; Matthews & Rosenberger, Reference Matthews and Rosenberger2008; Rosenberger & Matthews, Reference Rosenberger and Matthews2008). Recent molecular genetic analyses support the latter (Ruiz-Garcia et al., Reference Ruiz-Garcia, Pinedo-Castro and Shostell2014; Di Fiore et al., Reference Di Fiore, Chaves, Cornejo, Schmitt, Shanee and Cortes-Ortiz2015). Knowledge of this species comes mainly from long-term study sites in remnant high-elevation tropical Andean forests in the Región Amazonas and Región San Martín in Peru (Graves & O'Neil, Reference Graves and O'Neill1980; Leo Luna, Reference Leo Luna1980, Reference Leo Luna1982; Butchart et al., Reference Butchart, Barnes, Davies, Fernandez and Seddon1995; DeLuycker, Reference DeLuycker2007; Cornejo, Reference Cornejo2008; Shanee et al., Reference Shanee, Shanee and Maldonado2008; Shanee, Reference Shanee2011; Shanee et al., Reference Shanee, Shanee and Allgas-Marchena2013a,Reference Shanee, Shanee, Campbell, Allgas, Grow, Gursky-Doyen and Krztonb; Allgas et al., Reference Allgas, Shanee, Peralta and Shanee2014). The last assessment of viable habitat in this area, in 2009, estimated a reduction by almost 56% since surveys in 1981 (Buckingham & Shanee, Reference Buckingham and Shanee2009), leading to an estimated 93% decline of L. flavicauda numbers in this area (Shanee & Shanee, Reference Shanee, Shanee, Defler and Stevenson2014). Early estimates of the geographical range of L. flavicauda placed it in the pre-montane and montane forests between the Marañón and Huallaga rivers, but recent research has expanded that range southwards into Región Huánuco and east of the Río Huallaga near the border with Región Pasco (Shanee et al., Reference Shanee, Shanee and Allgas-Marchena2013a; Aquino et al., Reference Aquino, García and Charpentier2016a,Reference Aquino, García, Charpentier and Lópezb; Aquino et al., Reference Aquino, López, Falcón, Díaz and Gálvez2019; Fig. 1). There are also reports of L. flavicauda in areas of Región La Libertad (Parker & Barkley, Reference Parker and Barkley1981; Shanee et al., Reference Shanee, Shanee, Campbell, Allgas, Grow, Gursky-Doyen and Krzton2013b) and Región Loreto (Patterson & Wong, Reference Patterson, Wong and Pitman2014), but these potential occurrences have been neither consistently observed nor studied. Neither field surveys nor distribution niche modeling have placed L. flavicauda further south than south-east Huánuco (Shanee et al., Reference Shanee, Shanee and Allgas-Marchena2013a; Shanee et al., Reference Shanee, Allgas, Shanee and Campbell2015; Aquino et al., Reference Aquino, García, Charpentier and López2017; Aquino et al., Reference Aquino, López, Falcón, Díaz and Gálvez2019), although further field surveys of Pasco and Junín are necessary to assess its presence in these regions (Aquino et al., Reference Aquino, López, Falcón, Díaz and Gálvez2019). Here we report L. flavicauda 206 km south-east of previous observations in Huánuco.
Our study area is the upper and lower montane forest adjacent to the Río Pampa Hermosa, near the village of San Antonio in Región Junín (Fig. 2), where accessible forest at lower elevations has been cleared for small-scale cultivation of coffee, coca, corn and yucca. Cattle ranching is also a contributing factor to this deforestation. Because of the steep slopes and terrain, however, most of the forest remains intact, albeit with some selective logging. Our study area has a unique primate community (Supplementary Material 1) along with terrestrial mammals such as the Andean bear Tremarctos ornatus, red brocket deer Mazama americana, collared peccary Pecari tajacu, ocelot Leopardus pardalis and tayra Eira barbara. The University of Central Peru administers a 6,800 ha Área de Concesión de Conservación (Conservation Concession Area) that comprises a portion of our study area (Fig. 2).
During a camera-trap study of terrestrial large mammals, we opportunistically observed the primate community. We surveyed > 180 km of cleared logging trails and Andean bear trails over altitudes of 1,287–2,015 m. In addition to L. flavicauda, we observed other primate species (Supplementary Material 1).
We encountered L. flavicauda four times (Table 1), in primary forest. The monkeys did not flee, but rather approached and descended to observe us more closely, behaviour consistent with unhabituated lowland woolly monkeys Lagothrix lagotricha spp. and yellow-tailed woolly monkeys at other sites (FMC & CAS, pers. obs.), allowing us to take photographs (Plate 1). We were able to determine the composition of one of the groups, with 11 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 3 months old, suggesting births in October–December.
The yellow-tailed woolly monkeys in San Antonio are phenotypically distinct from those further north. All observed individuals had distinct white patches on the brow, one above each eye (Plate 1). 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., Reference Aquino, Zárate, López, García and Charpentier2015).
Despite being accessible from major towns such as Satipo, via road 24A, the forest in our study area is not heavily fragmented 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 surrounding 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. From there, the forest is contiguous for 16 km to the border of the Bosque de Protección Pui Pui. The area to the south of the river is more degraded, with widespread farming and cattle ranching contributing to fragmentation, creating a mosaic of habitat types, including pastures and secondary and riparian forests.
The greatest threats to the forests around San Antonio are selective logging and clear cutting for agriculture. These activities particularly affect the forest between Mariposa and the settlement of Calabaza, adjacent to road 24A and the Río Pampa Hermosa, with higher rates of deforestation eastwards to Satipo. The selective logging of rare and valuable trees, such as Cedrela angustifolia and Prumnopitys harmsiana, puts L. flavicauda at risk. Increased forest fragmentation could limit the species' access to lower elevation forests and important seasonal fruit resources. As the human population increases, poaching could become a risk, as at other sites (Shanee, Reference Shanee2011; Shanee & Shanee, Reference Shanee, Shanee, Defler and Stevenson2014). Although this does not currently affect L. flavicauda or the other primates around San Antonio, it is imperative that intact forests are managed properly, to prevent the degree of forest fragmentation prevalent in San Martín and Amazonas (Buckingham & Shanee, Reference Buckingham and Shanee2009; Shanee, Reference Shanee2011).
Our observations expand the geographical range of L. flavicauda to central Junín, well beyond the southernmost limit of the species proposed by Aquino et al. (Reference Aquino, Charpentier, García and López2016b, Reference Aquino, García, Charpentier and López2017). This lends urgency to expand the search for L. flavicauda in previously neglected regions of Junín and Pasco (Aquino et al., Reference Aquino, López, Falcón, Díaz and Gálvez2019). Non-invasive genetic analyses of this new population would reveal the extent of its genetic isolation and it is also important that there is further investigation of the viable habitat between Huánuco and the newly discovered population, to examine the degree of isolation between the Marañón–Huallaga and Junín populations.
The Rainforest Partnership and the regional government of Junín are working together to create a regional protected area that would protect remaining L. flavicauda habitat in Junín (Buckingham & Shanee, Reference Buckingham and Shanee2009; Aquino et al., Reference Aquino, García and Charpentier2016a). Rainforest Partnership also works with the community of San Antonio to develop sustainable incomes via ecotourism, which can empower the local community to protect this ecosystem and its rare and threatened species. The economic incentives provided by ecotourism are an effective conservation model in Peruvian forests (Gordillo Jordan et al., Reference Gordillo Jordan, Hunt, Stronza, Stronza and Durham2008; Stronza & Gordillo, Reference Stronza and Gordillo2008; Stronza & Pegas, Reference Stronza and Pegas2008), with community-run ecotourism being profitable for local communities and encouraging local conservation (Kirkby et al., Reference Kirkby, Guidice-Granados, Day, Turner, Velarde-Andrade and Dueñas-Dueñas2010, Reference Kirkby, Giudice, Day and Turner2011). The community conservation model has been shown to be effective for conservation of the yellow-tailed woolly monkey in north-east Peru, leading to both reduced deforestation and localized population increases (Shanee & Shanee, Reference Shanee and Shanee2015). Future research on primates in this area will need to be carried out jointly with the community members of San Antonio, to enable them to participate in scientific research and to engage them as conservation stewards (Horwich et al., Reference Horwich, Shanee, Shanee, Bose, Fenn, Chakraborty and Zlatic2015). This integrated approach will be essential for the conservation of this newfound population of L. flavicauda.
Acknowledgements
We thank Rainforest Partnership for making the mammal survey possible, the community of San Antonio for their help and knowledge, which led to the discovery of this new population, Eusebio Alanya Quiñones and Rosendo Ponce Cervantes for help and support in San Antonio and in the field, Volodymyr Izerskyy for insight and guidance, the University of Central Peru for allowing us to conduct our mammal survey in their Conservation Concession Area, Lucas Vega for field support, and Niyanta Spelman, Marshall Huggins and Mariela Palacios for comments on the text. The fieldwork by FMC, CT and CJ was carried under permit RDG 0107-2017-SERFOR-DGGSPFFS provided by Servicio Forestal y de Fauna Silvestre/Ministerio de Agricultura y Riego.
Author contributions
Fieldwork: SMM, FMC, JM, CT, CFJ; writing: SMM, FMC, CT, CAS, JM; editing: all authors; creation of maps: CAS; photographs: JM.
Conflicts of interest
None.
Ethical standards
This research abided by the Oryx guidelines on ethical standards and followed the Code of Best Practices for Field Primatology recommended by the American Society of Primatologists.