A Reassessment of the Extinction Risk of the Critically Endangered Oxapampa Poison Frog Ameerega Planipaleae (Dendrobatidae)

A reassessment of the extinction risk of the Critically Endangered Oxapampa poison frog Ameerega planipaleae (Dendrobatidae)

A RIADNE A NGULO,RUDOLF VON M AY and J AVIER I COCHEA

Abstract Assessments of extinction risk are required to in- River Basin. Relatively little is known about this frog’s natural form conservation action, but the usefulness of assessments history (Chávez et al., ), although it is diurnal, mostly is undermined if they are not current. Ameerega planipaleae, active in the afternoon, and can be found in the leaf litter of a poison frog endemic to the cloud forests of central Peru, secondary forests (Chávez et al., ). Habitat loss has been was last assessed in . We therefore sought to provide a concern since the species was first described. Morales & updated data to inform the reassessment of this species. Velazco () found individuals in a swampy forest Based on our findings, we recommend that this frog remain fragment, isolated by loss of surrounding habitat. The area categorized as Critically Endangered, but under modified surrounding the frog’s known range comprises farms and criteria, and that conservation actions are taken to reduce buildings (Chávez et al., ). The most recent migration the pressures of local threats, especially the overuse of of people from the Andes has pushed agriculture and live- agrochemicals. stock farming onto the higher valley slopes, and cultivation of Capsicum (known locally as rocoto), in particular, has Keywords Ameerega planipaleae, cloud forest, conservation driven loss of primary forest and use of agrochemicals, and actions, Critically Endangered, Epipedobates, habitat loss, constitutes the main threat in the Yanachaga–Chemillén Oxapampa poison frog, Peru National Park buffer zone, especially in Chacos (Laura Contreras, ), where A. planipaleae occurs. he identification of species at high risk of extinction is According to the information available at the time of its  fundamental for conservation of biodiversity (Collen assessment, A. planipaleae was assessed as Critically T  et al., ). The IUCN Red List Categories and Criteria Endangered based on criteria B ab(iii) (Icochea et al.,  () were developed for objective and quantitative assess- ). Previously the most recent sightings of this species – ment of the extinction risk of species. Application of these were in the buffer zone of Yanachaga Chemillén National  criteria for the IUCN Red List of Threatened Species and Park, where individuals were observed over multiple –  for national assessments is used to inform conservation plan- surveys during May April , with a total sampling   ning, monitoring and management (Hoffmann et al., ). effort of person-days (von May et al., ). Seven indi- For this, however, it is imperative that species are reassessed viduals were recorded by M. Medina-Müller and G. Chávez  – regularly, at least every  years (The Rules of Procedure for over person-days of surveys during May January   IUCN Red List Assessments –;IUCN,). (Medina-Müller & Chávez, ), and four individuals   Ameerega planipaleae, a frog of the family Dendrobatidae, were recorded by R. von May on April . was originally described as Epipedobates planipaleae by We sought to locate A. planipaleae and identify Morales & Velazco (), who indicated that the species any threats to its survival, and combine our findings with ’ was known only from its type locality, in the Llamaquizú all available published data to reassess the species conserva-   River Basin, on the western slope of Yanachaga–Chemillén tion status. Between April and July we conducted  National Park, Oxapampa province, Pasco region, Peru. four surveys, for a total of person-days, in the cloud forest – Although subsequent studies have recorded the species at of Yanachaga Chemillén National Park and its buffer zone. its type locality (Medina-Müller & Chávez, ;Chávez Three of these surveys included the Llamaquizú River Basin   et al., ), the geographical coordinates provided by (April/August and November/December ), cover- Morales & Velazco () do not match the description of ing both dry and rainy seasons.  the locality, placing the species outside the Llamaquizú Visual encounter surveys (Crump & Scott, ) were used, during daytime. Acoustic recordings of the species’ advertisement calls were played, to entice males to respond ARIADNE ANGULO (Corresponding author), RUDOLF VON MAY* and JAVIER ICOCHEA (King, ), because A. planipaleae is difficult to locate IUCN SSC Amphibian Specialist Group, 3701 Lake Shore Blvd W, P.O. Box 48586, Toronto, Ontario, M8W 1P5, Canada. E-mail aangulo@amphibians.org visually and calls are a reliable way to locate males (it is the only diurnal frog species with this type of call in the area). *Also at: Museum of Zoology & Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA Species presence was assessed based on both the visual en- Received  January . Revision requested  March . counter and auditory surveys. Coordinates of sites, recorded Accepted  April . First published online  September . with a global positioning system, were used to calculate extent

Oryx, 2019, 53(3), 557–560 © 2018 Fauna & Flora International doi:10.1017/S0030605318000571 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 26 Sep 2021 at 18:29:14, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000571 558 A. Angulo et al.

FIG. 1 The distribution of A. planipaleae in Peru and the current IUCN Red List polygon for the species, the known range and described type locality in the Chacos sector in the buffer zone of the Yanachaga–Chemillén National Park (indicated by the arrow), and the supposed location of the type locality in the species’ description, which does not align with the description of the type locality in the Llamaquizú River Basin.

of occurrence (EOO) and area of occupancy (AOO) (IUCN, Although A. planipaleae has not been found in trade, and ), with GeoCAT (Bachman et al., ). Our local field all species of the genus Ameerega are included in Appendix team also identified sites aurally. II of CITES (CITES, ), there is a general demand for We located A. planipaleae at  sites (one in April , poison frogs for the pet trade (CITES, ) and therefore three in August , three in November  and three in detailed information for the  sites is not included here, July ) in close proximity to each other (the furthest dis- as primary literature has been used to locate species coveted tance between sites was . km, with a mean distance of by the pet trade (Neslen, ). This information will, . km) over altitudes of ,–, m. Four of the records however, be made available to scientists, conservationists were visual (three adults and one juvenile) and seven (of and government officials upon request. males) were auditory. These records gave an estimated All of the known sites for this species fall outside the  EOO of . km , in the Chacos sector of the National species’ range polygon in the IUCN Red List, which is Park’s buffer zone. Combining these records with one – km east–north-east of the sites we located (Fig. ). published georeferenced record (Chávez et al., ; geo- This is probably a result of the constraints of the mapping graphical coordinates from the species description of technology available at the time of the  assessment. The Morales & Velazco, , and Medina-Müller & Chávez, IUCN Red List polygon does not include the type locality , were not used as they are believed to be erroneous) coordinates provided in the species description (Morales  increased the known EOO to . km and the known & Velazco, ), which lie further west of both the polygon  AOO (with a cell size of  km) to  km . and the documented sites for this species.

Ameerega planipaleae occurs in an area heavily impacted (SERFOR, Resolución Directoral No. 0288–2014-MINAGRI-DGFFS/ by human use, and is associated with various modified DGEFFS and Resolución de Dirección General No. 105-2014- habitats: secondary forests close to plantations of pines, SERFOR-DGGSPFFS) and the Servicio Nacional de Áreas Naturales Protegidas por el Estado (SERNANP, Resolución Jefatural No. small streams and ditches, an inactive fish farm, and small- 004-2014-SERNANP-DGANP-JEF) issued research permits for field holdings with Capsicum and Passiflora crops that are heavily work outside and within protected areas, respectively. This study was sprayed with agrochemicals such as Herbosato and Paraquat supported by Mohamed bin Zayed Species Conservation Fund Project (the latter is based on information provided by a local farm- No. 13257928 and Global Wildlife Conservation. The Department of er, a field team member who has knowledge of local agricul- Herpetology at the Museo de Historia Natural de San Marcos houses specimens collected. IUCN facilitated use of geographical information tural practices, and discarded agrochemical waste that we system data and software. RvM thanks the National Geographic found). Laura Contreras () also noted the pervasiveness Society (Grant # 9191-12) for support. This is publication 6 of Peru’s of Capsicum crops and associated agrochemical use in this Amphibian Specialist Group. area. The level of agrochemical use in the province is such that an agrochemical waste recycling project is being imple- Author contributions All authors designed the project, conducted fieldwork and wrote the article. mented (SPDA, ). Ameerega planipaleae,likeotherspeciesofAmeerega, Conflicts of interest None. has aquatic larvae, and the adults found were all in close proximity to running water, which often receives agro- Ethical standards This research complies with the journal’sCodeof chemical runoff. To date, there are no records of the spe- Conduct for authors. cies within Yanachaga–Chemillén National Park, in spite References of efforts by Park staff to locate the frog within the Park

boundary closest to the Chacos buffer zone sector to the BACHMAN, S., MOAT, J., HILL, A.W., DE LA TORRE,J.&SCOTT,B. south of the Park. () Supporting Red List threat assessments with GeoCAT: Based on published information and our data, we make geospatial conservation assessment tool. ZooKeys, , –. the following extinction risk assessment for A. planipaleae: CHÁVEZ, G., COSMÓPOLIS, C.H. & LUJÁN,L.() Annotated  () The species has an estimated EOO of . km , adjusted checklist and ecological notes of anurans from the southern region   of Yanachaga Chemillen National Park, central Andes of Peru. to km (as EOO should not exceed AOO; IUCN Standards Herpetotropicos, , –. and Petitions Subcommittee, ), which is within the CITES () Appendices I, II and III, Valid from  October .  threshold for Critically Endangered ( km ) under criter- Https://cites.org/eng/app/appendices.php [accessed  January  ion B.() The species has an estimated AOO of  km , ].  which is within the threshold for Critically Endangered CITES ( ) CITES Trade Database. Https://trade.cites.org/  [accessed  January ]. ( km ) under criterion B.() The ubiquitous use of agro- COLLEN, B., DULVY, N.K., GASTON, K.J., GÄRDENFORS, U., KEITH,D. ’ chemicals throughout much of the species restricted range A., PUNT, A.E. et al. () Clarifying misconceptions of extinction and the species’ obligatory association with water merit risk assessment with the IUCN Red List. Biology Letters, , considering it a single threat-defined location. () There is .  ongoing decline of the terrestrial and aquatic habitats of CRUMP, M.L. & SCOTT, N.J. ( ) Visual encounter surveys. In Measuring and Monitoring Biological Diversity. Standard Methods the species as a result of heavy and continued use of agro- for Amphibians (eds W.R. Heyer, M.A. Donnelly, R.W. McDiarmid, chemicals, loss of forest to agriculture, and afforestation L.A. Hayek & M.S. Foster), pp. –. Smithsonian Institution with commercial tree species. Press, Washington, DC, USA. We therefore propose that A. planipaleae remain cate- HOFFMANN, M., HILTON-TAYLOR, C., ANGULO, A., BÖHM, M.,  gorized as Critically Endangered but based on criteria BROOKS, T.M., BUTCHART, S.H.M. et al. ( ) The impact of conservation on the status of the world’s vertebrates. Science, , Bab(iii) + ab(iii) rather than Bab(iii). Given the species’ –. restricted range and the ongoing threats, conservationists ICOCHEA, J., LEHR, E., JUNGFER, K.-H. & LÖTTERS,S.() need to work with the local community to reduce the use Ameerega planipaleae.InThe IUCN Red List of Threatened Species of agrochemicals and explore more benign options to :e.TA. Http://dx.doi.org/./IUCN.UK.. control crop pests, and to investigate the use of native spe- RLTS.TA.en [accessed  May ].     cies as commercially viable options for timber plantations. IUCN ( ) IUCN Red List Categories and Criteria: Version . . nd edition. IUCN, Gland, Switzerland, and Cambridge, UK. Raising awareness of these issues is also important, as is IUCN () Rules of Procedure for IUCN Red List Assessments – the continued monitoring of the status of A. planipaleae. . Version .. Approved by the IUCN SSC Steering Committee in September . Http://cmsdocs.s.amazonaws.com/keydocuments/ Rules_of_Procedure_for_Red_List_-.pdf [accessed  Acknowledgements We thank the staff of Yanachaga–Chemillén January ]. National Park for their support, in particular park directors Genaro IUCN STANDARDS &PETITIONS SUBCOMMITTEE () Guidelines Yarupaitán and Salomé Antezano. Werner Loechle transported the for using the IUCN Red List Categories and Criteria. Version . team to field sites and Dante López and Edgar Curi provided field Http://www.iucnredlist.org/documents/RedListGuidelines.pdf support in Chacos. The Servicio Nacional Forestal y de Fauna Silvestre [accessed  January ].

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