New populations of pampas Ozotoceros bezoarticus discovered in threatened Amazonian savannah enclaves

D ANIEL G. ROCHA,ALEXANDRE V OGLIOTTI,DIOGO M. GRÄBIN W ILHAN R. C. ASSUNÇÃO,BRUNO C ONTURSI C AMBRAIA,ANA R AFAELA D ’ A MICO A NTONIO E LSON P ORTELA and R AHEL S OLLMANN

Abstract The savannah enclaves (i.e. patches) in the south- Supplementary material for this article is available at ern Brazilian Amazonia are among the most threatened and https://doi.org/./S poorly surveyed sites in Amazonia. As part of an extensive survey, we set camera traps in three of these savannah enclaves. We obtained  independent records he South American savannah is the largest and most of pampas deer Ozotoceros bezoarticus, a medium sized Tbiodiverse tropical savannah (Cardoso Da Silva & Bates, Neotropical cervid that is strongly associated with open ). Most of this biome, known as cerrado, is located in habitats and categorized as Vulnerable on the Brazilian Red central Brazil, and is categorized as one of  global conserva- List of threatened species. These savannah enclaves with tion hotspots (Myers et al., ). More than % of the cer- confirmed populations of pampas deer lie outside the rado has been cleared and only .% lies within protected species’ previously presumed historical range and are at areas (Strassburg et al., ). Significant patches of savannah, least  km from any known extant population. Together, known as enclaves, can also be found on the periphery of the  these savannah enclaves add c. , km to the pampas Amazon forest. These enclaves are heterogeneous mosaics of deer’s currently known range. The small pampas deer popu- open areas and forest with a highly diverse community com- lations in these enclaves are probably isolated by a matrix of prising savannah and forest species, including endemics Amazon forest, raising questions about spatial genetic struc- (Barbosa et al., ). They are highly threatened by expand- ture and meta-population dynamics, and making them vul- ing large-scale agriculture, and large tracts have already been nerable to local extinction. We highlight the need for further converted for cultivation of soya, rice, eucalyptus and studies, particularly genetic, to assess the conservation status pine, and ranching (Carvalho & Mustin, ). These of these populations, the results of which could potentially enclaves are poorly studied, particularly compared to other inform management decisions in other areas of the heavily cerrado areas (Carvalho & Mustin, ). Here, we report the fragmented range of this species. discovery of populations of pampas deer Ozotoceros bezoarti- cus in savannah enclaves located in the Arc of Deforestation, Keywords Brazil, camera trap, isolated population, an area of rapid agricultural expansion along the southern Neotropical cervid, Ozotoceros bezoarticus, pampas deer, border of Brazilian Amazonia,  km beyond the species’ savannah, southern Amazonia formerly presumed distribution. The pampas deer is a medium sized (– kg), predom- inantly diurnal cervid of Neotropical open grasslands and DANIEL G. ROCHA (Corresponding author, orcid.org/0000-0002-0100-3102)* shrublands (Rodrigues & Monteiro-Filho, ). Its histori- Graduate Group in Ecology, Department of Wildlife, Fish, and Conservation Biology, University of California, Davis, California, USA cal range encompassed extensive open habitats in Argentina, E-mail [email protected] , Paraguay, Bolivia and central Brazil, but as a result ALEXANDRE VOGLIOTTI Instituto de Ciências da Vida e da Natureza, Universidade of expansion of agriculture its habitat has been drastically Federal da Integração Latino Americana, Foz do Iguacu, Brazil reduced and fragmented (Weber & Gonzalez, ). Once † DIOGO M. GRÄBIN Grupo de Pesquisa em Ecologia e Conservação de Felinos na considered the most threatened South American cervid Amazônia, Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Brazil (González, ), the pampas deer is currently categorized ’ WILHAN R. C. ASSUNÇÃO,BRUNO CONTURSI CAMBRAIA,ANA RAFAELA D AMICO and as Near Threatened on the IUCN Red List (González et al., ANTONIO ELSON PORTELA Instituto Chico Mendes de Conservação da Biodiversidade, Brasilia, Brazil ). In Brazil, the country that holds most of the pampas ’ RAHEL SOLLMANN Department of Wildlife, Fish, and Conservation Biology, deer s current range, the species is categorized as Vulnerable University of California, Davis, California, USA (Duarte et al., ). Five subspecies of pampas deer are *Also at: Grupo de Pesquisa em Ecologia e Conservação de Felinos na recognized (González et al., ), and most of the extant Amazônia, Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Brazil † populations, except those in the Pantanal and the north- Also at: Programa de Pós Graduação em Ecologia e Conservação da ,   Biodiversidade, Universidade Estadual de Santa Cruz, Ilhéus, Brazil eastern Brazilian cerrado, are estimated to be , indivi-  Received  September . Revision requested  November . duals, with a decreasing trend (González et al., ). Accepted  December . First published online  August . Range-wide, the main threats to the species are habitat

Oryx, 2019, 53(4), 748–751 © 2019 Fauna & Flora International doi:10.1017/S0030605318001539 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 23 Sep 2021 at 13:25:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001539 New populations of pampas deer 749

loss and fragmentation, hunting and emerging diseases at least one hour apart; Meek et al., ) of pampas deer (González et al., ). (Supplementary Table , Supplementary Plate ), resulting  Our study area encompasses , km in the Brazilian in a trapping success of . records/ camera-trap states of Amazonas and Rondônia. The landscape comprises days. We detected the species at nine camera traps in a mosaic of land-cover types, including continuous Amazon open savannah sites, within three enclaves. Ten of the re- forest, open savannah enclaves (grasslands and bushlands), cords were of females, nine of males, and we could not de- transitional forest–savannah areas and human-impacted termine the sex for four records. Twenty records (%) were forest with different degrees of fragmentation. The climate between sunrise and sunset, and only three were of more in the region is tropical humid, with mean monthly tem- than one individual. We also sighted pampas deer, including peratures of – °C and mean annual precipitation of ,– fawns, opportunistically on several occasions during field- , mm. There is a rainy season from October to March work within the savannah enclaves. Our data did not allow and a dry season from April to September (ICMBio, ). us to estimate population size, density or other demographic As part of a wildlife survey during February –June parameters. , we installed camera traps at  open savannah and tran- The protected areas and savannah enclaves with newly sitional forest–savannah sites, which had not previously been confirmed populations of pampas deer lie outside the spe- systematically surveyed for , within the Campos cies’ previously presumed historical range, at least  km Amazônicos and Mapinguari National Parks, in locations from any previously known extant population (Fig. a). that had signs of medium-sized or large mammals (Fig. b; Together, the savannah enclaves with confirmed pampas  Supplementary Table ). Each site had one unbaited camera deer records add c. , km to the known range of the spe- trap (PC Hyperfire, Reconyx, Holmen, USA). Cameras cies (Table ), and unsurveyed enclaves in this region re-  were continuously active for a mean of . days, for a total present an additional , km of potential pampas deer of , camera-trap days. We estimated the size of the habitat. potential pampas deer habitat in the study area by calculating The savannah enclaves we surveyed are not connected. the total area of savannah and savannah–steppe habitat classes, Dating of carbon isotopes from our study area indicates following the Biomes Vegetation Cover map for Brazilian that vegetation cover has been relatively stable for at least Amazonia (MMA, ). the past , years (Gomes, ), suggesting that pampas Our camera-trap survey yielded  independent records deer populations in these enclaves may have been isolated (photos at the same site were considered independent when for a long time. It is likely that current gene flow between

FIG. 1 (a) Location of the study area, with past and present distribution of the pampas deer Ozotoceros bezoarticus. (b) Camera-trap locations, with and without pampas deer records, within savannah enclaves in the southern Brazilian Amazonia.

Oryx, 2019, 53(4), 748–751 © 2019 Fauna & Flora International doi:10.1017/S0030605318001539 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 23 Sep 2021 at 13:25:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001539 750 D. G. Rocha et al.

TABLE 1 The three southern Amazonia savannah enclaves (Fig. ) deer is greater than previously presumed, our study high- surveyed with camera traps, with the surveyed area, number of lights the need for further studies, particularly genetic, to camera-trap sites (each of which had one camera trap) and number assess the conservation status of these enclave populations, of records of pampas deer Ozotoceros bezoarticus. the results of which could potentially inform management Surveyed Area No. of camera- Pampas deer decisions in other areas of the heavily fragmented range savanna enclave (km2) trap sites records of this species. Eastern 2997.1 40 15 Central 572.2 19 7 Acknowledgements We thank Instituto Mamirauá, and Campos Western 369.3 5 1 Amazônicos and Mapinguari National Parks for logistical and finan- cial support. We thank França, Wesley, Finicius, Edinaldo, Antônio, Leandro and the many others who helped in the field. DGR received a scholarship from the CAPES/Doutorado Pleno no Exterior (#88881.128140). enclaves is low, given that our extensive camera trapping Author contributions Study design and data collection: DGR, in nearby forests did not record the species (unpubl. data .   DMG, WRCA, BCC, ARD and AEP; interpretation of results and for , camera trap-days). Genetic studies of the writing: DGR, RS and AV; revision: all authors. pampas deer in this area could provide information on the meta-population dynamics of the species, and on any Conflicts of interest None. genetic differentiation between populations in different en- claves and in relation to populations beyond Amazonia (it is Ethical standards This research abides by the Oryx guidelines on ethical standards. Survey permits were granted by ICMBio/SISBIO not yet known to which of the five pampas deer subspecies (52720-1, 54457-1). the Amazonian savannah populations belongs). Although this is the first scientific account of the pampas deer in the southern Amazonian savannahs, local farmers and settlers have long known the species to exist there References (pers. comms to ARD, WRCA and BCC), and report that BARBOSA, R.I., CAMPOS, C., PINTO,F.&FEARNSIDE, P.M. () The it was more abundant before the influx of people into this ‘Lavrados’ of Rroraima: biodiversity and conservation of Brazil’s region during the s. Any decline would not be unex- Aamazonian savannas. Functional Ecosystems and Communities, , pected given the extensive threats that wildlife face in the –. Arc of Deforestation. Because the population trend is prob- CARDOSO DA SILVA, J.M. & BATES, J.M. () Biogeographic ably negative and populations are presumed to be small and patterns and conservation in the South American cerrado: a tropical savanna hotspot. BioScience, , –. isolated, ensuring the persistence of these newly recorded CARVALHO, W.D. & MUSTIN,K.() The highly threatened and pampas deer populations may require management. This little known Amazonian savannahs. Nature Ecology & Evolution, , highlights the need for more detailed studies on pampas . deer demography and connectivity in these enclaves to DUARTE, J.M.B., VOGLIOTTI, A., DOS ZANETTI, E. S., DE OLIVEIRA,  assess the species’ conservation status and inform manage- M.L., TIEPOLO, L.M., RODRIGUES, L.F. et al. ( ) Avaliação do risco de extinção do veado-campeiro Ozotoceros bezoarticus ment. Most of the southern Amazonia savannah enclaves Linnaeus, , no Brasil. Biodiversidade Brasileira, , –. lie within protected areas; the presence of the Vulnerable GOMES, F.B. () Dinâmica paleoambiental holocênica no pampas deer reinforces the need for protection. Given that enclave de savana em meio a floresta situado nos setores a medium-sized mammal species such as the pampas deer Tabajara e Estanho do Parque Pacional Campos Amazônicos was unrecorded by the scientific community until recently, (AM/RO). PhD thesis. Universidade Federal do Paraná, Curitiba, Brazil. it is possible that the enclaves harbour other elusive and/or GONZÁLEZ,S.() Estado de conservação dos cervídeos da América threatened species. Unfortunately, being within a federal do Sul. Logos Tempo e Ciência, , –. protected area does not guarantee security. The boundaries GONZÁLEZ, S., ÁLVAREZ-VALIN,F.&MALDONADO, J.E. () of both Mapinguari and Campos Amazonicos national parks Morphometric differentiation of endangered pampas deer were altered in  and , respectively, to accommodate (Ozotoceros bezoarticus), with description of new subspecies from  – infrastructure developments such as highways and hydro- Uruguay. Journal of Mammalogy, , . GONZÁLEZ, S., JACKSON, III, J.J. & MERINO, M.L. () Ozotoceros electric dams, and other infrastructure projects are being bezoarticus.InThe IUCN Red List of Threatened Species : considered in this region. e.TA. Http://dx.doi.org/./IUCN.UK.-. Our study meets some of the research requirements for RLTS.TA.en [accessed  January ]. the pampas deer listed by IUCN and the Brazilian national ICMBIO (INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA  — assessment for the species, particularly the search for new BIODIVERSIDADE)( ) Plano de Manejo Parque Nacional dos Campos Amazônicos. Instituto Chico Mendes de Conservação da populations and as a contribution to the management of Biodiversidade, Brasília, Brazil.   protected areas (Duarte et al., ; González et al., ). MEEK, P.D., BALLARD, G., CLARIDGE, A., KAYS, R., MOSEBY, K., As well as establishing that the range of the pampas O’BRIEN,T.etal.() Recommended guiding principles for

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Oryx, 2019, 53(4), 748–751 © 2019 Fauna & Flora International doi:10.1017/S0030605318001539 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 23 Sep 2021 at 13:25:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001539