Scat Detection Dogs, DNA and Species Distribution Modelling Reveal a Diminutive Geographical Range for the Vulnerable Small Red Brocket Deer Mazama Bororo

Scat detection dogs, DNA and species distribution modelling reveal a diminutive geographical range for the Vulnerable small red brocket deer Mazama bororo

J OSÉ M AURÍCIO B ARBANTI D UARTE,ÂNGELA C RISTINA T ALARICO A LEXANDRE V OGLIOTTI,JOSÉ E DUARDO G ARCIA,MÁRCIO L EITE O LIVEIRA J ESÚS E. MALDONADO and S USANA G ONZÁLEZ

Abstract The small red brocket deer Mazama bororo is en- and is threatened by human encroachment, poaching, and demic to the Brazilian Atlantic Forest, a biome that has been predation by dogs, and based on our findings we recom- greatly fragmented and altered by human activities. This mend policy intervention for conservation planning of the elusive species is morphologically similar to the red brocket Ombrophilous Dense Forest. deer Mazama americana and the Brazilian dwarf brocket Keywords Atlantic Forest, Brazil, Cervidae, Cytochrome b, deer Mazama nana, and genetic typing is necessary for re- geographical range, Mazama bororo, non-invasive sampling liable identification. To determine the geographical range of M. bororo more accurately, we conducted non-invasive genetic sampling using scat detection dogs trained to locate deer  faeces. We surveyed protected areas located within the Introduction species’ potential distribution and collected a total of  scat samples in  of the protected areas. Using a polymerase he small red brocket deer Mazama bororo is one of chain reaction–restriction fragment length polymorphism Tthe most threatened, elusive and poorly known approach, we genotyped  scat samples (%) and de- Neotropical deer. It is categorized as Vulnerable on the tected M. bororo in seven localities in three Brazilian states. IUCN Red List (Duarte, ). The species inhabits rem- The results support a range extension of the small red brock- nants of the Atlantic Forest (Duarte & Jorge, ; Weber et deer to latitudes  and °S and longitudes  and °W. & González, ; Duarte, ; Duarte et al., ), the se- We show that the species’ distribution is associated cond largest rainforest of the American continent, which  with , km of the Ombrophilous Dense Forest in the once stretched almost continuously along the Brazilian Brazilian Atlantic Forest, and this conclusion is supported coast, extending inland in the south and into eastern by species distribution modelling. The small red brocket Paraguay and north-eastern Argentina (Tabarelli et al., deer is the largest endemic species in Brazil and may have ). This biome may hold up to % of all species of the smallest geographical distribution of any Neotropical flora and fauna (Silva & Casteleti, ), and has a history deer species. This species occupies fragmented landscapes of intensive habitat loss and fragmentation caused by human activity. More than % of the original forest cover has already been cleared, and the land converted to  JOSÉ MAURÍCIO BARBANTI DUARTE (Corresponding author), ÂNGELA CRISTINA non-forest use (Ribeiro et al., ). TALARICO AND MÁRCIO LEITE OLIVEIRA Núcleo de Pesquisa e Conservação de The small red brocket deer is difficult to observe because Cervídeos, Departamento de Zootecnia, Universidade Estadual Paulista, Via it inhabits dense forests. In addition, morphological similar- de Acesso Paulo Donato Castellane, s/n, CEP 14884-900, Jaboticabal, São Paulo, Brazil. E-mail [email protected] ities with sympatric brocket deer species preclude the use of

ALEXANDRE VOGLIOTTI Universidade Federal da Integração Latino-Americana, traditional methodologies for detection and species identifi- Foz do Iguaçu, Paraná, Brazil cation (Duarte & Jorge, ; Vogliotti & Duarte, ,

JOSÉ EDUARDO GARCIA Universidade Federal de Pernambuco, Centro Acadêmico ). Skins and skulls from Brazilian scientific collections de Vitória, Vitoria de Santo Antão, Pernambuco, Brazil revealed size, coloration and pelage differences between spe- JESÚS E. MALDONADO* Center for Conservation Genomics, Smithsonian cimens taken from within the extent of occurrence of M. Conservation Biology Institute, National Zoological Park, Washington, DC, USA bororo and specimens of red brocket deer M. americana from other regions of Brazil (Rossi, ). Although some SUSANA GONZÁLEZ† Genética de la Conservación, Departamento de Biodiversidad y Genética, Instituto de Investigaciones Biológicas Clemente morphological characteristics (weight, height, length of Estable, Ministerio de Educación y Cultura, Montevideo, Uruguay body, circumference of thorax, and length of metacarpus *Also at: Department of Vertebrate Zoology, National Museum of Natural and metatarsus) may be potential discriminators of the spe- History, Smithsonian Institution, Washington, DC, USA † cies in living individuals or when entire carcasses are avail- Also at: Sección Genética Evolutiva, Facultad de Ciencias, Universidad de la  República Oriental del Uruguay, Montevideo, Uruguay able (Duarte & Jorge, ), these characteristics are Received  September . Revision requested  November . difficult to evaluate in the field using camera traps or even Accepted  April . First published online  October . visual encounter data.

Oryx, 2017, 51(4), 656–664 © 2016 Fauna & Flora International doi:10.1017/S0030605316000405 Downloaded from https://www.cambridge.org/core. IP address: 170.106.202.226, on 24 Sep 2021 at 20:03:19, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605316000405 Distribution of small red brocket deer 657

Because of these morphological similarities, it was only has the smallest geographical distribution of any deer spe- through karyotype characterization and subsequent mo- cies described to date, and its distribution appears to have lecular confirmation (Duarte et al., ) that the small decreased significantly over the past  centuries. We there- red brocket deer was identified and described as a distinct fore suggest there is an urgent need to develop conservation species from the red brocket deer (n= and n=,re- and restoration actions for all remnants of the Atlantic spectively; Duarte & Jorge, ). Karyotyping has been Forest, and recommend that conservation efforts should tar- proposed as the most reliable tool to distinguish M. bororo get the reduction of the edge effects of forest fragments, from other sympatric species of brocket deer (Duarte, ; palm heart exploitation and poaching. Duarte & Merino, ; Duarte & Jorge, ; Vogliotti & Duarte, ). However, to obtain karyotypes using cytogenetic protocols it is necessary to capture live individuals Study area and collect fresh samples (blood and skin), which is difficult The sampling sites were selected based on the proposed dis- for this elusive species (Duarte et al., ). Efforts to locate tribution of M. bororo in the Serra do Mar coastal forests and capture the deer are expensive, time consuming and in- ecoregion (Duarte, ). We focused on sampling in the feasible. We conducted intensive field work surveys for  Ombrophilous Dense Forest, and we also included other as- years and were able to locate and capture only five free- sociated formations, such as the Mixed Ombrophilous living M. bororo (Vogliotti & Duarte, ). This difficulty Forest (Araucaria moist forest), Semideciduous Seasonal prompted us to develop faster, more efficient methods to de- Forest (Paraná–Paraíba interior forests) and some ecotones. tect this rare and elusive species and determine its geograph- The chosen areas were mainly government protected areas ical range, using non-invasive sampling of faecal material in and private reserves . , ha. Additionally, we surveyed combination with molecular markers (polymerase chain re- buffer areas surrounding protected areas where the scat de- action–restriction fragment length polymorphism, PCR– tection dogs were forbidden from entering. These buffer RFLP; González et al., ). areas were adjacent to the protected areas and had similar Visually locating deer faeces in dense forest is challen- ecological characteristics. In total, we surveyed  sites in ging (Rivero et al., ). To maximize the number of faecal the states of São Paulo, Paraná, Santa Catarina, Bahia, samples detected during surveys we used scat detection Espírito Santo and Minas Gerais (Fig. ; Table ). dogs, which have been proven to significantly improve the detection of faeces from rare and elusive species (Smith   et al., ; Oliveira et al., ), and have been used effect- Methods ively to locate faecal samples from a diversity of carnivores     (Smith et al., , ; Harrison, ; Long et al., ; Sample collection and storage Reed et al., ; Vynne et al., ), Xenarthrans (Vynne et al., ), and North Atlantic right whales Eubalaena Searches for faecal samples were conducted during June glacialis (Rolland et al., ). –October  by one or more observers and a handler It is challenging to predict the ranges of rare and elusive with two scat detection dogs. The dogs were trained by the species precisely but this information is critical for conser- military police of São Paulo State narcotics detection pro- vation planning. One approach that has become increasing- gramme and worked freely off-lead. The searches were con- ly important is species distribution modelling (Guisan et al., ducted along natural trails and the borders of rivers and ), which is used to derive spatially explicit predictions of forests. Although the Atlantic Forest is continually affected environmental and ecological suitability for a particular spe- by deforestation and exploitation (Galindo-Leal & Câmara, cies. This is achieved by the identification of statistical rela- ), we had to assume that no changes in habitat or deer tionships between observations of species occurrence and distribution occurred over the time period of the sampling. environmental or ecological descriptors that characterize As we aimed only to record presence data, the sampling ef- the species’ ecological niche. Species distribution modelling fort was not recorded in detail (e.g. time in hours, or meters has the potential to play a critical role in supporting spatial surveyed) and the duration of surveys varied from  day in conservation decision making (Addison et al., ). It has some areas to up to  week in others. This sampling scheme proven to be particularly useful when occurrence data are precluded gathering true absence data. limited, and the results can be used to inform planning The collected faecal samples were stored in absolute etha- for new surveys (Pearson, ). nol in  ml sterile polypropylene conical tubes. The sam- To determine the geographical range of M. bororo more ples were identified by location name, collection number, accurately we conducted intensive non-invasive surveys geographical coordinates and date. When multiple faecal using scat detection dogs in all potential areas of occurrence, pellets were found accumulated in the same location they and used the occurrence data in species distribution model- were considered to belong to a latrine. In these cases, to ling. Our results confirmed that the small red brocket deer avoid resampling the same individuals, we collected only

FIG. 1 Sampling sites (Table ) for deer scat across the Brazilian Atlantic Forest. Forest type is categorized according to Veloso et al. (), and percentage tree cover is based on Hansen et al. ().

representative samples from clusters of pellets found at between M. bororo and its sympatric brocket deer species separate locations. M. americana, M. nana and M. gouazoubira (González et al., ). The presence of the restriction site for DNA extraction and PCR–RFLP ECORII or BSTNI in position  was used to confirm species identification because it has been demonstrated to be Faecal DNA extractions were performed using a Qiamp unique to M. bororo (González et al., ). PCR products DNA Stool Mini Kit (QIAGEN, Hilden, Germany) accord- that failed to digest were subjected to cycle sequencing to ’ ing to the manufacturer s protocol. Extractions were carried verify species identification. PCR products were purified ™ out in a dedicated room free of PCR products to prevent using a Zymoclean DNA Recovery Kit (Zymo Research, contamination. Irvine, USA), and sequenced using an ABI Prism xl  PCR amplifications of a bp fragment of Cytochrome b DNA Analyzer (Applied Biosystems, Foster City, USA) with  μ were performed in a final volume of l and contained the IDMAZL and IDMAZH (forward and reverse) pri-      ×Invitrogenbuffer, . mM MgCl, . mM of each dNTP mers described in González et al. (). Sequences were ana-  μ – (deoxynucleotide triphosphate), pmol l of each primer lysed using MEGA . (Tamura et al., ). (IDMAZL and IDMAZH; González et al., ), . – U Taq DNA Polymerase (Invitrogen), and – ng μl of faecal DNA. For the thermal profile we followed González Species distribution modelling procedures et al. (). We included a negative control in each set of PCRs performed, to detect any possible contamination. We developed species distribution models using MaxEnt The amplified  bp fragment of Cytochrome b con- v. ..k (Phillips et al., ), the most adequate and frequent- tains three informative restriction sites that can discriminate ly used software for species distribution modelling (Baldwin,

TABLE 1 Sampling localities (see numbered locations in Fig. ), total number of faecal samples collected, and number of samples identified, by Mazama species.

No. of samples identified Locality (State*) Total M. bororo M. americana M. nana M. gouazoubira Unknown 1. Serra da Bocaina National Park (SP) 0 0 0 0 0 0 2. Parque do Zizo Private Reserve (SP) 0 0 0 0 0 0 3. Serra do Mar State Park, Santa Virgínia (SP) 0 0 0 0 0 0 4. Serra do Mar State Park, Picinguaba (SP) 0 0 0 0 0 0 5. Serra do Mar State Park, São Sebastião (SP) 0 0 0 0 0 0 6. Pico do Marumbi State Park (PR) 0 0 0 0 0 0 7. Rio Guarani State Park (PR) 0 0 0 0 0 0 8. Mata do Barão Private Reserve (PR) 0 0 0 0 0 0 9. Pratigi Environmental Protection Area (BA) 0 0 0 0 0 0 10. Fazenda Fugidos (BA) 0 0 0 0 0 0 11. Fazenda Michelin (BA) 0 0 0 0 0 0 12. Santa Lucia Biological Station (ES) 0 0 0 0 0 0 13. Fazenda Lombardia (ES) 0 0 0 0 0 0 14. Serra do Ibitipoca (MG) 0 0 0 0 0 0 15. FLONA São Francisco de Paula (RS) 0 0 0 0 0 0 16. Jaraguá State Park (SP) 0 0 0 0 0 0 17. Mata dos Godoy State Park (PR) 1 0 0 0 0 1 18. Fazenda Barra Mansa (PR) 3 0 0 0 0 3 19. Fazenda São Nicolau (PR) 4 0 0 0 0 4 20. Serra do Mar State Park, Cunha-Indaiá (SP) 1 0 1 0 0 0 21. Pau-Oco State Park (PR) 1 0 0 1 0 0 22. ARAUPEL (PR) 1 0 1 0 0 0 23. Itirapina Ecological Station (SP) 1 0 0 0 1 0 24. Jataí Ecological Station (SP) 21 0 0 0 1 20 25. Lauraceas State Park (PR) 2 0 0 2 0 0 26. Pau-Brasil National Park (BA) 2 0 0 0 2 0 27. Serra do Tabuleiro State Park (SC) 3 2 0 0 0 1 28. Serra do Mar State Park, Pedro de Toledo (SP) 3 0 0 0 3 0 29. Araucárias State Park (PR) 4 0 0 3 0 1 30. Caiuá Ecological Station (PR) 5 0 5 0 0 0 31. Carlos Botelho State Park (SP) 10 5 0 0 0 5 32. Fazenda Boa Sorte (ES) 6 0 0 0 6 0 33. Guaratuba Environmental Protection Area (PR) 6 2 0 4 0 0 34. Fazenda Barreiro Rico (SP) 8 0 8 0 0 0 35. Serra do Mar State Park, Curucutu (SP) 8 0 3 0 5 0 36. Lago Azul State Park (PR) 9 0 5 0 4 0 37. Jacupiranga State Park (SP) 9 6 0 0 3 0 38. Fazenda João XXIII (SP) 11 10 1 0 0 0 39. Morro do Diabo State Park (SP) 13 0 8 0 5 0 40. Monte Alegre Private Reserve (PR) 13 0 1 0 12 0 41. Biritiba-Mirim (SP) 19 0 0 0 19 0 42. Serra do Itajaí National Park (SC) 28 4 0 21 0 3 43. Cajuru Legal Reserve (SP) 52 0 45 0 0 7 44. Intervales State Park (SP) 87 87 0 0 0 0 45. Iguaçu National Park (PR) 112 0 80 20 0 12 46. Santa Bárbara Ecological Station (SP) 112 0 0 0 111 1 Total samples 555 116 158 51 172 58

*SP, São Paulo; PR, Paraná; BA, Bahia; ES, Espírito Santo; MG, Minas Gerais; RS, Rio Grande do Sul; SC, Santa Catarina

 ). In comparison to other approaches MaxEnt performs (c.  km ). We used % of the points to train the model and well with small sample sizes (Hernandez et al., ). % to test the model. They were sampled by bootstrap- Occurrence data were based on only  sample locations, ping  random partitions with replacement (Pearson, following the exclusion of multiple records in the same pixel ).

FIG. 2 Species distribution model for Mazama bororo, with the extent of occurrence, IUCN geographical ranges, the proposed geographical range, and locations of occurrence (numbered as in Table )of Mazama species. A circle with two colours indicates that two species were found at the same sampling site.

The environmental layers were composed of bioclimatic operating curve, omission error and a two-proportion bino- variables, including mean annual temperature (bio), tem- mial test (Fielding & Bell, ; Elith et al., ; Pearson, perature seasonality (the standard deviation, multiplied by ; Phillips & Dudík, ). To predict the species’ distri- , of the monthly temperature; bio), annual precipitation bution we assumed only the probabilistic values over the (bio), precipitation seasonality (bio), and precipitation minimum training presence logistic threshold. of the driest month (bio), from the WorldClim database (Hijmans et al., ), percentage tree cover in – (Hansen et al., ), altitude (Valeriano, ), and slope Results obtained from the AMBDATA database. We also produced raster maps with Euclidean distance from maps of the pro- Species identification from scat samples tected areas (Ministério do Meio Ambiente, ), forest We collected  deer scat samples from  of the  sur- remnants (Ribeiro et al., ) and the Ombrophilous veyed areas. PCR reactions amplified  (%) of the sam- Dense Forest (Veloso et al., ). The environmental layers ples successfully. The RFLP reaction failed for PCR products were selected based on variables that had a high likelihood of from  samples (.%). For these samples we then pro- being associated with M. bororo habitat in the humid coastal ceeded to sequence the PCR products directly, but only  Atlantic Forest distributed throughout mountain chains. of the PCR products yielded sequences of sufficient quality All layers were trimmed to match the limits of the to determine species. The PCR–RFLP reaction and sequen- Atlantic Forest (modelling scope) and rescaled to a reso-  cing indicated that  (%) samples were from M. bororo. lution of  km . All spatial analyses were conducted using The remaining samples were from M. gouazoubira (; ArcMap v. .. (ESRI, Redlands, USA). We evaluated the %), M. americana (; %) and M. nana (; %). The degree of correlation between environmental variables small red brocket deer was positively identified in only seven using PAST . (Hammer et al., ). Two bioclimatic localities within the states of São Paulo, Paraná and Santa variables (mean annual temperature and precipitation of Catarina (Fig. ). the driest month) were removed because of their high correlation (r . |.|) with altitude and precipitation seasonality, respectively. We performed a principal components Geographical range analysis to select the most explicative variables. The variables identified and subsequently used in the MaxEnt ana- The size of the area obtained by linking external points of  lysis were bio, bio, bio, distance from Ombrophilous positive occurrence (extent of occurrence) was , km , Dense Forest, altitude, and percentage tree cover. The result- encompassing the Serra do Mar and Serra de ing model was evaluated using the area under the receiver Paranapiacaba from the states of São Paulo, Paraná and

Santa Catarina. This region encompasses the Ombrophilous greater ecological plasticity (Pinder & Leeuwenberg, ; Dense Forest, an Atlantic Forest formation that is close Black-Décima et al., ) and resistance to anthropogenic to the Brazilian coastline, at –°S. We did not detect habitat alteration (Rodrigues et al., ), has been extend- M. bororo samples in the states of Espírito Santo or Bahia. ing its range to include deforested areas that were previously To define the proposed geographical range we added a buf- covered with Atlantic Forest. The role of competition in the fer zone of  km to the extent of occurrence, except for the distribution and survival of sympatric brocket species in this areas that extended to the ocean (Fig. ). This yielded a geo- area needs careful evaluation to define and mitigate better  graphical range of , km , which is the best estimate of the effect of habitat changes in conservation plans for the the actual distribution of the species to date. small red brocket. Morphometric and morphological studies of skulls and skins from various Brazilian collections (Rossi, ) failed Species distribution modelling to clearly differentiate M. bororo from M. americana, although the data supported the presence of a partially differ- The model developed in MaxEnt (Fig. ) was evaluated entiated population of M. americana distributed throughout satisfactorily by the mean area under the curve (. ± the south coast of Brazil. These results were considered to be SD .) external test with  random partitions and the most reasonable evidence of the historical distribution of was significantly different from random (P , .)ina M. bororo in the Atlantic Forest. It is important to note that two proportion binomial test. The omission error was the ranges of distribution established here and by Rossi .. The model predicted the occurrence of M. bororo () were based on different methods, and there are with the highest values of environmental suitability at many uncertainties involved in the reconstruction of the Serra de Paranapiacaba, Guaraqueçaba Environmental historical distribution. However, we suspect that the extent Protection Area and Serra do Tabuleiro State Park (Fig. ). of the decline in distribution has been dramatic, as the spe- The variables that most contributed to the species distribu- cies would have occupied the mountain ranges of the Serra tion model were percentage tree cover (.%), distance de Paranapiacaba and the Serra do Mar, from the eastern from Ombrophilous Dense Forest (.%) and temperature part of the state of Santa Catarina to the state of São Paulo seasonality (.%). in the south and south-east regions of Brazil. We estimate  that the historical geographical range was , km  Discussion (Fig. ). The original proposed extent of the geographical distri- Species of the genus Mazama display a high degree of mor- bution of M. bororo was based on the localities of proven- phological similarity (Duarte et al., ), making it difficult ance of the captive individuals used in the karyotypic to distinguish them by direct field observations or camera characterization that resulted in the species description. traps (Vogliotti & Duarte, ). Our findings confirmed These individuals originated in the cities of Capão Bonito, the sympatry of M. bororo, M. americana, M. nana and Barra do Turvo, São José dos Pinhais and Paranaguá and M. gouazoubira by the identification of more than one of these localities were used to set the distribution limits to the species in nine of  localities sampled. Furthermore, the south of São Paulo and east of Paraná states (Duarte, we found one or more sympatric Mazama species in three , ; Duarte & Jorge, ; Vogliotti & Duarte, ). of seven localities (.%) where M. bororo was also de- Our survey results support an extension of the geograph- tected. We detected M. nana in sympatry with M. bororo ical range of the small red brocket deer to the latitudes – in two separate localities, and with M. gouazoubira in an- °S and to the longitudes –°W (Fig. ), encompassing  other locality (Fig. ). These two species (M. nana and , km . This range is considered to be the extent of M. gouazoubira) are more common than M. bororo in occurrence, similar to the current area of occupancy because human-altered and less pristine environments (Vogliotti, it represents an ecological continuum constituted by pro- ). This suggests that the more suitable habitats used tected areas. A comparison of the historical distribution of  by M. bororo are being altered even in the protected areas , km (Rossi, ) with our results suggests that there where our sampling took place. This change in M. bororo has been an % decline in the distribution over the last  habitat may be the result of edge effects (Ribeiro et al., centuries. Given its recent description and hypothesized ), palm heart exploitation, poaching (Vogliotti & geographical range, there is little historical evidence to facili- Duarte, ) or global climatic changes (Allen et al., tate evaluation of the effects of anthropogenic development ). We hypothesize that M. nana may be invading on the original distribution of the small red brocket deer. areas that were formerly occupied only by M. bororo and Currently, the habitat in the species’ area of occupancy is that this invasion may be facilitated by the degradation of well-preserved, with few barriers to gene flow. If protected, the Ombrophilous Mixed Forest. In addition, M. gouazou- habitat connectivity will help to maintain adequate levels of bira, which is known to be one of the brocket species with genetic diversity in the future.

The small red brocket is the largest endemic animal of for help with sample collection, and Instituto Brasileiro de Brazil, with perhaps the smallest geographical distribution Meio Ambiente, Instituto Chico Mendes de Conservação of any Neotropical deer species. It is categorized as da Biodiversidade, Secretaria do Meio Ambiente do Vulnerable on the IUCN Red List because of its small popu- Estado do Paraná, Secretaria do Meio Ambiente do Estado lation size and ongoing decline inferred from poaching and de Santa Catarina and EUCATEX S.A. Indústria e habitat loss, and because all of the remaining individuals are Comércio, who authorized the collection of samples in the from a single subpopulation (Duarte, ). It is threatened Conservation Units under their authority. Lillian Parker by human encroachment (% of the Brazilian population provided comments that greatly improved this article. lives within the original limits of the Atlantic Forest), poaching, and predation by dogs (Duarte, ). Species distribution modelling indicates that the current Author contributions geographical distribution reported by IUCN should be re- vised to encompass northern areas with high environmental JMBD was the project coordinator and contributed to writ- suitability, as well as the southern part of the Serra do ing the article. ACT and JEG conducted laboratory analysis. Tabuleiro State Park and Serra do Itajaí National Park, AV contributed to non-invasive sampling and data manage- where we collected occurrence data. In addition, areas of ment. MLO contributed to non-invasive sampling, labora- high suitability where no sampling was carried out or no tory analysis, distribution modelling, and writing the deer species were detected during sampling should be revis- article. JEM provided scientific support and contributed to ited to confirm presence or absence. We also suggest that fu- writing the article. SG provided scientific support, con- ture species distribution models incorporate variables based ducted laboratory analysis and contributed to writing the on patch size and connectivity. Species distribution model- article. ling provides more detailed information than traditional distribution estimates as it gives a suitability index for  each  km pixel instead of a continuous distribution of va- References lues. It increases our understanding of species’ needs and

gives support to conservation policies such as those for ADDISON, P.F.E., RUMPFF, L., BAU, S.S., CAREY, J.M., CHEE, Y.E., the design and establishment of protected and conservation JARRAD, F.C. et al. () Practical solutions for making models priority areas. indispensable in conservation decision-making. Diversity and We have demonstrated the importance of incorporating Distributions, , –. traditional field techniques with non-invasive sampling and ALLEN, C.D., MACALADY, A.K., CHENCHOUNI, H., BACHELET, D., MC DOWELL, N., VENNETIER, M. et al. () A global overview of sophisticated molecular tools to elucidate geographical drought and heat-induced tree mortality reveals emerging climate range, extent of occurrence, and areas with the highest suit- change risks for forests. Forest Ecology and Management, , ability for occupancy by the elusive small red brocket deer. –. Such information is essential in designing strategies for spe- BALDWIN, R.A. () Use of maximum entropy modeling in wildlife  – cies conservation, particularly in the Neotropics, where new research. Entropy, , . BLACK-DÉCIMA, P., ROSSI, R.V., VOGLIOTTI, A., CARTES, J.L., species with limited distributions are being discovered. MAFFEI, L., DUARTE, J.M.B. et al. () Brown brocket deer Conservation efforts should aim more specifically to main- Mazama gouazoubira (Fischer, ). In Neotropical Cervidology tain the last remnants of the Atlantic Forest and to target the (eds J.M.B. Duarte & S. González), pp. –. FUNEP, Jaboticabal, reduction of the edge effects of forest fragments, poaching Brazil, and IUCN, Gland, Switzerland.  and palm heart exploitation. M. bororo should be consid- DUARTE, J.M.B. ( ) Aspectos taxonômicos e citogenéticos de algumas espécies de cervídeos brasileiros. MSc thesis. Universidade ered a flagship species and used as an indicator of the quality Estadual Paulista ‘Júlio de Mesquita Filho’, Jaboticabal, Brazil. and restoration of the habitat. DUARTE, J.M.B. () Guia de identificação de cervídeos brasileiros. FUNEP, Jaboticabal, Brazil. DUARTE, J.M.B. () Mazama bororo. The IUCN Red List of Threatened Species v. .. Http://www.iucnredlist.org [accessed  Acknowledgements March ]. DUARTE, J.M.B., GONZÁLEZ,S.&MALDONADO, J.E. () The This project was funded by the Projeto de Conservação e surprising evolutionary history of South American deer. Molecular Utilização Sustentável da Diversidade Biológica Brasileira, Phylogenetics and Evolution, , –. Fundação de Amparo a Pesquisa do Estado de São Paulo, DUARTE, J.M.B. & JORGE,W.() Morphologic and cytogenetic Conselho Nacional de Desenvolvimento Científico e description of the small red brocket (Mazama bororo Duarte, )  – Tecnológico (Brazil), Agencia Nacional de Investigación y in Brazil. Mammalia, , . DUARTE, J.M.B. & MERINO, M.L. () Taxonomia e Evolução. In Inovación, Programa de Desarrollo de las Ciencias Básicas, Biologia e conservação de cervídeos Sul-americanos: Blastoceros, and Comisión Sectorial de Investigación Científica (Uruguay). Ozotoceros e Mazama (ed. J.M.B. Duarte), pp. –. FUNEP, We thank Renato Cheffer and Hermógenes Aparecido Torres Jaboticabal, Brazil.

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VYNNE, C., SKALSKI, J.R., MACHADO, R.B., GROOM, M.J., JÁCOMO,A. TALARICO is a biologist, and her MSc research focused on the dis- T.A., MARINHO-FILHO, J. et al. () Effectiveness of tribution of the small red brocket deer. ALEXANDRE VOGLIOTTI scat-detection dogs in determining species presence in a tropical has worked on small red brocket deer research and conservation, savanna landscape. Conservation Biology, , –. and is currently focused on deer ecology and conservation plan- WEBER,M.&GONZÁLEZ,S.() Latin American deer diversity and ning in the Atlantic Forest. JOSÉ EDUARDO GARCIA is interested conservation: a review of status and distribution. Ecoscience, , in the conservation genetics of Brazilian wildlife. MÁRCIO LEITE –. OLIVEIRA’s research is focused on distribution modelling and molecular ecology of brocket deer. JESÚS E. MALDONADO applies Biographical sketches non-invasive genetic techniques to study conservation genetics, be- havioural ecology and evolutionary genetics of a diversity of rare JOSÉ MAURÍCIO BARBANTI DUARTE has worked on various aspects mammals. SUSANA GONZÁLEZ has conducted research in conser- of the genetics, evolution, ecology and conservation of Neotropical vation biology for over  years and is co-chair of the IUCN SSC deer species, particularly of the genus Mazama.ÂNGELA CRISTINA Deer Specialist Group.