The Roosevelt–Rondon expedition marmoset Mico marcai: unveiling the conservation status of a Data Deficient species
F ELIPE E NNES S ILVA,HANI R OCHA E L B IZRI,JONAS DA R OSA G ONÇALVES L ÍSLEY P. LEMOS,RODRIGO C OSTA-ARAÚJO,IVAN J. LIMA A LINE T AVARES S ANTOS,MARCELO I SMAR S ANTANA C AETANO L. B. FRANCO and J EAN P. BOUBLI
Abstract The Roosevelt–Rondon Expedition marmoset on the IUCN Red List based on criterion Ac. Other Mico marcai was first collected in and all information Amazonian marmosets require similar reassessment as on this primate previously came from three skins brought their ranges also fall in the path of the arc of deforestation. back by this expedition. As a result, M. marcai is categorized Keywords Brazil, conservation status, Data Deficient, forest as Data Deficient on the IUCN Red List. As the presumed loss, marmoset, Mico marcai,Roosevelt–Rondon Expedition, range of M. marcai lies on the path of the advancing arc southern Amazonia of deforestation in Brazil, the collection of relevant data to assess the conservation status of this Amazonian species is Supplementary material for this article is available at of some urgency. Here we present the first field data on the https://doi.org/./S distribution and population size of, and threats to, M. mar- cai, to reassess the species’ conservation status. During – we surveyed the species in the Marmelos– Introduction Aripuanã interfluve, and estimated its density using distance ’ sampling. We also used spatial predictive modelling to esti- he assessment of a species extinction risk is the first mate forest loss within the species range under two deforest- Tstep towards its conservation. Species for which eco- ation scenarios. We found the marmoset in localities logical and population data are lacking are categorized on and estimated its extent of occurrence to be , km . the IUCN Red List as Data Deficient (IUCN, ), but it We estimated the species’ density to be . individuals/ is preferable that such species are assessed fully as they km and extrapolated this to estimate a total population of could potentially be threatened. One such species is ’ , individuals (CI ,–,). Under a business- Marca s marmoset Mico marcai, endemic to southern as-usual deforestation scenario, c. , km of forest, Amazonia, an area heavily impacted by the advancing comprising % of the species’ range, would be lost in Brazilian agricultural frontier. In the Brazilian National three marmoset generations (c. years), and we, therefore, Threat Assessment of Primates (ICMBio, ) M. marcai recommend that M. marcai be categorized as Vulnerable was the only marmoset categorized as Data Deficient, and it has the same categorization on the IUCN Red List (Rylands & Silva Jr, ). This primate was first observed and collected by the Roosevelt–Rondon Expedition in FELIPE ENNES SILVA* (Corresponding author) and JEAN P. BOUBLI‡ School of Environment and Life Sciences, University of Salford, M5 4WT, Salford, UK but remained overlooked in the National Museum of Rio de E-mail [email protected] http://orcid.org/0000-0002-1315-0847 Janeiro mammal collection for years until Alperin (), HANI ROCHA EL BIZRI†,JONAS DA ROSA GONÇALVES†,‡,LÍSLEY P. LEMOS,IVAN in a revision of all marmosets of the argentata group, de- J. LIMA,ALINE TAVARES SANTOS†,‡ and CAETANO L. B. FRANCO Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Brazil scribed it as a new taxon, Callithrix argentata marcai. This taxon was later elevated to full species and included RODRIGO COSTA-ARAÚJO Laboratorio de Evolução e Genética Animal, Universidade Federal do Amazonas, Manaus, Amazonas, Brazil in the genus Mico (Rylands et al., ). http://orcid.org/0000-0002-6092-4892 The museum tag of the type specimen of M. marcai in- MARCELO ISMAR SANTANA Faculdade de Agronomia e Medicina Veterinária, dicates it was collected at the confluence of the Roosevelt Universidade de Brasília, Campus Universitário Darcy Ribeiro, Brasília, and Aripuanã Rivers (Alperin, ; Fig. ). In van Distrito Federal, Brazil Roosmalen et al. () described a new species of marmo- *Also at: Instituto de Desenvolvimento Sustentável Mamirauá, Tefé, Brazil †Also at: School of Science and the Environment, Manchester Metropolitan set, M. manicorensis; its type locality is the confluence of University, Manchester, UK, and Comunidad de Manejo de Fauna Silvestre the Manicoré and Madeira Rivers (Fig. ). However, the hy- en la Amazonía y en Latinoamérica, Iquitos, Peru ‡ pothesized distribution of M. manicorensis encompasses the Also at: Instituto Nacional de Pesquisas da Amazônia, Manaus, Amazonas, – Brazil Manicoré Aripuanã interfluve, including the type locality Received November . Revision requested January . of M. marcai. Based on examination of the few available spe- Accepted February . First published online November . cimens, Garbino () proposed that the van Roosmalen
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 540 F. E. Silva et al.
FIG. 1 Locations of the transects used to survey for Mico marcai during January–February , sightings from –, earlier records from other observers (van Roosmalen et al., ; Rohe, ; Garbino, ) and the type locality (Alperin, ), in the Aripuanã– Marmelos interfluve of the Brazilian Amazon. Juma SDR, Açaí Grande Juma Development Reserve.
et al. () manicorensis was a junior synonym of marcai. encroachment, logging and infrastructure projects (Nepstad Silva et al. () presented the first information on the spe- et al., ; Vieira et al., ). The study area lies in the mu- cies occurrence in the wild, near its type locality, and dis- nicipality of Manicoré that, with Apuí municipality, is the cussed potential threats to the species. main area for livestock production in Amazonas State, Here we present the first investigation of the distribution forming the arc of cattle ranching (Carrero et al., ). and potential population size of M. marcai, using both field The area is considered a deforestation hotspot because of surveys and existing records, and assess the species’ conser- the presence of the federal road BR-, also known as the vation status. In addition, using spatial predictive modelling, Trans-Amazonian Highway (Fearnside et al., ; Carrero we predict the potential effect of two alternative land-use & Fearnside, ). scenarios on the species’ habitat. We believe this is the first study to categorize the conservation status of a Data Deficient Amazonian primate using uring a combination Methods of field surveys and remote sensing data. Surveys
– Study area During we carried out six expeditions to the Marmelos–Aripuanã interfluve to survey for marmosets This study was carried out in the Marmelos–Aripuanã inter- and other primates, totalling days of fieldwork. Our sur- fluve, two right bank tributaries of the Madeira River in veys included the confluence of the Roosevelt and Aripuanã Brazil (Fig. ). The climate is tropical, with a short dry season rivers, the upper and lower Manicoré River, and the mid in July–September, a mean annual temperature of °C and Aripuanã River (Fig. ). Surveys were conducted using exist- a mean annual precipitation of ,–, mm/year ing trails and roads, and with small boats. We recorded the (Hayakawa & Rossetti, ). The vegetation comprises location of all sightings, with a GPS, and, using these loca- mostly upland forest, and seasonally flooded forests (open lity records and data from the literature (Ferrari, ; van and dense lowland rainforest), and patches of pioneer Roosmalen et al., ; Alperin, ;Röhe,;Garbino, and savannah-like vegetation (Supplementary Fig. ; ), we defined the species’ extent of occurrence (EOO, Anderson, ). This region lies within the arc of deforest- sensu IUCN, ). We followed the IUCN () guidelines ation region of Amazonia, which is under severe threat from to calculate the EOO as the minimum convex polygon that the rapidly expanding Brazilian agricultural frontier, urban contains all of the species’ records (IUCN, ). Assuming
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 Status of Mico marcai 541
rivers are effective barriers to primate dispersal (Ayres & the estimated geographical range of the species and used Clutton-Brock, ), we adjusted this EOO accordingly predictive deforestation models to assess how much of the to measure the total area potentially occupied by the species species range will be lost by the end of (in years). (i.e. its geographical range). The IUCN criterion A assesses extinction risk over three To estimate the species’ density and abundance we sur- generations, and years is c. three generations for Mico leu- veyed two sites during January–February . Survey tran- cippe (Mittermeier & Rylands, ; Nishijima et al., ; sects were near the species’ type locality and along the lower data on generation time or lifespan for M. marcai are Manicoré River. In total, we opened six transects in the for- unavailable). mer site and four in the latter, averaging . ± SD . km Data on the annual rate of deforestation during – in length (Fig. ). The positioning of transects was by ran- were obtained from PRODES (). For predicted for- domization, using ArcGIS .. (ESRI, Redlands, USA), of est loss, we considered two scenarios (Soares-Filho et al., each trail starting point and direction from the main access ): () governance, which assumes current deforestation points (roads or rivers). Nine transects were opened perpen- trends but with a % cap in forest loss as a result of current dicularly to these access points so that any gradient of envi- laws that prohibit farmers from clearing . % of forest on ronment and primate density from the start of the trail to the their properties, and that existing and proposed protected interior of the forest was accounted for. Transects were at areas are effectively managed, and () business-as-usual, least km apart to avoid spatial dependence. We followed which considers current deforestation trends across the standardized field protocols for data collection, using dis- Amazon basin plus the effect of infrastructure development tance sampling (Buckland et al., ) to estimate marmoset and low effectiveness in the management of protected areas. densities. Two observers walked transects at a mean speed of We calculated the amount of forest loss in each scenario . km/h, recording the number of individuals sighted and and the percentage that lies within the geographical range of the perpendicular distance from the transect to the centre M. marcai, to estimate the forest loss to be expected by . of the group. Transects were surveyed during .–. We then used the IUCN Red List criteria (IUCN, )to in one direction and .–. in the reverse direction. evaluate the risk of extinction. Each transect was surveyed at least three times, with a -day break between surveys to reduce the impact of the ob- Results servers’ presence on the detection rate. We estimated the density of marmosets using Distance . (Thomas et al., – ). This analysis fits detection functions to provide the Geographical range During we observed M. marcai groups in localities: () along the left bank of the probability of detecting groups and estimate the number of individuals potentially missed by the observers. The Aripuanã and Roosevelt Rivers, ( ) on both banks of the Manicoré River, and () on both banks of the Branco encounter rate (groups/km) and the mean number of in- dividuals per group were used to estimate density. River, a small tributary of the Marmelos River (Fig. ; χ Table ). Based on these observations and data from the We first used a test to determine the appropriate trun- cations and perpendicular distances intervals for adjusting literature, we calculated the adjusted EOO to be , km , the detection functions, at P . .. We compared the ad- limited to the east by the Aripuanã River, to the west by justments of the detection functions using the Akaike the Marmelos River, to the north by the Madeira River and Information Criterion (AIC). The model with the smallest to the south by the open savannah vegetation of the AIC value was considered the best-fit for the data. If more Campos Amazônicos National Park, an area believed to be than one function was considered a good fit (i.e. the differ- a distribution limit for other marmoset species (Ferrari, ;Garbino,; Fig. ). ence in their AIC values, ΔAIC, was , ), we selected the model for which the density estimate had the lowest coeffi- cient of variation. We then used the density value to esti- Density and abundance In total we walked . km on the mate the abundance of M. marcai as A=D*a, where A is transects. We observed groups of M. marcai on ’ abundance, D is density and a is the species geographical occasions, giving an encounter rate of . individuals/km range. (CV .). The best distribution of perpendicular distances was obtained with five intervals of m each Evaluation of conservation status (χ = .,df=,P=.; Fig. ). The Uniform function with one cosine adjustment term provided the best fit As recommended by IUCN (), we multiplied the lower (AIC .). The number of individuals detected per confidence interval of the species’ density by the predicted group increased with perpendicular distance (r = −.; geographical area to obtain a conservative, naive estimate of P=.) and we therefore estimated mean group size population size. We calculated forest lost up to within using linear regression, giving a value of . individuals/
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 542 F. E. Silva et al.
TABLE 1 Occurrence records (with decimal latitude and longitude) of Mico marcai from our field surveys in the Ariupanã–Marmelos inter- fluve (Fig. ) and published data.
Locality Latitude (S) Longitude (W) Reference BR 230 (Matá Matá = Vila do Carmo) 7.5212 60.6733 This study Acampamento BR 230 7.5348 60.6906 This study Igarapé do Acampamento 7.5443 60.6783 This study Vicinity BR 230 7.4932 60.6868 This study Prainha, left margin of Aripuanã River 7.2219 60.7316 This study Linha Nova Esperança between Branco River (right bank) and 7.9411 61.6427 This study Santo Antônio do Matupi Estrada do Estanho, PARNA Campos Amazonicos 8.1049 61.8560 This study Manicoré River (right bank), Comunidade Mocambo 5.9841 61.5374 This study Manicoré River (right bank), Comunidade Lago dos Remédios 5.9327 61.4449 This study Manicoré River (left bank), Comunidade do Bom Fim 6.0224 61.6492 This study Manicoré River (left bank), Comunidade Três Estrelas 6.0221 61.6319 This study Manicoré River (right bank), Comunidade Terra Preta 5.9948 61.5812 This study Seringal São Luis, in the vicinity of the town of Manicoré 5.8411 61.3053 van Roosmalen et al. (2000) Type locality (Rio Castanho = Roosevelt River) 7.5500 60.7167 This study, Alperin (2002) Açaí Grande Juma Development Reserve (SDR) 6.0146 60.2090 Rohe (2007) Humaitá-Apuí Road (BR-230), km 292, left bank of Rio Aripuanã 7.5333 60.6667 Garbino (2014) Opposite Tenharin settlement, right bank of Rio dos Marmelos (BR-230) 7.9500 62.0500 Garbino (2014)
estimate of population size (, individuals), these levels of forest loss extrapolate to a loss of , M. marcai under the governance and , under the business-as-usual scenarios by . This indicates that, according to the business-as-usual scenario, the species should be categorized as Vulnerable based on criteria Acd (an estimated % population reduction projected over the next years, c. three generations), as a result of a predicted decline in EOO.
Discussion
IUCN Red List guidelines (IUCN, )recommendthat FIG. 2 Distribution of perpendicular distances of observations of species should be assessed using all available evidence to M. marcai on transects in the Marmelos–Aripuanã interfluve avoid, if possible, placing a species in the Data Deficient (Fig. ). The trend line indicates the best detection function fitted category (IUCN ). This category does not mean a to the distance classes. species is without threats, but rather that it is a priority for research, and there are examples of Data Deficient spe- group (CI .–.,CV., range –). Density was cies being categorized as threatened once relevant data be- estimated to be . individuals/km (CI .–.,CV came available (Bland et al., ). This is also the case for .) and group density . per km (CI .–.;CV M. marcai, which we recommend should be categorized as .). The naive estimate of abundance within the Vulnerable. species’ range was , individuals (CI ,–,). Our analysis indicates that M. marcai has an estimated minimum population of , individuals in a geograph- ical range of , km . Variation in group size may bias Conservation status Data from PRODES () indicated density estimates but the coefficient of variation of the a loss of ,. km of forest cover up to (% of the group size for Mico marcai is .% with a confidence inter- species’ estimated geographical range), and spatial predictive val of –, which is lower than estimated group sizes of other models (Soares-Filho et al., ) indicate that , km Neotropical primate species (i.e. those in the genera Saimiri (%) of forest will be lost in the next years under the and Sapajus; Peres ). Furthermore, despite employing governance scenario, and , km (%) under the distance sampling in only two regions within the species’ business-as-usual scenario (Fig. ). Using our conservative EOO, we surveyed the predominant forest type (dense
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 Status of Mico marcai 543
FIG. 3 Extent of occurrence of M. marcai in the Aripuanã–Marmelos interfluve (Fig. ), accumulated forest loss from to (PRODES, ), and forest loss predicted by under governance and business-as-usual scenarios (see text for details).
lowland rainforest) within the species’ range rather than the area of occurrence of M. marcai and two other marmosets: few patches of open lowland rainforest and pioneer the sympatric Callibella humilis and the marmoset vegetation. found along the right bank of Aripuanã River, Mico Despite a relatively large estimated population, the high chrysoleucos (Silva et al., a,b). In addition, the Trans- rate of deforestation in this region, caused by the ever- Amazonian Highway, which has negatively affected the expanding Brazilian agriculture frontier and infrastructure conservation of southern Amazonia (Kirby et al., ; development (roads and hydroelectric power plants), Carrero & Fearnside, ), bisects the range of M. marcai, poses a grave threat to the survival of M. marcai and and the municipalities of Apuí and Manicoré lie in the arc other marmoset species. A projected loss of % of the spe- of cattle ranching. cies total range by under a business-as-usual scenario is In the Brazilian government, through the Chico a bleak outlook. Mendes Institute for Biodiversity Conservation, assessed Although part of the current geographical range of M. the conservation status of Brazilian primates (ICMBio, marcai is theoretically conserved by Indigenous Lands and ), in which nine Mico species were categorized as Least protected areas, these units are under pressure from the cur- Concern, two as Near Threatened, and one as Vulnerable, rent trend of protected area downgrading, downsizing, and with only M. marcai categorized as Data Deficient. degazettement in the Brazilian Amazon (Bernard et al., However, the threats to Amazonian marmosets have been ; Ferreira et al., ; Pack et al., ). Three main fac- documented in only a few studies (Gonçalves et al., ; tors drive this, decreasing the effectiveness of protected Ochoa-Quintero et al., ) and the range of many of areas within M. marcai’s range: () political instability and these species has been estimated from relatively few re- changes in governmental policies on land use and conserva- cords (Ferrari, ; Silva Jr & Noronha, ;van tion in the Amazon, () planned hydroelectric dams, espe- Roosmalen et al., ;Noronhaetal.;Fialho, cially on the southern tributaries of the Amazon River, and ;Garbino,). Most Mico species inhabit the arc () increases in human settlements surrounding the of deforestation, where forest loss and other threats are Indigenous Lands and protected areas. Four hydroelectric similar to or higher than those estimated here for M. mar- dams will be constructed within M. marcai’s range, flooding cai. For example, Ochoa-Quintero et al. () predicted a an area of ,. km (ANEEL, ). The planned decline of . % of the potential distribution of M. rondo- dams and reservoirs of Prainha and Samaúma on the ni by as a result of forest loss, which meets the IUCN Aripuanã River, and the reservoirs Inferninho and criteria for Endangered (A). As a follow-up of our field- Cachoeira Galinha on the Roosevelt River, will reduce the work and data analysis, we have passed our results and
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 544 F. E. Silva et al.
recommendations to the Red List Authority. We advocate Modelagem de desmatamento e emissões de gases de efeito estufa na that the conservation status of all Amazonian marmosets região sob influência da rodovia Manaus-Porto Velho (BR-). – should be re-examined following the methods we have Revista Brasileira de Meteorologia, , . FERRARI,S.() Update of Callithrix nigriceps distribution. used for M. marcai. Neotropical Primates, , –. FERREIRA, J., ARAGAO, L.E.O.C., BARLOW, J., BARRETO,P., Acknowledgements Data collection and analysis were supported BERENGUER, E., BUSTAMANTE, M. et al. () Brazil’s by International Association for Conscientiology Expansion, environmental leadership at risk. Science, , –. Mamirauá Institute for Sustainable Development, Conselho Nacional FIALHO, M.D.S. () Contribuição à distribuição do gênero Mico, de Desenvolvimento Científico e Tecnológico (CNPq 200502/2015-8), (Callitrichidae, Primates) no médio Teles Pires, Jacareacanga, Pará. Conservation Leadership Programme, Conservation International, Neotropical Primates, , –. Primate Conservation Inc., International Primatological Society, and GARBINO, G.S.T. () The southernmost record of Mico emiliae Idea Wild. We thank the Gordon and Betty Moore Foundation (Thomas, ) for the state of Mato Grosso, northern Brazil. (Grant Agreement for Instituto de Desenvolvimento Sustentável Neotropical Primates, , –. Mamirauá, #5344), Isaac Theobald and Aldeísa for logistical support, GARBINO, G.S.T. () The taxonomic status of Mico marcai (Alperin and Catitu and José’s family for support in the field. ) and Mico manicorensis (van Roosmalen et al., ) (Cebidae, Callitrichinae) from Southwestern Brazilian Amazonia. Author contributions Study design: FES, HEB, JRG, LPL, RCA, IJL, International Journal of Primatology, , –. CLBF, AST and MIS; data collection: FES, JRG, LPL, RCA, IJL, ATS GONÇALVES, E.C., FERRARI, S.F., SILVA, A.L., COUTINHO, P.E.G., and MIS; data analysis: FES, HEB, JRG, CLBF and JPB; all authors MENEZES, E.V. & SCHNEIDER, M.P. () Effects of habitat contributed to interpretation of results and writing. fragmentation on the genetic variability of silvery marmosets, Mico argentatus.InPrimates in Fragments: Ecology and Conservation (ed Conflicts of interest None. L.K. Marsh), pp. –. Kluwer Academic Publishers, New York, USA. HAYAKAWA, E.H. & ROSSETTI, D.F. () Late Quaternary dynamics Ethical standards This research adhered to Brazilian law governing in the Madeira river basin, southern Amazonia (Brazil), as revealed primate research and the principles of he American Society of by paleomorphological analysis. Anais da Academia Brasileira de Primatologists for the ethical treatment of primates. Research permits Ciências, , –. were granted by ICMBio/SISBio (number 44707-2). ICMBIO () Fauna Brasileira. Http://www.icmbio.gov.br/portal/ faunabrasileira [accessed November ]. References IUCN () IUCN red list categories and criteria. Version .nd edition. IUCN, Gland, Switzerland, and Cambridge, UK. ALPERIN,R.() Callithrix argentata (Linnaeus, ): considerações KIRBY, K., LAURANCE, W., ALBERNAZ, A., SCHROTH, G., FEARNSIDE, taxonômicas e descrição de subespécie nova. Boletim do Museu P., B ERGEN, S. et al. () The future of deforestation in the Paraense Emílio Goeldi, Série Zoologia, , –. Brazilian Amazon. Futures, , –. ALPERIN,R.() Sobre a localidade tipo de Mico marcai (Alperin, MITTERMEIER, R.A. & RYLANDS, A.B. () Mico leucippe. The IUCN ). Neotropical Primates, , –. Red List of Threatened Species . Http://dx.doi.org/./IUCN. ANDERSON, A.B. () White-Sand vegetation of Brazilian Amazonia. UK..RLTS.TA.en [accessed October ]. Biotropica, , –. NEPSTAD, D., CARVALHO, G., CRISTINA, A., ALENCAR, A., PAULO, Ä., ANEEL (AGÉNCIA NACIONAL DE ENERGIA ELÉTRICA)() BISHOP, J. et al. () Road paving, fire regime feedbacks, and the Despacho no .,de de Junho de . http://www.aneel.gov.br/ future of Amazon forests. Forest Ecology and Management, , –. inventario-hidreletricos [accessed July ]. NISHIJIMA, K., SAITOH, R., TANAKA, S., OHSATO-SUZUKI, M., OHNO, AYRES, J.M., DE MALGHAES LIMA, D., MARTINS, E.S. & BARREIROS, T. & K ITAJIMA,S.(). Life span of common marmoset J.K.L. () On the track of the road: changes in subsistence (Callithrix jacchus) at CLEA Japan breeding colony. Biogerontology, hunting in a Brazilian Amazonian village. In Neotropical , –. Wildlife Use and Conservation (eds J.G. Robinson & K.H. Redford), NORONHA, M.A., SPIRONELLO, W.R. & FERREIRA, D.C. (). New pp. –. The University of Chicago Press, Chicago, USA. occurrence records of Mico acariensis (Primates, Callitrichidae). BERNARD, E., PENNA, L.A.O. & ARAÚJO,E.() Downgrading, Neotropical Primates, , . downsizing, degazettement, and reclassification of protected areas OCHOA-QUINTERO, J., CHANG, C., GARDNER, T., REZENDE MESSIAS, in Brazil. Conservation Biology, , –. M., SUTHERLAND,W.&DELBEN,F.() Habitat loss on Rondon’s BLAND, L.M., COLLEN, B., ORME, C.D.L. & BIELBY,J.() Predicting marmoset potential distribution. Land, , . the conservation status of data-deficient species. Conservation PACK, S.M., FERREIRA, M.N., KRITHIVASAN, R., MURROW, J., Biology, , –. BERNARD,E.&MASCIA, M.B. () Protected area downgrading, BUCKLAND, S.T., ANDERSON, D.R., BURNHAM, K.P. & LAAKE, J.L. downsizing, and degazettement (PADDD) in the Amazon. () Distance Sampling: Estimating Abundance of Biological Biological Conservation, , –. Populations. Chapman and Hall, New York, USA. PERES, C.A. () Structure and spatial organization of an Amazonian CARRERO, G.C., ALBUJA, G., FRIZO, P., HOFFMAN, E.K., ALVES,C.& terra firme forest primate community. Journal of Tropical Ecology, , BEZERRA, C.D.S. () A Cadeia Produtiva da Carne Bovina no –. Amazonas. Instituto de Conservaçã e Desenvolvimento Sustentável PRODES () PRODES. Http://www.dpi.inpe.br/prodesdigital/ da Amazônia, Manaus, Brazil. prodes.php [accessed June ]. CARRERO, G.C. & FEARNSIDE, P.M. () Forest clearing dynamics RÖHE,F.() Mamíferos de médio e grande porte. In Biodiversidade and the expansion of landholdings in Apuí, a deforestation hotspot do Médio Madeira: Bases Científicas Para Propostas de Conservação on Brazil’s Transamazon highway. Ecology and Society, , . (eds L.R. Py-Daniel, C.P. Deus, A.L. Henriques, D.M. Pimpão & FEARNSIDE, P.M., DE GRAÇA, P.M.L.A., KEIZER, E.W.H., O.M. Ribeiro), pp. –. Instituto Nacional de Pesquisas da MALDONADO, F.D., BARBOSA, R.I. & NOGUEIRA, E.M. () Amazônia, Manaus, Brazil.
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303 Status of Mico marcai 545
RYLANDS, A.B., SCHNEIDER, H., LANGGUTH, A., MITTERMEIER, R.A., SILVA, F.E., NUNES, H.G. & BASTOS,A.() Rediscovery of Marca’s GROVES, C.P. & RODRÍGUEZ-LUNA,E.() An assessment of the marmoset and the challenges for its conservation. Oryx, , . diversity of new world primates. Neotropical Primates, , –. SOARES-FILHO, B.S., NEPSTAD, D.C., CURRAN, L.M., CERQUEIRA,G. RYLANDS, A.B. & SILVA,JR, J.S. () Mico marcai.InThe IUCN Red C., GARCIA, R.A., RAMOS, C.A. et al. () Modelling conservation List of Threatened Species . Http://dx.doi.org/./IUCN. in the Amazon basin. Nature, , –. UK..RLTS.TA.en [accessed November ]. THOMAS, L., BUCKLAND, S.T., REXSTAD, E.A., LAAKE, J.L., SILVA,JR, J.S. & NORONHA, M.A. () A new record for Callithrix STRINDBERG, S., HEDLEY, S.L. et al. () Distance software: mauesi Mittermeier, Schwarz and Ayres, . Neotropical Primates, design and analysis of distance sampling surveys for estimating , –. population size. Journal of Applied Ecology, , –. SILVA, F.E., COSTA-ARAÚJO, R., BOUBLI, J.P., SANTANA, M.I., VAN ROOSMALEN, M.G.M., VAN ROOSMALEN, T., MITTERMEIER,R. FRANCO, C.L.B., BERTUOL,F.etal.(a) In Search of a meaningful A. & RYLANDS, A.B. () Two new species of marmoset, genus classification for Amazonian marmosets: should dwarf marmosets be Callithrix Erxleben, (Callithrichidae, Primates), from the considered Mico congenerics? Zoologica Scripta, , –. Tapajós/Madeira interfluvium, South Central Amazonia, Brazil. SILVA, F.E., ENDO,W.,DE SOUSA E SILVA JÜNIOR, J., MARCELO,J.& Neotropical Primates, , –. SANTOS,A.(b) New insights into the distribution and VIEIRA, I.C.G., TOLEDO, P.M., SILVA, J.M.C. & HIGUCHI,H.() conservation status of the golden-white tassel-ear marmoset Mico Deforestation and threats to the biodiversity of Amazonia. Brazilian chrysoleucos (Primates, Callitrichidae). Primates, , –. Journal of Biology, , –.
Oryx, 2020, 54(4), 539–545 © 2018 Fauna & Flora International doi:10.1017/S0030605318000303 Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.139, on 25 Sep 2021 at 01:55:05, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000303