sign in sign up
<<
Home , Euryoryzomys macconnelli, Glyphonycteris, Hylaeamys yunganus, Neacomys dubosti, Neacomys paracou, Oecomys auyantepui

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/236736910

Mammals of Amapá State, Eastern Brazilian Amazonia: A revised taxonomic list with comments on distributions

Article in Mammalia · November 2013 DOI: 10.1515/mammalia-2012-0121

CITATIONS READS 33 360

14 authors, including:

Ana Carolina Moreira Martins Enrico Bernard University of Brasília Federal University of Pernambuco

10 PUBLICATIONS 116 CITATIONS 72 PUBLICATIONS 1,593 CITATIONS

SEE PROFILE SEE PROFILE

Renato Gregorin Alexandre Reis Percequillo Universidade Federal de Lavras (UFLA) University of São Paulo

62 PUBLICATIONS 1,066 CITATIONS 87 PUBLICATIONS 1,002 CITATIONS

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Natural history and ecology of two sympatric species of of the tribe (: ) in the Atlantic Forest View project

Functional and Phylogenetic Diversity of non-volant small in Atlantic Forest View project

All content following this page was uploaded by Ana Carolina Moreira Martins on 30 May 2014.

The user has requested enhancement of the downloaded file. DOI 10.1515/mammalia-2012-0121 Mammalia 2013; aop

Cl á udia Regina da Silva* , Ana Carolina Moreira Martins , Isai Jorge de Castro, Enri co Bernard , Elizandra Matos Cardoso , Danielle dos Santos Lima, Renato Gregorin , Rog é rio Vieira Rossi , Alexandre Reis Percequillo and Keliane da Cruz Castro Mammals of Amapá State, Eastern Brazilian Amazonia: a revised taxonomic list with comments on species distributions

Abstract: The Guiana Shield has large, preserved areas Isai Jorge de Castro and Keliane da Cruz Castro: Programa de with high biological diversity. However, the knowledge of Pó s-Gradua ç ã o em Biodiversidade Tropical, Universidade Federal this biodiversity differs among the regions with the - do Amapá (UNIFAP), Rodovia Juscelino Kubitschek, km-02, bairro Jardim Marco Zero, CEP 68.902-280, Macap á , Amap á , Brazil ian portion poorly known compared to the , Enrico Bernard: Departamento de Zoologia, Universidade Federal de , , and . In the Amap á State, the Pernambuco (UFPE), Rua Nelson Chaves s/n, Cidade Universit á ria, information on mammals is very heterogeneous and repre- CEP 50. 670-420, Recife, Pernambuco, Brazil sents a gap in the knowledge of the distribution and diver- Elizandra Matos Cardoso: Universidade do Estado do Amapá sity of some groups. We compiled a list of the mammals of (UEAP), Avenida Presidente Vargas, n. 650, bairro Centro, CEP 68.906-970, Macap á , Amap á , Brazil the Amapá based on the inventories, voucher specimens Danielle dos Santos Lima: Grupo de Pesquisa em Mamí feros deposited in the collection Fauna of Amapá at Instituto de Aquá ticos Amazô nicos, Instituto de Desenvolvimento Sustentá vel Pesquisas Cientí ficas e Tecnoló gicas do Estado do Amapá , Mamirau á (IDSM), Estrada do Bexiga, n. 2.584, bairro Fonte Boa, and previous published studies. We present a list of 181 CEP 69.470-000, Tef é , Amazonas, Brazil species. Chiroptera was the order with the high- Renato Gregorin: Departamento de Biologia, Universidade Federal de Lavras (UFLA), Caixa Postal 3037, CEP 37.200-000, Lavras, Minas est number of species (88) followed by Rodentia (32). The Gerais, Brazil list includes 17 new occurrences: 16 for Amap á (five mar- Rog é rio Vieira Rossi: Universidade Federal do Mato Grosso (UFMT), supials, eight , one canid, one cetacea and one ) Av. Fernando Corrê a da Costa, 2.367, bairro Boa Esperan ç a, CEP and one for Brazil (one rodent). This species list is the most 78.060-900, Cuiab á, Mato Grosso, Brazil complete taxonomic review for the Amapá, contributes to Alexandre Reis Percequillo: Escola Superior de Agricultura “ Luiz the knowledge of mammal diversity north of the Amazon de Queiroz ” (ESALQ), Universidade de S ã o Paulo (USP), Avenida P á dua Dias n. 11, Caixa Postal 9, CEP 13.418-900, Piracicaba, S ã o River, and helps increase the precision of the species ranges Paulo, Brazil in the Guianas and the eastern portion of the Amazon.

Keywords: diversity; Guiana Shield; inventory; new occurrences. Introduction

*Corresponding author: Cl á udia Regina da Silva, Laborat ó rio de The tropical forests harbor almost 50% of the Earth ’ s bio- Mam í feros, Instituto de Pesquisas Cient í ficas e Tecnol ó gicas do Estado diversity in only 7% of the terrestrial surface area (Whit- do Amapá (IEPA), Rodovia JK, Km 10, s/n, bairro Fazendinha, CEP more 1998 ). The Amazon is the largest and most diverse 68912-250, Macapá , Amapá , Brazil, e-mail: crsilva.ap@gmail. com ; and tropical forest in the world with over six million square Programa de Pó s-Gradua ç ã o em Gené tica, Conservaç ã o e Biologia kilometers across nine countries of (Silva Evolutiva, Instituto Nacional de Pesquisas da Amaz ô nia (INPA), et al. 2005 ). It has several regions with different levels Avenida Andr é Araú jo, n. 2936, bairro Petr ó polis, CEP 69.060-000, Manaus, Amazonas, Brazil of conservation and knowledge (Silva et al. 2005 , Lim Ana Carolina Moreira Martins: Programa de P ó s-Gradua ç ã o em et al. 2005 ). The endemic regions of the Amazon Basin Ecologia, Universidade Federal de Brasí lia (UnB), Campus Universitá rio have been proposed based mainly on the distribution Darcy Ribeiro, CEP 70910-900, Brasí lia, Distrito Federal, Brazil of taxa, such as the angiosperms (Prance 1982 ), verte- Isai Jorge de Castro, Elizandra Matos Cardoso, Danielle dos Santos brates (Webb 1978 ), amphibians (Duellman 1982 ), birds Lima and Keliane da Cruz Castro: Laborat ó rio de Mamí feros, Instituto de Pesquisas Cient í ficas e Tecnol ó gicas do Estado do (Haffer 1974 , Cracraft 1985 , Ribas et al. 2012 ), and non- Amap á (IEPA), Rodovia JK, Km 10, s/n, bairro Fazendinha, CEP volant mammals (Patton et al. 2000 , Voss et al. 2001 , 68912-250, Macap á , Amap á , Brazil Costa 2003 , Patton and Costa 2003 , Steiner and Catzeflis

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 2 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

2004 ). The main endemic regions are Imeri (northcen- Silva et al. 2008 , Thoisy et al. 2009 ). In the present study, tral Amazon), Inambari (southwestern Amazon), Napo our objective was to present a species list of the mammals (northwestern Amazon), Belé m-Par á (southeastern of Amapá , report the occurrence of the mammal species Amazon), and Guiana (northeastern Amazon) (Haffer in the protected areas, and contribute to the knowledge of 1974 , Cracraft 1985 , Patton et al. 2000 , Silva et al. 2005 ). the mammals in the endemic region of the Guianas and The Guiana region comprises the northeastern part of the eastern Amazon. Amazon from the Orinoco, Casiquiare, and Negro rivers in the west to the Amazon River in the south (Hershko- vitz 1969 , Eisenberg 1989 , Voss et al. 2001 ). This region Materials and methods comprises southeastern Venezuela, Guyana, Suriname, French Guiana, and northern Brazil, including the states of Amapá and Roraima, and the northern portion of Ama- Study area zonas and Par á . Several inventories have documented a high diver- The predominant vegetation of the Amap á is the terra sity of mammals and high degree of endemism in this firme forest, which covers over 70% of its territory. In region (Voss and Emmons 1996 , Barnett and Cunha 1998 , the rest of the state (the eastern band), the predominant Robinson 1998 , Simmons and Voss 1998 , Voss et al. 2001 , vegetation is composed of the savannas, flooded fields, Sanderson and Igná cio 2002, Sampaio et al. 2003 , Trolle and mangroves (IBGE 2004 ). The large preserved areas of 2003 , Lim and Engstrom 2005 ). The recent inventories in the terra firme may still be found in the state, where the Amap á have also documented a high diversity (Martins history of the environmental change and impact is recent et al. 2006 , Martins and Bernard 2008 , Silva 2008 , and concentrated along Highway BR156 and on the coast, Martins et al. 2011 ). However, a comprehensive list of the where water buffalos are raised (Monteiro 2009 , Oliveira mammal species and habitats is still lacking. In the past 2009). The state has 12 protected areas (except munici- 7 years, efforts to improve the knowledge on the mammal pal and private reserves) and five indigenous reserves diversity in Amap á , mainly for the rodents, marsupi- (Waj ã pi, Ua ç á , Galibi, Jumin ã , and Parque Ind í gena do als, and bats, added new species to the list of Carvalho Tumucumaque). The savannas may be found in Á rea de (1962) , which comprised 62 species. Proteç ã o Ambiental do Rio Curiaú (APA Curiaú ), Floresta The recent inventories began in 2004 with the project Estadual do Amap á (FLOTA Amap á ), and Reserva Extra- ‘ Invent á rios Bioló gicos no Corredor de Biodiversidade do tivista do Rio Cajari (RESEX Cajari). The western portion of Amapá ’ and explored mainly terra firme forest reserves Amapá is covered by large areas of the terra firme forest, (Bernard 2008 ). The biological inventories were con- which are protected by six reserves: Parque Nacional Mon- ducted primarily for the management plans of the reserves tanhas do Tumucumaque (PARNA Tumucumaque), Flo- with flooded fields, mangroves, and floodplain forests resta Nacional do Amapá (FLONA Amapá ), FLOTA Amapá , (Table 1 ). The savannas, which have been only recently Reserva do Desenvolvimento Sustent á vel do Rio Iratapuru studied, have been sampled mainly in association with (RDS Iratapuru), RESEX Cajari, and Esta ç ã o Ecol ó gica do the private companies that requested the environmental Jari (ESEC Jari). The coastal environments, mangroves, assessments. Despite the large protected areas in the state, and flooded fields are also protected by seven reserves: poaching, water buffalo farming in floodplain forests Parque Nacional do Cabo Orange (PARNA Cabo Orange), and flooded fields (Monteiro 2009 ), and the expansion Esta ç ã o Ecol ó gica Marac á -Jipioca (ESEC Marac á ), Reserva of agriculture and urban areas in the savannas (Oliveira Biol ó gica do Parazinho (REBIO Parazinho), Reserva 2009) are the emerging issues that may affect the wild Biol ó gica do Lago Piratuba (REBIO Piratuba), APA Curia ú , mammal populations. The mammal fauna is important to Á rea de Prote ç ã o Ambiental da Fazendinha (APA Fazend- the ecological processes related to the forest dynamics, inha), and RESEX Cajari. Herein, we present information such as seed dispersal (Charles-Dominique et al. 1981, on the occurrence of the mammals in the seven reserves Booman et al. 2009 , Grü newald et al. 2010), pollination (Table 1): PARNA Tumucumaque, FLONA Amapá , REBIO (Wester et al. 2009 ), and seed predation (Lambert et al. Piratuba, REBIO Parazinho, APA Curiaú , RESEX Cajari, 2005 ). In addition, the severe alterations to the mammal and RDS Iratapuru. These areas were sampled as part of assemblages directly affect the livelihood of the human the research projects and inventories for the management populations, as some mammals are game species (Parry plans. The other sampling events resulted from the aca- et al. 2009 ), indicators of environmental quality (Zocche demic studies, environmental assessment reports, and et al. 2010 ), and vectors of tropical diseases (Maia da joint efforts with the private sector.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 3 h) 2 (m 212,400 Mist nets nets Mist Visual census (h) census buckets) Pitfalls (night (night Pitfalls 42002950 3880 228.3 – 36.624 130.88 77.112 in the mammal inventories carried out in the state of of in the state out inventories carried in the mammal traps (night traps) (night traps Sherman and cage cage Sherman and plantation forest 4480 forest 2112 144 19,920 7500 4000 – forest forest 4940 forest 3212 162 4000 52,056 2880 1600 1440 130 37.200 220 174.744 forest forest forest forest forest forest forest forest forest 1500 forest 1800 1800 1650 1640 700 1640 792 1560 792 1500 700 55.40 forest 60 1500 720 forest 1500 720 16,272 64 9792 720 62 700 16,200 62 700 12,720 60 700 17,010 60 19,089 60 21,114 60 4000 21,096 62 4000 19,920 19,800 1400 1400 240 240 – – Eucalyptus Terra firme Terra and firme Terra floodplain and Savanna forest Terra firme Terra islands firme Terra firme Terra Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra firme Terra Year Vegetation Sampling effort 2008 2009 2011 and 2009 and (decimal (decimal degrees) Longitude Longitude 1.4974 -49.1375 2006 fields Flooded 500– 26 10,008 1.32281 -50.288601 2007 Floodplain forest – – 14,520 (decimal (decimal degrees) Locality Latitude Piratuba) Piratuba The study sites (with geographic coordinates), year sampled, vegetation type, collection method, and sampling effort used method, and type, collection sampled, vegetation year coordinates), geographic sites (with The study Table 1 Table Study site Amap á , northern Brazil, from 2004 to 2010. from 2004 to 2010. , northern Brazil, á Amap 20 River Horto Matapi Matapi; 0.484427 -51.2465ú Curia 28 APA (REBIO Village 2008 River/Tabaco Araguari riparian forest Savanna, 0.11667 -51.0500 2007 and 19 Jari River Itapeuara; 21 Rivero Bento; Aporema ã 22S Horto 23 ã o 24 Caldeir Waterfall; Araguari River25 River Gomes; Araguari Ferreira -0.492243 NovaVila 26 BR 156; Highway 1.3024 Cajari) BR 156 (RESEX Highway -52.693001 0.814676)á Amap (FLONA PPBio Plot 2008 and -50.7674 0.874676 -51.318501 -51.194901 -0.155045 -0.8833 2008 2009 forest fields and Flooded -51.548901 -1.06852 2009 -51.8500 riparian forest and Savanna 2010 -43.1100 riparian forest and Savanna 2010 2010 and 3500 2880 1600 1440 100 37.056 227 147.744 123 é Igarap do ç o Bra (FLONA 4 á ) Amap Tumucumaque) River (PARNA Amapari 5 Iratapuru) Jari River (RDS 6Tumucumaque) River (PARNA Mapaone 1.5957487 é Igarap Santo 1.308091 Ant ô nio (FLONA 8 á ) Amap Iratapuru) (RDS Baliza 0.288852é -52.492150 Igarap 9 Iratapuru) River (RDS Cupixi -51.58794410Tumucumaque) 1.12781 River (PARNA Anotaie -55.099811 2004Tumucumaque) River (PARNA Mutum 0.288852Tumucumaque) 12 River (PARNA Anacui -51.879581 2004 0.30778913 Gomes Ferreira Savanna; 3.22032 aua River (REBIO Piratuba) 2005 ç 14 Araque -53.0998 2.19333 0.582343 -52.027901 3.85395 Maresias Lake (REBIO Piratuba) -52.4515 2005 REBIO of surroundings Farm, Macarry -52.332199 -51.98902 -52.757702 2004 1.4871 200517 2005 18 2005 1.02524 2006 2006 1.4982 Cajari) (RESEX Village Marinho -49.8833 Jari RiverWaterfall; nio ô Santo Ant -51.161598 - 49.5781 2006 Mangrove 2006 -0.5905 -0.5989 riparian forest and Savanna 2006 Mangrove -52.5313 -52.2426 2007, 2008 1500 2007 700 750 600 60 17,832 – – 17 34 8112 8019 1516 Riverá BR 156; Marac Highway do Jari BR 156; Laranjal Highway -0.710733 -0.1509 -52.39848 -51.7438 2006 2006 Savanna 4000 1400 240–

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 4 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia h) 2 Data collection (m

Mist nets nets Mist The species list was based on the data compiled from Car- valho (1962) , Peracchi et al. (1984) , Martins et al. (2006) ,

Visual Griffiths and Gardner (2008) , Martins and Bernard (2008) ,

census (h) census Silva (2008) , Castro (2009) and Martins et al. (2011) . The unpublished inventories between 2004 and 2011 comple- mented this list (Table 1 and Figure 1 ). The voucher speci- mens were deposited in the collection Fauna of Amap á buckets) (CCFA), located at Instituto de Pesquisas Cient í ficas e

Pitfalls (night (night Pitfalls Tecnoló gicas do Estado do Amapá (IEPA). This material – – – 15,163.2 – – – 26,616 – – – 14,520 comprised skin and skull, and fluid-preserved speci- mens. The voucher specimens deposited before 2004 were also included in the species list. The record of Echimys chrysurus Zimmermann 1780 was based on a specimen from Museu Paraense Emilio Goeldi (MPEG 15186), and traps (night traps) (night traps Sherman and cage cage Sherman and the record of sp. Hershkovitz 1962 relates to the two specimens housed at the Museu Nacional da Universidade Federal do Rio de Janeiro (MNRJ 60713 and 60714). The nonvolant small mammals were collected with the

forest flooded flooded forest conventional traps (Sherman and wire mesh cages), pit- falls, air guns, and by hand. The collections were author- ized by the federal and state licenses (IBAMA 2/2004, islands Mangrove and floodplain Mangrove and forest Terra firme Terra fields 75/2004, 143/2004, 135/2005, 100/2005, 32/2005, 3/2005, 295/2006, 81/2007, 256/2009, 19140-1, SEMA 1/2008, Year Vegetation Sampling effort 2008 2/2009, 16/2009). The sampling effort was calculated by multiplying the number of traps by the working days (Table 1). To sample the medium and large mammals, we used visual census, indirect records (traces, vocalizations, and burrows), and, occasionally, shooting with guns. We (decimal (decimal degrees)

Longitude Longitude used mist nets to collect the bats (most were 12-m long), placed in the understory (up to 3 m above the ground), along previously opened trails. The sampling effort was calculated as the area of each net multiplied by the time of

1.2267 -50.090801 2007 Floodplain forestexposure, number – of nights, – and 27,864 number of nets following (decimal (decimal degrees) Straube and Bianconi (2002) . 1.18133056 -50.56000833 2008

Taxonomic considerations

For the bats and marsupials, the nomenclature follows Gardner (2008) . There were some exceptions: the genus Saussure 1860 was followed by the most recent revisions by Velazco (2005) , Velazco and Gardner (2009) , Velazco and Patterson (2008) , and Velazco et al. (2010) ; the name Marmosa Gray 1821 for the marsupials was assigned to Micoureus Lesson 1842 (Voss and Jansa Locality Latitude Villages (REBIO Piratuba) Villages (REBIO Piratuba)

Continued) 2009 ); Monodelphis touan (Shaw 1800) instead of Mono- delphis brevicaudata Erxleben 1777 (Pavan et al. 2012 ). For Table 1 Table 32 Lakes region (REBIO Piratuba) 1.43783 -50.575901 2009 forest fields and Flooded ( Study site 29 Bom Amigo Milagre de Jesus and 31 River (REBIO Piratuba) Sucuriju 1.65828 -49.9674 2007 and 30 Villages Lago Novo Firme and Terra the other groups, we followed Wilson and Reeder (2005)

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 5 with the following exceptions: Mazama nemorivaga Cuvier later corrected and the specimen identified as E. furinalis 1817 as valid species and not as a subspecies of Mazama D ’ Orbigny 1847 (Mok et al. 1982 ). gouazoubira Fischer 1814 (Rossi et al. 2010 ); Aotus infula- tus (Kuhl 1820) as valid and not as a subspecies of Aotus azarae Humboldt 1811 (Hershkovitz 1983 ); Chiropotes sagulatus (Traill 1821) as valid species from the previously Results and discussion treated as Chiropotes chiropotes (Humboldt 1811) (see Silva Jr. and Figueiredo 2002 , Silva Jr. et al. 2008 ); we fol- Excluding the exotic species, we recorded a total of 181 lowed Voss (2011) for Coendou melanurus (Wagner 1842); mammal species in Amap á . When we compare our data and considered the taxonomic arrangements proposed by to the list of Lim et al. (2005) , excluding five marine Weksler et al. (2006) for the rodents previously assigned to species, the remaining 178 species represent 64% of the Baird 1857 by Lynch -Alfaro et al. (2012) to the pri- 275 species of the nonmarine mammals recorded for the mates allocated in Cebus . We did not consider the record Guiana region (excluding the Brazilian portion). The most of Platyrrhinus lineatus E. Geoffroy 1810 (Martins et al. diverse order in the Amap á was Chiroptera with 88 species 2006 ) because Velazco and Patterson (2008) revised the or 48.6% of all the mammal species recorded in the state. genus based on the phylogenetic data and confirmed the Rodentia was the second order in terms of the number occurrence of this species only in the southwestern Brazil- of species and representing 17.6% of the total. The other ian Amazon. We did not consider the record of Eptesicus orders together corresponded to 33.9% of all the species fuscus Beauvois, 1796 by Piccinini (1974) because it was (Table 2).

Figure 1 The location of the study sites in the state of Amapá , northern Brazil. The numbers of the sampling localities can be seen in Table 1.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 6 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

Table 2 The mammal species recorded in the state of Amap á , and Gardner 2008a ). We collected two specimens of eastern Brazilian Amazon, for each order. G. emiliae (IEPA 2376 and 3454) in a savanna (Figure 1, PA 23) and another one in the terra firme forest (Figure1, PA Order Number of species Percentage1 (%) 26). Based on the marginal localities in Gardner (2008) , Didelphimorphia 15 8.3 Hyladelphys kalinowskii occurs in , Brazil (Amazo- Sirenia 2 1.1 nas State), French Guiana, and Guyana. However, this Cingulata 5 2.8 species is represented by very few specimens in the col- Pilosa 5 2.8 Primates 10 5.5 lections (Voss et al. 2001 , Astua 2006 ). The specimen Chiroptera 88 48.6 of H. kalinowskii (IEPA 1049) presented here, a female Carnivora 13 7.2 captured in March 2005, was collected by D. S. Fer- Cetacea 5 2.8 reira in the rural settlement of Nova Cana ã , municipal- Artiodactyla 5 2.8 ity of Porto Grande, Amap á . This is the second voucher Perissodactyla 1 0.5 specimen in the Brazilian collections. Marmosa lepida Rodentia 32 17.7 Total 181 100 is known from , Peru, , , Guyana, Suriname, French Guiana, and Brazil, in the 1 The percentages are calculated based on the total number of states of Amazonas and Pará (Lim et al. 2005 , Rossi species. 2005 , Creighton and Gardner 2008b ). We document the first record (IEPA 493) for the state of Amap á (Figure 1, We document 17 new occurrences, including 16 for PA 5). Chironectes minimus (Zimmermann 1780) was the the Amapá State: five marsupials: Cryptonanus sp. Voss, only species in the order recorded solely by observation. Lunde and Jansa, 2005 , Didelphis imperfecta Mondolfi This record was from the Marinho creek in the southern and Perez-Hernandez 1984, Gracilinanus emiliae (Thomas portion of Amapá (Figure 1, PA 17). Marmosops parvi- 1909), Hyladelphys kalinowskii (Hershkovitz 1992), and dens (Tate 1931) was broadly documented in the state Marmosa lepida (Thomas 1888); eight bats: Cormura brevi- (Figure 1, PA 1, 5, 7, 9, 10, 11, 17, 18, 19, 20, 23, 24, 26). The rostris (Wagner 1843), Peropteryx leucoptera Peters, 1869, first record for this marsupial was Parque Tumucumaque P . trinitatis (Miller 1899), carrikeri (Allen by Silva (2008) . 1910), brocki (Peterson 1968), Furipterus Two species of the manatee were recorded, including horrens Cuvier 1828, Cynomops planirostris (Peters 1866), the Amazonian Trichechus inunguis (Natterer 1883) in the and Eumops delticus Thomas 1923; one canid: Cerdocyon region of the mouth of the Amazon River and the marine thous (Linnaeus 1766); one cetacean: Balaenoptera bonae- T. manatus (Linnaeus 1758) with records from the north- rensis (Burmeister 1867) and one rodent: Pseudoryzomys ern coast of Amap á . These have been hunted on sp., see Silva et al. (2012) for more information. In addi- the coast. One individual was photographed harpooned in tion, we documented a new record of a rodent species for 2008 at the mouth of the Uaç á River in the Atlantic coast Brazil: Isothrix sinnamariensis (Vié , Volobouev, Patton (Oiapoque bay) in the north of Amap á State. and Granjon 1996) (Table 3). We also added two primate Five species of Pilosa were recorded, including Myr- species, Alouatta belzebul and Aotus infulatus, to the list mecophaga tridactyla (Linnaeus 1758). This species is con- presented by Lim et al. (2005) for the Guiana region. sidered vulnerable by the IUCN (2012), and we recorded it We recorded 15 species of Didelphimorphia (Table 3), in three different habitat types (Table 3). Tamandua tetra- among them five new occurrences for Amapá . We captured dactyla (Linnaeus 1758) is broadly documented through- the Cryptonanus sp. (IEPA 2077) at a single loca lity in the out the state. The black coloration form without a vest southeastern region of the state (Figure 1, PA 15). The speci- was dominant in the records (Figure 1, PA 11, 17, 18, 20, men has not yet been identified at the species level but this 21, 23, 24, and 27). The typical yellow coloration with or is the first record for the Amazon. Our record of Didelphis without the dark vest has not been collected in Amap á . imperfecta (IEPA 1144, 2415 and 2984) is the second for The voucher specimens deposited in the collection of Brazil; this species was previously known only from Monte CCFA are all black (IEPA 2061, 2378, and 2835). However, Roraima, in Roraima State (Cerqueira and Tribe 2008 ). We a yellow individual with a black vest was observed on the recorded D. imperfecta at three localities on the coast of banks of the Anacui River (Figure 1, PA 10). Amap á in the terra firme forest, flooded fields, and savan- We recorded five species of Cingulata in Amap á nas (Figure 1, PA 17, 20 and 21). Gracilinanus emiliae has been including Euphractus sexcinctus (Linnaeus 1758) (IEPA documented in French Guiana, Suriname, Guyana, Colom- 3090) in the savanna of the central region of the state bia, Venezuela, and northern Brazil in Par á State (Creighton (Figure 1, PA 11). Priodontes maximus (Kerr 1792), listed as

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 7

Table 3 The list of the mammal species recorded in the state of Amap á , northern Brazil, habitats where they were collected, and conserva- tion status according to IUCN (2012).

Classification Sampled habitats Status

Terra firme forest Savanna Floodable habitat

Didelphimorphia Didelphidae Caluromys philander XX LC Chironectes minimus X LC Cryptonanus sp. 2 X Didelphis imperfecta 2 XX LC Didelphis marsupialis XXXLC Gracilinanus emiliae2 XX DD Hyladelphys kalinowskii2 X LC Marmosa demerarae XX LC Marmosa lepida 2 X LC Marmosa murina XXLC Marmosops parvidens X LC Marmosops pinheiroi XXLC Metachirus nudicaudatus X LC Monodelphis touan XXXLC Philander opossum XXXLC Sirenia Trichechidae Trichechus inunguis XXVU Trichechus manatus XVU Pilosa Myrmecophagidae Cyclopes didactylus XXXLC Myrmecophaga tridactyla XX VU Tamandua tetradactyla XXXLC Bradypodidae Bradypus tridactylus XXXLC Megalonychidae Choloepus didactylus X LC Cingulata Dasypodidae Cabassous unicinctus XX LC Dasypus kappleri X LC Dasypus novemcinctus XXXLC Euphractus sexcinctus XLC Priodontes maximus XX VU Primates Cebidae Sapajus apella XXXLC Cebus olivaceus XXXLC Saguinus midas XX LC Saimiri sciureus XXXLC Aotidae Aotus infulatus XX LC Pitheciidae Chiropotes sagulatus X LC Pithecia pithecia X LC Atelidae Alouatta belzebul XX VU Alouatta macconnelli XXXLC Ateles paniscus X VU Chiroptera Emballunoridae

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 8 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

(Table 3 Continued)

Classification Sampled habitats Status

Terra firme forest Savanna Floodable habitat

Centronycteris maximilliani X LC Cormura brevirostris 2 XLC Diclidurus albus XXLC Diclidurus scutatus XXLC Peropteryx leucoptera2 XLC Peropteryx macrotis XLC Peropteryx trinitatis2 XDD Rhynchonycteris naso XXXLC Saccopteryx bilineata XXLC Saccopteryx canescens XLC Saccopteryx leptura XXXLC Phyllostomidae Ametrida centurio XXXLC caudifer XLC Anoura geoffroyi XXLC cinereus XXXLC Artibeus concolor XXXLC Artibeus gnomus XXLC Artibeus lituratus XXXLC Artibeus obscurus XXXLC Artibeus planirostris XXXLC brevicauda XXXLC Carollia perspicillata XXXLC trinitatum XX LC Chiroderma villosum XX LC minor XXLC Chrotopterus auritus XXXLC rotundus XXXLC Diaemus youngi XXLC Diphylla ecaudata XXLC sylvestris X LC longirostris2 XX DD Glossophaga soricina XXXLC Lampronycteris brachyotis XXLC degener X NE Lionycteris spurelli X LC thomasi XXXLC inusitata DD Lophostoma brasiliense X LC Lophostoma carrikeri 2 X LC Lophostoma schulzi X LC Lophostoma silvicolum XXXLC Macrophyllum macrophyllum XXLC Mesophylla macconnelli XLC megalotis XLC Micronycteris microtis XXLC Micronycteris minuta XXLC Micronycteris schmidtorum XX LC Micronycteris hirsuta2 X LC Mimon bennettii X LC Mimon crenulatum XXXLC Phylloderma stenops XXXLC discolor XXXLC Phyllostomus elongatus XXXLC Phyllostomus hastatus XXLC

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 9

(Table 3 Continued)

Classification Sampled habitats Status

Terra firme forest Savanna Floodable habitat

Platyrrhinus brachycephalus XXXLC Platyrrhinus incarum XXXNE pumilio XXXLC lilium XXXLC Sturnira tildae XXXLC saurophila XXLC Trachops cirrhosus XXXLC Trinycteris nicefori XXLC bilobatum XXXLC Uroderma magnirostrum XXXLC Vampyriscus bidens XX LC Vampyriscus brocki 2 XX LC thyone X LC Vampyrodes caraccioli XXLC Vampyrum spectrum X NT Thyropteridae Thyroptera tricolor XXLC Vespertilionidae Eptesicus brasiliensis XXLC Eptesicus furinalis XXLC Lasiuris blossevillii XLC Myotis albescens XXLC Myotis nigricans XLC Myotis riparius XXLC Noctilionidae Noctilio albiventris XX LC Noctilio leporinus XXLC Mormoopidae Pteronotus parnellii XXXLC Pteronotus personatus XLC Furipteridae Furipterus horrens 2 XLC Molossidae Cynomops planirostris2 XXXLC Eumops delticus 2 XX NE Eumops trumbulli XLC Molossus rufus X LC Molossus molossus XXXLC Nyctinomops laticaudatus XLC Promops nasutus X LC Carnivora Felidae Leopardus pardalis XX LC Panthera onca XXXNT Puma yagouaroundi XX LC Puma concolor XXXLC Canidae Cerdocyon thous 2 XX LC Speothos venaticus XX NT Mustelidae Eira barbara XXXLC Galictis vittata XXXLC Lontra longicaudis XXXDD Pteronura brasiliensis XXXEN

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 10 C.R. da Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

(Table 3 Continued)

Classification Sampled habitats Status

Terra firme forest Savanna Floodable habitat

Procyonidae Nasua nasua XXXLC Potos flavus XXXLC Procyon cancrivorus XXLC Perissodactyla Tapiridae Tapirus terrestris XXXVU Artiodactyla Tayassuidae Pecari tajacu XXXLC Tayassu pecari XX NT Cervidae Mazama americana XXXDD Mazama nemorivaga XXXLC Odocoileus virginianus XX LC Cetacea Baleonopteridae Balaenoptera bonaerensis XDD Delphinidae Sotalia fluviatilis XDD Sotalia guianensis XDD Tursiops truncatus XLC Iniidae Inia geoffrensis XDD Rodentia Sciuridae Sciurillus pusillus X DD Guerlinguetus aestuans X LC Cricetidae macconnelli X LC sciureus X LC megacephalus X LC X LC dubosti X LC X LC melanius XLC Neusticomys oyapocki X DD auyantepui XX LC XXXLC X LC X LC Oecomys sp. X sp. X Pseudoryzomys sp. X Sigmodon alstoni XLC brevicauda XLC Caviidae Hydrochoerus hydrochaeris XXXLC Cuniculidae Cuniculus paca XXXLC Dasyproctidae Dasyprocta leporina XXXLC Myoprocta acouchy XXLC Erethizontidae Coendou prehensilis XXXLC Coendou melanurus X

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 11

(Table 3 Continued)

Classification Sampled habitats Status

Terra firme forest Savanna Floodable habitat

Echimyidae Echimys chrysurus X LC Isothrix sinnamariensis 3 X LC Makalata didelphoides X LC Makalata sp. XLC Mesomys hispidus XXLC Proechimys cuvieri XXXLC Proechimys guyannensis XXXLC

1 EN, endangered; VU, vulnerable; NT, near threatened; LC, least concern; DD, data deficient; NE, not evaluated. 2 New occurrence for the state of Amap á . 3 New occurrence for Brazil.

vulnerable (IUCN 2012), was recorded in the areas of the Goi á s, and Piau í . We captured this species (IEPA 2936) terra firme forest and savanna (Figure 1, PA 10 and 11); and in the terra firme forest of RESEX Cajari close to Highway Cabassous unicinctus (Linnaeus 1758) (IEPA 1541), a rare BR156 (Figure 1, PA 25), which extended its range to the species in the state, was recorded in the terra firme forest eastern Amazon. Similarly for Vampyriscus brocki (IEPA and savanna (Figure 1, PA 18 and 20). 2118), until then recorded only in the states of Amazonas Of the 88 species recorded, eight are new records and Pará (Bernard et al. 2011 , Peracchi et al. 2011 ), we to Amapá . The family Emballonuridae had three new recorded it in the savanna (Figure 1, PA 20). occurrences: Cormura brevirostris (IEPA 1243) was rec- Ten species of primates are known from the state, ognized from the states of Pará , Amazonas, Maranhã o, including Alouatta belzebul recorded on the coast between and Rondô nia (Bernard et al. 2011 ), Peropteryx leucop- Macapá and the mouth of the Araguari River (IEPA 35 and tera (IEPA 1696) occurring in Amazonas, Par á , and Piau í 36). This species was collected in the municipality of (Peracchi et al. 2010 ), and Peropteryx trinitatis (IEPA Itaubal in 1988 and reported by Silva Junior et al. (2008). 1272) known to Par á and Maranh ã o (Hood and Gardner These records for Amap á represent a range extension, as 2008 ). These three species were captured in a floodplain the species had been previously recorded only to the south forest in the APA Curiaú (Figure 1, PA 27), municipality of of the Amazon River. A. belzebul was recorded in sympa- Macapá . We also recorded for the first time in Amapá , the try with Alouatta macconnelli (Elliot 1910) on the central species Furipterus horrens (IEPA 071) at the mouth of the coast of Amap á (Costa-Neto pers. comm.). It was recorded Jari River on the border with the Pará State (Figure 1, PA in the floodplain forest, flooded fields, and savannas. 18). In Brazil, this species occurs in the Amazon (Amazo- Aotus infulatus is in the list of Carvalho (1962) under nas and Par á ; Bernard et al. 2011 ), Caatinga, and Atlantic the name Aotus trivirgatus (Humboldt 1811). The current Forest (Reis et al. 2010 ). For Molossidae, there are two records place this species only on the coast of Amap á , in new records for Amap á : Cynomops planirostris (IEPA areas of the savanna, flooded field, and floodplain forest 980) captured in the flooded fields of REBIO Piratuba (Silva Junior et al. 2008). (Figure 1, PA 32) and Eumops delticus (IEPA 1255) cap- We recorded 13 species of Carnivora, including the tured in the savanna of APA Curiaú (Figure 1, PA 27). In canid Cerdocyon thous , a new occurrence for Amap á . This the Amazon, C. planirostris was known from the state of canid has a broad distribution, but the records from north- Mato Grosso (Pine et al. 1970 ). Eger (2008) considered the ern Brazil are restricted to the Pará State (Machado and whole Amazon, which extends to southeastern Brazil, as Hingst -Zaher 2009 ). Michalski and Peres (2005) reported a potential area of occurrence for this species. Likewise, the species in disturbed areas of the Amazonian Forest the expected geographic distribution of Eumops delticus in Mato Grosso, and the map of the potential distribu- includes southwestern Colombia along the Amazon River tion published by Courtenay and Maffei (2008) included to the southern Bahia State in Brazil (Eger 2008 ). For only the states of Acre and Amazonas as areas where the the family Phyllostomidae, there were two new records species is absent. C. thous was recorded mainly in the for Amap á , including Lophostoma carrikeri , which savannas (Figure 1, PA 11, 20), but we also recorded it in was known for the states of Amazonas, Par á , Roraima, a floodplain forest (Figure 1, PA 27). The only specimen

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 12 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia deposited in the collection (IEPA 3603) resulted from a plantations, as it was found in over 50% of the captures roadkill on Highway AP 70 within the savanna of APA with the Sherman and cage traps. The Oligoryzomys sp. Curiaú . We recorded three carnivore species listed on the was recorded in the savanna on the coast (Figure 1, PA 15, IUCN (2012) red list: Panthera onca (Linnaeus 1758) and 20, 22, 23, and 24). Based on a molecular analysis of the Speothos venaticus (Lund 1842), listed as near threat- specimens deposited in CCFA (IEPA 2481, IEPA 2888, IEPA ened, and Pteronura brasiliensis (Gmelin 1788) listed as 3040, and IEPA 3536) and the sequences deposited in the endangered. GenBank, we found that the sequences were similar to Regarding the ungulates, Tapirus terrestris (Lin- the specimen named as Oligoryzomys sp. collected in S ã o naeus 1758) (Perissodactyla) is listed as vulnerable by Bento Farm, municipality of Tartarugalzinho (Miranda IUCN (2012) and was recorded in the terra firme forest, et al. 2009 ). This specimen was grouped in a phylogenetic savanna, and floodable forest. Five species of Artiodac- study with (Saussure 1860) and tyla were recorded, including three cervids: Odocoileus Oligoryzomys messorius (Thomas 1901), both of which virginianus, Mazama americana (Erxleben 1777), and occur in the Amazon, and with Mazama nemorivaga (Cuvier 1817). There were also two Weksler and Bonvicino 2005, which is known from the peccaries: Tayassu pecari (Link 1795) and Pecari tajacu Cerrado (Miranda et al. 2009 ). These authors state that a (Linnaeus 1758). These species have a broad distribu- complete morphological description of Oligoryzomys sp. is tion in the state, except for O. virginianus, which occurs needed for a correct taxonomic identification. Five species only on the coast in the savannas and flooded fields, and of Oecomys Thomas 1906 were recorded for Amap á : T. pecari, listed as near threatened by IUCN (2012), which Oecomys rex (Thomas 1910) (IEPA 1539), Oecomys rutilus is apparently absent from most open environments due (Anthony 1921) (IEPA 1532), Oecomys bicolor (Thomas to hunting. 1860) (IEPA 1612), (Tate 1939) (IEPA Five Cetacea species were recorded in the state, 1134), and Oecomys sp. (IEPA 1611). The latter is probably including a new record of Balaenoptera bonaerensis in an undescribed species (Flores 2010 ), that was captured EEP, an island of lacustrine-marine influence, in April in the terra firme forest, savanna, and flooded habitats 2009. Although the northernmost record of B . bonaer- (Figure 1, PA 10, 18, 19, 20, 21). O. rutilus (Figure 1, PA 9, ensis on the eastern coast of South America was made in 10, 17, 18, 26), O . rex (Figure 1, PA 18), and O . auyantepui Suriname (Husson 1978 , Rice 1998 ), this species has been (Figure 1, PA 17, 18, 19, 26) were recorded only in the terra rarely observed on the Brazilian coast, and its occurrence firme forest. O. bicolor was recorded in the terra firme is apparently atypical. The most frequent records of this forest (Figure 1, PA 5, 18, 26), savanna (Figure 1, PA 20, 22, species were made at the tropical and subtropical lati- 23), and flooded area (Figure 1, PA 21). In the municipal- tudes (Zerbini et al. 1997 ). ity of Cachoeira Santo Antô nio, southern Amapá (PA 18), Rodentia was the second largest order with 32 species. all the five species of Oecomys were captured in sympa- The occurrence of Isothrix sinnamariensis (IEPA 1509) in try. Neusticomys oyapocki (Dubost and Peter 1978), whose Brazil is interesting, but not totally unexpected, as this first occurrence for Amapá was reported by Nunes (2002) , echimyid was known from French Guiana (Vié et al. was captured in the southern region on the banks of the 1996 ), Guyana (Lim et al. 2007 ), and Suriname (Lim and Jari River and in the central region in the FLONA Amapá Joemratie 2011 ). Our specimen was collected in an area of (Figure 1, PA 18, 26). We recorded two species of Makalata. managed Brazil nut trees (Bertholletia excelsa ) in RESEX One had a broad distribution in areas of the terra firme Cajari (Figure 1, PA 17), municipality of Laranjal do Jari, forest (Figure 1, PA 1, 3, 5, 6, 9, 10, 16, 26) and was referred southern Amap á . The two specimens of Pseudoryzomys to as Makalata didelphoides (Desmarest 1817) (IEPA 926, sp. were captured by Nunes (2001) in the savanna, Sã o IEPA 1146, IEPA 1147), although the karyotype 2N = 72 (Le ã o Bento Farm locality, also sampled by us (Figure 1, PA et al. unpublished data) differs from that described by 21). Although the specimens have not yet been identified Lima et al. (1998) . In the coastal region of mangroves and at the species level, this is the first record for the genus floodable fields (Figure 1, PA 13, 14, 21, 29), we recorded in Amap á . We recorded also the Makalata sp. (IEPA 2713, IEPA 2715, IEPA 2571). These (Allen and Chapman 1893) (IEPA 1626) and Sigmodon specimens differ from M. didelphoides by morphological alstoni (Thomas 1881) (IEPA 2786), which are found in and genetic characters (Duque et al. 2010). the savannas within the municipality of Ferreira Gomes Excluding the aquatic mammals, 137 species were (Figure 1, PA 23). Z. brevicauda was also recorded in the recorded in the terra firme forest, 86 in the savannas, areas of savanna in contact with the Eucalyptus planta- and 116 in the floodable environments, such as the fields tions (Figure 1, PA 20). This rodent was abundant in these and floodplain forests (Table 3). Most terra firme areas

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 13 of Amap á are reserves, which cover large continuous inventories and long-term studies, employing detailed areas and protect the habitats of endemic species, such analysis of morphologic variation coupled with a molecu- as Ateles paniscus (Linnaeus 1758), Chiropotes sagulatus , lar approach will contribute to a better classification of and Oecomys rutilus. In these environments, we recorded the species in the different habitats, which will help to 26 species not found in any other habitats (Table 3). The define the endemism, conservation status, and distribu- savannas are more vulnerable to the environmental alter- tion of the mammals in Amap á . ations because they are intensively occupied by humans, and only a few noncontinuous areas are protected Acknowledgements: We thank Adriano Peracchi and Dan- (Sanaioti et al. 1997 ). This scenario represents a risk for iela Dias for the identification of the bats; Tamara Flores, the natural populations and endemic species, such as Yuri Leite, Gilson E. Y. Ximenes, Marcelo Weksler, and Pseudoryzomys sp., Sigmodon alstoni , Zygodontomys Cibele Bonvicino identified some rodents; Caroline Duque brevi cauda , Cryptonanus sp., and Euphractus sexcinctus . sequenced the tissue samples of Makalata ; Suely Marques- This habitat has a few endemic species, but it is important Aguiar gave us access to the mammal collection of Museu for the species that are biologically and taxonomically Paraense Emilio Goeldi; José de Souza Silva Junior helped poorly known. The situation of the floodable habitats is us during the visits; Cleusa Yoshiko Nagamashi and her similar, but there are more and larger reserves protecting research group for analyzing the karyotypes of the rodents these habitats. We recorded 20 species only in this habitat, and marsupials, Dayse Swellen Silva Ferreira and Carlos mainly bats (Table 3). Eduardo Costa Campos who collected the Hyladelphys We predict that more species will be soon added kalinowskii , and Claudia Funi for drawing the map. We to the mammal list of Amapá , as Mustela sp. (Linnaeus thank Franç ois Catzeflis and two anonymous reviewers 1758) and Leopardus tigrinus (Schreber 1775). Both species for the many useful comments on the manuscript. have already been observed in the state, but confirma- tion through the voucher specimens is still needed. More Received November 8, 2012; accepted March 26, 2013

References

Astua, D. 2006. Range extension and first Brazilian record of the I. Marsupials, xenarthrans, shrews, and bats. University of rare Hyladelphys kalinowskii (Hershkovitz, 1992) (Didelphi- Chicago Press, Chicago and London. pp. 17 – 25. morphia, Didelphidae). Mammalia 70: 174 – 176. Charles-Dominique, P., M. Atramentowicz, M. Charles-Dominique, Barnett, A.A. and C.A. Cunha. 1998. Small mammals of Ilha de G é rard, H., A. Hladik, C.M. Hladik and M.F Pr é vost. 1981. Les Marac á . In: (W. Milliken and J. Ratter, eds.) Marac á : the mammifè res frugivores nocturnes d’ une forê t guyanaise: inter- biodiversity and environment of an Amazonian rainforest. relations plantes-animaux. Rev. Ecol. Terre Vie 35: 341 – 435. John Wiley and Sons Ltd, Baffins Lane, Chichester, England. Costa, L.P. 2003. The historical bridge between the Amazon and the pp. 189 – 210. Atlantic Forest of Brazil: a study of molecular phylogeography Bernard, E. 2008. Inventá rios Bioló gicos Rá pidos no Parque with small mammals. J. Biogeogr. 30: 71 – 86. Nacional Montanhas do Tumucumaque, Amap á , Brasil. Courtenay, O. and L. Maffei. 2008. Cerdocyon thous . In: IUCN 2012. RAP Bulletin of Biological Assessment 48. Conservation IUCN Red List of Threatened Species. Version 2012.1. http:// International, Arlington, VA. pp. 149. www.iucnredlist.org. Accessed on 20 July 2012. Bernard, E., V.C. Tavares and E. Sampaio. 2011. Compilaç ã o Cracraft, J. 1985. Deep-history biogeography: retrieving the historical atualizada das esp é cies de morcegos (Chiroptera) para a pattern of evolving continental biotas. Syst. Zool. 37: 396 – 427. Amaz ô nia Brasileira. Biota Neotrop. 11: 35 – 46. Creighton, G.K. and A.L. Gardner. 2008a. Genus Gracilinanus Booman, G.C., P. Laterra, V. Comparatore and N. Murillo. Gardner and Creighton, 1989. In: (Gardner, A.L., ed.) Mammals 2009. Post-dispersal predation of weed seeds by small of South America, Volume I. Marsupials, xenarthrans, shrews, vertebrates: interactive influences of neighbor land use and bats. University of Chicago Press, Chicago and London. and local environment. Agric. Ecosyst. Environ. 129: pp. 43 – 50. 277– 285. Creighton, G.K. and A.L. Gardner. 2008b. Genus Marmosa Gray, Carvalho, C.T. 1962. Lista preliminar dos mam í feros do Amap á . Pap. 1821. In: (A.L. Gardner, ed.), Mammals of South America, Avulsos do Dep. de Zool, S ã o Paulo, 15: 283 – 297. Volume I. Marsupials, xenarthrans, shrews, and bats. Castro, I.J. 2009. Assemblé ia de morcegos (Mammalia: Chiroptera) da University of Chicago Press, Chicago and London, pp. 51 – 61. Á rea de Prote ç ã o Ambiental do Rio Curia ú , Amap á . Universidade Duellman, W.E. 1982. Quaternary climatic-ecological fluctuations Federal do Amap á , Macap á (Master ’ s Thesis). pp. 78. in the lowland tropics: frog and forests. In: (G.T. Prance, ed.), Cerqueira, R. and C.J. Tribe. 2008. Genus Didelphis Linnaeus, 1758. Biological diversification in the tropics. Columbia University In: (Gardner, A.L., ed.) Mammals of South America, Volume Press, New York. pp. 389– 401.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 14 C.R. da Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

Duque, C.C., C.R. Silva, G.E. Iack-Ximenes and Y.L.R. Leite. 2010. terrestrial vertebrates of the Guiana Shield. Bull. Biol. Soc. Varia ç ã o gen é tica e morfol ó gica em Makalata didelphoides Washington. 13: 77 – 92. (Rodentia, Echimyidae) do Amapá . In: V Congresso Brasileiro de Lim, B.K., M.D. Engstrom, J.C Patton and J.W. Bickham. 2007. Mastozoologia, 2010, S ã o Pedro, SP. Resumos. pp. 896 – 897. Systematic relationships of the Guianan brush-tailed rat Eger, J.L. 2008. Family Molossidae. In: (A.L. Gardner, ed.) Mammals ( Isothrix sinnamariensis ) and its first occurrence in Guyana. of South America, Volume I. Marsupials, xenarthrans, shrews, Mammalia 70: 120 – 125. and bats. University of Chicago Press, Chicago and London. Lima, J.F.S., A. Languth and L.C. Sousa. 1998. The karyotype of pp. 399 – 440. Makalata didelphoides (Rodentia, Echimyidae). Z. Sä ugetierk. Eisenberg, J.F. 1989. Mammals of the Neotropics. The northern 63: 315 – 318. Neotropics. The University of Chicago Press, Chicago. pp. 449. Lynch-Alfaro, J.W., J.P. Boubli, L.E. Olson, A. Di Fiore, B. Wilson, G.A. Flores, T.A. 2010. Diversidade morfol ó gica e molecular do g ê nero Gutierrez-Espeleta, K.L. Chiou, M. Schulte, S. Neitzel, V. Ross, Oecomys Thomas, 1906 (Rodentia: Cricetidae) na Amaz ô nia D. Schwochow, M.T.T. Nguyen, I. Farias, C.H. and Janson, M.E. Oriental brasileira. Universidade Federal do Par á . Bel é m, Par á . Alfaro. 2012. Explosive Pleistocene range expansion leads to (Master’ s Thesis). pp. 113. widespread Amazonian sympatry between robust and gracile Gardner, A.L. 2008. Mammals of South America, Volume I. capuchin monkeys. J. Biogeogr. 39: 272 – 288. Marsupials, xenarthrans, shrews, and bats. The University of Machado, F.A. and E. Hingst-Zaher. 2009. Investigating South Chicago Press, Chicago and London. pp. 669. American biogeographic history using patterns of skull shape Griffiths, T.A. and A.L. Gardner. 2008. Subfamily Lonchophyllinae variation on Cerdocyon thous (Mammalia: Canidae). Biol. J. Griffiths, 1982. In: (A.L. Gardner, ed.) Mammals of South Linnean Soc. 98: 77– 84. America, Volume I. Marsupials, xenarthrans, shrews, and bats. Maia da Silva, F., R.D. Naiff, A. Marcili, M. Gordo, J.A. D ’ Affonseca University of Chicago Press, Chicago and London, pp. 244– 255. Neto, M.F. Naiff, A.M.R. Franco, M. Campaner, V. Valente, S.A. Gr ü newald, C., N. Breitbach and K. Bö hning-Gaese. 2010. Tree Valente, E.P. Camargo, M.M.G. Teixeira and M.A. Miles. 2008. visitation and seed dispersal of wild cherries by terrestrial Infection rates and genotypes of Trypanosoma rangeli and T. mammals along a human land-use gradient. Basic Appl. Ecol. cruzi infecting free-ranging Saguinus bicolor (Callitrichidae), a 11: 532 – 541. critically endangered primate of the Amazon Rainforest. Acta Haffer, J. 1974. Avian speciation in tropical South America. Publ. Trop. 107: 168 – 173. Nuttall Ornith. Club. 14: 1– 390. Martins, A.C.M. and E. Bernard. 2008. Invent á rios r á pidos de Hershkovitz, P. 1969. The evolution of mammals of the Neotropical morcegos no Parque Nacional Montanhas do Tumucumaque: region: a zoogeographic and ecological review. Q. Rev. Biol. Resultados das Expedi ç õ es I a V e S í ntese. In: (E. Bernard, ed.) 44: 1 – 70. Inventá rios Bioló gicos Rá pidos no Parque Nacional Montanhas Hershkovitz, P. 1983. Two new species of the night monkeys, genus do Tumucumaque, Amap á , Brasil. RAP Bull. Bio. Assess. Aotus (Cebidae, Platyrrhini): a preliminary report on Aotus Conservation International, Arlington, VA. 48:59 – 65. . Am. J. Primatol. 4: 209 – 248. Martins, A.C.M., E. Bernard and R. Gregorin. 2006. Rapid biological Hood, C. and A.L. Gardner. 2008. Family Emballonuridae Gervais, surveys of bats (Mammalia, Chiroptera) in three conservation 1856. In: (A.L. Gardner, ed.) Mammals of South America, units in Amap á , Brazil. Rev. Bras. Zool. 23: 1175 – 1184. Volume I. Marsupials, xenarthrans, shrews, and bats. Martins, A.C.M., E. Bernard, R. Gregorin and W.A.S. Silva. 2011. University of Chicago Press, Chicago and London. Filling data gaps on the diversity and distribution of Amazonian pp. 188 – 207. bats (Chiroptera): The case of Amap á , eastern most Brazil. Rev. Husson, A.M. 1978. The mammals of Suriname. Zoö logische Bras. Zool. 28: 177 – 185. Monographeieen van het Rijksmuseum van Natuurlijke Michalski, F. and C.A. Peres. 2005. Anthropogenic determinants Historie, Leiden. pp. 569. of primate and carnivore local extinctions in a fragmented IBGE. 2004. IBGE, Instituto Brasileiro de Geografia e Estat í stica. forest landscape of Southern Amazonia. Biol. Conserv. 124: Mapa de Vegetaç ã o do Brasil, 2a ediç ã o. Escala 1: 5.000.000. 383 – 396. IUCN. 2012. The IUCN Red List of Threatened Species. Version Miranda, G.B., L.F.B. Oliveira, J. Andrades-Miranda, A. Langguth, 2012.2. Available at: http://www.iucnredlist.org . Accessed on S.M. Callegari-Jacques and M.S. Mattevi. 2009. Phylogenetic October 20, 2012. and phylogeographic patterns in Sigmodontine rodents of the Lambert, T.D., J.R. Malcolm and B.L. Zimmerman. 2005. Effects of genus Oligoryzomys . J. Hered. 100: 309 – 321. mahogany (Swietenia macrophylla) logging on small mammal Mok, W.Y., D.E. Wilson, L.A. Lacey and R.C.C. Luiz ã o. 1982. Lista communities, habitat structure, and seed predation in the atualizada de quir ó pteros da Amaz ô nia brasileira. Acta Amaz. southeastern Amazon Basin. Forest Ecol. Manage. 206: 381– 398. 12: 814 – 23. Lim, B.K. and M.D. Engstrom. 2005. Mammals of Iwokrama Forest. Monteiro, F.J.C. 2009. Impactos Ambientais causados pelos Proc. Acad. Nat. Sci. Philadelphia 154: 71 – 108. b ú falos asselvajados nos campos inund á veis da Esta ç ã o Lim, B.K. and S. Joemratie. 2011. Rapid Assessment Program (RAP) Maracá -Jipioca (Costa Atlâ ntica do Amapá ). Universidade survey of small mammals in the Kwamalasamutu region of Federal do Amapá , Macapá – Amap á (Master’ s Thesis). Suriname. In: (B.J. O’ Shea, L.E. Alonso and T.H. Larsen, eds.) pp. 50. A rapid biological assessment of the Kwamalasamutu region, Nunes, A. 2001. Gradientes estruturais dos h á bitats em savanas Suriname. Conservation International, Arlington, VA, USA. amazô nicas: implicaç õ es sobre a distribuiç ã o e ocorrê ncia das pp. 144 – 149. espé cies de pequenos mamí feros (Rodentia, Didelphimorphia). Lim, B.K., M.D. Engstrom and J.G Ochoa. 2005. Mammals. In: Universidade Federal do Rio de Janeiro, Rio de Janeiro (Doctor ’ s (Hollowell, T. and R.P. Reynolds, eds.) Checklist of the Dissertation). pp. 129.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia 15

Nunes, A. 2002. First record of Neusticomys oyapocki (Muridae, Rossi, R.V. 2005. Revis ã o taxon ô mica de Marmosa Gray, 1821 Sigmodontinae) from the Brazilian Amazon. Mammalia 66: (Didelphimorphia, Didelphidae). Instituto de Bioci ê ncias, 445 – 447. Universidade de Sã o Paulo. Sã o Paulo (Doctor’ s Dissertation). Oliveira, C.P. 2008. Mé todo de Avaliaç ã o por Mú ltiplos Crité rios pp. 357. como Apoio ao Planejamento Ambiental: aplica ç ã o Rossi, R.V., R. Bodmer, J.M.B. Duarte and R.G. Trovati. 2010. experimental no Cerrado Central do Amapá , Brasil. Amazonian brown brocket deer Mazama nemorivaga (Cuvier Universidade Federal do Amap á , Macap á – Amap á (Master ’ s 1817). In: (J.M.B. Duarte and S. Gonzalez, eds.) Neotropical Thesis). pp. 50. cervidology: biology and medicine of Latin American deer. Parry, L., J. Barlowand and C.A. Peres. 2009. Allocation of hunting IUCN/FUNEP, Gland, pp[A1]. 202 – 210. effort by Amazonian smallholders: implications for conserving Sampaio, E.M., E.K.V. Kalko, E. Bernard, B. Rodr í guez-Herrera wildlife in mixed-use landscapes. Biol. Conserv. 142: and C.O. Handley Jr. 2003. A biodiversity assessment of 1777 – 1786. bats (Chiroptera) in a tropical lowland rainforest of central Patton, J.L. and L.P. Costa. 2003. Molecular phylogeography and Amazonia, including methodological and conservation consid- species limits in rainforest didelphid marsupials of South erations. Stud. Neotr. Fauna Environ. 38: 17 – 31. America. In: (M. Jones, C. Dickiman and M. Archer, eds.) Sanderson, J. and L. Ign á cio. 2002. Non-volant mammal survey. Predators with pouches: the biology of carnivorous marsupials. Results from the Eastern Kanaku Montains Lower Kwitaro CSIRO Publishing, Collingwood, Victoria. pp. 63 – 81. River, Guyana. In: (J.R. Montambault and O. Missa, eds.) A Patton, J.L., M.N.F. Silva and J.R. Malcolm. 2000. Mammals of the biodiversity assessment of the Eastern Kanuku Mountains, Rio Juru á and the evolutionary and ecological diversification of Lower Kwitaro River. RAP Bull. Bio. Assess. 26. Conservation Amazonia. Bull. Am. Mus. Nat. Hist. 244: 1 – 306. International, Washington, DC. pp. 47 – 50. Pavan, S.E., R.V. Rossi and H. Schneider. 2012. Species diversity Sanaioti, T.M., S. Bridgewater and J.A. Ratter. 1997. A floristic study in the Monodelphis brevicaudata complex (Didelphimorphia: of the savanna vegetation of the state of Amapa, Brazil, and Didelphidae) inferred from molecular and morphological data, suggestions for its conservation. Bol. Mus. Paraense Emilio with the description of a new species. Zool. J. Linn. Soc.-Lond. Goeldi, Bot. 13: 3 – 29. 165: 190 – 223. Silva, C.R. 2008. Invent á rios rá pidos de mam í feros n ã o-voadores Peracchi, A.L., L.R. Sans ã o and A.M.Tanurre. 1984. Quir ó pteros do no Parque Nacional Montanhas do Tumucumaque: resultados Territ ó rio Federal do Amapá , Brasil (Mammalia: Chiroptera). das Expedi ç õ es I a V e s í ntese. In: (E. Bernard, ed.) Invent á rios Arq. Univ. Fed. Rural do Rio de Janeiro. 7: 89 – 100. Biol ó gicos R á pidos no Parque Nacional Montanhas do Peracchi, A.L., P.H. Gallo, D. Dias, I.P. Lima and N.R. Reis. 2010. Tumucumaque, Amapá , Brasil. RAP Bull. Bio. Assess. 48. Ordem Chiroptera. In: (N.R. Reis, A.L. Peracchi, M.N. Fregonezi Conservation International, Arlington, VA. pp. 51 – 57. and B.K. Rossaneis, eds.) Mam í feros do Brasil: Guia de identi- Silva Jr., J.S. and W.M.B. Figueiredo. 2002. Revis ã o sistem á tica fica ç ã o, 1 a edi ç ã o. Technical Books, Rio de Janeiro, Brazil. dos cuxiú s, gê nero Chiropotes Lesson, 1840 (Primates, pp. 293 – 461 Pitheciidae), no Livro de Resumos: X Congresso Brasileiro Peracchi, A.L., I.P. Lima, N.R. Reis, M.R. Nogueira and H. Ort ê ncio-Filho. de Primatologia, p.21. Sociedade Brasileira de Primatologia, 2011. Ordem Chiroptera. In: (N.R. Reis, A.L. Peracchi, W.A. Pedro Bel é m. and I.P. Lima, eds.) Mam í feros do Brasil, 2a edi ç ã o. Editora da Silva J.M.C., A.B. Rylands and G.A.B Fonseca. 2005. O destino Universidade Estadual de Londrina, Londrina, Brazil. pp. 155– 234. das á reas de endemismo da Amaz ô nia. Megadiversidade 1: Piccinini, R.S. 1974. Lista provisó ria dos quiró pteros da coleç ã o 124 – 131. do Museu Paraense Em í lio Goeldi (Chiroptera). Bol. Mus. Silva Jr., J.S., C.R. Silva and T.P. Kasecker. 2008. Primatas do Paraense Emí lio Goeldi, Nova Sé rie Zool., Belé m 77: 132. Amap á : Guia de Identifica ç ã o de Bolso.S é rie “Guias de Pine, R.H., I.R. Bishop and R.L. Jackson. 1970. Preliminary list of Bolso Tropicais”. Conservation International. Panamericana mammals of the Xavantina/Cachimbo expedition (Central Editorial Ltda., Bogotá , Colô mbia. Disponí vel em: http://www. Brazil). Trans. R. Soc. Trop. Med. Hyg. 64: 668 – 670. biodiversidadedoamapa.net/publicacoes/PRIMATES_OF_ Prance, G.T. 1982. Forest refuges: evidence from woody AMAPA.pdf . angiosperms. In: (G.T. Prance, ed.) Biological diversification in Silva, C.R., A.C.M. Martins, I.J. Castro and E.M. Cardoso. 2012. Guia the tropics. Columbia University Press, New York. pp. 137 – 158. de mam í feros do Estado do Amapá. 1. Edi ç ã o. IEPA, Macap á , Reis, N.R., A.L. Peracchi, M.N. Fregonezi and B.K. Rossaneis. 2010. Brazil. pp. 301. Mamí feros do Brasil: Guia de Identificaç ã o. 1a edição. Technical Simmons, N.B. and R.S. Voss. 1998. The mammals of Paracou, Books, Rio de Janeiro, Brazil. pp. 560. French Guiana: a Neotropical lowland rainforest fauna, Part 1. Ribas, C.C., A. Aleixo, A.C.R. Nogueira, C.Y Miyaki and J. Cracraft. Bats. Bull. Am. Mus. Nat. Hist., 237: 1 – 219. 2012. A palaeobiogeographic model for biotic diversification Steiner, C. and F.M. Catzeflis. 2004. Genetic variation and within Amazonia over the past three million years. Proc. Royal geographical structure of five mouse-sized opossums Soc. B 279: 681 – 689. (Marsupialia, Didelphidae) throughout the Guiana region. Rice, D.W. 1998. Marine mammals of the world: systematic and J. Biogeogr. 31: 959 –973. distribution. Soc. Marine Mammalogy, 4: 1 – 231 (special Straube, F.C. and G.V. Bianconi. 2002. Sobre a grandeza e a unidade publication). utilizada para estimar esfor ç o de captura com utilizaç ã o de Robinson, F. 1998. The bats of the Ilha de Maracá . In: (W. Milliken redes-de-neblina. Chirop. Neotr. 8: 150 – 152. and J.A. Ratter, eds.) Marac á : the biodiversity and environment Thoisy, B., V. Lacoste, A. Germain, J. Muñ oz-Jord á n, C. Coló n, J.F. of an Amazonian rainforest, John Wiley and Sons, Chichester. Mauffrey, M. Delaval, F. Catzeflis, M. Kazanji, S. Matheus, P. pp. 165 – 187. Dussart, J. Morvan, A.A Seti é n, X. Deparis and A. Lavergne.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM 16 C.R. Silva et al.: Mammals of Amap á State, Eastern Brazilian Amazonia

2009. Dengue Infection in Neotropical Forest Mammals. Voss, R.S., D. Lunde and N. Simmons. 2001. The Mammals of Vector-Borne Zoonot. Dis. 9: 157 – 170. Paracou, French Guiana: a Neotropical lowland rainforest Trolle, M. 2003. Mammal survey in the Rio Jauaper í region, Rio fauna Part 2. Nonvolant species. Bull. Am. Mus. Nat. Hist. 263: Negro Basin, the Amazon, Brazil. Mammalia 67: 75 – 83. 1 – 236. Velazco, P.M. 2005. Morphological phylogeny of the bat genus Voss, R.S., D.P. Lunde and S.A. Jansa. 2005. On the contents of Platyrrhinus Saussure, 1860 (Chiroptera: Phyllostomidae) with Gracilinanus Gardner and Creighton, 1989, with the description the description of four new species. Field. Zool. 105: 1 – 53. of a previously unrecognized clade of small didelphid Velazco, P.M. and A.L. Gardner. 2009. A new species of Platyrrhinus marsupials. Am. Mus. Novit. 3482: 1 – 34. (Chiroptera: Phyllostomidae) from western Colombia and Webb, S.D. 1978. A history of savanna vertebrates in the new world. Ecuador, with emended diagnoses of Paquilus , P. dorsalis and Part II: South America and the great interchange. Annu. Rev. P. umbratus. Proc. Biol. Soc. Washington 122:249– 281. Ecol. Syst. 9: 393– 426. Velazco, P.M. and B.D. Patterson. 2008. Phylogenetics and Weksler, M., A.R. Percequillo and R.S. Voss. 2006. Ten new genera biogeography of the broad-nosed bats, Genus Platyrrhinus of Oryzomyine rodents (Cricetidae: Sigmodontinae). Am. Mus. (Chiroptera: Phyllostomidae). Mol. Phylogenet. Evol. 49: Novit. 3537: 1 – 29. 749 – 759. Wester, P., R. Stanway and A. Pauw. 2009. Mice pollinate the Velazco, P.M.; C.C. Aires, A.P. Carmignotto and A.M. Bezerra. 2010. Pagoda Lily, Whiteheadia bifolia (Hyacinthaceae) – first field Mammalia, Chiroptera, Phyllostomidae, Vampyrodes caraccioli observations with photographic documentation of rodent (Thomas, 1889): range extension and revised distribution map. pollination in South Africa. S. Afr. J. Bot. 75: 713 – 719. Check List 6: 49 – 51. Wilson, D.E. and D.M. Reeder (eds.). 2005. Mammal species of the Vi é , J.C., V. Volobouev and J.L. Patton. 1996. A new species of world: a taxonomic and geographic reference. 3rd edition. Isothrix (Rodentia: Echimyidae) from French Guiana. Mammalia Johns Hopkins University Press, Baltimore. pp. 2181. 60: 393 – 406. Whitmore, T.C. 1998. An introduction to Tropical Rain Forests. Voss, R.S. 2011. Revisionary notes on Neotropical porcupines 2nd edition. Oxford University Press, New York. pp. 282. (Rodentia: Erethizontidae). An annotated checklist of the species Zerbini, A.N., E.R. Secchi, S. Siciliano and P.C. Simõ es-Lopes. 1997. of Coendou Lac é p è de, 1799. Am. Mus. Novit. 3720: 1 – 36. A review of the occurrence and distribution of whales of the Voss, R.S. and L.H. Emmons. 1996. Mammalian diversity in genus Balaenoptera along the Brazilian coast. Rep. Int. Whal. Neotropical lowland rainforest: a preliminary assessment. Bull. Commn. 47: 407 – 417. Am. Mus. Nat. Hist. 230: 1 – 115. Zocche, J.J., D.D. Leffa, A.P. Damiani, F. Carvalho, R.A. Mendon ç a, Voss, R.S. and S.A. Jansa. 2009. Phylogenetic relationships and C.E.I. Santos, L.A. Boufleur, J.F. Dias and V.M. Andrade. 2010. classification of didelphid marsupials, an extant radiation of Heavy metals and DNA damage in blood cells of insectivore New World metatherian mammals. Bol. Am. Mus. Nat. Hist. bats in coal mining areas of Catarinense coal basin, Brazil. 322: 1 – 177. Environ. Res. 110: 684 – 691.

Brought to you by | University of Virginia Authenticated | 128.143.22.132 Download Date | 4/23/13 8:27 PM View publication stats