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Mastozoología neotropical

versión impresa ISSN 0327-9383versión On-line ISSN 1666-0536

Mastozool. neotrop. vol.24 no.1 Mendoza jun. 2017

 

ARTÍCULO

Terrestrial mammals of the Jequitinhonha River basin, Brazil: a transition area between Atlantic Forest and Cerrado

 

Lena Geise1, Luciana G. Pereira1, Diego Astúa2, Marcia Aguieiras1, Leonardo G. Lessa3, Paulo H. Asfora1, 2, Francisco Dourado4, and Carlos E. L. Esberárd5.

1 Laboratório de Mastozoologia, Departamento de Zoologia, IB, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil. [Correspondence: <lenageise@gmail.com>]
2 Laboratório de Mastozoologia, Departamento de Zoologia, CB, Universidade Federal de Pernambuco Recife, PE, Brazil.
3 Laboratório de Ecologia, Departamento de Ciências Biológicas, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, MG, Brazil.
4 Centro de Pesquisas e Estudo em Desastres, Departamento de Geologia Aplicada, FGEL, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil.
5 Laboratório de Diversidade de Morcegos, Departamento de Biologia Animal, Universidade Federal do Rio de Janeiro, Seropédica, RJ. Brazil.

Recibido 23 marzo 2016.
Aceptado 23 febrero 2017.
Editor asociado: G D’Elía


ABSTRACT.

Here we present an extensive survey for non-volant mammals along the margins of the Jequitinhonha River, which represents a contact area between the Cerrado and Atlantic Forest biomes. Our data were obtained after 13 trapping expeditions (from 2005 to 2012) on both banks of the river, from its source to its mouth, enriched by data obtained from a literature review and voucher specimens deposited in six mammal collections. All collected specimens were identified through their karyotypes and/or morphology. We obtained data for 75 localities (34 at the rigth margin, 42 at the left margin; 30 in the Cerrado and 45 in the Atlantic Forest). We obtained voucher records for 91 species, ca. 17% of all known Brazilian terrestrial non-volant mammals. Our results include range extensions for six species (Monodelphis scalops, Thylamys velutinus, Calomys mattevii, Wiedomys pyrrhorhinos, Galea spixii, Kerodon rupestris), and karyotype information for 26 species (11 marsupials and 15 rodents), with four new karyotypes. While most species have wide geographical range in both biomes, 26 were recorded only in the Cerrado and 19 were recorded only in the Atlantic Forest. Recorded species represent 28.7% (6.3% endemic) of the species known from the Cerrado and 21.5% (22.2% endemic) of those from the Atlantic Forest. The richness of the fauna recorded in this region supports its importance for the understanding of mammal biogeography, diversity and evolution.

RESUMO.

Mamíferos terrestres da bacia do Rio Jequitinhonha, Brasil: uma área de transição entre a Floresta Atlântica e o Cerrado.

Aqui apresentamos uma extensa pesquisa de mamíferos não-voadores ao longo das margens do Rio Jequitinhonha, região biogeográfica interessante que representa uma área de contato entre dois biomas brasileiros (Cerrado e Mata Atlântica), ainda pouco conhecidos para a fauna de mamíferos. Nossos dados foram obtidos após 13 expedições de captura (de 2005 a 2012), em ambas as margens do rio, da nascente até à foz, enriquecida por dados obtidos a partir de amostras de material depositado em seis coleções de mamíferos. Todos os espécimes coletados foram identificados através de seus cariótipos ou morfologia. Foram obtidos dados de 75 localidades (34 na margem direita, 41 à esquerda; 30 no Cerrado e 45 na Floresta Atlântica). Obtivemos registros de 91 espécies de mamíferos não-voadores, ca. de 17% de todos os mamíferos terrestres brasileiros conhecidos. Nossos resultados incluem extensões de distribuição de seis espécies (Monodelphis scalops, Thylamys velutinus, Calomys mattevii, Wiedomys pyrrhorhinos, Galea spixii, Kerodon rupestris), e informações de cariótipo de 26 espécies (11 marsupiais e 15 de roedores), com quatro novos cariótipos. Enquanto a maioria das espécies têm ampla distribuição geográfica, 26 ocorreram apenas no Cerrado e 19 apenas na Mata Atlântica. Foram registradas de 28.7% (6.3% endêmicas) de todas as espécies conhecidas para o Cerrado e 21.5% (22.2% endêmicas) da Floresta Atlântica. A riqueza da fauna registrada nesta região apoia a sua importância da compreensão na diversidade, biogeografia e evolução dos mamíferos.

Key words: Barriers; Didelphimorphia; Karyotypes; Rodentia; Species richness.

Palavras chave: Barreiras; Cariótipos; Didelphimorphia; Riqueza de espécies; Rodentia.


INTRODUCTION

Brazil is the largest country in the Neotropics and it has the largest mammal diversity in the world, with over 700 known species, a number that has been steadily increasing in the past decades (Costa et al., 2005; Paglia et al., 2012). Estimates from nearly 20 years ago had already predicted that the actual richness of Brazilian mammal species, given the extension of the country, was by far underestimated (Vivo, 1997). These facts only strengthen the importance of comprehensive and exhaustive surveys, particularly in those regions that have been poorly sampled, in order to accurately evaluate their species composition (Patterson, 2002; Costa et al., 2005; Lessa et al., 2008).

Not only is the Brazilian mammal fauna highly diverse, but also the country various biomes lead to varying levels of endemism, with different levels of threat to their mammals. Approximately 11% of the Brazilian mammal species are listed by the IUCN as globally threatened (IUCN, 2015) and 15% as nationally threatened by the Brazilian National Red List (MMA, 2014). Levels of endemism in Brazil are high, with ca. 30% of the recorded mammal species being endemic (Paglia et al., 2012). As a consequence of their high endemism and human pressure, two important Brazilian biomes, Atlantic Forest and Cerrado, were designated as global hotspots (Myers et al., 2000).

The Jequitinhonha River Basin appears to be a particularly interesting region because it runs into both Atlantic Forest and Cerrado. The vegetation along the Jequitinhonha River Basin changes along the river path. The region is formed by a mosaic of vegetal physiognomies presented in two biomes (Cerrado and Atlantic Forest), with the northwest part also close to the Caatinga, a uniquely Brazilian biome. Thus, such an environmental heterogeneity is likely to reveal a peculiar mammalian fauna composition, as it is surrounded by regions that harbor each a distinct mammal composition (Lessa and Paula, 2014). Additionally, this sequence of vegetation also includes contact zones, where several mammal species from more than one of these biomes can be found in sympatry (Geise and Astúa, 2009). However, the actual knowledge of mammals in the Jequitinhonha River Basin is still limited (Lessa et al., 2008). Thus, its mammal fauna needs to be properly diagnosed (Drumond et al., 2005) to provide a robust biogeographic data to further studies and more knowledge about the biodiversity of that region.

In this paper we report an extensive survey for non-volant mammals in both riverbanks of the Jequitinhonha River Basin, representing formations from two biomes (Cerrado and Atlantic Forest), along with karyotypic analyses. We also indicate how the Jequitinhonha River Basin region can be considered as an important ecotone discontinuity area.

MATERIALS AND METHODS

Study area

According to the document “Região Hidrográfica do Atlântico Leste”, organized by the Brazilian Ministry of Environment (MMA, 2006), the Jequitinhonha and Pardo rivers include four sub-basins: Jequitinhonha 1, Jequitinhonha 2, Jequitinhonha 3 and Pardo. Here we consider the area including three sub-basins (Jequitinhonha 1, 2 and 3) following the denomination provided by Instituto Brasileiro de Geografia e Estatística (IBGE, 1997), Ferreira (2011), Ferreira and Saadi (2011), Silva and Ferreira (2011) and Ferreira and Silva (2012), that includes part of the northeastern portion of the Minas Gerais state and a small portion of the southeast part of Bahia state. The basin is located between 16o - 18oS and 39o - 44oW, for a total area of 70 315 km2. Of these, 66 319 km2 are in Minas Gerais (MG) and 3996 km2 in Bahia (BA) state (IBGE, 1997). In the North, the Jequitinhonha River Basin borders the sub-basin of Pardo River, and in the South, the sub-basins of the Mucuri River and the South Bahia Coast (MMA, 2006). The source of the Jequitinhonha River lies near Serro City (MG), at an elevation of 1300 m and drains into the Atlantic Ocean at Belmonte City (BA). Some of the sampled localities are located outside the limits of the Jequitinhonha River drainage basin because for data collection and field work we included all municipalities that according to the Brazilian Institute of Geography and Statistics (IBGE, 2016) are completely or partially inside the basin limits.

Along the 920 km path of the Jequitinhonha River, 760 are in the Minas Gerais state and 160 in the state of Bahia (Ferreira, 2009). From the river source in the Cerrado down to its mouth in the Atlantic Forest, the climatic characteristics are variable, from humid to semiarid climates, and different vegetational formation are recorded (IBGE, 1997). Rains are usually concentrated from October to March, with 50% of all the rain occurring from December to February (Gonçalves, 1997). According to Silva and Ferreira (2011), in three localities, precipitation occurs in a very irregular pattern, Araçuaí, in the middle region of the basin, with an annual average of 766 mm, in Itamarandiba, closer to the source of the river, with 1050 mm, and in Pedra Azul, closer to the river mouth, with 860 mm. The social and environmental scenario of Jequitinhonha River Basin presents a dispersed population; the State interventions based on economic reorientation, focusing on technology and competitiveness, induce environmental degradation and generate economic, social and cultural negative consequences (Ferreira and Saadi, 2009).

As a whole, 75 localities were considered in this study; of these, 30 are in the Cerrado, while 45 are in the Atlantic Forest (Fig. 1). Eleven phytophysiognomies are found along the Jequitinhonha River Basin (IBGE, 2012) (Appendix I); two of them are non-natives as a consequence of the anthropic impact. Agrarian Activities (originally Savanna, Steppic Savanna/Seasonal Forest or Savanna/Broadleaf Forest) are present in 12 localities, and Secondary Vegetation and Agrarian Activities (originally Seasonal Deciduous Forest, Seasonal Semideciduous Forest or Broadleaf Forest) occur in 23 localities (IBGE, 2012). For original phytophysiognomy of each of these localities see Appendix I. The phytophysiognomies, Seasonal Decidual Submontante Forest, Moist Broadleaf Forest of Lowlands, Mangroves, Upper Montane Vegetational Refuges, Arboreous Steppic Savanna and Savanna/Broadleaf Forest are found at a single locality each. Four localities were at Arboreous Savanna, five Grassy-Woody Savanna, 25 Savanna/ Seasonal Forest (IBGE, 2012) (Appendix I).


Fig. 1. Mammal recording localities in the Cerrado and Atlantic Forest within and surrounding areas in the Jequitinhonha River Basin. Biome boundaries are according to IBGE (2016). White triangles indicate localities where trapping effort was carried out during the present study. For number of localities see Appendix I.

Field work

From those 75 localities where mammals were recorded in this study (see above), small mammals were trapped in 13. These localities were chosen to cover both left (localities 2, 5, 44, 45, and 73) and right (localities 6, 7, 8, 9, 43, 49, 53 and 75) banks of the Jequitinhonha River (Fig. 1, Appendix I), were vegetation was more preserved or where field activities could be carried on without security problems for researchers. Traps were set differently according to topography and presence of trees (arboreal traps set at up to 3 m high), mostly placed in lines ca. 15 to 20 m apart one from another. Three live traps models were used (Sherman®, Tomahawk® and pitfall) with banana and manioc pieces, peanut butter and bacon bits as bait in live-traps in areas of Atlantic Forest, and peanut butter, orange or pineapple pieces and cotton wool soaked in cod liver oil in dryer areas in Cerrado. In addition to the collected specimens of small mammals (marsupials and rodents), we also collected road-killed animals, obtained skulls from farmers, searched for tracks and made visualization in the field. Table 1 indicates the name, coordinates and trapping effort for each locality. Tissue (liver) samples, fixed in ethanol, were collected from all specimens, as well as ectoparasites. All specimens were prepared as skins, skulls, and partial skeletons. Specimens were collected under sample permits from ICMBio granted to L. Geise (IBAMA 0201.009374/02-86 and SISBIO 598633), to L.G. Lessa (SISBIO 19790-1 and 42892-1) and to C.E.L. Esberárd (SISBIO 10356-1).

Table 1
Trapping localities of the present study, including locality name, number (see Appendix I), coordinates, altitude or altitude range where traps were settled, period of the fieldwork and trapping effort.

Below we provide a short description of those localities we surveyed. Localities are numbered according to Appendix I.

Locality #2 - Pousada Rural Recanto do Vale (Fig. 2A). The vegetation is Grassy-Woody Savanna, in the Cerrado (IBGE, 2012). Traps were set in lines along a small creek, on sandy ground and near a small waterfall, on the rocks (“lajeiro”).


Fig. 2. Views of some surveyed localities: A) Pousada Rural Recanto do Vale (Locality 2) – Grassy-Woody Savanna; B) Fazenda Santa Cruz (Locality 6) – Grassy-Woody Savanna, where a Campo Limpo can be observed; C) Parque Estadual do Rio Preto (Locality 7) – Grassy-Woody Savanna with an overview of Cerrado lato sensu; D) Fazenda Sumidouro (Locality 8) – Savanna/Seasonal Forest, where a rocky margin of a small creak with arbustive vegetation can be observed; E) Pousada Água Quente (Locality 9) – Savanna/Seasonal Forest, depicting characteristic seasonal forest; F) Fazenda Ilha (Locality 43) – Savanna/Seasonal Forest, showing an arbustive and thorny vegetation; G) Fazenda Dona Marília (Locality 44) – Savanna/Seasonal Forest, showing an arbustive and thorny vegetation with some cactus; H) Fazenda Galiléia (Locality 45) – Savanna/Seasonal Forest – with the same vegetation observed in locality 44; I) Fazenda Palmares (Locality 49) – Secondary Vegetation and Agrarian Activities (originally Seasonal Semideciduous Forest), showing a pasture, with forest on the top of the hill; J) Fazenda Anga-Pehy (Locality 53) – Secondary Vegetation and Agrarian Activities (originally Seasonal Semideciduous Forest) = with the same vegetation observed in locality 49. All photos taken by Lena Geise, except that of locality 7, taken by Leonardo G. Lessa.

Locality #5 – Parque Nacional das Sempre Vivas (PARNASV). The vegetation is Upper Highlands Vegetational Refuges, in the Cerrado (IBGE, 2012). Traps were set in lines along a rupestrian fields area interspersed with forest patches in the southern part of the PARNASV.

Locality #6 - Fazenda Santa Cruz (Fig. 2B). The vegetation is Grassy-Woody Savanna, in the Cerrado (IBGE, 2012). Traps were set in open grasslands with rocky outcrops, in gallery forests and open vegetation formations. Some trapping lines were along characteristic Cerrado formation, with many pequi trees (Caryocar brasiliense, Caryocaraceae).

Locality #7 – Parque Estadual do Rio Preto (PERP) (Fig. 2C). The vegetation is Grassy-Woody Savanna, in the Cerrado (IBGE, 2012). The PERP is located in the southern area of the Espinhaço Mountain Range with a mosaic of vegetation physiognomies. Traps were settled in areas of riparian savanna, Cerrado stricto sensu and open grasslands.

Locality #8 - Fazenda Sumidouro (Fig. 2D). The vegetation is Savanna/Seasonal Forest, in the Cerrado (IBGE, 2012). Traps were set in fragments of forest formation surrounded by pasture, some lines along the Araçuaí River.

Locality #9 - Pousada Água Quente (Fig. 2E). The vegetation is Savanna/Seasonal Forest, in the Cerrado (IBGE, 2012). Trapping was carried out in Gallery Forest, with traps along the river, over rocks or sand and some in the river. Other lines were set in a Forest, at the slope of a small hill, a very humid area. Grasses covered the beginning of the line. The “campo sujo” was at another slope, with rocky and sandy soil, some areas recovering from fire.

Locality #43 - Fazenda Ilha (Fig. 2F). The vegetation is Savanna/Seasonal Forest, in the Atlantic Forest according to the map (IBGE, 2012), but local observation showed that it is clearly in the Cerrado. Lines were set in typical arboreal vegetation (close thorny arbustive vegetation, with small sparse trees), with sandy soil.

Locality #44 - Fazenda Dona Marília (Fig. 2G). The vegetation is Savanna/Seasonal Forest, in the Atlantic Forest according to the map (IBGE, 2012), but local observation showed that it is clearly in the Cerrado. Trapping lines were in open arboreal vegetation with an open bush formation. Trapping lines were along the Jequitinhonha River.

Locality #45 - Fazenda Galiléia (Fig. 2H). The vegetation is Savanna/Seasonal Forest, in the Atlantic Forest according to the map (IBGE, 2012), but local observation showed that it is clearly in the Cerrado. General vegetation where lines were mounted is arboreal vegetation (close thorny arbustive vegetation, with sparse low trees), with sandy soil. Trapping was carried out during the rainy season, so vegetation was green.

Locality #49 - Fazenda Palmares (Fig. 2I). The vegetation is Secondary Vegetation and Agrarian Activities (originally Seasonal Semideciduous Forest), in the Atlantic Forest (IBGE, 2012). Traps were set in disturbed forest fragments located on mountaintops surrounded by pastures.

Locality #53 - Fazenda Anga Pehy (Fig. 2J). The vegetation is Secondary Vegetation and Agrarian Activities (originally Seasonal Deciduous Forest), in the Atlantic Forest (IBGE, 2012). Traps were set in disturbed forest fragments located on mountaintops surrounded by pastures, one along a creek, another around a swampy area covered by graminae. Another vegetation was a dry altered forest, locally called “Mata da Chapada”.

Locality #73 - Fazenda Futurosa. The vegetation is Agrarian Activities (original vegetation was Savanna/ Broadleaf Forest), in the Atlantic Forest (IBGE, 2012). The sampled area is a forest fragment surrounded by eucalyptus plantations and the “Cabruca”, a cacao trees plantation grown under the Atlantic Forest canopy, also surrounded by pasture.

Locality #75 - Reserva Particular do Patrimônio Natural (RPPN), Estação Veracel. The vegetation is Moist Broadleaf Forest of Lowlands, in the Atlantic Forest. All trapping occurred in the preserved forest area.

Small mammal species identification (karyotypes and morphology)

Karyotypes were prepared in the field for all rodent specimens and at least one specimen of each collected species of marsupial. Metaphases were obtained with in vitro bone marrow culture according to Geise (2014). Conventional coloration with Giemsa 5% was used to observe diploid (2n) and fundamental (FN, excluding sexual chromosomes) numbers and chromosome morphology. Rodents were identified to species level by comparison with voucher specimens deposited in collections, species descriptions, and karyological analysis. Morphological characters (skin and skull) were considered for species identification in comparison to previous descriptions for Didelphimorphia. Nomenclature follows Wilson and Reeder (2005), Gardner (2008), Melo and Sponchiado (2012), Gurgel-Filho et al. (2015) and Patton et al. (2015).

Museum collections and literature review

Medium and large mammal (Cingulata, Pilosa, Primates, Lagomorpha, Carnivora, Perissodactyla, and Cetartiodactyla) records, in addition to other small mammal species, were obtained from museum collections (Museu Nacional do Rio de Janeiro, Museu de Zoologia da USP, Coleção do Laboratório de Mastozoologia e Manejo da Fauna do Departamento de Zoologia, Universidade Federal de Minas Gerais, Museu de Ciências Naturais da PUC Minas, Museu de Zoologia da Universidade Federal de Viçosa and Coleção de Mastozoologia da Universidade Federal dos Vales do Jequitinhonha e Mucuri).

Literature review was carried out to complete all mammal species occurrence. We do not consider specimens of Akodon cursor that were not identified through genetic techniques, as identification based solely on skull and skin morphology is not reliable for this species (Geise, 2012).

Localities characterization, species geographic pattern distribution and classification of endangered species

Coordinates and altitude for each locality were obtained at each capture location and gazetteers online (www.geonames.org, www.falingrain.com/ world and www.splink.cria.org.br/geoloc), using SAD 69 23 K Datum. Vegetation classification of each locality is according to the IBGE (2012).

For geographic range increase of species, we searched each species known geographic distribution provided by Gardner (2008), Geise and Astúa (2009), Cáceres (2012), Gurgel-Filho et al. (2015) and Patton et al. (2015). For biome endemism, we used Paglia et al. (2012). Classification of endangered species (Vulnerable, Endangered and Critically Endangered) is according to IUCN (2015) and MMA (2014). Near Threatened (NT) and Data Deficient (DD) are according to ICMBio (2014) and IUCN (2015).

RESULTS

Our collecting effort in 13 localities and with the inclusion of museum specimens and literature information resulted in a list of 91 mammal species in 75 localities along the Jequitinhonha River Basin (Appendices I and II); 15 species belong to the Order Carnivora, four to Cetartiodactyla, six to Cingulata, 14 to Didelphimorphia, one to Lagomorpha, one to Perissodactyla, three to Pilosa, 11 to Primates, and 36 species to Rodentia. We trapped 33 species of small mammals (13 marsupials and 20 rodents), three species were visualized (Cabassous unicinctus, Callithrix geoffroyi and Guerlinguetus brasiliensis), one was recorded from footprints (Procyon cancrivorus) and two species of medium sized-mammal were recovered as road-kills (Cerdocyon thous and Sylvilagus minensis) (Table 2).

Table 2
Registered mammal species, with their locality numbers (for localities name see Appendix I), type of record, biome, vegetation and conservation status. Type of record: F = footprint; R = References: 1. Chiarello et al. (2006), 2. Falcão et al. (2012), 3. Leal et al. (2008), 4. Lessa et al. (2008), 5. Lessa and Paula (2014), 6. Melo (2005), 7. Melo et al. (2004), 8. Oliveira and Gonçalves (2015), 9. Oliveira et al. (2013), 10. Pardiñas et al. (2014), 11. Pessôa et al. (2015), 12. Pinto and Rylands (1997), 13. Rylands et al. (1988), 14. Voss (2015); RK = Road killed animals; V = visualization; VS = voucher specimens. Biome according to IBGE (2012): CE = Cerrado and AF = Atlantic Forest. Vegetation according to IBGE (2012): a = Grassy-Woody Savanna; b = Upper Montane Vegetational Refuges; c = Savanna/ Seasonal Forest; d = Agrarian Activities (originally Savanna, Steppic Savanna/Seasonal Forest or Savanna/ Broadleaf Forest); e = Secondary Vegetation and Agrarian Activities (originally Seasonal Decidual, Semideciduous or Moist Broadleaf Forests); f = Arboreous Savanna; g = Arboreous Steppic Savanna; h = Seasonal Decidual Submontante Forest; i = Savanna/ Broadleaf Forest; j = Mangroves; k = Moist Broadleaf Forest of Lowlands. Legend for Conservation Status: LC = Least Concern, NT = Near Threatened, E = Endangered, CE = Critically Endangered, V = Vulnerable, according to International Union for Conservation of Nature (IUCN), Ministério do Meio Ambiente (MMA), Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio).






According to the IUCN (2015) 20 out of the 91 species recorded for the Jequitinhonha River Basin are threatened, while according to the MMA (2014) and ICMBio (2014) 27 species are threatened. For IUCN (2015), the most endangered species are Brachyteles hypoxanthus and Sapajus xanthosternos (with the status of Critically Endangered), and Leontopithecus chrysomelas and Sapajus robustus (with the status of Endangered). According to the MMA (2014) and ICMBio (2014) the worst cases are B. hypoxanthus as Critically Endangered, and L. chrysomelas, S. robustus, S. xanthosternos, Leopardus guttulus, Thalpomys lasiotis and Trinomys mirapitanga with the status of Endangered (Table 2).

We increased the known distribution for eight species. The record of Calomys mattevii increases the species distribution eastwards in 190 km from Juramento, MG (Gurgel-Filho et al., 2015) to Fazenda Dona Marília-Itinga, MG (locality 44). Galea spixii distribution increased southwards in 178 km from Campos Gerais de São Felipe, BA (Dunnum, 2015) to Araçuaí municipality (locality 34). The record of Kerodon rupestris in the Parque Estadual do Rio Preto, São Gonçalo do Rio Preto municipality (locality 7) increases the species distribution to the southeast in 330 km from Riacho da Cruz, MG (Dunnum, 2015). The record of Sooretamys angouya in Distrito Carne Seca, Fazenda Corredor, MG (locality 12) increases the species distribution to the northwest in 450 km from Rio São José, ES (Percequillo, 2015b). Thylamys velutinus was recorded in Rio do Pardo de Minas municipality, MG (locality 48), which increases the species distribution to the east in 150 km from Lagoa Santa, MG (Creighton and Gardner, 2008). The record of Monodelphis scalops at the Parque Nacional das Sempre Vivas, Diamantina municipality, MG (locality 5) increases the species distribution to the northwest in 400 km from Santa Teresa, ES (Pine and Handley, 2008). Wiedomys pyrrhorhinos had a distribution increase to the south in 145 km from Juramento, BA (Bonvicino, 2015) to Pousada Água Quente, Felício dos Santos municipality, MG (locality 9).

We obtained karyotype for 26 species (11 Didelphimorphia and 15 Rodentia; Table 3). Eight rodent species presented karyotype variation—Akodon cursor, Cerradomys scotti, Cerradomys subflavus, Cerradomys vivoi, Nectomys squamipes, Rhipidomys mastacalis, Trinomys albispinus and Wiedomys pyrrhorhinos (Table 3). Undescribed chromosomal variation was found in C. scotti, C. subflavus, T. albispinus and W. pyrrhorhinos. Cerradomys scotti specimens, collected in Fazenda Santa Cruz (locality 6) presented two distinct fundamental numbers, 68 (MN82753, Fig. 3) and 72 (MN82752). The karyotype with FN=68 is composed by six pairs of biarmed and 22 acrocentric chromosomes. The karyotype of C. subflavus (MN82759, collected also in locality 6) presented variation in the sexual pair, in which the X chromosome is a large submetacentric and the Y is a small acrocentric (Fig. 4). Trinomys albispinus was collected only in locality 45 (MN82935, from Fazenda Galiléia), the fundamental number (FN) 108, with 25 pairs of biarmed and four pairs of acrocentric chromosomes (Fig. 5). Wiedomys pyrrhorhinos presented two different fundamental numbers, FN=98 (MN82944, from Fazenda Ilha, locality 43; MN82938 and 82939 from Fazenda Galiléia, locality 45; MN82940, 82941, 82942 from Pousada Água Quente, locality 9), with 19 pairs of biarmed and 11 pairs of acrocentric chromosomes (Fig. 6A) and FN=99 (MN82943, from Fazenda Ilha, locality 43) composed by 19 pairs of biarmed and 10 pairs of acrocentric chromosomes, and a heteromorphic pair of small chromosomes (Fig. 6B).

Table 3
Species karyotyped with locality number (for name of locality see Appendix I). Diploid number (2n) and fundamental number (FN). * Indicates those species with new karyotype variation.


Fig. 3. Karyotype in conventional staining of a female Cerradomys scotti (MN82753), collected at Fazenda Santa Cruz (locality 6), showing 2n=58, FN=68, with six pairs of biarmed and 22 pairs of acrocentric chromosomes. X chromosome as a medium biarmed chromosome.


Fig. 4. Karyotype in conventional staining of male Cerradomys subflavus (MN82759), collected at Fazenda Santa Cruz (locality 6), showing 2n=54, FN=62, with five pairs of biarmed and 21 pairs of acrocentric chromosomes. X chromosome as a medium biarmed, and Y chromosome as a small acrocentric.


Fig. 5. Karyotype in conventional staining of Trinomys albispinus (MN82935) collected at Fazenda Galiléia (locality 45) showing 2n=60, FN=108, with 25 pairs of biarmed and four pairs of acrocentric chromosomes; male individual, X chromosome as a large biarmed, and Y a small acrocentric chromosome.


Fig. 6. Karyotypes in conventional staining of Wiedomys pyrrhorhinos collected at Fazenda Ilha (locality 43). A) MN82944, 2n=62, FN=98, with 19 pairs of biarmed and 11 pairs of acrocentric chromosomes; female individual, X chromosome as a medium acrocentric. B) MN82943, with 2n=62, FN=99, with 19 pairs of biarmed and 10 pairs of acrocentric chromosomes, and a heteromorphic pair of small chromosomes; female individual, X chromosome as a medium autosomal.

DISCUSSION

Our trapping efforts, coupled with all the information obtained from museums and the literature, provided a comprehensive view of the non-volant mammal diversity along the Jequitinhonha River Basin. Terrestrial mammal species richness recorded in Jequitinhonha River Basin represents 17% of all known terrestrial species in Brazil, not considering Calassomys apicalis, described after Paglia et al. (2012). Most recorded species (91) have a wide geographical distribution range and may occur in more than one biome in South America (Bonvicino et al., 2002; Geise and Astúa, 2009; Pereira and Geise, 2009; Carmignotto et al., 2012; Costa and Leite, 2012; Paglia et al., 2012); however, we collected 19 species only in Atlantic Forest localities and 26 in Cerrado localities.

Currently, 32 of 251 (not including C. apicalis) and 90 of 298 species of mammals occur/are endemic and registered in the Cerrado and Atlantic Forest, respectively (Carmignotto et al., 2012; Costa and Leite, 2012; Paglia et al., 2012). We trapped a considerable portion of this diversity, and recorded 28.7% (6.3% endemic) of all Cerrado and 21.5% (22.2% endemic) of all Atlantic Forest species, thus showing the biological importance of the surveyed area. We recorded species considered to be restricted to the Cerrado and Caatinga in the Atlantic Forest (Calomys mattevii, Didelphis albiventris, Gracilinanus agilis, Rhipidomys macrurus, Thrichomys apereoides and Wiedomys pyrrhorhinos), as well as species considered restricted to the Atlantic Forest in Cerrado areas (Callithrix geoffroyi, Dasyprocta leporina, Gracilinanus microtarsus, Guerlinguelus brasiliensis, Monodolphis scalops, Oxymycterus dasytrichus, Phyllomys lamarum, Sapajus robustus, Sooretamys angoya and Trinomys setosus) (Table 2). Such records show the need of carefully reassess the scheme of biome endemicity provided by Paglia et al. (2012).

Habitat and vegetation characteristics were observed during field work, differing from biome and vegetation maps (IBGE 2012), showing that the Cerrado and Atlantic Forest borders are not precisely delimited, either due to the low resolution of IBGE data or accelerated rates of deforestation. This could be seen in localities 43, 44 and 45, which are not Atlantic Forest, but dry vegetation of Cerrado (for a better conclusion, see Figs. 2F, 2G and 2H) or Fazenda Palmares (locality 49), according to Fig. 1 in the Atlantic Forest (Secondary Vegetation and Agrarian Activities, originally Seasonal Semidecidous Forest; IBGE, 2012), but according to fieldwork, a transition area between both biomes.

The importance of the species survey increases when the conservation status is considered. Eight major protected areas are located along the basin, three of them surveyed by us. Seven protected areas are in Minas Gerais state (six in Cerrado biome: Parque Nacional Sempre Vivas, Parque Estadual do Rio Preto, Parque Estadual de Biribiri, Parque Estadual do Pico do Itambé, Parque Estadual da Serra Negra, Parque Estadual de Grão Mogol; and one in Atlantic Forest biome: Reserva Biológica [REBIO] Mata Escura), and one in Bahia State (Atlantic Forest Biome: Reserva Particular de Proteção Natural [RPPN] Estação Veracel). In those protected areas, according to the information provided by environmental government agencies (ICMBio, 2016 and IEF/MG, 2016 accessed August/2016) 14 endangered taxa may occur (Alouatta spp., Brachyteles hypoxanthus, Callicebus spp., Callithrix geoffroyi, Chaetomys subspinosus, Chrysocyon brachyurus, Leopardus pardalis, Lontra longicaudis, Myrmecophaga tridactyla, Panthera onca, Priodontes maximus, Puma concolor, Sapajus robustus and Tapirus terrestris), all medium or large mammals. However, we have in our list three species of small mammals under conservation threat (Thalpomys lasiotis, Thylamys velutinus and Trinomys mirapitanga), with only few occurrences in protected areas. The sum of all those eight protected area is 2570 km2, which represents only a small fraction (3.7%) of the whole basin (70 315 km2). Most of the protected areas are in the Cerrado, even when a larger area of the basin lies in the Atlantic Forest (Fig. 1).

All collected marsupial species, a group known to have a very conservative chromosomal composition (Svartman and Vianna- Morgante, 1998; Astúa, 2015), showed diploid and autosomal numbers already described in the literature (Yunis et al., 1973; Carvalho et al., 2002; Paresque et al., 2004; Pereira et al., 2008).

We obtained new karyotypes for Cerradomys scotti, C. subflavus, Trinomys albispinus and Wiedomys pyrrhorhinos. The fundamental number described in the present paper for C. scotti is lower, with an increase of acrocentric chromosomes, than those previously reported (Bonvicino et al., 1999). The sexual pair here reported for one specimen of C. subflavus differs from the previously described karyotype (Bonvicino et al., 1999). The fundamental number of T. albispinus presented here (FN = 108) differs because of the presence of 25 biarmed pairs instead of 29 as described by Pessôa et al. (2015). The published karyotypes for W. pyrrhorhinos show that the species is highly variable (2n=62, FN=86, 90 and 104; Maia and Langguth, 1987; Gonçalves et al., 2005; Pereira and Geise, 2007). The karyotype presented here (2n=62, FN=98/99), with another different autosomal number, increases the known intraspecific variation.

Chromosome data available for Brazilian populations of squirrels are scarce (Fagundes et al., 2003), with most species presenting a similar karyotype, 2n=40, FN=74 (Sciurus aestuans ingrami) and 2n=40, FN=76 (S. a. alphonsei and S. a. spadiceus, described by Lima and Langguth 2002); both karyomorphs differ in the 19th pair, with metacentric chromosomes in the former and acrocentric in the second one. The specimens we collected match the description of Vivo and Carmignotto (2015) and Vivo (personal communication) for Guerlinguelus brasiliensis brasiliensis, which currently include S. a. alphonsei and S. a. spadiceus as synonyms. So, we conclude that the karyotype observed by us for our sample of G. brasiliensis is the same of those described by Lima and Langguth (2002).

The area surveyed and studied here shows few particular patterns of species distribution occurrence. Some are already known in literature, such as the rodent species Akodon cursor (Geise, 2012) and Cerradomys spp., where C. subflavus occurs only on the right side of the river as opposed to C. vivoi, which occurs north of the left side (Bonvicino et al., 1999; Weksler et al., 2006; Percequillo, 2015a). Leite et al. (2016) presented a complete explanation about the Rio Doce as a discontinuity area. Further extensive collecting effort in the Jequitinhonha River Basin may provide future basis to discuss if this region represents another area of faunal discontinuity for some lineages of small mammals.

Our study showed a high diverse terrestrial mammal fauna, with relevant records of new karyotypes, endangered fauna and sympatric occurrence of species of both adjacent biomes —Cerrado and Atlantic Forest. A continuity of trapping effort is necessary to further characterize (e.g., phylogeography) the registered species.

ACKNOWLEDGMENTS

We are thankful to Júlia Lins Luz, Maíra de Godoy Sant’Ana, Luciana de Moraes Costa, Thais Lira and Vera de Ferran for fieldwork help; to Heitor Bispo, Fábio Henrique Alves Bispo, Luiz Carlos da Silva, Rita de Cassia de Melo Tolentino and Georg Marksteinr (Pousada Água Quente and Fazenda Sumidouro), Sueli Vieira (Fazenda Ilha), Mr. Túlio (Fazenda Palmares), Mr. and Mrs. Guimarães (Fazenda Anga-Pehy) and all the staff of the Reserva Particular do Patrimônio Natural, Estação Veracel, for lodging and permission to work within their properties. Leila Maria Pessôa helped in the identification of Trinomys spp. Fabiano Rodrigues de Melo was of great help providing information about all Primates species; R. Moratelli kindly assessed Oxymycterus dasytrichus specimens in the Smithsonian Institution, Washington DC. Field work was carried out with funding provided by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Edital Universal # 473596/2006-7 and 472909/2009-6 andComCerrado#563134/2010-0 Edital nº 47/2010 - Chamada 2), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG - # APQ01034/09) and Programa SISBIOTA/CNPq (# 56314/2010.0). L. Geise receives productive grants from CNPq (# 306161/2016-8) and UERJ/Prociência, C.E.L. Esbérard received a CNPq productive grant (# 151029/2004-0) and financial support from FAPERJ to “Young Scientist of Our State” (E-16/170.449/2007 and E-26/102.201/2009). D. Astúa was supported by FAPERJ (E-26/150.353/2005) and by a CNPq fellowship (306647/2013- 3). Marcia Aguieiras had fellowship from FAPERJ (E-26/102.327/2011) and has a doctoral scholarship from CAPES. Paulo H. Asfora had a fellowship from FAPERJ (E-26/100.331/2007) and Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE - DCR-0053-2.04/11, Bolsa DCR e APQ-0020-2.04/12). F. Dourado receives financial support from FAPERJ to “Young Scientist of Our State” (E-16/203.218/2015). We are grateful to all comments made by two anonymous reviewers.

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APPENDIX I

Gazetteer with geographical and vegetation information for localities from Jequitinhonha River Basin with mammal registers, arranged from the source to the mouth region of the river. Underlined names = municipalities. Number before locality name corresponds to localities plotted in Fig. 1. Localities with our collecting effort are in bold. nln = no locality name. When coordinates of a locality were not found we used coordinates of the municipality. After coordinates, vegetation type (IBGE 2012): Agrarian Activities (originally Savanna, Steppic Savanna/Seasonal Forest or Savanna/ Broadleaf Forest) = AA; Arboreous Savanna = AS; Arboreous Steppic Savanna = ASS; Grassy-Woody Savanna = GWS; Mangroves = MA; Moist Broadleaf Forest of Lowlands = MBFL; Savanna/ Broadleaf Forest = S/BF; Savanna/Seasonal Forest = S/SF; Seasonal Decidual Submontante Forest = SDSF; Secondary Vegetation and Agrarian Activities (originally Seasonal Decidual, Semideciduous or Moist Broadleaf Forests) = SV/AA; Upper Montane Vegetational Refuges = UMVR.

MINAS GERAIS STATE: Serro, 1 – nln (18°36’10”S, 43°22’45”W, SV/AA, originally SSF); Diamantina, 2- Pousada Rural Recanto do Vale (18°23’43.2”S, 43°32’25.5”W, GWS), 3 - Lavrinha, Mineração Tejucana (18°14’58”S, 43°36’01”W, GWS), 4 - Conselheiro Mata (18°14’44”S, 43°54’02”W, GWS), 5 – Parque Nacional das Sempre Vivas (17°55’02”S; 43°47’11”W, UMVR), 6 - Fazenda Santa Cruz (18°16’16.2”S, 43°23’18.8”W, GWS); São Gonçalo do Rio Preto, 7 - Parque Estadual do Rio Preto (18°05’20”S, 43°20’25”W, GWS); Felício dos Santos, 8 - Fazenda Sumidouro (18°11’34.4”S, 43°14’35.2”W, S/ SF), 9 - Pousada Água Quente (18°05’32.5”S, 43°10’26.2”W, S/SF); Bocaiúva, 10 - nln (17°06’59”S, 43°49”58”W, S/SF), 11 - Mineração SADA (17°06’54”S, 43°49’16”W, S/SF), 12 - Distrito Carne Seca, Fazenda Corredor (17°02’14”S, 43°52’16”W, AA, originally S); Botumirim, 13 - Veredas de Botumirim, 32 km NW Caçaratiba (17°07’S, 43°02’W, S/SF); Turmalina, 14 - nln (17°17’30”S, 42°43’05”W, S/SF), 15 - Road close to Córrego Divisão, 1 km SW Peixe Cru and Alambique do Joel, 800 m Peixe Cru (17°16’56”S, 42°44’07”W, S/SF), 16 - Usina Hidrelétrica de Santa Rita (17°17’08”S, 42°43’48”W, S/ SF), 17- Leme do Prado, Estação Ecológica de Acauã, 17 km N from Turmalina (17°08’S, 42°46’W, S/SF), 18 - Rodovia MG 367, km 405 (17°13’07”S, 42°35’25”W, S/SF); Minas Novas, 19 - nln (17°12’05”S, 42°36’07”W, S/SF), 20 - Córrego da Chácara (17°45’S, 42°30’W, SV/AA, originally SSF); Cristália, 21 - nln (16°49’S, 42°41’W, S/SF), 22 - Córrego Contendas (16°45’S, 42°52’W, AS), 23 - Left margin of Jequitinhonha River (16°43’S, 42°37’W, S/SF); Berilo, 24 - Buriti, margin of Jequitinhonha River (16°49’S, 42°41’W, S/SF), 25 - Buriti, Fazenda Irmãos Atachi (16°51’S, 42°38’W, S/SF); Grão Mogol, 26 - Fazenda Giro (16°34’S, 43°02’W, AS), 27 - Usina Hidrelétrica Presidente Juscelino Kubitschek (UHE Irapé) (16°33’26”S, 42°53’38”W, AS), 28 - Fazenda Curral Velho, 28 km E from Grão Mogol, Fazenda Maria das Neves and Fazenda do Matão (16°33’34”S, 42°53’23”W, AS); Chapada do Norte, 29 - Rio Capivari (17°06’S, 42°32’W, S/SF); Francisco Badaró, 30 (16°58’52”S, 42°20’45”W, S/SF); Coronel Murta, 31- Ponte do Colatino, left margin of Jequitinhonha River (16°36’S, 42°12’W, AA, originally SS/SF); Virgem da Lapa, 32 - Fazenda Mandacarú (16°42’S, 42°13’W, S/SF), 33 - Fazenda Paiol (16°50’S, 42°13’W, AA, originally SS/SF); Araçuaí, 34 - nln (16°51’20”S, 42°03’25”W, AA, originally SS/SF), 35- Jenipapo de Minas, 50 km from Araçuaí (17°04’39”S, 42°15’25”W, SV/AA, originally SSF), 36 - Baixa Quente (16°57’00”S, 42°04’00”W, AA, originally SS/SF), 37 - Chapada do Lagoão, Serra do Tombo and Calhaquizinho (16°51’00”S, 42°04’13”W, AA, originally SS/ SF), 38 - Trilha do Rio Piauí (16°49’15”S, 41°52’47”W, AA, originally SS/SF), 39 - Fazenda Arqueana, Piauí river (16°43”S, 41°53’W, S/SF); Itinga, 40 – Taquaral (16°43’S, 41°52’W, S/SF), 41 - Fazenda Santana (16°40’S, 41°59’W, AA, originally SS/ SF), 42 - Fazenda Santa Maria (16°36’S, 41°56’W, AA, originally SS/SF), 43 - Fazenda Ilha (16°39’42.6”S, 41°52’5.1”W, S/ SF), 44 - Fazenda Dona Marília (16°36’46.1”S, 41°49’35.5”W, S/SF), 45 - Fazenda Galiléia (16°34’56.4”S, 41°47’23.4”W, S/SF); Salinas, 46 - Fazenda Bamburral, Fazenda Umburana and Ribeirão Bananal (16°10’15”S, 42°17’26”W, AA, originally SS/SF); Taiobeiras, 47 – nln (15°46’06”S, 42°14’33”W, SV/AA, originally SDF); Rio Pardo de Minas, 48 – nln (15°36’02”S, 42°32’22”W, S/SF); Padre Paraíso, 49 - Fazenda Palmares 17°07’18.6”S, 41°36’48.6”W, SV/AA, originally SSF); Itaobim, 50 - Galery forest from the Piauí river, BR367 road (16°33’42”S, 41°30’12”W, ASS); Joaíma, 51 - Joaíma-Santana de Araçuaí road (16°45’24.6”S, 41°26’47.5”W, SSF), 52 - Fazenda Anta Podre (16°40’S, 41°59’W, AA, originally SS/SF), 53 - Fazenda Anga Pehy (16°43’7.6”S, 41°14’57.6”W, SV/AA, originally SDF); Jequitinhonha, 54 - Mata da Torre da Telemig (16°21’S, 41°05’W, SV/AA, originally SSF), 55 - Reserva Biológica Federal da Mata Escura (16°24’28”S, 41°02’05”W SV/AA, originally SDF), 56 – nln (16°25’56”S, 41°00’06”W, SV/AA, originally SSF); Almenara, 57 - Fazenda Limoeiro (16°02’57”S, 40°51’02”W, SV/AA, originally SSF), 58 - nln (16°03’31”S, 40°39’26”W, SV/AA, originally SSF), 59 - Fazenda Estancia Betania (16°01’S, 40°51’W, SV/AA, originally SSF), 60 – Copasa (15°51’19”S, 40°38’55”W, SV/AA, originally SSF); Bandeira, 61 - Fazenda Serra Azul (15°48’64.4”S, 40°30’86.1”W, SV/AA, originally SSF), 62 - nln (15°52’59”S, 40°34’00”W, SV/AA, originally SSF); Jordania, 63 - nln (15°54’00”S, 40°10’59”W, SV/AA, originally SDF); Santa Maria do Salto, 64 - Fazenda Duas Barras (16°14’03”S, 40°08’42”W, SV/AA, originally SSF), Salto da Divisa, 65 - Fazenda Santana (15°57’S, 40°05’W, SV/AA, originally SDF), 66 – nln (16°00’57”S, 39°56’53”W, SDSF). BAHIA STATE; Itarantim, 67 - Fazenda Boa Vista (15°53’S, 40°09’W, SV/AA, originally SDF), 68 - Fazenda Bom Jardim (15°39’15”S, 40°03’48”W, SV/AA, originally SDF), 69 - Fazenda Alsácea (15°30’S, 40°04’W, SV/AA , originally); Itapebi, 70 - Fazenda Santa Inês (15°46’S, 39°40’W, SV/AA, originally SSF), 71 - nln (15°57’03”S, 39°32’02”W, SV/AA, originally MBF); Mascote, 72 - Fazenda São José (15°34’05”S, 39°17’07”W, S/BF); Belmonte, 73 - Fazenda Futurosa, Santa Maria Eterna (15°51’28”S, 39°24’38.2”W, AA, originally S/ BF); Passuí, 74 – nln (15°51’S, 38°54’W, MA); Santa Cruz de Cabrália, 75 – Reserva Particular do Patrimônio Natural Estação Veracel (16°21’11.6”S, 39°06’49.6”W, MBFL).

APPENDIX II

Mammal species from the Jequitinhonha River Basin. Species are listed in alphabetic order. Specimens captured by us are indicated by a star (*), specimens recovered from roads (road kill) are indicated by (RK) and karyotyped are indicated by a letter K (K). Localities are numbered as in Appendix I and Fig. 1, and specimens are ordered by sex. F = females, M = males, U shows a specimen of undetermined sex. Acronyms are: Museu Nacional do Rio de Janeiro (MN), Museu de Zoologia da USP (MZUSP), Coleção do Laboratório de Mastozoologia e Manejo da Fauna do Departamento de Zoologia, Universidade Federal de Minas Gerais (UFMG and CC), Museu de Ciências Naturais da PUC Minas (MCN-M), Museu de Zoologia da Universidade Federal de Viçosa (MZUFV) and Coleção de Mastozoologia da Universidade Federal dos Vales do Jequitinhonha e Mucuri (MDIA)). Field number acronyms are LG (L. Geise). After first citation of an acronym, only the number is given.

Akodon cursor -17 (F - UFMG2668, 2669K); 49 (M - MN82750*K); 53 (F - MN82738*K, 82741*K, 82742*K, 82743*K, 82744*K, 82745*K, 82746*K, 82748*K; M - MN82739*K, 82740*K, 82747*K, 82749*K).

Alouatta guariba - 33 - (U - UFMG1473).

Callithrix penicillata - 46 (M - MCN-M38); 74 (M - MN23794).

Calomys mattevii - 37 (U - MN42843); 44 (F - MN81105*K, 81106*K, 81107*K, 81109*K, 81110*K, 81113*, 81114*, 81115*; M - MN81108*K, 81111*K; U – MN81112*).

Calomys tener - 3 (M - UFMG1608); 12 (F - UFMG2454; M - UFMG2452, 2453); 27 (F - MCN-M1105); 34 (F - MCN-M1089, 1106; M - MCN-M1094); 46 (M - MN42840); 47 (F - MCN-M732); 48 (F - MCN-M728, U- MCN-M727).

Caluromys philander - 7 (M - MDIA43*); 8 (M - MN82751*K);

Cavia aperea - 5 (F - MCN-M1046; M - MDIA52*).

Cerdocyon thous - 43 (F - LG 1167RK); 50 (U – UFMG 3078).

Cerradomys scotti - 5 (M - MDIA24*); 6 (F - MN82753*K; M - MN82752*K); 7 (M - MDIA49*).

Cerradomys subflavus - 3 (U - UFMG1609, 1610, 1611); 5 (M - MDIA51*, 57*); 6 (F - MN82759*K); 7 (F - MDIA16*; M - UFMG2852, 2853; MDIA23*); 9 (F - MN82758*); 11 (M - MCN-M1); 12 (M - UFMG2457, 2458); 22 (F - UFMG1459); 27 (F - MCN-M1075); 35 (M - MZUFV1877, 1923); 45 (M - UFMG1453, 1454); 46 (F - MN42841, MCN-M332; M - MN42844); 48 (M - MCN-M725); 50 (F - UFMG907); 53 (F - MN82754*K, 82757*K; M - MN82755*K, 82756*K).

Cerradomys vivoi - 45 (F - MN82762*, 82763*K, 82764*K, 82765*K; M - MN82760*K, 82761*K, 82766*K); 54 (M - UFMG1458).

Conepatus semistriatus - 19 (M - MCN-M99); 36 (U - MN43924); 46 (U - MN42855).

Dasypus novemcinctus - 3 (U - UFMG3085, 3086);

Dasyprocta leporina -18 (M - UFMG1565)

Didelphis albiventris - 2 (F - MN82769*); 5 (M - MDIA50*); 9 (F - MN82770*K); 33 (F - UFMG1471; M - UFMG1472); 38 (U: UFMG1566); 43 (M - MN82771*); 45 (F - MN82767*); 46 (M - MN42834); 49 (F - MN82772*); 53 (F - MN82768*); 56 (F - UFMG905).

Didelphis aurita - 49 (F - MN82777*); 75 (F - MN82774*, 82775*; M - MN82773*, 82776*).

Euphractus sexcinctus - 15 (U - UFMG1105); 16 (U - UFMG3093); 46 (U - MN42849, 42851, 42852).

Euryoryzomys russatus - 53 (M - MN82778*K); 54 (M - UFMG1457); 72 (M - CC37).

Euryzygomatomys spinosus - 5 (M - MDIA78*; 84*).

Gracilinanus agilis - 2 (F - MN72692*); 3 (U – MCN-M315); 7 (M – MDIA06*; 14*, 19*; F - MDIA15*, UFMG2493, 2494); 9 (M - MN72693*K); 12 (F - UFMG2433, 2434, 2435); 31 (F - UFMG2495); 37 (M - MN42842; U - MN42845); 43 (F - MN82782*K, 82783*K, 82784*K, 82785*K, 82786*K; M - MN82779*K, 82780*K, 82781*K); 45 (F - MN72687*, 72690*, 72691*; M - MN72686*K, 72688*, 72689*; U - UFMG1464); 47 (F - MCN-M734).

Gracilinanus microtarsus - 2 (F - MN72702*K); 6 (F - MN82788*K); 7 (F - MDIA44*); 9 (F - MN82787*K; M - MN72701*K); 60 (U - UFMG1465).

Galea spixii - 34 (U - MCN-M989); 48 (F - MCN-M735, M - MCN-M761).

Guerlinguetus brasiliensis - 49 (F – MN82791*K; M - MN82790*K, 82792*K); 75 (F – MN82789*).

Hydrochoerus hydrochaeris - 71 (U - UFMG1048).

Hylaeamys seuanezi - 72 (M - CC35).

Kerodon rupestris - 13 (U - UFMG1101).

Leopardus wiedi - 50 (U - UFMG3076).

Metachirus nudicaudatus - 7 (F - MDIA12*; M - MDIA13*); 17 (U - UFMG2654, 2655); 54 (F - UFMG1462; M - UFMG1568; U – UFMG1567); 75 (F - MN82847*; M - MN82846*K).

Marmosa paraguayana - 7 (M - UFMG2648); 8 (F - MN82795*K; M - MN82794*K, 82796*K, 82797*K); 9 (M - MN82799*K, 82800*K); 17 (F - UFMG2611; M - UFMG2612, 2613); 30 (F - MCN-M36); 46 (F - MCN-M26); 75 (M - MN82798*).

Marmosa murina - 75 (M - MN82793*K).

Marmosops incanus - 2 (F - MN82812*K, 82814*K, 82815*K; M - MN82813*K); 3 (F - UFMG1607); 5 (M - MDIA69*, 85*); 6 (F - MN82820*K, 82821*, 82822*K, 82823*K); 7 (M - MDIA04*; UFMG2601); 8 (M - MN82808*K, 82809*K, 82810*K); 9 (F - MN82817*K, 82818*K; M - LG596*K, MN82816*K, 82819*K); 11 (F - MCN-M326); 12 (F - UFMG2436, 2440, 2441, 2442; M - UFMG2437, 2438); 14 (U - MN33840, 34426); 17 (F - UFMG2605); 27 (F - MCN-M1078, 1111); 28 (F - UFMG1102); 30 (F - MCN-M46; M - MCN-M318); 31 (U - UFMG2610); 33 (M - UFMG1468, 1469, 1470); 45 (M - MN82801*, 82802*K, 82803*); 49 (F - MN82824*K, 82828*K, 82829*K, 82830*, 82831*, 82835*, 82838*, 82839*K, 82840*K, 82842*, 82843*; M - MN82825*K, 82826*K, 82827*K, 82832*, 82833*, 82834*, 82836*, 82837*, 82841*, 82844*, 82845*); 53 (F - MN82804*; M - MN82805*, 82806*, 82807*K); 60 (M - UFMG1466, 1467).

Monodelphis americana - 9 (M - MN82848*K); 49 (M - MN82849*K, 82850*K).

Monodelphis domestica - 5 (M - MDIA47*; U - MCN-M1042); 6 (F - MN82866*K, 82867*K); 9 (F - MN82863*, 82864*K; M - MN82868*, 82865*K); 12 (F - UFMG2439); 30 (M - MCN-M41); 35 (M – MZUFV1925, 1926); 45 (F - MN82851*, 82852*K, 82856*, 82857*K, 82860*, 82861*, UFMG1463; M - MN82853*K, 82854*, 82855*, 82858*, 82859*, 82862*); 46 (U - MN46588, 46589; F - MCN-M24).

Monodelphis scalops - 5 (M - MDIA86*).

Necromys lasiurus - 5 (M - MDIA53*); 27 (M - MCN-M1079); 30 (F - MCN-M334); 46 (F - MCN-M35).

Nectomys squamipes- 5 (M - MDIA75*); 7 (M - UFMG2984, 2985); 8 (F - MN82881*K; M - MN82880*K, 82882*K); 9 (M - MN82883*K, 82884*K); 24 (M - UFMG1451, 1452); 49 (F - MN82886*K); 53 (F - MN82869*K, 82872*K, 82876*, 82877*; M - MN82870*K, 82871*K, 82873*K, 82874*K, 82875*, 82878*, 82879*); 75 (F - MN82885*K; M - MN82887*K).

Oecomys catherinae - 54 (M - UFMG1455); 72 (M - CC36).

Oligoryzomys nigripes - 5 (F - MDIA60*); 7 (M - MDIA11*); 9 (M - MN82888*K); 12 (F - UFMG2456, 2455); 31 (F - UFMG2743); 33 (F - UFMG1479); 47 (F - MCN-M733).

Oxymycterus dasytrichus - 5 (M - MDIA63*); 54 (F - UFMG1476; M - UFMG1475).

Philander frenatus- 9 (F - MN82889*K, 82890*, 82891*, 82892*).

Phyllomys lamarum - 17 (U - UFMG3016); 33 (M - UFMG1491).

Rhipidomys macrurus - 6 (M - MN82893*K); 12 (F - UFMG2460, 2461, 2462, 2463, 2464, M - UFMG2465), 31 (F - UFMG2934).

Rhipidomys mastacalis - 3 (U - UFMG1605, 1606); 4 (U – MCN-M49); 5 (M - MDIA76*, 77*); 6 (M - MN82896*K); 7 (F - UFMG2926, 2927, 2928, M - UFMG2925, 2929); 9 (M - MN82895*K), 17 (F - UFMG2930); 33 (F - UFMG1450); 46 (F – MN30021, U - MN30015); 49 (F - MN82897*K, 82900*K; M - MN82898*K, 82899*K); 54 (F - UFMG1461; M - UFMG1456, 1460); 73 (F - MN82894*K).

Sapajus robustus - 74 (F - MN23230, 23233, M - MN23228, 23229, 23232, 23234).

Sooretamys angouya - 12 (M - MCN-M1100).

Sylvilagus minensis - 48 (M - MCN-M860); 51 (M - MN82901RK).

Thalpomys lasiotis - 6 (M - MDIA9*).

Thrichomys apereoides - 2 (F - MN82914*K, 82915*K, 82916*K, 82917*, 82921*K, 82922*; M - MN82913*K, 82918*K, 82919*K, 82920*K); 5 (M - MDIA54*, 55*, 56*); 6 (F - MN82932*, 82934*K; M - MN82933*K); 7 (F - UFMG3005, 3006, 3007); 8 (F - MN82908*K, 82910*K, 82912*; M - MN82909*K, 82911*K); 9 (F - MN82923*K, 82927*K, 82928*K; M - MN82924*K, 82925*, 82926*K, 82929*K, 82930*K, 82931*K); 12 (F - UFMG2467, M - UFMG2468, 2469, 2472); 15 (U - UFMG1096); 24 (F - UFMG1489, 1490); 27 (U - MCN-M1065); 28 (M - UFMG1098, 1482, 1486, 1487; MCN-M1044; F - UFMG1480, 1481, 1483, 1484, 1485, 1488); 31 (U - UFMG3009); 35 (U – MZUFV1929, 1930, 1934; F - MZUFV1927; M - MZUFV1928); 44 (F - MN82903*K, 82904*K, 82905*K, 82906*K, 82907*K); 45 (F - MN82902*K); 47 (M - MCN-M762, 763).

Thylamys velutinus - 48 (F - MCN-M724).

Trinomys albispinus - 5 (F - MCN-M1132, M - MCN-M1033, 1131); 10 (MN 73436); 12 (F - UFMG2478, 2479, 2480, M - UFMG2473, 2474, 2475, 2476); 22 (F - UFMG1445, 1446, 1447; M - UFMG1441); 23 (F - UFMG1439, M - UFMG1442, 1448); 27 (F - MCN-M1073, 1076; M - MCN-M1050, 1067, 1068, 1074; U - MCN-M1039, MN73429); 28 (U - UFMG1103, F - MCN-M1036); 45 (M - MN82935*K); 54 (M - UFMG1440); 65 (F - MCN-M972); 66 (F - MCN-M993, 994, 996; M - MCN-M992, 995, 997).

Trinomys setosus - 9 (F - MN82937*K); 12 (M - UFMG2477); 17 (F - UFMG3036, 3037, 3038); 23 (M - UFMG1436); 53 (M - MN82936*K); 54 (F - UFMG1437, 1438, M - UFMG1449); 58 (MNRJ 73409); 60 (U - UFMG1443, 1444).

Wiedomys pyrrhorhinos - 7 (M - MDIA80*); 9 (F - MN82940*K, 82942*K; M - MN82941*K); 11 (F - MCN-M3); 12 (F - UFMG2466); 28 (F - UFMG1100; U - MCN-M1052); 34 (M - MCN-M1054); 43 (F - MN82943*K, 82944*K); 45 (F - MN82938*K, 82939*K, M - UFMG1474).

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