SMALL MAMMALS OF CHAPADA DOS VEADEIROS NATIONAL PARK ( CERRADO OF CENTRAL BRAZIL ) : ECOLOGIC , KARYOLOGIC , AND TAXONOMIC CONSIDERATIONS

This work is based on a survey of small mammals carried out in the Chapada dos Veadeiros National Park, a natural reserve located in the mountains of the Planalto Central Goiano in the Cerrado of Central Brazil. The 227 specimens collected represented six marsupial and 13 rodent species. Taxonomic, karyologic, and ecologic considerations are present and discussed in the present work. Our data reflected the faunal heterogeneity with respect to both elevation and vegetation because only eight of the 19 species were collected at both high and low elevations. The composition of the small mammal fauna of the park is influenced by predominance of forest formations at low elevations and cerrado with rupestrian areas at high elevations. Presence of endemic species and one undescribed demonstrated that the cerrado has an endemic fauna and a little known diversity of small mammals.


INTRODUCTION
The cerrado is the most extensive openvegetation biome of South America and one of the largest savanna-forest complexes in the world.With a core area spanning over 1.8-2 million km 2 on the Brazilian plateau, the cerrado is located in the middle portion of an open-vegetation belt between the Argentinean-Paraguayan Chaco and the caatinga of northeastern Brazil.This open-vegetation belt separates two major mesophytic biomes, the Atlantic rainforest and the Amazonian rainforest.Enclaves of typical cerrado physiognomy occur within other biomes.At its core area, the cerrado is characterized by an often well-delimited mosaic of vegetation types with abundant ecological islands and corridors, forming a savanna-forest complex (Eiten, 1972(Eiten, , 1983)).
The orders Rodentia and Didelphimorphia are the major components of the cerrado mammalian fauna (Redford & Fonseca, 1986).Given the degree of physiognomical complexity of the biome, it is natural that several studies have been devoted to the description of the small mammal composition associated with habitat heterogeneity.These studies primarily center on differences between areas of open vegetation and gallery forest (Henriques & Alho, 1981;Fonseca & Redford, 1984;Mares et al., 1986Mares et al., , 1989;;Marinho Filho et al., 1994;Bonvicino et al., 1996a).
In this paper we present a taxonomic account of the species collected at the Chapada dos Veadeiros National Park in the cerrado of central Brazil.We report on part of the diversity of small mammals of the cerrado and, due to the lack of previous taxonomic studies, we discuss problems of species identification.Finally, we consider some simple ecological and geographical patterns.

Study site and sampling design
Small mammals were sampled in three areas in the Chapada dos Veadeiros National Park (Fig. 1) representing most of its vegetation and elevation diversity.We followed Eiten (1972Eiten ( , 1983) ) for identification and description of vegetation types.The park is located in a mountainous region, the Planalto Central Goiano (Radam-Brasil, 1983) that include the highest peak of Goiás State (Pouso Alto, with 1,784 m).Area 1 was sampled in August 1996 and areas 2 and 3 in November 1996.Sherman and Tomahawk traps were spaced 15-20 m on ground line transects.
Area 1 (A1 -14 o 04'S, 47 o 45'W, near Morro do Chapéu, 65 km SSW of Cavalcante), whose collecting elevation ranged from 550 to 740 m, is in the lowest part of the park.A1 is a forest formation domain with extensive gallery forests bordered by cerradão (an evergreen vegetation with few deciduous trees but floristically different from semideciduous forest).A total of 991 trap-nights were spent in gallery forest (GF), cerradão (CD), cerrado rupestre (CR: thinly wooded savanna vegetation with rock outcrops), cerrado sensu stricto (CE: wooded savanna), and campo úmido (CU: a mesic grassland).Area 2 (A2 -14 o 01'S, 47 o 31'W, near Pouso Alto, 14 km NNW of Alto Paraíso), in the highest part of the park between 1,300 and 1,500 m of altitude, is a domain of open vegetation formations with extensive areas of cerrado rupestre and natural grass fields.A total of 1,208 trap nights were spent in GF, CE, CR, and CU.Area 3 (A3 -14 o 07'S, 47 o 41'W, near Morro da Baleia, 20 km W of Alto Paraíso), which included collecting altitudes ranging from 1,000 to 1,200 m, is a domain of open vegetation formations with extensive areas of vereda (VE: wet headwater prairies with palms) and natural fields.A total of 466 trap-nights were placed in GF, campo cerrado (CC: scarcely wooded savanna), and VE.
Chromosome preparations of rodent specimens were obtained from bone marrow cultures in RPMI 1640, 20% fetal calf serum, ethidium bromide (5 µg/ ml), and colchicine (10 -6 M) for 2 h.The abbreviation FN refers to autosome fundamental number.Skins and skulls are deposited in the mammal collection of the Museu Nacional (MN, Universidade Federal do Rio de Janeiro, Brazil).Collected specimens are listed in the species account; the abbreviation CRB preceding field number digits stands for C. R. Bonvicino.External measurements were obtained from collected adult specimens.Measurements (in millimeters) taken from adult specimens were head/body length (HB), tail length (T), feet length, including claws (F), internal length of the ear (E), and weight, in grams (W).
Ecological notes and reproduction: a single pregnant female (six embryos) collected in cerrado sensu stricto at the edge of gallery forest (area A1, August).

Specimen collected: MN46514 Micoureus demerarae (Thomas, 1905)
Taxonomy: M. demerarae, as recognized by Gardner (1993), includes several forms previously accepted as valid species or subspecies of the Marmosa cinerea group (Tate, 1933).M. demerarae is probably a composite, and Patton et al. (2000) regarded the Atlantic Forest populations as a distinct taxon (M.limae); however, Gardner (1993) treated M. limae and M. paraguayanus as synonymous with M. demerarae.The assignment of the Micoureus population in Chapada dos Veadeiros National Park (PNCV) to M. demerarae is provisional, as a more comprehensive analysis of the status of this genus is needed.
Ecological notes and reproduction: six individuals collected, three in gallery forest, two in cerrado sensu stricto and 1 in cerrado rupestre (area A1).Females were not pregnant or carrying pouched young (August).
Distribution: Uruguay, Paraguay, Argentina, Bolivia, and NE and C Brazil, in cerrado, caatinga, chaco, and the Pantanal (Hershkovitz, 1992); disjunct distribution in Peru and Colombia may represent another taxon (see above).

Monodelphis domestica (Wagner, 1842)
Taxonomy: M. domestica is the only name used for the majority of gray short-tailed opossum populations, including all those in the cerrado.An isolate population in Marajó, an island in the delta of the Amazon river, Amazon State, is taxonomically controversial, being regarded as a distinct species by some authors (M.maraxina; see Pine, 1979;Gardner, 1993).
Distribution: known only in the cerrado of central Brazil (Lemos et al., 2000).
Ecological notes: A single individual collected in gallery forest (area A2).

Thylamys velutinus (Wagner, 1842)
Taxonomy: T. velutinus is the only species of Thylamys occurring in the cerrado of central Brazil (Palma, 1995).Although Gardner (1993) synonymized T. karimii with T. pusillus, Palma (1995) presented morphological arguments for the inclusion of T. karimii under T. velutinus, and restricted the distribution of T. pusillus to Paraguay, Bolivia, and Argentina.The characters of the single captured specimen match those given by Tate (1933) and Palma (1995).
Ecological notes: A single individual collected in campo úmido, at the edge of gallery forest (area A2).
Ecological notes and reproduction: three individuals collected in cerrado rupestre (area A2).One pregnant female (one embryo) was collected in November.
Distribution: NE and C Brazil, in cerrado of Tocantins, Goiás, and Minas Gerais States.
Distribution: S of the Amazon river, C and N Brazil (Federal District, Minas Gerais, Goiás, Tocantins, Maranhão and Pará), in cerrado and the Amazon Forest (Weksler et al., 2001).
Ecological notes and reproduction: 32 individuals collected, 27 in gallery forest, 3 in cerradão, and 2 in cerrado sensu stricto on the edge of gallery forest (area A1).Five pregnant females were collected in August (2-3 embryos each).
Distribution: E Magdalena river basin in Colombia, throughout Venezuela (high and median Orinoco river basin), Peru (Ucayali river basin), Paraguay (Paraguay river basin), and Brazil (in the Paraguay and Amazons river basins; Bonvicino, 1994).
Ecological notes and reproduction: 11 individuals collected in gallery forest and vereda, always near water streams (areas A1, A2, and A3).Females were not pregnant (August and November).
Ecological notes and reproduction: 2 individuals collected in vereda (area A3).Females were not pregnant (November).
Distribution: Paraguay, Peru, southern Venezuela, Guyana, French Guyana, Suriname, and central and northern Brazil in the cerrado and Amazon Forest (Musser & Carleton, 1993).
Ecological notes and reproduction: 11 individuals collected, 9 in gallery forest, 1 in cerradão, and 1 in cerrado sensu stricto (areas A1 and A2).One pregnant female was collected in August (3 embryos) and one in November (4 embryos).
Distribution: endemic to the cerrado of C Brazil (Minas Gerais and Goiás States).
Ecological notes and reproduction: seven individuals collected, three in gallery forest, two in cerradão, one in cerrado sensu stricto on the edge of gallery forest, and one in campo úmido on the edge of gallery forest (A1).Females were not pregnant (August).

Oryzomys scotti Langguth and Bonvicino, 2002
Taxonomy and karyotype: this taxon is the most common species of the Oryzomys subflavus species group.It differs from the other taxa of the Oryzomys subflavus species group in its smaller body size, proportionally larger ear, lighter pelage coloration, and the presence of an alisphenoid strut.It differs from other cerrado Oryzomys species (not belonging to O. subflavus group) by its long incisive foramen, and absence of well-defined limits between the ventral and dorsal coloration.Karyologic analysis showed 2n = 58, FN = 72 (Fig. 2F).
Distribution: endemic in the cerrado of C Brazil (Minas Gerais, Goiás, and Tocantins states).
Ecological notes and reproduction: 12 individuals collected, 6 in cerrado sensu stricto, 2 in campo úmido on the edge of cerrado sensu stricto, 3 in open gallery forest with bamboo trees, and 1 in cerradão on the edge of cerrado sensu stricto (area A1).Two pregnant females were collected in August (3 embryos each).

Oligoryzomys rupestris Weksler & Bonvicino, 2005
Taxonomy and karyotype: this is another undescribed Oligoryzomys species with a different chromosome complement from all other members thus far described of that species, and presenting one of the lowest diploid numbers in this genus.Karyologic analysis showed 2n = 46, FN = 52 (Fig. 2H).A similar karyotype was previously attributed to Oligoryzomys sp.1 (Silva & Yonenaga-Yassuda, 1997).
Distribution: endemic to high altitude areas in the cerrado of C Brazil (Minas Gerais, Bahia, and Goiás states).
Ecological notes and reproduction: 9 individuals collected in cerrado rupestre or on the edge of this vegetation (area A2).Females were not pregnant (November).

Oxymycterus delator Thomas, 1903
Taxonomy and karyotype: Oxymycterus specimens of the cerrado of C Brazil have been traditionally identified as O. roberti (Hershkovitz, 1994).However, a taxonomic revision of the genus (Oliveira, 1998) showed that cerrado populations are included in O. delator, a species that was formerly restricted to Paraguay, and that O. roberti has restricted distribution in S Goiás and Minas Gerais.Karyologic analyses showed 2n = 54, FN = 62 (Fig. 2J).All species of this genus (sensu Hershkovitz, 1998) share the same karyotype.Distribution: Paraguay and C Brazil, in the cerrado and chaco (Oliveira, 1998).
Ecological notes and reproduction: seven individuals collected, three in cerrado sensu stricto, two in campo úmido, one in gallery forest, and one in cerrado rupestre (areas A1 and A2).Females were not pregnant (August and November).
Although our collecting methodology was not intended to produce quantitative data for analyzing differences of the small mammal structure and composition associated with habitat heterogeneity, our qualitative results indicated a marked compositional difference between different phytophysiognomies that has been extensively documented in previous studies (e.g., Mello & Moojen, 1979;Henriques & Alho, 1981;Fonseca & Redford, 1984;Alho et al., 1986;Mares et al., 1986Mares et al., , 1989;;Bonvicino et al., 1996a).Seven species were predominantly found in gallery forest (Didelphis albiventris, Micoureus demerarae, Monodelphis umbristriata, Proechimys roberti, Nectomys rattus, Oryzomys megacephalus, and Oryzomys lamia), three in cerrado rupestre (Galea cf.flavidens, Thrichomys sp., and Oligoryzomys sp. 2) and three in vereda and campo úmido (Oxymycterus delator, Pseudoryzomys simplex, and Thylamys velutinus).Six species were extensively distributed throughout cerrado habitats but three of them were not found in gallery forest (Oryzomys scotti, Necromys lasiurus, and Gracilinanus agilis) while the other three occurred in this vegetation (Monodelphis domestica, Oligoryzomys sp.1, and Calomys expulsus).With the exception of very few cases each species was captured in the same habitat as recorded in previous studies except for very few cases, which is probably due to the small sample size of some taxa.Our data also showed the heterogeneity of cerrado small mammal fauna across elevations since only eight of the 19 species were collected at both high and low elevations.The extensive areas of forest formations at low elevations and of cerrado rupestre at high elevations are probably the main factor influencing the compositional heterogeneity of the small mammals from these two areas of Chapada dos Veadeiros National Park.
Several authors have stressed the importance of gallery forest in boosting the diversity of the cerrado non-volant mammal fauna.This is because such areas are extensions or corridors of Amazonian and Atlantic forests into cerrado and, therefore, enable species adapted to these mesophytic habitats to inhabit open vegetation in the cerrado biome (Fonseca & Redford, 1984;Redford & Fonseca, 1986;Mares et al., 1986;Marinho-Filho, 1994).Our data is a further indication of the importance of gallery forest in housing a large parcel of cerrado diversity.Nevertheless, of the 19 species collected in the park, only 4, which are mesophyticadapted species (Nectomys rattus, Oryzomys megacephalus, Proechimys roberti and Micoureus demerarae), were distributed throughout the gallery forest of the cerrado and the Amazon forest.Other species occurring in the park have been listed as being present in the Atlantic or Amazon forests but, as mentioned previously, this was done without adequate taxonomic criteria.In addition, some scale factors account for erroneous conclusions.Thus, major biomes have been delimitated without considering either the mosaic transitional areas between them or, in the case of forested biomes, enclaves of cerrado vegetation types within them.
The data presented in the present work only allow hypotheses that involve historical and ecological factors to explain the present cerrado.To explain the small mammal diversity of the cerrado requires hypotheses based on more rigorous taxonomic studies of the cerrado taxa, further research on delimitation of their distribution in the vegetation mosaic of the cerrado, as well as comparisons with taxa found in extra-core cerrado locations.The importance of gallery forest in the formation of present cerrado mammalian fauna is well established.Probably equally important, as shown by species currently inhabiting only these environments, is the open vegetation belt composed of caatinga, cerrado, and chaco.Hypotheses relative to the specific process by which fauna in different areas of the cerrado, such as the high altitude sites that appear to contain similar endemic fauna not found at lower altitudes, are material for future research.Suggested sites for carrying out such investigations are the Planalto Central Goiano of the Brazilian Plateau (Pouso Alto in PNCV, in Serra Santana) and the Planalto do Espinhaço mountains of Eastern Brazil (Pico das Almas, Bahia, and Serra do Cipó, Minas Gerais, Fig. 2) where Oligoryzomys sp. 2 has also been collected (Silva & Yonenaga-Yassuda, 1997).