Unexpected mammalian records in the state of Maranhão Ocorrências inusitadas de mamíferos no estado do Maranhão

Evidence about unexpected occurrences of mammals in the state of Maranhão are presented in order to emphasive the transitional aspect of the state. An analysis was made of the geographic distribution area of eleven species of mammals that originally did not include the State and/or did not describe the habitats where the species were found. Results showed the influence of several biomes in the composition of the local mammalian fauna, confirming the State as a transitional area among morphoclimatic domains. There were expansions in the geographic distribution of some species, as well as the record of new habitats and taxa for Maranhão.


INTRODUCTION
The state of Maranhão is geographically located in an area under the influence of three major morphoclimatic domains, the Amazonian in the north, the Caatinga in the northeast and the Cerrado in central Brazil (Ab'saber, 1977).Consequently, the state presents, to a lesser or greater extent, characteristics of all these areas.The vegetation cover, with 14 types (IBGE, 1993), reflects this transitionality between the super-humid and the semi-arid.This, ultimately, would lead to a great biological diversity.Unfortunately, local plant and animal species diversity is poorly known, due to lack of surveys (Oliveira, 1996).This fact, associated with a considerably high level of environmental degradation, is responsible for altering the original biota before it is known.Landsat data showed that about 68% of original cover within Legal Amazon in the state is already altered or lost (Fearnside, 1995).The Cerrado area is also under significant pressure due to its agricultural potential, and special governmental incentives.
Recent surveys being conducted in several areas of the state have shown the presence of several species of mammals in areas and/or habitats from which they were previously unknown.This paper aims to compile data about these unexpected occurrences of mammals in Maranhão, assessing its transitional aspect and importance in mammalian biogeography.

MATERIAL AND METHODS
Data presented include only the unexpected occurrences, by which we mean species presence in habitats and/or areas outside their known distribution area.Species records came from field surveys being conducted in Amazonian and savanna (Cerrado) areas in the state of Maranhão (Oliveira, 1993;Oliveira et al., 2001).Small mammals were trapped by capture-recapture techniques (from 1997 to the present date; >6,000 trap/nights), whereas larger species were recorded by means of direct (visualization) or indirect (skin, skull, other remains) observations.Small mammal species identification was confirmed comparing the voucher specimens collected of each species with those of museum specimens from the collections of Museu de Zoologia da Universidade de São Paulo and Museu Paraense Emílio Goeldi.Collected specimens were deposited at the Mammal Collection of Universidade Estadual do Maranhão.Additionally, data were supplemented with records from the literature and interviews with knowledgeable locals.Information from interviews was used only if they were considered undisputedly correct (after morphological and ecological descriptions of the species, as well as its identification on colored plates).All species listed were either collected (small mammals) or seen (larger species).

RESULTS AND DISCUSSION
Until now, 11 unusual species of mammals were recorded in Maranhão state, most of which from the orders Rodentia and Didelphimorphia (Table 1).Of these, four are exclusively Amazonian, whereas the other three are mostly associated with this biome, although they can also be found in other ecosystems.
Chironectes minimus (water opossum; mucurad'água): this species has a poorly known geographic distribution that does not include Maranhão.In Brazil C. minimus is known for some areas of the Amazon Basin (the Amazon River mouth, including all Amapá state and the lower Tocantins River, and central area, between the Amazon, Madeira and Tapajós Rivers) and the southeast, as well as the southern region (Emmons;Feer, 1997;Eisenberg;Redford, 1999).In Maranhão, it is here recorded for the first time, for the region located between the Pindaré and Zutiua Rivers (Fazenda Mapisa and nearby Santa Luzia) and the area of the Indian Reserves of Alto Turiaçu and Caru (Figure 1).This considerably expands the species' distribution area.Observations were made in black water lakes and clear water streams in pristine/lightly disturbed forest with hilly topography, the kind of area from which most records of this animal come.Gracilinanus agilis (agile gracile mouse opossum; catita): this medium-sized mouse opossum is known to occur mostly in the dryer parts of Brazil.Habitat association is with the mesic areas of the Cerrado biome, that is, gallery forests, but would also include evergreen forests (Emmons;Feer, 1997;Eisenberg;Redford, 1999).In Maranhão, five specimens (two males, three females) were trapped in a heavily logged Amazonian forest near the border with Metachirus nudicaudatus (brown four-eyed opossum; mucura-de-quatro-olhos): the distribution area of this species in Brazil includes the Amazon Basin, Mato Grosso, Goiás, and from the coast of Bahia to northern Paraná (Cabrera, 1957;Emmons;Feer, 1997).There is no specific work dealing with the species' biogeography.The most carefully done maps available do not usually include the state of Maranhão, or do so only marginally (Emmons;Feer, 1997;Eisenberg;Redford, 1999).Therefore, this is the first record of this species in Maranhão (Table 1, Figure 3).Five females were trapped in lowland Amazonian rainforest.One in pristine/lightly disturbed forest with little undergrowth, a kind of habitat that the species seems to favor (Emmons;Feer, 1997), and four in heavily logged forest of the Gurupi area.Another individual, a male, was trapped in the border of a pristine/lightly disturbed forest in the Fazenda Mapisa.The presence of M. nudicaudatus in Maranhão could be expected, as it has been trapped in other relatively nearby areas of Eastern Amazon in Pará -Tucuruí and Capim Rivers in Paragominas (Eisenberg; Redford, 1999; Oliveira unp.data).The traditional exclusion of Maranhão from distribution maps reflects the lack of data both for the species and for the state.
Monodelphis umbristriata (= M. americana) (threestriped short-tailed opossum; catita): there is no agreement regarding the taxonomy and geographic distribution of this species.Gardner (1993) considered M. americana the species with three dorsal stripes found around Belém, Pará and adjacent areas.Conversely, Gomes (1991) assigns this area of Northern Brazil to M. umbristriata, whereas M. americana would be the species that would range from João Pessoa, Paraíba to southeastern Minas Gerais and São Paulo states and northern Paraná.This means that the former is the Amazonian form, whereas the latter is the Atlantic forest species.According to Gomes (1991) and Pine (1976), M. umbristriata is also found in Goiás (Veadeiros, Brasília) and southwest Minas Gerais (Passos).On the other hand, Gardner (1993) and Emmons and Feer (1997) assigned these populations to M. rubida, which, in their scheme, is synonymous with M. umbristriata, the state of Pará (Figure 2).For this area, Eisenberg and Redford (1999) considered only Gracilinanus emiliae, which, in fact, shows some similarities with G. agilis in coloration, but different body size and proportions.Measurements of specimens conform to those of the latter and are clearly different from those of the first.Costa and Patton (2006) reviewing Brazilian marsupial diversity, and its geographic and systematic limits, mention only three species for Brazil, Gracilinanus microtarsus of the Atlantic forest, G. emiliae for Eastern Amazonia, near Belém, and G. agilis of Northeastern Brazil.Thus, this record does not only considerably expand the distribution area of G. agilis, but also registers it for eastern Amazonian forests.with the exclusion of the Belém area population (Eisenberg; Redford, 1999).According to the description presented in Gomes (1991) the specimens from Maranhão would belong to M. umbristriata.In this state records are from areas of pristine/ lightly disturbed Amazonian rainforest of the Gurupi river area, and for a considerably disturbed riverine/secondary forest near Imperatriz (Figure 4), which suggests the species' resilience to disturbances.These areas are about 160 and 350 km away in a straight line to the nearest collecting localities in Pará (Gomes, 1991).In this way, these first records for Maranhão not only significantly expand the species' geographic distribution, but also mention new habitats Dasypus kappleri (greater long-nosed armadillo; tatuquinze-quilos): although Eisenberg and Redford's (1999) generic map included western Maranhão in the species range, Wetzel (1985) was not sure about its presence as known collecting localities were far from the state, whereas Emmons and Feer (1997) considered the Belém area as the eastern most limit for this armadillo.In Maranhão we know of three specimens captured by Ka'apor and Awá-Guajá indians for the Gurupi lowland rainforest area of western Maranhão.Four individuals hunted by local inhabitants (one nearby Santa Luzia, two in Buriticupu, and another in Arame) were reported as coming from pristine/lightly disturbed forest.Three individuals were observed in the same forest type, one nearby Grajaú and two in Fazenda Mapisa (Figure 5).These are the first records for this species in the state.Emmons and Feer (1997), and new records of Dasypus kappleri in the state of Maranhão.
Tolypeutes tricinctus (three-banded armadillo; tatubola): this armadillo, recently rediscovered by scientists (Santos et al., 1994) was originally described as endemic to the Caatinga biome (Fonseca et al., 1994).However, recent records have reported it for areas of deciduous forest in Bahia and savannas (cerrado, sensu stricto) in Maranhão (Table 1, Figure 6), close to areas of semiarid thorny scrub of the Caatinga domain, which the species seems to favor (Silva;Oren, 1993;Fonseca et al., 1994;Oliveira, 1995Oliveira, , 1996)).An animal was observed in São Figure 3. Known geographic range, as proposed by Emmons and Feer (1997), and new records of Metachirus nudicaudatus in the state of Maranhão.
Miguel, in the northeastern part of the State.There, transitional vegetation predominates, with a mosaic of savanna, babassu palm forest and semiarid thorny scrub.The animal was sighted in an area of cerradão (forest savanna).The occurrence of the three-banded armadillo in Maranhão reflects the state's transitionality.In Maranhão, its status was considered as critically endangered or even possibly extinct (Oliveira, 1997).
Figure 6.Known habitat, as proposed by Wetzel (1985), and new records of Tolypeutes tricinctus in the state of Maranhão.
Conepatus semistriatus (hog-nosed skunk; gambá): this skunk is more characteristic, in South America, of open and dry areas and borders of forests.The species is not considered to occur in the Amazon region.However, Oliveira (1996, [20?]) recorded it for disturbed areas and the border of pristine Amazonian rainforest in western Maranhão (Figure 7).Additional records were made for babassu palm forest/secondary forests.We speculate that (a) the species always occurred in the area, but due to lack of studies and surveys its presence has never been properly recorded, or (b) due the degradation of the pristine forest, proper conditions for its establishment in the region were created, and thus it expanded its geographic distribution area.
Coendou koopmani (black dwarf porcupine; cuandupreto): this is a recently described species of small porcupine with a darkened coloration.Its known distribution consists of a narrow strip along the southern margin of the Amazon River from above its confluence with the Madeira River (Island of Tayaúna) until Marajó Island and the Belém region, in Pará (Handley;Pine, 1992).Reports of Ka'apor, Guajajara and Awá-Guajá indians indicated the species' presence in the Indian Reservations of Alto Turiaçu, Caru and Pindaré.Additionally, local residents have reported it for Bom Jardim and Santa Luzia (Figure 8).According to the informants this would be a species of porcupine with little hair and totally dark, which agrees exactly with description of the main characteristics of C. koopmani.This species is distinctly different and smaller than C. prehensilis, the other species it is sympatric with.These records would expand the eastern limit of the black dwarf porcupine's distribution with at least 250 km.There are no data about the species' biology, except that it occurs in lowland terra-firme Amazonian rainforest (Emmons;Feer, 1997), the type of vegetation it is Figure 8. Known geographic range, as proposed by Emmons and Feer (1997), and new records of Coendou koopmani in the state of Maranhão.Peru and Ecuador (Eisenberg;Redford, 1999), while others also include a narrow strip along the southem margin of the Amazon River and the area around Belém, Pará (Emmons;Feer, 1997).In any event, this bamboo rat is most commonly associated with the western Amazonian faunal assemblage.In Maranhão specimens were collected in Buriticupu, Grajaú, Lago da Pedra, Lago Verde of São Mateus municipality and Palmeiral (Silva Jr.;Nunes, 2000).New records indicated the presence of bamboo rats in the localities of São José das Verdades, Fazenda Lagoa Nova and the nearby city of Lago Verde (Figure 10).Habitats included Amazonian terra-firme lightly, moderately or highly disturbed forests associated or not with babassu palm forests (Table 1).These habitats are different from those of bamboo patches and dense riverine vegetation, typically described for the species (Emmons, 1981;Silva Jr.;Nunes, 2000).Taking into account the distribution presented by Emmons and Feer (1997), the collecting localities were at least 500 km apart, besides being in previously unrecorded habitat types (Silva Jr.;Nunes, 2000), as was also observed for Echimys chrysurus (Oliveira;Mesquita, 1998).
Figure 10.Known geographic range of and habitat, as proposed by Emmons and Feer (1997), and new records of Dactylomys dactilynus in the state of Maranhão.
reported from in Maranhão.In this state it is found in both pristine/lightly disturbed as well as in considerably disturbed areas with babassu palm forests (Table 1).The latter would consist a new habitat for this porcupine.
Kerodon rupestris (rock cavy; mocó): the geographic distribution of this rodent goes from eastern Piauí and remaining states of the Brazilian northeast (except Maranhão) to northeastern Minas Gerais (Cabrera, 1957;Nowak, 1991).The rock cavy is considered endemic to the Caatinga domain (Willig;Mares, 1989).According to Oliveira (1993), the species' occurrence has been recorded in the savannas (cerrado, sensu stricto) of central-west Maranhão, thus expanding its distribution and habitat.New observations indicated the presence of K. rupestris in four new localities along the Parnaíba River, two on the left bank (Maranhão) and two on the right bank (Piauí).All observations were made in rocky environments.Reports of locals also confirmed the preference of the species for this habitat type.Inhabitants of São Miguel also mentioned the presence of K. rupestris in the region of the middle/lower Parnaíba River, although this remains to be confirmed.This animal is hunted for food in all these localities.Figure 9 shows all records of K. rupestris in this region.Dactylomys dactylinus (Amazon bamboo rat; ratotoró; rato-do-bambu): the distribution of this Echimyidae is confusing.Some authors restrict it to the western portion of the Brazilian Amazon and adjacent areas in Colombia, Echimys chrysurus (white-faced tree rat; rato-estrela): originally described for the Guianas and Amazon Basin east of the Negro and Xingu Rivers (Cabrera, 1957;Emmons ;Feer, 1997;Eisenberg;Redford, 1999), this arboreal rodent has been captured in an ecological tension area, whose vegetation is a mix of deciduous forest and savanna (IBGE, 1993), with the physiognomy of the latter (Oliveira;Mesquita, 1998), besides pristine/lightly disturbed Amazonian rainforest as well as considerably disturbed forest associated with babassu palm grooves, besides typical Amazonian forests of the Gurupi area (Table 1, Figure 11).Its presence in the riverine forests of northeastern Maranhão, not only expands the distribution of the white-faced tree rat (about 500 km), but also records it for new habitat, because it was previously considered to be restricted to multistratal mature Amazonian rainforest (Emmons;Feer, 1997;Oliveira;Mesquita, 1998;Eisenberg;Redford, 1999).This is an evidence of the ecotone status of the state of Maranhão.number of unexpected species of mammals will certainly rise, as more areas are properly sampled.

CONCLUSIONS
Results showed that Maranhão presented characteristics of an ecotone state, representing a key area for a better understanding of the biogeography of Neotropical mammals, especially Amazonian; the use of mammals to verify the transitionality proved efficient; the majority of the lack of information regarding the biogeography of mammals in Brazil and, especially, in Maranhão is a result of lack of studies/surveys in this area, which makes the State less diverse and the group less known.This idea is congruent with the discussions by Vivo (1996) and Silva Jr. (1998) about this issue; and Maranhão does not have a faunal assemblage typical of a single biome, but is rather a mix of ecosystems, which would increase its biodiversity, and thus make the State very important for biological conservation, despite its high levels of habitat degradation.
Data presented expanded the distribution area for five species (45,4%) inside their own biome, while the remaining six species (54,5%) not only expanded their geographic area, but were also recorded for new habitats.These findings suggest that the state of Maranhão is indeed a transitional area where the Amazonian domain assemblage gives way to that of the dry savannas (Cerrado), with an additional influence of the semiarid thorny scrub of the Caatinga.Similar results attesting the transitionality of the state were observed for the assemblages of birds, Euglossini bees and phlebotome flies in Maranhão (Hellmayr, 1929;Oren, 1988;Rebêlo, 1995;Rebêlo;Silva, 1999;Rebêlo;Oliveira, 2000;Rebêlo et al., 2000;Silva Jr., unp. data).The

Figure 2 .
Figure2.Known geographic range, as proposed byEmmons and Feer (1997), and new records of Gracilinanus agilis in the state of Maranhão.

Figure 1 .
Figure 1.Known geographic range, as proposed by Emmons and Feer (1997), and new records of Chironectes minimus in the state of Maranhão.

Figure 4 .
Figure 4. Geographic range, as proposed by Emmons and Feer (1997), and new records of Monodelphis umbristriata (= M. americana) in the state of Maranhão.

Figure 5 .
Figure5.New geographic range, as proposed byEmmons and Feer (1997), and new records of Dasypus kappleri in the state of Maranhão.

Figure 7 .
Figure 7. Known habitat, as proposed by Emmons and Feer (1997), and new records of Conepatus semistriatus in the state of Maranhão.

Figure 9 .
Figure 9. Known distribution, as proposed by Mares and Ojeda (1982), and new records of Kerodon rupestris in the state of Maranhão.

Figure 11 .
Figure 11.Known distribution, as proposed by Emmons and Feer (1997), and new records of Echimys chrysurus in the state of Maranhão.

Table 1 .
Unexpected mammalian records in the state of Maranhão.

Table 1 .
Unexpected mammalian records in the state of Maranhão.(finished)