D:\docs\Chiroptera Neotropical

Chiroptera Neotropical, 9(1-2), December 2003

REFERENCIAS Barquez R. M. 1987. Los murciélagos de Argentina. Facultad de Ciencias Naturales e Instituto Miguel Lillo, Universidad Nacional de Tucumán, Argentina. Doctoral Thesis. 525 pp. Barquez R. M., M. A. Mares & J. K. Braun. 1999. The Bats of Argentina. Special Publications. Museum of Texas Tech University. 275 pp. Uieda W. 2000. A review of complete albinism in bats with five new cases from Brazil. Acta Chiropterologica 2: 97-105.

BATS FROM THE CITY OF BELO HORIZONTE, MINAS GERAIS, SOUTHEASTERN BRAZIL Fernando Araujo Perini Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, Pampulha, Belo Horizonte, MG, Brazil, [email protected] Valéria da Cunha Tavares American Museum of Natural History, Central Park West at 79th Street, 10024, New York City, New York, USA, [email protected] Cecília Maria Dias Nascimento Faculdade Tecsoma, Rua Orlando Batista Ulhôa, 380, Bairro Vila Alvorada, Paracatu, MG, Brazil, [email protected] Abstract We report a list of species of bats occurring in Belo Horizonte, the capital of Minas Gerais state, southeastern Brazil. We recorded 16 species belonging to three families,Vespertilionidae, Molossidae, and Phyllostomidae. Artibeus lituratus was by far the most abundant species, representing 70% of the captures. Remnants of native vegetation in urban parks as well as the urban arborization which frequently includes chiropterocoric or chiropterophilous species, as well as the illumination that attracts a great range of insects and houses and buildings also attract and maintain a quite rich assemblage of bats living in Belo Horizonte. Roost search seems to be the most effective method to find mollosids that would not be recorded by mist netting. Key words: Chiroptera, urban environmet, urban parks Belo Horizonte is the, and one of the largest Brazilian cities, with more than 2 million inhabitants. The city

lies on the foothills of Serra do Curral (852 m), one of the southeastern branches of the Serra do Espinhaço, a mountainous range which extends from Minas Gerais state northward to Bahia. Belo Horizonte is located in a transitional area between the Cerrado and Atlantic rain forest, and has a number of parks and green areas, with mixed elements from both native remnants of vegetation and exotic plants. Despite the size of the city (the 3rd largest population in Brazil), there is no published study on its bat fauna. This is also surprising given the increasing interest on problems related to the presence of urban bat fauna in big cities due, for example, to public health problems (Almeida et al. 1994, Bredt & Uieda 1996, Bredt et al. 1996, Uieda 1995¸ dos Reis et al. 2002). Here we report a list of species of bats that occur in the city of Belo Horizonte, recorded between the years of 1994 and 2001 through captures in some urban parks, and sporadic surveys in the city. The three parks more intensively sampled (all in the northeastern region of the city) were: The Estação Ecológica of the Universidade Federal de Minas Gerais (EEUFMG), the Fundação Zoobotânica de Minas Gerais, and the Parque Fazenda Lagoa do Nado. During the year of 1995 we also worked for the Prefecture Zoonosis Control Service (Serviço de Controle de Zoonoses SCZ, Distrito Sanitário/Pampulha - DISAP) dealing with complaints about disturbances caused by bats in residences. Over this period, residents in the city used to call the Prefecture and registered their complaints; later, at least one of us usually would go in situ and try to resolve the problem. This service has resulted in some additional new records of bat species in Belo Horizonte. The EEUFMG is a small reserve of dry secondary forest and marshes, administrated by the Federal University of Minas Gerais for environmental education programs and research of undergraduate and graduate students. The Fundação Zoobotânica harbors the city zoo, and comprises large green areas and patches of Cerrado. The Parque Lagoa do Nado is a secondary growth dry forest, with many exotic trees and Eucalyptus. Through this period, bats were captured more intensively with mist-nets and hand-nets. Hand nets were used to capturing bats in artificial roosts, such as house cellars, dilatation crevices in buildings, and inside houses. Some bats captured during this period were sent to rabies examination. We recorded 16 species of bats in Belo Horizonte, belonging to three families (Vespertilionidae, Molossidae, and Phyllostomidae, Table 1). In the park areas, the phyllostomid bat Artibeus lituratus was the most abundant species of bat, representing, 70 % of captures in EEUFMG area. This bat is commonly seen

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flying across streets in Belo Horizonte, close to or in trees used for ornamentation of sidewalks, and a frequent visitor of backyards and house gardens in the city. Artibeus lituratus is a frequent bat in urban environments (Muller & Reis 1992, Sazima et al. 1994, Bredt & Uieda 1996). The abundance of A. lituratus and the occurrence of other frugivorous bats in the city could be related to the tree species used in arborization of sidewalks in the city and in parks. A great number of trees in Belo Horizonte seem to attract both fruit and nectar-feeding bats because they supply shelter and food for them. A similar situation occurs in the city of Brasília, Federal District (Rodrigues et al. 1994). In Belo Horizonte, plant species such as Terminalia catapa, Licania tomentosa, and species of Ficus, for example, attract fruit bats, and species such as Lafoensia glyptocarpa, and from the genus Bauhinia, attract nectar-feeding bats. We often observed individuals of Glossophaga soricina visiting flowers of Lafoensia glyptocarpa in a very busy street downtown, in the early evening. Phyllostomus discolor is another species that may benefit from both chiropterophylous and chiropterocoric plant species in the city. Additionally, trees with closed canopies can be used as temporary or permanent roosting places, and trees such as Magnolias, commonly seen in the city, function as permanent roosts for the bats. Artibeus jamaicensis is much less abundant than A. lituratus in the city. We captured, for example, a single

individual of A. jamaicensis from January to May 1995 in the EEUFMG, and 23 individuals of A. lituratus. The phyllostomids Plathyrrhinus lineatus and Sturnira lilium are the most frequently captured bats in Belo Horizonte, after A. lituratus. Carollia perspicillata was not frequently captured/observed in Belo Horizonte, a fact that seems not to be explained by the lack of resources for this bat in the city. Carollia perspicillata is generally abundant in reserves of southeastern Brazil, and feeds mainly in undergrowth fruits, like Piper and Solanum (Marinho-Filho 1991, Aguiar 1994, Pedro & Passos 1995, Pedro & Taddei 1997, Tavares 1999), which are widespread in the EEUFMG. This species is frequent in surveys of forested areas in Minas Gerais, such as the Caratinga reserve and the Parque Estadual do Rio Doce (Aguiar 1994, Tavares 1999), which contrasts with its low abundance in the city. Pygoderma bilobatum is usually found in very low densities, but may be locally common in some areas (Faria 1997). It was captured only occasionally in the EEUFMG. We recorded a single individual of the common vampire bat (Desmodus rotundus) in the city, which was negative for the rabies virus test. This individual was captured in EEUFMG, in the vicinity of a stable of the local police. Although not frequent, reports of aggressive bites by vampire bats are known in Belo Horizonte (Uieda 1995), especially in the suburban region of the city, where it is common to keep cattle and horses near residences.

Figure 1. Location of Minas Gerais in Brazil, and of the city of Belo Horizonte, MG Page 170


Some other characteristics of Brazilian cities are likely to attract some bat species. Urban illumination attracts many nocturnal insects, which may be preyed by insectivorous bats (Silva et al. 1996). We observed aerial insectivorous bats such as Molossus molossus hunting at dawn in many points of the city, and heard Eumops in flight. Molossid bats are underrepresented in surveys using mist nets at ground level in natural environments (Handley 1967, Pedro & Taddei, 1997, Bernard 2001). Bernard (2001), recognized a separate guild – “high flyers” - for molossids in Central Amazon. We believe that urban molossids repeat the “high flyer” behavior as city dwellers, and it is very probable that more species of molossids that we were unable to catch with mist-nets occur in the city. Molossid bats seem to be able to adapt to urban environments (Bredt & Uieda 1996) perhaps due to suitability of food resources, and for their apparently easy adaptation to artificial roosts. Therefore, it seems that the best way to capture molossids in cities is through roost search. Lasiurus cinereus, Tadarida brasiliensis, and Nyctinomops laticaudatus were recorded only in residences. Individuals of these three species were found in different residences in the Northeast of Belo Horizonte, in a region known as “Pampulha”. A single individual of Lasiurus cinereus was roosting inside a dog’s house; one individual of N. ladicaudatus was

received in a jar with alcohol after being bit with a stick while lying in the floor of a house, and another single individual of Tadarida brasiliensis was lying in a curtain inside a third house. The main reasons of complaints of residents in Belo Horizonte, and the bats associated with those complaints were (from the most to the less frequent complaint): bats in house gardens and backyards (Artibeus liturarus, Sturnira lilium, Glossophaga soricina, Plathyrrhinus lineatus), bat colonies in roofs and house cellars (Artibeus lituratus, Glossophaga soricina, Molossus molossus), bats in the external part of buildings, such as the space between buildings (Artibeus lituratus, Glossophaga soricina, Plathyrrhinus lineatus), in the streets (Artibeus lituratus), inside houses (Artibeus lituratus, Molossus molossus, Glossophaga soricina, Tadarida brasiliensis, Myotis nigricans), and in basements (Glossophaga soricina). The presence of fruit bats generally disturbs for the fear caused in the population and for the feces dropped by them, which may stick into walls and floors of the houses. Dropping of feces is also associated to the presence of insect-feeding bats, together with noise and bad smell, especially in the case of large colonies such as of Molossus molossus in roofs. Species of trees planted in backyards or gardens (such as mango and banana trees, among others), are a source of food resources that most commonly attract fruit bats to these places.

Table 1. Species of bats captured in the city of Belo Horizonte, MG.

Species

E.E.UFMG

Lagoa do Nado Fundação Zoobotânica Residences

Artibeus lituratus

X

X

X

Artibeus jamaicensis

X

X

X

Platyrrhinus lineatus

X

X

X

Sturnira lilium

X

X

X

X

Pygoderma bilabiatum

X

Glossophaga soricina

X

X

X

X

Phyllostomus discolor

X

X

X

Carollia perspicillata

X

Desmodus rotundus

X

Eptesicus brasiliensis

X

X X

Histiotus velatus Myotis nigricans

X X

X

Lasiurus cinereus Molossus molossus

X X

X

X

Nyctinomops laticaudatus

X

Tadarida brasiliensis

X Page 171


The use of fruit trees and trees that offer nectar for bats in sidewalks, allied with the maintenance of encroaches of preserved areas inside big cities in Brazil, such as Belo Horizonte, are factors that enable the maintenance of a relatively rich array of fruit bats in urban environments. However, as pointed out by Silva et al. (1996) adequate planning of urban tree planting is necessary to prevent disturbance caused by fruit bats in Brazilian cities. Silva et al. (1996) suggested that trees that attract bats should be restrict to parks and green areas. We agree with Silva et al. (1996) and believe that lowering the problems caused by bats in cities is a good strategy to prevent the bad image of bats, as well as to prevent more serious problems related to public health. We know more species may occur in the city. Inventories in other urban parks and other significant patches of forested areas remain to be investigated since we concentrated our surveys in the north-eastern region of Belo Horizonte. It is important to verify, as already observed for other large cities in southeastern Brazil (Bredt & Uieda 1996, Silva et al. 1996, Reis et al. 1998), that records of bats in houses and buildings appear to be a very important source of data for knowing the bat fauna of urban areas.

R.Rodrigues, M.Yoshizawa, M. S. Silva.,N. M. S.Harmani, P. N. T. Massunaga, S. P. Bürer, V. A. R. Potro & W.Uieda. 1996. Morcegos em áreas urbanas e rurais: manual de manejo e controle. Brasília, Fundação Nacional de Saúde, Ministério da Saúde. Faria D. 1997. Reports on the diet and reproduction of the Ipanema fruit bat, Pygoderma bilabiatum in a Brazilian forest fragment. Chiroptera Neotropical 3: 65-66. Handley Jr. C. O. 1967. Bats of the canopy of an Amazonian Forest. Atas do Simpósio sobre a biota Amazônica (Zool.) 5: 211-215. Marinho-Filho J. S. 1991. The coexistence of two frugivorous bat species and the phenology of their food plants in Brazil. Journal of Tropical Ecology 7: 59-67. Muller M. F. & N. R. Reis. 1992. Partição de recursos alimentares entre quatro espécies de morcegos frugívoros (Chiroptera, Phyllostomidae). Revista Brasileira de Zoologia 9: 345- 355.

ACKNOWLEDGMENTS

Pedro W. A. & F. C. Passos. 1995. Occurence and food habits of some bat species from the Linhares Forest Reserve, Espirito Santo, Brazil. Bat Research News 36: 1-2.

We thank C. M. Capistrano for the invitation for working in the DISAP program, and for financial support for one of us (V. T.). We are grateful to A. C. Oliveira Júnior, R. Franco, and W. Camisassa for the participation in fieldwork, and in the DISAP program.

Pedro W. A. & V. A. Taddei. 1997. Taxonomic assemblage of bats from Panga reserve, southeastern Brazil: abundance patterns and trophic relations in the Phyllostomidae (Chiroptera). Boletim do Museu de Biologia Mello Leitão (N. ser.) 6: 3-21.

REFERENCES

Reis N. R., A. L. Peracchi , I. P. Lima , M. L. Sekiama & M. S. Rocha. 1998. Updated list of the Chiroptera of the city of Londrina, Paraná, Brazil. Chiroptera Neotropical 4(2): 96-98.

Aguiar L. M. S. 1994. Comunidades de Chiroptera em três áreas de Mata Atlântica em diferentes estádios de sucessão - Estação Biológica de Caratinga, Minas Gerais. MSc. thesis. Belo Horizonte, Universidade Federal de Minas Gerais. Almeida M. F, E. A. C.Aguiar, L.F.A. Martorelli & M. M. S. Silva. 1994. Diagnóstico laboratorial de raiva em quirópteros realizados em área metropolitana na Região Sudeste do Brasil. Revista de Saúde Pública 28: 341-344. Bernard E. 2001. Vertical stratification of bat communities in primary forests of Central Amazon, Brazil. Journal of Tropical Ecology 17: 115-126. Bredt A. & W. Uieda. 1996. Bats from urban and rural environments of Distrito Federal, mid-western Brazil. Chiroptera Neotropical 2: 54-57. Bredt A., F. A. Araújo, J. Caetano-Júnior, M.G.

Reis N. R., I. P. de Lima & A. L. Peracchi. 2002. Morcegos (Chiroptera) da área urbana de Londrina, Paraná, Brasil. Revista Brasileira de Zoologia 19: 739 – 746. Rodrigues M. G. R., A. Bredt & W. Uieda. 1994. Arborização de Brasília, Distrito Federal, e possíveis fontes de alimento para morcegos fitófagos. Anais do II Congresso Brasileiro Arborização Urbana 2: 311-326. Sazima I., W. A. Fischer , M. Sazima & E. A.Fischer 1994. The fruit bat Artibeus lituratus as a forest and city dweller. Ciência e Cultura 46: 164-168. Silva M. M. S., N. M. S. Harmani , E. F. B. Gonçalves & W. Uieda. 1996. Bats from the metropolitan region of São Paulo, southeastern Brazil. Chiroptera

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Neotropical 2: 39-41. Tavares V. C. 1999. Ecomorfologia do vôo, dieta das espécies e composição de uma taxocenose de morcegos (Mammalia: Chiroptera) do Parque Estadual do Rio Doce, leste de Minas Gerais, Sudeste do Brasil. MSc thesis. Belo Horizonte, Universidade Federal de Minas Gerais. Uieda W. 1995. The common vampire bat in urban environments from southeastern Brazil. Chiroptera Neotropical 1: 22-24.

NOTES ON THE REPRODUCTION OF SIX

paper (1976) on bats from the northwestern region of the Brazilian state of São Paulo, and Willig’s studies (1985a, 1985b) on phyllostomids in northeastern Brazil. Herein I present data on reproduction of six species of phyllostomid bats at Serra do Japi, São Paulo, southeastern Brazil. The Serra do Japi is a quartizitic formation in the western region of Jundiaí (23o 11’S 46o 52’ W). The vegetation cover is subtropical humid forest (after Holdridge 1967). There is a warm wet season from October through March and a dry cooler season from April through August. Data was collected throughout 19 months (366 netting hours from August 1982 to February 1984). More information about climate and vegetation at Serra do Japi, and the methodology used in the present study is reported elsewhere (Marinho-Filho & Sazima 1989).

PHYLLOSTOMID BAT SPECIES IN SOUTHEASTERN

BRAZIL

Jader Marinho-Filho Departamento de Zoologia, Universidade de Brasília, 70910-900 Brasília, DF, Brazil. - [email protected] Abstract There are few extensive works on the reproductive phenology of phyllostomid bats. Herein I present data on reproduction of six species of phyllostomid bats at Serra do Japi, São Paulo, southeastern Brazil. Seemingly, sexual activity of frugivorous and nectarivorous species is more intense from July through November. Most pregnant females were collected between September and February and, consequently, most births should occur between October and March, period which corresponds to the warm and wet season, when food availability reaches its maximum at Serra do Japi. Key words: Atlantic Forest, bat reproduction, southeastern Brazil There are few extensive works on the reproductive phenology of phyllostomid bats. “Because of the paucity of the data, reproductive records from distant localities that were obtained over extended periods of time often formed the basis for the suggested patterns”, states Willig (1985a:17). Even using this methodology, it is not easy, when possible, to identify general patterns for species with large geographic distributions and about which information is scarce and fragmentary. Most information on phyllostomid reproductive patterns comes from studies conducted on the bat community of the Panama Canal Zone, Central America (Fleming et al. 1972, Bonaccorso 1979). The information gathered in Brazil is a set of fragmentary records, as can be seen in Wilson’s review (1979) on reproductive patterns of phyllostomids. Exceptions are Taddei’s

Adult bats were recognized on the basis of the following characteristics: adult fur color, ossified epiphysis, weight and forearm length. Reproductive condition of females was assessed by abdominal palpation and macroscopic examination of the teats. It is difficult to assess male’s reproductive condition even with histological techniques (Taddei 1976). I recorded as reproductive males individuals with well developed testes in the scrotum. Table 1 presents data on the reproductive condition for six species of phyllostomid bats: the frugivores, Carollia perspicillata, Sturnira lilium, Artibeus lituratus, Artibeus planirostris; Anoura caudifer a nectarivore, and Desmodus rotundus, the vampire bat. Although D. rotundus is reported as being sexually active throughout the year (Wilson 1979, Trajano 1985) I found pregnant females only in October and November. Nevertheless, reproductive males were captured in almost every month. This apparent contradiction is probably due to the small samples and the method used to assess reproductive condition of female bats (abdominal palpation), which does not permit the detection of early stages of pregnancy. This seems to be especially true for the vampire bat species, representing a potential source of error that only the dissection of specimens can avoid. W. Uieda (pers. comm.) working with Diaemus youngi in captivity could assess the reproductive status of pregnant females only in the last weeks of pregnancy. The information presented here for the frugivorous and nectarivorous species suggests a general pattern. Most of the pregnant females (94%) were collected between September and February and, consequently, most births should occur between October and March. This corresponds to the warm and wet season, when food availability reaches its maximum (Marinho-Filho 1991). Considering a mean gestation period of approximately

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