Filling gaps in the distribution of the white-winged vampire bat, Diaemus youngii (Phyllostomidae, Desmodontinae): new records for southern Amazonia

Preenchendo lacunas na distribuição do morcego-vampiro de asas brancas, Diaemus youngii (Phyllostomidae, Desmodontinae): novos registros para o sul da Amazônia

Mônica A. PEDROSO Patrício A. da ROCHA Marcus V. BRANDÃO Guilherme S. T. GARBINO Carolina O. de MORAES Caroline C. AIRES About the authors

ABSTRACT

Bats of the subfamily Desmodontinae are the only hematophagous mammals, represented by three species. Among them, Diaemus youngii has the fewest records in Brazil, being poorly known demographically and ecologically. We report the first record of D. youngii for Mato Grosso state, in central-western Brazil, and provide additional records for the states of Rondônia and Tocantins, in northern Brazil, extending the known distribution of D. youngii in the southern Amazon region.

KEYWORDS:
rainforest; hematophagous bat; Mato Grosso; Rondônia; Tocantins

RESUMO

Os morcegos da subfamília Desmodontinae compreendem as únicas três espécies de mamíferos hematófagos. Entre elas, Diaemus youngii é a espécie com menor número de registros no Brasil, sendo pouco conhecida demográfica e ecologicamente. Nós relatamos o primeiro registro de D. youngii para o estado do Mato Grosso, no centro-oeste do Brasil, e fornecemos registros adicionais para os estados de Rondônia e Tocantins, no norte do Brasil. Os registros ampliam a distribuição conhecida de D. youngii no sul da região amazônica.

PALAVRAS-CHAVE:
floresta pluvial; morcego hematófago; Mato Grosso; Rondônia; Tocantins

Bats of the subfamily Desmodontinae are very relevant to public health, as they are the only hematophagous mammals and major reservoirs and vectors of rabies virus (Johnson et al., 2014Johnson, N.; Aréchiga-Ceballos, N.; Aguilar-Setien, A. 2014. Vampire bat rabies: Ecology, epidemiology and control. Viruses, 6: 1911-1928.). The subfamily contains three species, Desmodus rotundus É. Geoffroy, 1810; Diphylla ecaudata Spix, 1823; and Diaemus youngii (Jentink, 1893) (Gardner 2008). Diaemus youngii has the fewest records in Brazil (Kwon and Gardner, 2008Kwon, M.; Gardner, A.L. 2008. Subfamily Desmodontinae. In: Gardner, A.L. (Ed.). Mammals of South merica, Volume 1, Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, p.218-224.), being poorly known demographically and ecologically. The species is listed as “least concern” by the International Union for Conservation of Nature (IUCN) global assessment, mainly due to its wide geographic range (Aguiar et al., 2006Aguiar, L.M.S.; Camargo, W.R.; Portella, A.S. 2006. Ocurrence of white-winged vampire bat, Diaemus youngi (Mammalia, Chiroptera), in the Cerrado of Distrito Federal, Brazil. Revista Brasileira de Zoologia, 23: 893-896.; Greenhall and Schutt, 1996Greenhall, A.M.; Schutt, Jr. W.A. 1996. Diaemus youngi. Mammalian Species, 533: 1-7. ; IUCN, 2017IUCN. 2017. The IUCN Red List of Threatened Species. Version 2017-2. ( (http://www.iucnredlist.org ). Accessed on 14 September 2017.
http://www.iucnredlist.org...
). Diaemus youngii occurs over most of the Neotropical region, from northeastern Mexico, to Central and South America, reaching its southern limit in Misiones, Northern Argentina (Kwon and Gardner, 2008). In Brazil, the species is present in several phytophysiognomies, from Amazonian forests, through open habitats of the Pantanal, Cerrado and Caatinga biomes, to its southern limits in the Atlantic Forest of Paraná state (Brazil). Despite its wide distribution, records of the species are still rare and scattered (Greenhall and Schutt, 1996; Aguiar et al., 2006; Kwon and Gardner, 2008), especially in southern Amazonia, where a single record was known so far (Tavares et al., 2017Tavares, V.C.; Nore, C.C.; Palmute, C.F.; Nogueira, E.P.P.; Gomes, J.D.; Marcos, M.H.; Silva, R.F.; Farias, S.G.; Bobrowiec, P.E.D. 2017. The bat fauna from southwestern Brazil and its affinities with the fauna of western Amazon. Acta Chiropterologica, 19: 93-106.). We report here the first record of D. youngii for Mato Grosso state, in central-western Brazil, and provide additional records for the states of Rondônia and Tocantins, in northern Brazil, extending the known distribution of the species in the southern Amazon (Figure 1).

Figure 1
Known occurrence localities for Diaemus youngii. Stars represent the new records and circles are records from the literature. For key to code numbers, see Supplementary Material, Table S1.

All specimens analyzed here (Table 1) are deposited in the zoological collection of the Museu de Zoologia of Universidade de São Paulo (MZUSP). Its measurements are in accordance with the ones given in literature (see Greenhall and Schutt, 1996Greenhall, A.M.; Schutt, Jr. W.A. 1996. Diaemus youngi. Mammalian Species, 533: 1-7. ).

Table 1
Sex, external and cranial measurements (in mm) of the Diaemus youngii specimens reported in here. RO = Rondônia state, MT = Mato Grosso state, TO = Tocantins state.

The three specimens were mist netted during bat inventories. On July 17, 2014, an adult male D. youngii (MZUSP 35712) (Figure 2A) from Abunã, district of Porto Velho, Rondônia state (9°35’S, 65°3’W), was collected by the four main authors of the present study. The predominant vegetation type in that area is alluvial ombrophilous dense forest, with medium and large trees, palms, woody vines, and epiphytes (sensu Ivanauskas et al., 2008Ivanauskas, N.M.; Monteiro, M.; Rodrigues, R.R. 2008. Classificação fitogeográfica das florestas do Alto Rio Xingu. Acta Amazonica, 38: 387-402.). The other two specimens refers to unpublished specimens from MZUSP collection. Specimen MZUSP 35713 (Figure 3), represented by a taxidermied skin and separated skull, was collected by Marília Kerr on April, 1997 at the Renato River, a tributary of the Teles Pires River, near the city of Cláudia (11°24’S, 55°2’W), state of Mato Grosso, Brazil. Further details on the latter collecting locality are available in Gualda-Barros et al. (2012Gualda-Barros, J.; Nascimento, F.O.; Amaral, M.K. 2012. A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia, 52: 261-279.). Specimen MZUSP 35358 (preserved in alcohol) was mist netted in Couto Magalhães (8°21’S, 49°10’W), Tocantins state, in October 2014 during a bat inventory near an electric power transmission line (LT Xingu-Estreito) (Figure 1).

Figure 2
(A) Diaemus youngii (MZUSP 35712) caught in Porto Velho, state of Rondônia; (B) detail of the pair of glands located laterally on the inner part of the cheeks; (C) detail of the white spot on the distal tip of dactylopatagium. This figure is in color in the electronic version.

Figure 3
Dorsal, ventral and lateral views of the skull, and lateral view of the mandible of Diaemus youngii (MZUSP 35713) from the state of Mato Grosso, Brazil. Scale bar = 10 mm. This figure is in color in the electronic version.

Diaemus youngii can be distinguished from the other two desmodontine genera by a suite of morphological characters: a pair of glands located laterally on the inner part of the cheeks (Figure 2B), that are exposed when the bat feels threatened and releases a strong-smelling liquid (Greenhall and Schutt, 1996Greenhall, A.M.; Schutt, Jr. W.A. 1996. Diaemus youngi. Mammalian Species, 533: 1-7. ); a white spot on the distal tip of the dactylopatagium and another spot between digits IV and V (Figure 2C); thumbs with only one basal pad, an absent calcar (in D. rotundus the calcar is present/, but greatly reduced, and in D. ecaudata it is conspicuous) (Kwon and Gardner, 2008Kwon, M.; Gardner, A.L. 2008. Subfamily Desmodontinae. In: Gardner, A.L. (Ed.). Mammals of South merica, Volume 1, Marsupials, Xenarthrans, Shrews, and Bats. University of Chicago Press, Chicago, p.218-224.); two upper and one lower molar (i1/2, c1/1, p1/2, m2/1= 22) (Figure 3), while D. ecaudata has two lower molars (i2/2, c1/1, p1/2, m2/2= 26) and D. rotundus has one upper and one lower (i1/2, c1/1, p1/2, m1/1= 20).

Our review of the records of D. youngii in Brazil show that records are concentrated in southeastern Brazil, in the states of São Paulo and Rio de Janeiro (Figure 1). This pattern is possibly a result of a collection bias, as in these two states intensive and long-duration surveys have been carried out, and consequently the bat fauna in the two regions is relatively better known (Esbérard and Bergallo, 2005Esbérard, C.E.; Bergallo, H.G. 2005. Research on bats in the state of Rio de Janeiro, southeastern Brazil.Mastozoologia Neotropical, 12: 237-243.; Garbino, 2016Garbino, G.S.T. 2016. Research on bats (Chiroptera) from the state of São Paulo, southeastern Brazil: annotated species list and bibliographic review. Arquivos de Zoologia, 47: 43-128.). Based on our review, there is a large sampling gap in the Cerrado of central Brazil, and in the interior Caatinga.

Roosts used by D. youngii include caves and cavities in trees (Aguiar et al., 2006Aguiar, L.M.S.; Camargo, W.R.; Portella, A.S. 2006. Ocurrence of white-winged vampire bat, Diaemus youngi (Mammalia, Chiroptera), in the Cerrado of Distrito Federal, Brazil. Revista Brasileira de Zoologia, 23: 893-896.; Greenhall and Schutt, 1996Greenhall, A.M.; Schutt, Jr. W.A. 1996. Diaemus youngi. Mammalian Species, 533: 1-7. ), however, contrary to D. ecaudata (Rocha et al., 2014Rocha, P.A.; Pedroso, M.S.; Feijó, A.; Filho, N.G.; Bruno A.T.P. 2014. Update on the distribution of Diphylla ecaudata Spix, 1823 (Mammalia, Chiroptera): New records from the. Check List, 10: 1541-1545.) and D. rotundus (Oliveira et al., 2009Oliveira, P.R.; Silva, D.A.R.; Rocha, J.H.; Melo, S.M.A.; Bombonato, N.G.; Carneiro e Silva, F.O. 2009. Levantamento, cadastramento e estimativa populacional das habitações de morcegos hematófagos, antes e após atividades de controle, no município de araguari, Mg. Arquivos do Instituto de Biologia, 76: 553-560.; Greenhall et al., 1983Greenhall, A.M.; Joermann, G.; Schmidt, U. 1983. Desmodus rotundus. Mammalian Species, 202: 1-6. ; Flores-Crespo and Arellano-Sota, 1991Flores-Crespo, R; Arellano-Sota, C. 1991. Biology and control of vampire bat. In: Baer, G.M. (Ed.). The Natural History of Rabies. CRC Press, Boca Raton, Flórida, p.462-474.; Bredt et al., 1999Bredt, A.; Uieda, W; Magalhães, E.D. 1999. Morcegos cavernícolas da região do Distrito Federal, centro-oeste do Brasil (Mammalia, Chiroptera). Revista Brasileira de Zoologia, 16: 731-770.), the species is not commonly found in caves. Diaemus youngii has been found in caves in the southeastern Brazilian state of São Paulo, but with a low capture rate (Trajano, 1984Trajano, E. 1984. Ecologia de populações de morcegos cavernícolas em uma região cárstica do sudeste do Brasil. Revista Brasileira de Zoologia, 2: 255-320.), while in the same state, McNab (1969McNab, B.K. 1969. The economics of temperature regulation in neutropical bats. Comparative Biochemistry and Physiology, 31: 227-268.) and Taddei (Information on the specimen found in the Chiroptera Collection, Department of Zoology, State University of São Paulo, São José do Rio Preto “DZSJRP 16615”) sampled the species in cavities in standing trees. In Trinidad, a large colony was found in a hollow Erythrina micropteryx tree, and only a single individual was captured in a cave (Goodwin and Greenhall, 1961Goodwin, G.G.; Greenhall, A.M. 1961. A review of the bats of Trinidad and Tobago: descriptions, rabies infection, and ecology. American Museum of Natural History, 122: 187-302.). Therefore, based on these data, it is suggested that additional records of D. youngii may be obtained by searching for roosts in hollow standing trees.

To have additional information on how and where to find the species, data on roost use and colony demographics are of special importance, expanding the knowledge of blood-feeding bats and their biology. The records presented in here contribute to the knowledge on the distribution of D. youngii in the Amazon region.

ACKNOWLEDGEMENTS

We are grateful to Arcadis Logos S/A for field campaigns and to Dr. Mario de Vivo and Juliana Gualda de Barros from Museu de Zoologia da Universidade de São Paulo - MZUSP, to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES for a graduate scholarship to MAP and for a research scholarship to PAR.

  • Aguiar, L.M.S.; Camargo, W.R.; Portella, A.S. 2006. Ocurrence of white-winged vampire bat, Diaemus youngi (Mammalia, Chiroptera), in the Cerrado of Distrito Federal, Brazil. Revista Brasileira de Zoologia, 23: 893-896.
  • Bredt, A.; Uieda, W; Magalhães, E.D. 1999. Morcegos cavernícolas da região do Distrito Federal, centro-oeste do Brasil (Mammalia, Chiroptera). Revista Brasileira de Zoologia, 16: 731-770.
  • Esbérard, C.E.; Bergallo, H.G. 2005. Research on bats in the state of Rio de Janeiro, southeastern Brazil.Mastozoologia Neotropical, 12: 237-243.
  • Flores-Crespo, R; Arellano-Sota, C. 1991. Biology and control of vampire bat. In: Baer, G.M. (Ed.). The Natural History of Rabies CRC Press, Boca Raton, Flórida, p.462-474.
  • Garbino, G.S.T. 2016. Research on bats (Chiroptera) from the state of São Paulo, southeastern Brazil: annotated species list and bibliographic review. Arquivos de Zoologia, 47: 43-128.
  • Greenhall, A.M.; Joermann, G.; Schmidt, U. 1983. Desmodus rotundus Mammalian Species, 202: 1-6.
  • Greenhall, A.M.; Schutt, Jr. W.A. 1996. Diaemus youngi Mammalian Species, 533: 1-7.
  • Goodwin, G.G.; Greenhall, A.M. 1961. A review of the bats of Trinidad and Tobago: descriptions, rabies infection, and ecology. American Museum of Natural History, 122: 187-302.
  • Gualda-Barros, J.; Nascimento, F.O.; Amaral, M.K. 2012. A new species of Callicebus Thomas, 1903 (Primates, Pitheciidae) from the states of Mato Grosso and Pará, Brazil. Papéis Avulsos de Zoologia, 52: 261-279.
  • Ivanauskas, N.M.; Monteiro, M.; Rodrigues, R.R. 2008. Classificação fitogeográfica das florestas do Alto Rio Xingu. Acta Amazonica, 38: 387-402.
  • IUCN. 2017. The IUCN Red List of Threatened Species. Version 2017-2. ( (http://www.iucnredlist.org ). Accessed on 14 September 2017.
    » http://www.iucnredlist.org
  • Johnson, N.; Aréchiga-Ceballos, N.; Aguilar-Setien, A. 2014. Vampire bat rabies: Ecology, epidemiology and control. Viruses, 6: 1911-1928.
  • Kwon, M.; Gardner, A.L. 2008. Subfamily Desmodontinae. In: Gardner, A.L. (Ed.). Mammals of South merica, Volume 1, Marsupials, Xenarthrans, Shrews, and Bats University of Chicago Press, Chicago, p.218-224.
  • McNab, B.K. 1969. The economics of temperature regulation in neutropical bats. Comparative Biochemistry and Physiology, 31: 227-268.
  • Oliveira, P.R.; Silva, D.A.R.; Rocha, J.H.; Melo, S.M.A.; Bombonato, N.G.; Carneiro e Silva, F.O. 2009. Levantamento, cadastramento e estimativa populacional das habitações de morcegos hematófagos, antes e após atividades de controle, no município de araguari, Mg. Arquivos do Instituto de Biologia, 76: 553-560.
  • Rocha, P.A.; Pedroso, M.S.; Feijó, A.; Filho, N.G.; Bruno A.T.P. 2014. Update on the distribution of Diphylla ecaudata Spix, 1823 (Mammalia, Chiroptera): New records from the. Check List, 10: 1541-1545.
  • Tavares, V.C.; Nore, C.C.; Palmute, C.F.; Nogueira, E.P.P.; Gomes, J.D.; Marcos, M.H.; Silva, R.F.; Farias, S.G.; Bobrowiec, P.E.D. 2017. The bat fauna from southwestern Brazil and its affinities with the fauna of western Amazon. Acta Chiropterologica, 19: 93-106.
  • Trajano, E. 1984. Ecologia de populações de morcegos cavernícolas em uma região cárstica do sudeste do Brasil. Revista Brasileira de Zoologia, 2: 255-320.

  • ASSOCIATE EDITOR:

    Paulo Bobrowiec
  • CITE AS:

    Pedroso, M.A.; da Rocha, P.A.; Brandão, M.V.; Garbino, G.S.T.; de Moraes, C.O.; Aires, C.C. 2018. Filling gaps in the distribution of the white-winged vampire bat, Diaemus youngii (Phyllostomidae, Desmodontinae): new records for southern Amazonia. Acta Amazonica 48: 154-157

SUPPLEMENTARY MATERIAL

Table S1
Locality records for Diaemus youngii in Brazil. The code numbers refer to the points shown in Figure 1. Datum: SAD69.

Publication Dates

  • Publication in this collection
    Apr-Jun 2018

History

  • Received
    23 Nov 2017
  • Accepted
    19 Feb 2018
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