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

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., 2014). 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, 2008), 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., 2006; Greenhall and Schutt, 1996; IUCN, 2017). 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., 2017). 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, 1996).

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.

Parameter¹	MZUSP 35712 (RO)	MZUSP 35713 (MT)	MZUSP 35358 (TO)
Sex	Male	Male	Male
Body length	76.46	71.15	73.61
Hind foot length	15.35	16.94	16.40
Ear length	17.49	16.06	18.05
Forearm length	54.39	48.94	53.14
Greatest length of skull	25.99	25.83	25.01
Condylobasal length	21.59	20.35	21.09
Mastoid breadth	13.20	11.84	12.69
Zygomatic breadth	14.20	13.94	13.84
Breadth of braincase	13.24	12.90	12.91
Postorbital constriction	6.60	6.00	6.36
Palatal length	8.08	7.82	7.61
Breadth across upp/er canines	6.53	6.35	6.43
Breadth across upper molars	6.80	6.53	6.41
Length of maxillary toothrow	5.56	5.30	5.97
Length of mandible	15.55	14.91	14.99

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., 2008). 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. (2012). 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, 1996); 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, 2008); 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, 2005; Garbino, 2016). 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., 2006; Greenhall and Schutt, 1996), however, contrary to D. ecaudata (Rocha et al., 2014) and D. rotundus (Oliveira et al., 2009; Greenhall et al., 1983; Flores-Crespo and Arellano-Sota, 1991; Bredt et al., 1999), 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, 1984), while in the same state, McNab (1969) 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, 1961). 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.

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• 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.

Code	Coordinates		State	Locality	Reference
	Lat	Long
1	7º 27› 00» S	73º 41’ 00” W	AC	Parque Nacional da Serra do Divisor, Cruzeiro do Sul	Nogueira et al. (1999)
2	9º 39’ 00” S	65º 27’ 00” W	RO	Distrito de Abunã, Porto Velho	This study
3	8º 48’ 06” S	63º 57’ 03” W	RO	UHE Santo Antônio, Porto Velho	Tavares et al. (2017)
4	2º 24’ 00” S	59º 43’ 00” W	AM	Projeto Dinâmica Biológica de Fragmentos Florestais (PDBFF), Manaus	Bernard (2001)
5	0º 30’ 00” S	51º 40’ 00” W	AP	Santa Luzia do Pacui, Macapá	Peracchi et al. (1984)
6	2º 27’ 02” S	54º 42’ 03” W	PA	Taperinha, Santarém	Piccinini (1974)
7	4º 16’ 39” S	55º 59’ 04” W	PA	Iataituba	Reis & Schubart (1979)
8	1º 27’ 21” S	48º 29’ 25” W	PA	Utinga, Belém	Handley (1967)
9	3º 41’ 00” S	45º 35’ 00” W	MA	Tufilândia	Dias et al. (2009)
10	7º 04’ 54” S	41º 29’ 55” W	PI	Picos	Pinto & Bento (1986)
11	6º 31’ 00” S	35º 44’ 00” W	PB	Parque Estadual Pedra da Boca, Araruna	Feijó et al. (2010)
12	7º 41’ 00” S	35º 39’ 00” W	PB	Lagoa da Pedra, Lajes, Umbuzeiro	Feijó & Langguth (2011)
13	8º 00’ 00’’ S	35º 03’ 00” W	PE	Estação Ecológica do Tapacurá, São Lourenço da Mata	Mares et al. (1981)
14	8º 25’ 29” S	49º 07’ 24” W	TO	Estreito, Couto Magalhães	This study
15	10º 34’ 00” S	46º 30’ 00” W	TO	Estação Ecológica Serra Geral do Tocantins	Gregorin et al. (2011)
16	12º 39’ 00” S	43º 03’ 00” W	BA	Nas proximidades de Paratinga, Vale Médio do Rio São Francisco	Sá-Neto & Marinho Filho (2013)
17	15º 34’ 00” S	39º 17’ 00” W	BA	Fazenda São José	Falcão (2007)
18	15º 30’ 00” S	48º 10’ 00” W	DF	Brazlândia	Aguiar et al. (2006)
19	11º 24’ 03” S	55º 02’ 58” W	MT	Cláudia	This study
20	19º 13’ 10” S	57º 02’ 30” W	MS	Nhecolândia	Oliveira et al. (2012)
21	20º 14’ 10” S	56º 22’ 30” W	MS	Miranda	Oliveira et al. (2012); Leite et al. (1998)
22	20º 32’ 23” S	55º 47’ 43” W	MS	Aquidauana	Oliveira et al. (2012)
23	20º 23’ 11” S	54º 36’ 27” W	MS	Instituto São Vicente, Campo Grande	Urbieta et al. (2017)
24	23º 23’ 00” S	51º 11’ 00” W	PR	Parque Estadual Mata do Godoy	Reis et al. (2003)
25	23º 40’ 25” S	49º 47’ 36” W	PR	Siqueira Campos	Margarido & Braga (2004)
26	25º 25’ 26” S	50º 00’ 16” W	PR	Palmeira	Thomas (1899)
27	24º 54’ 58” S	49º 14’ 33” W	PR	Cerro Azul	Graciolli & Carvalho (2001)
28	25º 28’ 00” S	48º 58’ 00” W	PR	Estação Roça Nova, Piraquara	Miller (1906)
29	24º 33’ 00” S	48º 39’ 00” W	SP	Caverna Alambari de Baixo, Iporanga	Trajano (1984)
30	23º 15’ 27” S	49º 28’ 01” W	SP	Sarutaiá	Uieda (1993)
31	21º 25’ 00” S	50º 28’ 00” W	SP	Bilac	Garbino (2016)
32	20º 46’ 00” S	49º 28’ 00” W	SP	APA Grota de Mirassol, Mirassol	Garbino (2016)
33	20º 52’ 00” S	49º 24’ 00” W	SP	Mata dos Macacos, São José do Rio Preto	Garbino (2016)
34	20º 57’ 00” S	49º 10’ 00” W	SP	Uchoa	Garbino (2016)
35	21º 19’ 00” S	49º 03’ 00” W	SP	Itajobi	Garbino (2016)
36	22º 59’ 00” S	48º 26’ 00” W	SP	Botucatu	Uieda (2005)
37	22º 27’ 00” S	47º 32’ 00” W	SP	Fazenda Paraguassu, Santa Gertrudes	Sazima & Uieda (1980)
38	23º 34’ 00” S	46º 43’ 00” W	SP	Butantan, São Paulo	Vieira (1942)
39	23º 25’ 00” S	46º 01’ 00” W	SP	Guararema	Garbino (2016)
40	23º 46’ 00” S	45º 45’ 00” W	SP	Barra do Uma, São Sebastião	Garbino (2016)
41	23º 02’ 00” S	44º 21’ 00” W	RJ	Ilha da Gipóia, Angra dos Reis	Carvalho et al. (2011)
42	23º 04’ 00” S	43º 53’ 00” W	RJ	Ilha de Marambaia, Rio de Janeiro	Lourenço et al. (2010)
43	22º 32’ 00” S	44º 11’ 00” W	RJ	Barra Mansa	Peracchi & Albuquerque (1971)
44	22º 22’ 00” S	43º 47’ 00” W	RJ	Santuário da Vida Silvestre da Serra da Concórdia, Barra do Piraí	Modesto et al. (2008)
45	22º 54’ 00” S	43º 14’ 00” W	RJ	U.F.R.R.J., Seropédica	Peracchi & Albuquerque (1984)
46	22º 23’ 00” S	41º 45’ 00” W	RJ	Parque Nacional da Restinga de Jurubatiba, Macaé	Luz et al. (2011)
47	22º 07’ 00” S	41º 29’ 00” W	RJ	Carmo	Avilla et al. (2001)
48	22º 06’ 00” S	41º 25’ 00” W	RJ	Parque Nacional Restinga de Jurubatiba, Quissamã	Bergallo et al. (2004)
49	19º 44’ 51” S	47º 56’ 21” W	MG	Uberaba	Uieda (1993); Stutz et al. (2004)
50	19º 42’ 00” S	43º 56’ 00” W	MG	São José da Lapa	Torquetti et al. (2013)

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Publication Dates

• Publication in this collection
  Apr-Jun 2018

History

• Received
  23 Nov 2017
• Accepted
  19 Feb 2018