NOTES ON GEOGRAPHIC DISTRIBUTION Check List 14 (2): 313-317

https://doi.org/10.15560/14.2.313

> PENSUFT.

Expansion of the known range of the Lesser Bulldog Bat, Noctilio
albiventris Desmarest, 1818 (Chiroptera, Noctilionidae) in the
Brazilian Cerrado

Ana P. M. Olimpio,'* Fabio H. S. Cardoso,” Cleison L. S. Costa,? Elmary C. Fraga,'?
Maria C. Barros!

1 Graduate Program (Masters) in Environmental Biodiversity and Health, Centro de Estudos Superiores de Caxias (CESC), Universidade Estadual
do Maranhao, Praga Duque de Caxias S/N, Bairro Alecrim, 65604-000, Caxias, MA, Brazil. 2 Laboratory of Genetics and Molecular Biology,
Centro de Estudos Superiores de Caxias, Universidade Estadual do Maranhéo (UEMA), Praca Duque de Caxias S/N, Bairro Alecrim, 65604-000,
Caxias, MA, Brazil.

Corresponding author: Maria C. Barros, mbdene@yahoo.com.br

Abstract

The Lesser Bulldog Bat, Noctilio albiventris, is found in all major Brazilian phytogeographic domains. We extend the
known distribution of this species in the Cerrado, where 3 specimens were collected in the municipality of Caxias,
which is within the Cerrado domain of the state of Maranh&o, northeastern Brazil. Our analysis of the COI gene
confirms the morphological identification of the specimens, based on a 99.8—100% similarity with known sequences.
This record extends the known distribution of N. albiventris 260 km to the east, in the state of Maranhao, and 986 km
to the north, in the Cerrado biome.

Keywords
Maranhao; bats; DNA barcode; mitochondrial gene.

Academic editor: Marcelo Rodrigues Nogueira | Received 6 October 2017 | Accepted 18 January 2018 | Published 9 March 2018

Citation: Olimpio APM, Cardoso FHS, Costa CLS, Fraga EC, Barros MC (2018) Expansion of the known range of the lesser bulldog bat, Noctilio
albiventris Desmarest, 1818 (Chiroptera, Noctilionidae) in the Brazilian Cerrado. Check List 14 (2): 313-317. https://do1.org/10.15560/14.2.313

Check List ire tc

Introduction

Noctilio Linnaeus, 1766 is the only genus in Noctilioni-
dae (Hood and Jones 1984, Nogueira et al. 2014). The
2 species currently recognized—the Lesser Bulldog Bat,
Noctilio albiventris Desmaret, 1818, and the Greater
Bulldog Bat, Noctilio leporinus (Linnaeus, 1758)—occur
in sympatry (Gardner 2008) and share the following
diagnostic characters: cleft upper lip, 3 phalanges on the
third finger, well-developed calcaneum and claws on the
feet, and tail shorter than the uropatagium (Hood and
Pitocchelli 1983, Reis et al. 2011). While similar in sev-

eral respects, these species can be promptly distinguished
based on their body size (Khan et al. 2014).

Noctilio albiventris is smaller than N. /eporinus, having
a wingspan of 400 mm (Hood and Pitocchelli 1983), head-
body length of 75 mm, and forearm length ranging from 55
to 65 mm (Nowak 1991). Its pelage is also shorter than that
of the latter species (Reis et al. 2013). Noctilio albiventris
presents a wide but discontinuous range from southern
Mexico to northern Argentina and western Uruguay (Reis
et al. 2007, Gardner 2008), including the Caribbean Islands
(Lopez-Baucells et al. 2016). In Brazil, it is found in all
major phytogeographic domains, including Amazonia

Copyright Olimpio et al. This isan open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original author and source are credited.

314

Check List 14 (2)

Figure 1. Variation in the ventral coloration of Noctilio albiventris from Caxias, state of Maranhao, northeastern Brazil. A. UFPB 9819. B. UFPB
9818. C. View of the dorsal stripe, UFPB 9820.

(Acre, Amazonas, Amapa, Para, Roraima, Maranhao, and
Mato Grosso states), Cerrado (Mato Grosso, Sao Paulo,
Tocantins, and Minas Gerais), Caatinga (Bahia, Ceara,
Piaui, Sergipe, and Minas Gerais), Pantanal (Mato Grosso
do Sul), Atlantic Forest (Rio de Janeiro, SAo Paulo, Parana,
and Sergipe), and Pampa (Parana) (Miretzki 2003, Gardner
2008, Dias et al. 2009, Bezerra and Marinho-Filho 2010,
Rocha et al. 2010, Peracchi and Nogueira 2010, Pavan et
al. 2013, Reis et al. 2013, Nogueira et al. 2015, Garbino
2016). We present here the first record of N. albiventris for
the Cerrado in the state of Maranhao and extend the known
distribution of this species in this biome.

Methods

Specimens were collected under the license IBAMA/
SISBIO 42670-3 and deposited in the Universidade Fed-

eral da Paraiba (UFPB), Joao Pessoa, Paraiba, Brazil.
They were fixed in 10% formalin and then transferred
to 70% alcohol. Body weight and forearm length were
obtained, respectively, with a Pesola spring scale and
a digital caliper, and age classes (juvenile/adult) were
determined according to Brunet and Austad (2004).
Total DNA was extracted from muscle tissue using the
Promega Wizard Genomic DNA Purification kit, follow-
ing the manufacturer’s instructions. The mitochondrial
cytochrome oxidase subunit 1 (COI) gene was amplified
by polymerase chain reaction (PCR) using the primers
LCO-1490 and HCO-2198, as described by Folmer et
al. (1994). The samples were sequenced by the dideoxy-
terminal method of Sanger et al. (1977), using a Big Dye
kit in an ABI Prism™ 3500 (Applied Biosystems, USA)
automatic sequencer. The sequences were plotted on the
BOLD Systems platform to obtain similarity.

Olimpio et al. | Distribution of Noctilio albiventris in the Brazilian Cerrado 315

100,05
100
99.95
99.9
99.85
99.8
99.75

99.7

Chordata Mammalia Chiroptera Noctilionidae Noctilio albiventris

Phylum Class Order Family Genus Species

=—@—Cx01 === Cx03/Cx05

Figure 2. Similarity obtained from the BOLD Systems platform for
specimens of Noctilio albiventris from Caxias, state of Maranhao,
northeastern Brazil.

Results

New records. Brazil, Maranhao, East Maranhaéo mesore-
gion, center of the municipality of Caxias, Acrisio Cruz
Street (04°51'32" S, 043°21'22" W), coll. Olimpio,
APMO; Cardoso, FHS; Costa, CLS, 15 February 2017, 3
adult males (UFPB98 18-9820).

The neighborhood in Caxias where the new record
originates has extensive tree cover and is located along
the Itapecuru River. The specimens of N. a/biventris were
sharing their roost with individuals of Molossus rufus E.
Geoffroy, 1805 (Molossidae) and Artibeus sp. Leach,
1821 (Phyllostomidae, Stenodermatinae).

Identification. The 3 specimens of N. a/biventris ranged
from 27.8 to 30.2 g, while forearm lengths ranged from
62 to 64 mm. AIl specimens presented the typical dorsal
stripe, but their coloration varied considerably, rang-
ing from grayish-brown to orange on the dorsum, and
light-gray to orange on the venter (Fig. 1). In both mea-
surements and coloration these specimens are consistent
with descriptions presented by Gardner (2008) and Reis
et al. (2011, 2013).

Results of the COI gene analysis confirm our mor-
phological identification of our specimens, with 100%,
99.8%, and 99.8% similarity with data available in the
BOLD Systems platform for specimens of N. albiventris
from Guyana (Fig. 2). From these results, we infer that our
specimens belong to the N. a. albiventris lineage.

Discussion

Noctilio albiventris roosts in caves, rock crevices, build-
ings, and tree holes, usually near water bodies (Hood
and Pitocchelli 1983, Nogueira and Pol 1998, Alcantara
et al. 2016). This species has also been recorded roost-
ing with Rhynchonycteris naso (Wied-Neuwied, 1820)
(Emballonuridae) and species of Molossus E. Geoffroy,
1805 (Hood and Pitocchelli 1983, Nogueira and Pol
1998). The only previous record of N. a/biventris for the
state of Maranhao is in the municipality of Santa Inés,

within the Amazon biome. Our specimens, therefore,
are only the second record of this species in Maranhao
and the first evidence of the occurrence of this species
in the Cerrado biome in this state. Based on the previous
nearest records in Maranhao (Santa Inés) and in the Cer-
rado biome (So Domingos River, Parana, 12°54'50.8"S,
047°34'00.7" W, Tocantins; Bezerra and Marinho-Filho
2010), the known distribution of N. a/biventris is extended
by, respectively, about 260 km to the east and 986 km to
the north (Fig. 3).

Data from the COI gene reveals less than 1% of
divergence with respect to N. albiventris specimens from
Guyana, which is below the 3% limit established by Hebert
et al. (2003) for separation of species and corroborate our
morphological identification. This mitochondrial gene has
been studied for several bat families (Noctilionidae, Phyl-
lostomidae, Vespertilionidae, and Molossidae) and is an
effective tool for species identification (Clare et al. 2007,
Clare et al. 2011, Gager et al. 2016). The subspecies, WN. a.
albiventris, to which we assign our Maranhao specimens,
is the most widely distributed among the 3 subspecific
taxa currently recognized for the species Noctilio albiven-
tris, and occurs from northern Venezuela to the Guianas,
and along the greater Amazon basin and the Brazilian
coast (Davis 1976, Gardner 2008, Pavan et al. 2013).

Acknowledegments

We are grateful to the Maranhao State Foundation for
Technology and Scientific Research (FAPEMA).

Authors’ Contributions

APMOlimpio: collected and identied specimens, ana-
lyzed genetic data, wrote and revised the manuscript;
FHSC collected and identified specimens; CLSC col-
lected, extracted DNA and analyzed genetic data; ECF
and MCBarros wrote and revised the manuscript.

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