(Mammalia: Chiroptera)

23890-000, Seropédica, RJ, Brazil.

CEP 21040-360. Rio de Janeiro, RJ, Brazil.

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bat species are now recognized for the Piaui.

Brazil has one of the highest mammal diversities in the world (Costa et al. 2005). Currently, about 701 native species of 12 orders are known for the country (Paglia et al. 2012). Chiroptera is the second most diverse order in the country with 177 species of 68 genera and nine families, which correspond to approximately 25% of the Brazilian mammal fauna (Gregorin et al. 2011a; Paglia et al. 2012; Nogueira et al. 2012; Castro et al. 2012). Despite these impressive numbers and the considerable increase in the number of recorded bat species in the last 15 years, there are large gaps of knowledge on the occurrence, biology and distribution of Brazilian bats since less than 10% of the Brazilian territory may be considered minimally sampled for Chiroptera (Bernard et al. 2011). Recent data point out that more than half of the original areas of Caatinga and Cerrado have been severely modified by human activities, in particular agriculture, with high risk of desertification and loss of endemic species (Casteletti et al. 2003; Costa et al. 2005). Although there are important survey works on bat faunas from several localities within the limits of these biomes (Mares et al. 1985; Willig 1985; 1986; Willig and Mares 1989; Goncalves and Gregorin 2004; Esbérard et al. 2005; Zortéa and Alho 2008; Gregorin et al. 2011b), they are considered the least known since only 7% of the Caatinga and 6% of the Cerrado may be considered partially inventoried for bats (Bernard et al. 2011).

The state of Piaui comprises several types of vegetation (CEPRO 1990; Castro 2007). The main predominant phytophysiognomies are xerophytic vegetation, associated with the semi-arid climate characteristic of the Caatinga biome in the eastern region of the state, and the shrubby non-deciduous arboreous vegetation of the Cerrado, associated with the sub-humid climate of the southwestern region of the state. There are also the mixed sub-deciduous seasonal forests or babacu forest, the dry forests, the vine

Corresponding author. E-mail: sicottimaas@yahoo.com.br

Chek List

Journal of species lists and distribution

New records of bats for the state of Piaui, northeastern Brazil

Andrea Cecilia Sicotti Maas’, Daniela Dias’, André Pol’, Mayara Almeida Martins 1, Roberta Miranda de Araujo, Bruno Bret Gil?, Michel Schutte * and Adriano Lucio Peracchi°

Universidade Federal Rural do Rio de Janeiro, Instituto de Biologia, Programa de Pés-graduac¢ao em Biologia Animal. Caixa postal 74524. CEP Fundacao Oswaldo Cruz, Laboratério de Biologia e Parasitologia de Mamiferos Silvestres Reservatérios, IOC. Avenida Brasil, 4365 Manguinhos. Universidade Federal de Lavras, Departamento de Zoologia Laboratorio de Diversidade e Sistematica de Mamiferos, Campus Universitario Ufla,

Ecology and Environment do Brasil LTDA. Rua da Assembléia, 100/6o0andar. Centro. CEP 20011-000. Rio de Janeiro, RJ, Brasil. Universidade Federal Rural do Rio de Janeiro, Instituto de Biologia, Laboratério de Mastozoologia. BR 465, km 47. CEP 23890-000. Seropédica,

ABSTRACT: We provide four news records of bats—Micronycteris hirsuta (Peters, 1869), Dermanura gnoma (Handley, 1987), Myotis riparius Handley, 1960, and Myotis lavali Moratelli, Peracchi, Dias and Oliveira, 2011 to the Piaui State, northestern Brazil. We also provide measurements and taxonomic comments about the species recorded. With these new records, 59

forests, the complexes of the coastal zone (mangroves, dunes, and restingas) and transitional areas between ecosystems, in particular the Cerrado/Caatinga ecotone, which covers the southern axis of the state (Castro 2007).

Southwestern Piaui is one of the most poorly sampled regions for bats in Brazil and as a consequence it is considered a priority area for bat inventories (Bernard et al. 2011). Although a large part of this region is part of the Cerrado biome, it also harbors a complex ecotone resulting from the transition to the Caatinga, in which different plant communities may occur, such as semi-deciduous Cerrado with caatinga elements (Prado 2003). Currently, there are 55 species pertaining to nine families known for the state of Piaui (Reis et al. 2007; Gregorin et al. 2008; Tavares et al. 2008; Peracchi et al. 2011).

In the present study, we report four news records of bats for the state of Piauf: Micronycteris hirsuta, Dermanura gnoma, Myotis riparius, and Myotis lavali, obtained from bat inventories carried out in two municipalities in the Cerrado and the Cerrado/Caatinga ecotone, in the southwestern region of the state.

Bats were captured from 13" July to 10" August 2010, in four sampling areas in the southwestern region of Piaul. We distributed the samplingareas within the municipalities of Ribeiro Goncalves, where cerrado grasslands (campos cerrados) and cerrado forests (cerrad6es) predominate; and Coldnia de Gurguéia, where cerrado grasslands, cerrado forests, and arboreous caatingas occur (Figure 1—CEPRO 1990; Castro 2007). For capturing bats we used 10 mist nets (9 m x 2.5 m), which remained open for six hours from sunset on, during five nights in each sampling area. On each night, we set up the nets at ground level, along trails or in gaps, at different sites. We checked the nets every 20 min. The total sampling effort in each area was 6,750 m2.h (following Straube and Bianconi 2002).

445

[| Cerrado

E== Caatinga

FIGURE 1. Map of the state of Piaui, showing the sampling sites. 1 - Ribeiro Gongalves, 2 - Colénia de Gurguéia.

In this region the Cerrado predominates and is composed mainly of shrubby and non-deciduous arboreous vegetations (CEPRO 1990; Castro 2007). The climate is hot sub-humid tropical, the average annual temperatures varies from 26.3 to 27.0°C, the annual rainfall varies from 1,207 to 1,790 mm, and the water deficit varies from 365 to 560 mm; the rains are unevenly distributed, but slightly concentrated from December to April (Castro 2007). Transitional areas between Cerrado and Caatinga are also represented in southwestern Piaui; there is Cerrado associated with xerophytic formations, such as arboreous and shrubby Caatinga (Castro 2007). The climate in the region is hot semi-arid tropical, with an average rainfall of 825.7 mm, and a dry season lasting on average six months (CEPRO 1990). Specimens were collected under ICMBio/ SISBIO license 02001.001111/2008-14.

Voucher specimens were preserved in alcohol 70° and are currently deposited in the Collection of Mammals at the Museu Nacional (MN), Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.

Following the protocol proposed by Taddei et al. (1998), and using digital calipers accurate to 0.02 mm, we recorded 12 measurements (in mm) for the specimens collected (Tables 1): forearm length (FA), greatest length of skull (GLS), condylo-incisive length (CIL), maxillary tooth-row length (MTL), breadth across the upper molars (BAM), breadth across the cingula of the upper canines (BAC), postorbital breadth (POB), braincase breadth (BCB), zygomatic breadth (ZB), mastoid breadth (MB), mandibular length (ML), and mandibular toothrow length (MDTL).

We report below the new records to the Piaui State. For each species we comment identifications and distributions.

Micronycteris hirsuta (Peters, 1869)

We collected one adult female Micronycteris hirsuta (MN 75011) (Figure 2A) and identified it following Sanborn (1949), Genoways and Williams (1986), Simmons (1996), Simmons et al. (2002) and Williams and Genoways (2008). Micronycteris hirsuta is the largest species of the

Maas et al. | New records of bats for the state of Piaui

genus and the measurements of the specimen collected (Table 1) fit the range recorded for specimens from other localities (e.g., Genoways and Williams 1986; Simmons 1996; Simmons and Voss 1998; Simmons et al. 2002). The dorsal fur is long, silky, dense, and dark grayish-brown. The venter is pale-brown. The ears are connected across the crown of the head by a low interauricular skin band, without notch. The lower incisors are markedly hypsodont, with long and narrow crowns and a bilobate cutting edge (Simmons et al. 2002).

In Brazil, M. hirsuta has been recorded only in the Amazon and Atlantic Forest (Paglia et al. 2012), in the states of Acre, Amazonas, Bahia, Espirito Santo, Para, Rio de Janeiro, and Roraima (Mok et al. 1982; Peracchi and Albuquerque, 1985; Nogueira et al. 1999; Simmons et al. 2002; Esbérard 2004; Bernard and Fenton 2007; Faria et al. 2006). Our specimen was collected from a secondary riparian forest, in a Cerrado area in the municipality of Ribeiro Goncalves (07°40’57” S; 45°09’30” W), approximately 15 km away from the Parnaiba River. In the Cerrado, riparian or gallery forests are humid mesophytic formations that occur along watercourses (Eiten 1990). Although our record may be considered the first for the Brazilian cerrado, it is important to highlight that this species seems to prefer humid environments in primary and secondary forests (Genoways and Williams 1986; Peracchi and Albuquerque 1993; Bernard and Fenton 2002; Esbérard 2004) and inside forest fragments (Faria 2006).

Dermanura gnoma (Handley, 1987)

The Dermanura gnoma specimen (MN _ 73548) was identified according to previous descriptions and measurements reported for this species (Handley 1987; Simmonsand Voss 1998; Goncalves and Gregorin 2004; Lim et al. 2008). Our specimen has pale-brown dorsal fur, and the ventral fur is even paler than the dorsal; it has distinct white and prominent facial stripes above and below the eyes, bright yellow color on the tragus, noseleaf and edge of the ears, and yellowish warts on the chin (Figure 2B). The specimen has also a small third lower molar, short rostrum with a concavity on the dorsal surface, inflated anterorbital region, posteriorly constricted mesopterygoid pit and maxillary tooth-row length below 6.20 mm (Table 1). Dermanura cinerea Gervais, 1856, recorded for the state of Piauf (Peracchi et al. 2010; 2011), is on average larger than D. gnoma and differs from it by having a dark noseleaf and pale cream tragus and edge of the ears, brown warts on the chin, absence of a third lower molar, long rostrum, not inflated anterorbital region, mesopterygoid pit not constricted posteriorly and maxillary tooth-row length over 6.20 mm (Handley 1987; Simmons and Voss 1998; Goncalves and Gregorin 2004; Lim et al. 2008).

In Brazil, D. gnoma is distributed in the Amazon, Atlantic Forest, and Cerrado (Paglia et al. 2012), in the states of Amazonas, Amapa, Bahia, Espirito Santo, Mato Grosso, Para, and Rondonia (Peracchi et al. 2011). The examined specimen was collected in a disturbed area in a buriti forest associated with a watercourse (07°36'43” S; 45°06’7” W), in the municipality of Ribeiro Gongalves. This species has been found in primary and secondary forests, riparian forests, and secondary forest, in dry and

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open areas such as Cerrado, as well as in disturbed areas, such as orchards and plantations (Handley 1987; Aguiar et al. 1995; Bernard and Fenton 2002; Marques-Aguiar et al. 2002; Goncalves and Gregorin 2004).

FIGURE 2. Bats collected in a cerrado area in the municipality of Ribeiro Gongalves, state of Piauf, Brazil: A) Micronycteris hirsuta and B) Dermanura gnoma. Photos by André Pol.

Myotis riparius Handley, 1960

We collected one adult female of M. riparius (MN 75016) that fits diagnostic traits and dimensions provided by LaVal (1973), Barquez etal. (1999), and L6pez-Gonzalez et al. (2001). The plagiopatagium is attached at the level of the toes by a broad band of membrane (Lépez-Gonzalez et al. 2001; figure 1, p. 141), and the fringe of hairs along the trailing edge of the uropatagium is absent. Our specimen has wooly and short fur, and short and narrow ears. The dorsal fur is bicolor with dark-brown base and light- brown burned tip, which contrast slightly. The ventral fur is markedly bicolor with dark-brown base and pale tip. A low sagittal crest is present and the ratio between the postorbital constriction and the breadth across the canines

Maas et al. | New records of bats for the state of Piaui

is over 1.00, as generally reported for this species (LaVal 1973; Lépez-Gonzalez et al. 2001). The second upper premolar (P3) is shorter than one-fourth of the height of P4 in labial view, and is aligned in the tooth-row. Variation in position and displacement of P3 exist in specimens of M. riparius and M. nigricans (Schinz, 1821) in some localities, P3 is not always crowded to the lingual side in M. riparius and may be crowded in some M. nigricans (see LaVal 1973; Simmons and Voss 1998; Lépez-Gonzalez et al. 2001; Dias and Peracchi 2007; 2008). Nonetheless, M. nigricans is on average smaller than M. riparius, and it usually has long and silky dorsal fur; the ratio between the postorbital constriction and the breadth across the canines is below 1.00 and the sagittal crest is usually absent (LaVal 1973; Lopez-Gonzalez et al. 2001).

Myotis riparius has been recorded in Brazil in the states of Acre, Amazonas, Amapa, Bahia, Espirito Santo, Minas Gerais, Mato Grosso, Para, Parana, Rio de Janeiro, Rio Grande do Sul, Santa Catarina, and Sao Paulo (Goncalves and Gregorin 2004; Peracchi et al. 2011). This species occurs in the Amazon, Atlantic Forest, Cerrado, and Caatinga (Paglia et al. 2012). In the Cerrado, a M. riparius specimen was collected in a gallery forest (Goncalves and Gregorin 2004) and others specimens collected in humid forest/humid grassland ecotone and cerrado strictu sensu/gallery forest ecotone (Gregorin et al. 2011b). Our specimen examined was collected in a gallery forest, in the municipality of Ribeiro Goncalves (07°41'49” S; 45°08'14” W), within the Cerrado biome. This record corroborated previous observations of a possible preference of this species for forest areas and humid environments, in particular close to rivers and watercourses, where it is frequently found foraging over water (eg. Dias and Peracchi 2007; Simmons and Voss 1998; Wilson 2008).

Myotis lavali Moratelli, Peracchi, Dias, and Oliveira, 2011

We collected one adult male (MN 75034) and two adult females (MN 73549, MN 75035) of Myotis lavali. This species presents long and silky fur and its plagiopatagium is attached to the toes by a broad band of membrane. The dorsal fur is markedly bicolor with brown hair bases (2/3 of total length) and light-brown tips. The ventral fur is also bicolor with dark-brown bases and yellowish tips. The fringe of hairs of hairs along the trailing edge of uropatagium is absent, golden hairs are present on its proximal dorsal surface and on the femur. The postorbital constriction is narrow, the breadth across the canines/ postorbital breadth ratio is over 1.00, the forehead is steeply sloping with regards to the skull, with a round supraoccipital region, and low sagittal crest present. This combination of characters distinguishes M. lavali from all other Brazilian species of Myotis Kaup, 1829 (Moratelli et al. 2011). In two specimens, the second upper premolar (P3) is aligned to the toothrow and in one specimen the P3 is displaced to the lingual side. Variations in position and displacement of P3 have been found among specimens of M. lavali (Moratelli et al. 2011).

We collected M. lavali specimens in a shrubby caatinga (08°10'54” S; 43°42’22” W), in the municipality of Colénia de Gurguéia, located in the Cerrado/Caatinga ecotone. Before the present record, M. lavali was only known

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through the type series from Exu, state of Pernambuco, and from specimens collected in the states of Ceara and Bahia, within the limits of the Caatinga. Most of these specimens were collected in sub-humid and deciduous forests, between elevations from 390 to 900 m with relatively cold and wet climatic conditions compared to the dry adjacent localities in lower altitudes within the limits of Caatinga biome (Moratelli et al. 2011).

The bat fauna of Piaui is still poorly known, but with these new records (™. hirsuta, D. gnoma, M. lavali, and M. riparius), 59 species are now recognized (Tavares et al.

Maas et al. | New records of bats for the state of Piaui

2008; Gregorin et al. 2008; Peracchi et al. 2011; present study). We expect a higher diversity due to the mosaic of vegetations found in Piaui (CEPRO 1990; Castro 2007), since it affects species occurrence and distribution, and it is possible to find taxonomic assemblages that are characteristic of different adjacent formations. Hence, the intensification of sampling efforts in localities that harbor all physiognomies could strongly contribute to a better knowledge of bat diversity in Piaui and, in a broader context, it could contribute to clarify bat ecology and distribution.

TABLE 1. Selected measurements of four bat species recorded for the first time in the state of Piaui, northeastern Brazil. M = male; F = female.

Micronycteris hirsuta Dermanura gnoma MN 75011 MN 73548 E M FA 45.54 Sy20 GLS 23.16 18.90 CIL 20.52 17.02 MTL Daa 5.96 BAM 7.24 7.96 BAC 4.22 5.12 POB 4.80 4.92 BCB 8.74 8.70 ZB 11.20 10.56 MB 10.00 10.00 ML 15.50 A152 MDTL 10.04 6.48

ACKNOWLEDGMENTS: We are grateful to Carlos Torres (in memoriam) and Joel Samardo help during the fieldwork. We also thank Isaac P. Lima for the preparation of digital images, the company Katzenhaus for translation of this article, as well as the two anonymous reviewers for their valuable contributions to the final version.

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RECEIVED: October 2012

ACCEPTED: January 2013

PUBLISHED ONLINE: May 2013

EDITORIAL RESPONSIBILITY: Patl M. Velazco

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