The bats of Rio Grande do Norte state, northeastern Brazil

Morcegos do estado do Rio Grande do Norte, nordeste do Brasil

Abstract

Rio Grande do Norte is one of the smallest states in Brazil but has a rich diversity of ecosystems, including Caatinga vegetation, remnants of Atlantic Forest, coastal habitats, mangroves and large karstic areas with caves. However, its chiropteran fauna is little known, and the state contains conspicuous gaps of information on the occurrence and distribution of bats in Brazil. In order to reduce this information gap, based on a review of scientific literature and regional mammal collections, we list 42 species of bats, including new occurrences for 13 species and discussion on their conservation status. Results show that more than half (54%) of the recorded species are phyllostomid bats, and about one third of the bats in the state roosts in underground cavities. The Caatinga harbored the highest bat richness in the state, including the occurrence of four vulnerable species (Furipterus horrens, Lonchorhina aurita, Natalus macrourus and Xeronycteris vieirai). The Atlantic Forest needs to be more sampled, including mangroves, coastal habitats and areas of Caatinga in the central region of the state (Borborema highlands), which are virtually unsurveyed. Although the recent increase of studies on bats in the state, future studies should complement conventional mistnetting with active roost search and bioacoustical records in order to obtain better data for unraveling the bat fauna of Rio Grande do Norte.

Keywords:
Atlantic Forest; Caatinga; Chiroptera; Species distribution; Vulnerable species

Resumo

O Rio Grande do Norte é um dos menores estados do Brasil, mas possui grande diversidade de ecossistemas, incluindo vegetação de Caatinga, Mata Atlântica, habitats costeiros, manguezais e grandes áreas cársticas com cavernas. No entanto, a fauna de quirópteros é pouco conhecida, e o estado contém lacunas importantes sobre a ocorrência e distribuição de morcegos no Brasil. Para reduzir essa lacuna de informação, com base em uma revisão da literatura científica e coleções regionais de mamíferos, listamos 42 espécies de morcegos, incluindo novas ocorrências para 13 espécies e discusões sobre seu estado de conservação. Os resultados mostram que mais de metade (54%) das espécies registradas são morcegos filostomídeos e cerca de um terço dos morcegos no estado se abrigam em cavidades subterrâneas. A Caatinga abrigou a maior riqueza de morcegos no estado, incluindo a ocorrência de quatro espécies vulneráveis (Furipterus horrens, Lonchorhina aurita, Natalus macrourus e Xeronycteris vieirai). A Mata Atlântica precisa ser mais amostradas, incluindo manguezais, habitats costeiros e áreas de Caatinga principalmente na região central do estado (planalto da Borborema), que são virtualmente inexplorados. Embora o recente aumento das investigações no estado em relação aos morcegos, estudos futuros devem complementar os métodos convencionais de captura com procura ativa de abrigos e monitoramento bioacústico para obter melhores dados na tarefa de desvendar a diversidade de morcegos do Rio Grande do Norte.

Palavras-chave:
Caatinga; Chiroptera; Espécies vulneráveis; Distribuição de espécies; Mata Atlântica

Introduction

About one-quarter of the Brazilian mammal species are bats (Paglia et al. 2012), currently comprising 183 known species (Nogueira et al. 2014, Feijó et al. 2015a, Fischer et al. 2015, Moratelli & Dias 2015, Gregorin et al. 2016, Rocha et al. 2016). Considering that Brazil harbors one of the largest mammal diversities in the world, its bat fauna is poorly known. Bat records indicate that less than 10% of the Brazilian territory can be considered minimally sampled, and about 60% has no single formal record of bat species (Bernard et al. 2011).

The state of Rio Grande do Norte (RN) represents a conspicuous gap of bat information in Brazil (Bernard et al. 2011). The earliest records of bats in RN date back to the past century, when Sanborn (1937), Goodwin (1959), Webster (1993), and Jones & Hood (1993) reported few bat records from the coastal region of the state (municipality of Natal) and deposited the specimens in biological collections in United States. Studies on bats in RN slowly began to increase in this century, with new records and distributional expansions (Feijó & Nunes 2010, Barros 2014, Basílio et al. 2017), ecology and natural history (Cordero-Schmidt et al. 2016, Cordero-Schmidt et al. 2017), community diversity (Barros et al. 2017, Vargas-Mena et al. in press), and subterranean fauna inventories (Ferreira et al. 2010); including a bilbliographic review on the bat fauna in northeastern Brazil by Garcia et al. (2014). Such studies together have recorded a richness of 38 species of bats in the state.

Despite the recent efforts in describing the bat fauna of RN, there are still gaps of knowledge. In addition, bat diversity and species distribution are poorly known in the state, and it is important for conservation strategies and policies (Costa et al. 2005). Therefore, we present an updated list of bat species based on available mammal collections and literature review in order to describe the bat species composition, distribution and richness that occur within the state's political boundaries and discuss conservation concerns based on the available data. We expect that this study will inform the scientific community, government agencies, non-governmental organizations, and general society about the diversity of bats that occurr in RN; will point out sites that need increased research efforts; and will be a reference baseline for ecological and diversity assessments, including those for environmental impact studies, to be carried out in the state.

Material and Methods

1. Study Site

The state of Rio Grande do Norte (RN) is located in the northeastern region of Brazil between the latitudes 4º49'53'' S and 6º58'57" S and longitudes 35º58'03" W and 38º36'12" W. It is limited to the north and the east by the Atlantic Ocean; to the west by the Ceará State, and the south with the state of Paraíba. RN has a territorial extension of 52,797 km² and is composed of 167 municipalities, being one of the smallest states in Brazil (IDEMA 2015).

The 95% of the state is characterized by a semiarid climate where the Caatinga domain occurs (IDEMA 2015). According to Köppen classification, the climate in this portion of the state is BShw (hot and dry), with a mean annual rainfall of less than 800 mm (Alvares et al., 2013). The Caatinga is a seasonally dry tropical forest composed by mosaics of xeric spiny shrub lands, columnar cacti, succulents, and deciduous woody forest stands (arboreal caatingas) (Leal et al. 2003). Physiognomy and plant composition variations determine eight different ecoregions in the Caatinga; however, only two occur in RN: the Northern Sertaneja Depression (NSD) and the Borborema Highlands (BH) (see Velloso et al. 2002). The NSD is characterized by extensive low plains, with elevations varying from 20-500 meters. The vegetation type is spiny shrub lands with herbaceous plants and remnants of arboreal Caatinga on slopes and low mountain ranges, and on the main river valleys there are ciliary remnants of Carnaúba palms (Copernicia prunifera). The BH ecoregion is mountainous with steep slopes and rugged relief, with rocky outcrops of granite. The altitude varies from 150-650 m and the vegetation is characterized by a shrubby-arboreal Caatinga with columnar cacti and arboreal Caatingas in more humid areas on the tops of the mountains.

On the east coast of the state, according to Köppen classification, the climate type is Aw with precipitations varying from 700-1500 mm (Alvares et al., 2013). This region harbors the northernmost distribution of the Atlantic Forest in Brazil (IDEMA 2015). The RN's Atlantic Forest is composed of remnants of evergreen and semi-evergreen forests stands, dunes, short bushy-forests on fixed dunes (known as "restingas"), and mangroves (INPE/SOS Mata Atlântica 2014). Ecotones occur in contact areas of Caatinga and Atlantic Forest.

Finally, RN contains an important speleological heritage with the occurrence of extensive calcareous outcrops or "lajedos" that harbors numerous caves. Most caves occur in the northern and western region of the state in the Caatinga (Cruz et al. 2010), with the majority of caves located in the NSD ecoregion. RN has the fourth highest number of underground cavities in Brazil with more than 1000 recorded caves (Bento et al. 2017).

2. Data collection

To find bat records within the political boundaries of RN, we searched in regional mammal collections (as primary data) and specialized bibliographic reviews (as secondary data). Primary data consisted of bat records in the mammal collections of the Universidade Federal de Pernambuco (UFPE) and the Universidade Federal of Rio Grande do Norte (UFRN) (Coleção Mastozoológica Adalberto Varela, CMAV). We only considered specimens with voucher number and location (geographic coordinates and municipality). We examined all bat specimens (N = 166) currently deposited at CMAV (except one specimen without specific collection site data), and all bat specimens deposited at UFPE (N = 128) that where collected in RN. The species were identified using taxonomic keys of Neotropical bats, such as Simmons (1996), Gardner (2008), Gregorin & Taddei (2002) and Díaz et al. (2016), as well as the original description of species on scientific articles. Specimens with doubtful identifications were confirmed by experts.

Secondary data were obtained from academic online databases (Google Scholar, Periódicos Capes, ScieELO, Science Direct, and Web of Science) using "Atlantic Forest", "bat", "Caatinga", "Chiroptera", "Mata Atlântica", "morcego", "quiróptero", and "Rio Grande do Norte" as keywords. Also, we consulted books and book chapters that deal with the subject. We compiled all the information available about bats in the state of RN and then selected only records originally published in peer-reviewed literature and books. Among the bat records from peer-reviewed literature and books, we selected only those supported by voucher specimens deposited in public scientific collections. Only the records that met both requirements (publication in peer-reviewed literature/books and availability of vouchers) were included in our list. However, all the bat records found in RN, regardless of presence of voucher specimens, are included in the Supplementary Material.

The species nomenclature and taxonomic arrangement followed Nogueira et al. (2014) and Phyllostomidae species followed Baker et al. (2016). We recognized Lonchophylla inexpectataMoratelli & Dias, 2015 as a different species from Lonchophylla mordax Thomas, 1903 (see Moratelli & Dias 2015). Finally, we assigned for each species its current international and national conservation status following the IUCN Red List of Threatened Species (IUCN 2016) and Brazil Red Book of Threatened Species of Fauna (ICMBio/MMA 2016) respectively; its region (Caatinga and Atlantic Forest) of occurrence; locality(ies) of record(s); literature reference(s) and/or collection number(s) when available.

Results

We found 75 published records, of which 38 satisfied our criteria (peer-reviewed literature/books with voucher specimens), plus 66 unpublished records (CMAV and UFPE collections), totalizing 104 bat records included in the final species list (Table 1) from 141 bat records inspected (Table S1, Supplementary Material). We found records of 50 bat species among the 141 records (Supplementary Materials) and just 42 species according to our criteria for inclusion in the RN list (Table 1). These 42 species represented eight families: Phyllostomidae (23 species), Molossidae (6), Vespertilionidae (5), Emballonuridae (3), Noctilionidae (2), Furipteridae (1), Mormoopidae (1), and Natalidae (1). Eight species cited in the literature did not entered in the official list due to absence of voucher specimens, Peropteryx kappleri Peters, 1867; Saccopteryx canescens Thomas, 1901; S. leptura Thomas, 1901; Anoura caudifer (É. Geoffroy, 1818); Artibeus fimbriatus Gray, 1838; Chiroderma villosum Peters, 1860; Myotis riparius Handley 1960 and M. simus Thomas, 1901.

Records were reported in 21 localities, 18 in the Caatinga and three in the Atlantic Forest (Figure 1). All localities in the Caatinga corresponded to the NSD, with no records for the BH. The state's Caatinga presented an accumulated richness of 32 bat species whereas the Atlantic Forest did 22 species. Nineteen species were exclusive to the Caatinga and nine to the Atlantic Forest (Table 1). The species with the highest number of collected specimens (with voucher numbers) were Myotis lavali (31 specimens), Pteronotus gymnonotus (30), Molossus molossus (28), Artibeus planirostris (26), and Glossophaga soricina (22). The species found in more than one locality were G. soricina (eight localities), Peropteryx macrotis (seven), Myotis lavali (six); and Desmodus rotundus, Carollia perspicillata, and Molossus molossus (four) (Table 1).

Figure 1
Map showing site localities where at least one bat has been sampled within the state of Rio Grande do Norte, northeastern Brazil. Coordinates of localities are: Natal (5º50'16.77" S, 35º12'7.38" W), Macaíba (5º51'19.17" S, 35º12'7.38" W), Maxaranguape (5º26'23.35" S, 35º21'19.26" W), Ceará- Mirim (5º37'40.82" S, 35º26'4.45" W), Taipu (5º36'52.07" S, 35º35'38.54" W), João Câmara (5º31'48.98" S, 35º49'59.06" W), Guamaré (5º7'35.42" S, 36º21'38.56" W), Galinhos (5º5'28.63" S, 36º16'54.60" W), Jandaíra (5º22'47.46" S, 36º 8'45.14" W), Nísia Floresta National Forest (FLONA Nísia Floresta), Nísia Floresta (6º5'5.44." S, 35º11'2.65" W), Lagoa Salgada (6º 8'59.54" S, 35º31'23.24" W), Nova Cruz (6º26'41.54" S, 35º24'7.17" W), Poço Branco (5º37'48.96" S, 35º39'8.31" W), Lajes (5º51'7.17" S, 36º 9'31.45" W), Seridó Ecological Station (ESEC do Seridó), Serra Negra do Norte (6º34'55.46" S, 37º15'9.91" W), Mossoró (5º12'29.13" S, 37º20'50.97" W), Furna Feia National Park (PARNA Furna Feia), Baraúna/Mossoró (5º3'24.13" S, 37º30'54.03" W), Governador Dix-Sept Rosado (5º23'37.14" S, 37º34'8.54" W), Felipe Guerra (5º34'38.75" S, 37º39'57.03" W), Caraúbas (5º41'10.09" S, 37º35'38.00" W), and Martins (6º2'54.68" S, 37º53'43.99" W)

Table 1
List of bat species recorded in the state of Rio Grande do Norte, northeastern Brazil, including conservation status according to International Union for Conservation of Nature (IUCN) and Brazilian Ministry of Environment (Ministério do Meio Ambiente, MMA), localities, voucher numbers and references of original records. Conservation status: LC - Least Concern; DD - Data Deficient; NE - Not Evaluated; NT - Near Threatened, and VU - Vulnerable. Regions are Atlantic Forest (AF) and Caatinga (CA). Localities are: Natal (1), Macaíba (2), Maxaranguape (3), Ceará-Mirim (4), Taipu (5), João Câmara (6), Guamaré (7), Galinhos (8), Jandaíra (9), Nísia Floresta National Forest, Nísia Floresta (10), Lagoa Salgada (11), Nova Cruz (12), Poço Branco (13), Lajes (14), Seridó Ecological Station, Serra Negra do Norte (15), Mossoró (16), Furna Feia National Park, Baraúna/Mossoró (17), Governador Dix-Sept Rosado (18), Felipe Guerra (19), Caraúbas (20), and Martins (21); coordinates are found in Fig. 1. Voucher specimens presented in collection number column correspond to the oldest specimen recorded in each locality. All collection numbers of revised specimens are found in Supplementary table. References in the original record column corresponds to the study who first recorded the species in the state. Collections abbreviations: CAS - California Academy of Science; CMAV - Coleção de Mamíferos Adalberto Varela, Universidade Federal do Rio Grande do Norte; CMUFS - Coleção de Mamíferos da Universidade Federal de Sergipe; MZUSP - Museu de Zoologia da Universidade de São Paulo; UFPB - Coleção de Mamíferos da Universidade Federal da Paraíba; UFPE - Coleção de Mamíferos da Universidade Federal de Pernambuco; USNM - United States National Museum. New species records are indicated with an asterisk (*).

Family/Subfamily/Species	IUCN/MMA	Region		Localities	Collection number	Original record
		AF	CA
Emballonuridae Gervais, 1856
Emballonurinae
Peropteryx leucoptera Peters, 1867	LC	X		10	UFPE 3193	Barros et al. 2017
Peropteryx macrotis (Wagner, 1843)	LC	X	X	1, 9, 13, 14, 18, 19, 20	USNM (not informed), CMAV 111, CMAV 107, CMAV 122, CMAV 130, CMAV 129, CMAV 131	Sanborn 1937; Vargas-Mena et al. in press; This study
Rhynchonycteris naso (Wied-Neuwied, 1820)*	LC		X	13	CMAV 105	This study
Phyllostomidae Gray, 1825
Micronycterinae
Micronycteris megalotis (Gray, 1842) *	LC		X	17	CMAV 134	This study
Micronycteris schmidtorum Sanborn, 1935*	DD		X	15	CMAV 140, CMAV 145	This study
Micronycteris sanborni Simmons, 1996*	LC		X	14	UFPE 3436	This study
Desmodontinae
Desmodus rotundus (É. Geoffroy, 1810)	LC	X	X	6, 10, 13, 17	CMAV 117, UFPE 3306, CMAV 038, CMAV 070	Barros et al. 2017; This study
Diphylla ecaudata Spix, 1823	LC		X	20	CMAV 135	Vargas-Mena et al. in press
Lonchorhininae
Lonchorhina aurita Tomes, 1863	LC/VU		X	19	CMAV 128	Vargas-Mena et al. in press
Phyllostominae
Chrotopterus auritus (Peters, 1856)	LC		X	21	CMUFS 259	Basílio et al. 2017
Lophostoma brasiliense Peters, 1866	LC	X		10	UFPE 2181	Barros et al. 2017
Phyllostomus discolor (Wagner, 1843)	LC	X	X	2, 5, 10	CMAV 018, CMAV 039, UFPE 3247	Barros et al. 2017; This study
Phyllostomus hastatus (Pallas, 1767)	LC	X		10	UFPE 3225	Barros et al. 2017
Tonatia bidens (Spix, 1823)	DD		X	20	CMAV 138	Vargas-Mena et al. in press
Trachops cirrhosus (Spix, 1823)	LC	X	X	10, 14	UFPE 3266, CMAV 069	Barros et al. 2017; This study
Glossophaginae
Anoura geoffroyi Gray, 1838*	LC		X	14	CMAV 144	This study
Glossophaga soricina (Pallas, 1766)	LC	X	X	1, 4, 5, 10, 12, 14, 15, 16	CAS (not informed number), CMAV 015, CMAV 061, UFPE 3257, CMAV 002, CMAV 124, UFPE 3423, CMAV 147	Barros et al. 2017; Vargas-Mena et al. in press; Webster 1993; This study
Lonchophyllinae
Lonchophylla mordax Thomas, 1903*	NT / LC		X	15, 16	CMAV 149, UFPE 3424,	Vargas-Mena et al. in press This study
Lonchophylla inexpectata Moratelli & Dias, 2015*	NE		X	14	CMAV 167	This study
Xeronycteris vieirai Gregorin & Ditchfield, 2005	DD/VU		X	14	CMAV 143	Cordero-Schmidt et al. 2017
Carolliinae
Carollia perspicillata (Linnaeus, 1758)
	LC	X	X	5, 6, 10, 17	CMAV 044, CMAV 120, UFPE 3290, CMAV 136	Barros et al. 2017; This study
Subfamily Stenodermatinae
Artibeus lituratus (Olfers, 1818)	LC	X		1, 10	CMAV 159, UFPE 3288	Barros et al. 2017; This study
Artibeus planirostris (Spix, 1823)	LC	X	X	1, 5, 10, 15	CMAV 004, CMAV 067, UFPE 3200, UFPE 3083	Barros et al. 2017; This study
Dermanura cinerea Gervais, 1856	LC	X		1, 10	USNM (not informed number), UFPE 3299	Barros et al. 2017; Handley 1987
Platyrrhinus lineatus (É. Geoffroy, 1810)	LC	X		1, 10	CMAV 012, UFPE 3208	Barros et al. 2017; This study
Sturnira lilium (É. Geoffroy, 1810)	LC	X		1, 10	CMAV 161, UFPE 3265	Barros et al. 2017; This study
Mormoopidae Saussure, 1860
Pteronotus gymnonotus (Wagner, 1843)
	LC		X	6, 19	CMAV 075, CMAV 125	Vargas-Mena et al. in press; This study
Noctilionidae Gray, 1821
Noctilio albiventris Desmarest, 1818*	LC		X	15	UFPE 3427	This study
Noctilio leporinus (Linnaeus, 1758)*	LC		X	5, 15	CMAV 037, UFPE 3426	This study
Furipteridae Gray, 1866
Furipterus horrens (Cuvier, 1828)	LC / VU		X	17, 20	CMAV 137, CMAV 132	Vargas-Mena et al. in press
Natalidae Gray, 1866
Natalus macrourus (Gervais, 1856)	NT / VU	X	X	1, 16, 19	USNM 242830, CMAV 148, CMAV 126	Goodwin 1959; Vargas-Mena et al. in press
Molossidae P. Gervais, 1856
Molossinae
Molossops temminckii (Burmeister, 1854)*	LC		X	15	UFPE 3433	This study
Molossus molossus (Pallas, 1766)	LC	X	X	1, 2, 8, 11	CMAV 001, CMAV 023, CMAV 152, UFPE 3068	Barros 2014; This study
Neoplatymops mattogrossensis (Vieira, 1942)*	LC		X	15	UFPE 3421	This study
Nyctinomops aurispinosus (Peale, 1848)	LC	X		3	USNM 3726	Shamel 1931
Nyctinomops macrotis (Gray, 1840)*	LC		X	7	CMAV 156	This study
Promops nasutus (Spix, 1823)	LC	X	X	7, 10	CMAV 154, UFPE 3218	Barros et al. 2017; This study
Vespertilionidae Gray, 1821
Vespertilioninae
Eptesicus furinalis (d'Orbigny & Gervais, 1847)*	LC	X	X	1, 8	CMAV 164, CMAV 150	This study
Lasiurus blossevillii ([Lesson, 1826])	LC	X		10	UFPE 3199	Barros et al. 2017
Lasiurus ega (Gervais, 1856)*	LC		X	7	CMAV 151	This study
Myotinae
Myotis lavali Moratelli, Peracchi, Dias & Oliveira, 2011	NE	X	X	1, 2, 6, 8, 10, 15	CMAV 010, CMAV 043, CMAV 005, CMAV 153, UFPE 3181, UFPE 3442	Barros et al. 2017; This study
Myotis nigricans (Schinz, 1821)	LC		X	12	UFPB 1631	Feijó & Nunes 2010

Regarding the conservation status, 31 species are categorized as Least Concern (LC), three as Data Deficient (DD), two as Not Evaluated (NE), and only Natalus macrourus is regarded as Near Threatened (NT) in the IUCN Red List of Threatened Species (IUCN 2016). In the Brazil Red Book of Threatened Species of Fauna (ICMBio/MMA 2016), 34 species are regarded as LC, two as DD, two as NE, and four species are considered Vulnerable (VU), Furipterus horrens, Lonchorhina aurita, Natalus macrourus and Xeronycteris vieira (Table 1).

Of the 42 species of bats presented herein, 13 are new records for RN which are listed below.

Family Emballonuridae Gervais, 1856

Rhynchonycteris naso (Wied-Neuwied, 1820)

The only known records of this species in the state are two specimens collected close to water in the Poço Branco dam (5º37'48.96" S, 35º39'8.31" W) at 65 m a.s.l. on 16 November 1990 in a transition area between the Atlantic Forest and Caatinga. Specimens presented pointed and elongated snout, two light and weak stripes on back and forearms (35.9-37.8 mm) with whitish tufts. Specimens are deposited in CMAV. Specimens examined: CMAV 105, 106.

Family Phyllostomidae Gray, 1825

Subfamily Micronycterinae

Micronycteris megalotis (Gray, 1842)

One specimen collected in a small calcareous outcrop surrounded by scrubby Caatinga vegetation close to the Porco do Mato cave in the Furna Feia National Park, Mossoró-Baraúna municipalities 5º3'24.13" S, 37º30'54.03"W) at 131 m a.s.l. It presented notch in ear band shallow; similar ventral and dorsal fur coloration; calcar longer than foot; and length of hair on the inner edge of the ear >4 mm. Specimen examined: CMAV 134.

Micronycteris schmidtorum Sanborn, 1935

Known from only one locality in Sítio Santa Rosa in Lajes municipality, where two individuals were captured in a riparian Caatinga close to a water dam (05º49'56.2"S, 36º12'16.0"W) at 295 m a.s.l. Both specimens presented ventral fur very pale gray to almost white and calcar (10.2 -10.4mm) longer than the foot (6.5-8.5 mm) which differentiates it from other Micronycteris bats with pale ventral fur (Fig 2A). Specimens examined: CMVA 140, 145.

Figure 2
Ventral pelage of A Micronycteris schmidtorum (CMAV 145) and B Micronycteris sanborni (UFPE 3440). Note very pale gray almost white color of the ventral fur of A that differs from pure white color of B. Lengths of foots, calcars and thumbs of A and B are found in results. Scale bar 10 mm

Micronycteris sanborni Simmons, 1996

Only one recorded site in the Seridó Ecological Station in Serra Negra do Norte municipality (6º34'55.4" S, 37º15'9.91" W) at 200 m a.s.l. One adult male, and two females were collected at the edge of a natural lake in Caatinga vegetation. Specimens presented diagnostic characteristics of M. sanborni: gap between I2 and canine, length of calcar similar or shorter (6.6-8.0 mm) than foot (7.6-8.1 mm), thumb shorter than 7.5 mm (6.8-7.7 mm) and pure white color in ventral fur (Fig 2B). Specimens examined: UFPE 3436, 3439, 3440.

Subfamily Glossophaginae

Anoura geoffroyi Gray, 1838

One male collected in Sítio Joazeiro at 230 m above sea level (a.s.l.) at the foothill of the Serra do Feiticeiro in a semi-open area with patches of scrubby caatinga vegetation, cacti, and some woody trees in Lajes municipality (05º45'55.7"S, 36º12'55.7"W). The specimen presented diagnostic characteristics of A. geoffroyi with no lower incisors, short semicircular uropatagium, and forearm length of 40.2mm. (A. caudifer has forearm of 34-39mm). Specimens examined: CMAV 144.

Subfamily Lonchophyllinae

Lonchophylla inexpectata Moratelli & Dias, 2015

This recently described species was recorded only at the Serra do Feticeiro in Lajes municipality (5º51'7.1"S, 36º9'31.4"W) at 325 m a.s.l. Six specimens were collected and identified as L. inexpectata by their pale-greyish ventral fur on the throat and abdomen that differs from L. mordax which has pale-brownish ventral fur as indicated by Moratelli & Dias (2015) (Fig 3A). Specimens examined: CMAV 121, 123, 141, 142, 146, 167.

Figure 3
Ventral pelage of A Lonchophylla inexpectata (CMAV 167) and B Lonchophylla mordax (CMAV 149). Note the pale-greyish ventral fur on the throat and abdomen of A that differs from the pale-brownish ventral fur of B. Scale bar 10 mm

Family Noctilionidae Gray, 1821

Noctilio albiventris Desmarest, 1818

One adult female collected in the Seridó Ecological Station, Serra Negra do Norte on the edge of a natural lake (6º34'55.4" S, 37º15'9.91" W) at 200 m a.s.l. We also captured an adult in Sítio Santa Rosa, Lajes municipality (05º49'56.2" S, 36º12'16.0" W) in a drying water reservoir on 10 May 2015, but only biometrical data and photographs data were taken. Specimens presented forearm length less than 70 mm (55.7 mm) which differentiates it from the similar but larger N. leporinus (FA: >70 mm) Specimens examined: UFPE 3427.

Noctilio leporinus (Linnaeus, 1758)

Collected only in two localities of Caatinga. The first record is of an adult male collected and deposited in CMAV on 17 January 1990 in Taipu municipality (5º36'52.07" S, 35º35'38.54" W) in an ecotone area close to the BR-404 highway with no habitat specification at 30 m of altitude. The second record corresponds to an adult male captured near a lake (6º34'55.4" S, 37º15'9.91" W) on 18 July 2012 in the Seridó Ecological Station, Serra Negra do Norte municipality at 200 m a.s.l. The specimens presented diagnostic characteristics of N. leporinus, forearm length of >70 mm (82.5-85.4 mm) and legs length exceeding head length that differentiates it from the smaller N. albiventris. Specimens examined: CMAV 037; UFPE 3426.

Family Molossidae Gervais, 1856

Molossops temminckii (Burmeister, 1854)

One adult female captured on 9 March 2013 in an semi-open area in the Seridó Ecological Station (6º34'55.4" S, 37º15'9.91" W) at 200 m a.s.l. It presented triangular ears, semi-squared antitragus and forearm less than 34 mm (30.2 mm), which differentiates it from its congener in Brazil (M. neglectus) that has a forearm greater than 36 mm. Specimen examined: UFPE 3433.

Neoplatymops mattogrossensis (Vieira, 1942)

This molossid bat has been captured only in the Seridó Ecological Station in open areas near a natural lake (6º34'55.4" S, 37º15'9.91" W) at 200 m a.s.l. All six captured specimens presented flattened head, upper incisors separated by a space and granulations or small protrusion in forearms; these characteristics separate N. mattogrossensis from other Neotropical small flat-headed molossids. Specimen examined: UFPE 3421, 3422, 3435, 3437, 3438, 3441.

Nyctinomops macrotis (Gray, 1840)

One adult female found dead on the ground at a wind farm in a coastal Caatinga in Guamaré municipality, north coast of the state (5º7'35.42" S, 36º21'38.56" W) near sea level. The bat presented damages on head, neck and dorsal area probably caused by a direct collision with the turbine blades. The specimen presented deeply wrinkled lips; joined ears; incisors 1/2, upper incisors parallel to each other; and forearm greater than 55mm (FA=58.2 mm), characteristic that differentiates it from other smaller Nyctinomops bats in Brazil (FA<55mm). Specimen examined: CMAV 156.

Family Vespertilionidae Gray, 1821

Eptesicus furinalis (d'Orbigny & Gervais, 1847)

Two specimens collected in different localities. An adult male captured in a house roof in Galinhos municipality in the coastal Caatinga (5º5'28.63" S, 36º16'54.60" W) at sea level and another adult male captured in garden area on the campus of the Federal University of Rio Grande do Norte (5º50'16.77"S, 35º12'7.38"W), at 45 m.a.s.l. Despite specimens presented forearms lengths of 40.1-41.0 mm that overlaps with smaller individuals of E. brasiliensis (forearm length of E. furinalis = 37.0 - 41.0 mm and E. brasiliensis = 40-46 mm), both presented characteristics of E. furinalis, narrow but not tapered tragus, short fur (5-6 mm), lower teeth row length less than 6.3 mm, and skull length less than 16.3 mm. Specimens examined: CMAV 150, 164.

Lasiurus ega (Gervais, 1856)

One adult male found dead at a wind farm in Guamaré municipality (5º7'35.42" S, 36º21'38.56" W) near sea level. The bat had damages on the head and dorsal region, probably caused by a collision with turbine blades; however, the skull suffered no damages. The specimen was identified as L. ega due to its olive-yellowish coloration in ventral and dorsal region; hairs covering down to the half of the uropatagium on the dorsal side; and single upper premolars. Specimen examined: CMAV 151.

Discussion

1. Species richness

The richness of bats in RN is greater than previously known. Of the 38 species of bats previously reported in RN (Feijó & Nunes 2010, Ferreira et al. 2010, Barros 2014, Garcia et al. 2014, Cordero-Schmidt et al. 2016, Basílio et al. 2017, Cordero-Schmidt et al. 2017, Vargas-Mena et al. in press) we found vouchers for only 29 species. However, by adding the 13 new species records that we present herein, the number of species with confirmed occurrence in the state is 42 (Table 1).

Compared to the neighboring states of Ceará and Paraíba, RN presents a lower bat richness. The state of Paraíba, with a diversity of 58 species (Feijó & Langguth 2011, Ferreira et al. 2013, Nunes et al. 2013, Leal et al. 2014, Beltrão et al. 2015, Vilar et al. 2015), is similar to RN in size and proportion of Caatinga and Atlantic Forest, however, it has been more sampled (Bernard et al. 2011). Similarly, the state of Ceará contains a richer bat diversity (66 species) (Gurgel-Filho et al. 2015, Silva et al. 2015), but its bat fauna has been more studied than for RN, including the firsts surveys on Caatingas' mammal communities (e.g., Mares et al. 1981, 1985, Willig 1983).

The bat richness found in RNs' Caatinga was higher than in the states' Atlantic Forest, probably because of the lower number of collection sites in the latter (Fig 1). Since all of sites in Caatinga are in the NSD, our study contributes to fill the knowledge gap in this part of the ecoregion by adding 15 new localities of bat data collection in relation to the records reported by Carvalho-Neto et al. (2016). Previous authors, after reviewing the bat species richness in the Caatinga, warned that the eastern part of the NSD and the north of the BH have not been comprehensively investigated. Based on Velloso et al. (2002) ecoregions of Caatinga, our map (Fig. 1) does not show records in the Borborema Highlands, thus the bat fauna of the northern distribution of this ecoregion is poorly known.

Although the Atlantic Forest showed only three localities of bat collections, the richness difference with the Caatinga is not large - a difference of 10 species. Considering that the Atlantic Forest in Brazil is richer in bat species than the Caatinga (Paglia et al. 2012), it is likely that an increase in research in this region will yield a higher richness than what was found in this study.

Phyllostomid bats represented more than half of the species records (54%). This proportion is similar to other Brazilian states, with the occurrence of Atlantic forest and Caatinga, like in Paraíba (Feijó & Langguth 2011) and Sergipe (Leal et al. 2013). Such dominance was expected since Phyllostomidae is the richest family in Brazil (Nogueira et al. 2014) and in the Neotropics (Solari & Martínez-Arias 2014).

Furthermore, all bat studies in RN were done using mist nets, a type of methodology heavily biased towards the capture of phyllostomids than species of other families (Barnett et al. 2006). Consequently, the diversity of aerial insectivorous bats, such as members of the Emballonuridae, Molossidae, and Vespertilionidae families, are poorly known in RN, probably because all of the studies conducted in RN used mainly mist-nets. Acoustic samplings (recordings of bat echolocation calls) detect aerial insectivores not sampled by conventional capture methods (Simmons & Voss 1998) and, thus, this method should be used together with bat captures to increase inventory completeness (MacSwiney et al. 2008). Moreover, in Neotropical dry forests where nearly half of the species are open-space insectivores, Silva & Bernard (2017) found that different bat species were detected using solely mist nets or bioacoustics, therefore authors conclude that a combination of both techniques is essential to achieve the local bat diversity in Caatinga areas.

The search for day roosts is another good alternative to increase the knowledge on bat species richness of the state. Caves are an important roost for local bat populations considering the high number of underground cavities that occur in RN. Inventories in such areas are likely to provide new species occurrences, and to contribute to a better understanding of the bat species distribution in the state. For instance, 17 species of bats have been already recorded to roost in RN's caves (Vargas-Mena et al. in press, Cordero-Schmidt et al. 2017), this is one-third of the total bat species presented herein.

The bat diversity in Brazil is still being discovered as recent taxonomic revisions of specimens in the biological collections have led to the description of new bat species. For instance, of these recently described species, Myotis lavali (Moratelli et al. 2011) and Lonchophylla inexpectata occur in RN. Myotis lavali was recently described from the Myotis nigricans (Schinz, 1821) complex after specimens' revision in biological collections. We revised M. nigricans specimens from CMAV and UFPE that occur in RN and all of them corresponded to M. lavali. The only record of M. nigricans in the state was provided by Feijó & Nunes (2010) from Nova Cruz municipality, close to Paraíba state; however, we did not have access to the collected specimen to confirm the taxon. Similarly, L. inexpectata was described from L. mordax by Moratelli & Dias (2015) after specimens' revision in biological collection, and is currently considered endemic to Caatinga.

The confirmation of the species that we found in the literature review without vouchered specimens is needed. Of those seven non-confirmed species, for Peropteryx kappleri we did not find any locality or record whatsoever, despite Garcia et al. (2014) record it in the state. The remaining six species were recorded by Farias (2009) (see Supplementary Material) in a small Atlantic Forest patch in the Jiquí Public Park in Parnamirim municipality. Considering the possible presence of these species in the state, we call the attention to future bat studies in the Atlantic Forest to collect and confirm their occurrence.

2. New species records

Here, we presented 13 bat species with no previous record in RN, which increases our knowledge on the occurrence and distribution of the chiropteran fauna of RN and Brazil. Species such as Rhynchonycteris naso, Micronycteris megalotis, M. sanborni, Anoura geoffroyi, Noctilio albiventris, N. leporinus, Molossops temminckii, Neoplatymops mattogrossensis, Eptesicus furinalis, and Lasiurus ega have been already recorded in the neighboring states of Paraíba (Feijó & Langguth 2011) and Ceará (Gurguel-Filho et al. 2015), therefore, their occurrence was expected in RN.

Two pale-bellied species of Micronycteris (M. schmidtorum and M. sanborni) were found to occur in the state (Fig. 2). Both records represent a northward expansion of the distribution of these species in Brazil. Micronycteris schmidtorum has a wide distribution in Brazil but records in the Caatinga are scarce (Rocha et al. 2017) and the closest locality is from Exu, Pernambuco State (Ascorra et al. 1991) - about 430 km from our record in Lajes. However, there is a closer record about 146 km southeast from Lajes in the Atlantic Forest in Guaribas Biological Reserve in Paraíba State (Rocha et al. 2017). M. sanborni is endemic to Brazil and known from 10 scattered localities (Feijó et al. 2015b). We only found it in the Seridó Biological Station and its closest previous record is from 42.6 km south in Patos in the Caatinga of Paraíba State (Feijó et al. 2015b). However, M. sanborni might be more common than previously thought because it is difficult to differentiate from other sympatric pale-bellied Micronycteris bats in Brazil. We encourage special attention when identifying this bat species to avoid misidentification and to better understand their distribution and habitat preferences.

The record of L. inexpectata in RN, specifically at the Serra do Feticeiro in Lajes, expands the distribution of the species northeastwards about 430 km from the closest record in Exu, Pernambuco State (Moratelli & Dias 2015). This record is noteworthy since the species has been registered only in the states of Bahia and Pernambuco (Moratelli & Dias 2015), where it is considered endemic to the Caatinga (Gutiérrez & Marinho-Filho 2017). However, sympatry in certain areas of the Caatinga of L. inexpectata with L. mordax can be found - L. mordax occurs along the eastern border of the Caatinga and the Atlantic Forest-Caatinga ecotone. We found both species in sympatry in Lajes, however its differentiation in the field is fuzzy which difficult identification (R. Moratelli pers. comm.). Although these two species can be differentiated by mandibular length (MAL) and ventral fur color (VFC) (L. mordax, MAL 15.5-17.0 mm, VFC pale brown; L. inexpectata MAL 14.1-16.3 mm, VFC whitish or pale gray on neck and abdomen), the six analyzed specimens of Lonchophylla of Lajes presented overlapping MAL (15.4-16.2 mm). Therefore, external characters for differentiating these species were restricted to the VFC (Fig. 3).

Regarding Nyctinomops macrotis, the species has been recorded mainly in the Atlantic Forest but as well in other regions; in Caatinga it is known for just one locality (Rocha et al. 2015). However, the record of N. macrotis in Guamaré expands the species distribution northeastward about 740 km from the closest record in Boqueirão da Onça in Bahia State (Rocha et al. 2015). This second record suggest that the species might occur in other areas of the Caatinga, thus, acoustic surveys should be done in order to detect this or other molossid bats in RN.

3. Conservation panorama

Four threatened bat species in Brazil occur in RN, corresponding to the 57% of the Brazilian threatened bat species (see ICMBio/MMA 2016). Furipterus horrens, Natalus macrourus, Lonchorhina aurita and Xeronycteris vieirai are vulnerable species (VU), a high extinction risk category (ICMBio/MMA 2016). Moreover, F. horrens and L. aurita roost mainly in caves (Reis et al. 2007), N. macrourus is cave-dependent (Tejedor & Davalos 2016) and, X. vieirai, is only known to roost in caves (Cordero-Schmidt et al. 2017). Therefore, their conservation status is linked to their dependence on cave roosts (Sagot & Chaverri 2015). Bats species that rely on a single roost type are linked to higher extinction risks, and management actions to preserve such species should prioritize the protection of roosting sites (e.g., cave-dependent species) (Sagot & Chaverri 2015). Consequently, the possible presence of these species should be considered when biospeleological inventories and cave-use licensing are carried out in the states' caves.

On the other hand, according to the IUCN international criteria, all bats that occur in RN are at lower risk of extinction, where just N. macrourus and L. mordax are near threatened (NT). This categorization was different from what we found at national level. Such a mismatch between these assessments, where species are considered nationally but not globally threatened, represents cases of globally common and stable species that are rather rare or declining at a local or regional level (Brito et al. 2010). However, L. mordax, previously classified as least concern (LC), is categorized as NT because now its distribution is restricted to just in three localities in eastern Brazil as consequence of its separation with L. inexpectata (Sampaio et al. 2016). Regarding this latter species, the IUCN has not yet evaluated its conservation status in Brazil, and it was therefore not included in threatened species lists (Gutiérrez & Marinho-Filho 2017). Given the endemic condition of L. inexpectata (Caatinga) and L. mordax (Eastern Brazil) their extinction risks should be assessed soon at the national and global level.

The evaluation of the distribution and analysis of pressures and threats to these vulnerable species is needed to assess their conservation needs. For instance, the vulnerable N. macrourus has already lost 54% of its habitat in Brazil, and only 4% of its potential distribution of the species is located within fully protected areas (Delgado-Jaramillo et al. 2017). In RN, only F. horrens and N. macrourus have populations integrally protected in the Furna Feia National Park in Baraúna and Mossoró municipalities (Vargas-Mena et al. in press), while X. vieirai and L. aurita occur in no protected areas.

The natural vegetation in RN has suffered substantial human impacts, only the 11% the state is under some protected area (Bento et al. 2013). The Atlantic Forest has been reduced by agricultural activities and urban expansion in coastal areas (INPE/SOS Mata Atlântica 2014), whereas Caatinga has suffered deforestation for human use and cattle activities that make it susceptible to desertification (Santos et al. 2011). Such human activities are already known to negatively affect the integrity of bat communities and their populations around the world (Furey & Racey 2016). Furthermore, RN has currently 125 wind farms, being the largest producer of wind energy in Brazil (ABBEólica 2017). Wind turbine facilities can cause high mortality among aerial insectivore bats (Barros et al. 2015; Schuster et al. 2015; Hein & Schirmacher 2016; O'Shea et al. 2016; Frick et al. 2017). Bat occurrences in the areas of wind farms, as well as the possible impacts of wind turbines on bats, are still unknown (Bernard et al. 2014). For instance, some of the new species records presented herein (e.g., N. macrotis and L. ega) are based on single specimens found dead probably by wind turbines in wind parks.

4. Main knowledge gaps

Although this study updates information regarding the bat fauna of RN, several gaps of knowledge on the distribution of bat species still remains in the state (Fig 1). Therefore, we propose additional effort of research and inventories in the following areas:

• The Northern Sertaneja Depression: all records of bats in the states' Caatinga are in this ecoregion. According to the distribution of the bat records, however the central region presented the most evident gap, and bat inventories are encouraged in such area. Moreover, most of protected areas of the state are found in this ecoregion and the Seridó Ecological Station in Serra Negra do Norte, the Açu National Forest in Açu and the Furna Feia National Park in Mossoró-Baraúna are areas where the bat fauna is poorly known and should be priorities for inventories in the state.

• The Borborema Highlands and other mountainous ranges in the central and southwestern region: this mountain ranges (ranging from 400-800 m of altitude), characterized by more humid areas with Caatinga vegetations, are virtually unexplored regarding bats, and particular assemblages are expected to occur in these areas. For instance, in the Serra do Feticeiro in Lajes do Cabugi, all five species of nectar feeding bats registered in the state are found in this sierra, including endemic and vulnerable species such as Xeronycteris vieirai and Lonchophylla inexpectata (Cordero-Schmidt et al. 2017). Considering that no conservation units are found in BH and other mountainous ranges, the sierras in the municipalities of Serra de Santana, Cerro Corá, Coronel Ezequiel, São Tomé Martins, Portalegre, Serrinha dos Pintos, and Luís Gomes, should be explored.

• Transitional areas of Caatinga with mangroves and coastal habitats all along the north coast such as in the municipalities of Dunas do Rosado, Galinhos, and Caiçara do Norte are unique ecotones with no data regarding bats, including the State Sustainable Development Reserve (RDS) Ponta do Tubarão, in Macau and Guamaré municipalities.

• Ecotone areas alongside the contact of Caatinga and Atlantic Forest are known as "Agreste", where bat communities may contain a mixture of species of both ecoregions.

• The southeastern region where there are remnants of Atlantic Forest; some of them in protected areas such as Private Reserve of Natural Heritage Mata da Estrela, in Baía Formosa municipality (the largest Atlantic Forest patch of RN), the northern part of the Nísia Floresta National Forest, in Nísia Floresta municipality (Barros et al. 2017), the Environmental Protection Area (APA) Jenipabú in Natal and Extremoz municipalities, and the Dunas State Park in Natal, one of the biggest urban park in Brazil.

• The Mangrove in the east and north coast are also unexplored.

• Finally, the karstic areas located in Mossoró, Baraúna, Felipe Guerra, Apodi, Governador Dix-Sept Rosado, and Jandaíra municipalities are sites with high density of underground cavities and potential sites to roost a wide diversity of bats. For instance, the Furna Feia cave located in the Furna Feia National Park harbors up to 10 species, the richest in the state (Vargas-Mena et al. in press).

Despite the small size of RN, the state has a potential to be an important refuge for bat diversity in northeastern Brazil, as long as bat inventories and specimens' collection increases in the future. Finally, bat inventories, including those for environmental impact studies, should complement conventional capture methods with bioacoustical monitoring and active searching of roost places to obtain a complete understanding of the bat fauna of Rio Grande do Norte.

Acknowledgments

We thanks to National Council for Scientific and Technological Development (CNPq) for research grants (Pesquisador Visitante Especial-PVE Project: 401467/2014-7; and CNPq/ICMBio 13/2011 - Project 552006/2011-4; to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the post-graduation scholarship to JCVM, KAP, MASB, EB and ECS; and CNPq for the productivity grant (309458/2013-7) to EMV. To Wildlife Conservation Society (WCS) Brazil for the logistical support. We are very grateful to Enrico Bernard for providing data of the Seridó Ecological Station; to Francisco Sagot-Martin for donating specimens from the municipality of Guamaré to CMAV; to Edson Leal for providing bibliographic material; to Ricardo Moratelli and Daniela Dias for the discussions and identification of Lonchophylla bats; to Cynthia Christina Ito for the photos of some specimens; to Diego Astúa for allowing the access to the collection; and to Christina M. Smith for English revision of the manuscript. We dedicate this paper to Prof. Adalberto Antônio Varela Freire (in memorian) for his pioneering work in collecting bats of Rio Grande do Norte, which provided most of the material recently organized in the mastozoological collection of the Federal University of Rio Grande do Norte, named - Coleção Mastozoológica Adalberto Varela.

Supplementary material

The following online material is available for this article:

Table S1 - List of bat records (Mammalia, Chiroptera) in the state of Rio Grande do Norte, northeastern Brazil, based on review of literature and specimens in collections. Abbreviations: CAS ‒ California Academy of Science; CMAV ‒ Coleção de Mamíferos Adalberto Varela, Universidade Federal do Rio Grande do Norte; CMUFS ‒ Coleção de Mamíferos da Universidade Federal de Sergipe; MZUSP ‒ Museu de Zoologia da Universidade de São Paulo; UFPB ‒ Coleção de Mamíferos da Universidade Federal da Paraíba; UFPE ‒ Coleção de Mamíferos da Universidade Federal de Pernambuco; USNM ‒ United States National Museum.

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Publication Dates

• Publication in this collection
  2018

History

• Received
  02 Aug 2017
• Reviewed
  06 Mar 2018
• Accepted
  09 Mar 2018