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An important site for conservation of bats in Brazil: Passa Três cave, São Domingos karst area, with an updated checklist for Distrito Federal (DF) and Goiás state
expand article infoMaria Elina Bichuette, Eliana do Amaral Gimenez§, Ives Simões Arnone|, Eleonora Trajano
‡ Universidade Federal de São Carlos, São Carlos, Brazil
§ Faculdades Integradas de Santa Fé do Sul, Santa Fé do Sul, Brazil
| Fundação para a Conservação e a Produção Florestal do Estado de São Paulo, São Paulo, Brazil
Open Access

Abstract

A checklist of bats from Distrito Federal (DF) and Goiás state (GO) and, particularly a single cave (Passa Três cave), located in São Domingos karst area (GO), central Brazil, is presented. Data is based on literature and surveys carried out during 2,000 years. In total, 66 species were recorded, with 30 using caves as shelters. Passa Três cave harbors nine Phyllostomidae species; the most abundant species were Platyrrhinus lineatus, Lonchorhina aurita, Desmodus rotundus and Carollia perspicillata; and the less abundants Trachops cirrhosus, Anoura caudifer and Glossophaga soricina. Besides, the cave is shelter of two threatened bats - Lonchophylla dekeyseri (Endangered category) and Lonchorhina aurita (Vulnerable category), included at Brazilian List of Threatened Fauna, and of a rare species, Lionycteris spurrelli. Passa Três cave shows enough attributes to be considered as a SICOM (Sites of Importance for Conservation of Bats), which would ensure its protection.

Keywords

Mammalia, Chiroptera, Caves, Conservation, central Brazil

Introduction

The Order Chiroptera comprises about 22% of all extant mammals, with more than 1,300 described species (BCI 2018) and currently with 182 species known from Brazil (SBEQ 2018). This number is still increasing, with approximately two new bat species described per year in Brazil in the past two decades (Paglia et al. 2012, Nogueira et al. 2014). In the Cerrado, bats surpass rodents in diversity, with 103 species from all nine families that occur in Brazil (Aguiar and Zortéa 2008), representing more than 50% of all mammal species in this phytophysiognomy. The Cerrado is one of the richest tropical savannas, with a high endemism of plants and birds and a high diversity of vertebrates, being considered a “hotspot” for biodiversity conservation (Mittermeier et al. 1999, Myers et al. 2000). According to Reis et al. (2011), 9% of 195 mammals recorded in the Cerrado are endemic to it. Among bats, the nectarivorous Lonchophylla bokermanni Sazima, Vizotto & Taddei, 1978, was reported as endemic from this hotspot (Nogueira et al. 2014).

The main treats to Cerrado are land expansion for cattle raching, soybean plantations and other land uses that had reduced it to only 20% of the original area (Myers et al. 2000, Strassburg et al. 2017). This can directly affect bat assemblages, changing the habitat structure and reducing shelter and food availability.

Bats use many types of roosts, including caves, rocky crevices, foliage roosts, hollow trees and man-made structures such as the buildings, mines and tunnels (Kunz 1982, Pacheco et al. 2010). For several species, caves are the main roosts (Kunz 1982, Arita 1996, Trajano 1995). Bats are the typical trogloxenes, or organisms that regularly use subterranean habitats but that must return periodically to the surface (in their case, daily to feed) in order to complete their life cycle, and some are obligatory trogloxenes, that depend on caves as obligatory shelters at least during part of their life cycles (Trajano 2012; Trajano and Carvalho 2017). Therefore the conservation of caves and their surrounding are crucial for maintenance of bat populations (Trajano 1995, Arnone 2008, Rocha and Bichuette 2016).

The Red Latinoamericana y del Caribe para la Conservación de los Murciélagos -RELCOM is an international NGO that congregates Latin-American and Caribbean national programs for bat conservation in 22 countries. Among its actions, RELCOM certificates Areas and Sites of Importance for Conservation of Bats (AICOMs and SICOMs), recognized with basis on criteria of diversity, presence of endangered and rare species, maternity colonies, and importance as roosting and migration areas. AICOMs and SICOMs differ only in area size, the latter are smaller. So far, RELCOM certified 80 (64 AICOMs and 16 SICOMs) in 15 countries. However, only recently Brazil have recognized the first and so far the only Brazilian AICOM, the “Alto Ribeira e Alto Paranapanema AICOM”, in southeast São Paulo state, SE Brazil (RELCOM 2017). Although many other Brazilian areas are known to fit the RELCOM criteria for Important Areas and Sites for Bat Conservation, no actions have been undertaken to certificate them.

We present herein a checklist of bat species from Distrito Federal and Goiás state, with data of a short-term study in Passa Três cave, São Domingos karst area, central Brazil and part of a State Park (Terra Ronca State Park - PETeR). We discuss the criteria of proposition of SICOMs and the possibility of application to Passa Três cave.

Brazil has ca. of 17,000 recorded caves (CECAV 2018) and a potential to 100,000 according to Auler et al. (2001), and most of this heritage is under threat by mining and other huge economic purposes, such as hydro electrical projects. The São Domingos karst area, Goiás state, central Brazil, is characterized by the presence of huge cave systems crossed by allochthonous streams, with large amounts of organic matter available for cave organisms, supporting rich aquatic and terrestrial communities (e.g., Bichuette and Trajano 2003, Simões et al. 2013, Bichuette et al. 2015). It is the second most intensively surveyed Brazilian karst area after the Alto Ribeira, but so far no comprehensive study on the bat communities from these caves has been undertaken.

Methods

Study Area

Passa Três cave is located in the Parque Estadual Terra Ronca - PETeR, one of the largest protected areas in Goiás state (Figures 1, 2). The Cerrado phytophysionomy, which is the second largest in Brazil, after Amazonian rainforest, comprises about 2 million km2 (IBGE 2004). There is still significant economic activity represented by cattle rising and agriculture threatening the original Cerrado. Therefore, although the cave is located inside a Conservation Unit, its protection is not warranted.

Figure 1. 

Study area, showing the limits of PETeR (Parque Estadual de Terra Ronca), northeastern state of Goiás, central Brazil. (Map organized in QGIS software, version 2.18, Author: Diego M. von Schimonsky).

The Passa Três cave (GO 14) (Lat -13,60 and Long -46,39), São Domingos County, is a relatively small and confined cave when compared with the cave systems in São Domingos karst area. The cave entrance (sinkhole – Figure 2A), used by the bats for emergence, is about 2.5 m high and 4 m wide; after a flooded low conduit, the cave stream joins the São Vicente I Cave. There are ca. 1.5 km of vadose galleries potential for bat use, mostly the stream conduit, width and height varying from 2 to 8 m, with plenty of concavities and crevices in the ceiling and potential shelters. Stable spelaeoclimate due to spatial confinement and low noise in comparison with larger caves, make Passa Três cave a particularly good shelter.

According to Köeppen classification (1948), the climate is Aw type, with two well-defined seasons: dry (May-September) and wet (October-April), with annual precipitation between 600 and 2,000 mm (Lima and Silva 2005).

Figure 2. 

Passa Três cave, São Domingos karst area, Goiás state, central Brazil. A cave entrance B cave stream conduit close to entrance with short ceiling passages. Photos: M. E. Bichuette.

Sampling

Bats were sampled in three occasions at the Passa Três cave entrance; all in the dry season of 2000 (July 25, September 9 and 14), using one mist net (7× 3 m) at the beginning of the night (4 h total collecting efforts). Bats were euthanized through cervical dislodgment (one specimen or a couple per species) and identified using taxonomic keys (Vizotto and Taddei 1973, Gardner 2008). Vouchers of part of studied (collected) material are deposited in the Vertebrates Collection of Laboratório de Estudos Subterrâneos of Universidade Federal de São Carlos (LESV).

Examined material (part): Anoura caudifer (LESV 0365 and 0366), Platyrrhinus lineatus (LESV 0355 and 0358), Glossophaga soricina (LESV 0356 and 0362), cirrhosus (LESV 0357, 0367 and 0391), Lonchorhina aurita (LESV 0358, 0360), Lionycteris spurrelli (LESV 0359 and 0381), Carollia perspicillata (LESV 0361), Lonchophylla dekeyseri (LESV 0363 and 0364).

Literature review

Secondary data were gathered from literature: Bredt et al. (1999), Esbérard et al. (2001), Esbérard et al. (2005), Zortéa and Tomaz (2006), Reis et al. (2007), Silva et al. (2009), Zortéa and Alho (2008), Silva et al. (2009), Bezerra and Marinho-Filho (2010), Zortéa et al. (2010), Chaves et al. (2012), Reis et al. (2013) and Guimarães (2014).

Following Garbino and Tejedor (2012) and Nogueira et al. (2014), we treat the Natalus species recorded in Brazil as Natalus macrourus (Gervais, 1856), replacing the names N. stramineus (Gray, 1838) and N. espiritosantensis Ruschi, 1951; A. planirostris (Spix, 1823) instead of Artibeus jamaicensis (Leach, 1821); Dermanura cinerea Gervais, 1856 instead of Artibeus cinereus (Gervais, 1856); and Cynamops planirostris (Peters, 1866) instead of Molossops planirostris (Peters, 1865). The list does not include Platyrrhinus helleri (Peters, 1866), which after revision, seems not to occur in Brazil (Velazco et al. 2010, Nogueira et al. 2014).

Results

An updated list of bats for Distrito Federal and Goiás state is shown in Table 1, with 66 species belonging to eight families, including 41 phyllostomids. Among these, 30 species were recorded in caves previously (22 belonging to Phyllostomidae family- see literature cited in Table 1). Two of them are threatened and included in the Brazilian List of Threatened Fauna (MMA 2016): Lonchophylla dekeyseri (Figure 3), Endangered (EN), and Lonchorhina aurita (Figure 4), Vulnerable (VU) and the rare species, Lionycteris spurrelli.

Figure 3. 

Lonchophylla dekeyseri, Endangered species at Brazilian List of Threatened Fauna. Photo: Roberto Leonam Morim Novaes.

Checklist of bats recorded in Distrito Federal and Goiás state. Source: 1 - Bredt et al. (1999), 2 - Esbérard et al. (2001), 3 - Esbérard et al. (2005), 4 - Zortéa and Tomaz (2006), 5 - Reis et al. (2007), 6 - Silva et al. (2009), 7 - Bezerra and Marinho-Filho 2010, 8 - Zortéa et al. (2010), 9 - Chaves et al. (2012), 10 - Reis et al. (2013), 11 - LESV, 12 - Zortéa and Alho (2008), 13 - Guimarães (2014), 14 – Present study. * Species recorded in caves.

Family/Subfamily/Species Data Source
Family Emballonuridae
Subfamily Emballonurinae
Centronycteris maximiliani (Fisher, 1829) 10
Peropteryx macrotis (Wagner, 1843)* 1, 3, 5, 6, 10
Rhynchonycteris naso (Wied-Neuwied, 1820) 10
Saccopteryx bilineata (Temminck, 1838) 10
Saccopteryx leptura (Schreber, 1774) 10
Family Furipteridae
Furipterus horrens (Cuvier, 1828)* 1, 2, 3, 10, 13
Family Mormoopidae
Pteronotus gymnonotus Natterer, 1843* 1, 3, 9, 10, 13
Pteronotus parnellii (Gray, 1843)* 1, 2, 3, 9, 10, 12, 13
Family Natalidae
Natalus macrourus (Gervais, 1856)* 2, 3, 6, 10, 13
Family Noctilionidae
Noctilio leporinus (Linnaeus, 1758) 7, 10
Family Molossidae
Subfamily Molossinae
Cynomops abrasus (Temminck, 1826) 10
Cynomops planirostris (Peters, 1866) 8
Eumops maurus (Thomas, 1901) 10
Molossops temminckii (Burmeister, 1854) 7, 8, 10, 12
Molossus molossus (Pallas, 1766) 10
Neoplatymops mattogrossensis (Vieira, 1942) 10
Family Phyllostomidae
Subfamily Carolliinae
Carollia brevicauda (Schinz, 1821) 10
Carollia perspicillata (Linnaeus, 1758)* 1, 2, 3, 6, 7, 8, 9, 10, 11, 12, 14
Subfamily Desmodontinae
Desmodus rotundus (É. Geoffroy Saint-Hilaire, 1810)* 1, 2, 3, 6, 7, 8, 9, 10, 12, 14
Diaemus youngii (Jentink, 1893) 10
Diphylla ecaudata Spix, 1823* 1, 2, 3, 7, 9
Subfamily Glossophaginae
Anoura caudifer (É. Geoffroy Saint-Hilaire, 1818)* 1, 2, 3, 7, 8, 11, 12, 13, 14
Anoura geoffroyi Gray, 1838* 1, 2, 3, 8, 10, 12
Choeroniscus minor (Peters, 1868)* 3, 10
Glossophaga soricina (Pallas, 1766)* 1, 2, 3, 6, 7, 8, 10, 11, 12, 14
Subfamily “Glyphonycterinae
Glyphonycteris behnii (Peters, 1865) 10, 12
Subfamily Lonchophyllinae
Lonchophylla mordax Thomas, 1903 5
Lonchophylla dekeyseri Taddei, Vizotto & Sazima, 1983* 1, 2, 3, 4, 5, 6, 7, 10, 11, 14
Lionycteris spurrelli Thomas, 1913 2, 5, 10, 11, 14
Subfamily Lonchorhininae
Lonchorhina aurita Thomas, 1863* 1, 2, 3, 5, 6, 9, 10 11, 13, 14
Subfamily Micronycteridae
Micronycteris megalotis (Gray, 1842)* 1, 3, 6, 8, 9, 10
Micronycteris minuta (Gervais, 1856)* 1, 2, 3, 5, 7, 10, 12
Subfamily Phyllostominae
Chrotopterus auritus (Peters, 1856)* 1, 2, 3, 5, 6, 7, 10, 12
Lophostoma brasiliensi Peters, 1866 10, 12
Lophostoma carrikeri (J.A. Allen, 1910) 5, 10
Macrophyllum macrophyllum (Schinz, 1821) 5, 10
Mimon bennettii (Gray, 1838)* 1, 2, 3, 5, 6, 7, 8, 10, 12
Mimon crenulatum (É. Geoffroy Saint-Hilaire, 1803) 8, 12
Tonatia bidens (Spix, 1823) 5, 7
Trachops cirrhosus (Spix, 1823)* 1, 2, 3, 5, 11, 14
Subfamily Stenodermatinae
Artibeus concolor Peters, 1865 4, 5, 10
Artibeus lituratus (Olfers, 1818)* 3, 5, 10, 12
Artibeus obscurus (Schinz, 1821) 5, 7
Artibeus planirostris Spix, 1823* 2, 3, 8, 9, 10, 12
Chiroderma villosum Peters, 1860 10
Chiroderma vizottoi (Taddei & Lim, 2010) 5
Dermanura cinerea Gervais, 1856 5, 8, 10, 12
Mesophylla macconnelli Thomas, 1901 4, 8, 10, 12
Phylloderma stenops (Peters, 1865)* 1, 2, 3, 5, 10
Phyllostomus discolor (Wagner, 1843) 5, 8, 10, 12
Phyllostomus hastatus (Pallas, 1767)* 1, 3, 5, 8, 9, 10, 12
Platyrrhinus incarium (Thomas, 1912) 5, 10
Platyrrhinus lineatus (É. Geoffroy Saint-Hilaire, 1810)* 1, 3, 5, 7, 10, 11, 12, 14
Sturnira lilium (É. Geoffroy Saint-Hilaire, 1810)* 3, 5, 7, 8, 10, 12
Uroderma bilobatum Peters, 1866 5, 10
Uroderma magnirostrum Davis, 1968 5, 7
Vampyressa pusilla (Wagner, 1843)* 3, 5, 10
Family Vespertilionidae
Subfamily Vespertilioninae
Eptesicus diminutus (Osgood 1915) 12
Eptesicus furinalis (d’Orbigny & Gervais, 1847) 7, 8
Eptesicus andinus J.A. Allen, 1914 5, 10
Eptesicus brasiliensis (Demarest, 1819)* 1, 5, 10
Histiotus laephotis Thomas, 1916 5
Histiotus velatus (I. Geoffroy, 1824) 5
Lasiurus blossevillii ([Lesson, 1826]) 5, 10
Lasiurus ega (Gervais, 1856) 10, 12
Myotis nigricans (Schinz, 1821)* 1, 2, 3, 5, 8, 10

We recorded nine species in Passa Três cave (in parenthesis, the number of specimens captured in July/September, both nights combined): Anoura caudifer (0/2), Carollia perspicillata (0/2), Desmodus rotundus (6/8), Glossophaga soricina (2/3), Lionycteris spurrelli (1/0), Lonchophylla dekeyseri (0/4), Lonchorhina aurita (1/1), Platyrrhinus lineatus (11/4) and Trachops cirrhosus (1/2). Pregnant females of P. lineatus and Lonchorhina aurita were captured in July; in September we recorded pregnant females of P. lineatus and T. cirrhosus. Moreover, Passa Três cave is a shelter of two threatened species, Lonchophylla dekeyseri (EN) and Lonchorhina aurita (VU).

Figure 4. 

Lonchorhina aurita, Vulnerable species at Brazilian List of Threatened Fauna. Photo: Roberto Leonam Morim Novaes.

Discussion

Majority of records for Distrito Federal (DF) and Goiás state (GO) are Phyllostomids, as observed by other authors (e.g. Bredt et al. 1999, Bezerra and Marinho-Filho 2010, Carrijo et al. 2011). In a regional scale, more than 40% of the species recorded in DF and GO use caves, which represents about 16% of Brazilian bats (30 of 179), a high percentage compared to other temperate regions.

Considering the Passa Três cave, all species are Phyllostomidae; the most abundant (e.g., Platyrrhinus lineatus, Lonchorhina aurita, Desmodus rotundus and Carollia perspicillata) follow partially the pattern observed in some limestone and sandstone caves in Brazil, when Desmodus rotundus and Carollia perspicillata are the most abundant. In some cases, Phyllostomus hastatus, has shown a high abundance (e.g.,Tocantins, in central Brazil, and Bahia, in northeastern Brazil; M.E. Bichuette, pers. obs.). However, P. hastatus has not been registered in Passa Três cave. The less abundant species (e.g., Trachops cirrhosus, Anoura caudifer and Glossophaga soricina) follow the pattern observed in some karst areas in Brazil (Trajano and Gimenez 1998, Arnone 2008).

Protection of roosting sites is an essential component of any strategy for the conservation of bats, with caves being the main roots for several bat species (Arita 1996, Kunz 1982). On the other hand, bat guano is an important food source for many subterranean organisms, especially for species restricted to subterranean habitats (troglobites), totally dependent on the resources present in these habitats and prone to rapid extinction following any ecological disequilibrium (e.g. alterations in the energy input), even very localized (Trajano 1995). Therefore, protecting bats is a fundamental part of any program or action for conservation of subterranean systems.

Passa Três cave follows the criteria of Site of Importance for Conservation of Bats (SICOM) according to the RELCOM. However, the proposition must be sent to RELCOM coordination for appreciation and validation. The following attributes were observed: presence of two threatened species – Lonchophylla dekeyseri and Lonchorhina aurita; presence of a rare species – Lionycteris spurrelli; a high diversity of bats compared to other caves in Brazil; reproducing colonies of at least three among these species, including the vulnerable L. aurita. Its protection is a priority since the Parque Estadual de Terra Ronca – PETeR has no Management Plan and is impacted by pastures, agriculture and poorly controlled visitation. In addition, the cave is the type-locality of two troglobitic (restricted to subterranean habitats) fishes, both included in the Brazilian Red List of Threatened species, the catfishes Ancistrus cryptophthalmus Reis, 1987 and Ituglanis passensis Fernández and Bichuette 2002 (Teleostei: Siluriformes) (Bichuette and Trajano 2003). Considering its peculiarity and attributes, it is urgent the inclusion of Passa Três in conservation programs, and implementation of monitoring programs.

Acknowledgements

We are grateful to Hertz F. Santos, Dirk Möller, Yvone Meyer-Lucht, Jens Poschadel, and Ramiro H. dos Santos for assistance in fieldwork at São Domingos karst area; to Roberto Leonam Morim Novaes for permission use of photographs of Figures 3 and 4; to Regina Schultz and Arnor V. Mello, Park officials during the study, for the infrastructure and support to carry out this work; to Diego M. von Schimonsky for map confection; to the Secretaria de Meio Ambiente, Recursos Hídricos, Infraestrutura, Cidades e Assuntos Metropolitanos (SECIMA) and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBIO) for the collection permits; to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, #98/13858-1) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, #303715/2011-1) for the financial support to the senior author. We also thank Adarene Motta and Susi Missel Pacheco for suggestions.

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