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Mammalia, Chiroptera, Rio Grande, state of Rio Grande do pecies

1* 2 3 ists L Medvedovisky 4 4, Dimas Gianuca 5, Adriana Gava 4 and Susi Missel Pacheco 6 Fernando Marques Quintela , Chyntia Ibarra , Stefan Vilges de Oliveira , Igor Gonçalves , Fabiano Correa

1 Universidade Federal do Rio Grande do Sul, Instituto de Biociências, Departamento de Zoologia. Avenida Bento Gonçalves 9500, Bairro Agronomia. CEP 91501-970. Porto Alegre, RS, Brasil. 2 Universidade Luterana do Brasil, Campus Canoas, Avenida Farroupilha 8001, Canoas. CEP 92425-900. Canoas, RS, Brasil. 3 MinistRio Grande,ério da RS, Saúde, Brasil. Secretaria de Vigilância em Saúde, Quadra 04 Bloco A. CEP 70304-000. Brasília, DF, Brasil. 4 Universidade Federal do Rio Grande, Instituto de Ciências Biológicas, Laboratório de Limnologia e Genética, Avenida Itália Km 8. CEP 96201-900.

5 Universidade Federal do Rio Grande, Instituto de Oceanografia, Laboratório de Elasmobrânquios e Aves Marinhas, Avenida Itália Km 8. CEP 96201-900. Rio Grande, RS, [email protected] 6 Instituto Sauver. Avenida Pernambuco 2623/404. CEP 90480-090. Porto Alegre, RS, Brasil. * Corresponding author. E-mail: Abstract:

Herein we present a checklist of the bat species recorded in the municipality of Rio Grande, coastal plain of Rio Grande do Sul state. Thirteen species of three families were recorded through field sampling, collection specimen analysis and bibliography compilation. Molossidae and Vespertilionidae, both with five Myotisrecorded albescens species, and were Molossus the most sp. representative families, while three species of Phyllostomidae were recorded. Seven species were found in urban areas. inIn coastalthe sampled areas naturalof southernmost environments, Brazil. six species were found in riparian systems, being recorded only in these formations. Riparian systems, hence, can represent relevant habitats for chiropteran conservation

Introduction Materials and Methods Chiroptera is the second largest mammalian order, The municipality of Rio Grande (31°47’02” – 32°39’45” S, 52°03’50” – 52°41’50” W) is located in Coastal Plain of which comprises around 22% of all the living mammals Rio Grande do Sul state, southern Brazil (Figure 1). The with around 1,120 described species (Simmons 2005), et al. 2011), of which 38 occurring in with average annual temperature of 18.1°C, total annual (Wilsonthe southernmost and Reeder state 2005). of Rio In Brazil, Grande 172 do bat Sul species (Pacheco have et precipitationclimate in the of city 1,162mm is classified (Maluf as humid 2000) sub-temperate, and rainiest albeen. 2007). recorded (Reis

municipalityperiod from July is inserted to September in Campos (Vieira Sulinos 1983). The altitude to northernMost of the and data central concerning regions bat of the species state records (e.g. Santos and 2004).varies from sea level to seven meters (Vieira 1983). The habitat occupancy in Rio Grande do Sul are restricted Species were recorded through captures biome in (IBGE mist 1997; Grillo et al. 2003; Witt et al. 2003; Bernardi et al. nests and diurnal shelters, analysis of specimens stored 1978; Wallauer andet Albuquerque al. 2006; 2007; 1986; Santos Rui et and al. Fabián 2008; Pacheco et al geomorphological2007; 2009; Weber unit of coastal plain, considered as part in collections and bibliography compilation. Field . 2008). In the southern portion of the Domingossampling were Petrolini conducted (31°59’ in S, seven 52°18’ areas, W); (2)being stream them: with (1) conservation in Atlantic Forest and Campos Sulinos human habitations and warehouses in rural locality of of an area of extreme biological importanceet al. for 2000), mammal little in the rural locality of Arraial (31°59’ S, 52°14’ W); (3) biomes herbaceous/shrub riparian vegetation and salt marshes (Conservation International do Brasil effort has been made for the understanding of the richness shrub grasslands, shrub dune formations and human and ecological features of mammalian fauna assemblages. habitations in rural locality of Marinheiros estuarine DesmodusPublished rotundus data on chiropteran occurrenceet al in. 1999), this island (32°00’ S; W 52°06’ W); (4) public squares and importantNyctinomops area laticaudatus have been restricted (É. Geoffroy, to punctual 1805) records (Pacheco of buildings in downtowncampus area Carreiros (32°02’ of S, Universidade 52°05’ W); (5) Federal shrub and Freitas 2003) and (É. MyotisGeoffroy, albescens 1818) (Fabián (É. Geoffroy, 1806) dograsslands, Rio Grande anthropogenic (FURG) (32°04’ shallow S, 52°10’lakes and W); buildings (6) coastal in (Quintela et al. stream,urban locality marshes, of restinga peat wood and sandy riparian restinga 2008). Aiming to contribute to information ofgathering Rio Grande, about southern the chiropteran Rio Grande fauna do inSul this coastal region, plain, we wood in the Área de Proteção Ambiental da Lagoa present a list of bat species recorded in the municipality Verde (APA Lagoa Verde) (32°09’ S; 52°11’ W); (7) human habitations in urban area of Cassino (32°11’ S, 52°09’ W). besides data on habitat occupancy. In October 1998 and from May 2005 to February 2010

Check List | Volume 7 | Issue 4 | 2011 443 Quintela et al. | Chiroptera of Rio Grande, southern Brazil we performed 26 sampling nights utilizing three mist nets Results and Discussion (9 x 3m) per night. Mist nets were installed at the height

We analyzed 110 specimens, 99 from field sampling of 0.5 m inside and at the border of forest fragments, and 11 from the zoological collection of ICB-FURG. These above and adjacent to water bodies and around built areas chiropteranspecimens are richness distributed known in so three far in families, Rio Grande 11 genera do Sul (bridges and buildings), comprising a total effort of 219,024 stateand 13 (Pacheco species (Tableet al 1), which represent 34.2% of the m²/h (Straube and Bianconi 2002). In sampling areas we also verified diurnal shelters (tree hollows, roofs, attics, . 2007). Individuals of 12 species dilatation gaps) in which presence of bats was previously 1).were The collected occurrence in field of Nyctinomops sampling. Four laticaudatus species in were the handidentified and hand by the nets. authors, We also collaborator analyzed specimens researchers from andthe identified in the zoological collection of ICB-FURG (Table locals. Individuals found in shelters were captured by only from literature review (Pacheco and Freitas 2003). municipalityFive species (Taim of Ecological Molossidae Station) were was recorded. determined All didactic collection of the Zoology Laboratory – Institute specimens of Tadarida brasiliensis of Biological Sciences (ICB)-FURG, collected from human and the single specimen of Promops nasutus (Spix, 1823) habitations in Cassino on an unknown date in 1998. (I. Geoffroy, 1824) Voucher specimens were deposited in the Museu de Molossus molossus (Pallas, Ciência e Tecnologia da Pontifícia, Universidade Católica were1766) sampled specimens in shelters were captured in urban in areas, mist whichnets over comprised coastal do Rio Grande do Sul (MCT), Museu de Ciências Naturais, asbestos and ceramic attics. Universidade Luterana do Brasil (MCNU) and Instituto Three specimens were also found dead in downtown Sauver (CIS). Collection was authorized by Chico Mendes sidewalksstream with after riparian storms. wood A single and building specimen dilatation of the genus gaps. Institute (ICMBio: process no. 325-1). Individuals were Molossus É. Geoffoy, 1805, which may represent a taxon identified according to La Val (1973),et al Vizotto. (2011). and Taddei Molossus (1973), Gregorin and Taddei (2002) and Barquez and Díaz (2009). Nomenclature follows Reis still not formally described (herein assigned as

Figure 1.

Location of Rio Grande do Sul state in Brazil (A), part of coastal plain (B) and sampled localities in the municipality of Rio Grande (C): Domingos Petrolini (1), Arraial (2), Marinheiros Island (3), downtown area (4), Campus Carreiros of Universidade Federal do Rio Grande (FURG) (5), Lagoa Verde Environmental Protection Area (6), Cassino (7). Check List | Volume 7 | Issue 4 | 2011 444 Quintela et al. | Chiroptera of Rio Grande, southern Brazil sp.), was captured in mist nets over coastal stream with insectivorous guild of vespertilionids and molossids. riparian wood. All of the species recorded in the present study were et al Histiotus velatus individuals were capturedFive speciesin mist nets of over Vespertlionidae stream with wereriparian registered. wood. A Riocited Grande by Pacheco and other 21. (2007) municipalities as occurring in southern in Piratini- Rio (I. Geoffroy, 1824) GrandeMirim-São do Sul.Gonçalo Moreover, hydrographic Pacheco etbasin, al. (2007) which pointed comprises out Eptesicus diminutus Acolony single was individual found inhabiting of Eptesicus the gaps brasiliensis of a ceramic (Desmarest, roof in a , Histiotus montanus 1819)warehouse was capturedlocated in in the mist middle net over of herbaceous sandy riparian grassland. wood, 1861)the occurrence, Lasiurus of cinereusother five (Palisot species de( Beauvois, 1796), while another one was found dead in an attic with ceramic Osgood,Lasiurus 1915ega (Gervais, 1855) and Myotis(Philippi levis & Landbeck, Myotis albescens 1824)) (1955) cited the occurrence of Chrotopterus(I. Geoffroy, auritus roof in urban area. A single individual of (Peters, in1856) Piritani-Mirin-São and Myotis ruber Gonçalo (É Geoffroy, basin, 1806) while Vieirain the reportedwas captured in a in preliminary mist net over phase coastal of thisstream study with (Quintela shrub/ etherbaceous al. 2008). riparian Two specimens vegetation, of Myotis which nigricans was previously (Schinz, vegetal physiognomy to that of Rio Grande and is located county of São Lourenço do Sul, which presents a similar with sandy riparian wood, while another specimen was captured1821) were in found mist netdead in in a a marsh bridge area. over Ana coastal individual stream of additionalabout 100 samplingkm away. effort Considering may increase the large de area species and thelist Lasiurus blossevillii hereinhabitat presented. heterogeneity of Rio Grande, it is possible that Four vespertilionids (E. brasiliensis, H. velatus, M. island. (Lesson & Garnot, 1826) was captured albescens and M. nigricans) and two molossids (Molossus sp. in aThree shrub species dune formation of the Phyllostomidae in the Marinheiros were recorded.estuarine and M. molossus), which correspond to 46% of the richness Specimens of Glossophaga soricina (Pallas, 1766) were found in the studied area, were recorded in riparian captured in attics with ceramic roof and mist nets formations. These were also the only environments where M. albescens and Molossus sp. were recorded. Myotis albescens singleinstalled specimen around ofit, Sturnira in shrub lilium grasslands (É. Geoffroy, of rural 1810) areas. was A status evaluation in Rio Grande do Sul (Pacheco and single specimen was found in ceramic roof in urban area. A Freitas 2003),is considered while Molossus as Data sp. Deficient may represent for conservation a species single specimen of Desmodus rotundus was captured in a captured in mist net in a public square in urban area. A play an important role in maintenance of chiropteran The higher richness of Molossidae in relation to other diversitynot yet described. in the region, In this hosting regard, populations riparian systems of species may stable in herbaceous grassland of rural area. which are naturally rare or not tolerant to high anthropic families in the present study did not corroborate with the great majority of previous surveys in e.g. urban Reis and et al. natural 2000; disturbance.Sturnira lilium Pacheco, P. nasutusand Marques and T. (2006) brasiliensis also emphasize lack data environmentsBaptista and Mello of Brazilian 2001; biomes,Dias et alwhere a clear dominanceet al. the importance of riparian forests for bat conservation. 2005;of Phyllostomidae Barros et al species. 2006; is Bordignon observed ( 2006; Arnone and Passos 2007; Andrade et al. 2008;. Gregorin2002; De etKnegt al. 2008; municipality.on natural habitat Captures occupancy of M. molossusin Rio Grande, and E. once brasiliensis all the Carvalho et al capturesand the presence of these ofspecies G. soricina occurred, H. velatus in urban and areasM. molossus of the representativeness in the studied area is also contrasting with the previous. 2009). studiesBeside Molossidae, aforementioned. Vespertilionidae However, N. inlaticaudatus the ICB-FURG collection also indicate the occurrence of of Frederico Westphalen, northernmost Rio Grande do Sul these species in urban areas. All of theseet al. species and (BernardiVespertilionidae et al. was the richest family in the municipality 2007; Pacheco are etcited al. as occurring in urban etareas al. (Santos (2002) also1978; pointed Bredt 1998;out that Silva N. laticaudatus1994; Weber commonly 2007; roosts Zortéa in in Rio Grande do 2009). Sul (Pacheco In a broader et al. 2007) geographical and Uruguay scale, 2010). Avila-Flores (AchavalVespertilionidae et al. 2007), is also which the suggests most representative a differentiation family in this case, N. laticaudatus hollows and crevices in modern man-madeS. lilium structures., Gannon Inet when compared to Phyllostomidae predominance in al. (1989) cite the occurrence can also of occur the in species highly mainlydisturbed in morebat species setentrional composition physiognomies in these such subtropical as Atlantic domains Forest areas of Rio Grande. In relation to hollow trees (Gannon et al. 1989; Fenton et al. 2000), forested habitats, while identified diurnal roosts includeet al. state(Emmons that there and Feeris a decrease 1997; Marinho-Filhoin Phyllostomidae 1996a) richness and 2000). Considering these aspects, it is supposed that Cerrado (Marinho-Filho 1996b). Willig and Selcer (1989) vineS. lilium tangles may and occur bases in restinga of palm forest fronds formations (Fenton of the richness within the higher latitudes. Furthermore, we also municipality. and an increase in Vesperlionidae and Molossidae dominance patterns, with a clear reduction of frugivorous inobserve Campos a severe Sulinos differentiation when compared in trophicto Atlantic guild Forest richness and a municipalityIn this study we inserted present in the an first area assessment with recognized of species importancerichness and for habitat mammalian occupancy conservation. by bats The in Rio application Grande, of appropriate methods can therefore reveal relevant representCerrado. In a Campos limiting Sulinos, factor forclimate frugivorous features phyllostomidsand reduction richness,of arboreal which vegetation, resulted in including the pattern fruiting of dominance trees, may of data on species abundance and ecology in the diversity of Check List | Volume 7 | Issue 4 | 2011 habitats of this coastal area. 445 Quintela et al. | Chiroptera of Rio Grande, southern Brazil

Table 1. et al. 1999; Pacheco and Freitas 2003; Quintela et al. Families and species of bats recorded in the municipality of Rio Grande, Rio Grande do Sul State, being: a = field sampling, b = IB-FURG collection, c = previous records (Fabian 2008); MN = number of specimens captured in mist nets, DR = number of specimens captured in diurnal roosts, DS = number of dead specimens found in habitats, IB = number of individuals stored in IB-FURG collection; Hg = herbaceous grassland, Rw = stream with sandy riparian wood, Rh = stream with herbaceous/arbustive riparian vegetation, Sd = shrub dune, Sg = shrub grassland, Sw = swamp, Ua =TAXON urban area, ? = no data available.RECORD MN DR DS IB HABITAT Phyllostomidae

Desmodus rotundus (É. Geoffroy, 1818) a,c 1 Hg

Glossophaga soricina (Pallas, 1766) 8 17 1 Sg, Ua

Sturnira lilium (É. Geoffroy, 1810) a,bA 1 Ua Molossidae

Molossus molossus (Pallas, 1766) 11 3 2 Rw, Ua

Molossus sp. a,bA 1 Rw Nyctinomops laticaudatus (É. Geoffroy, 1805) C ?

Promops nasutus (Spix, 1823) A 1 Ua

Tadarida brasiliensis 40 7 Ua

Vespertilionidae (I. Geoffroy, 1824) a,b Eptesicus brasiliensis (Desmarest, 1819) A 1 Rw, Ua

Histiotus velatus 7 2 1 Rw, Ua

Lasiurus blossevillii (I. Geoffroy, 1824) a,bA 1 Sd

Myotis albescens (É. Geoffroy,(Lesson & 1806) Garnot, 1826) A 1 Rh Myotis nigricans (Schinz, 1821) A 1 2 Rw, Sw

Acknowledgments:

We are grateful to Eduardo Martins da Silva, Flávio Conservation Internacional do Brasil, Fundação SOS Mata Atlântica, Visnardi-Filho, Rafael Martins Pinheiro, Vanice Gutierrez, Alexandro Fundação Biodiversitas, Instituto. 2000. deAvaliação Pesquisas e ações Ecológicas, prioritárias Secretaria para Marques Tozetti and Maurício Beux Santos for help in fieldwork, Ana ado conservação Meio Ambiente da biodiversidade do Estado de da São Mata Paulo Atlântica and SEMAD/e Campos Instituto Sulinos. Catarina de Oliveira and Cristina Loyola Zardo for lab support and Maria Estadual de Florestas MG EduardaLiterature Carvalho Cited for English review. Mamíferos de la República Brasília: Ministério do Meio Ambiente. 40 p. Arquivo Oriental del Uruguay, guia fotográfica De Knegt,Brasileiro L.V., de J.A. Medicina Silva, E.C.Veterinária Moreira e Zootecnia and G.L. Sales. 2005. Morcegos Achaval, F., M. Clara and M.C. Olmos. 2007. G.B. capturados no município de Belo Horizonte, 1999-2003. 2008. . 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Arquivos de conservation. Chiroptera Neotropical Zoologia Marinho-Filho, J. 1996b. The Brazilian Cerrado bat fauna andIn C.S. its Vieira,ieira C.C..F. 1983. 1955. Rio Lista Grande: remissiva geografia dos mamíferosfísica, humana do Brasil.e econômica . Porto 2(1): 37-39.Livro vermelho da fauna 8: 341-474. Pacheco,ameaçada S.M. andde extinção T.R.O. Freitas. no Rio Grande 2003. Quirópteros;do Sul p. 493-498 V , E 1973. Chave para determinação de Fontana, G.A. Bencke and R.E. Reis (ed.). Alegre: Sagra. 158 p. Boletim de Ciências, Faculdade de Filosofa, . Porto Alegre: Edipucrs. Vizotto,Ciências L.D. e Letras and V.A. Taddei. Pacheco,status S.M., do conhecimento M. Sodré, A.R. e Gama, plano deA. Bredt,ação para E.M. a Cavallini-Sanches,conservação no Brasil. R.V. quirópteros brasileiros. ChiropteraMarques, M.M. Neotropical Guimarães and G. Bianconi. 2010. Morcegos urbanos: 1:1-72. Wallauer,Rio Grande J.P. and do E.P. Sul, Albuquerque Brasil. Roessléria. 1986. Lista preliminar dos mamíferos 16(1):In 630-647. observados no Parque Florestal Estadual do Turvo, Tenente Portela, Pacheco,A. Christoff S.M. and (ed.). R.V. Mamíferos Marques. 2006.do Brasil: Conservação genética, sistemática,de morcegos ecologia no Rio Mammalia, Chiroptera, 8: 179-185. Phyllostomidae, Platyrrhinus eGrande conservação. do Sul; p. 91-106. T.R.O. Freitas, E. Vieira, S.M. Pacheco and Weber,lineatus M.M., N.C. Cáceres, D.O. Lima, V.L. Camilotti, C. Roman and L.T. CheckNeto. List 2006. São Carlos: Suprema. : Range expansion to the state of Rio Grande do Sul, Brazil. Pacheco, S.M., M.L. Sekiama, K.P.A.Ciência Oliveira, e Ambiente F. Quintela, M.M. Weber, 2(3): 96-98. R.V. Marques, D. Geiger and D.D. Silveira. 2007. Biogeografa de Weber,Grande M.M., do J. ArrudaSul, Brasil. and Biota N.C. Cáceres.Neotropica 2007. Ampliação da distribuição quirópteros da Região Sul. 35: 181-202. de quatro espécies de morcegos Mammal (Mammalia, species Chiroptera) of the world: no Rio A Pacheco, S.M., R.V.In Marques, G.V. Bianconi, M. Miretzki, A.A. Witt and K.P.A.(ed.). taxonomic and geographic reference 7(2):. 293-296. Oliveira.Morcegos 2008. no Brasil: Morcegos Biologia, de Floresta Sistemática, com Araucária ecologia no e sul conservação do Brasil;. Wilson,University D.E. and Press. D.M. Reeder. 2005. p. 351-360. S.M. Pacheco, R.V. Marques and C.E.L. Esberard Baltimore: JohnsHopkins Quintela, F.M., R.A. Porciuncula and S.M. Pacheco. 2008. Mammalia, Journal of Biogeography Porto Alegre: Armazém Digital.Myotis 575 p. albescens Willig, R.J. and K.W. Selcer. 1989. Bat species density gradients in the New in the state of Rio Grande do Sul, Brazil. Check List World: a statistical assessment. 16: 189-195. Chiroptera, Vespertilionidae, : new occurrenceMamíferos site do Witt, A.A., S.M. Pacheco, I.A. Accordi, G. Vinciprova,Divulgações A. Barcellos-Silveira do Museu de Brasil. 2a 4(1):79-81. Ciênciaand J.M. e Sá. Tecnologia 2003. Uso UBEA/PUCRS, de cavernas Publicaçãopor quirópteros Especial na região do Alto Reis, N.R., A.L. Peracchi, W.A. Pedro and I.P. Lima. 2011. Uruguai,, Noroeste do Rio Grande do Sul. In ed. Londrina: Nelio R. dos Reis. 439 p. Morcegos 2: 52. do Brasil. Reis, N.R., A.L. Peracchi, M.L. Revista Sekiama Brasileira and I.P. Lima.de Zoologia 2000. Diversidade Zortéa M. 2007. Subfamília Stenodermatinae; p. 107-128 Reis, N.R., 704.de morcegos (Chiroptera, Mammalia) em fragmentos florestais no A.L. Peracchi, W.A. Pedro and I.P. Lima (ed.). estado do Paraná, Brasil. 17(3): 697- Londrina: Universidade Estadual de Londrina.

Rui, Brasil.A.M. and Chiroptera M.E. Fabián. Neotropical 1997. Quirópteros de la familia Phyllostomidae Santos(Mammalia,, Chiroptera) en selvas del Estado de Rio Grande do Sul, Received: February 2011 3:75-77. Estudos Leopoldenses Last Revised: June 2011 127. A. B. 1978. Identificação e dados bio-ecológicos dos quirópteros Accepted: June 2011 do Vale do Rio dos Sinos e Arredores. 13: 76- Published online: July 2011 Editorial responsibility: Marcelo Rodrigues Nogueira Santos,Grande T. G., do M.R.Sul, Brasil. Spies, Biota K. Kopp, Neotropica R. Trevisan and S.Z. Cechin. 2008. SilvaMamíferos, F. 1994. Mamíferosdo Campus silvestres da Universidade do Rio Grande Federal do de Sul Santa Maria, Rio Appendix 1. 8(1): 1-7. Desmodus rotundus Glossophaga soricin In . Porto Alegre: Voucher list. Sturnira lilium Molossus D.M.Fundação Reeder Zoobotânica ed Mammal do Rio species Grande of do the Sul. world: 246 p. A taxonomic and molossus : (MCNU 2448); Molossus sp.a (MCNU (MCT 1725);2538- Simmons,geographic N.B. 2005.reference Order. Chiroptera; JohnsHopkins p: 312-529. University D.E. Wilson Press. and Tadarida42, MCNU brasiliensis 2551, MCT 1720); (CIS 0059); ( .). MCT 1724); (MCNU Eptesicus 2523-4, brasiliensis MCT 1726-8); Histiotus velatus Baltimore: (MCNULasiurus 2543-46, blossevillii MCNU 2549-50, MyotisMCNU albescens2555-58, Straube, F.C. Chiroptera and G.V. Bianconi.Neotropical 2002. Sobre a grandeza e a unidade (MCT 1721); Myotis nigricans (MCNU 2552); (MCNU utilizada para estimar esforço de captura com utilização de redes-de- 2559-66, MCT 1723); (CIS 0098); neblina. 8: 150-152. (MCNU 2547).

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