Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter May 24, 2016

Seasonality and habitat influence on bat assemblage structure in an urban Atlantic Forest remnant from Southeastern Brazil

Roberto Leonan M. Novaes EMAIL logo , Renan F. Souza , Saulo Felix , André C. Siqueira , Rafael S. Laurindo , Luis Fernando Menezes and Julie T. Shapiro
From the journal Mammalia


The Brazilian Atlantic Forest is a severely threatened biodiversity hotspot and many remnants exist only as fragments. In order to understand how bat assemblage structure within a forest fragment surrounded by an urban matrix might respond to seasonality and different habitats, we sampled bats over 39 nights in the forest fragment of Gericinó-Mendanha Massif, Rio de Janeiro State. From February 2006 to January 2010, we captured 874 bats, belonging to 25 species and eight different feeding guilds. Frugivorous species were the most abundant, representing 83.33% of captures, and the gleaning insectivores were the least abundant (1.47%). We did not find changes in bat species composition between seasons, although capture rate was higher in the rainy season. However, we did find significant differences in species abundance between seasons. The habitat influence did not significantly differentiate the assemblages, but species richness was higher in the mature ombrophilous forest. The community composition indicates that this conservation unit is an important remaining fragment for maintaining the diversity and richness of bats, although it is possible that historical processes of environmental exploitation have already resulted in a loss of species.


We are grateful to Ana C. Façanha, Flávio A.P. Mello, Luiz Fernando Dias-de-Oliveira, Luzianne Gomes, Mariana A.S. Louro, Mariana V.P. Aguiar, Paula C. Andrade, Raphael Silvares, Rogério Guedes, Tatiane S. Cardoso, Tiago Lobo and Vinícius de Bruycker for the fieldwork assistance; to SEMUAM/Nova Iguaçu for the research license in the Parque Natural Municipal de Nova Iguaçu (N001/2010). This project was also carried out with the support of Zootech®.


Appendix 1: Bats from Gericinó-Mendanha Massif deposited in the collection of bats Adriano Lucio Peracchi (ALP) of the Institute of Biology, Universidade Federal Rural do Rio de Janeiro, Brazil.

Phyllostomidae:Artibeus fimbriatus (ALP6791, ALP9470); Artibeus lituratus (ALP6790, ALP9471, ALP9472, ALP9473, ALP9474); Artibeus obscurus (ALP9475); Chiroderma doriae (ALP6785); Platyrrhinus lineatus (ALP9476); Platyrrhinus recifinus (ALP6792, ALP9477, ALP9478); Pygoderma bilabiatum (ALP9479, ALP9480); Sturnira lilium (ALP6789, ALP9481, ALP9482); Vampyressa pusilla (ALP6787, ALP9483); Desmodus rotundus (ALP6793, ALP9484, ALP9485); Anoura caudifer (ALP6786, ALP9486); Anoura geoffroyi (ALP9487); Glossophaga soricina (ALP6794, ALP9488); Lonchophylla peracchii (ALP9489, ALP9490); Carollia perspicillata (ALP6788, ALP9491, ALP9492, ALP9493, ALP9494); Micronycteris microtis (ALP9495); Micronycteris minuta (ALP9496); Phyllostomus hastatus (ALP6784, ALP9497); Tonatia bidens (ALP9498, ALP9499); Molossidae:Molossus molossus (ALP6795, ALP6796, ALP9500, ALP9501); Vespertilionidae:Eptesicus brasiliensis (ALP6821), Myotis nigricans (ALP6797, ALP9502, ALP9503, ALP9504, ALP9505, ALP9506, ALP9507); Myotis riparius (ALP9508, ALP9509, ALP9510).


Aguiar, L.M.S. and J.S. Marinho-Filho. 2007. Bat frugivory in a remnant of Southeastern Brazilian Atlantic Forest. Acta Chiropterol. 9: 251–260.10.3161/1733-5329(2007)9[251:BFIARO]2.0.CO;2Search in Google Scholar

Andrade, T.Y., W. Thies, P.K. Rogeri, E.K.V. Kalko and M.A.R. Mello. 2013. Hierarchiral fruit selection by Neotropical leaf-nosed bats (Chiroptera: Phyllostomidae). J. Mammal. 94: 1094–1101.10.1644/12-MAMM-A-244.1Search in Google Scholar

Asbjornsen H., M.S. Ashton, D.J. Voigt and S. Palacios. 2004. Effects of habitat fragmentation on the buffering capacity of edge environments in a seasonally dry tropical oak forest ecossystem in Oaxaca, Mexico. Agric. Ecosyst. Environ. 103: 481–495.10.1016/j.agee.2003.11.008Search in Google Scholar

Bernard, E. and M.B. Fenton. 2002. Bat mobility and roosts in a fragmented landscape in Central Amazonia, Brazil. Biotrop. 35: 262–277.10.1111/j.1744-7429.2003.tb00285.xSearch in Google Scholar

Bernard, E., L.M.S. Aguiar and R.B. Machado. 2011. Discovering the Brazilian bat fauna: a task for two centuries? Mammal Rev. 41: 23–39.10.1111/j.1365-2907.2010.00164.xSearch in Google Scholar

Bowen-Jones, E. and A. Entwistle. 2002. Identifying appropriate flagship species: the importance of culture and local contexts. Oryx 36: 189–195.10.1017/S0030605302000261Search in Google Scholar

Chiarello, A.G. 1999. Effects of fragmentation of the Atlantic Forest on mammal communities in South-eastern Brazil. Biol. Cons. 89: 71–82.10.1016/S0006-3207(98)00130-XSearch in Google Scholar

Clarke, K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Austral Ecol. 18: 117–143.10.1111/j.1442-9993.1993.tb00438.xSearch in Google Scholar

Colwell, R.K. 2013. EstimateS: statistical estimation of species richness and shared species from samples. Version 9.0. User’s guide and application published at: in Google Scholar

Costa, L.O., Y.L.R. Leite, S.L. Mendes and A.D. Ditchfield. 2005. Mammal conservation in Brazil. Conserv. Biol. 19: 672–679.10.1111/j.1523-1739.2005.00666.xSearch in Google Scholar

Costa, L.M., A.F.D. Prata, D. Moraes, C.F.V. Conde, T. Jordão-Nogueira and C.E.L. Esbérard. 2006. Deslocamento de Artibeus fimbriatus sobre o mar. Chirop. Neotrop. 12: 289–290.Search in Google Scholar

Costa, L.M., J. Almeida and C.E.L. Esbérard. 2007. Dados de reprodução de Platyrrhinus lineatus em estudo de longo prazo no Estado do Rio de Janeiro (Mammalia, Chiroptera, Phyllostomidae). Iheringia. Ser. Zool. 97: 152–156.10.1590/S0073-47212007000200004Search in Google Scholar

Dias, D., A.L. Peracchi and S.S.P. Silva. 2002. Quirópteros do Parque Estadual da Pedra Branca, Rio de Janeiro, Brasil (Mammalia, Chiroptera). Rev. bras. Zool. 19: 113–140.10.1590/S0101-81752002000600012Search in Google Scholar

Dias, D., C.E.L. Esbérard and A.L. Peracchi. 2008. Riqueza, diversidade de espécies e variação altitudinal de morcegos na Reserva Biológica do Tinguá, estado do Rio de Janeiro, Brasil (Mammalia, Chiroptera). In: (N.R. Reis, A.L. Peracchi and G.A.S. Santos, eds.) Ecologia de Morcegos. Editora Technical Books, Rio de Janeiro, Brazil. pp. 97–108.Search in Google Scholar

Dias, D., C.E.L. Esbérard and R. Moratelli. 2013. A new species of Lonchophylla (Chiroptera, Phyllostomidae) from the Atlantic Forest of southeastern Brazil, with comments on L. bokermanni. Zootaxa 3722: 347–360.10.11646/zootaxa.3722.3.4Search in Google Scholar

Esbérard, C.E.L. 2003. Diversidade de morcegos em área de Mata Atlântica regenerada no sudeste do Brasil. Rev. bras. Zoociên. 5: 189–204.Search in Google Scholar

Esbérard, C.E.L. and C. Daemon. 1999. Um novo método para marcação de morcegos. Chirop. Neotrop. 5: 116–117.Search in Google Scholar

Esbérard, C.E.L., M. Baptista, L.M. Costa, J.L. Luz and E.C. Lourenço. 2010. Morcegos de Paraíso do Tobias, Miracema, Rio de Janeiro. Biota Neotrop. 10: 249–255.10.1590/S1676-06032010000400030Search in Google Scholar

Esbérard, C.E.L., G.P. Freitas, J.L. Luz, K.M. Costa and L.N. Freitas. 2011. Intervalos máximos entre captura e recaptura de morcegos no estado do Rio de Janeiro, sudeste do Brasil. Chirop. Neotrop. 17: 957–962.Search in Google Scholar

Estrada, A. and R. Coates-Estrada. 2002. Bats in continuous forest, forest fragments and in an agricultural mosaic habitat-island at Los Tuxtlas, Mexico. Biol. Conserv. 103: 237–245.10.1016/S0006-3207(01)00135-5Search in Google Scholar

Godoy, M.S., W.D. Carvalho and C.E.L. Esbérard. 2014. Reproductive biology of the bat Sturnira lilium (Chiroptera, Phyllostomidae) in the Atlantic Forest of Rio de Janeiro, southeastern Brazil. Braz. J. Biol. 74: 913–922.10.1590/1519-6984.22612Search in Google Scholar PubMed

Gomes, L.A.C., A.S. Pires, M.A. Martins, E.C. Lourenço and A.L. Peracchi. 2014. Species composition and seasonal variation in abundance of Phyllostomidae bats (Chiroptera) in an Atlantic Forest remnant, southeastern Brazil. Mammalia 79: 1564–1547.10.1515/mammalia-2013-0108Search in Google Scholar

Gorresen, P.M. and M.R. Willig. 2004. Landscape responses of bats to habitat fragmentation in Atlantic Forest of Paraguay. J. Mammal. 85: 688–697.10.1644/BWG-125Search in Google Scholar

Hammer, Ø., D.A.T. Harper and P.D. Ryan. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Elect. 4: 1–9.Search in Google Scholar

IBGE (Instituto Brasileiro de Geografia e Estatística). 2012. Manual técnico da vegetação brasileira, 2aed. IBGE, Rio de Janeiro, Brazil. pp. 271.Search in Google Scholar

Kalko, E.K.V., CO. Handley Jr. and D. Handley. 1996. Organization, diversity, and long-term dynamics of a neotropical bat community. In (M.L. Cody and J.A. Smallwood, eds.) Long-term studies of vertebrate communities. Academic Press, New York, NY. pp. 503–553.10.1016/B978-012178075-3/50017-9Search in Google Scholar

Marques, J.T., M.J. Ramos-Pereira and J.M. Palmeirim. 2015. Patterns in the use of rainforest vertical space by Neotropical aerial insectivorous bats: all the action is up in the canopy. Ecography 38: 1–11.10.1111/ecog.01453Search in Google Scholar

Mello, M.A.R., W.R. Silva and E.K.V. Kalko. 2008. Movements of the bat Sturnira lilium and its role as a seed disperser of Solanaceae in the Brazilian Atlantic forest. J. Trop. Ecol. 24: 225–228.10.1017/S026646740800480XSearch in Google Scholar

Mello, M.A.R., E.K.V. Kalko and W.R. Silva. 2009. Ambient temperature is more important than food availability in explaining reproductive timing of the bat Sturnira lilium (Mammalia: Chiroptera) in a montane Atlantic Forest. Can. J. Zool. 87: 239–245.10.1139/Z09-010Search in Google Scholar

Menezes, Jr., L.F., A.C. Duarte, R.L.M. Novaes, A.C. Façanha, A.L. Peracchi, L.M. Costa, A.F.P. Fernandes and C.E.L. Esbérard. 2008. Deslocamento de Artibeus lituratus (Olfers, 1818) (Mammalia, Chiroptera) entre ilha e continente no Estado do Rio de Janeiro, Brasil. Biota Neotrop. 8: 243–245.10.1590/S1676-06032008000200021Search in Google Scholar

Meyer, C.F.J. and E.K.V. Kalko. 2008. Assemblage-level responses of phyllostomid bats to tropical forest fragmentation: land-bridge islands as a model system. J. Biogeogr. 35: 1711–1726.10.1111/j.1365-2699.2008.01916.xSearch in Google Scholar

Meyer, C.F.J., J. Fründ, W.P. Lizano and E.K.V. Kalko. 2008. Ecological correlates of vulnerability to fragmentation in Neotropical bats. J. appl. Ecol. 45: 281–391.10.1111/j.1365-2664.2007.01389.xSearch in Google Scholar

Murcia, C. 1995. Edge effects in fragmented forests: Implications for conservation. Trends Ecol. Evol. 10: 50–56.10.1016/S0169-5347(00)88977-6Search in Google Scholar

Nogueira, M.R., I.P. Lima, A.L. Peracchi and N.B. Simmons. 2012. New genus and species of nectar-feeding bat from the Atlantic Forest of southeastern Brazil (Chiroptera, Phyllostomidae, Glossophaginae). Am. Mus. Novit. 3747: 1–30.10.7934/P761Search in Google Scholar

Novaes, R.L.M. and C.C. Nobre. 2009. Dieta de Artibeus lituratus (Olfers, 1818) em área urbana na cidade do Rio de Janeiro: frugivoria e novo registro de folivoria. Chirop. Neotrop. 15: 487–493.Search in Google Scholar

Novaes, R.L.M., F.A.P. Mello, S. Felix, R. Silvares, A.C.S. Façanha, T.S. Cardoso, M.A.S. Louro, R.F. Souza, M.V.P. Aguiar, A.C. Siqueira and C.E.L. Esbérard. 2010. Lonchophylla bokermanni na Floresta Atlântica: distribuição, conservação e nova localidade de ocorrência para uma espécie ameaçada de extinção. Chirop. Neotrop. 16: 710–714.Search in Google Scholar

Ortêncio-Filho, H., T.E. Lacher and L.C. Rodrigues. 2014. Seasonal patterns in community composition of bats in forest fragments of the Alto Rio Paraná, southern Brazil. Stud. Neotrop. Fauna Environ. 49: 1–11.10.1080/01650521.2014.950834Search in Google Scholar

Paglia, A.P., G.A.B. Fonseca, A.B. Rylands, G. Herrmann, L.M.S. Aguiar, A.G. Chiarello, Y.L.R. Leite, L.P. Costa, S. Siciliano, M.C.M. Kierulff, S.L. Mendes, V.C. Tavares, R.A. Mittermeier and J.L. Patton. 2012. Lista anotada dos Mamíferos do Brasil, 2a ed. Occ. Pap. Conserv. Biol. 6: 1–76.Search in Google Scholar

Reis, N.R., A.L. Peracchi, I.P. Lima and W.A. Pedro. 2006. Riqueza de espécies de morcegos (Mammalia, Chiroptera) em dois diferentes habitats na região centro-sul do Paraná, sul do Brasil. Rev. bras. Zool. 23: 813–816.10.1590/S0101-81752006000300028Search in Google Scholar

Ribeiro, M.C., J.P. Metzger, A.C. Martensen, J.C. Ponzoni and M.M. Hirota. 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142: 1141–1153.10.1016/j.biocon.2009.02.021Search in Google Scholar

Santos, M.C.F., R.L. Moura and A.A. Valente. 2007. Bromeliaceae no Maciço do Gericinó-Mendanha, Rio de Janeiro, Brasil. Rev. Bras. Biociên. 5: 63–65.Search in Google Scholar

Sazima, I. and E.A. Fischer. 1994. The fruit bat Artibeus lituratus as a forest and city dwaller. Ciên. Cult. 46: 164–168.Search in Google Scholar

Schulze, M.D., N.E. Seavy and D.F. Whitacre. 2000. A comparison of the phyllostomid bat assemblage in undisturbed Neotropical forest and in forest fragments of a Slash-and-Burn farming mosaic in Petén, Guatemala. Biotrop. 32: 174–184.Search in Google Scholar

SEMUAM (Secretaria Municipal de Urbanismo e Meio Ambiente da Cidade de Nova Iguaçu). 2001. Plano de manejo do Parque Natural Municipal de Nova Iguaçu. Prefeitura de Nova Iguaçu, Fundo Nacional do Ambiente, Instituto Estadual de Florestas do Rio de Janeiro, Nova Iguaçu, Brazil. pp. 101.Search in Google Scholar

Shao, J. and D. Tu. 1995. The jackknife and bootstrap. Springer, New York, NY. pp. 517.10.1007/978-1-4612-0795-5Search in Google Scholar

Sikes, R.S., W.L. Gannon and The Animal Care and Use Committee of the American Society of Mammalogists. 2011. Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J. Mammal. 92: 235–253.10.1644/10-MAMM-F-355.1Search in Google Scholar

Soulé, M.E. and B.A. Wilcox. 1980. Conservation biology: an evolutionary-ecological perspective. Sinauer and Associates, Sunderland, UK. pp. 395.Search in Google Scholar

Stevens, G.C. 1992. The elevational gradiente in altitudinal range: an of rapport’s latitudinal rule to altitude. Am. Nat. 140: 893–911.10.1086/285447Search in Google Scholar PubMed

Straube, F.C. and G.V. Bianconi. 2002. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chirop. Neotrop. 8: 150–152.Search in Google Scholar

Talora, D.C. and L.P.C. Morellato. 2000. Fenologia de espécies arbóreas em floresta de planície litorânea do sudeste do Brasil. Rev. bras.Bot. 23: 13–26.10.1590/S0100-84042000000100002Search in Google Scholar

Teixeira, T.S.M., M.M. Weber, D. Dias, M.L. Lorini, C.E.L. Esbérard, R.L.M. Novaes, R. Cerqueira and M.M. Vale. 2014. Combining environmental suitability and habitat connectivity to map rare or Data Deficient species in the Tropics. J. Nat. Conserv. 22: 384–390.10.1016/j.jnc.2014.04.001Search in Google Scholar

Timm, R.M. 1994. The mammals fauna. In: (L.A. McDade, K.S. Bawa, H.A. Hespenheide and G.S. Hartshorn, eds.) La Selva: ecology and natural history of a Neotropical rainforest. University of Chicago Press, Chicago and London, IL and UK. pp. 229–237.Search in Google Scholar

Varzinczak, L.H., I.P. Bernardi and F.C. Passos. 2016. Is the knowledge of bat distribution in the Atlantic Rainforest sufficient? Comments about new findings and a case study in the Paraná State coastal area, Brazil. Mammalia 80: 263–269.10.1515/mammalia-2014-0130Search in Google Scholar

Velazco, P.M., R. Gregorin, R.S. Voss and N.B. Simmons. 2014. Extraordinary local diversity of disk-winged bats (Thyropteridae: Thyroptera) in northeastern Peru, with the description of a new species and comments on roosting behavior. Am. Mus. Novit. 3795: 1–28.10.1206/3795.1Search in Google Scholar

Wilson, D.E. 1973. Bat faunas: a trophic comparison. Syst. Zool. 22: 14–29.10.2307/2412374Search in Google Scholar

Wilson, D.E., C.F. Ascorra and S.T. Solari. 1996. Bats as indicators of habitat disturbance. In: (D.E. Wilson and S.A. Sandoval, eds.) Manu: the biodiversity of southeastern Peru. Smithsonian Instituition Press, Washington, DC. pp. 613–525.Search in Google Scholar

Received: 2015-7-3
Accepted: 2016-4-13
Published Online: 2016-5-24
Published in Print: 2017-5-1

©2017 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 28.1.2023 from
Scroll Up Arrow