Abstract
This study aimed to test through null models analysis the co-occurrence and nestedness patterns of bat species in a region of the Atlantic Rainforest. Data from 10 communities were tabulated in presence-absence matrices. Two metrics have been used to test the co-occurrence patterns: C-Score, which calculates the “checkerboard” pattern testing the interspecific competition between pairs of species, and V-Ratio, which calculates the covariance between species. All analyses were performed with EcoSim software. For nestedness analyses, we utilized the NODF metric through the Aninhado software. None of all the C-Score results showed a significant pattern of species association, indicating a higher coexistence among bat species. For V-Ratio, three results indicated nonrandom associations of species. The communities are highly nested, with poor species sites being subsets of richer sites. The diversification in this group allows the coexistence of species, decreasing the niche overlap. Nested pattern is common in mammal communities, and the significance of our results is in accordance with the results of the co-occurrence test. Competitive interactions may lead to differences in abundance of species in communities. However, as the method of bat sampling is considered biased, the results using binary data, as in our study, seems to be the most trustful method.
Acknowledgments
We would like to thank CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for a scholarship provided to LHV and a grant to FCP (303757/2012-4). CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) provided a doctorate scholarship to IPB. We would like to especially thank Gustavo Graciolli for the data from Parque Nacional do Superagui and Maurício O. Moura and Diego R. Bilski for the suggestions provided for the first version of the manuscript.
References
Agrawal, A.A., D.D. Ackerly, F. Adler, A.E. Arnold, C. Caceres, D.F. Doak, E. Post, P.J. Hudson, J. Maron, K.A. Mooney, M. Power, D. Schemske, J. Stachowicz, S. Strauss, M.G. Turner and E. Werner. 2007. Filling key gaps in population and community ecology. Front. Ecol. Environ. 5: 145–152.10.1890/1540-9295(2007)5[145:FKGIPA]2.0.CO;2Search in Google Scholar
Aguirre, L.F., L. Lens, R. van Damme and E. Matthysen. 2003. Consistency and variation in the bat assemblages inhabiting two forest islands within a Neotropical savanna in Bolivia. J. Trop. Ecol. 19: 367–374.10.1017/S0266467403003419Search in Google Scholar
Almeida-Neto, M., P.R. Guimarães and T.M. Lewinsohn. 2007. On nestedness analyses: rethinking matrix temperature and anti-nestedness. Oikos 116: 716–722.10.1111/j.0030-1299.2007.15803.xSearch in Google Scholar
Almeida-Neto, M., P. Guimarães, P.R. Guimarães, R.D Loyola and W. Ulrich. 2008. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117: 1227–1239.10.1111/j.0030-1299.2008.16644.xSearch in Google Scholar
Alves, L.A. 2008. Estrutura da comunidade de morcegos (Mammalia: Chiroptera) do Parque Estadual da Ilha do Cardoso, São Paulo. Master Thesis, Universidade Federal do Mato Grosso do Sul, Campo Grande, Brazil. pp. 40.Search in Google Scholar
Baker, M.A. and B.D. Patterson. 2009. Patterns in the local assembly of Egyptian rodent faunas: co-occurrence and nestedness. J. Arid Environ. 75: 14–19.10.1016/j.jaridenv.2010.08.005Search in Google Scholar
Beaudrot, L., M.J. Struebig, E. Meijaard, S. van Balen, S. Husson and A.J. Marshall. 2013. Co-occurrence patterns of Bornean vertebrates suggest competitive exclusion is strongest among distantly related species. Oecologia 173: 1053–1062.10.1007/s00442-013-2679-7Search 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
Bernardi, I.P. and F.C. Passos. 2011. Estrutura de comunidade de morcegos em relictos de floresta estacional decidual no sul do Brasil. Mastozool. Neotrop. 19: 1–12.Search in Google Scholar
Brito, J.E.C. 2011. Morcegos do Parque Estadual do Pico Marumbi: Frugivoria e germinação de sementes. Master Thesis, Universidade Federal do Paraná, Curitiba, Brazil. pp. 65.Search in Google Scholar
Connor, E.F. and D. Simberloff. 1979. The assembly of species communities: chance or competition? Ecology 60: 1132–1140.10.2307/1936961Search in Google Scholar
Dala-Rosa, S. 2004. Morcegos (Chiroptera, Mammalia) de um remanescente de restinga, Estado do Paraná, Brasil: ecologia da comunidade e dispersão de sementes. Master Thesis, Universidade Federal do Paraná, Curitiba, Brazil. pp. 128.Search in Google Scholar
Diamond, J.M. 1975. Assembly of species communities. In: (M.L. Cody and J.M. Diamond, eds.) Ecology and evolution of communities. Harvard University Press, Cambridge, MA. pp. 342–444.Search in Google Scholar
Diamond, J.M. and M.E. Gilpin. 1982. Examination of the ‘null’ model of Connor and Simberloff for species co-occurrences on islands. Oecologia 52: 64–72.10.1007/BF00349013Search in Google Scholar
Dumont, E. 2003. Bats and fruit: an ecomorphological approach. In: (T.H. Kunz and M.B. Fenton, eds.) Bat ecology. University of Chicago Press, Chicago, IL. pp. 398–429.Search in Google Scholar
Estrada, A. and R. Coates-Estrada. 2001. Bat species richness in live fences and corridors of residual rain forest vegetation at Los Tuxtlas, Mexico. Ecography 24: 94–102.10.1034/j.1600-0587.2001.240111.xSearch in Google Scholar
Estrada-Villegas, E., B.J. McGill and E.K.V. Kalko. 2012. Climate, habitat, and species interactions at different scales determine the structure of a Neotropical bat community. Ecology 93: 1183–1193.Search in Google Scholar
Freeman, P.W. 2000. Macroevolution in Microchiroptera: recoupling morphology and ecology with phylogeny. Evol. ecol. Res. 2: 317–335.Search in Google Scholar
Gardner, A.F. 2007. Order Chiroptera In: (A.F. Gardner, ed.) Mammals of South America. Volume I. Marsupials, xernarthrans, shrews and bats. The University of Chicago Press, Chicago, IL. pp. 187–580.Search in Google Scholar
Gause, G.F. 1934. The struggle for existence. Williams and Wilkins, Baltimore, MD. pp. 188.Search in Google Scholar
Geraldes, M.P. 1999. Estudo de uma taxocenose de morcegos na região do Ariri, Cananéia, SP. Master Thesis, Universidade de São Paulo, São Paulo, Brazil. pp. 92.Search in Google Scholar
Gotelli, N.J. 2000. Null model analysis of species co-occurrence patterns. Ecology 81: 2606–2621.10.1890/0012-9658(2000)081[2606:NMAOSC]2.0.CO;2Search in Google Scholar
Gotelli, N.J. and G.R. Graves. 1996. Null models in ecology. Smithsonian Institution Press, Washington, D.C. pp. 357.Search in Google Scholar
Gotelli, N.J. and D.J. McCabe. 2002. Species co-occurrence: a meta-analysis of J.M. Diamond’s assembly rules model. Ecology 83: 2091–2096.10.1890/0012-9658(2002)083[2091:SCOAMA]2.0.CO;2Search in Google Scholar
Gotelli, N.J. and G.L. Entsminger. 2006. EcoSim: null models software for ecology. Version 7.0.Search in Google Scholar
Guimarães, P.R. and P. Guimarães. 2006. Improving the analyses of nestedness for large sets of matrices. Environ. Model. Software 21: 1512–1513.10.1016/j.envsoft.2006.04.002Search in Google Scholar
Kaku-Oliveira, N.Y. 2010. Estrutura de comunidade, reprodução e dinâmica populacional de morcegos (Mammalia, Chiroptera) na Reserva Natural do Salto Morato, Guaraqueçaba, Paraná. Master Thesis, Universidade Federal do Paraná, Curitiba, Brazil. pp. 109.Search in Google Scholar
Kalko, E.K.V. 1998. Organisation and diversity of tropical bat communities through space and time. Zoology 101: 281–297.Search in Google Scholar
Kunz, T.H., E. Braun de Torrez, D. Bauer, T. Lobova and T.H. Fleming. 2011. Ecosystem services provided by bats. Ann. N.Y. Acad. Sci. 1223: 1–38.10.1111/j.1749-6632.2011.06004.xSearch in Google Scholar
Lopez-Gonzalez, C. 2003. Ecological zoogeography of the bats of Paraguay. J. Biogeogr. 31: 33–45.10.1111/j.1365-2699.2004.00940.xSearch in Google Scholar
MacArthur, R.H. and R. Levins. 1967. The limiting similarity convergence and divergence of coexisting species. Am. Nat. 101: 377–385.10.1086/282505Search in Google Scholar
Martínez-Morales, M.A. 2005. Nested species assemblages as a tool to detect sensitivity to forest fragmentation: the case of cloud forest birds. Oikos 108: 634–642.10.1111/j.0030-1299.2005.13706.xSearch in Google Scholar
May, R.M. 1984. An overview: real and apparent patterns in community structure, In: (D.R. Strong Jr., D. Simberloff, L.G. Abele and A.B. Thistle, eds.) Ecological communities: conceptual issues and the evidence. Princeton University Press, Princeton, NJ. pp. 3–16.Search in Google Scholar
McNab, B.K. 1971. The structure of tropical bat faunas. Ecology 52: 352–358.10.2307/1934596Search in Google Scholar
Mello, M.A.R. 2009. Temporal variation in the organization of a Neotropical assemblage of leaf-nosed bats (Chiroptera: Phyllostomidae). Acta Oecol. 35: 280–286.10.1016/j.actao.2008.11.008Search in Google Scholar
Meyer, C.F.J. and E.K.V. Kalko. 2008. Bat assemblages on Neotropical landbridge islands: nested subsets and null model analyses of species co-occurrence patterns. Divers. Distrib. 14: 644–654.10.1111/j.1472-4642.2007.00462.xSearch in Google Scholar
Mikich, S.B. 2002. A dieta dos morcegos frugívoros (Mammalia, Chiroptera, Phyllostomidae) de um pequeno remanescente de Floresta Estacional Semidecidual do sul do Brasil. Rev. Bras. Zool. 19: 239–249.Search in Google Scholar
Ministério do Meio Ambiente. 2006. Portaria N° 150 de 08 de Maio de 2006. Diário Oficial da União, Brasília, 17 maio 93: 73.Search in Google Scholar
Miranda, J.M.D., I.P. Bernardi and F.C. Passos. 2011. Chave ilustrada para determinação dos morcegos da Região Sul do Brasil. Curitiba, PR, Brazil. pp. 56.Search in Google Scholar
Muscarella, R. and T.H. Fleming. 2007. The role of frugivorous bats in tropical forest succession. Biol. Rev. 82: 573–590.10.1111/j.1469-185X.2007.00026.xSearch in Google Scholar PubMed
Myers, N., R.A. Mittermeier, C.G. Mittermeier, G.A.B. Fonseca and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–845.10.1038/35002501Search in Google Scholar PubMed
Nogueira, M.R., I.P. Lima, R. Moratelli, V.C. Tavares, R. Gregorin and A.L. Peracchi. 2014. Checklist of Brazilian bats, with comments on original records. Check List 10: 808–821.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: 169–179.10.1080/01650521.2014.950834Search in Google Scholar
Palmeirin, J.M., D.L. Gorchov and S. Stoleson. 1989. Trophic structure of a neotropical frugivore community: is there competition between birds and bats? Oecologia 79: 403–411.10.1007/BF00384321Search in Google Scholar PubMed
Passos, F.C., W.R. Silva, W.A. Pedro and M.R. Bonin. 2003. Frugivoria em morcegos (Mammalia, Chiroptera) no Parque Estadual de Intervales, sudeste do Brasil. Rev. Bras. Zool. 20: 511–517.Search in Google Scholar
Passos, F.C., J.M.D. Miranda, I.P. Bernardi, N.Y. Kaku-Oliveira, and L.C. Munster. 2010. Morcegos da Região Sul do Brasil: análise comparativa da riqueza de espécies, novos registros e atualizações nomenclaturais (Mammalia, Chiroptera). Iheringia Ser. Zool. 100: 25–34.10.1590/S0073-47212010000100004Search in Google Scholar
Patterson B.D. and W. Atmar. 1986. Nested subsets and the structure of insular mammalian faunas and archipelagos. Biol. J. Linn. Soc. 28: 65–82.10.1111/j.1095-8312.1986.tb01749.xSearch in Google Scholar
Patterson, B.D., M.R. Willig and R.D. Stevens. 2003. Trophic strategies, niche partitioning, and patterns of ecological organization. In: (T.H. Kunz and M.B. Fenton, eds.) Bat ecology. University of Chicago Press, Chicago, IL. pp. 536–579.Search in Google Scholar
Pech-Canche, J.M., C.E. Moreno and G. Halffter. 2011. Additive partitioning of phyllostomid bat richness at fine and coarse spatial and temporal scales in Yucatan, Mexico. Ecoscience 18: 42–51.10.2980/18-1-3392Search in Google Scholar
Pinto, D. and H. Ortêncio-Filho. 2006. Dieta de quatro espécies de filostomídeos frugívoros (Chiroptera, Mammalia) do Parque Municipal do Cinturão Verde de Cianorte, Paraná, Brasil. Chiropt. Neotrop. 12: 274–279.Search in Google Scholar
Pitta, E., S. Giokas and S. Sfenthourakis. 2012. Significant pairwise co-occurrence patterns are not the rule in the majority of biotic communities. Diversity 4: 179–193.10.3390/d4020179Search in Google Scholar
Rex, K., D. Kelm, K. Wiesner, T.H. Kunz and C.C Voigt. 2008. Species richness and structure of three Neotropical bat assemblages. Biol. J. Linn. Soc. 94: 617–629.10.1111/j.1095-8312.2008.01014.xSearch in Google Scholar
Rex, K., B.I. Czaczkes, R. Michener, T.H. Kunz and C.C. Voigt. 2010. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17: 37–46.10.2980/17-1-3294Search in Google Scholar
Riedinger, V., J. Muller, J. Stadler, W. Ulrich and R. Brandl. 2013. Assemblages of bats are phylogenetically clustered on a regional scale. Basic appl. Ecol. 14: 74–80.10.1016/j.baae.2012.11.006Search in Google Scholar
Rojas, D., A. Vale, V. Ferrero and L. Navarro. 2011. When did plants become important to leaf-nosed bats? Diversification of feeding habits in the family Phyllostomidae. Mol. Ecol. 20: 2217–2228.10.1111/j.1365-294X.2011.05082.xSearch in Google Scholar PubMed
Rubio, M.B.G. 2014. Estruturação das assembleias de morcegos em três locais do litoral do Paraná, Brasil. Master Thesis, Universidade Federal do Paraná, Curitiba, Brazil. pp. 88.Search in Google Scholar
Rubio, M.B.G., L.H. Varzinczak, I.P. Bernardi, F.C. Passos and J.M.D. Miranda. 2014. Bats from two sites of the Paraná State coastal area, southern Brazil. Chiropt. Neotrop. 20: 1255–1263.Search in Google Scholar
Scaramuzza, C.A.M., L.L. Simões, S.T. Rodrigues, G.M. Accacio, M. Hercowitz, M.R. Rosa, W.G. Silva, E.R. Pinage and M.S. Soares. 2011. Visão da biodiversidade da ecoregião da Serra do Mar, domínio biogeográfico Mata Atlântica. WWF, Brasília, DF, Brazil. pp. 169.Search in Google Scholar
Schluter, D. 1984. A variance test for detecting species associations, with some example applications. Ecology 65: 998–1005.Search in Google Scholar
Scultori, C. 2009. Comunidade de morcegos, interação com flores e estratificação vertical em Mata Atlântica no sul do Brasil. Master Thesis. Universidade Estadual de Campinas, Campinas, Brazil. pp. 158.Search in Google Scholar
Stevens, R.D. 2013. Gradients of bat diversity in Atlantic forest of South America: environmental seasonality, sampling effort and spatial autocorrelation. Biotropica 45: 764–770.Search in Google Scholar
Stevens, R.D. and M.R. Willig. 1999. Density compensation in New World bat communities. Oikos 89: 367–377.10.1034/j.1600-0706.2000.890218.xSearch in Google Scholar
Stevens, R.D., C. Lopez-Gonzalez and S.J. Presley. 2007. Geographical ecology of Paraguayan bats: spatial integration and metacommunity structure of interacting assemblages. J. Anim. Ecol. 76: 1086–1093.10.1111/j.1365-2656.2007.01288.xSearch 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. Chiropt. Neotrop. 8: 150–152.Search in Google Scholar
Stone, L. and A. Roberts. 1990. The checkerboard score and species distributions. Oecologia 85: 74–79.10.1007/BF00317345Search in Google Scholar PubMed
Ulrich W. and N.J. Gotelli. 2007. Null model analysis of species nestedness patterns. Ecology 88: 1824–1831.10.1890/06-1208.1Search in Google Scholar PubMed
Ulrich, W. and N.J. Gotelli. 2010. Null model analysis of species associations using abundance data. Ecology 91: 3384–3397.10.1890/09-2157.1Search in Google Scholar PubMed
Ulrich, W. and N.J. Gotelli. 2013. Pattern detection in null model analysis. Oikos 122: 2–18.10.1111/j.1600-0706.2012.20325.xSearch in Google Scholar
Voss, R.S. and L.H. Emmons. 1996. Mammalian diversity in Neotropical lowland rainforests: a preliminary assessment. Bull. Am. Mus. Nat. Hist. 230: 1–115.Search in Google Scholar
Weiher, E. and P. Keddy. 1999. Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, Cambridge, NJ. pp. 432.Search in Google Scholar
Wilson, D.E. and D.M. Reeder. 2005. Mammal species of the World: a taxonomic and geographic reference. Third edition. The Johns Hopkins University Press, Baltimore, MD. pp. 2142.Search in Google Scholar
Winifred, F.F., J.P. Hayes and Heady, P.A. 2009. Nestedness of desert bat assemblages: species composition patterns in insular and terrestrial landscapes. Oecologia 158: 687–697.10.1007/s00442-008-1168-xSearch in Google Scholar PubMed
Wright D.H., B.D. Patterson, G.M. Mikkelso, A. Cutler and W. Atmar. 1998. A comparative analysis of nested subset patterns of species composition. Oecologia 113: 1–20.10.1007/s004420050348Search in Google Scholar PubMed
Zina, J., C.P.A. Prado, C.A. Brasileiro and C.F.B. Haddad. 2012. Anurans of the sandy coastal plains of the Lagamar Paulista, state of São Paulo, Brazil. Biota Neotrop. 12: 251–260.10.1590/S1676-06032012000100020Search in Google Scholar
©2016 by De Gruyter
Articles in the same Issue
- Frontmatter
- Review
- The wild goat, Capra aegagrus Erxleben, 1777, of the island of Montecristo (Northern Tyrrhenian Sea, Italy): does it still exist?
- Original Studies
- Trophic relationships of sympatric small carnivores in fragmented landscapes of southern Brazil: niche overlap and potential for competition
- Dietary adaptation of white-headed langurs in a fragmented limestone habitat
- Winter foraging of chinkara (Gazella bennettii shikarii) in Central Iran
- Null model analysis on bat species co-occurrence and nestedness patterns in a region of the Atlantic Rainforest, Brazil
- Richness and distribution of porcupines (Erethizontidae: Coendou) from Colombia
- The level of rodent problems in poultry farms of Rawalpindi-Islamabad, Pakistan
- Survival and recruitment of the multimammate mouse, Mastomys natalensis (Smith 1834), in a rice agro-ecosystem
- New records of Cryptonanus guahybae (Tate, 1931) in southern Brazil inferred from molecular and morphological data
- Short Notes
- The wild goat of Montecristo Island: did it ever exist?
- First record of a bat from the Lakshadweep archipelago, southwestern India
- Status of pinnipeds in Southeast Asia
- Breeding habits of the Indian pangolin (Manis crassicaudata) in Potohar Plateau, Pakistan
- Litter size and basic diet of brown bears (Ursus arctos, Carnivora) in northeastern Turkey
Articles in the same Issue
- Frontmatter
- Review
- The wild goat, Capra aegagrus Erxleben, 1777, of the island of Montecristo (Northern Tyrrhenian Sea, Italy): does it still exist?
- Original Studies
- Trophic relationships of sympatric small carnivores in fragmented landscapes of southern Brazil: niche overlap and potential for competition
- Dietary adaptation of white-headed langurs in a fragmented limestone habitat
- Winter foraging of chinkara (Gazella bennettii shikarii) in Central Iran
- Null model analysis on bat species co-occurrence and nestedness patterns in a region of the Atlantic Rainforest, Brazil
- Richness and distribution of porcupines (Erethizontidae: Coendou) from Colombia
- The level of rodent problems in poultry farms of Rawalpindi-Islamabad, Pakistan
- Survival and recruitment of the multimammate mouse, Mastomys natalensis (Smith 1834), in a rice agro-ecosystem
- New records of Cryptonanus guahybae (Tate, 1931) in southern Brazil inferred from molecular and morphological data
- Short Notes
- The wild goat of Montecristo Island: did it ever exist?
- First record of a bat from the Lakshadweep archipelago, southwestern India
- Status of pinnipeds in Southeast Asia
- Breeding habits of the Indian pangolin (Manis crassicaudata) in Potohar Plateau, Pakistan
- Litter size and basic diet of brown bears (Ursus arctos, Carnivora) in northeastern Turkey