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Tadpole richness in riparian areas is determined by niche-based and neutral processes

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Abstract

In this study, we evaluate the effects of spatial and environmental factors on the structure of tadpole assemblages in Central Amazonia testing the following hypotheses: (1) environmental factors are more important than spatial ones in tadpole richness distribution and (2) habitat structure variables are more important than biotic variables in tadpole richness distribution. Tadpoles were sampled at 20 riparian plots between February and June 2010. Spatial and environmental components explained the major part of the variation in observed and estimated tadpole richness, respectively. Among all fitted models, the best model that explains species richness distribution is the one that contains only the number of ponds. Our results showed that tadpole richness in streamside ponds is influenced by niche-based processes and can be explained by local factors related to habitat structure. Predator density was not an important biotic factor in our study, contradicting the results found by other studies conducted in tropical areas. However, neutral processes are also important because spatial variation can explain the spatial distribution of species richness, probably as a result of dispersal limitation. Therefore, our results contribute to understanding of the local and landscape features which influence the amphibian species diversity in a tropical forest.

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References

  • Alford, R. A., 1999. Ecology: resource use, competition, and predation. In McDiarmid, R. W. & R. Altig (eds), Tadpoles: The Biology of Anuran Larvae. Chicago University Press, Chicago: 240–278.

    Google Scholar 

  • Araújo, A. C., A. D. Nobre, B. Kruijt, J. A. Elbers, R. Dallarosa, P. Stefani, C. von Randow, A. O. Manzi, A. D. Culf, J. H. C. Gash, P. Valentini & P. Kabat, 2002. Comparative measurements of carbon dioxide fluxes from two nearby towers in a central Amazonian rainforest: the Manaus LBA site. Journal of Geophysical Research 107: 8066–8091.

    Article  Google Scholar 

  • Azevedo-Ramos, C. & W. E. Magnusson, 1999. Tropical tadpole vulnerability to predation: association between laboratory results and prey distribution in an Amazonian savanna. Copeia 1999: 58–67.

    Article  Google Scholar 

  • Azevedo-Ramos, C., M. Van Sluys, J.-M. Hero & W. E. Magnusson, 1992. Influence of tadpoles velocity on predation by odonate naiads. Journal of Herpetology 26: 335–338.

    Article  Google Scholar 

  • Azevedo-Ramos, C., W. E. Magnusson & P. Bayliss, 1999. Predation as key structuring tadpoles assemblages in Savanna Area in Central Amazonia. Copeia 1999: 22–33.

    Article  Google Scholar 

  • Barnett, H. K. & J. S. Richardson, 2002. Predation risk and competition effects on the life-history characteristics of larval Oregon spotted frog and larval red-legged frog. Oecologia 132: 436–444.

    Article  Google Scholar 

  • Bertoluci, J., P. L. B. Rocha & M. T. Rodrigues, 2013. Field evidence of coupled cycles of arthropod predator-tadpole prey abundance in six aquatic systems of an Atlantic Rainforest site in Brazil. Herpetological Journal 23: 63–66.

    Google Scholar 

  • Bjorholm, S., J. C. Svenning, F. Skov & H. Balslev, 2008. To what extend does Tobler’s Ist law of geography apply to macroecology? A case study using American palms (Arecaceae). BMC Ecology 8: 11–20.

    Article  PubMed Central  PubMed  Google Scholar 

  • Borcard, D. & P. Legendre, 2002. All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling 153: 51–68.

    Article  Google Scholar 

  • Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045–1055.

    Article  Google Scholar 

  • Both, C., M. Solé, T. G. dos Santos & S. Z. Cechin, 2009. The role of spatial and temporal descriptors for neotropical tadpole communities in southern Brazil. Hydrobiologia 624: 125–138.

    Article  Google Scholar 

  • Both, C., S. Z. Cechin, A. S. Melo & S. M. Hartz, 2011. What controls tadpole richness and guild composition in ponds in subtropical grassland? Austral Ecology 36: 530–536.

    Article  Google Scholar 

  • Burnham, K. P. & D. R. Anderson, 2002. Model selection and multimodel inference: a practical information-theoretic approach, 2nd ed. Springer, New York.

    Google Scholar 

  • Burnham, K. P., D. R. Anderson & K. P. Huyvaert, 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65: 23–35.

    Article  Google Scholar 

  • Costa, F. R. C., W. E. Magnusson & R. C. Luizão, 2005. Mesoscale distribution patterns of Amazonian understorey herbs in relation to topography, soil and watersheds. Journal of Ecology 93: 863–878.

    Article  CAS  Google Scholar 

  • Cottenie, K., 2005. Integrating environmental and spatial processes in ecological community dynamics. Ecology Letters 8: 1175–1182.

    Article  PubMed  Google Scholar 

  • Crawley, M. J., 2007. The T Book. Wiley, England.

    Google Scholar 

  • Diniz-Filho, J. A. F., L. M. Bini & B. A. Hawkins, 2003. Spatial autocorrelation and red herrings in geographical ecology. Global Ecology and Biogeography 12: 53–64.

    Article  Google Scholar 

  • Dray, S., P. Legendre & P. R. Peres-Neto, 2006. Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling 196: 483–493.

    Article  Google Scholar 

  • Drucker, D. P., F. R. C. Costa & W. E. Magnusson, 2008. How wide is the riparian zone of small streams in tropical forests? A test with terrestrial herbs. Journal of Tropical Ecology 24: 65–74.

    Article  Google Scholar 

  • Duellman, W. E. & L. Trueb, 1994. Biology of Amphibians. The Johns Hopkins University Press, Baltimore and London.

    Google Scholar 

  • Eterovick, P. C. & I. M. Barata, 2006. Distribution of tadpoles within and among Brazilian streams: the influence of predators, habitat size and heterogeneity. Herpetologica 62: 365–377.

    Article  Google Scholar 

  • Eterovick, P. C. & I. S. Barros, 2003. Niche occupancy in south-eastern Brazilian tadpole communities in montane-meadow streams. Journal of Tropical Ecology 19: 439–448.

    Article  Google Scholar 

  • Eterovick, P. C. & G. W. Fernandes, 2002. Why do breeding frogs colonize some puddles more than others? Phyllomedusa 1: 31–40.

    Article  Google Scholar 

  • Evans, M., C. Yáber & J.-M. Hero, 1996. Factors influencing choice of breeding site by Bufo marinus in natural habitat. Copeia 1996: 904–912.

    Article  Google Scholar 

  • Fox, J. & S. Weisberg, 2011. An R companion to applied regression. R package version 2.0-13 [available on internet at http://socserv.socsci.mcmaster.ca/jfox/Books/Companion].

  • Gascon, C., 1991. Population and community level analyses of species occurrences of central Amazonian rainforest tadpoles. Ecology 72: 1731–1746.

    Article  Google Scholar 

  • Gascon, C., 1992. Aquatic predators and tadpoles prey in central Amazonia: field data and experimental manipulations. Ecology 73: 971–980.

    Article  Google Scholar 

  • Girdler, E. B. & B. T. C. Barrie, 2008. The scale-dependent importance of habitat factors and dispersal limitation in structuring Great Lakes shoreline plant communities. Plant Ecology 198: 211–223.

    Article  Google Scholar 

  • Guillaumet, J. & F. Kahn, 1982. Estrutura e dinamismo da floresta. Acta Amazonica 12: 61–77.

    Google Scholar 

  • Halverson, M. A., D. K. Skelly, J. M. Kiesecker & L. K. Freidenburg, 2003. Forest mediated light regime linked to amphibian distribution and performance. Oecologia 134: 360–364.

    CAS  PubMed  Google Scholar 

  • Hecnar, S. J. & R. T. M’Closkey, 1996. Amphibian species richness and distribution in relation to pond water chemistry in south-western Ontario, Canada. Freshwater Biology 36: 7–15.

    Article  CAS  Google Scholar 

  • Hecnar, S. J. & R. T. M’Closkey, 1997. The effects of predatory fish on amphibians species richness and distribution. Biological Conservation 79: 123–131.

    Article  Google Scholar 

  • Hero, J.-M., 1990. An illustrated key to tadpoles occurring in the Central Amazon rainforest, Manaus, Amazonas, Brasil. Amazoniana 11: 201–262.

    Google Scholar 

  • Hero, J.-M., C. Gascon & W. E. Magnusson, 1998. Direct and indirect effects of predation on tadpole community structure on Amazon rainforest. Australian Journal of Ecology 23: 474–482.

    Article  Google Scholar 

  • Hero, J.-M., W. E. Magnunson, C. F. D. Rocha & C. P. Catterall, 2001. Antipredator defenses influence the distribution of amphibian prey species in central Amazon rain forest. Biotropica 33: 131–141.

    Article  Google Scholar 

  • Heyer, W. R., 1976. Studies in larval amphibian habitat partitioning. Smithsonian Contributions to Zoology 242: 1–27.

    Google Scholar 

  • Hodnett, M. G., I. Vendrame, A. O. Marques-Filho, M. D. Oyama & J. Tomasella, 1997. Soil water storage and groundwater behaviour in a catenary sequence beneath forest in central Amazonia. II. Floodplain water table behaviour and implications for streamflow generation. Hidrology and Earth System Sciences 1: 279–290.

    Article  Google Scholar 

  • Hubbell, S. P., 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton University Press, Princenton and Oxford.

    Google Scholar 

  • Kerr, J. T., 1997. Species richness, endemism, and the choice for area for conservation. Conservation Biology 11(5): 1094–1100.

    Article  Google Scholar 

  • Klaver, R. W., C. R. Peterson & D. A. Patla, 2013. Influence of water conductivity on amphibian occupancy in the greater yellowstone ecosystem. Western North American Naturalist 73: 184–197.

    Article  Google Scholar 

  • Landeiro, V. L., W. E. Magnusson, A. S. Melo, H. M. V. Espírito-Santo & L. S. Bini, 2011. Spatial eigenfunction analyses in stream networks: do watercourse and Overland distances produce different results? Freshwater Biology 56: 1184–1192.

    Article  Google Scholar 

  • Legendre, P. & L. Legendre, 1998. Numeral Ecology, 2nd ed. Elsevier Science, Amsterdam.

    Google Scholar 

  • Lima, A. P., W. E. Magnusson, M. Menin, L. K. Erdtmann, D. J. Rodrigues, C. Keller & W. Hödl, 2012. Guia de sapos da Reserva Adolpho Ducke, Amazônia Central = Guide to the anurans to Reserva Adolpho Ducke, Central Amazonia, 2nd ed. Instituto Nacional de Pesquisas da Amazônia, Manaus.

    Google Scholar 

  • Lomolino, M. V. & G. A. Smith, 2003. Prairie dog towns as islands: applications of island biogeography and landscape ecology for conserving nonvolant terrestrial vertebrates. Global Ecology & Biogeography 12: 275–286.

    Article  Google Scholar 

  • Lucaks, P. M., W. L. Thompson, W. L. Kendall, W. R. Gould, P. F. Doherty, K. P. Burnham & D. R. Anderson, 2007. Concerns regarding a call for pluralism of information theory and hypothesis testing. Journal of Applied Ecology 44: 456–460.

    Article  Google Scholar 

  • Marques-Filho, A. O., M. N. G. Ribeiro, H. M. Santos & J. M. Santos, 1981. Estudos climatológicos da Reserva Florestal Ducke—Manaus—AM. IV. Precipitação. Acta Amazonica 11: 759–768.

    Google Scholar 

  • Masser, M. P. & J. W. Jensen, 1991. Calculation area and volume of ponds and tanks. Southern Regional Aquaculture Center 103: 1–7.

    Google Scholar 

  • Mendonça, F. P., W. E. Magnusson & J. Zuanon, 2005. Relationship between habitat characteristics and fish assemblages in small streams of Central Amazonia. Copeia 2005: 750–763.

    Article  Google Scholar 

  • Menin, M., A. P. Lima, W. E. Magnusson & F. Waldez, 2007. Topographic and edaphic effects on the distribution of terrestrially reproducing anurans in Central Amazonia: mesoscale spatial patterns. Journal of Tropical Ecology 23: 539–547.

    Article  Google Scholar 

  • Menin, M., A. P. Lima & D. J. Rodrigues, 2009. The tadpole of Vitreorana oyampiensis (Anura, Centrolenidae) in Central Amazonia, Brazil. Zootaxa 2203: 65–68.

    Google Scholar 

  • Menin, M., F. Waldez & A. P. Lima, 2011. Effects of environmental and spatial factors on the distribution of anuran species with aquatic reproduction in central Amazonia. Herpetological Journal 21: 255–261.

    Google Scholar 

  • Moore, M. K. & V. R. Townsend Jr, 1998. The interaction of temperature, dissolved oxygen and predation pressure in an aquatic predator–prey system. Oikos 81: 329–336.

    Article  Google Scholar 

  • Morin, P. J., 1999. Community Ecology. Blackwell Science, Malden.

    Google Scholar 

  • Pazin, V. F. V., W. E. Magnusson, J. Zuanon & F. P. Mendonça, 2006. Fish assemblages in temporary ponds adjacent to ‘terra-firme’ streams in Central Amazonia. Freshwater Biology 51: 1025–1037.

    Article  Google Scholar 

  • Peel, M. C., B. L. Finlayson & T. A. McMahon, 2007. Updated world map of the Köppen–Geiger climate classification. Hydrology and Earth System Sciences Discussions 4: 439–473.

    Article  Google Scholar 

  • Peltzer, P. M. & R. C. Lajmanovich, 2004. Anuran tadpole assemblage in riparian areas of middle Paraná River, Argentina. Biodiversity and Conservation 13: 1833–1842.

    Article  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Development Core Team, 2012. nlme: linear and nonlinear mixed effects models. R package version 3.1-104. R Foundation for Statistical Computing, Vienna.

  • R Development Core Team, 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.R-project.org].

  • Rangel, T. F. L. V. B., J. A. F. Diniz-Filho & L. M. Bini, 2006. Towards an integrated computational tool for spatial analysis in macroecology and biogeography. Global Ecology & Biogeography 15: 321–327.

    Article  Google Scholar 

  • Rangel, T. F., J. A. F. Diniz-Filho & L. M. Bini, 2010. SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography 33: 46–50.

    Article  Google Scholar 

  • Ribeiro, J. E. L. S., M. J. G. Hopkins, A. Vicentini, C. A. Sothers, M. A. S. Costa, J. M. Brito, M. A. D. Souza, L. H. P. Martins, L. G. Lohmann, P. A. C. L. Assunção, E. C. Pereira, C. F. Silva, M. R. Mesquita & L. C. Procópio, 1999. Flora da Reserva Ducke: guia de identificação das plantas vasculares de uma floresta de terra firme na Amazônia Central. Instituto Nacional de Pesquisas da Amazônia, Manaus.

    Google Scholar 

  • Richards, S. A., M. J. Whittingham & P. A. Stephens, 2011. Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behavioral Ecology and Sociobiology 65: 77–89.

    Article  Google Scholar 

  • Ricklefs, R. E. & R. J. Lovette, 1999. The roles of island area per se and habitat diversity in the species–area relationships of four Lesser Antillean faunal groups. Journal of Animal Ecology 68: 1142–1160.

    Article  Google Scholar 

  • Rodrigues, D. J., A. P. Lima, W. E. Magnusson & F. R. C. Costa, 2010. Temporary pond availability and tadpole species composition in Central Amazonia. Herpetologica 66: 113–119.

    Article  Google Scholar 

  • Rojas-Ahumada, D. P. & M. Menin, 2010. Composition and abundance of anurans in riparian and non-riparian areas in a forest in Central Amazonia, Brazil. South American Journal of Herpetology 5: 157–167.

    Article  Google Scholar 

  • Rojas-Ahumada, D. P., V. L. Landeiro & M. Menin, 2012. Role of environmental and spatial processes in structuring anuran communities across a tropical rain forest. Austral Ecology 37: 865–873.

    Article  Google Scholar 

  • Rome, L. C., E. D. Stevens & H. B. John-Alder, 1992. The influence of temperature and thermal acclimation on physiological function. In Feder, M. E. & W. W. Burggren (eds), Environmental Physiology of Amphibians. University of Chicago Press, Chicago: 183–205.

    Google Scholar 

  • Rossa-Feres, D. & J. Jim, 1996. Distribuição espacial em comunidades de girinos na região de Botucatu, São Paulo (Amphibia, Anura). Revista Brasileira de Biologia 56: 309–316.

    Google Scholar 

  • Schiesari, L., 2006. Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biology 51: 412–423.

    Article  CAS  Google Scholar 

  • Shaffer, H. B., R. A. Alford, B. D. Woodward, S. J. Richards, R. G. Altig & C. Gascon, 1994. Quantitative sampling of amphibian larvae. In Heyer, W. R., M. A. Donnelly, R. McDiarmid, L.-A. C. Hayek & M. S. Foster (eds), Measuring and Monitoring Biological Diversity: Standard Methods for Amphibians. Smithisonian Institution Press, Washington: 130–141.

    Google Scholar 

  • Skelly, D. K., L. K. Freidenburg & J. M. Kiesecker, 2002. Forest canopy and the performance of larval amphibians. Ecology 83: 983–992.

    Article  Google Scholar 

  • Smith, A. M. & D. M. Green, 2005. Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28(1): 110–128.

    Article  Google Scholar 

  • Strauß, A., E. Reeve, R.-D. Randrianiaina, M. Vences & J. Glos, 2010. The world’s richest tadpole communities show functional redundancy and low functional diversity: ecological data on Madagascar’s stream-dwelling amphibian larvae. BMC Ecology 10: 12.

    Article  PubMed Central  PubMed  Google Scholar 

  • Strauß, A., R. D. Randrianiaina, M. Vences & J. Glos, 2013. Species distribution and assembly patterns of frog larvae in rainforest streams of Madagascar. Hydrobiologia 702: 27–43.

    Article  Google Scholar 

  • Tews, J., U. Brose, V. Grimm, K. Tielborger, M. C. Wichmann, M. Schwager & F. Jeltsch, 2004. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 31: 79–92.

    Article  Google Scholar 

  • Triplehorn, C. A. & N. F. Johnson, 2011. Estudo dos insetos. Cengage Learning, São Paulo.

    Google Scholar 

  • Urban, M. C., 2004. Disturbance heterogeneity determines freshwater metacommunity structure. Ecology 85: 2971–2978.

    Article  Google Scholar 

  • Van Buskirk, J., 2005. Local and landscape influence on amphibian occurrence and abundance. Ecology 86: 1936–1947.

    Article  Google Scholar 

  • Werner, E. E. & K. Glennemeier, 1999 The influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999: 1–12.

  • Zimmerman, B. L. & R. O. Bierregaard, 1986. Relevance of the equilibrium theory of island biogeography and species-area relations to conservation with case from Amazonia. Journal of Biogeography 13: 133–143.

    Article  Google Scholar 

  • Zuur, A. F., E. N. Ieno, N. J. Walker, A. A. Saveliev & G. M. Smith, 2009. Mixed effects models and extensions in ecology with R. Springer, New York.

    Book  Google Scholar 

  • Zuur, A. F., E. N. Ieno & C. S. Elphick, 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology & Evolution 1: 3–14.

    Article  Google Scholar 

  • Zweimüller, I., 1995. Microhabitat use by two small benthic stream fish in a 2nd order stream. Hydrobiologia 303: 125–137.

    Article  Google Scholar 

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Acknowledgments

We are grateful to Marco A. Mendonça for logistic support and facilities at Fazenda UFAM. Anne d’Heursel for reviewing the English. E. Venticinque, R. Da Silveira, M.E. Oliveira, J. Zuanon, and F. Costa and anonymous reviewers for constructive comments on earlier drafts. J. Zuanon for fish identification. Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) for collection permits (# 11323-1). Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (# 470375/2006-0, 558318/2009-6), Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM # 586/10), SISBIOTA Program: CNPq (#563075/2010-4), and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP#10/52321-7) for financial support. This study was supported by graduate fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) to APA and a Research Productivity grant from CNPq to MM and DJR. MVG received a fellowship from CNPq (# 159946/2012-3). The Fazenda UFAM is part of the Programa de Pesquisa em Biodiversidade (PPBio) of the Brazilian Ministry of Science, Technology and Innovation (MCTI). This is contribution 37 of the Projeto Igarapés.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Diversidade Biológica, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Manaus, AM, Brazil

    Alexandre Pinheiro de Almeida & Marcelo Menin

  2. Instituto de Ciências Naturais, Humanas e Sociais, Universidade Federal de Mato Grosso, Sinop, MT, Brazil

    Domingos de Jesus Rodrigues

  3. Instituto Nacional de Ciência e Tecnologia de Estudos Integrados da Biodiversidade Amazônica, Ministério da Ciência, Tecnologia e Inovação, Conselho Nacional de Desenvolvimento Científico e Tecnológico – INCT-CENBAM/MCTI/CNPq, Manaus, Brazil

    Domingos de Jesus Rodrigues & Marcelo Menin

  4. Instituto Latino-Americano de Ciências da Vida e da Natureza, Universidade Federal da Integração Latino-Americana, Foz do Iguaçu, PR, Brazil

    Michel Varajão Garey

  5. Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal do Amazonas, Av. General Rodrigo O. Jordão Ramos, 3000, Manaus, AM, 69077-000, Brazil

    Marcelo Menin

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  1. Alexandre Pinheiro de Almeida
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de Almeida, A.P., de Jesus Rodrigues, D., Garey, M.V. et al. Tadpole richness in riparian areas is determined by niche-based and neutral processes. Hydrobiologia 745, 123–135 (2015). https://doi.org/10.1007/s10750-014-2099-7

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