Abstract
This study investigated the effects of activities carried out by traditional populations on aquatic ecosystems using the assemblages of Ephemeroptera, Plecoptera, and Trichoptera insect orders, and identified fluvial habitat characteristics modified by the disturbances. We surveyed two groups of streams—17 streams representing control conditions (CON) and 17 streams influenced by traditional population settlements (TPO). Genera richness and abundance of individuals did not vary between groups. With regard to physical habitat metrics, the percentage of leaf litter, amount of woody debris in the channel, proximity to farming, percentage of slow water in the channel, and the mean riparian vegetation cover all influenced benthic macroinvertebrate assemblages. Considerable differences were found in genera composition between the two groups. The genera Ulmeritoides, Miroculis, and Brasilocaenis were associated with the CON group, and Macronema and Campsurus with the TPO group. We conclude that even small-scale impacts, such as those performed by traditional Amazonian populations, can have major effects on aquatic biota, which reiterates the fragile nature of these ecosystems and emphasizes the need for adequate management of these activities.
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References
Allan, J. D., 2004. Landscapes and Riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology, Evolution, and Systematics 35: 257–284.
Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
Anderson, M. J. & T. J. Wilis, 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511–525.
Anderson, M. J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245–253.
Arnaiz, O. L., A. L. Wilson, R. J. Watts & M. M. Stevens, 2011. Influence of riparian condition on aquatic macroinvertebrate communities in an agricultural catchment in south-eastern Australia. Ecological Research 26: 123–131.
Azrina, M. Z., C. K. Yap, A. R. Ismail, A. Ismael & S. G. Tan, 2006. Anthropogenic impacts on the distribution and biodiversity of benthic macroinvertebrates and water quality of the Langat River, Peninsular Malaysia. Ecotoxicology and Environmental Safety 64: 337–347.
Behling, H. & M. L. Costa, 2000. Holocene environmental changes from the Rio Curuá record in the Caxiuanã Region, Eastern Amazon Basin. Quaternary Research 53: 369–377.
Bispo, P. C., L. G. Oliveira, V. L. Crisci & M. M. Silva, 2001. A pluviosidade como fator de alteração da entomofauna bentônica (Ephemeroptera, Plecoptera e Trichoptera) em córregos do Planalto Central do Brasil. Acta Limnologica Brasiliensia 13: 1–9.
Bispo, P. C., L. G. Oliveira, L. M. Bini & K. G. Sousa, 2006. Ephemeroptera, Plecoptera and Trichoptera from riffles in mountain streams of Central Brazil: environmental factors influencing the distribution and abundance of immatures. Brazilian Journal of Biology 66: 611–622.
Brand, C. & M. L. Miserendino, 2015. Testing the performance of macroinvertebrate metrics as indicators of changes in biodiversity after pasture conversion in Patagonian Mountain streams. Water, Air, & Soil Pollution 226: 370.
Brasil, L. S., L. Juen & H. S. R. Cabette, 2014. The effects of environmental integrity on the diversity of mayflies, Leptophlebiidae (Ephemeroptera), in tropical streams of the Brazilian Cerrado. Annales de Limnologie - International Journal of Limnology 50: 325–334.
Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: a Practical Information-Theoretical Approach. Springer, New York.
Caceres, M. D. & P. Legendre, 2009. Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566–3574.
Carvalho, E. M. & V. S. Uieda, 2010. Input of litter in deforested and forested areas of a tropical headstream. Revista Brasileira de Biologia 70: 283–288.
Costa, M. L., D. C. Kern, H. Behling & M. S. Borges, 2002. Geologia. In Lisboa, P. L.B. (Org). Caxiuanã: populações tradicionais, meio físico e diversidade biológica. Museu Paraense Emílio Goeldi, Belém: 179–205.
Cunha, E. J., L. F. A. Montag & L. Juen, 2015. Oil palm crops effects on environmental integrity of Amazonian streams and Hetereopteran (Hemiptera) species diversity. Ecological Indicators 52: 422–429.
Da-Silva, E. R., F. F. Salles & M. S. Baptista, 2002. As brânquias dos gêneros de Leptophlebiidae (Insecta: Ephemeroptera) ocorrentes no Estado do Rio de Janeiro. Biota Neotropica 2: 1–4.
Da-Silva, E. R., J. L. Nessimian & L. B. N. Coelho, 2010. Leptophlebiidae from Rio de Janeiro State, Brazil: nymphal habitats, mesohabitats, and habits (Insecta: Ephemeroptera). Biota Neotropica 10: 87–93.
Dale, V. H. & S. C. Beyeler, 2001. Challenges in the development and use of ecological indicators. Ecological Indicators 1: 3–10.
Dias-Silva, K., H. S. R. Cabette, L. Juen, P. Jr & De Marco, 2010. The influence of habitat integrity and physical-chemical water variables on the structure of aquatic and semi-aquatic Heteroptera. Zoologia (Curitiba) 27: 918–930.
Diegues, A. C. S., 2000. Etnoconservação: novos rumos para a proteção da natureza nos trópicos. Hucitec, São Paulo.
Domínguez, E., C. Molineri, M. L. Pescador, M. D. Hubbard & C. Nieto, 2006. Ephemeroptera of South America. In Adis, J. R., G. Rueda-Delgado & K. M. Wantzen (eds), Aquatic Biodiversity in Latin American (ABLA). Pensoft, Sofia-Moscow.
Domínguez, E., M. D. Hubbard, M. L. Pescador & C. Molineri, 2001. Ephemeroptera. In Fernandes, H. R. & E. Domínguez (eds), Guia para la determinación de los artrópodos bentónicos sudamericanos. Editorial Universitária de Tucumán, Tucumán.
Dufrene, M. & P. Legendre, 1997. Species assemblages and indicator species: the need for flexible asymmetrical approach. Ecological Monographs 67: 345–366.
Edmunds, G. F. Jr., S. L. Jensen & L. Berner, 1976. The Mayflies of North and Central America. Univ Of Minnesota Press, Reissue edition.
Feminella, J. W., 2000. Correspondence between stream macroinvertebrate assemblages and 4 ecoregions of the southeastern USA. Journal of the North American Benthological Society 19: 442–461.
Ferreira, L. V., S. S. Almeida & C. S. Rosário, 1997. As áreas de inundação, Caxiuanã. In Lisboa, P. F. B. (org) Caxiuanã. Museu Paraense Emílio Goeldi, Belém 195-211.
Ferreira, W., R. Ligeiro, R. M. Hughes, P. R. Kaufmann, L. G. Oliveira & M. Callisto, 2014. Importance of environmental factors on the richness and distribution of benthic macroinvertebrates in tropical headwater streams. Freshwater Science 33: 860–871.
Fraxe, T. J. P., H. S. Pereira & A. C. Witkoski, 2007. Comunidades ribeirinhas amazônicas: modos de vida e uso dos recursos naturais. Editora da Universidade do Amazonas, Manaus.
Gibson, L., T. M. Lee, L. P. Koh, B. W. Brook, T. A. Gardner, J. Barlow & N. S. Sodhi, 2011. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478: 378–381.
Giehl, N. F. S., K. Dias-Silva, L. Juen, J. D. Batista & H. S. R. Cabette, 2014. Taxonomic and numerical resolutions of Nepomorpha (Insecta: Heteroptera) in Cerrado Streams. PLoS ONE 9: e103623.
Green, R. E., S. J. Cornell, J. P. W. Scharlemann & A. Balmford, 2005. Farming and the fate of wild nature. Science 307: 550–555.
Hamada, N. & S. R. M. Couceiro, 2003. An illustrated key to nymphs of Perlidae (Insecta, Plecoptera) genera in Central Amazonia, Brazil. Revista Brasileira de Entomologia 47: 477–480.
Hamid, S. A. & M. D. Rawi, 2014. Ecological Functioning of Ephemeroptera, Plecoptera and Trichoptera (Insecta) in Rivers of Gunung Jerai Forest Reserve: diversity and distribution of functional feeding groups. Tropical Life Sciences Research 25: 61–73.
Heckenberger, M. J., J. C. Russell, J. R. Toney & M. J. Schmidt, 2007. The legacy of cultural landscapes in the Brazilian Amazon: implications for biodiversity. Philosophical Transactions of the Royal Society B: Biological Sciences 362: 197–208.
Hilda, N., J. M. Maia, M. Hiraoka, O. Shimi & N. Mizutani, 1997. Notes on annual and daily water levels changes at Breves and Caxiuanã, Amazon estuary. In Lisboa, P. L. B. (org). Caxiuanã. Museu Paraense Emilio Goeldi, Belém 97–103.
Hölscher, D., M. R. F. Möller, M. E. Denich & H. Fölster, 1997. Nutrient input-output budget of shifting agriculture in Eastern Amazonia. Nutrient Cycling in Agroecosystems 47: 49–57.
Homma, A. K. O., 1993. Extrativismo vegetal na Amazônia: limites e oportunidades. Empresa Brasileira de Pesquisa Agropecuária, Brasília.
Homma, A. K. O., 2012. Extrativismo vegetal ou plantio: qual a opção para a Amazônia? Estudos Avançados 26: 167–186.
Hughes, R. M., A. T. Herlihy & J. C. Sifneos, 2015. Predicting aquatic vertebrate assemblages from environmental variables at three multistate geographic extents of the western USA. Ecological Indicators 57: 546–556.
Hynes, H. B. N., 1970. The ecology of stream insects. Annual Review of Entomology 15: 25–42.
Instituto Chico Mendes de Conservação da Biodiversidade – ICMBIO, 2012. Plano de manejo Caxiuanã. Disponível em: http://www.icmbio.gov.br/acessado em Janeiro de 2015.
Jackson, D. A., 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74: 2204–2214.
Jackson, D. A., 1995. PROTEST: a procrustean randomization test of community environment concordance. Écoscience 2: 297–303.
Kaufmann, P. R. & J. M. Faustini, 2012. Simple measures of channel habitat complexity predict transient hydraulic storage in streams. Hydrobiologia 685: 69–95.
Kaufmann, P. R., P. Levine, E. G. Robison, C. Seeliger & D. V. Peck, 1999. Quantifying Physical Habitat in Wadeable Streams. Environmental Protection Agency, EPA/620/R-99/003. U.S, Washington, DC.
Kindt, R. & R. Coe, 2005. Tree Diversity Analysis: A Manual and Software for Common Statistical Methods for Ecological and Biodiversity Studies. World Agroforestry Centre (ICRAF), Nairobi.
Kleinman, P. J., R. B. Bryant & D. Pimentel, 1996. Assessing ecological sustainability of slash-and-burn agriculture through soil fertility indicators. Agronomy Journal 88: 122–127.
Laurance, W. F., J. Sayer & K. G. Cassman, 2014. Agricultural expansion and its impacts on tropical nature. Trends in Ecology & Evolution 29: 107–116.
Legendre, P. & L. Legendre, 1998. Numerical Ecology. Elsevier, Amsterdam.
Leite, G. F. M., F. T. C. Silva, J. F. J. Gonçalves & P. Salles, 2015. Effects of conservation status of the riparian vegetation on fish assemblage structure in neotropical headwater streams. Hydrobiologia 762: 223–238.
Lenat, D. R. & V. H. Resh, 2001. Taxonomy and stream ecology – the benefits of genus and species-level identification. Journal of the North American Benthological Society 20: 287–298.
Ligeiro, R., R. M. Hughes, P. R. Kaufmann, D. R. Macedo, K. R. Firmiano, W. Ferreira, D. Oliveira, A. S. Melo & M. Callisto, 2013. Defining quantitative stream disturbance gradients and the additive role of habitat variation to explain macroinvertebrate taxa richness. Ecological Indicators 25: 45–57.
Lobόn-Cerviá, J., L. L. Hess, K. M. Melack & C. A. R. M. Araujo-Lima, 2015. The importance of forest cover for fish richness and abundance on the Amazon floodplain. Hydrobiologia 750: 245–255.
Maloney, K. O., J. W. Feminella, R. M. Mitchell, S. A. Miller, P. J. Mulholland & J. N. Houser, 2008. Landuse legacies and small streams: identifying relationships between historical land use and contemporary stream conditions. Journal of the North American Benthological Society 27: 280–294.
Melo, A. S., 2005. Effects of taxonomic and numeric resolution on the ability to detect ecological patterns at a local scale using stream macroinvertebrates. Archiv fr Hydrobiologie 164: 309–323.
Melo, D. M. B., A. V. Krusche, M. M. Ribeiro, A. C. Migivama, M. E. C. Sales, J. F. Berredo & C. R. L Matos, 2013. A biogeoquímica das águas de Caxiuanã. In Lisboa, P. L. B. (org) Caxiuanã: paraíso ainda preservado. Museu Paraense Emilio Goeldi, Belém.
Merritt, R. W., K. W. Cummins & M. B. Berg, 2008. An Introduction to the Aquatic Insects of North America. Kendall Hunt Publishing, Dubuque.
Moran, E. F., 2009. Interações homem-ambiente em ecossistemas florestais: uma introdução. In Moran, E. F. & E. Ostrom (org). Ecossistemas florestais: interação homem-ambiente. São Paulo, Editora Senac.
Nakajima, T., T. Asaeda, T. Fujino & A. Nanda, 2006. Coarse particulate organic matter distribution in the pools and riffles of a second-order stream. Hydrobiologia 559: 275–283.
Nessimian, J. L., E. M. Venticinque, J. Zuanon, P. Marco-Jr, M. Gordo, L. Fidelis, J. D. Batista & L. Juen, 2008. Land use, habitat integrity, and aquatic insect assemblages in Central Amazonian streams. Hydrobiologia 614: 117–131.
Noda, S. N., H. Noda & A. L. U. Martins, 2002. Papel do processo produtivo tradicional na conservação dos recursos genéticos vegetais. In Rivas, A. & C. E. C. Freitas (org). Amazônia: uma perspectiva interdisciplinar. Editora da Universidade do Amazonas, Manaus: 155–178.
Nogueira, D. S., H. S. R. Cabette & L. Juen, 2011. Estrutura e composição da comunidade de Trichoptera (Insecta) de rios e áreas alagadas da bacia do rio Suiá-Miçú, Mato Grosso, Brasil. Ilheringia Série Zoologia 101: 173–180.
Olifiers, M. H., L. F. M. Dorvillé, J. L. Nessimian & N. Hamada, 2004. A Key to Brazilian Genera of Plecoptera (Insecta) based on Nymphs. Zootaxa 651: 1–15.
Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens & H. Wagner, 2015. Vegan: community ecology package. R package version 2: 1–3.
Oliveira, V. C., E. A. Gonçalves & R. G. Alves, 2014. Colonisation of leaf litter by aquatic invertebrates in an Atlantic Forest stream. Brazilian Journal of Biology 74: 267–273.
Oliveira-Junior, J. M. B., Y. Shimano, T. A. Gardner, R. M. Hughes, P. Marco Júnior & L. Juen, 2015. Neotropical dragonflies (Insecta: Odonata) as indicators of ecological condition of small streams in the eastern Amazon. Austral Ecology 40: 733–744.
Peck, D. V., A. T. Herlihy, B. H. Hill, R. M. Hughes, P. R. Kaufmann, D. J. Klemm, J. M. Lazorchak, F. H. Mccormick, S. A. Peterson, P. L. Ringold, T. Magee & M. R. Cappaert, 2006. Environmental Monitoring and Assessment Program – Surface Waters Western Pilot Study: Field Operations Manual for 16 Wadeable Streams. Environmental Protection Agency, EPA 600/R-06/003. U.S., Office of Research and Development, Washington, DC.
Peel, M. C., B. L. Finlayson & T. A. McMahon, 2007. Updated world map of the Koppen-Geiger climate classification. Hydrology and Earth System Sciences 11: 1633–1644.
Pereira, L. R., H. S. R. Cabette & L. Juen, 2012. The use of aquatic insects of order Trichoptera as bioindicators of habitat integrity. Annales de Limnologie - International Journal of Limnology 48: 303–313.
Pes, A. M. O., N. Hamada & J. L. Nessimian, 2005. Chaves de identificação de larvas para famílias e gêneros de Trichoptera (Insecta) da Amazônia Central, Brasil. Revista Brasileira de Entomologia 49: 181–2014.
Poff, N. L. & J. V. Ward, 1990. Physical habitat template of lotic systems: recovery in the context of historical pattern of spatiotemporal heterogeneity. Environmental Management 14: 629–645.
Pringle, C. M., 2001. Hydrologic connectivity and the management of biological reserves: a global perspective. Ecological Applications 11: 981–998.
R Core Team, 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Reijntjes, C., B. Haverkort & A. Waters-Bayer, 1992. Farming for the future: an introduction to low-external-input and sustainable agriculture. Macmillan, London.
Rigui-Carvallaro, K. O., M. R. Spies & A. E. Siegloch, 2010. Ephemeroptera, Plecoptera and Trichoptera assemblages in Miranda River basin, Mato Grosso do Sul State, Brasil. Biota Neotropica 10: 253–260.
Romero, R. M., M. Ceneviva-Bastos, G. H. Baviera & L. Casatti, 2013. Community structure of aquatic insects (Ephemeroptera, Plecoptera, and Trichoptera) in Cerrado streams of Paraguay, Paraná, and São Francisco river basins. Biota Neotropica 13: 97–107.
Roper, B. B., J. L. Kershner, E. Archer, R. Henderson & N. Bouwes, 2002. An evaluation of physical stream habitat attributes used to monitor streams. Journal of the American Water Resources Association 38: 1637–1646.
Sakamoto, Y., M. Ishiguro & G. Kitagawa, 1986. Akaike Information Criterion Statistics. D. Reidel Publishing Company, Dordrecht.
Salles, F. F. & E. Domíngues, 2012. Systematics and Phylogeny of Ulmeritus–Ulmeritoides revisited (Ephemeroptera: Leptophlebiidae). Zootaxa 3571: 49–65.
Salles, F. F., M. M. Lima, 2014. Chave interativa para identificação dos gêneros de Leptophlebiidae (Ephemeroptera) registrados para o Brasil, http://www.ephemeroptera.com.br (Accessed September 2014).
Samways, M. J., R. Osborn & I. Van Heerden, 1996. Distribution of benthic invertebrates at different depths in a shallow reservoir in the Kwa Zulu-Natal Midlands. Koedoe 39: 69–76.
Santana, M. R. A. & P. L. B. Lisboa, 2002. Estratégias de sobrevivência. In Lisboa, P. L. B. (org). Caxiuanã - populações tradicionais, meio físico e diversidade biológica. Museu Paraense Emílio Goeldi, Belém: 95–125.
Santos, M. A. S. & A. C. Santana, 2012. Caracterização socioeconômica da produção e comercialização de farinha de mandioca no município de Portel, arquipélago do Marajó, Estado do Pará. Revista Verde 7: 73–86.
Shimano, Y. & L. Juen, 2016. How oil palm cultivation is affecting mayfly assemblages in Amazon streams. Annales de Limnologie - International Journal of Limnology 52: 35–45.
Shimano, Y., H. S. R. Cabette, F. F. Salles & L. Juen, 2010. Composição e distribuição da fauna de Ephemeroptera (Insecta) em área de transição Cerrado-Amazônia, Brasil. Iheringia. Série Zoologia 100: 301–308.
Shimano, Y., L. Juen, D. S. Nogueira, H. S. R. Cabette & F. F. Salles, 2013. Environmental and spatial processes determining Ephemeroptera (Insecta) structures in tropical streams. Annales de Limnologie - International Journal of Limnology 49: 31–41.
Silveira, I. M. & H. D. A. Quaresma, 2013. Etnografia da ocupação de uma pequena “ilha de terra”. In Lisboa, P. L. B. (org). Caxiuanã: paraíso ainda preservado. Museu Paraense Emílio Goeldi, Belém: 187–203.
Southwood, T. R. E., 1977. Habitat, the templet for ecological strategies? Journal of Animal Ecology 46: 337–365.
Szott, L. T. & C. A. Palm, 1996. Nutrient stocks in managed and natural humid tropical fallows. Plant and Soil 186: 293–309.
Törnblom, J., J. M. Roberge & P. Angelstam, 2011. Rapid assessment of head water stream macroinvertebrate diversity: an evaluation of surrogates across a land-use gradient. Fundamental and Applied Limnology 178: 287–300.
Townsend, C. R., S. Doledec, R. Norris, K. Peacock & C. Arbuckle, 2003. The influence of scale and geography on relationships between stream community composition and landscape variables: description and prediction. Freshwater Biology 48: 768–785.
Venables, W. N. & B. D. Ripley, 2002. Modern Applied Statistics with S, 4th ed. Springer, New York.
Vondracek, B., K. L. Blann, C. B. Cox, J. F. Nerbonne, K. G. Mumford & B. A. Nerbonne, 2005. Land use, spatial scale, and stream systems: lessons from an agriculture region. Environmental Management 36: 775–791.
Wahizatul, A. A., S. H. Long & A. Ahmad, 2011. Composition and distribution of aquatic insect communities in relation to water quality in two freshwater streams of Hulu Terengganu, Terengganu. Journal of Sustainability Science and Management 6: 148–155.
Walker, I., 1994. The benthic litter-dwelling macrofauna of the Amazonian forest stream Tarum -Mirim: patterns of colonization and their implications for community stability. Hydrobiologia 291: 75–92.
Wandelli, E. V. & P. M. Fearnside, 2015. Secondary vegetation in central Amazonia: land-use history effects on aboveground biomass. Forest Ecology and Management 347: 140–148.
Wohl, E. & K. Jaeger, 2009. A conceptual model for the longitudinal distribution of wood in mountain streams. Earth Surf Processes Landforms 34: 329–344.
Zar, J. H., 1999. Biostatistical Analysis, 4th ed. Prentice Hall, Upper Saddle River.
Zuur, A. F., E. N. Ieno, N. Walker, A. A. Saveliev & G. Smith, 2009. Mixed effects models and extensions in ecology with R. Springer, New York.
Acknowledgements
We thank the Programa de Pesquisa em Biodiversidade da Amazônia Oriental (PPBio) and Fundação Amazônia Paraense de Amparo à Pesquisa (FAPESPA) (FAPESPA: ICAAF 03/2011) for financial support to this study. The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process no. 130468/2013-4) provided APJF with a graduate stipend, and LJ (process 307597/2016-4) and MC were awarded research productivity (CNPq no. 303380/2015-2), research project (CNPq no. 446155/2014-4), and Minas Gerais research (FAPEMIG PPM-IX—00525-15) grants. We thank Dr. Ana Maria O. Pes; Dr. Neusa Hamada; Dr. Frederico Falcão Salles; Patrick Barcellos, MSc; Lucas Lima, MSc; and Mylena Cardoso, MSc, for assistance with the identification of specimens. We would like to also thank Erlane Cunha, MSc, for providing area maps; Dr. Lenize Batista Calvão for her critical reading of the manuscript; and Dr. Bruno Spacek Godoy for assistance in statistical analysis. We are grateful to Leyton James Tierney for reviewing the English and officials of the Estação Científica Ferreira Penna for their coordination. Collection of biological materials was authorized by the Sistema de Autorização e Informação em Biodiversidade—SISBIO (n. 11841).
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de Faria, A.P.J., Ligeiro, R., Callisto, M. et al. Response of aquatic insect assemblages to the activities of traditional populations in eastern Amazonia. Hydrobiologia 802, 39–51 (2017). https://doi.org/10.1007/s10750-017-3238-8
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DOI: https://doi.org/10.1007/s10750-017-3238-8