Skip to main content

Advertisement

SpringerLink
Log in

Functional diversity of mayflies (Ephemeroptera, Insecta) in streams in mining areas located in the Eastern Amazon

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The effects of mining-induced changes on natural environments extend from terrestrial to aquatic ecosystems. Our study aimed to investigate how mining activities affect the functional beta diversity of Ephemeroptera nymphs and select species with specific traits. We tested whether: (a) preserved streams have higher functional beta diversity of Ephemeroptera than altered streams, and (b) environmental variation is the main predictor of functional beta diversity. This study was conducted in an environmental gradient of mining activities in 24 streams in the eastern Amazon. Our main results showed that environments altered by mining activities had higher iron and turbidity values, and a broader environmental variation. In addition, we showed that the functional beta diversity of mayflies was higher in streams altered by mining. The results indicated that there was greater dissimilarity of species between altered areas, but the groups of species in these areas presented higher importance of the nestedness component and loss of traits, indicating that subgroups of Ephemeroptera with similar functional traits are formed in these locations. We conclude that mining impacts can be observed at the level of functional traits of Ephemeroptera, especially in the (beta) variation among communities in environments under different environmental impacts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

We declare that we have included supplementary and supporting data in the manuscript.

References

  • Alirezazadeh, S., P. Borges, P. Cardoso, R. Gabriel, F. Rigal & L. Borda-de-Água, 2021. Spatial scaling patterns of functional diversity. Front. Ecol. Evol. 9: 607177.

    Article  Google Scholar 

  • Alvares, C. A., J. L. Stape, P. C. Sentelhas, J. L. M. Gonçalves & G. Sparovek, 2013. Koppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22(6): 711–728.

    Article  Google Scholar 

  • Anderson, M. J., 2006. Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245–253.

    Article  Google Scholar 

  • APHA, 2005. Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association/American Water Works Association/Water Environment Federation, Washington, DC:

    Google Scholar 

  • Atmar, W. & B. D. Patterson, 1993. The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96: 373–382.

    Article  Google Scholar 

  • Bady, P., S. Dolédec, C. Fesl, S. Gayraud, M. Bacchi & F. Scholl, 2005. Use of invertebrate traits for the biomonitoring of European large rivers: the effects of sampling effort on genus richness and functional diversity. Freshwater Biology 50: 159–173.

    Article  Google Scholar 

  • Baker, N. J. & R. Greenfield, 2019. Shift happens: changes to the diversity of riverine aquatic macroinvertebrate communities in response to sewage effluent runoff. Ecological Indicators 102: 813–821.

    Article  Google Scholar 

  • Barbosa, F. A. R., Souza, E. M. M., Vieira, F., Renault, C. P., Rocha, L. A., Maia-Barbosa, P. M. Oberdá, S. A. & S. A. Mingoti, 1997. Impactos Antrópicos e Biodiversidade Aquática. In: J. A. Paula (ed), Biodiversidade, População e Economia; uma região de Mata Atlântica. Belo Horizonte, Rona Editora.

  • Baselga, A., 2010. Partitioning the turnover and nestedness components of beta diversity. Global Ecology Biogeography 19: 134–143.

    Article  Google Scholar 

  • Baselga, A., D. Orme, David & S. Villeger, 2013. Betapart: partitioning beta diversity into turnover and nestedness components. Version 1.2. In. R package version. 1.

  • Beaver, C. J., 1990. Respiratory rate of mayfly nymphs in water with differing oxygen and ionic concentration. In Campbell, I. C. (ed), Mayflies and Stoneflies Kluwer Academic Publishers, Dordrecht: 105–107.

    Google Scholar 

  • Bezerra, L, 2017. Parte I. Escopo e contexto. In: Plano de Pesquisa Geossistemas Ferruginosos da Floresta Nacional de Carajás: Temas Prioritários para Pesquisa e Diretrizes para Ampliação do Conhecimento sobre os Geossistemas Ferruginosos da Floresta Nacional de Carajás e seu Entorno. Brasília, ICMBIO.

  • Bivand, R. & D. W. S. Wong, 2018. Comparing implementations of global and local indicators of spatial association. Test 27(3): 716–748.

    Article  Google Scholar 

  • Blanchet, F., P. Legendre & D. Borcard, 2008. Forward selection of explanatory variables. Ecology 89: 2623–2632.

    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 

  • Borcard, D., F. Gillet & P. Legendre, 2018. Numerical Ecology with R, Springer, New York:

    Book  Google Scholar 

  • Braak, C. J. F., A. Cormont & S. Dray, 2012. Improved testing of species traits–environment relationships in the fourth-corner problem. Ecology 93: 1525–1526.

    Article  Google Scholar 

  • Branco, C. C. Z., P. C. Bispo, C. K. Peres, A. F. Tonetto, R. A. Krupek, M. Barfield & R. D. Holt, 2020. Partitioning multiple facets of beta diversity in a tropical stream macroalgal metacommunity. Journal of Biogeografy 47: 1765–1780.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Brasil, L. S., E. L. Lima, Z. A. Spigolonic, D. R. Ribeiro-Brasil & L. Juen, 2020. The habitat integrity index and aquatic insect communities in tropical streams: a meta-analysis. Ecological Indicators 116: 1–7.

    Article  Google Scholar 

  • Cadotte, M. W., K. Carscadden & N. Mirotchnick, 2011. Beyond species: functional diversity and the maintenance of ecological processes and services. Journal of Applied Ecology 48: 1079–1087.

    Article  Google Scholar 

  • Callisto, M., M. Moretti & M. D. C. Goulart, 2001. Macroinvertebrados bentônicos como ferramenta para avaliar a saúde de riachos. Revista Brasileira De Recursos Hídricos 6: 71–82.

    Article  Google Scholar 

  • Callisto, M., M. S. Linares, W. P. R. M. KifferHughes, M. S. Moretti, D. R. Macedo & R. Solar, 2021. Beta diversity of aquatic macroinvertebrate assemblages associated with leaf patches in neotropical montane streams. Ecology and Evolution 11: 2551–2560.

    Article  Google Scholar 

  • Castro, D. M. P., P. G. Silva, R. Solar & M. Callisto, 2020. Unveiling patterns of taxonomic and functional diversities of stream insects across four spatial scales in the neotropical savana. Ecological Indicators. https://doi.org/10.1016/j.ecolind.2020.106769.

    Article  Google Scholar 

  • Cernansky, R., 2017. The biodiversity revolution. Nature 546(7656): 22–24.

    Article  CAS  Google Scholar 

  • Chessel, D., A. B. Dufour & J. Thioulouse, 2004. The ade4 Package-I- One-table methods. R News 4: 5–10.

    Google Scholar 

  • Chevenet, F., S. Dolédec & D. Chessel, 1994. A fuzzy coding approach for the analysis of long-term ecological data. Freshwater Biology 31: 295–309.

    Article  Google Scholar 

  • Clarke, K. R. & R. N. Gorley, 2006. PRIMER v6 (or v7): User Manual/Tutorial. PRIMER-E: Plymouth

  • Cruz, P., F. Salles & N. Hamada, 2013. A new genus and species of Baetidae (Insecta: Ephemeroptera) from Brazil. Annales De Limnologie - International Journal of Limnology 49: 1–12.

    Article  Google Scholar 

  • Cruz, G. M., A. P. J. Faria & L. Juen, 2022. Patterns and metacommunity structure of aquatic insects (Trichoptera) in Amazonian streams depend on the environmental conditions. Hydrobiologia 849: 2831–2843.

    Article  Google Scholar 

  • Cummins, K. W., 1973. Trophic relations of aquatic insects. Annual Review of Entomology 18(1): 183–206.

    Article  Google Scholar 

  • Cummins, K. W., R. W. Merritt & P. C. Andrade, 2005. The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in south Brazil. Studies on Neotropical Fauna and Environment 40: 69–89.

    Article  Google Scholar 

  • Dedieu, N., M. Rhone, R. Vigouroux & R. Céréghino, 2015. Assessing the impact of gold mining in headwater streams of Eastern Amazonia using Ephemeroptera assemblages and biological traits. Ecological Indicators 52: 332–350.

    Article  Google Scholar 

  • Devictor, V., D. Mouillot, C. Meynard, F. Jiguet, W. Thuiller & N. Mouquet, 2010. Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecology Letters 13(8): 1030–1040.

    Google Scholar 

  • DiBattista, J. D., M. B. Roberts, J. Bouwmeester, B. W. Bowen, D. J. Coker, D. F. Lozano-Cortes, J. H. Choat, M. R. Gaither, J. P. A. Hobbs, M. T. Khalil, M. Kochzius, R. F. Myers, G. Paulay, V. S. N. Robizch, P. Saenz-Agudelo, E. Salas, T. H. Sinclair-Taylor, R. J. Toonen, M. W. Westneat, S. T. Williams & M. L. Berumen, 2016. A review of contemporary patterns of endemism for shallow water reef fauna in the Red Sea. Journal of Biogeography 43: 423–439.

    Article  Google Scholar 

  • Ding, N., W. Yang, Y. Zhou, I. Gonzalez-Bergonzoni, J. Zhang, K. Chen & B. Wang, 2017. Different responses of functional traits and diversity of stream macroinvertebrates to environmental and spatial factors in the Xishuangbanna watershed of the upper Mekong River Basin, China. Science of the Total Environment 574: 288–299.

    Article  CAS  Google Scholar 

  • Dolédec, S., D. Chessel, C. J. F. Ter Braak & S. Champely, 1996. Matching species traits to environmental variables: a new three-table ordination method. Environmental and Ecological Statistics 3: 143–166.

    Article  Google Scholar 

  • Domínguez, E., C. Molineri, M. L. Pescador, M. D. Hubbard & C. Nieto, 2006. Ephemeroptera of South America. In Adis, J., J. R. Arias, G. Rueda-Delgado & K. M. Wantzen (eds), Aquatic Biodiversity of Latin America Pensoft, Moscow-Sofia: 1–646.

    Google Scholar 

  • Dray, S. & A. B. Dufour, 2006. The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22: 1–20.

    Google Scholar 

  • Dray, S., P. Choler, S. Dolédec, P. R. Peres-Neto, W. Thuiller, S. Pavoine & C. J. ter Braak, 2014. Combining the fourth-corner and the RLQ methods for assessing trait responsesto environmental variation. Ecology 95: 14–21.

    Article  Google Scholar 

  • Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guénard, G., Jombart, T., Larocque, G., Legendre, P., Madi, N. & H. Wagner, 2022. adespatial: Multivariate Multiscale Spatial Analysis. R package version 0.3–20, https://CRAN.R-project.org/package=adespatial.

  • Eriksen, C. H. & J. E. Mœur, 1990. Respiratory functions of motile tracheal gills in ephemeroptera nymphs, as exemplified by siphlonurus occidentals eaton. In Campbell, I. C. (ed), Mayflies and Stoneflies: Life Histories and Biology Series Entomologica, Vol. 44. Springer, Dordrecht.

    Google Scholar 

  • Espinosa, A. C. E., Y. Shimano, S. Rolim, L. Maioli, L. Juen & B. Dunck, 2020. Effects of mining and reduced turnover of Ephemeroptera (Insecta) in streams of the Eastern Brazilian Amazon. Journal of Insect Conservation 24: 1061–1072.

    Article  Google Scholar 

  • Fares, A. L. B., L. B. Calvão, N. R. Torres, E. S. C. Gurgel & T. S. Michelan, 2020. Environmental factors affect macrophyte diversity on Amazonian aquatic ecosystems inserted in an anthropogenic landscape. Ecological Indicators 113: 106–231.

    Article  Google Scholar 

  • Ferrari, J. R., T. R. Lookingbill, B. McCormick, P. A. Townsend & K. N. Eshleman, 2009. Surface mining and reclamation effects on flood response of watersheds in the Central Appalachian plateau region. Water Resources. https://doi.org/10.1029/2008WR007109.

    Article  Google Scholar 

  • Flowers, R. W. & C. De La Rosa, 2010. Capítulo 4: Ephemeroptera. Revista De Biología Tropical 58: 63–93.

    Google Scholar 

  • Gastauer, M., P. S. M. Sarmento, V. C. A. Santos, C. F. Caldeira, S. J. Ramos, G. S. Teodoro & J. O. Siqueira, 2020. Vegetative functional traits guide plant species selection for initial mineland rehabilitation. Ecological Engineering 148: 105763.

    Article  Google Scholar 

  • Gonçalves, I. C., B. Cid, A. F. Mortati, L. B. Quesado & J. L. Nessimian, 2003. Relative size of gills of Cloeodes jaragua Salles & Lugo-Ortiz, 2003, (Ephemeroptera, Baetidae) on pool and riffle areas of streams at the Atlantic Rainforest. Biota Neotropica 11: 217–220.

    Article  Google Scholar 

  • Guterres, A. P. M., E. J. Cunha & L. Juen, 2021. Tolerant semiaquatic bugs species (Heteroptera: Gerromorpha) are associated to pasture and conventional logging in the Eastern Amazon. Journal of Insect Conservation 25: 555–567.

    Article  Google Scholar 

  • He, F., W. Jiang, T. Tang & Q. Cai, 2015. Assessing impact of acid mine drainage on benthic macroinvertebrates: can functional diversity metrics be used as indicators? Journal of Freshwater Ecology 30: 513–524.

    Article  Google Scholar 

  • Heino, J., 2005. Positive relationship between regional distribution and local abundance in stream insects: a consequence of niche breadth or niche position? Ecography 28: 345–354.

    Article  Google Scholar 

  • Heino, J., 2008. Patterns of functional biodiversity and function environment relationships in lake littoral macroinvertebrates. Limnology and Oceanography 53: 1446–1455.

    Article  Google Scholar 

  • Heino, J. & K. T. Tolonen, 2017. Ecological drivers of multiple facets of beta diversity in a lentic macroinvertebrate metacommunity. Limnology and Oceanography 62: 2431–2444.

    Article  Google Scholar 

  • Heino, J., D. Schmera & T. Eros, 2013. Macroecological perspective of trait patterns in stream communities. Freshwater Biology 58: 1539–1555.

    Article  Google Scholar 

  • Hering, D., C. Meier, C. Rawer-Jost, C. K. Feld, R. Biss, A. Zenker & J. Böhmer, 2004. Assessing streams in Germany with benthic invertebrates: selection of candidate metrics. Limnologica - Ecology and Management of Inland Waters 34: 398–415.

    Article  Google Scholar 

  • IBAMA, 2003. Plano de Manejo para Uso Múltiplo da Floresta Nacional de Carajás. Companhia Vale do Rio Doce, STCP - Engenharia de Projetos LTDA.

  • ICMBio, 2016. Plano de Manejo da Floresta Nacional de Carajás. Volumen I – Diagnóstico. Ministério do Meio Ambiente. Instituto Chico Mendes da Conservação da Biodiversidade. Brasil.

  • Jacobus, L., C. Macadam & M. Sartori, 2019. Mayflies (Ephemeroptera) and their contributions to ecosystem services. InSects 10(6): 1–26.

    Article  Google Scholar 

  • Jamoneau, A., S. I. Passy, J. Soininen, T. Lebouche & J. Tison-Rosebery, 2018. Beta diversity of diatom species and ecological guilds: response to environmental and spatial mechanisms along the stream watercourse. Freshwater Biology 63: 62–73.

    Article  Google Scholar 

  • Juen, L., E. J. Cunha, F. G. Carvalho, M. C. Ferreira, T. O. Begot, A. Luiza- Andrade, Y. Shimano, H. Leão, P. S. Pompeu & L. F. A. Montag, 2016. Effects of oil palm plantations on the habitat structure and biota of streams in Eastern Amazon. River Research and Applications 32: 2081–2094.

    Article  Google Scholar 

  • Kembel, S. W., P. D. Cowan, M. R. Helmus, et al., 2010. Picante: r tools for integrating phylogenies and ecology. Bioinformatics 26: 1463–1464.

    Article  CAS  Google Scholar 

  • Kemp, P. S., Worthington, T.A. & T. E. L. Langford, 2010. A critical review of the effects of beavers on fish and fish stocks. Scottish Natural Heritage Commissioned Report. Scottish Natural Heritage.

  • Kluge, N. J., E. A. Novikova & A. K. Brodsky, 1984. Movements of larvae of the Ephemeroptera during swimming, respiration and cleaning. Zoologicheskij Zhurnal 63: 1345–1354.

    Google Scholar 

  • Laliberté, E., Legendre, P. & B. Shipley, 2014. FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0–12.

  • Lavorel, S., S. McIntyre, J. Landsberg & T. D. A. Forbes, 1997. Plant functional classifications: from general groups to specific groups based on response to disturbance. Trends in Ecology & Evolution 12: 474–478.

    Article  CAS  Google Scholar 

  • Leão, H., T. Siqueira, N. R. Torres & L. F. A. Montag, 2020. Ecological uniqueness of fish communities from streams in modified landscapes of Eastern Amazonia. Ecological Indicators. 111: 106039.

    Article  Google Scholar 

  • Legendre, P. & M. J. Anderson, 1999. Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs 69: 1–24.

    Article  Google Scholar 

  • Legendre, P. & L. Legendre, 2012. Numerical Ecology, 3rd ed. Elsevier, Amsterdam:

    Google Scholar 

  • Legendre, P., R. Galzin & M. L. Harmelin-Vivien, 1997. Relating behavior to habitat: solutions to the fourth-corner problem. Ecology 78: 547–562.

    Google Scholar 

  • Lewis, P. A., 1974. Taxonomy and Ecology of Stenonema mayflies (Heptageniidae: Ephemeroptera). National Environmental Research Center Office of Research and Development. USEPA. Cincinnati, Ohio, pp. 80.

  • Li, B., Y. Wang, W. Tan, N. Saintilan, G. Lei & L. Wen, 2021. Land cover alteration shifts ecological assembly processes in floodplain lakes: Consequences for fish community dynamics. Science of the Total Environment 782: 146724.

    Article  CAS  Google Scholar 

  • Luiza-Andrade, A., L. F. A. Montag & L. Juen, 2017. Functional diversity in studies of aquatic macroinvertebrates community. Scientometrics 111: 1643–1656.

    Article  Google Scholar 

  • Luiza-Andrade, A., L. S. Brasil, N. R. Torres, J. Brito, R. R. Silva, L. U. Maioli, M. F. Barbirato, S. G. Rolim & L. Juen, 2020. Effects of local environmental and landscape variables on the taxonomic and trophic composition of aquatic insects in a rare forest formation of the Brazilian Amazon. Neotropical Entomology 49(6): 821–831.

    Article  CAS  Google Scholar 

  • Martins, R. T., Oliveira, V. C. & A. K. M. Salcedo, 2014. Uso de insetos aquáticos na avaliação de impactos antrópicos em ecossistemas aquáticos. In: Hamada, N., J. L. Nessimian, R. B. Querino (eds). Insetos Aquáticos na Amazônia Brasileira: taxonomia, biologia e ecologia. Editora do INPA. Manaus: pp 724.

  • Meira, R. M., A. L. Peixoto, M. A. Coelho, A. P. Ponzo, V. G. Esteves, M. C. Silva, P. E. A. S. Câmara & J. A. Meira-Neto, 2016. Brazil’s mining code under attack: giant mining companies impose unprecedented risk to biodiversity. Biodiversity and Conservation 25(2): 407–409.

    Article  Google Scholar 

  • Melo, A. S., 2013. CommEcol: Community Ecology Analyses. R package version 1.5.8/r24. http://R-Forge.Rproject.org/projects/commecol

  • Merritt, R. W. & K. Cummins, 1996. An introduction to the aquatic insects of North America, 3rd ed. Kendall/Hunt, Dubuque:

    Google Scholar 

  • Nhiwatiwa, T., T. D. Bie, B. Vervaeke, M. Barson, M. Stevens, M. P. M. Vanhove & L. Brendonck, 2009. Invertebrate communities in dry-season pools of a large subtropical river: patterns and processes. Hydrobiologia 630: 169–186.

    Article  Google Scholar 

  • Nicacio, G., E. J. Cunha, N. Hamada & L. Juen, 2020. Contrasting beta diversity and functional composition of aquatic insect communities across local to regional scales in Amazonian streams. bioRxiv. https://doi.org/10.1101/2020.09.14.297077.

    Article  Google Scholar 

  • Notestine, M. K., 1994. Comparison of the respiratory currents produced by ephemeropteran nymphs with operculate gills. Journal of the Australian Entomological Society 33: 399–403.

    Article  Google Scholar 

  • Obeng, E. A., K. A. Oduro, B. D. Obiri, H. Abukari, R. T. Guuroh, G. D. Djagbletey, J. Appiah-Korang & M. Appiah, 2019. Impact of illegal mining activities on forest ecosystem services: local communities’ attitudes and willingness to participate in restoration activities in Ghana. Heliyon 5: e02617.

    Article  Google Scholar 

  • Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R. B. & H. Wagner, 2016. Vegan: Community Ecology Package. R package version 2.0–8. http://CRAN.R-project.org/package=vegan

  • Patterson, B. D. & W. Atmar, 1986. Nested subsets and the structure of insular mammalian faunas and archipelagos. Biological Journal of the Linnean Society 28: 65–82.

    Article  Google Scholar 

  • Pavoine, S. & S. Dolédec, 2005. The apportionment of quadratic entropy: a useful alternative for partitioning diversity in ecological data. Environmental and Ecological Statistics 12: 125–138.

    Article  CAS  Google Scholar 

  • Pavoine, S., J. Vallet, A. B. Dufour, S. Gachet & H. Daniel, 2009. On the challenge of treating various types of variables: application for improving the measurement of functional diversity. Oikos 118: 391–402.

    Article  Google Scholar 

  • Peláez, O. & C. S. Pavanelli, 2019. Environmental heterogeneity and dispersal limitation explain different aspects of β-diversity in Neotropical fish assemblages. Freshwather Biology 64: 497–505.

    Article  Google Scholar 

  • Peres-Neto, P. R., R. Legendre, S. Dray & D. Borcard, 2006. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87: 2614–2625.

    Article  Google Scholar 

  • Peru, N. & S. Dolédec, 2010. From compositional to functional biodiversity metrics in bioassessment: a case study using stream macroinvertebrate communities. Ecological Indicators 10: 1025–1036.

    Article  CAS  Google Scholar 

  • Petchey, O. L. & K. J. Gaston, 2006. Functional diversity: back to basics and looking forward. Ecology Letters 9: 741–758.

    Article  Google Scholar 

  • R Core Team, 2021. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna [available on internet at http://www.r-project.org/]

  • Rocha, M. P., L. M. Bini, S. Domisch, K. T. Tolonen, J. Jyrkänkallio-Mikkola, J. Soininen, J. Hjort & J. Heino, 2018. Local environment and space drive multiple facets of stream macroinvertebrate beta diversity. Journal of Biogeography. https://doi.org/10.1111/jbi.13457.

    Article  Google Scholar 

  • Rosenberg, D. M. & V. H. Resh, 1993. Freshwater Biomonitoring and Benthic Macroinvertebrates, Chapman & Hall, London:, 488.

    Google Scholar 

  • Salles, F., E. R. Silva & M. Hubbard, 2004. As espécies de Ephemeroptera (Insecta) registradas para o Brasil. Biota Neotropica 4: 1–34.

    Google Scholar 

  • Salles, F. F., J. L. Gattolliat, K. B. Angeli, M. R. De-Souza, I. C. Gongalves, J. L. Nessimian & M. Sartori, 2014. Discovery of an alien species of mayfly in South America (Ephemeroptera). ZooKeys 399: 1–16.

    Article  Google Scholar 

  • Shimano, Y., F. Salles & H. S. Cabette, 2011. Ephemeroptera (Insecta) from east of Mato Grosso State, Brazil. Biota Neotropica 11: 239–253.

    Article  Google Scholar 

  • Shimano, Y., F. Salles, L. R. Faria & H. S. Cabette, 2012. Distribuição espacial das guildas tróficas e estruturação da comunidade de Ephemeroptera (Insecta) em córregos do Cerrado de Mato Grosso, Brasil. Iheringia, Série Zoologia 102: 187–196.

    Article  Google Scholar 

  • Shimano, Y., L. Juen, F. Salles, D. S. Nogueira & H. S. R. Cabette, 2013. Environmental and spatial processes determining Ephemeroptera (Insecta) structures in tropical streams. Annales De Limnologie - International Journal of Limnology 49: 31–41.

    Article  Google Scholar 

  • Shimano, Y., M. Cardoso & L. Juen, 2018. Ecological studies of mayflies (Insecta, Ephemeroptera): can sampling effort be reduced without losing essential taxonomic and ecological information? Acta Amazonica 48: 137–214.

    Article  Google Scholar 

  • Shimano, Y., D. S. Nogueira & L. Juen, 2021. Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia 848: 4075–4092.

    Article  Google Scholar 

  • Shimano, Y., 2015. Ephemeroptera (Insecta) do Brasil: estado da arte, amostragem, influencias e distribuição. Tese de doutorado (PhD Dissertation), Universidade Federal do Pará, Belém, p. 141.

  • Sobral, F. L. & M. V. Cianciaruso, 2012. Estrutura filogenética e funcional de assembléias: (re)montando a ecologia de comunidades em diferentes escalas espaciais. Bioscience Journal 28: 617–631.

    Google Scholar 

  • Soininen, J., R. McDonald & H. Hillebrand, 2007. The distance decay of similarity in ecological communities. Ecography 30: 3–12.

    Article  Google Scholar 

  • Soininen, J., J. Heino & J. Wang, 2018. A meta-analysis of nestedness and turnover components of beta diversity across organisms and ecosystems. Global Ecology and Biogeography 27: 96–109.

    Article  Google Scholar 

  • Landa V. & T. Soldán, 1995. Mayflies as bioindicators of water quality and environmental change on a regional and global scale. In: Corkum L.D., J. J. H. Ciborowski, Current Directions in Research on Ephemeroptera. Canadian Scholars' Press, Inc. Toronto: 21–29.

  • Sonter, L. J., D. Herrera, D. J. Barrett, G. L. Galford, C. J. Moran & B. S. Soares-Filho, 2017. Mining drives extensive deforestation in the Brazilian Amazon. Nature Communications 8(1): 1–7.

    Article  CAS  Google Scholar 

  • Souza-Filho, P. W. M., T. C. Giannini, R. Jaffe, A. M. Giulietti, D. C. Santos & W. R. Nascimento, 2019. Mapping and quantification of ferruginous outcrop savannas in the Brazilian Amazon: a challenge for biodiversity conservation. PLoS ONE 14(1): e0211095.

    Article  CAS  Google Scholar 

  • Swenson, N. G., P. Anglada-Cordero & J. A. Barone, 2011. Deterministic tropical tree community turnover: evidence from patterns of functional beta diversity along an elevational gradient. Proceedings of the Royal Society B: Biological Sciences 278: 877–884.

    Article  Google Scholar 

  • Swenson, N. G. J. C., J. Davies, D. L. Erickson, J. Forero-Montana, A. H. Hurlbert, W. J. Kress, J. Thompson, M. Uriarte, S. J. Wright & J. K. Zimmerman, 2012. Temporal turnover in the composition of tropical tree communities: functional determinism and phylogenetic stochasticity. Ecology 93: 490–499.

    Article  Google Scholar 

  • Tapolczai, K., A. Bouchez, P. A. Stenger-Kovács, J. Padisák & F. Rimet, 2016. Trait-based ecological classifications for benthic algae: review and perspectives. Hydrobiologia 776: 1–17.

    Article  Google Scholar 

  • Viana, P., N. Mota, A. Gil, A. Salino, D. Zappi, R. Harley, A. Ilkiu-Borges, R. Secco, T. Almeida, M. Watanabe, J. Santos, M. Trovó, C. Maurity & A. Giulietti, 2016. Flora das cangas da Serra dos Carajás, Pará, Brasil: história, área de estudos e metodologia. Rodriguésia 67: 1107–1124.

    Article  Google Scholar 

  • Villéger, S. S., G. Grenouillet & S. Brosse, 2013. Decomposing functional beta-diversity reveals that low functional betadiversity is driven by low functional turnover in European fish assemblages. Global Ecology and Biogeography 22: 671–681.

    Article  Google Scholar 

  • Violle, C., M. L. Navas, D. Vile, E. Kazakou, C. Fortunel, I. Hummel & E. Garnier, 2006. Let the concept of trait be functional! Oikos 116: 882–892.

    Article  Google Scholar 

  • Wang, H., H. Fu, Z. Wen, C. Yuan, X. Zhang, L. Ni & T. Cao, 2021. Seasonal patterns of taxonomic and functional beta diversity in submerged macrophytes at a fine scale. Ecology and Evolution 11: 9827–9836.

    Article  CAS  Google Scholar 

  • Webb, C. T., J. A. Hoeting, G. M. Ames, M. I. Pyne & N. L. Poff, 2010. A structured and dynamic framework to advance traits-based theory and prediction in ecology. Ecology Letters 13: 267–283.

    Article  Google Scholar 

  • Weiher, E., D. Freund, T. Bunton, A. Stefanski, T. Lee & S. Bentiveng, 2011. Advances, challenges and a developing synthesis of ecological community assembly theory. Philosophical Transactions of the Royal Society. https://doi.org/10.1098/rstb.2011.0056.

    Article  Google Scholar 

  • Wichard, W., W. Arens & G. Eisenbeis, 2002. Biological Atlas of Aquatic Insects, Apollo Books, Stenstrup:, 339.

    Book  Google Scholar 

  • Wichard, W., 1979. Structure and function of the respiratory epithelium in the tracheal gills of mayfly larvae. In: Pasternak, K. & R. Sowa (eds), Proceedings of the Second International Conference on Ephemeroptera, Państwowe Wydawnictwo Naukowe, Warszawa-Kraków. pp. 306–309.

  • Wright, D. H., B. Patterson, G. Mikkelson, A. Cutler & W. Atmar, 1998. A comparative analysis of nested subset patterns of species composition. Oecologia 113: 1–20.

    Article  Google Scholar 

  • Zappi, D. C., 2017. Paisagens e plantas de Carajás/Landscapes and plants of Carajás. Instituto Tecnológico Vale, Belém: 248.

  • Zhou, C. F. & L. Y. Zheng, 2010. The Genus prosopistoma from China, with descriptions of two new species (Ephemeroptera: Prosopistomatidae). Aquatic inSects 26: 3–8.

    Article  Google Scholar 

  • Zorzal-Almeida, S., L. M. Bini & D. C. Bicudo, 2017. Beta diversity of diatoms is driven by environmental heterogeneity, spatial extent and productivity. Hydrobiologia 800: 7–16.

    Article  Google Scholar 

Download references

Acknowledgements

The first author thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) for granting a scholarship during her master’s degree, and the Federal University of Pará (UFPA), through the Dean for International Relations (PROINTER), Dean for Research and Graduate Studies (PROPESP), the Organization of American States (OEA), the Graduate Program in Ecology (PPGECO), and the Laboratory of Primary Producers (ECOPRO) for infrastructure, support, and financial resources. L. Juen thanks the Brazilian National Research Council (CNPq) for a productivity scholarship (process 304710/2019-9), and the Brazilian Institute for the Environment and Renewable Natural Resources (IBAMA) and Chico Mendes Institute for Biodiversity Conservation (ICMBio), which are responsible for the environmental licensing process for mining projects in Brazil, environmental monitoring programs, and the authorization of specimen collection in this study. We would also like to thank Amplo Engenharia e Gestão de Projeto for logistic support, and we are grateful to the Vale Company for allowing us to collect data within its area of operation in the Carajás region.

Funding

Funding was provided by CNPQ (Grant No. 304710/2019-9) and CAPES (Grant No. 001).

Author information

Authors and Affiliations

  1. Universidade Federal do Pará (UFPA), Programa de Pós-Graduação em Ecologia (PPGECO), Augusto Corrêa Street, 1, Guamá, Belém, PA, 66075-110, Brazil

    Ana Carolina Enríquez Espinosa, Erlane José Cunha, Leandro Juen & Bárbara Dunck

  2. Instituto Tecnológico Vale, Rua Boaventura da Silva, 955, Belém, PA, 66055-900, Brazil

    Erlane José Cunha

  3. Instituto Nacional de Pesquisa do Pantanal, Advanced Campus of the Museu Paraense Emílio Goeldi., Cuiabá, MT, 78060-900, Brazil

    Yulie Shimano

  4. Amplo Engenharia e Gestão de Projetos LTDA, Camões Street, 28, São Lucas, Belo Horizonte, MG, 30110-017, Brazil

    Samir Rolim

  5. Vale S.A., PA Rodovia Raymundo Mascarenhas, S/N Carajás, Parauapebas, PA, 68516 000, Brazil

    Leandro Mioli

  6. Universidade Federal Rural da Amazônia (UFRA), Instituto Socioambiental e dos Recursos Hídricos (ISARH), Avenida Perimetral, Belém, PA, 660778-30, Brazil

    Bárbara Dunck

Authors
  1. Ana Carolina Enríquez Espinosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erlane José Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yulie Shimano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Samir Rolim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Leandro Mioli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Leandro Juen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bárbara Dunck
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LJ conceived the study and designed the methods; YS collected the data; ACE, EC and BD analyzed the data; ACE, EC, LJ, YS and BD led the writing of the manuscript; LJ, ACE, EC, YS, SR, KF, and BD contributed critically to the different drafts and gave their final approval for submission.

Corresponding author

Correspondence to Bárbara Dunck.

Ethics declarations

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Handling editor: Marcelo S. Moretti

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 47 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Espinosa, A.C.E., Cunha, E.J., Shimano, Y. et al. Functional diversity of mayflies (Ephemeroptera, Insecta) in streams in mining areas located in the Eastern Amazon. Hydrobiologia 850, 929–945 (2023). https://doi.org/10.1007/s10750-022-05134-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-022-05134-x

Keywords

Search

Navigation