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Non-native fish species are related to the loss of ecological integrity in Neotropical streams: a multimetric approach

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Abstract

The use of multimetric indices (MMIs) became a common practice for evaluating ecological integrity of aquatic ecosystems. However, most developed MMIs ignore non-native species as an impact source to establish reference conditions. We developed an MMI to identify if non-native fish species are associated with Neotropical stream integrity by considering the presence of non-native species as an impact source. We calculated and evaluated responsiveness to the presence of non-native species using fish metrics, which were selected with a bootstrap procedure. Streams for calibration and validation were also selected with a bootstrap procedure. From the candidate MMIs generated, we selected models with different combinations of fish metrics. The generated MMIs presented a satisfactory performance in distinguishing reference streams from those impacted by non-native species. The abundance of non-native species was highly correlated with urbanization and seems to be more important than urbanization to drive native abundance loss. Our study is one of the first attempts to develop MMIs in which non-native species are considered as impact sources and used to identify impacted and reference sites. The final MMI that we developed might be a useful tool for aquatic biodiversity conservation and the development and application of non-native species control actions.

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References

  • Abell, R. M., M. L. Thieme, C. Revenga, M. Bryer, M. Kottelat, N. Bogutskaya, B. Coad, K. Mandrak, S. B. Contreras, W. Bussing, M. L. J. Stiassny, P. Skelton, G. R. Allen, P. Unmack, A. Naseka, R. Ng, N. Sindorf, J. Robertson, E. Armijo, J. V. Higgins, T. J. Heibel, E. Wikramanake, D. Olson, H. L. Lopez, R. E. Reis, J. G. Lundberg, M. H. Sabaj Perez & P. Petry, 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58: 403–414.

    Article  Google Scholar 

  • Abilhoa, V., L. F. Duboc & D. P. De Azevedo, 2008. The fish community in an Araucaria Forest stream, upper Iguaçu River basin, southern Brazil. Revista Brasileira de Zoologia 25: 238–246.

    Article  Google Scholar 

  • Abilhoa, V., R. R. Braga, H. Bornatowski & J. R. S. Vitule, 2011. Fishes of the Atlantic Rain Forest streams: ecological patterns and conservation. In Grillo, O. & G. Venora (eds), Changing Diversity in Changing Environment. InTech, Rijeka: 259–282.

    Google Scholar 

  • Aho, K., D. Derryberry & T. Peterson, 2014. Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95: 631–636.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Avma, 2001. Panel on euthanasia. Report of the AVMA panel on euthanasia. Journal of the American Veterinary Medical Association 218(5): 669–696.

    Article  Google Scholar 

  • Bailey, R. C., M. G. Kennedy, M. Z. Dervish & R. M. Taylor, 1998. Biological assessment of freshwater ecosystems using a reference condition approach: Comparing predicted and actual benthic invertebrate communities in Yukon streams. Freshwater Biology 39(4): 765–774.

    Article  Google Scholar 

  • Bailey, R. C., T. B. Reynoldson, A. G. Yates, J. Bailey & S. Linke, 2006. Integrating stream bioassessment and landscape ecology as a tool for land use planning. Freshwater Biology 52(5): 908–917.

    Article  Google Scholar 

  • Barbone, E., I. Rosati, S. Reizopoulou & A. Basset, 2012. Linking classification boundaries to sources of natural variability in transitional waters: a case study of benthic macroinvertebrates. Ecological Indicators 12: 105–122.

    Article  Google Scholar 

  • Barbour, M. T., J. Gerritsen, B. D. Snyder & J. B. Stribling, 1999. Rapid Bioassessment Protocols for Use in Streams and Wadeable Rivers: Periphyton, Benthic Macroinvertebrates and Fish.Second Edition.EPA 841-B- 99-002.U.S. Environmental Protection Agency, Office of Water; Washington, D.C.

  • Baumgartner, G., C. S. Pavanelli, D. Baumgartner, A. G. Bifi, T. Debona & V. A. Frana, 2012. Peixes do baixo rio Iguaçu. Maringá: EDUEM: 203 p. in Portuguese.

  • Blackburn, T. M., F. Essl, T. Evans, P. E. Hulme, J. M. Jeschke, I. Kühn, S. Kumschick, Z. Marková, A. Mrugała, W. Nentwig, J. Pergl, P. Pyšek, W. Rabitsch, A. Ricciardi, D. M. Richardson, A. Sendek, M. Vilá, J. R. U. Wilson, M. Winter, P. Genovesi & S. Bacher, 2014. A unified classification of alien species based on the magnitude of their environmental impacts. PLOS Biology 12(5): e1001850.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bockmann, F. A., L. Casatti & M. C. C. De Pinna, 2004. A new species of trichomycterid catfish from the Rio Paranapanema basin, southeastern Brazil (Teleostei: Siluriformes), with comments on the phylogeny of the family. Ichthyological Exploration of Freshwaters 15(3): 225–242.

    Google Scholar 

  • Bozzetti, M. & H. U. Schulz, 2004. An index of biotic integrity based on fish assemblages for subtropical streams in southern Brazil. Hydrobiologia 529: 133–144.

    Article  Google Scholar 

  • Brasher, A. M. D., C. D. Luton, S. L. Goodbred & R. H. Wolff, 2006. Invasion patterns along elevation and urbanization gradients in Hawaiian streams. Transactions of the American Fisheries Society 135: 1109–1129.

    Article  Google Scholar 

  • Cadotte, M. W., S. L. E. Yasui, S. Livingstone & J. S. MacIvor, 2017. Are urban systems beneficial, detrimental, or indifferent for biological invasion? Biological Invasions 19: 3489–3503.

    Article  Google Scholar 

  • Carniatto, N., S. M. Thomaz, E. R. Cunha, R. Fugi & R. Ota, 2013. Effects of an invasive alien Poaceae on aquatic macrophytes and fish communities in a Neotropical reservoir. Biotropica 45: 747–754.

    Article  Google Scholar 

  • Casatti, L., F. Langeani, A. M. Silva & R. M. C. Castro, 2006. Stream fishes, water and habitat quality in a pasture dominated basin, southeastern Brazil. Brazilian Journal of Biology 66: 681–696.

    Article  CAS  Google Scholar 

  • Casatti, L., C. P. Ferreira & F. Langeani, 2009. A fish-based biotic integrity index for assessment of lowland streams in southeastern Brazil. Hydrobiologia 623: 173–189.

    Article  Google Scholar 

  • Casatti, L., F. B. Teresa, T. Gonçalves-Souza, E. Bessa, A. R. Manzotti, C. S. Gonçalves & J. Zeni, 2012. From forests to cattail: how does the riparian zone influence stream fish? Neotropical Ichthyology 10(1): 205–214.

    Article  Google Scholar 

  • Clavero, M. & E. García-Berthou, 2005. Invasive species are a leading cause of animal extinctions. Trends in Ecology and Evolution 20: 110.

    Article  PubMed  Google Scholar 

  • Clavero, M., V. Hermoso, E. Aparicio & F. N. Godinho, 2013. Biodiversity in heavily modified waterbodies: native and introduced fish in Iberian reservoirs. Freshwater Biology 58: 1190–1201.

    Article  Google Scholar 

  • Copp, G. H., J. R. Britton, Z. Guo, V. Edmonds-Brown, J. Pegg, L. Vilizzi & P. I. Davison, 2017. Trophic consequences of non-native pumpkinseed Lepomis gibbosus for native fishes on pond fishes. Biological Invasions 19: 25–41.

    Article  Google Scholar 

  • Couceiro, S. R. M., N. Hamada, B. R. Forsberg, T. P. Pimentel & S. L. B. Luz, 2012. A macroinvertebrate multimetric index to evaluate the biological condition of streams in the Central Amazon region of Brazil. Ecological Indicators 18: 118–125.

    Article  Google Scholar 

  • Courtenay Jr., W. R., H. F. Sahlman, W. M. I. I. Miley & D. J. Herrema, 1974. Exotic fishes in fresh and brackish waters of Florida. Biological Conservation 6(4): 292–302.

    Article  Google Scholar 

  • Cunico, A. M., A. A. Agostinho & J. D. Latini, 2006. Influência da urbanização sobre as assembleias de peixes em três córregos de Maringá, Paraná (Influence of urbanization upon fish assemblages in thre estreams of Maringá, Paraná) Revista Brasileira de Zoologia 23: 1101–1110 (in Portuguese).

  • Daga, V. S., F. Skóra, A. A. Padial, V. Abilhoa, É. A. Gubiani & J. R. S. Vitule, 2015. Homogenization dynamics of the fish assemblages in Neotropical reservoirs: comparing the roles of introduced species and their vectors. Hydrobiologia 746: 327–347.

    Article  Google Scholar 

  • Daga, V. S., T. Debona, V. Abilhoa, É. A. Gubiani, & J. R. S. Vitule, 2016. Non-native fish invasions of a Neotropical ecoregion with high endemism: a review of the Iguaçu River. Aquatic Invasions 11(2): 209–223. https://doi.org/10.3391/ai.2016.11.2.01

  • Detenbeck, N. E. & D. A. Cincotta, 2008. Comparability of a regional and state survey: effects on fish IBI assessment for West Virginia, U.S.A. Hydrobiologia 603: 279–300.

    Article  Google Scholar 

  • Didham, R. K., J. M. Tylianakis, M. A. Hutchinson, R. M. Ewers & N. J. Gemmell, 2005. Are invasive species the drivers of ecological change? Trends in Ecology and Evolution 20: 470–474.

    Article  PubMed  Google Scholar 

  • Didham, R. K., J. M. Tylianakis, N. J. Gemmell, T. A. Rand & R. M. Ewers, 2007. Interactive effects of habitat modification and species invasion on native species decline. Trends in Ecology and Evolution 22: 489–496.

    Article  PubMed  Google Scholar 

  • Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. I. Kawabata, D. J. Knowler, C. Leveque, R. J. Naiman, A. H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81: 163–182.

    Article  PubMed  Google Scholar 

  • Elton, C. S., 1958. The ecology of invasions by animals and plants. Methuen, London.

    Book  Google Scholar 

  • Esteves, K. E. & J. Lobón-Cerviá, 2001. Composition and trophic structure of a fish community of a clear water Atlantic rainforest stream in southeastern Brazil. Envi-ronmental Biology of Fishes 62: 429–440. https://doi.org/10.1023/A:1012249313341.

  • Fausch, K. D., J. D. Lyons, P. L. Angermeier & J. R. Karr, 1990. Fish communities as indicators of environmental degradation. American Fisheries Society Symposium 8: 123–144.

    Google Scholar 

  • Ferreira, C. P. & L. Casatti, 2006. Integridade biótica de um córrego na bacia do Alto Rio Paraná avaliada por meio da comunidade de peixes. Biota Neotropica 6: 1–25.

    Google Scholar 

  • Fitzgerald, D. B., M. Tobler & K. O. Winemiller, 2016. From richer to poorer: successful invasion by freshwater fishes depends on species richness of donor and recipient basins. Global Change Biology 22(7): 2440–2450.

    Article  PubMed  Google Scholar 

  • Forneck, S. C., F. M. Dutra, C. E. Zacarkim & A. M. Cunico, 2016. Invasion risks by non-native freshwater fishes due to aquaculture activity in a Neotropical stream. Hydrobiologia 773: 193–205.

    Article  Google Scholar 

  • Frehse, F. A., R. R. Braga, G. A. Nocera & J. R. S. Vitule, 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biological Invasions 18: 3713–3725.

    Article  Google Scholar 

  • Froese, R. & D. Pauly, 2016.FishBase. http://www.fishbase.org (Accessed 20 June 2016).

  • Góis, K. S., F. M. Pelicice, L. C. Gomes & A. A. Agostinho, 2015. Invasion of an Amazonian cichlid in the Upper Paraná River: facilitation by dams and decline of a phylogenetically related species. Hydrobiologia 746: 401–413.

    Article  CAS  Google Scholar 

  • Google, 2014. Google Earth. Google Inc, Mountain View.

    Google Scholar 

  • Graça, W. J. & C. S. Pavanelli, 2007. Peixes da planície de inundação do alto rio Paraná e áreas adjacentes. EDUEM, Maringá.

    Google Scholar 

  • Grove, M. K., G. S. Bilotta, R. R. Woockman & J. S. Schwartz, 2015. Suspended sediment regimes in contrasting reference-condition freshwater ecosystems: Implications for water quality guidelines and management. Science of the Total Environment 502: 481–492.

    Article  PubMed  CAS  Google Scholar 

  • Hauer, R. H. & G. Lamberti. 2007. Methods in Stream Ecology, 2nd ed. Academic Press. London.

  • Havel, J. E., K. E. Kovalenko, S. M. Thomaz, S. Amalfitano & L. B. Kats, 2015. Aquatic invasive species: challenges for the future. Hydrobiologia 750: 147–170.

    Article  Google Scholar 

  • Hering, D., C. J. Feld, O. Moog & T. Ofenbock, 2006. Cook book for the development of a Multimetric Index for biological condition of aquatic ecosystems: experiences from the European AQEM and STAR projects and related initiatives. Hydrobiologia 566: 311–324.

    Article  Google Scholar 

  • Hermoso, V. & M. Clavero, 2013. Revisiting ecological integrity 30 years later: non-native species and the misdiagnosis of freshwater ecosystem health. Fish and Fisheries 14: 416–423.

    Article  Google Scholar 

  • Hermoso, V., M. Clavero, F. Blanco-Garrido & J. Prenda, 2010. Assessing the ecological status in species-poor systems: a fish-based index for Mediterranean Rivers (Guadiana River, SW Spain). Ecological Indicators 10: 1152–1161.

  • Hermoso, V., M. Clavero, F. Blanco-Garrido & J. Prenda, 2011. Invasive species and habitat degradation in Iberian streams: an analysis of their role in freshwater fish diversity loss. Ecological Applications 21: 175–188.

    Article  PubMed  Google Scholar 

  • Johnson, J. & K. Omland, 2004. Model selection in ecology and evolution. Trends in Ecology and Evolution 19(2): 101–108.

    Article  PubMed  Google Scholar 

  • Júlio Jr., H. F., C. D. Tós, A. A. Agostinho & C. S. Pavanelli, 2009. A massive invasion of fish species after eliminating a natural barrier in the upper Rio Paraná basin. Neotropical Ichthyology 7: 709–718.

    Article  Google Scholar 

  • Karr, J. R., 1981. Assessment of biotic integrity using fish communities. Fisheries 6: 21–27.

    Article  Google Scholar 

  • Karr, J. R., 1991. Biological integrity: A long-neglected aspect of water resource management. Ecological Applications 1: 66–84.

    Article  PubMed  Google Scholar 

  • Kennard, M. J., B. D. Harch, B. J. Pusey & A. H. Arthington, 2006. Accurately defining the reference condition for summary biotic metrics: a comparison of four approaches. Hydrobiologia 572: 151–170.

    Article  Google Scholar 

  • Kleynhans, C. J., 1999. The development of a fish index to assess the biological integrity of South African rivers. Water SA. 25: 265–278.

    Google Scholar 

  • Kühn, I., J. Wolf & A. Schneider, 2017. Is there an urban effect in alien plant invasions? Biological Invasions 19: 3505–3513.

    Article  Google Scholar 

  • Langeani, F., R. M. C. Castro, O. T. Oyakawa, O. A. Shibatta, C. S. Pavanelli & L. Casatti, 2007. Ichthyofauna diversity of the Upper Rio Paraná: present composition and future perspectives. Biota, Neotropica 7(3): 181–197.

    Article  Google Scholar 

  • Light, T. & M. P. Marchetti, 2006. Distinguishing between invasions and habitat changes as drivers of biodiversity loss among California’s freshwater fishes. Conservation Biology 21: 434–446.

    Article  Google Scholar 

  • Levine, J. M. & C. M. D’Antonio, 1999. Elton revisited: a review of evidence linking diversity and invasibility. Oikos 87: 15–26.

    Article  Google Scholar 

  • Linke, S., R. C. Bailey & J. Schwindt, 1999. Temporal variability of stream bioassessments using benthic macroinvertebrates. Freshwater Biology 42: 575–584.

    Article  Google Scholar 

  • Lockwood, J. L., P. Cassey & T. Blackburn, 2009. The more you introduce the more you get: the role of colonization pressure and propagule pressure in invasion ecology. Diversity and Distributions 15: 904–910.

    Article  Google Scholar 

  • Lövei, G. L., T. M. Lewinsohn & Invasions in Megadiverse Regions Network, 2012. Megadiverse developing countries face huge risks from invasives. Trends in Ecology & Evolution 27(1): 2–3.

    Article  Google Scholar 

  • Lowry, E., E. J. Rollinson, A. J. Laybourn, T. E. Scott, M. E. Aiello-Lammens, S. M. Gray, J. Mickley & J. Gurevitch, 2013. Biological invasions: a field synopsis, systematic review, and database of the literature. Ecology and Evolution 3: 182–196.

    Article  PubMed Central  Google Scholar 

  • MacDougall, A. S. & R. Turkington, 2005. Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86: 42–55.

    Article  Google Scholar 

  • Magalhães, A. L. B. & C. N. Jacobi, 2017. Colorful invasion in permissive Neotropical ecosystems: establishment of ornamental non-native poeciliids of the genera Poecilia/Xiphophorus (Cyprinodontiformes: Poeciliidae) and management alternatives. Neotropical Ichthyology 15(1): e160094.

    Article  Google Scholar 

  • Michelan, T. S., S. M. Thomaz, R. P. Mormul & P. Carvalho, 2010. Effects of an exotic-invasive macrophyte (tropical signal-grass) on native plant community composition, species richness and functional diversity. Freshwater Biology 55(6): 1315–1326.

    Article  Google Scholar 

  • 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 vegan, vers. 2.2-1. http://www.cran.r-project.org/package=vegan

  • Olden, J. D., N. LeRoy Poff, M. R. Douglas, M. E. Douglas & K. D. Fausch, 2004. Ecological and evolutionary consequences of biotic homogenization. Trends in Ecology & Evolution 19: 18–24.

    Article  Google Scholar 

  • Oliveira, T. D., A. C. Reis, C. O. Guedes, M. L. Sales, E, P. R. Braga, T. F. Ratton, B. P. Maia & A. L. B. Magalhães, 2014. Establishment of nonnative guppy Poecilia reticulata (Peters, 1859) (Cyprinodontiformes: Poeciliidae) in a Municipal Park located in Minas Gerais State, Brazil. Pan-American Journal of Aquatic Sciences 9 (1): 21–30.

  • Orsi, M. L. & J. R. Britton, 2014. Long-term changes in the fish assemblage of a neotropical hydroelectric reservoir. Journal of Fish Biology 84: 1964–1970.

    Article  PubMed  CAS  Google Scholar 

  • Oyakawa, O. T., A. Akama, K. C. Mautari & J. C. Nolasco, 2006. Peixes de riachos da Mata Atlântica: nas unidades de conservação do Vale do Rio Ribeira de Iguape no Estado de São Paulo. Editora Neotropica, São Paulo.

    Google Scholar 

  • Padial, A. A., A. A. Agostinho, V. M. Azevedo-Santos, F. A. Frehse, D. P. Lima-Junior, A. L. B. Magalhaes, R. P. Mormul, F. M. Pelicice, L. A. V. Bezerra, M. L. Orsi, M. Petrere-Junior & J. R. S. Vitule, 2017. The ‘‘Tilapia Law’’ encouraging non-native fish threatens Amazonian River basins. Biodiversity Conservation 26: 243–246.

    Article  Google Scholar 

  • Parker, I. M., D. Simberloff, W. M. Lonsdale, K. Goodell, M. Wonham, P. M. Kareiva, M. H. Williamson, B. VonHolle, P. B. Moyle, J. E. Byers & L. Goldwasser, 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biological Invasions 1: 3–19.

    Article  Google Scholar 

  • Pelicice, F. M., J. R. S. Vitule, D. P. Lima Junior, M. L. Orsi & A. A. Agostinho, 2014. A serious new threat to Brazilian freshwater ecosystems: the naturalization of non-native fish by decree. Conservation Letters 7: 55–60.

    Article  Google Scholar 

  • Pelicice, F. M., J. D. Latini & A. A. Agostinho, 2015. Fish fauna disassembly after the introduction of a voracious predator: main drivers and the role of the invader’s demography. Hydrobiologia 746: 271–283.

    Article  Google Scholar 

  • Pelicice, F. M., V. M. Azevedo-Santos, J. R. S. Vitule, M. L. Orsi, D. P. Lima Junior, A. L. B. Magalhães, P. S. Pompeu, M. Petrere Jr. & A. A. Agostinho, 2017. Neotropical Freshwater fishes imperilled by unsustainable policies. Fish and Fisheries 1–15(746): 271–283.

    Google Scholar 

  • Pinto, B. J. T. & F. G. Araújo, 2007. Assessing the biotic integrity of the fish community in a heavily impacted segment of a tropical river in Brazil. Brazilian Archives of Biology and Technology 50: 489–502.

    Article  Google Scholar 

  • Prenda, J., M. Clavero, F. Blanco-Garrido & V. Hermoso, 2006. Threats to the conservation of biotic integrity in Iberian fluvial ecosystems. Limnetica 25: 377–388.

    Google Scholar 

  • R Development Core Team, 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.

  • Ruaro, R. & E. A. Gubiani, 2013. A scientometric assessment of 30 years of the Index of Biotic Integrity in aquatic ecosystems: Applications and main flaws. Ecological Indicators 29: 105–110.

    Article  Google Scholar 

  • Ruaro, R., E. A. Gubiani, A. M. Cunico, Y. Moretto & P. A. Piana, 2016. Comparison of fish and macroinvertebrates as bioindicators of Neotropical streams. Environmental Monitoring and Assessment 188(1): 45.

    Article  PubMed  Google Scholar 

  • Sala, O. E., F. S. Chapin III, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sanwald, L. F. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker & D. H. Wall, 2000. Global biodiversity scenarios for the year 2100. Science 287: 1770–1774.

    Article  PubMed  CAS  Google Scholar 

  • Schoolmaster Jr., D. R., J. B. Grace & E. W. Schweiger, 2012. A general theory of multimetric indices and their Properties. Methods in Ecology and Evolution 3(4): 773–781.

    Article  Google Scholar 

  • Shea, K. & P. Chesson, 2002. Community ecology theory as a framework for biological invasions. Trends in Ecology and Evolution 17: 170–176.

    Article  Google Scholar 

  • Simberloff, D., J. L. Martin, P. Genovesi, V. Maris, D. A. Wardle, J. Aronson, F. Courchamp, B. Galil, E. García-Berthou, M. Pascal, P. Pyšek, R. Sousa, E. Tabacchi & M. Vilá, 2013. Impacts of biological invasions: what’s what and the way forward. Trends in Ecology & Evolution 28: 58–66.

    Article  Google Scholar 

  • Skóra, F., V. Abilhoa, A. A. Padial & J. R. S. Vitule, 2015. Darwin’s hypotheses to explain colonization trends: evidence from a quasi-natural experiment and a new conceptual model. Diversity and Distributions 21: 583–594. https://doi.org/10.1111/ddi.12308.

  • Snyder, C. D., J. A. Young, R. Villella & D. P. Lemarié, 2003. Influences of upland and riparian land use patterns on stream biotic integrity. Landscape Ecology 18: 647–664.

    Article  Google Scholar 

  • Stoddard, J. L., D. P. Larsen, C. P. Hawkins, R. K. Norris & R. H. Johnson, 2006. Setting expectations for the ecological condition of running waters: the concept of reference condition. Ecological Applications 16: 1267–1276.

    Article  PubMed  Google Scholar 

  • Stoddard, J. L., A. T. Herlihy, D. V. Peck, R. M. Hughes, T. R. Whittier & E. Tarquino, 2008. A Process for creating multimetric indices for large-scale aquatic surveys. Journal of the North American Benthological Society. 27(4): 878–891.

    Article  Google Scholar 

  • Strahler, A. N., 1957. Quantitative analysis of watershed geomorphology. Transactions American Geophysical Union 38: 913–920.

    Article  Google Scholar 

  • Tran, T. N. Q., M. C. Jackson, D. Sheath, H. Verreycken & J. R. Britton, 2015. Patterns of trophic niche divergence between invasive and native fishes in wild communities are predictable from mesocosm studies. Journal of Animal Ecology 84: 1071–1080. https://doi.org/10.1111/1365-2656.12360.

  • Vitule, J. R. S., C. A. Freire & D. Simberloff, 2009. Introduction of non-native freshwater fish can certainly be bad. Fish and Fisheries 10: 98–108.

    Article  Google Scholar 

  • Vitule, J. R. S., F. Skóra & V. Abilhoa, 2012. Homogenization of freshwater fish faunas after the elimination of a natural barrier by a dam in Neotropics. Diversity and Distributions 18: 111–120.

    Article  Google Scholar 

  • Vitule, J. R. S., A. P. L. da Costa, F. A. Frehse, L. A. V. Bezerra, T. V. T. Occhi, V. S. Daga & A. A. Padial, 2017. Comment on fish biodiversity and conservation in South America by Reis et al. (2016). Journal of Fish Biology 90: 1182–1190.

  • Winemiller, K. O., A. A. Agostinho & E. P. Caramaschi, 2008. Fish ecology in tropical streams. In Dudgeon, D. (ed.), Tropical Stream Ecology. Academic Press, Amsterdam: 107–146.

    Chapter  Google Scholar 

  • Yates, A. G. & R. C. Bailey, 2010. Selecting objectively defined reference sites for stream bioassessment programs. Environmental Monitoring and Assessment 170: 129–140.

    Article  PubMed  Google Scholar 

  • Zhu, D. & J. Chang, 2008. Annual variations of biotic integrity in the upper Yangtze River using an adapted index of biotic integrity (IBI). Ecological Indicators 8: 564–572.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank the National Council for Scientific and Technological Development (CNPq) for a scholarship granted to the first author (141371/2016-1) and supported A.M.Cunico (555185/2006-0). R. P. Mormul is Productivity Researcher at the Brazilian Council for Scientific and Technological Development (CNPq) and acknowledges this agency for funding. W.J. Graça was supported by Fundação Araucária (Secretaria da Ciência, Tecnologia e Ensino Superior do Paraná, covenant 471/2013, protocol 36204).

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Authors and Affiliations

  1. Programa de Pós-graduação em Ecologia de Ambientes Aquáticos Continentais, Universidade Estadual de Maringá (UEM), Maringá, PR, Brazil

    Renata Ruaro, Roger Paulo Mormul & Weferson Júnio da Graça

  2. Programa de Pós-Graduação em Recursos Pesqueiros e Engenharia de Pesca, Universidade Estadual do Oeste do Paraná (UNIOESTE), Toledo, PR, Brazil

    Éder André Gubiani & Pitágoras Augusto Piana

  3. Grupo de Pesquisa em Recursos Pesqueiros e Limnologia (GERPEL), Universidade Estadual do Oeste do Paraná (Unioeste), Toledo, PR, Brazil

    Éder André Gubiani & Pitágoras Augusto Piana

  4. Programa de Pós-Graduação em Conservação e Manejo de Recursos Naturais, Universidade Estadual do Oeste do Paraná (UNIOESTE), Cascavel, PR, Brazil

    Éder André Gubiani & Pitágoras Augusto Piana

  5. Programa de Pós-graduação em Aquicultura e Desenvolvimento Sustentável, Universidade Federal do Paraná, Rua Pioneiro, Palotina, PR, 2153, Brazil

    Almir Manoel Cunico

  6. Laboratório de Ecologia, Pesca e Ictiologia, Universidade Federal do Paraná, Rua Pioneiro, Palotina, PR, 2153, Brazil

    Almir Manoel Cunico

  7. Programa de Pós-Graduação em Biologia Comparada, Departamento de Biologia e Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia), Universidade Estadual de Maringá (UEM), Avenida Colombo, Maringá, PR, 5790, Brazil

    Roger Paulo Mormul & Weferson Júnio da Graça

Authors
  1. Renata Ruaro
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  2. Roger Paulo Mormul
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  3. Éder André Gubiani
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  4. Pitágoras Augusto Piana
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  5. Almir Manoel Cunico
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  6. Weferson Júnio da Graça
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Corresponding author

Correspondence to Renata Ruaro.

Additional information

Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II

Electronic supplementary material

Below is the link to the electronic supplementary material.

10750_2018_3542_MOESM1_ESM.docx

List of permanent licenses to collect zoological material by the policies of the Ethical Conduct Committee on Animal Use. Supplementary material 1 (DOCX 15 kb)

10750_2018_3542_MOESM2_ESM.doc

Fish species collected in the sampled sites, as well as number of individuals, trophic category (D = detritivorous, O = omnivorous, H = herbivorous, I = invertivorous and P = piscivorous), origin (N = native and NN= non-native), tolerance to environmental degradation (T = tolerant and I = intolerant) and position in water column (BP = benthopelagic, WC = water column, BEN = benthic and SUR = surface). Supplementary material 2 (DOC 252 kb)

10750_2018_3542_MOESM3_ESM.docx

R software script to prepare the multimetric index to identify sites impacted by non-native fish species. Supplementary material 3 (DOCX 24 kb)

10750_2018_3542_MOESM4_ESM.docx

Histogram of the metrics P values. The metrics that presented mean values of probability less than 0.20 (P < 0.20) were included in the MMIs models (Detritivorous fish; Tolerant species; Benthopelagic fish; Surface fish; Evenness; Abundance rank). Supplementary material 4 (DOCX 2879 kb)

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Ruaro, R., Mormul, R.P., Gubiani, É.A. et al. Non-native fish species are related to the loss of ecological integrity in Neotropical streams: a multimetric approach. Hydrobiologia 817, 413–430 (2018). https://doi.org/10.1007/s10750-018-3542-y

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  • DOI: https://doi.org/10.1007/s10750-018-3542-y

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