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Coexistence between native and nonnative species: the invasion process and adjustments in distribution through time for congeneric piranhas in a Neotropical floodplain

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Abstract

Our goal was to report the progress of Serrasalmus marginatus invasion process in the upper Paraná River floodplain by exploring its mechanisms and coexistence with its native congeneric Serrasalmus maculatus. We described their temporal abundance variations; nonnative species’ predominance in specific habitats; recruitment effectiveness for both species and its spatial variations; spatial organization pattern of native and nonnative species; and how their abundance is related to their co-occurrence. Abundance data encompassed 26 years after the invasion, while the proportion analyses between the species occurred on a monthly basis and in different environments, and the spatial organization pattern was assessed using C-score index. Results showed that the population of nonnative species had a fast increase along the early years followed by a decrease in the population of the native species. Recently, their proportion seems to be stabilizing, apparently resulting from a differentiation on the use of resources. The species are allowed by the spatial organization pattern to coexist in the floodplain, despite their variable co-occurrence in different environments. It is possible to state the persistence of native species in the floodplain at lower abundances in relation to the nonnative species as well as when occupying different habitats.

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References

  • Agostinho, C. S., 2003. Reproductive aspects of piranhas Serrasalmus spilopleura and Serrasalmus marginatus into the upper Paraná river, Brazil. Brazilian Journal of Biology 63: 1–6.

    Article  CAS  Google Scholar 

  • Agostinho, C. S. & H. F. Júlio Jr., 2002. Observation of an invasion of the piranha Serrasalmus marginatus Valenciennes, 1847 (Osteichthyes, Serrasalmidae) into the Upper Paraná River, Brazil. Acta Scientiarum 24: 391–395.

    Google Scholar 

  • Agostinho, C. S. & E. E. Marques, 1994. Idade e crescimento das piranhas Serrasalmus spilopleura e Serrasalmus marginatus (Osteichthyes, Serrasalminae) do alto rio Paraná. Revista UNIMAR 16: 175–187.

    Google Scholar 

  • Agostinho, A. A. & M. Zalewski, 1996. A Planície Alagável do Alto Rio Paraná: Importância e Preservação. EDUEM, Maringá.

    Google Scholar 

  • Agostinho, A. A., H. F. Julio Jr. & M. Petrere Jr., 1994. Itaipu reservoir (Brazil): impacts of the impoundment on the fish fauna and fisheries. In Cowx, I. G. (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Oxford: 171–184.

    Google Scholar 

  • Agostinho, C. S., A. A. Agostinho, E. E. Marques & L. M. Bini, 1997a. Abiotic factors influencing piranha attacks on netted fish in the Upper Paraná River, Brazil. North American Journal of Fisheries Management 17: 712–718.

    Article  Google Scholar 

  • Agostinho, A. A., H. F. Júlio Jr., L. C. Gomes, L. M. Bini & C. S. Agostinho, 1997b. Composição, abundância e distribuição espaço-temporal da ictiofauna. In Vazzoler, A. E. A. M., A. A. Agostinho & N. S. Hahn (eds), A Planície de Inundação do Alto Rio Paraná: Aspectos Físicos, Biológicos e Socioeconômicos. EDUEM, Maringá: 179–208.

    Google Scholar 

  • Agostinho, C. S., N. S. Hahn & E. E. Marques, 2003a. Patterns of food resource use by two congeneric species of piranhas (Serrasalmus) on the upper Paraná River floodplain. Brazilian Journal of Biology 63: 177–182.

    Article  CAS  Google Scholar 

  • Agostinho, A. A., F. A. Lansac-Tôha & A. M. Takeda, 2003b. Relações entre macrófitas e fauna aquática e suas implicações no manejo. In Thomaz, S. M. & L. M. Bini (eds), Ecologia e Manejo de Macrófitas Aquáticas. EDUEM, Maringá: 261–279.

    Google Scholar 

  • Agostinho, A. A., F. M. Pelicice & L. C. Gomes, 2008. Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Brazilian Journal of Biology 68: 1119–1132.

    Article  CAS  Google Scholar 

  • Agostinho, A. A., H. I. Suzuki, R. Fugi, D. C. Alves, L. H. Tonella & L. A. Espindola, 2015. Ecological and life history traits of Hemiodus orthonops in the invasion process: looking for clues at home. Hydrobiologia 746: 415–430.

    Article  Google Scholar 

  • Alexandre, P. C., E. A. Luiz, P. A. Piana, L. C. Gomes & A. A. Agostinho, 2004. Relação estoque-recrutamento para as piranhas Serrasalmus marginatus (Valenciennes, 1847) e Serrasalmus maculatus (Kner, 1860) no rio Baía, alto rio Paraná. Acta Scientiarum Biological Sciences 26: 303–307.

    Google Scholar 

  • Allen, C. R., K. T. Nemec, D. A. Wardwell, J. D. Hoffman, M. Brust, K. L. Decker, D. Fogell, J. Hogue, A. Lotz, T. Miller, M. Pummill, L. E. Ramirez-Yañez & D. R. Uden, 2013. Predictors of regional establishment success and spread of introduced non-indigenous vertebrates. Global Ecology and Biogeography 22: 889–899.

    Article  Google Scholar 

  • Alves, G. H. Z., B. R. S. Figueiredo, G. I. Manetta, P. A. Sacramento, R. M. Tófoli & E. Benedito, 2017. Trophic segregation underlies the coexistence of two piranha species after the removal of a geographic barrier. Hydrobiologia 797: 57–68.

    Article  Google Scholar 

  • Blackburn, T. M., P. Pyšek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarošík, J. R. U. Wilson & D. M. Richardson, 2011. A proposed unified framework for biological invasions. Trends in Ecology and Evolution 26: 333–339.

    Article  PubMed  Google Scholar 

  • 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. Vilà, 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: e1001850.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bøhn, T., P. Amundsen & A. Sparrow, 2008. Competitive exclusion after invasion? Biological Invasions 10: 359–368.

    Article  Google Scholar 

  • Catford, J. A., R. Jansson & C. Nilsson, 2009. Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Diversity Distributions 15: 22–40.

    Article  Google Scholar 

  • Darwin, C., 1859. On the Origin of Species. J. Murray, London.

    Google Scholar 

  • Diez, J. M., J. J. Sullivan, P. E. Hulme, G. Edwards & R. P. Duncan, 2008. Darwin’s naturalization conundrum: dissecting taxonomic patterns of species invasions. Ecology Letters 11: 674–681.

    Article  PubMed  Google Scholar 

  • Dudgeon, D., A. H. Arthington, M. O. Gessner, Z. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A. 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 

  • Ehrenfeld, J. C., 2010. Ecosystem consequences of biological invasions. Annual Review of Ecology, Evolution and Systematics 41: 59–80.

    Article  Google Scholar 

  • Gallien, L. & M. Carboni, 2017. The community ecology of invasive species: where are we and what’s next? Ecography 40: 335–352.

    Article  Google Scholar 

  • Gois, 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 

  • Gotelli, N. J. & D. J. McCabe, 2002. Species co-occurrence: a meta-analysis of J. T. Diamond’s assembly rules model. Ecology 83: 2091–2096.

    Article  Google Scholar 

  • Gubiani, E. A., L. C. Gomes, A. A. Agostinho & E. K. Okada, 2007. Persistence of fish population in the upper Paraná River: effects of water regulation by dams. Ecology of Freshwater Fish 16: 191–197.

    Google Scholar 

  • Havel, J. E., C. E. Lee & M. J. V. Zanden, 2005. Do reservoirs facilitate invasions into landscapes? BioScience 55: 518–525.

    Article  Google Scholar 

  • Jackman, S., 2012. pscl: Classes and Methods for R Developed in the Political Science Computational Laboratory, Stanford University. Department of Political Science, Stanford University. Stanford, CA. R package version 1.04.4. http://pscl.stanford.edu/.

  • Jégu, M. & G. M. dos Santos, 2001. Mise au point à propos de Serrasalmus spilopleura Kner, 1858 et réhabilitation de S. maculatus Kner, 1858 (Characidae: Serrasalminae). Cybium 25: 119–143.

    Google Scholar 

  • Jeschke, J. M., S. Bacher, T. M. Blackburn, J. T. A. Dick, F. Essl, T. Evans, M. Gaertner, P. E. Hulme, I. Kühn, A. Mrugała, J. Pergl, P. Pyšek, W. Rabitsch, A. Ricciardi, D. M. Richardson, A. Sendek, M. Vilà, M. Winter & S. Kumschick, 2014. Defining the impact of non-native species. Conservation Biology 28: 1188–1194.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Kleunen, M., W. Dawson, D. Schlaepfer, J. M. Jeschke & M. Fischer, 2010. Are invaders different? A conceptual framework of comparative approaches for assessing determinants of invasiveness. Ecology Letters 13: 947–958.

    PubMed  Google Scholar 

  • Kovalenko, K. E., E. D. Dibble, A. A. Agostinho & F. M. Pelicice, 2010. Recognition of non-native peacock bass, Cichla kelberi by native prey: testing the naiveté hypothesis. Biological Invasions 12: 3071–3080.

    Article  Google Scholar 

  • Li, S., T. Guo, M. W. Cadotte, Y. Chen, J. Kuang, Z. Hua, Y. Zeng, Y. Song, Z. Liu, W. Shu & J. Li, 2015a. Contrasting effects of phylogenetic relatedness on plant invader success in experimental grassland communities. Journal of Applied Ecology 52: 89–99.

    Article  CAS  Google Scholar 

  • Li, S., M. W. Cadotte, S. J. Meiners, Z. Hua, H. Shu, J. Li & W. Shu, 2015b. The effects of phylogenetic relatedness on invasion success and impact: deconstructing Darwin’s naturalization conundrum. Ecology Letters 18: 1285–1292.

    Article  PubMed  Google Scholar 

  • Lovell, S. J., S. F. Stone & L. Fernandez, 2006. The economic impacts of aquatic invasive species: a review of the literature. Agricultural and Resource Economics Review 35: 195–208.

    Article  Google Scholar 

  • Magellan, K. & E. García-Berthou, 2015. Influences of size and sex on invasive species aggression and native species vulnerability: a case for modern regression techniques. Reviews in Fish Biology and Fisheries 25: 537–549.

    Article  Google Scholar 

  • Martin, T. G., B. A. Wintle, J. R. Rhodes, P. M. Kuhnert, S. A. Field, S. J. Low-Choy, A. J. Tyre & H. J. Possingham, 2005. Zero tolerance ecology: improving ecological inference by modeling the source of zero observations. Ecology Letters 8: 1235–1246.

    Article  PubMed  Google Scholar 

  • McPeek, M. A. & R. Gomulkiewicz, 2005. Assembling and depleting species richness in metacommunities. In Holyoak, M., M. A. Leibold & R. D. Holt (eds), Metacommunities: Spatial Dynamics and Ecological Communities. The University of Chicago Press, Chicago: 355–373.

    Google Scholar 

  • Moyle, P. B. & T. Light, 1996. Biological invasions of freshwater: empirical rules and assembly theory. Biological Conservation 78: 149–161.

    Article  Google Scholar 

  • Okada, E. K., A. A. Agostinho & L. C. Gomes, 2005. Spatial and temporal gradients in artisanal fisheries of a large Neotropical reservoir, the Itaipu Reservoir, Brazil. Canadian Journal of Fisheries and Aquatic Sciences 62: 714–724.

    Article  Google Scholar 

  • Pereira, L. S., F. T. Mise, L. F. C. Tencatt, M. T. Baumgartner & A. A. Agostinho, 2017. Is coexistence between non-native and native Erythrinidae species mediated by niche differentiation or environmental filtering? A case study in the upper Paraná River floodplain. Neotropical Ichthyology 15: e160142.

    Google Scholar 

  • Procheş, S., J. R. U. Wilson, D. M. Richardson & M. Rejmánek, 2008. Searching for phylogenetic pattern in biological invasions. Global Ecology and Biogeography 17: 5–10.

    Google Scholar 

  • R Core Team, 2017. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.

  • Ricciardi, A. & M. Mottiar, 2006. Does Darwin’s naturalization hypothesis explain fish invasions? Biological Invasions 8: 1403–1407.

    Article  Google Scholar 

  • Roberto, M. C., B. F. Santana & S. M. Thomaz, 2009. Limnology in the Upper Paraná River floodplain: large-scale spatial and temporal patterns, and the influence of reservoirs. Brazilian Journal of Biology 69: 717–725.

    Article  CAS  Google Scholar 

  • Sazima, I. & F. A. Machado, 1990. Underwater observations of piranhas in western Brazil. Environmental Biology of Fishes 28: 17–31.

    Article  Google Scholar 

  • Simberloff, D., 2011. How common are invasion-induced ecosystem impacts? Biological Invasions 13: 1255–1268.

    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 Distributions 21: 583–594.

    Article  Google Scholar 

  • Souza Filho, E. E., R. C. Rocha, E. Comunello & J. C. Stevaux, 2004. Effects of the Porto Primavera Dam on physical environment of the downstream floodplain. In Thomaz, S. M., A. A. Agostinho & N. S. Hahn (eds), The Upper Paraná River and Its Floodplain: Physical Aspects, Ecology and Conservation. Backhuys Publishers, Leiden: 55–74.

    Google Scholar 

  • StatSoft, Inc., 2005. STATISTICA (data analysis software system). Version 7.1. www.statsoft.com.

  • Stone, L. & A. Roberts, 1990. The checkerboard score and species distributions. Oecologia 85: 74–79.

    Article  PubMed  Google Scholar 

  • Strayer, D. L., 2012. Eight questions about invasions and ecosystem functioning. Ecology Letters 15: 1199–1210.

    Article  PubMed  Google Scholar 

  • Strayer, D. L., V. T. Eviner, J. M. Jeschke & M. L. Pace, 2006. Understanding the long-term effects of species invasions. Trends in Ecology and Evolution 21: 645–651.

    Article  PubMed  Google Scholar 

  • Thomaz, S. M., L. M. Bini & R. L. Bozelli, 2007. Floods increase similarity among aquatic habitats in river-floodplain systems. Hydrobiologia 579: 1–13.

    Article  Google Scholar 

  • Thuiller, W., L. Gallien, I. Boulangeat, F. Bello, T. Münkemüller, C. Roquet & S. Lavergne, 2010. Resolving Darwin’s naturalization conundrum: a quest for evidence. Diversity and Distributions 16: 461–475.

    Article  Google Scholar 

  • Vazzoler, A. E. A. M., 1986. Manual de métodos para estudos biológicos de populações de peixes: reprodução e crescimento. Programa Nacional de Zoologia, Brasília.

    Google Scholar 

  • Villares Junior, G. A., L. M. Gomiero & R. Goitein, 2008. Alimentação de Serrasalmus maculatus (Kner, 1858) (Characiformes; Serrasalminae) no trecho inferior da bacia do rio Sorocaba, São Paulo, Brasil. Acta Scientiarum Biological Science 30: 267–273.

    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 

  • Wiens, J. J. & C. H. Graham, 2005. Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review of Ecology, Evolution and Systematics 36: 519–539.

    Article  Google Scholar 

  • Winemiller, K. O., P. B. McIntyre, L. Castello, E. Fluet-Chouinard, T. Giarrizzo, S. Nam, I. G. Baird, W. Darwall, N. K. Lujan, I. Harrison, M. L. J. Stiassny, R. A. M. Silvano, D. B. Fitzgerald, F. M. Pelicice, A. A. Agostinho, L. C. Gomes, J. S. Albert, E. Baran, M. Pretere Jr., C. Zarfl, M. Mulligan, J. P. Sullivan, C. C. Arantes, L. M. Sousa, A. A. Koning, D. J. Hoeinghaus, M. Sabaj, J. G. Lundberg, J. Armbruster, M. L. Thieme, P. Petry, J. Zuanon, G. Torrente Vilara, J. Snoeks, C. Ou, W. Rainboth, C. S. Pavanelli, A. Akama, A. van Soesbergen & L. Sáenz, 2016. Balancing hydropower and biodiversity in the Amazon, Congo and Mekong. Science 351: 128–129.

    Article  PubMed  CAS  Google Scholar 

  • Zeileis, A., C. Kleiber & S. Jackman, 2008. Regression models for count data in R. J Stat Softw 27. http://www.jstatsoft.org/v27/i08.

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Acknowledgements

The authors would like to thank the Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura (Nupélia) of the Universidade Estadual de Maringá (UEM) for providing the samplings and logistical support; projects Pesquisas Ecológicas de Longa Duração (PELD) and Programa de Apoio ao Desenvolvimento Científico e Tecnológico e Ciências Ambientais (PADCT/CIAMB) for delivering the data.The authors would also like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for having granted the scholarship to ACR, HSS, and MTB, as well as Hugo José Message and Daniel Alves dos Santos for remarkable improvements to the earliest version of this manuscript. The authors also thank S. M. Thomaz and the two anonymous reviewers for their helpful comments.

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Correspondence to Amanda Cantarute Rodrigues.

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

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Rodrigues, A.C., de Santana, H.S., Baumgartner, M.T. et al. Coexistence between native and nonnative species: the invasion process and adjustments in distribution through time for congeneric piranhas in a Neotropical floodplain. Hydrobiologia 817, 279–291 (2018). https://doi.org/10.1007/s10750-018-3541-z

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