Skip to main content

Advertisement

Log in

Importance of feeding strategies on the long-term success of fish invasions

  • INVASIVE SPECIES II
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

This study assessed the feeding strategies of nine fish species in their native (Cuiabá River) and in an invaded basin (upper Paraná River) to identify trophic variables that may explain the success of these species in the new basin, over 30 years. The following predictions were analyzed: (i) species that display omnivorous or piscivorous diets in the native basin are favored in the invasion process over the long term, and (ii) specialist feeders are favored in the invasion process provided that their food items are highly available in the invaded area. These predictions were supported by the data; the species that were successful invaders had high trophic plasticity (omnivores), consumed a wide variety of food items from specific trophic guilds (piscivores), or if a species had a specialized diet, the resources demanded are abundant (detritivores). Thus, in a long-term perspective, the food resources used by these species are rarely limiting in aquatic ecosystems, and these feeding characteristics should be one of the key factors determining the colonization success of fishes. Understanding the factors that determine the success of invasive species in new areas is critical for developing management policies aimed at minimizing the impacts of biological invasions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agostinho, C. S. & H. F. Júlio-Júnior, 2000. Observation of an invasion of the piranha Serrasalmus marginatus Velenciennes, 1947 (Osteichthyes, Serrasalmidae) into the Upper Parana River, Brazil. Acta Scientiarum 24: 391–395.

    Google Scholar 

  • Agostinho, A. A., L. E. Miranda, L. M. Bini, L. C. Gomes, S. M. Thomaz & H. I. Suzuki, 1999. Patterns of colonization in Neotropical reservoirs, and prognoses on aging. In Tundisi, J. G. & M. Straskraba (eds), Theoretical Reservoir Ecology and Its Applications. International Institute of Ecology, São Carlos: 227–265.

    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 Archives Biology Technology 63: 177–182.

    Article  CAS  Google Scholar 

  • Agostinho, A. A., L. C. Gomes, H. I. Suzuki & H. F. Júlio-Júnior, 2003b. Migratory fishes of the upper Paraná River basin Brazil. In Carolsfeld, J., B. Harvey, C. Ross & A. Baer (eds), Migratory Fishes of South America: Biology, Fisheries and Conservation Status. World Bank, Vitória: 19–89.

    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 

  • Anderson, M. & N. G. Ray, 2008. Permanova+ for Primer: Guide to Software and Statistical Methods. PRIMER-E Ltd., Plymouth.

    Google Scholar 

  • Azevedo-Santos, V. M. A., P. M. Fearnside, C. S. Oliveira, L. B. Magalhães, M. L. Orsi, A. A. Agostinho, F. A. Esteves, P. S. Pompeu, W. F. Laurance, M. Petrere-Jr, R. P. Mormul & J. R. S. Vitule, 2017. Removing the abyss between conservation science and policy decisions in Brazil. Biodiversity and Conservation 26: 1745–1752.

    Article  Google Scholar 

  • Barili, E., R. Fugi, G. C. Novakowski & A. A. Agostinho, 2012. Impoundment effects in the population of Auchenipterus osteomystax (Siluriformes: Auchenipteridae): a neotropical reservoir case. Revista de Biologia Tropical 60: 699–708.

    PubMed  Google Scholar 

  • Bartley, D. M. & R. P. Subasinghe, 1996. Historical aspects of international movement of living aquatic species. Revue Scientifique et Technique 15: 387–400.

    Article  PubMed  CAS  Google Scholar 

  • Blossey, B., 1993. Herbivory below ground and biological weed control: life history of a root-boring weevil on purple loosestrife. Oecologia 94: 380–387.

    Article  PubMed  Google Scholar 

  • Bohn, T., O. T. Sandlund, P. A. Amundsen & R. Primicerio, 2004. Rapidly changing life history during invasion. Oikos 106: 138–150.

    Article  Google Scholar 

  • Bonecker, C. C., F. A. Lansac-Tôha, L. F. M. Velho & D. C. Rossa, 2001. The temporal distribution pattern of copepods in Corumbá Reservoir, State of Goiás, Brazil. Hydrobiologia 453: 375–384.

    Article  Google Scholar 

  • Bowen, S. H., 1983. Detritivory in Neotropical fish communities. Environmental Biology of Fishes 9: 137–144.

    Article  Google Scholar 

  • Brown, L. R., 2000. Fish communities and their associations with environmental variables, lower San Joaquin River drainage, California. Environmental Biology of Fishes 57: 251–269.

    Article  Google Scholar 

  • Carpenter, S. R., B. J. Benson, R. Biggs, J. W. Chipman, J. A. Foley, S. A. Golding, R. B. Hammer, P. C. Hanson, P. T. J. Johnson, A. M. Kamarainen, T. K. Kratz, R. C. Lathrop, K. D. McMahon, B. Provencher, J. A. Rusak, C. T. Solomon, E. H. Stanley, M. G. Turner, M. J. Vander Zanden, C. H. Wu & H. Yuan, 2007. Understanding regional change: a comparison of two lake districts. Bioscience 57: 323–335.

    Article  Google Scholar 

  • Casimiro, A. C. R., D. A. Z. Garcia, A. D. A. Costa, J. R. Britton & M. L. Orsi, 2017. Impoundments facilitate a biological invasion: dispersal and establishment of non-native armoured catfish Loricariichthys platymetopon (Isbrückler & Nijssen, 1979) in a Neotropical river. Limnologica 62: 34–37.

    Article  Google Scholar 

  • Colautti, R. I. & H. J. MacIsaac, 2004. A neutral terminology to define ‘invasive’ species. Diversity and Distributions 10: 135–141.

    Article  Google Scholar 

  • Côté, I. M., S. J. Green & M. A. Hixon, 2013. Predatory fish invaders: insights from Indo-Pacific lionfish in the western Atlantic and Caribbean. Biological Conservation 164: 50–61.

    Article  Google Scholar 

  • Drolet, D. & A. Locke, 2016. Relative importance of propagule size and propagule number for establishment of non-indigenous species: a stochastic simulation study. Aquatic Invasions 11: 101–110.

    Article  Google Scholar 

  • Ferreira, F. S. & W. Vicentin, 2014. Trophic ecology of two piranha species, Pygocentrus nattereri and Serrasalmus marginatus (Characiformes, Characidae), in the floodplain of the Negro River, Pantanal. Acta Limnologica Brasiliensia 26: 381–391.

    Article  Google Scholar 

  • Fugi, R., N. S. Hahn & A. A. Agostinho, 1996. Feeding styles of five species of bottom-feeding fishes of the high Paraná River. Environmental Biology of Fishes 46: 297–307.

    Article  Google Scholar 

  • Garcia-Berthou, E., 2007. The characteristics of invasive fishes: what has been learned so far? Journal of Fish Biology 71: 33–55.

    Article  Google Scholar 

  • Gerking, S. D., 1994. Feeding ecology of fish. Academic Press, San Diego.

    Google Scholar 

  • Gido, K. B. & N. R. Franssen, 2007. Invasion of stream fishes into low trophic positions. Ecology Freshwater Fish 16: 457–464.

    Article  Google Scholar 

  • Gozlan, R. E., 2009. Biodiversity crisis and the introduction of non-native fish: solutions, not scapegoats. Fish and Fisheries 10: 109–110.

    Article  Google Scholar 

  • Grabowska, J. & M. Przybylski, 2014. Life-history traits of non-native freshwater fish invaders differentiate them from natives in the Central European bioregion. Reviews in Fish Biology Fisheries 25: 165–178.

    Article  Google Scholar 

  • Hahn, N. S. & R. Fugi, 2008. Environmental changes, habitat modifications and feeding ecology of freshwater fish. In Cyrino, J. E. P., D. P. Bureau & B. G. Kapoor (eds), Feeding and Digestive Functions of Fishes. Science Publishers, Enfield: 35–65.

    Chapter  Google Scholar 

  • Hahn, N. S., R. Fugi & I. F. Andrian, 2004. Trophic ecology of the fish assemblage. In Thomaz, S. M., A. A. Agostinho & N. S. Hahn (eds), The upper Paraná River and its floodplain. Backhuys Publishers, Leinde: 247–269.

    Google Scholar 

  • Hyslop, E. J., 1980. Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17: 411–429.

    Article  Google Scholar 

  • Johnson, P. T. J., J. D. Olden & M. J. V. Zanden, 2008. Dam invaders: impoundments facilitate biological invasions into freshwaters. Frontiers in Ecology and the Environment 6: 357–363.

    Article  Google Scholar 

  • Júlio-Júnior, 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 

  • Koehn, J. D., 2004. Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshwater Biology 49: 881–894.

    Article  Google Scholar 

  • Krebs, C. J., 1999. Ecology Methodology. Benjamin Cummings/Addison Wesley Educational Publishers, Menlo Park.

    Google Scholar 

  • Levine, J. M., C. M. D. Antonio, J. S. Dukes, K. Grigulis & S. Lavorel, 2003. Mechanisms underlying the impacts of exotic plant invasions. Proceedings of the Royal Society London 270: 775–781.

    Article  Google Scholar 

  • Lodge, D. M., 1993. Biological invasions: lessons of ecology. Trends in Ecology and Evolution 4: 133–137.

    Article  Google Scholar 

  • Luz-Agostinho, D. G., A. A. Agostinho, L. C. Gomes & H. F. Júlio-Júnior, 2008. Influence of flood pulses on diet composition and trophic relationships among piscivorous fish in the upper Parana River floodplain. Hydrobiologia 607: 187–198.

    Article  Google Scholar 

  • Makrakis, S., L. C. Gomes, M. C. Makrakis, D. R. Fernandez & C. S. Pavanelli, 2007. The Canal da Piracema at Itaipu Dam as a fish pass system. Neotropical Ichthyology 5: 185–195.

    Article  Google Scholar 

  • Marchetti, M. P., T. Light, P. B. Moyle & J. H. Viers, 2004. Fish invasions in California watersheds: testing hypotheses using landscape patterns. Ecological Applications 14: 1507–1525.

    Article  Google Scholar 

  • Moyle, P. B. & T. Light, 1996a. Fish invasions in California: do abiotic factors determine success? Ecology 77: 1666–1670.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Moyle P. B. & S. Ellsworth, 2004. Alien invaders. In Moyle P. & D. Kelt (eds), Essays on Wildlife Conservation. http://marinebio.org/Oceans/Conservation/Moyle.

  • Nurkse, K., J. Kotta, H. Orav-Kotta & H. Ojaveer, 2016. A successful non-native predator, round goby, in the Baltic Sea: generalist feeding strategy, diverse diet and high prey consumption. Hydrobiologia 777: 271–281.

    Article  CAS  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 Science 62: 714–724.

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Olden, J. D., M. J. Kennard, F. Leprieur, P. A. Tedesco, K. O. Winemiller & E. Garcia-Berthou, 2010. Conservation biogeography of freshwater fishes: recent progress and future challenges. Diversity and Distributions 16: 496–513.

    Article  Google Scholar 

  • Oporto, L. T., 2008. Modificações em longo prazo na ictiofauna da planície de inundação do alto rio Paraná, Brasil, Dissertation, Departamento de Biologia, Universidade Estadual de Maringá.

  • Ortega, J. C. G., H. F. Júlio-Junior, L. C. Gomes & A. A. Agostinho, 2015. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746: 147–158.

    Article  Google Scholar 

  • Pander, I., M. Mueller, M. Sacher & G. Juergen, 2016. The role of life history traits and habitat characteristics in the colonisation of a secondary floodplain by neobiota and indigenous macroinvertebrates species. Hydrobiologia 772: 229–245.

    Article  Google Scholar 

  • Pelicice, F. M. & A. A. Agostinho, 2009. Fish fauna destruction after the introduction of a non-native predator (Cichla kelberi) in a Neotropical reservoir. Biological Invasions 11: 1789–1801.

    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 nonnative fish by decree. Conservation Letters 7: 55–60.

    Article  Google Scholar 

  • Pereira, L. S., A. A. Agostinho & R. L. Delariva, 2016. Effects of river damming in Neotropical piscivorous and omnivorous fish: feeding, body condition and abundances. Neotropical Ichthyology 14: 267–278.

    Google Scholar 

  • Rahel, F. J., 2000. Homogenization of fish faunas across the United States. Science 288: 854–856.

    Article  PubMed  CAS  Google Scholar 

  • Rahel, F. J., 2007. Biogeographic barriers, connectivity and homogenization of freshwater faunas: it’s a small world after all. Freshwater Biology 52: 696–710.

    Article  Google Scholar 

  • Rejmánek, M., 1999. Invasive plants and invasible ecosystems. In Sandlund, T. O., P. J. Schei & A. Vilken (eds), Invasive Species and Biodiversity Management. Kluwer, Dordrecht: 400–431.

    Google Scholar 

  • Rocha, O., T. Matsumura-Tundisi, E. L. G. Espíndola, K. F. Roche & A. C. Rietzler, 1999. Ecological theory applied to reservoir zooplankton. In Tundisi, J. G. & M. S. Straskraba (eds), Theoretical Reservoir Ecology and its Applications. International Institute of Ecology (IIE), São Carlos: 457–476.

    Google Scholar 

  • Rodriguez, J. P., 2001. Exotic species introductions into South America: an underestimated threat? Biodiversity and Conservation 10: 1983–1996.

    Article  Google Scholar 

  • Ruesink, J. L., 2005. Global analysis of factors affecting the outcome of freshwater fish introductions. Conservation Biology 19: 1883–1893.

    Article  Google Scholar 

  • Sazima, I. & J. P. Pombal-Jr, 1988. Mutilação de nadadeiras em acarás, Geophagus brasiliensis, por piranhas, Serrasalmus spilopleura. Revista Brasileira de Biologia 48: 477–483.

    Google Scholar 

  • Simberloff, D., 2009. The role of propagule pressure in biological invasions. Annual Review of Ecology, Evolution, and Systematics 40: 81–102.

    Article  Google Scholar 

  • Simberloff, D. & M. Rejmánek, 2011. Encyclopedia of biological invasions. University of California Press, Berkeley.

    Google Scholar 

  • Souto, A. C., A. P. Vidotto-Magnoni, H. Brandão & E. D. Carvalho, 2011. Actinopterygii, Siluriformes, Loricariidae, Loricariichthys platymetopon Isbrücker and Nijssen, 1979: first record in Reservoir of Canoas II, middle Paranapanema River, border of the states of São Paulo and Paraná, Brazil. Check List 7: 279–281.

    Article  Google Scholar 

  • Takeda, A. M. & M. Grzybkowska, 1997. Seasonal dynamics and production of Campsurus violaceus nymphs (Ephemeroptera, Polymitarcyidae) in the Baia river, upper Paraná River floodplain, Brazil. Hydrobiologia 356: 149–155.

    Article  Google Scholar 

  • 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, 2011. 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. A. Agostinho & V. M. Azevedo-Santos, 2017. We need better understanding about functional diversity and vulnerability of tropical freshwater fishes. Biodiversity and Conservation 26: 757–762.

    Article  Google Scholar 

  • Welcomme, R. L., 1988. International introductions of inland aquatic species. FAO Fisheries Technical Paper, Roma.

  • Wilson, J. R. U., 1992. The diversity of life. W.W. Norton, New York and London.

    Google Scholar 

  • Wilson, J. R. U., E. E. Dormontt, P. J. Prentis, A. J. Lowe & D. M. Richardson, 2009. Something in the way you move: dispersal pathways affect invasion success. Trends in Ecology and Evolution 24: 136–144.

    Article  PubMed  Google Scholar 

  • Winemiller, K. O., 1989. Ontogenetic diet shifts and resource partitioning among piscivorous fishes in the Venezuelan llanos. Environmental Biology Fishes 26: 177–199.

    Article  Google Scholar 

  • Winemiller, K. O. & L. C. Kelso-Winemiller, 2003. Food habits of tilapiine cichlids of the Upper Zambezi River and floodplain during the descending phase of the hydrologic cycle. Journal of Fish Biology 63: 120–128.

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Nupélia/UEM, Itaipu Binacional, the Graduate Program in Ecology of Continental Aquatic Environments (Programa de Pós-Graduação em Ecologia de Ambientes Aquáticos Continentais—PEA), and CNPq/PELD for financial support and infrastructure to develop the study; the Nupélia statistical fisheries team, led by Edson K. Okada; Jayme L. L. Pereira for drawing the figures; and CAPES for the scholarship granted to Lívia Helena Tonella and Oscar Barrosos Vitorino Junior. Angelo A. Agostinho is a researcher in Scientific Productivity at the CNPq and acknowledges this agency for long-term provision of funds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lívia Helena Tonella.

Additional information

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tonella, L.H., Fugi, R., Vitorino, O.B. et al. Importance of feeding strategies on the long-term success of fish invasions. Hydrobiologia 817, 239–252 (2018). https://doi.org/10.1007/s10750-017-3404-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-017-3404-z

Keywords

Navigation