Abundance of invasive peacock bass increases with water residence time of reservoirs in southeastern Brazil

Abstract

Neotropical freshwater ecosystems are experiencing a great expansion in the number of invasive species, which is especially alarming since this region harbours 30% of the world’s fish biodiversity with high levels of endemism. We aimed to evaluate the main predictors of peacock basses (Cichla spp.) abundance outside their native range, which are the Amazon and Tocantins-Araguaia river basins. We used multivariate ordination techniques and multimodel inference to analyse peacock basses abundance in twelve reservoirs of the Paraíba do Sul river basin, southeastern Brazil. Interestingly, reservoirs at higher (southernmost) latitudes, located in more populated areas, had higher water temperature and lower turbidity, due to increased water residence time, and these three variables were also positively correlated with abundance of this warm-water invasive fish. Habitat structure was less important in explaining peacock basses abundance, which was not significantly related to biotic factors (fish species richness and time since peacock basses introduction). We hypothesize that the observed effects of reservoir management on limnological features and peacock bass abundance, particularly water residence time (as a mediator of temperature and turbidity), may apply to other Neotropical basins and could influence the impact of this invader.

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References

  1. 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 Prognosis on Aging. In Tundisi, J. G. & M. Straškraba (eds), Theoretical Reservoir Ecology and its Applications. International Institute of Ecology, São Carlos: 227–265.

    Google Scholar 

  2. Agostinho, A. A., L. C. Gomes & F. M. Pelicice, 2007. Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. Eduem, Maringá.

    Google Scholar 

  3. Bailly, D., F. A. S. Cassemiro, K. O. Winemiller, J. A. F. Diniz-Filho & A. A. Agostinho, 2016. Diversity gradients of Neotropical freshwater fish: evidence of multiple underlying factors in human-modified systems. Journal of Biogeography 43: 1679–1689.

    Article  Google Scholar 

  4. Bartón, K., 2016. Package “MuMIn” version 1.15.6. https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf

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

    Article  PubMed  Google Scholar 

  6. Borcard, D., P. Legendre & P. Drapeau, 1992. Partialling out the spatial component of ecological variation. Ecology 73: 1045–1055.

    Article  Google Scholar 

  7. Borcard, D., F. Gillet & P. Legendre, 2011. Numerical Ecology with R. Springer, New York: 319.

    Google Scholar 

  8. Brook, B. W., N. S. Sodhi & C. J. A. Bradshaw, 2008. Synergies among extinction drivers under global change. Trends in Ecology and Evolution 23: 453–460.

    Article  PubMed  Google Scholar 

  9. Bulleri, F., J. F. Bruno & L. Benedetti-Cecchi, 2008. Beyond competition: incorporating positive interactions between species to predict ecosystem invasibility. PLoS Biology 6: e162.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Burnham, K. P. & D. R. Anderson, 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York.

    Google Scholar 

  11. Byers, J. E., 2002. Impact of non-indigenous species on natives enhanced by anthropogenic alteration of selection regimes. Oikos 97: 449–458.

    Article  Google Scholar 

  12. Carmona-Catot, G., A. F. G. N. Santos, P. A. Tedesco & E. García-Berthou, 2014. Quantifying seasonality along a latitudinal gradient: from stream temperature to growth of invasive mosquitofish. Ecosphere 5(10): 1–23.

    Article  Google Scholar 

  13. Carol, J., L. Benejam, J. Benito & E. García-Berthou, 2009. Growth and diet of European catfish (Silurus glanis) in early and late invasion stages. Fundamental and Applied Limnology 174: 317–328.

    Article  Google Scholar 

  14. Cavalcanti, B. S. & G. G. Marques, 2016. Recursos hídricos e gestão de conflitos: a bacia hidrográfica do rio Paraíba do Sul a partir da crise hídrica de 2014–2015. Revista Portuguesa e Brasileira de Gestão 15: 4–16.

    Google Scholar 

  15. CEIVAP, 2017. Comitê de Integração da Bacia Hidrográfica do Rio Paraíba do Sul. http://www.ceivap.org.br/index.php

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

    Article  Google Scholar 

  17. Colautti, R. I., I. A. Grigorovich & H. J. MacIsaac, 2006. Propagule pressure: a null model for biological invasions. Biological Invasions 8: 1023–1037.

    Article  Google Scholar 

  18. Cucherousset, J. & J. D. Olden, 2011. Ecological impacts of nonnative freshwater fishes. Fisheries 36: 215–230.

    Article  Google Scholar 

  19. Dray, S., P. Legendre, & G. Blanchet, 2016. Packfor: Forward Selection with permutation (Canoco p.46). R package version 0.0-8/r136. https://R-Forge.R-project.org/projects/sedar/

  20. Espínola, L. A., C. V. Minte-Vera & H. F. Júlio, 2010. Invasibility of reservoirs in the Paraná Basin, Brazil, to Cichla kelberi Kullander and Ferreira, 2006. Biological Invasions 12: 1873–1888.

    Article  Google Scholar 

  21. Espínola, L. A., C. V. Minte-Vera, H. F. Júnio-Junior, L. N. Santos & K. O. Winemiller, 2015. Evaluation of factors associated with dynamics of Cichla ocellaris invasion of the Upper Parana River floodplain system, Brazil. Marine and Freshwater Research 66: 33–40.

    Article  Google Scholar 

  22. Gido, K. B., W. J. Matthews & W. C. Wolfinbarger, 2000. Long-term changes in a reservoir fish assemblage: stability in an unpredictable environment. Ecological Applications 10: 1517–1529.

    Article  Google Scholar 

  23. Gomes, J. H. C., A. C. I. M. Dias & C. W. C. W. C. Branco, 2008. Fish assemblage composition in three reservoirs in the State of Rio de Janeiro. Acta Limnologica Brasiliensia 20: 117–130.

    Google Scholar 

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

    Article  Google Scholar 

  25. Hawkins, C. P., J. N. Hogue, L. M. Decker & J. W. Feminella, 1997. Channel morphology, water temperature, and assemblage structure of stream insects. Journal of the North American Benthological Society 16: 728–749.

    Article  Google Scholar 

  26. Hickley, P., M. Muchiri, R. Britton & R. Boar, 2008. Economic gain versus ecological damage from the introduction of non-native freshwater fish: case studies from Kenya. The Open Fish Science Journal 1: 36–46.

    Article  Google Scholar 

  27. Hoeinghaus, D. J., C. A. Layman, D. A. Arrington & K. O. Winemiller, 2003. Movement of Cichla species (Cichlidae) in a Venezuelan floodplain river. Neotropical Ichthyology 1: 121–126.

    Article  Google Scholar 

  28. Irz, P., A. Laurent, S. Messad, O. Pronier & C. Argillier, 2002. Influence of site characteristics on fish community patterns in French reservoirs. Ecology of Freshwater Fish 11: 123–136.

    Article  Google Scholar 

  29. Jackson, D. A., 1993. Stopping rules in principal component analysis: a comparison of heuristical and statistical approaches. Ecology 74: 2204–2214.

    Article  Google Scholar 

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

    Article  Google Scholar 

  31. Kennedy, R. H. & W. W. Walker, 1990. Reservoir Nutrient Dynamics. In Thornton, K. W., B. L. Kimmel & F. E. Payne (eds), Reservoir Limnology: Ecological Perspectives. Wiley-Interscience, New York: 109–132.

    Google Scholar 

  32. Kindt, R., 2017. Package “BiodiversityR” for community ecology and suitability analysis. R package version 2.8-0. https://cran.r-project.org/web/packages/BiodiversityR/BiodiversityR.pdf

  33. Kovalenko, K. E., E. D. Dibble, A. A. Agostinho, G. Cantanhêde & R. Fugi, 2010. Direct and indirect effects of an introduced piscivore, Cichla kelberi and their modification by aquatic plants. Hydrobiologia 638: 245–253.

    Article  Google Scholar 

  34. Kullander, S. O. & E. J. G. Ferreira, 2006. A review of South American cichlid genus Cichla, with descriptions of nine new species (Teleostei: Cichlidae). Ichthyological Exploration of Freshwaters 17: 289–398.

    Google Scholar 

  35. Latini, A. O. & M. Petrere, 2004. Reduction of a native fish fauna by alien species: an example from Brazilian freshwater tropical lakes. Fisheries Management and Ecology 11: 71–79.

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  38. Levine, J. M., P. B. Adler & S. G. Yelenik, 2004. A meta-analysis of biotic resistance to exotic plants invasions. Ecology Letters 7: 975–989.

    Article  Google Scholar 

  39. Liew, J. H., H. H. Tan & D. C. J. Yeo, 2016. Dammed rivers: impoundments facilitate fish invasions. Freshwater Biology 61: 1421–1429.

    Article  Google Scholar 

  40. Lowe-McConnell, R. H., 1969. The cichlid fishes of Guyana, South America, with notes on their ecology and breeding behavior. Zoological Journal of the Linnean Society 48: 255–302.

    Article  Google Scholar 

  41. Mack, R. N., D. Simberloff, W. Mark Lonsdale, H. Evans, M. Clout & F. A. Bazzaz, 2000. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710.

    Article  Google Scholar 

  42. Marengo, J.A. & L.M. Alves, 2005. Tendências Hidrológicas da Bacia do Rio Paraíba do Sul. INPE e-print. http://mtc-m16c.sid.inpe.br/col/sid.inpe.br/ePrint@80/2005/05.11.13.21/doc/v1.pdf

  43. Marques, A. C. P. B., A. C. S. Franco, F. Salgueiro, E. García-Berthou & L. N. Santos, 2016. Genetic divergence among invasive and native populations of the yellow peacock cichlid Cichla kelberi. Journal of Fish Biology 89: 2595–2606.

    Article  PubMed  CAS  Google Scholar 

  44. Oksanen, J., F.G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. McGlinn, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymos, M. Henry, H. Stevens, E. Szoecs & H. Wagner, 2016. vegan: Community ecology package. R package version 2.4-1. https://CRAN.R-project.org/package=vegan

  45. 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 

  46. Peña, E. A. & E. H. Slate, 2006. Global validation of linear model assumptions. Journal of the American Statistical Association 101: 341–354.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Pinto, B.C.T., 2008. Condicionantes ambientais estruturadoras das assembléias de peixes da bacia do rio Paraíba do Sul: condição do uso da terra, do habitat físico e qualidade físico-química da água. PhD. Thesis in Animal Biology, PPGBA, Universidade Federal Rural do Rio de Janeiro, Seropédica, 200 pp.

  48. Quist, M. C., F. J. Rahel & W. A. Hubert, 2005. Hierarchical faunal filters: an approach to assessing effects of habitat and nonnative species on native fishes. Ecology of Freshwater Fish 14: 24–39.

    Article  Google Scholar 

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

  50. Richardson, W. B. & L. A. Bartsch, 1997. Effects of zebra mussels on food webs: interactions with juvenile bluegill and water residence time. Hydrobiologia 354: 141–150.

    Article  Google Scholar 

  51. Rueda, F., E. Moreno-Ostos & J. Armengol, 2006. The residence time of river water in reservoirs. Ecological Modelling 191: 260–274.

    Article  CAS  Google Scholar 

  52. Santos, L. N., A. F. Gonzales & F. G. Araújo, 2001. Dieta do tucunaré-amarelo Cichla monoculus (Bloch & Schneider) (Osteichthyes, Cichlidae), no reservatório de Lajes, Rio de Janeiro, Brasil. Revista Brasileira de Zoologia 18: 191–204.

    Article  Google Scholar 

  53. Santos, L. N., E. García-Berthou, A. A. Agostinho & J. D. Latini, 2011. Fish colonization of artificial reefs in a large Neotropical reservoir: material type and successional changes. Ecological Applications 21: 251–262.

    Article  PubMed  Google Scholar 

  54. Santos, L. N., A. C. S. Franco, A. Marques, F. Nóbrega & F. Salgueiro, 2016a. Molecular analysis confirms the introduction of a second species of yellow peacock cichlid Cichla monoculus Spix & Agassiz 1831 (Cichliformes: Cichlidae) in the Southeast Atlantic Hydrographic province, Brazil. BioInvasions Records 5: 277–284.

    Article  Google Scholar 

  55. Santos, L. N., F. Salgueiro, A. C. S. Franco, A. C. P. Marques & F. Nóbrega, 2016b. First record of the invasive blue peacock cichlid Cichla piquiti Kullander and Ferreira 2006 (Cichliformes: Cichlidae) in the Paraíba do Sul river basin, south eastern Brazil. BioInvasions Records 5: 267–275.

    Article  Google Scholar 

  56. Shafland, P. L., 1996. Reviews in fisheries science exotic fishes of Florida—1994. Reviews in Fisheries Science 4: 101–122.

    Article  Google Scholar 

  57. Sharpe, D. M. T., L. F. De León, R. González & M. E. Torchin, 2017. Tropical fish community does not recover 45 years after predator introduction. Ecology 98: 412–424.

    Article  PubMed  CAS  Google Scholar 

  58. Soballe, D. M. & B. L. Kimmel, 1987. A large-scale comparison of factors influencing phytoplankton abundance in rivers, lakes, and impoundments. Ecology 68: 1943–1954.

    Article  PubMed  CAS  Google Scholar 

  59. Straškraba, M., 1999. Retention Time as a Key Variable of Reservoir Limnology. In Tundisi, J.G. & M. Straškraba (eds), Theoretical Reservoir Ecology and its Applications. São Carlos: International Institute of Ecology, Brazilian Academy of Sciences, Backhuys Publishers: 385–410.

  60. Straškraba, M., J. G. Tundisi, & A. Duncan, 1993. In Comparative Reservoir Limnology and Water Quality Management. Springer, Netherlands: 213–288.

  61. Thomaz, S. M., A. A. Agostinho, L. C. Gomes, M. J. Silveira, M. Rejmánek, C. E. Aslan & E. Chow, 2012. Using space-for-time substitution and time sequence approaches in invasion ecology. Freshwater Biology 57: 2401–2410.

    Article  Google Scholar 

  62. Willis, S. C., J. Macrander, I. P. Farias & G. Ortí, 2012. Simultaneous delimitation of species and quantification of interspecific hybridization in Amazonian peacock cichlids (genus Cichla) using multi-locus data. BMC Evolutionary Biology 12: 96.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Winemiller, K. O., 2001. Ecology of peacock cichlids (Cichla spp.) in Venezuela. Journal of Aquariculture and Aquatic Sciences 9: 93–112.

    Google Scholar 

  64. Winemiller, K. O., D. C. Taphorn & A. Barbarino-Duque, 1997. Ecology of Cichla (Cichlidae) in two blackwater rivers of southern Venezuela. Copeia 1997: 690–696.

    Article  Google Scholar 

  65. Yeo, D. C. J. & C. S. W. Chia, 2010. Introduced species in Singapore: an overview. Cosmos 6: 23–37.

    Article  Google Scholar 

  66. Zaret, T. M. & R. T. Paine, 1973. Species introduction in a tropical lake. Science 182: 449–455.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank the Graduate Courses in Ecology (PPGE-UFRJ) and Neotropical Biodiversity (PPGBIO-UNIRIO). We also thank people at Laboratório de Ictiologia Teórica e Aplicada for providing logistic support and two anonymous reviewers for helpful comments that greatly improved the manuscript. This work was funded by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (Research Grant to LNS, E-112.644/2012, E-26/202.840/2015), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Research Grant to LNS, ref. 312194/2015-3), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (sandwich doctorate scholarship to ACSF, ref. 88887.127440/2016-00 and visiting professorship to EGB, ref. 88881.068352/2014-01). EGB was also supported by the Spanish Ministry of Economy and Competitiveness (Projects and CGL2015-69311-REDT, CGL2016-80820-R and PCIN-2016-168) and the Government of Catalonia (ref. 2014 SGR 484).

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Correspondence to Ana Clara Sampaio Franco.

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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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Franco, A.C.S., dos Santos, L.N., Petry, A.C. et al. Abundance of invasive peacock bass increases with water residence time of reservoirs in southeastern Brazil. Hydrobiologia 817, 155–166 (2018). https://doi.org/10.1007/s10750-017-3467-x

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Keywords

  • Cichlidae
  • Cichla ocellaris
  • Invasive species
  • Neotropical reservoir
  • Paraíba do Sul river basin
  • Reservoir limnology