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Invasion dynamics of the white piranha (Serrasalmus brandtii) in a Neotropical river basin

  • Daniel Fonseca Teixeira
  • Francisco Ricardo Andrade Neto
  • Laís Carvalho Gomes
  • Luciano Bellagamba Beheregaray
  • Daniel Cardoso CarvalhoEmail author
Original Paper

Abstract

Clarifying the intricate history of unrecorded fish invasions represents an important step in understanding the invasion process. Here, we elucidate the invasion of a Neotropical river basin in Southeastern Brazil by a very efficient predator, the white piranha (Serrasalmus brandtii). We used a temporal series of population dynamics data (2008–2016) and analyses of mitochondrial DNA sequences (COI, 16S, and control region) of specimens from the entire native (São Francisco River Basin, Southeastern Brazil) and invaded (Jequitinhonha River Basin, JRB) ranges. We detected low genetic diversity (h = 0.5835) and strong genetic structure in the invasive range (Fst = 0.9141), despite high genetic diversity (h = 0.8900) and low genetic structure (Fst from 0.0740 to 0.1348) in the native range. High genetic structure in the invaded range was associated with a hydroelectric dam that prevented the admixture of two independent introductory acts into the JRB (downstream and upstream of the Irapé Dam). The rapid invasion capability of Serrasalmus brandtii, with few propagules, indicates that the species should be included in ecological risk assessments for restocking efforts of other commercially or ecologically important fish species and dam construction in Brazil. The combination of genetic and population dynamic datasets enabled the reconstruction of a top predator fish invasion in the Neotropics and shed light on ecological factors that influenced its invasion success.

Keywords

Biological invasion DNA Invasive success Reservoirs Dam Jequitinhonha River Basin 

Notes

Acknowledgements

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (482852/2011-9 and 133324/2013-3), Projeto Peixe Vivo—CEMIG, Instituto Nacional de Ciências e Tecnologias (INCT) (13324/3013-3), Coordenação de Aperfeiçoamento de Pessoa de Nível Superior (CAPES) Pró-Equipamentos (783380/2013), FIP—PUC Minas and CAPES for financial support. We thank Pamela Cássia Santiago de Sousa for assistance with the maps. Daniel Cardoso de Carvalho is grateful to CNPq for the productivity fellowship (CNPq 306155/2018-4).

Supplementary material

10530_2019_2138_MOESM1_ESM.docx (40 kb)
Supplementary material 1 (DOCX 40 kb)

References

  1. Agostinho A, Pelicice F, Gomes L (2009) Dams and the fish fauna of the Neotropical region: impacts and management related to diversity and fisheries. Braz J Biol 68:1119–1132.  https://doi.org/10.1590/s1519-69842008000500019 CrossRefGoogle Scholar
  2. Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693.  https://doi.org/10.1093/nar/25.22.4692 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alves GHZ, Figueiredo BRS, Manetta GI et al (2017) Trophic segregation underlies the coexistence of two piranha species after the removal of a geographic barrier. Hydrobiologia 797:57–68.  https://doi.org/10.1007/s10750-017-3159-6 CrossRefGoogle Scholar
  4. Andrade FR, Silva LD, Guedes I, et al (2018) Non-native white piranhas graze preferentially on caudal fins from large netted fishes. Mar Freshw Res 70:585–593.  https://doi.org/10.1071/MF18202 CrossRefGoogle Scholar
  5. Bajer PG, Beck MW, Cross TK et al (2016) Biological invasion by a benthivorous fish reduced the cover and species richness of aquatic plants in most lakes of a large North American ecoregion. Glob Change Biol 22:3937–3947.  https://doi.org/10.1111/gcb.13377 CrossRefGoogle Scholar
  6. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48.  https://doi.org/10.1093/oxfordjournals.molbev.a026036 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blackburn TM, Bellard C, Ricciardi A (2019) Alien versus native species as drivers of recent extinctions. Front Ecol Environ.  https://doi.org/10.1002/fee.2020 CrossRefGoogle Scholar
  8. Brauer CJ, Unmack PJ, Smith S et al (2018) On the roles of landscape heterogeneity and environmental variation in determining population genomic structure in a dendritic system. Mol Ecol.  https://doi.org/10.1111/mec.14808 CrossRefPubMedGoogle Scholar
  9. Carol J, Benejam L, Benito J, García-Berthou E (2009) Growth and diet of European catfish (Silurus glanis) in early and late invasion stages. Fundam Appl Limnol 174:317–328.  https://doi.org/10.1127/1863-9135/2009/0174-0317 CrossRefGoogle Scholar
  10. Carvalho DC, Oliveira DAA, Sampaio I, Beheregaray LB (2014) Analysis of propagule pressure and genetic diversity in the invasibility of a freshwater apex predator: the peacock bass (genus Cichla). Neotrop Ichthyol 12:105–116.  https://doi.org/10.1590/S1679-62252014000100011 CrossRefGoogle Scholar
  11. Colautti RI, Lau JA (2006) Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Mol Ecol 24:1999–2017.  https://doi.org/10.1111/mec.13162 CrossRefGoogle Scholar
  12. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinform 9:539.  https://doi.org/10.1186/1471-2105-9-539 CrossRefGoogle Scholar
  13. Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225.  https://doi.org/10.1111/mec.13117 CrossRefPubMedGoogle Scholar
  14. D’Antonio C, Meyerson LA, Denslow J (2001) Exotic species and conservation. In: Soulé ME, Orians GH (eds) Conservation biology: research priorities for the next decade. Island Press, Washington, DC, pp 59–80Google Scholar
  15. de Almeida FS, Sodré LMK, Contel EPB (2003) Population structure analysis of Pimelodus maculatus (Pisces, Siluriformes) from the Tietê and Paranapanema Rivers (Brazil). Genet Mol Biol 26:301–305.  https://doi.org/10.1590/S1415-47572003000300014 CrossRefGoogle Scholar
  16. Carvalho DC, de Oliveira DAA, dos Santos JE et al (2009) Genetic characterization of native and introduced populations of the neotropical cichlid genus Cichla in Brazil. Genet Mol Biol 32:601–607.  https://doi.org/10.1590/S1415-47572009005000060 CrossRefPubMedPubMedCentralGoogle Scholar
  17. de Trindade MEJ, Jucá-Chagas R (2008) Diet of two serrasalmin species, Pygocentrus piraya and Serrasalmus brandtii (Teleostei: Characidae), along a stretch of the rio de Contas, Bahia, Brazil. Neotrop Ichthyol 6:645–650CrossRefGoogle Scholar
  18. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449.  https://doi.org/10.1111/j.1365-294X.2007.03538.x CrossRefPubMedGoogle Scholar
  19. Estoup A, Ravigné V, Hufbauer R et al (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47:51–72.  https://doi.org/10.1146/annurev-ecolsys-121415-032116 CrossRefGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinforma 1:117693430500100.  https://doi.org/10.1177/117693430500100003 CrossRefGoogle Scholar
  21. Feiner ZS, Rice JA, Aday DD (2013) Trophic niche of invasive white perch and potential interactions with representative reservoir species. Trans Am Fish Soc 142:628–641.  https://doi.org/10.1080/00028487.2013.763854 CrossRefGoogle Scholar
  22. Frantine-Silva W, Ferreira DG, Nascimento RHC et al (2015) Genetic analysis of five sedentary fish species in middle Laranjinha River (upper Paraná River basin): a case study. Genet Mol Res 14:18637–18649.  https://doi.org/10.4238/2015.December.28.13 CrossRefPubMedGoogle Scholar
  23. Freeman B, Nico LEO, Osentoski M et al (2007) Molecular systematics of Serrasalmidae: deciphering the identities of piranha species and unraveling their evolutionary histories. Zootaxa 1484:1–38CrossRefGoogle Scholar
  24. Gallardo B, Clavero M, Sánchez MI, Vilà M (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163.  https://doi.org/10.1111/gcb.13004 CrossRefGoogle Scholar
  25. Haddad V, Sazima I (2010) Piranha attacks in dammed streams used for human recreation in the State of São Paulo, Brazil. Rev Soc Bras Med Trop 43:596–598CrossRefGoogle Scholar
  26. Hagenblad J, Hülskötter J, Acharya KP et al (2015) Low genetic diversity despite multiple introductions of the invasive plant species Impatiens glandulifera in Europe. BMC Genet 16:103.  https://doi.org/10.1186/s12863-015-0242-8 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hagenlund M, Østbye K, Langdal K et al (2015) Fauna crime: elucidating the potential source and introduction history of European smelt (Osmerus eperlanus L.) into Lake Storsjøen, Norway. Conserv Genet 16:1085–1098.  https://doi.org/10.1007/s10592-015-0724-2 CrossRefGoogle Scholar
  28. Havel JE, Lee CE, Vander Zanden MJ (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55:518–525.  https://doi.org/10.1641/0006-3568(2005)055%5b0518:drfiil%5d2.0.co;2 CrossRefGoogle Scholar
  29. Herbold B, Moyle PB (1986) Introduced species and vacant niches. Am Nat 128:751–760.  https://doi.org/10.1086/284600 CrossRefGoogle Scholar
  30. Holčík J (1991) Fish introductions in Europe with particular reference to its central and eastern part. Can J Fish Aquat Sci 48:13–23.  https://doi.org/10.1139/f91-300 CrossRefGoogle Scholar
  31. Honorato-Sampaio K, Santos GB, Bazzoli N, Rizzo E (2009) Observations on the seasonal breeding biology and fine structure of the egg surface in the white piranha Serrasalmus brandtii from the São Francisco River basin, Brazil. J Fish Biol 75:1874–1882.  https://doi.org/10.1111/j.1095-8649.2009.02422.x CrossRefPubMedGoogle Scholar
  32. Hubert N, Duponchelle F, Nuñez J et al (2007) Isolation by distance and Pleistocene expansion of the lowland populations of the white piranha Serrasalmus rhombeus. Mol Ecol 16:2488–2503.  https://doi.org/10.1111/j.1365-294X.2007.03338.x CrossRefPubMedGoogle Scholar
  33. Johnson PTJ, Olden JD, Vander Zanden MJ (2008) Dam invaders: impoundments facilitate biological invasions into freshwaters. Front Ecol Environ 6:357–363.  https://doi.org/10.1890/070156 CrossRefGoogle Scholar
  34. Kalinowski ST, Muhlfeld CC, Guy CS, Cox B (2010) Founding population size of an aquatic invasive species. Conserv Genet 11:2049–2053.  https://doi.org/10.1007/s10592-009-0041-8 CrossRefGoogle Scholar
  35. Khedkar GD, Jamdade R, Kalyankar A et al (2014) Genetic fragmentation in India’s third longest river system, the Narmada. Springerplus 3:1–12.  https://doi.org/10.1186/2193-1801-3-385 CrossRefGoogle Scholar
  36. Kinziger AP, Nakamoto RJ, Harvey BC (2014) Local-scale invasion pathways and small founder numbers in introduced Sacramento pikeminnow (Ptychocheilus grandis). Conserv Genet 15:1–9.  https://doi.org/10.1007/s10592-013-0516-5 CrossRefGoogle Scholar
  37. Korsu K, Heino J, Huusko A, Muotka T (2012) Specific niche characteristics facilitate the invasion of an alien fish invader in boreal streams. Int J Ecol.  https://doi.org/10.1155/2012/813016 CrossRefGoogle Scholar
  38. Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116.  https://doi.org/10.1111/2041-210X.12410 CrossRefGoogle Scholar
  39. Leuzzi MSP, de Almeida FS, Orsi ML, Sodré LMK (2004) Analysis by RAPD of the genetic structure of Astyanax altiparanae (Pisces, Characiformes) in reservoirs on the Paranapanema River, Brazil. Genet Mol Biol 27:355–362.  https://doi.org/10.1590/S1415-47572004000300009 CrossRefGoogle Scholar
  40. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.  https://doi.org/10.1093/bioinformatics/btp187 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mol JH (2006) Attacks on humans by the piranha Serrasalmus rhombeus in Suriname. Stud Neotrop Fauna Environ 41:189–195.  https://doi.org/10.1080/01650520600630683 CrossRefGoogle Scholar
  42. Oliveira AK, Alvim MC, Peret AC, Alves CBM (2004) Diet shifts related to body size of the pirambeba Serrasalmus brandtii Lütken, 1875 (Osteichthyes, Serrasalminae) in the Cajuru Reservoir, São Francisco River Basin, Brazil. Braz J Biol 64:117–124.  https://doi.org/10.1590/S1519-69842004000100013 CrossRefPubMedGoogle Scholar
  43. Oliveira AV, Prioli AJ, Prioli SMAP et al (2006) Genetic diversity of invasive and native Cichla (Pisces: Perciformes) populations in Brazil with evidence of interspecific hybridization. J Fish Biol 69:260–277.  https://doi.org/10.1111/j.1095-8649.2006.01291.x CrossRefGoogle Scholar
  44. Palumbi S, Martin A, Romano S et al (1991) The Simple Fool’s Guide do PCR, v. 2.0. University of Hawaii, HonoluluGoogle Scholar
  45. Pamponet VCC, Carneiro PLS, Affonso PRAM et al (2008) A multi-approach analysis of the genetic diversity in populations of Astyanax aff. bimaculatus Linnaeus, 1758 (Teleostei: Characidae) from Northeastern Brazil. Neotrop Ichthyol 6:621–630.  https://doi.org/10.1590/S1679-62252008000400010 CrossRefGoogle Scholar
  46. Pimentel D (2007) Environmental and economic costs of vertebrate species invasions into the United States. In: Witmer GW, Pitt WC, Fagerstone KA (eds) Manag Vertebr Invasive Species Proc an Int Symp USDA/APHIS/WS, Natl Wildl Res Center, Fort Collins, CO 1–8.  https://doi.org/10.1093/nar/gkq443 CrossRefGoogle Scholar
  47. Pompeu PS (1999) Dieta da pirambeba Serrasalmus brandtii Reinhardt (Teleostei, Characidae) em quatro lagoas marginais do rio São Francisco, Brasil. Revta Bras Zool 16:19–26.  https://doi.org/10.1590/S0101-81751999000600003 CrossRefGoogle Scholar
  48. Pringle RM, Kartzinel TR, Palmer TM et al (2019) Predator-induced collapse of niche structure and species coexistence. Nature 570:58–64.  https://doi.org/10.1038/s41586-019-1264-6 CrossRefPubMedGoogle Scholar
  49. Pugedo ML, de Andrade Neto FR, Pessali TC et al (2016) Integrative taxonomy supports new candidate fish species in a poorly studied neotropical region: the Jequitinhonha River Basin. Genetica 144:341–349.  https://doi.org/10.1007/s10709-016-9903-4 CrossRefPubMedGoogle Scholar
  50. R Development Core Team (2016) RStudio| Open source and enterprise-ready professional software for RGoogle Scholar
  51. Reid AJ, Carlson AK, Creed IF et al (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev 94:849–873.  https://doi.org/10.1111/brv.12480 CrossRefGoogle Scholar
  52. Sales NG, Pessali TC, Andrade Neto FR, Carvalho DC (2018) Introgression from non-native species unveils a hidden threat to the migratory Neotropical fish Prochilodus hartii. Biol Invasions 20:555–566.  https://doi.org/10.1007/s10530-017-1556-4 CrossRefGoogle Scholar
  53. Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Ecol Evol 17:170–176.  https://doi.org/10.1016/S0169-5347(02)02495-3 CrossRefGoogle Scholar
  54. Silva ARM, Santos GB, Ratton T (2006) Fish community structure of Juramento reservoir, São Francisco River basin, Minas Gerais, Brazil. Rev Bras Zool 23:832–840.  https://doi.org/10.1590/S0101-81752006000300031 CrossRefGoogle Scholar
  55. Sofia SH, Silva CRM, Galindo BA et al (2006) Population genetic structure of Astyanax scabripinnis (Teleostei, Characidae) from an urban stream. Hydrobiologia 553:245–254.  https://doi.org/10.1007/s10750-005-1106-4 CrossRefGoogle Scholar
  56. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Teske PR, Golla TR, Sandoval-Castillo J, Emami-Khoyi A, van der Lingen C, von der Heyden S, Chiazzari B, van Vuuren BJ, Beheregaray LB (2018) Mitochondrial DNA is unsuitable to test for isolation by distance. Sci Rep 8:8448.  https://doi.org/10.1038/s41598-018-25138-9 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  59. Tsutsui ND, Suarez AV, Holway DA, Case TJ (2000) Reduced genetic variation and the success of an invasive species. Proc Natl Acad Sci 97:5948–5953.  https://doi.org/10.1073/pnas.100110397 CrossRefPubMedGoogle Scholar
  60. Walsh JR, Carpenter SR, Vander Zanden MJ (2016) Invasive species triggers a massive loss of ecosystem services through a trophic cascade. Proc Natl Acad Sci 113:4081–4085.  https://doi.org/10.1073/pnas.1600366113 CrossRefPubMedGoogle Scholar
  61. Ward RD, Zemlak TS, Innes BH et al (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857.  https://doi.org/10.1098/rstb.2005.1716 CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Programa de Pós-graduação em Zoologia de Vertebrados, Laboratório de Genética da ConservaçãoPontifícia Universidade Católica de Minas GeraisBelo HorizonteBrazil
  2. 2.Companhia Energética do Estado de Minas Gerais (CEMIG) – Programa Peixe VivoBelo HorizonteBrazil
  3. 3.Programa de pós-graduação em GenéticaUniversidade Federal de Minas GeraisBelo HorizonteBrazil
  4. 4.Molecular Ecology LaboratoryFlinders UniversityAdelaideAustralia

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