Skip to main content

Advertisement

Log in

Elucidating a history of invasion: population genetics of pirarucu (Arapaima gigas, Actinopterygii, Arapaimidae) in the Madeira River

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The spread of non-native fish species is increasing globally and threatening aquatic ecosystems. Identifying the origins, the pathways, and vectors is crucial for managing biological invasions. We conducted a genetic characterization of Arapaima gigas from the Madeira River, considering native and non-native populations, to elucidate the invasion of the upper and middle Madeira River basin by A. gigas. We analyzed 9 microsatellite loci of 141 individuals from native (lower Madeira) and invasive (upper Madeira) populations, in addition to a locality from Peru outside the Madeira River basin drainage area, that previously was suggested to be one of the possible origins of the invasion. The results of discriminant analysis of principal components, Bayesian modeling of population structure, clustering and assignment tests (using microsatellite data from other Amazon locations) showed a clear separation between native and invasive populations and revealed a mixture of individuals from upper and middle Madeira and Peru. We confirm that the invasive population originates from Peru and was introduced by fish escapees from farms. Multiple secondary introductions may have advanced the invasion speed. Such a scenario represents a conservation paradox, because in its native habitat, A. gigas is endangered, whereas it has become invasive in non-native areas.

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

Similar content being viewed by others

Data availability

The datasets generated during and analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

References

  • Allendorf, F. W. & L. L. Lundquist, 2003. Introduction: population biology, evolution, and control of invasive species. Conservation Biology 17: 24–30.

    Article  Google Scholar 

  • Araripe, J., P. S. D. Rêgo, H. Queiroz, I. Sampaio & H. Schneider, 2013. Dispersal capacity and genetic structure of Arapaima gigas on different geographic scales using microsatellite markers. PloS One 8: e54470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Attayde, J. L., N. Okun, J. Brasil, R. Menezes & Mesquita, 2007. Os impactos da introdução da tilápia do Nilo, Oreochromis niloticus, sobre a estrutura trófica dos ecossistemas aquáticos do Bioma Caatinga. Oecologia Brasiliensis 11: 450–461.

    Article  Google Scholar 

  • Balloux, F. & N. Lugon-Moulin, 2002. The estimation of population differentiation with microsatellite markers. Molecular Ecology 11: 155–165.

    Article  PubMed  Google Scholar 

  • Barker, B. S., K. Andonian, S. M. Swope, D. G. Luster & K. M. Dlugosch, 2017. Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis). Molecular Ecology 26: 1131–1147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bezerra, L. A. V., R. Angelini, J. R. S. Vitule, M. Coll & J. I. Sánchez-Botero, 2018. Food web changes associated with drought and invasive species in a tropical semiarid reservoir. Hydrobiologia 817: 475–489.

    Article  Google Scholar 

  • Blackburn, T. M., P. Cassey & J. L. Lockwood, 2009. The role of species traits in the establishment success of exotic birds. Global Change Biology 15: 2852–2860.

    Article  Google Scholar 

  • Blackburn, T. M., P. Pyšek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarošík, 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 

  • Britton, J. R., G. D. Davies & M. Brazier, 2009. Eradication of the invasive Pseudorasbora parva results in increased growth and production of native fishes. Ecology of Freshwater Fish 18: 8–14.

    Article  Google Scholar 

  • Britton, J. R. & M. L. Orsi, 2012. Non-native fish in aquaculture and sport fishing in Brazil: economic benefits versus risks to fish diversity in the upper River Paraná Basin. Reviews in Fish Biology and Fisheries 22: 555–565.

    Article  Google Scholar 

  • Broennimann, O., U. A. Treier, H. Müller-Schärer, W. Thuiller, A. T. Peterson & A. Guisan, 2007. Evidence of climatic niche shift during biological invasion. Ecology Letters 10: 701–709.

    Article  CAS  PubMed  Google Scholar 

  • Callaway, R. M. & J. L. Maron, 2006. What have exotic plant invasions taught us over the past 20 years? Trends in Ecology and Evolution 21: 369–374.

    Article  PubMed  Google Scholar 

  • Carrete, M., P. Edelaar, J. Blas, D. Serrano, J. Potti, N. J. Dingemanse & J. L. Tella, 2012. Don’t neglect pre-establishment individual selection in deliberate introductions. Trends in Ecology & Evolution 27: 67–68.

    Article  Google Scholar 

  • Carvajal-Vallejos, F. M., P. A. Van Damme, L. Cordova & C. Coca, 2011. La introducción de Arapaima gigas (paiche) en la Amazonía boliviana. In Van Damme, P., F. Carvajal-Vallejos & C. J. Molina (eds), Peces y Delfines de la Amazonía boliviana: Hábitats, potencialidades y amenazas Cochabamba, Editorial INIA: 367–396.

    Google Scholar 

  • Carvajal-Vallejos, F. M., S. V. Montellano, D. Lizarro, S. Villafán, A. J. Zeballos & P. A. Van Damme, 2017. La introducción del paiche (Arapaima gigas) en la Cuenca Amazónica boliviana y síntesis del conocimiento. In Van-Damme, P. A., et al., (eds), Bases técnicas para el manejo y aprovechamiento del paiche (Arapaima gigas) en la cuenca amazónica boliviana Cochabamba: 21.

    Google Scholar 

  • Carvalho, F. R., L. Casatti, A. R. Manzotti & D. C. Ravazzi, 2015. First record of Arapaima gigas (Schinz, 1822)(Teleostei: Osteoglossomorpha), the “pirarucu”, in the upper Paraná River basin, Southeast Brazil. Check List 11: 1–4.

    CAS  Google Scholar 

  • Casal, C. M. V., 2006. Global documentation of fish introductions: the growing crisis and recommendations for action. Biological Invasions 8: 3–11.

    Article  Google Scholar 

  • Casimiro, A. C. R., D. A. Z. Garcia, A. P. Vidotto-Magnoni, J. R. Britton, Â. A. Agostinho, F. S. D. Almeida & M. L. Orsi, 2018. Escapes of non-native fish from flooded aquaculture facilities: The case of Paranapanema River, southern Brazil. Zoologia (Curitiba). https://doi.org/10.3897/zoologia.35.e14638.

    Article  Google Scholar 

  • Castello, L. & D. J. Stewart, 2010. Assessing CITES non-detriment findings procedures for Arapaima in Brazil. Journal of Applied Ichthyology 26: 49–56.

    Article  Google Scholar 

  • Castello, L., D. G. McGrath, L. L. Hess, M. T. Coe, P. A. Lefebvre, P. Petry, M. N. Macedo, V. F. Renó & C. C. Arantes, 2013. The vulnerability of Amazon freshwater ecosystems. Conservation Letters 6: 217–229.

    Article  Google Scholar 

  • Catâneo, D. T. B. S. (2019). A invasão do pirarucu Arapaima gigas Schinz, 1822 na bacia do rio Madeira: histórico de introdução, determinação genética e manejo. MSc Thesis, Federal University of Rondônia. http://ri.unir.br/jspui/handle/123456789/2989.

  • Chapple, D. G., S. M. Simmonds & B. B. Wong, 2012a. Can behavioral and personality traits influence the success of unintentional species introductions? Trends in Ecology & Evolution 27: 57–64.

    Article  Google Scholar 

  • Chapple, D. G., K. A. Miller, F. Kraus & M. B. Thompson, 2012b. Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Diversity and Distributions 19: 134–146.

    Article  Google Scholar 

  • CBD- Convenção sobre Diversidade Biológica (1992). Ministério do Meio Ambiente. https://cites.org/eng/app/appendices.php. Accessed June 28, 2021.

  • CITES- Convention on International Trade in Endangered Species of Wild Fauna and Flora (1975). Appendices. https://cites.org/eng/app/appendices.php. Accessed June 28, 2021.

  • Coca Méndez, C., G. Rico López, F. M. Carvajal-Vallejos, R. Salas Peredo, J. M. Wojchiechowski & P. Van Damme (2012). Cadena de valor del pescado en el norte amazónico de Bolivia: contribución de especies nativas y de una especie introducida (el paiche-Arapaima gigas). Investigación ambiental/Fundación PIEB. http://hdl.handle.net/10625/53643.

  • Colautti, R. I., M. Manca, M. Viljanen, H. A. Ketelaars, H. Buergi, H. J. Macisaac & D. D. Heath, 2005. Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Molecular Ecology 14: 1869–1879.

    Article  CAS  PubMed  Google Scholar 

  • Connelly, N. A., T. B. Lauber, R. C. Stedman & B. A. Knuth, 2016. The role of anglers in preventing the spread of aquatic invasive species in the Great Lakes region. Journal of Great Lakes Research 42: 703–707.

    Article  Google Scholar 

  • Crawford, K. M. & K. D. Whitney, 2010. Population genetic diversity influences colonization success. Molecular Ecology 19: 1253–1263.

    Article  CAS  PubMed  Google Scholar 

  • DeWoody, J. A., J. Schupp, L. Kenefic, J. Busch, L. Murfitt & P. Keim, 2004. Universal method for producing ROX-labeled size standards suitable for automated genotyping. Biotechniques 37: 348–352.

    Article  CAS  PubMed  Google Scholar 

  • Dlugosch, K. M. & I. M. Parker, 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17: 431–449.

    Article  CAS  PubMed  Google Scholar 

  • Dietz, H. & P. J. Edwards, 2006. Recognition that causal processes change during plant invasion helps explain conflicts in evidence. Ecology 87: 1359–1367.

    Article  PubMed  Google Scholar 

  • Doria, C. R. C. & S. T. Brasil De Souza, 2012. A pesca nas bacias dos ríos Guaporé e baixo Mamoré, Amazônia brasileira. In Van Damme, P. A., M. Maldonado, M. Pouilly & C. R. C. Doria (eds), Águas del Iténez o Guaporé: recursos hidrobiológicos de un patrimonio binacional (Bolivia y Brasil) Edit, INIA, Cochabamba, Bolivia: 420.

    Google Scholar 

  • Doria, C. R. C., D. T. B. S. Catâneo, G. Torrente-Vilara & J. R. S. Vitule, 2020. Is there a future for artisanal fishing in the Amazon? The case of Arapaima gigas. Management of Biological Invasions 11: 1–8.

    Article  Google Scholar 

  • Doria, C. R. D. C., E. Agudelo, A. Akama, B. Barros, M. Bonfim, L. Carneiro, S. Romério Briglia-Ferreira, L. N. Carvalho, C. A. Bonilla-Castillo, D. T. B. S. Patricia Charvet, H. P. Catâneo, C. R. Silva, H. D. Garcia-Dávila, F. Beltrão dos Anjos, A. Duponchelle, I. Encalada, A. C. Fernandes, P. C. P. Florentino, T. L. O. Guarido, L. Guedes, O. M. Jimenez-Segura, M. R. Lasso-Alcalá, E. E. Macean, R. N. G. Marques, G. Mendes-Júnior, J. L. S. Miranda-Chumacero, T. V. T. Nunes, L. S. Occhi, W. Pereira, L. Castro-Pulido, R. Soares, G. Garcez, P. A. Van Torrente-Vilara, J. Zuanon. Damme & J. R. S. Vitule, 2021. The silent threat of non-native fish in the Amazon: ANNF database and review. Frontiers in Ecology and Evolution 9: 1–11.

    Article  Google Scholar 

  • Doyle, J. J. & J. L. Doyle, 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 19: 11–15.

    Google Scholar 

  • Earl, D. A. & B. M. vonHoldt, 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359–361.

    Article  Google Scholar 

  • Ellis, E. C., E. C. Antill & H. Kreft, 2012. All is not loss: plant biodiversity in the Anthropocene. PloS One 7: e30535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L. & H. E. Lischer, 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadjar, M., R. A. Islamy & E. Y. Herawati, 2019. First record of Arapaima gigas (Schinz, 1822) (Teleostei: Osteoglossomorpha), in the Brantas River, Sidoarjo, East Java, Indonesia. Biodiversitas Journal of Biological Diversity 20: 3527–3531.

    Article  Google Scholar 

  • Falush, D., M. Stephens & J. K. Pritchard, 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164: 1567–1587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farias, I. P., T. Hrbek, H. Brinkmann, I. Sampaio & A. Meyer, 2003. Characterization and isolation of DNA microsatellite primers for Arapaima gigas, an economically important but severely over-exploited fish species of the Amazon basin. Molecular Ecology Notes 3: 128–130.

    Article  CAS  Google Scholar 

  • Farias, I. P., S. Willis, A. Leão, J. T. Verba, M. Crossa, I. Sampaio, F. Porto-Foresti & T. Hrbek, 2019. The largest fish in the world’s biggest river: Genetic connectivity and conservation of Arapaima gigas in the Amazon and Araguaia-Tocantins drainages. PloS One 14: 1–27.

    Article  CAS  Google Scholar 

  • Fazzi-Gomes, P. F., N. Melo, G. Palheta, S. Guerreiro, M. Amador, A. K. Ribeiro-dos-Santos & I. Hamoy, 2017. Genetic diversity and differentiation in natural populations of Arapaima gigas from lower Amazon revealed by microsatellites. Genetics and Molecular Research. https://doi.org/10.4238/gmr16019552.

    Article  PubMed  Google Scholar 

  • Felsenstein, J., 1985. Phylogenies and the comparative method. The American Naturalist 125: 1–15.

    Article  Google Scholar 

  • Ferraris-Junior, C. J., 2003. Family Osteoglossidae: check list of the freshwater fishes of South and Central America, Edipucrs, Porto Alegre:, 30.

    Google Scholar 

  • Ferreira, E., 2013. Arapaimatidae. In Queiroz, L. J., et al., (eds), Peixes Do Rio Madeira 1st ed. São Paulo, Dialeto Latin American Documentary: 84–87.

    Google Scholar 

  • Fontenele, O. (1952). Hábitos de desova do pirarucu, “Arapaima gigas” (Cuvier) (pisces, Isospondyli, Arapaimidae) e evolução de sua larva (No. 153). Ministério da Viação e Obras Públicas, Departemento Nacional de Obras contra as Sêcas, Serviço de Piscicultura.

  • Goulding, M., R. Barthem & E. J. G. Ferreira, 2003. The Smithsonian atlas of the Amazon, Smithsonian Institution Press, Washington, DC:

    Google Scholar 

  • Guyot, J. L., J. M. Jouanneau & J. G. Wasson, 1999. Characterisation of river bed and suspended sediments in the Rio Madeira drainage basin (Bolivian Amazonia). Journal of South American Earth Sciences 12: 401–410.

    Article  Google Scholar 

  • Hrbek, T., I. P. Farias, M. Crossa, I. Sampaio, J. I. Porto & A. Meyer, 2005. Population genetic analysis of Arapaima gigas, one of the largest freshwater fishes of the Amazon basIn implications for its conservation. Animal Conservation 8: 297–308.

    Article  Google Scholar 

  • Hulme, P. E., S. Bacher, M. Kenis, S. Klotz, I. Kühn, D. Minchin, W. Nentwig, S. Olenin, V. Panov, J. Pergl, P. Pyšek, A. Roques, D. Sol, W. Solarz & M. Vilà, 2008. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology 45: 403–414.

    Article  Google Scholar 

  • IUCN- International Union for Conservation of Nature (1996). Arapaima gigas. The IUCN Red List of Threatened Species 1996. https://www.iucnredlist.org. Accessed 28 June 2021.

  • Jakobsson, M. & N. A. Rosenberg, 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23: 1801–1806.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T. & C. Collins, 2015. A tutorial for discriminant analysis of principal components (DAPC) using adegenet 2.0.0, Imperial College London, MRC Centre for Outbreak Analysis and Modelling, London:, 1–43.

    Google Scholar 

  • Keller, L. F. & D. M. Waller, 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17: 230–241.

    Article  Google Scholar 

  • Kelly, D. W., J. R. Muirhead, D. D. Heath & H. J. Macisaac, 2006. Contrasting patterns in genetic diversity following multiple invasions of fresh and brackish waters. Molecular Ecology 15: 3641–3653.

    Article  CAS  PubMed  Google Scholar 

  • Kolbe, J. J., R. E. Glor, L. R. Schettino, A. C. Lara, A. Larson & J. B. Losos, 2004. Genetic variation increases during biological invasion by a Cuban lizard. Nature 431: 177–181.

    Article  CAS  PubMed  Google Scholar 

  • Kowarik, I. (1995). Time lags in biological invasions with regard to the success and failure of alien species. Plant invasions: general aspects and special problems, 15–38.

  • Kumar, A. B., S. Raj, C. P. Arjun, U. Katwate & R. Raghavan, 2019. Jurassic invaders: flood-associated occurrence of arapaima and alligator gar in the rivers of Kerala. Current Science 116: 1628–1630.

    Google Scholar 

  • Latini, A. O., D. P. Lima-Junior, H. C. Giacomini, R. O. Latini, D. C. Resende, H. M. Espírito-Santo, D. F. Barros & T. L. Pereira, 2004. Alien fishes in lakes of the Doce river basin (Brazil): range, new occurrences and conservation of native communities. Lundiana: International Journal of Biodiversity 5: 135–142.

    Google Scholar 

  • Latini, A. O., D. C. Resende, V. B. Pombo & L. Coradin, 2016. Espécies exóticas invasoras de águas continentais no Brasil, MMA, Brasília:, 791.

    Google Scholar 

  • Latrubesse, E. M., J. C. Stevaux & R. Sinha, 2005. Tropical rivers. Geomorphology 70: 187–206.

    Article  Google Scholar 

  • Lizarro, D., L. Torres, P. A. Rodal & F. Moreno-Aulo, 2017. Primer registro del paiche, Arapaima gigas (Schinz 1822)(Osteoglossiformes: Arapaimidae) en el río Mamoré, Beni (Bolivia). Ecología En Bolivia 52: 33–37.

    Google Scholar 

  • Lockwood, J. L., P. Cassey & T. Blackburn, 2005. The role of propagule pressure in explaining species invasions. Trends in Ecology and Evolution 20: 223–228.

    Article  PubMed  Google Scholar 

  • Lockwood, J. L., P. Cassey & T. M. 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 

  • Lüling, K. H., 1964. Zur biologte und ökologte von Arapaima gigas (Pisces, Osteoglossidae). Zeitschrift Für Morphologie Und Ökologie Der Tiere 54: 436–530.

    Article  Google Scholar 

  • Marchetti, M. P. & T. Engstrom, 2016. The conservation paradox of endangered and invasive species. Conservation Biology 30: 434–437.

    Article  PubMed  Google Scholar 

  • Marková, J., R. Jerikho, Y. Wardiatno, M. M. Kamal, A. L. B. Magalhães, L. Bohatá, L. Kalous & J. Patoka, 2020. Conservation paradox of giant arapaima Arapaima gigas (Schinz, 1822)(Pisces: Arapaimidae): endangered in its native range in Brazil and invasive in Indonesia. Knowledge and Management of Aquatic Ecosystems. https://doi.org/10.1051/kmae/2020039.

    Article  Google Scholar 

  • Miranda-Chumacero, G., R. Wallace, H. Calderón, G. Calderón, P. Willink, M. Guerrero, T. M. Siles, K. Lara & D. Chuqui, 2012. Distribution of arapaima (Arapaima gigas)(Pisces: Arapaimatidae) in Bolivia: implications in the control and management of a non-native population. BioInvasions Record 1: 129–138.

    Article  Google Scholar 

  • Mitchell, C. E., & A. G Power, 2003. Release of invasive plants from fungal and viral pathogens. Nature, 421: 625–627.

  • Mortatti, J., J. R. Ferreira, L. A. Martinelli, R. L. Victória & A. C. F. Tancredi, 1989. Biogeochemistry of the Madeira river basin. GeoJournal 19: 391–397.

    Article  Google Scholar 

  • Nelson, J. S., 1994. Fishes of the World. John Wiley and Sons, New York.

  • Oberdorff, T., C. Jézéquel, M. Campero, F. Carvajal-Vallejos, J. F. Cornu, M. S. Dias, J. A. Maldonado-Ocampo, H. Ortega, J. F. Renno & P. A. Tedesco, 2015. Opinion paper: how vulnerable are Amazonian freshwater fishes to ongoing climate change? Journal of Applied Ichthyology 31: 4–9.

    Article  Google Scholar 

  • Oliveira, E. J., J. G. Pádua, M. I. Zucchi, R. Vencovsky & M. L. C. Vieira, 2006. Origin, evolution and genome distribution of microsatellites. Genetics and Molecular Biology 29: 294–307.

    Article  CAS  Google Scholar 

  • Oliveira, R. C., M. D. C. F. Santos, G. Bernardino, T. Hrbek & I. P. Farias, 2018. From river to farm: an evaluation of genetic diversity in wild and aquaculture stocks of Brycon amazonicus (Spix and Agassiz, 1829), Characidae, Bryconinae. Hydrobiologia 805: 75–88.

    Article  CAS  Google Scholar 

  • Orsi, M. L. & Â. A. Agostinho, 1999. Introdução de espécies de peixes por escapes acidentais de tanques de cultivo em rios da Bacia do Rio Paraná, Brasil. Revista Brasileira De Zoologia 16: 557–560.

    Article  Google Scholar 

  • Ortega, J. C., H. F. Júlio, 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 

  • Paetkau, D., W. Calvert, I. Stirling & C. Strobeck, 1995. Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4: 347–354.

    Article  CAS  PubMed  Google Scholar 

  • Parker, I. M., D. Simberloff, W. M. Lonsdale, K. Goodell, M. Wonham, P. M. Kareiva, M. H. Williamson, B. Von Holle, 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 

  • Pérez, J. E., M. Nirchio, C. Alfonsi & C. Muñoz, 2006. The biology of invasions: the genetic adaptation paradox. Biological Invasions 8: 1115–1121.

    Article  Google Scholar 

  • Piry, S., A. Alapetite, J. M. Cornuet, D. Paetkau, L. Baudouin & A. Estoup, 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. Journal of Heredity 95: 536–539.

    Article  CAS  PubMed  Google Scholar 

  • Pritchard, J. K., M. Stephens, N. A. Rosenberg & P. Donnelly, 2000. Association mapping in structured populations. The American Journal of Human Genetics 67: 170–181.

    Article  CAS  PubMed  Google Scholar 

  • Pyšek, P. & D. M. Richardson, 2010. Invasive species, environmental change and management, and health. Annual Review of Environment and Resources 35: 25–55.

    Article  Google Scholar 

  • Queiroz, H. L. D. (2000). Natural history and conservation of pirarucu, ‘Arapaima gigas’, at the Amazonian Várzea: red giants in muddy waters. Doctoral dissertation, University of St Andrews.

  • Rannala, B. & J. L. Mountain, 1997. Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences 94: 9197–9201.

    Article  CAS  Google Scholar 

  • Reed, D. H., & Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation biology, 17(1): 230–237.

  • Reusch, T. B., S. Bolte, M. Sparwel, A. G. Moss & J. Javidpour, 2010. Microsatellites reveal origin and genetic diversity of Eurasian invasions by one of the world’s most notorious marine invader, Mnemiopsis leidyi (Ctenophora). Molecular Ecology 19: 2690–2699.

    Article  CAS  PubMed  Google Scholar 

  • Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Article  PubMed  Google Scholar 

  • Romero J. S. (1960). El paiche, aspectos de su historia natural, ecología y aprovechamiento. lnf. Servicio Pesquerías y Caza. Ministerio de Agricultura. Lima-Perú, 63.

  • Roman, J. & J. A. Darling, 2007. Paradox lost: genetic diversity and the success of aquatic invasions. Trends in Ecology and Evolution 22: 454–464.

    Article  PubMed  Google Scholar 

  • Rosenberg, N. A., 2004. DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4: 137–138.

    Article  Google Scholar 

  • Saitou, N. & M. Nei, 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406–425.

    CAS  PubMed  Google Scholar 

  • Santos, L. N., A. A. Agostinho, A. F. Santos & E. García-Berthou, 2019. Reconciliation ecology in Neotropical reservoirs: can fishing help to mitigate the impacts of invasive fishes on native populations? Hydrobiologia 826: 183–193.

    Article  Google Scholar 

  • Seebens, H., T. M. Blackburn, E. E. Dyer, P. Genovesi, P. E. Hulme, J. M. Jeschke, S. Pagad, P. Pyšek, M. Kleunen, M. Winter, M. Ansong, M. Arianoutsou, S. Bacher, B. Blasius, E. G. Brockerhoff, G. Brundu, C. Capinha, C. E. Causton, L. Celesti-Grapow, W. Dawson, S. Dullinger, E. P. Economo, N. Fuentes, B. Guénard, H. Jäger, J. Kartesz, M. Kenis, I. Kühn, B. Lenzner, A. M. Liebhold, A. Mosena, D. Moser, W. Nentwig, M. Nishino, D. Pearman, J. Pergl, W. Rabitsch, J. Rojas-Sandoval, A. Roques, S. Rorke, S. Rossinelli, H. E. Roy, R. Scalera, S. Schindler, K. Štajerová, B. Tokarska-Guzik, K. Walker, D. F. Ward, T. Yamanaka & F. Essl, 2018. Global rise in emerging alien species results from increased accessibility of new source pools. Proceedings of the National Academy of Sciences 115: 2264–2273.

    Article  CAS  Google Scholar 

  • Schrieber, K. & S. Lachmuth, 2017. The genetic paradox of invasions revisited: the potential role of inbreeding× environment interactions in invasion success. Biological Reviews 92: 939–952.

    Article  PubMed  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 

  • Simon-Bouhet, B., P. Garcia-Meunier & F. Viard, 2006. Multiple introductions promote range expansion of the mollusc Cyclope neritea (Nassariidae) in France: evidence from mitochondrial sequence data. Molecular Ecology 15(6): 1699–1711.

    Article  CAS  PubMed  Google Scholar 

  • Sioli, H., 1968. Hydrochemistry and geology in the Brazilian Amazon region. Amazoniana: Limnologia Et Oecologia Regionalis Systematis Fluminis Amazonas 1: 267–277.

    Google Scholar 

  • Soares, L., J. Cavali, J. R. S. Vitule & C. R. D. C. Doria, 2020. Ciência Cidadã como forma de identificação de ocorrência de espécies não nativas na Amazônia. South American Journal of Basic Education, Technical and Technological 7: 145–159.

    Google Scholar 

  • Stewart, D. J., 2013a. Re-description of Arapaima agassizii (Valenciennes), a rare fish from Brazil (Osteoglossomorpha: Osteoglossidae). Copeia 2013: 38–51.

    Article  Google Scholar 

  • Stewart, D. J., 2013b. A new species of Arapaima (Osteoglossomorpha: Osteoglossidae) from the Solimões River, Amazonas State, Brazil. Copeia 2013: 470–476.

    Article  Google Scholar 

  • Takezaki, N., M. Nei & K. Tamura, 2014. POPTREEW: web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Molecular Biology and Evolution 31: 1622–1624.

    Article  CAS  PubMed  Google Scholar 

  • Torati, L. S., J. B. Taggart, E. S. Varela, J. Araripe, S. Wehner & H. Migaud, 2019. Genetic diversity and structure in Arapaima gigas populations from Amazon and Araguaia-Tocantins River basins. BMC Genetics 20(1): 1–13.

    Article  Google Scholar 

  • Torrente-Vilara, G., J. Zuanon, F. Leprieur, T. Oberdorff & P. A. Tedesco, 2011. Effects of natural rapids and waterfalls on fish assemblage structure in the Madeira River (Amazon Basin). Ecology of Freshwater Fish 20: 588–597.

    Article  Google Scholar 

  • Van Oosterhout, C., W. F. Hutchinson, D. P. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  CAS  Google Scholar 

  • Van Damme, P. A., C. C. Méndez, M. Zapata, F. M. Carvajal-Vallejos, J. Carolsfeld & J. D. Olden, 2015. The expansion of Arapaima cf. gigas (Osteoglossiformes: Arapaimidae) in the Bolivian Amazon as informed by citizen and formal science. Management of Biological Invasions 6: 375–383.

    Article  Google Scholar 

  • Vellend, M., L. Baeten, I. H. Myers-Smith, S. C. Elmendorf, R. Beauséjour, C. D. Brown, P. Frenne, K. Verheyen & S. Wipf, 2013. Global meta-analysis reveals no net change in local-scale plant biodiversity over time. Proceedings of the National Academy of Sciences 110: 19456–19459.

    Article  CAS  Google Scholar 

  • Vellend, M., 2017. The biodiversity conservation paradox. American Scientist 105: 94–101.

    Article  Google Scholar 

  • Vitorino, C. A., R. C. Oliveira, V. P. Margarido & P. C. Venere, 2015. Genetic diversity of Arapaima gigas (Schinz, 1822)(Osteoglossiformes: Arapaimidae) in the Araguaia-Tocantins basin estimated by ISSR marker. Neotropical Ichthyology 13: 557–568.

    Article  Google Scholar 

  • Vitorino, C. A., F. Nogueira, I. L. Souza, J. Araripe & P. C. Venere, 2017. Low genetic diversity and structuring of the Arapaima (Osteoglossiformes, Arapaimidae) population of the Araguaia-Tocantins basin. Frontiers in Genetics 8: 159.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vitule, J. R., T. V. Occhi, B. Kang, S. I. Matsuzaki, L. A. Bezerra, V. S. Daga, L. Faria, F. A. Frehse, F. Walter & A. A. Padial, 2019. Intra-country introductions unraveling global hotspots of alien fish species. Biodiversity and Conservation 28: 3037–3043.

    Article  Google Scholar 

  • Watson, L. C., D. J. Stewart & M. A. Teece, 2013. Trophic ecology of Arapaima in Guyana: giant omnivores in Neotropical floodplains. Neotropical Ichthyology 11: 341–349.

    Article  Google Scholar 

  • Weidel, B. C., D. C. Josephson & C. E. Kraft, 2007. Littoral fish community response to smallmouth bass removal from an Adirondack Lake. Transactions of the American Fisheries Society 136: 778–789.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the Foundation for the Development of Scientific and Technological Actions and Research of the State of Rondônia (FAPERO) for the financial support. The authors DTBSC and AMX thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for supporting a doctoral scholarship (financial code 001). We also thank the Laboratory of Animal Genetics and Evolution (LEGAL) of the Universidade Federal do Amazonas and Thematic Laboratory of Molecular Biology (LTBM) of the Instituto Nacional de Pesquisas da Amazônia (INPA) for logistical support. Pedro Senna Bittencourt helped with DAPC analysis. We are also grateful to the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for research grants provided to JRSV (Process Numbers: 302367/2018-7 and 303776/2015-3) and to CRCD (Process Numbers: 305836/2020-0).

Funding

This study was funded by Foundation for the Development of Scientific and Technological Actions and Research of the State of Rondônia (FAPERO), Coordination for the Improvement of Higher Education Personnel (CAPES, financial code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—process numbers: 302367/2018–7, 303776/2015–3 and 305836/2020–0.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dayana Tamiris Brito dos Santos Catâneo.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Additional information

Handling editor: Fernando M. Pelicice.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 12 KB)

Supplementary file2 (XLSX 23 KB)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Catâneo, D.T.B., Ximenes, A.M., Garcia-Davila, C.R. et al. Elucidating a history of invasion: population genetics of pirarucu (Arapaima gigas, Actinopterygii, Arapaimidae) in the Madeira River. Hydrobiologia 849, 3617–3632 (2022). https://doi.org/10.1007/s10750-022-04977-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-022-04977-8

Keywords

Navigation