Abstract
The objective of our study was to evaluate the efficacy of DNA barcoding as a tool to identify non-native fish in their early stages of life. Specimens were collected from 14 sites in the lower and middle regions of the Paranapanema River—the main tributary of the Upper Paraná River basin in southern Brazil. Over three reproductive periods from 2012 and 2015, 75 eggs and 170 larvae from 13 non-native fish species were identified. The most abundant species were Plagioscion squamosissimus (75 specimens) and Serrasalmus marginatus (68 specimens). The highest abundance was found near the Rosana hydroelectric plant reservoir. The removal of the natural physical barrier is the main reason that fish are introduced into the Paranapanema River basin with higher occurrence in the Rosana reservoir. P. squamosissimus was found in all reservoirs. DNA barcoding is a useful tool for identifying non-native fish during their reproductive phase. Furthermore, recording the presence of potentially invasive species in their early development stages may provide information useful for the rapid and effective control.
Similar content being viewed by others
References
Agostinho, C. S. & H. F. Julio Jr., 2002. Observation of an invasion of the piranha Serrasalmus marginatus Velenciennes, 1947(Osteichthyes, Serrasalmidae) into the Upper Parana River, Brazil. Acta Scientiarum 24: 391–395.
Agostinho, A. A., S. M. Thomaz & L. C. Gomes, 2005. Conservation of the biodiversity of Brazil’s inland waters. Conservation Biology 19: 646–652.
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.
Alexandre, P. C., E. A. Luiz, P. A. Piana, L. C. Gomes & A. A. Agostinho, 2008. Relação estoque-recrutamento para as piranhas Serrasalmus marginatus (Valenciennes, 1847) e S. maculatus (Kner, 1860) no rio Baía, alto rio Paraná. Acta Scientiarum: Biological Sciences 26: 303–307.
Azevedo-Santos, V. M., J. R. S. Vitule, E. García-Berthou, F. M. Pelicice & D. Simberloff, 2016. Misguided strategy for mosquito control. Science 351: 675.
Baumgartner, G., K. Nakatani, L. C. Gomes, A. Bialetzki & P. V. Sanches, 2004. Identification of spawning sites and natural nurseries of fishes in the upper Paraná River, Brazil. Environmental Biology of Fishes 71: 115–125.
Baumgartner, G., K. Nakatani, L. C. Gomes, A. Bialetzki, P. V. Sanches & M. C. Makrakis, 2008. Fish larvae from the upper Paraná River: do abiotic factors affect larval density? Neotropical Ichthyology 6: 551–558.
Bax, N., J. T. Carlton, A. Mathews-Amos, R. L. Haedrich, F. G. Howarth, J. E. Purcell, A. Rieser & A. Gray, 2001. The control of biological invasions in the world’s oceans. Conservation Biology 15: 1234–1246.
Bialetzki, A., K. Nakatani, P. V. Sanches, G. Baumgartner & L. C. Gomes, 2005. Larval fish assemblage in the Baía River (Mato Grosso do Sul State, Brazil): temporal and spatial patterns. Environmental Biology of Fishes 73: 37–47.
Blackburn, T. M., P. Pysek, S. Bacher, J. T. Carlton, R. P. Duncan, V. Jarosík, J. R. U. Wilson & D. M. Richardson, 2011. A proposed unified framework for biological invasions. Trends in Ecology and Evolution 26: 333–339.
Briski, E., M. E. Cristescu, S. A. Bailey & H. J. MacIsaac, 2011. Use of DNA barcoding to detect invertebrate invasive species from diapausing eggs. Biological Invasions 13: 1325–1340.
Briski, E., S. Ghabooli, S. A. Bailey & H. J. MacIsaac, 2016. Are genetic databases sufficiently populated to detect non-indigenous species? Biological Invasions 18: 1911–1922.
Colautti, R. I. & H. J. MacIsaac, 2004. A neutral terminology for defining invasive species. Diversity and Distributions 10: 135–141.
Comtet, T., A. Sandionigi, F. Viard & M. Casiraghi, 2015. DNA (meta) barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens. Biological Invasions 17: 905–922.
Consuegra, S., N. Phillips, G. Gajardo & C. G. de Leaniz, 2011. Winning the invasion roulette: escapes from fish farms increase admixture and facilitate establishment of nonnative rainbow trout. Evolutionary Applications 4: 660–671.
Didham, R. K., J. M. Tylianakis, N. J. Gemmell, T. A. Rand & R. M. Ewers, 2007. Interactive effects of habitat modification and species invasion on native species decline. Trends in Ecolology and Evolution 22: 489–496.
Frantine-Silva, W., S. H. Sofia, M. L. Orsi & F. S. Almeida, 2015. DNA barcoding of freshwater ichthyoplankton in the Neotropics as a tool for ecological monitoring. Molecular Ecology Resources 15: 1226–1237.
Goodwin, N. B., S. Balshine-Earn & J. D. Reynolds, 1998. Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society of London B: Biological Sciences 265: 2265–2272.
Havel, J. E., C. E. Lee & J. M. Vander Zanden, 2005. Do reservoirs facilitate invasions into landscapes? BioScience 55: 518–525.
Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. DeWaard, 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society B Biological Sciences 270: 313–321.
Hebert, P. D. N., S. Ratnasingham & J. R. DeWaard, 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B Biological Sciences 270: 96–99.
Hubert, N., B. Espiau, C. Meyer & S. Planes, 2015. Identifying the ichthyoplankton of a coral reef using DNA barcodes. Molecular Ecology Resources 15: 57–67.
Júlio Júnior, H. F., C. Dei 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.
Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16(111): 120.
Ko, H., Y. Wang, T. Chiu, M. Lee, M. Leu, K. Chang, W. Chen & K. Shao, 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS ONE 8: 3–9.
Langeani, F., R. M. C. Castro, O. T. Oyakawa, O. A. Shibatta, C. S. Pavanelli & L. Casatti, 2007. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotropica 5: 75–78.
Lewis, L. A., D. E. Richardson, E. V. Zakharov & R. Hanner, 2016. Integrating DNA barcoding of fish eggs into ichthyoplankton monitoring programs. Fishery Bulletin 114(2): 153–165.
Lockwood, J. L., M. F. Hoopes & M. P. Marchetti, 2007. Invasion Ecology. Blackwell Publishing, Oxford.
Lowe, M. R., W. Wu, M. S. Peterson, N. J. Brown-Peterson, W. T. Slack & P. J. Schofield, 2012. Survival, growth and reproduction of nonnative Nile Tilapia II: fundamental niche projections and invasion potential in the Northern Gulf of Mexico. PLoS ONE 7: e41580.
Nakatani, K., A. A. Agostinho, G. Baumgartner, A. Bialetzki, P. V. Sanches, M. C. Makrakis & C. S. Pavanelli, 2001. Ovos e larvas de peixes de água doce: desenvolvimento e manual de identificação. Eduem, Maringá.
Orsi, M. L., 2010. Estratégias reprodutivas de peixes da região média-baixa do Rio Paranapanema, reservatório de Capivara. Editora Blucher, São Paulo.
Ortega, J. C. G., H. F. Júlio Jr., L. C. Gomes & A. A. Agostinho, 2015. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746: 147–158.
Pegg, G. G., B. Sinclair, L. Briskey & W. J. Aspden, 2006. MtDNA barcode identification of fish larvae in the southern Great Barrier Reef, Australia. Scientia Marina 70: 7–12.
Pereira, L. H., R. Hanner, F. Foresti & C. Oliveira, 2013. Can DNA barcoding accurately discriminate megadiverse Neotropical freshwater fish fauna? BMC genetics 14: 20–34.
Ratnasingham, S. & P. D. N. Hebert, 2007. BOLD: The Barcode of Life Data System (www.bacodingoflife.org). Molecular Ecology Notes 7: 355–364.
Ratnasingham, S. & P. D. Hebert, 2013. A DNA-based registry for all animal species: the barcode index number (BIN) system. PLoS ONE 8(7): e66213.
Reis, R. E., J. S. Albert, F. Di Dario, M. M. Mincarone, P. Petry & L. A. Rocha, 2016. Fish biodiversity and conservation in South America. Journal of Fish Biology 89: 12–47.
Reynalte-Tataje, D. A., A. P. O. Nuñer, M. C. Nunes, V. Garcia, C. A. Lopes & E. Zaniboni-Filho, 2012. Spawning of migratory fish species between two reservoirs of the upper Uruguay River, Brazil. Neotropical Ichthyology 10: 829–835.
Simberloff, D., 2009. We can eliminate invasions or live with them. Successful management projects. Biological Invasions 11: 149–157.
Tamura, K., G. Stecher, D. Peterson, A. Filipski & S. Kumar, 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30: 2725–2729.
Togawa, R. C. & M. M. Brigido, 2003. PHPH: web based tool for simple electropherogram quality analysis. In 1st International Conference on Bioinformatics and Computational Biology – IcoBiCoBi. Ribeirão Preto, Brasil: 1. Available at: http://asparagin.cenargen.embrapa.br/phph/
Valdez-Moreno, M., N. V. Ivanova, M. Elias-Gutiérrez, S. C. Balderas & P. D. N. Hebert, 2009. Probing diversity in freshwater fishes from Mexico and Guatemala with DNA barcodes. Journal of Fish Biology 74: 377–402.
Valdez-Moreno, M., L. Vásquez-Yeomans, M. Elías-Gutiérrez, N. V. Ivanova & P. D. N. Hebert, 2010. Using DNA barcodes to connect adults and early life stages of marine fishes from the Yucatan Peninsula, Mexico: potential in fisheries management. Marine and Freshwater Research 61: 665–671.
Vitule, J. R. S., A. A. Agostinho, V. M. Azevedo-Santos, V. S. Daga, W. R. T. Darwall, D. B. Fitzgerald, F. A. Frehse, D. J. Hoeinghaus, D. P. Lima-Junior, A. L. B. Magalhães, M. L. Orsi, A. A. Padial, F. M. Pelicice, M. Petrere Jr., P. S. Pompeu & K. O. Winemiller, 2017. We need better understanding about functional diversity and vulnerability of tropical freshwater fishes. Biodiversity and Conservation 26: 757–762.
Ward, R. D., T. S. Zemlak, B. H. Innes, P. R. Last & P. D. Hebert, 2005. DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 360: 1847–1857.
Author information
Authors and Affiliations
Corresponding author
Additional information
Guest editors: John E. Havel, Sidinei M. Thomaz, Lee B. Kats, Katya E. Kovalenko & Luciano N. Santos / Aquatic Invasive Species II
Data Accessibility
Bold dataset for non-native species: http://www.boldsystems.org/index.php/Public_SearchTerms?query=DS-IFEL. BOLD projects: container project FELPR (Projects: PDCAI, accessions PDCAI001-13 to PDCAI134-13; PDCAP, accessions PDCAP001-14 to PDCAP287-14; PDCII accessions PDCII115-14). BOLD annexed project FUPR, accessions: BAST525-12, FUPR001-09 to FUPR1468-10. BOLD projects: PRP, Fish eggs and larvae of Paranapanema river (Accessions PRP001-16 to PRP960-16).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
BOLD TaxonID Tree for non-native fish species identified by DNA barcoding data along the lower–middle Paranapanema River (PDF 10 kb)
Rights and permissions
About this article
Cite this article
Almeida, F.S., Frantine-Silva, W., Lima, S.C. et al. DNA barcoding as a useful tool for identifying non-native species of freshwater ichthyoplankton in the neotropics. Hydrobiologia 817, 111–119 (2018). https://doi.org/10.1007/s10750-017-3443-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-017-3443-5