Skip to main content
SpringerLink
Log in

The expansion of exotic Chinook salmon (Oncorhynchus tshawytscha) in the extreme south of Patagonia: an environmental DNA approach

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The ability to detect species at low densities, greatly improves the success of management action on alien invasive species and decreases their possible impact on ecosystems. In the last two decades, exotic Chinook salmon (Oncorhynchus tshawytscha) have established populations in both Pacific and Atlantic river basins of Patagonia. The last established populations have been reported in the extreme south of Patagonia, on the island of Tierra del Fuego (TDF). The relatively recent appearance of Chinook salmon in TDF and the great phenotypic plasticity of this species, make it necessary to study their distribution and expansion as soon as possible, since they have the potential to negatively impact on native ecosystems. With the objective of knowing the current distribution status of exotic Chinook salmon in TDF, we optimized and implemented a detection method based on environmental DNA (eDNA). First, we designed Chinook salmon-specific primers, with no cross-amplification, using DNA from other species that are living at the same environment. Second, we validated the primers in situ by detecting Chinook salmon DNA from natural environments at the same time that we performed a conventional survey using an electrofishing survey method. Finally, we collected water samples from 10 river basins and one estuary within TDF and one river basin from Isla de los Estados (IE) and performed single-species real-time PCR assays. We were able to detect Chinook salmon DNA from 5 basins and from the estuary in TDF. These eDNA-based results allowed us to confirm the expansion of exotic Chinook salmon since they were first reported in TDF.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arismendi I, Soto D (2012) Are salmon-derived nutrients being incorporated in food webs of invaded streams? Evidence from southern Chile. Knowl Manag Aquat Ecosyst 405:01

    Article  Google Scholar 

  • Atkinson S, Carlsson JEL, Ball B, Egan D, Kelly Quinn M, Whelan K, Carlsson J (2018) A quantitative PCR based environmental DNA assay for detecting Atlantic salmon (Salmo salar L.). Aquat Conserv 28:1–6

    Article  Google Scholar 

  • Biggs J, Ewald N, Valentini A, Gaboriaud C, Dejean T, Griffiths RA, Foster J, Wilkinson JW, Arnell A, Brotherton P, Williams P, Dunn F (2015) Using eDNA to develop a national citizen science-based monitoring programme for the great crested newt (Triturus cristatus). Biol Conserv 183:19–28

    Article  Google Scholar 

  • Brandl S, Schumer G, Schreier BM, Conrad JL, May B, Baerwald MR (2015) Ten real-time PCR assays for detection of fish predation at the community level in the San Francisco Estuary-Delta. Mol Ecol Resour 15:278–284

    Article  CAS  PubMed  Google Scholar 

  • Carim KJ, Padgett-Stewart TM, Wilcox TM, Young MK, McKelvey K, Schwartz M (2015) Protocol for collecting eDNA samples from streams. General technical report, RMRS-GTR-355. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fort Collins, CO

  • Chalde T, Fernández DA (2017) Early migration and estuary stopover of introduced Chinook salmon population in the Lapataia river basin, southern Tierra del Fuego Island. Estuar Coast Shelf Sci 199:49–58

    Article  Google Scholar 

  • Chalde T, Casalinuovo M, Rojo J, Villatarco P, Boy C, Lesta S, Fernández DA (2016) New establishment of a Chinook salmon (Oncorhynchus tshawytscha) population in the extreme South of Patagonia. Dissertation, freshwater invasive species, Buenos Aires, Argentina

  • Ciancio J, Pascual MA, Botto F, Frere E, Iribarne O (2008) Trophic relationships of exotic anadromous salmonids in the southern Patagonian shelf as inferred from stable isotopes. Limnol Oceanogr 53:788–798

    Article  Google Scholar 

  • Correa C, Gross M (2008) Chinook salmon invade southern South America. Biol Invasions 10:615–639

    Article  Google Scholar 

  • Correa C, Moran P (2017) Polyphyletic ancestry of expanding Patagonian Chinook salmon populations. Sci Rep 7:14338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cussac VE, Habit E, Ciancio J, Battini MA, Riva Rossi C, Barriga JP, Baigún C, Crichigno S (2016) Freshwater fishes of Patagonia: conservation and fisheries. J Fish Biol 89:1068–1097

    Article  CAS  PubMed  Google Scholar 

  • Dejean T, Valentini A, Miquel C, Taberlet P, Bellemain E, Miaud C (2012) Improved detection of an alien invasive species through environmental DNA barcoding: the example of the American bullfrog Lithobates catesbeianus. J Appl Ecol 49:953–959

    Article  Google Scholar 

  • Di Prinzio CY, Arismendi I (2018) Early development and diets of non-native juvenile Chinook Salmon (Oncorhynchus tshawytscha) in an invaded river of Patagonia, southern South America. Austral Ecol. https://doi.org/10.1111/aec.12597

    Article  Google Scholar 

  • Dougherty MM, Larson ER, Renshaw MA, Gantz C, Egan SP, Erickson DM, Lodge DM (2016) Environmental DNA (eDNA) detects the invasive rusty crayfish Orconectes rusticus at low abundances. J Appl Ecol 53:722–732

    Article  PubMed  PubMed Central  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80

    Article  Google Scholar 

  • Espinosa MA (2008) Diatoms from Patagonia and Tierra del Fuego. Dev Quat Sci 11:383–392

    Google Scholar 

  • Fernandez S, Sandin M, Beaulieu PG, Clusa L, Martinez JL, Ardura A, García-Vázquez E (2018) Environmental DNA for freshwater fish monitoring: insights for conservation within a protected area. PeerJ 6:e4486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández DA, Ciancio J, Ceballos S, Riva-Rossi C, Pascual M (2010) Chinook salmon (Oncorhynchus tshawytscha, Walbaum 1792) in the Beagle Channel, Tierra del Fuego: the onset of an invasion. Biol Invasions 12:2991–2997

    Article  Google Scholar 

  • Goldberg CS, Pilliod DS, Arkle RS, Waits LP (2011) Molecular detection of vertebrates in stream water: a demonstration using rocky mountain tailed frogs and Idaho giant salamanders. PLoS ONE 6:e22746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg CS, Sepulveda A, Ray A, Baumgardt J, Waits LP (2013) Environmental DNA as a new method for early detection of New Zealand mudsnails (Potamopyrgus antipodarum). Freshw Sci 32:792–800

    Article  Google Scholar 

  • Goldberg CS, Turner CR, Deiner K et al (2016) Critical considerations for the application of environmental DNA methods to detect aquatic species. Methods Ecol Evol. https://doi.org/10.1111/2041-210X.12595

    Article  Google Scholar 

  • Gosztonyi AE (1970) Los peces de la expedición científica a la Isla de los Estados, Argentina (noviembre–diciembre 1967). Physis 30:173–180

    Google Scholar 

  • Healey MC (1991) Life history of Chinook salmon (Oncorhynchus tshawytscha). In: Groot GC, Margolis L (eds) Pacific salmon life histories. University of British Columbia Press, Vancouver, pp 311–394

    Google Scholar 

  • Hebert PD, Cywinska A, Ball SL, de Waard JR (2003) Biological identifications through DNA barcodes. Proc Biol Sci 270:313–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herder JE, Valentini A, Bellemain E, Dejean T, van Delft J, Thomsen P, Taberlet P (2014) Environmental DNA: a review of the possible applications for the detection of (invasive) species. Stichting RAVON, Nijmegen. Report 2013-104

  • Iturraspe R, Urciuolo A (2000) Clasificación y caracterización de las cuencas hídricas de Tierra del Fuego. Dissertation, XVIII Congreso Nacional del Agua, Santiago del Estero, Argentina

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  CAS  PubMed  Google Scholar 

  • Laramie MB, Pilliod DS, Goldberg CS (2015) Characterizing the distribution of an endangered salmonid using environmental DNA analysis. Biol Conserv 183:29–37

    Article  Google Scholar 

  • Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S (2008) Fish invasions in the world’s river systems: when natural processes are blurred by human activities. PLoS Biol 6:404–410

    CAS  Google Scholar 

  • McKee AM, Spear AF, Pierson TW (2015) The effect of dilution and the use of a post-extraction nucleic acid purification column on the accuracy, precision, and inhibition of environmental DNA samples. Biol Conserv 183:70–76

    Article  Google Scholar 

  • Mehta SV, Haight RG, Homans FR, Polasky S, Venette RC (2007) Optimal detection and control strategies for invasive species management. Ecol Econ 61:237–245

    Article  Google Scholar 

  • Miller SA, Dykes D, Polesky H (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:12–15

    Google Scholar 

  • Moreno CA, Jara HF (1984) Ecological studies on fish fauna associated with Macrocystis pyrifera belts in the south of Fueguian Islands, Chile. Mar Ecol Prog Ser 15:99–107

    Article  Google Scholar 

  • Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320

    Article  CAS  PubMed  Google Scholar 

  • Naylor R, Hindar K, Fleming IA, Goldburg R, Williams S, Volpe J, Whoriskey F, Eagle J, Kelso D, Mangel M (2005) Fugitive salmon: assessing the risks of escaped fish from net-pen aquaculture. Bioscience 55:427–437

    Article  Google Scholar 

  • Opel KL, Chung D, McCord BR (2010) A study of PCR inhibition mechanisms using real time PCR. Forensic Sci 55:25–33

    Article  CAS  Google Scholar 

  • Pascual MA, Macchi P, Urbanski J, Marcos F, Riva Rossi C, Novara M, Dell’Arciprete P (2002) Evaluating potential effects of exotic freshwater fish from incomplete species presence–absence data. Biol Invasions 4:101–113

    Article  Google Scholar 

  • Pascual MA, Cussac V, Dyer B, Soto D, Vigliano P, Ortubay S, Macchi P (2007) Freshwater fishes of Patagonia in the 21st century after a hundred years of human settlement, species introductions, and environmental change. Aquat Ecosyst Health Manag 10:212–227

    Article  Google Scholar 

  • Pascual MA, Lancelotti JL, Ernst B, Ciancio JE, Aedo E, García-Asorey M (2009) Scale, connectivity, and incentives in the introduction and management of non-native species: the case of exotic salmonids in Patagonia. Front Ecol Environ 7:533–540

    Article  Google Scholar 

  • Piaggio AJ, Engeman RM, Hopken MW, Humphrey JS, Keacher KL, Bruce WE, Avery ML (2014) Detecting an elusive invasive species: a diagnostic PCR to detect Burmese python in Florida waters and an assessment of persistence of environmental DNA. Mol Ecol Resour 14:374–380

    Article  CAS  PubMed  Google Scholar 

  • Ponce J, Fernández M (2014) Climatic and environmental history of Isla de los Estados. Springer, Berlin

    Book  Google Scholar 

  • Rasmussen RS, Morrissey MT, Hebert PDN (2009) DNA barcoding of commercially important salmon and trout species Oncorhynchus and Salmo) from North America. J Agric Food Chem 57:8379–8385

    Article  CAS  PubMed  Google Scholar 

  • Rees H, Maddison B, Middleditch D, Patmore J, Gough K (2014) The detection of aquatic animal species using environmental DNA: a review of eDNA as a survey tool in ecology. J Appl Ecol 51:1450–1459

    Article  CAS  Google Scholar 

  • Soto D, Jara F, Moreno C (2001) Escaped salmon in the inner seas, southern Chile: facing ecological and social conflicts. Ecol Appl 11:1750–1762

    Article  Google Scholar 

  • Soto D, Arismendi I, Di Prinzio C, Jara F (2007) Establishment of Chinook salmon (Oncorhynchus tshawytscha) in Pacific basins of southern South America and its potential ecosystem implications. Rev Chil Hist Nat 80:81–98

    Article  Google Scholar 

  • Taberlet P, Bonin A, Zinger L, Coissac E (2018) Environmental DNA: for biodiversity research and monitoring. Oxford University Press, Oxford, p 272

    Book  Google Scholar 

  • Takahara T, Minamoto T, Doi H (2013) Using environmental DNA to estimate the distribution of an invasive fish species in ponds. PLoS ONE 8:e56584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tréguier A, Paillisson JM, Dejean T, Valentini A, Schlaepfer M, Roussel JM (2014) Environmental DNA surveillance for invertebrate species: advantages and technical limitations to detect invasive crayfish Procambarus clarkii in freshwater ponds. J Appl Ecol 51:871–879

    Article  CAS  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3: new capabilities and interfaces. Nucleic Acids Res 40:e115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitousek PM, D’antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was funded by Ministerio de Educación de Argentina (SPU-VT12-UNTF5286), Universidad Nacional de Tierra del Fuego (PID-UNTDF B 16), Agencia Nacional de Promoción Científica y Tecnológica (PICT 0759-2015) and Consejo Nacional de Investigaciones Científicas y Técnicas (PIP 440). The authors thank to Javier Rojo, Sebastián Poljak and Miguel Casalinuovo for their valuable assistance in field sampling as well as Carolina Camilion and Noelia Paredes for their laboratory technical assistance.

Author information

Authors and Affiliations

  1. Instituto de Ciencias Polares, Recursos Naturales y Ambientes, Universidad Nacional de Tierra del Fuego (ICPA-UNTDF), Fuegia Basket 251, V9410BXE, Ushuaia, Argentina

    Cristina Fernanda Nardi & Daniel Alfredo Fernández

  2. Laboratorio de Ecología, Fisiología y Evolución de Organismos Acuáticos, Centro Austral de Investigaciones Científicas (CADIC-CONICET), Bernardo Houssay 200, V9410BFD, Ushuaia, Tierra del Fuego, Argentina

    Daniel Alfredo Fernández, Fabián Alberto Vanella & Tomás Chalde

  3. Extensión Áulica Ushuaia (UTN-FRRG), Facultad Regional Río Grande, Universidad Tecnológica Nacional, Perito Moreno 1425, V9410KSS, Ushuaia, Tierra del Fuego, Argentina

    Fabián Alberto Vanella & Tomás Chalde

Authors
  1. Cristina Fernanda Nardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel Alfredo Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fabián Alberto Vanella
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tomás Chalde
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tomás Chalde.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nardi, C.F., Fernández, D.A., Vanella, F.A. et al. The expansion of exotic Chinook salmon (Oncorhynchus tshawytscha) in the extreme south of Patagonia: an environmental DNA approach. Biol Invasions 21, 1415–1425 (2019). https://doi.org/10.1007/s10530-018-1908-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-018-1908-8

Keywords

Search

Navigation