Skip to main content
SpringerLink
Log in

Brown trout population structure highly affected by multiple stocking and river diversion in a high mountain national park

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Stocking is a widely applied practice for enhancement of fish populations exploited for recreational and commercial uses. In the present study, we investigate the genetic consequences of stocking and river diversion by analyzing 18 microsatellites in 440 brown trout (Salmo trutta L.) from three historical and ten contemporary populations from two river systems in a national park in Norway. Eight sources have been recorded for stocking in this area, but not concurrently. These stocking events took place after historical sampling and river diversion by construction of a barrier and a channel. A complete shift in the genetic structure between historical and contemporary populations was revealed. The genetic differentiation can be explained by stocking with just four non-native sources. The constructed barrier has helped to maintain a fraction of the historical genetic profile. Stocking success is discussed in relation to population exploitation, variation in natural recruitment, and reduced discharge due to river diversion. Our study demonstrates a high vulnerability of natural populations to stocking with non-native fish, of particular importance for fishery management and preservation of native fish.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Philos Trans Roy Soc B 353:177–186

    Article  CAS  Google Scholar 

  • Bakke Ø 1984. Dyregravene på Hardangervidda. En skisse av deres forekomst og bakgrunn. In: Norsk skogbruksmuseum årbok nr. 10, Elverum, pp 129–198 (in Norwegian)

  • Barson NJ, Haugen TO, Vøllestad LA, Primmer CR (2009) Contemporary isolation-by-distance, but not isolation-by-time, among demes of european grayling (Thymallus thymallus, Linnaeus) with recent common ancestors. Evolution 63:549–556

    Article  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Borgstrøm R, Museth J (2005) Accumulated snow and summer temperature: critical factors for recruitment to high mountain populations of brown trout (Salmo trutta L.). Ecol Freshw Fish 14:375–384

    Article  Google Scholar 

  • Cairney M, Taggart JB, Høyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar L.) and cross-species amplification in other salmonids. Mol Ecol 9:2175–2178

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J, Nilsson J (2000) Population genetic structure of brown trout (Salmo Trutta L.) within a northern boreal forest stream. Hereditas 132:173–181

    Article  PubMed  CAS  Google Scholar 

  • Carlsson J, Nilsson J (2001) Effects of geomorphological structures on genetic differentiation among brown trout populations in a northern boreal river drainage. Trans Am Fish Soc 130:36–45

    Article  Google Scholar 

  • Carlsson J, Olsen KH, Nilsson J, Overli O, Stabell OB (1999) Microsatellites reveal fine-scale genetic structure in stream-living brown trout. J Fish Biol 55:1290–1303

    Article  CAS  Google Scholar 

  • Cavalli-Sforza Ll, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Article  Google Scholar 

  • Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. PNAS 103:238–242

    Article  Google Scholar 

  • Cook N, Rahel FJ, Hubert WA (2010) Persistence of Colorado River cutthroat trout populations in isolated headwater streams of Wyoming. Trans Am Fish Soc 139:1500–1510

    Article  Google Scholar 

  • Dieringer D, Schlotterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Estoup A, Presa P, Krieg F, Vaiman D, Guyomard R (1993) CT)n and (GT)n microsatellites: a new class of genetic markers for Salmo trutta L. (brown trout. Heredity 71:488–496

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Felsenstein J (2004) PHYLIP (Phylogeny Inference Package), version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, Washington

  • García-Marín JL, Jorde PE, Ryman N, Utter F, Pla C (1991) Management implications of genetic differentiation between native and hatchery populations of brown trout (Salmo trutta) in Spain. Aquaculture 95:235–249

    Article  Google Scholar 

  • García-Marín JL, Sanz N, Pla C (1998) Proportions of native and introduced brown trout in adjacent fished and unfished Spanish rivers. Conserv Biol 12:313–319

    Article  Google Scholar 

  • Gharbi K, Gautier A, Danzmann RG, Gharbi S, Sakamoto T, Høyheim B, Taggart JB, Cairney M, Powell R, Krieg F, Okamoto N, Ferguson MM, Holm LE, Guyomard R (2006) A linkage map for brown trout (Salmo trutta): chromosome homeologies and comparative genome organization with other salmonid fish. Genetics 172:2405–2419

    Article  PubMed  CAS  Google Scholar 

  • Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates Sunderland, pp 19–34

  • Glover KA, Quintela M, Wennevik V, Besnier F, Sørvik AGE, Skaala Ø (2012) Three decades of farmed escapees in the wild: a spatio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS One 7:e43129

    Article  PubMed  CAS  Google Scholar 

  • Gosset C, Rives J, Labonne J (2006) Effect of habitat fragmentation on spawning migration of brown trout (Salmo trutta L.). Ecol Freshw Fish 15:247–254

    Article  Google Scholar 

  • Griffiths AM, Koizumi I, Bright D, Stevens JR (2009) A case of isolation by distance and short-term temporal stability of population structure in brown trout (Salmo trutta) within the River Dart, southwest England. Evol Appl 2:537–554

    Article  Google Scholar 

  • Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmo trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015

    Article  PubMed  CAS  Google Scholar 

  • Hansen MM, Bekkevold D, Jensen LF, Mensberg K-LD, Nielsen EE (2006) Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. J Appl Ecol 43:669–679

    Article  CAS  Google Scholar 

  • Hansen MM, Fraser DJ, Meier K, Mensberg K-LD (2009) Sixty years of anthropogenic pressure: a spatio-temporal genetic analysis of brown trout populations subject to stocking and population declines. Mol Ecol 18:2549–2562

    Article  PubMed  CAS  Google Scholar 

  • Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap p value in phylogenetic studies. Mol Biol Evol 9:366–369

    PubMed  CAS  Google Scholar 

  • Heggenes J, Røed KH (2006) Do dams increase genetic diversity in brown trout (Salmo trutta)? Microgeographic differentiation in a fragmented river. Ecol Freshw Fish 15:366–375

    Article  Google Scholar 

  • Heggenes J, Røed KH, Høyheim B, Rosef L (2002) Microsatellite diversity assessment of brown trout (Salmo trutta) population structure indicate limited genetic impact of stocking in a Norwegian alpine lake. Ecol Freshw Fish 11:93–100

    Article  Google Scholar 

  • Heggenes J, Skaala O, Borgstrøm R, Igland OT (2006) Minimal gene flow from introduced brown trout (Salmo trutta L.) after 30 years of stocking. J Appl Ichthyol 22:119–124

    Article  CAS  Google Scholar 

  • Hesthagen T, Floystad L, Hegge O, Staurnes M, Skurdal J (1999) Comparative life-history characteristics of native and hatchery-reared brown trout, Salmo trutta L., in a sub-Alpine reservoir. Fish Manag Ecol 6:47–61

    Article  Google Scholar 

  • Hesthagen T, Johnsen SI, Gran R (2010) Effect of supplementary stocking of juvenile brown trout, Salmo trutta, on yield in a Norwegian mountain reservoir. Fish Manag Ecol 17:186–191

    Article  Google Scholar 

  • Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:945–957

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Huitfeldt-Kaas HH (1911) Indberetning om fiskeriforholdene på Hardangervidden. In: Indstilling fra Fjeldbeitekomiteen om Hardangerviddens utnyttelse (Landbruksdepartementet, ed). Centraltrykkeriet, Kristiania, pp 81–98 (in Norwegian)

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  PubMed  CAS  Google Scholar 

  • Hynes RA, Ferguson A, McCann MA (1996) Variation in mitochondrial DNA and post-glacial colonization of north western Europe by brown trout. J Fish Biol 48:54–67

    Article  CAS  Google Scholar 

  • Indrelid S (1985) De første bosetterne. In: Barth EK (ed) Hardangervidda. Luter Forlag, Oslo, pp 97–111 (in Norwegian)

  • Iwamoto EM, Myers JM, Gustafson RG (2012) Resurrecting an extinct salmon evolutionarily significant unit: archived scales, historical DNA and implications for restoration. Mol Ecol 21:1567–1582

    Article  PubMed  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kohout J, Jašková I, Papoušek I, Šedivá A, Šlechta V (2012) Effects of stocking on the genetic structure of brown trout, Salmo trutta, in Central Europe inferred from mitochondrial and nuclear DNA markers. Fish Manag Ecol 19:252–263

    Article  Google Scholar 

  • Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830

    Article  PubMed  CAS  Google Scholar 

  • Kostow KE (2004) Differences in juvenile phenotypes and survival between hatchery stocks and a natural population provide evidence for modified selection due to captive breeding. Can J Fish Aquat Sci 61:577–589

    Article  Google Scholar 

  • Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158

    Article  Google Scholar 

  • Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res Popul Ecol 40:259–269

    Article  Google Scholar 

  • Lehtonen PK, Tonteri A, Sendek D, Titov S, Primmer CR (2009) Spatio-temporal genetic structuring of brown trout (Salmo trutta L.) populations within the River Luga, northwest Russia. Conserv Genet 10:281–289

    Article  Google Scholar 

  • Letcher BH, Nislow KH, Coombs JA, O’Donnell MJ, Dubreuil TL (2007) Population response to habitat fragmentation in a stream-dwelling brook trout population. PLoS One 2:e1139

    Article  PubMed  Google Scholar 

  • Nesje A, Bakke J, Dahl SO, Lie O, Matthews JA (2008) Norwegian mountain glaciers in the past, present and future. Glob Planet Change 60:10–27

    Article  Google Scholar 

  • Nesje A, Pilø LH, Finstad E, Solli B, Wangen V, Ødegård RS, Isaksen K, Støren EN, Bakke DI, Andreassen LM (2012) The climatic significance of artefacts related to prehistoric reindeer hunting exposed at melting ice patches in southern Norway. Holocene 22:485–496

    Article  Google Scholar 

  • Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461

    Article  Google Scholar 

  • O’Grady MF (1984) Observations on the contribution of planted brown trout (Salmo trutta L.) to spawning stocks in four Irish lakes. Aquac Res 15:117–122

    Article  Google Scholar 

  • O’Reilly PT, Hamilton LC, McConnell SK, Wright JM (1996) Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can J Fish Aquat Sci 53:2292–2298

    Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Eco Notes 6:288–295

  • Poteaux C, Bonhomme F, Berrebi P (1999) Microsatellite polymorphism and genetic impact of restocking in Mediterranean brown trout (Salmo trutta L.). Heredity 82:645–653

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2007) Documentation for structure software: version 2.2. University of Chicago, Chicago, p 36

    Google Scholar 

  • Prodöhl PA, Walker AF, Hynes R, Taggart JB, Ferguson A (1997) Genetically monomorphic brown trout (Salmo trutta L) populations, as revealed by mitochondrial DNA, multilocus and single-locus minisatellite (VNTR) analyses. Heredity 79:208–213

    Article  Google Scholar 

  • Qvenild T (2004) Hardangervidda: fiske og fjelliv. Naturforlaget, Oslo (in Norwegian)

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rexroad CE, Coleman RL, Hershberger WK, Killefer J (2002) Rapid communication: thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. J Anim Sci 80:541–542

    PubMed  CAS  Google Scholar 

  • Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198

    Article  PubMed  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (2008) GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Sekse T (1971) Jakt og fiske på Hardangerviddi. In: Kolltveit O (ed) Odda, Ullensvang og Kinsarvik i gamal og ny tid. Boktrykk L/L, Bergen, pp 153–163 (in Norwegian)

  • Sønstebø JH, Borgstrøm R, Heun M (2008a) Genetic structure in alpine brown trout Salmo trutta L. shows that indirect stocking affects native lake populations. J Fish Biol 72:1990–2001

    Article  Google Scholar 

  • Sønstebø JH, Borgstrøm R, Heun M (2008b) High genetic introgression in alpine brown trout (Salmo trutta L.) populations from Hardangervidda Norway. Ecol Freshw Fish 17:174–183

    Article  Google Scholar 

  • Swatdipong A, Vasemägi A, Niva T, Koljonen ML, Primmer CR (2010) High level of population genetic structuring in lake-run brown trout, Salmo trutta, of the Inari Basin, northern Finland. J Fish Biol 77:2048–2071

    Article  PubMed  CAS  Google Scholar 

  • Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399

    PubMed  CAS  Google Scholar 

  • Taylor EB, Stamford MD, Baxter JS (2003) Population subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications. Mol Ecol 12:2609–2622

    Article  PubMed  CAS  Google Scholar 

  • Thompson PD, Rahel FJ (1998) Evaluation of artificial barriers in small Rocky Mountain streams for preventing the upstream movement of brook trout. North Am J Fish Manag 18:206–210

    Article  Google Scholar 

  • Tysse Å, Garnås E (1996) Status og strategi for kultivering av ferskvassfisk i Buskerud. Fylkesmannen i Buskerud, Miljøavdelingen. Report nr. 5, Drammen (in Norwegian)

  • Van Houdt JKJ, Pinceel J, Flamand MC, Briquet M, Dupont E, Volckaert FAM, Baret PV (2005) Migration barriers protect indigenous brown trout (Salmo trutta) populations from introgression with stocked hatchery fish. Conserv Genet 6:175–191

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Weiss S, Schmutz S (1999) Performance of hatchery-reared brown trout and their effects on wild fish in two small Austrian streams. Trans Am Fish Soc 128:302–316

    Article  Google Scholar 

  • Whiteley A, Hastings K, Wenburg J, Frissell C, Martin J, Allendorf F (2010) Genetic variation and effective population size in isolated populations of coastal cutthroat trout. Conserv Genet 11:1929–1943

    Article  Google Scholar 

  • Wofford JEB, Gresswell RE, Banks MA (2005) Influence of barriers to movement on within-watershed genetic variation of coastal cutthroat trout. Ecol Appl 15:628–637

    Article  Google Scholar 

  • Yamamoto S, Morita K, Koizumi I, Maekawa K (2004) Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial–temporal changes in gene frequencies. Conserv Genet 5:529–538

    Article  CAS  Google Scholar 

  • Young ND, Tanksley SD (1989) Restriction fragment length polymorphism maps and the concept of graphical genotypes. Theor Appl Genet 77:95–101

    Article  Google Scholar 

Download references

Acknowledgments

John Gunner Dokk, Markus Sydenham, and Carsten Thaulow Pedersen assisted during field sampling. We thank Arne Bu and Olaf Bu for supplying samples from Nordvatn, Sylfest Laingen for samples from Nordmannslågen, and Odd Terje Sandlund for providing the historical scale samples. We furthermore acknowledge Gunnar Elnan in Eidfjord mountain board, Nils Runar Sporan and Henning Syvertsen in Statkraft, Sverre Tveiten, former at Norwegian directorate for nature management, for information regarding the stocking history, Thrond Haugen for comments on an earlier version of this manuscript, and Marie Davey for improving the English. We are also grateful to two anonymous reviewers whose comments considerably improved the manuscript. Financial support was given by Department of Ecology and Natural Resource Management (INA), Norwegian University of Life Science (UMB) and Statkraft. An unchangeable file containing all data and analyses is stored at UMB.

Author information

Authors and Affiliations

  1. Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, 1432, Ås, Norway

    Jens Thaulow, Reidar Borgstrøm & Manfred Heun

Authors
  1. Jens Thaulow
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reidar Borgstrøm
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Manfred Heun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manfred Heun.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thaulow, J., Borgstrøm, R. & Heun, M. Brown trout population structure highly affected by multiple stocking and river diversion in a high mountain national park. Conserv Genet 14, 145–158 (2013). https://doi.org/10.1007/s10592-012-0438-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-012-0438-7

Keywords

Search

Navigation