Conservation Genetics

, Volume 14, Issue 1, pp 145–158 | Cite as

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

  • Jens Thaulow
  • Reidar Borgstrøm
  • Manfred HeunEmail author
Research Article


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.


Microsatellites Brown trout Salmo trutta River diversion Stocking Genetic differentiation 



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.

Supplementary material

10592_2012_438_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 14 kb)


  1. Amos W, Harwood J (1998) Factors affecting levels of genetic diversity in natural populations. Philos Trans Roy Soc B 353:177–186CrossRefGoogle Scholar
  2. 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)Google Scholar
  3. 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 63:549–556PubMedCrossRefGoogle Scholar
  4. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  5. 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 14:375–384CrossRefGoogle Scholar
  6. 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 9:2175–2178PubMedCrossRefGoogle Scholar
  7. Carlsson J, Nilsson J (2000) Population genetic structure of brown trout (Salmo Trutta L.) within a northern boreal forest stream. Hereditas 132:173–181PubMedCrossRefGoogle Scholar
  8. 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 130:36–45CrossRefGoogle Scholar
  9. 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 55:1290–1303CrossRefGoogle Scholar
  10. Cavalli-Sforza Ll, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570CrossRefGoogle Scholar
  11. Christie MR, Marine ML, French RA, Blouin MS (2012) Genetic adaptation to captivity can occur in a single generation. PNAS 103:238–242CrossRefGoogle Scholar
  12. Cook N, Rahel FJ, Hubert WA (2010) Persistence of Colorado River cutthroat trout populations in isolated headwater streams of Wyoming. Trans Am Fish Soc 139:1500–1510CrossRefGoogle Scholar
  13. Dieringer D, Schlotterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  14. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449PubMedCrossRefGoogle Scholar
  15. 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 71:488–496PubMedCrossRefGoogle Scholar
  16. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  17. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  18. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package), version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, WashingtonGoogle Scholar
  19. 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 95:235–249CrossRefGoogle Scholar
  20. García-Marín JL, Sanz N, Pla C (1998) Proportions of native and introduced brown trout in adjacent fished and unfished Spanish rivers. Conserv Biol 12:313–319CrossRefGoogle Scholar
  21. 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 172:2405–2419PubMedCrossRefGoogle Scholar
  22. 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 19–34Google Scholar
  23. 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:e43129PubMedCrossRefGoogle Scholar
  24. Gosset C, Rives J, Labonne J (2006) Effect of habitat fragmentation on spawning migration of brown trout (Salmo trutta L.). Ecol Freshw Fish 15:247–254CrossRefGoogle Scholar
  25. 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 2:537–554CrossRefGoogle Scholar
  26. 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 11:1003–1015PubMedCrossRefGoogle Scholar
  27. 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 43:669–679CrossRefGoogle Scholar
  28. 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 18:2549–2562PubMedCrossRefGoogle Scholar
  29. Hedges SB (1992) The number of replications needed for accurate estimation of the bootstrap p value in phylogenetic studies. Mol Biol Evol 9:366–369PubMedGoogle Scholar
  30. Heggenes J, Røed KH (2006) Do dams increase genetic diversity in brown trout (Salmo trutta)? Microgeographic differentiation in a fragmented river. Ecol Freshw Fish 15:366–375CrossRefGoogle Scholar
  31. 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 11:93–100CrossRefGoogle Scholar
  32. 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 22:119–124CrossRefGoogle Scholar
  33. 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 6:47–61CrossRefGoogle Scholar
  34. 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 17:186–191CrossRefGoogle Scholar
  35. Hindar K, Ryman N, Utter F (1991) Genetic effects of cultured fish on natural fish populations. Can J Fish Aquat Sci 48:945–957CrossRefGoogle Scholar
  36. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  37. 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)Google Scholar
  38. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267PubMedCrossRefGoogle Scholar
  39. 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 48:54–67CrossRefGoogle Scholar
  40. Indrelid S (1985) De første bosetterne. In: Barth EK (ed) Hardangervidda. Luter Forlag, Oslo, pp 97–111 (in Norwegian)Google Scholar
  41. Iwamoto EM, Myers JM, Gustafson RG (2012) Resurrecting an extinct salmon evolutionarily significant unit: archived scales, historical DNA and implications for restoration. Mol Ecol 21:1567–1582PubMedCrossRefGoogle Scholar
  42. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  43. 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 19:252–263CrossRefGoogle Scholar
  44. Koskinen MT, Haugen TO, Primmer CR (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830PubMedCrossRefGoogle Scholar
  45. 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 61:577–589CrossRefGoogle Scholar
  46. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  47. Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res Popul Ecol 40:259–269CrossRefGoogle Scholar
  48. 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 10:281–289CrossRefGoogle Scholar
  49. 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:e1139PubMedCrossRefGoogle Scholar
  50. Nesje A, Bakke J, Dahl SO, Lie O, Matthews JA (2008) Norwegian mountain glaciers in the past, present and future. Glob Planet Change 60:10–27CrossRefGoogle Scholar
  51. 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 22:485–496CrossRefGoogle Scholar
  52. Nielsen EE, Hansen MM (2008) Waking the dead: the value of population genetic analyses of historical samples. Fish Fish 9:450–461CrossRefGoogle Scholar
  53. O’Grady MF (1984) Observations on the contribution of planted brown trout (Salmo trutta L.) to spawning stocks in four Irish lakes. Aquac Res 15:117–122CrossRefGoogle Scholar
  54. 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 53:2292–2298Google Scholar
  55. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Eco Notes 6:288–295Google Scholar
  56. Poteaux C, Bonhomme F, Berrebi P (1999) Microsatellite polymorphism and genetic impact of restocking in Mediterranean brown trout (Salmo trutta L.). Heredity 82:645–653PubMedCrossRefGoogle Scholar
  57. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  58. Pritchard JK, Wen X, Falush D (2007) Documentation for structure software: version 2.2. University of Chicago, Chicago, p 36Google Scholar
  59. 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 79:208–213CrossRefGoogle Scholar
  60. Qvenild T (2004) Hardangervidda: fiske og fjelliv. Naturforlaget, Oslo (in Norwegian)Google Scholar
  61. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  62. Rexroad CE, Coleman RL, Hershberger WK, Killefer J (2002) Rapid communication: thirty-eight polymorphic microsatellite markers for mapping in rainbow trout. J Anim Sci 80:541–542PubMedGoogle Scholar
  63. Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198PubMedCrossRefGoogle Scholar
  64. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  65. Rousset F (2008) GENEPOP ‘007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  66. 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)Google Scholar
  67. 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 72:1990–2001CrossRefGoogle Scholar
  68. Sønstebø JH, Borgstrøm R, Heun M (2008b) High genetic introgression in alpine brown trout (Salmo trutta L.) populations from Hardangervidda Norway. Ecol Freshw Fish 17:174–183CrossRefGoogle Scholar
  69. 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 77:2048–2071PubMedCrossRefGoogle Scholar
  70. Takezaki N, Nei M (1996) Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144:389–399PubMedGoogle Scholar
  71. 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 12:2609–2622PubMedCrossRefGoogle Scholar
  72. 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 18:206–210CrossRefGoogle Scholar
  73. Tysse Å, Garnås E (1996) Status og strategi for kultivering av ferskvassfisk i Buskerud. Fylkesmannen i Buskerud, Miljøavdelingen. Report nr. 5, Drammen (in Norwegian)Google Scholar
  74. 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 6:175–191CrossRefGoogle Scholar
  75. 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 4:535–538CrossRefGoogle Scholar
  76. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  77. 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 128:302–316CrossRefGoogle Scholar
  78. 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 11:1929–1943CrossRefGoogle Scholar
  79. Wofford JEB, Gresswell RE, Banks MA (2005) Influence of barriers to movement on within-watershed genetic variation of coastal cutthroat trout. Ecol Appl 15:628–637CrossRefGoogle Scholar
  80. 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 5:529–538CrossRefGoogle Scholar
  81. Young ND, Tanksley SD (1989) Restriction fragment length polymorphism maps and the concept of graphical genotypes. Theor Appl Genet 77:95–101CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Department of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway

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