Skip to main content
Log in

Population genetic structure after 125 years of stocking in sea trout (Salmo trutta L.)

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

Abstract

Stocking can be an effective management and conservation tool, but it also carries the danger of eroding natural population structure, introducing non-native strains and reducing genetic diversity. Sea trout, the anadromous form of the brown trout (Salmo trutta), is a highly targeted species that is often managed by stocking. Here, we assess the present-day population genetic structure of sea trout in a backdrop of 125 years of stocking in Northern Germany. The study area is characterized by short distances between the Baltic and North Sea river watersheds, historic use of fish from both watersheds for stocking, and the creation of a potential migration corridor between the Baltic and North Sea with the opening of the Kiel Canal 120 years ago. A survey of 24 river systems with 180 SNPs indicates that moderate but highly significant population genetic structure has persisted both within and between the Baltic and North Sea. This genetic structure is characterized by (i) heterogeneous patterns of admixture between the Baltic and North Sea that do not correlate with distance from the Kiel Canal and are therefore likely due to historic stocking practises, (ii) genetic isolation by distance in the Baltic Sea at a spatial scale of < 200 km that is consistent with the homing behaviour of sea trout, and (iii) at least one genetically distinct Baltic Sea river system. In light of these results, we recommend keeping fish of North Sea and Baltic Sea origin separate for stocking, and restricting Baltic Sea translocations to neighbouring river systems.

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
Fig. 5

Similar content being viewed by others

References

  • Aprahamian MW, Smith KM, McGinnity P, McKelvey S, Taylor J (2003) Restocking of salmonids—opportunities and limitations. Fish Res 62:211–227

    Article  Google Scholar 

  • Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1(2):342–355

    Article  PubMed  PubMed Central  Google Scholar 

  • Bell JD, Leber KM, Blankenship HL, Loneragan NR, Masuda R (2008) A new era for restocking, stock enhancement and sea ranching of coastal fisheries resources. Rev Fish Sci 16:1–9

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Berg OK, Berg M (1987) Migrations of sea trout, Salmo trutta L., from the Vardnes river in northern Norway. J Fish Biol 31(1):113–121

    Article  Google Scholar 

  • Butler JAR, Radford A, Riddington G, Laughton R (2009) Evaluating an ecosystem service provided by Atlantic salmon, sea trout and other fish species in the river Spey, Scotland: the economic impact of recreational rod fisheries. Fish Res 96(2–3):259–266

    Article  Google Scholar 

  • Cowx IG (1994) Stocking strategies. Fish Manage Ecol 1:15–30

    Article  Google Scholar 

  • Cowx IG (1998) Stocking and introduction of fish. Fishing News Books, Blackwell Science, Oxford

    Google Scholar 

  • Degerman E, Leonardsson K, Lundqvist H (2012) Coastal migrations, temporary use of neighboring rivers, and growth of sea trout (Salmo trutta) from nine northern Baltic Sea rivers. ICES J Mar Sci 69:971–980

    Article  Google Scholar 

  • DiCiccio TJ, Efron B (1996) Bootstrap confidence intervals. Stat Sci 11:189–228

    Article  Google Scholar 

  • Dierking J, Phelps L, Praebel K, Ramm G, Borcherding J, Brunke M, Eizaguirre C (2014) Anthropogenic hybridization between endangered migratory and commercially harvested stationary whitefish taxa (Coregonus ssp.). Evol Appl 7(9):1068–1083. https://doi.org/10.1111/eva.12166

    Article  PubMed  PubMed Central  Google Scholar 

  • Drywa A, Poćwierz-Kotus A, Wąs A, Dobosz S, Kent MP, Lien S, Bernaś R, Wenne R (2013) Genotyping of two populations of southern Baltic Sea trout Salmo trutta m. trutta using an Atlantic salmon derived SNP-array. Mar Genom 9:25–32

    Article  Google Scholar 

  • Earl DA, vonHoldt BM (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 

  • Elliot JM (1989) Wild brown trout Salmo trutta: an important national and international resource. Freshw Biol 21:1–5

    Article  Google Scholar 

  • Elsner B (1884) Bericht des Fischzüchters Elsner an den Vorstand des Central-Fischerei-Vereins für Schleswig Holstein. 7. Jahresbericht des Central-Fischerei-Vereins für Schleswig-Holstein. Verlag W. Böhl, Rendsburg, S. 25–42 (in German)

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Forseth T, Barlaup BT, Finstad B, Fiske P, Gjøsæter H, Falkegård M, Hindar A, Mo TA, Rikardsen AH, Thorstad EB, Vøllestad LA, Wennevik V (2017) The major threats to Atlantic salmon in Norway. ICES J Mar Sci. https://doi.org/10.1093/icesjms/fsx020

    Article  Google Scholar 

  • Frazer DJ (2008) How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol Appl 1(4):535–586

    Google Scholar 

  • Galil BS, Marchini A, Occipinti-Ambrogi A, Minchin D, Narščius A, Ojaveer H, Olenin S (2014) International arrivals: widespread bioinvasions in European Seas. Ethol Ecol Evol 26(2–3):152–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(8):e43129. https://doi.org/10.1371/journal.pone.0043129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gollasch S, Rosenthal H (2006) The Kiel Canal: the world’s busiest man-made waterway and biological invasions. In: Gollasch S, Galil BS, Cohen A (eds) Bridging divides: Maritime Canals as invasion corridors. Springer, Dordrecht, pp 5–90

    Chapter  Google Scholar 

  • Grant WS, Jasper J, Bekkevold D, Adkinson M (2017) Responsible genetic approach to stock restoration, sea ranching and stock enhancement of marine fishes and invertebrates. Rev Fish Biol Fisher 27(3):615–649

    Article  Google Scholar 

  • Hall CJ, Jordaan A, Frisk MG (2012) Centuries of anadromous forage fish loss: consequences for ecosystem connectivity and productivity. Bioscience 62(8):723–731

    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  CAS  PubMed  Google Scholar 

  • Hansen MM, Mensberg K-LD (1998) Genetic differentiation and relationship between genetic and geographical distance in Danish sea trout (Salmo trutta L.) populations. Heredity 81:493–504

    Article  Google Scholar 

  • Hansen MM, Nielsen EE, Ruzzante DE, Bouza C, Mensberg K-LD (2000) Genetic monitoring of supportive breeding in brown trout (Salmo trutta L.) using microsatellite DNA markers. Can J Fish Aquat Sci 57:2130–2139

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harris G (2017) Sea trout: science and management. Troubador Publishing Ltd. ISBN: 9781788035354

  • Harris GS, Millner NJ (2006) Sea trout: biology, conservation and management. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Hartmann U (1996) Zur Meerforelle (Salmo trutta L.) in Schleswig-Holstein. In: Verband Deutscher Sportfischer (ed) Die Meerforelle—Fisch des Jahres 1996, pp 76–104 (in German)

  • Hemmer-Hansen J, Nielsen EE, Grønkjaer P, Loeschke V (2007) Evolutionary mechanisms shaping the genetic population structure of marine fishes: lessons from the European flounder (Platichthys flesus L.). Mol Ecol 16:3104–3118

    Article  CAS  PubMed  Google Scholar 

  • Hess MA, Rabe CD, Vogel JL, Stephenson JJ, Nelson DD, Narum SR (2012) Supportive breeding boosts natural population abundance with minimal negative impacts on fitness of a wild population of Chinook salmon. Mol Ecol 21(21):5236–5250

    Article  PubMed  PubMed Central  Google Scholar 

  • ICES (2017) Report of the Baltic Salmon and Trout Assessment Working Group (WGBAST). 27. March-April 4th 2017, Gdansk Poland. ICES CM 2017/ACOM:10. p 298

  • Jakobsson M, Rosenberg NA (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 

  • Johannesson K, André C (2006) Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea. Mol Ecol 15:2013–2029

    Article  CAS  PubMed  Google Scholar 

  • Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555

    Article  PubMed  Google Scholar 

  • Kallio-Nyberg I, Veneranta L, Saloniemi I, Jutila E, Pakarinen T (2017) Spatial distribution of migratory Salmo trutta in the northern Baltic Sea. Boreal Environ Res 22:431–444

    Google Scholar 

  • Klemetsen A, Amundsen PA, Dempson JB, Jonsson B, Jonsson N, O´Connell MF, Mortensen E (2003) Atlantic Salmon (Salmo salar L.), brown trout (Salmo trutta L.) and Arctic charr (Salvelinus alpinus L.): a review of aspects of their life histories. Ecol Freshw Fish 12:1–59

    Article  Google Scholar 

  • Lassen H (1914) Die Salmonidenfischerei an unserer schleswig-holsteinischen Ostseeküste. In: 37. Jahresbericht des Central-Fischerei-Vereins für Schleswig-Holstein, 1913-1914, Verlag DJ, Carstens, Rendsburg, pp 173–192 (in German)

  • 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(2):281–289

    Article  Google Scholar 

  • Leitwein M, Gagnaire P-A, Desmarais E, Guendouz S, Rohmer M, Berrebi P, Guinand B (2016) Genome-wide nucleotide diversity of hatchery-reared Atlantic and Mediterranean strains of brown trout Salmo trutta compared to wild Mediterranean populations. J Fish Biol 89(6):2717–2734

    Article  CAS  PubMed  Google Scholar 

  • Limborg MT, Helyar SJ, de Bruyn M, Taylor MI, Nielsen EE, Ogden R, Carvalho GR, Consortium FPT, Bekkevold D (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol 21:3686–3703

    Article  CAS  PubMed  Google Scholar 

  • Limburg KE, Waldman JR (2009) Dramatic declines in Northern Atlantic diadromous fishes. Bioscience 59(11):955–965

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Can Res 27:209–220

    CAS  Google Scholar 

  • Mota M, Rochard E, Antunes C (2017) Status of the diadromous fish of the Iberian Peninsula: past, present and trends. Limnetica 35(1):1–18

    Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Nielsen EE, Hansen MM, Ruzzante DE, Meldrup D, Grønkjaer P (2003) Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Mol Ecol 12(6):1497–1508

    Article  PubMed  Google Scholar 

  • Nilsson J, Gross R, Asplund T, Dove O, Jansson H, Kelloniemi J, Kohlmann K, Löytynoja A, Nielsen EE, Paaver T, Primmer CR, Titov S, Vasemägi A, Veselov A, Ost T, Lumme J (2001) Matrilinear phylogeography of Atlantic salmon (Salmo salar L.) in Europe and postglacial colonization of the Baltic Sea. Mol Ecol 10(1):89–102

    Article  CAS  PubMed  Google Scholar 

  • Östergren J, Nilsson J, Lundquist H, Dannewitz J, Palm S (2016) Genetic baseline for conservation and management of sea trout in the northern Baltic Sea. Conserv Genet 17:177–191

    Article  Google Scholar 

  • Petereit C, Reusch THB, Dierking J, Hahn A (2013) Literaturrecherche, Aus- und Bewertung der Datenbasis zur Meerforelle (Salmo trutta trutta L.): Grundlage für ein Projekt zur Optimierung des Meerforellenmanagements in Schleswig-Holstein. GEOMAR Report N. Ser. 010. p 158. https://doi.org/10.3289/GEOMAR_REP_NS_10_2013. http://oceanrep.geomar.de/21919/

  • Piccolo JJ (2016) Conservation genomics: coming to a salmonid near you. J Fish Biol 89(6):2735–2740

    Article  CAS  PubMed  Google Scholar 

  • Poćwierz-Kotus A, Bernaś R, Dębowski P, Kent MP, Lien S, Kesler M, Titov S, Leliūna E, Jespersen H, Drywa A, Wenne R (2014) Genetic differentiation of southeast Baltic populations of sea trout inferred from single nucleotide polymorphisms. Anim Genet 45(1):96–104

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    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 (1997) Genetic differentiation and estimation of gene low from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  PubMed Central  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 

  • Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329

    Article  Google Scholar 

  • Ryman N, Ståhl G (1980) Genetic changes in hatchery stocks of brown trout (Salmo trutta). Can J Fish Aquat Sci 37:82–87

    Article  Google Scholar 

  • Samarasin P, Shuter BJ, Rodd FH (2017) After 100 years: hydroelectric dam-induced life-history divergence and population genetic changes in sockeye salmon (Oncorhynchus nerka). Conserv Genet 18(6):1449–1462

    Article  Google Scholar 

  • Samuiloviene A, Kontautas A, Gross R (2009) Genetic diversity and differentiation of sea trout (Salmo trutta) populations in Lithuanian rivers assessed by microsatellite DNA variation. Fish Physiol Biochem 35:649–659. https://doi.org/10.1007/s10695-009-9310-1

    Article  CAS  PubMed  Google Scholar 

  • Schindler DE, Hilborn R, Chasco B, Boatright CP, Quinn TP, Rogers LA, Webster MS (2010) Population diversity and the portfolio effect in an exploited species. Nature 465:609–612

    Article  CAS  PubMed  Google Scholar 

  • Schonevelde S (1624) Ichthyologia et nomenclaturae animalium marinorum, fluviatilium, lacustrium, quae in florentissimis ducatibus Slesvigi et Holsatiae & celeberrimo Emporio Hamburgo occurent triviales. Bibliopolis Heringianus, p 87 (in Latin)

  • Shirvell CS, Dungey RG (1983) Microhabitats chosen by brown trout for feeding and spawning in rivers. Trans Am Fish Soc 112:355–367

    Article  Google Scholar 

  • Sjöqvist C, Godhe A, Jonsson PR, Sundqvist L, Kremp A (2015) Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea-Baltic Sea salinity gradient. Mol Ecol 24(11):2871–2885

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith SA, Bell G, Bermingham E (2014) Cross-Cordillera exchange mediated by the Panama Canal increased the species richness of local freshwater fish assemblages. Proc R Soc B 271:1889–1896

    Article  Google Scholar 

  • Sparrevohn CR, Storr-Paulsen M (2012) Eel, cod and seatrout harvest in Danish recreational fishing during 2011. DTU Aqua Report No. 253-2012 Charlottenlund. National Institute of Aquatic Resources, Technical University of Denmark, p 20

  • Taylor MD, Chick RC, Lorenzen K, Agnalt A-L, Leber KM, Blankenship HL, Haegen GV, Loneragan NR (eds) (2017) Fisheries enhancement. Fish Res 186(Part 2):407–598

  • Thaulow J, Borgstrøm R, Heun M (2013) Brown trout population structure highly affected by multiple stocking and river diversion in a high mountain national park. Conserv Genet 14(1):145–158

    Article  Google Scholar 

  • Thaulow J, Borgstrøm R, Heun M (2014) Genetic persistence of an initially introduced brown trout (Salmo trutta L.) population despite restocking of foreign conspecifics. Ecol Freshw Fish 23:485–497

    Article  Google Scholar 

  • Thorstadt EB, Økland F, Aarestrup K, Heggberget TG (2008) Factors affecting the within-river spawning migration of Atlantic salmon, with emphasis on human impacts. Rev Fish Biol Fisher 18(4):345–371

    Article  Google Scholar 

  • Wąs A, Bernaś R (2016) Long-term and seasonal genetic differentiation in wild and enhanced stocks of the sea trout (Salmo trutta f. trutta L.) from the Vistula River, in the southern Baltic—management implications. Fish Res 175:57–65

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wenne R, Bernaś R, Poćwierz-Kotus A, Drywa A, Wąs A (2016) Recent genetic changes in enhanced populations of sea trout (Salmo trutta m. trutta) in the Southern Baltic rivers revealed with SNP analysis. Aquat Living Resour 29:103

    Article  CAS  Google Scholar 

Download references

Acknowledgements

CP was funded by the Federal-Fishing Fund “Fischereiabgabe” of Schleswig-Holstein, the European Fisheries Fund (EFF) and GEOMAR through the Ministry of Energy, Agriculture, the Environment and Rural Areas of Schleswig-Holstein in the frame of the projects “Sea Trout Literature Study, ParrQuant, VariParr & SMARRT (30/SH305E)”. We thank all people involved in the electrofishing campaigns conducted for tissue sampling, especially Tim Kuchenbecker, Jens Wein, Sebastian Albrecht, Enno Prigge and the staff of the Fish Hatchery Altmühlendorf. We also acknowledge the respective local Water and Soil Organizations for permissions and access to their rivers and the Angling Clubs for their help during field samplings.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christoph Petereit.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petereit, C., Bekkevold, D., Nickel, S. et al. Population genetic structure after 125 years of stocking in sea trout (Salmo trutta L.). Conserv Genet 19, 1123–1136 (2018). https://doi.org/10.1007/s10592-018-1083-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-018-1083-6

Keywords

Navigation