Skip to main content

Advertisement

Log in

Identification of an endemic Mediterranean brown trout mtDNA group within a highly perturbed aquatic system, the Llobregat River (NE Spain)

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Brown trout (Salmo trutta L.) is an important resource both for conservation and recreational fisheries in Iberian Peninsula, but the species is threatened in Llobregat River, an important river drainage in Catalonia (NE Spain), due to the high anthropological influence. In order to ascertain the native genetic diversity, phylogenetic relationships, population structure and stocking impact in this drainage, 295 individuals collected from eight different locations distributed throughout the main river course and the main tributary (i.e. Llobregat River and Cardener River, respectively) were analysed for the period 1990–2017. The complete mitochondrial DNA (mtDNA) control region and the LDH-C* diagnostic locus for monitoring the stocking were analysed. Moderate-high levels of genetic introgression were detected (frequency ~ 0.300), affecting especially the main course. Despite the stocking introgression and the expected genetic depletion by genetic drift due to population isolation, a new mtDNA haplotype group pertaining to the Mediterranean lineage was found restricted to the Cardener River. This haplogroup is responsible of the high population differentiation observed between rivers in the Llobregat drainage (ΦCT = 0.456, P < 0.001) and highlights the conservation interest of that region. Management strategies to achieve fisheries sustainability and conserve endemic resources in the region are proposed.

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

Similar content being viewed by others

References

  • ACA, 2017. Connectivitat longitudinal als rius de les Conques Internes de Catalunya. Estructures presents als rius i actuacions de millora realitzades. Agència Catalana de l’Aigua, Departament de Territori i Sostenibilitat, Generalitat de Catalunya, Barcelona.

  • Allendorf, F. W., R. F. Leary, N. P. Hitt, K. L. Knudsen, L. L. Lundquist & P. Spruell, 2004. Intercrosses and the US Endangered Species Act: should hybridized populations be included as Westslope cutthroat trout? Conservation Biology 18: 1203–1213.

    Article  Google Scholar 

  • Almodovar, A., G. G. Nicola, B. Elvira & J. L. García-Marín, 2006. Introgression variability among Iberian brown trout Evolutionary Significant Units: the influence of local management and environmental features. Freshwater Biology 51: 1175–1187.

    Article  Google Scholar 

  • Almodovar, A., G. G. Nicola, D. Ayllon & B. Elvira, 2012. Global warming threatens the persistence of Mediterranean brown trout. Global Change Biology 18: 1549–1560.

    Article  Google Scholar 

  • Aparicio, E., E. Garcia-Berthou, R. M. Araguas, P. Martinez & J. L. García-Marín, 2005. Body pigmentation pattern to assess introgression by hatchery stocks in native Salmo trutta from Mediterranean streams. Journal of Fish Biology 67: 931–949.

    Article  Google Scholar 

  • Araguas, R. M., N. Sanz, R. Fernandez, F. M. Utter, C. Pla & J. L. García-Marín, 2008. Genetic refuges for a self-sustained fishery: experience in wild brown trout populations in the eastern Pyrenees. Ecology of Freshwater Fish 17: 610–616.

    Article  Google Scholar 

  • Araguas, R. M., N. Sanz, R. Fernandez-Cebrian, F. M. Utter, C. Pla & J. L. García-Marín, 2009. Role of genetic refuges in the restoration of native gene pools of brown trout. Conservation Biology 23: 871–878.

    Article  Google Scholar 

  • Araguas, R. M., M. Vera, E. Aparicio, N. Sanz, R. Fernandez-Cebrian, C. Marchante & J. L. García-Marín, 2017. Current status of the brown trout (Salmo trutta) populations within eastern Pyrenees genetic refuges. Ecology of Freshwater Fish 26: 120–132.

    Article  Google Scholar 

  • Arthington, A. H., N. K. Dulvy, W. Gladstone & I. J. Winfield, 2016. Fish conservation in freshwater and marine realms: status, threats and management. Aquatic Conservation: Marine and Freshwater Ecosystems 26: 838–857.

    Article  Google Scholar 

  • Bandelt, H. J., P. Forster & A. Rohl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  Google Scholar 

  • Bernas, R., A. Burzynski, P. Debowski, A. Pocwierz-Kotus & R. Wenne, 2014. Genetic diversity within sea trout population from an intensively stocked southern Baltic river, based on microsatellite DNA analysis. Fisheries Management and Ecology 21: 398–409.

    Article  Google Scholar 

  • Bernatchez, L., 2001. The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 55: 351–379.

    Article  CAS  Google Scholar 

  • Berrebi, P., D. Jesenek & A. Crivelli, 2017. Natural and domestic introgressions in the marble trout population of Soa River (Slovenia). Hydrobiologia 785: 277–291.

    Article  Google Scholar 

  • Bouza, C., R. Vilas, J. Castro & P. Martínez, 2008. Mitochondrial haplotype variability of brown trout populations from Northwestern Iberian Peninsula, a secondary contact area between lineages. Conservation Genetics 9: 917–920.

    Article  Google Scholar 

  • Cortey, M. & J. L. García-Marín, 2002. Evidence for phylogeographically informative sequence variation in the mitochondrial control region of Atlantic brown trout. Journal of Fish Biology 60: 1058–1063.

    Article  CAS  Google Scholar 

  • Cortey, M., C. Pla & J. L. García-Marín, 2004. Historical biogeography of Mediterranean trout. Molecular Phylogenetics and Evolution 33: 831–844.

    Article  Google Scholar 

  • Cortey, M., M. Vera, C. Pla & J. L. García-Marín, 2009. Northern and Southern expansions of Atlantic brown trout (Salmo trutta) populations during the Pleistocene. Biological Journal of the Linnean Society 97: 904–917.

    Article  Google Scholar 

  • Dahl-Jensen, D., M. R. Albert, A. Aldahan, N. Azuma, D. Balslev-Clausen, M. Baumgartner, A. M. Berggren, M. Bigler, T. Binder, T. Blunier, J. C. Bourgeois, E. J. Brook, S. L. Buchardt, C. Buizert, E. Capron, J. Chappellaz, J. Chung, H. B. Clausen, I. Cvijanovic, S. M. Davies, P. Ditlevsen, O. Eicher, H. Fischer, D. A. Fisher, L. G. Fleet, G. Gfeller, V. Gkinis, S. Gogineni, K. Goto-Azuma, A. Grinsted, H. Gudlaugsdottir, M. Guillevic, S. B. Hansen, M. Hansson, M. Hirabayashi, S. Hong, S. D. Hur, P. Huybrechts, C. S. Hvidberg, Y. Iizuka, T. Jenk, S. J. Johnsen, T. R. Jones, J. Jouzel, N. B. Karlsson, K. Kawamura, K. Keegan, E. Kettner, S. Kipfstuhl, H. A. Kjaer, M. Koutnik, T. Kuramoto, P. Koehler, T. Laepple, A. Landais, P. L. Langen, L. B. Larsen, D. Leuenberger, M. Leuenberger, C. Leuschen, J. Li, V. Lipenkov, P. Martinerie, O. J. Maselli, V. Masson-Delmotte, J. R. McConnell, H. Miller, O. Mini, A. Miyamoto, M. Montagnat-Rentier, R. Mulvaney, R. Muscheler, A. J. Orsi, J. Paden, C. Panton, F. Pattyn, J. R. Petit, K. Pol, T. Popp, G. Possnert, F. Prie, M. Prokopiou, A. Quiquet, S. O. Rasmussen, D. Raynaud, J. Ren, C. Reutenauer, C. Ritz, T. Rockmann, J. L. Rosen, M. Rubino, O. Rybak, D. Samyn, C. J. Sapart, A. Schilt, A. M. Z. Schmidt, J. Schwander, S. Schuepbach, I. Seierstad, J. P. Severinghaus, et al., 2013. Eemian interglacial reconstructed from a Greenland folded ice core. Nature 493: 489–494.

    Article  CAS  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fabiani, A., P. Gratton, I. A. Zappes, M. Seminara, A. D’Orsi, V. Sbordoni & G. Allegrucci, 2018. Investigating the genetic structure of trout from the Garden of Ninfa (central Italy): suggestions for conservation and management. Fisheries Management and Ecology 25: 1–11.

    Article  Google Scholar 

  • Fernandez-Cebrian, R., R. M. Araguas, N. Sanz & J. L. García-Marín, 2014. Genetic risks of supplementing trout populations with native stocks: a simulation case study from current Pyrenean populations. Canadian Journal of Fisheries and Aquatic Sciences 71: 1243–1255.

    Article  Google Scholar 

  • Frankham, R., J. D. Ballou & D. A. Briscoe, 2002. Introduction to conservation genetics. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Fumagalli, L., A. Snoj, D. Jesensek, F. Balloux, T. Jug, O. Duron, F. Brossier, A. J. Crivelli & P. Berrebi, 2002. Extreme genetic differentiation among the remnant populations of marble trout (Salmo marmoratus) in Slovenia. Molecular Ecology 11: 2711–2716.

    Article  CAS  Google Scholar 

  • García-Marín, J. L., P. E. Jorde, N. Ryman, F. Utter & C. Pla, 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, J. L., R. M. Araguas, M. Vera & N. Sanz, 2017. Understanding the brown trout population genetic structure in the Iberian Peninsula. In Lobón-Cerviá, J. & N. Sanz (eds), Brown Trout: biology, ecology and management. Wiley, Chichester: 103–126.

    Chapter  Google Scholar 

  • Gonzalez, S., R. Lopez-Roldan & J. L. Cortina, 2012. Presence and biological effects of emerging contaminants in Llobregat River basin: a review. Environmental Pollution 161: 83–92.

    Article  CAS  Google Scholar 

  • Hansen, M. M., D. Bekkevold, L. F. Jensen, K. L. D. Mensberg & E. E. Nielsen, 2006. Genetic restoration of a stocked brown trout Salmo trutta population using microsatellite DNA analysis of historical and contemporary samples. Journal of Applied Ecology 43: 669–679.

    Article  CAS  Google Scholar 

  • Hansen, M. M., D. J. Fraser, K. Meier & K. L. D. Mensberg, 2009. Sixty years of anthropogenic pressure: a spatio-temporal genetic analysis of brown trout populations subject to stocking and population declines. Molecular Ecology 18: 2549–2562.

    Article  CAS  Google Scholar 

  • Jadan, M., I. Strunjak-Perovic, N. Topic-Popovic & R. Coz-Rakovac, 2015. Three major phylogenetic lineages of brown trout (Salmo trutta Linnaeus, 1758) in the Krka River system (Croatia) revealed by complete mitochondrial DNA control region sequencing. Journal of Applied Ichthyology 31: 192–196.

    Article  CAS  Google Scholar 

  • Kohout, J., I. Jaskova, I. Papousek, A. Sediva & V. Slechta, 2012. Effects of stocking on the genetic structure of brown trout, Salmo trutta, in Central Europe inferred from mitochondrial and nuclear DNA markers. Fisheries Management and Ecology 19: 252–263.

    Article  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    Article  CAS  Google Scholar 

  • Marce, R., J. Honey-Roses, A. Manzano, L. Moragas, B. Catllar & S. Sabater, 2012. The Llobregat River basin: a paradigm of impaired rivers under climate change threats. The Handbook of Environmental Chemistry 21: 1–26.

    Article  Google Scholar 

  • Maric, S., O. Askeyev, A. Askeyev, S. Monakhov, N. Yanybaev, I. Askeyev, D. Galimova & A. Snoj, 2016. Lack of mtDNA variation among remote middle Volga and upper Ural brown trout suggests recent and rapid recolonization. Journal of Applied Ichthyology 32: 948–953.

    Article  Google Scholar 

  • Maric, S., S. S. Bajec, J. Schoffmann, V. Kostov & A. Snoj, 2017. Phylogeography of stream-dwelling trout in the Republic of Macedonia and a molecular genetic basis for revision of the taxonomy proposed by S. Karaman. Hydrobiologia 785: 249–260.

    Article  CAS  Google Scholar 

  • McDermid, J. L., S. Nienhuis, M. Al-Shamlih, T. J. Haxton & C. C. Wilson, 2014. Evaluating the genetic consequences of river fragmentation in lake sturgeon (Acipenser fulvescens Rafinesque, 1817) populations. Journal of Applied Ichthyology 30: 1514–1523.

    Article  Google Scholar 

  • McMeel, O. M., E. M. Hoey & A. Ferguson, 2001. Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1*90 and*100 alleles. Molecular Ecology 10: 29–34.

    Article  CAS  Google Scholar 

  • Meraner, A., S. Baric, B. Pelster & J. Dalla Via, 2007. Trout (Salmo trutta) mitochondrial DNA polymorphism in the centre of the marble trout distribution area. Hydrobiologia 579: 337–349.

    Article  CAS  Google Scholar 

  • Moore, W. S., 1995. Inferring phylogenies from mtDNA variation mitochondrial-gene trees versus nuclear-gene trees. Evolution 49: 718–726.

    PubMed  Google Scholar 

  • Muñoz, M. & M. Casadevall, 1997. Fish remains from Arbreda Cave (Serinyà Girona), northeast Spain, and their palaeoecological significance. Journal of Quaternary Science 12: 111–115.

    Article  Google Scholar 

  • Nei, M. & F. Tajima, 1981. DNA polymorphism detectable by restriction endonucleases. Genetics 97: 145–163.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nonnis Marzano, F., N. Corradi, R. Papa, J. Tagliavini, F. N. Marzano & G. Gandolfi, 2003. Molecular evidence for introgression and loss of genetic variability in Salmo (trutta) macrostigma as a result of massive restocking of Apennine populations (Northern and Central Italy). Environmental Biology of Fishes 68: 349–356.

    Article  Google Scholar 

  • Ormerod, S. J., 2009. Climate change, river conservation and the adaptation challenge. Aquatic Conservation: Marine and Freshwater Ecosystems 19: 609–613.

    Article  Google Scholar 

  • Pfenninger, M. & D. Posada, 2002. Phylogeographic history of the land snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution 56: 1776–1788.

    Article  Google Scholar 

  • Prat, N. & M. Rieradevall, 2006. 25-years of biomonitoring in two Mediterranean streams (Llobregat and Besòs basins, NE Spain). Limnetica 25: 541–550.

    Google Scholar 

  • Rasmussen, G., 1986. The population dynamics of brown trout (Salmo trutta L.) in relation to year-class size. Polskie Archiwum Hydrobiologii 33: 489–508.

    Google Scholar 

  • Rousset, F., 2008. GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources 8: 103–106.

    Article  Google Scholar 

  • Ryman, N., F. Utter & L. Laikre, 1995. Protection of intraspecific biodiversity of exploited fishes. Reviews in Fish Biology and Fisheries 5: 417–446.

    Article  Google Scholar 

  • Sambrook, J., E. F. Fritsch & T. Maniatis, 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  • Sanz, N., J. L. García-Marín & C. Pla, 2002. Managing fish populations under mosaic relationships. The case of brown trout (Salmo trutta) in peripheral Mediterranean populations. Conservation Genetics 3: 385–400.

    Article  Google Scholar 

  • Sanz, N., M. Cortey, C. Pla & J. L. García-Marín, 2006. Hatchery introgression blurs ancient hybridization between brown trout (Salmo trutta) lineages as indicated by complementary allozymes and mtDNA markers. Biological Conservation 130: 278–289.

    Article  Google Scholar 

  • Saura, M. & R. Faria, 2011. Genetic tools for restoration of fish populations. Journal of Applied Ichthyology 27: 5–15.

    Article  Google Scholar 

  • Schenekar, T., E. Lerceteau-Koehler & S. Weiss, 2014. Fine-scale phylogeographic contact zone in Austrian brown trout Salmo trutta reveals multiple waves of post-glacial colonization and a pre-dominance of natural versus anthropogenic admixture. Conservation Genetics 15: 561–572.

    Article  Google Scholar 

  • Snoj, A., I. Bogut & S. Susnik, 2008. Evidence of a genetically distinct population of Vrljika softmouth trout Salmo obtusirostris Heckel evolved by vicariance. Journal of Fish Biology 72: 1945–1959.

    Article  Google Scholar 

  • Soler, A., A. Canals, S. L. Goldstein, N. Otero, N. Antich & J. Spangenberg, 2002. Sulfur and strontium isotope composition of the Llobregat river (NE Spain): tracers of natural and anthropogenic chemicals in streams waters. Water, Air, and Soil Pollution 136: 207–224.

    Article  CAS  Google Scholar 

  • Sonstebo, J. H., R. Borgstrom & M. Heun, 2008. High genetic introgression in alpine brown trout (Salmo trutta L.) populations from Hardangervidda, Norway. Ecology of Freshwater Fish 17: 174–183.

    Article  Google Scholar 

  • Sostoa, A., N. M. Caiola, F. Casals, E. Garcia-Berthou, C. Alcaraz, L. Benejam, A. Maceda, C. Solà & A. Munné, 2010. Ajust de l’Index d’Integritat Biològica (IBICAT) basat en l’ús dels peixos com a indicadors de la qualitat ambiental als rius de Catalunya. Agència Catalana de l’Aigua, Departament de Medi Ambient i Habitatge, Generalitat de Catalunya, Barcelona.

    Google Scholar 

  • Splendiani, A., M. Giovannotti, P. N. Cerioni, M. L. Caniglia & V. Caputo, 2006. Phylogeographic inferences on the native brown trout mtDNA variation in central Italy. Italian Journal of Zoology 73: 179–189.

    Article  CAS  Google Scholar 

  • Splendiani, A., P. Ruggeri, M. Giovannotti & V. Caputo, 2013. Role of environmental factors in the spread of domestic trout in Mediterranean streams. Freshwater Biology 58: 2089–2101.

    Article  Google Scholar 

  • Splendiani, A., P. Ruggeri, M. Giovannotti, S. Pesaresi, G. Occhipinti, T. Fioravanti, M. Lorenzoni, P. Nisi Cerioni & V. Caputo Barucchi, 2016. Alien brown trout invasion of the Italian peninsula: the role of geological, climate and anthropogenic factors. Biological Invasions 18: 2029–2044.

    Article  Google Scholar 

  • Suarez, J., J. M. Bautista, A. Almodovar & A. Machordom, 2001. Evolution of the mitochondrial control region in Palaearctic brown trout (Salmo trutta) populations: the biogeographical role of the Iberian Peninsula. Heredity 87: 198–206.

    Article  CAS  Google Scholar 

  • Susnik, S., J. Schoffmann & S. Weiss, 2005. Genetic verification of native brown trout from the Persian Gulf (Catak Cay River, Tigris basin). Journal of Fish Biology 67: 879–884.

    Article  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    CAS  PubMed  Google Scholar 

  • Trigo, R. M., D. Pozo-Vazquez, T. J. Osborn, Y. Castro-Diez, S. Gamiz-Fortis & M. J. Esteban-Parra, 2004. North Atlantic oscillation influence on precipitation, river flow and water resources in the Iberian Peninsula. International Journal of Climatology 24: 925–944.

    Article  Google Scholar 

  • Vera, M., M. Cortey, N. Sanz & J. L. García-Marín, 2010. Maintenance of an endemic lineage of brown trout (Salmo trutta) within the Duero river basin. Journal of Zoological Systematics and Evolutionary Research 48: 181–187.

    Article  Google Scholar 

  • Vera, M., J. L. García-Marín, P. Martínez, R. M. Araguas & C. Bouza, 2013. Identification and conservation of remnant genetic resources of brown trout in relict populations from Western Mediterranean streams. Hydrobiologia 707: 29–45.

    Article  CAS  Google Scholar 

  • Vera, M., J. L. García-Marín, P. Martínez & C. Bouza, 2015. Phylogenetic diversity within the endemic brown trout Duero lineage: implications for conservation and management. Marine and Freshwater Research 66: 1066–1071.

    Article  Google Scholar 

  • Vera, M., P. Martínez & C. Bouza, 2018. Stocking impact, population structure and conservation of wild brown trout populations in inner Galicia (NW Spain), an unstable hydrologic region. Aquatic Conservation: Marine and Freshwater Ecosystems 28: 435–443.

    Article  Google Scholar 

  • Walsh, P. S., D. A. Metzger & R. Higuchi, 1991. CHELEX-100 as a medium for simple extraction of dna for pcr-based typing from forensic material. Biotechniques 10: 506–513.

    CAS  PubMed  Google Scholar 

  • Weiss, S. & S. Schmutz, 1999. Performance of hatchery-reared brown trout and their effects on wild fish in two small Austrian streams. Transactions of the American Fisheries Society 128: 302–316.

    Article  Google Scholar 

  • WWF, 2016. Living Planet Report 2016. Risk and resilience in a new era. WWF International, Gland.

    Google Scholar 

Download references

Acknowledgements

Authors wish to thank M. López, S. Sánchez-Darriba and S. Gómez for their laboratory support; E. Aparicio for his fieldwork; and J. Ruiz, C. Marchante and J. Capdevila from the Inland Fisheries Service of the Generalitat de Catalunya Autonomous Government (Spain) for their technical advice. Authors are also indebted with Prof. M. Power and two anonymous reviewers for their constructive comments on the earlier version of this manuscript. A. Casanova was funded by a predoctoral reasearch fellowship from Xunta de Galicia Autonomous Government (Spain). This study has been supported by Spanish Science and Technology Ministry projects (REN2000-0740-C02-01; REN2003-05931/GLO), University of Girona project (MPCUdG2016/060), Generalitat de Catalunya (Spain) contracts (AMB/acs/itt 2001-3; AG-2017-617) and Xunta de Galicia project (GRC2014/010).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Vera.

Additional information

Handling editor: Michael Power

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vera, M., Bouza, C., Casanova, A. et al. Identification of an endemic Mediterranean brown trout mtDNA group within a highly perturbed aquatic system, the Llobregat River (NE Spain). Hydrobiologia 827, 277–291 (2019). https://doi.org/10.1007/s10750-018-3775-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-018-3775-9

Keywords

Navigation