Biological Invasions

, Volume 18, Issue 7, pp 2029–2044 | Cite as

Alien brown trout invasion of the Italian peninsula: the role of geological, climate and anthropogenic factors

  • A. Splendiani
  • P. Ruggeri
  • M. Giovannotti
  • S. Pesaresi
  • G. Occhipinti
  • T. Fioravanti
  • M. Lorenzoni
  • P. Nisi Cerioni
  • V. Caputo BarucchiEmail author
Original Paper


Environmental, climate and historical factors are important to explain patterns of freshwater biodiversity and population dynamics in the Mediterranean area. This region is one of the most important areas for the maintenance of native lineages for brown trout. The aim of this study was the identification of the main drivers for the spread and the distribution of genetic introgression between alien brown trout and two native Mediterranean salmonids (brown and marble trout). Estimates of mitochondrial and nuclear introgression were from both the literature and original data and were used as dependent variables in a multivariate framework, correlating them to a suite of environmental and climate parameters. The last glacial maximum appeared as an important factor explaining the geographic pattern of alien brown trout genes throughout the Alps. Here, native populations of Mediterranean salmonids persisted in former refugia. Throughout the Italian Peninsula and major islands, geological setting of catchment and current climate conditions are key factors for securing the persistence of native trout populations. The reevaluation of genetic data regarding the spread of alien brown trout lineage into Mediterranean salmonids populations with a landscape approach allowed us to reveal the role of important factors implicated with the current pattern of distribution of remnant native populations of salmonids. This information provides new insights for improving conservation strategies and management of taxa threatened by the incipient global climate changes.


Landscape genetics Introgression Last glacial maximum Salmonids Mediterranean trout Marble trout Multivariate statistics 



The authors wish to thank some local anglers for their assistance in specimen collection (Alfeo Busilacchio, Luca Ercoli, Luigi Evangelisti, Lucio Santoni, Adriano Togni and Mauro Zavaldi). We are also grateful to Lucio Lucadamo and Ezio Basso for providing us with specimens from Calabria and Sesia River, respectively. We also thank Valerio Ketmaier for his valuable suggestions. Finally, we wish to thank Gianandrea La Porta for his helpful comments during the revision of the manuscript. This research was supported by funds from Università Politecnica delle Marche (Ancona, Italy).

Supplementary material

10530_2016_1149_MOESM1_ESM.docx (56 kb)
Supplementary material 1 (DOCX 55 kb)


  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622CrossRefGoogle Scholar
  2. Almodóvar A, Nicola GG, Elvira B, García-Marín JL (2006) Introgression variability among Iberian brown trout evolutionary significant units: the influence of local management and environmental features. Freshw Biol 51:1175–1187CrossRefGoogle Scholar
  3. Almodóvar A, Nicola GG, Ayllón D, Elvira B (2011) Global warming threatens the persistence of Mediterranean brown trout. Glob Change Biol 18:1549–1560CrossRefGoogle Scholar
  4. Arlinghaus R (2006) Understanding recreational angling participation in Germany: preparing for demographic change. Hum Dimens Wildl 11:1–12CrossRefGoogle Scholar
  5. Arlinghaus R, Tillner R, Bork M (2015) Explaining participation rates in recreational fishing across industrialised countries. Fisher Manag Ecol 22:45–55CrossRefGoogle Scholar
  6. Baratti M, Nonnis Marzano F, Fratini S et al (2006) Caratterizzazione genetica delle popolazioni di Trota fario del Parco delle Foreste Casentinesi. Biol Ambient 1:237–240Google Scholar
  7. Baxter CV, Frissell CA, Hauer FR (1999) Geomorphology, logging roads, and the distribution of bull trout spawning in a forested river basin: implications for management and conservation. Trans Am Fish Soc 128:854-867CrossRefGoogle Scholar
  8. 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 55:351–379CrossRefPubMedGoogle Scholar
  9. Bernatchez L, Wilson CC (1998) Comparative phylogeography of nearctic and palearctic freshwater fishes. Mol Ecol 7:431–452CrossRefGoogle Scholar
  10. Bianco PG (2013) An update on the status of native and exotic freshwater fishes of Italy. J Appl Icht 30:62–77CrossRefGoogle Scholar
  11. Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055CrossRefGoogle Scholar
  12. Borroni I (2005) Indagine genetica sulle trote del torrente Tanarello e sulle trote “mediterranee” di provenienza commerciale seminate in provincia di Imperia. In: Indagini di approfondimento della carta ittica della Provincia di Imperia bacini del Tanarello e dell’Arroscia. Provincia d’Imperia, CDGoogle Scholar
  13. Brook DB (2008) Sinergies between climate change, extinctions and invasive vertebrates. Wildl Res 35:249–252CrossRefGoogle Scholar
  14. Budy P, Thiede GP, Lobón-Cerviá J, Gonzalez Fernandez G, McHugh P, McIntosh A, Vøllestad LA, Becares E, Jellyman P (2013) Limitation and facilitation of one of the world’s most invasive fish: an intercontinental comparison. Ecology 94(2):356–367CrossRefPubMedGoogle Scholar
  15. Carr SC, Robertson KM, Platt WJ, Peet RK (2009) A model of geographic, environmental and regional variation in vegetation composition of pyrogenic grasslands of Florida. J Biogeogr 36:1600–1612CrossRefGoogle Scholar
  16. Cataudella S, Bronzi P (2001) Acquacoltura responsabile, verso le produzioni acquatiche del terzo millennio. (Eds Unimar—Uniprom) 2001, RomaGoogle Scholar
  17. Clavero M, Hermoso V, Kark S, Levin N (2010) Geographical linkages between threats and imperilment in freshwater fish in the Mediterranean Basin. Divers Distrib 16:744–754CrossRefGoogle Scholar
  18. DeHaan PW, Schwabe LT, Ardren WR (2010) Spatial patterns of hybridization between bull trout, Salvelinus confluentus, and brook trout, Salvelinus fontinalis, in an Oregon stream network. Conserv Genet 11(3):935–949CrossRefGoogle Scholar
  19. Della Croce P, Pool GC, Payn RA, Izurieta V (2014) Simulating the effects of stream network topology on the spread of introgressive hybridization across fish populations. Ecol Model 279:68–77CrossRefGoogle Scholar
  20. Dudgeon D, Arthington AH, Gessner MO et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182CrossRefPubMedGoogle Scholar
  21. Dwyer WP, Piper RG (1984) Three-year hatchery and field evaluation of four strains of rainbow trout. North Am J Fish Manag 10:458–461CrossRefGoogle Scholar
  22. Evans DO, Willox CC (1991) Loss of exploited, indigenous populations of lake trout, Salvelinus namaycush, by stocking of non-native stocks. Can J Fish Aquat Sci 48(S1):134–147CrossRefGoogle Scholar
  23. Ferguson A (2007) Genetic impacts of stocking on indigenous brown trout populations. Environment Agency Science Report SC040071/SR, Bristol, 93 pp. ISBN 978-1-84432-798-0Google Scholar
  24. Filipe F, Markovic D, Pletterbauer F et al (2013) Forecasting fish distribution along stream networks: brown trout (Salmo trutta) in Europe. Divers Distrib 19:1059–1071CrossRefGoogle Scholar
  25. Forneris G, Lucarda A (2006) Caratteristiche genetiche delle popolazioni di trote in Valle d’Aosta. Progetto Interreg IIIA Rapport final, CAP. IIGoogle Scholar
  26. Fruciano C, Pappalardo AM, Tigano C, Ferrito V (2014) Phylogeographical relationships of Sicilian brown trout and the effects of genetic introgression on morphospace occupation. Biol J Linn Soc 112:387–398CrossRefGoogle Scholar
  27. García-Marín JL, Sanz N, Pla C (1999) Erosion of the native genetic resources of brown trout in Spain. Ecol Freshw Fish 8:151–158CrossRefGoogle Scholar
  28. Gibertoni PP, Penserini M (2010) Studi ittiologici, caratterizzazione genetica, selezione di parco riproduttori e produzione di novellame autoctono per le acque di Lunigiana (MS) e media valle Serchio (LU). Fish Sci J 0:10–17Google Scholar
  29. Giuffra E, Bematchez L, Guyomard R (1994) Mitochondria1 control region and protein coding genes sequence variation among phenotypic forms of brown trout Salmo trutta from northern Italy. Mol Ecol 3:161–171CrossRefPubMedGoogle Scholar
  30. Giuffra E, Guyomard R, Forneris G (1996) Phylogenetic relationships and introgression patterns between incipient parapatric species of Italian brown trout (Salmo trutta L. complex). Mol Ecol 5:207–220CrossRefGoogle Scholar
  31. Goode JR, Buffington JM, Tonina D et al (2013) Potential effects of climate change on streambed scour and risks to salmonid survival in snow-dominated mountain basins. Hydrol Process 27:750–765CrossRefGoogle Scholar
  32. Gratton P, Allegrucci G, Gandolfi A, Sbordoni V (2013) Genetic differentiation and hybridization in two naturally occurring sympatric trout Salmo spp. forms from a small karstic lake. J Fish Biol 82:637–657CrossRefPubMedGoogle Scholar
  33. Gratton P, Allegrucci G, Sbordoni V, Gandolfi A (2014) The evolutionary jigsaw puzzle of the surviving trout (Salmo trutta L. complex) diversity in the Italian region. A multilocus Bayesian approach. Mol Phylogenet Evol 97:292–304CrossRefGoogle Scholar
  34. Halbisen MA, Wilson CC (2009) Variable introgression from supplemental stocking in Southern Ontario populations of lake trout. Trans Am Fish Soc 138(4):699–719CrossRefGoogle Scholar
  35. 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 11:1003–1015CrossRefPubMedGoogle Scholar
  36. Hansen MM, Loeschcke V (1996) Genetic differentiation among Danish brown trout populations, as detected by RFLP analysis of PCR amplified mitochondrial DNA segments. J Fish Biol 48:422–436Google Scholar
  37. Hansen MM, Ruzzante DE, Nielsen EE, Mensberg KLD (2000) Microsatellite and mitochondrial DNA polypmorphism reveals life-history dependent interbreeding between hatchery and wild brown trout (Salmo trutta L.). Mol Ecol 9:583–594CrossRefPubMedGoogle Scholar
  38. Harbicht AB, Alshamlih M, Wilson CC, Fraser DJ (2014) Anthropogenic and habitat correlates of hybridization between hatchery and wild brook trout. Can J Fish Aquat Sci 71:688–697CrossRefGoogle Scholar
  39. Heggenes J, Roed K, Hoyheim 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
  40. Hewitt GM (1996) Some genetic consequences of ice ages. Biol J Linn Soc 58:247–276CrossRefGoogle Scholar
  41. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  42. Hitt NP, Frissell CA, Muhlfeld CC, Allendorf FW (2003) Spread of hybridization between native westslope cutthroat trout, Oncorhynchus clarki lewisi, and nonnative rainbow trout, Oncorhynchus mykiss. Can J Fish Aquat Sci 60:1440–1451CrossRefGoogle Scholar
  43. Horton RE (1945) Erosional development of streams and their drainage basins, hydrophysical approach to quantitative morphology. Geol Soc Am Bull 56:275–370CrossRefGoogle Scholar
  44. Jonsson B, Jonsson N (2011) Ecology of Atlantic salmon and brown trout: habitat as a template for life histories. Fish Fish Ser 33:680Google Scholar
  45. Ketmaier V, Bianco PG (2004) Monitoraggio genetico e ibridazione tra popolazioni atlantiche e mediterranee di Salmo trutta in Abruzzo e Campania. In: Casagrandi R, Melià P (eds) Ecologia. Atti del XIII Congresso Nazionale della Società Italiana di Ecologia (Como, 8–10 settembre 2003). Aracne, Roma. Full paper available online
  46. Kottelat M, Freyhof J (2007) Handbook of European freshwater fishes. Publications Kottelat, CornolGoogle Scholar
  47. Largiadèr CR, Scholl A (1995) Effect of stocking on the genetic diversity of brown trout populations of the Adriatic and Danubian drainages in Switzerland. J Fish Biol 47(Suppl A):209–225CrossRefGoogle Scholar
  48. Lelek A, Bushe G (1992) Fische des Rheins: früher und heute. Springer, Berlin, pp 164–165CrossRefGoogle Scholar
  49. Lucentini L, Palomba A, Gigliarelli L et al (2006) Genetic characterization of a putative indigenous brown trout (Salmo trutta fario) population in a secondary stream of the Nera River Basin (Central Italy) assessed by means of three molecular markers. Ital J Zool 73:263–273CrossRefGoogle Scholar
  50. Madeira MJ, Gómez-Moliner BJ, Barbé AM (2005) Genetic introgression on freshwater fish populations caused by restocking programmes. Biol Invasions 7:117–125CrossRefGoogle Scholar
  51. Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28:614–621CrossRefPubMedGoogle Scholar
  52. Marie AD, Bernatchez L, Garant D (2012) Environmental factors correlate with hybridization in stocked brook charr (Salvelinus fontinalis). Can J Fish Aquat Sci 69:1–10CrossRefGoogle Scholar
  53. Marr SM, Olden JD, Leprieu F et al (2013) A global assessment of freshwater fish introductions in Mediterranean-climate regions. Hydrobiologia 719:317–329CrossRefGoogle Scholar
  54. McMeel OM, Hoey EM, Ferguson A (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. Mol Ecol 10:29–34CrossRefPubMedGoogle Scholar
  55. Meraner A, Baric S, Pelster B, Dalla Via J (2007) Trout (Salmo trutta) mitochondrial DNA polymorphism in the centre of the marble trout distribution area. Hydrobiologia 579:337–349CrossRefGoogle Scholar
  56. Meraner A, Baric S, Pelster B, Dalla Via J (2010) Microsatellite DNA data point to extensive but incomplete admixture in a marble and brown trout hybridisation zone. Conserv Genet 11:985–998CrossRefGoogle Scholar
  57. Meraner A, Gratton P, Baraldi F, Gandolfi A (2013) Nothing but a trace left? Autochthony and conservation status of Northern Adriatic Salmo trutta inferred from PCR multiplexing, mtDNA control region sequencing and microsatellite analysis. Hydrobiologia 702:201–213CrossRefGoogle Scholar
  58. Mezzera M, Largiadèr CR (2001) Evidence for selective angling of introduced trout and their hybrids in a stocked brown trout population. J Fish Biol 59:287–301CrossRefGoogle Scholar
  59. Miró A, Ventura M (2013) Historical use, fishing management and lake characteristics explain the presence of non-native trout in Pyrenean lakes: Implications for conservation. Biol Conserv 167:17–24CrossRefGoogle Scholar
  60. Muhlfeld CC, McMahon TE, Boyer MC, Gresswell RE (2009) Local habitat, watershed, and biotic factors influencing the spread of hybridization between native westslope cutthroat trout and introduced rainbow trout. Trans Am Fish Soc 138:1036–1051CrossRefGoogle Scholar
  61. Muhlfeld CC, Kovach RP, Jones LA et al (2014) Invasive hybridization in a threatened species is accelerated by climate change. Nat Clim Change 4:620–624CrossRefGoogle Scholar
  62. Nimis PL, Bolognini G (1993) Quantitative phytogeography of the Italian beech forest. Vegetation 109:125–143CrossRefGoogle Scholar
  63. Nonnis Marzano F, Corradi N, Papa R, Tagliavini J, Gandolfi G (2003) Molecular evidence for introgression and loss of genetic variability in Salmo (trutta) macrostigma as a result of massive restocking of Appenine populations (Northern and Central Italy). Environ Biol Fish 68:349–356CrossRefGoogle Scholar
  64. Olden JD, Kennard MJ, Leprieur F et al (2010) Conservation biogeography of freshwater fishes: recent progress and future challenges. Divers Distrib 16:496–513CrossRefGoogle Scholar
  65. Poteaux C, Bonhomme F, Berrebi P (1999) Microsatellite polymorphism and genetic impact of restocking in Mediterranean brown trout (Salmo trutta L.). Heredity 82:645–653CrossRefPubMedGoogle Scholar
  66. Ricciardi A, Rasmussen JB (1999) Extinction rates of North American freshwater fauna. Conserv Biol 13:1220–1222CrossRefGoogle Scholar
  67. Rubidge EM, Taylor EB (2005) An analysis of spatial and environmental factors influencing hybridization between native westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow trout (O. mykiss) in the upper Kootenay River drainage, British Columbia. Conserv Genet 6:369–384CrossRefGoogle Scholar
  68. Sabatini A, Cannas R, Follesa MC et al (2011) Genetic characterization and artificial reproduction attempt of endemic Sardinian trout Salmo trutta L., 1758 (Osteichthyes, Salmonidae): experience in captivity. Ital J Zool 78:20–26CrossRefGoogle Scholar
  69. Schöffmann J, Sušnik S, Snoj A (2007) Phyloghenetic origin of Salmo trutta L. 1758 from Sicily, based on mitochondrial and nuclear DNA analyses. Hydrobiologia 575:51–55CrossRefGoogle Scholar
  70. Schorr G, Holstein N, Pearman PB, Guisan A, Kadereit JW (2012) Integrating species distribution models (SDMs) and phylogeography for two species of Alpine Primula. Ecol Evol 2:160–1277CrossRefGoogle Scholar
  71. Shenekar T, Lercerteau-Köhler E, Weiss S (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. Conserv Genet 15:561–572CrossRefGoogle Scholar
  72. Simberloff D (1996) Hybridization between native and introduced wildlife species: importance for conservation. Wildl Biol 2:143–150Google Scholar
  73. Snoj A, Marić S, Bajec SS et al (2011) Phylogeographic structure and demographic patterns of brown trout in North-West Africa. Mol Phylogenet Evol 61:203–211CrossRefPubMedGoogle Scholar
  74. Splendiani A, Ruggeri P, Giovannotti M, Caputo Barucchi V (2013) Role of environmental factors in the spread of domestic trout in Mediterranean streams. Freshw Biol 58:2089–2101CrossRefGoogle Scholar
  75. Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Amer Geophys Union 38:913-920CrossRefGoogle Scholar
  76. ter Braak CJF (1995) Ordination. In: Jongman RHJ, ter Braak CJF, van Tongeren OFR (eds) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge, pp 91–173CrossRefGoogle Scholar
  77. ter Braak CJF, Smilauer P (1998) Canoco Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination Version 4.0. Microcomputer Power, Ithaca, New YorkGoogle Scholar
  78. Tribsch A, Schonswetter P (2003) Patterns of endemism and comparative phylogeography confirm palaeoenvironmental evidence for Pleistocene refugia in the Eastern Alps. Taxon 52:477–497CrossRefGoogle Scholar
  79. Utter F (2001) Patterns of subspecific anthropogenic introgression in two salmonid genera. Rev Fish Biol Fish 10:265–279CrossRefGoogle Scholar
  80. Vicentini C, Pizzul E, Battistella S (2006) Analisi del polimorfismo genetico e uso di marcatori molecolari per la gestione di Salmo [trutta] trutta (Linnaeus, 1758) nel Friuli Venezia Giulia. Biol Ambient 20:205–210Google Scholar
  81. Yau MM, Taylor BT (2013) Environmental and anthropogenic correlates of hybridization between westslope cutthroat trout (Oncorhynchus clarkii lewisi) and introduced rainbow trout (O. mykiss). Conserv Genet 14:885–900CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • A. Splendiani
    • 1
  • P. Ruggeri
    • 1
  • M. Giovannotti
    • 1
  • S. Pesaresi
    • 2
  • G. Occhipinti
    • 1
  • T. Fioravanti
    • 1
  • M. Lorenzoni
    • 3
  • P. Nisi Cerioni
    • 1
  • V. Caputo Barucchi
    • 1
    Email author
  1. 1.Dipartimento di Scienze della Vita e dell’Ambiente (DiSVA)Università Politecnica delle MarcheAnconaItaly
  2. 2.Dipartimento di Scienze Agrarie, Alimentari e Ambientali (D3A)Università Politecnica delle MarcheAnconaItaly
  3. 3.Dipartimento di Chimica, Biologia e BiotecnologieUniversità di PerugiaPerugiaItaly

Personalised recommendations