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Keywords:

  • AFLP ;
  • hitch-hiking;
  • illegal spread;
  • introduced species;
  • stocking

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

European minnow Phoxinus phoxinus (L.) from four different water bodies (the lakes Eivindbuvatn and Grungevatn, and the hydroelectric reservoirs Ståvatn and Totak) in the upper part of the Tokke drainage system, outside the native range of this species, and from one possible source population (River Hunnselva), were analysed to identify the origin of a newly established population in Ståvatn Reservoir. Amplified fragment length polymorphism analyses identified three genetically different populations in the Tokke drainage system, well separated from the purported source population. Thus, the River Hunnselva population connected to a brown trout, Salmo trutta L., hatchery from which European minnow theoretically could have ‘hitchhiked’ was not the source. As such, the dispersal of European minnow in Norway, even in a restricted area within one drainage system, appears to occur from multiple sources and possibly involves the illegal use of the species as live bait.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The increased spread of invasive fish species has been related to human activity (Copp et al. 2005; LaRue et al. 2011), often in conjunction with commercial and recreational purposes (Ogutu-Ohwayo & Hecky 1991; Litvak & Mandrak 1993; Jackson 2002). The negative effects of introducing freshwater fish to an ecosystem may include increased predation (Witte et al. 1992), habitat degradation (Cudmore & Mandrak 2004), increased competition for resources (Baxter et al. 2004, 2007), hybridization (Allendorf & Leary 1988; Hansen et al. 2001), change of food web composition (Næstad & Brittain 2010), and disease and parasite transmission (Stewart 1991; Gozlan et al. 2005). Unintentional and intentional releases of fish species are second only to habitat destruction as a major cause for the degradation of freshwater biodiversity. In Norway, about one-fourth of all freshwater fish species are introduced (Hesthagen & Sandlund 2007), and new non-native species are still being recorded. In addition, extensive spread of both translocated native and exotic species occurs (Hesthagen & Sandlund 2007).

Norway is a major producer of hydroelectric power, which satisfies 98.5% of the country's power demands (IEA 2010). The majority of the hydroelectric reservoirs is found in mountain areas where brown trout, Salmo trutta L., was often the only fish species present. Damming and water level fluctuations in the reservoirs have negative effects on brown trout recruitment (Huitfeldt-Kaas 1935), and hatchery brown trout have therefore been stocked annually since the early 1900s to compensate recruitment losses (Vøllestad & Hesthagen 2001). In this context, much attention has been directed towards the extensive spread of European minnow, Phoxinus phoxinus (L.), as a contaminant, or hitchhiker, of hatchery brown trout stocking consignments (Hesthagen & Sandlund 2004).

The European minnow is native to the south-eastern and northern parts of Norway (Huitfeldt-Kaas 1918). However, it is presently found in all counties (Hesthagen & Sandlund 2007; Museth et al. 2007), having undergone considerable dispersal during the past hundred years. Controlling the spread of European minnow in Norway is of great concern, given the ecological impact of its introduction to new water bodies. The establishment of European minnow in high mountain lakes is reported to affect brown trout recruitment and production, mainly due to competition for food between the two species (Hesthagen et al. 1992; Museth et al. 2007, 2010), and by changing the composition of the benthic fauna (Brittain et al. 1988; Næstad & Brittain 2010). Inability to stop the spread of European minnow in Norway, despite it being regarded as a pest, makes it important to address the question of how the species continues to spread (Museth et al. 2007). One of the largest Norwegian hatchery companies has been accused of spreading European minnow with its brown trout stocking, due to its proximity to, and use of, water from a river within the natural distribution of European minnow. An expert review of the routines employed at this hatchery (conducted without DNA analyses) concluded it was unlikely that European minnow spread has been facilitated by the company, especially since the 1970s (Eie 2003). Application of DNA markers makes it possible to identify the genetic relationship between populations (Campbell et al. 2003; Sønstebø et al. 2007) and the origin of single individuals (Nielsen et al. 2001). Consequently, the aim of this study was to identify the origin of a newly established population of European minnow in the high mountain reservoir, Ståvatn (western Norway), to determine whether the founder population emanates from within the same hydrosystem or from a more distant water course that supplies water to a brown trout hatchery used to stock high mountain lakes and reservoirs.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

European minnows were sampled by electric fishing in the littoral zone of four water bodies in the Tokke drainage system; the high mountain reservoir, Ståvatn (ST), situated nearby the southern border of the Hardangervidda National Park; two downstream lakes, Eivindbuvatn (EI), Grungevatn (GR); and a connected reservoir, Totak (TO), all of which are outside the native range of European minnow (Fig. 1). In addition, sampling was performed in the River Hunnselva (HU) (Fig. 1), which is within the native range of European minnow (Huitfeldt-Kaas 1918). This location served as the water source for a hatchery (Eie 2003) that supplied brown trout consignments for the annual stocking of EI (1959–2000), ST (1961–2005) and TO (1960–2005), until the hatchery ceased operations in 2008. Introduced populations of European minnow have been present in GR (Håstein et al. 1978) and TO (Hesthagen & Sandlund 1997) since at least the 1970s. Forty individuals were collected from each of ST, EI, GR and HU in 2009, and from TO in 2011 (= 6) and 2012 (= 34). After capture, all sampled individuals were immediately killed with a blow to the head, and thereafter, total length was measured to nearest mm. Tissue samples of the collected fish were stored in 96% ethanol until DNA was extracted from 20–25 mg tissue using the EZNA tissue DNA kit (Omega BIO-TEK) according to manufacturer's instructions.

image

Figure 1. Map of southern Norway with geographical position of the European minnow sampling areas (Upper part of Tokke drainage system in Vinje municipality, and River Hunnselva) (top right), with an enlargement of sampling sites in the Tokke drainage system (top left). River Hunnselva is within the natural distribution of European minnow, located approximately 210 km from the other sampling sites. Bottom left, four structure analyses with = 2–5. Bottom right, two PCoAs with dimensions 1 vs. 2 and 1 vs. 3, respectively. The splits A, B and C are shown in both the structure analyses and the PCoAs. Red indicates ST (Ståvatn), yellow GR (Grungevatn), blue EI (Eivindbuvatn), purple TO (Totak) and green HU (Hunnselva).

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AFLP fingerprinting was performed according to Vos et al. (1995). Eight primer combinations (the MseI primers are: CAA, CAC, CAG, CAT, CTA, CTT, CTG and CTT were used in combination with the EcoRI primer TGA) were screened with seven fish (HU fish nr. 05 (HU05), HU06, ST01, ST02, EI01, EI02 and GR01) to select four primer combinations for further analyses. Genotyping of 200 individuals was undertaken with one EcoRI primer (TGA) labelled with γ-33P-ATP, in combination with one of four unlabelled MseI primers (CAC, CAG, CTG and CTT). PCR products were analysed by 5% polyacrylamide gel electrophoresis (PAGE) run at 80 W for 1.5 h. AFLPs were visualised by placing dried gels onto KODAK BioMax MR films for ≈ 48 h. AFLP fragments of identical base length were scored by naked eye as present (1) or absent (0) and arranged in a binary matrix, on which further analyses were performed. Error rate was calculated by regenotyping 16 individuals with the selected four primer combinations.

GenAlex v6.2 (Peakall & Smouse 2006) was used to estimate the number of private AFLPs, and pairwise and overall genetic differentiation (φPT, an analogue to FST), as well as to perform an analysis of molecular variance (amova). The program aflp-surv v1.1 (Vekemans et al. 2002) was used to estimate the number and proportion of polymorphic loci, in addition to calculating pairwise and overall FST values, following Lynch and Milligan (1994) whilst assuming Hardy–Weinberg genotypic proportions and implementing the Bayesian method with non-uniform prior distribution of allele frequencies (Zhivotovsky 1999). Principal coordinate analysis (PCoA) of the 200 individual fish was performed with ntsys v2.2 (Rohlf 2009) after computation of a DICE (Dice 1945) derived genetic distance (similarity minus one gives distance) matrix. structure v2.3.3 (Pritchard et al. 2000; Falush et al. 2003; Hubisz et al. 2009) was used to assign individual fish to K (ranging from 1 to 10) groups with ten iterations each (after 500 000 burn-in iterations and 3 000 000 MCMC repeats) using the recessive alleles model for dominant marker data, assuming admixture and correlated alleles (Falush et al. 2007). The structure analysis was run on the Bioportal at the University of Oslo (Kumar et al. 2009). Individuals were not assigned to populations prior to structure initiation. The number of structure clusters was undertaken as per Falush et al. (2003) and Evanno et al. (2005), in combination with PCoA.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The size distributions of the European minnow samples indicate several cohorts present in each location (Table 1). A total of 178 AFLPs were obtained from the four primer combinations with an estimated error rate of 1.4%. The total number of polymorphic AFLPs was 165, with a range from 132 to 150 (74.2–84.3%) within the individual populations; HU had the highest number, and EI the lowest (Table 1). Three private AFLPs were found for HU compared with the remaining four populations, with frequencies of 50.0, 37.5 and 27.5%, respectively, whereas no private AFLP was observed for the remaining populations. In a pairwise comparison between HU and ST, 42 private AFLPs (26 unique for HU and 16 for ST) were identified, of which five had frequencies above 70%. Three of those were specific for HU and two for ST, giving a criss-cross situation separating these two populations (Table 2).

Table 1. Summary of sampled European minnow populations and genotyping results, given by number (n) and length range of scored individuals, number of AFLPs (#loc. P.) and proportion of polymorphic AFLPs (PLP)
AbbreviationSampling location n Length range (cm)#loc. P.PLP (%)
HURiver Hunnselva402.5–8.215084.3
STReservoir Ståvatn405.3–8.214380.3
EILake Eivindbuvatn403.2–9.313274.2
GRLake Grungevatn404.3–8.214380.3
TOReservoir Totak402.3–11.414581.5
Table 2. Frequency (Freq.) of private AFLPs in a criss-cross comparison between Hunnselva (HU) and Ståvatn (ST). Only population-specific AFLPs with frequencies above 70% are shown
AFLP numberHU Freq.ST Freq.
1287.50
10975.00
8672.50
70097.5
61077.5

The FST values obtained by aflp-surv were slightly lower than the φPT values derived from GenAlEx (Table 3); however, the results from the two different calculation methods are in accordance with each other. Genetic differentiation between ST, EI and GR vs. HU and TO vs. EI showed the highest φPT values; the lowest genetic differentiation was found between ST and GR (Table 3). The observed average genetic differentiation (φPT = 0.254, FST = 0.171) was within the range of reported genetic differentiation for freshwater (FST = 0.222) and anadromous fishes (FST = 0.108) (Ward et al. 1994). Also, the amova indicated that 26% of genetic variation occurred at the between-population level.

Table 3. Pairwise φPT (below diagonal) and FST values (above diagonal) for the five sampled European minnow populations
 HUSTEIGRTO
  1. HU, Hunnselva; ST, Ståvatn; EI, Eivindbuvatn; GR, Grungevatn; TO, Totak.

HU 0.2360.2710.2320.100
ST0.340 0.0980.0330.188
EI0.3870.141 0.0790.220
GR0.3510.0450.121 0.170
TO0.1660.2670.3150.258 

The first three dimensions of the PCoA analysis account for 42.6% of the total variation (Fig. 1), with dimension 1 (PC1) accounting for 32.0% and separating HU and TO from ST, EI and GR (marked as split A). Dimension 2 (PC2) (7.0%) mostly separates HU and TO (marked as split B). Individuals from ST and GR are overlapping, but show separation from EI along dimension 3 (PC3) (5.6%) (marked by split C). Two individuals from GR were grouping with individuals from EI, indicating a possible downstream migration. The method of Evanno et al. (2005) suggests = 2, whereas Falush et al. (2003) suggests = 4 for the data. This discrepancy (2 vs. 4) is addressed by comparing with the PCoA; the splits A, B and C (see Fig. 1, right column) are re-identified in the structure analyses (see Fig. 1, left column), providing support for = 4.

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

High-volume anonymous DNA markers like AFLPs are ideally suited for studying species migrations, origins and genome composition. The presented AFLP analyses showed that the newly established European minnow population in Ståvatn Reservoir cannot be derived from the River Hunnselva population because of the large genetic distance and the criss-cross specificity of private AFLPs at high frequencies. Although brown trout from the hatchery connected to Hunnselva were used for stocking Ståvatn from 1961 to 2005, European minnow were unlikely to have been introduced accidentally as a contaminant during those stocking events. This conclusion does not support the widely accepted assumption that brown trout stocking is the most likely dispersal mechanism for the introductions of European minnow into new environments in Norway, despite such hitch-hiking having been documented for other countries (e.g. Lintermans 2004 and references therein).

The analyses showed that the newly established European minnow population in Ståvatn is genetically similar to the population in Lake Grungevatn, which is situated downstream of Ståvatn. Surprisingly, the population in Eivindbuvatn is genetically different from both of these populations, despite the lake being positioned geographically between Ståvatn and Grungevatn. This pattern implies that i) fish were translocated upstream from Grungevatn to Ståvatn, but not continuously from lake to lake and ii) Eivindbuvatn represents an independent invasion. Totak Reservoir has been suggested as a possible source of European minnow invasions in nearby water bodies such as Ståvatn Reservoir (Eie 2003). However, as the population in Totak Reservoir is genetically unique, both in this study (Fig. 1) and in a previous study of multiple mtDNA haplotypes (Vøllestad et al. 1999), this population likely represents an entirely independent invasion. So, a somewhat complex situation emerges for European minnow populations in this relatively restricted geographical area, similar to that recorded for other introduced species. For example, topmouth gudgeon, Pseudorasbora parva (Temminck & Schlegel), has dispersed over long distances in a stepping-stone manner from the original introduced population in Romania to at least 32 European countries since the 1960s (Simon et al. 2011). This demonstrates how fast and complex such invasions may be at a large geographical scale.

During recent decades, several fish species (e.g. gudgeon, Gobio gobio L., and sunbleak, Leucaspius delineates (Henkel)), originating most likely from continental Europe, have likewise been introduced to, and dispersed in, southern Norway (Eken & Borgstrøm 1994; Hesthagen & Sandlund 2007). The use of live bait by recreational fishers has been suggested as a major introduction pathway for the occurrence of species outside their native range (Jackson 2002; Lintermans 2004; Caffrey et al. 2008), including European minnow in Norway (Huitfeldt-Kaas 1918; Hesthagen & Sandlund 1997, 2010). European minnow is also intentionally introduced as a prey fish for brown trout (Hesthagen & Sandlund 2010). Once introduced into a new environment, the European minnow has demonstrated the capacity to disperse to downstream locations (Museth et al. 2007) and considerably increase its distribution area within a short time. The clustering of individual fish in Grungevatn with the Eivindbuvatn population (Fig. 1) indicates that such downstream dispersal has occurred through two dams that separate these two lakes. The tracking of biological invasions is therefore of high importance in establishing the necessary knowledge base for developing effective management strategies to prevent future invasions and control the spread of existing populations (Estoup & Guillemaud 2010).

In conclusion, the introduction of European minnow in the Tokke drainage system was not as a contaminant of brown trout stocking events, but was more likely to have been through human-mediated introductions either as a live bait or to provide a prey fish for brown trout. The three genetically distinct European minnow populations identified within the same hydrosystem could not have derived from a single source population, so hitch-hiking was not a dispersal pathway for European minnow in this hydrosystem. Despite attempts to limit the spread of European minnow in Norway, the species continues to expand to new locations outside its native range. The results suggest that the underlying cause of the European minnow expansion is most likely connected to its use as live bait by recreational fishers or due to intentional stocking to provide an additional food source for brown trout. As both unauthorised stocking and use of live bait are forbidden in Norway, the results highlight a need for more effective control and information to fishers.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The authors thank J. G. Dokk for help with the field sampling, K. M. Thue for initial laboratory assistance, J. A. Eie for providing information concerning his report on European minnow spreading and G. H. Copp and two anonymous reviewers for their constructive comments on the manuscript. Laboratory expenses were funded by Røldal Mountain board, Vågsli landowner association and Statskog SF (the Norwegian state-owned land and forest enterprise), who granted us a priori right to publish. The English was improved by M. L. Davey. Financial support was given by the Department of Ecology and Natural Resource Management (INA), Norwegian University of Life Science (UMB). An unchangeable file containing all data is stored at UMB. The authors declare no conflict of interests.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  • Allendorf F.W. & Leary R.F. (1988) Conservation and distribution of genetic variation in a polytypic species, the cutthroat trout. Conservation Biology 2, 170184.
  • Baxter C.V., Fausch K.D., Murakami M. & Chapman P.L. (2004) Fish invasion restructures stream and forest food webs by interrupting reciprocal prey subsidies. Ecology 85, 26562663.
  • Baxter C.V., Fausch K.D., Murakami M. & Chapman P.L. (2007) Invading rainbow trout usurp a terrestrial prey subsidy from native charr and reduce their growth and abundance. Oecologia 153, 461470.
  • Brittain J.E., Brabrand Å., Saltveit S.J., Bremnes T. & Røsten E. (1988) The Biology and Population Dynamics of Gammarus lacustris in Relation to the Introduction of Minnows, Phoxinus phoxinus, into Øvre Heimdalsvatn, a Norwegian Subalpine Trout Lake. University of Oslo: Laboratorium for Ferskvannsøkologi og Innlandsfiske. Report No. 109. 56 pp.
  • Caffrey J.M., Acevedo A., Gallagher K. & Britton R. (2008) Chub (Leuciscus cephalus): a new potentially invasive fish species in Ireland. Aquatic Invasions 3, 201209.
  • Campbell D., Duchesne P. & Bernatchez L. (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Molecular Ecology 12, 19791991.
  • Copp G.H., Garthwaite R. & Gozlan R.E. (2005) Risk identification and assessment of non-native freshwater fishes: a summary of concepts and perspectives on protocols for the UK. Journal of Applied Ichthyology 21, 371373.
  • Cudmore B. & Mandrak N.E. (2004) Biological synopsis of grass carp (Ctenopharyngodon idella). Canadian MS Report Fisheries and Aquatic Sciences. No. 2705: v + 44 pp.
  • Dice L.R. (1945) Measures of the amount of ecologic association between species. Ecology 26, 297302.
  • Eie J.A. (2003) Vurdering av mulig spredning av ørekyte via regulantpålagte utsettinger av ørret fra A/L Settefisk. Drammen: Promitek AS. 87 pp + supplements. (in Norwegian).
  • Eken M. & Borgstrøm R. (1994) First report of Gobio gobio from Norway. Fauna 47, 120123 (in Norwegian with English summary).
  • Estoup A. & Guillemaud T. (2010) Reconstructing routes of invasion using genetic data: why, how and so what? Molecular Ecology 19, 41134130.
  • Evanno G., Regnaut S. & Goudet J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 26112620.
  • Falush D., Stephens M. & Pritchard J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 15671587.
  • Falush D., Stephens M. & Pritchard J.K. (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574578.
  • Gozlan R.E., St-Hilaire S., Feist S.W., Martin P. & Kent M.L. (2005) Biodiversity - Disease threat to European fish. Nature 435, 1046.
  • Hansen M.M., Ruzzante D.E., Nielsen E.E. & Mensberg K.-L.D. (2001) Brown trout (Salmo trutta) stocking impact assessment using microsatellite DNA markers. Ecological Applications 11, 148160.
  • Håstein T., Saltveit S.J. & Roberts R.J. (1978) Mass mortality among minnows Phoxinus phoxinus (L.) in Lake Tveitevatn, Norway, due to an aberrant strain of Aeromonas salmonicida. Journal of Fish Diseases 1, 241249.
  • Hesthagen T. & Sandlund O.T. (1997) Changes in the distribution of minnow (Phoxinus phoxinus) in Norway: causes and effects. Trondheim: Norwegian Institute for Nature Research Fagrapport No. 13. 16 pp. (in Norwegian with English summary).
  • Hesthagen T. & Sandlund O.T. (2004) Fish distribution in a mountain area in south-eastern Norway: human introductions overrule natural immigration. Hydrobiologia 521, 4959.
  • Hesthagen T. & Sandlund O.T. (2007) Non-native freshwater fishes in Norway: history, consequences and perspectives. Journal of Fish Biology 71, 173183.
  • Hesthagen T. & Sandlund O.T. (2010) NOBANIS - Invasive alien species fact sheet - Phoxinus phoxinus. - From: Online database of the European network on invasion alien species – NOBANIS. Available at: www.nobanis.org (accessed 6 January 2011).
  • Hesthagen T., Hegge O. & Skurdal J. (1992) Food choice and vertical distribution of European minnow, Phoxinus phoxinus, and young native and stocked brown trout, Salmo trutta, in the littoral zone of a subalpine lake. Nordic Journal of Freshwater Research 67, 7276.
  • Hubisz M.J., Falush D., Stephens M. & Pritchard J.K. (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9, 13221332.
  • Huitfeldt-Kaas H.H. (1918) Ferskvandsfiskenes utbredelse og indvandring i Norge med et tillæg om krebsen. Kristiania: Centraltrykkeriet. 106 pp. (in Norwegian).
  • Huitfeldt-Kaas H.H. (1935) Der Einfluss der Gewässerregelungen auf den Fischbestand in Binnenseen. Oslo: Nationaltrykkeriet. 105 pp. (in German).
  • IEA (2010) Key World Energy Statistics 2010 ©. Paris: International Energy Agency. 78pp.
  • Jackson D. (2002) Ecological effects of Micropterus introductions: the dark side of black bass. American Fisheries Society Symposium 31, 221232.
  • Kumar S., Skjæveland Å., Orr R.J.S., Enger P., Ruden T., Mevik B.H. et al. (2009) AIR: a batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses. BMC Bioinformatics 10, 357.
  • LaRue E., Ruetz C. III, Stacey M. & Thum R. (2011) Population genetic structure of the round goby in Lake Michigan: implications for dispersal of invasive species. Hydrobiologia 663, 7182.
  • Lintermans M. (2004) Human-assisted dispersal of alien freshwater fish in Australia. New Zealand Journal of Marine and Freshwater Research 38, 481501.
  • Litvak M.K. & Mandrak N.E. (1993) Ecology of freshwater baitfish use in Canada and the United States. Fisheries 18, 613.
  • Lynch M. & Milligan B.G. (1994) Analysis of population genetic structure with RAPD markers. Molecular Ecology 3, 9199.
  • Museth J., Hesthagen T., Sandlund O.T., Thorstad E.B. & Ugedal O. (2007) The history of the minnow Phoxinus phoxinus (L.) in Norway: from harmless species to pest. Journal of Fish Biology 71, 184195.
  • Museth J., Borgstrøm R. & Brittain J.E. (2010) Diet overlap between introduced European minnow (Phoxinus phoxinus) and young brown trout (Salmo trutta) in the lake, Øvre Heimdalsvatn: a result of abundant resources or forced niche overlap? Hydrobiologia 642, 93100.
  • Næstad F. & Brittain J.E. (2010) Long-term changes in the littoral benthos of a Norwegian subalpine lake following the introduction of the European minnow (Phoxinus phoxinus). Hydrobiologia 642, 7179.
  • Nielsen E.E., Hansen M.M., Schmidt C., Meldrup D. & Grønkjær P. (2001) Fisheries - population of origin of Atlantic cod. Nature 413, 272.
  • Ogutu-Ohwayo R. & Hecky R.E. (1991) Fish introductions in Africa and some of their implications. Canadian Journal of Fisheries and Aquatic Sciences 48, 812.
  • Peakall R. & Smouse P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288295.
  • Pritchard J.K., Stephens M. & Donnelly P. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945959.
  • Rohlf F.J. (2009) NTSYSpc: numerical taxonomy system. ver. 2.21c. Exeter Software, Setauket, New York.
  • Simon A., Britton R., Gozlan R., van Oosterhout C., Volckaert F.A.M. & Hänfling B. (2011) Invasive cyprinid fish in Europe originate from the single introduction of an admixed source population followed by a complex pattern of spread. PLoS ONE 6, e18560.
  • Sønstebø J.H., Borgstrøm R. & Heun M. (2007) A comparison of AFLPs and microsatellites to identify the population structure of brown trout (Salmo trutta L.) populations from Hardangervidda, Norway. Molecular Ecology 16, 14271438.
  • Stewart J.E. (1991) Introductions as factors in diseases of fish and aquatic invertebrates. Canadian Journal of Fisheries and Aquatic Sciences 48, 110117.
  • Vekemans X., Beauwens T., Lemaire M. & Roldan-Ruiz I. (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Molecular Ecology 11, 139151.
  • Vøllestad A. & Hesthagen T. (2001) Stocking of freshwater fish in Norway: management goals and effects. Nordic Journal of Freshwater Research 75, 143152.
  • Vøllestad A., Refseth U.H., Nesbø C.L. & Jakobsen K.S. (1999) Slektskap og kolonisering hos ørekyt. Oslo: Report, Biologisk institutt, Universitetet i Oslo. 22 pp. (in Norwegian).
  • Vos P., Hogers R., Bleeker M., Reijans M., Vandelee T., Hornes M. et al. (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 44074414.
  • Ward R.D., Woodwark M. & Skibinski D.O.F. (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. Journal of Fish Biology 44, 213232.
  • Witte F., Goldschmidt T., Wanink J., van Oijen M., Goudswaard K., Witte-Maas E. et al. (1992) The destruction on an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environmental Biology of Fishes 34, 128.
  • Zhivotovsky L.A. (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Molecular Ecology 8, 907913.