Conservation Genetics

, Volume 11, Issue 1, pp 279–292

Historical and recent genetic bottlenecks in European grayling, Thymallus thymallus

  • Akarapong Swatdipong
  • Craig R. Primmer
  • Anti Vasemägi
Research Article
  • 436 Downloads

Abstract

Sharp declines in population size, known as genetic bottlenecks, increase the level of inbreeding and reduce genetic diversity threatening population sustainability in both short- and long-term. We evaluated the presence, severity and approximate time of bottlenecks in 34 European grayling (Thymallus thymallus) populations covering the majority of the species distribution using microsatellite markers. We identified footprints of population decline in all grayling populations using the M ratio test. In contrast to earlier simulation studies assuming isolated populations, forward simulations allowing low levels of migration demonstrated that bottleneck footprints measured using the M ratio can persist within small populations much longer (up to thousands of generations) than previously anticipated. Using a coalescence approach, the beginning of population reduction was dated back to 1,000–10,000 years ago which suggests that the extremely low M ratio in European grayling is most likely caused by the last glaciation and subsequent post-glacial recolonization processes. In contrast to the M ratio, two alternative methods for bottleneck detection identified more recent bottlenecks in six populations and thus, from a conservation perspective, these populations warrant future monitoring. Based on a single time-point analysis using approximate Bayesian computation methodology, all grayling populations exhibited very small effective population sizes with the majority of Ne estimates below 50. Taken together, our results demonstrate the predominate role of genetic drift in European grayling populations in the short term but also emphasize the importance of gene flow counteracting the effects of genetic drift and loss of variation over longer evolutionary timescales.

Keywords

Thymallus thymallus Genetic bottleneck M ratio Heterozygosity excess test Mode-shift test Microsatellite 

References

  1. Abdelkrim J, Pascal M, Samadi S (2005) Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus). Mol Ecol 14:2923–2931CrossRefPubMedGoogle Scholar
  2. Aspi J, Roininen E, Kiiskila J, Ruokonen M, Kojola I, Bljudnik L, Danilov P, Heikkinen S, Pulliainen E (2009) Genetic structure of the northwestern Russian wolf populations and gene flow between Russia and Finland. Conserv Genet 10:815–826CrossRefGoogle Scholar
  3. Balloux F (2001) EASYPOP (Version 1.7): a computer program for population genetics simulations. J Hered 92:301–302CrossRefPubMedGoogle Scholar
  4. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedGoogle Scholar
  5. Beaumont MA (2004) msvar1.3 update. http://www.rubic.rdg.ac.uk/~mab/stuff/
  6. Beebee T, Rowe G (2001) Application of genetic bottleneck testing to the investigation of amphibian declines: a case study with natterjack toads. Conserv Biol 15:266–270Google Scholar
  7. Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568CrossRefPubMedGoogle Scholar
  8. Bernatchez L, Wilson CC (1998) Comparative phylogeography of nearctic and palearctic fishes. Mol Ecol 7:431–452CrossRefGoogle Scholar
  9. Bouza C, Castro J, Martinez P, Amaro R, Fernandez C, Ondina P, Outeiro A, Miguel ES (2007) Threatened freshwater pearl mussel Margaritifera margaritifera L. in NW Spain: low and very structured genetic variation in southern peripheral populations assessed using microsatellite markers. Conserv Genet 8:937–948CrossRefGoogle Scholar
  10. Briscoe DA, Malpica JM, Robertson A, Smith GJ, Frankham R, Banks RG, Barker JSF (1992) Rapid loss of genetic-variation in large captive populations of Drosophila flies—implications for the genetic management of captive populations. Conserv Biol 6:416–425CrossRefGoogle Scholar
  11. Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462CrossRefPubMedGoogle Scholar
  12. Chen YH, Opp SB, Berlocher SH, Roderick GK (2006) Are bottlenecks associated with colonization? Genetic diversity and diapause variation of native and introduced Rhagoletis completa populations. Oecologia 149:656–667CrossRefPubMedGoogle Scholar
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  14. Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344PubMedGoogle Scholar
  15. Dhuyvetter H, Gaublomme E, Desender K (2005) Bottlenecks, drift and differentiation: the fragmented population structure of the saltmarsh beetle Pogonus chalceus. Genetica 124:167–177CrossRefPubMedGoogle Scholar
  16. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170CrossRefPubMedGoogle Scholar
  17. Dinerstein E, McCracken GF (1990) Endangered greater one-horned rhinoceros carry high-levels of genetic-variation. Conserv Biol 4:417–422CrossRefGoogle Scholar
  18. Duftner N, Koblmuller S, Weiss S, Medgyesy N, Sturmbauer C (2005) The impact of stocking on the genetic structure of European grayling (Thymallus thymallus, Salmonidae) in two alpine rivers. Hydrobiologia 542:121–129CrossRefGoogle Scholar
  19. England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7:303–308CrossRefGoogle Scholar
  20. Excoffier L, Estoup A, Cornuet JM (2005) Bayesian analysis of an admixture model with mutations and arbitrarily linked markers. Genetics 169:1727–1738CrossRefPubMedGoogle Scholar
  21. Fave MJ, Turgeon J (2008) Patterns of genetic diversity in Great Lakes bloaters (Coregonus hoyi) with a view to future reintroduction in Lake Ontario. Conserv Genet 9:281–293CrossRefGoogle Scholar
  22. Fernandez-Stolz GP, Stolz JFB, De Freitas TRO (2007) Bottlenecks and dispersal in the tuco-tuco das dunas, Ctenomys Flamarioni (rodentia: Ctenomyidae), in southern Brazil. J Mammal 88:935–945CrossRefGoogle Scholar
  23. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327CrossRefPubMedGoogle Scholar
  24. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  25. Fraser DJ, Hansen MM, Ostergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems. Mol Ecol 16:3866–3889CrossRefPubMedGoogle Scholar
  26. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  27. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  28. Gross R, Kuhn R, Baars M, Schroder W, Stein H, Rottmann O (2001) Genetic differentiation of European grayling populations across the Main, Danube and Elbe drainages in Bavaria. J Fish Biol 58:264–280CrossRefGoogle Scholar
  29. Gross R, Lulla P, Naver T (2007) Genetic variability and differentiation of rainbow trout (Oncorhynchus mykiss) strains in northern and Eastern Europe. Aquaculture 272:S139–S146CrossRefGoogle Scholar
  30. Guinand B, Scribner KT (2003) Evaluation of methodology for detection of genetic bottlenecks: inferences from temporally replicated lake trout populations. C R Biol 326:S61–S67CrossRefPubMedGoogle Scholar
  31. Gum B, Gross R, Rottmann O, Schroder W, Kuhn R (2003) Microsatellite variation in Bavarian populations of European grayling (Thymallus thymallus): implications for conservation. Conserv Genet 4:659–672CrossRefGoogle Scholar
  32. Gum B, Gross R, Kuehn R (2005) Mitochondrial and nuclear DNA phylogeography of European grayling (Thymallus thymallus): evidence for secondary contact zones in central Europe. Mol Ecol 14:1707–1725CrossRefPubMedGoogle Scholar
  33. Gum B, Gross R, Kuehn R (2006) Discriminating the impact of recent human mediated stock transfer from historical gene flow on genetic structure of European grayling Thymallus thymallus L. J Fish Biol 69:115–135CrossRefGoogle Scholar
  34. Gum B, Gross R, Geist J (2009) Conservation genetics and management implications for European grayling, Thymallus thymallus: synthesis of phylogeography and population genetics. Fish Manag Ecol 16:37–51CrossRefGoogle Scholar
  35. Hale KA, Briskie JV (2007) Decreased immunocompetence in a severely bottlenecked population of an endemic New Zealand bird. Anim Conserv 10:2–10CrossRefGoogle Scholar
  36. Haugen TO, Vøllestad LA (2001) A century of life-history evolution in grayling. Genetica 112:475–491CrossRefPubMedGoogle Scholar
  37. Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112CrossRefGoogle Scholar
  38. Hill WG (1981) Estimation of effective population-size from data on linkage disequilibrium. Genet Res 38:209–216CrossRefGoogle Scholar
  39. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70Google Scholar
  40. Hood GM (2006) PopTools 2.7.5. Albany, Western AustraliaGoogle Scholar
  41. Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996) Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol Ecol 5:269–281PubMedGoogle Scholar
  42. Johnson JA, Tingay RE, Culver M, Hailer F, Clarke ML, Mindell DP (2009) Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Mol Ecol 18:54–63PubMedGoogle Scholar
  43. Kaukoranta M, Koljonen M-L, Koskiniemi J, Pennanen J, Tammi J (2000) Atlas of Finnish fishes, English summary. Distribution of lamprey, brook lamprey, salmon, trout, Arctic charr, whitefish, vandace, grayling, asp, vimba, spined loach and bullhead, and status of the stocks. Finnish Game and Fisheries Research Institute, Helsinki, Finland, p 40Google Scholar
  44. King JP, Kimmel M, Chakraborty R (2000) A power analysis of microsatellite-based statistics for inferring past population growth. Mol Biol Evol 17:1859–1868PubMedGoogle Scholar
  45. Kontula T, Vainola R (2001) Postglacial colonization of Northern Europe by distinct phylogeographic lineages of the bullhead, Cottus gobio. Mol Ecol 10:1983–2002CrossRefPubMedGoogle Scholar
  46. Korkea-Aho T (2003) Individual-based population genetic analysis of grayling (Thymallus thymallus) from a single water system. Department of Biological and Environmental Sciences, University of Helsinki, Helsinki, p 80Google Scholar
  47. Koskinen MT, Ranta E, Piironen J, Veselov A, Titov S, Haugen TO, Nilsson J, Carlstein M, Primmer CR (2000) Genetic lineages and postglacial colonization of grayling (Thymallus thymallus, Salmonidae) in Europe, as revealed by mitochondrial DNA analyses. Mol Ecol 9:1609–1624CrossRefPubMedGoogle Scholar
  48. Koskinen MT, Piironen J, Primmer CR (2001) Interpopulation genetic divergence in European grayling (Thymallus thymallus, Salmonidae) at a microgeographic scale: implications for conservation. Conserv Genet 2:133–143CrossRefGoogle Scholar
  49. Koskinen MT, Haugen TO, Primmer CR (2002a) Contemporary fisherian life-history evolution in small salmonid populations. Nature 419:826–830CrossRefPubMedGoogle Scholar
  50. Koskinen MT, Knizhin I, Primmer CR, Schlotterer C, Weiss S (2002b) Mitochondrial and nuclear DNA phylogeography of Thymallus spp. (grayling) provides evidence of ice-age mediated environmental perturbations in the world’s oldest body of fresh water, Lake Baikal. Mol Ecol 11:2599–2611CrossRefPubMedGoogle Scholar
  51. Koskinen MT, Nilsson J, Veselov AJ, Potutkin AG, Ranta E, Primmer CR (2002c) Microsatellite data resolve phylogeographic patterns in European grayling, Thymallus thymallus, Salmonidae. Heredity 88:391–401CrossRefPubMedGoogle Scholar
  52. Koskinen MT, Sundell P, Piironen J, Primmer CR (2002d) Genetic assessment of spatiotemporal evolutionary relationships and stocking effects in grayling (Thymallus thymallus, Salmonidae). Ecol Lett 5:193–205CrossRefGoogle Scholar
  53. Koyuk A, Bennett A, Tallmon D (2008) ONeSAMP 1.1. http://genomics.jun.alaska.edu/
  54. Lambert DM, King T, Shepherd LD, Livingston A, Anderson S, Craig JL (2005) Serial population bottlenecks and genetic variation: translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufusater). Conserv Genet 6:1–14CrossRefGoogle Scholar
  55. Lande R (1994) Risk of population extinction from fixation of new deleterious mutations. Evolution 48:1460–1469CrossRefGoogle Scholar
  56. Le Page SL, Livermore RA, Cooper DW, Taylor AC (2000) Genetic analysis of a documented population bottleneck: introduced Bennett’s wallabies (Macropus rufogriseus rufogriseus) in New Zealand. Mol Ecol 9:753–763CrossRefPubMedGoogle Scholar
  57. Lehtonen PK, Tonteri A, Sendek D, Titov S, Primmer CR (2009) Spatio-temporal genetic structuring of brown trout (Salmo trutta L.) populations within the River Luga, northwest Russia. Conserv Genet 10:281–289CrossRefGoogle Scholar
  58. Lucchini V, Galov A, Randi E (2004) Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13:523–536CrossRefPubMedGoogle Scholar
  59. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  60. Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211–1216PubMedGoogle Scholar
  61. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247CrossRefPubMedGoogle Scholar
  62. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998b) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974CrossRefPubMedGoogle Scholar
  63. Mardulyn P, Vaesen M-A, Milinkovitch MC (2008) Controlling population evolution in the laboratory to evaluate methods of historical inference. PLoS ONE 3:e2960CrossRefPubMedGoogle Scholar
  64. Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. 2. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689PubMedGoogle Scholar
  65. Meldgaard T, Nielsen EE, Loeschcke V (2003) Fragmentation by weirs in a riverine system: a study of genetic variation in time and space among populations of European grayling (Thymallus thymallus) in a Danish river system. Conserv Genet 4:735–747CrossRefGoogle Scholar
  66. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  67. Nei M, Chakraborty R, Fuerst PA (1976) Infinite allele model with varying mutation-rate. Proc Natl Acad Sci USA 73:4164–4168CrossRefPubMedGoogle Scholar
  68. Nylander E (2004) Kalatalous tilastoina 2004: Finnish fisheries statistic. Finnish Game and Fisheries Research Institute, p 28Google Scholar
  69. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447CrossRefPubMedGoogle Scholar
  70. Peel D, Ovenden J, Peel S (2004) NeEstimator: software for estimating effective population size, version 1.3. Queensland Government, Department of Primary Industries and FisheriesGoogle Scholar
  71. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  72. Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383–387PubMedGoogle Scholar
  73. Queney G, Ferrand N, Marchandeau S, Azevedo M, Mougel F, Branco M, Monnerot M (2000) Absence of a genetic bottleneck in a wild rabbit (Oryctolagus cuniculus) population exposed to a severe viral epizootic. Mol Ecol 9:1253–1264CrossRefPubMedGoogle Scholar
  74. Rand DM (1996) Neutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Conserv Biol 10:665–671CrossRefGoogle Scholar
  75. Raymond M, Rousset F (1995) Genepop (version 1.2)—population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  76. Russello MA, Brazaitis P, Gratten J, Watkins-Colwell GJ, Caccone A (2007) Molecular assessment of the genetic integrity, distinctiveness and phylogeographic context of the saltwater crocodile (Crocodylus porosus) on Palau. Conserv Genet 8:777–787CrossRefGoogle Scholar
  77. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  78. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Lab, Dept. of Anthropology, University of GenevaGoogle Scholar
  79. Schwartz MK, Tallmon DA, Luikart G (1998) Review of DNA-based census and effective population size estimators. Anim Conserv 1:293–299CrossRefGoogle Scholar
  80. Shimoda N, Knapik EW, Ziniti J, Sim C, Yamada E, Kaplan S, Jackson D, de Sauvage F, Jacob H, Fishman MC (1999) Zebrafish genetic map with 2000 microsatellite markers. Genomics 58:219–232CrossRefPubMedGoogle Scholar
  81. Spear SF, Peterson CR, Matocq MD, Storfer A (2006) Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611CrossRefGoogle Scholar
  82. Stamford MD, Taylor EB (2005) Population subdivision and genetic signatures of demographic changes in Arctic grayling (Thymallus arcticus) from an impounded watershed. Can J Fish Aquat Sci 62:2548–2559CrossRefGoogle Scholar
  83. Steinfartz S, Glaberman S, Lanterbecq D, Marquez C, Rassmann K, Caccone A (2007) Genetic impact of a severe El Niño event on Galápagos marine Iguanas (Amblyrhynchus cristatus). PloS ONE 2:e1285CrossRefPubMedGoogle Scholar
  84. Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166PubMedGoogle Scholar
  85. Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19:1981–1990PubMedGoogle Scholar
  86. Susnik S, Snoj A, Dovc P (2001) Evolutionary distinctness of grayling (Thymallus thymallus) inhabiting the Adriatic river system, as based on mtDNA variation. Biol J Linn Soc 74:375–385CrossRefGoogle Scholar
  87. Susnik S, Berrebi P, Dovc P, Hansen MM, Snoj A (2004) Genetic introgression between wild and stocked salmonids and the prospects for using molecular markers in population rehabilitation: the case of the Adriatic grayling (Thymallus thymallus L. 1785). Heredity 93:273–282CrossRefPubMedGoogle Scholar
  88. Swatdipong A, Vasemägi A, Koskinen M, Piironen J, Primmer C (2009) Unanticipated population structure of European grayling in its northern distribution: implications for conservation prioritization. Front Zool 6:6CrossRefPubMedGoogle Scholar
  89. Tallmon DA, Luikart G, Beaumont MA (2004) Comparative evaluation of a new effective population size estimator based on approximate Bayesian computation. Genetics 167:977–988CrossRefPubMedGoogle Scholar
  90. Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301CrossRefGoogle Scholar
  91. Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc R Soc Lond Ser B: Biol Sci 267:2375–2384Google Scholar
  92. Uiblein F, Jagsch A, Honsig-Erlenburg W, Weiss S (2001) Status, habitat use, and vulnerability of the European grayling in Austrian waters. J Fish Biol 59:223–247Google Scholar
  93. Vähä JP, Erkinaro J, Niemela E, Primmer CR (2007) Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Mol Ecol 16:2638–2654CrossRefPubMedGoogle Scholar
  94. Vasemägi A, Gross R, Paaver T, Koljonen ML, Säisä M, Nilsson J (2005) Analysis of gene associated tandem repeat markers in Atlantic salmon (Salmo salar L.) populations: implications for restoration and conservation in the Baltic Sea. Conserv Genet 6:385–397CrossRefGoogle Scholar
  95. Vitalis R, Couvet D (2001) Estimation of effective population size and migration rate from one- and two-locus identity measures. Genetics 157:911–925PubMedGoogle Scholar
  96. Wang YQ, Williams DA, Gaines MS (2005) Evidence for a recent genetic bottleneck in the endangered Florida Keys silver rice rat (Oryzomys argentatus) revealed by microsatellite DNA analyses. Conserv Genet 6:575–585CrossRefGoogle Scholar
  97. Waples RS (1989) A generalized-approach for estimating effective population-size from temporal changes in allele frequency. Genetics 121:379–391PubMedGoogle Scholar
  98. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184CrossRefGoogle Scholar
  99. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562CrossRefGoogle Scholar
  100. Witzenberger KA, Hochkirch A (2008) Genetic consequences of animal translocations: A case study using the field cricket, Gryllus campestris L. Biol Conserv 141:3059–3068CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Akarapong Swatdipong
    • 1
  • Craig R. Primmer
    • 1
  • Anti Vasemägi
    • 1
    • 2
  1. 1.Division of Genetics and Physiology, Department of Biology (Vesilinnantie 5)University of TurkuTurkuFinland
  2. 2.Department of Aquaculture, Institute of Veterinary Medicine and Animal ScienceEstonian University of Life SciencesTartuEstonia

Personalised recommendations