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Reviews in Fish Biology and Fisheries

, Volume 25, Issue 4, pp 587–602 | Cite as

Patterns, latitudinal clines and countergradient variation in the growth of roach Rutilus rutilus (Cyprinidae) in its Eurasian area of distribution

  • Ali Serhan Tarkan
  • Lorenzo Vilizzi
Reviews

Abstract

The roach Rutilus rutilus is a eurythermal generalist that has been translocated and introduced mainly beyond the southern limits of its native Eurasian range of distribution. Although largely studied in most aspects of its ecology, no global assessment is available on its growth. Such information is critical for management purposes, especially in view of further dispersal of this ‘potential pest’ and climate change predictions. To address this knowledge gap, a meta-analysis was carried out of the age and growth of 301 roach populations from 231 water bodies across the species’ native and translocated/introduced Eurasian range of distribution with the aim to identify habitat and climate-related differences in growth patterns, latitudinal clines, and the possible presence of countergradient growth variation (CGV). Faster growth rates were identified under warm relative to temperate and cold climates, and these were related to optimised resource allocation. Latitudinal clines indicated decreasing trends with increasing latitude in growth and body size, in line with life-history theory. However, the presence of thresholds encompassing the previously-reported 50°N latitude value suggested a ‘plateau’ or decrease in growth at lower latitudes, and CGV was identified for 1+ to 10+ fish. It is argued that increased water temperatures are likely to cause a northern shift in the observed thresholds and a ‘homogenisation’ of the species’ population dynamics resulting in faster growth rates, but with more pronounced effects in continental Eurasia.

Keywords

Growth index von Bertalanffy growth function Latitudinal clines Countergradient growth variation Köppen–Geiger Piecewise regression Mixed effects models 

Notes

Acknowledgments

We are grateful to Bořek Drozd (University of South Bohemia, Czech Republic), Gordon H. Copp and Phil Davison (Cefas, UK), Hui Wei (Chinese Academy of Fishery Sciences, China), Riikka Puntila (University of Helsinki, Finland) and Tamsin Vicary (Freshwater Biological Association, UK) for contributing key references towards the literature review. Contribution to this study by LV was through a 2221 Fellowship Programme granted by The Scientific & Technological Research Council of Turkey (TÜBİTAK) and The Department of Science Fellowships & Grant Programs (BİDEB).

Supplementary material

11160_2015_9398_MOESM1_ESM.docx (337 kb)
Supplementary material 1 (DOCX 337 kb)

References

  1. Almeida D, Ribeiro F, Leunda PA, Vilizzi L, Copp GH (2013) Effectiveness of FISK, an invasiveness screening tool for non-native freshwater fishes, to perform risk identification assessments in the Iberian Peninsula. Risk Anal 33:1404–1413. doi: 10.1111/risa.12050 CrossRefPubMedGoogle Scholar
  2. Angilletta MJ Jr, Dunham AE (2003) The temperature-size rule in ectotherms: simple evolutionary explanations may not be general. Am Nat 162:332–342CrossRefPubMedGoogle Scholar
  3. Bajer PG, Sorensen PW (2010) Recruitment and abundance of an invasive fish, the common carp, is driven by its propensity to invade and reproduce in basins that experience winter-time hypoxia in interconnected lakes. Biol Invasions 12:1101–1112. doi: 10.1007/s10530-009-9528-y CrossRefGoogle Scholar
  4. Bates DM (2010) lme4: mixed-effects modeling with R. Springer, BerlinGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7Google Scholar
  6. Begg GA, Waldman JR (1999) An holistic approach to fish stock identification. Fish Res 43:35–44. doi: 10.1016/S0165-7836(99)00065-X CrossRefGoogle Scholar
  7. Begg GA, Friedland KD, Pearce JB (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fish Res 43:1–8. doi: 10.1016/S0165-7836(99)00062-4 CrossRefGoogle Scholar
  8. Belk MC, Houston DD (2002) Bergmann’s rule in ectotherms: a test using freshwater fishes. Am Nat 160:803–808CrossRefPubMedGoogle Scholar
  9. Beverton RJH (1987) Longevity in fish: some ecological and evolutionary considerations. In: Woodhead AD, Thompson KH (eds) Evolution of longevity in animals. Plenum Press, New York, pp 161–186Google Scholar
  10. Blanck A, Lamouroux N (2007) Large-scale intraspecific variation in life-history traits of European freshwater fish. J Biogeogr 34:862–875. doi: 10.1111/j.1365-2699.2006.01654.x CrossRefGoogle Scholar
  11. Bolker B, R Development Core Team (2014) bbmle: tools for general maximum likelihood estimation. R package version 1.0.16Google Scholar
  12. Britton JR (2007) Reference data for evaluating the growth of common riverine fishes in the UK. J Appl Ichthyol 23:555–560. doi: 10.1111/j.1439-0426.2007.00845.x CrossRefGoogle Scholar
  13. Britton JR, Davies GD, Pegg J (2012) Spatial variation in the somatic growth rates of European barbel Barbus barbus: a UK perspective. Ecol Freshw Fish 22:21–29. doi: 10.1111/j.1600-0633.2012.00588.x CrossRefGoogle Scholar
  14. Brown GP, Shine R (2005) Female phenotype, life history, and reproductive success in free-ranging snakes (Tripidonophis mairii). Ecology 86:2763–2770. doi: 10.1890/04-1805 CrossRefGoogle Scholar
  15. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  16. Burrough RJ, Kennedy CR (1979) The occurrence and natural alleviation of stunting in a population of roach, Rutilus rutilus (L.). J Fish Biol 15:93–109. doi: 10.1111/j.1095-8649.1979.tb03574.x CrossRefGoogle Scholar
  17. Chavarie L, Dempson JB, Schwarz C, Reist J, Power G, Power M (2010) Latitudinal variation in growth among Arctic charr in eastern North America: evidence for countergradient variation? Hydrobiologia 650:161–177. doi: 10.1007/s10750-009-0043-z CrossRefGoogle Scholar
  18. Chezik KA, Lester NP, Venturelli PA (2014) Fish growth and degree-days I: selecting a base temperature for a within-population study. Can J Fish Aquat Sci 71:47–55. doi: 10.1139/cjfas-2013-0295 CrossRefGoogle Scholar
  19. Chitravadivelu K (1974) Growth, age composition, population density, mortality, production and yield of Alburnus alburnus (Linnaeus, 1758) and Rutilus rutilus (Linnaeus, 1758) in the inundation region of Danube—Žofín. Acta Univ Carol Biol 1972:1–76Google Scholar
  20. Conover DO, Present TM (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83:316–324. doi: 10.1007/BF00317554 CrossRefGoogle Scholar
  21. Conover DO, Brown JJ, Ehtisham A (1997) Countergradient variation in growth of young striped bass (Morone saxatilis) from different latitudes. Can J Fish Aquat Sci 54:2401–2409. doi: 10.1139/f97-147 Google Scholar
  22. Copp GH, Fox MG, Przybylski M, Godinho F, Vila-Gispert A (2004) Life-time growth patterns of pumpkinseed Lepomis gibbosus introduced to Europe relative to native North American populations. Folia Zool 53:237–254Google Scholar
  23. Copp GH, Bianco PG, Bogutskaya NG, Erős T, Falka I, Ferreira MT, Fox MG, Freyhof J, Gozlan RE, Grabowska J, Kováč V, Moreno-Amich R, Naseka AM, Peňáz M, Povž M, Przybylski M, Robillard M, Russell IC, Stakėnas S, Šumer S, Vila-Gispert A, Wiesner C (2005) To be, or not to be, a non-native freshwater fish? J Appl Ichthyol 21:242–262. doi: 10.1111/j.1439-0426.2005.00690.x CrossRefGoogle Scholar
  24. Copp GH, Britton JR, Cucherousset J, García-Berthou E, Kirk R, Peeler EJ, Stakėnas S (2009) Voracious invader or benign feline? A review of the environmental biology of European catfish Silurus glanis in its native and introduced range. Fish Fish 10:252–282. doi: 10.1111/j.1467-2979.2008.00321.x CrossRefGoogle Scholar
  25. Costello A, Maslin M, Montgomery H, Johnson AM, Ekins P (2011) Global health and climate change: moving from denial and catastrophic fatalism to positive action. Philos Trans R Soc A 369:1866–1882. doi: 10.1098/rsta.2011.0007 CrossRefGoogle Scholar
  26. Cowx IG (1988) Distribution and variation in the growth of roach, Rutilus rutilus (L.), and dace, Leuciscus leuciscus (L.), in a river catchment in south-west England. J Fish Biol 33:59–72. doi: 10.1111/j.1095-8649.1988.tb05448.x CrossRefGoogle Scholar
  27. Cragg-Hine D, Jones JW (1969) The growth of dace Leuciscus leuciscus (L.), roach Rutilus rutilus (L.) and chub Squalius cephalus (L.) in Willow Brook, Northamptonshire. J Fish Biol 1:59–82. doi: 10.1111/j.1095-8649.1969.tb03845.x CrossRefGoogle Scholar
  28. Epler P, Popek W, Luszczek-Trojnar E, Drag-Kozak E, Szczerbik P, Socha M (2005) Age and growth rate of the roach (Rutilus rutilus L.) from the Solina and the Tresna (Zywieckie Lake) dam reservoires [sic]. Acta Sci Polon Pisc 4:59–70Google Scholar
  29. Erickson TR, Stefan HG (1996) Correlations of Oklahoma stream temperatures with air temperatures. University of Minnesota, St. Anthony Falls Laboratory, Project Report No. 398Google Scholar
  30. Fleming IA, Gross MR (1990) Latitudinal clines: a trade-off between egg number and size in Pacific salmon. Ecology 71:1–11. doi: 10.2307/1940241 CrossRefGoogle Scholar
  31. Frimodt C (1995) Multilingual illustrated guide to the world’s commercial coldwater fish. Blackwell Science, OxfordGoogle Scholar
  32. Froese R, Pauly D (eds) (2014) FishBase. World Wide Web electronic publication. www.fishbase.org, version (11/2014)
  33. García-Berthou E (1999) Spatial heterogeneity in roach (Rutilus rutilus) diet among contrasting basins whitin a lake. Arch Hydrobiol 146:239–256Google Scholar
  34. Gayanilo FC, Sparre P, Pauly D (2005) FAO-ICLARM Stock Assessment Tools II (FiSAT II). User’s guide. FAO Computerized Information Series (Fisheries), No. 8, Revised version, FAO, RomeGoogle Scholar
  35. Giannetto D, Carosi A, Ghetti L, Pompei L, Viali P, Lorenzoni M (2014) Size selectivity of gill-nets and growth of roach Rutilus rutilus (Linnaeus, 1758) an alien species in Piediluco lake (Italy). Knowl Manag Aquat Ecosys 413:07. doi: 10.1051/kmae/2014001 CrossRefGoogle Scholar
  36. Goldspink CR (1977) The return of marked roach (Rutilus rutilus L.) to spawning grounds in Tjeukemeer, The Netherlands. J Fish Biol 11:599–603. doi: 10.1111/j.1095-8649.1977.tb05717.x CrossRefGoogle Scholar
  37. Goldspink CR (1978) Comparative observations on the growth rate and year class strength of roach Rutilus rutilus L. in two Cheshire lakes, England. J Fish Biol 12:421–433. doi: 10.1111/j.1095-8649.1978.tb04185.x CrossRefGoogle Scholar
  38. Goldspink CR (1979) The population density, growth rate and production of roach Rutilus rutilus (L.) in Tjeukemeer, The Netherlands. J Fish Biol 15:473–498. doi: 10.1111/j.1095-8649.1979.tb03632.x CrossRefGoogle Scholar
  39. Graham CT, Harrod C (2009) Implications of climate change for the fishes of the British Isles. J Fish Biol 74:1143–1205. doi: 10.1111/j.1095-8649.2009.02180.x CrossRefPubMedGoogle Scholar
  40. Griffiths D (1997) The status of the Irish freshwater fish fauna: a review. J Appl Ichthyol 13:9–13. doi: 10.1111/j.1439-0426.1997.tb00091.x CrossRefGoogle Scholar
  41. Harrod C, Griffiths D, McCarthy TK, Rosell R (2001) The Irish pollan, Coregonus autumnalis: options for its conservation. J Fish Biol 59(Suppl. A):339–355. doi: 10.1111/j.1095-8649.2001.tb01395.x CrossRefGoogle Scholar
  42. Hartley PHT (1947) The coarse fishes of Britain. Freshwater Biological Association, Scientific Publication No. 12, Wray Castle, Ambleside, WestmorlandGoogle Scholar
  43. Hellawell JM (1972) The growth, reproduction and food of the roach Rutilus rutilus (L.) of River Lugg, Hertfordshire. J Fish Biol 4:469–486. doi: 10.1111/j.1095-8649.1972.tb05696.x CrossRefGoogle Scholar
  44. Hickley P, Dexter FK (1979) A comparative index of quantifying growth in length of fish. Fish Manage 10:147–151. doi: 10.1111/j.1365-2109.1979.tb00270.x Google Scholar
  45. Holčik J, Hruška V (1966) On the spawning substrate of roach, Rutilus rutilus (Linnaeus 1758), and bream, Abramis brama (Linnaeus 1758), and notes on the ecological characteristics of some European fishes. Věst Česk Spol Zool 30:22–29Google Scholar
  46. Horppila J (1994) The diet and growth of roach (Rutilus rutilus) in Lake Vesijärvi and possible changes in the course of biomanipulation. Hydrobiologia 294:35–41. doi: 10.1007/BF00017623 CrossRefGoogle Scholar
  47. Jamet JL, Desmolles F (1994) Growth, reproduction and condition of roach (Rutilus rutilus (L.)), perch (Perca fluviatilis, L.) and ruffe (Gymnocephalus cernuus (L.)) in eutrophic Lake Aydat (France). Int Rev ges Hydrobiol Hydrogr 79:305–322CrossRefGoogle Scholar
  48. Kas’yanov AN, Izyumov YG, Kas’yanova NV (1995) Growth of roach, Rutilus rutilus, in Russia and adjacent countries. J Ichthyol 35:256–273Google Scholar
  49. Ketmaier V, Bianco PG, Durand JD (2008) Molecular systematics, phylogeny and biogeography of roaches (Rutilus, Teleostei, Cyprinidae). Mol Phylogenet Evol 49:362–367. doi: 10.1016/j.ympev.2008.07.012 CrossRefPubMedGoogle Scholar
  50. Kipling C (1983) Changes in the population of pike (Esox lucius) in Windermere from 1944 to 1981. J Anim Ecol 52:989–999CrossRefGoogle Scholar
  51. Kitchell JF, Stewart DJ, Weininger D (1977) Applications of a bioenergetics model to yellow perch (Perca flavescens) and walleye (Stizostedion vitreum vitreum). J Fish Res Board Can 34:1922–1935. doi: 10.1139/f77-258 CrossRefGoogle Scholar
  52. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F (2006) World map of the Köppen–Geiger climate classification updated. Meteorol Z 15:259–263. doi: 10.1127/0941-2948/2006/0130 CrossRefGoogle Scholar
  53. Kováč V, Copp GH, Sousa RP (2009) Life-history traits of invasive bighead goby Neogobius kessleri (Günther, 1861) from the middle Danube River, with a reflection on which goby species may win the competition. J Appl Ichthyol 25:33–37. doi: 10.1111/j.1439-0426.2009.01189.x Google Scholar
  54. Kozlovskiy SV (1992) Observations of the spawning behavior of roach and bream in Saratovskoye reservoir. J Ichthyol 32:134–136Google Scholar
  55. Kozlowski J (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol Evol 7:15–19. doi: 10.1016/0169-5347(92)90192-E CrossRefPubMedGoogle Scholar
  56. Kozlowski J (1996) Optimal allocation of resources explains interspecific life-history pattern in animals with indeterminate growth. Proc R Soc Lond B Biol Sci 263:559–566CrossRefGoogle Scholar
  57. Lappalainen J, Tarkan AS (2007) Latitudinal gradients in onset date, onset temperature and duration of spawning of roach. J Fish Biol 70:441–450. doi: 10.1111/j.1095-8649.2007.01315.x CrossRefGoogle Scholar
  58. Lappalainen A, Westerbom M, Heikinheimo O (2005) Roach (Rutilus rutilus) as an important predator on blue mussel (Mytilus edulis) populations in a brackish water environment, the northern Baltic Sea. Mar Biol 147:323–330. doi: 10.1007/s00227-005-1598-5 CrossRefGoogle Scholar
  59. Lappalainen J, Tarkan AS, Harrod C (2008) A meta-analysis of latitudinal variations in life history traits of roach Rutilus rutilus over its geographical range: linear or non-linear relationships? Freshw Biol 53:1491–1501. doi: 10.1111/j.1365-2427.2008.01977.x CrossRefGoogle Scholar
  60. Larmuseau MHD, Freyhof J, Volckaert FAM, Van Houdt JKJ (2009) Matrilinear phylogeography and demographical patterns of Rutilus rutilus: implications for taxonomy and conservation. J Fish Biol 75:332–353. doi: 10.1111/j.1095-8649.2009.02322.x CrossRefPubMedGoogle Scholar
  61. Li H, Shen J, Ma X, Liu Y, Zhao Y, Liu Q, Hao Z (2009) Growth characteristics of roach Rutilus rutilus (L.) in Ulungur Lake in Xinjiang Uigur Autonomous Region. J Huazhong Agric Univ 28:202–206 (in Chinese with an abstract in English) Google Scholar
  62. Linfield RSJ (1979) Changes in the rate of growth in a stunted roach Rutilus rutilus population. J Fish Biol 15:275–298. doi: 10.1111/j.1095-8649.1979.tb03608.x CrossRefGoogle Scholar
  63. Lobón-Cerviá J, Dgebuadze Y, Utrilla CG, Rincón PA, Grando-Lorencio C (1996) The reproductive tactics of dace in central Siberia: evidence for temperature regulation of the spatio-temporal variability of its life-history. J Fish Biol 48:1074–1087. doi: 10.1111/j.1095-8649.1996.tb01805.x CrossRefGoogle Scholar
  64. Magnuson JJ, Crowder LB, Medvick PA (1979) Temperature as an ecological resource. Am Zool 19:331–343. doi: 10.1093/icb/19.1.331 CrossRefGoogle Scholar
  65. Mann RHK (1973) Observations on the age, growth, reproduction and food of the roach, Rutilus rutilus (L.) in two rivers in southern England. J Fish Biol 5:707–736. doi: 10.1111/j.1095-8649.1973.tb04506.x CrossRefGoogle Scholar
  66. Mann RHK (1991) Growth and production. In: Winfield IJ, Nelson JS (eds) Cyprinid fishes: systematics, biology and exploitation. Chapman and Hall, London, pp 456–482CrossRefGoogle Scholar
  67. Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940. doi: 10.1016/S0531-5565(03)00159-1 CrossRefPubMedGoogle Scholar
  68. Michel P, Oberdoff T (1995) Feeding habits of fourteen European freshwater fish species. Cybium 19:5–46Google Scholar
  69. Mills CA (1981) The spawning of roach, Rutilus rutilus (L.) in a chalk stream. Aquac Res 12:49–54. doi: 10.1111/j.1365-2109.1981.tb00009.x CrossRefGoogle Scholar
  70. Mills CA (1988) The effect of extreme northerly climatic conditions on the life history of minnow, Phoxinus phoxinus. J Fish Biol 33:545–561. doi: 10.1111/j.1095-8649.1988.tb05498.x CrossRefGoogle Scholar
  71. Naddafi R, Abdoli A, Hassanzadeh Kiabi B, Mojazi Amiri B, Karami M (2005) Age, growth and reproduction of the Caspian roach (Rutilus rutilus caspicus) in the Anzali and Gomishan wetlands, North Iran. J Appl Ichthyol 21:492–497. doi: 10.1111/j.1439-0426.2005.00669.x CrossRefGoogle Scholar
  72. New M, Hulme M, Jones P (1999) Representing twentieth-century space-time climate variability. Part I: development of a 1961–90 mean monthly terrestrial climatology. J Climate 12:829–856. doi: 10.1175/1520-0442(1999)012%3C0829:RTCSTC%3E2.0.CO;2 CrossRefGoogle Scholar
  73. Ogle DH (2014) FSA: fisheries stock analysis. R package version 0.4.6Google Scholar
  74. Okgerman H, Oral M, Yigit S (2009) Biological Aspects of Rutilus rutilus (roach) in Sapanca Lake (Turkey). J Anim Vet Adv 8:441–446Google Scholar
  75. Papadopol M (1970) Ecological characteristics of the main species of minnows (Pisces, Cyprinidae) from the Danube delta. Věst Česk Spol Zool 33:240–251Google Scholar
  76. Papageorgiou NK (1979) The length weight relationship, age, growth and reproduction of the roach Rutilus rutilus (L.) in Lake Volvi. J Fish Biol 14:529–538. doi: 10.1111/j.1095-8649.1979.tb03552.x CrossRefGoogle Scholar
  77. Pęczalka A (1968) Development and reproduction of roach (Rutilus rutilus L.) in the Szczecin Firth. Pol Arch Hydrobiol 15:103–120Google Scholar
  78. Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen–Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. doi: 10.5194/hess-11-1633-2007 CrossRefGoogle Scholar
  79. Persson L (1983) Effects of intra- and inerspecific competition on dynamics and size structure of a perch Perca fluviatilis and a roach Rutilus rutilus population. Oikos 41:126–132CrossRefGoogle Scholar
  80. Pierce RB, Tomcko CM, Margenau TL (2003) Density dependence in growth and size structure of northern pike populations. N Am J Fish Manag 23:331–339. doi: 10.1577/1548-8675(2003)023<0331:DDIGAS>2.0.CO;2 CrossRefGoogle Scholar
  81. Ponton D, Gerdeaux D (1987) La population de gardons (Rutilus rutilus (L.)) du lac Léman en 1983–85. Structure en age, detérminisme du recrutement, analyse de la croissance. Bull Fr Pêche Piscic 305:45–53Google Scholar
  82. Power M, McKinley RS (1997) Latitudinal variation in Lake Sturgeon size as related to the thermal opportunity for growth. Trans Am Fish Soc 126:549–558. doi: 10.1577/1548-8659(1997)126<0549:LVILSS>2.3.CO;2 CrossRefGoogle Scholar
  83. Przybylski M, Boron A, Kruk A (2004) Growth of barbel, Barbus barbus (L.) in the upper Warta River, Odra River system. Ecohydrol Hydrobiol 4:183–190Google Scholar
  84. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  85. Ricker WE (1975) Computation and interpretation of biological statistics of fish population. Bulletin (Fisheries Research Board of Canada), 191. Department of the Environment, Fisheries and Marine Service, Ottawa, pp 382Google Scholar
  86. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New YorkGoogle Scholar
  87. Rypel AL (2012a) Concordant estimates of countergradient growth variation in striped bass (Morone saxatilis) using comparative life-history data. Can J Fish Aquat Sci 69:1261–1265. doi: 10.1139/f2012-069 CrossRefGoogle Scholar
  88. Rypel AL (2012b) Meta-analysis of growth rates for a circumpolar fish, the northern pike (Esox lucius), with emphasis on effects of continent, climate and latitude. Ecol Freshw Fish 21:521–532. doi: 10.1111/j.1600-0633.2012.00570.x CrossRefGoogle Scholar
  89. Rypel AL (2014) Do invasive freshwater fish species grow better when they are invasive? Oikos 123:279–289. doi: 10.1111/j.1600-0706.2013.00530.x CrossRefGoogle Scholar
  90. Silverstein JT, Wolters WR, Holland M (1999) Evidence of differences in growth and food intake regulation in different genetic strains of channel catfish. J Fish Biol 54:607–615. doi: 10.1111/j.1095-8649.1999.tb00639.x CrossRefGoogle Scholar
  91. Sonderegger D (2012) SiZer: significant zero crossings. R package version 0.1-4Google Scholar
  92. Sonderegger DL, Wang H, Clements WH, Noon BR (2009) Using SiZer to detect thresholds in ecological data. Front Ecol Environ 7:190–195. doi: 10.1890/070179 CrossRefGoogle Scholar
  93. Tarkan AS (2006) Reproductive ecology of two cyprinid fish in an oligotrophic lake near the southern limits of their distribution range. Ecol Freshw Fish 15:131–138. doi: 10.1111/j.1600-0633.2006.00133.x CrossRefGoogle Scholar
  94. Tsoumani M, Georgiadis A, Giantsis IA, Leonardos I, Apostolidis AP (2014) Phylogenetic relationships among Southern Balkan Rutilus species inferred from cytochrome b sequence analysis: micro-geographic resolution and taxonomic implications. Biochem Syst Ecol 54:172–178. doi: 10.1016/j.bse.2014.02.006 CrossRefGoogle Scholar
  95. van Dijk PAH, Staaks G, Hardewig I (2002) The effect of fasting and refeeding on temperature preference, activity and growth of roach, Rutilus rutilus. Oecologia 130:496–504. doi: 10.1007/s00442-001-0830-3 CrossRefGoogle Scholar
  96. Vázquez DP, Stevens RD (2004) The latitudinal gradient in niche breadth: concepts and evidence. Am Nat. doi: 10.1086/421445 PubMedGoogle Scholar
  97. Vilizzi L, Kováč V (2014) Alternative ontogenies and developmental plasticity: implications for ecological and evolutionary studies on species complexes. Fish Fish 15:523–531. doi: 10.1111/faf.12048 CrossRefGoogle Scholar
  98. Vilizzi L, Copp GH, Britton JR (2013) Age and growth of European barbel Barbus barbus (Cyprinidae) in the small, mesotrophic River Lee and relative to other populations in England. Knowl Manag Aquat Ec 409:09. doi: 10.1051/kmae/2013054
  99. Vilizzi L, Ekmekçi FG, Tarkan AS, Jackson Z (2015) Growth of common carp Cyprinus carpio in Anatolia (Turkey), with a comparison to native and invasive areas worldwide. Ecol Freshw Fish 24:165–180. doi: 10.1111/eff.12141 CrossRefGoogle Scholar
  100. Vøllestad LA, L’Abée-Lund JH (1987) Reproductive biology of stream spawning roach, Rutilus rutilus. Environ Biol Fish 18:219–227. doi: 10.1007/BF00000361 CrossRefGoogle Scholar
  101. Volta P, Jepsen N (2008) The recent invasion of Rutilus rutilus (L.) (Pisces: Cyprinidae) in a large South-Alpine lake: Lago Maggiore. J Limnol 67:163–170CrossRefGoogle Scholar
  102. Vostradovsky J (1973) Freshwater fishes. The Hamlyn Publishing Group Limited, LondonGoogle Scholar
  103. White RWG, Williams WP (1978) Studies of the ecology of fish populations in the Rye Meads sewage effluent lagoons. J Fish Biol 13:379–400. doi: 10.1111/j.1095-8649.1978.tb03446.x CrossRefGoogle Scholar
  104. Więsky K, Załachowski W (2000) Growth of roach Rutilus rutilus (L.) in the River Odra estuary. Acta Ichthyol Pisc 30:3–17Google Scholar
  105. Williams WP (1967) The growth and mortality of four species of fish in the River Thames at Reading. J Anim Ecol 36:695–720CrossRefGoogle Scholar
  106. Wilson RS (1971) The decline of a roach Rutilus rutilus (L.) population in Chew Valley Lake. J Fish Biol 3:129–137. doi: 10.1111/j.1095-8649.1971.tb03655.x CrossRefGoogle Scholar
  107. Zaugg B (1987) Quelques aspects de dynamique des populations, de biologie générale et de biométrie du gardon (Rutilus rutilus L.) dans 4 lacs du plateau suisse. PhD Thesis, Université de Neuchâtel, SwitzerlandGoogle Scholar
  108. Zivkov M, Raikova-Petrova G (2001) Comparative analysis of age compositon, growth rate and conditiond of roach, Rutilus rutilus (L.), in three Bulgarian reservoirs. Acta Zool Bulg 53:47–60Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Faculty of FisheriesMuğla Sıtkı Koçman UniversityKötekli, MuğlaTurkey

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