Polar Biology

, Volume 38, Issue 11, pp 1813–1823 | Cite as

Age and growth of marine three-spined stickleback in the White Sea 50 years after a population collapse

  • Peter Yershov
  • Alexey Sukhotin
Original Paper


In the early 1960s, the population of White Sea marine three-spined stickleback (Gasterosteus aculeatus), a key forage fish, declined drastically, and the species almost completely disappeared from catches. The population started to recover in the late 1990s, and its abundance has increased exponentially since then. Using contemporary and historical data, we contrast the age structure of spawning stock and fish growth before and after the population decline. Most stickleback spawners in 2009–2011 were 2 and 3 years old, with the 3-year-old fish being more abundant. The proportion of 2-year-old fish in recent catches is higher than that 50 years ago, indicating some rejuvenation of the population after the prolonged decline. Moreover, White Sea sticklebacks in the present population grow faster than those in the 1950s. The observed shifts are concurrent with the long-term changes in the temperature regime in the coastal areas of the White Sea, which determine zooplankton abundance and the duration of the feeding season of fish. The variation in life-history traits among both anadromous and marine stickleback populations within a distribution range was examined. The stickleback showed a considerable interpopulation variation in growth, longevity and age/size at maturity, which appeared generally related to thermal conditions at the marine feeding areas.


Stickleback Age Growth Sexual maturity Gasterosteusaculeatus White Sea Population structure Population dynamics 



We are grateful to our colleagues from the Saint Petersburg University—Dr. Tatiana Ivanova, Dr. Dmitry Lajus and Dr. Mikhail Ivanov—for their assistance in collecting the materials and for providing data on stickleback yearlings. We wish to thank the anonymous referees for valuable suggestions on improving the manuscript. This research was supported by the ongoing projects of the Russian Academy of Sciences, “Ecosystems of the White Sea and the adjacent Arctic seas: biodiversity dynamics under the changing climate” and “Life-history strategies and mechanisms of adaptations in fish and invertebrates in the Arctic seas” and by a RFBR Grant # 14-04-004466 to AS.

Supplementary material

300_2015_1743_MOESM1_ESM.pdf (159 kb)
Supplementary material 1 (PDF 159 kb)


  1. Abdel’-Malek SA (1963) Foraging of the adult three-spined stickleback (Gasterosteus aculeatus L.) in the Kandalaksha Bay of the White Sea. Nauchnye Doklady Vysshey Shkoly 3:31–36 (in Russian) Google Scholar
  2. ACIA (2004) Impacts of a warming Arctic: Arctic Climate Impact Assessment. Cambridge University Press (
  3. Aguirre WE, Akinpelu O (2010) Sexual dimorphism of head morphology in three-spined stickleback Gasterosteus aculeatus. J Fish Biol 77:802–821CrossRefPubMedGoogle Scholar
  4. Aguirre WE, Ellis KE, Kusenda M, Bell MA (2008) Phenotypic variation and sexual dimorphism in anadromous three-spine stickleback: implications for postglacial adaptive radiation. Biol J Linn Soc 95:465–478CrossRefGoogle Scholar
  5. Aneer G (1973) Biometric characteristics of the three-spined stickleback (Gasterosteus aculeatus L.) from the Northern Baltic Proper. Zool Scr 2:157–162CrossRefGoogle Scholar
  6. Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1–58CrossRefGoogle Scholar
  7. Baker JA (1994) Life history variation in female threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 146–187Google Scholar
  8. Baker JA, Foster SA, Heins DC, Bell MA, King RW (1998) Variation in female life-history traits among Alaskan populations of the threespine stickleback, Gasterosteus aculeatus L. (Pisces: Gasterosteidae). Biol J Linn Soc 63:141–159Google Scholar
  9. Baker JA, Heins DC, Foster SA, King RW (2008) An overview of life-history variation in female threespine stickleback. Behaviour 145:579–602CrossRefGoogle Scholar
  10. Bell MA, Foster SA (1994) Introduction to the evolutionary biology of the threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 1–27Google Scholar
  11. Berger V, Naumov A, Zubaha M, Usov N, Smolyar I, Tatusko R, Levitus S (2003) 36-Year time series (1963–1998) of zooplankton, temperature and salinity in the White Sea. Saint Petersburg–Washington, 362 pGoogle Scholar
  12. Berrigan D, Charnov EL (1994) Reaction norms for age and size at maturity in response to temperature: a puzzle for life historians. Oikos 70:474–478CrossRefGoogle Scholar
  13. Bhattacharya CG (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23:115–135CrossRefPubMedGoogle Scholar
  14. Bloum DM, Hagen DW (1990) Breeding ecology and evidence of reproductive isolation of a widespread stickleback fish (Gasterosteidae) in Nova Scotia, Canada. Biol J Linn Soc 39:195–217CrossRefGoogle Scholar
  15. Borg B, van Veen T (1982) Seasonal effects of photoperiod and temperature on the ovary of the three-spined stickleback, Gasterosteus aculeatus L. Can J Zool 60:3387–3393CrossRefGoogle Scholar
  16. Brey T (2001) Population dynamics in benthic invertebrates. A virtual handbook. Version 01.2.
  17. Bugaev VF (1992) Three-spined stickleback Gasterosteus aculeatus from Kamchatka River. Voprosy Ikhtiologii 32:71–82 (in Russian) Google Scholar
  18. Bugaev VF, Vronskiy BB, Zavarzina LO, Zorbidi ZhKh, Ostroumov AG, Tiller IV (2007) Fishes of Kamchatka River. KamchatNIRO, Petropavlovsk-Kamchatskiy (in Russian) Google Scholar
  19. Chronicle of nature by the Kandalaksha Reserve for 1948–2006. Book 2-52. Kandalaksha, Archives of Kandalaksha Nature Reserve (in Russian) Google Scholar
  20. Coad BW, Power G (1973) Observations on the ecology and phenotypic variation of the threespine stickleback, Gasterosteus aculeatus L., 1758, and the blackspotted stickleback, G. wheatlandi Putnam, 1867 (Osteichthyes: Gasterosteidae) in Amory Cove, Quebec. Can Field-Nat 87:113–122Google Scholar
  21. Comiso JC, Parkinson CL, Gersten R, Stock L (2008) Accelerated decline in the Arctic sea ice cover. Geophys Res Lett 35:L01703CrossRefGoogle Scholar
  22. Confer A, Vu V, Drevecky CJ, Aguirre WE (2012) Occurrence of Schistocephalus solidus in anadromous threespine stickleback. J Parasitol 98:676–678CrossRefPubMedGoogle Scholar
  23. Crivelli AJ, Britton RH (1987) Life history adaptations of Gasterosteus aculeatus in a Mediterranean wetland. Environ Biol Fish 18:109–125CrossRefGoogle Scholar
  24. Dufresne F, FitzGerald GJ, Lachance S (1990) Age and size-related differences in reproductive success and reproductive costs in threespine sticklebacks (Gasterosteus aculeatus). Behav Ecol 1:140–147CrossRefGoogle Scholar
  25. Ershov PN (2010) Changes in the diet of the coastal cod Gadus morhua marisalbi in the Kandalaksha Gulf of the White Sea under conditions of increased abundance of three-spined stickleback Gasterosteus aculeatus. J Ichthyol 50:84–88CrossRefGoogle Scholar
  26. Gayanilo FC, Sparre P, Pauly D (2005) FAO-ICLARM Stock Assessment Tools II (FISAT II). Revised version. User’s Guide. FAO, RomeGoogle Scholar
  27. Genner MJ, Sims DW, Southward AJ, Budd GC et al (2010) Body size-dependent responses of a marine assemblage to climate change and fishing over a century-long scale. Glob Change Biol 16:517–527CrossRefGoogle Scholar
  28. Georgiev AP (2014) Processes of alterations of fish fauna in some Karelian lakes as a response to climate change. Nauchniye diskussii 1:27–33 (in Russian) Google Scholar
  29. Gillanders BM, Black BA, Meekan MG, Morrison MA (2012) Climatic effects on the growth of a temperate reef fish from the Southern Hemisphere: a biochronological approach. Mar Biol 159:1327–1333CrossRefGoogle Scholar
  30. Hiddink JG, ter Hofstede R (2008) Climate induced increases in species richness of marine fishes. Glob Change Biol 14:453–460CrossRefGoogle Scholar
  31. Higuchi M, Goto A, Yamazaki F (1996) Genetic structure of threespine stickleback, Gasterosteus aculeatus, in Lake Harutori, Japan, with reference to coexisting anadromous and freshwater forms. Ichthyol Res 43:349–358CrossRefGoogle Scholar
  32. Hutchings JA (2005) Life history consequences of overexploitation to population recovery in Northwest Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 62:824–832CrossRefGoogle Scholar
  33. Jones JW, Hynes HBN (1950) The age and growth of Gasterosteus aculeatus, Pygosteus pungitius and Spinachia vulgaris, as shown by their otoliths. J Anim Ecol 19:59–73CrossRefGoogle Scholar
  34. Karve AD, von Hippel FA, Bell MA (2008) Isolation between sympatric anadromous and resident threespine stickleback species in Mud Lake, Alaska. Environ Biol Fish 81:287–296CrossRefGoogle Scholar
  35. Karve AD, Baker JA, von Hippel FA (2013) Female life-history traits of a species pair of threespine stickleback in Mud Lake, Alaska. Evol Ecol Research 15:171–187Google Scholar
  36. Kitamura T, Kume M, Takahashi H, Goto A (2006) Juvenile bimodal length distribution and sea-run migration of the lower modal group in the Pacific Ocean form of three-spined stickleback. J Fish Biol 69:1245–1250CrossRefGoogle Scholar
  37. Kitano J, Mori S, Peichel CL (2007) Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus). Copeia 2:336–349CrossRefGoogle Scholar
  38. Kume M (2011) Clutch and egg sizes of two migratory forms of the threespine stickleback Gasterosteus aculeatus in eastern Hokkaido, Japan. Zool Stud 50:309–314Google Scholar
  39. Kuznetsov VV, Matveeva TA (1963) On biological specific features of zostera of the White Sea. In: Nikolaev II, Rusanova MN, Kuderskii LA (eds) Problems of use of commercial resources of the White Sea and inland water bodies of Karelia, Issue 1. Akad Nauk SSSR, Moscow, pp 145–149 (in Russian) Google Scholar
  40. L’Abee-Lund JH, Jonsson B, Jensen AJ, Saettem LM, Heggberget TG, Johnson BO, Naesje TF (1989) Latitudinal variation in life-history characteristics of sea-run migrant brown trout Salmo trutta. J Anim Ecol 58:525–542CrossRefGoogle Scholar
  41. Lajus DL, Ivanova TS, Shatskikh EV, Ivanov MV (2013) “Population Waves” of the three-spined stickleback in the White Sea. Priroda 4:43–52 (in Russian) Google Scholar
  42. Michaud WK, Dempson JB, Power M (2010) Changes in growth patterns of wild Arctic charr (Salvelinus alpinus (L.)) in response to fluctuating environmental conditions. Hydrobiologia 650:179–191CrossRefGoogle Scholar
  43. Mori S (1990) Two morphological types in the reproductive stock of three-spined stickleback, Gasterosteus aculeatus, in Lake Harutori, Hokkaido Island. Environ Biol Fish 27:21–31CrossRefGoogle Scholar
  44. Mukhomediyarov FB (1966) Three-spined stickleback (Gasterosteus aculeatus L.) from Kandalaksha Bay of the White Sea. Voprosy Ikhtiologii 6:454–467 (in Russian) Google Scholar
  45. Münzing J (1959) Biologie, Variabilität und Genetik von Gasterosteus aculeatus L. (Pisces) Untersuchungen im Elbegebiet. Internationale Revue der Gesamten Hydrobiologie und Hydrographie 44:317–382 (in German) CrossRefGoogle Scholar
  46. Narver DW (1969) Phenotypic variation in threespine sticklebacks (Gasterosteus aculeatus) of the Chignik river system, Alaska. J Fish Res Board Can 26:405–412CrossRefGoogle Scholar
  47. Ottersen G, Hjermann D, Stenseth NC (2006) Changes in spawning stock structure strengthen the link between climate and recruitment in a heavily fished cod (Gadus morhua) stock. Fish Oceanogr 15:230–243CrossRefGoogle Scholar
  48. Patimar R, Najafabadi MH, Souraki MG (2010) Life history features of the nonindigenous three-spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) in the Gomishan wetland (southeast Caspian Sea, Iran). Turk J Zool 34:461–470Google Scholar
  49. Pennycuick L (1971) Quantitative effects of three species of parasites on a population of three-spined sticklebacks, Gasterosteus aculeatus. J Zool 165:143–162CrossRefGoogle Scholar
  50. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefPubMedGoogle Scholar
  51. Peterson BJ, Holmes RM, McClelland JW, Vorosmarty CJ, Lammers RB, Shiklomanov AI, Shiklomanov IA, Rahmstorf S (2002) Increasing river discharge to the Arctic Ocean. Science 298:2171–2173CrossRefPubMedGoogle Scholar
  52. Pichugin MYu, Pavlov DS, Savvaitova KA (2008) Life cycle and structure of populations of three-spined stickleback Gasterosteus aculeatus (fam. Gasterosteidae) in rivers of northwestern Kamchatka (with reference to the Utkholok river). J Ichthyol 48:151–161CrossRefGoogle Scholar
  53. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefPubMedGoogle Scholar
  54. Reist JD, Wrona FJ, Prowse TD, Power M, Dempson JB, Beamish RJ, King JR, Carmichael TJ, Sawatzky CD (2006) General effects of climate change on Arctic fishes and fish populations. Ambio 35:370–380CrossRefPubMedGoogle Scholar
  55. Saat T, Turovski A (2003) Three-spined stickleback, Gasterosteus aculeatus L. In: Ojaveer E, Pihu E, Saat T (eds) Fishes of Estonia. Estonian Academy Publishers, Tallinn, pp 274–280Google Scholar
  56. Saimoto RK (1993) Life-history of marine threespine stickleback in Oyster lagoon, British Columbia. M.Sc. Thesis, University of British ColumbiaGoogle Scholar
  57. Snyder RJ (1991) Migration and life histories of the threespine stickleback: evidence for adaptive variation in growth rate between populations. Environ Biol Fish 31:381–388CrossRefGoogle Scholar
  58. Stige LC, Ottersen G, Dalpadado P, Chan KS, Hjermann D, Lajus DL, Yaragina NA, Stenseth NC (2010) Direct and indirect climate forcing in a multispecies marine system. Proc Biol Sci 277:3411–3420PubMedCentralCrossRefPubMedGoogle Scholar
  59. Stolarski JT (2013) Growth and energetic condition of Dolly Varden char in coastal arctic waters. Ph.D. Dissertation, University of Alaska FairbanksGoogle Scholar
  60. Thresher RE, Koslow JA, Morison AK, Smith DC (2007) Depth-mediated reversal of the effects of climate change on long-term growth rates of exploited marine fish. Proc Natl Acad Sci USA 104:7461–7465PubMedCentralCrossRefPubMedGoogle Scholar
  61. Usov N, Kutcheva I, Primakov I, Martynova D (2013) Every species is good in its season: do the shifts in the annual temperature dynamics affect the phenology of the zooplankton species in the White Sea? Hydrobiologia 706:11–33CrossRefGoogle Scholar
  62. van Mullem PJ, van der Vlugt JC (1964) On the age, growth and migration of anadromous stickleback Gasterosteus aculeatus L. investigated in mixed populations. Archives Neerlandaises de Zoologie 16:111–139CrossRefGoogle Scholar
  63. Vebel A (1934) The White Sea stickleback as a target species. For the fishing industry of the North 10:176–188 (in Russian) Google Scholar
  64. von Biela VR, Zimmerman CE, Moulton LL (2011) Long-term increases in young-of-the-year growth of arctic cisco Coregonus autumnalis and environmental influences. J Fish Biol 78:39–56CrossRefGoogle Scholar
  65. von Hippel FA, Weigner H (2004) Sympatric anadromous-resident pairs of threespine stickleback species in young lakes and streams at Bering Glacier, Alaska. Behaviour 141:1441–1464CrossRefGoogle Scholar
  66. Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, LondonCrossRefGoogle Scholar
  67. Yershov PN (2010) Long-term changes in the food composition of the shorthorn sculpin Myoxocephalus scorpius (Linnaeus, 1758) in the Kandalaksha Bay of the White Sea. Vestnik SPBGU 2:55–62 (in Russian) Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.White Sea Biological Station, Zoological InstituteRussian Academy of Sciences (RAS)Saint PetersburgRussia
  2. 2.Saint Petersburg State UniversitySaint PetersburgRussia

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