Marine Biology

, Volume 151, Issue 1, pp 393–400 | Cite as

The indirect effects of eutrophication on habitat choice and survival of fish larvae in the Baltic Sea

  • Jonna Engström-ÖstEmail author
  • Emmi Immonen
  • Ulrika Candolin
  • Johanna Mattila
Research Article


The structure of the habitat is usually crucial for growth and survival of young life stages. Presently, some nursery areas of fish larvae are changing due to eutrophication, e.g. due to enhanced growth of ephemeral filamentous algae at the expense of perennial species. We studied the influence of two habitats, one with filamentous algae (Cladophora glomerata) and the other with bladder wrack (Fucus vesiculosus), on habitat choice of pike larvae (Esox lucius) in the absence/presence of a predator or a competitor. We further tested whether the habitat choice is adaptive in increasing survival under predation threat. In contrast to expectations, pike larvae preferred the habitat with ephemeral filamentous algae to the bladder wrack, thriving in clean waters, independent of the presence/absence of both predator/competitor. In addition, the survival of the larvae was higher in the filamentous algae in the presence of predators, which suggested that the habitat preference of the larvae was adaptive. The structure of the bladderwrack habitat was probably too open for newly hatched larvae, which implies that F. vesiculosus and other large brown algae are not as important refuges for young larvae as previously thought.


Macroalgae Predation Risk Filamentous Alga Habitat Choice Predation Threat 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We wish to thank two reviewers for valuable comments on the manuscript. H. Strandberg gave us the pike larvae. M. Lehtiniemi taught us stomach analysis. M. Viitasalo purchased the fish tanks. A.-M. Åström weighed the algae. M. Öst showed us how to use the condition index and helped with statistical issues. J. Lindeberg was responsible for animal care. Tvärminne Zoological Station provided working facilities and accommodation. We greatly acknowledge funding from the Academy of Finland (to J.E.-Ö.) (project no. 202382), and Walter and Andrée de Nottbeck Foundation (to E.I.). The experiments comply with current laws of Finland. Animal welfare was respected during all stages of the study. Permission (no. 69–04) was granted by the Animal Care Committee at the University of Helsinki, Finland.


  1. Amaral ACZ, Jablonski S (2005) Conservation of marine and coastal biodiversity in Brazil. Cons Biol 19:625–631CrossRefGoogle Scholar
  2. Aneer G (1987) High natural mortality of Baltic herring (Clupea harengus) eggs caused by algal exudates? Mar Biol 94:163–169. DOI 10.1007/BF00392928CrossRefGoogle Scholar
  3. Armbruster P, Lande R (1993) A population viability analysis for African elephant (Loxodonta africana)—how big should reserves be? Cons Biol 7:602–610CrossRefGoogle Scholar
  4. Borg Å, Pihl L, Wennhage H (1997) Habitat choice by juvenile cod (Gadus morhua L.) on sandy soft bottoms with different vegetation types. Helgoländer Meeresunters 51:197–212CrossRefGoogle Scholar
  5. Candolin U, Voigt H-R (1998) Predator-induced nest site preference: safe nests allow courtship in sticklebacks. Anim Behav 56:1205-1211. DOI 10.1006/anbe.1998.0892CrossRefGoogle Scholar
  6. Casselman JM (1996) Age, growth and environmental requirements of pike. In: Craig JF (ed) Pike—biology and exploitation. Chapman & Hall, London, pp 70–101Google Scholar
  7. Casselman JM, Lewis CA (1996) Habitat requirements of northern pike (Esox lucius). Can J Fish Aquat Sci 53(Suppl 1):161–174CrossRefGoogle Scholar
  8. Connor EF, McCoy ED (1979) The statistics and biology of the species–area relationship. Am Nat 113:791–833CrossRefGoogle Scholar
  9. Craig JF (ed) (1996) Pike—biology and exploitation, 1st edn. Chapman & Hall, LondonGoogle Scholar
  10. Craig JF, Babaluk JA (1989) Relationship of condition of walleye (Stizostedion vitreum) and northern pike (Esox lucius) to water clarity, with special reference to Dauphin Lake, Manitoba. Can J Fish Aquat Sci 46:1581–1586CrossRefGoogle Scholar
  11. Diehl S (1988) Foraging efficiency of three freshwater fishes: effects of structural complexity and light. Oikos 53:207–214CrossRefGoogle Scholar
  12. Downes BJ, Lake PS, Schreiber ESG, Glaister A (1998) Habitat structure and regulation of local species diversity in a stony, upland stream. Ecol Monogr 68:237–257CrossRefGoogle Scholar
  13. Eklöv P, Diehl S (1994) Piscivore efficiency and refuging prey: the importance of predator search mode. Oecologia 98:344–353. DOI 10.1007/BF00324223CrossRefGoogle Scholar
  14. Engström-Öst J, Isaksson I (2006) Effects of macroalgal exudates and oxygen deficiency on survival and behaviour of fish larvae. J Exp Mar Biol Ecol 335:227–234. DOI 10.1016/j.jembe.2006.03.007CrossRefGoogle Scholar
  15. Engström-Öst J, Lehtiniemi M (2004) Threat-sensitive predator avoidance by pike larvae. J Fish Biol 65:251–261. DOI 10.1111/j.0022-1112.2004.00448.xCrossRefGoogle Scholar
  16. Engström-Öst J, Lehtiniemi M, Jónasdóttir SH, Viitasalo M (2005) Growth of pike larvae (Esox lucius) under different conditions of food quality and salinity. Ecol Freshwat Fish 14:385–393. DOI 10.1111/j.1600-0633.2005.00113.xCrossRefGoogle Scholar
  17. Flynn AJ, Ritz DA (1999) Effect of habitat complexity and predator style on capture success of fish feeding on aggregated prey. J Mar Biol Ass UK 79:487–494CrossRefGoogle Scholar
  18. Isaksson I, Pihl L (1992) Structural changes in benthic macrovegetation and associated epibenthic faunal communities. Neth J Sea Res 30:131–140CrossRefGoogle Scholar
  19. Isaksson I, Pihl L, van Montfrans J (1994) Eutrophication-related changes in macrovegetation and foraging of young cod (Gadus morhua L.): a mesocosm experiment. J Exp Mar Biol Ecol 177:203–217. DOI 10.1016/0022-0981(94)90237-2CrossRefGoogle Scholar
  20. Johnson DA, Welsh BL (1985) Detrimental effects of Ulva lactuca (L.) exudates and low oxygen on estuarine crab larvae. J Exp Mar Biol Ecol 86:73–83. DOI 10.1016/0022-0981(85)90043-7CrossRefGoogle Scholar
  21. Kohn AJ, Leviten PJ (1976) Effect of habitat complexity on population density and species richness in tropical intertidal predatory gastropod assemblages. Oecologia 25:199–210. DOI 10.1007/BF00345098CrossRefGoogle Scholar
  22. Koivula K, Rönkä A (1998) Habitat deterioration and efficiency of antipredator strategy in a meadow-breeding wader, Temminck’s stint (Calidris temminckii). Oecologia 116:348–355. DOI 10.1007/s004420050597CrossRefGoogle Scholar
  23. Lappalainen A (2002) The effects of recent eutrophication on freshwater fish communities and fishery on the northern coast of the Gulf of Finland, Baltic Sea. PhD Thesis, University of Helsinki, 24 pGoogle Scholar
  24. Leger DW, Didrichsons IA (1994) An assessment of data pooling and some alternatives. Anim Behav 48:823–832. DOI 10.1006/anbe.1994.1306CrossRefGoogle Scholar
  25. Lehtiniemi M (2005) Swim or hide—predator cues cause species specific reactions in young fish larvae. J Fish Biol 66:1285–1299. DOI 10.1111/j.0022-1112.2005.00681.xCrossRefGoogle Scholar
  26. Lehtonen H (1986) Fluctuations and long-term trends in the pike Esox lucius (L.) population in Nothamn, western Gulf of Finland. Aqua Fenn 16:3–9Google Scholar
  27. Lemmetyinen R, Mankki J (1975) The three-spined stickleback (Gasterosteus aculeatus) in the food chain of the northern Baltic Sea. Merentutkimuslait Julk/Havsforskningsinst Skr 239:155–161Google Scholar
  28. Lindén E, Lehtiniemi M, Viitasalo M (2003) Predator avoidance behaviour of Baltic littoral mysids Neomysis integer and Praunus flexuosus. Mar Biol 143:845–850. DOI 10.1007/s00227-003-1149-xCrossRefGoogle Scholar
  29. Milinski M (1986) Constraints placed by predators on feeding behaviour. In: Pitcher TJ (ed) The behaviour of teleost fishes. John Hopkins University Press, Baltimore, pp 236–252CrossRefGoogle Scholar
  30. Moksnes P-O, Pihl L, van Montfrans J (1998) Predation on postlarvae and juveniles of the shore crab Carcinus maenas: importance of shelter, size and cannibalism. Mar Ecol Prog Ser 166:211–225CrossRefGoogle Scholar
  31. Nilsson J, Andersson J, Karås P, Sandström O (2004) Recruitment failure and decreasing catches of perch (Perca fluviatilis L.) and pike (Esox lucius L.) in the coastal waters of southeast Sweden. Boreal Environ Res 9:295–306Google Scholar
  32. Norkko J, Bonsdorff E, Norkko A (2000) Drifting algal mats as an alternative habitat for benthic invertebrates: Species-specific responses to a transient resource. J Exp Mar Biol Ecol 248:79–104. DOI 10.1016/S0022-0981(00)00155-6CrossRefGoogle Scholar
  33. Ojaveer E, Lindroth A, Bagge O, Lehtonen H, Toivonen J (1981) Fishes and fisheries. In: Voipio A (ed) The Baltic Sea. Elsevier, Amsterdam, pp 275–350CrossRefGoogle Scholar
  34. Ormerod SJ, Tyler SJ (1990) Assessments of body condition in dippers Cinclus cinclus: potential pitfalls in the derivation and use of condition indices based on body proportions. Ring Migr 11:31–41CrossRefGoogle Scholar
  35. Pedersen BH (1997) The cost of growth in young fish larvae, a review of new hypotheses. Aquaculture 155:259–269CrossRefGoogle Scholar
  36. Persson L, Crowder LB (1997) Fish-habitat interactions mediated via ontogenetic niche shifts. Ecol Stud Ser 131:3–23Google Scholar
  37. Pöyry J, Lindgren S, Salminen J, Kuussaari M (2005) Responses of butterfly and moth species to restored cattle grazing in semi-natural grasslands. Biol Cons 122:465–478CrossRefGoogle Scholar
  38. Roast SD, Widdows J, Pope N, Jones MB (2004) Sediment-biota interactions: Mysid feeding activity enhances water turbidity and sediment erodability. Mar Ecol Prog Ser 281:145–154CrossRefGoogle Scholar
  39. Rudstam LG, Hansson S, Larsson U (1986) Abundance, species composition and production of mysid shrimps in a coastal area of the northern Baltic proper. Ophelia Suppl 4:225–238Google Scholar
  40. Salovius-Laurén S (2004) Drifting and attached macroalgae: distribution, degradation and utility for macroinvertebrates. PhD Thesis, Åbo Akademi University, 36 pGoogle Scholar
  41. Selén R (1999) Haukikannan muutokset läntisen Suomenlahden ulkosaaristossa 1939–1996 - Tutkimuskohteena Nothamnin saaristoalueen haukikanta (in Finnish). MSc Thesis, Univ Helsinki, 47 p Google Scholar
  42. Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. Trends Ecol Evol 12:375–376CrossRefGoogle Scholar
  43. Skov C, Berg S, Jacobsen L, Jepsen N (2002) Habitat use and foraging success of 0+ pike (Esox lucius L.) in experimental ponds related to prey fish, water transparency and light intensity. Ecol Freshwat Fish 11:65–73. DOI 10.1034/j.1600-0633.2002.00008.xCrossRefGoogle Scholar
  44. Skov C, Jacobsen L, Berg S (2003) Post-stocking survival of 0+ pike in ponds as a function of water transparency, habitat complexity, prey availability and size heterogeneity. J Fish Biol 62:311–322. DOI 10.1046/j.1095-8649.2003.00023.xCrossRefGoogle Scholar
  45. Sokal RR, Rohlf FJ (1995) Biometry. W.H. Freeman and Company, New YorkGoogle Scholar
  46. Vøllestad LA, Skurdal J, Qvenild T (1986) Habitat use, growth, and feeding of pike (Esox lucius L.) in four Norwegian lakes. Arch Hydrobiol 108:107–117Google Scholar
  47. Wallentinus I (1984) Comparisons of nutrient uptake rates for Baltic macro-algae with different thallus morphologies. Mar Biol 80:215–225. DOI 10.1007/BF02180189CrossRefGoogle Scholar
  48. Wennhage H, Pihl L (1994) Substratum selection by juvenile plaice (Pleuronectes platessa L.): impact of benthic microalgae and filamentous macroalgae. Neth J Sea Res 32:343–351CrossRefGoogle Scholar
  49. Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548CrossRefGoogle Scholar
  50. Werner RG (2002) Habitat requirements. In: Fuiman LA, Werner RG (eds) Fishery science—the unique contributions of early life stages. Blackwell, Oxford, pp 161–182Google Scholar
  51. Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, London & SidneyCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Jonna Engström-Öst
    • 1
    Email author
  • Emmi Immonen
    • 2
  • Ulrika Candolin
    • 3
  • Johanna Mattila
    • 4
  1. 1.Finnish Institute of Marine ResearchHelsingforsFinland
  2. 2.Environmental and Marine BiologyÅbo Akademi UniversityÅboFinland
  3. 3.Department of Ecology and EvolutionUppsala UniversityUppsalaSweden
  4. 4.Husö Biological Station and Environmental and Marine BiologyÅbo Akademi UniversityÅboFinland

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