Estuaries and Coasts

, Volume 41, Issue 2, pp 549–559 | Cite as

Impact of Spawning Substrate Complexity on Egg Survival of Atlantic Herring (Clupea harengus, L.) in the Baltic Sea

  • Lena von Nordheim
  • Paul Kotterba
  • Dorothee Moll
  • Patrick Polte


Shallow shore zones are generally considered to provide juvenile habitats for many invertebrate and fish species and additionally serve as spawning grounds for important components of oceanic food webs and fishery resources such as herring (Clupea spp.). Herring attach their demersal eggs to benthic substrates, rendering reproduction success vulnerable to environmental changes and local habitat alterations. However, little information is available on the effects of different substrates on the survival of demersal eggs. Hypothesizing that the structural complexity of spawning substrates generally affects herring egg survival and that the effect magnitude depends on the suitability of ambient environment, field experiments were conducted on a major spawning ground of C. harengus in the Southwestern Baltic Sea. Herring eggs were artificially spawned on substrates of different structural complexities and incubated in situ under differing temperature regimes, at the beginning and the end of the natural herring spawning season, to include the full suite of stressors occurring on littoral spawning beds. Results of this study indicate a positive relation between high structural complexity of spawning substrates and herring egg survival. Mean egg mortality was three times higher on substrates of lowest complexity than on highly complex substrates. These differences became even more prominent under unfavorable conditions that appeared with rising water temperatures later in the spawning season. Although the mechanisms are still unclear, we conclude that structural complexity, particularly formed by submerged aquatic vegetation, provides a crucial prerequisite for the successful reproduction of substrate spawning marine fishes such as herring in the Baltic Sea.


Clupea harengus Coastal spawning grounds Structural complexity Egg mortality Spawning substrate Baltic Sea herring 



We thank all colleagues from the Thuenen Institute of Baltic Sea Fisheries who assisted with laboratory and field work and particularly Kate McQueen for correcting the English. Thanks are extended to the crew of the research vessel “FRV Clupea” and Stefan Forster and Holger Pielenz, University of Rostock. The authors thank the marina Im Jaich, Lauterbach for their logistical support. The research leading to these results has received funding from the German Federal Environmental Foundation (DBU), the BONUS projects BIO-C3 and INSPIRE (both funded jointly by the EU and the Federal Ministry of Education and Research of Germany (BMBF 03F0681; 03F0682), and the EU Data Collection Framework (DCF).

Supplementary material

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ESM 1 (DOCX 1.39 mb).


  1. Aneer, G. 1987. High natural mortality of Baltic herring (Clupea harengus) eggs caused by algal exudates? Marine Biology 94 (2): 163–169.CrossRefGoogle Scholar
  2. Aneer, G. 1989. Herring (Clupea harengus L.) spawning and spawning ground characteristics in the Baltic Sea. Fisheries Research 8 (2): 169–195.CrossRefGoogle Scholar
  3. Aneer, G., and S. Nellbring. 1982. A SCUBA-diving investigation of Baltic herring (Clupea harengus membras L.) spawning grounds in the Askö-Landsort area, northern Baltic proper. Journal of Fish Biology 21 (4): 433–442.CrossRefGoogle Scholar
  4. Aneer, G., G. Florell, U. Kautsky, S. Nellbring, and L. Sjöstedt. 1983. In-situ observations of Baltic herring (Clupea harengus membras) spawning behaviour in the Askö-Landsort area, northern Baltic proper. Marine Biology 74 (2): 105–110.CrossRefGoogle Scholar
  5. Angel, A., and F.P. Ojeda. 2001. Structure and trophic organization of subtidal fish assemblages on the northern Chilean coast: the effect of habitat complexity. Marine Ecology Progress Series 217: 81–91.CrossRefGoogle Scholar
  6. Apstein, C. 1909. Die Bestimmung des Alters pelagisch lebender Fischeier. Mitteilungen des deutschen Seefischereivereins 25: 364–373 [Age determination of pelagic fish eggs.]Google Scholar
  7. Aro, E. 1989. A review of fish migration patterns in the Baltic. Rapports et Procès-verbaux des Réunions du Conseil International pour l'Exploration de la Mer 190: 72–96.Google Scholar
  8. Balon, E.K. 1975. Reproductive guilds of fishes: a proposal and definition. Journal of the Fisheries Board of Canada 32 (6): 821–864.CrossRefGoogle Scholar
  9. Beck, M.W., K.L. Heck Jr., K.W. Able, D.L. Childers, D.B. Eggleston, B.M. Gillanders, B. Halpern, C.G. Hays, K. Hoshino, T.J. Minello, R.J. Orth, P.F. Sheridan, and M.P. Weinstein. 2001. The identification, conservation, and management of estuarine and marine nurseries for fish and invertebrates. Bioscience 51 (8): 633–641.CrossRefGoogle Scholar
  10. Blaxter, J.H.S. 1956. Herring rearing II—the effect of temperature and other factors on development. Marine Research Scotland 5: 2–19.Google Scholar
  11. Blaxter, J.H.S., and G. Hempel. 1961. Biologische Beobachtungen bei der Aufzucht von Herringsbrut. Helgoländer Wissenschaftliche Meeresuntersuchungen 7: 260–283 [Biological observations during the rearing of herring offspring.]CrossRefGoogle Scholar
  12. Blaxter, J.H.S., and G. Hempel. 1963. The influence of egg size on herring larvae (Clupea harengus L.). Journal du Conseil 28 (2): 211–240.CrossRefGoogle Scholar
  13. Blaxter, J.H.S., and F.G.T. Holliday. 1963. The behaviour and physiology of herring and other clupeoids. Advances in Marine Biology 1: 261–393.CrossRefGoogle Scholar
  14. Braum, E. 1973. Einflüsse chronischen exogenen Sauerstoffmangels auf die Embryogenese des Herings (Clupea harengus). Netherlands Journal of Sea Research 7: 363–375 [Influence of chronical exogenic oxygen deficiency on the embryogenesis of herring (Clupea harengus).]CrossRefGoogle Scholar
  15. Bricker, S., B. Longstaff, W. Dennison, A. Jones, K. Boicourt, C. Wicks, and J. Woerner. 2007. Effects of nutrient enrichment in the nation’s estuaries: a decade of change. NOAA Coastal Ocean Program Decision Analysis Series 26: 328.Google Scholar
  16. Caddy, J.F. 2007. Marine habitat and cover: their importance for productive coastal fishery resources. UNESCO Publishing.Google Scholar
  17. de Groot, S.J. 1980. The consequences of marine gravel extraction on the spawning of herring, Clupea harengus Linné. Journal of Fish Biology 16 (6): 605–611.CrossRefGoogle Scholar
  18. Dethier, M.N., E.S. Graham, S. Cohen, and L.M. Tear. 1993. Visual versus random-point percent cover estimations: ‘objective’ is not always better. Marine ecology progress series, 96(9).Google Scholar
  19. Dibble, E.D., K.J. Killgore, and G.O. Dick. 1996. Measurement of plant architecture in seven aquatic plants. Journal of Freshwater Ecology 11: 311–318.CrossRefGoogle Scholar
  20. Dionne, M., and C.L. Folt. 1991. An experimental analysis of macrophyte growth forms as fish foraging habitat. Canadian Journal of Fisheries and Aquatic Sciences 48 (1): 123–131.CrossRefGoogle Scholar
  21. Duarte, C.M. 1995. Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41 (1): 87–112.CrossRefGoogle Scholar
  22. Dutilleul, P., P. Clifford, S. Richardson, and D. Hemon. 1993. Modifying the t test for assessing the correlation between two spatial processes. Biometrics 49: 305–314.CrossRefGoogle Scholar
  23. Geffen, A.J., and R.D. Nash. 2012. Egg development rates for use in egg production methods (EPMs) and beyond. Fisheries Research 117: 48–62.CrossRefGoogle Scholar
  24. Gratwicke, B., and M.R. Speight. 2005. The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. Journal of Fish Biology 66: 650–667.CrossRefGoogle Scholar
  25. Haegele, C.W., and J.F. Schweigert. 1985. Distribution and characteristics of herring spawning grounds and description of spawning behavior. Canadian Journal of Fisheries and Aquatic Sciences 42 (S1): 39–55.CrossRefGoogle Scholar
  26. Hay, D.E. 1985. Reproductive biology of Pacific herring (Clupea harengus pallasi). Canadian Journal of Fisheries and Aquatic Sciences 42 (S1): 111–126.CrossRefGoogle Scholar
  27. Heck, K.L., Jr., and R.J. Orth. 1980. Seagrass habitats: the roles of habitat complexity, competition and predation in structuring associated fish and motile macroinvertebrate assemblages. In Estuarine perspectives, 449–464. Academic Press.Google Scholar
  28. Heck, K.L., Jr., G. Hays, and R.J. Orth. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Marine Ecology Progress Series 253: 123–136.CrossRefGoogle Scholar
  29. Hyndes, G.A., J.A. Kendrick, L.D. MacArthur, and E. Stewart. 2003. Differences in the species- and size-composition of fish assemblages in three distinct seagrass habitats with differing plant and meadow structure. Marine Biology 142 (6): 1195–1206.CrossRefGoogle Scholar
  30. Jackson, E.L., A.A. Rowden, M.J. Attrill, S.J. Bossey, and M.B. Jones. 2001. The importance of seagrass beds as a habitat for fishery species. Oceanography and Marine Biology 39: 269–304.Google Scholar
  31. Kanstinger, P., J. Beher, G. Grenzdörffer, C. Hammer, K.B. Huebert, D. Stepputis, and M.A. Peck. 2016. What is left? Macrophyte meadows and Atlantic herring (Clupea harengus) spawning sites in the Greifswalder Bodden, Baltic Sea. Estuarine, Coastal and Shelf Science. doi: 10.1016/j.ecss.2016.03.004.
  32. Klinkhardt, M. 1984. Zum Einfluss des Salzgehaltes auf die Befruchtungsfähigkeit des Laiches der Rügenschen Frühjahrsheringe. Fischerei-Forschung Rostock 22 (3): 73–75 [On the influence of salinity on fertilization success of Ruegen spring herring spawn.]Google Scholar
  33. Klinkhardt, M. 1986. Gedanken zur Abhängigkeit der Laichentwicklung Rügenscher Frühjahrsheringe (Clupea harengus L.) von Umweltparametern. Fischerei-Forschung 24: 22–27 [Dependence of Ruegen spring herring egg development on environmental parameters.]Google Scholar
  34. Klinkhardt, M. 1996. Der Hering: Clupea harengus (Vol. 199). Spektrum Akademischer Verlag. [The herring: Clupea harengus.].Google Scholar
  35. Klinkhardt, M., and E. Biester. 1984. Erste Ergebnisse von experimentellen Felduntersuchungen am Laich von Rügenschen Frühjahrsheringen. Fischerei-Forschung Rostock 22 (3): 76–78 [First results of experimental field studies on spawn of Ruegen spring herring.]Google Scholar
  36. Kotterba, P., C. Kühn, C. Hammer, and P. Polte. 2014. Predation of threespine stickleback (Gasterosteus aculeatus) on the eggs of Atlantic herring (Clupea harengus) in a Baltic Sea lagoon. Limnology and Oceanography 59 (2): 578–587.CrossRefGoogle Scholar
  37. Kotterba, P., D. Moll, C. Hammer, M.A. Peck, D. Oesterwind, and P. Polte. 2017. Predation on Atlantic herring (Clupea harengus) eggs by the resident predator community in coastal transitional waters. Limnology and Oceanography. doi: 10.1002/lno.10594.
  38. Kovalenko, K.E., S.M. Thomaz, and D.M. Warfe. 2012. Habitat complexity: approaches and future directions. Hydrobiologia 685: 1–17.CrossRefGoogle Scholar
  39. Lillie, R.A., and J. Budd. 1992. Habititat architecture of Myriophyllum spicatum L. as an index to habitat quality for fish and macroinvertebrates. Journal of Freshwater Ecology 7 (2): 113–125.CrossRefGoogle Scholar
  40. Mann, H.B., and D.R. Whitney. 1947. On a test of whether one of two random variables is stochastically larger than the other. The annals of mathematical statistics: 50–60.Google Scholar
  41. Maravelias, C.D., D.G. Reid, and G. Swartzman. 2000. Seabed substrate, water depth and zooplankton as determinants of the prespawning spatial aggregation of North Atlantic herring. Marine Ecology Progress Series 195: 249–259.CrossRefGoogle Scholar
  42. Meese, R.J., and P.A. Tomich. 1992. Dots on the rocks: a comparison of percent cover estimation methods. Journal of Experimental Marine Biology and Ecology 165 (1): 59–73.CrossRefGoogle Scholar
  43. Munkes, B. 2005a. Eutrophication, phase shift, the delay and the potential return in the Greifswalder Bodden, Baltic Sea. Aquatic Sciences 67 (3): 372–381.CrossRefGoogle Scholar
  44. Munkes, B. 2005b. Seagrass systems: stability of seagrass systems against anthropogenic impacts (Doctoral dissertation, Christian-Albrechts Universität Kiel).Google Scholar
  45. Nagelkerken, I., M. Sheaves, R. Baker, and R.M. Connolly. 2015. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish and Fisheries 16 (2): 362–371.CrossRefGoogle Scholar
  46. Oeberst, R., B. Klenz, T. Gröhsler, M. Dickey-Collas, R.D. Nash, and C. Zimmermann. 2009. When is year-class strength determined in western Baltic herring? ICES Journal of Marine Science: Journal du Conseil 66 (8): 1667–1672.CrossRefGoogle Scholar
  47. Ojaveer, E. 1981a. On embryonal mortality of spring spawning herring on spawning grounds in the northeasrern Gulf of Riga. Rapports et procès-verbaux des réunions / Conseil permanent international pour l'exploration de la mer 178: 401.Google Scholar
  48. Ojaveer, E. 1981b. Influence of temperature, salinity, and reproductive mixing of Baltic herring groups on its embryonal development. Rapports et procès-verbaux des réunions / Conseil permanent international pour l'exploration de la mer 178: 409–415.Google Scholar
  49. Orth, R.J., T.J. Carruthers, W.C. Dennison, C.M. Duarte, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, S. Olyarnik, F.T. Short, M. Waycott, and S.L. Williams. 2006. A global crisis for seagrass ecosystems. Bioscience 56 (12): 987–996.CrossRefGoogle Scholar
  50. Oulasvirta, P., J. Rissanen, and R. Parmanne. 1985. Spawning of Baltic herring (Clupea harengus L.) in the western part of the Gulf of Finland. Finnish Fisheries Research 5: 41–54.Google Scholar
  51. Parrish, B.B., and A. Saville. 1965. The biology of the north-east Atlantic herring populations. Oceanography and Marine Biology: An Annual Review 3: 323–373.Google Scholar
  52. Parrish, B.B., A. Saville, R.E. Craig, I.G. Baxter, and R. Priestley. 1959. Observations on herring spawning and larval distribution in the Firth of Clyde in 1958. Journal of the Marine Biological Association of the United Kingdom 38 (3): 445–453.CrossRefGoogle Scholar
  53. Peck, M.A., P. Kanstinger, L. Holste, and M. Martin. 2012. Thermal windows supporting survival of the earliest life stages of Baltic herring (Clupea harengus). ICES Journal of Marine Science: Journal du Conseil 69 (4): 529–536.CrossRefGoogle Scholar
  54. Petr, T. 2000. Interactions between fish and aquatic macrophytes in inland waters. A review. FAO Fisheries Technical Paper 396: 185.Google Scholar
  55. Polte, P., and H. Asmus. 2006. Intertidal seagrass beds (Zostera noltii) as spawning grounds for transient fishes in the Wadden Sea. Marine Ecology Progress Series 312: 235–243.CrossRefGoogle Scholar
  56. Polte, P., P. Kotterba, C. Hammer, and T. Gröhsler. 2014. Survival bottlenecks in the early ontogenesis of Atlantic herring (Clupea harengus, L.) in coastal lagoon spawning areas of the western Baltic Sea. ICES Journal of Marine Science: Journal du Conseil 71 (4): 982–990.CrossRefGoogle Scholar
  57. Rajasilta, M., J. Eklund, J. Hänninen, M. Kurkilahti, J. Kääriä, P. Rannikko, and M. Soikkeli. 1993. Spawning of herring (Clupea harengus membras L.) in the Archipelago Sea. ICES Journal of Marine Science, 50 (3): 233–246.Google Scholar
  58. Rajasilta, M., J. Eklund, J. Kääriä, and K. Ranta-Aho. 1989. The deposition and mortality of the eggs of the Baltic herring, Clupea harengus membras L., on different substrates in the south-west archipelago of Finland. Journal of Fish Biology 34 (3): 417–427.CrossRefGoogle Scholar
  59. Rajasilta, M., P. Laine, and J. Eklund. 2006a. Mortality of herring eggs on different algal substrates (Furcellaria spp. and Cladophora spp.) in the Baltic Sea—an experimental study. Hydrobiologia 554 (1): 127–130.CrossRefGoogle Scholar
  60. Rajasilta, M., J. Eklund, P. Laine, N. Jönsson, and T. Lorenz. 2006b. Intensive monitoring of spawning populations of the Baltic herring (Clupea harengus membras L.). Final report of the study project ref 96-068: 1997–1999.Google Scholar
  61. Rannak, L. 1971. On recruitment to the stock of spring herring in the north-eastern Baltic. Rapports et procès-verbaux des réunions / Conseil permanent international pour l'exploration de la mer 160: 76–82.Google Scholar
  62. Reinicke, R. 1989. Der Greifswalder Bodden - geographisch - geologischer Überblick, Morphogenese und Küstendynamik. Schriftreihe des Meeresmuseums Stralsund, Band 5: 3–9 [Greifswald Bay - geographic - geologic overview, morphogenesis and coastal dynamics.]Google Scholar
  63. Scabell, J. 1988. Der Rügensche Frühjahrshering - das Laichgeschehen (Doctoral dissertation, University of Rostock). [Ruegen spring herring – the spawning event.]Google Scholar
  64. Schiewer, U. 2001. Salzhaff, Greifswalder Bodden, Darß-Zingster Boddenkette: Gewässereutrophierung und Pufferkapazität – ein Vergleich. Rostocker Meeresbiologische Beiträge 9: 5–19 [Salzhaff, Greifswald Bay, Darß-Zingster Boddenkette: Water eutrophication and buffering capacity—a comparison.]Google Scholar
  65. Sheaves, M., R. Baker, I. Nagelkerken, and R.M. Connolly. 2015. True value of estuarine and coastal nurseries for fish: incorporating complexity and dynamics. Estuaries and Coasts 38 (2): 401–414.CrossRefGoogle Scholar
  66. Sinclair, M., and M.J. Tremblay. 1984. Timing of spawning of Atlantic herring (Clupea harengus harengus) populations and the match-mismatch theory. Canadian Journal of Fisheries and Aquatic Sciences 41 (7): 1055–1065.CrossRefGoogle Scholar
  67. Stigge, H. 1989. Der Wasserkörper Bodden und seine Hydrodynamik. Der Greifswalder Bodden. Schriftenreihe des Meeresmuseums Stralsund, Band 5: 10–14 [The waterbody of Greifswald Bay and its hydrodynamic.]Google Scholar
  68. Thiriet, P., A. Cheminée, L. Mangialajo, and P. Francour. 2014. How 3D complexity of macrophyte-formed habitats affect the processes structuring fish assemblages within coastal temperate seascapes. In Underwater Seascape, 185–199. Springer International Publishing.Google Scholar
  69. Waycott, M., C.M. Duarte, T.J. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladinea, J.W. Fourqurean, K.L. Heck Jr., A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences 106 (30): 12377–12381.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2017

Authors and Affiliations

  • Lena von Nordheim
    • 1
    • 2
  • Paul Kotterba
    • 1
  • Dorothee Moll
    • 1
    • 2
  • Patrick Polte
    • 1
  1. 1.Thünen-Institute of Baltic Sea FisheriesRostockGermany
  2. 2.Institute for Hydrobioloy and Fisheries ScienceHamburgGermany

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