Skip to main content

Advertisement

SpringerLink
Log in

Critical threshold size for overwintering sandeels (Ammodytes marinus)

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Several ecologically and commercially important fish species spend the winter in a state of minimum feeding activity and at lower risk of predation. To enable this overwintering behaviour, energetic reserves are generated prior to winter to support winter metabolism. Maintenance metabolism in fish scales with body size and increases with temperature, and the two factors together determine a critical threshold size for passive overwintering below which the organism is unlikely to survive without feeding. This is because the energetic cost of metabolism exceeds maximum energy reserves. In the present study, we estimated the energetic cost of overwintering from a bioenergetic model. The model was parameterised using respirometry-based measurements of standard metabolic rate in buried A. tobianus (a close relative to A. marinus) at temperatures from 5.3 to 18.3°C and validated with two independent long-term overwintering experiments. Maximum attainable energy reserves were estimated from published data on A. marinus in the North Sea. The critical threshold size in terms of length (L th) for A. marinus in the North Sea was estimated to be 9.5 cm. We then investigated two general predictions: (1) Fish smaller than L th display winter feeding activity, and (2) size at maturation of iteroparous species is larger than L th to ensure sufficient energy reserves to accommodate both the metabolic cost of passive overwintering and reproductive investments. Both predictions were found to be consistent with data on size at maturation and total body energy in December and February.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Behrens JW, Steffensen JF (2007) The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785) Mar Biol 150:1365–1377

    Google Scholar 

  • Behrens JW, Præbel K, Steffensen JF (2006) Swimming energetics of the Barents Sea capelin (Mallotus villosus) during the spawning migration period. J Exp Mar Biol Ecol 331:208–216

    Article  Google Scholar 

  • Behrens JW, Stahl HJ, Steffensen JF, Glud RN (2007) Oxygen dynamics around buried lesser sandeels Ammodytes tobianus (Linnaeus 1785): mode of ventilation and oxygen requirements. J Exp Biol 210:1006–1014

    Article  Google Scholar 

  • Bergstad OA, Høines ÅS, Kruger-Johnsen EM (2001) Spawning time, age and size at maturity, and fecundity of sandeel, Ammodytes marinus, in the north-eastern North Sea and in unfished coastal waters off Norway. Aquat Liv Res 14:293–301

    Article  Google Scholar 

  • Biro PA, Post JR, Abrahams MV (2005) Ontogeny of energy allocation reveals selective pressure promoting risk-taking behaviour in young fish cohorts. Proc R Soc B 272:1443–1448

    Article  Google Scholar 

  • Boulcott P, Wright PJ (2008) Critical timing for reproductive allocation in a capital breeder: evidence from sandeels. Aquat Biol 3:31–40

    Article  Google Scholar 

  • Boulcott P, Wright PJ, Gibb FM, Jensen H, Gibb IM (2007) Regional variation in maturation of sandeels in the North Sea. ICES J Mar Sci 64:369–376

    Article  Google Scholar 

  • Brett JR (1973) Energy expenditure of sockeye salmon, Oncorhynchus nerka, during sustained performance. J Fish Res Board Canada 30:1799–1809

    Article  Google Scholar 

  • Campbell HA, Fraser KPP, Bishop CM, Peck LS, Egginton S (2008) Hibernation in an Antarctic fish: on ice for winter. Plos One 3:e1743

    Article  Google Scholar 

  • Christensen A, Jensen H, Mosegaard H, John MS, Schrum C (2008) Sandeel (Ammodytes marinus) larval transport patterns in the North Sea from an individual-based hydrodynamic egg and larval model. Can J Fish Aquat Sci 65:1498–1511

    Article  Google Scholar 

  • Christiansen JS, Præbel K, Siikavuopio SI, Carscadden JE (2008) Facultative semelparity in capelin Mallotus villosus (Osmeridae) - an experimental test of a life history phenomenon in a sub-arctic fish. J Exp Mar Biol Ecol 360:47–55

    Article  Google Scholar 

  • Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905

    Article  Google Scholar 

  • Conover DO (1992) Seasonality and the scheduling of life-history at different latitudes. J Fish Biol 41:161–178

    Article  Google Scholar 

  • Doeller JE (1995) Cellular energetics of animals from high sulfide environments. Am Zool 35:154–162

    CAS  Google Scholar 

  • Downhower JF (1976) Darwins finches and evolution of sexual dimorphism in body size. Nature 263:558–563

    Article  CAS  Google Scholar 

  • Engelhard GH, Heino M (2004) Maturity changes in Norwegian spring-spawning herring Clupea harengus: compensatory or evolutionary responses? Mar Ecol Prog Ser 272:245–256

    Article  Google Scholar 

  • Fiksen Ø, Carlotti F (1998) A model of optimal life history and Diel vertical migration in Calanus finmarchicus. Sarsia 83:129–147

    Google Scholar 

  • Fullerton AH, Garvey JE, Wright RA, Stein RA (2000) Overwinter growth and survival of largemouth bass: interactions among size, food, origin, and winter severity. Trans Am Fish Soc 129:1–12

    Article  Google Scholar 

  • Garvey JE, Marschall EA (2003) Understanding latitudinal trends in fish body size through models of optimal seasonal energy allocation. Can J Fish Aquat Sci 60:938–948

    Article  Google Scholar 

  • Garvey JE, Ostrand KG, Wahl DH (2004) Energetics, predation, and ration affect size-dependent growth and mortality of fish during winter. Ecology 85:2860–2871

    Article  Google Scholar 

  • Greenstreet SPR, Holland GJ, Guirey EJ, Armstrong E, Fraser HM, Gibb IM (2010) Combining hydroacoustic seabed survey and grab sampling techniques to assess “local” sandeel population abundance. ICES J Mar Sci 67:971–984

    Article  Google Scholar 

  • Hislop JRG, Harris MP, Smith JGM (1991) Variation in the calorific value and total energy content of the lesser sandeel (Ammodytes marinus) and other fish preyed on by seabirds. J Zool 224:501–517

    Article  Google Scholar 

  • Høines ÅS, Bergstad OA (2001) Density of wintering sand eel in the sand recorded by grab catches. Fish Res 49:295–301

    Article  Google Scholar 

  • Hurst TP (2007) Causes and consequences of winter mortality in fishes. J Fish Biol 71:315–345

    Article  Google Scholar 

  • Huse I, Ona E (1996) Tilt angle distribution and swimming speed of overwintering Norwegian spring spawning herring. ICES J Mar Sci 53:863–873

    Article  Google Scholar 

  • Jensen H, Rindorf A, Wright PJ, Mosegaard H (2011) Inferring the location and scale of mixing between habitat areas of lesser sandeel through information from the fishery. Ices J Mar Sci 68:43–51

    Article  Google Scholar 

  • Jobling M (1994) Fish bioenergetics. Chapman and Hall, London

    Google Scholar 

  • Kvist T, Gislason H, Thyregod P (2001) Sources of variation in the age composition of sandeel landings. ICES J Mar Sci 58:842–851

    Article  Google Scholar 

  • Macer CT (1966) Sandeels (Ammodytidae) in the south-western North Sea: Their biology and fishery. MAFF Fishery Invest Lond Ser II 24:1–55

    Google Scholar 

  • Nilsson GE, Renshaw GMC (2004) Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131–3139

    Article  CAS  Google Scholar 

  • Paul AJ, Paul JM (1998) Comparisons of whole body energy content of captive fasting age zero Alaskan Pacific herring (Clupea pallasi Valenciennes) and cohorts over-wintering in nature. J Exp Mar Biol Ecol 226:75–86

    Article  Google Scholar 

  • Plaistow SJ, Lapsley CT, Beckerman AP, Benton TG (2004) Age and size at maturity: sex, environmental variability and developmental thresholds. Proc R Soc Lond Ser B 271:919–924

    Article  Google Scholar 

  • Reeves, SA (1994) Seasonal and annual variation in catchability of sandeels at Shetland. ICES CM. D:19

  • Schindler DE (1999) Migration strategies of young fishes under temporal constraints: the effect of size-dependent overwinter mortality. Can J Fish Aquat Sci 56:61–70

    Article  Google Scholar 

  • Schultz ET, Conover DO (1997) Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia 109:516–529

    Article  Google Scholar 

  • Schultz ET, Conover DO (1999) The allometry of energy reserve depletion: test of a mechanism for size-dependent winter mortality. Oecologia 119:474–483

    Article  Google Scholar 

  • Schultz ET, Conover DO, Ehtisham A (1998) The dead of winter: size dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae : Menidia menidia) from different latitudes. Can J Fish Aquat Sci 55:1149–1157

    Article  Google Scholar 

  • Schultz ET, Lankford TE, Conover DO (2002) The covariance of routine and compensatory juvenile growth rates over seasonality gradient in coastal fish. Oecologia 133:501–509

    Article  Google Scholar 

  • Sharples J, Ross ON, Scott BE, Greenstreet SPR, Fraser H (2006) Inter-annual variability in the timing of stratification and the spring bloom in the North-western North Sea. Cont Shelf Res 26:733–751

    Article  Google Scholar 

  • Shuter BJ, Post JR (1990) Climate, population viability, and the zoogeography of temperate fishes. Trans Am Fish Soc 119:314–336

    Article  Google Scholar 

  • Skogen MD, Svendsen E, Berntsen J, Aksnes D, Ulvestad KB (1995) Modeling the primary production in the North Sea using a coupled 3-dimensional physical-chemical-biological ocean model. Est Coast Shelf Sci 41:545–565

    Article  CAS  Google Scholar 

  • Ultsch GR (1989) Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol Rev 64:435–515

    Article  Google Scholar 

  • van de Wolfshaar KE, de Roos AM, Persson L (2008) Population feedback after successful invasion leads to ecological suicide in seasonal environments. Ecology 89:259–268

    Article  Google Scholar 

  • van Deurs M, Christensen A, Frisk C, Mosegaard H (2010) Overwintering strategy of sandeel ecotypes from an energy/predation trade-off perspective. Mar Ecol Prog Ser 416:201–215

    Article  Google Scholar 

  • Varpe Ø, Fiksen Ø (2010) Seasonal plankton-fish interactions: light regime, prey phenology, and herring foraging. Ecology 91:311–318

    Article  Google Scholar 

  • Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Global Change Biol 10:1844–1856

    Article  Google Scholar 

  • Winslade P (1974) Behavioral studies on lesser sandeel Ammodytes marinus (Raitt) III. Effect of temperature on activity and environmental control of annual cycle of activity. J Fish Biol 6:587–599

    Article  Google Scholar 

  • Wright PJ, Jensen H, Tuck I (2000) The influence of sediment type on the distribution of the lesser sandeel, Ammodytes marinus. J Sea Res 44:243–256

    Article  Google Scholar 

Download references

Acknowledgments

We thank Niels Gerner Andersen and Dorthe Frandsen for making the use of bomb calorimetry possible. We thank the ocean monitoring division at DTU Aqua for providing sandeel field data, in particular Cecilia Kvaavik. We thank people behind the NORWECOM model for providing free access to modelled North Sea temperature data. MVD was funded by the Danish Research Council supported projects FISHNET and SLIP. All experiments were carried out in line with ethical guidelines on animal handling.

Author information

Authors and Affiliations

  1. DTU Aqua National Institute of Aquatic Resources, Technical University of Denmark (DTU), Jægersborg Alle 1, Charlottenlund Castle, 2920, Charlottenlund, Denmark

    Mikael van Deurs

  2. Department of Biology, Lund University, Ecology Building, 223 62, Lund, Sweden

    Martin Hartvig

  3. Marine Biological Laboratory, University of Copenhagen, Strandpromenaden 5, 3000, Helsingør, Denmark

    Mikael van Deurs & John Fleng Steffensen

Authors
  1. Mikael van Deurs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Hartvig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. John Fleng Steffensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mikael van Deurs.

Additional information

Communicated by K. D. Clements.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 27 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Deurs, M., Hartvig, M. & Steffensen, J.F. Critical threshold size for overwintering sandeels (Ammodytes marinus). Mar Biol 158, 2755–2764 (2011). https://doi.org/10.1007/s00227-011-1774-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1774-8

Keywords

Search

Navigation