Skip to main content

The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785)

Marine Biology volume 150, pages 1365–1377 (2007)Cite this article

Abstract

Lesser sandeel (Ammodytes tobianus) is abundant in near-shore areas where it is a key prey. It exhibits the behaviour of alternating between swimming in schools and lying buried in the sediment. We first determined the species’ standard metabolic rate (SMR), critical partial pressure of oxygen \((P_{{\rm O}_{2{\rm crit}}})\) and maximal oxygen uptake \((M_{{\rm O}_{2{\rm max}}}).\) The sandeel were then exposed to an acute stepwise decline in water oxygen pressure (18.4, 13.8, 9.8, 7.5, 5.8, 4.0, and 3.1 kPa \(P_{{\rm O}_{2}}\)). Swimming speed and routine- and post-experimental blood lactate levels were measured, in addition to levels associated with strenuous exercise. The SMR was 69.0  ± 8.4 mg O2 kg−1 h−1 and the \(M_{{\rm O}_{2{\rm max}}}\) about seven times as high. The \(P_{{\rm O}_{2{\rm crit}}}\) was found to be 4.1 kPa. A rapid decrease (within 1 h) in \(P_{{\rm O}_{2}}\) from 18.4 to 3.1 kPa had no significant effect on routine swimming speed (0.9  ± 0.06 bl s−1), but steady levels at the lowest \(P_{{\rm O}_{2}}\) (3.1 kPa) gradually reduced the swimming speed by 95% after 40 min. The routine blood lactate levels were 2.2  ± 0.6 mmol l−1, while the levels in the strenuously exercised groups were significantly higher with 5.4  ± 1.6 and 5.8  ± 1.3 mmol l−1. The highest levels were observed in post-experimental fish with 7.5  ± 2.7 mmol l−1. We argue that, as sandeel showed no decrease in swimming speed (to offset stress) nor an increased speed to escape the hypoxia, the fish either rely on a low SMR and being a reasonable strong oxygen regulator \((\hbox{low}\;P_{{\rm O}_{2{\rm crit}}})\) as a mean to cope when exposed to acute hypoxia, or that the hypoxia simply developed too fast for the fish to decide on an appropriate strategy. Not showing a behavioural response may in the present case be maladaptive, as the consequence was major physiological stress which the fish however appears tolerant towards. The high routine blood lactate levels suggest that anaerobic metabolism is associated with swimming in sandeel, which may be related to the specific lifestyle of the fish where they regularly bury in the sediment.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

\(P_{{\rm O}_{2{\rm crit}}}\) :

Critical partial pressure of oxygen

\(M_{{\rm O}_{2{\rm max}}}\) :

maximal oxygen uptake

MS:

metabolic scope

\(P_{{\rm O}_{2}}\) :

partial pressure of oxygen

SMR:

Standard metabolic rate

References

  • Anderson L, Rydberg L (1993) Exchange of water and nutrients between the Skagerrak and the Kattegat. Estuar Coast Shelf Sci 36:159–181

    Article  Google Scholar 

  • Baker DW, Wood AM, Litvak MK, Kieffer JD (2005) Haematology of juvenile Acipenser onyrinchus and Acipenser brevirostrum at rest and following forced activity. J Fish Biol 66:208–221

    Article  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(2):208–216

    Article  Google Scholar 

  • Bejda AJ, Studholme AL, Olla BL (1987) Behavioural responses of red hake, Urophycis chuss, to decreasing concentrations of dissolved oxygen. Environ Biol Fish 19:261–268

    Article  Google Scholar 

  • Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Bd Can 21(5):1183–1226

    Article  Google Scholar 

  • Cech JJ, Crocker CE (2002) Physiology of sturgeon: effects of hypoxia and hypercapnia. J Appl Ichthyol 18:320–324

    Article  Google Scholar 

  • Claireaux G, Webber DM, Kerr SR, Boutilier RG (1995) Physiology and behaviour of free swimming Atlantic cod, Gadus morhua, facing fluctuating salinity and oxygen conditions. J Exp Biol 198:61–69

    CAS  PubMed  Google Scholar 

  • Claireaux G, Webber DM, Lagardère J-P, Kerr SR (2000) Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J Sea Res 44:257–265

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Conley DJ, Kaas H, Møhlenberg B, Rasmussen B, Windolf J (2000) Characteristics of Danish estuaries. Estuaries 23:820–837

    Article  CAS  Google Scholar 

  • Conley DJ, Carstensen J, Ærtebjerg G, Christensen PB, Dalsgaard T, Hansen JLS, Josefson AB (in press) Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol Appl Sp issue Coast Eutrophs: accepted

  • Dalla Via J, van den Thillart G, Cattani O, Cortesi P (1998) Behavioral responses and biochemical correlates in Solea solea to gradual hypoxic exposure. Can J Zool 76:2108–2113

    Article  Google Scholar 

  • Domenici P, Steffensen JF, Batty RS (2000) The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring. J Fish Biol 57:1526–1538

    Article  Google Scholar 

  • Driedzic WR, Hochachka PW (1978) Metabolism in fish during exercise. In: Hoar WS, Randall DJ (Eds) Fish physiology, vol VII. Academic, New York

    Google Scholar 

  • Fischer P, Rademacher K, Kils U (1992) In situ investigations on the respiration and behaviour of the eelpout Zoarces viviparous under short-term hypoxia. Mar Ecol Prog Ser 88:181–184

    Article  Google Scholar 

  • Fry FEJ (1971) The effect of environmental factors on the physiology of fish. In: Hoar WS and Randall DJ (Eds) Fish physiology, vol VI. Academic , New York, pp 1–98

    Google Scholar 

  • Gauld A (1990) Movements of lesser sandeels (Ammodytes marius Raitt) tagged in the northwestern North Sea. Journal du Conseil. Int Council Explor Sea 46:229–231

    Google Scholar 

  • Gillis GB (1998) Neuromuscular control of anguilliform locomotion: patterns of red and white muscle activity during swimming in the American ell Anguilla rostrata. J Exp Biol 201:3245–3256

    PubMed  Google Scholar 

  • Gislason H, Kirkegaard E (1998) Is the industrial fishery in the North Sea sustainable? In: Symes D (Ed) Northern waters: management issues and practice. Fishing news books. Blackwell, Oxford, pp 195–208

    Google Scholar 

  • HELCOM (2003) The 2002 oxygen depletion event in the Kattegat, Belt Sea and Western Baltic. Baltic Sea Environment Proceeding No: 90

  • Herbert NA, Steffensen JF (2005) The response of Atlantic cod, Gadus morhua, to progressive hypoxia: fish swimming speed and physiological stress. Mar Biol 147:1403–1412

    Article  Google Scholar 

  • Hoffmann E (2000) Fisk og fiskebestande I Limfjorden 1984–1999. DFU-rapport 75-00. In Danish

  • Holland GJ, Greenstreet SPR, Gibb IM, Fraser HM, Robertson MR (2005) Identifying sandeel Ammodytes marinus sediment habitat preferences in the marine environment. Mar Ecol Prog Ser 303:269–282

    Article  Google Scholar 

  • Johansen JL, Herbert NA, Steffensen JF (2006) The behavioural and physiological response of Atlantic cod (Gadus morhua L.) to short-term acute hypoxia. J Fish Biol 68:1918–1924

    Article  Google Scholar 

  • Lefrançois C, Claireaux G (2003) Influence of ambient oxygenation and temperature on metabolic scope and heart rate in the common sole Solea solea. Mar Ecol Prog Ser 259:273–284

    Article  Google Scholar 

  • Le François NR, Lamarre SG, Blier PU (2005) Is white anaerobic glycolysis capacity indicative of competitive ability in Arctic charr. J Fish Biol 66:1167–1176

    Article  Google Scholar 

  • Lutz PL (1989) Interaction between hypometabolism and acid-base balance. Can J Zool 67:3018–3023

    Article  Google Scholar 

  • Lutz PL, Nilsson GE (1997) Contrasting strategies for anoxic brain survival—glycolysis up or down. J Exp Biol 200:411–419

    CAS  PubMed  Google Scholar 

  • Møhlenberg F (1999) Effect of meterology and nutrient load on oxygen depletion in a Danish micro-tidal estuary. Aquatic Ecol 33:55–64

    Article  Google Scholar 

  • Macer CT (1966) Sand eels (Ammodytidae) in the southwestern North Sea; their biology and fishery. Fishery Investigations, Series 2, Great Britain Minist Agric, Fish Food 24:1–55

    Google Scholar 

  • Martínez M, Guderley H, Dutil J-D, Winger PD, He P, Walsh SJ (2003) Condition, prolonged swimming performance and muscle metabolic capacities of cod Gadus morhua. J Exp Biol 206:503–511

    Article  Google Scholar 

  • Metcalfe JD, Butler PJ (1984) Changes in activity and ventilation in response to hypoxia in unrestrained, unoperated dogfish (Scyliorhinus canicula L.). J Exp Biol 108:411–418

    CAS  PubMed  Google Scholar 

  • Meyer TL, Cooper RA, Langton RW (1979) Relative abundance, behaviour, and food habits of the American sand lance, Ammodytes americanus, from the Gulf of Maine. Fish Bul (Washington DC) 77:243–253

    CAS  Google Scholar 

  • Milligan CL, Wood CM (1987) Regulation of blood oxygen transport and red cell pHi after exhaustive activity in rainbow trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). J Exp Biol 133:263–282

    CAS  PubMed  Google Scholar 

  • Munch-Pedersen S (2004) Fiskebestande og fiskeri i 2003. DFU-Rapport 95-01. In Danish

  • Muus BJ, Nielsen JG (1997) Havfisk og fiskeri I Nordvesteuropa. 5. udgave, Gads Forlag pp 214–216. In Danish

  • Neuenfeldt S (2002) The influence of oxygen saturation on the distributional overlap of predator (cod, Gadus morhua) and prey (herring, Clupea harengus) in the Bornholm Basin of the Baltic Sea. Fish Oceangr 11:11–17

    Article  Google Scholar 

  • Nilsson GE, Rosen P, Johannson D (1993) Anoxic depression of spontaneous locomotor activity in crucian carp quantified by a computer imagine technique. J Exp Biol 180:153–162

    Google Scholar 

  • Petersen JK, Pihl L (1995) Responses to hypoxia of plaice, Pleuronectes platessa, and dab, Limanda limanda, in the south-east Kattegat: distribution and growth. Environ Biol Fish 43:311–321

    Article  Google Scholar 

  • Pinto JM, Pearson WH, Anderson JW (1984) Sediment preferences and oil contamination in the Pacific sand lance Ammodytes hexapterus. Mar Biol 83:193–204

    Article  Google Scholar 

  • Popp Madsen K (1994) Sandeel or not sandeel. An important question for the Danish fishery. (In Danish) Fish og Hav 45:27–34

    Google Scholar 

  • Pörtner H-O, Branco LGS, Malvin GM, Wood SC (1994) A new function for lactate in the toad Bufo marinus. J Appl Physiol 76:2405–2410

    Article  Google Scholar 

  • Quinn T, Schneider DE (1991) Respiration of the teleost fish Ammodytes hexapterus in relation to its burrowing behaviour. Comp Biochem Physiol 98A:71–75

    Article  Google Scholar 

  • Randall DJ, Burrgren WW, Farrell AP, Haswell MS (1981) The evolution of air-breathing vertebrates. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Rasmussen B, Gustafsson BG, Ærtebjerg G, Lundsgaard C (2003) Oxygen concentration at the entrance to the Baltic Sea from 1975 to 2000. J Mar Systems 42:13–30

    Article  Google Scholar 

  • Schaarschmidt T, Jürss K (2003) Locomotor capacity of Baltic Sea and freshwater populations of the threespine stickleback (Gasterosteus aculeatus). Comp Biochem Physiol A 135:411–424

    Article  Google Scholar 

  • Schurmann H, Steffensen JF (1997) Effect of temperature, hypoxia and activity on the metabolism of juvenile cod. J Fish Biol 50:1166–1180

    Google Scholar 

  • Scott JS (1968) Morphometrics, distribution, growth, and maturity of offshore sand lance (Ammodytes dubius) on the Nova Scotia Banks. J Fish Res Bd Canada 25:1775–1785

    Article  Google Scholar 

  • Steffensen JF (1989) Some errors in respirometry of aquatic breathers: how to avoid and correct them. Fish Physiol Biochem 6:49–59

    Article  CAS  Google Scholar 

  • Steinhausen MF, Steffensen JF, Andersen NG (2005) Tail beat frequency as a predictor of swimming speed and oxygen consumption of saithe (Pollachius virens) and whiting (Merlangius merlangus) during forced swimming. Accepted by Mar Biol 148:197–204

    Article  Google Scholar 

  • Stigebrandt A, Gustafsson BG (2003) Response of the Baltic Sea to climate change-theory and observations. J Sea Res 49:243–251

    Article  Google Scholar 

  • van den Thillart G, Dalla Via J, Vitali G, Cortesi P (1994) Influence of long-term hypoxia on the energy metabolism of Solea solea. I. Critical O2 levels for aerobic and anaerobic metabolism. Mar Ecol Prog Ser 104: 109–117

    Article  Google Scholar 

  • Van Raaij MTM, Pitt DSS, Balm PHM, Steffens AB, van den Thillart G (1996) Behavioural strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Horm Behav 30:85–92

    Article  CAS  Google Scholar 

  • Videler JJ (1993) Fish swimming. Chapman & Hall, London

    Book  Google Scholar 

  • Watcher De B, Sartoris F-J, Pörtner H-O (1997) The anaerobic endproduct lactate has a behavioural and metabolic signalling function in the shore crab Carcinuc maenas. J Exp Biol 200:1015–1024

    Google Scholar 

  • Winslade P (1974a) Behavioural studies on lesser sandeel Ammodytes marius (Raitt) I. The effect of food availability on activity and the role of olfaction in food detection. J Fish Biol 6:565–576

    Article  Google Scholar 

  • Winslade P (1974b) Behavioural studies on lesser sandeel Ammodytes marius (Raitt) II. The effect of light intensity on activity. J Fish Biol 6:577–586

    Article  Google Scholar 

  • Winslade P (1974c) Behavioural studies on lesser sandeel Ammodytes marius (Raitt) III. The effect of temperature on activity and the environmental control of the annual cycle of activity. J Fish Biol 6:587–599

    Article  Google Scholar 

  • Wright PJ, Pedersen PA, Donald L, Anderson C, Lewy P, Proctor R (1998) The influence of physical factors on the distribution of lesser sandeel and its relevance to fishing pressure in the North Sea. CM-Int Counc Explor Sea (1998/AA:3)

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

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Neill Herbert, University of Glasgow, for assistance with the experimental design. The study was financially supported by a Ph.D. stipend from the Copenhagen Global Change Initiative (COGCI) Ph.D. School to Jane W. Behrens. The experiments comply with the Danish laws on animal ethics.

Author information

Authors and Affiliations

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

    Jane W. Behrens & John F. Steffensen

Authors
  1. Jane W. Behrens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. John F. Steffensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jane W. Behrens.

Additional information

Communicated by M. Kühl, Helsingør.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Behrens, J.W., Steffensen, J.F. The effect of hypoxia on behavioural and physiological aspects of lesser sandeel, Ammodytes tobianus (Linnaeus, 1785). Mar Biol 150, 1365–1377 (2007). https://doi.org/10.1007/s00227-006-0456-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0456-4

Keywords

  • Blood Lactate
  • Swimming Speed
  • White Muscle
  • Experimental Tank
  • Acute Hypoxia