Abstract
The frequency of low O2 (hypoxia) has increased in coastal marine areas but how fish avoid deleterious water masses is not yet clear. To assess whether the presence and oxygen pressure (PO2) level of an O2 refuge affects the hypoxia avoidance behaviour of fish, individual Atlantic cod (Gadus morhua L.) were exposed to a range of O2 choices in a 2-way choice chamber at 11.4°C over two different experiments. Cod in the first experiment were allowed access to a fixed O2 refuge (fully air-saturated seawater) whilst oxygen pressure (PO2) on the other side was reduced in steps to a critically low level, i.e. 4.3 kPa—a point where cod can no longer regulate O2 consumption. Under these conditions, cod did not avoid any level of hypoxia and fish swimming speed also remained unchanged. In contrast, strong avoidance reactions were exhibited in a second experiment when fish were again exposed to 4.3 kPa but the safety, i.e. PO2, of the refuge was reduced. Fish not only spent less time at 4.3 kPa as a result of fewer sampling visits but they also swam at considerably slower speeds. The presence of an avoidance response was thus strongly related to refuge PO2 and it is unlikely that cod, and possibly other fish species, would enter low O2 to feed in the wild if a sufficiently safe O2 refuge was not available. It is therefore hypothesized that the feeding range of fish may be heavily compressed if hypoxia expands and intensifies in future years.
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Abbreviations
- PO2:
-
Partial pressure of oxygen
References
Brady DC, Targett TE, Tuzzolino DM (2009) Behavioral responses of juvenile weakfish (Cynoscion regalis) to diel-cycling hypoxia: swimming speed, angular correlation, expected displacement, and effects of hypoxia acclimation. Can J Fish Aquat Sci 66:415–424
Brandt SB, Gerken M, Hartman KJ, Demers E (2009) Effects of hypoxia on food consumption and growth of juvenile striped bass (Morone saxatilis). J Exp Mar Biol Ecol 381:S143–S149
Burleson M (1995) Oxygen availability: sensory systems. In: Hochachka PW, Mommsen TP (eds) Environmental and ecological biochemistry. Elsevier, New York, pp 1–18
Burleson ML, Wilhelm DR, Smatresk NJ (2001) The influence of fish size on the avoidance of hypoxia and oxygen selection by largemouth bass. J Fish Biol 59:1336–1349
Chabot D, Claireaux G (2008) Environmental hypoxia as a metabolic constraint on fish: the case of Atlantic cod, Gadus morhua. Mar Pollut Bull 57:287–294
Chabot D, Dutil JD (1999) Reduced growth of Atlantic cod in non-lethal hypoxic conditions. J Fish Biol 55:472–491
Claireaux G, Webber DM, Kerr SR, Boutilier RG (1995) Physiology and behavior of free swimming Atlantic cod (Gadus morhua) facing fluctuating salinity and oxygenation conditions. J Exp Biol 198:61–69
Claireaux G, Webber DM, Lagardere JP, 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
D’Amours D (1993) The distribution of cod (Gadus morhua) in relation to temperature and oxygen in the Gulf of St. Lawrence. Fish Oceanogr 2:24–29
Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929
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
Eby LA, Crowder LB (2002) Hypoxia-based habitat compression in the Neuse River Estuary: context-dependent shifts in behavioral avoidance thresholds. Can J Fish Aquat Sci 59:952–965
Gilbert D, Sunby B, Gobeil C, Mucci A, Tremblay G-H (2005) A seventy-two-year record of diminishing deep-water oxygen in the St. Lawrence estuary: the Northwest Atlantic connection. Limnol Oceanogr 50:1654–1666
Hagy JD, Boynton WR, Keefe CW, Wood KV (2004) Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow. Estuaries 27:634–658
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
Höglund LB (1961) The reactions of fish in concentration gradients. Fish Board Swed Rep 43:1–147
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
Jones JRE (1952) The reactions of fish to water of low oxygen concentration. J Exp Biol 29:403–415
Kaartvedt S, Røstad A, Klevjer TA (2009) Sprat Sprattus sprattus can exploit low oxygen waters for overwintering. Mar Ecol Prog Ser 390:237–249
Kidwell DM, Lewitus AJ, Jewett EB, Brandt S, Mason DM (2009) Ecological impacts of hypoxia on living resources. J Exp Mar Biol Ecol 381:S1–S3
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 Oceanogr 11:11–17
Neuenfeldt S, Beyer JE (2003) Oxygen and salinity characteristics of predator-prey distributional overlaps shown by predatory Baltic cod during spawning. J Fish Biol 62:168–183
Neuenfeldt S, Andersen KH, Hinrichsen H-H (2009) Some Atlantic cod Gadus morhua in the Baltic Sea visit hypoxic water briefly but often. J Fish Biol 75:290–294
Perry SF, Gilmour KM (2002) Sensing and transfer of respiratory gases at the fish gill. J Exp Zool 293:249–263
Pinheiro JC, Bates DM (2000) Mixed effects models in S and S-Plus. Springer, London
Plante S, Chabot D, Dutil JD (1998) Hypoxia tolerance in Atlantic cod. J Fish Biol 53:1342–1356
Roberts JJ, Höök TO, Ludsin SA, Pothoven SA, Vanderploeg HA, Brandt SB (2009) Effects of hypolimnetic hypoxia on foraging and distributions of Lake Erie yellow perch. J Exp Mar Biol Ecol 381:S132–S142
Rose KA, Adamack AT, Murphy CA, Sable SE, Kolesar SE, Craig JK, Breitburg DL, Thomas P, Brouwer MH, Cerco CF, Diamond S (2009) Does hypoxia have population-level effects on coastal fish? Musings from the virtual world. J Exp Mar Biol Ecol 381:S188–S203
Schurmann H, Steffensen JF (1992) Lethal oxygen levels at different temperatures and the preferred temperature during hypoxia of the Atlantic cod, Gadus morhua. J Fish Biol 41:927–934
Schurmann H, Steffensen JF (1994) Spontaneous swimming activity of Atlantic cod Gadus morhua exposed to graded hypoxia at 3 temperatures. J Exp Biol 197:129–142
Schurmann H, Steffensen JF (1997) Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J Fish Biol 50:1166–1180
Shingles A, McKenzie DJ, Claireaux G, Domenici P (2005) Reflex cardioventilatory responses to hypoxia in the flathead gray mullet (Mugil cephalus) and their behavioral modulation by perceived threat of predation and water turbidity. Physiol Biochem Zool 78:744–755
Skjæraasen JE, Nilsen T, Meager JJ, Herbert NA, Moberg O, Tronci V, Johansen T, Salvanes AGV (2008) Hypoxic avoidance behaviour in cod (Gadus morhua L.): the effect of temperature and haemoglobin genotype. J Exp Mar Biol Ecol 358:70–77
Stierhoff KL, Tyler RM, Targett TE (2009) Hypoxia tolerance of juvenile weakfish (Cynoscion regalis): laboratory assessment of growth and behavioral avoidance responses. J Exp Mar Biol Ecol 381:S173–S179
Taylor JC, Rand PS, Jenkins J (2007) Swimming behavior of juvenile anchovies (Anchoa spp.) in an episodically hypoxic estuary: implications for individual energetics and trophic dynamics. Mar Biol 152:939–957
Thomas P, Rahman MS, Khan IA, Kummer JA (2007) Widespread endocrine disruption and reproductive impairment in an estuarine fish population exposed to seasonal hypoxia. Proc R Soc B Biol Sci 274:2693–2702
Tomkiewicz J, Lehmann KM, St John MA (1998) Oceanographic influences on the distribution of Baltic cod, Gadus morhua, during spawning in the Bornholm Basin of the Baltic Sea. Fish Oceanogr 7:48–62
Turner RE, Rabalais NN, Swenson EM, Kasprzak M, Romaire T (2005) Summer hypoxia in the northern Gulf of Mexico and its prediction from 1978 to 1995. Mar Environ Res 59:65–77
Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45
Acknowledgments
We gratefully acknowledge funding from the European Union Fisheries Directorate (via contract QLRS-2002-00799, Project ETHOFISH), as well as the Norweigan Research Council (152862/120). Ethical approval was granted by the Experimental Animal Committee (Ministry of Justice, Denmark), through license numbers 1999/561 -232 and 2004/561 -894, and the Norwegian Veterinary Authorities for Experimental Research (Site license number 18).
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Communicated by M. A. Peck.
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Herbert, N.A., Skjæraasen, J.E., Nilsen, T. et al. The hypoxia avoidance behaviour of juvenile Atlantic cod (Gadus morhua L.) depends on the provision and pressure level of an O2 refuge. Mar Biol 158, 737–746 (2011). https://doi.org/10.1007/s00227-010-1601-7
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DOI: https://doi.org/10.1007/s00227-010-1601-7
Keywords
- Swimming Speed
- Test Arena
- Avoidance Reaction
- Average Residence Time
- Visit Number