Environmental hypoxia as a metabolic constraint on fish: The case of Atlantic cod, Gadus morhua

Marine Pollution Bulletin

Volumn 57, Issue 6-12, 2008, Pages 287-294

  Chabot, D ^a   Claireaux, G ^b  

^a MAURICE LAMONTAGNE INSTITUTE   (Canada)

^b UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

Author keywords

Food ingestion; Growth rate; Hypoxia; Metabolic scope; Survival; Swimming

Indexed keywords

ANIMALS; CONSTRAINT THEORY; GROWTH RATE; MATHEMATICAL MODELS;

FOOD INGESTION; HYPOXIA; METABOLIC SCOPE (MS);

METABOLISM;

DISSOLVED OXYGEN; FEEDING BEHAVIOR; FOOD INTAKE; GADOID; GROWTH RATE; HYPOXIA; INGESTION RATE; METABOLISM; POLLUTION EFFECT; SURVIVAL; SWIMMING BEHAVIOR;

ARTICLE; ATLANTIC COD; ENVIRONMENTAL EXPOSURE; FOOD INTAKE; GROWTH RATE; HYPOXIA; LABORATORY TEST; MARINE ENVIRONMENT; METABOLIC RATE; NONHUMAN; SWIMMING;

ANAEROBIOSIS; ANIMALS; ENVIRONMENT; FISHES; GADUS MORHUA; OXYGEN;

ATLANTIC OCEAN; BALTIC SEA; CANADA; EURASIA; EUROPE; GULF OF SAINT LAWRENCE; KATTEGAT; NORTH AMERICA; NORTHERN EUROPE; SCANDINAVIA;

ANIMALIA; DICENTRARCHUS LABRAX; GADUS MORHUA; SCOPHTHALMIDAE; SCOPHTHALMUS MAXIMUS; SOLEA SOLEA;

EID: 46549085784     PISSN: 0025326X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.marpolbul.2008.04.001     Document Type: Article

References (96)

1. Aarnio K., Bonsdorff E., and Rosenback N. Food and feeding habits of juvenile flounder Platichthys flesus (L), and turbot Scophthalmus maximus L. in the Åland archipelago, northern Baltic Sea. Journal of Sea Research 36 (1996) 311-320
2. Andrews J.W., Murai T., and Gibbons G. The influence of dissolved oxygen on the growth of channel catfish. Transactions of the American Fisheries Society 102 (1973) 835-838
3. Bell G.W., and Eggleston D.B. Species-specific avoidance responses by blue crabs and fish to chronic and episodic hypoxia. Marine Biology 146 (2005) 761-770
4. Benson B.B., and Krause D.J. The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnology and Oceanography 29 (1984) 620-632
5. Blaikie H.B., and Kerr S.R. Effect of activity level on the apparent heat increment in Atlantic cod, Gadus morhua. Canadian Journal of Fisheries and Aquatic Sciences 53 (1996) 2093-2099
6. Braber L., and De Groot S.J. The food of five flatfish species (Pleuronectiformes) in the southern North Sea. Netherlands Journal of Sea Research 6 (1973) 163-172
7. Bugden G.L. Changes in temperature-salinity characteristics of the deeper waters of the Gulf of St. Lawrence over the past several decades. Canadian Special Publication of Fisheries and Aquatic Sciences 113 (1991) 139-147
8. Castonguay M., Rollet C., Fréchet A., Gagnon P., Gilbert D., and Brethes J.-C. Distribution changes of Atlantic cod (Gadus morhua) in the northern Gulf of St. Lawrence in relation to an oceanic cooling. ICES Journal of Marine Science 56 (1999) 333-344
9. Chabot D. Chronic non-lethal levels of hypoxia limit distribution and growth of Atlantic cod (Gadus morhua) in the northern Gulf of St. Lawrence, Canada. In: Rupp G.L., and White M.D. (Eds). Proceedings of the Seventh International Symposium on Fish Physiology, Toxicology and Water Quality, Tallinn, Estonia, May 12-15, 2003, EPA 600/R-04/049. US (2001), Environmental Protection Agency, Ecosystems Research Division, Athens, Georgia, USA 183-205.
10. Chabot D., and Dutil J.-D. Reduced growth of Atlantic cod in non-lethal hypoxic conditions. Journal of Fish Biology 55 (1999) 472-491
11. Chabot D., Dutil J.-D., and Couturier C. Impact of chronic hypoxia on food ingestion, growth and condition of Atlantic cod (Gadus morhua). ICES Annual Science Conference 89th Statutory Meeting, Theme session on Growth and Condition in Gadoid Stocks and Implications for Sustainable Management (V) (2001), ICES, Copenhagen, Denmark 1-17.
12. Chatelier A., McKenzie D.J., Prinet A., Galois R., Robin J., Zambonino J., and Claireaux G. Associations between tissue fatty acid composition and physiological traits of performance and metabolism in the seabass (Dicentrarchus labrax). Journal of Experimental Biology 209 (2006) 3429-3439
13. Chouinard G.A., and Fréchet A. Fluctuations in the cod stocks of the Gulf of St. Lawrence. ICES Marine Science Symposia 198 (1994) 121-139
14. Claireaux G., and Dutil J.-D. Physiological response of the Atlantic cod (Gadus morhua) to hypoxia at various environmental salinities. Journal of Experimental Biology 163 (1992) 97-118
15. Claireaux G., and Lagardère J.-P. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. Journal of Sea Research 42 (1999) 157-168
16. Claireaux G., and Lefrançois C. Linking environmental variability and fish performance: integration through the concept of scope for activity. Philosophical Transactions of the Royal Society B: Biological Sciences 362 (2007) 2031-2041
17. Claireaux G., Webber D.M., Kerr S.R., and Boutilier R.G. Physiology and behaviour of free-swimming Atlantic cod (Gadus morhua) facing fluctuating salinity and oxygenation conditions. Journal of Experimental Biology 198 (1995) 61-69
18. Claireaux G., Webber D.M., Lagardère J.-P., and Kerr S.R. Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research 44 (2000) 257-265
19. Claireaux G., Couturier C., and Groison A.-L. Effect of temperature on maximum swimming speed and cost of transport in juvenile European sea bass (Dicentrarchus labrax). Journal of Experimental Biology 209 (2006) 3420-3428
20. Comeau L.A., Campana S.E., and Chouinard G.A. Timing of Atlantic cod (Gadus morhua L.) seasonal migrations in the southern Gulf of St. Lawrence: interannual variability and proximate control. ICES Journal of Marine Science 59 (2002) 333-351
21. Coote A.R., and Yeats P.A. Distribution of nutrients in the Gulf of St. Lawrence. Journal of the Fisheries Research Board of Canada 36 (1979) 122-131
22. Couturier, C., 2007. Effets des caractéristiques physico-chimiques et biorhéologiques de l'eau sur la physiologie, les performances adaptatives et la sélection de l'habitat chez la sole commune Solea solea (Linnaeus, 1758). Ph.D. thesis, Université de La Rochelle, La Rochelle, France.
23. Craig J.K., Crowder L.B., Gray C.D., McDaniel C.J., Henwood T.A., and Hanifen J.G. Ecological effects of hypoxia on fish, sea turtles, and marine mammals in the northwestern Gulf of Mexico. In: Rabalais N.N., Caddy J.F., Smith J.W., Marcus N., and Turner R.E. (Eds). Coastal Hypoxia: Consequences for Living Resources and Ecosystems (2001), American Geophysical Union, Washington, DC, USA 269-292
24. D'Amours D. The distribution of cod (Gadus morhua) in relation to temperature and oxygen level in the Gulf of St. Lawrence. Fisheries Oceanography 2 (1993) 24-29
25. Das T., and Stickle W.B. Detection and avoidance of hypoxic water by juvenile Callinectes sapidus and C. similis. Marine Biology 120 (1994) 593-600
26. Diaz R.J. Overview of hypoxia around the world. Journal of Environmental Quality 30 (2001) 275-281
27. Diaz R.J., and Rosenberg R. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology: An Annual Review 33 (1995) 245-303
28. Diaz R.J., Nestlerode J., and Diaz M.L. A global perspective on the effects of eutrophication and hypoxia on aquatic biota. In: Rupp G.L., and White M.D. (Eds). Proceedings of the Seventh International Symposium on Fish Physiology, Toxicology and Water Quality, Tallinn, Estonia, May 12-15, 2003, EPA 600/R-04/049. US (2004), Environmental Protection Agency, Ecosystems Research Division, Athens, Georgia, USA 1-33
29. Dutil J.-D., Sylvestre E.-L., Gamache L., Larocque R., and Guderley H. Burst-coast use, swimming performance, and metabolism of Atlantic cod (Gadus morhua) in sub-lethal hypoxic conditions. Journal of Fish Biology 71 (2007) 1-13
30. Dyer M.F., Pope J.G., Fry P.D., Law R.J., and Portmann J.E. Changes in fish and benthos catches off the Danish coast in September 1981. Journal of the Marine Biological Association of the United Kingdom 63 (1983) 767-775
31. Eby L.A., and Crowder L.B. Hypoxia-based habitat compression in the Neuse River Estuary: context-dependent shifts in behavioral avoidance thresholds. Canadian Journal of Fisheries and Aquatic Sciences 59 (2002) 952-965
32. Eby L.A., Crowder L.B., McClellan C.M., Peterson C.H., and Powers M.J. Habitat degradation from intermittent hypoxia: impacts on demersal fishes. Marine Ecology Progress Series 291 (2005) 249-262
33. Fry F.E.J. Effects of the environment on animal activity. University of Toronto Studies, Biology Series 55 (1947) 1-62
34. Fry F.E.J. The effect of environmental factors on the physiology of fish. In: Hoar W.S., and Randall D.J. (Eds). Environmental Relations and Behavior (VI) (1971), Academic Press, New York 1-98
35. Gilbert D., Sundby B., Gobeil C., Mucci A., and Tremblay G.-H. A seventy-two year record of diminishing deep-water oxygen in the St. Lawrence estuary: the northwest Atlantic connection. Limnology and Oceanography 50 (2005) 1654-1666
36. Gilbert D., Chabot D., Archambault P., Rondeau B., and Hébert S. Appauvrissement en oxygène dans les eaux profondes du Saint-Laurent marin - Causes possibles et impacts écologiques. Le Naturaliste canadien 131 (2007) 67-75
37. Herbert N.A., and Steffensen J.F. The response of Atlantic cod, Gadus morhua, to progressive hypoxia: fish swimming speed and physiological stress. Marine Biology 147 (2005) 1403-1412
38. Howarth R., Billen G., Swaney D., Townsend A., Jaworski N., Lajtha K., Downing J., Elmgren R., Caraco N., Jordan T., Berendse F., Freney J., Kudeyarov V., Murdoch P., and Zhao-Liang Z. Regional nitrogen budgets and riverine N&P fluxes for the drainages to the North Atlantic Ocean: natural and human influences. Biogeochemistry 35 (1996) 75-139
39. Jobling M. A review of the physiological and nutritional energetics of cod, Gadus morhua L., with particular reference to growth under farmed conditions. Aquaculture 70 (1988) 1-19
40. Jordan A.D., and Steffensen J.F. Effects of ration size and hypoxia upon specific dynamic action (SDA) in the cod. Physiological Biochemistry and Zoology 80 (2007) 178-185
41. Justić D., Rabalais N.N., and Turner R.E. Impacts of climate change on net productivity of coastal waters: implications for carbon budgets and hypoxia. Climate Research 8 (1997) 225-237
42. Kennedy V.S. Anticipated effects of climate change on estuarine and coastal fisheries. Fisheries 15 (1990) 16-24
43. Kolar C.S., and Rahel F.J. Interaction of a biotic factor (predator presence) and an abiotic factor (low oxygen) as an influence on benthic invertebrate communities. Oecologia 95 (1993) 210-219
44. Kramer D.L. Dissolved oxygen and fish behavior. Environmental Biology of Fishes 18 (1987) 81-92
45. Landry C.A., Steele S.L., Manning S., and Cheek A.O. Long term hypoxia suppresses reproductive capacity in the estuarine fish, Fundulus grandis. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology 148 (2007) 317-323
46. Lefrançois C., and Claireaux G. Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea. Marine Ecology Progress Series 259 (2003) 273-284
47. Levin L.A. Oxygen minimum zone benthos: adaptation and community response to hypoxia. Oceanography and Marine Biology: An Annual Review 41 (2003) 1-45
48. Lilly G.R. Interannual variability in predation by cod (Gadus morhua) on capelin (Mallotus villosus) and other prey off southern Labrador and northeastern Newfoundland. ICES Marine Science Symposia 193 (1991) 133-146
49. Lim H.-S., Diaz R.J., Hong J.-S., and Schaffner L.C. Hypoxia and benthic community recovery in Korean coastal waters. Marine Pollution Bulletin 52 (2006) 1517-1526
50. Link J.S., and Garrison L.P. Trophic ecology of Atlantic cod Gadus morhua on the northeast US continental shelf. Marine Ecology Progress Series 227 (2002) 109-123
51. Lotka A.J. Contribution to the energetics of evolution. Proceedings of the National Academy of Sciences 8 (1922) 147-151
52. Mallekh R., and Lagardère J.P. Effect of temperature and dissolved oxygen concentration on the metabolic rate of the turbot and the relationship between metabolic scope and feeding demand. Journal of Fish Biology 60 (2002) 1105-1115
53. Marcus N.H., Richmond C., Sedlacek C., Miller G.A., and Oppert C. Impact of hypoxia on the survival, egg production and population dynamics of Acartia tonsa Dana. Journal of Experimental Marine Biology and Ecology 301 (2004) 111-128
54. Maxime V., Pichavant K., Boeuf G., and Nonnotte G. Effects of hypoxia on respiratory physiology of turbot, Scophthalmus maximus. Fish Physiology and Biochemistry 22 (2000) 51-59
55. Montagna P.A., and Ritter C. Direct and indirect effects of hypoxia on benthos in Corpus Christi Bay, Texas, USA. Journal of Experimental Marine Biology and Ecology 330 (2006) 119-131
56. Neill W.H., Miller J.M., Van der Veer H.W., and Winemiller K.O. Ecophysiology of marine fish recruitment: a conceptual framework for understanding interannual variability. Netherlands Journal of Sea Research 32 (1994) 135-152
57. Nelson J.A., and Claireaux G. Sprint swimming performance of juvenile European sea bass. Transactions of the American Fisheries Society 134 (2005) 1274-1284
58. Nissling A., and Westin L. Egg buoyancy of Baltic cod (Gadus morhua) and its implications for cod stock fluctuations in the Baltic. Marine Biology 111 (1991) 33-35
59. Nissling A., Kryvi H., and Vallin L. Variation in egg buoyancy of Baltic cod Gadus morhua and its implications for egg survival in prevailing conditions in the Baltic Sea. Marine Ecology Progress Series 110 (1994) 67-74
60. Nixon S.W. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41 (1995) 199-219
61. Perry S.F., and McDonald G. Gas exchange. In: Evans D.H. (Ed). The Physiology of Fishes (1993), CRC Press, Boca Raton, Florida 251-278
62. Petersen J.K., and Pihl L. Responses to hypoxia of plaice, Pleuronectes platessa, and dab, Limanda limanda, in the south-east Kattegat: distribution and growth. Environmental Biology of Fishes 43 (1995) 311-321
63. Pichavant K., Person-Le-Ruyet J., Le Bayon N., Severe A., Le Roux A., Quemener L., Maxime V., Nonnotte G., and Boeuf G. Effects of hypoxia on growth and metabolism of juvenile turbot. Aquaculture 188 (2000) 103-114
64. Pichavant K., Person-Le-Ruyet J., Le Bayon N., Severe A., Le Roux A., and Boeuf G. Comparative effects of long-term hypoxia on growth, feeding and oxygen consumption in juvenile turbot and European sea bass. Journal of Fish Biology 59 (2001) 875-883
65. Pihl L. Effects of oxygen depletion on demersal fish in coastal areas of the south-east Kattegat. In: Ryland J.S., and Tyler P.A. (Eds). Proceedings of the 23rd European Marine Biology Symposium - Reproduction, Genetics and Distributions of Marine Organisms (1989), Olsen and Olsen, Fredensborg, Denmark 431-439
66. Pihl L. Changes in the diet of demersal fish due to eutrophication-induced hypoxia in the Kattegat, Sweden. Canadian Journal of Fisheries and Aquatic Sciences 51 (1994) 321-336
67. Pihl L., Baden S.P., Diaz R.J., and Schaffner L.C. Hypoxia-induced structural changes in the diet of bottom-feeding fish and crustacea. Marine Biology 112 (1992) 349-361
68. Plante S., Chabot D., and Dutil J.-D. Hypoxia tolerance in Atlantic cod. Journal of Fish Biology 53 (1998) 1342-1356
69. Priede I.G. Metabolic scope in fishes. In: Tytler P., and Calow P. (Eds). Fish Energetics: New Perspectives (1985), Croom Helm, London 33-64
70. Reidy S.P., Kerr S.R., and Nelson J.A. Aerobic and anaerobic swimming performance of individual Atlantic cod. Journal of Experimental Biology 203 (2000) 347-357
71. Rose G.A. Cod spawning on a migration highway in the north-west Atlantic. Nature 366 (1993) 458-461
72. Samuelsson M. Interannual salinity variations in the Baltic Sea during the period 1954-1990. Continental Shelf Research 16 (1996) 1463-1477
73. Scholz U., and Waller U. The oxygen requirements of three fish species from the German Bight: cod Gadus morhua, plaice Pleuronectes platessa, and dab Limanda limanda. Journal of Applied Ichthyology 8 (1992) 72-76
74. Schurmann H., and Steffensen J.F. Lethal oxygen levels at different temperatures and the preferred temperature during hypoxia of the Atlantic cod, Gadus morhua L. Journal of Fish Biology 41 (1992) 927-934
75. Schurmann H., and Steffensen J.F. Spontaneous swimming activity of Atlantic cod Gadus morhua exposed to graded hypoxia at three temperatures. Journal of Experimental Biology 197 (1994) 129-142
76. Schurmann H., and Steffensen J.F. Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. Journal of Fish Biology 50 (1997) 1166-1180
77. Schurmann H., Claireaux G., and Chartois H. Changes in vertical distribution of sea bass (Dicentrarchus labrax L.) during a hypoxic episode. Hydrobiologia (1998) 207-213
78. Shang E.H., Yu R.M., and Wu R.S. Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environmental Science and Technology 40 (2006) 3118-3122
79. Siikavuopio S.I., Dale T., Mortensen A., and Foss A. Effects of hypoxia on feed intake and gonad growth in the green sea urchin, Strongylocentrotus droebachiensis. Aquaculture 266 (2007) 112-116
80. Soofiani N.M., and Hawkins A.D. Energetic costs at different levels of feeding in juvenile cod, Gadus morhua L. Journal of Fish Biology 21 (1982) 577-592
81. Steinhausen M.F., Andersen N.G., and Steffensen J.F. The effect of external dummy transmitters on oxygen consumption and performance of swimming Atlantic cod. Journal of Fish Biology 69 (2006) 951-956
82. Stewart N.E., Shumway D.L., and Doudorff P. Influence of oxygen concentration on growth of juvenile largemouth bass. Journal of the Fisheries Research Board of Canada 24 (1967) 475-494
83. Sundnes G. On the transport of live cod and coalfish. Journal du Conseil International de l'Exploration de la Mer 22 (1957) 191-196
84. Tang Y., Nelson J.A., Reidy S.P., Kerr S.R., and Boutilier R.G. A reappraisal of activity metabolism in Atlantic cod (Gadus morhua). Journal of Fish Biology 44 (1994) 1-10
85. Thomas P., Rahman M.S., Kummer J.A., and Lawson S. Reproductive endocrine dysfunction in Atlantic croaker exposed to hypoxia. Marine Environmental Research 62 Suppl. (2006) S249-S252
86. Tomkiewicz J., Lehmann K.M., and St. John M.A. Oceanographic influences on the distribution of Baltic cod, Gadus morhua, during spawning in the Bornholm Basin of the Baltic Sea. Fisheries Oceanography 7 (1998) 48-62
87. Uzars D. Feeding of cod (Gadus morhua callarias L.) in the Central Baltic in relation to environmental changes. ICES Marine Science Symposia 198 (1994) 612-623
88. 2 levels for aerobic and anaerobic metabolism. Marine Ecology Progress Series 104 (1994) 109-117
89. Van der Veer H.W., Berghahn R., Miller J.M., and Rijnsdorp A.D. Recruitment in flatfish, with special emphasis on North Atlantic species: progress made by the Flatfish Symposia. ICES Journal of Marine Science 57 (2000) 202-215
90. Wannamaker C.M., and Rice J.A. Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States. Journal of Experimental Marine Biology and Ecology 249 (2000) 145-163
91. Whitmore C.M., Warren C.E., and Doudoroff P. Avoidance reactions of salmonid and centrarchid fishes to low oxygen concentrations. Transactions of the American Fisheries Society 89 (1960) 17-26
92. Wilhelm Filho D., Torres M.A., Zaniboni-Filho E., and Pedrosa R.C. Effect of different oxygen tensions on weight gain, feed conversion, and antioxidant status in piapara, Leporinus elongatus (Valenciennes, 1847). Aquaculture (2005) 349-357
93. Winger P.D., He P., and Walsh S.J. Factors affecting the swimming endurance and catchability of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 57 (2000) 1200-1207
94. Wu R.S.S. Period defaunation and recovery in subtropical epibenthic community in relation to organic pollution. Journal of Experimental Marine Biology and Ecology 64 (1982) 253-269
95. Wu R.S.S. Hypoxia: from molecular responses to ecosystem responses. Marine Pollution Bulletin 45 (2002) 35-45
96. Wu R.S.S., Zhou B.S., Randall D.J., Woo N.Y.S., and Lam P.K.S. Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environmental Science and Technology 37 (2003) 1137-1141