Northern shrimp (Pandalus borealis) oxygen consumption and metabolic enzyme activities are severely constrained by hypoxia in the Estuary and Gulf of St. Lawrence

Journal of Experimental Marine Biology and Ecology

Volumn 448, Issue , 2013, Pages 298-307

  Dupont Prinet, Aurélie ^a   Pillet, Marion ^a   Chabot, Denis ^b   Hansen, Tanya ^b   Tremblay, Réjean ^a   Audet, Céline ^a  

^a INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

^b MAURICE LAMONTAGNE INSTITUTE   (Canada)

Author keywords

Antioxidant; Biochemical pathways; Critical oxygen threshold; Crustacean; Enzyme activities; Metabolic rate

Indexed keywords

ANOXIC CONDITIONS; ANTIOXIDANT; BIOCHEMICAL COMPOSITION; COMMERCIAL SPECIES; CRUSTACEAN; DISSOLVED OXYGEN; EGG PRODUCTION; ENZYME ACTIVITY; FORAGING BEHAVIOR; METABOLISM; OXYGEN; VERTICAL MIGRATION;

ATLANTIC OCEAN; CANADA; GULF OF SAINT LAWRENCE; QUEBEC [CANADA]; SAINT LAWRENCE ESTUARY;

EID: 84883179181     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2013.07.019     Document Type: Article

References (87)

1. Abele D., Puntarulo S. Formation of reactive species and induction of antioxidant defence systems in polar and temperate marine invertebrates and fish. Comp. Biochem. Physiol A. 2004, 138:405-415.
2. Abele D., Heise K., Pörtner H.O., Puntarulo S. Temperature dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J. Exp. Biol. 2002, 205:1831-1841.
3. Abele-Oeschger D., Oeschger R. Hypoxia-induced autoxidation of haemoglobin in the benthic invertebrates Arenicola marina (Polychaeta) and Astarte borealis (Bivalvia) and the possible effects of sulphide. J. Exp. Mar. Biol. Ecol. 1995, 187:63-80.
4. Airriess C.N., McMahon B.R. Cardiovascular adaptations enhance tolerance of environmental hypoxia in the crab Cancer magister. J. Exp. Biol. 1994, 190:23-41.
5. Apollonio S., Stevenson D.K., Dunton E.E. Effects of temperature on the biology of the northern shrimp, Pandalus borealis, in the Gulf of Maine. NOAA Tech. Rep. NMFS 1986, 42. (22 pp.).
6. Bailey D.M., Genard B., Collins M.A., Rees J.-F., Unsworth S.K., Battle E.J.V., Bagley P.M., Jamieson A.J., Priede I.G. High swimming and metabolic activity in the deep-sea eel Synaphobranchus kaupii revealed by integrated in situ and in vitro measurements. Physiol. Biochem. Zool. 2005, 78:335-346.
7. Barr L. Diel vertical migration of Pandalus borealis in Kachemak Bay, Alaska. J. Fish Board Can. 1970, 27:669-676.
8. Bergström B.I. The biology of Pandalus. Adv. Mar. Biol. 2000, 38:57-253.
9. Brett J.R. Environmental factors and growth. Bioenergetics and Growth 1979, vol. VIII:599-675. Academic Press, New York. W.S. Hoar, D.J. Randall, J.R. Brett (Eds.).
10. Brett J.R., Groves T.D.D. Physiological energetic. Bioenergetics and Growth 1979, vol. VIII:279-352. Academic Press, New York. W.S. Hoar, D.J. Randall, J.R. Brett (Eds.).
11. Bridges C.R., Brand A.R. Oxygen consumption and oxygen-independence in marine crustaceans. Mar. Ecol. Prog. Ser. 1980, 2:133-141.
12. Bugden G.L. Changes in temperature-salinity characteristics of the deeper waters of the Gulf of St Lawrence over the past several decades. Can. Spec. Publ. Fish. Aquat. Sci. 1991, 113:139-147.
13. Cerezo Valverde J., Aguado-Giménez F., Dolores Hernández M., García García B. Oxygen consumption response to gradual hypoxia in spider crab Maja brachydactyla: critical and lethal oxygen saturations and recovery ability. J. World Aquac. Soc. 2012, 43:433-441.
14. Chabot D., Rondeau A., Sainte-Marie B., Savard L., Surette T., Archambault P. Distribution of benthic invertebrates in the Estuary and Gulf of St. Lawrence. Canadian Science Advisory Secretariat Research Document, 2007/018 vii+108 2007.
15. Childress J.J. The respiratory rates of midwater crustaceans as a function of depth of occurrence and relation to the oxygen minimum layer off Southern California. Comp. Biochem. Physiol. A 1975, 50:787-799.
16. Childress J.J., Somero G.N. Depth-related enzymatic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar. Biol. 1979, 52:273-283.
17. Choi J., Roche H., Caquet T. Effects of physical (hypoxia, hyperoxia) and chemical (potassium dichromate, fenitrothion) stress on antioxidant enzyme activities in Chironomus riparius Mg. (Diptera, Chironomidae) larvae: potential biomarkers. Environ. Toxicol. Chem. 2000, 19:495-500.
18. Claireaux G., Lagardère J.P. Influence of temperature, oxygen and salinity on the metabolism of the European sea bass. J. Sea Res. 1999, 42:157-168.
19. Claireaux G., Webber D.M., Lagardere J.P., Kerr S.R. Influence of water temperature and oxygenation on the aerobic metabolic scope of Atlantic cod (Gadus morhua). J. Sea Res. 2000, 44:257-265.
20. Cochran R.E., Burnett L.E. Respiratory responses of the salt marsh animals, Fundulus heteroclitus, Leiostomus xanthurus, and Palaemonetes pugio to environmental hypoxia and hypercapnia and to the organophosphate pesticide, azinosmethyl. J. Exp. Mar. Biol. Ecol. 1996, 195:125-144.
21. Coiro L.L., Poucher S.L., Miller D.C. Hypoxic effects on growth of Palaemonetes vulgaris larvae and other species: using constant exposure data to estimate cyclic exposure response. J. Exp. Mar. Biol. Ecol. 2000, 247:243-255.
22. Crear B.J., Forteath G.N.R. The effect of extrinsic and intrinsic factors on oxygen consumption by the southern rock lobster, Jasus edwardsii. J. Exp. Mar. Biol. Ecol. 2000, 252:129-147.
23. Crocker C.E., Cech J.J. Effects of environmental hypoxia on oxygen consumption rate and swimming activity in juvenile white sturgeon, Acipenser transmontanus, in relation to temperature and life intervals. Environ. Biol. Fish. 1997, 50:383-389.
24. D'Amours D. The distribution of cod (Gadus morhua) in relation to temperature and oxygen level in the Gulf of St Lawrence. Fish. Oceanogr. 1993, 2:24-29.
25. Daoud D., Chabot D., Audet C., Lambert Y. Temperature induced variation in oxygen consumption of juvenile and adult stages of the northern shrimp, Pandalus borealis. J. Exp. Mar. Biol. Ecol. 2007, 347:30-40.
26. Di Giulio R.T., Benson W.H., Sanders B.M., Van Veld P.A. Biochemical mechanisms: metabolism, adaptation, and toxicity. Fundamentals of Aquatic Toxicology, Effects, Environmental Fate, and Risk Assessment 1995, 523-561. Taylor and Francis, London. G. Rand (Ed.).
27. Dorcas M.E., Hopkins W.A., Roe J.H. Effects of body mass and temperature on standard metabolic rate in the eastern diamondback rattlesnake (Crotalus adamanteus). Copeia 2004, 145-151.
28. Dupont-Prinet A., Chatain B., Grima L., Vandeputte M., Claireaux G., McKenzie D.J. Physiological mechanisms underlying a trade-off between growth rate and tolerance of feed deprivation in the European sea bass (Dicentrarchus labrax). J. Exp. Biol. 2010, 213:1143-1152.
29. Dupont-Prinet A., Vagner M., Chabot D., Audet C. Impact of hypoxia in the St. Lawrence Estuary on the metabolism of Greenland halibut (Reinhardtius hippoglossoides). Can. J. Fish. Aquat. Sci 2013, 70:461-469.
30. Eckert R., Randall D., Burggren W., French K., Math F., Propper A., Henquell L. Physiologie animale: mécanismes et adaptations. Traduction de la 4e édition américaine 1999, De Boeck université (Ed.).
31. Flohé L., Ötting F. Superoxide dismutase assays. Methods Enzymol. 1985, 105:93-105.
32. Fry F.E.J. The effect of environmental factors on the physiology of fish. Environmental Relations and Behavior (VI) 1971, 1-98. Academic Press, New York. W.S. Hoar, D.J. Randall (Eds.).
33. Galbraith P.S., Larouche P., Chassé J., Petrie B. Sea-surface temperature in relation to air temperature in the Gulf of St. Lawrence: interdecadal variability and long term trends. Deep-Sea Res. II 2012, 77-80:10-20.
34. Garcia E.G. The northern shrimp (Pandalus borealis) offshore fishery in the Northeast Atlantic. Advances in Marine Biology 2007, 147-266. Academic Press. D.W. Sims (Ed.).
35. Garcia H.E., Gordon L.I. Oxygen solubility in seawater - better fitting equations. Limnol. Oceanogr. 1992, 37:1307-1312.
36. Gilbert D., Sundby B., Gobeil C., Mucci A., Tremblay G.-H. A seventy-two-year record of diminishing deep-water oxygen in the St Lawrence estuary: the northwest Atlantic connection. Limnol. Oceanogr. 2005, 50:1654-1666.
37. Gilbert D., Chabot D., Archambault P., Rondeau B., Hébert S. Appauvrissement en oxygène dans les eaux profondes du Saint-Laurent marin: Causes possibles et impacts écologiques. Nat. Can. 2007, 131:67-75.
38. González-Peña M.D., Moreira M. Effect of dietary cellulose level on specific dynamic action and ammonia excretion of the prawn Macrobrachium rosenbergii (De Man 1879). Aquac. Res. 2003, 34:821-827.
39. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 2001, Oxford University Press, Oxford, UK, (936 pp.).
40. Hand S.C., Somero G.N. Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and a sulfite-rich deep-sea environment. Biol. Bull. 1983, 165:167-181.
41. Hermes-Lima M., Storey J.M., Storey K.B. Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp. Biochem. Physiol. B 1998, 120:437-448.
42. Herreid C.F. Hypoxia in invertebrates. Comp. Biochem. Physiol. 1980, 67A:311-320.
43. Jamieson P.M., Nyirenda M.J., Walker B.R., Chapman K.E., Seckl J.R. Interactions between oestradiol and glucocorticoid regulatory effects on liver-specific glucocorticoid-inducible genes: possible evidence for a role of hepatic 11beta-hydroxysteroid dehydrogenase type 1. J. Endocrinol. 1999, 160:103-109.
44. Jobling M. A study of some factors affecting rates of oxygen consumption of plaice Pleuronectes platessa L. J. Fish Biol. 1982, 20:501-516.
45. Killen S., Marras S., Steffensen J.F., McKenzie D.J. Aerobic capacity influences the spatial position of individuals within fish schools. Proc. R. Soc. B 2011, 279:357-364.
46. Kramer G.L. Studies on the lethal dissolved oxygen levels for young brown shrimp, Penaeus aztecus Ives. Proceedings of the annual meeting - World Mariculture Society 1975, 6:157-167.
47. Lefrancois C., Claireaux G. Influence of ambient oxygenation and temperature on metabolic scope and scope for heart rate in the common sole Solea solea. Mar. Ecol. Prog. Ser. 2003, 259:273-284.
48. Mallekh R., Lagardere 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. J. Fish Biol. 2002, 60:1105-1115.
49. Mangum C.P. Adaptation of the oxygen transport system to hypoxia in the blue crab, Callinectes sapidus. Am. Zool. 1997, 37:604-611.
50. Marie B., Genard B., Rees J.F., Zal F. Effect of ambient oxygen concentration on activities of enzymatic antioxidant defences and aerobic metabolism in the hydrothermal vent worm, Paralvinella grasslei. Mar. Biol. 2006, 150:273-284.
51. Marqueze A., Ribarcki F., Kirst I., Kucharski L.C., Da Silva R.S.M. Glucose metabolism in the hepatopancreas of the crab Neohelice granulata maintained on carbohydrate-rich or high-protein diets: anoxia and recovery. J. Exp. Mar. Biol. Ecol. 2011, 404:40-46.
52. McCue M.D. Specific dynamic action: a century of investigation. Comp. Biochem. Physiol. A 2006, 144:381-394.
53. McMahon B.R. Respiratory and circulatory compensation to hypoxia in crustaceans. Respir. Physiol. 2001, 128:349-364.
54. McMahon B.R., Wilkens J.L. Respiratory and circulatory responses to hypoxia in the lobster Homarus americanus. J. Exp. Biol. 1975, 62:637-655.
55. Miller D.C., Poucher S.L., Coiro L. Determination of lethal dissolved oxygen levels for selected marine and estuarine fishes, crustaceans, and a bivalve. Mar. Biol. 2002, 140:287-296.
56. Nelson J.A., Chabot D. General energy metabolism. Encyclopedia of Fish Physiology: From Genome to Environment 2011, vol. 3:1566-1572. Academic Press, San Diego.
57. Newell R.C., Johson L.G., Kofoed L.H. Adjustment of the components of energy balance in response to temperature change in Ostrea edulis. Oecologia 1977, 30:97-110.
58. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 70:158-169.
59. Pannunzio T.M., Storey K.B. Antioxidant defenses and lipid peroxidation during anoxia stress and aerobic recovery in the marine gastropod Littorina littorea. J. Exp. Mar. Biol. Ecol. 1998, 221:277-292.
60. Parrilla-Taylor D.P., Zenteno-Savín T. Antioxidant enzyme activities in Pacific white shrimp (Litopenaeus vannamei) in response to environmental hypoxia and reoxygenation. Aquac. 2011, 318:379-383.
61. Paschke K., Cumillaf J.P., Loyola S., Gebauer P., Urbina M., Chimal M.E., Pascual C., Rosas C. Effect of dissolved oxygen level on respiratory metabolism, nutritional physiology, and immune condition of southern king crab Lithodes santolla (Molina, 1782) (Decapoda, Lithodidae). Mar. Biol. 2010, 157:7-18.
62. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 1977, 83:346-356.
63. Petrescu I., Bojan O., Saied M. Determination of phosphoenolpyruvate carboxykinase activity with deoxyguanosine 5'-diphosphate as nucleotide substrate. Anal. Biochem. 1979, 96:279-281.
64. Portelance B., Gagne A., Pilote S. Étude de la distribution verticale de la crevette nordique (Pandalus borealis) avec un échantillonneur vertical étagé et une caméra sous-marine. Québec (province): Direction générale des pêches maritimes 1988, Direction de la recherche scientifique et technique, (39 pp.).
65. Pörtner H.O. Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J. Exp. Biol. 2010, 213:881-893.
66. O2(S) in oxyconforming and oxyregulating animals, gas-exchange, metabolic rate and the mode of energy production. Vertebrate Gas Transport Cascade - adaptations to environment and mode of life 1993, 330-357. CRC Press Inc., Boca Raton. J.E.P. Bicudo (Ed.).
67. Pörtner H.O., Peck M.A. Climate change effects on fishes and fisheries: towards a cause-and-effect understanding. J. Fish Biol. 2010, 77:1745-1779.
68. R Development Core Team R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2011, (http://www.R-project.org/).
69. Reiber C.L., McMahon B.R. Progressive hypoxia's effects on the crustacean cardiovascular system: a comparison of the freshwater crayfish (Procambarus clarkii) and the lobster (Homarus americanus). J. Comp. Physiol. B 1998, 168:68-76.
70. Ruppert E.E., Fox R.S., Barnes R.D. Invertebrate Zoology: A Functional Ecology Approach 2003, Brooks Cole College Publishing, Orlando, FL, (1008 pp.).
71. Savard L. Stock status indicators and reference points consistent with a precautionary approach for northern shrimp in the Gulf of St. Lawrence. DFO Canadian Scientific Advisory Secretariat Research Document, 2012/006, ii + 2012, (29 pp.).
72. Savard L., Bourdages H. Update of the estimation of northern shrimp Pandalus borealis biomass and abundance from the trawl survey in the Estuary and the northern Gulf of St. Lawrence in 2012. DFO Can. Sci. Advis. Sec. Res. Doc., 2012/004: ii+33 2012.
73. Schmidt-Nielsen K. Scaling: Why Is Animal Size So Important 1984, Cambridge University Press, Cambridge, UK, (241 pp.).
74. Schmidt-Nielsen K. Animal Physiology: Adaptation and Environment 1990, Cambridge University Press, Cambridge, UK, (699 pp.).
75. Schurmann H., Steffensen J.F. Effects of temperature, hypoxia and activity on the metabolism of juvenile Atlantic cod. J. Fish Biol. 1997, 50:1166-1180.
76. Secor S.M. Specific dynamic action: a review of the postprandial metabolic response. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 2009, 179:1-56.
77. Shumway S.E., Perkins H.C., Schick D.F., Stickney A.P. Synopsis of biological data on the pink shrimp, Pandalus borealis Kroeyer, 1838. FAO Fish. Synop. 1985, 144. (57 pp.).
78. Simard Y., Savard L. Variability, spatial patterns and scales of similarity in size-frequency distributions of the northern shrimp (Pandalus borealis) and its migrations in the Gulf of St Lawrence. Can. J. Fish. Aquat. Sci. 1990, 47:794-804.
79. Soñanez-Organis J.G., Rodriguez-Armenta M., Leal-Rubio B., Peregrino-Uriarte A.B., Gomez-Jiménez S., Yepiz-Plascencia G. Alternative splicing generates two lactate dehydrogenase subunits differentially expressed during hypoxia via HIF-1 in the shrimp Litopenaeus vannamei. Biochimie 2012, 94:1250-1260.
80. Steffensen J.F. Some errors in respirometry of aquatic breathers - how to avoid and correct for them. Fish Physiol. Biochem. 1989, 6:49-59.
81. Taylor D.L., Peck M.A. Daily energy requirements and trophic positioning of the sand shrimp Crangon septemspinosa. Mar. Biol. 2004, 145:167-177.
82. Thompson R.K., Pritchard A.W. Respiratory adaptations of two burrowing crustaceans, Callianassa californiensis and Upogebia pugettensis (Decapoda, Thalassinidea). Biol. Bull. 1969, 136:274-287.
83. 2 levels for aerobic and anaerobic metabolism. Mar. Ecol. Prog. Ser. 1994, 104:109-117.
84. Wang T., Lefevre S., Huong D.T.T., Van Cong M. The effects of hypoxia on growth and digestion. Fish Physiology 2009, vol. 27:361-396. Academic Press/Elsevier, San Diego, California. J.J. Richards, C.J. Brauner, A.P. Farrell (Eds.).
85. Young R.E. Responses to respiratory stress in relation to blood pigment affinity in Goniopsis cruentata (Latreille) and (to a lesser extent) in Cardisoma guanhumi Latreille. J. Exp. Mar. Biol. Ecol. 1973, 11:91-102.
86. Zahl I., Kiessling A., Samuelsen O., Olsen R. Anesthesia induces stress in Atlantic salmon (Salmo salar), Atlantic cod (Gadus morhua) and Atlantic halibut (Hippoglossus hippoglossus). Fish Physiol. Biochem. 2010, 36:719-730.
87. Zeuthen E. Oxygen uptake as related to body size in organisms. Q. Rev. Biol. 1953, 28:1-12.