Effect of closed v. intermittent-flow respirometry on hypoxia tolerance in the shiner perch Cymatogaster aggregata

Journal of Fish Biology

Volumn 88, Issue 1, 2016, Pages 252-264

  Snyder, S ^a   Nadler, L E ^b   Bayley, J S ^c   Svendsen, M B S ^d   Johansen, J L ^e   Domenici, P ^f   Steffensen, J F ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b JAMES COOK UNIVERSITY   (Australia)

^c AARHUS UNIVERSITY   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e University of Texas at Austin   (United States)

^f CNR   (Italy)

Author keywords

Aquatic breathers; Critical oxygen saturation level; Hypoxic; Physiology; Respiration; Stress

Indexed keywords

AMMONIA; CARBON DIOXIDE; OXYGEN;

ANIMAL; ANOXIA; COMPARATIVE STUDY; METABOLISM; OXYGEN CONSUMPTION; PERCH; PHYSIOLOGY;

AMMONIA; ANIMALS; ANOXIA; CARBON DIOXIDE; OXYGEN; OXYGEN CONSUMPTION; PERCHES;

EID: 84956739417     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/jfb.12837     Document Type: Article

References (69)

1. Aboagye, D. L. & Allen, P. J. (2014). Metabolic and locomotor responses of juvenile paddlefish Polyodon spathula hypoxia and temperature. Comparative Biochemistry and Physiology A 169, 51-59.
2. Ball, I. R. (1967). The relative susceptibilities of some species of fresh-water fish to poisons - I. Ammonia. Water Research 1, 767-775.
3. Brett, J. R. & Zala, C. A. (1975). Daily pattern of nitrogen excretion and oxygen consumption of sockeye salmon (Oncorhynchus nerka) under controlled conditions. Journal of the Fisheries Research Board of Canada 32, 2479-2486.
4. Brix, O., Clements, K. D. & Wells, R. M. G. (1999). Haemoglobin components and oxygen transport in relation to habitat selection in triplefin fishes (Tripterygiidae). Journal of Comparative Physiology B 169, 329-334.
5. Burnett, L. E. (1997). The challenges of living in hypoxic and hypercapnic aquatic environments. American Zoologist 37, 633-640.
6. Cameron, J. N. (1976). Branchial ion uptake in arctic grayling: resting values and effects of acid-base disturbance. Journal of Experimental Biology 64, 711-725.
7. Carter, C., Houlihan, D., Kiessling, A., Médale, F. & Jobling, M. (2001). Physiological effects of feeding. In Food Intake in Fish (Houlihan, D., Boujard, T. & Jobling, M., eds), pp. 297-331. Oxford: Blackwell Science.
8. Cech, J. J. (1990). Respirometry. In Methods for Fish Biology (Schreck, C. B. & Moyle, P. B., eds), pp. 335-362. Bethesda, MD: American Fisheries Society.
9. Cech, J. J. & Brauner, C. J. (2011). Techniques in respiratory physiology. In Encyclopedia of Fish Physiology from Genome to Environment (Farrell, A. P., ed.), pp. 846-853. San Diego, CA: Academic Press.
10. Cech, J. J. & Crocker, C. E. (2002). Physiology of sturgeon: effects of hypoxia and hypercapnia. Journal of Applied Ichthyology 18, 320-324.
11. Cech, J. J., Campagna, C. G. & Mitchell, S. J. (1979). Respiratory responses of largemouth bass (Micropterus salmoides) to environmental changes in temperature and dissolved oxygen. Transactions of the American Fisheries Society 108, 166-171.
12. Chabot, D., Steffensen, J. F. & Farrell, A. P. (2016). The determination of standard metabolic rate in fishes. Journal of Fish Biology (in press, this issue).
13. Chapman, L. J., Chapman, C. A., Nordlie, F. G. & Rose, A. E. (2002). Physiological refugia: swamps, hypoxia tolerance and maintenance of fish diversity in the Lake Victoria region. Comparative Biochemistry and Physiology A 133, 421-437.
14. Claireaux, G. & Chabot, D. (2016). Responses by fishes to environmental hypoxia: integration through Fry's concept of aerobic metabolic scope. Journal of Fish Biology (in press, this issue).
15. Claireaux, G., Webber, D. M., Lagardere, J. P. & Kerr, S. R. (2000). Influence of water temperature and oxygen on the aerobic metabolic scope of Atlantic cod (Gadus morhua). Journal of Sea Research 44, 257-265.
16. Clark, T. D., Sandblom, E. & Jutfelt, F. (2013). Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance, and recommendations. Journal of Experimental Biology 216, 2771-2782.
17. Cochran, R. E. & Burnett, L. E. (1996). Respiratory responses of the salt marsh animals, Fundulus heteroclitus, Leiostomus xanthurus, and Palaemonetes pugio to environmental hypoxia and hypercapnia and to the organophosphate pesticide, azinphosmethyl. Journal of Experimental Marine Biology and Ecology 195, 125-144.
18. Crocker, C. E. & Cech, J. J. (2002). The effects of dissolved gases on oxygen consumption rate and ventilation frequency in white sturgeon, Acipenser transmontanus. Journal of Applied Ichthyology 18, 338-340.
19. Cruz-Neto, A. P. C. & Steffensen, J. F. (1997). The effects of acute hypoxia and hypercapnia on oxygen consumption of the freshwater European eel. Journal of Fish Biology 50, 759-769.
20. Davis, J. C. (1975). Minimal dissolved oxygen requirements of aquatic life with emphasis of Canadian species: a review. Journal of the Fisheries Research Board of Canada 32, 2295-2332.
21. Diaz, R. J. & Breitburg, D. L. (2009). The hypoxic environment. In Hypoxia in Fishes (Richards, J. G., Farrell, A. P. & Brauner, C. J., eds), pp. 1-23. San Diego, CA: Elsevier.
22. Diaz, R. J. & Rosenberg, R. (2008). Spreading dead zones and consequences for marine ecosystems. Science 321, 926-929.
23. Domenici, P., Steffensen, J. F. & Batty, R. S. (2000). The effect of progressive hypoxia on swimming activity and schooling in Atlantic herring. Journal of Fish Biology 57, 1526-1538.
24. Eliason, E. J. & Farrell, A. P. (2014). Effect of hypoxia on specific dynamic action and postprandial cardiovascular physiology in rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology A 171, 44-50.
25. Eriksen, N. T. (2002). Accuracy and precision of aquatic respirometers with emphasis on monophase oxystats. Fish Physiology and Biochemistry 26, 139-147.
26. Eschmeyer, W. N., Herald, E. S. & Hammann, H. (1983). A Field Guide to Pacific Coast Fishes of North America. Boston, MA: Houghton Mifflin Company.
27. Herbert, N. A. & Steffensen, J. F. (2005). The response of Atlantic cod, Gadus morhua, to progressive hypoxia: fish swimming speed and physiological stress. Marine Biology 147, 1403-1412.
28. Herbert, N. A. & Steffensen, J. F. (2006). Hypoxia increases the behavioral activity of schooling herring: a response to physiological stress or respiratory distress? Marine Biology 149, 1217-1225.
29. Johansen, J. L. & Jones, G. P. (2011). Increasing ocean temperature reduced the metabolic performance and swimming ability of coral reef damselfishes. Global Change Biology 17, 2971-2979.
30. Johansen, J. L., Herbert, N. A. & Steffensen, J. F. (2006). The behavioural and physiological response of Atlantic cod Gadus morhua L. to short-term acute hypoxia. Journal of Fish Biology 68, 1918-1924.
31. Kaufmann, R., Forstner, H. & Wieser, W. (1989). Respirometry - methods and approaches. In Techniques in Comparative Respiratory Physiology (Bridges, C. R. & Butler, P. J., eds), pp. 51-76. Cambridge: Cambridge University Press.
32. Keys, A. B. (1930). The measurement of the respiratory exchange of aquatic animals. Biological Bulletin 59, 187-198.
33. Killen, S. S., Marras, S., Ryan, M. R., Domenici, P. & McKenzie, D. J. (2012). A relationship between metabolic rate and risk-taking behaviour is revealed during hypoxia in juvenile European sea bass. Functional Ecology 26, 134-143.
34. Lindstrom, M. J. & Bates, D. M. (1988). Newton-Raphson and EM algorithms for linear mixed effects models for repeated-measures data. Journal of the American Statistical Association 83, 1014-1022.
35. Magaud, H., Migeon, B., Morfin, P., Garric, J. & Vindimian, E. (1997). Modelling fish mortality due to urban storm run-off: interacting effects of hypoxia and un-ionized ammonia. Water Research 31, 211-218.
36. Mandic, M., Todgham, A. E. & Richards, J. G. (2009). Mechanisms and evolution of hypoxia tolerance in fish. Proceedings of the Royal Society B 276, 735-744.
37. Mandic, M., Speers-Roesch, B. & Richards, J. G. (2013). Hypoxia tolerance in sculpins is associated with high anaerobic enzyme activity in brain but not in liver or muscle. Physiological and Biochemical Zoology 86, 92-105.
38. Marvin, D. E. & Heath, A. G. (1968). Cardiac and respiratory responses to gradual hypoxia in three ecologically distinct species of fresh-water fish. Comparative Biochemistry and Physiology 27, 349-355.
39. McKenzie, D. J., Taylor, E. W., Dalla Valle, A. Z. & Steffensen, J. F. (2002). Tolerance of acute hypercapnic acidosis by the European eel (Anguilla anguilla). Journal of Comparative Physiology B 172, 339-346.
40. McKenzie, D. J., Piccolella, M., Dalla Valle, A. Z., Taylor, E. W., Bolis, C. L. & Steffensen, J. F. (2003). Tolerance of chronic hypercapnia by the European eel Anguilla anguilla. Journal of Experimental Biology 206, 1717-1726.
41. Meade, J. W. (1985). Allowable ammonia for fish culture. Progressive Fish-Culturist 47, 135-145.
42. Mucci, A., Starr, M., Gilbert, D. & Sundby, B. (2011). Acidification of Lower St Lawrence Estuary bottom waters. Atmosphere-Ocean 49, 206-218.
43. Nelson, J. A. (2016) Oxygen consumption rate versus rate of energy utilisation of fishes: a comparison and brief history of the two measurements. Journal of Fish Biology (in press, this issue).
44. Niimi, A. J. & Beamish, F. W. (1974). Bioenergetics and growth of largemouth bass (Micropterus salmoides) in relation to body weight and temperature. Canadian Journal of Zoology 52, 447-456.
45. Nilsson, G. E. & Ostlund-Nilsson, S. (2004). Hypoxia in paradise: widespread hypoxia tolerance in coral reef fishes. Proceedings of the Royal Society B 271, S30-S33.
46. Nilsson, G. E., Ostlund-Nilsson, S. & Munday, P. L. (2010). Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate. Comparative Biochemistry and Physiology A 156, 389-393.
47. Perry, S. F., Jonz, M. G. & Gilmour, K. M. (2009). Oxygen sensing and the hypoxic ventilatory response. In Hypoxia in Fishes (Richards, J. G., Farrell, A. P. & Brauner, C. J., eds), pp. 193-253. San Diego, CA: Elsevier.
48. Porter, S. M. (2001). Effects of size and light on respiration and activity of walleye pollock (Theragra chalcogramma) larvae. Journal of Experimental Marine Biology and Ecology 256, 253-265.
49. 2 on marine animals: from Earth history to global change. Journal of Geophysical Research 110, 1-15.
50. Pursche, A. R., Suthers, I. M. & Taylor, M. D. (2009). Tethering induces increased stress artifacts in social fish species. Journal of Fish Biology 74, 1525-1531.
51. Randall, D. J. & Tsui, T. K. N. (2002). Ammonia toxicity in fish. Marine Pollution Bulletin 45, 17-23.
52. Remen, M., Imsland, A. K., Stefansson, S. O., Jonassen, T. M. & Foss, A. (2008). Interactive effects of ammonia and oxygen on growth and physiological status of juvenile Atlantic cod (Gadus morhua). Aquaculture 274, 292-299.
53. Riggs, A. (1970). Gas exchange in fish. In Fish Physiology, Vol. 4 (Hoar, W. S. & Randall, D. J., eds), pp. 253-292. New York, NY: Academic Press.
54. Schurmann, H. & Steffensen, J. F. (1997). Effects of temperature, hypoxia and activity on the metabolism of juvenile cod. Journal of Fish Biology 50, 1166-1180.
55. Smart, G. (1976). The effect of ammonia exposure on gill structure of rainbow trout (Salmo gairdneri). Journal of Fish Biology 8, 471-475.
56. Sollid, J., De Angelis, P., Gundersen, K. & Nilsson, G. E. (2003). Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. Journal of Experimental Biology 206, 3667-3673.
57. Speers-Roesch, B., Mandic, M., Groom, D. J. E. & Richards, J. G. (2013). Critical oxygen tensions as predictors of hypoxia tolerance and metabolic responses during hypoxia exposure in fishes. Journal of Experimental Marine Biology and Ecology 440, 239-249.
58. Steffensen, J. F. (1989). Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry 6, 49-59.
59. Steffensen, J. F., Bushnell, P. G. & Schurmann, H. (1994). Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation. Polar Biology 14, 49-54.
60. Stevens, E. D. (1992). Use of plastic materials in oxygen-measuring systems. Journal of Applied Physiology 72, 801-804.
61. Stramma, L., Prince, E. D., Schmidtko, S., Luo, J., Hoolihan, J. P., Visbeck, M., Wallace, D. W. R., Brandt, P. & Kortzinger, A. (2011). Expansion of oxygen minimum zones may reduce available habitat for tropical pelagic fishes. Nature Climate Change 2, 33-37.
62. Svendsen, M. B. S., Bushnell, P. G. & Steffensen, J. F. (2016). Design and setup of intermittent-flow respirometry system for aquatic organisms. Journal of Fish Biology (in press, this issue).
63. Tang, P. S. (1933). On the rate of oxygen consumption by tissues and lower organisms as a function of oxygen tension. Quarterly Review of Biology 8, 260-274.
64. Thetmeyer, H. (1997). Diel rhythms of swimming activity and oxygen consumption in Gobiusculus flavescens (Fabricius) and Pomatochistus minutus (Pallas) (Teleostei: Gobiidae). Journal of Experimental Marine Biology and Ecology 218, 187-198.
65. Truchot, J.-P. (1988). Problems of acid-base balance in rapidly changing intertidal environments. American Zoologist 28, 55-64.
66. Ultsch, G. R., Ott, M. E. & Heisler, N. (1980). Standard metabolic rate, critical oxygen tension and aerobic scope for spontaneous activity of trout (Salmo gairdneri) and carp (Cyprinus carpio) in acidified water. Comparative Biochemistry and Physiology A 67, 329-335.
67. Vedel, N. E., Korsgaard, B. & Jensen, F. B. (1998). Isolated and combined exposure to ammonia and nitrite in rainbow trout (Oncorhynchus mykiss): effects on electrolyte status, blood respiratory properties and brain glutamine/glutamate concentrations. Aquatic Toxicology 41, 325-342.
68. Zhang, J., Gilbert, D., Gooday, A. J., Levin, L., Naqvi, W. A., Middelburg, J. J., Scranton, M., Ekau, W., Pena, A., Dewitte, R., Oguz, T., Monteiro, P. M. S., Urban, E., Rabalais, N. N., Ittekkot, V., Kemp, W. M., Ulloa, O., Emgren, R., Escobar-Briones, E. & Van der Plas, A. K. (2010). Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences 7, 1443-1467.
69. Pinheiro, J., Bates D., DebRoy, S., Sarkar, D. & R Core Team (2015). nlme: Linear and Nonlinear Mixed Effects Models. R Package Version 3.1. Available at http://CRAN.R-project.org/package=nlme/ (last accessed 2 February 2015).