Acid-base and ion balance in fishes with bimodal respiration

Journal of Fish Biology

Volumn 84, Issue 3, 2014, Pages 682-704

  Shartau, R B ^a   Brauner, C J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Air breathing; Facultative; Intracellular pH; Ionoregulation; Obligate; pH regulation

Indexed keywords

ACID BASE BALANCE; ADAPTATION; AIR; ANIMAL; ANOXIA; ARTICLE; BREATHING; CELL PH; EVOLUTION; FACULTATIVE; FISH; GILL; IONOREGULATION; OBLIGATE; PH; PH REGULATION; PHYSIOLOGY;

AIR BREATHING; FACULTATIVE; INTRACELLULAR PH; IONOREGULATION; OBLIGATE; PH REGULATION;

ACID-BASE EQUILIBRIUM; ADAPTATION, PHYSIOLOGICAL; AIR; ANIMALS; ANOXIA; BIOLOGICAL EVOLUTION; FISHES; GILLS; HYDROGEN-ION CONCENTRATION; RESPIRATION;

EID: 84895197130     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/jfb.12310     Document Type: Article

References (79)

1. Amin-Naves, J., Giusti, H. & Glass, M. L. (2004). Effects of acute temperature changes on aerial and aquatic gas exchange, pulmonary ventilation and blood gas status in the South American lungfish, Lepidosiren paradoxa. Comparative Biochemistry and Physiology A 138, 133-139.
2. 2-tolerant chondrostean, white sturgeon (Acipenser transmontanus). Comparative Biochemistry and Physiology A 161, 61-68.
3. Baker, D. W., Matey, V., Huynh, K. T., Wilson, J. M., Morgan, J. D. & Brauner, C. J. (2009). Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 296, R1868-R1880.
4. 2 tolerance in white sturgeon (Acipenser transmontanus) is associated with protection of maximum cardiac performance during hypercapnia in situ. Physiological and Biochemical Zoology 84, 239-248.
5. Beitinger, T. L., Pettit, M. J. & Hutchison, V. H. (1985). Oxygen transfer characteristics of the blood of reedfish, Erpetoichthys calabaricus. Comparative Biochemistry and Physiology 82, 553-558.
6. Berenbrink, M., Koldkjaer, P., Kepp, O. & Cossins, A. R. (2005). Evolution of oxygen secretion in fishes and the emergence of a complex physiological system. Science 307, 1752-1757.
7. Brauner, C. J. & Baker, D. W. (2009). Patterns of acid-base regulation during exposure to hypercarbia in fish. In Cardio-Respiratory Control in Vertebrates: Comparative and Evolutionary Aspects (Glass, M. L. & Wood, S. C., eds), pp. 43-63. Berlin: Springer-Verlag.
8. Brauner, C. J. & Berenbrink, M. (2007). Gas transport and exchange. In Primitive Fishes, Fish Physiology (McKenzie, D. J., Farrell, A. P. & Brauner, C. J., eds), pp. 213-282. New York, NY: Elsevier.
9. Brauner, C. J. & Randall, D. J. (1996). The interaction between oxygen and carbon dioxide movements in fishes. Comparative Biochemistry and Physiology A 113, 83-90.
10. Brauner, C. J., Wang, T., Wang, Y., Richards, J. G., Gonzalez, R. J., Bernier, N. J., Xi, W., Patrick, M. & Val, A. L. (2004a). Limited extracellular but complete intracellular acid-base regulation during short-term environmental hypercapnia in the armoured catfish, Liposarcus pardalis. Journal of Experimental Biology 207, 3381-3390.
11. Brauner, C. J., Matey, V., Wilson, J. M., Bernier, N. J. & Val, A. L. (2004b). Transition in organ function during the evolution of air-breathing; insights from Arapaima gigas, an obligate air-breathing teleost from the Amazon. Journal of Experimental Biology 207, 1433-1438.
12. Burleson, M., Shipman, B. & Smatresk, N. (1998). Ventilation and acid-base recovery following exhausting activity in an air-breathing fish. Journal of Experimental Biology 201, 1359-1368.
13. Cameron, J. N. & Wood, C. M. (1978). Renal function and acid-base regulation in two Amazonian erythrinid fishes: Hoplias malabaricus, a water breather, and Hoplerythrinus unitaeniatus, a facultative air breather. Canadian Journal of Zoology 56, 917-930.
14. Dejours, P. (1988). Respiration in Water and Air: Adaptations, Regulation and Evolution. Amsterdam: Elsevier.
15. Evans, D. H., Piermarini, P. M. & Choe, K. P. (2005). The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiological Reviews 85, 97-177.
16. Farmer, C. G. & Jackson, D. C. (1998). Air-breathing during activity in the fishes Amia calva and Lepisosteus oculatus. Journal of Experimental Biology 201, 943-948.
17. Gilmour, K. M. & Perry, S. F. (2009). Carbonic anhydrase and acid-base regulation in fish. Journal of Experimental Biology 212, 1647-1661.
18. Gilmour, K. M., Euverman, R. M., Esbaugh, A. J., Kenney, L., Chew, S. F., Ip, Y. K. & Perry, S. F. (2007). Mechanisms of acid-base regulation in the African lungfish Protopterus annectens. Journal of Experimental Biology 210, 1944-1959.
19. Gonzalez, R. J., Milligan, L., Pagnotta, A. & McDonald, D. G. (2001). Effect of air breathing on acid-base and ion regulation after exhaustive exercise and during low pH exposure in the bowfin, Amia calva. Physiological and Biochemical Zoology 74, 502-509.
20. Gonzalez, R. J., Brauner, C. J., Wang, Y. X., Richards, J. G., Patrick, M. L., Xi, W., Matey, V. & Val, A. L. (2010). Impact of ontogenetic changes in branchial morphology on gill function in Arapaima gigas. Physiological and Biochemical Zoology 83, 322-332.
21. Goss, G. G., Perry, S. F., Fryer, J. N. & Laurent, P. (1998). Gill morphology and acid-base regulation in freshwater fishes. Comparative Biochemistry and Physiology A 119, 107-115.
22. Graham, J. B. (1997). Air Breathing Fishes: Evolution, Diversity, and Adaptation. San Diego, CA: Academic Press.
23. Hanson, L. M., Baker, D. W., Kuchel, L. J., Farrell, A. P., Val, A. L. & Brauner, C. J. (2009). Intrinsic mechanical properties of the perfused armoured catfish heart with special reference to the effects of hypercapnic acidosis on maximum cardiac performance. Journal of Experimental Biology 212, 1270-1276.
24. Heisler, N. (1982). Intracellular and extracellular acid-base regulation in the tropical fresh-water teleost fish Synbranchus marmoratus in response to the transition from water breathing to air breathing. Journal of Experimental Biology 99, 9-28.
25. Heisler, N. (1984). Acid-base regulation in fishes. In Fish Physiology, Vol. 10 (Hoar, W. S. & Randall, D. J., eds), pp. 315-401. San Diego, CA: Academic.
26. Heisler, N., Weitz, H. & Weitz, A. M. (1976). Hypercapnia and resultant bicarbonate transfer processes in an elasmobranch fish (Scyliorhinus stellaris). Bulletin Européen de Physiopathologie Respiratoire 12, 77-86.
27. Hochachka, P. W., Moon, T. W., Bailey, J. & Hulbert, W. C. (1978). The osteoglossid kidney: correlations of structure, function, and metabolism with transition to air breathing. Canadian Journal of Zoology 56, 820-832.
28. Huang, C.-Y. & Lin, H.-C. (2011). The effect of acidity on gill variations in the aquatic air-breathing fish, Trichogaster lalius. Comparative Biochemistry and Physiology A 158, 61-71.
29. Huang, C.-Y., Lee, W. & Lin, H.-C. (2008). Functional differentiation in the anterior gills of the aquatic air-breathing fish, Trichogaster leeri. Journal of Comparative Physiology B 178, 111-121.
30. +-ATPase in the gills of the aquatic air-breathing fish Trichogaster microlepis in response to salinity variation. Comparative Biochemistry and Physiology A 155, 309-318.
31. Hughes, G. M. & Morgan, M. (1973). The structure of fish gills in relation to their respiratory function. Biological Reviews 48, 419-475.
32. Huynh, K. T., Baker, D. W., Harris, R., Church, J. & Brauner, C. J. (2011). Capacity for intracellular pH compensation during hypercapnia in white sturgeon primary liver cells. Journal of Comparative Physiology B 181, 893-904.
33. Ishimatsu, A. & Itazawa, Y. (1983). Blood oxygen levels and acid-base status following air exposure in an air-breathing fish, Channa argus: the role of air ventilation. Comparative Biochemistry and Physiology A 74, 787-793.
34. Janis, C. M., Devlin, K., Warren, D. E. & Witzmann, F. (2012). Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis. Proceedings of the Royal Society B 279, 3035-3040.
35. Johansen, K. & Lenfant, C. (1968). Respiration in the African lungfish Protopterus Aethiopicus: II. Control of breathing. Journal of Experimental Biology 49, 453-468.
36. Johansen, K., Lenfant, C., Schmidt-Nielsen, K. & Petersen, J. (1968). Gas exchange and control of breathing in the electric eel, Electrophorus electricus. Zeitschrift für vergleichende Physiologie 61, 137-163.
37. Johansen, K., Hanson, D. & Lenfant, C. (1970). Respiration in a primitive air breather, Amia calva. Respiration Physiology 9, 162-174.
38. Lapennas, G. N. (1983). The magnitude if the Bohr coefficient: optimal for oxygen delivery. Respiration Physiology 54, 161-172.
39. Larsen, B. K. & Jensen, F. B. (1997). Influence of ionic composition on acid-base regulation in rainbow trout (Oncorhynchus mykiss) exposed to environmental hypercapnia. Fish Physiology and Biochemistry 16, 157-170.
40. Lefevre, S., Domenici, P. & McKenzie D.J. (2014). Swimming in air breathing fishes. Journal of Fish Biology 84 661-681.
41. Lenfant, C. & Johansen, K. (1968). Respiration in the African lungfish Protopterus aethiopicus: I. Respiratory properties of blood and normal patterns of breathing and gas exchange. Journal of Experimental Biology 49, 437-452.
42. Lenfant, C., Johansen, K. & Grigg, G. C. (1966). Respiratory properties of blood and pattern of gas exchange in the lungfish Neoceratodus forsteri (Krefft). Respiration Physiology 2, 1-21.
43. Lin, H.-C. & Sung, W.-T. (2003). The distribution of mitochondria-rich cells in the gills of air-breathing fishes. Physiological and Biochemical Zoology 76, 215-228.
44. McKenzie, D. J. & Randall, D. J. (1990). Does Amia calva aestivate? Fish Physiology and Biochemistry 8, 147-158.
45. McKenzie, D. J., Steffensen, J. F., Taylor, E. W. & Abe, A. S. (2012). The contribution of air breathing to aerobic scope and exercise performance in the banded knifefish Gymnotus carapo L. Journal of Experimental Biology 215, 1323-1330.
46. + exchange with the environment after exhaustive exercise in the rainbow trout. Journal of Experimental Biology 123, 93-121.
47. Nilsson, S. (1986). Control of gill blood flow. In Fish Physiology: Recent Advances (Nilsson, S. & Holmgren, S., eds), pp. 86-101. London: Croom Helm.
48. - transport in trout gill mitochondrion-rich cells. American Journal of Physiology 296, R1161-R1169.
49. Patel, M., Iftikar, F. I., Leonard, E. M., Ip, Y. K. & Wood, C. M. (2009a). Ionoregulatory physiology of two species of African lungfishes Protopterus dolloi and Protopterus annectens. Journal of Fish Biology 75, 862-884.
50. Patel, M., Iftikar, F. I., Smith, R. W., Ip, Y. K. & Wood, C. M. (2009b). Water balance and renal function in two species of African lungfish Protopterus dolloi and Protopterus annectens. Comparative Biochemistry and Physiology A 152, 149-157.
51. Perry, S. F. (1997). The chloride cell: structure and function in the gills of freshwater fishes. Annual Review of Physiology 59, 325-347.
52. 2 excretion in fish: unanswered questions and emerging models. Respiratory Physiology and Neurobiology 154, 199-215.
53. Perry, S. F., Gilmour, K. M., Swenson, E. R., Vulesevic, B., Chew, S. F. & Ip, Y. K. (2005). An investigation of the role of carbonic anhydrase in aquatic and aerial gas transfer in the African lungfish Protopterus dolloi. Journal of Experimental Biology 208, 3805-3815.
54. Perry, S. F., Euverman, R., Wang, T., Loong, A. M., Chew, S. F., Ip, Y. K. & Gilmour, K. M. (2008). Control of breathing in African lungfish (Protopterus dolloi): a comparison of aquatic and cocooned (terrestrialized) animals. Respiratory Physiology and Neurobiology 160, 8-17.
55. Perry, S. F., Vulesevic, B., Grosell, M. & Bayaa, M. (2009). Evidence that SLC26 anion transporters mediate branchial chloride uptake in adult zebrafish (Danio rerio). American Journal of Physiology 297, R988-R997.
56. Putnam, R. W. & Roos, A. (1997). Intracellular pH. In Handbook of Physiology, Vol. 14 (Hoffman, J. & Jamieson, J., eds), pp. 389-440. Oxford: Oxford University Press.
57. Rahn, H., Rahn, K. B., Howell, B. J., Gans, C. & Tenney, S. M. (1971). Air breathing of the garfish (Lepisosteus osseus). Respiration Physiology 11, 285-307.
58. Randall, D. J., Farrell, A. P. & Haswell, M. S. (1978a). Carbon dioxide excretion in the pirarucu (Arapaima gigas), an obligate air-breathing fish. Canadian Journal of Zoology 56, 977-982.
59. Randall, D. J., Farrell, A. P. & Haswell, M. S. (1978b). Carbon dioxide excretion in the jeju, Hoplerythrinus unitaeniatus, a facultative air-breathing teleost. Canadian Journal of Zoology 56, 970-973.
60. Randall, D. J., Cameron, J. N., Daxboeck, C. & Smatresk, N. (1981). Aspects of bimodal gas exchange in the bowfin, Amia calva L. (Actinopterygii: Amiiformes). Respiration Physiology 43, 339-348.
61. Sanchez, A. P., Giusti, H., Bassi, M. & Glass, M. L. (2005). Acid-base regulation in the South American lungfish Lepidosiren paradoxa: effects of prolonged hypercarbia on blood gases and pulmonary ventilation. Physiological and Biochemical Zoology 78, 908-915.
62. Sardella, B. A. & Brauner, C. J. (2007). The osmo-respiratory compromise in fish: the effects of physiological state and the environment. In Fish Respiration and Environment (Fernandes, M. N., Rantin, F. T., Glass, M. L. & Kapoor, B. G., eds), pp. 147-165. Enfield, NH: Science Publishers.
63. Smatresk, N. J. & Cameron, J. N. (1982). Respiration and acid-base physiology of the spotted gar, a bimodal breather. II. Responses to temperature change and hypercapnia. Journal of Experimental Biology 96, 281-293.
64. Stewart, P. A. (1983). Modern quantitative acid-base chemistry. Canadian Journal of Physiology and Pharmacology 61, 1444-1461.
65. Toews, D. P., Holeton, G. F. & Heisler, N. (1983). Regulation of the acid-base status during environmental hypercapnia in the marine teleost fish Conger conger. Journal of Experimental Biology 107, 9-20.
66. Truchot, J.-P. (1987). Comparative Aspects of Extracellular Acid-Base Balance. Berlin: Springer.
67. Ultsch, G. R. (1987). The potential role of hypercarbia in the transition from water-breathing to air-breathing in vertebrates. Evolution 41, 442-445.
68. Ultsch, G. R. (1996). Gas exchange, hypercarbia and acid-base balance, paleoecology, and the evolutionary transition from water-breathing to air-breathing among vertebrates. Palaeogeography Palaeoclimatology Palaeoecology 123, 1-27.
69. Ultsch, G. R. (2012). Metabolism, gas exchange, and acid-base balance of giant salamanders. Biological Reviews 87, 583-601.
70. Urbina, M. & Glover, C. (2012). Should I stay or should I go?: physiological, metabolic and biochemical consequences of voluntary emersion upon aquatic hypoxia in the scaleless fish Galaxias maculatus. Journal of Comparative Physiology B 182, 1057-1067.
71. Vokac, Z., Ahmed, N. E. D. & Abdel Magid, A. M. (1972). The in vitro respiratory properties of blood of the primitive fish Polypterus senegalus. Journal of Experimental Biology 57, 461-469.
72. Wells, R. M. G., Baldwin, J., Seymour, R. S., Christian, K. A. & Farrell, A. P. (2007). Air breathing minimizes post-exercise lactate load in the tropical Pacific tarpon, Megalops cyprinoides Broussonet 1782 but oxygen debt is repaid by aquatic breathing. Journal of Fish Biology 71, 1649-1661.
73. Wilkie, M. P., Morgan, T. P., Galvez, F., Smith, R. W., Kajimura, M., Ip, Y. K. & Wood, C. M. (2007). The African lungfish (Protopterus dolloi): ionoregulation and osmoregulation in a fish out of water. Physiological and Biochemical Zoology 80, 99-112.
74. Wood, C. M. & LeMoigne, J. (1991). Intracellular acid-base responses to environmental hyperoxia and normoxic recovery in rainbow trout. Respiration Physiology 86, 91-113.
75. Wood, S. C., Johansen, K. & Weber, R. E. (1972). Haemoglobin of the coelacanth. Nature 239, 283-285.
76. Wood, S. C., Weber, R. E. & Davis, B. J. (1979). Effects of air-breathing on acid-base balance in the catfish, Hypostomus sp. Comparative Biochemistry and Physiology A 62, 185-187.
77. Wood, C. M., Turner, J. D. & Graham, M. S. (1983). Why do fish die after severe exercise? Journal of Fish Biology 22, 189-201.
78. Wood, C. M., Turner, J. D., Munger, R. S. & Graham, M. S. (1990). Control of ventilation in the hypercapnic skate Raja ocellata: II. Cerebrospinal fluid and intracellular pH in the brain and other tissues. Respiration Physiology 80, 279-298.
79. Wyman, J. (1964). Linked functions and reciprocal effects in hemoglobin: a second look. Advances in Protein Chemistry 19, 223-286.