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© 2014. Published by The Company of Biologists Ltd | The Journal of Experimental Biology (2014) 217, 3191-3192 doi:10.1242/jeb.095513 CLASSICS Hughes and Shelton: the oxygen carried in the blood is usually 1984) and studies of gas exchange in far greater than that in an equivalent elasmobranchs and birds also owe much fathers of fish respiration volume of water. Hughes and Shelton to the analysis by Hughes and Shelton. concluded, therefore, that water flow As fish gas exchange systems became over the gills must be much higher than better understood and described, blood flow through the gills to deliver mammalian terms such as V (ventilation), the required rate of oxygen transfer for Q (blood flow) and the V/Q ratio were metabolism. Hughes and Shelton adopted to facilitate comparison between introduced the term ‘capacity rate ratio’ different gas exchange systems so that (ratio of flow × oxygen content of blood the terms ‘capacity rate ratio’, and and water) and analyzed the effects of ‘effectiveness of transfer’ have largely this on oxygen transfer. They also disappeared from discussions of gas introduced the term ‘effectiveness of exchange. transfer’, defined as the actual rate of Fish Respiration oxygen transfer in relation to the At the time of the review, knowledge David Randall discusses George Hughes maximum possible rate of transfer. There of the blood circulation in fish was and Graham Shelton’s classic paper ‘Respiratory mechanisms and their were insufficient data for a detailed limited. Fish had been placed in sealed nervous control in fish’, published in analysis, but what they pointed out was chambers and the extent to which Advances in Comparative Physiology and that effectiveness depended on the oxygen could be removed from the Biochemistry in 1962. capacity rate ratio of blood and water and water assessed. Goldfish could remove the conditions for transfer across the gills almost all of the oxygen from the water George Hughes and Graham Shelton were as well as the countercurrent flow of even if haemoglobin oxygenation was members of the Cambridge University blood and water. blocked by adding carbon monoxide to group of experimental biologists applying the water. From these experiments, physical and chemical principles to the The amount of oxygen removed from Hughes and Shelton concluded that fish understanding of biological function. water flowing over the gills (percent could maintain standard oxygen Hughes was Shelton’s PhD supervisor utilization) had been observed to be as consumption at low temperatures and Shelton was mine when they high as 70–80% in resting fish. without the use of haemoglobin. This published their review ‘Respiratory Experiments presented in the review observation presaged the discovery of mechanisms and their nervous control in showed that increased flows of water icefish, which lack haemoglobin and fish’ in 1962 (Hughes and Shelton, 1962). across the gills were associated with a have a very high cardiac output to Hughes was, in my opinion, the more decrease in the amount of oxygen maintain capacity rate ratio. There was classical biologist whereas Shelton was removed. Assuming that the cost of only limited discussion in the review of more mechanistic and analytical in his breathing might be as high as 20% of CO2 transfer and no discussion of the approach to biological problems. The total energy output in resting fish and third respiratory gas, ammonia, reflecting review is now more than 50 years old but might increase with increases in the paucity of data on transfer of these is still refreshing to read and was clearly ventilation, Hughes and Shelton gases at that time. The next 50 years a major step forward in our understanding concluded that with increasing gill would see a large increase of our of respiratory mechanisms in fish, ventilation and the associated decreasing understanding of CO2 and ammonia bringing together a disparate set of oxygen percent utilization, the cost of transfer in fish. It is now clear that gills observations into a summary of breathing could limit maximum play an important role in ion as well as respiration in fish that formed a swimming activity. However, their gas transfer, and that they are a very framework for future work in the area. assumption of the costs of breathing was complex structure, not simply a barrier Their description of the respiratory too high and active fish are able to between blood and water. apparatus, in terms of both the skeleton maintain oxygen percent utilization from and musculature and the pumping water. Also, they did not consider ram The extensive and elegant discussion of mechanism, remains the basis for a more ventilation, i.e. the ventilation of the gills the neural control of breathing, along detailed knowledge of an extensive range due to forward movement of the fish with with the modelling of oxygen exchange of fish today. Pressure changes in the its mouth open, and in addition, many across the gills, is probably the most buccal and opercular chambers were fish supplement oxygen uptake by important component of the review. recorded and analyzed, showing that fish exchange across their skin. Despite that, Recording from the central nervous maintain a unidirectional but oscillating the systems approach promulgated by system was difficult and, at that time, the flow of water countercurrent to gill blood Hughes and Shelton did facilitate the equipment was often made by the flow. development of concepts such as investigator. Signal to noise was a large symmorphosis (Weibel et al., 1998). problem. In the early 1960s, when I was Water contains only small amounts of Subsequent model analysis of gas a graduate student, Shelton and I were dissolved oxygen. The amount of exchange in bony fish (Piiper and Scheid, recording activity from a fish brain and Classics is an occasional column, featuring historic publications from the literature. Written by modern experts in the field, these articles discuss each classic paper’s impact on the field of biology and their own work. The Journal of Experimental Biology 3191 CLASSICS The Journal of Experimental Biology (2014) doi:10.1242/jeb.095513 as we lowered the electrode into the important to derive broader biological References brain we heard music from a radio principles and a more comprehensive Hughes, G. M. and Shelton, G. (1962). Respiratory mechanisms and their nervous control in fish. Adv. station in Germany. We recorded the view.’ The review by Hughes and Comp. Physiol. Biochem. 1, 275-364. event but made no special conclusions Shelton of respiratory mechanisms and Kinkead, R. (2009). Phylogenetic trends in respiratory rhythmogenesis: insights from ectothermic regarding the fish brain. I find that the their control in fish was much more vertebrates. Resp. Physiol. Neurobiol. 168, 39-48. Hughes and Shelton discussion of than a synthesis of work to date. It Milsom, W. K. and Perry, S. F. (eds) (2012). Special problems of defining a central respiratory generated a greater interest in the subject Issue: New Insights into Structure/Function Relationships in Fish Gills. Resp. Physiol. Neurobiol. centre is still valuable reading. They and was a springboard for many 184, 213-346. agreed with Kinkead (Kinkead, 2009) subsequent studies (see Milsom and Piiper, J. and Scheid, P. (1984). Model analysis of gas that ‘current data indicate that respiratory transfer in fish. In Fish Physiology, Vol. XA (ed. W. S. Perry, 2012). Hoar and D. J. Randall), pp. 229-262. New York: rhythmogenesis is a phylogenetically Academic Press. ancient function that was highly Weibel, E. R., Taylor, C. R. and Bolis L. (eds) (1998). David Randall Principles of Animal Design: The Optimization and conserved throughout evolution and that University of British Columbia Symmorphosis Debate. Cambridge, UK: Cambridge a comparative approach remains [email protected] University Press. The Journal of Experimental Biology 3192.
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