What diving animals might tell us about blood flow regulation.

Abstract

WHAT DIVING ANIMALS MIGHT TELL US ABOUT BLOOD FLOW REGULATION BRETT A. GOODEN* and ROBERT ELSNERt The ability of air-breathing aquatic mammals and birds to dive for long durations has intrigued physiologists for over 100 years. Much of this capacity results from enhanced oxygen storage and selective vasoconstriction in tissues other than the brain, with consequent conservation of oxygen. However, this view may be too simplistic, since recent studies have revealed a rapid and profound inhibition of the ability of arteries to constrict when subjected to ischemia or pure hypoxia [1, 2]. Nowhere in nature is the apparent conflict between local tissue metabolic needs and survival of the whole organism better demonstrated than in the protection of marine mammals from asphyxia during diving. Central nervous control of tissue blood flow during diving appears, on initial scrutiny, to be at odds with the autoregulatory control of blood flow at the tissue level. These matters raise fundamental and fascinating questions for physiological investigation. Seals and the Theory of Selective Ischemia While most dives in nature are brief and undemanding, the ability to perform occasional long diving maneuvers is an integral part of the seal's evolutionary endowment. The seal's capability for dealing with the progressive asphyxia of long dives in nature or with similar dives performed in the laboratory is our concern here. Breath-hold diving of the Antarctic marine mammal, the Weddell seal, represents one of the more remarkable examples of physiological adaptation to diving. This animal is capable of swimming under ice for periods of 1 hour or longer on a single breath of air [3, pp. 227-61; A]. The Weddell seal lives on fish and *Address: 7 Hay Road, Linden Park, South Australia 5065. Formerly of Queen's Medical Centre, University of Nottingham, United Kingdom. flnstitute of Marine Science, University of Alaska, Fairbanks, Alaska 99701.© 1985 by The University of Chicago. All rights reserved. 003 1-5982/85/2803-0435$0 1 .00 Perspectives in Biology and Medicine 28, 3 ¦ Spring 1985 \ 465 for much of the year must hunt its prey under the sea ice. The average swimming speed is about 8 kph, but this is probably interspersed with brief bursts of intense activity during hunting. During the last few decades we have learned much about the mechanisms that allow the seal to perform such extraordinary feats (for review, see [5]). Both anatomical and physiological adaptations are involved, but perhaps the most important of these are the cardiovascular adjustments that take place during diving. About 45 years ago the research of Laurence Irving and P. F. Scholander laid the foundations of our knowledge of these profound changes [6-8]. Results of studies by them and others on experimentally dived animals may be summarised as follows. Shortly after the beginning of such dives, cardiac output and heart rate are diminished, and blood flow is drastically reduced in most vascular beds of the seal, including the skeletal muscle, kidneys, and gut. The evidence indicates that blood flow is actually arrested in some regions. This change in flow reduces the overall metabolic rate of the animal and hence conserves the available oxygen for the vital and oxygen lacksensitive tissues—the heart and the brain. By the process of this selective ischemia the animal becomes effectively a "heart-brain" preparation. In general these responses have been shown to hold, with variations, for a wide variety of animals during laboratory and free dives. The more profound the cardiovascular changes, the greater is the resistance to diving asphyxia. Hence, man, who usually shows only a modest cardiovascular response during breath-hold diving, is a relatively poor diver . Species differences in blood- and muscle-oxygen stores and in anaerobic capacity also play important roles [5]. Diving by seals elicits graded responses varying in intensity with duration and the severity of imposed stresses. Brief dives (less than approximately 20 minutes in free-swimming Weddell seals [4] and 8 minutes in quiet, restrained harbor seals [9]) depend largely on oxygen-sustained metabolism, whereas anaerobic capabilities provide additional metabolic support for the more stressful and longer-duration dives. Trained command dives by seals in the laboratory, when the animal is relaxed, elicit a less intense...