The study of diving animals offers the scientist an ideal opportunity to study the physiological consequences and defence mechanisms required to survive extended breath-holding. It is also of great interest to diving physicians to see how diving animals avoid the perils induced by exposure to pressure and hypothermia.
The northern elephant seal and the sperm whale can dive to 1500 metres. The southern elephant seal can stay submerged for 2 hours, although usual dives are 20 to 30 minutes in duration. The Weddell seal regularly dives for food to greater than 100 metres and can remain submerged for up to 60 minutes. Typical humans, with some practice, can breath-hold underwater for 1 to 2 minutes and descend to 10 to 15 metres.
How are marine mammals able to achieve these remarkable underwater depth and/or duration exposures that appear to defy conventional wisdom with respect to limits of hypoxia? How also do they achieve these feats without developing some of the disorders (e.g. hypoxic blackouts, barotrauma, decompression sickness, nitrogen narcosis, O2 toxicity or high-pressure neurological syndrome) that are the subjects of subsequent chapters in this book?
Obvious anatomical adaptations include a streamlined shape, low-friction body surface (skin or fur) and the development of flippers or fins. Dolphins can reach speeds of 20 knots with remarkably low energy consumption. A dorsal blowhole in whales and dolphins also aids energy efficient respiration. Of more interest to the diving physician and physiologist are the mechanisms to cope with prolonged apnoea. The adaptations that allow diving animals to achieve long periods underwater are both physiological and biochemical.
All diving mammals have an increased total body O2 store. The relative contribution of the lungs, blood and muscles storage areas depends on the diving pattern of the animal.
Deep diving mammals do not dive at full lung capacity and may exhibit reduced lung perfusion during dives for reasons discussed later, so the bulk of O2 is stored in blood and muscle. Such animals have increased blood volume (~15 per cent of body mass versus ~5 to 7 per cent for humans), and the blood has a higher haemoglobin concentration. About 70 per cent of the total O2 store is found in the blood. They also have a markedly increased myoglobin concentration (5 to 12 times that found in a human), especially in the swim muscles, and this myoglobin increase is proportional to the diving capacity of the animal. Myoglobin carries approximately 25 per cent of the total O2 sore. Only a tiny proportion (~5 per cent) is found in the lungs (versus ~25 per cent in humans).
An intriguing and controversial mechanism for augmenting O2 storage and delivery during a dive is the pre-dive sequestration of oxygenated red cells in the spleen followed by the release of these cells by splenic contracture during a dive. The time course of release into the systemic circulation may be further regulated by a valve-like sphincter in the vena cava. The fact that this occurs is not disputed, but its role in marine mammal diving adaptation is uncertain. It has been noted that re-sequestration after release on one dive typically takes far longer than the typical surface interval between subsequent dives during a dive series. Thus, any benefit may be restricted to the initial dive. It is possible that this adaptation is more important for keeping blood haematocrit (and viscosity) at optimal levels when the animal is not diving than for improving oxygenation during dives.
Oxygen consumption and the diving response
The increases in blood volume, haemoglobin and myoglobin described earlier all contribute to the seal’s impressive O2 supply, but O2 still needs to be conserved. Indeed, it can be readily calculated that if the submerged seal continued to metabolize at the same rate as before diving, its O2 stores would not be sufficient during long dives. Not surprisingly, these animals exhibit multiple strategies aimed at conserving O2 and ensuring that it is supplied preferentially to vital organs during the period of a dive.
The term diving response refers to a sequence of physiological events, including apnoea, bradycardia and redistribution of cardiac output, which are under the control of multiple reflexes. O2 conservation is thus partly accomplished by selective redistribution of circulating blood. Blood may be preferentially distributed to swimming rather than non-swimming muscles. Studies indicate that pinniped skeletal muscles have an enhanced oxidative capacity to maintain aerobic metabolism under the relatively hypoxic conditions associated with diving and that these adaptations are more pronounced in swimming than in non-swimming muscles. Other tissues that are most critical for survival (e.g. retina, brain, spinal cord, adrenal glands and, in pregnant seals, the placenta) are also selectively perfused. The seal essentially shuts off the flow of blood to non-essential tissues and organs, such as the kidneys, until it resurfaces.
Rapid onset of bradycardia (to as low as 10 per cent of baseline rate) at the start of a dive may be seen in diving species. This reduces cardiac work and O2 consumption. A substantial reduction in cardiac output has been shown in Weddell seals. Because stroke volume falls by only about 30 per cent, the predominant effector of this reduction is the bradycardia.
Arterial blood pressure is reasonably well preserved despite this reduction in cardiac output, and this is important to maintain perfusion of vital organs. Maintenance of arterial pressure is facilitated by the stretching of the elastic walls of large arteries during systole and their recoil during diastole. This function is augmented in many species of marine mammals by a bulbous enlargement of the root of the aorta, the aortic bulb. The aortic bulb approximately doubles the diameter of the ascending aorta in harbour and Weddell seals, thus providing an elastic capacitance for maintaining pressure and flow into the constricted arterial tree during the long diastolic intervals characteristic of diving. The entire human aorta contains less volume than the aortic bulb alone in seals of a similar body weight. The increase in left ventricular afterload that would be expected as a consequence of elevated peripheral resistance and decreased large artery compliance is reduced by this unique anatomy. The net result is a diminished peak systolic pressure, which reduces cardiac work and O2 consumption while at the same time maintaining stroke volume.
The electrocardiogram of the diving animal shows some progressive changes during prolonged apnoeic dives. In addition to bradycardia, these changes may include the gradual diminution or even abolition of the P wave. Cardiac rhythm is then apparently set independently of the sino-atrial node by a ventricular pacemaker site. Other cardiac dysrhythmias occasionally appear.
With prolonged dives certain tissues switch to anaerobic metabolism, which produces lactic acid as a by-product. There is an increased tolerance to lactic acid in the muscles through increased buffering capacity. High levels of lactic acid, however, lower the pH of the blood and can lead to acidosis, causing a weakening of the heart’s ability to contract. Acidosis is avoided by confining anaerobic metabolism to the skeletal muscles and other tissues isolated from the blood supply. When the animals resurface, these tissues release the lactic acid into the blood for metabolism by the liver.
Modified diving behaviour to limit muscle activity and thus O2 consumption has been demonstrated in Weddell seals. Prolonged downward gliding, with minimal muscular effort, as a result of reducing buoyancy with lung compression at depth can result in up to a 60 per cent reduction in energy costs. Gliding is used during dives exceeding 18 metres in depth and occupies approximately 75 per cent of the descent.
Structural adaptations to accommodate thoracic compression during deep dives include a flexible rib cage, stiffened alveolar ducts and attachments of the diaphragm such as to permit some shifting of abdominal contents into the thorax. These changes