Oxygen is the final electron receptor in the metabolism of marine mammals as it is in all other mammals. Marine mammals obtain oxygen from the air they breathe at the surface. In contrast, most feeding, mating, and other activities essential to survival occur beneath the surface. Thus most marine mammals minimize the time they are at the surface and have evolved to load oxygen quickly and use it efficiently. For marine mammals, the breath-holding portion of the breathing cycle is significantly extended compared to the oxygen intake portion.
Because a distinguishing feature of marine mammals is their breath-holding ability, this characteristic has received much more attention than their breathing. However, a number of aspects of marine mammal breathing have necessarily been modified from terrestrial mammals in order to accommodate their submerged lifestyles. As with many modifications from terrestrial mammals, those related to breathing show the greatest difference in those species that dive the deepest and the longest.
Cetaceans, sea lions, and manatees usually take only one breath per surfacing. Manatees return to a normal, shallow dive after a single breath. The deeper-diving cetaceans take a series of breaths, each in a subsequent surfacing, before an other dive. Seals remain at the surface for a series of breaths after a dive.
I. Lung Oxygen Stores
Every inspiration that fills the lungs with air brings in four times as much nitrogen as oxygen. Because nitrogen is neither bound to a carrier in the blood nor metabolized in the tissues, the partial pressure of nitrogen in the blood will equilibrate with that in the lungs. If gas exchange is allowed to take place during a dive, the resulting higher partial pressure of nitrogen in the blood and tissues will result in the formation of nitrogen gas bubbles when the external pressure is reduced as the animal comes to the surface. Thus deep-diving marine mammals limit the exchange of gas from lungs to blood during dives.
Most phocids have been observed to exhale before diving. Weddell seal (Leptonychotes weddellii) pups, which are observed to dive after an inspiration, are an occasional exception. At this developmental stage they are shallow divers. California sea lions (Zalophus californianus) may dive after a partial inspiration, but then vent air during descent. Dolphins and porpoises making shallow dives routinely dive on inspiration. These breathing behaviors correlate well both with the proportion of total oxygen stores in the lung at the start of a dive and with lung size in proportion to the body size of various marine mammals. Phocids dive with 7% of total oxygen stores in the lung, fur seals with 13%, and delphinids with 22% (Fig. 1). The proportionate size of the lung in phocids and manatees is about the same as in terrestrial mammals such as the horse and human (Fig. 2), whereas the lung size is greater than expected in delphinids and smaller than expected in whales. An outlier in these considerations is the sea otter (Enhtjdra lutris) whose lung is close to three times the expected size for its body mass and accounts for 75% of oxygen stores. The sea otter is not a deep-diving marine mammal, and the relatively large lung in the sea otter may be primarily used for buoyancy when the animal is resting at the surface.
II. Tidal Volume
The tidal volume of marine mammals is a larger proportion of the total lung capacity (TLC) than it is of terrestrial mammals. In a typical terrestrial mammal the volume of air inhaled and exhaled in one breath is in the range of 10 to 15% of TLC. In marine mammals, tidal volume is typically greater than 75% of TLC. The maximum tidal volume or vital capacity (VC) in terrestrial mammals is no more than 75% of TLC, whereas in marine mammals the VC can exceed 90% of TLC. Several factors contribute to the large tidal volume in marine mammals. Marine mammal lungs contain more elastic tissue than those of terrestrial mammals. The ribs contain more cartilage and are thus more compliant than those of terrestrial mammals. The lung is also more compliant. Marine mammal lungs can collapse and re-inflate repeatedly, whereas in terrestrial mammals, lung collapse is a serious situation that requires intervention to reinflate. Although both terrestrial mammals and marine mammals inspire actively and expire passively, the features noted earlier allow a much greater elastic recoil of the lungs, chest cavity, and diaphragm, and thus a greater tidal volume in proportion to TLC.
The terminal portions of the airways in all marine mammals are supported and reinforced by cartilage or muscle. One purpose of this reinforcement is to provide a less collapsible region into which alveolar gases can be forced during a dive to prevent gas exchange with blood at high pressures. This prevents increased nitrogen tensions in the blood and tissues as noted previously. A second purpose of the reinforcement is to keep the terminal airways open even at high flow rates of gases in and out of the lung during a breath and to allow high expiratory flow rates even as the lung volume decreases. Figure 3 shows the flow volume profile comparison during exhalation between a harbor porpoise and a human. There are two striking differences. First, the flow rates are much higher in terms of VC/sec. Second, the flow rates remain very high; even down to a small fraction of the VC. These two factors together allow veiy rapid exhalation of the full VC. Inspiration takes somewhat longer.
Figure 1 Generalized total oxygen store of major taxa of marine mammals expressed in ml ()2 kg~2. Numbers in parentheses are the percentage of total oxygen store found in the lungs, blood, and muscle, respectively.
Figure 2 The maximum amount of air the lungs can hold, and the amount of air breathed in and out with each breath, calculated per 100 kg of body mass for a horse, a human, a seal, a manatee (Trichechus sp.), a harbor porpoise (Phocoena phocoena), a bottlenose dolphin, a bottlenose whale (Hyperoodon sp.), and a fin whale (Bal-aenoptera physalus).
The bottlenose dolphin (Tursiops truncatus) completes an exhalation and inhalation cycle in approximately a third of a second. With a tidal volume of 10 liters, flow rates through the air passages can be as high as 70 liters/sec. In gray whale (Es-chrichtius robustus) calves the duration of expiration and inhalation is closer to half a second, but the tidal volume can be as great of 62 liters, and the maximum flow rate as great as 202 liters/sec. Gas flows through the external nares at speeds up to 44 m/sec during inspiration and 200 m/sec during expiration.
Cetaceans usually initiate expiration prior to the blowholes breaking the surface. The explosive nature of the expiration creates the small droplets that make the blow visible and clears the upper respiratory passages and the area around the blowholes of any residual water. Most of the time the blowholes are above the surface is used for inspiration.
The large tidal volume allows for more oxygen loading and greater carbon dioxide unloading during a single breath at the surface. Even in a resting state, the carbon dioxide content of expired air in seals is twice as great as it is in humans. After extended breath holds, alveolar oxygen levels can be as low as 1.5%. The oxygen and carbon dioxide content of expired air after surfacing can provide indirect evidence of physiological adjustments to diving. In bottlenose dolphins, the oxygen content in the first breath after a dive to 200 m is greater than it is in the first breath after an equivalent amount of swimming at 20 m. The interpretation is that the collapse of lungs in the deeper dive prevented the exchange of oxygen with the blood during the dive. For the same reason, the content of carbon dioxide in the first breath is always less after a dive to depth than after a dive near the surface. In gray seals (Halichoerus grypus), the end tidal partial pressure of oxygen in the first exhalation after surfacing is similar to that in the last breath before submergence, again indicating that the lungs were collapsed at depth and there was no gas exchange.
Figure 3 Comparison of the flow-volume curves of a human (dashed line) and a harbor porpoise (solid line). Note that in the human, after the volume falls below about 80% of vital capacity, the flow rate declines steadily, but this is not the case in the porpoise.
III. Hyperventilation
Marine mammals often hyperventilate both before and after a dive. Hyperventilation before a dive leads to increased oxygen tensions and reduced carbon dioxide tensions. Hyperventilation arises through an increase in the frequency of breathing and the tidal volume. Although both can initially increase during hyperventilation, lung dynamics requires an eventual reciprocal relationship between tidal volume and frequency of breathing. In Weddell seals, hyperventilation of five to six times resting is accomplished by increasing the tidal volume 1.5 to 2 times and the respiratory frequency 3 times. If the respiratory frequency rises above 25 breaths/min, the tidal volume, as a proportion of the TLC, is close to that of terrestrial mammals. Harp seals with respiratory rates of 27 breaths/min and harbor seals (Phoca vitulina) with rates of 35 breaths/min have tidal volumes between 20 and 30% of TLC. Because marine mammals normally have such large tidal volumes, they have much less ability to increase total ventilation in response to exercise than terrestrial animals. A human can increase respiration by 4 times and can increase tidal volume by greater than 4 times for an overall increase in ventilation of more than 16 times resting compared to the 5 to 6 times resting maximum for a Weddell seal.
Marine mammals often exhibit an increase in heart rate on approach to the surface. It has been suggested that this anticipatory tachycardia coincides with the restored perfusion of peripheral tissues so the oxygen levels in the blood drop even lower as the carbon dioxide levels rise. These changes in blood gases increase the gradient between partial pressures in the blood and the lungs and lead to more rapid oxygen uptake and carbon dioxide exhausting during the first breaths at the surface. When gray seals show no anticipatory tachycardia, they do not achieve the maximum rate of oxygen uptake during the first few breaths.
The increased heart rate and breathing on surfacing lead to a rapid restoration of oxygen tensions. In fact, in Weddell seals the blood oxygen partial pressures in the postdive recovery period routinely end up exceeding the resting values. It appears that the purging of carbon dioxide is more critical for determining readiness to dive again than is the replenishing of oxygen. In Weddell seals the partial pressure of carbon dioxide falls to resting levels within a couple minutes after aerobic dives, but may take up to 10 min to reach resting levels after long dives, which rely on anaerobic metabolism. The fact that hyperventilation can continue for an hour after the partial pressures of oxygen and carbon dioxide return to resting levels indicates that prolonged hyperventilation is driven more by lactate-induced changes in the acid-base balance in the blood.
IV. Ventilation Control
Seals show a more fully developed mammalian reflexive response of increased ventilation to decreases in inspired oxygen concentration or increases in inspired carbon dioxide concentration at an earlier age than terrestrial mammals. However, adult seals show little ventilatory response to decreased oxygen concentration. Instead the adult seals respond by increasing the proportion of time they are at the surface relative to the total time between dives. Apparently the adult seals are able to substitute behavioral control of diving patterns for reflexive control of ventilation.
Breathing hyperoxic gas increases the dive time of Weddell seals, has no effect on the dive time of manatees, and shortens the dive time of hooded seals. A suggested explanation for the latter surprising finding is that the seal breathing a hyperoxic gas mixture dove before it had exchanged all the carbon dioxide and the increased carbon dioxide tensions resulted in the shortened dive time.
Both the nostrils of pinnipeds and the blowhole of cetaceans are normally closed when the controlling muscles are relaxed. The closure in pinnipeds is maintained by muscle tone and pressure of the moustacial pad. Contraction of the nasal and moustacial pad muscles results in a movement of the pad and opening of the nostrils. In cetaceans, muscles must contract to open the blowhole and to move the nasal plug so that it is not blocking the airway.
Pinnipeds on land often show a breathing pattern similar to that during diving with breathing periods (eupnea) being shorter than breath hold periods (apnea). The ratio between apnea and eupnea while on land is greatest in those species that normally dive for the longest periods. The periods of apnea also tend to be longer when the animals are asleep than when they are awake. Even the longest bouts of sleep apnea appear to be aerobic: plasma lactate and glucose remain stable even though oxygen tensions drop to very low levels, carbon dioxide tensions increase, and respiratory acidosis occurs. In elephant seal (Mirounga spp.) pups, awake apnea does not exceed about 5 min whereas sleep apnea can be as long as 14 min. The pups show a parallel increase in mean sleep apnea and mean dive duration during their first year of life.
Pups of several species have been observed to have a higher breathing rate than adults. Weddell seal pups take 16 breaths/min compared to the 8 breaths/min rate of adults. Pups of Australian (Neophoca cinerea) and New Zealand (Phocarc-tos hookeri) sea lions take 13 breaths/min whereas adults of these species typically breathe 3 to 5 times per minute.
On land and in the water different stages of sleep in pinnipeds are associated with different breathing patterns in different species. During rapid eye movement sleep, breathing is regular and at rates up to 16/min in gray seals, irregular in harp seal pups, and absent in elephant seal pups. Elephant seal pups sleeping in shallow water rise to the surface to breathe without showing brain wave patterns associated with wakefulness. In contrast, Caspian seals (Pusa caspica) sleeping below the surface awake prior to surfacing and breathing.
Some species of delphinids show unihemispheric brain waves associated with sleep. Thus there is one cerebral hemisphere that is always awake to control surfacing and breathing patterns. Northern fur seals (Callorhinus ursinus) sleeping in water also sometimes show unihemispheric sleep patterns with one cerebral hemisphere awake to control surfacing and breathing. In contrast to delphinids, no pinniped has shown exclusively unihemispheric sleep brain waves.
V. Oxygen Loading and Dive Time
Several authors have modeled the diving behavior of marine mammals based on oxygen loading curves at the surface compared with energy expenditure while below the surface. There have been various models based on what the animal may be attempting to maximize, be it time in a deep prey patch, gross energy intake during a dive, net energy intake, energetic efficiency, etc. All the models conclude that there should be some relationship between die duration of a dive and the time breathing at the surface, either predive or postdive. Although some species do show such relationships over certain dive time intervals, not all species show the expected patterns. The time Weddell seals spend at the surface is independent of preceding dive duration up to the aerobic dive limit. Beyond that time, the surface time increases exponentially with the preceding dive time. However, gray seals show a direct proportionality between dive time and surface time up to dive times of 7 min. Surface time is independent of dive time for dive times greater than 7 min. Surface time of sperm whales (Physeter mcicrocephalus) shows a slight trend to decrease with increasing dive time, but is basically independent of dive time. Elephant seals can maintain, over periods greater than 24 hr, a pattern of long, deep dives followed by surface intervals of 3 min or less. Some of these differences are attributable to species variation among groups with different diving strategies and oxygen loading needs. Additional explanations of the breakdown of models relating surface oxygen uptake to underwater duration and activity include lowered metabolic rates underwater, passive gliding descents, and animals not maximizing any of the foraging-related parameters. For example, ringed seals (Pusa hispida) appear to be constrained by a risk aversive strategy. Diving under shore fast ice, ringed seals gain access to air only at a few breathing holes. If a seal finds a breathing hole occupied by another seal or detects a polar bear above die hole, it will need oxygen reserves to locate an alternate breathing site.
VI. Water Conservation during Breathing
Because marine mammals obtain most of their water requirements from their prey and through metabolic production of water, conservation of water is an important adaptation in marine mammals. Renal adaptations for water conservation are discussed elsewhere, but water can also be lost through ventilation. Both pinnipeds and cetaceans exhale air that is not saturated with water vapor. In bottlenose dolphins the respiratory water loss is reduced by 70% over what it would be compared to a terrestrial mammal breathing dry air. Countercurrent heat exchange and induced turbulence in the nares and nasal sac system allow for the extraction of a majority of the water vapor in the air coming from the lungs. In seals, the bones in the anterior part of the nasal cavity (turbinates) create a very dense mesh through which the expired air must pass. Moist air flowing over this large surface area gives up much of this water before being exhaled.
VII. Breathing Patterns in Response to Disturbance
Changes in breathing patterns have been used extensively as indicators of disturbance of marine mammals in response to human activity. In many cases, a statistically significant change has been observed in the interbreath interval, total number of breaths during a surfacing, or proportion of time spent at the surface. Although these changes may be statistically significant, it is questionable whether they are biologically significant for an individual animal or indicative of any long-term consequences for the population.
