The nostrils (blowholes) of whales open externally and are usually at the highest point on the head. Toothed whales have one blowhole and have asymmetrical skulls, because one of the nasal passages has become reduced. The two nasal passages are separate at the base of the skull, but join close just below the surface to form one opening. In extreme cases, one passage is devoted to sound production, leaving the other as the sole breathing tube. The blowhole typically takes the form of a crescent-shaped slit protected by a fatty and fibrous pad or plug. Efficient adaptation means that the slit is closed by water pressure, but can be opened by muscular action when the whale surfaces to breathe.

Baleen whales have a double blowhole, as the paired nostrils remain separate. The blowhole is a double hole forming two parallel slits that are close together when shut.

There is a direct connection between the blowhole and the lungs, so that a suckling calf cannot get milk into its lungs.

Whales must surface to breathe air, as they do not take up oxygen from the water. When they dive, they must hold their breath. Before a whale dives, it expels air from its lungs. Special valves close the blowhole when the whale submerges.

When a whale dives, it takes just enough air to fill its relatively small lungs. Only a proportion of the air is nitrogen, so that only a small amount can dissolve in the body fluids and tissues from one filling of the lungs. This amount does not enter the blood and tissues, because the whale's lungs compress as it dives, driving the air into the windpipe and its branches and into the extensive nasal passages. The thickened membrane linings of the nasal passages prevent gas exchange to the tissues. The comparatively flexible chest and the very obliquely set diaphragm aid breathing, because the pressure of the abdominal viscera (organs) pushing against the whale on one side makes the lungs of the other side collapse.

Oxygen combines with the haemoglobin of the blood and with the myoglobin of the muscles to provide 80-90% of the oxygen supply used during prolonged diving. Arterial networks act as shunts to maintain the normal blood supply to the brain, but effect a reduced supply to the muscles and an oxygen debt, which is repaid when the whale surfaces. The heartbeat is lower to economize the oxygen supply. The respiratory centre in the brain is relatively insensitive to carbon dioxide accumulating in the blood and tissues.

Whales encounter hydrostatic pressures at great depths, but these are alleviated, as whales do not breathe air under pressure and noncompressible fluids permeate the body tissues. Free gases are the only substances in the body that can be appreciably compressed by the pressure of great depths. When these gases collapse, they are driven into the more rigid, thick-walled parts of the respiratory system.

As the whale ascends, its lungs gradually expand again. The blowhole opens wide and the foul-smelling air, which accumulates during the dive, is expelled explosively. This produces a cloud of spray (the spout) as water from around the blowhole is forced into the air. The visible spout is from the condensation of water vapour entering the air from the lungs, and possibly from the discharge of the mucous oil foam filling the air sinuses. Whales do not blow liquid water out of the lungs.

After the whale exhales, it takes in fresh air. The air sacs return to their expanded condition for maximum gas exchange and the whale is ready to dive again.

I'm sorry if this is complicated, but I hope that you appreciate the important physiological adaptations which enable whales to dive deeply and for periods of many minutes.

Breath-by-breath measurements of end-tidal O2 and CO2 concentrations in harbor porpoise reveal that the respiratory gas exchange ratio (RR; CO2 output/O2 uptake) of the first lung ventilation in a breathing bout after a prolonged breath-hold is always well below the animal's metabolic respiratory quotient (RQ) of 0.85. Thus the longest apneic pauses are always followed by an initial breath having a very low RR(0.6-0.7), which thereafter increases with each subsequent breath to values in excess of 1.2. Although the O2 stores of the body are fully readjusted after the first three to four breaths following a prolonged apneic pause, a further three to four ventilations are always needed, not to load more O2 but to eliminate built-up levels of CO2. The slower readjustment of CO2 stores relates to their greater magnitude and to the fact that they must be mobilized from comparatively large and chemically complex HCO /CO2 stores that are built up in the blood and tissues during the breath-hold. These data, and similar measurements on gray seals (12), indicate that it is the readjustment of metabolic RQ and not O2 stores per se that governs the amount of time an animal must spend ventilating at the surface after a dive.

cetaceans are exclusively aquatic mammals that range in size from the smallest porpoises (70-100 kg) to the largest animal on the planet, the 150-ton blue whale. They spend the vast majority of their life underwater and surface only periodically to ventilate their lungs with a single breath. The largest whales, with their unusually large blood volumes and high Hb and myoglobin concentrations, can take aboard enough oxygen at the surface to sustain their low mass-specific metabolic rates for dives lasting >1 h (6, 7, 14). Because harbor porpoises represent the lower extreme of cetacean body size, they are of intrinsic interest to respiratory physiologists because they are presumed to have the highest mass-specific metabolic rates and to enjoy the most active lifestyle of all whales.

We had a unique opportunity to study the respiratory physiology of captive harbor porpoises in a strandings rehabilitation facility for marine mammals in Harderwijk, Netherlands. Our experiments on juvenile harbor porpoises confirm that they have the highest oxygen consumption per kilogram body weight and the highest heart rates of all cetaceans studied thus far (13). Whereas their diving O2stores in blood, lung, and muscle are slightly greater than one would predict for a terrestrial mammal of comparable size, their high mass-specific metabolic rate dictates a lifestyle that restricts aerobic underwater activities to 3-4 min [their so-called aerobic dive limit (ADL)] (10, 13) before having to surface to breath. This offers them little scope to achieve great diving depths and almost certainly limits their foraging activities to shallower environments than the larger whales. Indeed, recent field studies of free-ranging juvenile harbor porpoises instrumented with time-depth recorders bear out our measurements of a 3- to 4-min ADL (13) as maximum depths and dive durations were on the order of 150 m and 3.5-4.7 min (8, 15). After such dives, harbor porpoises normally visit the surface for up to 6 "rolls" spaced ∼10 s apart (15). Each roll coincides with a lung ventilation, or blow, lasting <1 s (13) during which time all gas exchange must occur. Our survey of cetacean ventilatory dynamics (13) indicates that rapid, high-flow velocity breathing is a characteristic feature of all whales, enabling them to exchange large percentages of their total lung gas during the brief periods when they "porpoise" through the air-water interface.

Current concepts of diving in marine mammals focus on oxygen as a "resource" that must be periodically recharged at the expense of loss of time underwater. As such, the time taken to "gather" the resource at the surface is viewed as an inescapable "cost" of the diving habit. We present data showing that the O2 store of the porpoise is fully readjusted after the first three to four breaths after a prolonged apneic pause. However, a further two to three ventilations are needed, not to load more O2 but to eliminate built-up levels of CO2. Although the slower readjustment of CO2 stores is a predictable feature of unsteady-state gas exchange, its potential importance as the proximate signal that brings the surface period to an end has been largely ignored.

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MATERIALS AND METHODS

Two juvenile harbor porpoises (28.3 and 27.8 kg) were trained in a small tank to breathe freely into a facemask that was positioned over the blowhole each time the animal surfaced to ventilate its lungs. Over a 3-wk training period, the animals were lifted each day from the holding tank (an oval pool 8 × 6-m diameter, 1.5-m deep) to the experimental tank (2 × 0.8 × 0.8-m). During each experimental session, the animal was allowed to breathe freely through a Hall's facemask (VetDrug, Bury St. Edmunds, UK), and breath-by-breath O2 ([O2]) and CO2 concentrations ([CO2]) were recorded. The facemask was a wide rubber funnel with flexible rims (so that it fit easily over the blowhole without allowing any air to escape), and both the mask and the flow meter had minimal resistance to the porpoise's respiratory flows, being essentially open tubes. The inspiratory and expiratory flows were measured using an ultrasonic low-resistance flow meter (BRDL, Birmingham Univ.; 20-l/s version; see Ref. 12) mounted on the top of the mask so that the porpoise could breathe freely through the flow meter. Respiratory gases were measured by drawing a continuous subsample of the animal's expiratory and inspiratory flows at a constant flow rate (600 ml/min) through capillary tubing from the center of the respiratory gas flow, passing through a Ministart drying filter (deadspace 0.1 ml, Sartorius) to Servomex gas analyzers (model 1505 miniature infrared CO2 and 728 zirconia O2; Servomex). O2 and CO2 measures were output as percent end-tidal (minimum) O2 and percent end-tidal (maximum) CO2 and converted to partial pressures (assuming partial pressure of water in air at 37°C is 6.26 kPa). The response time of the oxygen analyzer (installed in the system) was ∼500-600 ms, whereas that for CO2 was ∼300-400 ms. The maximum possible sample gas flow rates were used to minimize the delay of the system, and the gas analyzers were positioned on a wheeled platform next to the experimental container to minimize the delay between sampling and analysis. The O2and CO2 gas sensors were calibrated using precision gas mixtures (pure N2; 12% O2 and 4% CO2 in N2; 10% CO2 in N2; supplied and certified to 0.01% by Hoekloos Gases, Amsterdam, Netherlands). Data were sampled and stored by a 386 Dell PC with "ANALYSE" software specifically developed for this work. For further details of the respirometry system, instrument response times, calibration, and system operation, see Reed et al. (12).

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RESULTS AND DISCUSSION

Breathing episodes after the longest breath-holds in the present study were normally grouped into distinct bouts of six to eight lung ventilations, with short interbreath intervals (Fig.1). Breath-by-breath measurements of end-tidal [O2] and [CO2] in porpoise revealed that the respiratory gas exchange ratio (RR; the ratio of CO2 output and O2 uptake) of the first lung ventilation in a breathing bout after a prolonged breath-hold was always well below the animal's time-averaged metabolic respiratory quotient (RM) of 0.85 (13). Thus the longest apneic pauses were always followed by an initial breath having a very low RR (0.6-0.7), which thereafter increased with each subsequent breath to values in excess of 1.2 (Fig.2). It is evident from these data that over the course of the breathing bout, the CO2 stores readjust relatively slowly compared with oxygen.

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Fig. 1.

Respiratory gas exchange during a period of intermittent ventilation by an individual harbor porpoise. The longest apneic pauses (top) were always followed by an initial breath having a very low respiratory gas exchange ratio (RR; 0.6-0.7;middle), which thereafter increased with each subsequent breath to values in excess of 1.2. Note that the changes in RR track those of end-tidal Po 2(bottom). Breath-by-breath measurements of end-tidal Po 2 and Pco 2 were used to compute RR.

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Fig. 2.

Relationship between the RR (ratio of CO2 output and O2 uptake) and preceding breath-hold duration during breathing bouts after prolonged apneic pauses (i.e., 22- to 44-s duration). Individual breath-holds from 2 harbor porpoises are denoted by different symbols. The 7 different symbols at far right (i.e., >20-s duration) show the RRvalues measured during the first lung ventilation after 7 individual breath-holds lasting 22-46 s. The shorter breath-holds (i.e., <20-s duration) show RR values for the subsequent 4-6 lung ventilations of the breathing bout that followed each of the 7 prolonged apneic pauses.

The effects of differential rates of store adjustment on the RR can be conveniently illustrated on the O2-CO2 diagram (5). The gas exchange ratio of the stores is indicated by a fan of lines radiating from the inspired gas composition (Fig.3). Although diving physiologists have normally assumed the postdive ventilation of marine mammals to be concerned primarily with the recharging of O2 stores, our data for harbor porpoises show that when the O2 stores have attained near-equilibrium values (Hb-O2 saturation, >95%), the CO2 stores are still readjusting (Figs. 1 and3). Indeed, this is to be expected if one considers that the majority of the CO2 eliminated during breathing must be mobilized from large and chemically complex HCO /CO2 stores contained primarily within tissues and blood. By comparison, O2 store adjustments proceed more quickly, because they are largely confined to exchanges between the blood and lungs. Although comparatively high myoglobin concentrations can be found in the muscle of diving marine mammals (6), the CO2 capacitance (β-CO2 = Δ[CO2]/ΔPco 2) for body tissues is much higher than the corresponding O2capacitance (β-O2 = Δ[O2]/ΔPo 2), because β-CO2 is determined by both the physical solubility (α-CO2), which is ∼25 times higher than for O2, and the chemical binding of CO2 as bicarbonate; i.e., β-CO2 = α-CO2+ (Δ[HCO ]/ΔPco 2), where changes in bicarbonate concentration are stoichiometric with the amount of proton buffering (9). Thus, whereas the major tissue O2 stores are confined to muscle, any tissues with chemical groups that act as H+ acceptors can act as potential CO2 stores. The high capacitance for CO2 compared with O2 means that for a given change in the stores (e.g., if RM = 1), the corresponding change in Pco 2 will be much smaller than that for Po 2. This is why increases of arterial blood Pco 2 of only 10 mmHg are seen during 20-min voluntary dives of Weddell seals, when corresponding oscillations in arterial Po 2 reach upwards of 60 mmHg (11), and why lung RR < RM in the initial stages of the postapneic breathing bout (Figs. 1, 2, and 4).

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Fig. 3.

Moment-to-moment changes in alveolar partial pressures of O2 (PAo2) and CO2 (PAco2) during several breathing bouts after prolonged apneic pauses of 22-44 s in 2 harbor porpoises. RR is shown by the fan of lines that radiates from the point of interception of the Po 2 and Pco 2 of inspired gases (see Ref. 5).

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Fig. 4.

RR of 2 gray seals (A: 160-kg female;B: 185-kg male) during postdive breathing bouts. Each breath is expressed as a fractional proportion of the total time spent at the surface after a dive. Data for 5 postdive breathing bouts in each seal were computed from end-tidal Po 2 and Pco 2 measures found in Ref. 12.

For comparative purposes, mean lung R values during postapneic breathing bouts were computed from breath-by-breath measurements of end-tidal Po 2 and Pco 2in the porpoise (see Fig. 1) and the gray seal (12). When seals surface to breathe after a dive, they normally remain at the surface with their nares exposed to air for a series of lung ventilations. Our analysis shows that the RR values in the early stages of a postdive breathing bout are much lower than in the later stages of the bout, when RR values increase in both animals to levels far in excess of the metabolic RQ (Figs. 1 and 4). The only significant difference between the postapneic development of an increasing RR in harbor porpoises and gray seals is that the gas composition of the first few breaths after a dive in the seal is thought to reflect that of a largely underperfused lung during the breath-hold (12). As the circulation to the periphery of the seal is reestablished, the peak end-tidal Pco 2 values increase far less than the corresponding fall in Po 2, leading to an overall decrease in RR and to the curvilinear relationship for RR shown in Fig. 4. The fact that we do not see such curvilinear relationships in the harbor porpoise (Fig. 1) is further support of our contention that the lung is probably used as an O2 store throughout the breath-hold and that peripheral vasoconstriction is only slow to develop (13).

One may well ask whether the time a marine mammal spends at the surface after a dive always exceeds the time taken to recharge the O2 stores. For example, in Weddell seals diving voluntarily for up to 57 min, the mean time on surfacing to reach an expired Po 2 of 60 mmHg (90% Hb-O2saturation) was 0.56 min, whereas mean surface time was upwards of 3 min (10). In the case of the harbor porpoise, which surfaces for only one breath at a time, this means that after long dives, they may be constrained to a period of porpoising behavior near the surface if they are to readjust fully their body O2 and CO2 stores. Given that it takes more time to liberate CO2 than to uptake O2, one questions whether such animals would ever forego full readjustment of their CO2 stores. By rapidly charging themselves with O2, they could cut the surface period short, still dive aerobically, "put up with" the added CO2/pH burden, and then eventually offload the built-up CO2 at some later date by spending even longer times at the surface. There could well be times when loading O2 quickly might be advantageous if, for example, being at the surface posed a threat or getting underwater quickly (e.g., for feeding) temporarily outweighed the benefits of full readjustment of body gas stores.

The overriding emphasis in current models of marine mammal diving focuses on the effectiveness of O2 store management during the dive and on the time taken to recharge the O2 store at the surface. On the other hand, factors effecting the rate-dependent steps in CO2 storage, transport, and removal have been largely ignored. Taken together, the data we present suggest that we may need to refocus our interpretation of postdive breathing behavior in marine mammals to acknowledge the possibility that it is the readjustment of the body CO2 store, not the O2store per se, that governs the amount of time an animal must spend ventilating at the surface.

Perspectives

The extended breath-hold capacities of diving marine mammals raise the question of whether these animals possess any special mechanisms to accelerate CO2 removal to facilitate greater matching between O2 and CO2 exchange rates. Some years ago, Boutilier et al. (1) showed that the nonbicarbonate buffering capacity (β-NB) of the separated plasma of the killer whale and gray seal was two- to fourfold higher than in terrestrial mammals. This suggested that the increased β-NB of separated plasma could facilitate enhanced CO2 removal directly from the plasma (i.e., thereby avoiding rate-limiting red blood cell anion exchange) as long as there were sufficient amounts of the enzyme carbonic anhydrase in contact with the extracellular compartment. Although the presence of carbonic anhydrase in the pulmonary vasculature of the rat is known to enhance CO2 excretion (3, 4), it is not considered nearly as important as the erythrocytic enzyme, owing to the relatively low β-NB of separated plasma. All else being the same, the greater β-NB of separated plasma in the diving forms (1) would not only enable greater carriage of blood total CO2 from the site of production to the lung but, when there, could also facilitate enhanced extracellular formation of CO2 by providing the protons needed to drive extracellular bicarbonate dehydration. Other buffering characteristics, such as the comparatively high buffering power seen in the muscle of marine mammals (2), indicate to us that prolonged voluntary dives (with large acid-base disturbances and large amounts of tissue CO2 storage) will be important to focus on in future studies of unsteady-state gas exchange in these animals.

Killer whales are among the fastest swimming marine mammals.

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Killer whales can swim at speeds of up to 45 kph (28 mph), but probably only for a few seconds at a time.

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Killer whales usually cruise at much slower speeds, less than 13 kph (8 mph). They can cruise slowly for long periods of time.

Killer whales are agile and maneuverable in the water

When swimming near the surface, a killer whale usually stays below water for 30 seconds or less.

Swimming energetics.

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Blubber smooths the contour of a killer whale and contributes to its characteristic fusiform shape, which is quite energy efficient for swimming. Compared to other body shapes, this body shape creates less drag (the opposing force an object generates as it travels through water).

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Killer whales and many other toothed whales sometimes "porpoise" at the surface: they swim fast enough to break free of the water, soaring briefly up and out and then back under in one continuous movement, which they generally repeat. Porpoising uses less energy than swimming fast at the surface.

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Wave-riding also saves energy. Killer whales and many other toothed whales sometimes ride ocean swells or a boat's bow wave or stern wake. Riding a wave or a wake, a killer whale can go almost twice as fast using the same energy cost.

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A killer whale calf swims close to its mother and can be carried in the mother's "slip stream," a type of hydrodynamic wake that develops as the mother swims. This helps the calf swim with less energy and enables the mother and calf to keep up with the pod.

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DIVING

Although not generally deep divers, foraging killer whales can dive to at least 100 m (328 ft.) or more.

The deepest dive known for a killer whale was performed under experimental conditions and was 274.3 m (900 ft.).

In the eastern North Pacific, resident killer whales usually make three or four 15-second dives and then a dive that lasts about 3-4 minutes, repeating this pattern.

Transient whales in the eastern North Pacific sometimes show a similar breathing pattern as the residents, but they often stay submerged for more than 5 minutes and occasionally for more than 15 minutes in a single dive.

All marine mammals have physiological responses for diving. These responses enable a killer whale to conserve oxygen while under water.

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Killer whales, like other mammals, have a slower heart rate while diving. A killer whale's heart rate can slow from 60 beats to 30 beats per minute while diving.

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When diving, blood is shunted away from tissues tolerant of low oxygen levels toward the heart, lungs, and brain, where oxygen is needed most.

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Certain protein molecules-hemoglobin and myoglobin-store oxygen in body tissues. Hemoglobin occurs in red blood cells. Myoglobin occurs in muscle tissue. The muscle of whales has a higher myoglobin concentration than the muscle of land mammals.

Unlike humans, marine mammals don't get "the bends" when they dive.

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As pressure increases with depth, the amount of gas that goes into solution in a diver's blood and body tissues also increases. At about 2 atmospheres of pressure (about 60 feet), tissues are saturated. If a human diver returns to the surface too quickly, the gases, especially nitrogen, come out of solution and form bubbles in the muscles and blood. This painful and sometimes fatal condition is called "the bends."

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The bends is most common in scuba divers, but human breath-hold divers can also get the bends from deep diving. Human breath-hold divers dive on fully inflated lungs. Under pressure, a human's bronchioles collapse. Lung air is forced into the alveoli: the numerous tiny areas of the lungs where gas exchange takes place. Here gases are absorbed under pressure.

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Unlike human scuba divers, a whale doesn't breathe air under pressure. It inhales only at the surface. Furthermore, in diving mammals, the alveoli collapse at about 3 atmospheres of pressure (about 90 feet), forcing air into the bronchioles (rigid air passages), a region where gases are not exchanged.

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RESPIRATION

A killer whale breathes through a single blowhole on top of its head.

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The blowhole is relaxed in a closed position. To open the blowhole, a killer whale contracts the muscular flap covering the blowhole.

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A whale holds its breath below water.

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A killer whale opens its blowhole and begins to exhale just before reaching the surface of the water.

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At the surface, the whale quickly inhales and closes the muscular flap.

A killer whale breathes air through its blowhole on top of its head.

The visible spout of water that rises from a killer whale's blowhole is not coming from the lungs, which (like ours) do not tolerate water.

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Water that is on top of the blowhole when the powerful exhale begins is forced up with the exhaled respiratory gases.

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Especially in cool air, a mist may form; it is water vapor condensing as the respiratory gases expand in the open air.

When a whale breathes, the visible blow that appears to be water is really water vapor condensing in the respiratory gases as they expand in the cooler ambient air.

In comparison to a human, a killer whale can hold its breath longer and exchange more lung air with each breath.

The resting respiratory rate of killer whales at SeaWorld is about three to seven breaths every five minutes.

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THERMOREGULATION

Like all mammals, killer whales are warm-blooded. A killer whale's core body temperature is about 36.4º to 38ºC (97.5º-100.4ºF)-close to that of a human. Living in the sea poses a particular challenge to marine mammals, because water conducts heat about 27 times faster than same-temperature air.

The large size of a killer whale helps minimize heat loss.

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In general, as an animal increases in size, its surface area decreases relative to volume. A whale's fusiform body shape and reduced limb size further decrease this surface-to-volume ratio.

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A low surface-to-volume ratio helps an animal retain body heat: the large body core produces metabolic heat. Only through the relatively smaller surface area exposed to the external environment (the skin) is that heat lost.

Just under a killer whale's skin lies a thick layer of blubber, composed of fat cells and fibrous connective tissue. This blubber layer, from 7.6 to 10 cm (3-4 in.) thick, insulates the whale and streamlines its body. Blubber helps insulate a whale from heat loss. There is a heat gradient from the body core, through the blubber, to the skin.

In general, killer whales have a higher metabolic rate than land mammals of similar size. This increased metabolism generates a great deal of body heat.

Mammals lose body heat when they exhale. Because they breathe less frequently than land mammals, killer whales conserve a considerable amount of heat.

A killer whale's circulatory system helps maintain body temperature; it adjusts to conserve or dissipate body heat.

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Some arteries of the flippers, flukes, and dorsal fin are surrounded by veins. Thus, some heat from the blood traveling through arteries is transferred to venous blood rather than the environment. This phenomenon is called countercurrent heat exchange.

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When a killer whale dives, circulation decreases at the skin, shunting blood to the insulated body core.

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During prolonged exercise or in warm water a whale may need to dissipate body heat. In this case, circulation increases near the surface of the flippers, flukes, and dorsal fin. Excess heat is shed to the external environment.

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In male killer whales, a countercurrent heat exchange system cools arterial blood that is flowing to the testes. Another countercurrent heat exchange system regulates the temperature of a developing fetus in gestating females.

A countercurrent heat exchange system exists in the flippers, flukes, and dorsal fin of a killer whale.

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SLEEP

Studies suggest that in bottlenose dolphins (closely related to killer whales) and beluga whales, sleep probably occurs in only one brain hemisphere at a time. This may help a whale monitor its environment, keep swimming, and control its respiration.

Observers note that killer whales typically rest, motionless, at various times throughout the day and night for short periods of time or for as long as eight hours straight. While resting, killer whales may swim slowly or make a series of 3 to 7 short dives of less than a minute before making a long dive for up to three minutes.

When sleep researchers studied two newborn killer whale calves and their mothers at SeaWorld San Diego, they discovered that the mothers and calves didn't appear to sleep or rest at all for the first month of a calf's life. Over the next several months, the whales gradually increased the amount of time they spent resting to normal adult levels. Four bottlenose dolphin calf-mother pairs showed the same sleep-behavior pattern. Staying active and responsive after birth may be an adaptation for avoiding predators and maintaining body temperature while the calf builds up a layer of blubber.

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