Marine mammals have had to develop methods to retain heat in cold seas (physiologically, biochemically, anatomically, or behaviorally), yet must be able to lose excess heat when they are on land or extremely active in the water. If the problem were one of simply evolving methods to stay warm in a cold ocean, it would be much easier to wrap themselves in deep blubber and fur or to stay very active and not have to deal with the consequences of heat loading. However, the difficulty of that solution is that the animal could get too warm, which would in turn would cause problems with metabolic regulation, reproductive chemistry, neural function, and so on. Thus, the thermoregulatory mechanisms that have evolved in marine mammals function not only to conserve heat, but to dump it when necessary. As poorly insulated humans, we must bring our artificial insulation with us and use exposure suits, wet suits, and a variety of man-made materials if we are to spend any significant time in the sea. For marine mammals, the insulation is already on board and probably serves multiple purposes beyond just thermoregulation.
I. The Physics of Heat and Temperature
The terms “heat” and “temperature” are often incorrectly exchanged for one another, yet they have very different physical aspects. “Heat” is the energy that reflects the molecular motion of atoms and molecules. As energy, heat can flow from an area where the energy is high (something that is “hot”) to an area where the energy is low (something that is “cold”). We quantify how hot something is by using a variety of temperature scales (Kelvin, Celsius, Fahrenheit), Thus, the temperature of an object is our definition of the level of heat energy contained by that object. The unit of energy is the calorie, and a single calorie is defined as the amount of heat necessary to raise 1 g of water by 1°C. In common usage in the United States, the calorie associated with food and dieting is actually the kilocalorie (kcal; 1000 calories). In strict scientific terms, a single calorie is defined as 4.184 J.
As with any energy that flows, there is usually some sort of resistance that impedes the flow of that energy. In the field of thermoregulation, that resistance is insulation (the inverse of insulation is thermal conductance). Thus, poor conductors are excellent insulators. Blubber, for example, makes an excellent insulator and conducts heat poorly. The unit of conductance is represented by the term “k” and has the units of calorie sec-1 cm-1 °C_I. These units define how many calories will flow through an insulator that is 1 cm thick per second for every degree Celsius difference between the hot and the cold side. Materials such as silver have an extremely high k value and thus conduct heat very well. Relatively, water is a better insulator than silver by 1000X. However, the point that is relevant to marine mammals is that air is a better insulator than water by 25 X. In other words, water conducts heat away from a warm body 25 X more effectively than air. This becomes an important point for the discussion of how fur works to help keep some marine mammals warm.
One final physics description is the definition of how heat flows from a warm to a cold object. Heat will flow when there is a temperature gradient between two sides of a conducting material depending on the magnitude of the temperature gradient, the thickness of the material, the inherent thermal conductance of the material, and the area that is exposed to the gradient. In biological terms, this means that heat would flow from the interior of a warm blooded mammal through the fat and skin to the cold outside air or water. Because water conducts heat 25 X times more effectively than air, this means that heat flows out of a warm object in the cold water much more efficiently than it does when that same object is in air. Thus, as humans, we can easily stand around outside in 70°F air, but would find being in 70°F water very cold after a while. This principle states that the thicker the insulator, the less heat flow, and the larger the temperature gradient, the greater the driving force. Therefore, to stay warm, an animal would want an effective insulator, a small surface area (reduced appendage size, rolling up into a ball, etc.), a low temperature gradient (seek a warmer area or allow the body temperature to fall, i.e., hibernators), and have a thick insulator. An excellent general discussion of the physics of heat and energy transfer can be found in Schmidt-Nielsen (1997) and in Kooyman (1981) for marine mammals.
II. What Is “Thermoregulation?”
Having discussed the physics of heat, the next step is to define the act of regulating temperature (thermoregulation) in the biological realm. In the broadest sense, animals can be classified as either endotherms or ectotherms, although some animals cross between those two stages. An endotherm is an animal that generates and controls its internal heat so that its body core temperature can be regulated at a level different than ambient. Birds and mammals are the most commonly cited examples of endotherms. However, an ectotherm is an animal that allows its body temperature to mimic and follow the ambient temperature. Most fish and invertebrates are ectotherms. All marine mammals are endotherms and regulate their normal body temperature at about 37°C. Animals that hold their body temperature constant are called homeotherms while those that vary body temperature are called heterotherms. Most mammals are therefore homeothermic endotherms, although there are fascinating new data that suggest marine mammals may let their body temperature vary quite widely.
What is the importance of 37°C to a mammal? Perhaps the most critical point is that the actual value of 37°C is not as important as the constancy of that value. There are no biochemical or physical requirements about 37°C that make it the perfect temperature for a mammal, and most isolated biochemical reactions still work above and below that temperature. However, the mammalian body has evolved to balance its myriad of biochemical reactions at 37°C. If an animal gets much warmer or colder, the system comes out of equilibrium and there can be significant failures in metabolic regulation. Thus, the study of hibernators is a fascinating example of adaptation to this problem. There is a concept in thermal chemistry called QI0, which is defined as the change in the rate of a reaction for every 10°C change in temperature. In most biological systems, Qio is about two. This means that if the temperature of an animal increased by 10°C, its metabolic rate would probably double. Because the millions of chemical reactions in the body all have slightly different QI0 values, it is easy to see how small changes in the core temperature could disrupt the biochemical balance. Some reaction rates would increase more than others and the flow of molecules from one biochemical pathway to another would be compromised.
The goal of thermoregulation then is to maintain a constancy of temperature by adjusting all the properties discussed earlier (the temperature gradient, the conductance, the surface area, etc.). Of course, for an endotherm, there is the additional factor that the animal is generating heat through metabolic processes. To maintain a constant body temperature for an endotherm, the produced heat must equal the heat lost to the environment. Put on too much of an insulator and the core temperature goes up if metabolic heat production stays constant. The perfect example is a human in Alaska wearing a thick, down jacket outside in the winter to stay warm but getting much too hot on cross-country skis wearing that same down jacket. The analogy to marine mammals is straightforward: a whale or a seal may put on large amounts of blubber but, as a consequence, overheat when extremely active. A human can simply take off the down jacket while exercising. A whale, however, does not have the option of taking off its blubber layer; it must be able to dump heat and therefore thermoregulate using other methods.
There are several ways in which heat is transferred to the environment from a warm body. Evaporation is the process of dumping enough heat into a liquid to turn it into a gas. This is the process of cooling down by sweating. Radiation is the movement of heat through the release of electromagnetic energy from the warm body to the cold environment without physical contact (heat energy from the sun traveling through space and warming the earth or a whale radiating in the infrared wavelengths; Cuyler et al., 1992). Conduction refers to the transfer of heat energy (calories) by physical contact between the warm body and the cold environment (putting your hand into cold water). Finally, convection is a specialized case of conduction where the heat that is transferred from the warm body is moved away from the area by a current of air or water. Thus, the environment provides an infinite sink for the heat (wind chill is the example in air or moving through very cold water as opposed to staying still in the water).
On the whole then, in order to maintain a constant body temperature, the heat that is generated in an endothermic mammal must be balanced by the heat lost or gained through radiation, evaporation, conduction, and convection. This is the fundamental equation of thermoregulatory biology.
There is a long and fascinating history to the study of thermoregulation in mammals. In the modem era, the study of arctic mammals and birds under cold conditions and the definition of the “thermoneutral zone (TNZ)” came about largely from the work of Laurence Irving and Per Scholander (1950). The thermoneutral zone is the range of temperature over which an endotherm does not need to regulate its metabolism in order to maintain its body temperature constant. At the lower critical temperature, for example, a mammal would need to increase its heat production in order to stay warm. A great deal of this theory depends on the quality of fur for terrestrial mammals, and detailed studies on the thermal properties of fur were also addressed about the same time by Harold “Ted” Hammel (1955).
III. Thermoregulation in Marine Mammals
So far, all of this discussion could be applied to any biological system, not just marine mammals. Is there anything unique about thermoregulation in this group of marine endotherms? Both King (1983) and Riedman (1990) provide some excellent summaries of the broad field of thermoregulation in this group of mammals.
A unifying characteristic of most marine mammals is that they spend a great portion of their lives, if not their entire lives, in a liquid environment that is significantly colder than their core temperature of 37°C. Based on the discussion earlier on the fundamental aspects of thermoregulation, it should be clear that this aquatic life represents a significant thermal challenge to these mammals. While radiation and evaporation are probably insignificant sources of heat loss, conduction and convection are massive. However, in the Antarctic, seals will move to the relatively warm polar water (at —1.8 C°) when the real or wind chill temperature outside falls below about —40 C°. Clearly, there is a balance where the extreme cold of the ice-covered water, even with its higher thermal conductance, represents less of a thermal challenge than being outside on the surface.
Marine mammals use either fur or blubber for insulation and, like all endotherms, balance their metabolic heat production with various pathways of heat loss. However, the use of blubber or fur has its own biological costs. While blubber is used for thermoregulation, it is also a primary source of metabolic fuel for a marine mammal and plays a role in buoyancy regulation. Blubber is a fairly unique tissue for marine mammals and is not found outside of that group except for a similar tissue in polar bears (Ursus maritimus) and some penguins. Fur, however, is found in both terrestrial and marine mammals. However, the highest quality (density) fur is found in the sea otter. Fur is a veiy good insulator as long as it is carefully maintained, groomed, and kept dry on the layer next to the skin. Fur seals and sea otters (Enhydra lutris) spend up to 12% of the daily energy use just maintaining their fur coats.
A. Heat Conservation and Generation
Marine mammals have no unusual heat-generating mechanisms or tissues that are not seen in any other mammal. For example, while some large warm-bodied fishes have specialized heat-generating tissues behind their eyes, no such organs or tissues exist in marine mammals. Some old data suggest that marine mammals may have an elevated metabolic rate for their mass, but this theory is not generally currently accepted (La-vigne and Kovacs, 1988) with the possible exception of the sea otter. The only heat-generating specialized tissue that has ever been found in marine mammals is brown fat in harp seal (Pagophilus groenlandicus) pups (Blix et al., 1979). This tissue is thermogenically active via oxidation of lipid compounds, but only for about the first 3 days after birth. This is an important source of heat for these young pups, but not unique, as brown fat is found in other terrestrial mammals where it serves the same purpose. As noted earlier, marine mammals also have a typical mammalian body core temperature. In fact, upon close examination of the data, there appears to be nothing special about marine mammals that would distinguish them from terrestrial mammals when it comes to heat-generating mechanisms or abilities. Like the hibernators though, they may be able to tolerate more significant alterations in body temperature gradients than most terrestrial mammals.
Given the particularly nondescript aspects of marine mammal heat generation, there must be something that is different about them since they can live in an extremely cold liquid environment that would be fatal to all terrestrial mammals. Again, given the fundamental balance equation of thermoregulation, this suggests that they must have adapted significant ways to alter the heat loss through reduced conduction and convection. They have done this through the use of blubber, fur, and vascular adaptations.
B. Blubber
Blubber is most often incorrectly assumed to be an inert fat layer beneath the skin. However, it actually is a complex, active tissue that consists of a loose, spongy material where the matrix of the sponge is made up of collagen fibers and the volume is made of adipocytes (fat, or lipid cells). As the blubber layer increases or decreases, the collagen matrix remains the same, and it is the movement of lipid in and out of that matrix that accounts for the change in blubber quality and characteristics. However, all blubber is not the same; it varies from species to species in terms of the ratio of collagen to lipid and it can even vary within the same animal from location to location or with depth. Blubber depth can range from just a millimeter or two in newborn pinniped pups to 50 cm in large whales. The key issue here is that blubber, by itself, is a good insulator, as it can be up to 93% lipid with very little water content and has roughly the thermal conductance of asbestos. Because lipid has a conductance of only about one-third that of water, it acts as a relatively good insulator. Blubber acts as an internal insulator for marine mammals because it occurs below the skin layer. Therefore, the skin layer itself will be only marginally warmer than the surrounding water. In polar waters, for example, the skin of a whale or a seal would be just a degree or two above freezing. The thermal gradient exists from the skin surface to the tissues and organs in the core.
In addition to varying between species and with location, blubber can also vary across time in the same animal. This can be seen in the significant seasonal variation in blubber thickness in a seal as it moves between the breeding season (where it is fattest) and the leaner periods associated with molting and mating. For example, northern elephant seals (Miroungaangiistirostris) can range between 50% to less than 20% body fat depending on the season. Clearly, this temporal change in blubber impacts not only thermoregulation, but also buoyancy and energy reserves during periods of fasting or lactation. Consequently, the role of blubber and its relative thickness as an indicator of nutritional condition has been followed quite closely in recent studies that seek to address the population health of marine mammals. If a population of marine mammals is nutritionally compromised, one would hypothesize that the blubber layer should be reduced due to consumption of the blubber as a fuel source.
Blubber should be thought of as a very dynamic tissue with multiple stressors and pressures on its biology. Because it is a critical tissue for several different processes in marine mammals, it cannot be modeled in a strictly thermal scenario. For example, during a time of fasting, the animal will be utilizing blubber heavily, which would be inconsistent if it were also being challenged with an increasing thermal demand. Hence, fasting periods associated with breeding occur in wanner months or in warmer water for most marine mammals. Rosen and Re-nouf (1997) have written about the relationships between blubber seasonal distribution and thermal problems in seals.
C. Fur
As with terrestrial mammals, fur in marine mammals functions by trapping dry air next to the skin and keeping water (or cold air for a land mammal) away from the skin surface. Thus, the gradient here is from the skin outward with a warm skin surface and cold outer layers of the fur. The most-cited example of the use of fur by a marine mammal is that of the sea otter and it provides an excellent example of how this animal lives in a cold environment (Williams et al., 1992). The sea otter is faced with a major thermal challenge, as it is a small mammal (large surface area to volume ratio through which to lose heat). It utilizes a dense fur with a series of guard hairs and under-furs to keep its skin warm. However, the cost of this luxurious fur coat is a tremendous amount of maintenance with up to 12% of daily energy expenditure being spent on grooming the coat. This is an absolutely essential cost, however, as without the fur, the animal would lose too much heat to the marine environment.
Many species of seals utilize blubber for thermal protection as adults, but will use a specialized fur, called lanugo, as newborns. Lanugo, or pup fur, is a very effective insulator in the air and is usually both long and very “fluffy.” On newborn pups, it functions as protection against the cold air during the time that they are on land or ice for nursing. Lanugo is useless in water and allows the skin to chill to essentially water temperature. A pup must shed its lanugo and develop a significant blubber layer before it can enter the water and be an effective swimmer and diver. Not all species of seal or sea lion pups are born with lanugo, but its purpose is well documented in many cases. Lavigne and Kovacs (1988) provide an excellent description of the first few days of life for harp seals as they adapt from the warm temperature inside the womb to the icy cold of being boni on the ice.
It is the reliance on a high-quality fur in the sea otter and fur seals that makes these mammals particularly vulnerable to oil spills. Oil permeates the fur and destroys the air pockets that provide the thermal insulation for the animal. After the Exxon Valdez oil spill (EVOS) in Alaska, there was a massive clean-up operation on the hundreds of sea otters that were brought to rescue and rehabilitation centers. The goal was to clean the fur to restore its thermal insulation properties. However, cleaning the fur of man-made oils also cleans the fur of the natural oils (primarily squalene) that help make the fur water resistant. Therefore, small amounts of lipid had to be added and groomed back into the fur of the otters after they were cleaned of the heavy oil. For a general summary of the impact of the EVOS event on marine mammals, see Loughlin (1997); for a detailed discussion on otters, see Williams and Davis (1995).
D. Vascular Adaptations
It is in the area of vascular adaptions for thermoregulation that marine mammals have evolved several unusual adaptations. The first of these is termed the rete mirabile, which is Latin for a “wonderful net.” This net, which is a countercur-rent heat exchanger (Scholander and Schevill, 1955), involves an intertwined network of veins and arteries such that the cold blood returning from the extremities in the veins runs next to the warm blood going out to extremities in the arteries. From the previous discussion on heat flow, it is easy to see how the heat flows from the arteries to the close-by veins thus tending to conserve the heat in the interior and cool the arterial blood going out to the colder regions of the body. Marine mammals have exquisite control of blood flow in their body not only for thermoregulation but also for diving. However, these two demands are themselves interrelated, and the control of one impacts the control of the other. For example, it would do no good for a diving seal to be closely controlling blood flow for oxygen conservation but then to override that control to dump or gain heat. In fact, Eisner and Gooden (1983) discussed some experiments with seals where the diving response inhibited thermoregulatory-driven circulatory adjustments. In another innovative study, divers were able to applv heat flow probes to the skin of dolphins while both divers and dolphins were underwater. The results show that the animals tend to defer heat regulation and favor oxygen conservation vascular adjustments when both must coincide (Noren et al., 1999).
These retes are found in several locations in marine mammals (and in some cold-adapted birds), with the most-cited examples being in the flukes of whales and the flippers of pinnipeds (Tarasoff and Fisher. 1970; Kvadsheim and Folkow, 1997). There has been the fascinating description of another rete, but in this case, the rete is used to cool down the reproductive organs of dolphins and seals by bringing in cold blood from the extremities (Rommel et al., 1995).
The next vascular adjustment seen in marine mammals deals with those mammals that utilize thick blubber as an insulating material. As mentioned several times earlier, this is a good technique for staying warm, but can cause serious problems if trying to cool. In fact, large whales have such a tremendous thermal mass and a low surface area to volume ratio that they may have a much more serious problem dumping heat than conserving it (Hokkanen, 1990). Because marine mammals do not sweat, the answer is that blubber is not just an inert organic blanket surrounding the animal, but is instead vascularized with a series of anastomoses, or blood flow shunts. These shunts can control the amount of blood moving through the blubber and reaching the skin, thereby controlling the amount of heat lost to the environment. If a seal needs to dump heat, the anastomoses open and warm blood can reach the surface of the skin. When Weddell seals (Leptonychotes weddellii) in the Antarctic dump excess heat, clouds of steam come off the animal as the blood reaches the surface of their skin. In some cases, the seals get so warm that they partially melt their way into the ice and leave perfect “seal shadows.” Conversely, when these shunts are closed, the same seals will be completely covered in snow with no signs of melting at any location except near the eyes and nose.
As mentioned earlier, the balance of blood flow throughout the body of marine mammals can be complex and is controlled by multiple demands: diving, exercise, and heat regulation. Diving requires limited blood circulation, simultaneous underwater exercise requires increased circulation, and thermoregulation can require both. How these animals balance those conflicting demands is an area where much more work needs to be done. This can be seen in even simple manipulations of seals and sea lions. When taking blood samples from the flippers of pinnipeds, the flippers must be warm or there is no blood flow out to the periphery. However, if anesthesia or sedation is required to work with the animal, those procedures may also cause a series of vascular adjustments and can dump great amounts of heat quickly. Then, extra heat needs to be added to the animal to keep the core temperature up and blood flow open to the flippers.
The balance between diving and thermoregulation has another interesting aspect if one looks at it from the point of view of diving physiology. One of the central demands for diving is that oxygen must be conserved in order to extend the dive. This can be done by a variety of means and one of those means is to reduce the demand for oxvgen by reducing the metabolic rate. In the discussion earlier, the concept of Qio was mentioned, which describes how a reaction rate changes with temperature. If a marine mammal were to reduce its body temperature while diving, the impact from the QI() relationship would therefore decrease the demand for oxygen, thus extending dive time. There is some evidence from freely diving pinnipeds suggesting that the animals can drop their core temperatures during diving and would thus gain some diving time by reducing the metabolic rate. The exact mechanisms by which this is done are not yet known, but temperature drops have been described in freely diving Weddell seals (Kooyman et al, 1980; Hill et al, 1987) and northern elephant seals (Andrews. 1999).
E. Behavioral Thermoregulation
Most of the mechanisms discussed earlier are biochemical, anatomical, or physiological mechanisms for regulating heat production or loss in a marine mammal. Of course, a marine mammal is not a static system and the animal can alter the demands placed upon it with behavioral modification. For example. sea otters are often seen floating with all four paws out of the water. The paws are highly vascularized, but not well insulated with fur. Thus, they would be a tremendous source of heat loss if in contact with the water. The otters keep their paws away from the water if they are trying to stay warm. Similarly, it is not unusual to see rafts of California sea lions (Zalo-phiis califomianus) floating at the surface with their large fore-flippers extended out of the water. On the beach, both seals and sea lions will move up or down the tidal zone area to either cool off or warm up. When too hot, sea lions will maximize their surface area by spreading out their flippers, while if too cold, they will lie on top of their flippers. As discussed earlier, Weddell seals will head to the water if the actual or convective temperature drops below about —40°C. However, elephant seals will flip cool sand onto their backs to help keep their body temperature down on sunny days, and Hawaiian monk seals (Monachus schauinslandi) will find shade under bushes or in small ravines out on hot, sandy atolls. All of these behavioral mechanisms are not unique to marine mammals, however, except that the animals have the ability to use the sea to cool down as necessary. A good example of both feeding and thermoregulation are the humpback whales (Megaptera novaean-gliae) that come into cool Alaskan waters during the summer for feeding, but head south to warm, Hawaiian waters for breeding. A review of these behavior patterns for pinnipeds is found in King (1983).
IV. Summary
What are the essential elements of thermoregulation in marine mammals? Like all endotherms. these mammals must obey the physics of heat balance when holding body temperature constant. The methods for producing heat (resting metabolism and exercise) must balance the windows for heat loss (primarily conduction and convection) (Whittow, 1987). Because marine mammals do not appear to have any special adaptations for producing excess heat, most of their ability to thermoregulate comes with their ability to control heat loss. Control of these heat loss mechanisms is via biochemical, anatomical, physiological. and behavioral means. However, as in all levels of adaptation to the environment, systems cannot be considered or modeled in isolation. The problem with balancing blood flow for thermoregulation while also controlling blood flow for diving is an excellent example of this problem.
It is easiest to observe the behavioral means that marine mammals use to stay warm or to cool down: the movement up or down a beach with the tide, the use of shade, flipping of sand, swimming to warmer or colder water, exposing flippers, etc. Behind all of these behavioral patterns are the physiological or anatomical mechanisms that make the behavioral patterns effective. Countercurrent heat exchangers, blood shunts under the blubber, and even the chemistry of the blubber and the microstructure of the fur are all part of the thermoregulatory system. Ultimately, however, we are still left with the paradox of heat balance in marine mammals: they live in a cold, thermally challenging environment that no terrestrial mammal could survive. However, the very means they have utilized to stay warm in cold seas have come at a cost: for many species, they have had to also evolve the means to get rid of excess heat.
The exquisite balance between all these competing demands and systems is what makes the study of thermoregulatory biology in these mammals such a rewarding experience.
