Osmoregulation (marine mammals)

In organism can be thought of as a large volume of fluid surrounded by a body wall. Mammals must maintain both the concentration and the volume of this internal fluid within a very narrow range and can only tolerate minor deviations. Even though most marine mammals live in an aquatic medium, the animals’ internal fluid composition differs from the ambient environment and therefore requires active processes to maintain it. Osmoregulation describes the way in which the internal water and electrolyte concentration of this internal environment is maintained. When animals feed they take in both water and electrolytes that must be excreted. While they gain water from metabolizing food, they lose water through evaporation when they breathe to obtain the oxygen necessaiy for metabolism. Maintenance of a constant internal environment requires that whatever comes into the animal must equal what goes out. The easiest way to understand osmoregulation is to account for the ways water and electrolytes enter and leave the organism (Fig. 1). For example, if a dolphin consumes a large volume of water and electrolytes, it must have the capability to excrete an equivalently large volume in the feces and urine, through breathing, and in milk during lactation. Conversely, if a seal on the beach does not have access to food or water, it must be able to survive on the water produced from metabolism and have mechanisms in place to reduce water loss. Following the relative rates of water and electrolyte input and output helps us understand the mechanisms that marine mammals use for osmoregulation.

Figure 1 Schematic of ways by which water and electrolytes enter and leave a marine mammal. Excretion of electrolyte and water as milk occurs only when females are lactating.

I. Water and Electrolyte Ingestion

Water and electrolytes enter the animal through the ingestion of food and water. Water that is consumed as water, i.e., water contained in the food or actively drunk, is called preformed water. Compared to terrestrial mammals, marine mammals consume a water-rich diet of fish and marine invertebrates, which are composed of between 70 and 80% water. Prey are also composed of electrolytes and nitrogen that require water for excretion by the kidney. Marine mammals face different osmoregulatory problems depending on the type of prey that they consume. For example, the ratio of water to electrolytes is quite different between vertebrate and invertebrate prey. The internal fluid of vertebrates is one-third the electrolyte concentration of seawater, whereas the internal fluid of invertebrates is essentially the same as seawater. Thus, a dolphin eating squid will get almost three times as much electrolytes than if it consumed fish. Furthermore, an animal such as a manatee with access to fresh water can drink fresh water to flush electrolytes, whereas an oceanic dolphin can only drink seawater. Water is also produced as a by-product of metabolism; this is called metabolic water production (MWP). Because the amount of metabolic water produced varies with the fuel oxidized, different diets produce varying amounts of metabolic water. For example, 1.07 g of water is generated for eveiy gram of fat oxidized, 0.56 g of water per gram of carbohydrate, and only 0.39 g of water per gram of protein.

II. Water and Electrolyte Output

Both water and electrolytes are excreted in the urine and feces, whereas only water is lost through evaporation. Water is lost via evaporation both across the skin (cutaneous water loss) and through the lungs (respiratory evaporative water loss). Because marine mammals lack sweat glands there is no loss of electrolytes (salts) across the skin. Unlike sea birds and marine reptiles, marine mammals lack specialized glands to excrete salts. All salt excretion is through the kidney, and marine mammals have developed a specialized kidney to handle the large volume of electrolytes and water they process.

III. Do Marine Mammals Drink Seawater?

In most cases, marine mammals can derive sufficient water from their diet so that they do not need to ingest seawater. Measurements of the water, electrolyte, and nitrogen intake, coupled with measurements of evaporative, urinary, and fecal water loss, suggest that a feeding seal can get all of the water it needs from its prey (through both preformed and metabolic water). This is due to the high water content of the prey coupled with the low evaporative water loss of an animal living in a marine environment.

Do animals drink seawater when they become osmotically stressed in environments where the evaporate water loss is high? To determine whether a marine mammal can gain fresh water by drinking seawater we need to know whether the animal can excrete urine that is more concentrated than seawater. The more concentrated the urine, the greater the amount of “fresh water” that can be derived from the ingestion of seawater. A simple calculation can show how much water is gained or lost relative to the concentrating ability of the kidney (Table I). For example, if a humpback whale, Megaptera novaean-gliae, consumed 1000 ml of seawater and its kidney had the ability to excrete urine with a chloride concentration of 820 mmol X liter”1, it could gain 350 ml of fresh water. Whereas humans, who cannot produce urine as concentrated as seawater, would lose 350 ml of fresh water for every liter of seawater they consumed. The maximum urine concentrating ability of marine mammals and a few terrestrial mammals is presented in Table II.

So, do marine mammals drink seawater? Many species of marine mammals have the capacity to drink seawater, but they do not always do so. Fur seals and sea lions have been observed drinking seawater while fasting on the rookery. However, visual observations are not quantitative and do not allow an assessment of the relative importance of seawater ingestion to water balance. Isotopically labeled water and/or electrolytes have been used to quantify seawater drinking in a variety of marine mammals (Table III). In these studies, the amount of water and/or electrolytes consumed in the food was added to that produced by metabolism and compared to the total amount of water and/or electrolytes that passed through the animal is measured by isotopic tracers. Using these methods, investigators found that sea otters, Enhydra lutris, and bottlenose dolphins, Tursiops trunccttus, that were feeding and Galapagos fur seals, Arctocephalus galapagoensis, short-beaked common dolphins, Delphinus delphis, and short-finned pilot whales, Globi-cephala melas, that were fasting all consumed substantial amounts of seawater. In contrast, feeding and fasting harbor seals, Phoca vitulina, feeding northern fur seals, Callorhinus ursinus, and fasting Antarctic fur seals, A. gazella all had negligible amounts of seawater ingestion. Fasting northern elephant seal pups, Mirounga angustirostris. fast for up to 3 months without any measurable ingestion of seawater. The need to drink seawater varies with climate and habitat. For example, Galapagos fur seal females drank during the perinatal fast, whereas female Antarctic fur seals did not. The need to drink seawater in the Galapagos is most likely due to the in-creased evaporative water loss associated with a warm tropical environment.

TABLE 1

Differences in Urine Concentrating Ability of Humpback Whale, M. noraeangliae, and Human Given to Show a Gain or Loss of Body Water after Ingestion of 1 Liter of Seawater

TABLE 11

Maximum Urine Chloride Concentration and Maximum Osmolarity Measured for Marine Mammals Compared to Values of Representative Terrestrial Mammal

IV. Relative Reductions in Water Loss

As described earlier, marine mammals do not need to drink seawater because they have reduced their evaporative water loss. Amazingly, northern elephant seals can fast for months without access to food or water. The onlv water available to fasting seals is MWP from the oxidation of fat and protein in their tissue. Remember that a positive water balance requires that water input equals water output. This requires that water lost in the urine, feces, and from evaporation be equal to or less than water produced from metabolism (MWP). How then do elephant seals, and probably other seals and sea lions, reduce their water loss?

A. Cutaneous Water Loss

Given their aquatic lifestyle, marine mammals have very low evaporative cutaneous water loss. In water there would be no evaporative water loss, and on land, because pinnipeds lack sweat glands, their evaporative loss is quite low. However, common dolphins and harbor porpoises, Phocoena phocoena, appear to lose a substantial amount of water across their skin surface. Common dolphins lose as much as 4 liter H20 day” 1 or 70% of their total water intake. It may be that seawater ingestion is necessary to make up for the water lost across the skin.

B. Respiratory Evaporative Water Loss

Endotherms lose water through respiration by the simple physics of warming and saturating the air they breathe. Ambient air is inhaled, warmed, and humidified to core body temperature. For example, air fully saturated (100% relative humidity) with water at 10°C contains 10 mg H20 per liter of air, whereas fully saturated air in the lungs at 37°C contains 40 mg H2O per liter of air. Unless there is a mechanism to recover water, a seal would lose 30 mg of H20 for everv liter of 10°C air it inhaled.

Marine mammals employ a fevy tricks to reduce the water lost through respiration. The first is to breathe periodically, i.e., to inhale, hold their breath, and then exhale. This is called apneustic breathing. Apneustic breathing increases the amount of oxygen extracted per liter of air inhaled. Whereas terrestrial animals typically extract 4% oxygen per breath, marine mammals can extract as much as 8% per breath. This allows marine mammals to breathe less frequently and thereby lose less water because they make fewer respirations to obtain an equivalent amount of oxygen. Pinnipeds, sea otters, and polar bears, Ursus maritimus, reduce their respiratory evaporative water loss further by employing a nasal countercurrent heat exchanger. It has been suggested that dolphins, which lack nasal turbinates, recover respiratory water through the adiabatic cooling associated with explosive respirations.

TABLE III

Rate of Seawater Ingestion Measured Using Isotopie Tracer Techniques in Marine Mammals

Nasal Countercurrent Heat Exchanger Marine mammals, rodents, and desert ungulates have small passageways in their nasal passages that allow them to recover water vapor and heat that was added to the air at inhalation. Nasal turbinates are composed of very small passageways that allow intimate contact between the inhalant air and the nasal membranes (Fig. 2).

As the cold air passes across the small nasal passage, it is warmed and water evaporates. Heat and moisture are transferred from the nasal passage to the air so that by the time it leaves the nasal turbinate it is warmed and humidified to body temperature. In the process of warming the inhaled air, the membranes lining the nasal passages have cooled. On the following exhalation the warm moisture-laden air is cooled as it passes over the cool membranes. As the air temperature declines water vapor condenses and is recovered in the nasal passage (Fig. 3).

C. Fecal Water

Loss Although there are no direct measurements, fecal water loss of feeding cetaceans is probably quite high. Fecal water loss in pinnipeds feeding on fish is comparable to that of terrestrial carnivores. However, it is not clear how marine mammals that ingest seawater avoid the laxative effect of MgS04. Fasting animals have negligible fecal water loss, as their fecal production is quite small.

Figure 2 (A) Sagittal section of a weanling elephant seal skull showing the nasal turbinates. (B) Cross section through one-half of the skull at line “X” in A. From Huntley et al. (1984).

Figure 3 Temperature at 1-cm intervals within the nasal passage of a weanling elephant seals where the ambient air temperature was 15°C (O) and 5°C (•). From Huntley et al. (1984).

TABLE IV

Water, Lipid, and Protein Content of Marine Mammal Milk Compared to Human and Cow

D. Urinary Water Loss

The rate and amount of water lost in the urine are directly related to both the urine concentrating ability of the kidney and the hydration state of the animal. The kidney ultimately regulates the water and electrolyte state of the animal. When there is a surplus of water, the kidney produces diluted urine, whereas during periods of water stress, the kidney excretes concentrated urine. The kidney must be able to excrete metabolic end products in the form of urea and all excess electrolytes with the water that remains after cutaneous, respiratory, fecal, and in some cases, lactational water loss. While at sea, marine mammals either get all of their water from their prey or they drink seawater. This requires the processing of large urine volumes at moderate to high urine concentrations, and most marine mammals (cetaceans, pinnipeds, sea otters) have a specialized lobulate or reniculate kidney that enables them to do this.

Pinnipeds, such as the northern elephant seal, undergo prolonged fasts on land without access to water. These animals are able to stay in water balance by a combination of low rates of evaporative water loss coupled with low rates of urine production. Elephant seals utilize fat almost entirely (96-98%) for their metabolism while fasting. Fat oxidation produces only C02 and H2O, whereas the oxidation of protein results in CO2, H2O, and urea. Urea is the end product deamination of amino acids and requires water to be excreted by the kidney. Therefore, fat is not only an efficient way to store energy, it is also economical with respect to water balance.

V. Water Balance during Reproduction

Many female pinnipeds do not have access to water while they suckle their young and thus could become dehydrated during lactation. However, marine mammal milk is high in lipids and low in water compared to terrestrial mammals (Table IV). This has the advantage of providing the young with the maximum amount of energy with minimal loss of water from the mother. This is likely an advantageous by-product of the energetics of marine mammal lactation and not a derived adaptation for water balance. It is important to note that pups also do not have access to water and therefore must be capable of maintaining their water balance entirely from water contained in the milk and that derived from its oxidation.