The three parts of an itemized water budget are gain, loss and storage (Shoemaker and Nagy, 1977). Positive storage occurs when an animal retains excess water, as do toads in their urinary bladder, and negative storage is synonymous with dehydration. The most common avenues of water gain are ingestion in the food or by drinking, osmosis through permeable skin, as in frogs and toads, and production of metabolic water de novo during oxidation of carbohydrates, fats and protein for energy production. Water leaves animals by evaporation across skin, lungs, or any permeable surface at a rate that is dependent on the temperature and humidity of the air, as well as the permeability of the evaporating surface. The factors that influence the rate of loss may differ, depending on whether evaporation is taking place from the lungs, skin, or eyes. Water is lost as part of the voided urine and feces, and in any glandular secretions released by the animal.
Extant amphibians contain more water when fully hydrated, 77 to 83% of body mass, than the 70% of body mass found in extant reptiles and mammals (Bentley, 1966). The gain side of the water budget of a typical amphibian is simplified by the fact that most amphibians do not drink liquid water (Shoemaker et al, 1992). Metabolic water production is determined by the rate of energy metabolism, which in amphibians is relatively low. Typically it ranges from 0.1 to 0.3% of body mass per day, depending on the size of the amphibian. This amount is very small in comparison to the main avenue of water intake, osmotically across the skin. Amphibians can take up water at rates ranging from 30 to 360% of their body mass per day.
Highly permeable skin is a feature shared by all the Lissamphibia, permitting cutaneous respiration (Guimond and Hutchison, 1976); regulation of acid/base balance by CO2 release (Stiffler et al., 1990); active transport of salt (Stiffler, 1988); release of nitrogenous wastes as ammonia by diffusion into water (Shoemaker, 1987); evaporative cooling, modulating changes in body temperature (Spotila, 1972); and perhaps most important, water absorption through the skin (Shoemaker and Nagy, 1977). "The entire skin of amphibians is a site of seemingly unbridled flux," according to Feder (1992). The skin of Lissamphibia provides almost no barrier to evaporative water loss or gain, enabling the amphibian to rapidly deplete or replenish its stores of water. In some cases the permeable skin is not uniformly distributed over the body but is localized, particularly in a pelvic patch on the ventral surface where it can be pressed against a damp substrate (Stille, 1958).
The largest avenue of water efflux in amphibians is evaporative water loss across the moist and permeable skin. It can range from 3 to 160% of body mass per day (Tracy, 1975), depending on body size, ambient conditions of temperature, wind, and insolation, and on exposure of the animal to these conditions. Water evaporation via lungs and eyes is small relative to skin evaporation. Fecal water losses are determined by the dehydrating capability of the large intestine, which is moderate, and by food consumption, which depends on energy needs. Because amphibians have relatively low energy and food needs, fecal water losses are small relative to evaporative losses. Similarly, water losses via glandular secretions are typically small, but may be large on occasion (Lillywhite, 1971). Water lost as urine can be substantial, ranging from zero to 60% of body mass per day, depending on species and hydration state (Shoemaker and Nagy, 1977). The majority of nitrogenous wastes are excreted via this route. The final composition of the urine is determined by three organs, the kidneys, the cloaca, and the urinary bladder, all of which modify urine composition.
Accumulation of nitrogenous wastes is a constraint on terrestriality in extant Lissamphibia. Aquatic amphibians produce copious dilute urine because water is freely available. They excrete nitrogenous wastes partially through this urine, and partially as ammonia by diffusion across the skin (Shoemaker et al., 1992). Diffusional release of ammonia into air is much lower. Because ammonia is toxic, amphibians switch to forming a less toxic substance, urea, and both aquatic and terrestrial forms generally stop excreting urine when out of water (Shoemaker et al., 1992). In many amphibians, the bladder acts as a fluid store, and water in it is gradually reabsorbed. Meanwhile, urea accumulates in the body and diffuses throughout the body fluids. As a result, amphibians are limited in the duration of their terrestrial excursions by plasma urea levels. This problem becomes particularly acute if the animal is feeding away from water because then additional wastes are produced. As most amphibians typically do not excrete urine on land, they must return to water to rehydrate and only following rehydration is urine formed again and the urea excreted. A few species of frogs which live in arid habitats are able to produce uric acid, and their water requirements are reduced as a result. These same species can have very low rates of evaporative water loss by producing a waxy, waterproofing secretion that is spread over the skin, as in the case of Phyllomedusa, and by several layers of dead, skin, as in the case of Chiromantis (Shoemaker et al., 1992).
The more terrestrial species of lissamphibians are capable of both positive and negative storage of water. Many desert anurans have large urinary bladders, and can store large amounts of water as dilute urine in their bladders. The largest amount of stored urine found to date is 130% of standard (bladder-empty) body mass in burrowed Australian desert frogs, Cyclorana platycephala (Shoemaker et al., 1992). When frogs and toads with full bladders are restricted from access to free water, they reabsorb bladder water and maintain normal blood osmotic concentrations while losing water by high evaporation. When bladder water reserves are gone, these anurans continue to survive subsequent dehydration by tolerating additional loss of body water as well as the progressively increasing osmotic concentration in their body fluids. Dehydration tolerance varies with habitat aridity and taxonomic affiliation (Shoemaker et al., 1992), being highest (near 50% of body mass) in desert-dwelling spadefoot toads (McClanahan,
1967). The animal must either return to water, where it can rehydrate by osmosis, or find a hiding place such as a burrow, with a high humidity to limit net evaporation and some moisture in soil or leaf litter for osmotic uptake (McClanahan, 1972). Amphibians that live in seasonally-arid habitats avoid activity during the dry parts of the year, except occasionally foraging at night. They may form cocoons, accumulate urea to maintain a favorable osmotic gradient between themselves and the soil, reduce their already low metabolic rate, and use other physiological and morphological mechanisms to enhance water balance while water availability is low.
In short, most amphibians are built to process water rapidly. Their skin offers little resistance to evaporation; an amphibian away from water will die of dehydration in less than a day or two. Three main points emerge from this analysis. The skin's permeability mandates that it will be a major route of water loss during terrestrial activity away from water. The skin is also the major avenue of water gain, thus behavior, particularly selection of microhabitat, is critically important in achieving water balance in most amphibians while they are active. Third, the more terrestrial and arid-adapted amphibians are able to achieve water balance during seasons when liquid water is unavailable, but usually only by being inactive in burrows or other hiding places.
Reptiles generally have water requirements that are only about 1 to 5% of those of amphibians and reptiles have much lower rates of water exchange. Reptilian skin has a very high resistance to evaporative water loss (Lillywhite and Maderson, 1988). Thus, those avenues of water flux that were inconsequential in amphibians, such as metabolic water production and fecal water loss, are major aspects of reptilian water budgets.
The main avenue of water intake for many reptiles is in the diet, with intake rates ranging from 0.7 to 2.7% of body mass per day in small arid-habitat species. Metabolic water production in reptiles is determined by the rate of energy metabolism and ranges from 0.1 to 0.5% of body mass per day. This amount accounts for 10 to 20% of total water gain in several small, diurnal, arid-habitat reptiles (Shoemaker and Nagy, 1977). Many species living in temperate habitats can maintain or increase body mass during rainless spring and summer periods when drinking water is not available.
Some reptiles "drink" with the tongue touched to drops of water on vegetation or other substrates. Water gained by drinking may be very important, as in desert tortoises (Nagy and Medica, 1986) and in lizards living in mesic habitats, although actual rates of drinking in the field are largely unknown (Nagy, 1982). Some reptiles have grooves in the skin to channel water droplets of rain or condensation toward the mouth (Withers, 1993).
As with amphibians, evaporation is often the largest avenue of water loss from reptiles. However, the rate can be nearly three orders of magnitude less (Shoemaker and Nagy, 1977; Shoemaker et al., 1992), as little as 0.25% of body mass per day (Mautz, 1982), because of their relatively impermeable skin. Even so, evaporation accounts for 25-75% of total water loss in several species of arid-habitat reptiles (Nagy, 1982). Reptiles living in moist habitats have much higher rates of evaporation, up to 30% of body mass per day in tropical lizards, and 200% per day in dry air in a tropical burrowing snake. In typical reptiles, about half of the total evaporation occurs through the skin, whereas the other half occurs through the respiratory tract. The wet surfaces of eyes can account for 15-65% of total evaporative loss (Mautz, 1982).
Terrestrial reptiles can dehydrate their feces fairly well, as dry as 40% water by mass, and ranging from 20 to 60% of total water loss. Herbivorous reptiles produce more feces per unit of metabolizable energy than carnivorous reptiles, due to the lower digestibility and the lower energy content of plants compared to animal matter. However, if herbivores obtain succulent green plant matter to eat, they ingest much more dietary water than do carnivores (Shoemaker and Nagy, 1977).
Urinary water loss by reptiles can be quite low, amounting to as little as 0.08% of body mass per day in an active desert lizard maintaining a balanced water budget (Shoemaker and Nagy, 1977). They conserve urinary water by excretion of a large portion of their nitrogenous waste as uric acid rather than as urea or ammonia. Uric acid has two beneficial properties. First, it has a low solubility, so it precipitates out of solution at low concentrations and can be eliminated in solid form, saving the water otherwise needed to dissolve urea or ammonia. Neither amphibians nor reptiles can produce urine hyperosmotic to the plasma, so this savings is substantial. Second, uric acid precipitates along with dietary cations such as sodium and potassium, thereby saving the water these ions would otherwise require for their elimination in dissolved form. Thus, the evolution of uricotelism has reduced the water requirements of reptiles, allowing increased independence from free water sources.
Many mesic- and xeric-habitat reptiles have salt glands that produce concentrated salt secretions that eliminate excess dietary salts with little accompanying water. Among desert lizards having nasal salt glands, water losses via nasal secretions are low, 0.1 to 0.3% of body mass per day, but account for about 10% of the small total water loss.
Regarding storage of water, some reptiles are somewhat like amphibians, having the capacity to store up to 30% of their body mass as dilute urine in a urinary bladder. Of course, water-loaded reptiles can produce copious urine while returning their body water volumes to normal, so urinary water losses can exceed 30% of body mass per day (Shoemaker and Nagy, 1977). The desert tortoise can survive up to 50% loss of body mass due to dehydration, after it has exhausted the urinary bladder stores, while the body fluid osmotic concentration rises, as in amphibians. It does not urinate for months and only then after a rainfall allows it to rehydrate (Nagy and Medica, 1986).
To summarize, the ability of many species of reptiles to achieve water balance without drinking is due to their selection of moist foods, and to their low rates of water loss. Reptiles living in dry habitats are relatively waterproof, and most reptiles have water requirements that are only about 1-5% of those of amphibians. The reptiles have nearly impermeable skin, they produce relatively dry feces and may have nasal salt glands that eliminate dietary salts with little water loss. They make urate salts to eliminate waste nitrogen and dietary salts in precipitated form. Desert reptiles may store water in a urinary bladder and tolerate extensive dehydration. These adaptations allow arid-habitat reptiles to be active during dry periods, and to attain water balance using only the succulence of their diet, without needing free water for drinking or any other purpose.
Comparison of Extant Modes of Maintaining Water Balance
Many amphibians can tolerate wide swings in body hydration (Shoemaker et al., 1969; van Buerden, 1984). When full, the mass of water in the urinary bladder may equal the mass of the fully hydrated amphibian with the bladder empty. Water may be reabsorbed into the body from the bladder during terrestrial excursions (Shoemaker, 1964), and after that, the animal may tolerate extreme water deficits before rehydration occurs. In contrast, most reptiles do not experience variation in internal fluid concentration, and maintain body hydration state with low water flux rates. Some species of reptiles, especially those living in very hygric habitats such as wet tropics or moist soil, have water flux rates that are very similar to those of amphibians, including high rates of water gain and loss by evaporation, but these animals do not vary internal fluid concentration substantially.
Semiterrestrial anurans can withstand the loss of about half their body water (400 ml kg"l) and the resultant doubling of body fluid concentrations (Shoemaker and Nagy, 1977). Among amphibians, internal fluids may concentrate to 700 or 800 mOsm, while the desert tortoise, among the most xeric-adapted reptiles, can concentrate its body fluids to 600 mOsm under extreme conditions (Minnich, 1977), although typically in the field concentration goes no higher than 340 mOsm (Minnich, 1979). The time scale in which dehydration occurs in xeric reptiles is also much longer than the brief period that can be tolerated by xeric amphibians.
What an animal can withstand in the laboratory and what it chooses to do in the field may not be the same. Feder and Londos (1984) found that salamanders ceased foraging well before their performance was impaired or their tolerance to desiccation was reached, and they suggested that salamanders voluntarily abandon foraging well before their physiological limits were reached. It is logical to assume that animals will not push themselves to extremes during routine activities such as foraging. This being the case, the time and distance a slow moving, wet animal could spend away from water is quite limited, although it could be extended by the choice of shaded, moist microhabitats, or by moving about during precipitation or at night when water condenses on the soil and leaf litter. Reptiles, with water requirements of only 1-5% that of amphibians, can survive with much less access to water and can use body water more efficiently, permitting much longer terrestrial excursions into much drier habitats.
One can postulate that once semiterrestrial animals became more restrained in their use of water it was necessary for them to become more deliberate in their temperature regulation. The effects on body temperature when water loss is curtailed through the skin may be very important, as damp skin promotes heat loss, or conversely, minimizes heat gain. A wet-skinned frog in full sun may have a body temperature only a couple of degress higher than a frog in full shade, although double the rate of evaporative water loss (Tracy, 1976). On the other hand, if two ectothermic animals are the same size, but one has wet skin and the other dry, the wet one will be cooler even if both are held in full sun at the same air temperature (Spotila et al., 1992). Increasing environmental temperature will cause body temperatures of both wet and dry animals to increase, but not at the same rate or to the same extent. In the modelling by Spotila et al. (1992), dry skin body temperatures increased from 26 to 42.4° C whereas wet-skinned body temperatures increased only from 23.4 to 28.3° C under the identical conditions. In the field, body temperatures of amphibians are generally much lower than those of reptiles (Avery, 1982; Hutchison and Dupre, 1992).
The profound difference in thermal response between a wet-skinned and a dry-skinned animal provides a potential explanation for the contrast in the types of thermoregulation between Lissamphibia and extant reptiles. Lissamphibians generally do not show a preferred body temperature or a specific activity temperature (Hutchison and Dupre, 1992). Thermoregulation in modern amphibians relies mostly on "passive" evaporative cooling and behavioral selection of damp shaded habitats (Hutchison and Dupre, 1992). It is likely that temperature regulation in Lissamphibia is subservient to hydric constraints. In other words, in amphibians, if there is a conflict between hydroregulation and thermoregulation, then thermoregulation takes a lower priority.
Reptiles, by contrast, in general have very narrow ranges of preferred activity temperatures (Brattstrom, 1965). Although ectothermic, many reptiles are able to regulate their body temperature very narrowly with behavioral means (Avery, 1982). The importance of behavioral thermoregulation is shown by the fact that different species of reptiles in the same environment may have different activity temperatures, and reptiles of the same species from different habitats may have the same body temperatures for activity (Bartholomew, 1982). Nocturnal desert geckoes have a lower acitivity temperature than diurnal lizards, but no difference in water flux rates (Nagy and Degen 1988). In addition, the excursion of body temperature between activity and inactivity is much greater in reptiles, as their active temperatures are generally higher than those of amphibians, even for nocturnal reptiles, while body temperatures during inactivity may be substantially lower.
Animals benefit in several ways from a higher body temperature, but it is important to remember that higher body temperatures are enabled or permitted, according to biophysical principles, as a result of the change from wet and permeable to dry and impermeable skin. Permitting a relatively high body temperature reduces the need for loss of evaporative water for cooling in a hot environment. Increased body temperature also increases metabolic rate, which could increase alertness and responsiveness, important for predation or predator avoidance (Bennett, 1991). On the other hand, dry skin creates some new problems for the heat budget of the animal, by increasing sensitivity to a variety of environmental parameters, including solar radiation, wind speed, and heat convection, even though it decreases sensitivity to humidity (Spotila et al., 1992). Body temperature in dry-skinned animals is much more affected by skin reflectance and by body size than is the temperature of a wet-skinned animal. Thus, the reduction in skin permeability to water increases the lability of the body temperature and its sensitivity to some terrestrial conditions.
The wide range of potential body temperatures available to a dry-skinned animal, along with an increased sensitivity to highly variable environmental conditions, could create difficulties for an animal that did not make any effort to control its body temperature. In other words, dry skin not only makes it possible to increase body temperature, it appears to necessitate the inititation of intentional, fairly precise, behavioral temperature selection.
As compared to amphibians, amniotes use more energy on a daily basis. At the same body temperature, the resting metabolic rate of amphibians is only two-thirds that of reptiles of identical mass (Regal, 1983; Pough, 1983). This difference is correlated with the decreased water content as a percentage of total mass in amniotes. A semiterrestrial animal that stays cool as a result of evaporative water loss may be constrained to a low metabolic rate niche. This may explain the absence of herbivory in adult amphibians, as herbivorous reptiles may require high body temperatures for digestion of plant material (Bartholomew, 1966). Reptiles in general operate at a higher metabolic rate than amphibians, and this may be an important part of the physiological distinction between these two groups.
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