The Cape clawless otter (Aonyx capensis) is one of the few species of mammals that occur in both freshwater and marine habitats, and it therefore must be able to tolerate the high rates of water flux typical of aquatic animals as well as the desiccating effects of seawater. The clawless otter has paired, discrete multirenculate kidneys (total mass = 172 g) comprised of both unipapillary and bipapillary renculi weighing an average of 2.6 and 3.2 g, respectively. The average thickness of the cortex is 2.3 mm, and thicknesses of the outer and inner medulla are 2.4 and 6.4 mm, respectively. These measurements and the overall structure of the kidney of the Cape clawless otter are intermediate between those of freshwater and marine mammals.

Hummingbirds have rates of water turnover that are among the highest of any bird, consuming up to five times their body mass in nectar each day. To determine if the processing of these extraordinary volumes of water is associated with structural specializations in the kidney, we examined the renal morphology of Anna's hummingbird (Calypte anna) using scanning electron microscopy of vascular and tubular casts. The glomerular tufts are simple, containing a single, unbranched capillary that is spiraled or folded back on itself only one or two times. There is no evidence that nectarivory in this species is associated with a relative increase in the size of the glomeruli. The medullary cones are small, containing only a few loops of Henle and collecting ducts. The vasa recta form a complex network of branching and anastomosing capillaries. In this nectarivore, the structures necessary to produce urine that is hyperosmotic to plasma are poorly developed or absent, which is consistent with urine osmolalities that are uniformly low. J. Morphol. 240:95-100, 1999. © 1999 Wiley-Liss, Inc.

We measured levels of glucose and glycated hemoglobin in the blood of three of the world's smallest nectarivorous birds, the Anna's (Calypte anna), Costa's (Calypte costae), and ruby-throated hummingbirds (Archilochus colubris). Plasma glucose levels of hummingbirds that were fasted overnight (17 mM) were higher than those in any mammal and are among the highest ever measured in a fasting vertebrate. Glucose levels in hummingbirds just after feeding were extreme, rising as high as 42 mM. The surprisingly high blood glucose concentrations in hummingbirds were accompanied by glycated hemoglobin levels that are the highest ever measured in birds but are lower than those of non-diabetic humans. How hummingbirds tolerate blood glucose levels that cause serious neurological and microvascular pathologies in diabetic humans and animals remains unknown.

Mammals with relatively long loops of Henle for their body size tend to have greater than average urinary concentrating ability, but the relationship between urine osmolality (Uosm) and absolute length of the loop of Henle (generally estimated as medullary thickness) is neither proportional nor direct. Uosm is independent of the thickness of the outer medulla (corresponding to the length of the medullary thick ascending limb), which scales similarly with body mass in animals from mesic, arid, and freshwater environments. After adjustment for the effect of body size, there is a significant relationship between the thickness of the inner medulla (corresponding to length of the thin ascending limb) and concentrating ability, but only in species from mesic environments; for these, the thickness of the inner medulla accounts for only 16% of the interspecific variability in Uosm. In marine mammals, both the cortex and medulla are surprisingly thin, yet these animals produce very concentrated urine for their size. A functional dependence of urinary concentrating ability on the length of the loop of Henle is a central tenet of countercurrent multiplier theory, but the correlation of maximum urine concentration with loop length is weak at best and largely reflects the influence of the thin ascending limb.

Currently accepted theories of the urine concentrating mechanism of the mammalian kidney predict that concentrating ability should increase with increasing length of the loop of Henle. However, larger mammals have longer nephrons than do smaller ones, yet concentrating ability declines with increasing body mass (M, in kg) as M-0.097. Greenwald & Stetson (1988, News Physiol. Sci. 3, 46-49) have suggested that the diminished concentrating ability of large mammals reflects their lower mass-specific metabolic rate. They propose that, because the urine concentrating mechanism depends upon the energy-dependent transport of sodium chloride, concentrating ability should be closely related to mass-specific metabolic rate. Examination of the allometric scalings with body mass of medullary thickness and metabolic rate indicate that the rate of increase in length of the loop of Henle with body size (M0.129) is insufficient to offset the decline in mass-specific metabolism (M-0.24). The residual product of these scalings (M-0.11) indicates that urine concentrating ability should be inversely related to body size and is similar to the observed allometry of concentrating ability (M-0.097). The decline in concentrating ability of the kidney with body size is probably not a result of inability of the kidney to adapt physiologically or structurally to changes in size, but rather reflects the scaling of the need to conserve water. Small mammals, because of their high rates of evaporative and respiratory water loss, have a much higher rate of water turnover than do large mammals (Vwater.kg-1 alpha M-0.20). Because the need to concentrate the urine diminishes with increasing body size, the increase in loop length need only partially compensate for the simultaneous decline in metabolism.

Hummingbirds subsist almost entirely on a liquid diet composed of floral nectar, and, when energy demands are high, they can consume more than three times their body mass in fluid per day. At the same time, however, the hummingbird's high metabolism requires efficient extraction of energy and nutrients from a dilute food source that is passing rapidly through the gastrointestinal (GI) tract. The ability of the hummingbird to efficiently process and excrete such large volumes of water must surely entail structural or functional specializations of the kidney and GI tract. The rate of water flux and nutrient extraction efficiency are also influenced, however, by the animal's feeding behavior. Because meal size affects the passage rate of food through the digestive tract (and, therefore, assimilation efficiency), feeding frequency and the amount of nectar consumed per feeding bout will affect the efficiency of nutrient absorption. Ultimately, the water and nutrient content of the nectar produced by the plants should reflect the ability of the hummingbird pollinator to balance its required intake of energy and electrolytes with its ability to excrete the accompanying water load. The simultaneous regulation of water and energy balance in hummingbirds consequently involves the complex integration of renal and intestinal functions and of these physiological processes with behavior and ecology. The hummingbird is a unique animal: its kidney appears to be structurally similar to that of a reptile, but its rate of water flux is more typical of an amphibian. Nonetheless, it sustains a metabolic level as high as that of any endotherm. The inextricable links among energetics, nutrition, and osmotic regulation in hummingbirds provide a fascinating example of the functional integration of vertebrate organ systems operating at the extreme.

B. H. Blake (Comp. Biochem. Physiol. A Comp. Physiol. 58: 413-419, 1977.) and W. A. Calder and E. J. Braun (Am. J. Physiol. 244 (Regulatory Integrative Comp. Physiol. 13): R601-R606, 1983.) have predicted that urine concentrating ability of mammals should decline with increasing body mass (M, in kg) as M-0.08. Edwards (29), on the other hand, speculated that concentrating ability should be independent of body mass. Using information compiled from the literature for 245 species of mammals, I examined the scaling of urine concentrating ability with body mass. Maximum urine concentration (Uosm, in mosmol/kgH2O) declined exponentially with body mass as Uosm = 2,564 M-0.097, and generally only the smallest species (less than 400 g) could produce urine with an osmolality greater than 4,000 mosmol/kgH2O. Medullary thickness (MT, in mm) and, therefore, the length of the loop of Henle, increased with body mass as MT = 8.147 M0.129. The thickness of the medulla relative to the size of the kidney (RMT), however, declined with body size (RMT = 5.408 M-0.108). The relative thickness of the medulla accounted for only 59% of the variability among species in concentrating ability, indicating that there are other morphological or physiological factors that significantly influence urine concentrating ability.

In reptiles, there are two pairs of kidneys at birth: the mesonephros and the metanephros. The metanephric kidney in reptiles, as in all amniote vertebrates, is retained as the functional kidney in adults. However, the reptilian mesonephros does not degenerate until after birth, and its function during this time is unknown. In neonates of the iguanid lizard Sceloporus jarrovi, the metanephric kidney is only 63% as large as predicted from the allometric relationship between kidney mass and body mass in adults. However, the kidney mass of neonatal lizards conforms to this prediction if the mesonephric and metanephric masses are combined. Some other amniote vertebrates appear to follow this pattern as well: in marsupials, which retain the mesonephros for a short period after birth, the sum of mesonephric and metanephric mass in neonates conforms to the allometry of kidney mass on body mass for adults. In contrast, the mesonephros of eutherian mammals is degenerate at birth and the metanephric kidney alone is of the predicted size. That the scaling of kidney mass in neonatal lizards and marsupials is the same as that of adults only if the mass of both the mesonephros and metanephros are combined suggests that the mesonephric kidney in these vertebrates plays a significant role in the regulation of water and ion balance during development and for at least a short time after birth.

1.1.The length of geslation of the viviparous lizard Sceloporus jarrovi is strongly dependent upon the body temperature of the pregnant female.2.2.Significantly more abnormal or dead offsping were born of pregnant females maintained at constant temperatures of 26, 36 and 38°C than in the control group that was allowed to behaviourally thermoregulate for 8 h · d−1 or in animals maintained at constant temperatures between 28 and 34°C.3.3.Pregnant females allowed to thermoregulate for 8 h · d−1 had larger young than lizards maintained at constant temperatures. Among animals kept at constant temperatures, neonate size declined with temperature between 28 and 36°C.4.4.Survivorship of adults did not vary among animals maintained at constant temperatures of 26—36°C or in the control group, but animals that eventually died survived longer at cooler temperatures. No adult animals survived constant exposure to 38°C.5.5.Adult lizard at 28, 30 and 32°C and in the control group were able to maintain body mass, but those at higher temperatures lost weight.

Pregnant females of the viviparous lizard species Sceloporus jarrovi regulate their body temperatures at a lower level than do males or nonpregnant females. It has been suggested that such a shift in preferred body temperature during pregnancy reflects the presence of divergent optimal temperatures for the female and for development of her young; a pregnant female must compromise between these temperatures in order to maximize her fitness. We examine this hypothesis using a Leslie matrix model of life history that quantitatively predicts the mean body temperature that would optimally compromise between conflicting thermal optima for mother and embryos. The predictions of the model are in close agreement (0.4°C or less) with temperatures observed in the field. According to the model, a pregnant female maintaining the mean body temperature typical of males or nonpregnant females would have ≈13% lower fitness than a pregnant female maintaining the optimal temperature. This is mainly due to increased embryo mortality, but reduced growth and increased mortality of the female also contribute to the loss of fitness. In the model, the optimal mean body temperature depends on the precision of thermoregulation. Thermoregulation by gravid females in the field is imprecise, with a standard deviation of 1.4° during active thermoregulation. If females are (unrealistically) assumed to maintain a perfectly constant body temperature (i.e., a standard deviation of 0°), the optimal mean temperature in the model is ≈2° higher than the mean temperature of gravid females in the field. Although specifically designed to incorporate features of the physiology and life history of Sceloporus jarrovi, the model can be generalized and applied to other situations involving compromise among multiple optima.

Both male and female Sceloporus jarrovi thermoregulate on every day during the summer when weather is suitable for lizard activity. Pregnant females, however, regulate a lower body temperature (: = 32.0 C) than do males or postparturient females (9 = 34.5 C) and, using the standard deviation about the mean as a measure of precision, also thermoregulate more carefully (FSD: females = 0.9 C, males and post-parturient females = 1.4 C). The variability in mean body temperature both within and between pregnant and non-pregnant lizards is related to shifts in the maximum and minimum body temperatures voluntarily tolerated in the field. Demographic and climatic considerations that make early birth advantageous at both high and low altitudes result in the prediction that lizards should regulate the highest body temperature possible during pregnancy. The shift to a lower preferred body temperature by female S. jarrovi during pregnancy could thus reflect a compromise by the female between two conflicting thermal optima, her own preferred body temperature and a lower optimum temperature for development of her embryos.

Neonatal lizards of the viviparous species Sceloporus jarrovi possess at birth a urinary bladder that contains a large amount (14% of body mass at birth) of very dilute (36 mosm/kg) urine. After birth, no additional urine is added to the bladder, and the fluid it contains declines in volume and increases in osmotic concentration as the bladder degenerates to the vestigial organ found in adults. Neonatal lizards can reabsorb the fluid in the bladder, and, under desiccating conditions, the reabsorbed fluid serves to maintain a constant plasma osmotic pressure (mean = 289 mosm/kg). However, after the bladder is empty, plasma osmolality increases to as high as 400 mosm/kg during dehydration. Lizards evaporatively lose water at a rate of ∼36 μl·day⁻¹, but the reabsorption rate of water from the bladder is only 21 μl·day⁻¹. Thus throughout the course of dehydration, the water content of the body (exclusive of the bladder) diminishes-but to a lesser extent when the bladder contains fluid than when it is empty. In neonatal lizards, the urinary bladder appears to be useful, as it is in amphibians, as an extrarenal osmoregulatory organ that can buffer body water compartments against osmotic perturbation.

Urinary bladders are found in adults of some species of lizards and not in others. We report here that urinary bladders are present in the neonates of six species of iguanid lizards that lack bladders as adults (Sceloporus jarrovi, S. magister, S. poinsetti, S. undulatus, Urosaurus ornatus, and Uta stansburiana). These bladders are filled with dilute fluid in both oviparous and viviparous species. Within a few days after birth, the bladder lumen begins to collapse and the bladder eventually degenerates to a finger-like vestige in adults.