Carol A. Beuchat

The Integration of Osmoregulation and Energy Balance in Hummingbirds

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 hummingbirds 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 waterflux and nutrient extraction efficiency are also influenced, however, by the animals 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 waterflux 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.

A Quantitative Test of Life History Theory: Thermoregulation by a Viviparous Lizard

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.

HYPERGLYCEMIA IN HUMMINGBIRDS AND ITS CONSEQUENCES FOR HEMOGLOBIN GLYCATION

We measured levels of glucose and glycated hemoglobin in the blood of three of the worlds smallest nectarivorous birds, the Annas (Calypte anna), Costas (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.

Metabolic Consequences of Viviparity in a Lizard, Sceloporus jarrovi

Metabolic rates of gravid females of the viviparous lizard Sceloporus jarrovi are higher than those of nonreproductive lizards: the allometric relationship between oxygen consumption and body mass in gravid females (V̇o2 = 0.437 m.735) has a statistically equivalent slope but a significantly higher intercept than that for males (V̇o2 = 0.225 m.812). The elevated metabolism of females during pregnancy is greater than can be accounted for by the increased mass of the pregnant female, indicating that the mass-specific oxygen consumption of the embryos is not scaling to maternal body mass. In fact, metabolism of gravid females is even higher than predicted if embryo metabolism is scaling to embryo body mass. Mean oxygen consumption of newborn S. jarrovi (mean body mass = 0.75 g) was 0.245 cm³ O₂ · h⁻¹, which is 1.4 times higher than that predicted from the allometric relationship for nonpregnant adults, but it is not statistically different from estimates of metabolism of embryos just before birth. During parturition, oxygen consumption of the female is 57%–162% higher than resting levels. The elevated oxygen consumption of viviparous female lizards during gestation could constitute a significant component of reproductive effort in these species.

Metabolism and the scaling of urine concentrating ability in mammals: Resolution of a paradox?

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.

Decomposition of nitrogenous compounds by intestinal bacteria in hummingbirds

Abstract Degradation of urinary nitrogen-containing compounds by bacteria in the ceca of birds occurs in a number of herbivorous and omnivorous species, and cecal absorption of the products of that degradation has been reported in chickens. This recycling of nitrogen may play an important role in nitrogen balance, especially in those species with low dietary nitrogen intake. We report, for the first time, degradation of nitrogenous compounds by intestinal bacteria in a bird that is nectarivorous and lacks ceca, Annas Hummingbird (Calypte anna). Hummingbirds subsist year-round on a liquid diet with an exceptionally low-nitrogen content. Ureteral urine containing ammonia, urea, and uric acid has been observed in the lower intestinal tract of Annas Hummingbird. Bacteria obtained from intestinal contents and homogenates of the anterior and posterior intestine of this species were able to break down uric acid, urea, and potassium urate, but not sodium urate. This degradation is the necessary first step in the recycling of nitrogen. Assessing its significance will involve determining whether the products of microbial breakdown are subsequently absorbed across the intestinal walls of these unique animals.

Glomerular and medullary architecture in the kidney of Anna's Hummingbird

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 Annas 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.

Role of the urinary bladder in osmotic regulation of neonatal lizards

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.

A Model of Optimal Thermoregulation during Gestation by Sceloporus jarrovi, a Live-Bearing Lizard

Reptiles are ectotherms; that is, they depend on external sources of heat to maintain their body temperature. Body temperature is regulated behaviorally rather than metabolically, primarily via habitat choice (sun vs. shade), orientation to thermal energy sources, and posture. Many of the processes involved in a reptile’s ability to procure, process, and assimilate food, to escape from predation, and to reproduce vary in efficiency as a function of body temperature. These include the capacity for and ability to recover from activity, egestion and digestion rates, auditory sensitivity, renal function and gonadal growth (see Dawson 1975 for a review).