Eldon J. Braun

Glucose regulation in birds

Birds maintain higher plasma glucose concentrations (P(Glu)) than other vertebrates of similar body mass and, in most cases, appear to store comparatively very little glucose intracellularly as glycogen. In general, birds are insensitive to the regulation of P(Glu) by insulin. However, there appears to be no phylogenetic or dietary pattern in the avian response to exogenous insulin. Moreover, the high levels of P(Glu) do not appear to lead to significant oxidative stress as birds are longer-lived compared to mammals. Glucose is absorbed by the avian gastrointestinal tract by sodium-glucose co-transporters (SGLTs; apical side of cells) and glucose transport proteins (GLUTs; basolateral side of cells). In the kidney, both types of glucose transporters appear to be upregulated as no glucose appears in the urine. Data also indicate that the avian nervous system utilizes glucose as a metabolic substrate. In this review, we have attempted to bring together information from a variety of sources to portray how glucose serves as a metabolic substrate for birds by considering each organ system involved in glucose homeostasis.

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.

Injury of Rat Renal Vessels Following Extracorporeal Shock Wave Treatment

The locations of extracorporeal shock wave treatment induced renal vascular injury and the sources of significant renal hemorrhage were determined in a rat model by means of two different vascular casting procedures. Silicone-rubber injected vascular preparations for light microscopy or corrosion casts for scanning electron microscopy were made following gross examination of the treated organs and their contralateral controls. After 1000 shock waves at 18 kV, five out of 20 treated kidneys appeared to be normal or minimally affected, while 15 showed gross evidence of marked vascular injury. Gross interstitial hemorrhage (15/20), subcapsular hematomas (7/20), and hemorrhages into the renal pelvis (5/20) were confirmed by extravasations of casting materials. These could be traced back to their vascular sources in several instances. Disruptions of interlobar and arcuate veins gave rise to most significant interstitial, subcapsular, and renal pelvic extravasations. On a microscopic scale cortical venules were among the most frequently injured vessels. The arterial vasculature was not spared. Arterial injury ranged from complete arcuate occlusion to small afferent arteriolar and glomerular capillary extravasations. The significance of shock wave induced vascular injury is discussed with respect to potential clinical side effects of ESWL.

Microanatomy of the renal cortex in the domestic fowl

Two aspects of the avian renal cortical microanatomy previously were unclear. The precise in situ folding patterns and orientations of the nephrons with respect to the other cortical elements had not been demonstrated. It also was not known whether certain nephron segments are supplied exclusively by either the arterial or the portal blood flow. In the present study, a new casting compound was developed to allow selective examination of the cortical components by light microscopy. Cortical nephrons at the surface of the kidney were serially sectioned and reconstructed in order to determine: (a) their relationships to the vasculature and collecting ducts; (b) the location and characteristics of the tubule segments; and (c) the primary and secondary folding patterns of the tubules. The anatomical findings were documented individually and then summarized in a comprehensive diagram of the superficial cortical microanatomy. In addition, an in vivo method was used to determine the extent of portal blood distribution to the nephron segments. It was demonstrated that renal portal blood suffuses all of the segments except for the loops of Henle.

Contributions of the kidneys and intestines to water conservation, and plasma levels of antidiuretic hormone, during dehydration in house sparrows (Passer domesticus)

SummaryThe contributions of the kidneys, the small intestine and the lower intestine (rectum plus cloaca) to water conservation during dehydration in unanaesthetized, unrestrained house sparrows (Passer domesticus) were assessed. Thirty hours of acute dehydration resulted in a 12% loss in body mass and a significant increase in plasma osmolality. Glomerular filtration rate declined by 55%, from 7.7 to 3.5 ml/h, and urine flow rate delined by more than 80%, from 0.2 to 0.03 ml/h. These changes are likely attributable to a large increase in plasma levels of arginine vasotocin during dehydration, from <26 pg/ml in hydrated birds to greater than 200 pg/ml after 30 h dehydration. Flow of water from the ileum to the lower intestine was reduced during dehydration, primarily because of a reduced flow of dry matter (with no significant reduction in water content). The rate of water loss in the excreta declined from 0.2 ml/h in hydrated birds to 0.04 ml/h in dehydrated birds. The rate of water reabsorption in the lower intestine (equal to the rate of water loss in the excreta minus the combined rates of inflow into the lower intestine from the urine and the ileal contents) slightly exceeded the rate of water flow from the ileum in both hydrated and dehydrated birds. We suggest that much of the water reabsorbed in the lower intestine of hydrated birds derives from the urine, but that primarily water from ileal contents is reabsorbed in dehydrated birds. That is, urine undergoes significant post-renal modification in hydrated but not dehydrated house sparrows.

Regulation of renal and lower gastrointestinal function: role in fluid and electrolyte balance ☆

For the majority of vertebrates, the kidneys are not the sole organs that function to maintain homeostasis of body fluid and electrolytes. Mammals are unusual in this respect, as the kidneys are the organs that fill this role. For non-mammalian vertebrates, other organs such as gills, skin, salt glands, urinary bladders and the gastrointestinal (GI) system function in concert with the kidneys in the control of fluid and ion balance. Birds are of particular interest and unique as they do not possess a urinary bladder and the renal output enters the lower GI tract. The physiology of the interaction of avian kidneys and lower GI tract is an excellent example of integrative physiology and several aspects of it have been examined, for example, the role of the avian antidiuretic hormone (arginine vasotocin, AVT) in controlling renal output. AVT produces both a tubular and glomerular antidiuresis. The glomerular antidiuresis is important, as the fluid from the kidneys that enters the GI should not be highly concentrated. Another hormone, aldosterone, has been shown to play an important role in regulating the transport of sodium by the GI epithelium. In addition, the lower GI tract plays a significant role in recycling a portion of the nitrogen that leaves the kidneys as uric acid. Furthermore, the output of avian kidneys contains large amount of protein that is conserved by the lower GI tract.

Comparative renal function in reptiles, birds, and mammals

In this article, the regulation of the homeostasis of the extracellular fluid is compared for reptiles, birds, and mammals. The principle focus is on the role of the kidneys in this process. Although the basic elements of renal function are similar in the three classes, birds and mammals are set apart from reptiles in that the kidneys of these species have the ability to produce urines that are hyperosmotic to plasma. Reptiles and birds are set apart from mammals by the fact that these two groups excrete nitrogen as uric acid and not urea as do mammals. Reptiles and birds are further set apart from mammals in that the kidneys of these two groups are not the sole organs that function to regulate the composition of the extracellular fluid. In addition to having functional salt glands, the lower gastrointestinal tracts of reptiles and birds function in concert with the kidneys in the maintenance of homeostasis. There is a much greater range in body mass among mammals than in the other two groups. This has necessitated that the kidneys of mammals change size, shape, and internal organization to be able to carry out their homeostatic function. The kidneys of reptiles and birds do not follow a similar pattern. It would appear that no one group has the advantage over the other with respect to regulation of the composition of the extracellular fluid because representatives of all groups inhabit a broad range of environments and ecological habitats.

Osmoregulation in the Field by Salt-Marsh Savannah Sparrows Passerculus sandwichensis beldingi

We studied the osmoregulatory strategy of salt-marsh savannah sparrows (Passerculus sandwichensis beldingi) in the field in Baja California, Mexico, and we compared these birds with a subspecies of savannah sparrow found concurrently in the uplands surrounding the salt marsh. Passerculus sandwichensis beldingi had higher plasma osmolalities (349 vs. 339 mmol/kg), higher ureteral urine osmolalities (577 vs. 477 mmol/kg), higher urine sodium concentrations (126 vs. 74 meq/L), higher urine flow rates (7–10 vs. 1.7 μL/min), and larger kidneys (0.36vs. 0.21 g/pair of kidneys) than the upland sparrows. Other unusual findings in the salt-marsh birds were the presence of substantial volumes of hyperosmotic fluids (up to 811 mmol/kg) in the lower intestine and uric acid extending into the ileum. The rectal epithelium of P. s. beldingi was relatively smooth, with few low apical membrane extensions, whereas that of the upland sparrows had a dense apical microvillous brush border. The maximum urine concentration that we measured in freshly captured P. s. beldingi was 2.7 times plasma osmolality. Our findings suggest an osmoregulatory strategy that includes a high intake of solute, a copious urine flow to excrete this solute load, and, at least at times, substantial refluxing into the intestines of hyperosmotic urinary fluids. This unusual strategy presumably reflects the unusual circumstance of a bird without salt glands living in a salt marsh.

Renal anatomy in sparrows from different environments

The renal anatomy of three species of sparrows, two from mesic areas, the House Sparrow (Passer domesticus) and Song Sparrow (Melospiza melodia), and one salt marsh species, the Savannah Sparrow (Passerculus sandwichensis) was examined. Electron microscopy was used to describe the ultrastructure of the nephron. In addition, stereology was used to quantify the volumes of cortex, medulla, and major vasculature of the kidneys, and the volumes and surface areas occupied by individual nephron components. There appeared to be no differences in the ultrastructural anatomy of the nephrons among the sparrows. Proximal tubules contained both narrow and wide intercellular spaces filled with interdigitations of the basolateral membrane. The thin limbs of Henle contained very wide intercellular spaces which were absent in the thick limbs of Henle. The distal tubule cells contained short, apical microvilli and infoldings of the basolateral membrane. In cross section, the medullary cones of all birds display an outer ring of thick limbs of Henle which surround an inner ring of collecting ducts, which in turn surround a central core of thin limbs of Henle. The Savannah Sparrow has a significantly higher volume of medulla compared to the two more mesic species. Within the cortex, the Savannah Sparrow also has a significantly higher volume of proximal tubules but a significantly lower volume of distal tubules than the other species. Within the medulla, the Savannah Sparrow has a significantly higher volume and surface area of capillaries, and a significantly higher surface area of thick limbs of Henle and collecting ducts than the mesic species. These data suggest that the salt marsh Savannah Sparrow has the renal morphology necessary to produce a more highly concentrated urine than the mesic zone species. J. Morphol. 243:283–291, 2000

Avian metabolism: its control and evolution

This review discussed metabolism in poultry and wild birds with an emphasis on what remains to be elucidated. Circulating concentrations of glucose are much greater in both poultry and wild birds than in mammals which in turn are higher than in reptiles. The basis for this difference is unknown but does not appear to be related to the requirements of flight. Furthermore, birds exhibit a refractoriness to potential adverse effects of very high circulating concentrations of glucose. Again the basis of this is unclear. There is substantial information on the control of metabolism in poultry, although which hormones are exerting physiologic roles remains to be clarified. There is a tacit but unverified assumption that the control mechanisms are the same in wild birds and in poultry. Despite, significant research focus on metabolism in poultry and to a less extent wild birds, there is a dearth of studies determining metabolism in a quantitative manner.