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Morphology of the Kidney in a Nectarivorous Bird, the Anna's Hummingbird Calypte Anna

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Morphology of the Kidney in a Nectarivorous Bird, the Anna's Hummingbird Calypte Anna J. Zool., Lond. (1998) 244, 175±184 # 1998 The Zoological Society of London Printed in the United Kingdom Morphology of the kidney in a nectarivorous bird, the Anna's hummingbird Calypte anna G. Casotti1*, C. A. Beuchat2 and E. J. Braun3 1 Department of Biology, West Chester University, West Chester, PA, 19383, U.S.A. 2 Department of Biology, San Diego State University, San Diego, CA, 92182, U.S.A. 3 Department of Physiology, Arizona Health Sciences Center, University of Arizona, P.O. Box 245051, Tucson, AZ, 85724±5051, U.S.A. (Accepted 21 April 1997) Abstract The kidneys of Anna's hummingbird (Calypte anna) differ in several signi®cant ways from those of other birds that have been examined. The kidneys of this nectarivore contain very little medullary tissue; 90% of the total volume of the kidneys is cortical tissue, with medulla accounting for only an additional 2%. More than 99% of the nephrons are the so-called `reptilian type', which lack the loop of Henle. The few looped (`mammalian type') nephrons are incorporated into only a few medullary cones per kidney. The loopless nephrons are similar to those of other birds. However, the looped nephrons differ in that they lack the thin descending limb of the loop of Henle, which is found in other birds and is thought to play an important role in the countercurrent multiplier system in the avian kidney. Instead, the cells of the nephron segment following the pars recta of the proximal tubule resemble those of the thick ascending limb, with the large populations of mitochondria that are typical of transporting epithelia and no reduction in cell height. The absence of a descending thin limb in Anna's hummingbird is not necessarily a correlate of the hummingbird's liquid diet, because thin limbs have been documented in the kidneys of two other hummingbird species, the rufous hummingbird (Selasphorus rufus) and the broad-tailed hummingbird (Selasphorus platycercus). The functional correlates of the unique renal morphology in Anna's humming- bird warrant further study. Key words: Calypte anna, hummingbird, kidney, nephron, renal morphology INTRODUCTION (<100 mOsm), although they did measure some urine samples that were probably isosmotic or even slightly Hummingbirds are among the smallest birds, ranging in hyperosmotic (reported in Beuchat et al., 1990). The body mass from 2±20 g (Brown & Bowers, 1985). They concentrations of electrolytes in the urine of the birds are largely nectarivorous and, because of their small (4±19 mM Na+, 10±27 mM K+) mirror the low electro- size and high mass-speci®c metabolic rate, they must lyte levels typical of the nectar produced by humming- consume each day amounts of nectar greater than their bird-pollinated plant species (Baker & Baker, 1975; body mass to meet their energy requirements (Lasiewski, Hiebert & Calder, 1983). 1963; Hainsworth & Wolf, 1972; Beuchat, Chaplin & Despite the high rates of ¯uid intake by humming- Morton, 1979; Powers & Nagy, 1988; Weathers & Stiles, birds, there are environmental situations in which the 1989). birds must deal with potential dehydration. Rates of High rates of nectar intake by hummingbirds can evaporative water loss in these small birds are very high, necessitate excretion of substantial amounts of excess even at modest ambient temperatures (Lasiewski, 1964; water (Beuchat, Calder & Braun, 1990), so the kidneys Powers, 1992), and the amount of nectar required for must be capable of rapidly processing large volumes of energy balance can be inadequate to maintain positive very dilute urine. Calder & Hiebert (1983) have mea- water balance (Calder, 1979). In these circumstances, sured osmolalities of urine samples collected from birds hummingbirds must be able to minimize urinary water in the ®eld and noted that they were typically very dilute loss through renal or post-renal mechanisms. Hummingbirds and other nectarivorous birds face an unusual and challenging suite of osmoregulatory pro- *All correspondence to: Dr Giovanni Casotti, Department of Biology, blems, and we might expect their kidneys to differ West Chester University, West Chester, PA 19383, USA structurally from those of non-nectarivorous birds. 176 G. Casotti, C. A. Beuchat and E. J. Braun Considerable attention has been directed at docu- The relative volumes of the cortex, medulla and menting renal structure of other species of birds in the vasculature were estimated using point-counting techni- context of increasing our understanding of the urinary ques (Gundersen & Jensen, 1987; Gundersen et al., concentrating mechanism (see reviews by Dantzler, 1988). The volumes of components of the nephron (the 1989; Braun, 1993; Nishimura, 1993). Only one study, renal corpuscle, proximal tubule, limbs of Henle, distal on the other hand, has addressed the anatomy of the tubule, and cortical and medullary collecting ducts) hummingbird kidney. Johnson & Mugaas (1970b) were estimated in the same way. examined the kidneys of two species of hummingbirds, the broad-tail hummingbird (Selasphorus platycercus) and the rufous hummingbird (Selasphorus rufus). They Nephron morphology noted that hummingbird kidneys ``contain a poorly developed renal medulla consisting almost entirely of To examine the gross morphology of the nephron, 2 collecting ducts with only a few associated looped birds were killed with carbon dioxide and the kidneys nephrons''. The only quantitative data they report, for a dissected from the synsacrum. The tissue was placed in a single rufus hummingbird, are sizes of cortical and solution of alcoholic ferric chloride (95 ml ethyl alcohol, medullary regions, diameters of thick and thin limbs of 5 ml concentrated HCl, 30 g ferric chloride) overnight at the loops of Henle, and number of collecting ducts. 4 8C. This was followed by digestion for 2 h in 20% HCl The goal of this study was to document aspects of at 37 8C, after which the tissue was placed in cold (4 8C) renal structure that might re¯ect the unique physiolo- acid ferric chloride (200 mg ferric chloride, 0.2 ml acetic gical demands that must be met by the kidney in a acid, 100 ml distilled water). After soaking the kidney in nectarivorous bird, with a special emphasis on those water for 4±12 h to soften, individual nephrons were features related to the concentrating and diluting capa- dissected free using ®nely drawn glass needles and were city of the kidney. transferred to a drop of 50% glycerol on a microscope slide. Nephrons were viewed under a compound micro- scope, and computer-digitized images were captured MATERIALS AND METHODS and stored for later analysis. The left kidneys of the birds were used to examine Animals the cellular ultrastructure of the loop of Henle and collecting duct. The kidneys were ®xed as described Male Anna's hummingbirds were collected in San Diego above. Individual medullary cones were identi®ed by the and Riverside Counties, California, U.S.A. They were connective tissue sheath that surrounds the loops of housed in the laboratory in ¯ight cages and provided a Henle of looped nephrons, as well as the collecting ducts commercial hummingbird diet ad libitum. (Nektar-Plus, originating from both looped and loopless nephrons. Nekton). Kidneys were removed from the birds and Each medullary cone, minus its associated cortical processed within 72 hours of capture. Mean body mass tissue, was removed from the kidney and its length was 5.2 0.4 g (n = 17). measured ( 0.01 mm) using an ocular micrometer on a dissecting microscope. This measurement approximates the length of the longest loops of Henle within each cone Renal composition (Boykin & Braun, 1993). The tissue was then processed routinely for transmission electron microscopy; it was Birds (n = 5) were killed with carbon dioxide, the post®xed in 1% Dalton's osmium tetroxide, washed in a abdominal cavity was opened, and the dorsal aorta was series of graded alcohols, then in®ltrated with propylene cannulated. The kidneys were ¯ushed with 0.2 M phos- oxide and embedded in epon resin. Sections were cut to phate buffer, followed by half-strength Karnovsky's a thickness of 90 nm, stained with uranyl acetate and ®xative (350 mOsm). The kidneys were then dissected lead citrate, and viewed on a transmission electron from the synsacrum. microscope. The length and width of the right kidneys were measured using vernier callipers to 0.01 mm and their volumes estimated by water displacement (Scherle, Enumeration of nephrons 1970). The tissue was then processed routinely for light histology, after which length and width were measured To determine the total number of nephrons in each again. Linear tissue shrinkage (length and width) due to kidney, 5 birds were killed and the kidneys ¯ushed with histological processing ranged from 22±27%. This is phosphate buffer as described above. To make the within the range reported for honeyeater kidneys glomeruli easier to count, they were stained by perfusing (Casotti, Richardson & Bradley, 1993). The kidney the kidneys with 5% alcian blue 8GS until the dye exited tissue was embedded in paraf®n wax and a series of the caudal vena cava and the kidneys turned blue. Both transverse serial sections were cut at 10 equally-spaced kidneys were dissected from the synsacrum and ®xed in intervals along its length using stereological procedures 50% ethanol for 24 h, then transferred to a mixture of outlined in Mayhew (1991). The resulting sections were 50% ethanol and 1% ammonium hydroxide for 1.5 h. stained with haematoxylin and eosin. Following digestion in 20% HCl for 2 h at 37 8C, each Renal anatomy of Anna's hummingbird 177 kidney was transferred into a volumetric ¯ask con- (a) 100 taining 10 ml of distilled water. The kidney was agitated using a magnetic stir plate and bar until the tissue was 80 broken up and individual glomeruli could be identi®ed under the microscope.
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