Renal Anatomy in Sparrows from Different Environments
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JOURNAL OF MORPHOLOGY 243:283–291 (2000) Renal Anatomy in Sparrows From Different Environments Giovanni Casotti1* and Eldon J. Braun2 1Department of Biology, West Chester University, West Chester, Pennsylvania 2Department of Physiology, Arizona Health Sciences Center, Tucson, Arizona ABSTRACT The renal anatomy of three species of spar- birds display an outer ring of thick limbs of Henle which rows, two from mesic areas, the House Sparrow (Passer surround an inner ring of collecting ducts, which in turn domesticus) and Song Sparrow (Melospiza melodia), and surround a central core of thin limbs of Henle. The Savan- one salt marsh species, the Savannah Sparrow (Passercu- nah Sparrow has a significantly higher volume of medulla lus sandwichensis) was examined. Electron microscopy compared to the two more mesic species. Within the cor- was used to describe the ultrastructure of the nephron. In tex, the Savannah Sparrow also has a significantly higher addition, stereology was used to quantify the volumes of volume of proximal tubules but a significantly lower vol- cortex, medulla, and major vasculature of the kidneys, ume of distal tubules than the other species. Within the and the volumes and surface areas occupied by individual medulla, the Savannah Sparrow has a significantly higher nephron components. There appeared to be no differences volume and surface area of capillaries, and a significantly in the ultrastructural anatomy of the nephrons among the higher surface area of thick limbs of Henle and collecting sparrows. Proximal tubules contained both narrow and ducts than the mesic species. These data suggest that the wide intercellular spaces filled with interdigitations of the salt marsh Savannah Sparrow has the renal morphology basolateral membrane. The thin limbs of Henle contained necessary to produce a more highly concentrated urine very wide intercellular spaces which were absent in the than the mesic zone species. J. Morphol. 243:283–291, thick limbs of Henle. The distal tubule cells contained 2000. © 2000 Wiley-Liss, Inc. short, apical microvilli and infoldings of the basolateral membrane. In cross section, the medullary cones of all KEY WORDS: medulla; kidney; avian; bird; stereology The avian kidney is unique in structure among (Table 1). In contrast, the U/P osmolality ratio of T1 vertebrate kidneys in having two types of nephrons: mammals spans a broad range from about 1.8 in the those with and without a loop of Henle (looped and Mountain Beaver (Aplodontia rufa) (Schmidt- loopless, respectively) (Braun and Dantzler, 1972). Nielsen and Pfeiffer, 1970) to 26.8 in the Desert The loopless nephrons stay within the cortex while Hopping Mouse (Leggadina hermanburgensis) (Mac- the looped nephrons extend from the cortex and into Millen and Lee, 1967). The reason for the limited discrete medullary areas called medullary cones. urine-concentrating ability in birds compared to Within each cone, the number of loops of Henle mammals is uncertain; however, it may be related to decreases as the tip of the cone is approached. This the fact that most of the nephrons within the avian cascade in loop length may aid in establishing an kidney are of the loopless type. Without a loop of interstitial osmotic gradient along the length of the Henle, urine cannot be concentrated, and as all medullary cones. The intramedullary osmotic gradi- nephrons within the avian kidney (regardless of ent facilitates the production of a hyperosmotic type) empty into a common collecting duct, the fluid urine by the passive reabsorption of water from the from the loopless nephrons may be diluting the fluid collecting ducts as they pass through the intersti- from the looped nephrons. tium of the medullary cones (Layton, 1986; Nish- Despite numerous studies undertaken, no good imura et al., 1989; Layton and Davies, 1993; Layton index has been found that correlates anatomical et al., 1997). structure and the ability to concentrate urine in Birds and mammals are the only classes of verte- either birds or mammals. Most studies have concen- brates that are consistently able to produce a hyper- osmotic urine. In birds, this ability to produce a hyperosmotic urine is limited compared to that of mammals. The urine-to-plasma osmolality ratio Contract grant sponsor: West Chester University Faculty Develop- (U/P ratio), a measure of concentrating ability, in ment; Contract grant number: FD98020; Contract grant sponsor: NSF; Contract grant number: IBN 9515450. birds ranges from 0.2 in Anna’s Hummingbird to 3.0 in the Budgerigar, with most species having a *Correspondence to: Giovanni Casotti, Department of Biology, West ratio of about 2.0 when they are deprived of water Chester University, West Chester, PA. E-mail: [email protected] © 2000 WILEY-LISS, INC. 284 G. CASOTTI AND E.J. BRAUN TABLE 1. Urine to plasma osmolality ratios among birds to allow such a conclusion to be drawn. Birds inhab- Species Habitat U/P ratio iting arid environments may not always produce the most concentrated urine (Table 1). Budgerigar4 domestic 0.3–3.0u 5,6 u Our study presents data on the renal morphology Domestic fowl domestic 1.6–2.1 of three species of sparrows, two from mesic habitats Ring-necked pheasant3 domestic 0.6–1.5u Kookaburra1 wet 2.3–2.7v and one inhabiting a salt marsh area. Our aim is to Singing honeyeater1 wet 2.3–2.4v highlight the morphology of the kidneys of birds Red wattlebird1 wet 2.0–2.4v from different environments in an attempt to corre- 6 Bobwhite quail mesic 1.6 late differences in renal anatomy with habitat and California quail6 mesic 1.7 Senegal dove1 mesic 1.7v published data on renal concentrating ability for House sparrow8 mesic 1.0–1.7u these species. The gross and microanatomy of the Song sparrow8 semi-arid 0.7–2.2u kidneys are described and the volumes and luminal Anna’s hummingbird7 semi-arid 0.2–0.6f 7 f surface areas of the nephron components are quan- Rufous hummingbird semi-arid 0.2–1.1 tified using stereological techniques. House finch6 semi-arid 2.1–2.3 House sparrow3 semi-arid 1.0–2.2u 3 u White-crowned sparrow semi-arid 1.3–2.1 MATERIALS AND METHODS White-winged dove3 semi-arid 1.2–1.8u Crested pigeon1 arid 1.7–1.8v Animals Emu1 arid 1.1–1.4v Galah1 arid 2.1–2.5v Sparrows (males and females) used in this study Gambel’s quail6 arid 2.5 were taken from two different areas. Two species, Zebra finch3 arid 1.1u–2.8v the House Sparrow, Passer domesticus, and Song Glaucous-winged gull3 marine 1.6–1.9u 2 f Sparrow, Melospiza melodia, were collected in the Savannah sparrow salt marsh 1.6–2.7 field in Pennsylvania, under state license, using f Field samples, uureteral, vvoided. mist nets. These birds were transported in cages 1 Skadhauge, 1974. back to the laboratory for processing of tissue on the 2 Goldstein et al., 1990. day of collection. A third species, the Savannah 3 Goldstein and Braun, 1989. 4 Krag and Skadhauge, 1972. Sparrow, Passerculus sandwichensis, was collected 5 Skadhauge and Schmidt-Nielsen, 1967. in Baja California by E.J. Braun. Mean body mass of 6 Reviewed in Dantzler, 1970. the birds was: House Sparrows 26.5 Ϯ 1.3 gm (n ϭ 7 Beuchat et al., 1990. Ϯ ϭ 8 6), Song Sparrows 20.5 1.3 gm (n 5), and Sa- Data from present study. vannah Sparrows 18.7 Ϯ 1.8 gm (n ϭ 5). trated on the kidneys of mammals and are summa- U/P Ratios rized in detail by Beuchat (1996). Briefly, indices examined in mammals include absolute medullary Upon capture of the House and Song Sparrows, thickness, relative medullary thickness, and length ureteral urine was collected with small close-ended of the loop of Henle. The summary presented by cannulas (constructed from micropipette tips) con- Beuchat (1996) indicates that for mammals urine taining an opening that was placed over the ureteral concentrating ability is not a simple function of the orifices. A sample of whole blood was taken from the length of the loop of Henle, nor of any other single brachial vein of each bird. Both urine and blood variable measured, and that a number of other vari- samples were placed on ice until transported back to ables may be involved. For birds, similar morpholog- the laboratory. The urine was tested for osmolality ical indices have been examined in an attempt to using a vapor pressure osmometer (Wescor, Utah). find a relationship between structure and function Whole blood was centrifuged and the plasma ex- with respect to concentrating ability. These include tracted and tested for osmolality using the osmom- relative thickness of the renal medulla (Johnson, eter. The osmotic concentration of urine to plasma 1974), relative medullary area (Sperber, 1944), per- was then calculated. cent of looped nephrons and the number of medul- As noted earlier, the Savannah Sparrow kidneys lary cones (Goldstein and Braun, 1989), and the lack were donated by E.J.B. from another study (Gold- of the thin ascending limb in the avian nephron stein et al., 1990). Urine to plasma osmolality ratios (Beuchat, 1990). As in mammals, these variables are were calculated in the same manner in that study not strongly correlated with the ability to produce a and the data are presented in Table 1. concentrated urine. In birds, available data on urine concentrating Animal Preparation ability are limited, hence this makes it difficult to find a correlation between urine concentrating abil- Birds were killed with an overdose intraperitoneal ity and renal morphology (Table 1). It might be injection of sodium pentobarbital, the abdominal expected that an animal inhabiting an arid environ- cavity opened, and the dorsal aorta cannulated.