Comparison of renal and salt gland function in three species of wild ducks
Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
* Author for correspondence (e-mail: dcbennet{at}interchange.ubc.ca)
Accepted 23 June 2003
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: osmoregulation, kidney, salt gland, mallard, Anas platyrhynchos, canvasback, Aythya valisineria, Barrow's goldeneye, Bucephala islandica
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Three processes central to osmoregulation in marine birds are filtration of
sodium (Na+) and water from the plasma by the kidneys, reabsorption
of filtered water and Na+ by cells along the renal tubules, and
secretion of Na+ by the salt glands. These processes must have
evolved simultaneously to adapt to the osmoregulatory requirements of birds
that use habitats of widely disparate salinities, ranging from freshwater to
full-strength seawater. Renal filtration of marine birds is unaffected by
either acclimation to saline or acute saline loading and almost all the
filtered Na+ (and water) is reabsorbed along the renal tubules,
regardless of plasma [Na+]
(Hughes, 1995). The reabsorbed
Na+ can be secreted by the salt glands in less water than was
imbibed with it. The concentration and rate of salt gland secretion determines
the amount of osmotically free water it can generate for the birds' other
physiological processes (Schmidt-Nielsen,
1960
).
Many species of ducks switch seasonally between freshwater and saline
habitats. When the drinking water of Pekin ducks is changed from freshwater to
saline, their salt glands hypertrophy, enhancing their capacity to excrete
salt (Schmidt-Nielson and Kim,
1964), but the glomerular filtration rate (GFR) is little affected
(Holmes et al., 1968
) and the
fractional reabsorption of Na+ is reduced
(Holmes et al., 1968
;
Hughes et al., 1989
). Whether
these responses occur in wild ducks has not been reported.
Therefore, in this study, we compared simultaneous kidney and salt gland
function in three species of ducks: freshwater mallards (tribe Anatini,
Anas platyrhynchos), estuarine canvasbacks (tribe Aythyini, Aythya
valisineria) and marine Barrow's goldeneyes (tribe Mergini, Bucephala
islandica). Goldeneyes, the most saline-tolerant, have larger kidney mass
(Kalisiska et al.,
1999
; D. C. Bennett and M. R. Hughes, unpublished data) and
extracellular fluid volume (Bennett,
2002
) than mallards, the least saline-tolerant species.
Canvasbacks have large kidneys like the goldeneyes (D. C. Bennett and M. R.
Hughes, unpublished data), but a smaller extracellular fluid volume, like the
mallards (Bennett, 2002
). Water
flux rates of all three species (Bennett,
2002
) are roughly twice the rate predicted allometrically for
seabirds (Hughes et al., 1987
;
Nagy and Peterson, 1988
). We
hypothesize that (1) neither saline acclimation nor acute saline loading
affect GFR in any of the three species, and (2) saline tolerance is determined
by the efficiency of renal tubular reabsorption of water and Na+,
and secretion of Na+ by the salt glands.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Experiments
These experiments followed the guidelines set forth by the Canadian Council
on Animal Care. Each duck was fasted overnight and weighed. Venous catheters
were placed in the left and right tibiotarsal veins (for infusion of saline
and markers and for blood sampling, respectively) and were kept patent with
heparinized isotonic saline. The duck's wings were lightly bound to the body
with Velcro straps and the bird was placed on a foam-lined restrainer. The
duck's head projected into a large funnel that directed SGS into preweighed
glass vials. The SGS of poor secretors was collected by capillary tube. A
cannula inserted into the cloaca diverted ureteral urine into a preweighed
plastic tube.
An initial 1 ml blood sample was taken and the duck was given a priming injection of 37 kBq of 14C-inulin (marker for GFR) and 370 kBq of 3H-para-aminohippuric acid (3H-PAH; marker for effective renal plasma flow, ERPF). An infusion of 75 mmol l1 NaCl, containing 0.15 kBq ml1 of 14C-inulin and 1.1 kBq ml1 of 3H-PAH, was begun (0.175 ml min1). After a 1 h equilibration period, four 1015 min urine samples were collected. Then infusate NaCl concentration was increased to 500 mmol l1 and urine was collected at 1020 min intervals until the duck began to secrete. Four simultaneous 1020 min collections of urine and SGS were made. Finally, infusate NaCl concentration was reduced to 75 mmol l1 and three simultaneous 1020 min collections of urine and SGS were made. Urine and SGS volumes were determined by weighing their tubes before and after the collection period. A blood sample (0.4 ml) was taken at the mid-point of each collection period.
Blood, urine and SGS samples were centrifuged for 3 min at 15 600 g and the supernatant fluids were transferred into 1.5 ml centrifuge tubes and stored at 20°C until assayed. Plasma, urine and infusate 3H and 14C concentrations were determined using a Beckman LS 6500 liquid scintillation counter (Fullerton CA, USA). Determinations of [Na+] and [K+] of plasma, urine and SGS were made by cesium internal standard flame photometry (Model 943, Instrumentation Laboratory S.p.A, Milano, Italy); and osmolality (Osm) of the plasma and urine by vapor pressure osmometry (Model 5500; Wescor Inc., Logan UT, USA). Subscripts pl, u and sgs designate plasma, urine and salt gland secretion, respectively.
Calculations and statistics
All calculations are as described in Pitts
(1968) and Goldstein
(1993
). GFR and ERPF were
calculated as:
![]() |
![]() |
![]() |
![]() |
All analyses and calculations were made on each sample collected and were, within individuals, averaged for each infusate, so that each infusate period for an individual duck is represented by a single value. The 500 mmol l1 NaCl infusion was divided into two periods: prior to secretion and active secretion. Data are reported as means ± standard errors (S.E.M.) and statistically analyzed using SYSTAT 9 for Windows (SPSS Science, Chicago, IL, USA). Differences among species and infusion periods and between treatments and sexes were assessed by repeated-measures analysis of variance (ANOVA). Significance is claimed at P<0.05, although higher P values suggesting trends are also reported. Relationships among variables were examined using correlation and stepwise linear regression.
To examine the relationships of GFR to habitat and diet of birds, we collected GFR data on 27 species of adult non-dehydrated birds, disregarding the methods used to measure GFR (Table 1). Data were obtained from original sources whenever possible. For each species we calculated a single data point that is the mean of all reported values. GFR was standardized by regressing it on body mass, after log10log10 transformation, and analysing the residuals by ANOVA.
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
Kidney function
GFR was significantly greater in goldeneyes than in either mallards or
canvasbacks (P<0.005) and differed between freshwater and
saline-acclimated ducks only in canvasbacks
(Fig. 4), due mainly to lower
GFR in freshwater females. GFR did not vary among the infusion periods in any
species (P>0.5). ERPF was significantly lower in canvasbacks than
in either mallards or goldeneyes (P<0.008). When ducks were
infused with hypertonic saline, ERPF increased only in mallards
(P<0.03; Fig. 4).
Neither saline acclimation nor sex affected ERPF.
|
Fractional reabsorption of water and Na+ varied significantly among the three species (P<0.02 and P<0.0004, respectively; Fig. 5). They were highest in goldeneyes, lowest in canvasbacks and intermediate in mallards (Fig. 5). Fractional reabsorption of water and Na+ of mallards was not affected by saline acclimation, sex or infusate concentration, but both tended to be higher in saline-acclimated canvasbacks (P<0.08 and P<0.01, respectively), due almost exclusively to the low values of one freshwater female. In goldeneyes, fractional reabsorption of water increased (P<0.005) and reabsorption of Na+ decreased (P<0.002) with infusion period (Fig. 5). Fractional reabsorption of K+ did not differ among or within species, except that it was significantly lower in freshwater mallards during the final infusion of 75 mmol l1 NaCl (Fig. 5). Goldeneyes had lower UFR than either mallards or canvasbacks (P<0.01). UFR was affected by saline only in canvasbacks, and was lower in saline-acclimated ducks (P=0.04) and reduced by saline infusion in freshwater ducks (P<0.01; Fig. 4).
|
Overall, Osmu (Fig. 1) and [K]u (Fig. 3), but not [Na]u (Fig. 2), varied among species (P=0.0007, P=0.0005 and P=0.14, respectively). Goldeneyes had the highest Osmu and [K]u and, together with canvasbacks, the lowest [Na]u. Canvasbacks also have the lowest Osmu and [K]u. Osmu, [Na]u and [K]u varied significantly among infusion periods (all P<0.00001; Figs 1, 2, 3), but only Osmu varied between treatments (P=0.04), due primarily to lower Osmu of freshwater canvasbacks (Fig. 1). During hypertonic saline infusion, all three species significantly increased Osmu and it remained high during active salt secretion. [Na]u and [K]u increased in mallards and goldeneyes regardless of their drinking water regime. In canvasbacks, only freshwater ducks increased [Na]u and none increased [K]u.
Urine flow rate is correlated to both GFR and fractional reabsorption of
water (FRH2O) in all three species
(Fig. 6). UFR and GFR were
positively correlated in mallards and goldeneyes, but not in canvasbacks
(Fig. 6). Stepwise linear
regression indicated that UFR of mallards and goldeneyes was predicted by a
combination of both GFR and FRH2O:
![]() |
![]() |
![]() |
|
Salt gland function
The time required to initiate secretion did not vary among the species
(P=0.12) nor was it affected by treatment (P=0.89) or sex
(P=0.35). It required 59.3±3.8 min (N=24 ducks) of
infusion (500 mmol l1 NaCl at 0.175 ml
min1) to initiate secretion. Freshwater mallards and one
freshwater female canvasback produced only a trace of SGS.
[Na+]sgs did not vary among the species
(P=0.56) or between the sexes (P=0.23). Saline acclimation
increased [Na+]sgs of mallards and goldeneyes
(P=0.04 and P=0.01, respectively), but not of canvasbacks
(P=0.25; Fig. 7). Salt
gland secretion rate varied among species (P=0.0003;
goldeneyes>mallards> canvasbacks) and was increased by saline
acclimation only in mallards (Fig.
7).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Kidney function
Saline acclimation and acute saline loading have little effect on GFR of
ducks (Holmes et al., 1968;
Hughes, 1980
; Hughes et al.,
1989
,
1999
;
Fig. 4) or other species with
salt glands (Douglas, 1966
;
Hughes, 1995
). GFR of
goldeneyes is roughly twice that of mallards, canvasbacks and Pekin ducks
(Table 1,
Fig. 4), but is similar to that
of other marine birds (gulls; Douglas,
1966
; Hughes,
1980
,
1995
;
Hughes et al., 1993
). The
Canada goose Branta canadensis, the most terrestrial of the
anseriforms studied to date, has the lowest GFR
(Hughes, 1980
). This suggests
that birds well adapted to highly saline water have higher GFR, and that GFR
may vary among habitat types. We examined the generality of this relationship
by comparing GFR of 27 species of adult birds for which data are available
(Table 1). GFR varied
significantly among birds from different habitat types (P=0.02; Figs
8,
9). Marine species had a
significantly higher GFR (P=0.02) and terrestrial arid species had a
significantly lower GFR (P=0.05) than species from either terrestrial
mesic or freshwater habitats, which did not differ significantly from each
other (P=0.9).
|
|
Yokota et al. (1985)
identified the need to eliminate water loads and metabolic wastes as the major
factors that tend to increase GFR among vertebrates. The results of the
preceding analysis support this hypothesis. The high GFR of marine birds is
consistent with their larger kidneys
(Hughes, 1970
;
Kalisi
ska et al.,
1999
), greater water flux
(Hughes et al., 1987
;
Nagy and Peterson, 1988
;
Bennett, 2002
) and
Na+ flux (Goldstein and
Bradshaw, 1998a
; Goldstein,
2002
) and larger extracellular fluid volumes
(Bennett, 2002
).
Marine birds are carnivorous and should presumably excrete large amounts of
urates. Whether these patterns reflect adaptations to a marine environment
and/or effects of a carnivorous diet have not yet been examined. Only one
terrestrial avian carnivore, the American kestrel Falco sparverius,
has been studied and it has a low GFR
(Lyons and Goldstein, 2002;
Table 1) and small kidneys,
like other birds that lack salt glands
(Hughes, 1970
). We found no
relationship between diet and GFR, standardized to body mass (P=0.58;
Table 1). Large renal mass and
a high rate of body fluid filtration appear to be adaptations to the saline
environment. Studies on terrestrial avian carnivores, including Falconiform
birds that have salt glands (Cade and
Greenwald, 1966
), might clarify these relationships.
Goldeneyes, the most marine of the three duck species, have the highest
fractional reabsorption of water and Na+
(Fig. 5), thus a low UFR
(Fig. 4) and
[Na+]u (Fig.
2). They significantly increased the fractional reabsorption of
water and decreased the fractional reabsorption of Na+ when infused
with hypertonic saline (Fig.
5), as did gulls (Hughes,
1995). In contrast, mallards had a lower fractional reabsorption
of water and Na+ (Fig.
5) and produced a greater volume of urine
(Fig. 4) that had a higher
[Na+] (Fig. 2).
Although canvasbacks produced a large volume of urine like mallards
(Fig. 4), they had a low
[Na+]u like goldeneyes
(Fig. 2). Saline infusion did
not affect fractional reabsorption of water and Na+ in mallards and
canvasbacks (Fig. 5).
Birds can adjust UFR by two mechanisms: they may vary the rate of fluid
delivery to the renal tubules (GFR) and/or adjust tubular water reabsorption.
Neither GFR nor fractional water reabsorption of the three species of wild
ducks were much affected by saline acclimation or by acute saline loading
(Figs 4,
5). With the exception of
female freshwater canvasbacks, both mechanisms regulated urine flow of ducks
equally well (Fig. 6). Chickens
(Wideman, 1988), red
wattlebirds Anthochaera carunculata
(Goldstein and Bradshaw,
1998b
) and kestrels (Lyons and
Goldstein, 2002
) also use both mechanisms to adjust urine flow.
Fractional reabsorption of water is considered the more important regulator of
urine flow in wattlebirds (Goldstein and
Bradshaw, 1998b
) and probably Chukars Alectoris chukar
(Goldstein, 1990
).
ERPF of mallards and goldeneyes (Fig.
4) is similar to ERPF of gulls
(Raveendran, 1987) and galahs
(Roberts, 1991b
), but lower
than that of Pekin ducks, chickens and quail
(Table 1). Canvasbacks
(Fig. 4) have the lowest ERPF
of any avian species studied, while domesticated varieties of birds (chicken
and Pekin duck) have the highest ERPF
(Table 1). We found no
relationship between ERPF (Table
1), standardized to body mass
(Fig. 8), and habitat
(P=0.92; Fig. 9).
Species differences in ERPF do not suggest any significant pattern, as other
attributes of avian osmoregulation, such as water flux, extracellular fluid
volume and kidney size, appear to do.
Salt gland function
[Na+]sgs, of saline infused ducks, did not differ
among the three species, and was higher following saline acclimation only in
mallards and goldeneyes (Fig.
7). Salt gland secretion rate did differ among the three species
and was highest in goldeneyes (Fig.
7). Only goldeneyes secreted all the infused Na+
via their salt glands. Goldeneyes were able to drink 550 mmol
l1 NaCl without changing water intake, yet never secreted
when handled during saline acclimation
(Bennett, 2002).
Saline-acclimated mallards did excrete all infused Na+, but
incorporated renal excretion to do so. Canvasbacks were unable to excrete all
the infused Na+. At salinities above 225 mmol l1
NaCl, mallards decreased water flux (drinking), but canvasbacks tolerated 450
mmol l1 NaCl with no change in water flux
(Bennett, 2002
). The SGS of
saline infused canvasbacks is more concentrated than their drinking water, yet
is produced at a low rate (Fig.
7). Their limited extrarenal Na+ excretion, together
with their low renal Na+ excretion
(Fig. 2), suggest they should
be unable to eliminate all the Na+ they ingested
(Bennett, 2002
). Nevertheless,
they tolerated 450 mmol l1 NaCl
(Bennett, 2002
). How they did
so, despite their apparently limited ability to excrete Na+,
remains unresolved, but may involve water and Na+ transport by the
anterior and posterior segments of the intestinal tract.
This paradox could be satisfied if the gut did not absorb all the ingested
Na+. There is some evidence that this may be so. Pekin ducks drink
approximately 225 ml kg1 day1
(Fletcher and Holmes 1968;
Bennett et al., 2003
). If they
drink 300 mmol l1 NaCl, their estimated Na+ flux
would be 67.5 mmol l1 kg1
day1, but Na+ flux measured by 22Na
turnover was only 21.4 mmol l1 kg1
day1 (Roberts and
Hughes, 1984
). We are currently examining Na+ balance
in the three species of ducks used in this study.
Many species of birds modify their urine in the lower intestinal tract to
conserve water and/or Na+. For example, water and Na+
excretion rates of chickens (Skadhauge,
1968) and quail (Anderson and
Braun, 1985
) are higher in ureteral urine than in voided urine
(cloacal fluid). Schmidt-Nielson et al.
(1963
) suggested that birds
with salt glands might reabsorb Na+ and water from the urine in the
lower intestinal tract. By secreting the reabsorbed Na+
extrarenally in less water than was absorbed with it, they could generate
osmotically free water. Postrenal modification of urine has the potential to
play an important osmoregulatory role in ducks. Pekin ducks
(Hughes and Raveendran, 1994
)
and mallards (Hughes et al.,
1999
) reflux urine into their hindgut. Mallards reflux about 20%
of their urine, regardless of drinking water salinity
(Hughes et al., 1999
). The
capacity for Na+ uptake in the hindgut of Pekin ducks is only
slightly diminished by saline acclimation
(Skadhauge et al., 1984
), and
their cloacal fluid (Hughes et al.,
1992
) is more concentrated than their urine
(Hughes et al., 2003
).
Postrenal modification of urine may help explain the inconsistencies in
osmoregulatory responses of canvasback ducks.
Morphology
It is interesting to speculate on the morphological basis for the
differences in kidney and salt gland function observed in this study. The
larger kidneys and GFR of goldeneyes, and marine birds in general, presumably
reflect an increased number of glomeruli. But whether the higher fractional
reabsorption of water and Na+
(Fig. 5) and
urine-concentrating capacity (Fig.
1) is due to a higher proportion of mammalian-type nephrons and
fewer reptilian-type nephrons is not known. The proportion of kidney mass
composed of medullary cones is high in marine species
(Goldstein and Braun, 1989;
Goldstein, 1993
), which
presumably reflects a high proportion of mammalian-type nephrons. Wideman and
Nissley (1992
) found that
domestic chickens that thrived on saline drinking water had higher ratios of
mammalian-type to reptilian-type nephron as compared to those that lost body
mass.
Staaland (1967) examined
the anatomical basis for variations in salt gland function in Charadriiform
birds. He found that the SGS concentration was correlated with the length of
the secretory tubule. Although SGS rate was not measure in that study,
Staaland (1967
) suggested that
salt gland size, and presumably the number of lobules, determines SGS flow
rate. Given that we found SGS flow rate and not [Na+]SGS
differed among the three species measured in this study
(Fig. 7), it could be argued
that goldeneyes have relatively larger salt glands, containing more lobules,
than either mallards or canvasbacks, but all three species have similar
lobular anatomy (secretory tubule length).
Conclusions
We hypothesized that (1) neither saline acclimation nor acute saline
loading affect GFR in any of the three species, and (2) saline tolerance is
determined by the efficiency of renal tubular reabsorption of water and
Na+, and secretion of Na+ by the salt glands. The
results support both hypotheses. Goldeneyes, the most marine species, had the
highest rates of filtration (GFR), fractional reabsorption of water and
Na+, and salt gland Na+ excretion and were the only
species that secreted all the infused Na+ via the salt
glands. Rates of these processes were all lower in mallards, the most
freshwater species. However, the high volume and Na+ concentration
of urine of saline-acclimated mallards, coupled with extrarenal Na+
secretion, eliminated all the infused Na+. If mallards infused with
500 mmol l1 NaCl can excrete all infused Na+, why
can they not drink greater than 300 mmol l1 NaCl? In
contrast, canvasbacks were unable to to excrete all the infused
Na+, yet tolerated higher drinking water salinities than mallards
(Bennett, 2002). This suggests
that osmoregulation of canvasbacks involves levels of Na+ and water
regulation by organs other than the kidneys and the salt glands. It may be
that the intestinal tract plays an important role in conservation of water in
canvasbacks.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Anderson, G. L. (1980). Kidney function and postrenal modification of urine in desert quail. PhD thesis, University of Arizonia, USA. pp. 187.
Anderson, G. L. and Braun, E. J. (1985). Postrenal modification of urine in birds. Am. J. Physiol. 248,R93 -R98.[Medline]
Bennett, D. C. (2002). Effect of saline intake on osmotic homeostasis in ducks. PhD thesis, University of British Columbia, Vancouver, Canada. pp. 114.
Bennett, D. C., Gray, D. A. and Hughes, M. R. (2003). Effect of saline intake on water flux and osmotic homeostasis in Pekin ducks (Anas platyrhynchos). J. Comp. Physiol. B 173,27 -36.[Medline]
Bennett, D. C., Hughes, M. R., Elliott, J. E., Scheuhammer, A. M. and Smits, J. E. (2000). Effect of cadmium on Pekin duck total body water, water flux, renal filtration, and salt gland function. J. Toxicol. Environ. Health A 59, 43-56.[CrossRef][Medline]
Berger, L., Yu, T. F. and Gutman, A. B. (1960).
Effects of drugs that alter uric acid excretion in man on uric acid clearance
in the chicken. Am. J. Physiol.
198,575
-580.
Bradley, E. L. and Holmes, E. L. (1971). The effects of hypophysectomy on adrenocortical function in the duck (Anas platyrhynchos). J. Endocrinol. 49,437 -457.[Medline]
Braun, E. J. (1976). Intrarenal blood flow
distribution in the desert quail following salt loading. Am. J.
Physiol. 231,1111
-1118.
Braun, E. J. (1978). Renal resonse of the starling. Am. J. Physiol. 234,F270 -F278.[Medline]
Braun, E. J. and Dantzler, W. H. (1972).
Function of mammalian-type and reptilian-type nephrons in kidney of desert
quail. Am. J. Physiol.
222,617
-629.
Braun, E. J. and Dantzler, W. H. (1974).
Effects of ADH on single-nephron glomerular filtration rates in the avian
kidney. Am. J. Physiol.
226, 1-8.
Braun, E. J. and Dantzler, W. H. (1975).
Effects of water load on renal glomerular and tubular function in desert
quail. Am. J. Physiol.
229,222
-228.
Cade, T. J. and Greenwald, L. (1966). Nasal salt gland in falconiform birds. Condor 68,338 -350.
Chan, M. Y., Bradley, E. L. and Holmes, W. N. (1972). The effects of hypophysectomy on the metabolism of adrenal steroids in the pigeon (Columba livia). J. Endocrinol. 52,435 -450.[Medline]
Clark, N. B. and Wideman, R. F., Jr (1980). Calcitonin stimulation of urine flow and sodium excretion in the starling. Am. J. Physiol. 238,R406 -R412.[Medline]
Dantzler, W. H. (1966). Renal response of
chickens to infusion of hypertonic sodium chloride solution. Am. J.
Physiol. 210,640
-646.
Dawson, T.J., Maloney, S. K. and Skadhauge, E. (1991). The role of the kidney in electrolyte and nitrogen excretion in a large flightless bird, the emu, during different osmotic regimes, including dehydration and nesting. J. Comp. Physiol. B 161,165 -171.
Douglas, D. S. (1966). Low urine salt concentrations in salt loaded gulls. Physiologist 9, 171.
Fletcher, G. L. and Holmes, W. N. (1968). Observations on the intake of water and electrolytes by the duck (Anas platyrhynchos) maintained on freshwater and on hypertonic saline. J. Exp. Biol. 49,325 -329.
Gerstberger, R., Kaul, R., Gray, D. A. and Simon E. (1985). Arginine vasotocin and glomerular filtration rate in salt-acclimated ducks. Am. J. Physiol. 248,F663 -F667.[Medline]
Glahn, R. P., Wideman, R. F., Jr and Cowen, B. S. (1988a). Effect of dietary acidification and alkalinization on urolith formation and renal function in single comb white leghorn laying hen. Poult. Sci. 67,1694 -1701.[Medline]
Glahn, R. P., Wideman, R. F., Jr and Cowen, B. S. (1988b). Effect of gray strain infectious bronchitis virus and high dietary calcium on renal function of single comb white leghorn pullets at 6, 10, and 18 weeks of age. Poult. Sci. 67,1250 -1263.[Medline]
Goldstein, D. L. (1990). Effects of different sodium intakes on renal and cloacal sodium excretion in chukars (Aves: Phasianidae). Physiol. Zool. 63,408 -419.
Goldstein, D. L. (1993). Renal response to saline infusion in chicks of Leach's storm petrels (Oceanodroma leucorhoa). J. Comp. Physiol. B 163,167 -173.
Goldstein, D. L. (2002). Water and salt blance in seabirds. In Biology of Marine Birds (ed. E. A. Schreiber and J. Burger), pp. 467-483. London: CRC Press.
Goldstein, D. L. and Bradshaw, S. D. (1998a). Regulation of water and sodium balance in the field by Australian Honeyeaters (Aves: Meliphagidae). Physiol. Zool. 71,214 -225.[Medline]
Goldstein, D. L. and Bradshaw, S. D. (1998b). Renal function in red wattlebirds in response to varying fluid intake. J. Comp. Physiol. B 168,265 -272.[CrossRef]
Goldstein, D. L. and Braun, E. J. (1988). Contributions of the kidneys and intestines to water conservation, and plasma levels of antidiuretic hormone, during dehydration in house sparrows (Passer domesticus). J. Comp. Physiol. B 158,353 -361.[Medline]
Goldstein, D. L. and Braun, E. J. (1989). Structure and concentrating ability in the avian kidney. Am. J. Physiol. 256,R501 -R509.[Medline]
Goldstein, D. L. and Rothschild, E. L. (1993). Daily rhythms in rates of glomerular filtration and cloacal excretion in captive and wild song sparrows (Melospiza melodia). Physiol. Zool. 66,708 -719.
Gray, D. A. and Eramus, T. (1988). Glomerular filtration changes during vasotocin-induced antidiuresis in kelp gull. Am. J. Physiol. 255,R936 -R939.[Medline]
Gregg, C. M. and Wideman, F. R., Jr (1990). Morphological and functional comparisons of normal and hypertrophied kidneys of adult domestic fowl (Gallus gallus). Am. J. Physiol. 258,F403 -F413.[Medline]
Harriman, A. E. (1967). Laughing gulls offered saline in preference and survival tests. Physiol. Zool. 49,273 -278.
Holmes, W. N. and Adams, B. M. (1963). Effects of adrenocortical and neurohypophysiol hormones on the renal excretory pattern in the water-loaded duck (Anas platyrhynchos). Endocrinol. 73,5 -10.[Medline]
Holmes, W. N., Fletcher, G. L. and Stewart, D. J. (1968). The patterns of renal electrolyte excretion in the duck (Anas platyrhynchos) maintained on freshwater and on hypertonic saline. J. Exp. Biol. 45,487 -508.
Hughes, M. R. (1970). Relative kidney size in nonpasserine birds with salt glands. Condor 72,164 -168.
Hughes, M. R. (1980). Glomerular filtration rate in saline acclimated ducks, gulls and geese. Comp. Biochem. Physiol. 65A,211 -213.[CrossRef]
Hughes, M. R. (1995). Responses of gull kidneys and salt glands to NaCl-loading. Can. J. Physiol. Pharmacol. 73,1727 -1732.[Medline]
Hughes, M. R., Bennett, D. C., Gray, D. A., Sharp, P. J., Elliott, J. E. and Scheuhammer, A. M. (2003). Effects of cadmium ingestion on plasma and osmoregulatory hormone concentrations in male and female Pekin ducks. J. Toxicol. Environ. Health A 66, 71-85.
Hughes, M. R., Bennett, D. C., Sullivan, T. M. and Hwang, H. (1999). Retrograde movement of urine into the gut of salt water acclimated Mallards (Anas platyrhynchos). Can. J. Zool. 77,342 -346.[CrossRef]
Hughes, M. R., Goldstein, D. L. and Raveendran, L. (1993). Osmoregulatory responses of Glaucous-winged gulls (Larus glaucescens) to dehydration and hemorrhage. J. Comp. Physiol. B 163,524 -531.[Medline]
Hughes, M. R., Kojwang, D. and Zenteno-Savin, T. (1992). Effects of cecal ligation and saline acclimation on plasma concentration and organ mass in male and female Pekin ducks, Anas platyrhynchos. J. Comp. Physiol. B 162,625 -631.
Hughes, M. R. and Raveendran, L. (1994). Ion and luminal marker concentrations in the gut of saline-acclimated ducks. Condor 96,295 -299.
Hughes, M. R., Roberts, J. R. and Thomas, B. R. (1987). Total body water and its turnover in free-living nestling Glaucous-winged gulls with a comparison of body water and water flux in avian species with and without salt glands. Physiol. Zool. 60,481 -491.
Hughes, M. R., Roberts, J. R. and Thomas, B. R. (1989). Renal function in freshwater and chronically saline-stressed male and female Pekin ducks. Poult. Sci. 68,408 -416.[Medline]
Hyden, S. and Knutson, P.-G. (1959). Renal clearance and distribution volume of polyethylene glycol and inulin in the chicken. Kungl. Lantbrukshögskolans. Annaler. 25,253 -259.
Kalisiska, E., Da
czak, A., Pierko, M. and
Wysocki, D. (1999). Relationships between kidney mass and
body size in some Anseriformes. Anat. Histol. Embryol.
28, 55-59.[CrossRef][Medline]
Korr, I. M. (1939). The osmotic function of the chicken kidney. J. Cell. Comp. Physiol. 13,175 -193.
Krag, B. and Skadhauge, E. (1972). Renal salt and water excretion in the budgerygah (Melopsittacus undulates). Comp. Biochem. Physiol. 41A,667 -683.[CrossRef]
Laverty, G. and Dantzler, W. H. (1982). Micropuncture of superficial nephrons in avian (Sturnus vulgaris) kidney. Am. J. Physiol. 243,F561 -F569.[Medline]
Laverty, G. and Dantzler, W. H. (1983). Micropuncture study of urate transport by superficial nephrons in avian (Sturnus vulgaris) kidney. Pflüg. Arch. 397,232 -236.[Medline]
Laverty, G. and Wideman, R. F., Jr (1989). Sodium excretion rates and renal responses to acute salt loading in the European starling. J. Comp. Physiol. B 259,401 -408.
Leary, A. M., Roberts, J. R. and Sharp, P. J. (1998). The effect of infusion of hypertonic saline on glomerular filtration rate and arginine vasotocin, prolactin and aldosterone in the domestic chicken. J. Comp. Physiol. B 168,313 -321.[Medline]
Lyons, M. E. and Goldstein, D. L. (2002). Osmoregulation by nestling and adult American Kestrels (Falco sparverius) Auk 119,426 -435.
Nagy, K. A. and Peterson, C. C. (1988). Scaling of water flux rate in animals. Univ. Calif. Publ. Zool. 120.
Nechay, B. R. and Nechay, L. (1959). Effects of probenicid, sodium salicylate, 2,4-dinitrophenol and pyrazinamide on renal secretion of uric acid in chickens. J. Pharmacol. Exp. Ther. 126,291 -295.[Medline]
Orloff, J. and Davidson, D. G. (1959). The mechanism of potassium secretion in the chicken. J. Clin. Invest. 38,21 -30.[Medline]
Palmore, W. P., Fregly, M. J. and Simpson, C. F. (1981). Catecholamine-mediated diuresis in turkeys. Proc. Soc. Exp. Biol. Med. 167, 1-5.
Pitts, R. F. (1938). The excretion of phenol red by chickens. J. Cell. Comp. Physiol. 11, 99-115.
Pitts, R. F. (1968). Physiology of the Kidney and Body Fluids. 2nd Edition. Chicago, IL, USA: Year Book Medical Publishers Inc.
Pitts, R. F. and Korr, I. M. (1938). The excretion of urea by the bird. J. Cell. Comp. Physiol. 11,117 -122.
Radin, M. J., Hoepf, T. M. and Swayne, D. E. (1993). Use of a single injection solute clearance method for the determination of glomerular filtration rate and effective renal plasma flow in chickens. Lab. Animal Sci. 43, 594-596
Raveendran, L. (1987). The effect of intravenous salt loading on osmoregulation of hydrated Glaucous-winged gulls, Larus glaucescens. MSc thesis, University of British Columbia, Vancouver, Canada.
Roberts, J. R. (1991a). Effects of water deprivation on renal function and plasma arginine vasotocin in the feral chicken, Gallus gallus (Phasianidae). Aust. J. Zool. 39,439 -446.
Roberts, J. R. (1991b). Renal function and plasma arginine vasotocin during water deprivation in an Australian parrot, the galah (Cacatua roseicapilla). J. Comp. Physiol. 161B,620 -625.
Roberts, J. R. (1992). Renal function and plasma arginine vasotocin during an acute salt load in feral chickens. J. Comp. Physiol. 162B,54 -58.
Roberts, J. R., Baudinette, R. V. and Wheldrake, J. F. (1985). Renal clearance studies in Stubble Quail coturnix pectoralis and King Quail Coturnix chinensis under conditions of hydration, dehydration, and salt loading. Physiol. Zool. 58,340 -349.
Roberts, J. R. and Dantzler, W. H. (1989). Glomerular filtration rate in conscious unrestrained starlings under dehydration. Am. J. Physiol. 256,R836 -R839[Medline]
Roberts, J. R. and Dantzler, W. H. (1992). Micropuncture study of avian kidney effect of prolactin. Am. J. Physiol. 262,R933 -R937.[Medline]
Roberts, J. R. and Hughes, M. R. (1983). Glomerular filtration rate and drinking rate in Japanese Quail, Coturnix coturnix japonica, in response to acclimation to saline water. Can. J. Zool. 61,2394 -2398.
Roberts, J. R. and Hughes, M. R. (1984). The effects of hypertonic sodium chloride injection on body water distribution in ducks (Anas platyrhynchos), gulls (Larus glaucescens), and roosters (Gallus domesticus). Comp. Biochem. Physiol. 52A,21 -28.[CrossRef]
Sanner, E. (1965). Studies on biogenic amines and reserpine induced block of the diuretic action of hydrochlorothiazide and theophylline in the chicken. Acta. Pharmacol. Toxicol. 22(Suppl 1),386 .
Schmidt-Nielsen, K. (1960). The salt-secreting gland of marine birds. Circulation 21,955 -967.
Schmidt-Nielsen, K., Borut, A., Lee, P. and Crawford, E., Jr (1963). Nasal salt excretion and the possible function of the cloaca in water conservation. Science 142,1300 -1301.[Medline]
Schmidt-Nielsen, K. and Kim, Y.-T. (1964). The effect of salt intake on the size and function of the salt glands in ducks. Auk 81,160 -172.
Schütz, H., Gray, D. A. and Gerstberger, R. (1992). Modulation of kidney function in conscious Pekin ducks by atrial natriuretic factor. Endocrinol. 130,678 -684.[Abstract]
Shannon, J. A. (1938a). The excretion of exogenous creatinine by the chicken. J. Cell. Comp. Physiol. 11,123 -134.
Shannon, J. A. (1938b). The excretion of uric acid by the chicken. J. Cell. Comp. Physiol. 11,135 -148.
Shideman, J. R., Evans, R. L., Bierer, D. W. and Quebbemann, A. J. (1981). Renal venous portal contribution to PAH and uric acid clearance in the chicken. Am. J. Physiol. 240,F46 -F53.[Medline]
Shoemaker, V. H. (1967). Renal function in the morning dove. Am. Zool. 7, 736.
Simon, E. and Gray, D. A. (1991). Control of renal handling of potassium loads in ducks with active salt glands. Am. J. Physiol. 261,R231 -R238.[Medline]
Singh, D. S. and Bhattacharyya, N. K. (1983). Renal function in Hy-line layers fed sal-meal diets. Indian J. Anim. Sci. 53,349 -350.
Skadhauge, E. (1964). The effect of unilateral infusion of arginine vasotocin into the portal circulation of the avian kidney. Acta. Endocrinol. (Copenhagen) 47,3221 -330.
Skadhauge, E. (1968). The cloacal storage of urine in the rooster. Comp. Bichem. Physiol. 24, 7-18.[CrossRef][Medline]
Skadhauge, E. and Schmidt-Nielson, B. (1967).
Renal function in domestic fowl. Am. J. Physiol.
212,793
-798.
Skadhauge, E., Munck, B. G. and Rice, G. E. (1984). Regulation of NaCl and water reabsorption in duck intestine. In Lecture Notes on Coastal and Estuarine Studies, Vol. 9. Osmoregulation in estuarine and marine animals (ed. A. Pequeux, R. Gilles and L. Bolis), pp. 131-142. New York: Springer-Verlag.
Sperber, I. (1960). Excretion. In Biology and Physiology of Birds, Vol.1 (ed. A. J. Marshall), pp.469 -492. London: Academic Press.
Staaland, H. (1967). Anatomical and physiological adaptations of the nasal glands in Charadriiformes birds. Comp. Biochem. Physiol. 23,933 -944.[CrossRef][Medline]
Svendsen, C. and Skadhauge, E. (1976). Renal function in hens fed graded levels of ochratoxin A. Acta Pharmacol. Toxicol. 38,186 -194.[Medline]
Sykes, A. H. (1960a). The renal clearance of uric acid and p-amino hippurate in the fowl. Res. Vet. Sci. 1,308 -314.
Sykes, A. H. (1960b). The excretion of inulin, creatine and ferrocyanide by the fowl. Res. Vet. Sci. 1, 315-320.
Thomas, D. H. and Phillips, J. G. (1975). Studies in avian adrenal steroid function III: Adrenalectomy and the renal-cloacal response in water-loaded domestic ducks (Anas platyrhynchos L.). Gen. Comp. Endocrinol. 26,412 -419.
Vena, V. E., Lac, T. H. and Wideman, R. F., Jr (1990). Dietary sodium, glomerular filtration rate autoregulation, and glomerular size distribution profiles in domestic fowl (Gallus gallus). J. Comp. Physiol. B 160, 7-16.
Vogel, G., Stoeckert, I., Kroger, W. and Dobberstein, I. (1965). Harn und Harnbereitung bei terrestrisch lebenden Vögeln: Untersuchungen am Truthuhn (Meleagris pavo L.). Zentralbl. Veterinarmed. Reihe A 12,132 -160.
Walter, A. and Hughes, M. R. (1978). Total body water volume and turnover rate in fresh water and sea water adapted Glaucous-winged gulls, Larus glaucescens. Comp. Biochem. Physiol. 61A,233 -237.[CrossRef]
Wideman, R. F., Jr (1988). Avian kidney anatomy and physiology. CRC Crit. Rev. Poult. Biol. 1, 133-176.
Wideman, R. F., Jr, Clark, N. B. and Braun, E. J. (1980). Effects of phosphate loading and parathyroid hormone on starling renal phosphate excretion. Am. J. Physiol. 239,F233 -F243.[Medline]
Wideman, R. F., Jr and Gregg, C. M. (1988). Model for evaluating avian renal hemodynamics and glomerular filtration rate autoregulation. Am. J. Physiol. 254,R925 -R932.[Medline]
Wideman, R. F., Jr and Laverty, G. (1986). Kidney function in domestic fowl with chronic occlusion of the ureter and caudal renal vein. Poult. Sci. 65,2148 -2155.[Medline]
Wideman, R. F., Jr and Nissley, A. C. (1992). Kidney structure and responses of two commercial single comb white leghorn strains to saline in the drinking water. Brit. Poult. Sci. 33,489 -504.
Wideman, R. F., Jr and Satnick, J. L. (1989). Physiological evaluation of diuresis in commercial broiler breeders. Brit. Poult. Sci. 30,313 -326.
Wideman, R. F., Jr, Satnick, J. L., Mitsos, W. J., Bennett, K. R. and Smith, S. R. (1987). Effect of saline adaptation and renal portal sodium infusion on glomerular size distributions and kidney function in domestic fowl. Poult. Sci. 66,348 -356.[Medline]
Williams, J. B. and Braun, E. J. (1996). Renal compensation for cecal loss in Gambel's quail (Callipepla gambelii). Comp. Biochem. Physiol. 113A,333 -341.[CrossRef]
Williams, J. B., Pacelli, M. M. and Braun, E. J. (1991). The effect of water deprivation on renal function in conscious unrestrained gambel's quail (Callipepla gambelii). Physiol. Zool. 64,1200 -1216.
Yokota, S. D., Benyajati, S. and Dantzler, W. H. (1985). Comparative aspects of glomerular filtration in vertebrates. Renal Physiol. Basel 8, 193-221.