Comparison of renal and salt gland function in three species of wild ducks.

Abstract

Three processes central to osmoregulation of marine birds were compared in three species of ducks that differ in habitat affinity, diet and saline tolerance. These processes are filtration of Na+ and water from the plasma by the kidneys, their reabsorption along the renal tubules, and secretion by the salt glands. Barrow's goldeneyes Bucephala islandica, the most marine species, have the highest rates for all three processes and only this species can secrete all the infused salt via the salt glands. Rates of all three processes are lower in mallards Anas platyrhynchos, the most freshwater species. Following saline acclimation, mallards could excrete all the infused Na+ by a combined Na+ excretion of the kidneys and salt glands. Canvasbacks Aythya valisineria, despite being more saline tolerant than mallards, are unable to excrete all the infused Na+. They produce a large volume of urine (like mallards) that has a low [Na+] (like goldeneyes). Salt gland secretion Na+ concentration did not differ among the three species, but only goldeneyes secrete at a rate sufficient to eliminate all infused Na+ via the salt glands. Differences in saline tolerance of these ducks species cannot be fully explained by differences in their filtration, reabsorption and secretion of Na+ and water, suggesting that the intestinal tract plays an important role.

Full text

Page 1

All marine birds have salt glands that, together with the
kidneys, maintain body fluid homeostasis, despite the excess
sodium chloride (NaCl) they ingest. They have similar total
body water, but twice the daily water flux of birds that lack salt
glands (Hughes et al., 1987; Nagy and Peterson, 1988). Among
species that produce highly concentrated salt gland secretion
(SGS), the salinity of the drinking water has no effect on
drinking rate (Harriman, 1967; Walter and Hughes, 1978;
Bennett et al., 2003). Such birds become dehydrated only when
they drink water more concentrated than their SGS (Bennett et
al., 2003).
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
(Kalisin ´ska 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
3273
The Journal of Experimental Biology 206, 3273-3284
© 2003 The Company of Biologists Ltd
doi:10.1242/jeb.00551
Three processes central to osmoregulation of marine
birds were compared in three species of ducks that differ
in habitat affinity, diet and saline tolerance. These
processes are filtration of Na+and water from the plasma
by the kidneys, their reabsorption along the renal tubules,
and secretion by the salt glands. Barrow’s goldeneyes
Bucephala islandica, the most marine species, have the
highest rates for all three processes and only this species
can secrete all the infused salt via the salt glands. Rates
of all three processes are lower in mallards Anas
platyrhynchos, the most freshwater species. Following
saline acclimation, mallards could excrete all the infused
Na+by a combined Na+excretion of the kidneys and salt
glands. Canvasbacks Aythya valisineria, despite being
more saline tolerant than mallards, are unable to excrete
all the infused Na+. They produce a large volume of urine
(like mallards) that has a low [Na+] (like goldeneyes). Salt
gland secretion Na+concentration did not differ among
the three species, but only goldeneyes secrete at a rate
sufficient to eliminate all infused Na+via the salt glands.
Differences in saline tolerance of these ducks species
cannot be fully explained by differences in their filtration,
reabsorption and secretion of Na+and water, suggesting
that the intestinal tract plays an important role.
Key words: osmoregulation, kidney, salt gland, mallard, Anas
platyrhynchos, canvasback, Aythya valisineria, Barrow’s goldeneye,
Bucephala islandica.
Summary
Introduction
Comparison of renal and salt gland function in three species of wild ducks
Darin C. Bennett and Maryanne R. Hughes
Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC, V6T 1Z4,
Canada
*Author for correspondence (e-mail: dcbennet@interchange.ubc.ca)
Accepted 23 June 2003

Page 2

3274 D. C. Bennett and M. R. Hughes
Table·1. Glomerular filtration rate (GFR) and effective renal plasma flow (ERPF) of birds with and without salt glands in
relation to habitat type and diet
Species Mass (g)GFR (ml·min–1) ERPF (ml·min–1)Habitat DietSource
Without salt glands:
Order Struithioniformes
Dromaius novaehollandiae
Order Galliformes
Alectoris chukar
Coturnix chinensis
Coturnix pectoralis
Coturnix japonica
Gallus gallus var. dom.
Meleagris pavo
Callipepla gambelii
Order Psittaciformes
Melopsittacus undulatus
Cacatua roseicapilla
Order Trochiliformes
Calypta anna
Order Columbiformes
Zenaidura macroura
Columbia livia
Order Falconiformes
Falco sparverius
Order Passeriformes
Anthochaera carunculata
Sturnus vulgarus
Nectarinia osea
Passer domesticus
Melospiza melodia
40700 16.2TAO1
511.7
51.4
107.3
122.3
1890
7400
158.4
0.58
0.55
0.68
1.55
4.13
5.68
0.23
TA
TM
TA
TM
TM
TM
TA
O
O
H
H
O
H
H
2
3
3
4
1.50
4.07
32.325–33
34, 35
36–42
37.5
335.9
0.14
0.79
TA
TA
O
O
43
443.76
5.10.04 TMN45
119
569.3
0.27
4.04
2.05 TM
TM
H
H
46
47
126.00.27 TMC 48
99
77.1
5.8
22.8
18.4
0.35
0.50
0.03
0.13
0.13
TM
TM
TM
TM
TM
N
O
N
H
O
49
4.2750–57
58
59
60
With salt glands:
Order Anseriformes
Branta canadensis
Anas platyrhynchos
Anas platyrhynchos var. dom.
Aythya valisineria
Bucephala islandica
Order Charadriiformes
Larus argentatus
Larsus dominicanus
Larus glaucescens
3670
983
2513
1052
767
6.24
2.70
7.44
2.27
4.06
FW
FW
FW
FW
MR
H
O
O
O
C
61
11.00
52.85
5.23
10.63
61–63
64–72
62
62
1000
905
900
4.40
3.09
3.84
MR
MR
MR
C
C
C
73
74
13.6161, 75–77
TA, terrestrial arid; TM, terrestrial mesic; FW, freshwater; MR, marine; H, herbivore; O, omnivore; N, nectivore; C, carnivore.
Source: 1Dawson et al. (1991), 2Goldstein (1990), 3Roberts et al. (1985), 4Roberts and Hughes (1983), 5Berger et al. (1960), 6Dantzler
(1966), 7Glahn et al. (1988a,b), 8Gregg and Wideman (1990), 9Hyden and Knutson (1959), 10Korr (1939), 11Leary et al. (1998), 12Nechay and
Nechay (1959), 13Orloff and Davidson (1959), 14Pitts (1938), 15Pitts and Korr (1938), 16Radin et al. (1993), 17Roberts (1991a), 18Roberts
(1992), 19Sanner (1965), 20Shannon (1938a,b), 21Shideman et al. (1981), 22Singh and Battacharyya (1983), 23Skadhauge (1964), 24Skadhauge
and Schmidt-Nielson (1967), 25Sperber (1960), 26Svendsen and Skadhauge (1976), 27Sykes (1960a,b), 28Vena et al. (1990), 29Wideman and
Gregg (1988), 30Wideman and Laverty (1986), 31Wideman and Nissley (1992), 32Wideman and Satnick (1989), 33Wideman et al. (1987),
34Palmore et al. (1981), 35Vogel et al. (1965), 36Anderson (1980), 37Braun (1976), 38Braun and Dantzler (1972), 39Braun and Dantzler (1974),
40Braun and Dantzler (1975), 41Williams and Braun (1996), 42Williams et al. (1991), 43Krag and Skadhauge (1972), 44Roberts (1991b), 45S.
Medler (unpublished data), 46Shoemaker (1967), 47Chan et al. (1972), 48Lyons and Goldstein (2002), 49Goldstein and Bradshaw (1998b),
50Braun (1978), 51Clark and Wideman (1980), 52Laverty and Dantzler (1982),53Laverty and Dantzler (1983), 54Laverty and Wideman (1989),
55Roberts and Dantzler (1989), 56Roberts and Dantzler (1992), 57Wideman et al. (1980), 58T. J. McWhorter (unpublished data), 59Goldstein and
Braun (1988), 60Goldstein and Rothschild (1993), 61Hughes (1980), 62This study, 63Hughes et al. (1999), 64Bennett et al. (2000), 65Bradley and
Holmes (1971), 66Gerstberger et al. (1985), 67Holmes and Adams (1963), 68Holmes et al. (1968), 69Hughes et al. (1989), 70Schutz et al. (1992),
71Simon and Gray (1991), 72Thomas and Phillips (1975), 73Douglas (1966), 74Gray and Eramus (1988), 75Hughes (1995), 76Hughes et al.
(1993), 77Raveendran (1987).

Page 3

3275
Renal and salt gland function of ducks
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
Animals
24 adult ducks (eight mallards,
Anas platyrhynchos
Canvasbacks,
Aythya
Gray, and eight Barrow’s goldeneyes,
Bucephala islandica Gmelin) were
held in large partially covered outdoor
enclosures at the University of British
Columbia Animal Care Facility.
Groups included equal numbers of
males and females. Water was
presented in 70·liter plastic wading
pools and completely replenished
twice daily. Half the ducks of each
species drank freshwater, while the
other half drank 300·mmol·l–1NaCl.
They ate duck pellets (17% protein,
2750·kcal·kg–1;
Abbottsfield, BC, Canada) containing
12.7% water and 68, 145 and
190·mmol·l–1·kg–1Na+, K+and Cl–,
respectively.
L.,
valisineria
eight
Buckerfield’s,
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·l–1NaCl, containing 0.15·kBq·ml–1of 14C-inulin
and 1.1·kBq·ml–1of 3H-PAH, was begun (0.175·ml·min–1).
After a 1·h equilibration period, four 10–15·min urine samples
were collected. Then infusate NaCl concentration was
increased to 500·mmol·l–1and urine was collected at
10–20·min intervals until the duck began to secrete. Four
simultaneous 10–20·min collections of urine and SGS were
made. Finally, infusate NaCl concentration was reduced to
75·mmol·l–1and three simultaneous 10–20·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
290
600
300
310
320
A
B
C
330
0
200
400
0
?
500
?
500
?
500
0.5
1.0
1.5
2.0
MallardCanvasbackGoldeneye
75–+7575–+7575–+75
Infusate [NaCl] (mmol l–1)
Osmolality (mOsmol kg–1)
Fig.·1. Effect of hypotonic and hypertonic saline infusion (75 and 500·mmol·l–1NaCl,
respectively) on (A) plasma and (B) urine osmolality and (C) their ratio (Urine:Plasma) in
freshwater (open symbols) and saline-acclimated (filled symbols) in mallards Anas
platyrhynchos (circles), canvasbacks Aythya valisineria (triangles) and Barrow’s goldeneyes
Bucephala islandica (squares). The period of 500·mmol·l–1NaCl infusion was subdivided into
two parts: the period prior to secretion (–) and the period of secretion (+). Values are means ±
S.E.M. (N=4 ducks per treatment).

Page 4

3276
[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:
GFR = [inulin]uUFR / [inulin]pl
and
ERPF = [PAH]uUFR / [PAH]pl·,
where [marker]uand [marker]plare the marker (inulin or PAH)
concentrations in the urine and plasma, respectively, and UFR
is the urine flow rate. Fractional reabsorption of water (FRH2O)
was calculated as:
FRH2O = (1–[inulin]pl/ [inulin]u) × 100
and fractional reabsorption of Na+and K+(FRNa and FRK,
respectively) was calculated as:
FRion = (GFR[ion]pl– UFR[ion]u) / GFR[ion]pl·,
where [ion]pl
concentrations of the plasma and urine, respectively.
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·l–1NaCl infusion
was divided into two periods: prior to secretion and active
secretion. Data are reported as means ± standard errors (S.E.M.)
and statistically
SYSTAT 9 for Windows (SPSS
Science,
Differences
infusion
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 step-
wise linear regression.
To examine the relationships of
GFR to habitat and diet of birds, we
collected GFR data on 27 species
ofadult
disregarding the methods used to
measure GFR (Table·1). Data were
obtained
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
onbody mass, after log10–log10
transformation, and analysing the
residuals by ANOVA.
and [ion]u
represent the Na+
and K+
analyzed using
Chicago,
among
periods
IL,
species
and
USA).
and
between
non-dehydrated birds,
from original sources
Results
Plasma composition
Overall, Osmpl, [Na]pl and [K]pl
varied significantly among species
and infusion periods, but not between
the treatments or sexes. Mallards had
a lower Osmpl (P<0.06; Fig.·1) and
[Na]pl (P<0.002; Fig.·2) and a higher
[K]pl (P<0.002; Fig.·3) than both
canvasbacks and goldeneyes. Infusion
of hypertonic saline significantly
D. C. Bennett and M. R. Hughes
140
150
150
160
170
0
50
100
0
0.2
0.4
0.6
0.8
1.0
MallardCanvasbackGoldeneye
A
B
C
?
500
?
500
?
500
75–+7575–+7575–+75
Infusate [NaCl] (mmol l–1)
Sodium concentration (mmol l–1)
Fig.·2. Effect of hypotonic and hypertonic saline infusion (75 and 500·mmol·l–1NaCl,
respectively) on (A) plasma and (B) urine sodium concentration and (C) their ratio
(Urine:Plasma) in freshwater (open symbols) and saline-acclimated (filled symbols) mallards
Anas platyrhynchos (circles), canvasbacks Aythya valisineria (triangles) and Barrow’s
goldeneyes Bucephala islandica (squares). The period of 500·mmol·l–1NaCl infusion was
subdivided into two parts: the period prior to secretion (–) and the period of secretion (+).
Values are means ± S.E.M. (N=4 ducks per treatment).

Page 5

3277
Renal and salt gland function of ducks
increased Osmpl, [Na]pl and [K]pl in all three species and
these remained high during active salt secretion. Osmpl and
[Na]pl, but not [K]pl, decreased after the infusion of hypotonic
75·mmol·l–1NaCl was reinstated.
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
inmallards (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·l–1
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 Osmuand
[K]u and, together with canvasbacks,
the lowest [Na]u. Canvasbacks also
have the lowest Osmuand [K]u. Osmu,
[Na]uand [K]uvaried significantly among infusion periods (all
P<0.00001; Figs·1–3), 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:
2.0
150
2.5
3.0
3.5
4.0
0
50
100
0
10
20
30
40
Mallard Canvasback Goldeneye
A
B
C
?
500
?
500
?
500
75–+7575–+7575–+75
Infusate [NaCl] (mmol l–1)
Potassium concentration (mmol l–1)
Fig.·3. Effect of hypotonic and hypertonic saline infusion (75 and 500·mmol·l–1NaCl,
respectively) on (A) plasma and (B) urine potassium concentration and (C) their ratio
(Urine:Plasma) in freshwater (open symbols) and saline-acclimated (filled symbols) mallards
Anas platyrhynchos (circles), canvasbacks Aythya valisineria (triangles) and Barrow’s
goldeneyes Bucephala islandica (squares). The period of 500·mmol·l–1NaCl infusion was
subdivided into two parts: the period prior to secretion (–) and the period of secretion (+).
Values are means ± S.E.M. (N=4 ducks per treatment).

Page 6

3278
Mallards: UFR = 2.0 + (0.039×GFR) – (0.021×FRΗ2Ο),
r=0.83, P<0.0001,
Goldeneyes: UFR = 3.6 + (0.012×GFR) – (0.036×FRH2O),
r=0.95, P<0.0001,
and could be similarly predicted in canvasbacks if one
freshwater female were excluded:
Canvasbacks: UFR = 1.6 + (0.021×GFR) – (0.016×FRH2O),
r=0.81, P<0.0001,
otherwise UFR of canvasbacks was predicted solely by 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·l–1NaCl at 0.175·ml·min–1) to initiate
secretion. Freshwater mallards and one freshwater female
canvasback produced only a trace of SGS. [Na+]sgsdid 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
Kidneys and salt glands of marine birds act interactively to
maintain the volume and composition of body fluids within
some homeostatically controlled range. The salt glands
secrete excess NaCl as a hypertonic
fluid and are the primary site of Na+
excretion, while the kidneys rid the
body of excess water, nitrogenous
wastes and other osmolytes. To this end,
kidneys of marine birds should maintain
a high GFR and a high tubular
reabsorption
Therefore, secretion of excess NaCl
directly reflects renal Na+filtration
andreabsorption.
simultaneously compared the filtration
and reabsorption of Na+and water from
the kidneys, and secretion of Na+by the
salt glands in three species of ducks of
utilize habitats of different salinities.
of Na+
and water.
This study
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
relationship by comparing GFR of 27
species of adult birds for which data
are available (Table·1). GFR varied
of this
D. C. Bennett and M. R. Hughes
0
6
10
20
30
0
2
4
0
0.1
0.2
0.3
Mallard CanvasbackGoldeneye
A
B
C
?
500
?
500
?
500
75–+ 7575–+75 75–+75
Infusate [NaCl] (mmol l–1)
Rate (ml min–1)
Fig.·4. Effect of hypotonic and hypertonic saline infusion (75 and 500·mmol·l–1NaCl,
respectively) on (A) effective renal plasma flow (ERPF), (B) glomerular flow rate (GFR) and
(C) urine flow rate (UFR) in freshwater (open symbols) and saline-acclimated (filled
symbols) mallards Anas platyrhynchos (circles), canvasbacks Aythya valisineria (triangles)
and Barrow’s goldeneyes Bucephala islandica (squares). The period of 500·mmol·l–1NaCl
infusion was subdivided into two parts: the period prior to secretion (–) and the period of
secretion (+). Values are means ± S.E.M. (N=4 ducks per treatment).

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3279
Renal and salt gland function of ducks
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;
Kalisin ´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
75
80
85
90
95
100
90
92
94
96
98
100
–100
–50
0
50
100
MallardCanvasbackGoldeneye
A
B
C
?
500
?
500
?
500
75–+ 7575 –+7575 –+75
Infusate [NaCl] (mmol l–1)
Fractional reabsorption (%)
Fig.·5. Effect of hypotonic and hypertonic saline infusion (75 and 500·mmol·l–1NaCl,
respectively) on the fractional reabsorption of (A) water, (B) sodium and (C) potassium in
freshwater (open symbols) and saline-acclimated (filled symbols) mallards Anas platyrhynchos
(circles), canvasbacks Aythya valisineria (triangles) and Barrow’s goldeneyes Bucephala
islandica (squares). The period of 500·mmol·l–1NaCl infusion was subdivided into two parts:
the period prior to secretion (–) and the period of secretion (+). Values are means ± S.E.M.
(N=4 ducks per treatment).

Page 8

3280
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·l–1NaCl 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·l–1
NaCl, mallards decreased water flux (drinking), but
canvasbacks tolerated 450·mmol·l–1NaCl 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
D. C. Bennett and M. R. Hughes
02468
0
0.1
0.2
0.3
0.
A
4
B
r=0.52, P=0.002
02468
r=–0.43, P=0.14
02468
r=0.76, P<0.0001
859095100
0
0.1
0.2
0.3
0.4
r=–0.46, P=0.008
60708090100
r=–0.26, P=0.01
96979899100
r=–0.84, P<0.0001
MallardCanvasbackGoldeneye
Glomerular filtration rate (ml min–1)
Fractional reabsorption of water (%)
Urine flow rate (ml min–1)
Fig.·6. Relationship between urine flow rate and (A) glomerular filtration rate and (B) the fractional reabsorption of water in freshwater (open
symbols) and saline-acclimated (filled symbols) mallards Anas platyrhynchos (circles), canvasbacks Aythya valisineria (triangles) and Barrow’s
goldeneyes Bucephala islandica (squares).
400
500
600
700
800
[Na+]SGS (mmol l–1)
FWSW
–0.05
0
0.05
0.10
0.15
0.20
Flow rate (ml min–1)
FWSW
Saline treatment
Fig.·7. Salt gland secretion [Na+] and flow rate in freshwater (open symbols) and
saline-acclimated (filled symbols) mallards Anas platyrhynchos
canvasbacks Aythya valisineria (triangles) and Barrow’s goldeneyes Bucephala
islandica
(squares) infused intravenously with 500·mmol·l–1
0.175·ml·min–1. Values are means ± S.E.M. (N=4 ducks per treatment).
(circles),
NaCl at

Page 9

3281
Renal and salt gland function of ducks
450·mmol·l–1NaCl (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·kg–1·day–1(Fletcher
and Holmes 1968; Bennett et al., 2003). If they drink
300·mmol·l–1NaCl, their estimated Na+flux would be
67.5·mmol·l–1·kg–1·day–1, but Na+flux measured by 22Na
turnover was only 21.4·mmol·l–1·kg–1·day–1(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
–2
–1
0
1
2
A
B
GFR=0.013 m0.76
r2 =0.89
Log(GFR)
012345
0
0.5
1.0
1.5
2.0
ERPF=0.10 m0.71
r2 =0.78
Log(ERPF)
Log(mass)
Fig.·8. (A) Glomerular filtration rate (GFR) and (B) effective renal
plasma flow (ERPF) as a function of body mass (m) in birds. Data
and sources are given in Table·1.
–0.4
0.4
–0.2
0
0.2
0.4
A
B
P=0.02
–0.4
–0.2
0
0.2
P=0.92
TA TM FW MR
Habitat
Residuals
Fig.·9. Comparison of (A) glomerular filtration rate (GFR) and (B)
effective renal plasma flow (ERPF) of birds in relation to habitat type
(TA, terrestrial arid; TM, terrestrial mesic; FW, freshwater; MR,
marine). Data are calculated from residuals of logGFR or logERPF
on log(body mass) (Fig.·8; raw data and sources are given in
Table 1) and are expressed as mean residual values ±S.E.M.

Page 10

3282
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·l–1NaCl can excrete all infused Na+, why can
they not drink greater than 300·mmol·l–1NaCl? 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.
We thank Anne Cheng and Susan Lee for assisting with
this experiment and Arthur Van Der Horst and Sam Gopaul
for excellent care of our experimental birds. We thank Drs
Lee Gass and John Gosline for their comments on earlier
drafts of this manuscript. We thank Todd McWhorter and Dr
Scott Medler for their unpublished data. This research was
conducted in accordance with the guidelines set forth by the
Canadian Council on Animal Care and was supported by the
Natural Sciences and Engineering Research Council of
Canada (Grant A-3442, to M.R.H.). Manuscript preparation
was supported by a grant contributed by Dr G. C. Hughes.
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