Renal function in Palestine sunbirds: elimination of excess water does not constrain energy intake
1 Department of Ecology and Evolutionary Biology, University of Arizona,
Tucson, AZ 85721, USA
2 Department of Zoology and Physiology, University of Wyoming, Laramie, WY
82071, USA
3 Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert
Research, and Department of Life Sciences, Ben-Gurion University of the Negev,
Sede Boqer Campus, 84990 Midreshet Ben-Gurion, Israel
* Author for correspondence at present address: Department of Wildlife Ecology, 226 Russell Labs, 1630 Linden Drive, University of Wisconsin-Madison, Madison, WI 53706, USA (e-mail: tjmcwhorter{at}wisc.edu)
Accepted 30 June 2004
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Summary |
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Key words: Palestine sunbird, Nectarinia osea, glomerular filtration rate, nectar, glucose, osmoregulation, water balance, kidney, renal function
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Introduction |
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Nectar-feeding birds are faced with the conflicting demands of eliminating
excess water and metabolic by-products while retaining electrolytes,
metabolites and substrates for energy metabolism
(Yokota et al., 1985). Plasma
glucose levels in hummingbirds are high and surprisingly variable (ranging
from 17 mmol l-1 in fasted birds to as much as 40 mmol
l-1 in feeding individuals;
Beuchat and Chong, 1998
),
resulting in relatively high estimated glucose filtered loads (the product of
GFR and the concentration of glucose in plasma). How do these birds prevent
the loss of glucose to urine? In the mammals and birds for which renal glucose
recovery has been investigated (summarized in
Beyenbach, 1985
), the high
plasma glucose concentrations found in nectar-feeding birds would lead to
severe renal glucose loss and presumably osmotic diuresis. Hummingbirds
produce extremely dilute urine (Calder and
Hiebert, 1983
; Lotz and
Martínez del Rio, 2004
) and the morphology of their kidneys
suggests that they are well suited for water disposal
(Johnson and Mugaas, 1970
;
Casotti et al., 1998
;
Beuchat et al., 1999
). Because
hummingbirds also appear to absorb essentially all ingested water
(McWhorter and Martínez del Rio,
1999
), they probably rely on a large renal capacity for water
elimination (and thus energetically expensive renal glucose and electrolyte
reabsorption) and on relatively high rates of evaporative water loss
(Lasiewski, 1964
;
Powers, 1992
) to maintain
water balance. The problem of excess ingested water, however, can be handled
both from the supply and disposal sides of the equation. McWhorter et al.
(2003
) recently found that one
species of nectar-feeding sunbird (Nectariniidae) reduces the fractional
absorption of ingested water with increasing water intake rate. Sunbirds may
therefore avoid a substantial absorbed water load, and thus the associated
costs of recovering metabolites in the kidney and potential limitations to
energy intake, when feeding on dilute nectars.
Here we report the results of experiments designed to examine the
relationship between energy and water intake and kidney function in the
Palestine sunbird [Nectarinia osea (Bonaparte 1856)], an Old World
passerine nectarivore. Despite water intake rates that exceed several times
their body mass per day (Lotz and
Nicolson, 1999; McWhorter et
al., 2003
; Nicolson and
Fleming, 2003
), sunbirds, unlike hummingbirds, may not face
exceptional renal water loads. We hypothesized that GFR in the Palestine
sunbird would be lower than in hummingbirds and consistent with the allometric
prediction of 4.3 ml h-1 for a bird of its body mass
(Yokota et al., 1985
;
Williams et al., 1991
), and
would not be especially sensitive to water loading
(Goldstein and Bradshaw,
1998
). With this hypothesis in mind, we predicted that sunbirds
would have plasma glucose concentrations comparable to those of hummingbirds
(Beuchat and Chong, 1998
), but
relatively lower glucose filtered loads, and would consequently excrete very
little glucose (McWhorter and
Martínez del Rio, 2000
). We further predicted that
fractional water reabsorption (FWR) by the kidney would decrease with
increasing water load (Goldstein and
Bradshaw, 1998
).
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Materials and methods |
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Experimental design
We relied on the behavioral responses of birds to nectar of varying energy
density in the design of this experiment. Typically, nectar-feeding birds
reduce their food (hereafter `nectar', normally the source of both energy and
water in these animals) intake rate with increasing sugar concentration
(López-Calleja et al.,
1997; McWhorter and Martínez del Rio,
1999
,
2000
;
McWhorter and López-Calleja,
2000
; Martínez del Rio
et al., 2001
). Manipulation of sugar concentration therefore leads
to a wide range of variation in the quantity of nectar (and thus water)
ingested. We used a repeated-measures design in which we measured GFR and
renal fractional recovery of filtered water (FWR) in eight sunbirds fed five
different sugar solutions (146, 292, 584, 876 and 1168 mmol l-1
sucrose) at two ambient temperatures (15±1 and 30±2°C). In a
separate repeated-measures experiment, we measured urine and excreted fluid
osmotic concentration and glucose concentration in eight sunbirds fed on four
sugar solutions (146, 292, 584 and 1168 mmol l-1 sucrose) at three
ambient temperatures (5±2, 15±1 and 30±2°C). In both
experiments, we randomized the order in which diet and temperature treatments
were presented to subjects. Ambient temperature was varied within the range
that these sunbirds normally experience to elicit a wide range of energy
demands and thus nectar intake rates. Finally, we measured the plasma glucose
concentration of nine sunbirds, both when feeding on their normal maintenance
diet (described above) and after a 12 h overnight fast, in a repeated-measures
design. Birds were randomly assigned to the first treatment (i.e., fed
vs fasted) and all measurements were conducted at
25±2°C.
GFR was estimated with a single injection of 14C-labeled inulin,
using a modification of the slope-intercept method
(Hall et al., 1977;
Florijn et al., 1994
). The
only assumption we made in modifying this method was that the rate of marker
disappearance from plasma was equal to the rate of appearance in excreta. The
concentration of marker would of course be different among plasma, urine and
excreta because of reabsorption of filtered water in the kidney and mixing of
urine with gut contents in the cloaca. Our method allowed us to measure renal
function in unanesthetized, actively feeding birds with minimal disturbance.
GFR (µl h-1) was estimated as:
![]() | (1) |
where Qi is the quantity of marker injected (disints
min-1), KQRC is the fractional inulin turnover
rate (h-1), and Ai(0) is the zero-time
intercept concentration of marker in plasma (disints min-1
µl-1). Fractional inulin turnover rate was estimated by fitting
negative exponential functions (Hall et
al., 1977) to the relationship between the concentration of
14C in excreta and time. The slope of the fractional inulin
turnover curve was then used to extrapolate the plasma marker concentration of
a single blood sample, taken 2-3 h afterinjection, to the zero-time intercept
concentration (and thus also estimate the inulin distribution space). This
method was used because of the sensitivity of small birds to repeated blood
sampling. Fractional recovery of filtered water in the kidney (FWR) was
estimated as 1 minus the ratio of marker concentration in plasma
(PM) to that in urine (UM)
(FWR=1-[PMxUM-1]).
Experimental measurements
GFR and FWR measurements
We injected 4.63x104 Bq of
inulin-[14C]-carboxylic acid (molecular mass 5175±95;
Amersham, Piscataway, NJ, USA) in 15 µl of distilled water into the
pectoralis of each bird approximately 1.5 h after the lights came on.
Injection volumes were verified gravimetrically by weighing syringes (25
µl, Hamilton Company, Reno, NV, USA) to ±0.0001 g before and after
injection. Fresh excreta samples were collected for 2-3 h, after which a
ureteral urine sample was collected with a closed-ended polyethylene cannula
(Goldstein and Braun, 1989)
and a blood sample (approximately 50 µl) was collected by puncturing the
brachial vein. We separated plasma from blood cells before radioisotope
analysis. Liquid scintillation cocktail (ACS II, Amersham) was added to all
excreta, plasma, urine and injection samples, which were counted correcting
for quench and lumex (chemiluminescence) in a Packard Tri-Carb 1600TR Liquid
Scintillation Analyzer (Perkin-Elmer Life and Analytical Sciences, Boston, MA,
USA).
Excreted fluid and ureteral urine glucose and osmotic concentration measurements
Fresh excreta samples were collected from actively feeding sunbirds over a
30 min period, pooled for each bird separately, and immediately frozen for
later analysis. After excreta collection was completed, we captured birds and
collected a ureteral urine sample with a closed-end polyethylene cannula
(Goldstein and Braun, 1989).
We measured the osmotic concentration of the samples using an Osmette II
freezing point depression osmometer (Precision Systems Inc., Natick, MA, USA),
and glucose concentration using a clinical diagnostic kit (Procedure No. 315,
enzymatic determination by the Trinder reaction; Sigma Chemical, St Louis, MO,
USA).
Plasma glucose measurements
We collected blood samples (approximately 30 µl) by puncturing the
brachial vein 1 h after the lights came on. Fed birds were allowed to feed
normally for 1 h before sampling. Plasma was separated from the blood sample
and immediately assayed for glucose concentration as above.
Statistical analysis
Since relationships between nectar intake rate and sugar concentration in
nectar-feeding birds are power functions
(López-Calleja et al.,
1997; McWhorter and Martínez del Rio,
1999
,
2000
;
McWhorter and López-Calleja,
2000
; Martínez del Rio
et al., 2001
; Nicolson and
Fleming, 2003
), we determined the effects of temperature and
individual bird (subject) on nectar intake rate using linear models of
loge-transformed intake and sucrose concentration data. Analysis of
covariance (ANCOVA) was used on loge-transformed data to compare
the slope and intercept of this relationship among experimental temperatures.
The relationships between the osmotic and glucose concentrations of ureteral
urine and excreted fluid and water intake rate were best described by power
functions, so we similarly applied linear models to
loge-transformed data. We used linear models on untransformed data
to assess significance and subject and temperature effects in all other cases.
Repeated-measures analysis of variance (RM-ANOVA) was used to assess
differences in plasma glucose concentration between fed and fasted birds. All
values are presented as means ±
S.E.M.
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Results |
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The relationships between the concentration of 14C-labeled inulin in excreta (disints min-1 µl-1) and time were well described by negative exponential functions (r2=0.61-0.99, N=37). The decline in the concentration of 14C-labeled inulin in excreta with time therefore followed one-compartment, first-order kinetics (Fig. 2). Fractional inulin turnover rate (KQRC) was significantly higher at 30°C (1.816±0.098 h-1) than at 15°C (1.513±0.085 h-1, ANOVA F1,35=5.45, P=0.025). Inulin distribution space estimated by the intercept method ranged from 19.14 to 23.49% of body mass (21.11±0.57%, N=8; multiple estimates for individual subjects averaged).
|
Glomerular filtration rate (GFR) in Palestine sunbirds ranged from 820.7 to 3597.31 µl h-1 (1976.22±91.95 µl h-1, N=37; Fig. 3). There was a significant effect of temperature (F1,34=9.7, P=0.004) and water intake rate (F1,34=8.47, P=0.006) on GFR, but no significant effect of subject (F7,27=1.99, P=0.11), so we removed the latter variable from the model. To examine the effects of water intake independently of temperature, we constructed separate linear models for measurements at each temperature. GFR was correlated with water intake rate at 15°C (y=0.37x+1435.8, r2=0.3, F1,18=7.56, P=0.013), but not at 30°C (F1,15=0.91, P=0.36). Mean GFR was significantly higher at the higher temperature (1792.4±129.78 vs 2192.48±111.65 µl h-1 for 15 and 30°C, respectively; ANCOVAtemperature F1,34=9.7, P=0.004).
|
Fractional water reabsorption (FWR) in the kidney ranged from 0.64 to 0.98 (0.82±0.02, N=29) and decreased significantly with water intake rate as predicted (F1,19=6.65, P=0.018; Fig. 4). Because there were no significant effects of subject (F7,19=1.21, P=0.34) or temperature (F1,19=0.08, P=0.77), we removed these variables from the model and estimated a common relationship between FWR and water intake rate (y=-1.6x10-4x+0.91, r2=0.34).
|
Excreted fluid and ureteral urine glucose and osmotic concentration measurements
Osmotic concentration declined significantly with increasing water intake
rate (F1,40=48.36, P<0.0001), and was
significantly greater in ureteral urine than in excreted fluid
(F1,31=57.91, P<0.0001;
Fig. 5B). Since there were no
effects of subject (F9,31=0.91, P=0.53) or
temperature (F2,31=1.72, P=0.2), we removed these
variables from the model. We described the relationship between osmotic
concentration and water intake rate using separate power functions for
ureteral urine and excreted fluid
(y=18045.61x-0.82, r2=0.49,
F1,11=10.47, P=0.008, N=13, and
y=1101.14x-0.57, r2=0.65,
F1,28=51.1, P<0.0001, N=32,
respectively; Fig. 5B).
Ureteral urine osmotic concentration ranged from 14.96 to 329 mOsm
kg-1 (115.5±25.28, N=13), and that of excreted
fluid ranged from 12.33 to 95 mOsm kg-1 (30.82±3.82,
N=32).
|
Glucose concentration declined significantly with increasing water intake rate (F1,37=13.47, P=0.0008), and was significantly higher in ureteral urine than in excreted fluid (F1,28=17.1, P<0.0003; Fig. 5A). There were no effects of subject (F9,28=0.9, P=0.54) or temperature (F2,28=2.21, P=0.13), so we removed these variables from the model. Glucose concentration was not significantly correlated with water intake rate when ureteral urine data were considered separately (F1,9=0.67, P=0.43, N=11), probably because of small sample size, particularly at higher rates of water intake. The relationship between glucose concentration and water intake rate in excreted fluid was adequately described by a power function (y=26.18x-0.62, r2=0.4, F1,27=8.21, P=0.008, N=31; Fig. 5A). Glucose concentration in ureteral urine ranged from 0.28 to 10.39 mmol l-1 (2.97±1.05, N=11), and that in excreted fluid ranged from 0.12 to 3.52 mmol l-1 (0.6±0.12, N=31).
Plasma glucose measurements
Plasma glucose concentration was significantly greater in fed
(28.18±0.68 mmol l-1) than in fasted sunbirds
(16.08±0.75 mmol l-1; F1,7=335.44,
P<0.0001, N=8).
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Discussion |
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In general, the data support our predictions. Glomerular filtration rate
was lower than expected (46% of the value predicted based on body mass;
Yokota et al., 1985;
Williams et al., 1991
;
however, these allometric predictions are based on larger, usually
anesthetized birds and therefore may well not extrapolate to small
unanesthetized birds), and was not exceptionally sensitive to water loading
(Fig. 3). When standardized to
metabolic body mass (kg0.75), mean GFR in Palestine sunbirds
(93.91±4.37 ml kg-0.75 h-1) was approximately 60%
and 75% of that in two species of hummingbirds (see below). Plasma glucose
concentrations were high and varied 1.8-fold between fasted and fed sunbirds,
but because GFR was low, glucose filtered load also remained relatively low
(0.056 mmol h-1 in fed birds). Essentially the entire glucose
filtered load (98%) was recovered by the kidneys. Renal fractional water
reabsorption decreased from 0.98 to 0.64 with increasing water load
(Fig. 4), comparable to
observations in nectar-feeding red wattlebirds (Anthochaera
carunculata; Goldstein and Bradshaw,
1998
). The fraction of ingested water absorbed by Palestine
sunbirds decreases with water intake rate
(McWhorter et al., 2003
),
however, so their low GFR and high proportional renal recovery of glucose is
not surprising. They deal with the problem of water over-ingestion by not
absorbing all the water that they consume, rather than by absorbing it and
then filtering it in the kidney. In this discussion, we explore the
consequences of these adaptations to high water loads for the simultaneous
maintenance of water and energy balance. We posit that the energetic cost of
recovering filtered metabolites, and the potential for these processes to
limit energy intake, are much lower in sunbirds than in hummingbirds
(Nicolson and Fleming,
2003
).
Water ingestion and subsequent absorption in intestine has the potential to
constrain an animal's energy intake rate by exceeding its capacity for water
disposal (McWhorter and Martínez
del Rio, 1999; Martínez
del Rio et al., 2001
). Water loads (preformed water in nectar plus
metabolic water) greater than the sum of evaporative water loss and maximum
renal water elimination (GFR minus a minimum fractional water reabsorption
necessary to retain filtered metabolites) will overwhelm osmoregulatory
processes and lead to water intoxication unless the animal decreases nectar
intake. Nectar intake by sunbirds in this study increased with no detectable
plateau as diet sucrose concentration and ambient temperature decreased
(Fig. 1). Indeed, the slopes of
the relationships between nectar intake and diet sugar concentration at both
15°C and 30°C were not significantly different from -1, indicating
that birds were compensating completely for changes in nectar energy density
(Martínez del Rio et al.,
2001
). In addition, the 1.6-fold higher average sucrose intake
rate observed at 15°C corresponds almost exactly to the 1.5-fold increase
in metabolic rate observed in Palestine sunbirds between ambient temperatures
of 15°C and 30°C in the laboratory (C. Hambly, B. Pinshow, E. J.
Harper and J. R. Speakman, unpublished data). The sugar concentrations in the
diets used in this study span the range of sugar concentrations found in the
nectar of bird-pollinated plants (Pyke and
Waser, 1981
; Gryj et al.,
1990
; Stiles and Freeman,
1993
). Our results suggest, therefore, that water processing does
not limit energy intake in Palestine sunbirds over the range of sugar
concentrations that they encounter naturally.
McWhorter et al. (2003)
found that the fraction of ingested water absorbed (fW) by
Palestine sunbirds decreased from 100% to 36% with increasing water intake
rate (VI). In addition, Goldstein and Bradshaw
(1998
) found evidence
suggesting that dietary water was not completely absorbed from the gut of
nectar-feeding red wattlebirds under conditions of high water intake.
Therefore, in spite of water intake rates that exceed several times their body
mass per day (Lotz and Nicolson,
1999
; McWhorter et al.,
2003
; Nicolson and Fleming,
2003
), Palestine sunbirds may not face exceptional renal water
loads when feeding on dilute nectars. In
Fig. 6 we compare water intake
rate, estimated water load and urine flow rate [GFR-(GFRxFWR)] as a
function of diet sucrose concentration for birds in this study (data for both
temperatures combined). Water load was estimated as water absorption rate
[fWxVI, where
fW=0.36+(56.93xVI-1);
McWhorter et al., 2003
] plus
metabolic water production (estimated based on sucrose assimilation rate,
assuming carbohydrate catabolism). Estimated water load increases much more
slowly with decreasing sucrose concentration in nectar than does water intake
rate, and roughly parallels urine flow rate. The difference between water load
and urine flow rate represents water lost by evaporation (approximately 30% of
water load). The ability of Palestine sunbirds to modulate the absorption of
preformed water in nectar substantially reduces the water load that must
subsequently be eliminated by the kidney.
|
Excreted fluid glucose concentrations are comparably low in Palestine
sunbirds (0.6±0.12 mmol l-1) and broad-tailed hummingbirds
(Selasphorus platycercus; 1.3±0.6 mmol l-1;
McWhorter and Martínez del Rio,
2000). Does renal glucose processing and conservation differ
between sunbirds and hummingbirds? Glucose filtered loads in Palestine
sunbirds were relatively low (0.056 mmol h-1 in fed birds) in spite
of plasma glucose concentrations similar to those of hummingbirds
(Beuchat and Chong, 1998
). GFR
data are available for two species of hummingbirds: Calypte anna,
body mass 5.1 g, GFR 2.4 ml h-1 (125.76 ml kg-0.75
h-1; S. Medler, unpublished data), and Selasphorus
platycercus, body mass 3.6 g, GFR 2.3 ml h-1 (156.5 ml
kg-0.75 h-1; B. Hartman-Bakken, T. J. McWhorter, E.
Tsahar and C. Martínez del Rio, unpublished data). Assuming an average
plasma glucose concentration of 35 mmol l-1 in fed hummingbirds
(based on measurements in three species;
Beuchat and Chong, 1998
), the
predicted glucose filtered load would be 0.084 and 0.081 mmol h-1
for C. anna and S. platycercus, respectively, or about
1.5-fold that of the larger sunbird. The glucose filtered load that must be
recovered by the kidneys of Palestine sunbirds is 1.9- to 2.4-fold lower than
that estimated for hummingbirds when standardized to metabolic body mass (2.26
vs 4.4 and 5.47 mmol h-1 kg-0.75 for C.
anna and S. platycercus, respectively). Although excreta and
urine concentrations of other metabolites (e.g. amino acids) and electrolytes
were not measured in this study, the above argument may be applied to them as
well. The ability of sunbirds to modulate their absorbed water load may
therefore resolve the potential conflicts between eliminating excess water and
metabolic by-products while retaining electrolytes, metabolites and energy
(Yokota et al., 1985
).
Palestine sunbirds rely on the integrated functioning of two organ systems
to maintain water balance in spite of highly variable and often extremely high
water intake rates: (1) fractional absorption of dietary water is modulated in
the gastrointestinal tract (McWhorter et
al., 2003) and (2) FWR is modulated by the kidney. GFR in sunbirds
appears to be relatively insensitive to water loading. Similarly, Goldstein
and Bradshaw (1998
) concluded
that changes in urine flow rate in nectar-feeding red wattlebirds were more
closely related to modulation of renal FWR than to changes in GFR. The
correlation between GFR and water intake rate at 15°C but not at 30°C
suggests that GFR in sunbirds is more sensitive to water loading at low
ambient temperatures (Fig. 3).
Estimated water load (absorbed plus metabolic water) was higher at 15°C,
so this is not surprising. However the significantly higher mean GFR at
30°C (at least at low rates of water intake) is perplexing. It is possible
that evaporative water loss was higher at 15°C because of increased
metabolic demands (Powers,
1992
; Williams,
1996
) and thus that GFR was modulated in response to water deficit
when birds were feeding on concentrated sucrose solutions
(Williams et al., 1991
). The
observed decrease in ureteral urine osmotic concentration with increasing
water intake (Fig. 5B) supports
our contention that modulation of renal FWR, rather than of GFR, determines
renal water elimination in sunbirds. The low osmotic and glucose
concentrations of excreted fluid relative to ureteral urine
(Fig. 5) support the idea that
sunbirds are relying on modulation of ingested water absorption in their
gastrointestinal tract to reduce renal water loads, although this could also
result from post-renal modification of urine
(Braun, 1999
). Sunbirds and
hummingbirds lose exceptionally small amounts of glucose and electrolytes in
excreted fluid (McWhorter and
Martínez del Rio, 2000
;
Lotz and Martínez del Rio,
2004
). We posit that the energetic cost of recovering filtered
metabolites, and the potential for these processes to limit energy intake, are
much lower in sunbirds than in hummingbirds (see also
Nicolson and Fleming,
2003
).
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Acknowledgments |
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