Hummingbirds arrest their kidneys at night: diel variation in glomerular filtration rate in Selasphorus platycercus
1 Department of Zoology and Physiology, University of Wyoming, Laramie, WY
82071, USA
2 Department of Wildlife Ecology, University of Wisconsin, Madison, WI
53706, USA
3 Department of Biology, Technion Israel Institute of Technology,
Haifa 32000, Israel
* Author for correspondence (e-mail: bradley{at}uwyo.edu)
Accepted 11 August 2004
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Summary |
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Key words: hummingbird, Selasphorus platycercus, glomerular filtration rate, renal fractional water reabsorption, diurnal variation, phylogenetically independent contrast, nectarivory, glomerular intermittency
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Introduction |
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As a consequence of ingesting food that is principally water
(Baker, 1975), hummingbird
water fluxes range from one to seven times their body mass
(Mb) per day
(Martínez del Rio et al.,
2001
). Because hummingbirds absorb essentially all ingested water
that enters the gastrointestinal tract
(McWhorter and Martínez del Rio,
1999
), the renal system must play a critical role in maintaining
water balance. To avoid overhydration
(Faenestil, 1977
),
hummingbirds must rapidly eliminate a large fraction of ingested water. How do
hummingbird kidneys respond to these high water loads? Glomerular filtration
rate (GFR) sets the pace of water reabsorption and/or elimination by the
kidney. Although GFR appears to be less sensitive to water loading than to
water deprivation (Williams et al.,
1991
), we hypothesized that hummingbirds would increase GFR to
eliminate excess ingested water (McWhorter
et al., 2004
). A second complementary possibility is that renal
fractional water reabsorption (FWR) would decrease as water load increases
(Goldstein and Bradshaw,
1998
). Although the need to process large water loads may be, in
part, ameliorated by high evaporative water loss (EWL) rates
(Powers, 1992
), these water
losses can constitute a serious problem for hummingbirds when they are not
feeding. Their inability to concentrate urine
(Lotz and Martínez del Rio,
2004
) in combination with their high EWL rates suggests a
potentially acute risk of dehydration for hummingbirds. Water conservation is
therefore necessary when they are not feeding, for example at night and during
extended periods of flight.
How do hummingbirds reduce urinary water losses during non-feeding periods?
GFR decreases in response to water deprivation in several bird species
(Yokota et al., 1985;
Williams et al., 1991
;
Goldstein and Skadhauge,
2000
). Because hummingbirds do not feed at night, they are likely
to be dehydrated in the early morning and need to conserve water
(Fleming et al., 2004
). We
hypothesized that GFR would be lower during both the night and morning
relative to the evening (Goldstein and
Rothschild, 1993
). We also predicted that hummingbirds would
reduce GFR during an episode of water deprivation.
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Materials and methods |
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Experimental design
We conducted two experiments. The first investigated diel variation in
renal function in hummingbirds feeding naturally. The second experiment probed
the effect of food (and thus water) deprivation on renal function. In
experiment 1, we measured both renal FWR and GFR from roughly 18:00 to 19:59 h
(`evening'). In the same experiment, we measured GFR from 20:00 to 06:59 h
(`night') and from 07:00 to approximately 08:30 h (`morning'). Experiment 2
was conducted from approximately 11:00 to 15:00 h. In this experiment, we
first measured GFR in hummingbirds feeding voluntarily (`midday') and then
removed the sucrose solutions from their cages (`fast'). After this 1.5 h
fast, we returned the sucrose solutions and continued measuring GFR in freely
feeding hummingbirds.
During experiments, hummingbirds were housed individually in opaque
Plexiglas® cages (0.3x0.3x0.3 m). One cage panel was a
Mylar®-coated, one-way glass mirror. Each cage contained one perch that
was fitted with an insulated CuCn thermocouple (±0.1°C;
Omega Corporation, Stamford, CT, USA) and suspended from an electronic
balance (±0.01 g; Scout II; Ohaus Corporation, Florham Park, NJ, USA).
Hummingbirds were acclimated to these cages for 2 days before each trial.
Hummingbirds increase their food intake when the sugar concentration of
their food decreases (Martínez del
Rio et al., 2001). To vary ingested water loads, we fed
hummingbirds 292 and 876 mmol l1 sucrose solutions. The
fractional water contents of these solutions are 0.94 and 0.81, respectively.
In this report, `food intake' is the volume of sucrose solution ingested;
`water intake' is the ingested volume of preformed water; and `food/water'
refers to the sucrose solutions. Hummingbirds fed ad libitum on these
sucrose solutions for
4 h before a trial. We assigned trial order and
sucrose concentration randomly for each hummingbird, and hovering was required
to feed. All measurements were conducted at 24±1°C and the
photoperiod held constant.
GFR and renal FWR estimates in hummingbirds
We estimated GFR using a single injection of
[14C]L-glucose
(Chang et al., 2004) and a
modified version of the slope-intercept method
(Hall et al., 1977
;
Florijn et al., 1994
). Our
sole modification was that the marker disappearance rate from plasma is
matched by its rate of appearance in excreta. In addition to the assumption of
constant GFR made by the slope-intercept method
(Hall et al., 1977
;
Florijn et al., 1994
), our
modification assumes constant renal FWR. Therefore, our method of estimating
GFR can only be applied with a single compartment model of marker clearance.
This same modification was used by McWhorter et al.
(2004
). It allows the
investigation of renal function in unanesthetized free-flying birds.
Using our modified version of the slope-intercept method, three parameters
are needed to estimate GFR: (1) Qi, the quantity of marker
injected (disints min1, hereafter d.p.m.); (2)
Ai(0), the zero-time intercept concentration of marker in
plasma (d.p.m. ml1); and (3)
14C, the fractional
turnover rate of marker (h1). Marker distribution space
(SP; in ml) is then:
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![]() | (2) |
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Experimental measurements
SP, GFR and renal FWR
We injected each hummingbird in the pectoralis muscle with 9.25
x104 Bq of [1-14C]-L-glucose (Lot
#345-058-050; Moravek Biochemicals, Brea, CA, USA) dissolved in 10 µl of
deionized water. Injections were at 18:00 and
11:00 h for
experiments 1 and 2, respectively. After injections, we collected excreta
samples for >1 h. Following the initial excreta collection for experiment
1, we collected both a ureteral urine, using a close-ended polyethylene
cannula (Goldstein and Braun,
1989
), and blood sample (
10 µl). The blood sample was
obtained by clipping a single toenail. We collected these samples between
19:40 and 19:59 h. We resumed collecting excreta the following morning.
Fig. 1 illustrates our
procedure for experiment 1. In experiment 2, we collected excreta samples
before and after an
1.5 h food/water deprivation period. Excreta samples
were collected, using glass capillary tubes, from the wax paper that lined the
cage bottom. We counted d.p.m. (LS 6000IC; Beckman Coulter, Fullerton, CA,
USA) after dissolving injectate aliquots, excreta, ureteral urine and plasma
samples in 7.0 ml liquid scintillation cocktail (EcoLume; ICN Biomedicals,
Costa Mesa, CA, USA). All analyses were corrected for 14C
background, quench and chemiluminescence.
|
Body temperature (Tb)
Hummingbirds can enter torpor (Calder
and Calder, 1992). To find out if hummingbirds remained
normothermic during our measurements, we obtained estimates of
Tb using insulated CuCn thermocouples affixed to
each perch and digital thermometers (±0.1°C; HH506;
Omega
Corporation). The length of the perches (20 mm) forced birds to sit atop the
thermocouple so that it contacted the abdomen skin surface. We calibrated
perching temperatures with cloacal temperatures. Our criterion for hypothermia
was any Tb estimate lower than 39.0°C
(Calder and Calder, 1992
).
During the 11 h night phase, we measured Tb every 0.5 h;
for all other experiments, we monitored Tb
continuously.
Statistical analyses
Because the relationships between food intake and sugar concentration for
nectarivorous birds are well described by power functions
(Martínez del Rio et al.,
2001), we loge-transformed food intake and sucrose
concentration data. To determine the effect of food intake rate and subject on
GFR, we used repeated-measures analysis of variance (RM-ANOVA). To test for
differences among means, we used Tukey's Honest Significant Difference
(Tukey's HSD). In all other cases, we used linear models on non-transformed
data to assess significance. We report values as means ± 1
S.D.
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Results |
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Our estimate of SP in broad-tailed hummingbirds was 0.74±0.15 ml (N=9), which is approximately 20.6±4.2% of Mb. [14C]L-glucose equilibration time was 19±11 min (N=20). The integrals of the relationship between [14C] of excreta with time indicated that we recovered 97.3±1.1% of Qi (N=20). Because subject was a nonsignificant parameter in all our models (P>0.2), we removed this factor from all analyses.
Renal function and time of day
During the evening and morning, food intake rate increased significantly as
the sucrose concentration decreased (RM-ANOVA: F1,7=10.83,
P=0.0133, N=9). During the evening, food intake rates were
1.17±0.37 (N=5) and 0.56±0.14 ml h1
(N=4) on the 292 and 876 mmol l1 solutions,
respectively. Food intake rates during the morning were 1.11±0.39
(N=5) and 0.65±0.20 ml h1 (N=4) on
the 292 and 876 mmol l1 solutions, respectively. GFR during
these same time periods was not influenced by sucrose concentration (RM-ANOVA:
F1,7=1.54, P=0.25, N=9). We therefore
removed sucrose concentration from the analyses described in this section.
There were significant differences among our GFR estimates (RM-ANOVA:
F2,7=59.9, P<0.0001, N=9), with
Tukey's HSD tests revealing that GFREVENING,
GFR'NIGHT and GFRMORNING were all different from
each other (Fig. 2).
GFREVENING was 2.3±0.5 ml h1
(N=9), 110% of the allometric prediction
(GFR=0.013Mb0.76;
Bennett and Hughes, 2003
;
Fig. 2). There were no
differences in [14C] of excreta between the last evening and first
morning samples (paired t-test: t8=0.52,
P=0.62, N=9; Fig.
1) and GFR'NIGHT was 0.1±0.2 ml
h1 (N=9), suggesting an overnight interruption of
whole-kidney GFR (Fig. 2). Our
GFR'NIGHT estimate was not different from 0 (t-test:
t8=0.83, P>0.2, N=9).
GFRMORNING was 0.9±0.6 ml h1
(N=9) and was lower than GFREVENING by a factor of 2.6
(Fig. 2).
|
Contrary to our prediction, water intake rate did not influence GFR during the evening or morning (linear regression: evening, P=0.27, N=9; morning, P=0.34, N=9; Fig. 3A). However, during the evening, renal FWR decreased linearly as water intake rate increased (y=0.13x+0.89, r2=0.66, P=0.03, N=7; Fig. 3B).
|
GFR during food/water deprivation
At midday, food intake rate increased significantly as sucrose
concentration decreased (RM-ANOVA: F1,7=30.44,
P=0.0009, N=9). These intake rates were 0.9±0.3
(N=5) and 0.4±0.2 ml h1 (N=4) on
the 292 and 876 mmol l1 solutions, respectively. GFR,
however, was not affected by sucrose concentration (RM-ANOVA:
F1,7=0.75, P=0.42, N=9). Following the
1.5 h food/water deprivation period, sucrose concentration did not affect
food intake rate (RM-ANOVA: F1,7=0.94, P=0.36,
N=9) or GFR (RM-ANOVA: F1,7= 0.00,
P=0.9930, N=9). We removed sucrose concentration from our
analyses presented in this section.
Before food/water removal, GFRMIDDAY was 1.8±0.4 ml h1; (N=9; Fig. 4). During the food/water deprivation period, GFR'FAST (0.9±0.5 ml h1; N=9) was 50% lower than GFRMIDDAY (Fig. 4). When we returned the food/water, GFRRETURNED was 1.4±1.0 ml h1 (N=9; Fig. 4). Our GFR estimates differed significantly (RM-ANOVA: F2,7=9.79, P=0.0094, N=9), but Tukey's HSD tests showed that these differences were only between GFRMIDDAY and GFR'FAST; both GFRMIDDAY and GFR'FAST were not significantly different from GFRRETURNED (Fig. 4). GFRMIDDAY increased significantly as water intake rate increased (y=0.78x+1.36, r2=0.52, P=0.03, N=9; Fig. 5A). However, GFRRETURNED was not influenced by water intake rate (linear regression: P=0.71, N=9; Fig. 5B).
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|
Tb and Mb estimation
Hummingbirds were normothermic throughout all experimental trials except at
night, where they spent 10.4±5.3% of the 11 h dark phase hypothermic
(N=10). The rate of change in Mb
(Mb) during the night was 0.04±0.01 g
h1 (N=10) and decreased linearly as time spent
hypothermic increased (y=0.02x+0.06,
r2=0.69, P=0.0028, N=10;
Fig. 6). During the food/water
deprivation period,
Mb was 0.25±0.11
g h1 (N=8) and was significantly higher than
overnight
Mb (paired t-test:
t7=4.94, P=0.0017, N=8).
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Discussion |
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Diurnal variation in renal function
Broad-tailed hummingbirds displayed significant diurnal variation in GFR.
They had a low GFR in the morning (0.9±0.6 ml h1;
Fig. 2), an intermediate GFR at
midday (1.8±0.4 ml h1;
Fig. 4) and a high GFR in the
evening (2.3±0.5 ml h1;
Fig. 2). It is likely that
hummingbirds filter slowly in the morning to conserve water and hydrate after
a night of water losses (Fleming et al.,
2004). Because intake rates during the day are sufficient for
birds to hydrate within a few hours
(Collins, 1981
), the
observation of a gradual increase in GFR throughout the day is perplexing but
seems to be a pattern shared by other birds. Goldstein and Rothschild
(1993
) reported a similar
pattern in song sparrows (Melospiza melodia).
GFR during food/water deprivation
When hummingbirds were deprived of food/water, they reduced mean GFR
(Fig. 4). This finding is
consistent with the responses to water deprivation observed in other birds
(Williams et al., 1991;
Goldstein and Skadhauge,
2000
). There is, however, one notable difference. In most of the
other species examined, the reduction in GFR occurs progressively over a
period of several days (Williams et al.,
1991
). Yet, hummingbirds modulated GFR within 1.5 h of deprivation
(Fig. 4). This observation is
not surprising, but it illustrates that GFR in hummingbirds is particularly
sensitive and responsive to food/water deprivation. Although broad-tailed
hummingbirds reduced mean GFR significantly during the deprivation period,
they displayed a wide range of responses
(Fig. 7). The reduction in mean
GFR ranged from moderate (
25%; Fig.
7B) to almost complete (
90%;
Fig. 7C). This variation may be
explained by differences in water balance status among birds prior to
food/water removal.
|
GFR during the night
Although our observation is not the first evidence of intermittent renal
filtration in birds (Braun and Dantzler,
1972; Goldstein,
1993
), it represents the first account of what appears to be
interrupted whole-kidney GFR in a normothermic bird. Our observation of
arrested nighttime renal filtration in broad-tailed hummingbirds (Figs
1,
2) is noteworthy for two
reasons. First, because hummingbirds were normothermic for
90% of the
night, the cessation of renal filtration was not a result of reduced pressure
in the renal arteries due to hypothermia
(Glahn et al., 1993
). We
cannot, however, rule out a nocturnal dip in systemic blood pressure
(Miyazaki et al., 2002
).
Second, a sudden decrease in whole-kidney GFR disrupts homeostatic processes
and can have pathological consequences
(Anderson and Schier, 2001
).
How do hummingbirds cope with arresting whole-kidney GFR? This is an
intriguing question, but one that is presently open. The ability to interrupt
GFR, however, is better understood.
In birds, the reduction in GFR is believed to result from vasoconstriction
of the pre-glomerular arterial vessels that supply `loopless' nephrons
(Dantzler, 1989). This
vasoconstriction is mediated by arginine vasotocin
(Braun, 1976
;
Giladi et al., 1997
;
Goecke and Goldstein, 1997
).
In hummingbirds, more than 99% of all nephrons are loopless
(Casotti et al., 1998
).
Consequently, hummingbirds cannot concentrate urine
(Lotz and Martínez del Rio,
2004
), but they can reduce urinary water losses by decreasing GFR.
This mechanism has a potential drawback. In mammals, the cessation of
filtration due to vasoconstriction of afferent arterioles can lead to damage
of renal cells from ischemia (Hays,
1992
). How do hummingbirds nourish these cells when GFR is
suspended?
Birds, like other vertebrates with intermittent glomerular filtration, have
a renal portal system (Dantzler,
1989; Smith et al.,
2000
). Dantzler
(1989
) hypothesized that this
renal portal circulation may perfuse nonfiltering loopless nephrons in the
absence of a post-glomerular blood supply. Additionally, other researchers
have noted glomerular bypasses in the arterial vasculature of the avian kidney
(Siller and Hindle, 1969
;
Kurihara and Yasuda, 1975
).
Although these features may allow the perfusion of renal cells when filtration
is suspended, their relative importance is unknown.
GFR and nectarivory
One would expect high GFRs in animals with the astounding water intakes
that characterize nectarivorous birds
(Yokota et al., 1985;
McWhorter et al., 2004
).
Accordingly, our estimate of GFR in broad-tailed hummingbirds exceeded the
allometric prediction (Table
1). The other available data for nectarivorous birds, however,
suggest that GFRs are lower than expected
(Table 1;
Bennett and Hughes, 2003
;
McWhorter et al., 2004
). To
find out if diurnal GFR is higher or lower than expected from
Mb in nectarivorous birds
(Calder and Braun, 1983
), we
used phylogenetically independent contrasts (PICs) and the method proposed by
Garland and Adolph (1994
). We
used the DNADNA hybridization tapestry of Sibley and Ahlquist
(1991
) as a hypothesis for the
phylogenetic relationships and evolutionary distances of birds
(Fig. 8A). Briefly, we
constructed a regression through the origin with all the standardized
phylogenetic contrasts of log10(Mb) and
log10(GFR). This regression excluded the nectarivorous species. We
then determined whether the contrasts including nectarivorous birds were
within or outside the 95% confidence interval for this relationship.
|
|
Before phylogenetic correction, the relationship between
Mb (g) and GFR (ml h1) was described by
a power function (y=0.85x0.74,
r2=0.90, N=28;
Fig. 8B). The exponent obtained
using PICs (0.72±0.10; N=23;
Fig. 8C) was similar to that
obtained from the phylogenetically uncorrected regression (0.74±0.26;
Fig. 8B). The points for the
contrasts that included the clades of nectarivorous birds fell within the 95%
confidence interval for the regression line. Despite the high water fluxes
that characterize nectarivorous birds, these animals do not seem to have
unusual rates of glomerular filtration. This conclusion, however, must be
treated with caution. An overnight mean GFR of 0 may qualify broad-tailed
hummingbirds as outliers. If labile GFRs
(Goldstein and Rothschild,
1993; present study) are common among birds, the time of GFR
measurement cannot be ignored in comparative analyses.
Hummingbird illustrations are by Annie Hartman Bakken. We owe a debt to two anonymous reviewers, whose keen criticisms helped us to measurably improve an earlier draft of this manuscript. We thank Dr Graham Mitchell for his insightful comments and mammalian bias, which reminded us of the important observation that birds are not mammals. Our capture, care and experimental protocols were approved by the University of Wyoming Animal Use and Care Committee. Hummingbirds were collected under United States Fish & Wildlife and Wyoming Game & Fish permits issued to C.M.R. Support for this research was provided by grants from the National Science Foundation (NSF; IBN-0110416) and the National Institutes of Health/National Center for Research Resources (RR-16474) awarded to C.M.R. and B.H.B., respectively; T.J.M. was supported by an NSF grant to William H. Karasov (IBN-0216709). B.H.B. extends his thanks to Dr Lloyd A. and Patricia L. Bakken.
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