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First published online November 19, 2004
Journal of Experimental Biology 207, 4383-4391 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01238

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Hummingbirds arrest their kidneys at night: diel variation in glomerular filtration rate in Selasphorus platycercus

Bradley Hartman Bakken^1,*, Todd J. McWhorter², Ella Tsahar³ and Carlos Martínez del Rio¹

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

View larger version (15K): [in a new window]   Fig. 1. Semi-logarithmic plot of data from one representative broad-tailed hummingbird illustrating (1) our protocol for estimating evening, night and morning glomerular filtration rates (GFR) and evening renal fractional water reabsorption and (2) that 14C-labeled L-glucose appearance in excreta with time follows single-compartment, first-order kinetics. This particular humming bird had an evening and morning GFR of 1.9 and 1.1 ml h–1, respectively (determined using equation 2); night GFR for this bird was 0.0 ml h–1 (determined using equation 4). Although data of [14C] of excreta are loge-transformed here for clarity, our analyses were performed on non-transformed data (Motulsky and Ransnas, 1987). We injected this particular hummingbird at 17:43 h and collected excreta samples until 19:43 h. Ureteral urine and plasma samples were taken from this hummingbird at 19:45 and 19:47 h, respectively. Our morning excreta collections suggested that whole-kidney GFR was interrupted overnight: there were no differences between the [14C] of excreta in the first morning and last evening samples.

View larger version (10K): [in a new window]   Fig. 2. Diel variation in glomerular filtration rate (GFR) in broad-tailed hummingbirds. Our GFR estimates for the evening, night and morning were 2.3±0.5, –0.1±0.2 and 0.9±0.6 ml h–1 (N=9), respectively, and were significantly different from each other. GFRMORNING was lower than GFREVENING by a factor of 2.6, and GFR'NIGHT was not different from 0. GFREVENING was approximately 110% of the allometric prediction (GFRPREDICTED=2.1 ml h–1; Bennett and Hughes, 2003).

View larger version (14K): [in a new window]   Fig. 3. Renal fractional water reabsorption (FWR) is responsive to water loading in broad-tailed hummingbirds. (A) There was no relationship between water intake rate and glomerular filtration rate (GFR) during the evening (filled circles) or morning (open circles). (B) Hummingbirds decreased renal FWR to dispose of excess ingested water during the evening (y=–0.13x+0.89, r2=0.66, N=7).

View larger version (11K): [in a new window]   Fig. 4. Glomerular filtration rates (GFR) in broad-tailed hummingbirds before, during and after a 1.5 h food/water deprivation episode. During food/water removal, mean GFR was significantly reduced relative to the pre-removal period (GFR'FAST and GFRMIDDAY were equal to 0.9±0.5 and 1.8±0.4 ml h–1, respectively; N=9). When we returned the food/water, GFRRETURNED (1.4±1.0 ml h–1; N=9) was not different from either GFRMIDDAY or GFR'FAST. GFRPREDICTED is equal to 2.1 ml h–1 (Bennett and Hughes, 2003).

View larger version (13K): [in a new window]   Fig. 5. Glomerular filtration rate (GFR) is responsive to water loading in broad-tailed hummingbirds. (A) During midday, prior to food/water removal, GFR increased linearly with increased water intake rate (y=0.78x+1.36, r2=0.52, N=9). (B) When we returned the food/water, following the 1.5 h deprivation period, there was no relationship between water intake rate and GFR.

View larger version (16K): [in a new window]   Fig. 6. Overnight body mass (Mb) losses in broad-tailed hummingbirds are influenced by the time spent hypothermic. The rate of change in body mass (Mb; g h–1) during the night decreased as time (h) spent hypothermic increased (y=–0.02x+0.06, r2=0.69, N=10).

View larger version (19K): [in a new window]   Fig. 7. Despite the overall trend (Fig. 4), broad-tailed hummingbirds showed heterogeneous responses to food/water deprivation. Values associated with each regression line are glomerular filtration rate (GFR; ml h–1) estimates. Solid regression lines denote estimates obtained using equation 2; broken regression lines denote estimates made using equation 4. Although data of [14C] of excreta are loge-transformed here for clarity, our analyses were performed on non-transformed data (Motulsky and Ransnas, 1987). (A) Data from one representative hummingbird. (B) Data from one hummingbird illustrating that GFR'FAST was not always substantially reduced (25%). (C) Data from one hummingbird showing a GFR'FAST that was considerably reduced (90%). The hummingbirds in B and C exhibited a GFRRETURNED greater than GFRMIDDAY.

View larger version (36K): [in a new window]   Fig. 8. Do nectarivorous birds have different diurnal glomerular filtration rates (GFRs) compared with equal-sized birds with other dietary habits? (A) Phylogeny of avian species with GFR data (Table 1). (B) The relationship between body mass (Mb; g) and GFR (ml h–1) was described by a power function with an exponent equal to 0.74±0.26 (N=28). (C) The phylogenetically independent contrasts between log10(Mb) and log10(GFR) for nectarivorous birds (filled circles) are within the 95% confidence interval (represented by the broken lines) of the regression line relating the standardized contrasts of log10(Mb) and log10(GFR) for species with other dietary habits. The exponent of this phylogenetically corrected relationship equals 0.72±0.10 (N=23).