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First published online March 14, 2005
Journal of Experimental Biology 208, 1025-1034 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01495

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Can birds be ammonotelic? Nitrogen balance and excretion in two frugivores

Ella Tsahar^1,*, Carlos Martínez del Rio², Ido Izhaki³ and Zeev Arad¹

¹ Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel
² Department of Zoology and Physiology, University of Wyoming, Laramie WY, 82071, USA
³ Department of Biology, University of Haifa at Oranim, K. Tivon 36006, Israel

View larger version (18K): [in a new window]   Fig. 1. The effect of sugar concentration on sugar intake. Tristram's grackles (A) and Yellow-vented bulbuls (B) exhibit a typical intake response: their sugar intake (top) was independent of sugar concentration. They decrease volume of intake (I) (bottom) as the sugar concentration in food (C) increases (Martínez del Rio et al., 2001). The intake response of both species is well described by power functions (I=543C-0.85, r2=0.94 and I=285C-0.85, r2=0.79 for Tristram's grackles and yellow-vented bulbuls, respectively). Closed circles, low protein concentration in diet; open circles, high protein concentration in diet (see text for the concentration values). Because there were no significant effects of protein content on volumetric intake the power functions were fitted to pooled data.

View larger version (16K): [in a new window]   Fig. 2. Apparent nitrogen retention increased significantly with nitrogen intake in both species. Minimal nitrogen requirements (MNR) and total endogenous nitrogen losses (TENL) were determined using the x and y intercepts of the least-squares linear regression, respectively. Yellow-vented bulbuls: y=0.78x-5.4, r2=0.99, F1,8=797, P<0.0001; y=0.86x-3.4, r2=0.99, F1,8=7208, P<0.0001, first and third day, respectively. Tristram's grackle: y=0.8x-19.8, r2=0.98, F1,6=277.6, P<0.0001; y=0.8x-11, r2=0.97, F1,6=231.2, P<0.0001, first and third day, respectively. TENL in both species decreased significantly between the first and third day of experiment. In yellow-vented bulbuls, but not in Tristram's grackles, MNR also decreased on the third day. MNR and TENL values are presented in Table 2. Open squares and solid lines represent measurements on day 1 and closed squares and broken lines represent measurements on day 3.

View larger version (13K): [in a new window]   Fig. 3. Effect of water and nitrogen intake on excreta. In yellow-vented bulbuls, both water and protein intake had a significant effect on the proportion of nitrogen excreted as ammonia. The proportion of nitrogen excreted as ammonia was positively correlated with water intake (A: y=0.6x+18.4, r2=0.54, F1,18=21.3, P=0.0002). The residuals of this relationship were negatively correlated with protein intake (B: y=-0.03x+5.5, r2=0.23, F1,18=5.4, P=0.03).

View larger version (21K): [in a new window]   Fig. 4. Chemical composition of nitrogen excreted. Yellow-vented bulbuls were ammonotelic in roughly half of our measurements, whereas all but one of Tristram's grackles were uricotelic. Open circles, ammonia; closed circles, urate.

View larger version (15K): [in a new window]   Fig. 5. The effect of protein intake on plasma uric acid. For a given protein intake, the plasma concentration of uric acid was significantly higher in yellow-vented bulbuls (open circles) than in Tristram's grackles (closed circles). Plasma uric acid concentration was positively correlated with protein intake in Tristram's grackles, (y=0.0004x+1.07, F1,6=11.22, r2=0.65, P=0.015), but not in yellow-vented bulbuls (F1,5=0.07, P=0.8). We standardized protein intake by mass0.75 to place both species along an axis of similar magnitude.