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Apparent Absorption Efficiencies of Nectar Sugars in the Cape Sugarbird, with a Comparison of Methods

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Apparent Absorption Efficiencies of Nectar Sugars in the Cape Sugarbird, with a Comparison of Methods 106 Apparent Absorption Ef®ciencies of Nectar Sugars in the Cape Sugarbird, with a Comparison of Methods Susan Jackson1,* was artifactual, and we do not recommend use of this method. Susan W. Nicolson1 Apparent absorption ef®ciencies calculated with method 2 un- Ben-Erik van Wyk2 derestimated true absorption ef®ciency, because refractometry 1Zoology Department, University of Cape Town, measures nonsugar solutes, but this error is biologically sig- Rondebosch 7700, South Africa; 2Botany Department, Rand ni®cant only when ef®ciencies are low. Afrikaans University, P.O. Box 524, Auckland Park 2006, Johannesburg, South Africa Accepted by G.K.S. 8/15/97 Introduction Nectarivorous birds consume dilute solutions of sucrose, fruc- ABSTRACT tose, and glucose and apparently assimilate these sugars very Nectarivore sugar preferences and nectar composition in the ef®ciently. Absorption ef®ciencies (AE) of 97%±99.5% for the Cape Floristic Kingdom (southern Africa) differ from trends three sugars have been measured in three families of specialized reported for analogous systems in America and Europe in that nectarivores: American hummingbirds (Hainsworth 1974; Kar- sugarbirds and sunbirds show no aversion to sucrose, which asov et al. 1986; MartõB nez del Rio et al. 1988; MartõB nez del Rio is the dominant nectar sugar in many of their food plants. To 1990b), Australian honeyeaters (Collins and Morellini 1979; elucidate the physiological bases (if any) of nectarivore sugar Collins et al. 1980), and African sunbirds (Lotz and Nicolson preferences, we determined apparent sugar absorption ef®- 1996). Of the above studies, two (MartõB nez del Rio 1990b; Lotz ciencies in a passerine endemic to this region, the Cape sugar- and Nicolson 1996) reported data for all three sugars, whereas bird Promerops cafer. Apparent absorption ef®ciencies for the the remainder used single sugars (sucrose or glucose). three major nectar sugars, sucrose, glucose, and fructose, were The ability to absorb sucrose is not ubiquitous among birds extremely high (ú 99%), as in other specialized avian nectari- and is, not surprisingly, linked to sugar preferences. Frugivo- vores. Xylose, a pentose sugar recently reported in the nectar rous passerines show apparent absorption ef®ciencies (AE*) of some Proteaceae, was absorbed and/or metabolized inef®- for sucrose that range from 0% (American robin, Turdus mi- ciently, with a mean of 47.1% of ingested sugar recovered in gratorius, and European starling, Sturnus vulgaris; MartõB nez del cloacal ¯uid. We did not measure the proportions of xylose Rio and Stevens 1989; Karasov and Levey 1990) to 61% (cedar that were absorbed and/or metabolized. We also compared waxwings, Bombycilla cedrorum; MartõB nez del Rio et al. 1989). three methods of estimating absorption ef®ciency: (1) measure- These ef®ciencies are affected by differing activities of the intes- ments of total sugar in cloacal ¯uid with refractometry, without tinal disaccharidase sucrase, which must hydrolyze sucrose into correction for differences between volumes of ingesta and ex- its components glucose and fructose before absorption can creta; (2) the same measurements combined with correction occur (MartõB nez del Rio et al. 1989; MartõB nez del Rio 1990a), for volume differences; and (3) HPLC analyses quantifying and by passage rates of fruit pulp through the gut, which individual sugars in cloacal ¯uid, with correction for volume in¯uence the time available for this hydrolysis. Variation in differences. Refractometry has been frequently used in previous AE*s of sucrose is matched by sucrose aversions of varying studies. For all sugars except xylose, method 1 yielded results intensity (Schuler 1983; MartõB nez del Rio et al. 1989; Brugger similar to those obtained with method 2, but the convergence 1992). Two of the three species of American nectar-consuming passerines that have been studied also avoid sucrose; yellow- *To whom correspondence should be addressed. Present address: Department breasted chats, Icteria virens, and yellow-winged caciques, Caci- of Physiology, Wits Medical School, 7 York Road, Parktown 2193, South Africa; cus melanicterus, prefer hexoses to sucrose, whereas streak- E-mail: [email protected]. backed orioles, Icterus pustulatus, are indifferent (MartõB nez del Physiological Zoology 71(1):106±115. 1998. q 1998 by The University of Rio et al. 1992). These preferences, coupled with the fact that Chicago. All rights reserved. 0031-935X/98/7101-9685$03.00 passerine-pollinated plants in the genera Erythrina, Campsis, 9g11$$ja08 12-23-97 08:14:56 pzas UC: PHYS ZOO Absorption Ef®ciencies in Nectarivorous Birds 107 and Fuchsia produce hexose-dominated nectar in the Old 4.2 g each of sucrose, glucose, and fructose plus 2.5 g of Com- World, led to a prediction that nectarivorous passerines in the plan (Boots Pharmaceuticals, Isando, South Africa) per 100 Old World, like those in America, might prefer hexoses to mL of water. Complan is made from instant skim milk powder, sucrose (MartõB nez del Rio et al. 1992). However, recent ®ndings corn syrup solids, vegetable oil, sucrose, lecithin, vitamins, and necessitate revision of this comparison. Specialized passerine minerals, and its composition per 100 g is as follows (values nectarivores from southern Africa, such as lesser double-col- calculated per wet weight): energy content, 1,818 kJ; protein, lared sunbirds, Nectarinia chalybea, and Cape sugarbirds, Pro- 20 g; fat, 13.8 g; carbohydrates, 56.7 g; vitamin A, 2,682 IU; merops cafer, are not averse to sucrose (Lotz and Nicolson vitamin B6, 1.5 mg; vitamin B12, 4.5 mg; vitamin C, 72.4 mg; 1996; Jackson et al. 1998), and the nectars of many of these vitamin D, 150.9 IU; vitamin E, 8.6 IU; thiamine, 1.44 mg; birds' food plants (e.g., Erica spp.; Barnes et al. 1995) are ribo¯avin, 1.76 mg; Ca, 720 mg; Fe, 7.09 mg; biotin, 49.1 IU; sucrose-dominant. folic acid, 192 mg; pantothenic acid, 4.7 mg; niacin, 10.9 mg; The pentose sugar xylose was recently discovered in the P, 587.3 mg; I, 185.5 mg; Mg, 75.8 mg; Cu, 0.7 mg; Z, 7.1 mg; nectar of Protea and Faurea species of the Proteaceae, a major Mn, 0.9 mg; Na, 292.9 mg; and choline, 80.4 mg. The sugar ornithophilous family in southern Africa and Australia. Xylose concentration of this solution is thus 10.95%. Unless otherwise comprises up to 39% of total nectar sugar in some species of stated, all references to relative solute masses and to solution these two genera (van Wyk and Nicolson 1995) but is rejected concentrations (%) are on a weight : weight basis (weight by both N. chalybea and P. cafer in choice tests (Lotz and solute : total weight solution). The solution was presented to Nicolson 1996; Jackson et al. 1998). This is surprising, because the birds ad lib. in plastic feeders and was changed twice daily. P. cafer has coevolved with the Proteaceae and is one of only At the end of the experiments, the birds were banded and two avian nectarivores endemic to the Cape Floristic Kingdom released at the site of capture. Additional housing details are of southern Africa (fynbos). given in Jackson et al. (1998). On the basis of the above recently acquired information about their sugar preferences and the nectar composition of Experimental Procedure their food plants, we predicted that Cape sugarbirds would not show the poor sucrose AEs suggested by MartõB nez del Rio et During tests for AE* (feeding experiments), we measured the al. (1992) for passerine nectarivores. We tested our prediction volumes of food intake and of cloacal ¯uid production. To by comparing AE*s of sucrose, glucose, and fructose in this permit measurement of exact excreta volumes, we con®ned species. We included xylose as a fourth sugar in our compari- birds to cylindrical cages (diameter 36 cm, height 50 cm). sons, because of its presence in Protea nectar. While in these cages, birds fed ad lib. from glass feeders made The secondary aim of our study was a methodological com- from 25-mL pipettes that permitted measurement of volumes parison. Published studies of sugar AE*s in nectarivores have remaining and, hence, estimation of volumes of liquid con- employed different methods of measurement of excreted sug- sumed to the nearest 0.05 mL. The bottom ends of the pipettes ars. We therefore compared two commonly used refractometry were expanded to form glass bulbs 2.5 cm in diameter, with methods of estimating sugar AE*s with a third technique, con- circular holes of diameter 4±5 mm. These drinking apertures current measurements of cloacal ¯uid sugars with HPLC. were surrounded by a 3-mm-wide ring of red nail varnish to enhance their visibility. The protocol was as follows. Between 1700 and 1800 hours, Material and Methods we transferred individual birds from the holding cages to the cylindrical cages, weighing the birds in the process. At this Bird Capture and Maintenance time, we switched foods from the maintenance diet to a 20% Ten adult female Cape sugarbirds were caught during their sugar solution. Between 1320 and 1350 hours the following nonbreeding season (March±April 1995 and October 1995) in day, we noted the level of liquid in the feeders, replaced these mist nets and were housed separately in holding cages measur- with fresh feeders containing a measured volume of the same ing 70 1 80 1 40 cm and covered with plastic-coated screen sugar solution, and slipped a plastic tray containing a 1.5-cm mesh (size, 2 mm). Only females were used because the long layer of liquid paraf®n under each cage. Both collection of tails of male sugarbirds would hamper their movements in the cloacal ¯uid and measurements of food consumption com- cages, and there is no a priori evidence supporting a sex- menced and ended simultaneously; after exactly 4 h, we termi- linked difference in diet or sugar AE*s.
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