Physiological Basis and Ecological Consequences of Sugar Preferences in Cedar Waxwings

-In paired preference tests Cedar Waxwings (Bombycilla cedrorum) preferred glucose, fructose, and a mixture of glucose and fructose over sucrose. Preferences for simple sugars were ranked as: glucose = glucose + fructose > fructose > sucrose. To be absorbed by the brush border membrane, sucrose is hydrolyzed into its monosaccharide components, glucose and fructose. Because Cedar Waxwings preferred glucose and fructose over sucrose, we predicted that they would be sucrase deficient. We tested this by measuring the efficiency with which Cedar Waxwings absorbed glucose, fructose, and sucrose in vivo, and by directly assaying for sucrase in preparations of intestinal mucosa. Absorption efficiencies measured using a double isotope method falsified our prediction. Cedar Waxwings were able to absorb sucrose (absorption efficiency = 61% ? 1.2), but absorbed glucose and fructose more efficiently (absorption efficiencies = 92%? 1.5 and 88%? 3.5, respectively). The presence of sucrase activity in Cedar Waxwings was confirmed in preparations of intestinal mucosa. Using a radioactively labeled inert marker, we found very short mean residence times of food particles in the gut of Cedar Waxwings (ca. 41 min). Because sucrose has to be hydrolyzed before it can be absorbed, the efficiency with which it is utilized may be hindered by the extremely fast passage rates in Cedar Waxwings. We suggest that the preference of Cedar Waxwings for monosaccharides over sucrose is due to the relative inefficiency of sucrose absorption. However, absorption efficiencies cannot explain the strong preference of glucose over fructose. In consequence, neither the caloric value of the sugars nor the absorption efficiency was adequate to explain the sugar preferences exhibited by Cedar Waxwings. We conclude that the preferences for simple sugars appear to be determined by the complex interaction between digestive constraints, postingestional effects, and taste. Received 19 January 1988, accepted 10 August 1988. THE disaccharide sucrose and the monosaccharide hexoses, fructose and glucose, are the most common simple sugars in fruit pulp and nectar (Chan and Kwok 1975; Baker and Baker 1983, 1986; Reid and Freeman MS). Hummingbird-pollinated plants produce nectars with a high proportion of sucrose whereas passerinepollinated plants produce nectars with a low proportion of sucrose and high proportion of hexoses (Cruden and Toledo 1977; Baker and Baker 1982, 1983). Small bird-dispersed fruits, which are typically consumed by passerines, contain mainly hexoses, whereas cultivated fruits used for human consumption tend to have high sucrose contents (Baker and Baker 1986, pers. comm.). These differences in sugar composition remain largely unexplained. It has been postulated that chemical characteristics of nectar and fruit pulp evolved in response to the 3Present address: Department of Zoology, University of Florida, Gainesville, Florida 32611 USA. preferences of pollinators and seed dispersers (Baker and Hurd 1968, Howell 1979, Levey 1987). With few exceptions (Hainsworth and Wolf 1976, Stiles 1976), the sugar preferences of birds that feed on nectar and fruit are unknown. Glucose, fructose, and sucrose have different modes of intestinal transport, and produce different metabolic effects after ingestion and absorption (Sestoft 1983). Even though they are similar chemically and in caloric value, these sweet substances may not be biologically equivalent. The European Starling (Sturnus vulgaris) rejects sucrose solutions but readily accepts solutions of fructose and glucose (Schuler, 1983). Sucrose aversion in the Starling is associated with a deficiency of the intestinal enzyme sucrase which hydrolyzes sucrose into fructose and glucose (Martinez del Rio et al. 1988). Animals that lack sucrase cannot digest and absorb sucrose. Consequently, the presence of undigested sucrose in the intestine of these animals can cause severe osmotic diarrhea. In this way, 64 The Auk 106: 64-71. January 1989 This content downloaded from 207.46. 13.20 on Tue, 27 Dec 2016 17:57:48 UTC All use subject to http://about.jstor. org/terms January 1989] Sugar Preferences in Cedar Waxwings 65 the absence of intestinal sucrase can be associated with aversion for sucrose (Sunshine and Kretchmer 1964). We studied the sugar preferences of the Cedar Waxwing (Bombycilla cedrorum), one of the most heavily frugivorous birds in temperate North America (Martin et al. 1951), and analyzed the influence of taste and postingestional factors on these preferences. Because most birddispersed fruits in temperate North America are hexose-dominated (I. Baker and H. G. Baker in litt.), we predicted that Cedar Waxwings would prefer glucose and fructose over sucrose. We also hypothesized that this preference would be a result of sucrase deficiency. We examined these hypotheses by simple choice tests; by estimating the efficiency with which the birds digested and absorbed sucrose, glucose, and fructose in vivo; and by assaying for sucrase in preparations of intestinal mucosa.