How do Frugivores Process Fruit? Gastrointestinal Transit and Glucose Absorption in Cedar Waxwings (Bombycilla Cedrorum)

-We used image-intensification radiology to examine gut function in six Cedar Waxwings (Bombycilla cedrorum) fed artificial fruits that contained barium-labeled pulp and seeds. Despite the absence of an anatomical crop, waxwings were able to store fruits orad to the gizzard in a distensible portion of the esophagus. By doing so, they were able to increase meal sizes above what their gizzards could contain at any one time. Thus, they could partially overcome the digestive bottleneck that results from a bulky diet. Gizzard contraction increased in frequency with gizzard fullness. Seeds and pulp were separated in the gizzard; most pulp passed into the intestine before the seeds. Once in the intestine, however, seeds moved especially quickly (x = 0.14 cm/s) into the rectum. Both pulp and seeds resided for a relatively long time in the rectum, where antiperistalsis was clearly visible. Unlike other birds that have been studied, the functions of antiperistalsis in waxwings probably do not include cecal filling, since ceca of waxwings are minute. We hypothesize that the function of antiperistalsis in waxwings (and other fruit-eating birds) is to mix digesta in the intraluminal zone adjacent to the rectal mucosa, thereby increasing nutrient absorption. This hypothesis is consistent with the observation that fruit-eating birds typically have low digestive efficiencies. In particular, absorption of nutrients in the rectum may be important, given that digesta therein may still contain significant amounts of nutrients. Indeed, active uptake of D-glucose, a primary constituent of fruit pulp, was as high in the rectum as elsewhere in the gut. We also found that waxwings typically defecated only the distal 50% of rectal contents. Presumably, digesta in the proximal portion was higher in nutrients and so was retained longer for more thorough absorption. This pattern contrasts to most other vertebrates in which the rectum empties completely and sugar uptake in the rectum is negligible. We suggest that functional adaptations to frugivory (i.e. how fruit is processed) are likely more important than structural adaptations. Received 9 May 1991, accepted 15 December 1991. FRUITS ARE a unique food source that combine a large proportion of well-protected seeds with a nutritious, easily digestible covering. Presumably, fruit-eating birds possess gut adaptations that allow them to efficiently process this mix of high and low digestibility components. Many studies have attempted to find such adaptations, but there is little agreement among them. For example, some researchers report that fruit-eating birds have especially short guts (e.g. Walsberg 1975, Pullainen et al. 1981), others that they have long guts (e.g. Al-Dabbagh et al. 1987, Jordano 1987), and yet others that they have guts of normal length (Herrera 1984). Apparently, there are few (if any) general morphological adaptations of avian guts to frugivory. The major adaptations may be functional, relating to how fruit is processed rather than to gut structure (Herrera 1984, Karasov and Levey 1990). Little is known about functioning of the gut in fruit-eating birds. Most studies have simply treated birds as "black boxes"-patterns of ingestion and defecation are compared, then transit and digestive processes are inferred (Johnson et al. 1985, Bairlein 1987, Worthington 1989, Levey and Grajal 1991). For example, retention time is one of the most important parameters of food processing (Van Soest 1982, Penry and Jumars 1987). The statistic that is usually reported is the mean time from ingestion to defecation. Yet, what is needed for accurate interpretation is the time a meal spends in each segment of the gut (Penry and Jumars 1987, Martinez del Rio and Karasov 1990). This type of information can yield new insights. In the case of hummingbirds, for example, if cropemptying time determines foraging bout frequency, these birds would likely be energy maximizers rather than foraging-time minimizers (Diamond et al. 1986, Karasov et al. 1986). Image-intensification radiology (IIR) allows