Anecdotal evidence suggests that birds have smaller intestines than mammals. In the present analysis, we show that small birds and bats have significantly shorter small intestines and less small intestine nominal (smooth bore tube) surface area than similarly sized nonflying mammals. The corresponding >50% reduction in intestinal volume and hence mass of digesta carried is advantageous because the energetic costs of flight increase with load carried. But, a central dilemma is how birds and bats satisfy relatively high energy needs with less absorptive surface area. Here, we further show that an enhanced paracellular pathway for intestinal absorption of water-soluble nutrients such as glucose and amino acids may compensate for reduced small intestines in volant vertebrates. The evidence is that L-rhamnose and other similarly sized, metabolically inert, nonactively transported monosaccharides are absorbed significantly more in small birds and bats than in nonflying mammals. To broaden our comparison and test the veracity of our finding we surveyed the literature for other similar studies of paracellular absorption. The patterns found in our focal species held up when we included other species surveyed in our analysis. Significantly greater amplification of digestive surface area by villi in small birds, also uncovered by our analysis, may provide one mechanistic explanation for the observation of higher paracellular absorption relative to nonflying mammals. It appears that reduced intestinal size and relatively enhanced intestinal paracellular absorption can be added to the suite of adaptations that have evolved in actively flying vertebrates.digestion ͉ gut morphometrics ͉ nutrient absorption ͉ paracellular uptake B irds have structural, physiological, and biochemical refinements that adapt them for flight (1), but basic differences in digestive processing between flying and nonflying vertebrates have never been described to our knowledge. The phrase ''eating like a bird'' wrongly suggests that birds have relatively small appetites, whereas in fact the typical wild bird eats about one-third more dry matter each day than does the typical nonflying mammal (2). Flight, a very energetically demanding activity, contributes to high daily energy demands, but its structural prescription for low weight also may shape an aspect of fliers' digestive apparatus in a way that runs counter to that system's role in providing fuel to meet high energy demands.There is anecdotal evidence that birds have relatively shorter intestines than mammals (3), and shorter intestines are associated with less surface area and volume, parameters directly correlated with digestive capacity. Indeed, in both birds and mammals, digestive adjustments to higher feeding rates almost always include an increase in gut size and thus an increase in digestive enzymes and nutrient transporters (4). For birds that fly, however, the size of the digestive tract and consequently the mass of digesta it carries may need to be minimized because the cost of flight ...

Bats tend to have less intestinal tissue than comparably sized nonflying mammals. The corresponding reduction in intestinal volume and hence mass of digesta carried is advantageous because the costs of flight increase with load carried and because take-off and maneuverability are diminished at heavier masses. Water soluble compounds, such as glucose and amino acids, are absorbed in the small intestine mainly via two pathways, the transporter-mediated transcellular and the passive, paracellular pathways. Using the microchiropteran bat Artibeus literatus (mean mass 80.6±3.7 g), we tested the predictions that absorption of water-soluble compounds that are not actively transported would be extensive as a compensatory mechanism for relatively less intestinal tissue, and would decline with increasing molecular mass in accord with sieve-like paracellular absorption. Using a standard pharmacokinetic technique, we fed, or injected intraperitonealy the metabolically inert carbohydrates L-rhamnose (molecular mass = 164 Da) and cellobiose (molecular mass = 342 Da) which are absorbed only by paracellular transport, and 3-O-methyl-D-glucose (3OMD-glucose) which is absorbed via both mediated (active) and paracellular transport. As predicted, the bioavailability of paracellular probes declined with increasing molecular mass (rhamnose, 90±11%; cellobiose, 10±3%, n = 8) and was significantly higher in bats than has been reported for laboratory rats and other mammals. In addition, absorption of 3OMD-glucose was high (96±11%). We estimated that the bats rely on passive, paracellular absorption for more than 70% of their total glucose absorption, much more than in non-flying mammals. Although possibly compensating for less intestinal tissue, a high intestinal permeability that permits passive absorption might be less selective than a carrier-mediated system for nutrient absorption and might permit toxins to be absorbed from plant and animal material in the intestinal lumen.

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We previously demonstrated in intact house sparrows substantial absorption in vivo of L-glucose, the stereoisomer of D-glucose that is assumed not to interact with the intestine's D-glucose transporter. Results of some studies challenge this assumption for other species. Therefore, we tested it in vitro and in vivo, based on the principle that if absorption of a compound (L-glucose) is mediated, then absorption of its tracer will be competitively inhibited by high concentrations of either the compound itself or other compounds (e.g., D-glucose) whose absorption is mediated by the same mechanism. An alternative hypothesis that L-glucose absorption is primarily paracellular predicts that its absorption in vivo will be increased (not decreased) in the presence of D-glucose, because the permeability of this pathway is supposedly enhanced when Na(+)-coupled glucose absorption occurs. First, using intact tissue in vitro, we found that uptake of tracer-radiolabeled L-glucose was not significantly inhibited by high concentrations (100 mM) of either L-glucose or 3-O-methyl-D-glucose, a non-metabolizable but actively transported D-glucose analogue. Second, using intact house sparrows, we found that fractional absorption of the L-glucose tracer was significantly increased, not reduced, when gavaged along with 200 mM 3-O-methyl-D-glucose. This result was confirmed in another experiment where L-glucose fractional absorption was significantly higher in the presence vs. absence of food in the gut. The greater absorption was apparently not due simply to longer retention time of digesta, because no significant difference was found among retention times. Our results are consistent with the idea that L-glucose is absorbed in a non-mediated fashion, largely via the paracellular pathway in vivo.

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In nature, birds are faced with variable food sources that may differ in composition (protein vs. carbohydrates) and quality (highly digestible material vs. indigestible fiber). Studies in passerine birds and some commercial poultry demonstrate that the gastrointestinal tract can respond to varying diet composition and quality by changing morphology and/or activities of digestive enzymes. However, studies in additional avian species are warranted to understand generalities of these trends. We first fed juvenile mallards (Anas platyrhynchos), chickens (Gallus gallus), and quails (Coturnix coturnix) on either high-carbohydrate or high-protein diets. For the most part, birds fed the high-carbohydrate diet had higher small intestinal and cecal disaccharidase activities (maltase and sucrase). However, only mallards exhibited higher small intestinal aminopeptidase-N (APN) activities when fed the high-protein diet. These results differ from passerine birds, which largely modulate small intestinal proteases, but not disaccharidases. In another trial, we fed Canada geese (Branta canadensis) diets that varied in both their protein and fiber concentrations for approximately 3.5 months. Birds fed the high-fiber diets had significantly longer small intestines and caeca compared to those fed low-fiber diets. Additionally, geese fed the high-fiber diets exhibited lower mass-specific activities of small intestinal sucrase, and higher activities of APN when summed across the small intestine and ceca. Similar to the avian species above, geese fed the high-protein diets did not exhibit flexibility in their small intestinal APN activities. Overall, these experiments demonstrate that responsiveness of the avian digestive tract to diet composition may have phylogenetic or ecological constraints. Studies on other avian taxa are needed to understand these patterns.

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