Paracellular Absorption: A Bat Breaks the Mammal Paradigm

Enrique Caviedes-Vidal,Ariovaldo P Cruz-Neto,Juan Gabriel Chediack,Lye Otani,William H Karasov,Verónica Fasulo,Stuart Humphries

doi:10.1371/journal.pone.0001425

Abstract

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.

Highlights

Among mammals, bats are unique in their capacity for flapping flight, which requires high rates of energy expenditure
The parameters from the biexponential fits (Table 1) were used subsequently to calculate the time course of absorption. It is apparent from visual comparison of areas under the curve (AUC) for the oral vs. injection administration (Fig. 1) that fractional absorption was least for cellobiose
Paracellular absorption in great fruit-eating bats compared with nonflying mammals

Summary

Introduction

Bats are unique in their capacity for flapping flight, which requires high rates of energy expenditure. Biologists familiar with comparative digestive anatomy have noted that when contrasting comparably sized bats and non flying mammals without taken into account phylogeny, tend to have less intestinal tissue than nonflying mammals [3,4,5]. This pattern was confirmed in our allometric comparisons of gastrointestinal tract morphometrics of bats and nonflying mammals (E.C-V and W.H.K, unpublished data). A central dilemma that emerges in this consideration of bats vs nonflying mammals is how bats satisfy relatively high energy needs with relatively low intestinal nominal surface area for absorption

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