Abstract
Water-soluble nutrients are absorbed by the small intestine via transcellular and paracellular mechanisms. Based on a few previous studies, the capacity for paracellular nutrient absorption seems greater in flying mammals than in nonflying mammals, but there has been little investigation of the mechanisms driving this difference. Therefore, we studied three species each of bats (Artibeus lituratus, Sturnira lilium and Carollia perspicillata) and nonflying mammals (Akodon montensis, Mus musculus and Rattus norvegicus). Using standard pharmacokinetic techniques in intact animals, we confirmed the greater paracellular nutrient absorption in the fliers, comparing one species in each group. Then we conducted in situ intestinal perfusions on individuals of all species. In both approaches, we measured the absorption of 3OMD-glucose, a nonmetabolizable glucose analog absorbed both paracellularly and transcellularly, as well as L-arabinose, which has no mediated transport. Fractional absorption of L-arabinose was three times higher in the bat (S. lilium: 1.2±0.24) than in the rodent (A. montensis: 0.35±0.04), whereas fractional absorption of 3OMD-glucose was complete in both species (1.46±0.4 and 0.97±0.12, respectively). In agreement, bats exhibited two to 12 times higher l-arabinose clearance per square centimeter nominal surface area than rodents in intestinal perfusions. Using L-arabinose, we estimated that the contribution of the paracellular pathway to total glucose absorption was higher in all three bats (109-137%) than in the rodents (13-39%). These findings contribute to an emerging picture that reliance on the paracellular pathway for nutrient absorption is much greater in bats relative to nonflying mammals and that this difference is driven by differences in intestinal permeability to nutrient-sized molecules.
Highlights
Water-soluble nutrients are absorbed at the small intestine via the transcellular and paracellular pathways
The difference in L-arabinose absorption between the bat and the rodent is in accordance with the pattern of absorption of nutrient-sized paracellular probes in other small bats, birds and nonflying mammals (Table 1), giving additional support to the hypothesis that high paracellular nutrient absorption is an adaptation for flight (Caviedes-Vidal et al, 2007)
Regardless of any putative dietary association, our results show that the differences among taxa in paracellular nutrient absorption that we have observed in intact animals can be demonstrated at the level of the intestine as well
Summary
Water-soluble nutrients are absorbed at the small intestine via the transcellular and paracellular pathways. The paracellular pathway is not transporter mediated; water-soluble compounds reach the basolateral space by traversing tight junctions (formed by adjacent enterocytes) by diffusion or solvent drag (Pappenheimer and Reiss, 1987). Caviedes-Vidal et al (Caviedes-Vidal et al, 2007) hypothesized that this heavy reliance on paracellular nutrient absorption evolved independently in flying mammals and birds, which have similar daily energy needs compared with nonfliers, probably to compensate for fliers’ lower absorptive surface area in smaller and lighter intestines relative to nonfliers. Without the special need for the complementary paracellular absorption pathway, natural selection may favor absorption of water-soluble nutrients by specific apical transporters in order to maintain a better selective barrier against hydrosoluble toxins (Karasov et al, 2012)
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