Paracellular Absorption: A Bat Breaks the Mammal Paradigm

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.

Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

“…Because the role of diet on paracellular nutrient absorption is not yet clear, and because previous studies focused on species that consume primarily carbohydrate-rich diets Tracy et al, 2007;Caviedes-Vidal et al, 2008;Brun et al, 2014), we examined species that all rely substantially on protein-rich diets. It was previously suggested that carnivores might rely more extensively on paracellular nutrient absorption than herbivores (McWhorter et al, 2013).…”

“…For these reasons, we determined fractional recovery by serial blood sampling (for details, see Caviedes-Vidal et al, 2008;Karasov et al, 2012). Individual bats were dosed with an oral gavage (in saline and 50 mmol l −1 glucose) or intraperitoneal injection (in saline), and a blood sample was taken from the antebrachial or uropatagial vein after ~5, 15, 30, 45, 60 and 90 min.…”

Flight is the key to postprandial blood glucose balance in the fruit bats Eonycteris spelaea and Cynopterus sphinx

“…Both flying and resting fruit bats can use ingested sugars as a direct fuel, just like hummingbirds (Amitai et al., 2010; Voigt & Speakman, 2007; Welch & Suarez, 2008). Additionally, an elevated amount of sugar intake is parallel with an increased speed of paracellular nutrient absorption in fruit bats (Caviedes‐Vidal et al., 2008; Tracy et al., 2007). Therefore, these bats can uptake large quantities of sugar each night.…”

High paracellular nutrient absorption in intact bats is associated with high paracellular permeability in perfused intestinal segments

“…In particular, paracellular absorption accounts for 60-90% of the glucose absorption in all small birds and bats studied to date (Caviedes-Vidal et al, 2008;Caviedes-Vidal et al, 2007;Chediack et al, 2003;Tracy et al, 2007). In contrast, transporter-mediated absorption is much more important in terrestrial mammals (Lavin and Karasov, 2008;.…”