Capacity for Absorption of Water-Soluble Secondary Metabolites Greater in Birds than in Rodents

Abstract

Plant secondary metabolites (SMs) are pervasive in animal foods and potentially influence feeding behavior, interspecies interactions, and the distribution and abundance of animals. Some of the major classes of naturally occurring SMs in plants include many water-soluble compounds in the molecular size range that could cross the intestinal epithelium via the paracellular space by diffusion or solvent drag. There are differences among species in paracellular permeability. Using Middle Eastern rodent and avian consumers of fruits containing SMs, we tested the hypothesis that avian species would have significantly higher paracellular permeability than rodent species. Permeability in intact animals was assessed using standard pharmacological methodology to measure absorption of two radiolabeled, inert, neutral water-soluble probes that do not interact with intestinal nutrient transporters, L-arabinose (M r = 150.1 Da) and lactulose (M r = 342.3 Da). We also measured absorption of labeled 3-O-methyl-D-glucose (3OMD-glucose; M r = 194.2 Da), which is a nonmetabolized analogue of D-glucose that is passively absorbed through the paracellular space but also transported across the enterocyte membranes. Most glucose was absorbed by all species, but arabinose fractional absorption ( f ) was nearly three times higher in birds (1.03±0.17, n = 15 in two species) compared to rodents (0.37±0.06, n = 10 in two species) (P<0.001). Surprisingly, the apparent rates of absorption in birds of arabinose exceeded those of 3OMD-glucose. Our findings are in agreement with previous work showing that the paracellular pathway is more prominent in birds relative to nonflying mammals, and suggests that birds may be challenged by greater absorption of water-soluble, dietary SMs. The increased expression of the paracellular pathway in birds hints at a tradeoff: the free energy birds gain by absorbing water-soluble nutrients passively may be offset by the metabolic demands placed on them to eliminate concomitantly absorbed SMs.

Cold exposure increases intestinal paracellular permeability to nutrients in the mouse

“…Previous work showed that this time period is long enough to measure fractional absorption of arabinose (Fasulo et al, 2013a ]-L-arabinose recoveries by 1.11 to account for this difference in probe recovery, producing an 'adjusted cumulative % injection dose recovered'. Although L-arabinose is not metabolized and theoretically can be fully recovered, recoveries of injected inert probes are often less than 100% (Karasov et al, 2012). To account for this loss, we normalized our gavage data using the i.p.…”

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

“…The degree of use of the paracellular pathway varies widely among vertebrates (Caviedes-Vidal et al, 2007; Fasulo et al, 2013a). For example, it is minor in terrestrial mammals, but several small birds and bats actually absorb the majority of glucose paracellularly (Karasov and Cork, 1994;Caviedes-Vidal and Karasov, 1996;Levey and Cipollini, 1996;Afik et al, 1997;Tracy et al, 2007;Karasov et al, 2012;Fasulo et al, 2013b). This phenomenon has been hypothesized to derive from an evolutionary pressure to reduce mass in flying animals (CaviedesVidal et al, 2007) while having as a trade-off greater exposure to water-soluble toxins (Diamond, 1991).…”

Effects of nicotine on the digestive performance of nectar-feeding birds reflect their relative tolerance to this alkaloid

“…However, because the passive pathway is less selective than a carrier-mediated system, birds may be more vulnerable to hydrophilic secondary metabolites (Diamond 1991). Karasov et al (2012), using two bird species (including yellow-vented bulbuls) and two rodent species,…”

“…Sugars such as sucrose, glucose and fructose are the main nutrients in nectar and fruits (Baker et al 1998;Martínez del Rio et al 1992) and their efficient digestion depends in part on passive absorption by the paracellular pathway, especially in small birds and bats (CaviedesVidal et al 2007;Karasov et al 2012;Napier et al 2008). This could be disadvantageous for consumers if fruits and nectar contain hydrophilic secondary metabolites, because they will be easily absorbed by the paracellular route (Diamond 1991;Karasov et al 2012).…”

“…This could be disadvantageous for consumers if fruits and nectar contain hydrophilic secondary metabolites, because they will be easily absorbed by the paracellular route (Diamond 1991;Karasov et al 2012). In addition, nectar sugar concentration is highly variable Nicolson 2002) and specialist nectar-feeding birds are able to accurately regulate daily energy intake by varying their food intake according to the sugar content of nectar (Nicolson and Fleming 2003).…”