Paracellular absorption is relatively low in the herbivorous Egyptian spiny-tailed lizard, Uromastyx aegyptia

Abstract

Absorption of small water-soluble nutrients in vertebrate intestines occurs both by specific, mediated transport and by non-specific, passive, paracellular transport. Although it is apparent that paracellular absorption represents a significant route for nutrient absorption in many birds and mammals, especially small, flying species, its importance in ectothermic vertebrates has not previously been explored. Therefore, we measured fractional absorption (ƒ) and absorption rate of three paracellular probes (arabinose, L-rhamnose, cellobiose) and of 3-O-methyl D-glucose (absorbed by both mediated and paracellular pathways) by the large herbivorous lizard, Uromastyx aegyptia, to explore the relative importance of paracellular and mediated transport in an ectothermic, terrestrial vertebrate. Fractional absorption of 3-O-methyl D-glucose was high (ƒ = 0.73±0.04) and similar to other vertebrates; ƒ of the paracellular probes was relatively low (arabinose ƒ = 0.31±0.03, L-rhamnose ƒ = 0.19±0.02, and cellobiose ƒ = 0.14±0.02), and decreased with molecular mass, a pattern consistent with other vertebrates. Paracellular absorption accounted for approximately 24% of total 3-O-methyl D-glucose uptake, indicating low reliance on this pathway for these herbivorous lizards, a pattern similar to that found in other terrestrial vertebrates, and different from small flying endotherms (both birds and bats).

Figure 1. Concentration-time curves for carbohydrate probes.

Mean plasma concentrations (± se; n = 7), normalized to the dose given, as a function of the time since oral administration (gavage) or injection, of (A) 3-O-methyl d-glucose, (B) arabinose, (C) rhamnose, and (D) cellobiose. Inserts display the same results on a semi-log plot. The line in the inserts is the mono-exponential fit of the model C _t = Ae^−αt for 3-O-methyl d-glucose, arabinose and cellobiose, or the bi-exponential fit of the model C _t = Ae^−αt+Be^−βt for rhamnose (see Table 1 for specific parameter values).

Figure 2. Fractional absorption (f) values for carbohydrate probes.

Fractional absorption (± se; n = 7) of probes absorbed via mediated transport or paracellular uptake. Fractional absorption of 3-O-methyl d-glucose was significantly higher than any of the paracellular probes. Paracellular probes showed decreasing fractional absorption with molecular size. Letters indicate statistically distinguishable groups at p<0.05.

Figure 3. Time course of probe absorption and relative contribution of non-mediated absorption.

Analysis of the time course of probe absorption (A), apparent rate of carbohydrate probe absorption (B), and proportional contribution of non-mediated absorption to total uptake during the first 96 h after treatment, when the majority of the probes were absorbed (C). The ratio of l-rhamnose to 3-O-methyl d-glucose cumulative absorption gives an indication of the proportional contribution of non-mediated absorption to total uptake, which averaged 0.24±0.03, suggesting that non-mediated absorption is a relatively small component of total absorption in Uromastyx aegyptia. There were significant differences overall in the absorption rates of l-rhamnose and 3-O-methyl d-glucose. Asterisks in (B) indicate specific time points where absorption rates were significantly different between probes (*** p<0.001).

Figure 4. Comparison of paracellular absorption amongst birds, mammals and reptiles.

Fractional absorption of paracellular probes as a function of body mass for birds, fruit bats, non-flying mammals, and reptiles. Each point represents the mean (± sd) of all species in that group measured to date. Because diffusion in water declines with molecular mass^1/2 , ƒ values were adjusted for probe mass, relative to the molecular mass of l-glucose, using a multiplier calculated from the formula: 1 - ((lglu^0.5-Prb^0.5)/lglu^0.5), where lglu is the molecular mass of l-glucose and Prb is the molecular mass of the paracellular probe used. Uromastyx aegyptia has fractional absorption values similar to other herbivores. See Supporting Information Table S1 for the species plotted, as well as the paracellular probes used and references.