Mechanism and rate of glucose absorption differ between an Australian honeyeater (Meliphagidae) and a lorikeet (Loriidae)

Abstract

SUMMARYEfficient mechanisms of glucose absorption are necessary for volant animals as a means of reducing mass during flight: they speed up gut transit time and require smaller volume and mass of gut tissue. One mechanism that may be important is absorption via paracellular (non-mediated) pathways. This may be particularly true for nectarivorous species which encounter large quantities of sugar in their natural diet. We investigated the extent of mediated and non-mediated glucose absorption in red wattlebirds Anthochaera carunculata (Meliphagidae) and rainbow lorikeets Trichoglossus haematodus (Loriidae) to test the hypothesis that paracellular uptake accounts for a significant proportion of total glucose uptake in these species. We found that routes of glucose absorption are highly dynamic in both species. In lorikeets, absorption of L-glucose (non-mediated uptake) is slower than that of D-glucose (mediated and non-mediated uptake), with as little as 10% of total glucose absorbed by the paracellular pathway initially (contrasting previous indirect estimates of ~80%). Over time, however, more glucose may be absorbed via the paracellular route. Glucose absorption by both mediated and non-mediated mechanisms in wattlebirds occurred at a faster rate than in lorikeets, and wattlebirds also rely substantially on paracellular uptake. In wattlebirds, we recorded higher bioavailability of L-glucose (96±3%) compared with D-glucose (57±2%), suggesting problems with the in vivo use of radiolabeled D-glucose. Further trials with 3-O-methyl-D-glucose revealed high bioavailability in wattlebirds (90±5%). This non-metabolisable glucose analogue remains the probe of choice for measuring uptake rates in vivo, especially in birds in which absorption and metabolism occur extremely rapidly.

A Comparison of Pharmacokinetic Methods for In Vivo Studies of Nonmediated Glucose Absorption

“…In rainbow lorikeets, the bioavailability of d-glucose calculated using the standard AUC pharmacokinetic protocol was not significantly different from apparent assimilation efficiency calculated using a traditional mass-balance approach (Napier et al 2008a) or from estimates based on the steady state feeding pharmacokinetic protocol (Karasov and Cork 1994). However, in the red wattlebird, estimated bioavailability of d-glucose using the AUC protocol was erroneously low (∼57%), did not match apparent assimilation efficiency values established through mass-balance approach (∼99%), and logically should have exceeded values for the bioavailability of l-glucose (estimated at 92%-96%; Napier et al 2008a). The erroneously low values for bioavailability of d-glucose were interpreted as presystemic catabolism and/or sequestering of the marker in tissues, subsequently confirmed by using 3-O-methyl-d-glucose (∼90%), a nonmetabolizable d-glucose analogue that competes for the same cotransporters as d-glucose (Napier et al 2008a).…”

“…However, in the red wattlebird, estimated bioavailability of d-glucose using the AUC protocol was erroneously low (∼57%), did not match apparent assimilation efficiency values established through mass-balance approach (∼99%), and logically should have exceeded values for the bioavailability of l-glucose (estimated at 92%-96%; Napier et al 2008a). The erroneously low values for bioavailability of d-glucose were interpreted as presystemic catabolism and/or sequestering of the marker in tissues, subsequently confirmed by using 3-O-methyl-d-glucose (∼90%), a nonmetabolizable d-glucose analogue that competes for the same cotransporters as d-glucose (Napier et al 2008a). The appearance of l-glucose in the bloodstream is also exceptionally fast in red wattlebirds: values had already peaked by the first blood sample at 2.5-5 min while the peak for l-glucose absorption in rainbow lorikeets was recorded around 45 min.…”

“…Absorption of small, nontransported, metabolically inert, water-soluble probe molecules (e.g., stereoisomers of simple sugars such as l-glucose) is used to assess paracellular nutrient absorption McWhorter 2005;McWhorter et al 2006;Caviedes-Vidal et al 2007;Napier et al 2008aNapier et al , 2008b. This typically involves measuring the fraction of an oral dose of a probe that reaches the systemic circulation, known as the "fractional absorption" or "systemic bioavailability" (Gibaldi 1991).…”

“…We have also compared the digestive handling of sugars by the red wattlebird and rainbow lorikeet (the latter species examined by Karasov and Cork in establishment of the steady state feeding method) and recorded substantial differences between the species (Napier et al 2008a). In rainbow lorikeets, the bioavailability of d-glucose calculated using the standard AUC pharmacokinetic protocol was not significantly different from apparent assimilation efficiency calculated using a traditional mass-balance approach (Napier et al 2008a) or from estimates based on the steady state feeding pharmacokinetic protocol (Karasov and Cork 1994).…”

“…We have also compared the digestive handling of sugars by the red wattlebird and rainbow lorikeet (the latter species examined by Karasov and Cork in establishment of the steady state feeding method) and recorded substantial differences between the species (Napier et al 2008a). In rainbow lorikeets, the bioavailability of d-glucose calculated using the standard AUC pharmacokinetic protocol was not significantly different from apparent assimilation efficiency calculated using a traditional mass-balance approach (Napier et al 2008a) or from estimates based on the steady state feeding pharmacokinetic protocol (Karasov and Cork 1994). However, in the red wattlebird, estimated bioavailability of d-glucose using the AUC protocol was erroneously low (∼57%), did not match apparent assimilation efficiency values established through mass-balance approach (∼99%), and logically should have exceeded values for the bioavailability of l-glucose (estimated at 92%-96%; Napier et al 2008a).…”