Carbohydrate absorption by blackcap warblers (Sylvia atricapilla) changes during migratory refuelling stopovers

Abstract

SUMMARYPasserine birds migrating long distances arrive at stopover sites to refuel having lost as much as 50% of their initial body mass (m b ), including significant losses to digestive organs that may serve as a reservoir of protein catabolised for fuel during flight. Birds newly arrived at a stopover show slow or no m b gain during the initial 2-3 days of a stopover, which suggests that energy assimilation may be limited by reduced digestive organs. Measurements of migrants and captive birds subjected to simulated migratory fasts have shown reductions in intestine mass, morphological changes to the mucosal epithelium, and reductions in food intake and assimilation rate upon initial refeeding. We found that blackcaps (Sylvia atricapilla, Linnaeus) newly arrived at a migratory stopover after crossing the Sahara and Sinai deserts had significantly increased paracellular nutrient absorption (noncarrier mediated uptake occurring across tight junctions between enterocytes) that may provide partial compensation for reduced digestive capacity resulting from changes to intestinal tissues. Indeed, newly arrived birds also had a slightly reduced capacity for absorption of a glucose analogue (3-O-methyl-D-glucose) transported simultaneously by both carrier-mediated and nonmediated mechanisms. Increased paracellular absorption coupled with extended digesta retention time may thus allow migratory blackcaps to maintain high digestive efficiency during initial stages of refuelling while digestive organs are rebuilt.

Cold exposure increases intestinal paracellular permeability to nutrients in the mouse

“…This increase was modest, and the proportion of our probe that was absorbed did not approach that achieved by some small birds and bats [greater than 50% bioavailability in birds and bats (Caviedes-Vidal et al, 2007;Fasulo et al, 2013b)]. An increase in paracellular permeability to nutrient-sized probes has also been observed in other cases of elevated absorptive demand in pythons 1day post-feeding (Secor and Diamond, 1997) and in migratory birds during refueling after a long flight (Tracy et al, 2010). Nonetheless, the increase in permeability we observed need not be adaptive in nature, but could simply reflect other processes.…”

“…Birds that arrive at a migratory stopover often have decreased intestine mass, but are under selective pressure to gain energy reserves quickly. At a migratory stopover, carrier-mediated absorption of a glucose analog tended to be lower in blackcaps, but non-mediated absorption of nutrient-sized probes was elevated in birds that had recently arrived compared with those that had been refueling for several days (Tracy et al, 2010). Another example is pythons, sit-and-wait predators with infrequent meals, in which the percentage of glucose that is absorbed passively increases to ~50% on the day after meal ingestion, and then returns to low levels by the third day (Secor and Diamond, 1997).…”

Obese super athletes: fat-fueled migration in birds and bats

“…Digesta retention time, activities of digestive enzymes (including lipases), and intestinal transporters may be modified in migratory birds to match changes in diet nutrient composition (Afik et al, 1995(Afik et al, , 1997aMcWilliams and Karasov, 2001;Stein et al, 2005). Bird intestines have a much greater capacity for passive nutrient absorption than that of mammals (excepting bats -see below), and leakiness may be modulated during stopover to promote rapid fueling (Afik et al, 1997b;Caviedes-Vidal et al, 2007;Tracy et al, 2010). Liver glucose-6-phosphate dehydrogenase activity nearly doubled and malic enzyme activity increased fivefold in rosy pastors (Sturnus roseus) and white wagtails (Motacilla alba) during the premigration period (Shah et al, 1978).…”

Body composition of north and southbound migratory blackcaps is influenced by the lay‐of‐the‐land ahead

“…For the initial two to three days m b may not change, or may even decrease, and only then do birds start to rapidly gain m b , which is accompanied by an increase in their fat stores (Karasov and Pinshow 1998, Gannes 2002). Of the explanations offered for this phenomenon some were behavioral (Gwinner et al 1985) and some physiological, including reduced assimilating capacity of the GIT (Gannes 2002, Tracy et al 2010). This delay in mass‐gain correlates with rebuilding the GIT; thereafter, stopover time is devoted to the accumulation of energy stores (Karasov et al 2004, Tracy et al 2010).…”

“…Of the explanations offered for this phenomenon some were behavioral (Gwinner et al 1985) and some physiological, including reduced assimilating capacity of the GIT (Gannes 2002, Tracy et al 2010). This delay in mass‐gain correlates with rebuilding the GIT; thereafter, stopover time is devoted to the accumulation of energy stores (Karasov et al 2004, Tracy et al 2010).…”