The performing animal: causes and consequences of body remodeling and metabolic adjustments in red knots facing contrasting thermal environments

Abstract

Using red knots () as a model, we determined how changes in mass and metabolic activity of organs relate to temperature-induced variation in metabolic performance. In cold-acclimated birds, we expected large muscles and heart as well as improved oxidative capacity and lipid transport, and we predicted that this would explain variation in maximal thermogenic capacity (M). We also expected larger digestive and excretory organs in these same birds and predicted that this would explain most of the variation in basal metabolic rate (BMR). Knots kept at 5°C were 20% heavier and maintained 1.5 times more body fat than individuals kept in thermoneutral conditions (25°C). The birds in the cold also had a BMR up to 32% higher and a M 16% higher than birds at 25°C. Organs were larger in the cold, with muscles and heart being 9-20% heavier and digestive and excretory organs being 21-36% larger than at thermoneutrality. Rather than the predicted digestive and excretory organs, the cold-induced increase in BMR correlated with changes in mass of the heart, pectoralis, and carcass. M varied positively with the mass of the pectoralis, supracoracoideus, and heart, highlighting the importance of muscles and cardiac function in cold endurance. Cold-acclimated knots also expressed upregulated capacity for lipid transport across mitochondrial membranes [carnitine palmitoyl transferase (CPT)] in their pectoralis and leg muscles, higher lipid catabolism capacity in their pectoralis muscles [β-hydroxyacyl CoA-dehydrogenase (HOAD)], and elevated oxidative capacity in their liver and kidney (citrate synthase). These adjustments may have contributed to BMR through changes in metabolic intensity. Positive relationships among M, CPT, and HOAD in the heart also suggest indirect constraints on thermogenic capacity through limited cardiac capacity.

Evolutionary design of a flexible, seasonally migratory, avian phenotype: why trade gizzard mass against pectoral muscle mass?

“…In freeliving shorebirds, gizzard mass atrophy prior to long-distance flights precedes pectoral muscle mass hypertrophy by more than a week [22,43,46]. From an energy management perspective, it seems adaptive to delay the build-up of pectoral muscle mass until shortly before migration given the high metabolic cost of the flight muscles [36], although we cannot exclude the possibility that this pattern reflects an unknown constraint. Second, while large, rapid changes in gizzard mass may be predictably associated with migration (see above), the same royalsocietypublishing.org/journal/rspb Proc.…”

“…Red knots (Calidris canutus), a medium-sized migratory shorebird, provide a rare opportunity to study level-specific trait covariation of internal traits, because non-destructive methods have been developed that allow for accurate estimation of internal organs [30]. Red knots have also served as good experimental animals to test for seasonally changing phenotypic traits that are related to migration but are maintained in captivity [33,34], together with the bodily consequences of differences in ecological contexts such as ambient temperature [35,36], predation risk [16] and diet ( [37], this study).…”

Ecological and evolutionary consequences of metabolic rate plasticity in response to environmental change

“…A number of studies have therefore attempted (with mixed success) to test whether individual variation in whole-animal oxygen consumption can arise from differences in the relative size or activity of these body components. As an example, Vézina et al [55] found that variation in both BMR and M-sum of red knots (Calidris canutus) was explained by variation in the residual mass of key organs after correction for body mass. Thus, individuals with relatively large hearts and muscles for their size tended to have higher BMRs, while a high M-sum was associated with proportionally large muscles, heart and stomach.…”

“…An alternative approach to determining the drivers of whole-animal metabolic rates is to examine variation in the functioning of key organs and tissues, rather than their size. One relevant measure is 'metabolic intensity', conceptually defined as the energy consumption per unit mass of tissue but in practice usually measured indirectly as either mitochondrial density or the activity of key rate-limiting mitochondrial enzymes [55]. Variation in both minimal and maximal metabolic rate among individuals has been found to correlate with differences in cytochrome c oxidase and/or citrate synthase activity in their mitochondria [55,59], although these correlations are not always evident [56].…”

“…One relevant measure is 'metabolic intensity', conceptually defined as the energy consumption per unit mass of tissue but in practice usually measured indirectly as either mitochondrial density or the activity of key rate-limiting mitochondrial enzymes [55]. Variation in both minimal and maximal metabolic rate among individuals has been found to correlate with differences in cytochrome c oxidase and/or citrate synthase activity in their mitochondria [55,59], although these correlations are not always evident [56]. An alternative approach to quantifying mitochondrial function is to measure oxygen consumption rates of either isolated mitochondria or the mitochondria within samples of permeabilized tissue.…”