Phenotypic flexibility in metabolic adjustments and digestive function in white-shouldered starlings: responses to short-term temperature acclimation

Abstract

ABSTRACT Changing the intrinsic rate of metabolic heat production is the main adaptive strategy for small birds to cope with different ambient temperatures. In this study, we tested the hypothesis that the small passerine the white-shouldered starling (Sturnus sinensis) can modulate basal metabolism under temperature acclimation by changing the morphological, physiological and biochemical state of its tissues and organs. We measured the effects of temperature on body mass, basal metabolic rate (BMR), wet mass of various internal organs, state 4 respiration (S4R) and cytochrome c oxidase (CCO) activity in the pectoral muscle and organs, metabolites in the pectoral muscle, energy intake, histological dynamics and the activity of duodenal digestive enzymes. Warm acclimation decreased BMR to a greater extent than cold acclimation. At the organ level, birds in the cold-acclimated group had significantly heavier intestines but significantly lighter pectoral muscles. At the cellular level, birds in the cold-acclimated group showed significantly higher S4R in the liver and heart and CCO activity in the liver and kidney at both the mass-specific and whole-organ levels. A metabolomic analysis of the pectoral tissue revealed significantly higher lipid decomposition, amino acid degradation, ATP hydrolysis, and GTP and biotin synthesis in cold-acclimated birds. Acclimation to cold significantly increased the gross energy intake (GEI), feces energy (FE) and digestive energy intake (DEI) but significantly decreased the digestive efficiency of these birds. Furthermore, cold-acclimated birds had a higher maltase activity and longer villi in the duodenum. Taken together, these data show that white-shouldered starlings exhibit high phenotypic flexibility in metabolic adjustments and digestive function under temperature acclimation, consistent with the notion that small birds cope with the energy challenges presented by a cold environment by modulating tissue function in a way that would affect BMR.