The role of temperature as a driver of metabolic flexibility in the Red-billed Leiothrix (Leiothrix lutea)

Abstract

Background: The thermoregulatory ability of animals is strongly influenced by the temperature of their environment. Acclimation to cold requires a range of physiological and morphological adjustments. In this study, we tested the hypothesis that a small passerine, the Red-billed Leiothrix (Leiothrix lutea), can maintain homeothermy in cold conditions by adjusting the physiology and biochemistry of its tissue and organs and return to its former physiological and biochemical state when moved to a warm temperature. Methods: Phenotypic variation in thermogenic activity of the Red-billed Leiothrixs (Leiothrix lutea) was investigated under warm (35 °C), normal (25 °C) or cold (15 °C) ambient temperature conditions. Oxygen consumption was measured using an open-circuit respirometry system. Mitochondrial state-4 respiration and cytochrome-c oxidase (COX) activity in liver, kidney heart and pectoral muscle were measured with a Clark electrode. Results: Birds acclimated to an ambient temperature of 15 °C for 4 weeks significantly increased their basal metabolic rate (BMR) compared to a control group kept at 25 °C. Birds acclimated to 35 °C decreased their BMR, gross energy intake (GEI) and digestible energy intake (DEI). Furthermore, birds acclimated to 15 °C increased state-4 respiration in their pectoral muscles and cytochrome-c oxidase (COX) activity in their liver and pectoral muscle, compared to the 25 °C control group. Birds acclimated to 35 °C also displayed lower state-4 respiration and COX activity in the liver, heart and pectoral muscles, compared to those kept at 25 °C. There was a positive correlation between BMR and state-4 respiration, and between BMR and COX activity, in all of the above organs except the liver and heart. Conclusions: Our study illustrates that the morphological, physiological, and enzymatic changes are associated with temperature acclimation in the Red-billed Leiothrix, and supports the notion that the primary means by which small birds meet the energetic challenges of cold conditions is through metabolic adjustments.

Evidence for a maintenance cost for birds maintaining highly flexible basal, but not summit, metabolic rates

“…In addition, for the three species acclimated to cold temperatures of 3 °C or lower for 3 weeks or more (white-throated sparrow 32 , dark-eyed junco 33 , and house sparrow, Passer domesticus 37 ), white-throated and house sparrows showed significant positive correlations between ΔBMR and BMR. In contrast, for the three species acclimated to milder cold treatments of ≥ 10 °C (Southern red bishop, Euplectes orix 26 , Chinese hwamei, Garrulax canorus 36 , red-billed leiothrix, Leiothrix lutea 35 ), only the Southern red bishop showed a positive correlation between BMR and ΔBMR, and the Chinese hwamei showed a significant negative correlation between BMR and ΔBMR (Table 1 ). Thus, a significant positive relationship between ΔBMR and BMR occurred more often with colder acclimation temperatures.…”

“…If a study included cold, warm, and control (i.e., a room temperature treatment that was equivalent to pre-acclimation temperature exposure) acclimation treatments, we calculated ΔBMR, ΔM sum , or ΔScope only from cold and warm acclimation treatments where a flexible change in metabolic traits might be expected. Studies for which a control group was excluded from analyses included van de Ven et al 26 , Cui et al 35 , and Stager et al 33 , 34 (cold acclimation only). The Li et al 36 study included a warm temperature treatment (35 °C) that was the same as the captivity acclimation temperature, but the authors did vary photoperiod for both temperature treatment groups from that experienced during captivity acclimation, so we retained the warm treatment group from this study in our analyses.…”

Avian adjustments to cold and non‐shivering thermogenesis: whats, wheres and hows

“…Young birds with poor thermal insulation require greater heat production than can be generated by shivering (Dawson & Carey, 1976; Duchamp et al ., 1999; Aschoff, 1981). Shivering (both number of episodes and intensity) of cold‐acclimatized birds is significantly lower than that of warm‐acclimated birds exposed to acute cold (Dawson & Marsh, 1989; Cui et al ., 2019). After prolonged cold acclimation, two‐month old male leghorns (young adults) and muscovy ducklings ( Cairina moschata ) do not shiver but maintain high oxygen consumption levels and euthermic T b (El Halawani, Wilson & Burger, 1970; Barré et al ., 1986 a ).…”