Seasonal Variation of Metabolic Thermogenesis in Eurasian Tree Sparrows (Passer montanus) over a Latitudinal Gradient

Abstract

Phenotypic flexibility of various morphological and physiological characters is widespread in animals. Resident endothermic animals of temperate climates provide a natural experiment in phenotypic flexibility. In this study, we took an integrative approach to assess seasonal and geographic influences on metabolism in Eurasian tree sparrows (Passer montanus). We measured resting metabolic rate (RMR), masses of internal organs, mitochondrial respiration capacities in liver and muscle, cytochrome C oxidase (COX) activities in liver and muscle, and circulating levels of plasma triiodothyronine (T3) and thyroxine (T4) in summer and winter sparrows at two sites from southeastern (Wenzhou) and northeastern (Qiqihar) China that differ in climate. Body masses of tree sparrows were significantly higher in winter than in summer at both sites but did not differ with latitude. RMRs of tree sparrows varied significantly with both latitude and season, with RMRs of Qiqihar birds being higher than those of Wenzhou birds and with RMRs being higher in winter than in summer. Consistently, dry masses of brain, lung, liver, gizzard, small intestine, rectum, and total digestive tract varied significantly with either latitude or season. State 4 respiration and COX activity in liver and muscle were remarkably higher in Qiqihar and increased significantly in winter. Circulating levels of plasma T3 also showed significant seasonal and latitudinal variation and was higher in Qiqihar in winter than in other groups. These data suggest that tree sparrows mainly coped with cold by enhancing thermogenic capacities through heightened activity of respiratory enzymes and higher levels of plasma thyroid hormones (T3). These results are consistent with a pronounced seasonal and latitudinal phenotypic flexibility mediated through physiological and biochemical adjustments in Eurasian tree sparrows.

Temperature and photoperiod as environmental cues affect body mass and thermoregulation in Chinese bulbulsPycnonotus sinensis

“…Mitochondrial respiration and enzyme activity in this study were significantly correlated with RMR in either liver or pectoral muscle, which suggests that variation in cellular oxidative phosphorylation capacity (state-4 respiration and COX activity) is a prominent mediator of RMR variation in Chinese bulbuls. Some studies have examined correlations of cellular metabolic capacity with metabolic output in birds, and our results are consistent with data from Eurasian tree sparrow (Passer montanus), where variation in state-4 respiration and COX activity was correlated with variation in RMR (Zheng et al, 2008b(Zheng et al, , 2014b. In the present study, cold temperature induced an increase in liver and muscle state-4 respiration and COX activity in Chinese bulbuls, which also displayed enhanced thermogenic capacity.…”

“…Thus, temperature is an important factor affecting thermogenesis in Chinese bulbuls. These results are also consistent with those obtained for other avian species, including the Eurasian tree sparrow (Zheng et al, 2008b(Zheng et al, , 2014b and little buntings (Emberiza pusilla) (Zheng et al, 2013b). It would be interesting to examine, in further studies, whether increased state-4 respiration and COX activity in bulbuls is also due to their responses to chronic shivering (Bicudo et al, 2001;Zhou et al, 2016).…”

“…For example, winter-acclimatized Chinese bulbuls increase their state-4 respiration and COX activity in liver and muscle tissue, which suggests that these adjustments could play an important role in winter thermogenesis (Villarin et al, 2003;Zheng et al, 2014a). State-4 respiration and COX activity in the liver and muscle of birds may either increase or remain seasonally stable during winter acclimatization or migration (Swanson, 2010;Zheng et al, 2008bZheng et al, , 2013bZheng et al, , 2014b. In hwamei, cold acclimation increased the oxidative capacity of the pectoral muscles and liver, which collectively could make a significant contribution to non-shivering thermogenesis (Zhou et al, 2016).…”

Flying high: Limits to flight performance by sparrows on the Qinghai-Tibet Plateau

“…For example, relative heart mass (but not relative lung mass) increases in the same species at a high-latitude location relative to a comparison population at a lower latitude, as do resting metabolic rates and various enzyme activities in the liver and muscle, although body mass stays approximately constant (Zheng et al, 2014). The three sites under consideration here lie within 5°of latitude from each other, but likely exhibit substantial differences in mean daily temperature (e.g.…”

Daily variation in body mass and thermoregulation in male Hwamei (Garrulax canorus) at different seasons

“…Many birds display phenotypic flexibility in maintaining energy requirements, capable of up and down body mass regulation over a period of time in response to thermal acclimation (Vézina et al 2006;Zheng et al 2013a), season (Zheng et al 2008a(Zheng et al , 2008b(Zheng et al , 2014aPetit et al 2014), elevation (Lindsay et al 2009) and latitude (Wikelski et al 2003;Zheng et al 2013bZheng et al , 2014b. Thermoregulatory responses are known to differ seasonally in birds, often dependent on the environment and region in which they reside (Bush et al 2008;Zheng et al 2008aZheng et al , 2014a. Non-migratory birds at temperate latitudes undergo drastic seasonal variation in day length, temperature and food availability (Yuni and Rose 2005;Wiersma et al 2007).…”