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Interspecific Variation of Thermoregulation Between Small Migratory and Resident Passerines in Wenzhou

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Interspecific Variation of Thermoregulation Between Small Migratory and Resident Passerines in Wenzhou ZOOLOGICAL RESEARCH Interspecific variation of thermoregulation between small migratory and resident passerines in Wenzhou Qing-Gang QIAO1, Hong-Ji LIANG1, Min-Lan BAI1, Wei-Hong ZHENG1,2, Jin-Song LIU1,2,* 1 School of Life and Environmental Sciences, Wenzhou University, Wenzhou 325035, China 2 Zhejiang Provincial Key Lab for Subtropical Water Environment and Marine Biological Resources Protection, Wenzhou 325035, China ABSTRACT thermogenesis. Taken together, these data illustrate small migratory and resident passerines that exhibit Physiological adaptation arises from several the different characteristics of thermoregulation. fundamental sources of phenotypic variation. Most analyses of metabolic adaptation in birds have Keywords: Basal metabolic rate; Body temperature; focused on the basal metabolic rate (BMR), the Thermal conductance; Eophona migratoria; Lonchura lower limit of avian metabolic heat production. In this striata; Aegithalos concinnus study, we investigated thermoregulation in three passerine species; the yellow-billed grosbeak INTRODUCTION1 Eophona migratoria, white-rumped munia Lonchura striata and black-throated bushtit Aegithalos Heat production in response to ambient temperature is concinnus, in Wenzhou, China. Metabolic rate was commonly referred to as facultative, or adaptive, thermogenesis measured using the closed-circuit respirometer (Angilletta et al., 2010; Silva, 2006; Zhou et al., 2016). containing 3.5 L animal chambers. Body temperature Endotherms primarily use mechanisms that equalize rates of (Tb) was measured during metabolic measurements heat production and loss to maintain a high and constant body using a lubricated thermocouple. The minimum temperature (Corp et al., 1997; Liu et al., 2004a). The necessity thermal conductance of these species was of maintaining an optimal body temperature is one of the major calculated by measuring their Tb and metabolic rates. factors influencing the abundance and distribution of birds (Liu The yellow-billed grosbeak remained largely et al., 2005; Weathers, 1979), and birds have evolved many normothermic, and the white-rumped munia and morphological and physiological adaptations to achieve this black-throated bushtit exhibited variable Tb at ambient (Swanson & Merkord, 2013; Wiersma et al., 2007). temperatures (Ta). Mean metabolic rates within Physiological adaptation arises from several fundamental thermal neutral zone were 2.48±0.09 O2 (mL)/g/h for sources of phenotypic variation. Most analyses of metabolic yellow-billed grosbeaks, 3.44±0.16 O2 (mL)/g/h for adaptation in birds have focused on the basal metabolic rate white-rumped munias, and 3.55±0.20 O2 (mL)/g/h for (BMR), the lower limit of avian metabolic heat production black-throated bushtits, respectively. Minimum (McKechnie et al., 2006; McNab, 2009). BMR is a standardized thermal conductance of yellow-billed grosbeak, baseline metabolic parameter that reflects a species’ resting white-rumped munia and black-throated bushtit were energy requirements in the absence of the increased metabolic 0.13±0.00, 0.36±0.01, and 0.37±0.01 O2 (mL)/g/h/˚C, demands associated with thermoregulation, digestion, activity respectively. The ecophysiological characteristics of or circadian rhythms (McKechnie, 2008; McNab, 2009; Zhou et these species were: (1) the yellowbilled grosbeak al., 2016). BMR is a widely-accepted benchmark of metabolic had relatively high Tb and BMR, a low lower critical expenditure for birds that is commonly used as a measure of temperature and thermal conductance, and a metabolic rate that was relatively insensitive to Received: 05 Feburary 2016; Accepted: 20 May 2016 variation in Ta; all of which are typical of cold adapted species and explain its broader geographic Foundation items: This study was financially supported by grants from distribution; (2) the white-rumped munia and black- the National Natural Science Foundation of China (No. 31470472), the throated bushtit had high thermal conductance, National Undergraduate “Innovation” Project and the Zhejiang lower critical temperature, and relatively low BMR, Province “Xinmiao” Project all which are adapted to warm environments where *Corresponding author, E-mail: [email protected] there is little selection pressure for metabolic DOI:10.13918/j.issn.2095-8137.2016.3.167 Science Press Zoological Research 37(3): 167-175, 2016 167 the energetic cost of thermoregulation. It has consequently been the focus of considerable research interest from MATERIALS AND METHODS environmental physiologists and comparative physiologists (e.g., Liu et al., 2005; Zheng et al., 2014a). Animals Ambient temperature (Ta) is considered one of the most important environmental factors affecting birds because it Seven yellow-billed grosbeaks (six male, one female), ten causes marked changes in their energy expenditure (Nzama et white-rumped munias (six male, four female) and nine black- al., 2010) and has driven the evolution of a suite of throated bushtits (seven male, two female) were captured by morphological and physiological adaptations (Swanson et al., mist nets in Wenzhou city (N27°29', E120°51'), Zhejiang 2014). A considerable body of research has been conducted to Province, China. The yellow-billed grosbeak Eophona examine the effects of temperature on animal adaptation, migratoria is a granivorous and insectivorous migratory bird. survival, and reproductive success (Sgueo et al., 2012; Zhou et The white-rumped munia Lonchura striata is a gregarious bird al., 2016). In a comparative study of small birds with different that feeds mainly on seeds. The black-throated bushtit habitats and habits, Rezende et al. (2002) recently emphasized Aegithalos concinnus mainly feeds on small insects and spiders, the ecological significance of BMR. For example, tropical birds as well as small seeds, fruits and berries (particularly typically have a lower BMR than cold temperate birds, which is raspberries). The climate in Wenzhou is warm-temperate with thought to be an adaptation to avoid heat stress and conserve the mean annual temperature is 18 ˚C. There are seven months water (Weathers, 1997; Wiersma et al., 2007). Conversely, the of the year (March through September) in which the maximum higher BMR of cold temperate and Arctic birds is thought to be temperature is above 37 ˚C (Zheng et al., 2008a; 2014a). All an adaptation to colder temperatures and shorter breeding experiments were carried out from October to December 2012. seasons (Klaassen, 1995; Zheng et al., 2014b). It has been Animals were kept in individual cages (50 cm×30 cm×20 cm) suggested that the BMR of a number of long-distance migratory under natural photoperiod (14L:10D) with lights on at 0600h birds is lower in their tropical overwintering range than at their and temperature (25 ˚C). Food and water were supplied ad temperate breeding grounds (Lindström & Klaassen, 2003; libitum. Yellow-billed grosbeaks and white-rumped munias were Zheng et al., 2013). The higher metabolic capacities of high fed millet seeds, and black-throated bushtits were fed bird cake latitude species may involve a combination of genetic and mealworm Tenebriomolitor larvae. The mean body mass responses to climatic factors (Liknes & Swanson, 2011; of yellow-billed grosbeaks, white-rumped munias and black- Swanson, 2010; Wikelski et al., 2003). These findings indicate throated bushtits was 50.5±0.6 g (47.9-52.4 g), 12.6±0.3 g that environmental conditions are very important in shaping the (11.1-14.5 g) and 6.8±0.1 g (6.4-7.4 g), respectively. All thermoregulatory features of a species. There is now experimental procedures were approved by the Wenzhou City considerable evidence to show that the metabolic Animal Care and Use Committee, Zhejiang Province, China characteristics of birds are part of a network of physiological (Wu et al., 2015). mechanisms that mediate major life-history trade-offs (Wikelski et al., 2003). Measurement of metabolic rate The yellow-billed grosbeak Eophona migratoria is a migratory Oxygen consumption was measured using a closed-circuit bird that inhabits vast areas of northeast Asia. The white- respirometer according to the methods described by Górecki rumped munia Lonchura striata is a common resident breeder (1975) and Liu et al. (2004a; 2005). The volume of the in southern China and South Asia. The distribution of the black- metabolic chamber was 3.5 L and its temperature was throated bushtit Aegithalos concinnus ranges from the foothills controlled by a water bath in Artificial Climatic Engine (BIC-300, of the Himalayas, across northern India through Nepal, to Shanghai) and maintained to ±0.5 ˚C. Every bird was tested northern Vietnam and Taiwan (MacKinnon & Phillipps, 2000). only one Ta per day with at least two days between tests (Xia et Although all three species experience the same temperature al., 2013). Oxygen consumption rates were measured over a and photoperiod in autumn and winter in Wenzhou, the yellow- temperature range of 5 ˚C to 35 ˚C. Food was withheld four billed grosbeak is a Palearctic bird that migrates to Wenzhou in hours before animals were placed in the metabolic chamber to winter whereas the white-rumped munia and black-throated minimize the heat increment associated with feeding before bushtit are Indomalayan species that are resident in Wenzhou, each test. Birds were weighed to the nearest 0.1 g before being and their thermoregulatory responses could differ (e.g., climatic put in the chamber. Water and CO2 were absorbed from the air differences across the ranges). To test the hypothesis
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