Comparative Biochemistry and Physiology, Part A 179 (2015) 113–119
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Seasonal variation in body mass, body temperature and thermogenesis in the Hwamei, Garrulax canorus Mei-Xiu Wu a, Li-Meng Zhou a, Li-Dan Zhao a, Zhi-Jun Zhao a,b, Wei-Hong Zheng a,b, Jin-Song Liu a,b,⁎ a b
School of Life and Environmental Sciences, Wenzhou University, Wenzhou 325035, China Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, Wenzhou 325035, China
a r t i c l e
i n f o
Article history: Received 16 December 2013 Received in revised form 15 September 2014 Accepted 18 September 2014 Available online 26 September 2014 Keywords: Garrulax canorus Body temperature Basal metabolic rate Thermal conductance Seasonal variation
a b s t r a c t The basal thermogenesis of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, particularly changes in ambient temperature (Ta). Many birds living in regions with seasonal fluctuations in Ta typically respond to cold by increasing their insulation and adjusting their metabolic rate. To understand these metabolic adaptations, body temperature (Tb), metabolic rate (MR), thermal neutral zone (TNZ) and thermal conductance were measured within a range of temperatures from 5 to 40 °C in free-living Hwamei, Garrulax canorus, in both winter and summer. Body mass was 61.2 ± 0.3 g in winter and 55.5 ± 1.0 g in summer, and mean Tb was 41.6 ± 0.1 °C in winter and 42.3 ± 0.1 °C in summer. TNZ was between 28.3 and 35.1 °C in winter and between 28.7 and 33.2 °C in summer. The mean basal metabolic rate (BMR) within TNZ was 203.32 ± 11.81 ml O2 h−1 in winter and 168.99 ± 6.45 ml O2 h−1 in summer. Minimum thermal conductance was 3.73 ± 0.09 joules g−1 h−1 °C−1 in winter and 3.26 ± 0.06 joules g−1 h−1 °C−1 in summer. Birds caught in winter had higher body mass, MR, and more variable TNZ than those in summer. The increased winter BMR indicates improved ability to cope with cold and maintenance of a high Tb. These results show that the Hwamei's metabolism is not constant, but exhibits pronounced seasonal phenotypic flexibility associated with maintenance of a high Tb. © 2014 Published by Elsevier Inc.
1. Introduction Phenotypic flexibility refers to phenotypic changes that are reversible, temporary and repeatable, such as acclimation and acclimatization (Piersma and Drent, 2003, Starck and Rahmaan, 2003; Starck, 2009; Liknes and Swanson, 2011a). In birds, phenotypic flexibility in metabolic power output is an important component of thermoregulatory responses to the elevated energy requirements experienced in seasonal environments (McKechnie et al., 2007). Not always, seasonal changes in ambient temperature require species to show seasonal acclimatization to facilitate thermoregulatory homeostasis (Chamane and Downs, 2009). Proper adjustments of thermoregulatory mechanisms ensure the survival of birds when they are subjected to seasonal changes in their natural environment, including temperature, photoperiod, food quality and availability (Zheng et al., 2008a). This includes seasonal changes in thermogenesis, which is highest in winter and lowest in summer (Pohl and West, 1973; Dawson and Carey, 1976; Lindsay et al., 2009a,b; Swanson et al., 2009; Liknes and Swanson, 2011b). Basal metabolic rate (BMR) refers to the energy expenditure of an animal at rest (i.e. in thermoneutrality) during the inactive phase of ⁎ Corresponding author at: School of Life and Environmental Sciences, Wenzhou University, Wenzhou's Chashan University Town, Wenzhou 325035, China. E-mail address: [email protected] (J.-S. Liu).
http://dx.doi.org/10.1016/j.cbpa.2014.09.026 1095-6433/© 2014 Published by Elsevier Inc.
the day, when the animal is not processing food, molting, or reproducing (Zheng et al., 2008a; McNab, 2009; Swanson, 2010). To avoid stress, BMR is measured within the thermal neutral zone (TNZ); a range of temperatures within which endotherms can maintain body temperature using only the heat provided by BMR (Chamane and Downs, 2009). It has been shown that BMR can consume as much as 50–60% of daily energy expenditure (DEE) and variation in BMR may be associated with peak or sustained metabolic rates, species richness and distribution, reproductive effort, activity levels and life-history strategies (McKinney and McWilliams, 2005; Zhao et al., 2010; Wells and Schaeffer, 2012). Comparing small birds from different habitats and different ecologies, Wiersma et al. (2007) stated that tropical birds have a slow life-history and evolve a reduced BMR. Wikelski et al. (2003) emphasized that birds live in tropical environments have lower BMR than predicted for their body from allometric equations, which has been explained as an adaptation to avoid heat stress. Conversely, alpine and boreal high latitude small birds have higher metabolic levels than expected based on their body mass, which has been explained as a direct, or indirect, result of adaptation to a colder climate and shorter breeding season, both of which require higher metabolic capacity (Dawson and Carey, 1976; Zheng et al., 2008b; Swanson and Plamer, 2009; Swanson, 2010). For a number of long-distance migrants, it has been suggested that BMR in their tropical winter range is lower
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than that at their colder breeding grounds (Lindström and Klaassen, 2003; Zheng et al., 2013a). Birds that are acclimated to seasonal decreases in ambient temperature generally increase the capacity to produce heat, which is probably associated with increased BMR (Cooper and Swanson, 1994; Yuni and Rose, 2005; Chamane and Downs, 2009). For example, Pohl and West (1973) showed that the BMR of captive winter-acclimatized common redpolls Acanthis flammea was higher than that measured in summer. Zheng et al. (2008b) also found that Eurasian tree sparrows Passer montanus captured in winter had higher BMR than those captured in summer. Similar results have also been observed in free-living species. The BMR of laughing doves Streptopela senegalensis increased following acclimation to cold temperatures but reduced when they were transferred to a warm room (McKechnie et al., 2007). Williams and Tieleman (2000) observed an increase in the BMR of captive, cold-acclimated hoopoe larks Alaemon alaudipes. These results suggest that the ability to elevate BMR is an important component of winter acclimatization or cold acclimation that is important to winter survival (Zheng et al., 2008b; Swanson, 2010). The Hwamei, Garrulax canorus (Passeriformes, Timaliidae) is an endemic Asian species found in central and southern China, northern Indochina, Hainan and Taiwan (MacKinnon and Phillipps, 2000; Li et al., 2006). Within its natural range, the Hwamei preferentially inhabits scrubland, open woodland, secondary forest, parks and gardens up to 1800 m above sea level (Zheng and Zhang, 2002). Due to the male's elaborate song, the Hwamei are one of the most popular cage birds among the global Chinese community (Li et al., 2006). The Hwamei is omnivorous and mainly feeds on arthropods (insects and spiders) in the breeding season, but also eat plants (fruits and seeds) in autumn and winter (Zheng and Zhang, 2002). The reported ecological physiological properties of the Hwamei are relatively lower BMR than predicted for their body from allometric equations (Aschoff and Pohl, 1970; McKechnie and Wolf, 2004; McKechnie and Swanson, 2010), high body temperature, narrow thermal neutral zone (TNZ) and high metabolic water production/evaporative water loss (MWP/EWL) (Liu et al., 2005; Xia et al., 2013). These characteristics suggest that this species is adapted to warm, mesic climates, where metabolic thermogenesis and water conservation are not strong selective pressures. This study follows up on previous work and investigates seasonal changes in body mass and metabolic performance of the Hwamei in southeast China. We selected this species because it is endemic to Asia and resident in Zhejiang Province where we are based (Zhang et al., 2010), and because there is little available data on the ecological physiology of the Hwamei and the Timaliidae in general (Liu et al., 2005; Xia et al., 2013). To the best of our knowledge, this is the first investigation of seasonal variation in body mass and thermoregulation in the Hwamei. The aim of this study was to evaluate the effects of seasonal changes in body temperature (Ta) on the resting metabolic rate (RMR), BMR and Tb of the Hwamei. Our objectives were to determine summer and winter RMR over a range of Tas by measuring oxygen consumption, to determine summer and winter BMR, and to determine if constant body temperature was maintained over a range of Tas. We predicted that the Hwamei would cope with winter temperatures by changing its body mass, metabolic rate, TNZ and thermal conductance, all of which increase the capacity to survive in cold environments. 2. Materials and methods 2.1. Animals This study was carried out in Wenzhou City, Zhejiang Province (27°29′N, 120°51′E, 14 m in elevation), China. Twenty Hwameis (5 males and 5 females in winter, and 7 males and 3 females in summer) were live-trapped in forest between January 2010 and July 2011. In Wenzhou, the climate is warm-temperate with an average annual rainfall of 1700 mm spread across all months and slightly more precipitation
during winter and spring. The mean winter (December to February) and summer (June to August) temperatures between 2010 and 2011 were 8.4 °C and 31.2 °C, respectively (Wenzhou Bureau of Meteorology). Body mass to the nearest 0.1 g was determined immediately upon capture with an electronic balance (Sartorius BT25S, Germany). Birds were then transported to the laboratory and kept outdoors for 1 or 2 days in cages 50 × 30 × 20 cm3 under natural photoperiod and temperature before physiological measurements were taken. Food and water were supplied ad libitum. All animal procedures were licensed under the Institutional Animal Care and Use Committee of the Institute of Zoology, Chinese Academy of Sciences. 2.2. Metabolic trials Birds' metabolic rates were estimated from measurements of oxygen consumption, obtain with an open-circuit respirometry system (AEI Technologies S-3A/I, USA). The metabolic chambers designed from 1.5 L plastic metabolic chambers, and a perch was provided in respirometry chamber (Smit and McKechnie, 2010). We regulated chamber temperature by putting in a temperaturecontrolled cabinet (Artificial climatic engine BIC-300, China) capable of regulating temperature to ± 0.5 °C. We scrubbed water vapor and CO2 using a silica gel/soda lime/silica column before passing through the oxygen analyzer. We measured oxygen content in excurrent gas from the metabolic chamber with an oxygen sensor (AEI Technologies N-22M, USA). During metabolic rates measurements, we adjusted flow rates of excurrent gas at 300 ml min − 1 in summer and 600 ml min− 1 in winter with a flow control system (AEI technologies R–1, USA) to maintain fractional concentration of O2 in respirometry chambers about 20%, and calibrated to ± 1% accuracy with a general purpose thermal mass flow-meter (TSI 4100 Series, USA) (McNab, 2006). We conducted each oxygen consumption at a different ambient temperature in a randomly determined order (5, 10, 15, 20, 25, 28, 30, 32, 35, 37.5 and 40 °C for summer, and 5, 10, 15, 20, 25, 27.5, 30, 32.5, 35, 37.5 and 40 °C for winter). We obtained baseline O2 concentrations before and after each test (Li et al., 2010). All measurements of gas exchange were obtained during the rest-phase of birds' circadian cycles (between 20:00 and 24:00) in darkened chambers, and from individuals that could reasonably be expected to be postabsorptive. Food was removed 4 h before each measurement period to minimize the heat increment associated with feeding. We ensured that the birds were perching calmly in the chambers, and then started recording oxygen consumption data at least 1 h after the rest-phase. Each animal was generally in the metabolic chamber for at least 2 h. From these data, we calculated 5 min running means of instantaneous oxygen consumption over the entire test period using equation 2 of Hill (1972), and considered the lowest 5 min mean oxygen consumption over the test period as resting metabolic rate (Smit and McKechnie, 2010). We expressed all values for oxygen consumption as ml O 2 h− 1 and corrected to STPD conditions (Schmidt-Nielsen, 1997). Body temperature (T b) was measured during metabolic measurements using a lubricated thermocouple. This was inserted cloacally to a depth at which a slight withdrawal did not result in a change in the reading (1–2 cm). Thermocouple outputs were digitized using a thermocouple meter (Beijing Normal University Instruments Co.). Body mass was measured to the nearest 0.1 g before and after the experiments, and mean body mass was used in calculations. All measurements were made daily between 20:00 and 24:00. 2.3. Thermal conductance Total thermal conductance (C, joules g − 1 h − 1 °C − 1 ) at any given ambient temperature was calculated using the formula: C = MR / (T b – T a ), where MR is metabolic rate (joules g − 1 h − 1 ), T b is body temperature (°C), and T a is ambient temperature (°C).
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This formula was suggested by Aschoff (1981) for calculating conductance at any given Ta. 2.4. Statistics The data were analyzed using the SPSS statistical package (version 12.0 for windows). The difference in body mass between winter and summer was examined using an independent-samples T test. The effect of ambient temperature on metabolic rate, Tb and thermal conductance was analyzed using a repeated measure ANOVA or ANCOVA with body mass as a covariate. Where appropriate, multiple post-hoc comparisons were performed using the least significant difference method (LSD). The differences in metabolic rate between winter and summer groups were analyzed using ANCOVA with body mass as a covariate. All results were plotted or expressed as mean ± SEM and P b 0.05 was taken to be statistically significant. Straight lines or curves were fitted to data as appropriate to analyze the relationship between energetic parameters and Ta. 3. Results Because there were no significant differences between the sexes in any measured parameters (body mass, F1,18 = 0.094, P N 0.05; Tb, F1,17 = 2.138, P N 0.05; metabolic rate, F1,17 = 0.062, P N 0.05; thermal conductance, F1,17 = 0.365, P N 0.05) data from males and females were pooled. 3.1. Body mass and body temperature (Tb) Mean winter and summer body mass was 61.2 ± 0.3 g (range: 58.9 to 62.5 g) and 55.5 ± 1.0 g (range: 51.1 to 60.0 g), respectively. Birds captured in winter had a significantly higher body mass than those captured in summer (t18 = 5.660, P b 0.001) (Table 1). Birds captured in winter displayed significant fluctuations in Tb over a range of ambient temperatures from 5 °C to 40 °C (F10,99 = 4.081, P b 0.001). Mean winter Tb ranged from 41.3 ± 0.2 °C at 5 °C to 42.4 ± 0.2 °C at 40 °C. There was no significant change in winter Tb from 5 °C to 35 °C, and mean winter Tb was 41.5 ± 0.1 °C (F8,77 = 0.825, P N 0.05, Fig. 1). Birds captured in summer displayed no significant change in Tb within a range of ambient temperatures from 5 °C to 40 °C (F10,91 = 0.482, P N 0.05); however, Tbs measured at 40 °C were significantly different from those measured at other temperatures (post-hoc, P b 0.05, Fig. 1).
Fig. 1. Mean body temperature (Tb) vs. ambient temperature in wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer displayed no significant change in Tb within a range of ambient temperatures from 5 °C to 40 °C, but birds captured in winter displayed significant fluctuations in Tb over a range of ambient temperatures from 5 °C to 40 °C. Mean Tb in winter was significantly higher than in summer.
Mean winter and summer Tb were significantly different (41.6 ± 0.1 °C vs. 42.3 ± 0.1 °C, respectively; F1,209 = 70.052, P b 0.001, Fig. 1; Table 1). 3.2. Metabolic rate (MR) and thermal neutral zone (TNZ) Birds captured in winter had significantly different MR over a span of ambient temperatures ranging from 5 °C to 40 °C (F10,98 = 32.594, P b 0.001, Fig. 2). We were unsuccessful in identifying a join-point using a two-phase regression procedure (Nickerson et al., 1989), so we instead fit a linear regression model to data below 27.5 °C and above 37.5 °C. Below 27.5 °C, MR increased linearly with decreasing temperature, −1 2 MR ml O2 h ¼ 431:97–8:07T a Pb0:001; R ¼ 0:726; n ¼ 60 :
Table 1 Energetic parameters of wild Hwamei Garrulax canorus measured in winter and summer at Wenzhou, China.
Sample size (n) Body mass (g) Body temperature (°C) BMR (ml O2 h−1) a b R2 P TNZ (°C) Tlc (°C) Tuc (°C) Conductance (joules g−1 h−1 °C−1) a b R2 P
Winter
Summer
10 61.2 41.6 203.32 431.97 −8.07 0.726 b0.001 28.3–35.1 28.3 35.1 3.73 −0.77 0.05 0.819 b0.001
10 55.5 42.3 168.99 334.77 −5.78 0.753 b0.001 28.7–33.2 28.7 33.2 3.26 −0.97 0.06 0.845 b0.001
The equations are in the form of MR (ml O2 h−1) = a + b × Ta and Log conductance (joules g−1 h−1 °C−1) = a + b × Ta. Each value in the table represents mean ± SEM. BMR is the basal metabolic rate, TNZ is the thermal neutral zone, Tlc is the lower critical temperature and Tuc is the upper critical temperature of the TNZ.
Fig. 2. Mean metabolic rates vs. ambient temperature in wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer and winter had significantly different metabolic rate over a span of ambient temperatures ranging from 5 °C to 40 °C, and winter basal metabolic rate was significantly higher than that measured in summer.
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Above 37.5 °C, MR increased with increasing temperature, −1 2 MR ml O2 h ¼ –118:50 þ 9:18 T a Pb0:01; R ¼ 0:230; n ¼ 30 : Between 27.5 and 37.5 °C, MR appeared independent of Ta, averaging 203.32 ± 11.81 ml O2 h−1 (n = 50). This is about 2.1-fold higher than predicted value based on body mass (McKechnie and Wolf, 2004). The lines described by the above equations intersected MR at 28.3 °C, the lower critical temperature, and at 35.1 °C, the upper critical temperature. Thus, the TNZ extended from 28.3 to 35.1 °C. There were also significant differences in summer MR measured over a wide range of ambient temperatures from 5 °C to 40 °C (F10,90 = 46.356, P b 0.001, Fig. 2). Between 28 °C and 35 °C, MR appeared to be independent of Ta and averaged 168.99 ± 6.45 ml O2 h−1 (n = 36); 1.7-fold higher than predicted value (McKechnie and Wolf, 2004). For Tas below 28 °C, −1 2 MR ml O2 h ¼ 334:77–5:78T a Pb0:001; R ¼ 0:753; n ¼ 60 :
Maximum C was reached at 40 °C, and averaged 29.27 ± 2.41 joules g− 1 h− 1 °C− 1 (Fig. 3). Birds captured in summer also showed a significant increase in C from 5 °C to 40 °C (F10,90 = 213.695, P b 0.001, Fig. 3). Within a temperature range of 5 to 20 °C, birds could keep their Cs stable and this averaged 3.26 ± 0.06 joules g−1 h−1 °C−1, 1.1-fold higher than predicted value (Aschoff, 1981). However, within a temperature of 25–40 °C, C increased significantly with increasing Ta, the relationship being described by the equation: −1 −1 B −1 2 Log C; joules g h C ¼ –0:97 þ 0:06T a Pb0:001; R ¼ 0:845; n ¼ 62 :
Within this temperature range, C reached 38.12 ± 2.29 joules g−1 h−1 °C−1 at a Ta of 40 °C (Fig. 3). Within a temperature range of 5–20 °C, the mean C of birds caught in winter was significantly higher than that of those caught in summer; (F1,78 = 19.999, P b 0.001, Fig. 3). 4. Discussion
For Tas above 35 °C, −1 2 ¼ –336:57 þ 15:25T a Pb0:001; R ¼ 0:711; n ¼ 30 : MR ml O2 h These lines intersected MR at 28.7 °C and at 33.2 °C, so the TNZ was between 28.7 and 33.2 °C. Winter BMR was significantly higher than that measured in summer (F1, 85 = 27.826, P b 0.001, Fig. 2). 3.3. Thermal conductance (C) Thermal conductance (C) in winter increased significantly with increasing Ta (F10,98 = 91.105, P b 0.001, Fig. 3). Mean C was 3.73 ± 0.09 joules g−1 h−1 °C−1 within a temperature range of 5 °C to 20 °C, 1.3-fold higher than predicted value (Aschoff, 1981). Within and above the TNZ, C increased significantly with increasing Ta, the relationship between C and Ta being described by the equation: −1 −1 −1 2 ¼ –0:77 þ 0:05T a Pb0:001; R ¼ 0:819; n ¼ 70 : Log C; joules g h BC
Fig. 3. Mean thermal conductance vs. ambient temperature of wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer and winter had significantly different thermal conductance over a span of ambient temperatures ranging from 5 °C to 40 °C, and winter thermal conductance was significantly higher than that measured in summer.
Small, northern, warm and temperate habitat birds cope with seasonal change through a wide array of strategies. These include, but are not limited to, adjustments in body mass, body fat, metabolic rates and behavior. The results of this study show that the Hwamei maintains stable body temperature, below and within the thermal neutral zone (TNZ), in both winter and summer. However, birds captured in winter had a significantly higher metabolic rate and a broader TNZ than those caught in summer. As discussed above, the result of these seasonal changes is that thermoregulation in cold conditions is more expensive for winter-acclimated Hwameis than for summer acclimated birds. 4.1. Body mass and body temperature Seasonal changes in body mass, especially in small birds, are considered to be adaptive strategies important for survival (Pendergast and Boag, 1973; Cooper, 2000). Several factors, such as temperature, photoperiod, food quantity and quality, and physiological status, have been implicated in the regulation of variation in body mass (Dawson et al., 1983; Marsh and Dawson, 1989; Swanson, 1991; O'Connor, 1995; Cooper, 2007). Many small birds inhabiting seasonal environments, such as common redpolls (Pohl and West, 1973), American goldfinches Carduelis tristis (Dawson and Carey, 1976), dark-eyed juncos Junco hyemalis (Swanson, 1990, 1991), white-breasted nuthatches Sitta carolinensis and downy woodpeckers Picoides pubescens (Liknes and Swanson, 1996), Chinese bulbuls Pycnonotus sinensis (Zheng et al., 2008a, 2010, 2014) and Eurasian tree sparrows (Zheng et al., 2008b), either maintain a stable body mass or increase in body mass, when exposed to winter conditions. Our results indicate that the Hwamei undergoes seasonal changes in body mass, and is, on average, 10% heavier in winter than in summer. This increased winter body mass could reflect both increased thermogenic capacity and the accumulation of energy reserves (Dawson et al., 1983; Landys-Ciannelli et al., 2003; Cooper, 2007). An increase in the body mass of birds during winter often results from increases in fat deposits and/or of metabolically active tissues (Williams and Tieleman, 2000; Zheng et al., 2008b). Compared with mammals, birds have relatively high Tb and metabolic rates (McNab, 1966; Prinzinger et al., 1991). Our data indicate significant seasonal variation in Tb in the Hwamei. Over a range of Tas from 5 °C to 40 °C, winter Tb averaged 41.6 °C compared to 42.3 °C in summer. This is similar to the Tb of 41.7 °C recorded in the same Hwamei population by Liu et al. (2005), and is higher than the previously reported Tb for passerine birds of 39.0 °C (Prinzinger et al., 1991). Relatively high and stable Tb may be a characteristic of the Hwamei. Similar results have been reported in white-breasted nuthatches and downy woodpeckers (Liknes and Swanson, 1996), American tree sparrows
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Spizella arborea (Swanson, 2001), American goldfinches (Liknes et al., 2002) and New Holland honeyeaters (Yuni and Rose, 2005) from different sites. 4.2. Basal metabolic rate (BMR) Many factors such as body size, climate, phylogeny, life history traits and food habits can affect variation in BMR (White et al., 2007; Swanson and Plamer, 2009; Nzama et al., 2010; Hegemann et al., 2012). Many small, winter-active birds inhabiting warm and temperate latitudes in the Northern hemisphere increase their BMR in winter compared to that in summer; for example, downy woodpeckers and white-breasted nuthatches (Liknes and Swanson, 1996), Chinese bulbuls (Zheng et al., 2008a), Eurasian tree sparrows (Zheng et al., 2008b), and dark-eyed juncos (Swanson, 1990). Our results indicate that the Hwamei's BMR is 20% higher in winter than in summer. Similar results have previously been reported in the same population of Hwameis (Liu et al., 2005). The TNZ metabolic rate measured by Liu et al. (2005) in June was 167 ml O2 h−1, which is similar to that measured during summer in this study. How much does BMR vary seasonally in those species showing labile BMR? Liknes et al. (2002) suggested that the increased fat stored in Nearctic birds during winter provides them with a larger energy reservoir to draw upon during cold exposure, which could in turn accommodate a higher winter BMR. Dawson and O'Connor (1996) also mentioned that winter increases in BMR could serve as an emergency response for protection of peripheral tissues from cold injury and for initiation of shivering, thus decreasing energetic costs of thermoregulation (Swanson, 2010). Regarding the relationship of increases in BMR with increases in cold tolerance, Dawson and O'Connor (1996) suggested that BMR was simply a by-product of other systemic changes in cold acclimation. The byproduct possibility seems most likely, as the increased metabolic machinery required for enhanced thermogenesis in winter probably entails higher maintenance costs (Swanson, 1991, 2010). With respect to metabolic adjustments, the BMR of an animal is the sum of the MRs of its organs and other metabolically active structures (Zheng et al., 2008a; Swanson, 2010; Clapham, 2012). The mechanisms driving seasonal metabolic adjustments in birds may occur at multiple hierarchical levels. McKechnie (2008) and Swanson (2010) have identified major physiological and morphological pathways whereby metabolic rates are up-regulated, namely adjustments in organ mass (Williams and Tieleman, 2000; Liu and Li, 2006; Vézina et al., 2006) and adjustments in mass-specific metabolic intensity and transport capacities for substrates (Zheng et al., 2008b, 2010, 2013a, 2014). For example, Zheng et al. (2014) showed significant seasonal variation in some central organ masses (log dry organ mass residuals versus log BMR residuals) and indicators (state-4 respiration and cytochrome c oxidase) of cellular metabolic intensity in liver and muscle, and variation in heart and pectoralis muscle masses and liver and muscle markers of cellular metabolic intensity were significantly positively correlated with RMR variation in individual bulbuls, so the winter increases in organ masses and activities of respiratory enzyme activities documented in this study are likely related to the seasonal differences in RMR. Similarly, Zheng et al. (2013b) showed that the mass of the liver, kidney and total gastrointestinal tract (log dry organ mass residuals versus log BMR residuals) of cold acclimated (10 °C) bulbuls was higher than that of warm acclimated (30 °C) birds, and that state-4 respiration and cytochrome c oxidase were higher in the liver and muscle in cold acclimated bulbuls than in warm acclimated birds. These results suggest that plasticity in nutritional and metabolic organ mass is very important for the regulation of thermogenesis in small birds exposed to seasonal changes and temperature acclimation. Changes in liver and muscle mitochondrial respiration and cytochrome c oxidase (COX) activity are the cytological mechanisms responsible for elevating BMR in winter or during cold acclimation (Swanson, 2010; Zheng et al., 2010, 2013b, 2014). Our recent data indicated that the masses of liver, small intestine and total gastrointestinal tract (log dry organ mass residuals versus log BMR
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residuals) in winter Hwameis were significantly higher compared with summer Hwameis (L.M. Zhou et al., unpublished data). Our recent data in Hwameis also indicated that winter Hwameis showed significantly higher state-4 respiration and activities of COX in liver, heart, kidney and muscle than summer Hwameis (L.M. Zhou et al., unpublished data). These data may explain the organ masses and activities of respiratory enzyme activities is one of the cytological mechanisms of elevating RMR.
4.3. Thermal neutral zone (TNZ) and thermal conductance (C) By definition, TNZ is the range of ambient temperatures, within which body temperature regulation is achieved only by control of sensible heat loss, i.e. without regulatory changes in metabolic heat production or evaporative heat loss (IUPS Thermal Commission, 1987). Some birds, like monk parakeets Myiopsitta monachus (Weathers and Caccamise, 1978) and rock kestrels Falco rupicolis (Bush et al., 2008) show a shift in the TNZ so that the lower critical temperature (Tlc) is lower in winter than in summer, whereas others, like American goldfinches (Dawson and Carey, 1976) and Chinese bulbuls (Zheng et al., 2008a) do not. Our results indicate that the Hwamei has a TNZ of 28.7 °C to 33.2 °C in summer but a TNZ of 28.3 to 35.1 °C in winter (Table 1). High BMR and wide TNZ are adaptive strategies to cold (Schmidt-Nielsen, 1997). In this study, Tuc of Hwameis in winter is 35.1 °C, higher than that of those in summer. The higher Tuc in winter is probably a result of higher thermal conductance and body temperature in winter. Thermal conductance, the reciprocal of insulation, traditionally has been calculated as the slope of the line relating oxygen consumption to Ta below TNZ (Weathers, 1997). Thermal conductance depends on body mass. The major reasons for this are size dependent changes in the surface to volume ratio, the relationship between plumage thickness and size and the fact that the thickness of the boundary layer depends on the radius of curvature which in turn changes with size (Aschoff, 1981). In general, birds that live at low latitudes have higher conductance than expected based on their body mass. This is analogous to the increased conductance seen in desert species (Weathers, 1997). In birds native to hot climates, a high thermal conductance may aid heat loss when Ta is less than Tb (Burton and Weathers, 2003). High thermal conductance and tolerance to hyperthermia are factors thought to shift the TNZ to higher Tas (Weathers, 1997). We found that the Hwamei has higher thermal conductance in winter than summer, which is consistent with data previously reported on Chinese bulbuls (Zheng et al. 2008a). Marschall and Prinzinger (1991) noted a positive correlation between thermal conductance and BMR, species with a lower than expected BMR having a lower than expected conductance and vice versa. A positive relationship between thermal conductance and BMR appears to hold for species like red-capped Pipra mentalis and golden-collared manakins Manacus vitellinus (Bartholomew et al., 1983), orangecheeked waxbills Estrilda melpoda and cut-throat finches Amadina fasciata (Marschall and Prinzinger, 1991). From the perspective of thermoregulation, high Cs are unfavorable to birds in winter; however, in small birds, increasing metabolic heat production is main way to compensate heat loss in winter. Seasonal changes in insulation are not prominently involved in winter acclimatization of Hwameis. This shows that like several other relatively small birds they rely mostly on metabolic capacity rather than insulation to maintain their body temperature in cold weathers. In conclusion, our results indicate that the Hwamei has higher body mass, BMR and a broader TNZ in winter than in summer. This supports the previous hypothesis that the Hwamei undergoes seasonal fluctuations in body mass and metabolic rate to cope with seasonal climate change. The Hwamei's higher winter body mass and metabolic rate, and broader winter TNZ, probably enhance its winter survival whereas its narrower summer TNZ could enhance its ability to survive hot
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weather. These traits are consistent with the wide temperature variation between winter and summer in Wenzhou. Acknowledgements We are grateful to Dr. David L. Swanson for providing several references. We thank Dr. Ron Moorhouse for revising the English and giving some suggestions. We also thank the anonymous reviewers for their numerous helpful comments and suggestions. This study was financially supported by grants from the National Natural Science Foundation of China (No. 31070366 and 31470472), the Natural Science Foundation (LY13C030005) in Zhejiang Province and the Zhejiang Province “Xinmiao” Project. References Aschoff, J., 1981. Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp. Biochem. Physiol. A 69, 611–619. Aschoff, J., Pohl, H., 1970. Der ruheumsatz von vögeln als funktion der tazeszeitund der körpergrösse. J. Ornithol. 111, 38–47. Bartholomew, G.A., Vleck, C.M., Bucher, T.L., 1983. 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Comparative Biochemistry and Physiology, Part A journal homepage: www.elsevier.com/locate/cbpa
Seasonal variation in body mass, body temperature and thermogenesis in the Hwamei, Garrulax canorus Mei-Xiu Wu a, Li-Meng Zhou a, Li-Dan Zhao a, Zhi-Jun Zhao a,b, Wei-Hong Zheng a,b, Jin-Song Liu a,b,⁎ a b
School of Life and Environmental Sciences, Wenzhou University, Wenzhou 325035, China Zhejiang Provincial Key Lab for Water Environment and Marine Biological Resources Protection, Wenzhou 325035, China
a r t i c l e
i n f o
Article history: Received 16 December 2013 Received in revised form 15 September 2014 Accepted 18 September 2014 Available online 26 September 2014 Keywords: Garrulax canorus Body temperature Basal metabolic rate Thermal conductance Seasonal variation
a b s t r a c t The basal thermogenesis of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, particularly changes in ambient temperature (Ta). Many birds living in regions with seasonal fluctuations in Ta typically respond to cold by increasing their insulation and adjusting their metabolic rate. To understand these metabolic adaptations, body temperature (Tb), metabolic rate (MR), thermal neutral zone (TNZ) and thermal conductance were measured within a range of temperatures from 5 to 40 °C in free-living Hwamei, Garrulax canorus, in both winter and summer. Body mass was 61.2 ± 0.3 g in winter and 55.5 ± 1.0 g in summer, and mean Tb was 41.6 ± 0.1 °C in winter and 42.3 ± 0.1 °C in summer. TNZ was between 28.3 and 35.1 °C in winter and between 28.7 and 33.2 °C in summer. The mean basal metabolic rate (BMR) within TNZ was 203.32 ± 11.81 ml O2 h−1 in winter and 168.99 ± 6.45 ml O2 h−1 in summer. Minimum thermal conductance was 3.73 ± 0.09 joules g−1 h−1 °C−1 in winter and 3.26 ± 0.06 joules g−1 h−1 °C−1 in summer. Birds caught in winter had higher body mass, MR, and more variable TNZ than those in summer. The increased winter BMR indicates improved ability to cope with cold and maintenance of a high Tb. These results show that the Hwamei's metabolism is not constant, but exhibits pronounced seasonal phenotypic flexibility associated with maintenance of a high Tb. © 2014 Published by Elsevier Inc.
1. Introduction Phenotypic flexibility refers to phenotypic changes that are reversible, temporary and repeatable, such as acclimation and acclimatization (Piersma and Drent, 2003, Starck and Rahmaan, 2003; Starck, 2009; Liknes and Swanson, 2011a). In birds, phenotypic flexibility in metabolic power output is an important component of thermoregulatory responses to the elevated energy requirements experienced in seasonal environments (McKechnie et al., 2007). Not always, seasonal changes in ambient temperature require species to show seasonal acclimatization to facilitate thermoregulatory homeostasis (Chamane and Downs, 2009). Proper adjustments of thermoregulatory mechanisms ensure the survival of birds when they are subjected to seasonal changes in their natural environment, including temperature, photoperiod, food quality and availability (Zheng et al., 2008a). This includes seasonal changes in thermogenesis, which is highest in winter and lowest in summer (Pohl and West, 1973; Dawson and Carey, 1976; Lindsay et al., 2009a,b; Swanson et al., 2009; Liknes and Swanson, 2011b). Basal metabolic rate (BMR) refers to the energy expenditure of an animal at rest (i.e. in thermoneutrality) during the inactive phase of ⁎ Corresponding author at: School of Life and Environmental Sciences, Wenzhou University, Wenzhou's Chashan University Town, Wenzhou 325035, China. E-mail address: [email protected] (J.-S. Liu).
http://dx.doi.org/10.1016/j.cbpa.2014.09.026 1095-6433/© 2014 Published by Elsevier Inc.
the day, when the animal is not processing food, molting, or reproducing (Zheng et al., 2008a; McNab, 2009; Swanson, 2010). To avoid stress, BMR is measured within the thermal neutral zone (TNZ); a range of temperatures within which endotherms can maintain body temperature using only the heat provided by BMR (Chamane and Downs, 2009). It has been shown that BMR can consume as much as 50–60% of daily energy expenditure (DEE) and variation in BMR may be associated with peak or sustained metabolic rates, species richness and distribution, reproductive effort, activity levels and life-history strategies (McKinney and McWilliams, 2005; Zhao et al., 2010; Wells and Schaeffer, 2012). Comparing small birds from different habitats and different ecologies, Wiersma et al. (2007) stated that tropical birds have a slow life-history and evolve a reduced BMR. Wikelski et al. (2003) emphasized that birds live in tropical environments have lower BMR than predicted for their body from allometric equations, which has been explained as an adaptation to avoid heat stress. Conversely, alpine and boreal high latitude small birds have higher metabolic levels than expected based on their body mass, which has been explained as a direct, or indirect, result of adaptation to a colder climate and shorter breeding season, both of which require higher metabolic capacity (Dawson and Carey, 1976; Zheng et al., 2008b; Swanson and Plamer, 2009; Swanson, 2010). For a number of long-distance migrants, it has been suggested that BMR in their tropical winter range is lower
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than that at their colder breeding grounds (Lindström and Klaassen, 2003; Zheng et al., 2013a). Birds that are acclimated to seasonal decreases in ambient temperature generally increase the capacity to produce heat, which is probably associated with increased BMR (Cooper and Swanson, 1994; Yuni and Rose, 2005; Chamane and Downs, 2009). For example, Pohl and West (1973) showed that the BMR of captive winter-acclimatized common redpolls Acanthis flammea was higher than that measured in summer. Zheng et al. (2008b) also found that Eurasian tree sparrows Passer montanus captured in winter had higher BMR than those captured in summer. Similar results have also been observed in free-living species. The BMR of laughing doves Streptopela senegalensis increased following acclimation to cold temperatures but reduced when they were transferred to a warm room (McKechnie et al., 2007). Williams and Tieleman (2000) observed an increase in the BMR of captive, cold-acclimated hoopoe larks Alaemon alaudipes. These results suggest that the ability to elevate BMR is an important component of winter acclimatization or cold acclimation that is important to winter survival (Zheng et al., 2008b; Swanson, 2010). The Hwamei, Garrulax canorus (Passeriformes, Timaliidae) is an endemic Asian species found in central and southern China, northern Indochina, Hainan and Taiwan (MacKinnon and Phillipps, 2000; Li et al., 2006). Within its natural range, the Hwamei preferentially inhabits scrubland, open woodland, secondary forest, parks and gardens up to 1800 m above sea level (Zheng and Zhang, 2002). Due to the male's elaborate song, the Hwamei are one of the most popular cage birds among the global Chinese community (Li et al., 2006). The Hwamei is omnivorous and mainly feeds on arthropods (insects and spiders) in the breeding season, but also eat plants (fruits and seeds) in autumn and winter (Zheng and Zhang, 2002). The reported ecological physiological properties of the Hwamei are relatively lower BMR than predicted for their body from allometric equations (Aschoff and Pohl, 1970; McKechnie and Wolf, 2004; McKechnie and Swanson, 2010), high body temperature, narrow thermal neutral zone (TNZ) and high metabolic water production/evaporative water loss (MWP/EWL) (Liu et al., 2005; Xia et al., 2013). These characteristics suggest that this species is adapted to warm, mesic climates, where metabolic thermogenesis and water conservation are not strong selective pressures. This study follows up on previous work and investigates seasonal changes in body mass and metabolic performance of the Hwamei in southeast China. We selected this species because it is endemic to Asia and resident in Zhejiang Province where we are based (Zhang et al., 2010), and because there is little available data on the ecological physiology of the Hwamei and the Timaliidae in general (Liu et al., 2005; Xia et al., 2013). To the best of our knowledge, this is the first investigation of seasonal variation in body mass and thermoregulation in the Hwamei. The aim of this study was to evaluate the effects of seasonal changes in body temperature (Ta) on the resting metabolic rate (RMR), BMR and Tb of the Hwamei. Our objectives were to determine summer and winter RMR over a range of Tas by measuring oxygen consumption, to determine summer and winter BMR, and to determine if constant body temperature was maintained over a range of Tas. We predicted that the Hwamei would cope with winter temperatures by changing its body mass, metabolic rate, TNZ and thermal conductance, all of which increase the capacity to survive in cold environments. 2. Materials and methods 2.1. Animals This study was carried out in Wenzhou City, Zhejiang Province (27°29′N, 120°51′E, 14 m in elevation), China. Twenty Hwameis (5 males and 5 females in winter, and 7 males and 3 females in summer) were live-trapped in forest between January 2010 and July 2011. In Wenzhou, the climate is warm-temperate with an average annual rainfall of 1700 mm spread across all months and slightly more precipitation
during winter and spring. The mean winter (December to February) and summer (June to August) temperatures between 2010 and 2011 were 8.4 °C and 31.2 °C, respectively (Wenzhou Bureau of Meteorology). Body mass to the nearest 0.1 g was determined immediately upon capture with an electronic balance (Sartorius BT25S, Germany). Birds were then transported to the laboratory and kept outdoors for 1 or 2 days in cages 50 × 30 × 20 cm3 under natural photoperiod and temperature before physiological measurements were taken. Food and water were supplied ad libitum. All animal procedures were licensed under the Institutional Animal Care and Use Committee of the Institute of Zoology, Chinese Academy of Sciences. 2.2. Metabolic trials Birds' metabolic rates were estimated from measurements of oxygen consumption, obtain with an open-circuit respirometry system (AEI Technologies S-3A/I, USA). The metabolic chambers designed from 1.5 L plastic metabolic chambers, and a perch was provided in respirometry chamber (Smit and McKechnie, 2010). We regulated chamber temperature by putting in a temperaturecontrolled cabinet (Artificial climatic engine BIC-300, China) capable of regulating temperature to ± 0.5 °C. We scrubbed water vapor and CO2 using a silica gel/soda lime/silica column before passing through the oxygen analyzer. We measured oxygen content in excurrent gas from the metabolic chamber with an oxygen sensor (AEI Technologies N-22M, USA). During metabolic rates measurements, we adjusted flow rates of excurrent gas at 300 ml min − 1 in summer and 600 ml min− 1 in winter with a flow control system (AEI technologies R–1, USA) to maintain fractional concentration of O2 in respirometry chambers about 20%, and calibrated to ± 1% accuracy with a general purpose thermal mass flow-meter (TSI 4100 Series, USA) (McNab, 2006). We conducted each oxygen consumption at a different ambient temperature in a randomly determined order (5, 10, 15, 20, 25, 28, 30, 32, 35, 37.5 and 40 °C for summer, and 5, 10, 15, 20, 25, 27.5, 30, 32.5, 35, 37.5 and 40 °C for winter). We obtained baseline O2 concentrations before and after each test (Li et al., 2010). All measurements of gas exchange were obtained during the rest-phase of birds' circadian cycles (between 20:00 and 24:00) in darkened chambers, and from individuals that could reasonably be expected to be postabsorptive. Food was removed 4 h before each measurement period to minimize the heat increment associated with feeding. We ensured that the birds were perching calmly in the chambers, and then started recording oxygen consumption data at least 1 h after the rest-phase. Each animal was generally in the metabolic chamber for at least 2 h. From these data, we calculated 5 min running means of instantaneous oxygen consumption over the entire test period using equation 2 of Hill (1972), and considered the lowest 5 min mean oxygen consumption over the test period as resting metabolic rate (Smit and McKechnie, 2010). We expressed all values for oxygen consumption as ml O 2 h− 1 and corrected to STPD conditions (Schmidt-Nielsen, 1997). Body temperature (T b) was measured during metabolic measurements using a lubricated thermocouple. This was inserted cloacally to a depth at which a slight withdrawal did not result in a change in the reading (1–2 cm). Thermocouple outputs were digitized using a thermocouple meter (Beijing Normal University Instruments Co.). Body mass was measured to the nearest 0.1 g before and after the experiments, and mean body mass was used in calculations. All measurements were made daily between 20:00 and 24:00. 2.3. Thermal conductance Total thermal conductance (C, joules g − 1 h − 1 °C − 1 ) at any given ambient temperature was calculated using the formula: C = MR / (T b – T a ), where MR is metabolic rate (joules g − 1 h − 1 ), T b is body temperature (°C), and T a is ambient temperature (°C).
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This formula was suggested by Aschoff (1981) for calculating conductance at any given Ta. 2.4. Statistics The data were analyzed using the SPSS statistical package (version 12.0 for windows). The difference in body mass between winter and summer was examined using an independent-samples T test. The effect of ambient temperature on metabolic rate, Tb and thermal conductance was analyzed using a repeated measure ANOVA or ANCOVA with body mass as a covariate. Where appropriate, multiple post-hoc comparisons were performed using the least significant difference method (LSD). The differences in metabolic rate between winter and summer groups were analyzed using ANCOVA with body mass as a covariate. All results were plotted or expressed as mean ± SEM and P b 0.05 was taken to be statistically significant. Straight lines or curves were fitted to data as appropriate to analyze the relationship between energetic parameters and Ta. 3. Results Because there were no significant differences between the sexes in any measured parameters (body mass, F1,18 = 0.094, P N 0.05; Tb, F1,17 = 2.138, P N 0.05; metabolic rate, F1,17 = 0.062, P N 0.05; thermal conductance, F1,17 = 0.365, P N 0.05) data from males and females were pooled. 3.1. Body mass and body temperature (Tb) Mean winter and summer body mass was 61.2 ± 0.3 g (range: 58.9 to 62.5 g) and 55.5 ± 1.0 g (range: 51.1 to 60.0 g), respectively. Birds captured in winter had a significantly higher body mass than those captured in summer (t18 = 5.660, P b 0.001) (Table 1). Birds captured in winter displayed significant fluctuations in Tb over a range of ambient temperatures from 5 °C to 40 °C (F10,99 = 4.081, P b 0.001). Mean winter Tb ranged from 41.3 ± 0.2 °C at 5 °C to 42.4 ± 0.2 °C at 40 °C. There was no significant change in winter Tb from 5 °C to 35 °C, and mean winter Tb was 41.5 ± 0.1 °C (F8,77 = 0.825, P N 0.05, Fig. 1). Birds captured in summer displayed no significant change in Tb within a range of ambient temperatures from 5 °C to 40 °C (F10,91 = 0.482, P N 0.05); however, Tbs measured at 40 °C were significantly different from those measured at other temperatures (post-hoc, P b 0.05, Fig. 1).
Fig. 1. Mean body temperature (Tb) vs. ambient temperature in wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer displayed no significant change in Tb within a range of ambient temperatures from 5 °C to 40 °C, but birds captured in winter displayed significant fluctuations in Tb over a range of ambient temperatures from 5 °C to 40 °C. Mean Tb in winter was significantly higher than in summer.
Mean winter and summer Tb were significantly different (41.6 ± 0.1 °C vs. 42.3 ± 0.1 °C, respectively; F1,209 = 70.052, P b 0.001, Fig. 1; Table 1). 3.2. Metabolic rate (MR) and thermal neutral zone (TNZ) Birds captured in winter had significantly different MR over a span of ambient temperatures ranging from 5 °C to 40 °C (F10,98 = 32.594, P b 0.001, Fig. 2). We were unsuccessful in identifying a join-point using a two-phase regression procedure (Nickerson et al., 1989), so we instead fit a linear regression model to data below 27.5 °C and above 37.5 °C. Below 27.5 °C, MR increased linearly with decreasing temperature, −1 2 MR ml O2 h ¼ 431:97–8:07T a Pb0:001; R ¼ 0:726; n ¼ 60 :
Table 1 Energetic parameters of wild Hwamei Garrulax canorus measured in winter and summer at Wenzhou, China.
Sample size (n) Body mass (g) Body temperature (°C) BMR (ml O2 h−1) a b R2 P TNZ (°C) Tlc (°C) Tuc (°C) Conductance (joules g−1 h−1 °C−1) a b R2 P
Winter
Summer
10 61.2 41.6 203.32 431.97 −8.07 0.726 b0.001 28.3–35.1 28.3 35.1 3.73 −0.77 0.05 0.819 b0.001
10 55.5 42.3 168.99 334.77 −5.78 0.753 b0.001 28.7–33.2 28.7 33.2 3.26 −0.97 0.06 0.845 b0.001
The equations are in the form of MR (ml O2 h−1) = a + b × Ta and Log conductance (joules g−1 h−1 °C−1) = a + b × Ta. Each value in the table represents mean ± SEM. BMR is the basal metabolic rate, TNZ is the thermal neutral zone, Tlc is the lower critical temperature and Tuc is the upper critical temperature of the TNZ.
Fig. 2. Mean metabolic rates vs. ambient temperature in wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer and winter had significantly different metabolic rate over a span of ambient temperatures ranging from 5 °C to 40 °C, and winter basal metabolic rate was significantly higher than that measured in summer.
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Above 37.5 °C, MR increased with increasing temperature, −1 2 MR ml O2 h ¼ –118:50 þ 9:18 T a Pb0:01; R ¼ 0:230; n ¼ 30 : Between 27.5 and 37.5 °C, MR appeared independent of Ta, averaging 203.32 ± 11.81 ml O2 h−1 (n = 50). This is about 2.1-fold higher than predicted value based on body mass (McKechnie and Wolf, 2004). The lines described by the above equations intersected MR at 28.3 °C, the lower critical temperature, and at 35.1 °C, the upper critical temperature. Thus, the TNZ extended from 28.3 to 35.1 °C. There were also significant differences in summer MR measured over a wide range of ambient temperatures from 5 °C to 40 °C (F10,90 = 46.356, P b 0.001, Fig. 2). Between 28 °C and 35 °C, MR appeared to be independent of Ta and averaged 168.99 ± 6.45 ml O2 h−1 (n = 36); 1.7-fold higher than predicted value (McKechnie and Wolf, 2004). For Tas below 28 °C, −1 2 MR ml O2 h ¼ 334:77–5:78T a Pb0:001; R ¼ 0:753; n ¼ 60 :
Maximum C was reached at 40 °C, and averaged 29.27 ± 2.41 joules g− 1 h− 1 °C− 1 (Fig. 3). Birds captured in summer also showed a significant increase in C from 5 °C to 40 °C (F10,90 = 213.695, P b 0.001, Fig. 3). Within a temperature range of 5 to 20 °C, birds could keep their Cs stable and this averaged 3.26 ± 0.06 joules g−1 h−1 °C−1, 1.1-fold higher than predicted value (Aschoff, 1981). However, within a temperature of 25–40 °C, C increased significantly with increasing Ta, the relationship being described by the equation: −1 −1 B −1 2 Log C; joules g h C ¼ –0:97 þ 0:06T a Pb0:001; R ¼ 0:845; n ¼ 62 :
Within this temperature range, C reached 38.12 ± 2.29 joules g−1 h−1 °C−1 at a Ta of 40 °C (Fig. 3). Within a temperature range of 5–20 °C, the mean C of birds caught in winter was significantly higher than that of those caught in summer; (F1,78 = 19.999, P b 0.001, Fig. 3). 4. Discussion
For Tas above 35 °C, −1 2 ¼ –336:57 þ 15:25T a Pb0:001; R ¼ 0:711; n ¼ 30 : MR ml O2 h These lines intersected MR at 28.7 °C and at 33.2 °C, so the TNZ was between 28.7 and 33.2 °C. Winter BMR was significantly higher than that measured in summer (F1, 85 = 27.826, P b 0.001, Fig. 2). 3.3. Thermal conductance (C) Thermal conductance (C) in winter increased significantly with increasing Ta (F10,98 = 91.105, P b 0.001, Fig. 3). Mean C was 3.73 ± 0.09 joules g−1 h−1 °C−1 within a temperature range of 5 °C to 20 °C, 1.3-fold higher than predicted value (Aschoff, 1981). Within and above the TNZ, C increased significantly with increasing Ta, the relationship between C and Ta being described by the equation: −1 −1 −1 2 ¼ –0:77 þ 0:05T a Pb0:001; R ¼ 0:819; n ¼ 70 : Log C; joules g h BC
Fig. 3. Mean thermal conductance vs. ambient temperature of wild Hwamei caught in winter and summer at Wenzhou, China. Values are mean ± SEM. Birds captured in summer and winter had significantly different thermal conductance over a span of ambient temperatures ranging from 5 °C to 40 °C, and winter thermal conductance was significantly higher than that measured in summer.
Small, northern, warm and temperate habitat birds cope with seasonal change through a wide array of strategies. These include, but are not limited to, adjustments in body mass, body fat, metabolic rates and behavior. The results of this study show that the Hwamei maintains stable body temperature, below and within the thermal neutral zone (TNZ), in both winter and summer. However, birds captured in winter had a significantly higher metabolic rate and a broader TNZ than those caught in summer. As discussed above, the result of these seasonal changes is that thermoregulation in cold conditions is more expensive for winter-acclimated Hwameis than for summer acclimated birds. 4.1. Body mass and body temperature Seasonal changes in body mass, especially in small birds, are considered to be adaptive strategies important for survival (Pendergast and Boag, 1973; Cooper, 2000). Several factors, such as temperature, photoperiod, food quantity and quality, and physiological status, have been implicated in the regulation of variation in body mass (Dawson et al., 1983; Marsh and Dawson, 1989; Swanson, 1991; O'Connor, 1995; Cooper, 2007). Many small birds inhabiting seasonal environments, such as common redpolls (Pohl and West, 1973), American goldfinches Carduelis tristis (Dawson and Carey, 1976), dark-eyed juncos Junco hyemalis (Swanson, 1990, 1991), white-breasted nuthatches Sitta carolinensis and downy woodpeckers Picoides pubescens (Liknes and Swanson, 1996), Chinese bulbuls Pycnonotus sinensis (Zheng et al., 2008a, 2010, 2014) and Eurasian tree sparrows (Zheng et al., 2008b), either maintain a stable body mass or increase in body mass, when exposed to winter conditions. Our results indicate that the Hwamei undergoes seasonal changes in body mass, and is, on average, 10% heavier in winter than in summer. This increased winter body mass could reflect both increased thermogenic capacity and the accumulation of energy reserves (Dawson et al., 1983; Landys-Ciannelli et al., 2003; Cooper, 2007). An increase in the body mass of birds during winter often results from increases in fat deposits and/or of metabolically active tissues (Williams and Tieleman, 2000; Zheng et al., 2008b). Compared with mammals, birds have relatively high Tb and metabolic rates (McNab, 1966; Prinzinger et al., 1991). Our data indicate significant seasonal variation in Tb in the Hwamei. Over a range of Tas from 5 °C to 40 °C, winter Tb averaged 41.6 °C compared to 42.3 °C in summer. This is similar to the Tb of 41.7 °C recorded in the same Hwamei population by Liu et al. (2005), and is higher than the previously reported Tb for passerine birds of 39.0 °C (Prinzinger et al., 1991). Relatively high and stable Tb may be a characteristic of the Hwamei. Similar results have been reported in white-breasted nuthatches and downy woodpeckers (Liknes and Swanson, 1996), American tree sparrows
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Spizella arborea (Swanson, 2001), American goldfinches (Liknes et al., 2002) and New Holland honeyeaters (Yuni and Rose, 2005) from different sites. 4.2. Basal metabolic rate (BMR) Many factors such as body size, climate, phylogeny, life history traits and food habits can affect variation in BMR (White et al., 2007; Swanson and Plamer, 2009; Nzama et al., 2010; Hegemann et al., 2012). Many small, winter-active birds inhabiting warm and temperate latitudes in the Northern hemisphere increase their BMR in winter compared to that in summer; for example, downy woodpeckers and white-breasted nuthatches (Liknes and Swanson, 1996), Chinese bulbuls (Zheng et al., 2008a), Eurasian tree sparrows (Zheng et al., 2008b), and dark-eyed juncos (Swanson, 1990). Our results indicate that the Hwamei's BMR is 20% higher in winter than in summer. Similar results have previously been reported in the same population of Hwameis (Liu et al., 2005). The TNZ metabolic rate measured by Liu et al. (2005) in June was 167 ml O2 h−1, which is similar to that measured during summer in this study. How much does BMR vary seasonally in those species showing labile BMR? Liknes et al. (2002) suggested that the increased fat stored in Nearctic birds during winter provides them with a larger energy reservoir to draw upon during cold exposure, which could in turn accommodate a higher winter BMR. Dawson and O'Connor (1996) also mentioned that winter increases in BMR could serve as an emergency response for protection of peripheral tissues from cold injury and for initiation of shivering, thus decreasing energetic costs of thermoregulation (Swanson, 2010). Regarding the relationship of increases in BMR with increases in cold tolerance, Dawson and O'Connor (1996) suggested that BMR was simply a by-product of other systemic changes in cold acclimation. The byproduct possibility seems most likely, as the increased metabolic machinery required for enhanced thermogenesis in winter probably entails higher maintenance costs (Swanson, 1991, 2010). With respect to metabolic adjustments, the BMR of an animal is the sum of the MRs of its organs and other metabolically active structures (Zheng et al., 2008a; Swanson, 2010; Clapham, 2012). The mechanisms driving seasonal metabolic adjustments in birds may occur at multiple hierarchical levels. McKechnie (2008) and Swanson (2010) have identified major physiological and morphological pathways whereby metabolic rates are up-regulated, namely adjustments in organ mass (Williams and Tieleman, 2000; Liu and Li, 2006; Vézina et al., 2006) and adjustments in mass-specific metabolic intensity and transport capacities for substrates (Zheng et al., 2008b, 2010, 2013a, 2014). For example, Zheng et al. (2014) showed significant seasonal variation in some central organ masses (log dry organ mass residuals versus log BMR residuals) and indicators (state-4 respiration and cytochrome c oxidase) of cellular metabolic intensity in liver and muscle, and variation in heart and pectoralis muscle masses and liver and muscle markers of cellular metabolic intensity were significantly positively correlated with RMR variation in individual bulbuls, so the winter increases in organ masses and activities of respiratory enzyme activities documented in this study are likely related to the seasonal differences in RMR. Similarly, Zheng et al. (2013b) showed that the mass of the liver, kidney and total gastrointestinal tract (log dry organ mass residuals versus log BMR residuals) of cold acclimated (10 °C) bulbuls was higher than that of warm acclimated (30 °C) birds, and that state-4 respiration and cytochrome c oxidase were higher in the liver and muscle in cold acclimated bulbuls than in warm acclimated birds. These results suggest that plasticity in nutritional and metabolic organ mass is very important for the regulation of thermogenesis in small birds exposed to seasonal changes and temperature acclimation. Changes in liver and muscle mitochondrial respiration and cytochrome c oxidase (COX) activity are the cytological mechanisms responsible for elevating BMR in winter or during cold acclimation (Swanson, 2010; Zheng et al., 2010, 2013b, 2014). Our recent data indicated that the masses of liver, small intestine and total gastrointestinal tract (log dry organ mass residuals versus log BMR
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residuals) in winter Hwameis were significantly higher compared with summer Hwameis (L.M. Zhou et al., unpublished data). Our recent data in Hwameis also indicated that winter Hwameis showed significantly higher state-4 respiration and activities of COX in liver, heart, kidney and muscle than summer Hwameis (L.M. Zhou et al., unpublished data). These data may explain the organ masses and activities of respiratory enzyme activities is one of the cytological mechanisms of elevating RMR.
4.3. Thermal neutral zone (TNZ) and thermal conductance (C) By definition, TNZ is the range of ambient temperatures, within which body temperature regulation is achieved only by control of sensible heat loss, i.e. without regulatory changes in metabolic heat production or evaporative heat loss (IUPS Thermal Commission, 1987). Some birds, like monk parakeets Myiopsitta monachus (Weathers and Caccamise, 1978) and rock kestrels Falco rupicolis (Bush et al., 2008) show a shift in the TNZ so that the lower critical temperature (Tlc) is lower in winter than in summer, whereas others, like American goldfinches (Dawson and Carey, 1976) and Chinese bulbuls (Zheng et al., 2008a) do not. Our results indicate that the Hwamei has a TNZ of 28.7 °C to 33.2 °C in summer but a TNZ of 28.3 to 35.1 °C in winter (Table 1). High BMR and wide TNZ are adaptive strategies to cold (Schmidt-Nielsen, 1997). In this study, Tuc of Hwameis in winter is 35.1 °C, higher than that of those in summer. The higher Tuc in winter is probably a result of higher thermal conductance and body temperature in winter. Thermal conductance, the reciprocal of insulation, traditionally has been calculated as the slope of the line relating oxygen consumption to Ta below TNZ (Weathers, 1997). Thermal conductance depends on body mass. The major reasons for this are size dependent changes in the surface to volume ratio, the relationship between plumage thickness and size and the fact that the thickness of the boundary layer depends on the radius of curvature which in turn changes with size (Aschoff, 1981). In general, birds that live at low latitudes have higher conductance than expected based on their body mass. This is analogous to the increased conductance seen in desert species (Weathers, 1997). In birds native to hot climates, a high thermal conductance may aid heat loss when Ta is less than Tb (Burton and Weathers, 2003). High thermal conductance and tolerance to hyperthermia are factors thought to shift the TNZ to higher Tas (Weathers, 1997). We found that the Hwamei has higher thermal conductance in winter than summer, which is consistent with data previously reported on Chinese bulbuls (Zheng et al. 2008a). Marschall and Prinzinger (1991) noted a positive correlation between thermal conductance and BMR, species with a lower than expected BMR having a lower than expected conductance and vice versa. A positive relationship between thermal conductance and BMR appears to hold for species like red-capped Pipra mentalis and golden-collared manakins Manacus vitellinus (Bartholomew et al., 1983), orangecheeked waxbills Estrilda melpoda and cut-throat finches Amadina fasciata (Marschall and Prinzinger, 1991). From the perspective of thermoregulation, high Cs are unfavorable to birds in winter; however, in small birds, increasing metabolic heat production is main way to compensate heat loss in winter. Seasonal changes in insulation are not prominently involved in winter acclimatization of Hwameis. This shows that like several other relatively small birds they rely mostly on metabolic capacity rather than insulation to maintain their body temperature in cold weathers. In conclusion, our results indicate that the Hwamei has higher body mass, BMR and a broader TNZ in winter than in summer. This supports the previous hypothesis that the Hwamei undergoes seasonal fluctuations in body mass and metabolic rate to cope with seasonal climate change. The Hwamei's higher winter body mass and metabolic rate, and broader winter TNZ, probably enhance its winter survival whereas its narrower summer TNZ could enhance its ability to survive hot
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