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Relationships between interspecific differences in the mass of internal organs, biochemical markers of metabolic activity, and the thermogenic properties of three small passerines
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The capacity for thermogenesis is considered part of an animal's adaptive strategy for survival,and basal metabolic rate (BMR) is one of the fundamental physiological standards for assessing the energy cost of thermoregulation in endotherms. BMR has been shown to be a highly flexible phenotypic trait both between,and within,species,but the metabolic mechanisms involved in the regulation of BMR,which range from variation in organ mass to biochemical adjustments,remain unclear. In this study,we investigated the relationship between organ mass,biochemical markers of metabolic tissue activity,and thermogenesis,in three species of small passerines: wild Bramblings (Fringilla montifringilla),Little Buntings (Emberiza pusilla) and Eurasian Tree Sparrows (Passer montanus),caught in Wenzhou,southeastern China.
Oxygen consumption was measured using an open-circuit respirometry system. Mitochondrial state-4 respiration and cytochrome c oxidase (COX) activity in liver and pectoral muscle were measured with a Clark electrode.
Our results show that Eurasian Tree Sparrows had significantly higher BMR,digestive organ mass,mitochondrial state-4 respiration capacity and COX activity in liver and muscle,than Bramblings and Little Buntings. Furthermore,interspecific differences in BMR were strongly correlated with those indigestive tract mass,state-4 respiration and COX activity.
Our findings suggest that the digestive organ mass,state-4 respiration and COX activity play an important role in determining interspecific differences in BMR.
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Relationships between interspecific differences in the mass of internal organs, biochemical markers of metabolic activity, and the thermogenic properties of three small passerines
)
Abstract
The capacity for thermogenesis is considered part of an animal's adaptive strategy for survival,and basal metabolic rate (BMR) is one of the fundamental physiological standards for assessing the energy cost of thermoregulation in endotherms. BMR has been shown to be a highly flexible phenotypic trait both between,and within,species,but the metabolic mechanisms involved in the regulation of BMR,which range from variation in organ mass to biochemical adjustments,remain unclear. In this study,we investigated the relationship between organ mass,biochemical markers of metabolic tissue activity,and thermogenesis,in three species of small passerines: wild Bramblings (Fringilla montifringilla),Little Buntings (Emberiza pusilla) and Eurasian Tree Sparrows (Passer montanus),caught in Wenzhou,southeastern China.
Oxygen consumption was measured using an open-circuit respirometry system. Mitochondrial state-4 respiration and cytochrome c oxidase (COX) activity in liver and pectoral muscle were measured with a Clark electrode.
Our results show that Eurasian Tree Sparrows had significantly higher BMR,digestive organ mass,mitochondrial state-4 respiration capacity and COX activity in liver and muscle,than Bramblings and Little Buntings. Furthermore,interspecific differences in BMR were strongly correlated with those indigestive tract mass,state-4 respiration and COX activity.
Our findings suggest that the digestive organ mass,state-4 respiration and COX activity play an important role in determining interspecific differences in BMR.
References(60)
Bicudo JE, Vianna CR, Chaui-Berlinck JG. Thermogenesis in birds. Biosci Rep. 2001;21:181-8.
Brand MD, Turner N, Ocloo A, Else PL, Hulbert AJ. Proton conductance and fatty acyl composition of liver mitochondria correlates with body mass in birds. Biochem J. 2003;376:741-8.
Brookes PS, Buckingham JA, Tenreiro AM, Hulbert AJ, Brand MD. The proton permeability of the inner membrane of liver mitochondria from ectothermic and endothermic vertebrates and from obese rats: correlations with standard metabolic rate and phospholipid fatty acid composition. Comp Biochem Phys B. 1998;119:325-34.
Chappell MA, Bech C, Buttemer WA. The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol. 1999;202:2269-79.
Daan S, Masman D, Groenewold A. Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am J Physiol. 1990;259:R333-40.
Dridi S, Onagbesan O, Swennen Q, Buyse J, Decuypere E, Taouis M. Gene expression, tissue distribution and potential physiological role of uncoupling protein in avian species. Comp Biochem Phys A. 2004;139:273-83.
Else PL, Brand MD, Turner N, Hulbert AJ. Respiration rate of hepatocytes varies with body mass in birds. J Exp Biol. 2004;207:2305-11.
Estabrook RW. Mitochondrial respiratory control and the polarographic measurement of ADP: O ratio. Method Enzymol. 1967;10:41-7.
Guderley H, Turner N, Else PL, Hulbert AJ. Why are some mitochondria more powerful than others: insights from comparisons of muscle mitochondria from three terrestrial vertebrates. Comp Biochem Phys A. 2005;142:172-80.
Hammond KA, Chappell MA, Cardullo RA, Lin RS, Johnsen TS. The mechanistic basis of aerobic performance variation in red jungle fowl. J Exp Biol. 2000;203:2053-64.
Hammond KA, Szewczak J, Krόl E. Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient. J Exp Biol. 2001;204:1991-2000.
Hill RW. Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol. 1972;33:261-3.
Kersten M, Piersma T. High levels of energy expenditure in shorebirds; metabolic adaptations to an energetically expensive way of life. Ardea. 1987;75:175-87.
Li YG, Yang ZC, Wang DH. Physiological and biochemical basis of basal metabolic rates in Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus). Comp Biochem Phys A. 2010;157:204-11.
Liknes ET, Swanson DL. Phenotypic flexibility of body composition associated with seasonal acclimatization in passerine birds. J Ther Biol. 2011;36:363-70.
Lindström Å, Klaassen M. High basal metabolic rates in shorebirds: a circumpolar view. Condor. 2003;105:420-7.
Liu JS, Li M. Phenotypic flexibility of metabolic rate and organ masses among tree sparrows Passer montanus in seasonal acclimatization. Acta Zool Sin. 2006;52:469-77.
Liu JS, Zhang ZY, Ma H, Hou ZS. Characteristics of resting metabolic rate in little bunting (Emberiza pusilla) and chestnut bunting (E. rutila). Acta Zool Sin. 2001;47:347-50.
Liu JS, Wang DH, Wang Y, Chen MH, Song CG, Sun RY. Energetics and thermoregulation of the Carpodacus roseus, Fringilla montifringilla and Acanthis flammea. Acta Zool Sin. 2004;50:357-63.
Liu JS, Chen YQ, Li M. Thyroid hormones increase liver and muscle thermogenic capacity in the little buntings (Emberiza pusilla). J Therm Biol. 2006;31:386-93.
Liu JS, Li M, Shao SL. Seasonal changes in thermogenic properties of liver and muscle in tree sparrows Passer montanus. Acta Zool Sin. 2008;54:777-84.
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with Folin phenol reagent. J Biol Chem. 1951;193:265-75.
Lv JW, Xie ZL, Sun YR, Sun CR, Liu LR, Yu TF, Xu XJ, Shao SL, Wang CH. Seasonal plasticity of duodenal morphology and histology in Passer montanus. Zoomorphology. 2014;133:435-43.
MacKinnon J, Phillipps K. A field guide to the birds of China. London: Oxford University Press; 2000.
Marsh RL, Dawson WR, Camilliere JJ, Olson JM. Regulation of glycolysis in the pectoralis muscles of seasonally acclimatized American goldfinches exposed to cold. Am J Physiol. 1990;258:R711-7.
McKechnie AE. Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Phys B. 2008;178:235-47.
McKechnie AE, Freckleton RP, Jetz W. Phenotypic plasticity in the scaling of avian basal metabolic rate. Proc R Soc B Biol Sci. 2006;273:931-7.
McKinney RA, McWilliams SR. A new model to estimate daily energy expenditure for wintering waterfowl. Wilson Bull. 2005;117:44-55.
McNab BK. The relationship among flow rate, chamber volume and calculated rate of metabolism in vertebrate respirometry. Comp Biochem Phys A. 2006;145:287-94.
McNab BK. Ecological factors affect the level and scaling of avian BMR. Comp Biochem Phys A. 2009;152:22-45.
Mullur R, Liu YY, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev. 2014;94:355-82.
Piersma T, Bruinzeel L, Drent R, Kersten M, Van der Meer J, Wiersma P. Variability in basal metabolic rate of a long-distance migrant shorebird (Red Knot, Calidris canutus) reflects shifts in organ sizes. Physiol Zool. 1996;69:191-217.
Pitit M, Vézina F. Phenotype manipulations confirm the role of pectoral muscles and haematocrit in avian maximal thermogenic capacity. J Exp Biol. 2014;217:824-30.
Rasmussen UF, Vielwerth SE, Rasmussen VH. Skeletal muscle bioenergetics: a comparative study of mitochondria isolated from pigeon pectoralis, rat soleus, rat biceps brachii, pig biceps femoris and human quadriceps. Comp Biochem Phys A. 2004;137:435-46.
Rolfe DF, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev. 1997;77:731-58.
Schmidt-Nielsen K. Animal physiology: adaptation and environment. London: Cambridge University Press; 1997.
Scott I, Evans PR. The metabolic output of avian (Sturnus vulgaris, Calidris alpina) adipose tissue, liver and skeletal muscle: implications for BMR/body massrelationships. Comp Biochem Phys A. 1992;103:329-32.
Smit B, McKechnie AE. Avian seasonal metabolic variation in a subtropical desert: basal metabolic rates are lower in winter than in summer. Funct Ecol. 2010;24:330-9.
Steyermark AC, Miamen AG, Feghahati HS, Lewno AW. Physiological and morphological correlates of among-individual variation in standard metabolic rate in the leopard frog Rana pipiens. J Exp Biol. 2005;208:1201-8.
Sundin U, Moore G, Nedergaard J, Cannon B. Thermogenin amount and activity in hamsterbrown fat mitochondria: effect of cold acclimation. Am J Physiol. 1987;252:R822-32.
Swanson DL, Zhang YF, Liu JS, Merkord CL, King MO. Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J Exp Biol. 2014;217:866-75.
Villarin JJ, Schaeffer PJ, Markle RA, Lindstedt SL. Chronic cold exposure increases liver oxidative capacity in the marsupial Monodelphis domestica. Comp Biochem Phys A. 2003;136:621-30.
Weathers WW. Energetics and thermoregulation by small passerines of the humid, lowland tropics. Auk. 1997;114:341-53.
Wells ME, Schaeffer PJ. Seasonality of peak metabolic rate in non-migrant tropical birds. J Avian Biol. 2012;43:481-5.
Wiersma P, Muñoz-Garcia A, Walker A, Williams JB. Tropical birds have a slow pace of life. Proc Natl Acad Sci. 2007;104:9340-5.
Wikelski M, Spinney L, Schelsky W, Scheuerlein A, Gwinner E. Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc R Soc B Biol Sci. 2003;270:2383-8.
Williams J, Tieleman BI. Flexibility in basal metabolic rate and evaporative water loss among hoopoe larks exposed to different environmental temperatures. J Exp Biol. 2000;203:3153-9.
Wu MS, Xiao YC, Yang F, Zhou LM, Zheng WH, Liu JS. Seasonal variation in body mass and energy budget in Chinese bulbuls (Pycnonotus sinensis). Avian Res. 2014;5:4.
Wu MX, Zhou LM, Zhao LD, Zhao ZJ, Zheng WH, Liu JS. Seasonal variation in body mass, body temperature and thermogenesis in the Hwamei, Garrulax canorus. Comp Biochem Phys A. 2015;179:113-9.
Yen PM. Physiological and molecular basis of thyroid hormone action. Physiol Rev. 2001;81:1097-142.
Zheng WH, Liu JS, Jang XH, Fang YY, Zhang GK. Seasonal variation on metabolism and thermoregulation in Chinese bulbul. J Therm Biol. 2008a;33:315-9.
Zheng WH, Li M, Liu JS, Shao SL. Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp Biochem Phys A. 2008b;151:519-25.
Zheng WH, Lin L, Liu JS, Xu XJ, Li M. Geographic variation in basal thermogenesis in little buntings: relationship to cellular thermogenesis and thyroid hormone concentrations. Comp Biochem Phys A. 2013a;164:240-6.
Zheng WH, Lin L, Liu JS, Pan H, Cao MT, Hu YL. Physiological and biochemical thermoregulatory responses of Chinese bulbuls Pycnonotus sinensis to warm temperature: phenotypic flexibility in a small passerine. J Therm Biol. 2013b;38:483-90.
Zheng WH, Liu JS, Swanson DL. Seasonal phenotypic flexibility of body mass, organ masses, and tissue oxidative capacity and their relationship to RMR in Chinese bulbuls. Physiol Biochem Zool. 2014a;87:432-44.
Zheng WH, Li M, Liu JS, Shao SL, Xu XJ. Seasonal variation of metabolic thermogenesis in Eurasian tree sparrows Passer montanus over a latitudinal gradient. Physiol Biochem Zool. 2014b;87:704-18.
Zhou LM, Xia SS, Chen Q, Wang RM, Zheng WH, Liu JS. Phenotypic flexibility of thermogenesis in the Hwamei (Garrulax canorus): responses to cold acclimation. Am J Physiol. 2016;310:R330-6.
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Acknowledgements
We thank Dr. Ron Moorhouse revising the English and giving some suggestions, and all the members of Animal Physiological Ecology Group, Wenzhou University Institute of Applied Ecology, for their helpful suggestions. This study was financially supported by Grants from the National Natural Science Foundation of China (No. 31470472), the National Undergraduate "Innovation" Project and Zhejiang Province's "Xinmiao" Project.
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