Abstract
Endothermy is a conspicuous and important adaptation in birds. Even though juvenile and adult birds are endothermic and maintain a constant, high body temperature by means of internal heat production, they begin life expressing an ectothermic phenotype. Depending on where a species falls along a continuum of maturity at hatching, from precocial to altricial, they begin to express endothermic traits either close to the time of hatching or as nestlings over a period of 1–3 weeks. Developing endothermy requires attaining a high basal metabolic rate and associated aerobic scope to produce sufficient internal heat, insulation to retain the internally produced heat, and a thermostat that “turns on” heat production in response to cooling ambient temperatures. To support the high metabolic costs of endothermy, the animal must have the capacity to deliver sufficient oxygen and nutrients to the heat-generating tissues. In this review, we examine the development of physiological and morphological traits that are required for endothermy and discuss their potential to limit the development of endothermy. These include ventilatory and cardiovascular function, contribution of visceral organ masses, membrane lipid composition, substrate supply pathways, and skeletal muscle physiology. The developmental trajectories of each of these systems in precocial and altricial species can have significant effects on the development of an endothermic phenotype.






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- CPT:
-
Carnitine palmitoyl transferase
- DHA:
-
Docosahexaenoic acid
- EP:
-
Externally pipped
- ETS:
-
Electron transport system
- FABP:
-
Fatty acid binding protein
- GLUT4:
-
Glucose transporter
- IP:
-
Internally pipped
- LPL:
-
Lipoprotein lipase
- OXPHOS:
-
Oxidative phosphorylation
- PMR:
-
Peak metabolic rate
- RMR:
-
Resting metabolic rate
- TNZ:
-
Thermal neutral zone
- TRPM8:
-
Transient receptor potential cation channel subfamily M member 8
- UCP:
-
Uncoupling protein
References
Abraham CL, Evans RM (1999) The development of endothermy in American white pelicans. Condor 101:832–841
Ar A, Sidis Y (2002) Nest microclimate during incubation. In: Deeming DC (ed) Avian Incubation: behaviour, environment, and evolution. Oxford University Press, Oxford, pp 143–160
Aulie A (1977) The effect of intermittent cold exposure on the thermoregulatory capacity of Bantam chicks, Gallus domesticus. Comp Biochem Physiol: Mol Integr Physiol 56A:545–549
Austin GT, Ricklefs RE (1977) Growth and development of the rufous-winged sparrow (Aimophila carpalis). Condor 79:37–50
Bech C, Østnes JE (1999) Influence of body composition on the metabolic rate of nestling European shags (Phalacrocorax aristotelis). J Comp Physiol B 169:263–270
Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654
Berman JM (2013) Characterising behavioural thermoregulation in the bearded dragon: The role of TRPM8 (MSc thesis). Brock University, St. Catherines, Ontario
Bícego KC, Mortola JP (2017) Thermal tachypnea in avian embryos. J Exp Biol. doi:10.1242/jeb.171702
Boland R, Martonosi A, Tillack TW (1974) Developmental changes in the composition and function of sarcoplasmic reticulum. J Biol Chem 249:612–623
Booth DT (1987) Metabolic response of mallee fowl Leipoa ocellata embryos to cooling and heating. Physiol Zool 60:446–453
Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275:81–86
Braun EJ, Sweazea KL (2008) Glucose regulation in birds. Comp Biochem Physiol B: Biochem Mol Biol 151:1–9
Bucher TL, Bartholomew GA (1986) The early ontogeny of ventilation and hemeothermy in an altricial bird, Agapornis reseicollis (psittaciformes). Respiration physiology 65(2):197–212
Choi I-H, Ricklefs RE, Shea RE (1993) Skeletal muscle growth, enzyme activities, and the development of thermogenesis: a comparison between altricial and precocial birds. Physiol Zool 66:455–473
Clarke A, Pörtner H-O (2010) Temperature, metabolic power and the evolution of endothermy. Biol Rev Camb Philos Soc 85:703–727
Crossley D, Altimiras J (2000) Ontogeny of cholinergic and adrenergic cardiovascular regulation in the domestic chicken (Gallus gallus). Am J Physiol Regul Integr Comp Physiol 279:R1091-R1098
Crossley DA, Bagatto BP, Dzialowski EM, Burggren WW (2003) Maturation of cardiovascular control mechanisms in the embryonic emu (Dromiceius novaehollandiae). J Exp Biol 206:2703–2710
Dawson WR, Whittow G (1994) The emergence of endothermy in the black-footed and Laysan albatrosses. J Comp Physiol B 164(4):292–298
Dégletagne C, Roussel D, Rouanet JL, Baudimont F, Moureaux E-M, Harvey S, Duchamp C, Le Maho Y, Raccurt M (2013) Growth prior to thermogenesis for a quick fledging of adélie penguin chicks (Pygoscelis adeliae). PLOS One 8:e74154
Dietz M, Van Kampen M (1994) The development of thermoregulation in turkey and guinea fowl hatchlings: similarities and differences. J Comp Physiol B 164(1):69–75
Dietz MW, Drent RH, Ricklefs RE (1995) Biphasic development of metabolic rate in young precocial birds: a possible physiological basis. In: Dietz MW (ed) Development of metabolism and thermoregulation in galliforms: effects of body mass, growth rate and functional maturity. PhD thesis, Utrecht University, pp 57–76
Dietz MW, van Mourik S, Tøien Ø, Koolmees PA, Tersteeg-Zijderveld MHG (1997) Participation of breast and leg muscles in shivering thermogenesis in young turkeys and guinea fowl. J Comp Physiol B 167:451–460
Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool/Rev Can Zool 71:1602–1608
Duchamp C, Barre H (1993) Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings. Am J Physiol Regul Integr Comp Physiol 265(5):R1076-R1083
Duchamp C, Rouanet J-L, Barré H (2002) Ontogeny of thermoregulatory mechanisms in king penguin chicks (Aptenodytes patagonicus). Comp Biochem Physiol A 131:765–773
Dumonteil E, Barré H, Meissner G (1993) Sarcoplasmic reticulum Ca2+-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis. Am J Physiol Cell Physiol 265:C507-C513
Dunn EH (1975) The timing of endothermy in the development of altrical birds. Condor 77:288–293
Dunn EH (1976a) Development of endothermy and existance energy expenditure of nestling double-crested cormorants. Condor 78:350–356
Dunn EH (1976b) The relationship between brood size and age of effective homeothermy in nestling house wrens. Wilson Bull 88:478–482
Dyer MI (1968) Respiratory metabolism studies on red-winged blackbird nestlings. Can J Zool 46:223–233
Dzialowski EM, Burggren WW, Komoro T, Tazawa H (2007) Development of endothermic metabolic response in embryos and hatchlings of the emu (Dromaius novaehollandiae). Respir Physiol Neurobiol 155:286–292
Dzialowski EM, Sirsat TS, Sirsat SKG, Price ER (2016) Breathing while altricial: the ontogeny of ventilatory chemosensitivity in red-winged blackbird (Agelaius phoeniceus) nestlings. Am J Physiol Regul Integr Comp Physiol 311:R1105-R1112
Else PL, Hulbert AJ (1981) Comparison of the “mammal machine” and the “reptile machine”: energy production. Am J Physiol Regul Integr Comp Physiol 240:R3-R9
Else PL, Hulbert AJ (1987) Evolution of mammalian endothermic metabolism: “leaky” membranes as a source of heat. Am J Physiol Regul Integr Comp Physiol 253:R1-R7
Else PL, Wu BJ (1999) What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms? J Comp Physiol B 169:296–302
Eme J, Gwalthney J, Owerkowicz T, Blank JM, Hicks JW (2010) Turning crocodilian hearts into bird hearts: growth rates are similar for alligators with and without right-to-left cardiac shunt. J Exp Biol 213:2673–2680
Eppley ZA (1984) Development of thermoregulatory abilities in Xantus’ murrelet chicks Synthliboramphus hypoleucus. Physiol Zool 57:307–317
Eppley ZA, Russell B (1995) Perinatal changes in avian muscle: implications from ultrastructure for the development of endothermy. J Morphol 225:357–367
Farkas K, Ratchford IAJ, Noble RC, Speake BK (1996) Changes in size and docosahexaenoic acid content of adipocytes during chick embryo development. Lipids 31:313–321
Fongy A, Romestaing C, Blanc C, Lacoste-Garanger N, Rouanet J-L, Raccurt M, Duchamp C (2013) Ontogeny of muscle bioenergetics in Adélie penguin chicks (Pygoscelis adeliae). Am J Physiol Regul Integr Comp Physiol 305:R1065-1075
Freeman BM (1966) The effects of cold, noradrenaline and adrenaline upon the oxygen consumption and carbohydrate metabolism of the young fowl (Gallus domesticus). Comp Biochem Physiol A 18:369–382
Freeman BM (1967) Some effects of cold on the metabolism of the fowl during the perinatal period. Comp Biochem Physiol 20:179–193
Freeman BM, Vince MA (1974) Development of the Avian Embryo. Chapman and Hall, London
Fukuoka S, Khandoker AH, Dzialowski EM, Burggren WW, Tazawa H (2006) Development of endothermic heart rate response in emu (Dromaius novaehollandiae) embryos. In: Yahav S, Tzschentke B (eds) New insights into fundemental physiology and peri-natal adaptation of domestic fowl. Nottingham University Press, Nottingham, pp 29–42
Goodridge AG (1968) Lipolysis in vitro in adipose tissue from embryonic and growing chicks. Am J Physiol 214:902–907
Grav HJ, Borch-Iohnsen B, Dahl HA, Gabrielsen GW, Steen JB (1988) Oxidative capacity of tissues contributing to thermogenesis in eider (Somateria mollissima) ducklings: changes associated with hatching. J Comp Physiol B 158:513–518
Grubb BR (1983) Allometric relations of cardiovascular function in birds. Am J Physiol Heart Circ Physiol 245:H567-572
Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol Regul Integr Comp Physiol 282:R1405-R1413
Hill RW, Beaver DL (1982) Inertial thermostability and thermoregulation in broods of redwing blackbirds. Physiol Zool 55:250–266
Hillman SS, Hedrick MS (2015) A meta-analysis of in vivo vertebrate cardiac performance: implications for cardiovascular support in the evolution of endothermy. J Exp Biol 218:1143–1150
Hillman SS, Hancock TV, Hedrick MS (2013) A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange. J Comp Physiol B 183:167–179
Hissa R, Saarela S, Rintamäki H, Lindén H, Hohtola E (1983) Energetics and development of temperature regulation in Capercaillie Tetrao urogallus. Physiol Zool 56:142–151
Hohtola E (2004) Shivering thermogenesis in birds and mammals. In: Barnes BM, Carey HV (eds) Life in the cold: evoluion, mechanisms, adaptation, and application. Twelfth International Hibernation Symposium. Biological Papers of the University of Alaska, number 27. Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska, pp 241–252
Hohtola E, Visser GH (1998) Development of locomotion and endothermy in altricial and precocial birds. In: Starck JM, Ricklefs RE (eds) Avian Growth and Development. Oxford University Press, New York, pp 157–173
Hoppeler H, Weibel E (2000) Structural and functional limits for oxygen supply to muscle. Acta Physiol Scand 168(4):445–456
Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199:257–274
Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208:1593–1599
Hulbert AJ, Faulks S, Buttemer WA, Else PL (2002a) Acyl composition of muscle membranes varies with body size in birds. J Exp Biol 205:351–3569
Hulbert AJ, Rana T, Couture P (2002b) The acyl composition of mammalian phospholipids: an allometric analysis. Comp Biochem Physiol B: Biochem Mol Biol 132:515–527
Ide ST, Ide R, Mortola JP (2017) The contribution of heart rate to the oxygen consumption of the chicken embryo during cold- or hypoxia-hypometabolism. Comp Biochem Physiol A: Mol Integr Physiol 203:49–58
Khandoker AH, Fukazawa K, Dzialowski EM, Burggren WW, Tazawa H (2004) Maturation of the homeothermic response of heart rate to altered ambient temperature in developing chick hatchlings (Gallus gallus domesticus). Am J Physiol Regul Integr Comp Physiol 286:R129-R137
Konarzewski M, Lilja C, Kozlowski J, Lewończuk (1990) On the optimal growth of the alimentary tract in avian postembryonic development. J Zool 222:89–101
Langslow DR (1972) The development of lipolytic sensitivity in the isolated fat cells of Gallus domesticus during the foetal and neonatal period. Comp Biochem Physiol B: Biochem Mol Biol 43B:689–701
Le Peuch CJ, Ferraz C, Walsh MP, Demaille JG, Fischer EH (1979) Calcium and cyclic nucleotide dependent regulatory mechanisms during development of chick embryo skeletal muscle. Biochemistry 18:5267–5273
Liknes ET, Guglielmo CG, Swanson DL (2014) Phenotypic flexibility in passerine birds: seasonal variation in fuel storage, mobilization and transport. Comp Biochem Physiol A: Mol Integr Physiol 174:1–10
Lilja C (1983) A comparative study of postnatal growth and organ development in some species of birds. Growth 47:317–339
Lilja C (1997a) On the pattern of organ growth in the common tern (Sterna hirundo). Growth Dev Aging 61:11–18
Lilja C (1997b) Oxygen consumption and vital organ masses in youn growing quail (Coturnix coturnix japonica). Acta Physiol Scand 160:113–114
Marjoniemi K, Hohtola E (1999) Shivering thermogenesis in leg and breast muscles of galliform chicks and nestlings of the domestic pigeon. Physiol Biochem Zool 72:484–492
Marsh RL (1979) Development of endothermy in nestling bank swallows (Riparia riparia). Physiol Zool 52:340–353
Marsh RL, Wickler SJ (1982) The role of muscle development in the transition to endothermy in nestling bank swallows, Riparia riparia. J Comp Physiol B 149:99–105
McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940
McKechnie AE, Whitfield MC, Smit B, Gerson AR, Smith EK, Talbot WA, McWhorter TJ, Wolf BO (2016) Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern hemisphere columbids. J Exp Biol 219(14):2145–2155
Menna TM, Mortola JP (2003) Ventilatory chemosensitivity in the chick embryo. Respir Physiol Neurobiol 137:69–79
Mills SH, Heath JE (1972) Responses to thermal stimulation of the preoptic area in the house sparrow, Passer domesticus. Am J Physiol 222:914–919
Moe B, Stølevik E, Bech C (2005) Ducklings exhibit substantial energy-saving mechanisms as a response to short-term food storage. Physiol Biochem Zool 78:90–104
Morrison SF (2011) 2010 Carl Ludwig distinguished lectureship of the APS neural control and autonomic regulation section: central neural pathways for thermoregulatory cold defense. J Appl Physiol 110:1137–1149
Mortola JP (2009) Gas exchange in avian embryos and hatchlings. Comp Biochem Physiol A 153:359–377
Mortola JP, Toro-Velasquez PA (2014) Breathing pattern and ventilatory chemosensitivity of the 1-day old Muscovy duck (Cairina moschata) in relation to its metabolic demands. Comp Biochem Physiol A 167:35–39
Morton ML, Carey C (1971) Growth and the development of endothermy in the mountain white-crowned sparrow (Zonotrichia leucophrys oriantha). Physiol Zool 44:177–189
Nakamura K (2011) Central circuitries for body temperature regulation and fever. Am J Physiol Regul Integr Comp Physiol 301:R1207-1228
Newman SA, Mezentseva NV, Badyaev AV (2013) Gene loss, thermogenesis, and the origin of birds. Ann N Y Acad Sci 1289:36–47
Nickerson JG, Alkhateeb H, Benton CR, Lally J, Nickerson J, Han X-X, Wilson MH, Jain SS, Snook LA, Glatz JFC, Chabowski A, Luiken JJFP, Bonen A (2009) Greater transport efficiencies of the membrane fatty acid transporters FAT/CD36 and FATP4 compared with FABPpm and FATP1 and differential effects on fatty acid esterification and oxidation in rat skeletal muscle. J Biol Chem 284:16522–16530
Oliveira JE, Druyan S, Uni Z, Ashwell CM, Ferket PR (2013) Metabolic profiling of late-term turkey embryos by microarrays. Poult Sci 92:1011–1028
Olson JM (1992) Growth, the development of endothermy, and the allocation of energy in red-winged blackbirds (Agelaius phoeniceus) during the nestling period. Physiol Zool 65:124–152
Olson JM (1994) The ontogeny of shivering thermogenesis in the red-winged blackbird (Agelaius phoeniceus). J Exp Biol 191:59–88
Olson JM (2001) Ontogeny of catabolic and morphological properties of skeletal muscle of the red-winged blackbird (Agelaius phoeniceus). J Comp Physiol B 171:527–542
Østnes JE, Jenssen BM, Bech C (2001) Growth and development of homeothermy in nestling European shags (Phalacrocorax aristotelis). Auk 118:983–995
Palokangas R, Vihko V, Nuuja I (1973) The effects of cold and glucagon on lipolysis, glycogenolysis and oxygen consumption in young chicks. Comp Biochem Physiol A: Mol Integr Physiol 45A:489–495
Pearson JT (1998) Development of thermoregulation and posthatching growth in the altricial cockatiel Nymphicus hollandicus. Physiol Zool 71(2):237–244
Pereyra ME, Morton ML (2001) Nestling growth and thermoregulatory development in subalpine dusky flycatchers. Auk 118:116–136
Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93:993–1017
Ricklefs RE (1967) Relative growth, body constituents, and energy content of nestling barn swallows and red-winged blackbirds. Auk 84:560–570
Ricklefs RE (1975) Patterns of growth in birds. III. Growth and development of the cactus wren. Condor 77:34–45
Ricklefs RE, Hainsworth FR (1968) Temperature regulation in nestling cactus wrens: the development of homeothermy. Condor 70:121–127
Ricklefs RE, Webb T (1985) Water content, thermogenesis, and growth rate of skeletal muscles in the European starling. Auk 102:369–376
Rowland LA, Bal NC, Periasamy M (2015) The role of skeletal-muscle-based thermogenic mechanisms in vertebrate endothermy. Biol Rev 90:1279–1297
Schmidt-Nielsen K (1997) Animal Physiology: Adaptation and the environment, Fifth Edition. Cambridge University Press, Cambridge
Scott GR (2011) Elevated performance: the unique physiology of birds that fly at high altitude. J Exp Biol 214:2455–2462
Seebacher F (2009) Responses to temperture variation: integration of thermoregulation and metabolism in vertebrates. J Exp Biol 212:2885–2891
Seebacher F, Schwartz TS, Thompson MB (2006) Transition from ectothermy to endothermy: the development of metabolic capacity in a bird (Gallus gallus). Proc R Soc Lond Ser B: Biol Sci 273:565–570
Seki Y, Sato K, Akiba Y (2005) Changes in muscle mRNAs for hexokinase, phosphofructokinase-1 and glycogen synthase in acute and persistent hypoglycemia induced by tolbutamide in chickens. Comp Biochem Physiol B: Biochem Mol Biol 142:201–208
Seymour RS, Runciman S, Baudinette RV, Pearson JT (2004) Developmental allometry of pulmonary structure and function in the altricial Australian pelican Pelecanus conspicillatus. J Exp Biol 207:2663–2669
Shell L, Burggren WW, Muirhead D, Nelson TC, Dzialowski EM (2016) Circulatory changes associated with the closure of the ductus arteriosus in hatching emu (Dromaius novaehollandiae). Comp Biochem Physiol A 191:202–208
Shilov IA (1973) Heat regulation in birds (an ecological-physiological outline). Amerind Publishing Co. Pvt. Ltd., New Delhi
Sirsat SKG (2016) Maturation of endothermic capacity within the avian developmental spectrum: a characterization of thermoregulatory metamorphosis (PhD Dissertation). University of North Texas, Denton TX
Sirsat TS, Dzialowski EM (2016) Ventilation changes associated with hatching and maturation of an endothermic phenotype in the Pekin duck, Anas platyrhynchos domestica. Am J Physiol Regul Integr Comp Physiol 310:R766-R775
Sirsat SKG, Sirsat TS, Crossley JL, Sotherland PR, Dzialowski EM (2016a) The 12-day thermoregulatory metamorphosis of Red-winged Blackbirds (Agelaius phoeniceus). J Comp Physiol B 186:651–663
Sirsat SKG, Sirsat TS, Faber A, Duquaine A, Winnick S, Sotherland PR, Dzialowski EM (2016b) Development of endothermy and concomitant increases in cardiac and skeletal muscle mitochondrial respiration in the precocial Pekin duck (Anas platyrhynchos domestica). J Exp Biol 219:1214–1223
Sirsat SKG, Sirsat TS, Price ER, Dzialowski EM (2016c) Post-hatching development of mitochondrial function, organ mass and metabolic rate in two ectotherms, the American alligator (Alligator mississippiensis) and the common snapping turtle (Chelydra serpentina). Biol Open 5:443–451
Smith EK, O’Neill JJ, Gerson AR, McKechnie AE, Wolf BO (2017) Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert songbirds. J Exp Biol 220:3290–3300
Sogge MK, Kern MD, Kern R, van Riper III C (1991) Growth and development of thermoregulation in nestling San Miguel Island song sparrows. Condor 93:773–776
Speake BK, Wood NAR (2005) Timing of incorporation of docosahexaenoic acid into brain and muscle phospholipids during precocial and altricial modes of avian development. Comp Biochem Physiol B: Biochem Mol Biol 141:147–158
Speake BK, Cerolini S, Maldjian A, Noble RC (1997) The preferential mobilisation of C20 and C22 polyunsaturated fatty acids from the adipose tissue of the chick embryo: potential implications regarding the provision of essential fatty acids for neural development. Biochim Biophys Acta 1345:317–326
Speake BK, Murray AMB, Noble RC (1998) Transport and transformations of yolk lipids during development of the avian embryo. Prog Lipid Res 37:1–32
Starck JM, Ricklefs RE (1998) Patterns of development: The altricial-precocial spectrum. In: Starck JM, Ricklefs RE (eds) Avian growth and development: Evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 3–30
Steen JB, Gabrielsen GW (1988) The development of homeothermy in common eider ducklings (Somateria mollissima). Acta Physiol Scand 132:557–561
Sutter GC, Macarthur RA (1992) Development of thermoregulation in a precocial aquatic bird, the American coot (Fulica americana). Comp Biochem Physiol A 101(3):533–543
Swanson DL, Thomas NE, Liknes ET, Cooper SJ (2012) Intraspecific correlations of basal and maximal metabolic rates in birds and the aerobic capacity model for the evolution of endothermy. PLOS One 7:e34271
Sweazea KL, Braun EJ (2005) Glucose transport by English sparrow (Passer domesticus) skeletal muscle: have we been chirping up the wrong tree? J Exp Zool 303A:143–153
Szabó A, Fébel H, Horn P, Bázár G, Romvári R (2006) Ontogenic development of the fatty acyl chain composition of the turkey (Meleagris gallopavo) pectoralis superficialis muscle membranes (an allometric approach). Acta Biol Hung 57:165–180
Szdzuy K, Mortola JP (2007) Monitoring breathing in avian embryos and hatchlings by the barometric technique. Respir Physiol Neurobiol 159:241–244
Szdzuy K, Fong LM, Mortola JP (2008) Oxygenation and establishment of thermogenesis in the avian embryo. Life Sci 82:50–58
Tazawa H (2005) Cardiac rhythms in avian embryos and hatchlings. Avian Poult Biol Rev 16:123–150
Tazawa H, Okuda A, Nakazawa S, Whittow G (1989) Metabolic responses of chicken embryos to graded, prolonged alterations in ambient temperature. Comp Biochem Physiol A 92:613–617
Teulier L, Rouanet J-L, Rey B, Roussel D (2014) Ontogeny of non-shivering thermogenesis in Muscovy ducklings (Cairina moschata). Comp Biochem Physiol: Mol Integr Physiol 175:82–89
Thil M-A, Speake BK, Groscolas R (2003) Changes in tissue fatty acid composition during the first month of growth of the king penguin chick. J Comp Physiol B 173:190–206
Trayer IP, Perry SV (1966) The myosin of developing skeletal muscle. Biochemische Zeitschrift 345:87–100
Tzschentke B, Basta D (2000) Development of hypothalamic neuronal thermosensitivity in birds during the perinatal period. J Therm Biol 25:119–123
Tzschentke B, Basta D (2002) Early development of neuronal hypothalamic thermosensitivity in birds: influence of epigenetic temperature adaptation. Comp Biochem Physiol A 131:825–832
Vézina F, Love OP, Lessard M, Williams TD (2009) Shifts in metabolic demands in growing altricial nestlings illustrate context-specific relationships between basal metabolic rate and body composition. Physiol Biochem Zool 82:248–257
Visser GH (1998) Development of temperature regulation. In: Starck JM, Ricklefs RE (eds) Avian Growth and Development. Oxford University Press, New York, pp 117–156
Visser GH, Ricklefs RE (1995) Relationship between body composition and homeothermy in neonates of precocial and semiprecocial birds. Auk 112:192–200
Walter I, Seebacher F (2009) Endothermy in birds: underlying molecular mechanisms. J Exp Biol 212:2328–2336
Welch KC Jr, Allalou A, Sehgal P, Cheng J, Ashok A (2013) Glucose transporter expression in an avian nectarivore: the ruby-throated hummingbird (Archilochus colubris). PLOS One 8:e77003
Whittow GC, Tazawa H (1991) The early development of thermoregulation in birds. Physiol Zool 64:1371–1390
Wone BWM, Donovan ER, Cushman JC, Hayes JP (2013) Metabolic rates associated with membrane fatty acids in mice selected for increased maximal metabolic rate. Comp Biochem Physiol A 165:70–78
Wu BJ, Hulbert AJ, Storlien LH, Else PL (2004) Membrane lipids and sodium pumps of cattle and crocodiles: an experimental test of the membrane pacemaker theory of metabolism. Am J Physiol Regul Integr Comp Physiol 287:R633-R641
Yarbrough CG (1970) The development of endothermy in nestlin gray-crowned rosy finches, Leucosticte tephrocotis griseonucha. Comp Biochem Physiol 34:917–925
Yoneta H, Dzialowski EM, Burggren WW, Tazawa H (2007) Endothermic heart rate response in broiler an White Leghorn chicks (Gallus gallus domesticus) during the first two days of post-hatch life. Comp Biochem Physiol: Mol Integr Physiol 147:529–535
Zajac DM, Cerasale DJ, Landman S, Guglielmo CG (2011) Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. Gen Comp Endocrinol 174:269–275
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We thank Sarah Sirsat, Tushar Sirsat, Paul Sotherland, and Chris Mallery for discussion of the topic.
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This review was funded in part by National Science Foundation (IOS1146758).
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Communicated by I. D. Hume.
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Price, E.R., Dzialowski, E.M. Development of endothermy in birds: patterns and mechanisms. J Comp Physiol B 188, 373–391 (2018). https://doi.org/10.1007/s00360-017-1135-0
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DOI: https://doi.org/10.1007/s00360-017-1135-0