Journal of Comparative Physiology B

, Volume 184, Issue 8, pp 945–959 | Cite as

Sugar flux through the flight muscles of hovering vertebrate nectarivores: a review

  • Kenneth C. WelchJr.Email author
  • Chris C. W. Chen


In most vertebrates, uptake and oxidation of circulating sugars by locomotor muscles rises with increasing exercise intensity. However, uptake rate by muscle plateaus at moderate aerobic exercise intensities and intracellular fuels dominate at oxygen consumption rates of 50 % of maximum or more. Further, uptake and oxidation of circulating fructose by muscle is negligible. In contrast, hummingbirds and nectar bats are capable of fueling expensive hovering flight exclusively, or nearly completely, with dietary sugar. In addition, hummingbirds and nectar bats appear capable of fueling hovering flight completely with fructose. Three crucial steps are believed to be rate limiting to muscle uptake of circulating glucose or fructose in vertebrates: (1) delivery to muscle; (2) transport into muscle through glucose transporter proteins (GLUTs); and (3) phosphorylation of glucose by hexokinase (HK) within the muscle. In this review, we summarize what is known about the functional upregulation of exogenous sugar flux at each of these steps in hummingbirds and nectar bats. High cardiac output, capillary density, and blood sugar levels in hummingbirds and bats enhance sugar delivery to muscles (step 1). Hummingbird and nectar bat flight muscle fibers have relatively small cross-sectional areas and thus relatively high surface areas across which transport can occur (step 2). Maximum HK activities in each species are enough for carbohydrate flux through glycolysis to satisfy 100 % of hovering oxidative demand (step 3). However, qualitative patterns of GLUT expression in the muscle (step 2) raise more questions than they answer regarding sugar transport in hummingbirds and suggest major differences in the regulation of sugar flux compared to nectar bats. Behavioral and physiological similarities among hummingbirds, nectar bats, and other vertebrates suggest enhanced capacities for exogenous fuel use during exercise may be more wide spread than previously appreciated. Further, how the capacity for uptake and phosphorylation of circulating fructose is enhanced remains a tantalizing unknown.


Glucose Fructose Hummingbird Bat Fuel use Sugar homeostasis 



Much of the work summarized in this review was supported by grants from the National Sciences Foundation, UC MEXUS-CONACYT, and the Natural Sciences and Engineering Research Council of Canada. The authors thank D. Groom, A. Myrka, R. K. Suarez, and B. Velten for comments on a draft of this work.


  1. Adamson RH, Michel CC (1993) Pathways through the intracellular clefts of frog mesenteric capillaries. J Physiol Lond 466:303–327PubMedCentralPubMedGoogle Scholar
  2. Adopo E, Peronnet F, Massicotte D et al (1994) Respective oxidation of exogenous glucose and fructose given in the same drink during exercise. J Appl Physiol 76:1014–1019PubMedGoogle Scholar
  3. Amitai O, Holtze S, Barkan S et al (2010) Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars. J Exp Biol 213:2693–2699. doi: 10.1242/jeb.043505 PubMedCrossRefGoogle Scholar
  4. Bertoldo A, Pencek RR, Azuma K et al (2006) Interactions between delivery, transport, and phosphorylation of glucose in governing uptake into human skeletal muscle. Diabetes 55:3028–3037. doi: 10.2337/db06-0762 PubMedCrossRefGoogle Scholar
  5. Beuchat CA, Chong CR (1998) Hyperglycemia in hummingbirds and its consequences for hemoglobin glycation. Comp Biochem Physiol A Mol Integr Physiol 120:409–416PubMedCrossRefGoogle Scholar
  6. Bishop CM (1997) Heart mass and the maximum cardiac output of birds and mammals: implications for estimating the maximum aerobic power input of flying animals. Phil Trans R Soc Lond B 352:447–456. doi: 10.1098/rstb.1997.0032 CrossRefGoogle Scholar
  7. Bishop CM (2005) Circulatory variables and the flight performance of birds. J Exp Biol 208:1695–1708. doi: 10.1242/jeb.01576 PubMedCrossRefGoogle Scholar
  8. Blomstrand E, Challiss RA, Cooney GJ, Newsholme EA (1983) Maximal activities of hexokinase, 6-phosphofructokinase, oxoglutarate dehydrogenase, and carnitine palmitoyltransferase in rat and avian muscles. Biosci Rep 3:1149–1153PubMedCrossRefGoogle Scholar
  9. Bonadonna RC, Saccomani MP, Seely L et al (1993) Glucose transport in human skeletal muscle. The in vivo response to insulin. Diabetes 42:191–198. doi: 10.2337/diabetes.42.1.191 PubMedCrossRefGoogle Scholar
  10. Brand MD (2005) The efficiency and plasticity of mitochondrial energy transduction. Biochem Soc T 33:897–903CrossRefGoogle Scholar
  11. Braun EJ, Sweazea KL (2008) Glucose regulation in birds. Comp Biochem Physiol B Biochem Mol Biol 151:1–9PubMedCrossRefGoogle Scholar
  12. Brooks GA, Mercier J (1994) Balance of carbohydrate and lipid utilization during exercise: the “crossover” concept. J Appl Physiol 76:2253–2261PubMedGoogle Scholar
  13. Burelle Y, Lamoureux M-C, Pèronnet F et al (2006) Comparison of exogenous glucose, fructose and galactose oxidation during exercise using 13C-labelling. Br J Nutr 96:56–61. doi: 10.1079/BJN20061799 PubMedCrossRefGoogle Scholar
  14. Caviedes-Vidal E, McWhorter TJ, Lavin SR et al (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci USA 104:19132–19137PubMedCentralPubMedCrossRefGoogle Scholar
  15. Chai P, Dudley R (1996) Limits to flight energetics of hummingbirds hovering in hypodense and hypoxic gas mixtures. J Exp Biol 199:2285–2295PubMedGoogle Scholar
  16. Chen CCW, Welch KC Jr (2014) Ruby-throated hummingbirds can fuel hovering flight with either glucose or fructose. Func Ecol 28:589–600Google Scholar
  17. Diamond DL, Carruthers A (1993) Metabolic control of sugar transport by derepression of cell surface glucose transporters. An insulin-independent recruitment-independent mechanism of regulation. J Biol Chem 268:6437–6444PubMedGoogle Scholar
  18. Diamond JM, Karasov WH, Phan D, Carpenter FL (1986) Digestive physiology is a determinant of foraging bout frequency in hummingbirds. Nature 320:62–63PubMedCrossRefGoogle Scholar
  19. Duchman SM, Ryan AJ, Schedl HP et al (1997) Upper limit for intestinal absorption of a dilute glucose solution in men at rest. Med Sci Sports Exerc 29:482–488. doi: 10.1097/00005768-199704000-00009 PubMedCrossRefGoogle Scholar
  20. Fernandez MJ, Dudley R, Bozinovic F (2011) Comparative energetics of the giant hummingbird (Patagona gigas). Physiol Biochem Zool 84:333–340PubMedCrossRefGoogle Scholar
  21. Fueger PT, Bracy DP, Malabanan CM et al (2004a) Distributed control of glucose uptake by working muscles of conscious mice: roles of transport and phosphorylation. Am J Physiol Endocrinol Metab 286:E77–E84. doi: 10.1152/ajpendo.00309.2003 PubMedCrossRefGoogle Scholar
  22. Fueger PT, Hess HS, Bracy DP et al (2004b) Regulation of insulin-stimulated muscle glucose uptake in the conscious mouse: role of glucose transport is dependent on glucose phosphorylation capacity. Endocrinology 145:4912–4916. doi: 10.1210/en.2004-0465 PubMedCrossRefGoogle Scholar
  23. Fueger PT, Li CY, Ayala JE et al (2007) Glucose kinetics and exercise tolerance in mice lacking the GLUT4 glucose transporter. J Physiol 582:801–812. doi: 10.1113/jphysiol.2007.132902 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Furler SM, Jenkins AB, Storlien LH, Kraegen EW (1991) In vivo location of the rate-limiting step of hexose uptake in muscle and brain tissue of rats. Am J Physiol Endocrinol Metab 261:E337–E347Google Scholar
  25. Hawley JA, Bosch AN, Weltan SM et al (1994) Glucose kinetics during prolonged exercise in euglycaemic and hyperglycaemic subjects. Pflugers Arch 426:378–386. doi: 10.1007/BF00388300 PubMedCrossRefGoogle Scholar
  26. Hermanson JW, Ryan JM, Cobb MA et al (1998) Histochemical and electrophoretic analysis of the primary flight muscle of several phyllostomid bats. Can J Zool 76:1983–1992. doi: 10.1139/z98-158 CrossRefGoogle Scholar
  27. Hernandez A, Martinez del Rio C (1992) Intestinal disaccharides in five species of phyllostomoid bats. Comp Biochem Physiol Biochem Mol Biol 103:105–111. doi: 10.1016/0305-0491(92)90420-V CrossRefGoogle Scholar
  28. Hoppeler H, Weibel ER (1998) Limits for oxygen and substrate transport in mammals. J Exp Biol 201:1051–1064PubMedGoogle Scholar
  29. Jackson S, Nicolson SW, van Wyk B (1998) Apparent absorption efficiencies of nectar sugars in the cape sugarbird, with a comparison of methods. Physiol Zool 71:106–115. doi: 10.1086/pbz.1998.71.issue-1 PubMedCrossRefGoogle Scholar
  30. Jandrain BJ, Pallikarakis N, Normand S et al (1993) Fructose utilization during exercise in men: rapid conversion of ingested fructose to circulating glucose. J Appl Physiol 74:2146–2154PubMedCrossRefGoogle Scholar
  31. Jentjens RLPG, Venables MC, Jeukendrup AE (2004) Oxidation of exogenous glucose, sucrose, and maltose during prolonged cycling exercise. J Appl Physiol 96:1285–1291. doi: 10.1152/japplphysiol.01023.2003 PubMedCrossRefGoogle Scholar
  32. Jeukendrup AE, Jentjens R (2000) Oxidation of carbohydrate feedings during prolonged exercise—current thoughts, guidelines and directions for future research. Sports Med 29:407–424PubMedCrossRefGoogle Scholar
  33. Jeukendrup AE, Wagenmakers AJM, Stegen JHCH, et al. (1999) Carbohydrate ingestion can completely suppress endogenous glucose production during exercise. In: Am J Physiol Endocrinol Metab.
  34. Johansen K (1987) The world as a laboratory: physiological insights from Nature’s experiments. In: McLennan H, Ledsome JR, McIntosh CHS (eds) Advances in Physiological Research. Plenum Press, New York, pp 377–396CrossRefGoogle Scholar
  35. Karasov WH, Phan D, Diamond JM, Carpenter FL (1986) Food passage and intestinal nutrient absorption in hummingbirds. Auk 103:453–464Google Scholar
  36. Kelm DH, Simon R, Kuhlow D et al (2011) High activity enables life on a high-sugar diet: blood glucose regulation in nectar-feeding bats. Proc R Soc B 278:3490–3496. doi: 10.1098/rspb.2011.0465 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Kristiansen S, Darakshan F, Richter EA, Hundal HS (1997) Fructose transport and GLUT-5 protein in human sarcolemmal vesicles. Am J Physiol Endocrinol Metab 36:E543–E548Google Scholar
  38. Lasiewski RC (1963) Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol Zool 36:122–140. doi: 10.1086/635265 Google Scholar
  39. Lê K-A, Tappy L (2006) Metabolic effects of fructose. Curr Opin Clin Nutr Metab Care 9:469–475. doi: 10.1097/01.mco.0000232910.61612.4d PubMedCrossRefGoogle Scholar
  40. Maina JN (2000) What it takes to fly: the structural and functional respiratory refinements in birds and bats. J Exp Biol 203:3045–3064PubMedGoogle Scholar
  41. Martínez del Rio C (1990) Dietary, phylogenetic, and ecological correlates of intestinal sucrase and maltase activity in birds. Physiol Zool 63:987–1011Google Scholar
  42. Mathieu-Costello O, Suarez RK, Hochachka PW (1992a) Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respir Physiol 89:113–132. doi: 10.1016/0034-5687(92)90075-8 PubMedCrossRefGoogle Scholar
  43. Mathieu-Costello O, Szewczak JM, Logemann RB, Agey PJ (1992b) Geometry of blood-tissue exchange in bat flight muscle compared with bat hindlimb and rat soleus muscle. Am J Physiol Regul Integr Comp Physiol 262:R955–R965Google Scholar
  44. Mayes PA (1993) Intermediary metabolism of fructose. Am J Clin Nutr 58:754S–765SPubMedGoogle Scholar
  45. McWhorter TJ, Bakken BH, Karasov WH, Martinez del Rio C (2006) Hummingbirds rely on both paracellular and carrier-mediated intestinal glucose absorption to fuel high metabolism. Biol Lett 2:131–134PubMedCentralPubMedCrossRefGoogle Scholar
  46. Mqokeli BR, Downs CT (2012) Blood plasma glucose regulation in Wahlberg’s Epauletted fruit bat. Afr Zool 47:348–352CrossRefGoogle Scholar
  47. Mueckler M (1994) Facilitative glucose transporters. Eur J Biochem 219:713–725PubMedCrossRefGoogle Scholar
  48. Napier KR, McWhorter TJ, Nicolson Fleming PA (2013) Sugar preferences of avian nectarivores are correlated with intestinal sucrase activity. Physiol Biochem Zool 86:499–514. doi: 10.1086/672013 PubMedCrossRefGoogle Scholar
  49. Nesher R, Karl IE, Kipnis DM (1985) Dissociation of effects of insulin and contraction on glucose transport in rat epitrochlearis muscle. Am J Physiol Cell Physiol 249:C226–C232Google Scholar
  50. Nicolson SW, Fleming PA (2014) Drinking problems on a “simple” diet: physiological convergence in nectar-feeding birds. J Exp Biol 217:1015–1023. doi: 10.1242/jeb.054387 PubMedCrossRefGoogle Scholar
  51. Ploug T, Galbo H, Vinten J et al (1987) Kinetics of glucose transport in rat muscle: effects of insulin and contractions. Am J Physiol Endocrinol Metab 253:E12–E20Google Scholar
  52. Polakof S, Mommsen TP, Soengas JL (2011) Glucosensing and glucose homeostasis: from fish to mammals. Comp Biochem Physiol B Biochem Mol Biol 160:123–149. doi: 10.1016/j.cbpb.2011.07.006 PubMedCrossRefGoogle Scholar
  53. Post RL, Morgan HE, Park CR (1961) Regulation of glucose uptake in muscle. J Biol Chem 236:269–272PubMedGoogle Scholar
  54. Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93:993–1017. doi: 10.1152/physrev.00038.2012 PubMedCrossRefGoogle Scholar
  55. Roberts TJ, Weber JM, Hoppeler H et al (1996) Design of the oxygen and substrate pathways. II. Defining the upper limits of carbohydrate and fat oxidation. J Exp Biol 199:1651–1658PubMedGoogle Scholar
  56. Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758PubMedGoogle Scholar
  57. Rose AJ, Richter EA (2005) Skeletal muscle glucose uptake during exercise: how is it regulated? Physiology 20:260–270. doi: 10.1152/physiol.00012.2005 PubMedCrossRefGoogle Scholar
  58. Schondube JE, Martinez del Rio C (2004) Sugar and protein digestion in flowerpiercers and hummingbirds: a comparative test of adaptive convergence. J Comp Physiol B 174:263–273. doi: 10.1007/s00360-003-0411-3 PubMedCrossRefGoogle Scholar
  59. Shen B, Han X, Zhang J et al (2012) Adaptive evolution in the glucose transporter 4 Gene Slc2a4 in old world fruit bats (Family: Pteropodidae). PLoS ONE 7:e33197. doi: 10.1371/journal.pone.0033197 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Suarez RK (1992) Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48:565–570. doi: 10.1007/BF01920240 PubMedCrossRefGoogle Scholar
  61. Suarez R (1998) Oxygen and the upper limits to animal design and performance. J Exp Biol 201:1065–1072PubMedGoogle Scholar
  62. Suarez RK, Welch Jr. KC (2009) Stoking the brightest fires of life among vertebrates. Cardio-respiratory control in vertebrates. pp 381–394Google Scholar
  63. Suarez RK, Lighton JRB, Moyes CD et al (1990) Fuel selection in rufous hummingbirds: ecological implications of metabolic biochemistry. Proc Natl Acad Sci USA 87:9207–9210PubMedCentralPubMedCrossRefGoogle Scholar
  64. Suarez RK, Welch KC Jr, Hanna SK, Herrera MLG (2009) Flight muscle enzymes and metabolic flux rates during hovering flight of the nectar bat, Glossophaga soricina: further evidence of convergence with hummingbirds. Comp Biochem Physiol A Mol Integr Physiol 153:136–140. doi: 10.1016/j.cbpa.2009.01.015 PubMedCrossRefGoogle Scholar
  65. Suarez RK, Herrera MLG, Welch KC Jr (2011) The sugar oxidation cascade: aerial refueling in hummingbirds and nectar bats. J Exp Biol 214:172–178. doi: 10.1242/jeb.047936 PubMedCrossRefGoogle Scholar
  66. Sweazea KL, Braun EJ (2006) Glucose transporter expression in English sparrows (Passer domesticus). Comp Biochem Physiol B Biochem Mol Biol 144:263–270. doi: 10.1016/j.cbpb.2005.12.027 PubMedCrossRefGoogle Scholar
  67. Tappy L, Randin JP, Felber JP et al (1986) Comparison of thermogenic effect of fructose and glucose in normal humans. Am J Physiol Endocrinol Metab 250:E718–E724Google Scholar
  68. Taylor CR (1987) Structural and functional limits to oxidative metabolism: insights from scaling. Annu Rev Physiol 49:135–146. doi: 10.1146/ PubMedCrossRefGoogle Scholar
  69. Thomas-Delloye V, Marmonier F, Duchamp C et al (1999) Biochemical and functional evidences for a GLUT-4 homologous protein in avian skeletal muscle. Am J Physiol Regul Integr Comp Physiol 277:1733–1740Google Scholar
  70. Topping DL, Mayes PA (1971) The concentrations of fructose, glucose and lactate in the splanchnic blood vessels of rats absorbing fructose. Ann Nutr Metab 13:331–338. doi: 10.1159/000175352 CrossRefGoogle Scholar
  71. Uldry M, Thorens B (2004) The SLC2 family of facilitated hexose and polyol transporters. Pflugers Arch Eur J Phy 447:480–489CrossRefGoogle Scholar
  72. Vock R, Weibel ER, Hoppeler H et al (1996) Design of the oxygen and substrate pathways. V. Structural basis of vascular substrate supply to muscle cells. J Exp Biol 199:1675–1688PubMedGoogle Scholar
  73. Voigt CC, Speakman JR (2007) Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Func Ecol 21:913–921CrossRefGoogle Scholar
  74. Voigt CC, Winter Y (1999) Energetic cost of hovering flight in nectar-feeding bats (Phyllostomidae: Glossophaginae) and its scaling in moths, birds and bats. J Comp Physiol B 169:38–48Google Scholar
  75. Wasserman DH, Kang L, Ayala JE et al (2011) The physiological regulation of glucose flux into muscle in vivo. J Exp Biol 214:254–262. doi: 10.1242/jeb.048041 PubMedCentralPubMedCrossRefGoogle Scholar
  76. Weber J-M (2011) Metabolic fuels: regulating fluxes to select mix. J Exp Biol 214:286–294. doi: 10.1242/jeb.047050 PubMedCrossRefGoogle Scholar
  77. Weber J-M, Haman F (2004) Oxidative fuel selection: adjusting mix and flux to stay alive. Int Congr Ser 1275:22–31. doi: 10.1016/j.ics.2004.09.043 CrossRefGoogle Scholar
  78. Weber JM, Brichon G, Zwingelstein G et al (1996a) Design of the oxygen and substrate pathways. IV. Partitioning energy provision from fatty acids. J Exp Biol 199:1667–1674PubMedGoogle Scholar
  79. Weber JM, Roberts TJ, Vock R et al (1996b) Design of the oxygen and substrate pathways. III. Partitioning energy provision from carbohydrates. J Exp Biol 199:1659–1666PubMedGoogle Scholar
  80. Weibel ER (1984) The Pathway for Oxygen. Harvard University Press, CambridgeGoogle Scholar
  81. Weibel ER, Taylor CR, Gehr P et al (1981) Design of the mammalian respiratory system. IX. Functional and structural limits for oxygen flow. Respir Physiol 44:151–164PubMedCrossRefGoogle Scholar
  82. Weibel ER, Taylor CR, Weber JM et al (1996) Design of the oxygen and substrate pathways. VII. Different structural limits for oxygen and substrate supply to muscle mitochondria. J Exp Biol 199:1699–1709PubMedGoogle Scholar
  83. Welch KC Jr, Altshuler DL (2009) Fiber type homogeneity of the flight musculature in small birds. Comp Biochem Physiol B 152:324–331. doi: 10.1016/j.cbpb.2008.12.013 PubMedCrossRefGoogle Scholar
  84. Welch KC Jr, Suarez RK (2007) Oxidation rate and turnover of ingested sugar in hovering Anna’s (Calypte anna) and rufous (Selasphorus rufus) hummingbirds. J Exp Biol 210:2154–2162PubMedCrossRefGoogle Scholar
  85. Welch KC Jr, Bakken BH, Martínez del Rio C, Suarez RK (2006) Hummingbirds fuel hovering flight with newly ingested sugar. Physiol Biochem Zool 79:1082–1087PubMedCrossRefGoogle Scholar
  86. Welch KC Jr, Altshuler DL, Suarez RK (2007) Oxygen consumption rates in hovering hummingbirds reflect substrate-dependent differences in P/O ratios: carbohydrate as a `premium fuel’. J Exp Biol 210:2146–2153PubMedCrossRefGoogle Scholar
  87. Welch KC Jr, Herrera MLG, Suarez RK (2008) Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. J Exp Biol 211:310–316PubMedCrossRefGoogle Scholar
  88. Welch KC Jr, Allalou A, Sehgal P et al (2013) Glucose transporter expression in an avian nectarivore: the ruby-throated hummingbird (Archilochus colubris). PLoS ONE 8:e77003PubMedCentralPubMedCrossRefGoogle Scholar
  89. Wilson R, Turner APF (1992) Glucose oxidase: an ideal enzyme. Biosens Bioelectron 7:165–185. doi: 10.1016/0956-5663(92)87013-F CrossRefGoogle Scholar
  90. Witteveen M, Brown M, Downs CT (2014) Does sugar content matter? Blood plasma glucose levels in an occasional and a specialist avian nectarivore. Comp Biochem Physiol A Mol Integr Physiol 167:40–44. doi: 10.1016/j.cbpa.2013.09.017 PubMedCrossRefGoogle Scholar
  91. Zierath JR, Nolte LA, Wahlstrom E et al (1995) Carrier-mediated fructose uptake significantly contributes to carbohydrate metabolism in human skeletal muscle. Biochem J 311:517–521PubMedCentralPubMedGoogle Scholar
  92. Zinker BA, Lacy DB, Bracy D et al (1993) Regulation of glucose uptake and metabolism by working muscle: an in vivo analysis. Diabetes 42:956–965. doi: 10.2337/diab.42.7.956 PubMedCrossRefGoogle Scholar
  93. Zurlo F, Larson K, Bogardus C, Ravussin E (1990) Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 86:1423–1427PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Toronto ScarboroughTorontoCanada
  2. 2.Department of Cell and Systems BiologyUniversity of TorontoTorontoCanada
  3. 3.School of Kinesiology and Health ScienceYork UniversityTorontoCanada

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