Carbon stable-isotope tracking in breath for comparative studies of fuel use

Annals of the New York Academy of Sciences

Volumn 1365, Issue 1, 2016, Pages 15-32

  Welch, Kenneth C ^a   Péronnet, François ^b   Hatch, Kent A ^c   Voigt, Christian C ^d   McCue, Marshall D ^e  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c LONG ISLAND UNIVERSITY   (United States)

^d LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^e ST MARY'S UNIVERSITY   (United States)

Author keywords

CO2; Fuel use; Metabolism; Respirometry; Stable isotopes

Indexed keywords

CARBON 13; CARBON DIOXIDE; FRUCTOSE; FUEL; GALACTOSE; GLUCOSE; GLYCOGEN; MALTOSE; PALATINOSE; SUCROSE; TREHALOSE; CARBON;

AEROBIC METABOLISM; ARCHILOCHUS COLUBRIS; ARTICLE; BEHAVIOR; BREATHING; CALYPTE ANNA; CAROLLIA PERSPICILLATA; DIET RESTRICTION; ECOLOGY; ENERGY TRANSFER; ENERGY YIELD; ESTERIFICATION; FLIGHT; FLYING FOX; FOOD AVAILABILITY; GAS CHROMATOGRAPHY; HUMAN; INFRARED SPECTROSCOPY; ISOTOPE RATIO MASS SPECTROMETRY; KINETICS; LIPID METABOLISM; MASS SPECTROMETRY; METABOLISM; MIGRANT BIRD; NECTARIVORE; NONDISPERSIVE INFRARED SPECTROSCOPY; NONHUMAN; OXIDATION; PHYLOGENY; PROTEIN METABOLISM; RESPIROMETRY; SELASPHORUS RUFUS; STARVATION; TURNOVER TIME; ANIMAL; CALORIC INTAKE; ENERGY METABOLISM; EXERCISE; EXHALATION; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

ANIMALS; CARBON ISOTOPES; ENERGY INTAKE; ENERGY METABOLISM; EXERCISE; EXHALATION; HUMANS; OXIDATION-REDUCTION;

EID: 84962891446     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12737     Document Type: Article

References (146)

1. 2 exhaled by living beings. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D. 266: 522-523.
2. 2 exhaled by higher animals. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D. 267: 225-226.
3. 2 in man and higher animals. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D. 273: 240-241.
4. Bender, M.M. 1968. Mass spectrometric studies of carbon 13 variations in corn and other grasses. Radiocarbon 10: 5.
5. 12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10: 1239-1244.
6. 12C ratio as a function of respiration and nature of tissues, in higher animals]. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D. 273: 1423-1425.
7. 2 exhaled by man]. C. R. Acad. Sci. Hebd. Seances. Acad. Sci. D. 277: 2261-2264.
8. Lacroix, M., F. Mosora, M. Pontus, et al. 1973. Glucose naturally labeled with carbon-13: use for metabolic studies in man. Science 181: 445-446.
9. 13C-glucose metabolic studies in human diabetes and obesity. Diabetes 24: 185-189.
10. 2 breath tests. Am. J. Clin. Nutr. 33: 2375-2385.
11. 13C-glucose. Metabolism 25: 1575-1582.
12. 13C]glucose. J. Appl. Physiol. 43: 258-261.
13. Pirnay, F., M. Lacroix, F. Mosora, et al. 1977. Effect of glucose ingestion on energy substrate utilization during prolonged muscular exercise. Europ. J. Appl. Physiol. 36: 247-254.
14. Benadé, A.J.S., C.R. Jansen, G.G. Rogers, et al. 1973. The significance of an increased RQ after sucrose ingestion during prolonged aerobic exercise. Pflugers Arch. 342: 199-206.
15. Costill, D.L., A. Bennett, G. Branam, et al. 1973. Glucose ingestion at rest and during prolonged exercise. J. Appl. Physiol. 34: 764-769.
16. McClelland, G.B. 2004. Fat to the fire: the regulation of lipid oxidation with exercise and environmental stress. Comp. Biochem. Physiol. B 139: 443-460.
17. Jeukendrup, A.E. 2008. Carbohydrate feeding during exercise. Eur. J. Sports Sci. 8: 77-86.
18. Weber, J.-M. 2011. Metabolic fuels: regulating fluxes to select mix. J. Exp. Biol. 214: 286-294.
19. Ambrose, S.H. & M.J. DeNiro . 1986. The isotopic ecology of East African mammals. Oecologia 69: 395-406.
20. Peterson, B.J. & B. Fry . 1987. Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18: 293-320.
21. Kelly, J.F. 2000. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can. J. Zool. 78: 1-27.
22. 2: its advantage and potential application to field research to infer diet, changes in diet over time, and substrate metabolism in birds. Integ. Comp. Biol. 42: 21-33.
23. 2 can be used to determine not just present, but also past diets in birds. J. Comp. Physiol. B 172: 263-268.
24. 2 in small vertebrates. Oecologia 141: 1-6.
25. Starck, J.M., P. Moser, R.A. Werner, et al. 2004. Pythons metabolize prey to fuel the response to feeding. Proc. R. Soc. B 271: 903-908.
26. Podlesak, D.W., S.R. McWilliams & K.A. Hatch . 2005. Stable isotopes in breath, blood, feces and feathers can indicate intra-individual changes in the diet of migratory songbirds. Oecologia 142: 501-510.
27. Carleton, S.A., B.H. Bakken & C.M. del Rio . 2006. Metabolic substrate use and the turnover of endogenous energy reserves in broad-tailed hummingbirds (Selasphorus platycercus). J. Exp. Biol. 209: 2622-2627.
28. Sponheimer, M., T.F. Robinson, T.E. Cerling, et al. 2006. Turnover of stable carbon isotopes in the muscle, liver, and breath CO2 of alpacas (Lama pacos). Rapid Commun. Mass Spectrom. 20: 1395-1399.
29. Voigt, C.C., L. Baier, J.R. Speakman, et al. 2008. Stable carbon isotopes in exhaled breath as tracers for dietary information in birds and mammals. J. Exp. Biol. 211: 2233-2238.
30. Voigt, C.C., P. Grasse, K. Rex, et al. 2008. Bat breath reveals metabolic substrate use in free-ranging vampires. J. Comp. Physiol. B 178: 9-16.
31. Voigt, C.C., Sörgel, K. & D.K.N. Dechmann . 2010. Refueling while flying: foraging bats combust food rapidly and directly to power flight. Ecology 91: 2908-2917.
32. Welch, K.C., Jr. 2011. The power of feeder-mask respirometry as a method for examining hummingbird energetics. Comp. Biochem. Physiol. A: Mol. Integ. Physiol. 158: 276-286.
33. Welch, K.C., Jr., B.H. Bakken, C. Martínez del Rio, et al. 2006. Hummingbirds fuel hovering flight with newly ingested sugar. Physiol. Biochem. Zool. 79: 1082-1087.
34. Voigt, C.C. & J.R. Speakman . 2007. Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Func. Ecol. 21: 913-921.
35. Welch, K.C., Jr. & R.K. Suarez . 2007. Oxidation rate and turnover of ingested sugar in hovering Anna's (Calypte anna) and rufous (Selasphorus rufus) hummingbirds. J. Exp. Biol. 210: 2154-2162.
36. Welch, K.C., Jr., M.L.G. Herrera & R.K. Suarez . 2008. Dietary sugar as a direct fuel for flight in the nectarivorous bat Glossophaga soricina. J. Exp. Biol. 211: 310-316.
37. Amitai, O., S. Holtze, S. Barkan, et al. 2010. Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars. J. Exp. Biol. 213: 2693-2699.
38. Chen, C.C.W. & K.C. Welch . 2014. Hummingbirds can fuel expensive hovering flight completely with either exogenous glucose or fructose. Funct. Ecol. 28: 589-600.
39. Craig, H. 1957. Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim. Cosmochim. Acta 12: 133-149.
40. Slater, C., T. Preston & L.T. Weaver . 2001. Stable isotopes and the international system of units. Rapid Commun. Mass Spectrom. 15: 1270-1273.
41. 13C-breath tests: current state of the art and future directions. Digest. Liver Dis. 39: 795-805.
42. 13C-breath tests. Food Nutr. Bull. 23: 53-56.
43. Parra, M.D. & J.A. Martinez . 2006. Nutritional aspects of breath testing based on stable isotopes. Nutr. Rev. 64: 338-347.
44. Voigt, C.C., K. Rex, R.H. Michener, et al. 2008. Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157: 31-40.
45. Voigt, C.C. 2009. Studying animal diets in situ using portable stable isotope analyzers. Biotropica 41: 271-274.
46. 13C enrichment of lipid and protein pools in the body reveals circadian changes in oxidative fuel mixture during prolonged fasting: a case study using Japanese quail. Comp. Biochem. Physiol. A: Mol. Integ. Physiol. 166: 546-554.
47. 2-breath testing reveals shifts in fuel mix during starvation. J. Comp. Physiol. B 183: 1039-1052.
48. Istfan, N.W., P.R. Ling, B.R. Bistrian, et al. 1988. Systemic exchangeability of enteral leucine: relationship to plasma flux. Am. J. Physiol. 254: R688-R698.
49. Matthews, D.E., M.A. Marano & R.G. Campbell . 1993. Splanchnic bed utilization of leucine and phenylalanine in humans. Am. J. Physiol. Endocrinol. Metabol. 264: E109-E118.
50. Stoll, B., D.G. Burrin, J. Henry, et al. 1997. Phenylalanine utilization by the gut and liver measured with intravenous and intragastric tracers in pigs. Am. J. Physiol. Gastrointest. Liver Physiol. 273: G1208-G1217.
51. 15N]leucine kinetics in relation to enteral and parenteral amino acid supply. Am. J. Physiol. Endocrinol. Metabol. 262: E687-E694.
52. 13C in tissues. Condor 94: 181-188.
53. Bauchinger, U. & S.R. McWilliams . 2012. "Tissue-Specific Mass Changes During Fasting: The Protein Turnover Hypothesis." In Comparative Physiology of Fasting, Starvation, and Food Limitation. M.D. McCue, Ed.: 193-206. Berlin, Heidelberg: Springer.
54. Voigt, C.C., F. Matt, R. Michener, et al. 2003. Low turnover rates of carbon isotopes in tissues of two nectar-feeding bat species. J. Exp. Biol. 206: 1419-1427.
55. MacAvoy, S.E., S.A. Macko & L.S. Arneson . 2005. Growth versus metabolic tissue replacement in mouse tissues determined by stable carbon and nitrogen isotope analysis. Can. J. Zool. 83: 631-641.
56. Johnson, H.A., R.L. Baldwin, J. France, et al. 1999. A model of whole-body protein turnover based on leucine kinetics in rodents. J. Nutr. 129: 728-739.
57. Cherel, Y., K.A. Hobson & S. Hassani . 2005. Isotopic Discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol. Biochem. Zool. 78: 106-115.
58. 2, Bone Collagen, Bioapatite, and Soft Tissues." In Prehistoric Human Bone: Archaeology at the Molecular Level. J.B. Lambert & G. Grupe, Eds.: 121-155. Berlin, Heidelberg: Springer.
59. 13C egg proteins for metabolic tracer studies. Int. J. Biol. 5: 69-84.
60. McCue, M.D. 2011. Tracking the oxidative and non-oxidative fates of isotopically labeled nutrients in animals. Bioscience 61: 217-230.
61. Saris, W.H., B.H. Goodpaster, A.E. Jeukendrup, et al. 1993. Exogenous carbohydrate oxidation from different carbohydrate sources during exercise. J. Appl. Physiol. 75: 2168-2172.
62. 13C-labelled pasta meals following rest or exercise in man. Br. J. Nutr. 85: 671-680.
63. 13C substrates for metabolic studies in exercise: methodological considerations. J. Appl. Physiol. 69: 1047-1052.
64. 2 is directly proportional to exercise intensity in humans. Comp. Biochem. Physiol. A: Mol. Integ. Physiol. 179: 164-171.
65. Brooks, G.A. & J. Mercier . 1994. Balance of carbohydrate and lipid utilization during exercise: the 'crossover' concept. J. Appl. Physiol. 76: 2253-2261.
66. DeNiro, M.J. & S. Epstein . 1977. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197: 261-263.
67. 13C-labelling. Br. J. Nutr. 96: 56-61.
68. -1) and performance. Med. Sci. Sports Exerc. 45: 336-341.
69. Mahon, A.D. & B.W. Timmons . 2013. Application of stable isotope tracers in the study of exercise metabolism in children: a primer. Pediatr. Exerc. Sci. 26: 3-10
70. 3 infused by gut and vein: effect of feeding. Am. J. Physiol. Endocrinol. Metabol. 257: E426-E438.
71. Leslie, M.A., R.A. Coleman, S. Moehn, et al. 2006. Relationship between bicarbonate retention and bone characteristics in broiler chickens. Poultry Sci. 85: 1917-1922.
72. Moehn, S., R.F. Bertolo, P.B. Pencharz, et al. 2004. Pattern of carbon dioxide production and retention is similar in adult pigs when fed hourly, but not when fed a single meal. BMC Physiol. 4: 1-8.
73. 13C-labelled Na-bicarbonate. Comp. Biochem. Physiol. A: Mol. Integ. Physiol. 158: 323-328.
74. 2. J. Exp. Biol. 213: 782-789.
75. Brand, M.D. 1994. The stoichiometry of proton pumping, ATP synthesis and oxygen consumption in mitochondria. Biochemist 16: 20-24.
76. 13C breath testing. Physiol. Biochem. Zool. 84: 32-42.
77. McCue, M.D., C.C. Voigt, M. Jefimow, et al. 2014. Thermal acclimation and nutritional history affect the oxidation of different classes of exogenous nutrients in Siberian hamsters, Phodopus sungorus. J. Exp. Zool. 321: 503-514.
78. Farquhar, G.D., J.R. Ehleringer & K.T. Hubick . 1989. Carbon isotope discrimination and photosynthesis. Ann. Rev. Plant Physiol. Plant Mol. Bio. 40: 503-537.
79. Hayes, J.M. 2001. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. Rev. Mineral. Geochem. 43: 225-277.
80. Voigt, C.C., J. Melzheimer, S. Thalwitzer, et al. 2013. A breath test to assign carnivore diets to browsers or grazers. Wildlife Biol. 19: 311-316.
81. Jeukendrup, A.E. 2004. Carbohydrate intake during exercise and performance. Nutrition 20: 669-677.
82. Hawley, J.A., S.C. Dennis, A. Nowitz, et al. 1992. Exogenous carbohydrate oxidation from maltose and glucose ingested during prolonged exercise. Eur. J. Appl. Physiol. 64: 523-527.
83. Guezennec, C.Y., P. Satabin, F. Duforez, et al. 1989. Oxidation of corn starch, glucose, and fructose ingested before exercise. Med. Sci. Sports Exerc. 21: 45-50.
84. Massicotte, D., F. Peronnet, G. Brisson, et al. 1989. Oxidation of a glucose polymer during exercise: comparison with glucose and fructose. J. Appl. Physiol. 66: 179-183.
85. Rehrer, N.J., A.J. Wagenmakers, E.J. Beckers, et al. 1992. Gastric emptying, absorption, and carbohydrate oxidation during prolonged exercise. J. Appl. Physiol. 72: 468-475.
86. Guezennec, C.Y., P. Satabin, F. Duforez, et al. 1993. The role of type and structure of complex carbohydrates response to physical exercise. Int. J. Sports Med. 14: 224-231.
87. 13C]glucose during exercise. J. Appl. Physiol. 79: 720-725.
88. Achten, J., R.L. Jentjens, F. Brouns, et al. 2007. Exogenous oxidation of isomaltulose is lower than that of sucrose during exercise in men. J. Nutr. 137: 1143-1148.
89. Venables, M.C., F. Brouns & A.E. Jeukendrup . 2008. Oxidation of maltose and trehalose during prolonged moderate-intensity exercise. Med. Sci. Sports Exerc. 40: 1653-1659.
90. 13C-labeled lactate and glucose ingested simultaneously during exercise. J. Appl. Physiol. 82: 440-446.
91. Adopo, E., F. Peronnet, D. Massicotte, et al. 1994. Respective oxidation of exogenous glucose and fructose given in the same drink during exercise. J. Appl. Physiol. 76: 1014-1019.
92. Scow, J.S., A. Tavakkolizadeh, Y. Zheng, et al. 2011. Acute 'adaptation' by the small intestinal enterocyte: a posttranscriptional mechanism involving apical translocation of nutrient transporters. Surgery 149: 601-605.
93. Jentjens, R.L.P.G., C. Shaw, T. Birtles, et al. 2005. Oxidation of combined ingestion of glucose and sucrose during exercise. Metabolism 54: 610-618.
94. Hawley, J.A., A.N. Bosch, S.M. Weltan, et al. 1994. Glucose kinetics during prolonged exercise in euglycaemic and hyperglycaemic subjects. Pflugers Arch. 426: 378-386.
95. Weibel, E.R., C.R. Taylor & H. Hoppeler . 1991. The concept of symmorphosis: a testable hypothesis of structure-function relationship. Proc. Natl. Acad. Sci. U. S. A. 88: 10357-10361.
96. Temesi, J., N.A. Johnson, J. Raymond, et al. 2011. Carbohydrate ingestion during endurance exercise improves performance in adults. J. Nutr. 141: 890-897.
97. Saris, W.H., M.A. van Erp-Baart, F. Brouns, et al. 1989. Study on food intake and energy expenditure during extreme sustained exercise: the Tour de France. Int. J. Sports Med. 10(Suppl. 1): S26-S31.
98. Santalla, A., C.P. Earnest, J.A. Marroyo, et al. 2012. The Tour de France: an updated physiological review. Int. J. Sports Physiol. Perform. 207: 200-209.
99. Kuipers, H., H.A. Keizer, F. Brouns, et al. 1987. Carbohydrate feeding and glycogen synthesis during exercise in man. Pflugers Arch. 410: 652-656.
100. Baker, H.G. 1975. Sugar concentrations in nectars from hummingbird flowers. Biotropica 7: 37-41.
101. Baker, H.G., I. Baker & S.A. Hodges . 1998. Sugar composition of nectars and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30: 559-586.
102. Suarez, R.K. 1992. Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48: 565-570.
103. Voigt, C.C. & Y. Winter . 1999. Energetic cost of hovering flight in nectar-feeding bats (Phyllostomidae hyGlossophaginae) and its scaling in moths, birds and bats. J. Comp. Physiol. B 169: 38-48.
104. Chai, P. & R. Dudley . 1996. Limits to flight energetics of hummingbirds hovering in hypodense and hypoxic gas mixtures. J. Exp. Biol. 199: 2285-2295.
105. Jenni, L. & S. Jenni-Eiermann . 1998. Fuel supply and metabolic constraints in migrating birds. J. Avian Biol. 29: 521-528.
106. Guglielmo, C.G. 2010. Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr. Comp. Biol. 50: 336-345.
107. Lasiewski, R.C. 1962. The energetics of migrating hummingbirds. Condor 64: 324.
108. Pearson, O.P. 1950. The metabolism of hummingbirds. Condor 52: 145-152.
109. Carpenter, F.L., M.A. Hixon, C.A. Beuchat, et al. 1993. Biphasic mass gain in migrant hummingbirds: body composition changes, torpor, and ecological significance. Ecology. 74: 1173-1182.
110. A., Rojas-Martínez, A., Valiente-Banuet, M., Del Coro Arizmendi, et al. 1999. Seasonal distribution of the long-nosed bat (Leptonycteris curasoae) in North America: does a generalized migration pattern really exist? J. Biogeogr. 26: 1065-1077.
111. Fleming, T.H. & P. Eby . 2003. "Ecology of Bar Migration." In Bat Ecology. T.H. Kunz & M.B. Fenton, Eds.: 156-208. University of Chicago Press.
112. Suarez, R.K., J.R.B. Lighton, C.D. Moyes, et al. 1990. Fuel selection in rufous hummingbirds: ecological implications of metabolic biochemistry. Proc. Natl. Acad. Sci. U. S. A. 87: 9207-9210.
113. Welch, K.C., Jr. & C.C.W. Chen . 2014. Sugar flux through the flight muscles of hovering vertebrate nectarivores: a review. J. Comp. Physiol. B 184: 945-959.
114. Jeukendrup, A.E. & R. Jentjens . 2000. Oxidation of carbohydrate feedings during prolonged exercise-current thoughts, guidelines and directions for future research. Sports Med. 29: 407-424.
115. Lê, K.-A. & L. Tappy . 2006. Metabolic effects of fructose. Curr. Opin. Clin. Nutr. Metab. Care 9: 469-475.
116. Welch, K.C., Jr., A. Allalou, P. Sehgal, et al. 2013. Glucose transporter expression in an avian nectarivore: the ruby-throated hummingbird (Archilochus colubris). PLoS One 8: e77003.
117. Braun, E.J. & K.L. Sweazea . 2008. Glucose regulation in birds. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 151: 1-9.
118. Tucker, V.A. 1975. The energetic cost of moving about: walking and running are extremely inefficient forms of locomotion. Much greater efficiency is achieved by birds, fish and bicyclists. Am. Scientist 63: 413-419.
119. Battley, P.F., N. Warnock, T.L. Tibbitts, et al. 2012. Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J. Avian Biol. 43: 21-32.
120. DeNiro, M.J. & S. Epstein . 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42: 495-506.
121. Caloin, M. 2004. Modeling of lipid and protein depletion during total starvation. Am. J. Physiol. Endocrinol. Metabol. 287: E790-E798.
122. Castellini, M.A. & L.D. Rea . 1992. The biochemistry of natural fasting at its limits. Experentia 48: 575-582.
123. Bernard, S.F., E. Mioskowski & R. Groscolas . 2002. Blockade of fatty acid oxidation mimics phase II-phase III transition in a fasting bird, the king penguin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283: R144-R152.
124. Jenni-Eiermann, S. & L. Jenni . 1998. What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol. Cons. Fauna 102: 312-319.
125. Goedecke, J.H., A.S.C. Gibson, L. Grobler, et al. 2000. Determinants of the variability in respiratory exchange ratio at rest and during exercise in trained athletes. Am. J. Physiol. Endocrinol. Metabol. 279: E1325-E1334.
126. Lighton, J.R.B. & L.G. Halsey . 2011. Flow-through respirometry applied to chamber systems: pros and cons, hints and tips. Comp. Biochem. Physiol. A: Mol. Integ. Physiol. 158: 265-275.
127. Walsberg, G. & B. Wolf . 1995. Variation in the respiratory quotient of birds and implications for indirect calorimetry using measurements of carbon dioxide production. J. Exp. Biol. 198: 213-219.
128. Wang, T., C.C.Y. Hung & D.J. Randall . 2006. The comparatie physiology of food deprivation: from feast to famine. Annu. Rev. Physiol. 68: 223-251.
129. Cahill, G. F., Jr. 1976. Starvation in man. Clin. Endocrinol. Metabol. 5: 397-415.
130. McCue, M.D., H.B. Lillywhite & S.J. Beaupre, 2012. "Physiological Responses to Starvation in Snakes: Low Energy Specialists." In Comparative Physiology of Fasting, Starvation, and Food Limitation. M.D. McCue, Ed.: 103-131. Berlin, Heidelberg: Springer.
131. Navarro, I. & J. Gutiérrez . 1995. "Fasting and starvation." In Biochemistry and Molecular Biology of Fishes 4: Metabolic Biochemistry. P.W. Hochachka & T.P. Mommsen, Eds.: 393-434. Elsevier.
132. Higginson, A.D., J.M. McNamara & A.I. Houston . 2014. The starvation-predation trade-off shapes the strategic use of protein for energy during fasting. J. Theor. Biol. 359: 208-219.
133. Speakman, J.R. & K.R. Westerterp . 2013. A mathematical model of weight loss under total starvation: evidence against the thrifty-gene hypothesis. Dis. Model. Mech. 6: 236-251.
134. Khalilieh, A., M.D. McCue & B. Pinshow . 2012. Physiological responses to food deprivation in the house sparrow, a species not adapted to prolonged fasting. Am. J. Physiol. Regul. Integr. Comp. Physiol. 303: R551-R561.
135. McCue, M.D. 2007. Snakes survive starvation by employing supply- and demand-side economic strategies. Zoology 110: 318-327.
136. 2 breath testing and small molecule metabolomics. Integr. Comp. Biol. In press.
137. Voigt, C.C., I.M. Borrisov & S.L. Voigt-Heucke . 2012. Terrestrial locomotion imposes high metabolic requirements on bats. J. Exp. Biol. 215: 4340-4344.
138. Voigt, C.C. & M.W. Holderied . 2012. High manoeuvring costs force narrow-winged molossid bats to forage in open space. J. Comp. Physiol. B 182: 415-424.
139. Suarez, R.K., M., L.G. Herrera & K.C. Welch, Jr. 2011. The sugar oxidation cascade: aerial refueling in hummingbirds and nectar bats. J. Exp. Biol. 214: 172-178.
140. Price, E.R., A. Brun, Caviedes-Vidal, E., et al. 2015. Digestive adaptations of aerial lifestyles. Physiology 30: 69-78.
141. Voigt, C.C., K., Sörgel, J. Šuba, et al. 2012. The insectivorous bat Pipistrellus nathusii uses a mixed-fuel strategy to power autumn migration. Proc. R. Soc. B 279: 3772-3778.
142. Speakman, J. 1997. Doubly Labelled Water: Theory and Practice. Springer Science & Business Media.
143. 13C]glucose and endogenous energy substrate oxidation during prolonged treadmill running. J. Appl. Physiol. 92: 1255-1260.
144. McCue, M.D. & A. Cardentey . 2014. Isotope labeled metabolic tracers are not created equal: comparing the oxidative kinetics of free-versus biochemically-integrated dietary nutrients. Integr. Comp. Biol. 54: e136.
145. Jentjens, R.L.P.G., L. Moseley, R.H. Waring, et al. 2004. Oxidation of combined ingestion of glucose and fructose during exercise. J. Appl. Physiol. 96: 1277-1284.
146. 13C breath testing. Integr. Comp. Biol. In press.