Skip to main content

Stoking the Brightest Fires of Life Among Vertebrates

  • Chapter
  • First Online:

Abstract

Hummingbirds and nectarivorous bats in flight display some of the highest rates of aerobic metabolism among vertebrates. Analysis of the pathway of oxygen, i.e., the “oxygen transport cascade”, reveals the concerted upregulation of capacities for O2 flux from the external environment, through the respiratory and cardiovascular systems, into muscle mitochondria. Pathways for aerobic energy metabolism are highly conserved, but enzymatic capacities for carbohydrate and fatty acid oxidation, as well as for aerobic ATP synthesis, are also upregulated in concert. Despite evidence indicating sufficient capacities for fatty acid oxidation to support hovering, repeated bouts of hover-feeding in hummingbirds and nectar bats involve the oxidation of carbohydrate. Recent studies reveal that recently ingested sugar directly fuels flight, giving rise to the concept of the “sucrose oxidation cascade”. The ecological and bioenergetic advantages conferred by sugar oxidation during foraging are discussed.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Bartholomew GA, Lighton JRB (1986) Oxygen consumption during hover-feeding in free-ranging Anna hummingbirds. Journal of Experimental Biology 123:191–199

    PubMed  CAS  Google Scholar 

  • Berger M (1985) Sauerstoffverbrauch von Kolibris (Colibri coruscans und C. thalassinus) beim Horizontalflug. BIONA Report 3. In: W Nachtigall (ed) Biona-Report 3, Bird Flight. G Fischer, Stuttgart, pp 307–314

    Google Scholar 

  • 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. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 352:447–456

    Google Scholar 

  • Blem CR (1976) Patterns of lipid storage and utilization in birds. American Zoologist 16:671–684

    CAS  Google Scholar 

  • Blomstrand E, Ekblom B, Newsholme EA (1986) Maximum activities of key glycolytic and oxidative enzymes in human muscle from differently trained individuals. Journal of Physiology 381:111–118

    Google Scholar 

  • Brand MD (2005) The efficiency and plasticity of mitochondrial energy transduction. Biochemical Society Transactions 33:897–904

    Article  PubMed  CAS  Google Scholar 

  • Carpenter FL, Hixon MA (1988) A new function for torpor: fat conservation in a wild migrant hummingbird. Condor 90:373–378

    Article  Google Scholar 

  • Carpenter FL, Paton DC, Hixon MA (1983) Weight gain and adjustment of feeding territory size in migrant hummingbirds. Proceedings of the National Academy of Sciences of the United States of America 80:7259–7263

    Article  PubMed  CAS  Google Scholar 

  • Chai P, Dudley R (1995) Limits to vertebrate locomotor energetics suggested by hummingbirds hovering in heliox. Nature 377:722–725

    Article  CAS  Google Scholar 

  • Chantler PD (1982) Caged ATP set free in muscle. Nature 300:682–683

    Article  PubMed  CAS  Google Scholar 

  • Crabtree B, Newsholme EA (1972a) The activities of lipases and carnitine palmitoyltransferase in muscles from vertebrates and invertebrates. The Biochemical Journal 130:697–705

    PubMed  CAS  Google Scholar 

  • Crabtree B, Newsholme EA (1972b) The activities of phosphorylase, hexokinase, phosphofructokinase, lactate dehydrogenase and the glycerol 3-phosphate dehydrogenases in muscles from vertebrates and invertebrates. The Biochemical Journal 126:49–58

    PubMed  CAS  Google Scholar 

  • Delarue J, Normand S, Pachiaudi C, Beylot M, Lamisse F, Riou JP (1993) The contribution of naturally labelled 13C fructose to glucose appearance in humans. Diabetologia 36:338–345

    Article  PubMed  CAS  Google Scholar 

  • di Prampero PE (2003) Factors limiting maximal performance in humans. European Journal of Applied Physiology 90:420–429

    Article  PubMed  Google Scholar 

  • Dubach M (1981) Quantitative analysis of the respiratory system of the house sparrow, budgerigar and violet-eared hummingbird. Respiration Physiology 46:43–60

    Article  PubMed  CAS  Google Scholar 

  • Dudley R (2000) The Biomechanics of Insect Flight. Princeton University Press, Princeton

    Google Scholar 

  • Epting RJ (1980) Functional dependence of the power for hovering on wing disc loading in hummingbirds. Physiological Zoology 53:347–357

    Google Scholar 

  • Fell DA (2000) Signal transduction and the control of expression of enzyme activity. Advances in Enzyme Regulation 40:35–46

    Article  PubMed  CAS  Google Scholar 

  • Fons R, Sicart R (1976) Contribution à la connaissance du metabolisme énergétique chez deux crocidurinae: Suncus etruscus (Savi, 1822) et Crocidura russula (Hermann, 1780) (Insectivora, Soricidae). Mammalia 40:299–311

    Article  PubMed  CAS  Google Scholar 

  • Gass CL, Romich MT, Suarez RK (1999) Energetics of hummingbird foraging at low ambient temperature. Canadian Journal of Zoology 77:314–320

    Article  Google Scholar 

  • Grinyer I, George JC (1969) Some observations on the ultrastructure of the hummingbird pectoral muscles. Canadian Journal of Zoology 47:771–774

    Article  PubMed  CAS  Google Scholar 

  • 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 377–396

    Chapter  Google Scholar 

  • Johansen K, Berger M, Bicudo JEPW, Ruschi A, De Almeida PJ (1987) Respiratory properties of blood and myoglobin in hummingbirds. Physiological Zoology 60:269–278

    Google Scholar 

  • Jones JH (1998) Optimization of the mammalian respiratory system: symmorphosis versus single species adaptation. Comparative Biochemistry and Physiology 120B:125–138

    CAS  Google Scholar 

  • Kleiber M (1961) The Fire of Life. Wiley, New York

    Google Scholar 

  • Kristiansen S, Darakhshan F, Richter EA, Handal HS (1997) Fructose transport and GLUT5 protein in human sarcolemmal vesicles. American Journal of Physiology 273:E543–E548

    PubMed  CAS  Google Scholar 

  • Lasiewski RC (1963) Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiological Zoology 36:122–140

    CAS  Google Scholar 

  • Lasiewski RC (1964) Body temperatures, heart and breathing rate, and evaporative water loss in hummingbirds. Physiological Zoology 37:212–223

    Google Scholar 

  • Lasiewski RC, Galey FR, Vasquez C (1965) Morphology and physiology of the pectoral muscles of hummingbirds. Nature 205:404–405

    Article  Google Scholar 

  • Maina JN (2000) What it takes to fly: the structural and functional respiratory requirements in birds and bats. Journal of Experimental Biology 203:3045–3064

    PubMed  CAS  Google Scholar 

  • Mainwood GW, Rakusan K (1982) A model for intracellular energy transport. Canadian Journal of Physiology and Pharmacology 60:98–102

    Article  PubMed  CAS  Google Scholar 

  • Mathieu-Costello O, Suarez RK, Hochachka PW (1992) Capillary-to-fiber geometry and mitochondrial density in hummingbird flight muscle. Respiratory Physiology 89:113–132

    Article  CAS  Google Scholar 

  • McWhorter TJ, Martinez del Rio C (2000) Does gut function limit hummingbird food intake? Physiological and Biochemical Zoology 73:313–324

    Article  PubMed  CAS  Google Scholar 

  • 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. Biology Letters 2:131–134

    Article  PubMed  CAS  Google Scholar 

  • Newsholme EA, Crabtree B (1986) Maximum catalytic activity of some key enzymes in provision of physiologically useful information about metabolic fluxes. Journal of Experimental Zoology 239:159–167

    Article  PubMed  CAS  Google Scholar 

  • Odum EP, Connell CE, Stoddard HL (1961) Flight energy and estimated flight ranges of some migratory birds. Auk 78:515–527

    Google Scholar 

  • Rosser BWC, George JC (1986) The avian pectoralis: histochemical characterization and distribution of muscle fiber types. Canadian Journal of Zoology 64:1174–1185

    Article  Google Scholar 

  • Srere PA (1985) Organization of proteins within the mitochondrion. In: Welch GR (ed) Organized Multienzyme Systems Catalytic Properties. Academic Press, New York, pp 1–61

    Google Scholar 

  • Suarez RK (1992) Hummingbird flight: sustaining the highest mass-specific metabolic rates among vertebrates. Experientia 48:565–570

    Article  PubMed  CAS  Google Scholar 

  • Suarez RK (1996) Upper limits to mass-specific metabolic rates. Annual Review of Physiology 58:583–605

    Article  PubMed  CAS  Google Scholar 

  • Suarez RK (1998) Oxygen and the upper limits to animal design and performance. Journal of Experimental Biology 201:1065–1072

    PubMed  CAS  Google Scholar 

  • Suarez RK, Gass CL (2009) Hummingbird foraging and the relation between bioenergetics and behaviour. Comparative Biochemistry and Physiology (in press)

    Google Scholar 

  • Suarez RK, Brown GS, Hochachka PW (1986) Metabolic sources of energy for hummingbird flight. American Journal of Physiology 251:R537–R542

    PubMed  CAS  Google Scholar 

  • Suarez RK, Brownsey RW, Vogl W, Brown GS, Hochachka PW (1988) Biosynthetic capacity of hummingbird liver. American Journal of Physiology 255:R699–R702

    PubMed  CAS  Google Scholar 

  • Suarez RK, Lighton JRB, Moyes CD, Brown GS, Gass CL, Hochachka PW (1990) Fuel selection in rufous hummingbirds: ecological implications of metabolic biochemistry. Proceedings of the National Academy of Science U S A 87:9207–9210

    Article  CAS  Google Scholar 

  • Suarez RK, Lighton JRB, Brown GS, Mathieu-Costello O (1991) Mitochondrial respiration in hummingbird flight muscles. Proceedings of the National Academy of Science U S A 88:4870–4873

    Article  CAS  Google Scholar 

  • Suarez RK, Lighton JRB, Joos B, Roberts SP, Harrison JF (1996) Energy metabolism, enzymatic flux capacities and metabolic flux rates in flying honeybees. Proceedings of the National Academy of Science U S A 93:12616–12620

    Article  CAS  Google Scholar 

  • Suarez RK, Staples JF, Lighton JRB, West TG (1997) Relationships between enzymatic flux capacities and metabolic flux rates in muscles: nonequilibrium reactions in muscle glycolysis. Proceedings of the National Academy of Science U S A 94:7065–7069

    Article  CAS  Google Scholar 

  • Taylor CR (1987) Structural and functional limits to oxidative metabolism: Insights from scaling. Annual Review of Physiology 49:135–146

    Article  PubMed  CAS  Google Scholar 

  • Voigt CC, Winter Y (1999) Energetic cost of hovering flight in nectar-feeding bats (Phyllostomidae: Glossophaginae) and its scaling in moths, birds and bats. Journal of Comparative Physiology 169:38–48

    CAS  Google Scholar 

  • Weibel ER (1984) The Pathway for Oxygen. Harvard University Press, Cambridge, MA, USA

    Google Scholar 

  • Weibel ER (1985) Design and performance of muscular systems: an overview. Journal of Experimental Biology 115:405–412

    PubMed  CAS  Google Scholar 

  • Welch JKC, Bakken BH, Martinez del Rio C, Suarez RK (2006) Hummingbirds fuel hovering flight with newly-ingested sugar. Physiological and Biochemical Zoology 79:1082–1087

    Article  PubMed  CAS  Google Scholar 

  • Welch JKC, Suarez RK (2007) Oxidation rate and turnover of ingested sugar in hovering Anna's (Calypte anna) and rufous (Selasphorus rufus) hummingbirds. Journal of Experimental Biology 210:2154–2162

    Article  PubMed  CAS  Google Scholar 

  • Welch JKC, Suarez RK (2009) Altitude and temperature effects on the energetic cost of hover-feeding in migratory rufous hummingbirds, Selasphorus rufus. Canadian Journal of Zoology (in press)

    Google Scholar 

  • Welch JKC, Altshuler DL, Suarez RK (2007) Oxygen consumption rates in hovering hummingbirds reflect substrate-dependent differences in P/O ratios: carbohydrate as a ‘premium fuel’. Journal of Experimental Biology 210:2146–2153

    Article  PubMed  CAS  Google Scholar 

  • Welch JKC, Herrera LG, Suarez RK (2008a) Dietary sugar as a direct fuel for flight in the nectarivorous bat, Glossophaga soricina. Journal of Experimental Biology (in press)

    Google Scholar 

  • Welch Jr. KC, Herrera LG, Suarez RK (2008b) Dietary sugar as a direct fuel for flight in the nectarivorous bat, Glossophaga soricina. Journal of Experimental Biology (in press)

    Google Scholar 

  • Winter Y, Voigt C, von Helversen O (1998) Gas exchange during hovering flight in a nectar-feeding bat Glossophaga soricina. Journal of Experimental Biology 201:237–244

    PubMed  CAS  Google Scholar 

  • Woeltje KF, Kuwajima M, Foster DW, McGarry JD (1987) Characterization of the mitochondrial carnitine palmitoyltransferase enzyme system. I. Use of detergents and antibodies. Journal of Biological Chemistry 262:9822–9827

    PubMed  CAS  Google Scholar 

  • Yacoe ME, Cummings JW, Myers P, Creighton GK (1982) Muscle enzyme profile, diet and flight in South American bats. American Journal of Physiology 242:R189–R194

    PubMed  CAS  Google Scholar 

  • Zierath JR, Nolte LA, Wahlstrom E, Galuska D, Shepherd PR, Kahn BB, Wallberg-Henriksson H (1995) Carrier-mediated fructose uptake significantly contributes to carbohydrate metabolism in human skeletal muscle. Biochemistry Journal 311:517–521

    CAS  Google Scholar 

Download references

Acknowledgements

Supported by grants from the NSF IOB 0517694 and UC MEXUS CONA-CYT.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raul K. Suarez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Suarez, R.K., Welch, K.C. (2009). Stoking the Brightest Fires of Life Among Vertebrates. In: Glass, M., Wood, S. (eds) Cardio-Respiratory Control in Vertebrates. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-93985-6_15

Download citation

Publish with us

Policies and ethics