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Insects breathe discontinuously to avoid oxygen toxicity

Abstract

The respiratory organs of terrestrial insects consist of tracheal tubes with external spiracular valves that control gas exchange. Despite their relatively high metabolic rate, many insects have highly discontinuous patterns of gas exchange, including long periods when the spiracles are fully closed. Two explanations have previously been put forward to explain this behaviour: first, that this pattern serves to reduce respiratory water loss1, and second, that the pattern may have initially evolved in underground insects as a way of dealing with hypoxic or hypercapnic conditions2. Here we propose a third possible explanation based on the idea that oxygen is necessary for oxidative metabolism but also acts as a toxic chemical that can cause oxidative damage of tissues even at relatively low concentrations. At physiologically normal partial pressures of CO2, the rate of CO2 diffusion out of the insect respiratory system is slower than the rate of O2 entry; this leads to a build-up of intratracheal CO2. The spiracles must therefore be opened at intervals to rid the insect of accumulated CO2, a process that exposes the tissues to dangerously high levels of O2. We suggest that the cyclical pattern of open and closed spiracles observed in resting insects is a necessary consequence of the need to rid the respiratory system of accumulated CO2, followed by the need to reduce oxygen toxicity.

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Figure 1: The rate of release of CO2 from a pupa of Attacus atlas over time.
Figure 2: The discontinuous gas exchange cycle (DGC) in a pupa of A. atlas.
Figure 3: Respiratory regulation in pupae of A. atlas during the flutter phase at different atmospheric O2 concentrations.
Figure 4: Intratracheal p O 2 in pupae of A. atlas during the flutter phase as a function of external O2 concentration.

References

  1. Levy, R. I. & Schneiderman, H. A. Discontinuous respiration in insects. II. The direct measurement and significance of changes in tracheal gas composition during the respiratory cycle of silkworm pupae. J. Insect Physiol. 12, 83–104 (1966)

    CAS  Article  Google Scholar 

  2. Lighton, J. R. B. Notes from the underground: toward ultimate hypotheses of cyclic, discontinuous gas-exchange in tracheate arthropods. Am. Zool. 38, 483–491 (1998)

    Article  Google Scholar 

  3. Wigglesworth, V. B. The Principles of Insect Physiology (Methuen, London, 1970)

    Google Scholar 

  4. Krogh, A. Studien ueber tracheenrespiration. II. Ueber gasdiffusion in den tracheen. Pfluegers Arch. 179, 95–112 (1920)

    CAS  Article  Google Scholar 

  5. Krogh, A. Studien über die tracheenrespiration. III. Die kombination von mechanischer ventilation mit gasdiffusion nach versuchen an dytiscidenlarven. Pflugers Arch. 179, 113–120 (1920)

    CAS  Article  Google Scholar 

  6. Slama, K. A new look at insect respiration. Biol. Bull. 175, 289–300 (1988)

    Article  Google Scholar 

  7. Westneat, M. W. et al. Tracheal respiration in insects visualized with synchrotron x-ray imaging. Science 299, 558–560 (2003)

    ADS  CAS  Article  Google Scholar 

  8. Slama, K. Active regulation of insect respiration. Ann. Entomol. Soc. Am. 92, 916–929 (1999)

    Article  Google Scholar 

  9. Lighton, J. R. B. Discontinuous gas exchange in insects. Annu. Rev. Entomol. 41, 309–324 (1996)

    CAS  Article  Google Scholar 

  10. Hadley, N. F. Ventilatory patterns and respiratory transpiration in adult terrestrial insects. Physiol. Zool. 67, 175–189 (1994)

    ADS  Article  Google Scholar 

  11. Chown, S. L. & Holter, P. Discontinuous gas exchange cycles in Aphodius fossor (Scarabaeidae): a test of hypotheses concerning origins and mechanisms. J. Exp. Biol. 203, 397–403 (2000)

    CAS  PubMed  Google Scholar 

  12. Williams, A. E. & Bradley, T. J. The effect of respiratory pattern on water loss in desiccation-resistant Drosophila melanogaster. J. Exp. Biol. 201, 2953–2959 (1998)

    CAS  PubMed  Google Scholar 

  13. Lighton, J. R. B. & Garrigan, D. Ant breathing: testing regulation and mechanism hypotheses with hypoxia. J. Exp. Biol. 198, 1613–1620 (1995)

    CAS  PubMed  Google Scholar 

  14. Bradley, T. J., Brethorst, L., Robinson, S. & Hetz, S. Changes in the rate of CO2 release following feeding in the insect Rhodnius prolixus. Physiol. Biochem. Zool. 76, 302–309 (2002)

    Article  Google Scholar 

  15. Richardson, R. S., Noyszeski, E. A., Kendrick, K. F., Leigh, J. S. & Wagner, P. D. Myoglobin O2 desaturation during exercise: evidence of limited O2 transport. J. Clin. Invest. 96, 1916–1926 (1995)

    CAS  Article  Google Scholar 

  16. Jamieson, D. Oxygen toxicity and reactive oxygen metabolites in mammals. Free Radic. Biol. Med. 7, 87–108 (1989)

    CAS  Article  Google Scholar 

  17. Fridovich, I. Oxygen is toxic! Bioscience 27, 462–466 (1977)

    Article  Google Scholar 

  18. Sohal, R. S., Agarwal, S. & Orr, W. C. Simultaneous overexpression of copper-and zinc-containing superoxide dismutase and catalase retards age-related oxidative damage and increases metabolic potential in Drosophila melanogaster. J. Biol. Chem. 270, 15671–15674 (1995)

    CAS  Article  Google Scholar 

  19. Schwarze, S. R., Weindruch, R. & Aiken, J. M. Oxidative stress and aging reduce Cox 1 RNA and cytochrome oxidase activity in Drosophila. Free Radic. Biol. Med. 25, 740–747 (1998)

    CAS  Article  Google Scholar 

  20. Orr, W. C. & Sohal, R. S. Extension of life-span by over-expression of superoxide dismutase and catalase in Drosophila melanogaster. Science 263, 1128–1130 (1994)

    ADS  CAS  Article  Google Scholar 

  21. Sun, J., Folk, D., Bradley, T. J. & Tower, J. Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster without changing metabolic rate. Genetics 161, 661–672 (2002)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Yan, L. J. & Sohal, R. S. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl Acad. Sci. USA 94, 11168–11172 (1997)

    ADS  CAS  Article  Google Scholar 

  23. Lighton, J. R. B. & Fielden, L. J. Gas exchange in wind spiders (Arachnida, Solphugidae). Independent evolution of convergent control strategies in solphugids and insects. J. Insect Physiol. 42, 347–357 (1996)

    CAS  Article  Google Scholar 

  24. Fielden, L. J. & Lighton, J. R. B. Effects of water stress and relative humidity on ventilation in the tick Dermacentor andersoni (Acari, Iodidae). Physiol. Zool. 69, 599–617 (1996)

    Article  Google Scholar 

  25. Lighton, J. R. B. & Joos, B. Discontinuous gas exchange in the pseudoscorpion Garypus californicus is regulated by hypoxia, not hypercapnia. Physiol. Biochem. Zool. 75, 345–349 (2002)

    Article  Google Scholar 

  26. Lighton, J. R. B. Discontinuous CO2 emission in a small insect, the formicine ant Camponotus vicinus. J. Exp. Biol. 134, 363–376 (1988)

    Google Scholar 

  27. Weibel, E. R. Symmorphosis and optimization of biological design: introduction and questions. In Principles of Animal Design (Cambridge Univ. Press, Cambridge, 1998)

    Google Scholar 

  28. Weibel, E. R. et al. Design of the oxygen and substrate pathways. 7. Different structural limits for oxygen and substrate supply to muscle mitochondria. J. Exp. Biol. 199, 1699–1709 (1996)

    CAS  PubMed  Google Scholar 

  29. Davis, A. L. V., Chown, S. L. & Scholtz, C. H. Discontinuous gas-exchange cycles in Scarabaeus dung beetles (Coleoptera: Scarabaeidae): Mass-scaling and temperature dependence. Physiol. Biochem. Zool. 72, 555–565 (1999)

    CAS  Article  Google Scholar 

  30. Hetz, S. K., Wasserthal, L. T., Hermann, S., Kaden, H. & Oelssner, W. Direct oxygen measurements in the tracheal system of Lepidopterous pupae using miniaturized amperometric sensors. Bioelectrochem. Bioenerg. 33, 165–170 (1994)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank N. Heisler for comments and for providing equipment. T.J.B. would like to thank N. Heisler for his hospitality during a research visit. This work was supported by an NSF grant to T.J.B.

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Correspondence to Timothy J. Bradley.

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Hetz, S., Bradley, T. Insects breathe discontinuously to avoid oxygen toxicity. Nature 433, 516–519 (2005). https://doi.org/10.1038/nature03106

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