Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly

Toby Fountain, Richard G. Melvin, Suvi Ikonen, Annukka Ruokolainen, Luisa Woestmann, Ville Hietakangas, Ilkka Hanski

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Flying insects have the highest known mass-specific demand for oxygen, which makes it likely that reduced availability of oxygen might limit sustained flight, either instead of or in addition to the limitation due to metabolite resources. The Glanville fritillary butterfly (Melitaea cinxia) occurs as a large metapopulation in which adult butterflies frequently disperse between small localpopulations.Here,we examine how the interaction between oxygen availability and fuel use affects flight performance in the Glanville fritillary. Individualswere flown under either normoxic (21 kPa O2) or hypoxic (10 kPa O2) conditions and their flight metabolism was measured. To determine resource use, levels of circulating glucose, trehalose and whole-body triglyceride were recorded after flight. Flight performancewas significantly reduced in hypoxic conditions. When flown under normoxic conditions, we observed a positive correlation among individuals between post-flight circulating trehalose levels and flight metabolic rate, suggesting that low levels of circulating trehalose constrains flight metabolism. To test this hypothesis experimentally, we measured the flight metabolic rate of individuals injected with a trehalase inhibitor. In support of the hypothesis, experimental butterflies showed significantly reduced flight metabolic rate, but not resting metabolic rate, in comparison to control individuals. By contrast, under hypoxia there was no relationship between trehalose and flight metabolic rate. Additionally, in this case, flight metabolic rate was reduced in spite of circulating trehalose levels that were high enough to support high flight metabolic rate under normoxic conditions. These results demonstrate a significant interaction between oxygen and energy availability for the control of flight performance.

Original languageEnglish (US)
Pages (from-to)1488-1494
Number of pages7
JournalJournal of Experimental Biology
Volume219
Issue number10
DOIs
StatePublished - May 15 2016
Externally publishedYes

Bibliographical note

Funding Information:
This study was funded by grants from the European Research Council [AdG grant number 232826]; and the Academy of Finland [Finnish CoE Programme, grant numbers 256453 and 250444] to I.H.

Publisher Copyright:
© 2016. Published by The Company of Biologists Ltd.

Keywords

  • Flight capacity
  • Glanville fritillary
  • Hypoxia
  • Metabolism
  • Respirometry
  • Trehalose

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