title: Oxygen and energy availability interact to determine flight performance in the Glanville fritillary butterfly.
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 local populations. Here, we examine how the interaction between oxygen availability and fuel use affects flight performance in the Glanville fritillary. Individuals were 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 performance was 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.
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland toby.fountain@helsinki.fi.
authors.forename: Toby
authors.initials: T
authors.lastname: Fountain
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Richard G
authors.initials: RG
authors.lastname: Melvin
authors.affiliation: Lammi Biological Station, University of Helsinki, Lammi 16900, Finland.
authors.forename: Suvi
authors.initials: S
authors.lastname: Ikonen
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Annukka
authors.initials: A
authors.lastname: Ruokolainen
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Luisa
authors.initials: L
authors.lastname: Woestmann
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Ville
authors.initials: V
authors.lastname: Hietakangas
authors.affiliation: Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Ilkka
authors.initials: I
authors.lastname: Hanski
mesh_terms: D000818:Animals; D001481:Basal Metabolism / Q000187:drug effects / Q000502:physiology; D002080:Butterflies / Q000187:drug effects / Q000502:physiology*; D004734:Energy Metabolism / Q000187:drug effects; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005260:Female; D005426:Flight, Animal / Q000187:drug effects / Q000502:physiology*; D031410:Fritillaria / Q000469:parasitology*; D005947:Glucose / Q000032:analysis; D000860:Hypoxia / Q000378:metabolism; D008297:Male; D010100:Oxygen / Q000378:metabolism*; D012044:Regression Analysis; D012146:Rest; D013217:Starvation / Q000378:metabolism; D014198:Trehalase / Q000037:antagonists & inhibitors / Q000378:metabolism; D014199:Trehalose / Q000032:analysis
chemical_list: D004791:Enzyme Inhibitors; D014199:Trehalose; D014198:Trehalase; D005947:Glucose; D010100:Oxygen
keywords: Flight capacity; Glanville fritillary; Hypoxia; Metabolism; Respirometry; Trehalose