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 O 2 ) or hypoxic (10 kPa O 2 ) 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.

Regulatory Functions of Nilaparvata lugens GSK-3 in Energy and Chitin Metabolism

“…Trehalose can act as an energy reserve for the life activities of insects under stress, such as starvation and dryness (Yasugi et al, 2017). Under various stresses, trehalose accumulation occurs in insects (Fountain et al, 2016;Tamang et al, 2017;Paithankar et al, 2018). This study found that the trehalose content increased extremely significantly 48 h after dsGSK-3 injection (Figure 2C), and the two trehalase activities decreased extremely significantly (Figures 3A,B), showing consistency.…”

Effects of flight and food stress on energetics, reproduction, and lifespan in the butterfly Melitaea cinxia

“…However, flight in the Glanville fritillary is solely fuelled by carbohydrates (rq = 1) (Haag et al 2005), similar to the case of some other insects, such as bees (Suarez et al 2005). Starvation was shown to reduce circulating glucose and trehalose levels in the Glanville fritillary, but no significant change in haemolymph triglyceride levels was found (Fountain et al 2016). These findings suggest that while lipids have an important role in egg production, lipid oxidation may not be used for energy production in this non-migratory species, and the lower CO 2 production would thus indicate a genuinely lower RMR.…”

Cold adaptation across the elevation gradient in an alpine butterfly species complex

“…In addition to temperature, many other factors may constrain butterfly flight at high elevation, including predation pressure, oxygen and energy availability (Fountain et al, 2016), wind, and radiation (Cormont et al, 2011). Wing loading is positively correlated with speed and manoeuvrability (Tennekes, 2009), and we observed that the wing loading increases with elevation, regardless of species (Table 4).…”