Performance benefits of stable, warm muscles are believed to be important for the evolution of endothermy in mammals, birds and flying insects. However, thermal performance curves have never been measured for a free-flying endotherm, as it is challenging to vary body temperatures of these animals, and maximal flight performance is difficult to elicit. We varied air temperatures and gas densities to manipulate thoracic temperatures of flying honeybees from 29°C to 44°C, with low air densities used to increase flight metabolic rates to maximal values. Honeybees showed a clear thermal performance curve with an optimal temperature of 39°C. Maximal flight metabolic rates increased by approximately 2% per 1°C increase in thoracic temperature at suboptimal thoracic temperatures, but decreased approximately 5% per 1°C increase as the bees continued to heat up. This study provides the first quantification of the maximal metabolic performance benefit of thermoregulation in an endotherm. These data directly support aerobic capacity models for benefits of thermoregulation in honeybees, and suggest that improved aerobic capacity probably contributes to the multiple origins of endothermic heterothermy in bees and other insects.

Complex environments, characterized by co-varying factors (e.g. temperature and food availability) may cause animals to invest resources differentially into fitness-related traits. Thus, experiments manipulating multiple environmental factors concurrently provide valuable insight into the role of the environment in shaping not only important traits (e.g. dispersal capacity or reproduction), but also trait–trait interactions (e.g. trade-offs between traits). We used a multi-factorial design to manipulate variation in temperature (constant 28 °C vs. 28 ± 5 °C daily cycle) and food availability (unlimited vs. intermittent access) throughout development in the sand field cricket (Gryllus firmus). Using a univariate approach, we found that temperature variability and unlimited food availability promoted survival, development, growth, body size and/or reproductive investment. Using principal components as indices of resource allocation strategy, we found that temperature variability and unlimited food reduced investment into flight capacity in females. Thus, we detected a sex-specific trade-off between flight and other life-history traits that was developmentally plastic in response to variation in temperature and food availability. We develop an experimental and statistical framework to reveal shifts in correlative patterns of investment into different life-history traits. This approach can be applied to a range of biological systems to investigate how environmental complexity influences traits and trait trade-offs.

Flying endothermic insects thermoregulate, likely to improve flight performance. Males of the Sonoran Desert bee, Centris caesalpiniae Cockerell, seek females at aggregations beginning at sunrise and cease flight near midday when air temperature peaks. To identify the thermoregulatory mechanisms for C. caesalpiniae males, we measured tagma temperatures, wingbeat frequency, water loss rates, metabolic rates, and tagma masses of flying bees across shaded air temperatures of 19 to 38°C. Surface area, wet mass, and dry mass declined with air temperature, suggesting that individual bees do not persist for the entire morning. The largest bees may be associated with cool, early mornings because they are best able to warm themselves and/or because they run the risk of overheating in the hot afternoons. Thorax temperatures were high (38 to 45°C) and were moderately well-regulated, while head and abdomen temperatures were cooler and less controlled. The abdominal temperature excess ratio increased as air temperature rose, indicating active heat transfer from the pubescent thorax to the relatively bare abdomen with warming. Mass-specific metabolic rate increased with time, air, and thorax temperatures, but wingbeat frequency did not vary. Mass-specific water loss rate increased with air temperature, but this was a minor mechanism of thermoregulation. Using a heat budget model, we showed that whole-body convective conductance more than doubled through the morning, providing strong evidence that the primary mechanism of regulating thorax temperature during flight for these bees is increased use of the abdomen as a convector at higher air temperatures.

No abstract