Mechanisms of thermal stability during flight in the honeybee Apis mellifera

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Abstract
Thermoregulation of the thorax allows honeybees (Apis mellifera) to maintain the flight muscle temperatures necessary to meet the power requirements for flight and to remain active outside the hive across a wide range of air temperatures (Ta). To determine the heat-exchange pathways through which flying honeybees achieve thermal stability, we measured body temperatures and rates of carbon dioxide production and water vapor loss between Ta values of 21 and 45 °C for honeybees flying in a respirometry chamber. Body temperatures were not significantly affected by continuous flight duration in the respirometer, indicating that flying bees were at thermal equilibrium. Thorax temperatures (Tth) during flight were relatively stable, with a slope of Tth on Ta of 0.39. Metabolic heat production, calculated from rates of carbon dioxide production, decreased linearly by 43 % as Ta rose from 21 to 45 °C. Evaporative heat loss increased nonlinearly by over sevenfold, with evaporation rising rapidly at Ta values above 33 °C. At Ta values above 43 °C, head temperature dropped below Ta by approximately 1–2 °C, indicating that substantial evaporation from the head was occurring at very high Ta values. The water flux of flying honeybees was positive at Ta values below 31 °C, but increasingly negative at higher Ta values. At all Ta values, flying honeybees experienced a net radiative heat loss. Since the honeybees were in thermal equilibrium, convective heat loss was calculated as the amount of heat necessary to balance metabolic heat gain against evaporative and radiative heat loss. Convective heat loss decreased strongly as Ta rose because of the decrease in the elevation of body temperature above Ta rather than the variation in the convection coefficient. In conclusion, variation in metabolic heat production is the dominant mechanism of maintaining thermal stability during flight between Ta values of 21 and 33 °C, but variations in metabolic heat production and evaporative heat loss are equally important to the prevention of overheating during flight at Ta values between 33 and 45 °C.