Honeybee larvae and pupae are extremely stenothermic, i.e. they strongly depend on accurate regulation of brood nest temperature for proper development (33–36°C). Here we study the mechanisms of social thermoregulation of honeybee colonies under changing environmental temperatures concerning the contribution of individuals to colony temperature homeostasis. Beside migration activity within the nest, the main active process is “endothermy on demand” of adults. An increase of cold stress (cooling of the colony) increases the intensity of heat production with thoracic flight muscles and the number of endothermic individuals, especially in the brood nest. As endothermy means hard work for bees, this eases much burden of nestmates which can stay ectothermic. Concerning the active reaction to cold stress by endothermy, age polyethism is reduced to only two physiologically predetermined task divisions, 0 to ∼2 days and older. Endothermic heat production is the job of bees older than about two days. They are all similarly engaged in active heat production both in intensity and frequency. Their active heat production has an important reinforcement effect on passive heat production of the many ectothermic bees and of the brood. Ectothermy is most frequent in young bees (<∼2 days) both outside and inside of brood nest cells. We suggest young bees visit warm brood nest cells not only to clean them but also to speed up flight muscle development for proper endothermy and foraging later in their life. Young bees inside brood nest cells mostly receive heat from the surrounding cell wall during cold stress, whereas older bees predominantly transfer heat from the thorax to the cell wall. Endothermic bees regulate brood comb temperature more accurately than local air temperature. They apply the heat as close to the brood as possible: workers heating cells from within have a higher probability of endothermy than those on the comb surface. The findings show that thermal homeostasis of honeybee colonies is achieved by a combination of active and passive processes. The differential individual endothermic and behavioral reactions sum up to an integrated action of the honeybee colony as a superorganism.
SUMMARYIn order to survive cold northern winters, honeybees crowd tightly together in a winter cluster. Present models of winter cluster thermoregulation consider the insulation by the tightly packed mantle bees as the decisive factor for survival at low temperatures, mostly ignoring the possibility of endothermic heat production. We provide here direct evidence of endothermic heat production by `shivering' thermogenesis. The abundance of endothermic bees is highest in the core and decreases towards the surface. This shows that core bees play an active role in thermal control of winter clusters. We conclude that regulation of both the insulation by the mantle bees and endothermic heat production by the inner bees is necessary to achieve thermal stability in a winter cluster.
The relation between the respiratory activity of resting honeybees and ambient temperature (T a ) was investigated in the range of 5-40 °C. Bees were kept in a temperature controlled flow through respirometer chamber where their locomotor and endothermic activity, as well as abdominal ventilatory movements was recorded by infrared thermography.Surprisingly, true resting bees were often weakly endothermic (thorax surface up to 2.8 °C warmer than abdomen) at a T a of 14-30 °C. Above 33 °C many bees cooled their body via evaporation from their mouthparts. A novel mathematical model allows description of the relationship of resting (standard) metabolic rate and temperature across the entire functional temperature range of bees. In chill coma (<11 °C) bees were ectothermic and CO 2 release was mostly continuous. CO 2 release rate (nl s −1 ) decreased from 9.3 at 9.7 °C to 5.4 at 5 °C. At a T a of >11 °C CO 2 was released discontinuously. In the bees' active temperature range mean CO 2 production rate (nl s −1 ) increased sigmoidally (10.6 at 14.1 °C, 24.1 at 26.5 °C, and 55.2 at 38
Graphical abstract.Research highlights▶ Thorax temperature was regulated from 37.0–45.3 °C (ambient temperature: 3–39 °C). ▶ Solar heat gain was used to increase thorax temperature by about 1–3 °C. ▶ High thorax temperature allowed regulation of an optimal head temperature. ▶ Flexible thermal strategy enabled foraging in a broad ambient temperature range.
Graphical abstract.Highlights► We demonstrate the benefits of a combined use of infrared thermography with respiratory measurements in insect ecophysiological research. ► Infrared thermography enables repeated investigation of behaviour and thermoregulation without behavioural impairment. ► Comparison with respirometry brings new insights into the mechanisms of energetic optimisation of bee and wasp foraging. ► Combination of methods improves interpretation of respiratory traces in determinations of insect critical thermal limits.
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