Helmut Kovac

Honeybee Colony Thermoregulation – Regulatory Mechanisms and Contribution of Individuals in Dependence on Age, Location and Thermal Stress

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.

Lifespan of Apis Mellifera Carnica Pollm. Infested by Varroa Jacobsoni Oud. in Relation to Season and Extent of Infestation

SummaryLongevity, duration of hive-bound period, and foraging period, of worker bees, infested or not infested during their pupal development, were investigated during the whole year. Shortening of lifespan depended on the extent of infestation and on season. Influence of infestation on lifespan could be shown during hive-bound and foraging periods; no influence could be shown on flight activity. Drastic differences occurred during winter; in 4 observation hives, only 4–18% of the infested bees that had emerged in September, survived until the following March.

Oxygen consumption and body temperature of active and resting honeybees

We measured the energy turnover (oxygen consumption) of honeybees (Apis mellifera carnica), which were free to move within Warburg vessels. Oxygen consumption of active bees varied widely depending on ambient temperature and level of activity, but did not differ between foragers (>18 d) and middle-aged hive bees (7-10 d). In highly active bees, which were in an endothermic state ready for flight, it decreased almost linearly, from a maximum of 131.4 microl O(2) min(-1) at 15 degrees C ambient temperature to 81.1 microl min(-1) at 25 degrees C, and reached a minimum of 29.9 microl min(-1) at 40 degrees C. In bees with low activity, it decreased from 89.3 microl O(2) min(-1) at 15 degrees C to 47.9 microl min(-1) at 25 degrees C and 14.7 microl min(-1) at 40 degrees C. Thermographic measurements of body temperature showed that with increasing activity, the bees invested more energy to regulate the thorax temperature at increasingly higher levels (38.8-41.2 degrees C in highly active bees) and were more accurate. Resting metabolism was determined in young bees of 1-7 h age, which are not yet capable of endothermic heat production with their flight muscles. Their energy turnover increased from 0.21 microl O(2) min(-1) at 10 degrees C to 0.38 microl min(-1) at 15 degrees C, 1.12 microl min(-1) at 25 degrees C, and 3.03 microl min(-1) at 40 degrees C. At 15, 25 and 40 degrees C, this was 343, 73 and 10 times below the values of the highly active bees, respectively. The Q(10) value of the resting bees, however, was not constant but varied in a U-shaped manner with ambient temperature. It decreased from 4.24 in the temperature range 11-21 degrees C to 1.35 in the range 21-31 degrees C, and increased again to 2.49 in the range 30-40 degrees C. We conclude that attempts to describe the temperature dependence of the resting metabolism of honeybees by Q(10) values can lead to considerable errors if the measurements are performed at only two temperatures. An acceptable approximation can be derived by calculation of an interpolated Q(10) according to the exponential function (V(O(2))=0.151 x 1.0784(T(a))) (interpolated Q(10)=2.12).

Thermoregulation of water foraging honeybees—Balancing of endothermic activity with radiative heat gain and functional requirements

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.

Thermoregulation of honeybees (Apis mellifera) foraging in spring and summer at different plants

Abstract The body temperature of honeybees (Apis mellifera carnica Pollm.) was determined by infrared measuring instruments without touching the animals. From spring until summer the insects were observed on 13 different species of plants while foraging nectar and pollen within their natural environment. In this way it was possible for the first time to measure the body surface temperatures of all three parts of the body continuously and often simultaneously without disturbing the animals in their activity. It was remarkable that in spring at an ambient temperature from 12–20 °C on average the thorax was warmer by 6.4 °C and the head by 4.1°C than in summer (ambient temperature: 20–26 °C). The temperatures of all three parts of the body always exceeded ambient temperature. The thorax was the warmest part of the body. Concerning caput and abdomen, which were distinctly cooler, a slight dependence on the ambient temperature could be observed. The temperature of the abdomen, the coolest part of the body, never fell below 20.6 °C. It was obvious that heat was exchanged between the thorax and the two other parts of the body. The average thoracic temperature amounted to 35.7 °C in spring and to 29.3 °C in summer. The mean temperature of the head was 30.9 °C in spring and 26.8 °C in summer, that of the abdomen 25.2 °C and 23.1 °C. The higher body temperatures in spring possibly protect the bees against cooling at the lower ambient temperature.

Thermoregulation of foraging honeybees on flowering plants: seasonal variability and influence of radiative heat gain.

1. During nectar and pollen foraging in a temperate climate, honeybees are exposed to a broad range of ambient temperatures, challenging their thermoregulatory ability. The body temperature that the bees exhibit results from endothermic heat production, exogenous heat gain from solar radiation, and heat loss. In addition to profitability of foraging, season was suggested to have a considerable influence on thermoregulation. To assess the relative importance of these factors, the thermoregulatory behaviour of foragers on 33 flowering plants in dependence on season and environmental factors was investigated.

Resting metabolism and critical thermal maxima of vespine wasps (Vespula sp.).

Graphical abstract Highlights ► Vespine wasps have a very high mass-specific resting metabolic rate. ► They exhibit a steep increase of resting metabolism with ambient temperature. ► Wasp thermolimit was considerably below that of honeybees (44.9 vs. 48.9 °C). ► Infrared thermography allowed accurate estimation of the respiratory thermolimit.

Energetic optimisation of foraging honeybees: flexible change of strategies in response to environmental challenges.

Heterothermic insects like honeybees, foraging in a variable environment, face the challenge of keeping their body temperature high to enable immediate flight and to promote fast exploitation of resources. Because of their small size they have to cope with an enormous heat loss and, therefore, high costs of thermoregulation. This calls for energetic optimisation which may be achieved by different strategies. An ‘economizing’ strategy would be to reduce energetic investment whenever possible, for example by using external heat from the sun for thermoregulation. An ‘investment-guided’ strategy, by contrast, would be to invest additional heat production or external heat gain to optimize physiological parameters like body temperature which promise increased energetic returns. Here we show how honeybees balance these strategies in response to changes of their local microclimate. In a novel approach of simultaneous measurement of respiration and body temperature foragers displayed a flexible strategy of thermoregulatory and energetic management. While foraging in shade on an artificial flower they did not save energy with increasing ambient temperature as expected but acted according to an ‘investment-guided’ strategy, keeping the energy turnover at a high level (∼56–69 mW). This increased thorax temperature and speeded up foraging as ambient temperature increased. Solar heat was invested to increase thorax temperature at low ambient temperature (‘investment-guided’ strategy) but to save energy at high temperature (‘economizing’ strategy), leading to energy savings per stay of ∼18–76% in sunshine. This flexible economic strategy minimized costs of foraging, and optimized energetic efficiency in response to broad variation of environmental conditions.

Honeybee economics: optimisation of foraging in a variable world.

In honeybees fast and efficient exploitation of nectar and pollen sources is achieved by persistent endothermy throughout the foraging cycle, which means extremely high energy costs. The need for food promotes maximisation of the intake rate, and the high costs call for energetic optimisation. Experiments on how honeybees resolve this conflict have to consider that foraging takes place in a variable environment concerning microclimate and food quality and availability. Here we report, in simultaneous measurements of energy costs, gains, and intake rate and efficiency, how honeybee foragers manage this challenge in their highly variable environment. If possible, during unlimited sucrose flow, they follow an ‘investment-guided’ (‘time is honey’) economic strategy promising increased returns. They maximise net intake rate by investing both own heat production and solar heat to increase body temperature to a level which guarantees a high suction velocity. They switch to an ‘economizing’ (‘save the honey’) optimisation of energetic efficiency if the intake rate is restricted by the food source when an increased body temperature would not guarantee a high intake rate. With this flexible and graded change between economic strategies honeybees can do both maximise colony intake rate and optimise foraging efficiency in reaction to environmental variation.

Contribution of honeybee drones of different age to colonial thermoregulation

In addition to honeybee workers, drones also contribute to colonial thermoregulation. We show the drones’ contribution to thermoregulation at 5 different experimental temperatures ranging from 15– 34 °C. The frequency and the degree of endothermy depended on the drones’ local ambient temperature and age. Location on brood or non-brood areas had no influence. The frequency of endothermic drones and the intensity of endothermy increased with decreasing temperature. 30% of drones of 8 days and older heated their thorax by more than 1 °C above the abdomen. The youngest drones (0–2 days) did not exceed this level of endothermy. Though young drones were less often engaged in active heat production, their contribution to brood warming was not insignificant because their abundance on the brood nest was 3.5 times higher than that of the oldest drones (⩾13 days). Results suggest that the stimulus for the drones’ increased frequency of heating at low experimental temperatures was their low local ambient air and/or comb temperature.ZusammenfassungHonigbienen sind bekannt für ihre Fähigkeit zur Endothermie, die sie u. a. dafür nutzen, die Brutnesttemperatur in einem Bereich zwischen 32– 36 °C konstant zu halten. Diese Aufgabe wird im Wesentlichen von den Arbeiterinnen übernommen. Ziel dieser Untersuchung war zu klären, ob auch die Drohnen einen Beitrag zur kolonialen Thermoregulation leisten und ob dabei eine Altersabhängigkeit festgestellt werden kann.Dafür wurden frisch geschlüpfte Drohnen mit Farbpunkten an Thorax und Abdomen markiert und anschließend einem Beobachtungs stock, der mit einem brütenden Volk besetzt war, zugesetzt. Dieser war auf beiden Seiten mit einer Infrarot durchlässigen Folie ausgestattet, sodaß mit einer Thermografiekamera die Körpertemperatur der Bienen und die Temperatur der Wabenoberfläche gemessen werden konnte. Der Beobachtungs stock befand sich in einem klimatisierten Raum, in dem die Versuche bei 5 verschiedenen experimentellen Temperaturen zwischen 15–34 °C durchgeführt wurden. Als Maß für die Heizstärke oder Heizleistung der Drohnen wurde die Temperaturdifferenz zwischen Thorax und Abdomen, bzw. Wabe oder umgebender Luft gewählt. Während den Messungen wurde die Position auf den Waben bestimmt, der Zellinhalt ermittelt und die umgebende Lufttemperatur gemessen.Drohnen waren seltener am Brutnest anzutreffen als Arbeiterinnen. Ihre Aufenthaltshäufigkeit am Brutnest sank von 27,1 % im Alter von 0–2 d auf 7,8 % im Alter von ⩾ 13 d ab. Bei den Arbeiterinnen nahm die Häufigkeit viel stärker ab, von 72,6 % auf 27,7 % (Abb. 2). Bei unseren Versuchen beteiligten sich die Drohnen auch an der kolonialen Thermoregulation. Dieses Ergebnis wurde vor allem bei niedrigen Versuchstemperaturen, d.h. bei starker thermischer Belastung, sichtbar. Bei den Experimenten mit 15 °C zeigten sie die stärkste Heizleistung, wobei hier eine klare Altersabhängigkeit ersichtlich wurde (Abb. 3–5). Drohnen ab dem Alter von 8 Tagen heizten häufiger (30–42 %, Fig. 4) und stärker als die beiden jüngeren Altersgruppen (0–12 %, Abb. 4). Dieses Ergebnis läßt sich daraus erklären, daß junge Drohnen (< 2 Tage) die Fähigkeit zur Wärmeproduktion wahrscheinlich noch nicht voll entwickelt haben, wie wir bei Arbeiterinnen bereits feststellen konnten.Die relative Häufigkeit heizender Drohnen war mit einer Ausnahme (15 °C) auf der Brut und auf brutfreien Wabenflächen gleich (Abb. 4, Inserts). Bei den Versuchen mit 15 °C heizten vor allem die älteren Drohnen (> 2 Tage) in den kälteren, peripheren brutfreien Bereichen stärker. Die Ergebnisse einer ANCOVA und Korrelationsanalyse zeigten, daß nicht der Wabeninhalt (Brut), sondern die Waben- und/oder lokale Lufttemperatur das thermische Verhalten der Tiere bestimmte. Diese Ergebnisse weisen darauf hin, daß die Drohnen nicht wie die Arbeiterinnen durch die Anwesenheit von Brut zum Heizen stimuliert wurden, sondern daß sie nur zu ihrem eigenen Wohlbefinden die Körpertemperatur erhöhten, und um ein Absinken ihrer Umgebungstemperatur zu verhindern. Trotzdem tragen sie durch ihre gegenüber einer Arbeiterin wesentlich größere Körpermasse nicht unbedeutend zur kolonialen Thermoregulation bei.