Endothermic heat production in honeybee winter clusters
Institut für Zoologie, Universität Graz, Universitätsplatz 2, A-8010 Graz, Austria
* Author for correspondence (e-mail: anton.stabentheiner{at}uni-graz.at)
Accepted 17 October 2002
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Summary |
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Key words: honeybee, Apis, winter cluster, heat production, endothermy, thermoregulation, thermography
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Introduction |
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The `heat entrapment model' favours the hypothesis that thermal stability
and a high core temperature (approximately 20-35°C) of broodless winter
clusters is achieved predominantly via regulation of the heat loss by
the mantle bees. The cluster is supposed to maintain a high core temperature
by the metabolism of resting or slowly moving bees alone, without additional
active heat production by `shivering' with the flight muscles
(Lemke and Lamprecht, 1990;
Heinrich, 1993
;
Myerscough, 1993
;
Watmough and Camazine, 1995
).
`Shivering' heat production by the inner bees is, if at all, assumed only at
temperatures below approximately -10°C
(Heinrich, 1993
), where the
metabolism of winter clusters begins to increase steeply as the ambient
temperature decreases (Southwick,
1988
; Moritz and Southwick,
1992
).
The more general `superorganism model' agrees with this hypothesis
concerning the important role of the insulating mantle bees but, in addition,
assumes that there are always some bees inside the cluster that actively
produce heat by `shivering' thermogenesis, the amount depending on ambient
temperature (Moritz and Southwick,
1992; Omholt and Lonvik,
1990
; Fahrenholz et al.,
1989
). We present here direct evidence of shivering thermogenesis
in the core of winter clusters.
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Materials and methods |
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In another experiment, a broodless winter cluster was thermographed day and night (1 picture s-1) from the side of the narrow ends of the combs (ThermaCam SC2000). To avoid any disturbance of the cluster, all recording equipment was placed in an adjacent laboratory, and recordings were evaluated only from night-time and two days after the experimental loggia had been entered for the last time.
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Results |
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Fig. 1 provides direct evidence of endothermic heat production by bees inside a winter cluster. In addition to many bees with no or only little endothermy, a considerable number of bees with actively heated thoraces was observed. Intense endothermy was directly visible because of the hot thorax (Fig. 1), but weak endothermy could not be judged easily because of the steep temperature gradients inside the clusters (Figs 1, 2). Therefore, we counted only bees with Tthorax at least 0.2°C higher than Thead and Tabdomen as definitely endothermic (Thead<Tthorax>Tabdomen). Most endothermic bees were located in the core (approximately 15-16% of all bees on the central comb), and their abundance decreased towards the surface (Figs 1, 3). This relationship was reversed in those bees that were assumed to primarily follow the local temperature gradient, with no or only minute endothermic heat production (Thead>Tthorax>Tabdomen; Fig. 3). Among the surface bees on the flat side of the combs, which experienced the most extreme thermal strain, 56% belonged to this latter class (Fig. 3A). Bees sitting `the wrong way round' in the temperature gradient (i.e. with the head pointing outwards to the lower temperature) were seldom on the cluster surface and in the outer ring of bees on the central comb but occurred at a higher frequency inside the cluster (Fig. 3).
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Because of the steep and variable temperature gradients inside a winter
cluster (Figs 1,
2), the amount of endothermy
cannot be estimated directly from the differences between
Tthorax and ambient or abdominal temperature. However,
comparison of the bees that were classified to primarily follow the local
temperature gradient (Class `c' in Fig.
3) with the bees classified as endothermic (Class `a' in
Fig. 3) shows that, although in
Class `c' the difference of
TthoraxTabdomen decreased
towards the core as expected, it remained nearly the same in Class `a' despite
the decreasing temperature gradients (Fig.
4). The relative proportion of bees with a
TthoraxTabdomen of >2°C
was lower in Class `a' than in Class `c' (30% versus 65%,
respectively) in the outermost bee layer, slightly higher in the intermediate
bees (36% versus 22%) but clearly higher (40% versus 14%) in
the core (relationship between Classes `a' and `c' was significantly different
among all three parts of the cluster at P<0.05, Bonferroni
2 test; compare Fig.
4). The outermost bees minimized endothermy. Strongly endothermic
bees that remained stationary, as were found in the core, were not observed on
the cluster surface nor in the outer ring of bees on the central comb (Figs
1,2,3).
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Additional (and conclusive) evidence that there is always a certain number of endothermic bees inside a broodless winter cluster at air temperatures around the freezing point was provided by the experiment where the cluster surface was thermographed continuously for many hours. Evaluation of 21 h of recordings from night-time (21:00 h-08:00 h) showed that bees appeared on the cluster surface at a rate of 6-80 bees h-1. All of them were endothermic, with a mean Thead of 21.6±3.58°C, a Tthorax of 27.5±4.09°C and a Tabdomen of 20.9±3.62°C (N=1183 values, 781 bees; compare Fig. 1). Of these bees, 90% re-entered the cluster within 10 s, and the rest re-entered within 3 min. We conclude that visiting the surface by endothermic bees is part of the natural behaviour in winter clusters.
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Discussion |
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We conclude that current models of winter cluster thermoregulation
(Lemke and Lamprecht, 1990;
Myerscough, 1993
;
Watmough and Camazine, 1995
)
that neglect the role of active (endothermic) heat production are incomplete.
The following points have to be incorporated in these models (see below).
Some of a winter cluster's bees are endothermic, and most of these bees are
located inside the cluster although these bees are not in immediate danger of
freezing or falling into chill coma. From efficiency considerations, one would
expect the bees to make the most of the heat if it is produced in the core. In
fact, most endothermic bees were located in the core (approximately 15% of all
bees on the central comb), and their abundance decreased towards the surface
(Figs
1,2,3)
and not the other way round. However, not only the probability but also the
intensity of endothermy increased with increasing local temperature in the
cluster (towards the core; Figs
1,
4). The heat of the endothermic
core bees is of benefit for the thermal comfort of themselves and
their sisters on the cluster periphery. This supports a main assumption of the
superorganism model of winter cluster thermoregulation which says that the
core bees play an active role in thermal control
(Moritz and Southwick,
1992).
Resting metabolism although higher in the core is not alone
the source of the heat that is necessary to compensate for the heat loss
(Fig. 1), because there must be
some convection in the cluster (either cyclic or permanent) that allows the
cluster to get rid of the CO2 produced
(Heinrich, 1981;
Van Nerum and Buelens, 1997
)
by both the endothermic bees through shivering thermogenesis and the
ectothermic bees according to their resting metabolism.
Southwick (1983,
1988
) and Southwick and
Heldmaier (1987
) showed that
the oxygen consumption of winter clusters increases as the ambient temperature
decreases. The increase is moderate between approximately +10°C and
-5°C and is steep below approximately -5°C to -10°C. In swarm
clusters, the steep increase has already started at +10°C
(Heinrich, 1981
). Oxygen
consumption also increases with decreasing cluster size
(Southwick, 1985
). Therefore,
the frequency and intensity of endothermic heat production have to be assumed
to increase with decreasing ambient temperature and cluster size. On the other
hand, we suggest that at higher ambient temperatures large (swarm) clusters
that have come to rest (e.g. at night) may be able to largely reduce
endothermy (Heinrich,
1981
).
If the thorax cools below the chill coma temperature of 9-11°C,
honeybees are no longer able to activate their flight muscles for heating
(Free and Spencer-Booth, 1960;
Esch, 1988
;
Goller and Esch, 1990
) and
eventually fall off the cluster. Watmough and Camazine
(1995
) assumed that the outer
bees react with thoracic heating to avoid chill coma. Efficiency
considerations, however, suggest that the surface bees should avoid endothermy
because any heat from the surface bees is immediately lost to the surrounding
air. Our data show that endothermy seldom occurs in the outer bees and, if it
does occur, is only weak (Figs
1,2,3).
Intense endothermy of surface bees was observed only in an emergency case when
only one layer of bees was left on the flat side on an outer comb. Before the
bees walked to the adjacent beeway between the combs they heated up their
thoraces. On the opposite cluster surface, where up to four layers of bees
were sitting, intense endothermy was not observed. There, the body
temperatures resembled the situation shown in
Fig. 1C (our unpublished
observations).
It should be pointed out that the occurrence of endothermy inside winter
clusters does not contradict the hypothesis of self-organized cluster
thermoregulation (Heinrich,
1981,
1993
;
Moritz and Southwick, 1992
;
Watmough and Camazine, 1995
).
It is well conceivable that the endothermic bees decide individually to start
shivering thermogenesis or to stay ectothermic. However, in order to optimize
energetic investment, the core bees should know about the thermal needs of the
bees sitting closer to the surface. Future investigations will have to solve
the question of whether or not the endothermic bees that visit the surface
play a role in the regulation of heat production in winter clusters.
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Acknowledgments |
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References |
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