Hot bees in empty broodnest cells: heating from within
1 Beegroup Würzburg, Lehrstuhl für Verhaltensphysiologie und
Soziobiologie, Universität Am Hubland, D-97074 Würzburg,
Germany
2 Institut für Bienenkunde (Polytechnische Gesellschaft), FB Biologie
der J. W. Goethe-Universität Frankfurt am Main, Karl-von-Frisch-Weg 2,
D-61440 Oberursel, Germany
* Author for correspondence (e-mail: thermo{at}biozentrum.uni-wuerzburg.de)
Accepted 22 August 2003
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Summary |
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Individually marked worker bees on the surface of sealed brood cells maintained thorax temperatures (Tth) between 32.2±1.0°C and 38.1±2.5°C (mean ± S.D.; N=20 bees) with alternating warming and cooling periods. Most of the observed bees made one or several long-duration visits (>2 min) to empty cells within the sealed brood area. Tth at the time bees entered a cell [Tth(entry)] was 34.142.5°C (N=40). In 83% of these cell visits, Tth(entry) was higher (up to 5.9°C; mean 2.5±1.5°C; N=33) than the mean Tth of the same bee. High values of Tth(entry) resulted from preceding heating activity on the comb surface and from warm-ups just prior to cell visits during which Tth increased by up to +9.6°C.
Bees inside empty cells had mean Tth values of 32.7±0.1°C (resting bees) to 40.6±0.7°C (heat-producing bees) during long-duration cell visits without performing any visible work. Heating behaviour inside cells resembles heating behaviour on the brood cap surface in that the bees appear to be inactive, but repeated warmings and coolings occur and Tth does not fall below the optimum brood temperature.
Bees staying still inside empty cells for several minutes have previously been considered to be `resting bees'. We find, however, that the heating bees can be distinguished from the resting bees not only by their higher body temperatures but also by the continuous, rapid respiratory movements of their abdomens. By contrast, abdominal pumping movements in resting bees are discontinuous and interrupted by long pauses.
Heat transfer to the brood from individual bees on the comb surface and from bees inside empty cells was simulated under controlled conditions. Heating on the comb surface causes a strong superficial warming of the brood cap by up to 3°C within 30 min. Heat transfer is 1.92.6 times more efficient when the thorax is in touch with the brood cap than when it is not. Heating inside empty cells raises the brood temperature of adjacent cells by up to 2.5°C within 30 min. Heat flow through the comb was detectable up to three brood cells away from the heated thorax.
Key words: honeybee, Apis mellifera carnica, thermoregulation, heat transfer, brood, comb
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Introduction |
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If the brood-rearing temperature deviates from the optimum
3336°C range for longer periods, malformations and mortality of the
brood increase (Himmer, 1927,
1932
;
Muzalewskij, 1933
;
Weiss, 1962
). After emergence,
the behavioural performance of worker bees is reduced if rearing temperature
during pupal stage was in the lower range
(Tautz et al., 2003
).
Very little is known about how individual bees in the brood area contribute
to the stability of brood nest temperature. Harrison
(1987) found that most bees in
a colony contribute to colonial heating in that they maintain a thorax
temperature (Tth) above local ambient temperature.
However, not all bees contribute equally, and variation of up to 12°C
among individuals can be found (Harrison,
1987
). Using chronically implanted thermocouples, which allow the
combination of behavioural observations with continuous long-term temperature
measurements of individual bees, Esch
(1960
) identified worker bees
that specialized in the activity of brood nest warming. Such bees sit
motionless on the surface of brood cells while maintaining a
Tth above 35°C with intermittent warming and cooling
and without performing any other work during this time. Schmaranzer et al.
(1988
) have confirmed these
findings with non-invasive methods. Endoscopic and thermographic observation
of individual bees by Bujok et al.
(2002
) showed that
brood-heating individuals often press their warm thoraces firmly onto the caps
of sealed brood cells while staying motionless, thereby enhancing heat
transfer to the brood by means of conduction. Heat transfer from such bees to
the brood left a `hot spot' in the thermographic image at the place where
these bees had previously been sitting.
Our initial setup was designed to learn more about the long-term temperatures and behaviour of individual worker bees that are engaged in brood incubation. The results unveiled a remarkable, hitherto unknown behaviour of the honeybee and directed our interest to an elusive aspect of thermoregulation in its colonies: in the present work, we describe a series of observations showing that seemingly resting bees inside empty cells participate in the regulation of brood temperature and serve as a heat source for neighbouring sealed brood cells. Using an infrared-sensitive thermovision camera and a modified brood nest that allowed us to monitor all events inside empty cells between sealed brood cells, we investigated the behaviour and the thorax temperature of individual bees before and after visits to empty cells, during their stay inside empty cells and the participation of cell-visiting bees in broodnest warming. Different modes of heat transfer from worker bees to the brood were simulated under controlled conditions and allowed us to detect heat transfer from cell visitors to the adjacent brood even in a populous observation hive.
We find that many bees that are apparently resting inside empty cells in the brood comb are participating in the regulation of brood temperature by serving as a heat source for the neighbouring, sealed, brood cells. This hitherto unrecognised thermal activity of bees inside cells is remarkable because long-duration cell visitors were previously considered to be resting and also because heat production inside cells provides a way to transfer heat to the brood more efficiently than heating via the brood caps.
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Materials and methods |
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Measurement of thorax temperatures
Thorax surface temperatures (Tth) of worker bees were
measured by remote sensing thermography. A real-time infrared-sensitive camera
(Radiance PM 1/1.5.1b; waveband 3.55.6 µm; accuracy
±0.7°C; Raytheon-Amber, Goleta, CA, USA) allowed the simultaneous
measurement of the temperatures of many bees without disturbing them. A 19 mm
extension tube was used for close-up recordings of individual bees inside
cells. Absolute temperatures were calculated by the camera's internal software
using the emissivity value (e=0.97) of the bee's thorax
(Stabentheiner and Schmaranzer,
1987) and were encoded as an eight-step greyscale in the image.
Single infrared images were relayed to a computer and were analysed with
camera-specific software (AmberTherm v1.28). The attenuation of thermal
radiation by the plastic film was compensated during analysis using the
Tth values of dead, artificially heated bees, which were
measured in a different setup with and without the film in place.
Setups A and B: temperature and behaviour of worker bees
Setup A: thoracic temperature of bees on the brood comb surface prior
to cell visits
This setup was designed for temperature measurements of bees on the surface
of brood cells before and after cell visits. A common observation hive with
two combs standing on top of each other
(von Frisch, 1965) was used.
During a period of 7 weeks prior to the observation, 3500 worker bees (reared
at 35°C from brood combs in an incubator), all with individual colour
marks on their abdomen (Kleinhenz and
Tautz, 2003
), were introduced into the colony. A 10 cmx11 cm
piece of brood comb was set into the centre of the upper comb 9 days prior to
the observation, allowing the larvae to develop to sealed stage. During the
observation, room and hive temperatures (Troom and
Thive, respectively) were measured every 15 min with
NiCrNi thermocouples connected to a digital twin thermometer (Voltcraft
502; Conrad electronic, Hirschau, Germany). Thermocouples were not placed in
the brood area itself because they impeded the movement of the bees across the
comb. Thive outside the brood area (7.5 cm from the centre
of the comb) was 30.4±0.3°C at a Troom value of
22.3±0.3°C.
Observations were made from 05:30 h to 07:10 h (CEST). The brood area was
videotaped (Panasonic AG-7350 and AG-5700) continuously during the observation
period with the thermovision camera and a synchronized standard video system
to identify individual bees by their colour codes. 20 bees were followed as
long as they were visible in the brood area (491 min per individual;
mean ± S.D., 39.0±26.5 min; total time 780 min).
Tth was measured at least five times per minute and
immediately before [Tth(entry)] and after
[Tth(exit)] cell visits. Short cell inspections (<2
min) were not noted. Net temperature differences during a cell visit were
calculated as
(Tth)net=Tth(exit)Tth(entry).
All Tth values were obtained from bees inside the brood
area, although walking bees may also come across empty cells (scattered
between the sealed brood cells) at the time when Tth was
measured.
Setup B: thoracic temperature of bees inside empty cells
Since only the tip of the abdomen of bees inside comb cells is visible in
common observation hives, it was necessary to use a different setup
(Fig. 1): the queen, 1500
worker bees and three comb pieces (A, B and C; each 17 cmx4 cm) were
obtained from a 10-frame hive. The comb pieces were cut out of a storage comb
(piece A) and a mixed brood/storage comb (pieces B and C) and placed in a
small observation hive with the centre wall of the comb perpendicular to the
front window (Fig. 1). This
allowed the interior of the first cell in each row to be seen through the
infrared-transparent front cover (Fig.
1). These cells are referred to as `observation cells'. Bees were
allowed 2 days to settle before observations started. Air temperature inside
the hive between brood combs (Thive; see
Fig. 1) and
Troom were measured with thermistors (accuracy
±0.1°C) connected to a digital data logger (Almemo 2290-8; Ahlborn,
Holzkirchen; Germany) and were recorded every 2 s.
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Close-up thermographic recordings of three observation cells adjacent to the sealed brood (Fig. 2) provided us with data on individual bees during cell visits. Individual bees could be resolved until they left the camera's field of view (Fig. 2). During a 130 min observation period (10:30 h to 12:40 hCEST), the Thive value was 33.2±0.6°C at the Troom value of 23.1±0.3°C. Tth of worker bees inside the observation cells was measured every 15 s. Only cell visits of >2 min were considered.
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The respiratory pumping movements of the abdomen of bees lying still were recorded from the videotapes using computer software (The Observer 3.0; Noldus Information Technology, Wageningen, The Netherlands), which allowed registration of pumping movements up to 3 s1.
On three consecutive days, bees in a total of 84104 observation
cells in the central part of the combs were thermographed simultaneously to
investigate the bee temperatures in different regions of the hive. Two types
of observation cells were defined. Type 1: observation cells adjacent to and
sharing at least one common cell wall with a sealed brood cell during the
whole observation period. Type 2: observation cells adjacent to non-brood
cells during the whole observation period. Observations were made daily from
7:30 h to 9:10 h (CEST) at ambient conditions (Troom and
Thive), as given in
Table 1. Every 5 min during
these 100 min observations, the Tth values of all bees in
cells were measured from infrared images that were relayed to a computer. Data
were analyzed using a one-tailed KolmogoroffSmirnoff test
(Bortz et al., 2000). The
Tth values of bees visiting type 1 observation cells
(adjacent to brood cells) were tested separately for brood combs B and C and
for each of the three observation days.
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Setups C and D: heat transfer from worker bees to the brood
How do bees inside cells and bees on the comb surface contribute to the
temperature of brood cells? We used two different set-ups to answer this
question. First (setup C), we simulated worker heating under controlled
conditions to determine the extent and rates of warming in the adjacent brood
cells. Second (setup D), we recorded brood cell temperatures in a common
observation hive and analysed them with regard to the presence of cell
visitors in the adjacent cells.
Setup C: simulation of worker heating
This setup was used to simulate worker heating with an artificially heated
thorax and to measure its influence on the temperature of nearby brood cells.
A brood comb was kept inside an incubator (B 5042; Heraeus, Hanau, Germany)
and thermistors for measurement of Tbrood were implanted
in the bottom of three neighbouring sealed brood cells
(Fig. 3). The thermistors were
inserted from the back of the comb without damaging the caps of the
investigated brood cells. Cells on the back of the comb that had been emptied
to access the cell ground were later re-filled with a dead bee to substitute
the brood and were closed with drops of beeswax. In some cases, we also
measured the temperatures just beneath the brood caps
(Tcap) near the comb surface
(Fig. 3). To leave the pupae
and brood caps intact, we inserted these thermistors through the caps of
neighbouring cells and guided them to the investigated brood cells through
small perforations in the common cell walls
(Fig. 3).
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The initial brood cell temperature (Tbrood) before artificial heating started varied slightly on different days and in different combs but was kept in a narrow range from 32.8°C to 33.9°C in all cases. Regulatory oscillations of the air temperature inside the incubator (up to ±0.40°C; period length 1424 min) were buffered widely by the surrounding mass of comb and brood: when no simulation was conducted, Tbrood in the comb's core was constant within ±0.10°C of the given level for periods up to 24 h.
We confined our simulation to the thorax, since it is the major heat
source: in living honeybees, heat flow to the abdomen is greatly reduced by a
countercurrent heat exchanger in the narrow petiole region, which conserves
heat in the thorax (Heinrich,
1979,
1993
;
Heinrich and Esch, 1994
) and
keeps the abdominal temperature near ambient level (see Figs
2,
5;
Stabentheiner and Schmaranzer,
1987
; Stabentheiner and
Hagmüller, 1991
). A small resistor, about the size and mass
(M=29 mg) of a bee's thorax, served as a heat source. The resistor
was placed inside the isolated thorax of a dead bee to mimic its heat exchange
properties. Internal Tth beneath the cuticle was measured
with a thermistor and may be 1°C higher than the corresponding surface
temperatures (Stabentheiner and
Schmaranzer, 1987
). During simulation, the thermistor values
(Tbrood, Tcap and
Tth) were read at a resolution of 0.01°C and were
stored automatically every second (Almemo 2290-8). Each heating cycle lasted
30 min, a time-span covering the mean duration of long cell visits
(1015 min) and most of the longest, non-interrupted cell visits that
were found in the previous experiments (Tables
2,
3). Controlled heating of the
thorax was achieved by applying constant voltage to the resistor. Using data
from Tables 2 and
3, we simulated
Tth from 35.2±0.4°C to 41.7±0.9°C
(mean ± S.D. during the whole heating cycle).
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In different cycles, we varied the location of the thorax to simulate three basic behavioural patterns involving different modes of heat transfer (radiation and conduction) to the brood.
Variation A. The thorax was inside an empty cell adjacent to one of the brood cells that contained a thermistor. This arrangement simulated long-duration cell visits of heating bees as described in the present study (setups A and B). The thorax was placed near the bottom of the empty cell, since bees enter comb cells with their head and thorax first (Figs 2, 3).
Variation B. The thorax was located on the comb surface and its
ventral side touched the brood cap. This behaviour can be observed in worker
bees that are engaged in a special brood-heating activity
(Bujok et al., 2002). Such bees
stay motionless while producing heat without doing any other work during this
time (Esch, 1960
;
Schmaranzer et al., 1988
).
Bujok et al. (2002
) reported
that such bees take a characteristic, crouched body posture for several
minutes and contact the brood cap by pressing their heated thorax against
it.
Variation C. As for variation B, but the thorax did not touch the
brood cap. From endoscopic inspections of working and walking bees
(Bujok et al., 2002) and
observations at oblique angles in hives with transparent covers, we estimated
a distance of 1.01.5 mm between the thorax and brood cap. Greater
distances may occur but were found mainly in resting bees in the periphery of
the comb (Kaiser, 1988
;
Kaiser et al., 1996
) and were
not simulated.
Setup D: brood cell temperatures and cell visitors within a
colony
Can heat transfer from cell-visiting worker bees to the adjacent brood also
be detected in populous colonies where many individuals contribute to the nest
climate? As shown by the simulation experiment (results of setup C), the
implantation of thermoprobes at the bottom of brood cells for measurements of
Tbrood is suitable to assess this question: due to their
great distance to the probe (1114 mm), there is only slight
interference from heating bees on the comb surface, whereas the thoraces of
cell visitors are close (45 mm) and cause significantly higher warming
rates (Table 4). Furthermore,
fluctuations of local Thive are buffered by the
surrounding mass of brood and comb (see setup C).
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A common observation hive with two combs standing on top of each other was
established from a 20-frame colony 8 days before the observation started. To
control the size and location of the brood area, we inserted a rectangular
piece of brood (11 cmx11 cm) from the original colony into the
centre of the upper comb. Both sides of the hive were covered with a plate of
Perspex (0.5 cm), each containing a 20 cmx10 cm `window' made of plastic
film in the centre of the upper comb, and were thermally insulated (
5
cm). On the observation side of the hive, part (20 cmx10 cm) of the
insulation was removed during the observation to view the bees in the brood
region through the plastic film and to determine their Tth
by contactless thermography as described above.
Investigations on brood temperatures and cell visits were done in an area
of 6x8 comb cells (referred to as `area of interest') containing
empty cells and sealed brood. Five sealed brood cells, each of them surrounded
by 46 empty cells, were equipped with temperature probes at the cell
bottom for the measurement of Tbrood. The probes (two
thermistors and three thermocouples) were inserted from the back of the hive
into the interior of the brood cells. This left the brood comb surface and
brood caps on the observation side undamaged, and the movement of bees was not
impeded by wires. The location of the probes was the same as in setup C (brood
cell #1 in Fig. 3) to allow
comparison with data obtained from the simulation.
A special construction on top of the hive (referred to as the `cell-finder'; not shown) allowed us to select a certain brood cell on the observation side of the hive and to find the corresponding position on the opposite side of the comb. The cell-finder consisted mainly of a solid log with two parallel arms projecting downwards on both sides of the hive. Two thin steel pointers (diameter 1 mm; one pointer at the end of each arm) pointed inwards to the same position but on different sides of the comb. The whole construction was movable along the top of the hive and its height could be adjusted to point at any position within the brood area. The cell-finder was essential for orientation on two sides of a comb within a hive, because the bottom of each cell is formed by parts of three cells on the opposite side of the comb, and consecutive rows of cells are shifted half a cell diameter to match the hexagonal shape of the cells. After finding the corresponding position, one pointer was used to penetrate the plastic film on the back and to make a small hole in the bottom of the selected brood cell. The tip of the temperature probe was then implanted in the brood cell and the wires were fixed with tape. At the end of the experiment, the probes were pushed forward through the brood caps to confirm their position in the selected cell.
Data collection and analysis
During a 3-hour observation period (7:20 h to 10:20 hCEST), we investigated
the temperatures of the five sealed brood cells and the visits of worker bees
to the adjacent empty cells. For each visit, we noted its duration,
Tth(entry) and Tth(exit) from our
real-video recordings and from the thermographic images. Short cell
inspections (<2 min) were not considered. For control purposes, the thorax
temperatures of bees on the comb surface inside the area of interest were
measured from the thermographic images every 2.5 min. The behaviour of the
warmest bees (Tth36°C) was observed ±2 min
from the time of measurement to see whether these bees were roaming around or
standing motionless at a certain location for longer periods.
Thermistor values were recorded automatically every second (Almemo 2290-8). The thermocouples were connected to digital thermometers that provided no storage function. We recorded their displays continuously with a videocamera and later the values were read from the tapes every 15 s. Additional thermocouples measured Thive in the brood area and Troom outside the hive.
The brood cell temperatures were analysed in two ways. First, we
investigated whether the presence or absence of cell visitors had any
influence on Tbrood at all. Therefore, the temperature
recordings of each brood cell were classified according to the number of
long-duration cell visitors (Nvisitors) currently
occupying the empty cells adjacent to this brood cell. The first 1.5 min after
a change of Nvisitors were not included to allow the brood
temperature to change to a noticeable extent
(Table 4). The experimental
conditions (Troom=26.0±0.7°C; partial removal
of the insulation) ensured that brood warming rather than brood cooling was
necessary to keep the brood temperature in the optimum range of
3336°C. Since cell visitors may transfer heat to the brood and
raise its temperature (results from setups AC), we hypothesized that
Tbrood increases with Nvisitors.
Jonckheere's trend test (Bortz et al.,
2000) was used to analyze the datasets for each brood cell.
Second, we investigated whether heat transfer from individual cell visitors
to the brood is also detectable in this intact colony with many living bees.
Results from the simulation experiment (setup C) proposed that cell visitors
with high Tth (>36°C) increase the temperature of
the adjacent brood cell at rates that are significantly higher (0.2 deg.
min1) than the rates that are caused by bees on the comb
surface, even if they press their thoraces on the comb and enhance heat
transfer by means of conduction (Table
4). However, the Tth of cell visitors is not
known in a common observation hive and may vary during long-duration cell
visits (setups A, B). Therefore, we focussed on those bees that already had
high Tth when they entered a cell
[Tth(entry)
36°C] and we analysed the changes of
Tbrood within the first 2 min after the start of these
cell visits.
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Results |
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16 of the observed bees made a total of 42 visits to empty cells surrounded by sealed brood cells. Visit duration ranged from 0.7 min to 32.9 min (mean 9.7±7.8 min; total time 369 min; N=38 completely recorded cell visits).
Repeated measurements of Tth over a period of at least 0.5 min allowed the detection of changes in the thermal behaviour of individual bees. This was possible prior to 27 cell visits with observation times ranging from 0.9 min to 43.0 min (10.0±9.4 min; N=27) before these bees entered a cell. In other cases, the bees were visible on the comb surface for only a few seconds between consecutive cell visits and allowed only single temperature measurements to be taken. Most bees raised their thoracic temperatures before entering a cell (Fig. 4) by values between +1.1°C and +9.6°C (mean 4.2±2.5°C; N=22 of 27 cell entries) during warming periods of 0.4 min to 4.9 min (mean 2.1±1.1 min; N=22). Cell visits occurred when the bees were still increasing their temperature or shortly after reaching the highest Tth of a warming cycle, providing Tth(entry) values up to 42.5°C (Table 2). In 83% of all cell visits, Tth(entry) was higher (up to 5.9°C) than the mean Tth of the same bee during the whole observation period (Table 2).
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Thorax temperatures at the end of cell visits
[Tth(exit)] ranged from 34.3°C to 40.9°C
(Table 2). Individual bees
showed net temperature changes
[(Tth)net] during cell visits over a
range of 4.4°C to +4.1°C (N=38).
With this setup, Tth could not be recorded during cell
visits. However, the onset of heat production during long-duration cell visits
was suspected from the positive (Tth)net
values of some cell visitors and when the interior of the visited cell started
`glowing' conspicuously in the thermographic image with increasing and varying
intensity (Fig. 5).
Consequently, setup B was designed to provide more precise information about
the Tth during cell visits.
Setup B: thoracic temperature of individual bees within the
cells
16 bees visited at least one of the three observation cells that were
monitored with the close-up camera and remained within this cell for more than
2 min. Individual bees visited the same cell for periods ranging from 2.8 min
to >63 min but with short interruptions when the bees exited and then
re-entered the cells (Table 3).
The longest stay without interruption was 33.8 min. The
Tth values of the 16 bees ranged from 32.2°C to
41.7°C.
Three of the 16 bees showed vigorous body movements inside the cell, repeatedly moving forwards and backwards, turning around their longitudinal axes and applying their mandibles to the cell walls. These three individuals were considered to be `working' (Table 3).
The remaining 13 bees lay still inside the observation cells, except for a few seconds after entering or before leaving the cell. Five of these 13 bees exhibited low and almost constant Tth values ranging from 32.7±0.1°C to 33.4±0.3°C and were regarded as resting (`resting bees' in Table 3; Fig. 6D; visitor to cell `y' in Fig. 2B). Short bursts of pumping movements of their abdomens were interrupted by long pauses of up to 58 s (Fig. 7A,B).
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Eight of the 13 still bees maintained high (but not constant)
Tth during most of the cell visit (`heat-producing bees'
in Table 3; Fig. 6AC;
Fig. 2A).Individual
Tth during cell visits varied in the range of 2.1°C to
6.6°C (mean 4.2±1.6°C; N=8 bees) with intermittent
cooling and heating periods. During the longest visits,
Tth sometimes dropped several degrees but did not fall
below 34.5°C before increasing again. Tth(entry) of
these eight bees ranged from 34.4°C to 40.3°C (mean
38.3±1.6°C; N=11 cell entries of eight bees). Three bees
allowed longer temperature measurements before entering a cell and showed
warm-ups (+2.9°C in 1.5 min and +3.3°C in 1.5 min) or high, rather
stable Tth values (39.4±0.5°C for 2 min). Net
temperature differences [(Tth)net] at
the beginning and at the end of cell visits ranged from 2.7°C to
+3.9°C (Table
3;Fig.
6AC).
Bees with high Tth showed rapid, almost continuous respiratory pumping movements of the abdomen (Fig. 7C),which frequently exceeded 3 s1 in bees with the highest Tth (>38°C).
Thoracic temperature of bees visiting cells outside the brood
area
Tth values of bees visiting cells adjacent to storage
or empty cells outside the brood area were lower than the mean
Tth values of bees visiting cells adjacent to brood. The
differences between the Tth values of these two groups of
bees were, with one exception, statistically significant on all observation
days (Table 1).
Setup C: simulation of worker heating
The presence of a heated thorax in an empty cell adjacent to or on the cap
of a sealed brood cell caused clearly detectable warmings that were continuous
throughout the heating cycle (Table
4). The extent and rate of warming depended on the
Tth that was applied, on the location of the thorax
(variations A, B and C) and on the location of the thermistors at the cell
bottom (Tbrood) or beneath the cap
(Tcap). Details are presented below and in
Table 4. Generally, warming
rates inside the brood cell were highest at the beginning and declined during
the simulation.
Variation A: location of the thorax inside an empty cell
Heating from inside an empty cell clearly raised the temperature of the
surrounding brood up to three cells away from the heated thorax. Within a 30
min period, the temperature of brood cell #1
(Fig. 3) increased by values of
up to +2.5°C at maximum warming rates of 0.5 deg. min1
(Table 4). At the end of the
heating cycles with Tth values of 35.2°C, 36.3°C,
38.6°C and 41.7°C, the Tbrood of brood cell #2 had
been raised by values of 0.32±0.03°C, 0.41±0.07°C,
0.75±0.05°C and 1.14±0.04°C, respectively (data not
shown in Table 4; final values
at t=30 min, mean ± S.D. from 34 cycles
each), at warming rates of up to 0.1 deg. min1. At the same
time, the temperature of brood cell #3 increased by values of
0.14±0.02°C, 0.16±0.04°C, 0.30±0.03°C and
0.45±0.03°C at warming rates of <0.05 deg.
min1.
Variations B and C: location of the thorax on the comb surface
The presence of a heated thorax on the brood cap raised
Tcap by up to 3.0±0.5°C within 30 min. The
maximum warming rates (MWR) and Tcap values
indicate that heat transfer to the brood cell was 1.92.6 times more
efficient when the thorax touched the brood cap (variation B) than when it was
11.5 mm away (variation C; Table
4). Differences between variations B and C were significant
(Tth=39.8°C; one-tailed Wilcoxon, MannWhitney
U-test; Sachs, 1999
;
P<0.05 for each test of
Tcap at
t=2, 5, 10 and 30 min and for the maximum warming rates).
The changes of Tbrood at the cell bottom are important with regard to setup D because they determine the extent of `interference' from worker bees on the comb surface. Warming rates of Tbrood of up to 0.15 deg. min1 may be caused by thoraces on the comb surface (Tth up to 40.3±0.7°C; Table 4) and by thoraces inside cells with Tth<36.3±0.4°C (one-tailed Wilcoxon, MannWhitney U-test, P>0.05, not significant).
Thoraces inside cells with Tth36.3±0.4°C
caused significantly higher warming rates (MWR 0.19±0.01 deg.
min1 to 0.52±0.03 deg. min1) than
the warmest thoraces on the comb surface
(Tth=40.3±0.7°C), even when the latter ones
touched the brood cap and heat transfer was enhanced by means of conduction
(one-tailed Wilcoxon, MannWhitney U-test,
P<0.05).
Tbrood of the remote brood cells #2 and #3
(Fig. 3; final values at
t=30 min; data not shown in Table
4) was raised by 0.50±0.09°C and
0.38±0.13°C, respectively, when the thorax was in touch with the
brood cap (Tth=40.3±0.7°C; N=5) and by
values of 0.33±0.10°C and 0.22±0.07°C, respectively,
when it did not touch it (Tth=40.1±0.8°C;
N=7). Warming rates were 0.05 deg. min1 in all
cases.
Setup D: cell visits and temperatures of adjacent brood cells
During a 3 h observation period at
Troom=26.0±0.7°C and
Thive=32.3±0.6°C, the temperatures of the five
investigated brood cells were maintained well in the optimum range for brood
development at 33.6±0.6°C (coolest cell) to 35.1±0.3°C
(warmest cell) (Table 5).
Tbrood never fell below 32.6°C (measured in the
outermost cell) and was repeatedly raised up to 35.9°C. In different
cells, warmings and coolings frequently occurred simultaneously
(Fig. 8).
|
|
Bees on the comb surface
At any time during the observation, the comb surface in the `area of
interest' (6x8 cells) was covered by 616 bees (11.4±2.1
bees) with Tth values ranging from 31.1°C to
42.8°C (830 values from 73 still images; mean Tth per
image was 32.7±0.8°C to 35.2±1.4°C). The behaviour of
bees with Tth36.0°C (N=56) was
investigated more closely to check for possible influence on the warming rates
of Tbrood (Table
4, variations B and C). The majority of these bees were present
only for a short time on the comb surface in the investigated area: 10 bees
were crossing the area of interest while roaming around in the brood area
without standing still at a certain location. Eight bees were present on the
comb surface only for a few seconds during short interruptions of a cell visit
(setups A, B) or between consecutive cell visits to different cells. 34
records of Tth
36.0°C were obtained from bees that
either had been visiting or were about to visit an empty cell within ±2
min of the time when we recorded their temperature and thus were no longer
present on the comb surface. Six bees (including two bees that finally entered
a cell) were standing motionless for at least 0.5 min in the area of interest,
on or near the investigated brood cells (duration of immobility: 0.54.9
min; mean ± S.D. 2.4±1.9 min; N=6).
Cell visitors
A total of 98 long-duration cell visits with visit durations from 2.2 min
to 46.6 min (mean 14.9±10.7 min; N=92 completely recorded cell
visits) to the empty cells adjacent to the brood were observed. During most of
the time, 13 empty cells adjacent to a certain brood cell were occupied
simultaneously by cell visitors (Table
5). The increase of Tbrood with the number of
cell visitors (Nvisitors) was highly significant
(Jonckheere's trend test, P<0.001 for each of the five
investigated cells).
The thorax temperatures of the cell visitors were consistent with those
from the other experiments (setups A, B), indicating previous heating activity
on the comb surface before entering the cell and heat production during the
long-duration cell visits: Tth(entry) values ranged from
33.0°C to 41.9°C, and Tth(exit) values ranged from
33.3°C to 40.0°C. The (Tth)net
of these bees ranged from 4.9°C to +5.3°C.
Changes of Tbrood within two minutes of the
disappearance of warm bees (Tth36°C) into one of
the adjacent empty cells were investigated in detail [N=73 cell
visits with Tth(entry) from 36°C to 42°C]. In 81%
of these visits, heat transfer from the cell-visiting bees to the brood was
detectable as an increase in the warming rate of Tbrood by
at least +0.2 deg. min1 shortly after the start of the cell
visit (delay: 25.1±18.8 s; N=59). The warming rates changed
from 0.0±0.2 deg. min1 just prior to the cell visit
to maximum values of 0.5±0.3 deg. min1 within the
subsequent 2 min period (N=59). The differences were statistically
significant (Student's t-test, paired samples, P<0.001).
In the temperature recording (Fig.
8), these visits usually marked a change to stable
Tbrood>Thive from a previous
cool-down cycle (i.e. warming rates of <0 before the beginning of a cell
visit) or they marked a change to a warm-up cycle from previously stable
Tbrood or from a previous cool-down cycle. The highest
warming rates were detected when two or three empty cells adjacent to the same
brood cell were visited simultaneously or within a short time (<2 min) by
two or three bees with Tth(entry)
36°C or when the
beginning of a cell visit coincided with a warm-up cycle that was caused by
other bees (warming rate of >0 at the start of a cell visit), thereby
increasing the warming rate to up to 1.5 deg. min1.
In 19% of the cell visits (N=14), no influence on Tbrood or only a faint increase in the warming rate of the adjacent brood cell could be detected (<0.2 deg. min1), suggesting that these bees temporarily stopped or reduced heat production after entering the cell. The brood temperatures at the beginning of these cell visits were already well in the optimum range for brood development (Tbrood=35.1±0.6°C; N=14), i.e. further warming was not essential at that time, and were significantly higher than in those cases where we subsequently noted an increase in the warming rate (Tbrood=34.4±0.6°C; N=59; two-tailed Wilcoxon, MannWhitney U-test, P<0.01).
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Discussion |
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---|
Our observations show that some of the bees that undertake long-duration
cell visits are engaged in heat production whereas others are indeed resting.
Both heating and resting bees lie quietly inside cells but the heating bees
maintain a Tth above Thive whereas the
resting bees do not. However, they can be distinguished from each other by
their abdominal respiratory pumping movements, which are discontinuous with
long breaks in resting and sleeping bees
(Fig.
7A,B;Kaiser, 1988;
Kaiser et al., 1996
) but rapid
and continuous in heating bees (Fig.
7C), implying high rates of respiration
(Bailey, 1954
;
Fraenkel, 1932
;
Heinrich, 1972
). Similar
continuous and rapid respiratory movements have been described for various
insects during warm-up before flight
(Heinrich, 1993
;
Krogh and Zeuthen, 1941
;
Sotavalta, 1954
) and for
brood-incubating hornets (Vespa crabro;
Ishay and Ruttner, 1971
) and
bumblebees (Bombus spp.), where conspicuous differences in the
abdominal pumping movements of resting and heating individuals also occur
(Heinrich, 1972
). It should be
stressed, however, that the abdominal movements must be observed for some
minutes to detect long respiratory breaks that characterize the resting bees.
Otherwise, a resting bee could be mistaken for a heating bee at the time when
bursts of pumping movements occur (see Fig.
7B,C).
Net temperature changes during cell visits
Cell visitors may have high Tth(entry) due to preceding
heating activity on the brood cap surface immediately prior to a cell visit.
If the bees that enter the cells do not continue to generate higher than
normal body temperatures they would simply cool down to the ambient
temperature of the brood, which would gain relatively little heat in the
exchange.
The calculation of (Tth)net values
was helpful at an early stage of this work when the Tth of
bees in a common observation hive were investigated. The onset of heat
production of bees inside cells was clearly indicated when net warmings with
(
Tth)net>0 (up to +4.1°C; Figs
4B,
6A; Tables
2,
3) were found, although the
amount of heat transferred to the brood comb cannot be calculated from this
value. The occurrence of intermittent cooling and heating periods during long
cell visits reduces the usefulness of the
(
Tth)net values.
During detailed observation of individual bees inside empty cells
(Table 3;
Fig. 6), the
Tth values of these bees were in a range of 9.5°C
(32.241.7°C). Highest values of
|(Tth)net| would be
expected if Tth(entry) is close to one extreme of this
temperature range and Tth(exit) is on the other extreme,
i.e. if a bee changes its behaviour from resting to heating or vice
versa. However, the
|(
Tth)net| values we
measured were small (up to 3.9°C) in comparison with the total range of
9.5°C that might have been found under the experimental conditions. This
was because the Tth(entry) values were usually between
these extremes due to preceding heating activity on the comb surface and
because the Tth values of heating bees inside cells varied
individually only within a range of 2.16.6°C and did not drop down
to the level of resting bees.
Despite repeated cooling and warming during long cell visits, the
(Tth)net may not be detected at all if
only Tth(entry) and Tth(exit) are
known. This is clearly shown in Table
3, where Tth of two bees varied in a range of
5.3°C and 4.6°C during their cell visits, but
Tth(entry) and Tth(exit) were similar
and almost no net temperature changes were detected
[(
Tth)net values between
0.4°C and +0.3°C; see Table
3, y1 and z5; Fig.
6B]. Especially during long cell visits, intermittent heating
activity of a bee may be masked if an apparent cooling occurs, i.e.
(
Tth)net<0
(Table 3, y2, y5, z5, z7).
Likewise, the detection of (
Tth)net>0
does not imply that heat production was continuous throughout the cell visit.
This finding is relevant for our observation of bees on the comb surface in a
common observation hive (Table
2 and setup D) where only Tth(entry) and
Tth(exit) could be measured.
Heating behaviour inside cells
Why do bees with elevated Tth enter empty cells in the
brood area and maintain high Tth during their long cell
visits without performing any visible work? Resting or sleeping bees do not
maintain high Tth values and their body temperatures are
at ambient levels (Kaiser,
1988). The eight `still' bees whose thoracic temperatures we
measured inside cells were obviously not resting since they were engaged in
heat production during most of the time. It is known that honeybee workers on
the comb surface produce heat to warm their brood
(Esch, 1960
;
Harrison 1987
;
Kronenberg and Heller, 1982
;
Schmaranzer et al., 1988
;
Bujok et al., 2002
) and to keep
it in a temperature range that is optimal for development (Himmer,
1927
,
1932
;
Muzalewskij, 1933
;
Weiss, 1962
). The observation
cells in which we found heating bees were directly adjacent to sealed pupae
cells, which leads us to propose that bees with high Tth
are warming the pupae in the adjacent cells. Due to their high
Tth(entry) and the maintenance of high
Tth during cell visits, these bees are a potential heat
source for the neighbouring brood. This strategy provides a way to transfer
heat from workers to the brood nest in addition to that achieved by workers on
the brood cap surface. The transfer of heat from worker bees to the brood
during long-duration cell visits has to be expected due to the temperature
gradient between the heated thorax and the surrounding cells and was clearly
detectable during our simulation experiment and in an intact colony in an
observation hive. A similar cell-visiting behaviour adjacent to sealed brood
is known for wasps that rear their brood in paper nests with a similar cell
arrangement (Ishay, 1972
).
Heat transfer to adjacent brood
Heat transfer from individual cell visitors to the brood was simulated with
setup C and could also be detected in most cell visits of bees with a
Tth(entry)36°C in setup D. Not all prominent
warmings of Tbrood occurred within 2 min of the start of
these cell visits. This is because long-duration cell visitors may stop and
resume heating at any time during their stay inside a cell (setup B), and,
during 70.488.1% of the observation time of setup D, there were two or
more cell visitors simultaneously occupying empty cells that were adjacent to
a certain brood cell (Table 5,
Nvisitors
2). Although the Tth of
long-duration cell visitors are not known in a common observation hive and
cannot be estimated from their Tth(entry) and
Tth(exit) values [see discussion of the
(
Tth)net values], there is some
indication that the prominent warmings of the investigated brood cells were
caused mainly by bees inside empty cells rather than by bees on the comb
surface. First, bees on the comb surface are further away from the
Tbrood probe and cause significantly lower warming rates
at the cell bottom, even if they touch the brood caps with their thorax and
enhance heat transfer by means of conduction
(Table 4). The temperatures of
most bees on the comb surface were in a range that was covered by the
simulation parameters (Tth in
Table 4). Although heat
transfer from such bees could be detected with our methods, they may not
account for the unusual high warming rates at the cell bottom (up to +1.5 deg.
min1). Second, most of the bees with
Tth
36°C were present for only a short time in the
area of interest while roaming around. Interestingly, the majority of these
warm bees were associated with cell visits (N=42 of 56 bees) and they
were visible on the comb surface only during a short interruption or between
two consecutive cell visits or they were about to enter or had recently left
an empty cell adjacent to a brood cell. Third, due to its size, a brood cap
may be covered only by one thorax of a bee on the comb surface. Additional
heat transfer from bees on the caps of neighbouring brood cells occurs (setup
C, variations B and C, brood cells #2 and #3) but may be negligible in this
setup. This is not only because of the brief presence of warm bees with
Tth
36°C in the area of interest but also because
the investigated brood cells were mainly surrounded by empty cells. By
contrast, several bees inside empty cells that are adjacent to the same brood
cell may produce heat simultaneously (Fig.
2A) and cause warming rates that are higher than those that were
simulated with only one thorax as source of heat
(Table 4, variation A, MWR up
to 0.5 deg. min1). Finally, in a different analytical
approach that considered the number of cell visitors at any time during the
observation, the influence of Nvisitors on
Tbrood was found to be highly significant in all
investigated brood cells (Table
5), confirming that cell visitors contribute to the temperature of
the adjacent brood cells.
Efficiency of heat transfer
In the simulation (setup C), thoraces touching the brood cap raised
Tcap by values of up to +3.0°C within 30 min whereas
thoraces inside empty cells raised Tbrood only by values
of +2.5°C in the same time. Although different heat transfer properties of
the brood caps and the cell walls cannot be excluded, this difference is
thought to be mainly due to the different distances of the thoraces to the
thermoprobes: the Tcap probe was located just beneath the
brood cap, 1 mm away from the thorax that was on the cap, whereas the
Tbrood probe was placed at the cell bottom and in the
centre of the brood cell,
45 mm away from the thorax that was
inside the empty cell (Fig.
3).
The size of the thorax allows it to cover only one brood cap completely or
up to three brood caps partially. Conductive heat transfer is possible only
from the ventral side of the thorax that is in touch with the brood caps,
whereas the lateral and dorsal thorax surfaces are exposed to the hive air.
Thermal radiation from these surfaces is obviously not transferred to specific
brood cells but may contribute to a less specific warming of the air between
two combs, of the neighbouring comb's surface or of nearby bees. In comparison
to the heating behaviour on the surface of brood combs, the use of empty cells
for brood nest warming appears to be advantageous for two reasons. First, in
colonies that do not produce abnormal offspring, empty cells make up
812% of cells within the brood nest
(Woyke, 1984). Due to the
hexagonal arrangement of comb cells, a heating bee inside an empty cell in the
brood area can be fully surrounded by up to six brood cells, and heat that is
emitted from the ventral, dorsal and lateral thorax surfaces may be
transferred to six pupae in the adjacent cells. Second, heat loss to the
abdomen and to the hive air is minimized because the heat source (i.e. the
thorax) is deep in the comb (almost down to the middle wall) and heat flow to
the cooler abdomen is reduced by a countercurrent heat exchanger in the narrow
petiole region (see Fig. 2;
Heinrich, 1993
;
Heinrich and Esch, 1994
).
Worker bees that are pressing their thoraces against the brood caps
(Bujok et al., 2002) enhance
heat transfer by factors of 1.92.6 in comparison with motionless bees
of the same Tth that do not contact the brood cap
(Table 4). The strong
superficial warming of the brood cell by up to +3.0±0.5°C (setup C,
Tcap in variation B) compares well to the maximum value of
3.2°C for `hot spots' that were detected inside a populous observation
hive and with different methods by Bujok et al.
(2002
). Bees displaying this
brood incubation behaviour usually touch the brood caps with the tips of their
antennae (Bujok et al., 2002
),
where thermoreceptors and other sensilla are located
(Heran, 1952
;
Lacher, 1964
), suggesting that
sensory feedback is used to adjust the temperature of specific brood cells.
This assumption is supported by our recordings of brood cell temperatures
(Fig. 8), which were repeatedly
raised to 35.9°C but not to higher temperatures that are detrimental to
the brood (Himmer, 1927
,
1932
;
Muzalewskij, 1933
;
Weiss, 1962
;
Tautz et al., 2003
). By doing
this, the bees also counteracted the cooling of the brood below the lower
limit for optimum brood development. Although most of the bees in a colony
contribute to the hive's microclimate due to their body temperature, precise
regulation of brood temperature is obviously done on a smaller scale by
individuals that display specialized brood incubation behaviour on the comb
surface (Esch, 1960
;
Schmaranzer et al., 1988
;
Bujok et al., 2002
) and inside
empty cells (present study) in the absence of any other activity, thereby
efficiently transferring heat to the sealed brood cells in their vicinity.
Further studies need to show what exactly elicits this behaviour at a certain
location in the brood area.
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Acknowledgments |
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