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Research Article
Hot bees in empty broodnest cells: heating from within
Marco Kleinhenz, Brigitte Bujok, Stefan Fuchs, Jürgen Tautz
Journal of Experimental Biology 2003 206: 4217-4231; doi: 10.1242/jeb.00680
Marco Kleinhenz
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Brigitte Bujok
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Stefan Fuchs
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Jürgen Tautz
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  • Fig. 1.
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    Fig. 1.

    Observation hive with three comb pieces (A, B, C), allowing thermographic temperature measurements of bees inside observation cells. Comb cells in the background are indicated but could not be seen during the observations. The comb chamber was covered with infrared transparent film. The smaller chamber was half filled with sugar dough and contained the queen (Q) in a cage. Insulation covering the hive (4 cm polystyrene walls on all sides; not shown) was partially removed while the observations were being made. Hive temperature (Thive) was measured with a thermistor (T) inside a plastic tube.

  • Fig. 2.
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    Fig. 2.

    Close-up thermographic recordings of bees inside three empty cells adjacent to brood cells. A and B show a view of the same cells at different times. x, y and z each indicate the bottom of one of the observation cells. The white lines indicate the middle wall. (A) Three heating bees with different thorax temperatures (Tth); all of them are seen from their dorsal sides. (B) A resting bee in cell y and a heating bee in cell z (turned upside-down). Cell x is empty. Abbreviations: abd, abdomen; hd, head; th, thorax; w, wing. Asterisks mark the wax walls of two sealed pupae cells adjacent to the observation cells. The temperatures refer to the bee thorax.

  • Table 1.

    Thorax temperatures (Tth) of bees visiting empty cells adjacent to sealed brood cells (type 1) or non-brood cells (type 2)

    Type 1 (adjacent to brood cells)
    Comb B Comb C Day
    35.7±3.1 (6, 28)35.8±2.4 (13, 71)1
    34.8±2.9 (6, 54)34.8±2.7 (13, 80)2
    Tth (°C) (N, n) 34.7±3.3 (6, 53) 35.6±2.6 (13, 95) 3
    Type 2 (adjacent to non-brood cells)Comb A32.4±2.5 (19, 130)P<0.01P<0.011
    30.4±1.7 (23, 179)P<0.01P<0.012
    28.5±0.9 (23, 194)P<0.01P<0.013
    Comb B33.3±1.7 (27, 167)P<0.01P<0.011
    33.4±2.3 (35, 261)P<0.01P<0.012
    31.1±1.9 (35, 295)P<0.01P<0.013
    Comb C32.5±1.0 (19, 31)P<0.01P<0.011
    34.0±2.1 (27, 139)n.s.P<0.052
    32.5±1.7 (27, 176)P<0.01P<0.013
    • Data from three observation periods performed on three consecutive days (setup B). Comb A contained no brood and only the side facing the hive centre (Fig. 1) was analysed. Values of Tth are means ± S.D. (N, n). N, number of cells observed; n, number of measurements (Tth of bees inside cells) obtained from 20 infrared images during a 100 min period. Troom was 23.0±0.3°C, 22.5±0.4°C and 21.0±0.3°C on the days 1, 2, and 3, respectively, and Thive in the colony's centre was maintained at 34.2±0.3°C, 35.0±0.3°C and 34.4±0.4°C, respectively. P, result of Kolmogoroff-Smirnoff test; n.s., not significant (P>0.05).

  • Fig. 3.
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    Fig. 3.

    Simulation of worker heating with an artificially heated thorax (setup C). The cross-section shows one side of a comb. In different cycles, the thorax was placed inside an empty cell (variation A) or on the comb surface either touching the cap (variation B: d=0 mm) or at a distance of 1.0–1.5 mm from the brood cap (variation C). The locations of thermistors for measurement of thorax temperature (Tth), cap temperature (Tcap) and brood temperature (Tbrood) are indicated. Other than shown, the Tcap thermistors were not introduced from brood cell #2 but from adjacent cells in the background that were not used for temperature measurements. Abbreviations: d, distance; m, middle wall of the comb; R, resistor inside an isolated bee thorax.

  • Fig. 5.
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    Fig. 5.

    Thermogram of worker bees in the brood area, as seen in a common observation hive. The sealed area appears grey with no further details in this image; open cells are identifiable by the hexagonal structure of the cell rims. One bee with heated thorax [A; Tth(entry)=37.9°C] is about to enter an open cell adjacent to three sealed brood cells and pokes its head and the anterior part of its thorax into the cell (the dark structure on the heated thorax is the scutellum, seen from posterior-dorsal). Worker bee B has just left the open cell in the centre of the image [Tth(exit)=37.3°C]. The view on cell visitors C and D is partly hidden by bees on the comb surface. The onset of heat production during cell visits is roughly indicated when the cell interior and thorax (visible as a ring-like structure around the dark silhouette of the cool abdomen) start `glowing' with increasing intensity. Note the different intensities caused by cell visitors E and F.

  • Table 2.

    Thorax temperatures (Tth) of individually marked bees on the surface of a capped brood cell, before and after visits to empty cells (setup A)

    Bee ID Observation time (min)Tth on comb surface (°C) (N) Duration of cell visit (min)Tth(entry) (°C)Tth(exit) (°C) (ΔTth)net (°C)
    50532.836.6±2.1 (102)10.637.738.7+1.0
    6.342.540.6-1.9
    51489.536.5±1.5 (231)2.337.737.70.0
    2.839.637.7-1.9
    13.138.739.0+0.3
    16.539.339.7+0.4
    24.439.738.8-0.9
    68555.533.7±1.4 (122)13.935.037.3+2.3
    5.137.338.5+1.2
    9.138.937.9-1.0
    6.537.437.6+0.2
    11918.633.0±0.2 (48)----
    122516.834.1±0.5 (30)>7.7-35.4-
    3.635.434.4-1.0
    1.234.134.3+0.2
    125323.234.8±1.3 (46)10.134.136.0+1.9
    4.035.136.9+1.8
    2.536.437.6+1.2
    1.037.137.0-0.1
    24428.333.0±0.4 (58)----
    263635.136.3±3.3 (149)14.241.640.3-1.3
    268657.334.0±1.3 (305)12.635.536.5+1.0
    27214.232.2±1.0 (28)----
    27418.432.6±1.4 (51)-37.5--
    274954.235.6±1.7 (282)13.434.338.4+4.1
    0.737.837.2-0.6
    304962.535.7±1.7 (268)30.839.437.4-2.0
    308390.938.1±2.5 (149)32.942.538.1-4.4
    6.840.139.3-0.8
    3.639.140.2+1.1
    5.541.040.9-0.1
    19.639.339.7+0.4
    -38.1--
    309618.334.6±1.0 (107)----
    309950.237.8±1.4 (231)6.636.840.1+3.3
    3.239.139.0-0.1
    4.040.240.6+0.4
    3.939.940.2+0.3
    311920.533.9±0.7 (33)15.634.235.0+0.8
    322533.138.1±2.2 (161)4.737.236.2-1.0
    6.140.938.0-2.9
    334769.535.5±1.4 (287)10.037.138.0+0.9
    14.135.338.8+3.5
    773841.434.4±1.5 (46)>6.8-36.8-
    16.636.835.7-1.1
    11.335.437.7+2.3
    • Values of Tth are means ± S.D. (N). N, number of measurements per individual. Observation time includes the time on the brood comb surface and the time inside cells.

  • Table 3.

    Thorax temperatures (Tth) of worker bees inside three observation cells (setup B)

    Observation time (min)Tth inside cell (°C)Tth at the beginning and at the end of cell visits (°C)
    Ref. Total Inside cell Mean ± S.D. Range Int.Tth(entry)Tth(exit) (ΔTth)net
    Heat-producing bees
    x329.829.337.8±1.534.3—39.4—34.438.3+3.9
    x43.52.836.0±0.734.5—36.6—36.634.5—2.1
    y165.363.3*39.0±1.035.3—40.62—*37.7—
    38.438.7+0.3
    38.038.1+0.1
    y239.538.339.8±1.434.7—41.3140.339.1—1.2
    39.537.6—1.9
    y518.813.840.6±0.937.4—41.7139.240.6+1.4
    40.137.4—2.7
    z521.817.538.5±1.035.3—39.9—38.037.6—0.4
    z616.815.040.3±0.737.7—41.1—37.739.6+1.9
    z714.511.339.4±0.638.1—40.2—38.738.1—0.6
    Resting bees
    x29.84.832.7±0.132.2—32.8232.832.80.0
    32.832.7—0.1
    32.232.6+0.4
    x87.56.332.7±0.132.2—33.0—32.732.9+0.2
    x910.87.533.0±0.332.6—33.5133.533.0—0.5
    32.832.7—0.1
    z115.014.5*33.4±0.332.9—33.9——*33.0—
    z218.312.832.7±0.232.2—32.8—32.732.2—0.5
    Working bees
    x118.311.834.7±1.432.9—38.310———
    x56.36.035.7±0.932.8—36.73———
    x149.38.334.2±0.732.8—36.04———
    • `Ref.' refers to one of the three cells (x, y or z) and individual bees (characterized by ascending numbers) that were observed continuously. Missing numbers represent visits of ≤2 min. Visits that are marked with an asterisk lasted longer than the time that is indicated but were not recorded from the beginning. Tth was measured every 15 s. Thorax temperatures at the beginning and at the end of cell visits [Tth(entry) and Tth(exit), respectively] are also shown when a bee left and re-entered the same cell after a short interruption (data not shown for working bees). `Int.' refers to the number of short interruptions if the cell visit was not continuous.

  • Table 4.

    Simulation of worker heating with an artificially heated thorax at varying locations (setup C, variations A, B and C)

    Tth (°C) Probet=2 mint=5 mint=10 mint=30 min MWRN
    Variation A: thorax inside an empty cell
    35.2±0.4ΔTbrood0.21±0.010.37±0.060.53±0.030.71±0.030.15±0.013
    36.3±0.4ΔTbrood0.27±0.020.48±0.020.65±0.080.93±0.070.19±0.013
    38.6±0.6ΔTbrood0.51±0.040.91±0.041.21±0.061.63±0.070.34±0.023
    41.7±0.9ΔTbrood0.79±0.041.40±0.071.89±0.082.54±0.040.52±0.034
    39.5±1.0ΔTcap0.45±0.070.88±0.111.19±0.181.58±0.020.31±0.043
    Variation B: thorax on the comb surface, contacting the brood cap
    37.5±0.4ΔTbrood0.13±0.060.33±0.110.47±0.140.72±0.130.12±0.046
    40.3±0.7ΔTbrood0.17±0.060.46±0.100.73±0.131.12±0.230.14±0.035
    37.5±0.4ΔTcap1.05±0.231.40±0.211.55±0.191.82±0.200.89±0.344
    39.8±0.8ΔTcap1.84±0.492.38±0.462.66±0.442.99±0.481.54±0.636
    Variation C: thorax on the comb surface, not contacting the brood cap (distance 1.0—1.5 mm)
    35.8±0.3ΔTbrood0.05±0.020.15±0.040.25±0.050.38±0.070.06±0.024
    37.9±0.5ΔTbrood0.07±0.020.23±0.050.38±0.090.59±0.120.07±0.013
    40.1±0.8ΔTbrood0.10±0.060.32±0.140.51±0.190.80±0.290.09±0.057
    39.8±0.7ΔTcap0.79±0.091.14±0.061.37±0.061.49±0.050.60±0.123
    • Tth is the thorax temperature during the whole heating cycle of 30 min duration. Tbrood was measured at the bottom of brood cell #1 (Fig. 3; see text for the remote brood cells #2 and #3). Tcap was measured just beneath the brood cap.Δ Tbrood and ΔTcap are the temperature rises after t=2 min, 5 min, 10 min and 30 min in comparison with the initial comb temperature (32.8±0.1°C to 33.9±0.1°C before heating started). MWR, maximum warming rate (deg. min—1) of Tbrood or Tcap in the beginning of each heating cycle. All values are means ± S.D. of N heating cycles.

  • Fig. 4.
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    Fig. 4.

    Thorax temperatures (Tth) of three different honeybees in the sealed brood area on the comb surface. (A) A 2 min warm-up (+4.7°C) prior to a cell visit provides a Tth(entry) of 39.4°C. (B) Heat production during a cell visit is revealed by a net warming, with (ΔTth)net=+4.1°C. Heating was not resumed during a subsequent short-duration visit (0.7 min) to the same cell. (C) Repeated warmings prior to consecutive cell visits. Asterisks mark periods of 30 s or longer during which the bee's thorax was hidden by another bee and no temperature measurements could be made.

  • Fig. 6.
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    Fig. 6.

    Thorax temperatures (Tth) of different honeybees during long visits to empty cells adjacent to sealed brood cells. Bees that are lying still inside cells may be engaged in heat production (A–C) or resting (D). Heating bees with net temperature changes (ΔTth)net=+3.9°C (A) and– 0.3°C (B). During a longer cell visit (C), repeated cooling and heating and short interruptions (arrows) occur. Symbols: ↓, bee enters cell; ↑, bee leaves cell. Tth of bee outside cell (open circles) and inside cell (filled circles) are plotted.

  • Fig. 7.
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    Fig. 7.

    Diagram of respiratory pumping movements of the abdomen of bees inside cells. Pumping movements are drawn as spikes from 0 to 1 at the time of occurrence. (A) Resting bee with Tth=33.4±0.3°C. Thick lines are bursts of several pumping movements, which are shown at a higher temporal resolution in B. (C) Heating bee with Tth=36.4±0.3°C. Note that the time-scale of A is different from that of B and C.

  • Table 5.

    Temperatures of five brood cells (indexed from a to e) in relation to the number of long-lasting cell visitors (Nvisitors) in the adjacent cells (setup D)

    Nvisitors
    Cell Total time 0 1 2 3 4 5 6
    a100%0%21.9%51.3%25.6%1.3%0%—
    35.1±0.3°C—34.9±0.2°C35.0±0.2°C35.4±0.2°C35.4±0.0°C——
    b100%0%12.0%34.3%35.7%15.0%3.1%0%
    35.0±0.5°C—34.2±0.2°C34.8±0.3°C35.3±0.3°C35.7±0.1°C35.8±0.1°C—
    c100%3.6%20.8%39.4%22.2%6.4%7.5%0%
    34.2±0.4°C33.9±0.1°C34.0±0.3°C34.2±0.4°C34.2±0.3°C34.2±0.3°C34.5±0.4°C—
    d100%14.7%13.3%46.8%21.4%3.7%——
    34.2±0.4°C33.8±0.2°C33.9±0.4°C34.2±0.4°C34.4±0.3°C35.0±0.2°C——
    e100%5.2%24.4%55.6%13.4%1.4%0%0%
    33.6±0.6°C32.9±0.1°C33.3±0.3°C33.7±0.5°C34.3±0.3°C34.9±0.0°C——
    • The number of empty cells adjacent to a certain sealed brood cell was 6 for cells b, c and e. Cells a and d were surrounded by 5 or 4 empty cells and 1 or 2 non-visitable sealed brood cells, respectively. The % values are the times during which a certain number of cell visitors were present (% of the total observation time of 180 min). Brood cell temperatures (mean ± S.D.) are given separately for elongated periods (>1.5 min) with a constant number of Nvisitors and for the total observation time, irrespective of Nvisitors. The increase of brood temperature with the number of cell visitors was significant (Jonckheere's trend test, P<0.001 for each of the five brood cells). Sample sizes of the classified temperatures (0—6) are N=506, 447 and 448 (cells a, b and c) and N=7672 and 8686 values (cells d and e; see text for the sampling rates), respectively. Thive=32.3±0.6°C (air temperature in the brood nest); Troom=26.0±0.7°C.

  • Fig. 8.
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    Fig. 8.

    Interior temperatures of three different brood cells (Tbrood) in an observation hive (setup D), measured simultaneously at the bottom of each cell. All cells were in the same region of the brood nest, 2–3 intermittent cells away from each other, and were adjacent to 4–6 empty cells. Note that cooling and warming may occur simultaneously in different cells. An open circle on the temperature curve marks the time when a bee with a thorax temperature (Tth) of ≥36°C entered an empty cell adjacent to this brood cell for a long-duration cell visit (≥2 min). See Results (setup D) and Discussion for cell visits that are not followed by a temperature change within 2 min and for temperature changes that are not preceded by such a cell visit. Temperatures of cells d and e were stored every second with a resolution of 0.01°C. The Tbrood of cell a was read from video every 15 s with a resolution of 0.1°C (consecutive values are connected by a line for better visualisation of the curve). The asterisk marks a gap of 11 min in the data record of cell a.

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Research Article
Hot bees in empty broodnest cells: heating from within
Marco Kleinhenz, Brigitte Bujok, Stefan Fuchs, Jürgen Tautz
Journal of Experimental Biology 2003 206: 4217-4231; doi: 10.1242/jeb.00680
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Research Article
Hot bees in empty broodnest cells: heating from within
Marco Kleinhenz, Brigitte Bujok, Stefan Fuchs, Jürgen Tautz
Journal of Experimental Biology 2003 206: 4217-4231; doi: 10.1242/jeb.00680

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