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First published online March 14, 2005
Journal of Experimental Biology 208, 1161-1173 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01510

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Honeybee flight metabolic rate: does it depend upon air temperature?

William A. Woods, Jr^1,*, Bernd Heinrich² and Robert D. Stevenson¹

¹ Department of Biology, University of Massachusetts Boston, Boston, Massachusetts 02125-3393, USA
² Department of Biology, University of Vermont, Burlington, Vermont 05405, USA

View larger version (17K): [in a new window]   Fig. 1. Data traces from three honeybees of 78 measured in an 0.5 l glass respirometry chamber within a transparent temperature control cabinet under shaded outdoor conditions. Periods of unprovoked, uninterrupted free flight, termed first-quality flight (FQF) are indicated, as well as periods that were excluded from FQF data because of declining wingbeat frequency (WBF) (A) or intermittent flight (B). In A, metabolic rate (MR) declined by 28% and WBF by 22% during the final 3 min of respirometry. In the higher temperature measurement (Bi), MR during the first min after flight became intermittent and was 41% lower than during FQF, and during the final min was 54% lower. In the lower temperature measurement (Bii), MR during the final 2 min was 4% lower than during FQF.

View larger version (13K): [in a new window]   Fig. 5. Relationships of (A) thorax (Tth), (B) head (Th) and (C) abdomen (Tab) temperatures to air temperature (Ta) for honeybees that sustained flight for >2/3 of the final period of respirometry (35 of the 78 bees in Fig. 8). Four bees (open symbols) that showed the largest declines in wingbeat frequency (18-25%) during measurement are excluded from the least-squares regressions shown. Regressions: Tth=0.181Ta+33.35, N=32, r2=0.27, P<0.01; Th=0.328Ta+23.02, N=32, r2=0.50, P<0.00001; Tab=0.566Ta+12.04. Regressions including bees with declining wingbeat frequencies (not shown): Tth=0.369Ta+27.27, N=36, r2=0.38, P<0.0001; Th=0.420Ta+20.04, N=36, r2=0.58, P<<0.00001; Tab=0.592Ta+11.22, N=36, r2=0.86, P<<0.00001.

View larger version (20K): [in a new window]   Fig. 7. For honeybees whose wingbeat frequency (WBF) declined <5% during respirometry (closed circles; 54 of the 78 bees in Fig. 8), mean WBF over the period corresponding to the averaged metabolic rate trace was independent of air temperature (Ta) (regression shown, N=54, r2<0.01, P=0.69). For the 24 bees whose WBF declined by >5% (open circles), despite some low WBF values at lower Ta, the relationship was not significant (regression not shown, N=24, r2=0.06, P=0.25).

View larger version (11K): [in a new window]   Fig. 2. (A) Flight metabolic rate (FMR) and wingbeat frequencies (WBF) vs air temperature (Ta) for periods of first-quality flight lasting for at least 1 min, for honeybees in an 0.5 l glass chamber within a transparent temperature control cabinet under shaded outdoor conditions. 19 of 78 bees measured displayed this behavior. FMR was independent of Ta (FMR=-1.675Ta+584.9, N=19, r2=0.03, P=0.51). (B) WBF was associated with Ta between 19 and 37°C (least-squares regression shown, WBF=1.362Ta+194.8, N=19, r2=0.31, P=0.014), but not between 26 and 37°C (regression not shown, N=14, r2<0.01, P=0.89).

View larger version (15K): [in a new window]   Fig. 3. For the 19 honeybees maintaining first-quality flight for 1 min or longer (Fig. 2), metabolic expenditure during each wingbeat declined as air temperature increased (r2=0.21, P=0.046).

View larger version (16K): [in a new window]   Fig. 4. For the 19 honeybees that displayed at least 1 min continuous of first-quality flight (Fig. 2), the fraction of the entire measurement period spent in flight declined as air temperature (Ta) increased (r2=0.63, P<0.0001).

View larger version (11K): [in a new window]   Fig. 6. (A) Relationships of head (Rh, filled symbols) and abdomen (Rab, open symbols) temperature excess ratios, and with Rh=(Th-Ta)/(Tth-Ta) and Rab=(Tab-Ta)/(Tth-Ta) to air temperature for honeybees that sustained flight for >2/3 of the final 1 min ofrespirometry. The four bees that showed the largest declines in wingbeat frequency (18-25%; see Fig. 5) are represented by squares. (B) Evaporative heat loss vs Ta for the same honeybees as in A. The four bees showing the largest declines in wingbeat frequency in A are indicated by square symbols.

View larger version (28K): [in a new window]   Fig. 8. For 78 honeybees including those in Figs 1, 2, 3, 4, all measured under the same conditions, the association between metabolic rate and air temperature weakened as the fraction of time spent in flight increased [least-squares regressions: for 0-39% flight (circles), N=28, r2=0.60, P<0.00001; for 40-79% flight (squares), N=36, r2=0.31, P<0.001; for 80-100% flight (triangles), N=15, r2=0.02, P=0.58].

View larger version (12K): [in a new window]   Fig. 9. The response of metabolic rate (MR) to air temperature (Ta) for a separate sample of 52 honeybees flying in an 0.5 l glass chamber, with chamber agitation administered as needed to keep bees airborne. Closed symbols denote measurements made outdoors under shaded conditions; open symbols denote indoor measurements. Square symbols represent additional indoor measurements from a different time of year, and are not included in the regressions. (A) For bees that maintained flight and made few or no landing attempts with little or no chamber agitation, MR was independent of Ta (N=31, r2=0.05, P=0.23). (B) For bees that made repeated landing attempts and were kept airborne by chamber agitation, MR was inversely associated with Ta (N=21, r2=0.61, P<0.0001).

View larger version (20K): [in a new window]   Fig. 10. The relationships of metabolic rate and air temperature for five studies of honeybees. The present study plus those of Roberts and Harrison (1999) and Heinrich (1980b) are of wholly or largely voluntary flight; those of Harrison et al. (1996, 2001) are of bees under constant agitation. Traces denote regressions for studies that include measurements at intermediate temperatures; data points denote mean values for studies not reporting measurements at intermediate temperatures. Metabolic rate is independent of air temperature only in the present study and in Heinrich (1980b). The data from Harrison et al. (2001) are for bees removed from the hive during winter.

View larger version (15K): [in a new window]   Fig. 11. Comparison of the relationships of force production and flight metabolic rate with thorax temperature for honeybees. (A) The relationship between flight metabolic rate and thorax temperature for voluntary flight from three studies. Data from Roberts and Harrison (1999) are re-analyzed by discrete temperature ranges. (B) The relationship between force production and thorax temperature in tethered flight (from Coelho, 1991).

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