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

Journal of Experimental Biology

Volumn 208, Issue 6, 2005, Pages 1161-1173

  Woods Jr , William A ^a   Heinrich, Bernd ^b   Stevenson, Robert D ^a  

^a UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Apis mellifera; Bee; Flight energetics; Thermoregulation; Water loss; Wingbeat frequency

Indexed keywords

CARBON DIOXIDE;

ANIMAL; ARTICLE; BEE; BODY TEMPERATURE; COMPARATIVE STUDY; ENERGY METABOLISM; FLYING; FORELIMB; METABOLISM; PHYSIOLOGY; TEMPERATURE; THERMOREGULATION; UNITED STATES;

ANIMALS; BEES; BODY TEMPERATURE; CARBON DIOXIDE; ENERGY METABOLISM; FLIGHT, ANIMAL; TEMPERATURE; VERMONT; WATER LOSS, INSENSIBLE; WING;

APIS MELLIFERA; APOIDEA;

EID: 17144401907     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.01510     Document Type: Article

References (58)

1. Baird, J. M. (1986). A field study of thermoregulation in the carpenter bee, Xylocopa virginica virginica (Hymenoptera:Anthophoridae). Physiol. Zool. 59, 157-167.
2. Balderrama, N. M., Almeida, L. O. and Nunez, J. A. (1992). Metabolic rate during foraging in the honey bee. J. Comp. Physiol. B 162, 440-447.
3. Bartholomew, G. A., Vleck, D. and Vleck, C. M. (1981). Instantaneous measurements of oxygen consumption during pre-flight warm-up and post-flight cooling in sphingid and saturniid moths. J. Exp. Biol. 90, 17-32.
4. Bastian, J. and Esch, H. (1970). The nervous control of the flight muscles of the honeybee. Z. Vergl. Physiol. 67, 307-324.
5. Beenakkers, A. M. Th., Van Der Horst, D. J. and Van Marrewijk, W. J. A. (1984). Insect flight muscle metabolism. Insect Biochem. 14, 243-260.
6. Bertsch, A. (1984). Foraging in male bumblebees (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62, 325-326.
7. Borrell, B. and Medeiros, M. (2004). Thermal stability and muscle efficiency in hovering orchid bees (Apidae, Euglossini). J. Exp. Biol. 207, 2925-2933.
8. Cahill, K. and Lustick, S. (1976). Oxygen consumption and thermoregulation in Apis mellifera workers and drones. Comp. Biochem. Physiol. 55A, 355-357.
9. Casey, T. M. (1989). Oxygen consumption during flight. In Insect Flight (ed. G. J. Goldsworthy and C. H. Wheeler), pp. 257-272. Boca Raton: CRC Press.
10. Coelho, J. R. (1991). The effect of thorax temperature on force production during tethered flight in the honeybee (Apis mellifera) drones, workers and queens. Physiol. Zool. 64, 823-835.
11. Cooper, P. D., Schaffer, W. M. and Buchmann, S. L. (1985). Temperature regulation of honey bees (Apis mellifera) foraging in the Sonoran desert. J. Exp. Biol. 114, 1-15.
12. Dudley, R. (2000). The Biomechanics of Insect Flight. Princeton, NJ: Princeton University Press.
13. Dyer, F. C. (1996). Spatial memory and navigation by honeybees on the scale of the foraging range. J. Exp. Biol. 199, 147-154.
14. Ellington, C. P., Machin, K. E. and Casey, T. M. (1990). Oxygen consumption of bumblebees in forward flight. Nature 347, 472-473.
15. Esch, H. (1976). Body temperature and flight performance of honeybees in a servo-mechanically controlled wind tunnel. J. Comp. Physiol. 109, 265-277.
16. Esch, H. E. and Burns, J. E. (1996). Distance estimation by foraging honeybees. J. Exp. Biol. 199, 155-162.
17. Esch, H., Nachtigall, W. and Kogge, S. N. (1975). Correlations between aerodynamic output, electrical activity indirect flight muscles and wing positions of bees flying in a servomechanically controlled wind tunnel. J. Comp. Physiol. 100, 147-159.
18. Feller, P. and Nachtigall, W. (1989). Flight of the honey bee. II: Inner- and surface thorax temperatures and energetic criteria, correlated to flight parameters. J. Comp. Physiol. B 158, 719-727.
19. Feuerbacher, E., Fewell, J. H., Roberts, S. P., Smith, E. F. and Harrison, J. F. (2003). Effects of load type (pollen or nectar) and load mass on hovering metabolic rate and mechanical power output of the honeybee Apis mellifera. J. Exp. Biol. 206, 1855-1865.
20. Harrison, F. F., Nielsen, D. I. and Page, R. E. (1996a). Malate dehydrogenase phenotype, temperature and colony effects on the flight metabolic rate in the Honey-bee, Apis mellifera. Funct. Ecol. 10, 81-88.
21. Harrison, J. F., Camazine, S., Marden, J. H., Kirkton, S. D., Rozo, A. and Yang, X. (2001). Mite not make it home: tracheal mites reduce the safety margin for oxygen delivery of flying honeybees. J. Exp. Biol. 204, 805-814.
22. Harrison, J. F. and Fewell, J. (2002). Environmental and genetic influences of flight metabolic rate in the honey bee, Apis mellifera. Comp. Biochem. Physiol. 133A, 323-333.
23. Harrison, J. F., Fewell, J. H., Roberts, S. P. and Hall, H. G. (1996b). Achievement of thermal stability by varying metabolic heat production in flying honeybees. Science 274, 88-90.
24. Harrison, J. F. and Hall, H. G. (1993). African-European honeybee hybrids have low intermediate metabolic capacities. Nature 363, 258-260.
25. Heinrich, B. (1976). Heat exchange in relation to blood flow between thorax and abdomen in bumblebees. J. Exp. Biol. 64, 561-585.
26. Heinrich, B. (1979). Thermoregulation of African and European honeybees during foraging, attack and hive exits and returns. J. Exp. Biol. 80, 217-229.
27. Heinrich, B. (1980a). Mechanisms of body-temperature regulation in honeybees, Apis mellifera. I. Regulation of head temperatures. J. Exp. Biol. 85, 61-72.
28. Heinrich, B. (1980b). Mechanisms of body-temperature regulation in honeybees, Apis mellifera. II. Regulation of thoracic temperatures at high air temperatures. J. Exp. Biol. 85, 73-87.
29. Heinrich, B. (ed.) (1981). Insect Thermoregulation. New York, NY: John Wiley & Sons.
30. Heinrich, B. (1993). The Hot-Blooded Insects. Cambridge, MA: Harvard University Press.
31. Heinrich, B. and Esch, H. (1997). Honeybee thermoregulation (Letter). Science 276, 1015.
32. Hrassnig, N. and Crailsheim, K. (1999). Metabolic rates and metabolic power of honeybees in tethered flight related to temperature and drag (Hymenoptera: Apidae). Entomol. Gen. 24, 23-30.
33. Jungmann, R., Rothe, U. and Nachtigall, W. (1989). Flight of the honey bee. I: Thorax surface temperature and thermoregulation during tethered flight. J. Comp. Physiol. B 158, 711-718.
34. Kammer, A. E. and Heinrich, B. (1974). Metabolic rates related to muscle activity in bumblebees. J. Exp. Biol. 61, 219-227.
35. Kenagy, G. J. and Stevenson, R. D. (1982). Role of body temperature in the seasonality of daily activity in tenebrionid beetles of eastern Washington. Ecology 63, 1491-1503.
36. May, M. L. (1995). Dependence of flight behavior and heat production on air temperature in the green darner dragonfly Anax junius (Odonata: Aeshnidae). J. Exp. Biol. 198, 2385-2392.
37. Miall, R. C. (1978). The flicker fusion frequencies of six laboratory insects, and the response of the compound eye to mains fluorescent 'ripple'. Physiol. Entomol. 3, 99-106.
38. Moffatt, L. (2000). Changes in the metabolic rate of the foraging honeybee: effect of the carried weight or of the reward weight? J. Comp. Physiol. A 186, 299-306.
39. Moffatt, L. (2001). Metabolic rate and thermal stability during honeybee foraging at different reward rates. J. Exp. Biol. 204, 759-766.
40. Monteith, J. L. (1973). Principles of Environmental Physics. New York, NY: American Elsevier Publishing Company
41. Nachtigall, W., Rothe, U., Feller, P. and Jungmann, R. (1989). Flight of the honeybee. III: Flight metabolic power calculated from gas analysis, thermoregulation and fuel consumption. J. Comp. Physiol. B 158, 729-737.
42. Nicolson, S. W. and Louw, G. N. (1982). Simultaneous measurement of evaporative water loss, oxygen consumption and thoracic temperature during flight in a carpenter bee. J. Exp. Zool. 222, 287-296.
43. Roberts, S. P. and Harrison, J. F. (1998). Mechanisms, of thermoregulation in flying bees. Amer. Zool. 38, 492-502.
44. Roberts, S. P. and Harrison, J. F. (1999). Mechanisms of thermal stability during flight in the honeybee Apis mellifera. J. Exp. Biol. 202, 1523-1533.
45. Roberts, S. P., Harrison, J. F. and Hadley, N. F. (1998). Mechanisms of thermal balance in flying Centris pallida (Hymenoptera: Anthophoridae). J. Exp. Biol. 201, 2321-2331.
46. Sotavalta, O. (1947). The flight tone (wing stroke frequency) of insects. Acta Entomol. Fennica 4, 1-117.
47. Sotavalta, O. (1954). The effect of wing inertia on the wing-stroke frequency of moths, dragonflies and cockroach. Acta Entomol. Fennica 20, 93-101.
48. Spangler, H. G. (1992). The influence of temperature on the wingbeat frequencies of free-flying honeybees, Apis mellifera L. (Hymenoptera: Apidae). Bee Sci. 2, 181-186.
49. Srinivasan, M. V., Lehrer, M., Kirchner, W. H. and Zhang, S. W. (1991) Range perception through apparent image speed in freely flying honeybees. Vis. Neurosci. 6, 519-535.
50. Srinivasan, M. V., Zhang, S. W. and Bidwell, N. J. (1997). Visually mediated odometry in honeybees. J. Exp. Biol. 200, 2513-2552.
51. Srinivasan, M. V., Zhang, S., Lehrer, M. and Collett, T. (1996). Honeybee navigation en route to the goal: visual flight control and odometry. J. Exp. Biol. 199, 237-244.
52. Stavenga, D. G., Schwering, P. B. W. and Tinbergen, J. (1993). A three-compartment model describing temperature changes in tethered flying blowflies. J. Exp. Biol. 185, 325-333.
53. Stevenson, R. D. (1985). The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am. Nat. 126, 362-386.
54. Stevenson, R. D. and Woods, W. A. (1997). Honeybee thermoregulation (Letter). Science 276, 1015-1016.
55. van Praagh, J. P. (1972). Towards a controlled-environment room suitable for normal colony life of honeybees. 1. Description and general observations. J. Apic. Res. 11, 77-87.
56. Waddington, K. D. (1990). Foraging profits and thoracic temperature of honey bees (Apis mellifera). J. Comp. Physiol. B 160, 325-329.
57. Wehner, R., Michel, B. and Antonsen, A. (1996). Visual navigation in insects: coupling of egocentric and geocentric information. J. Exp. Biol. 199, 129-140.
58. Wolf, T. J., Schmid-Hempel, P., Ellington, C. P. and Stevenson, R. D. (1989). Physiological correlates of foraging efforts in honey-bees: oxygen consumption and nectar load. Funct. Ecol. 3, 417-424.