Skip to main content

Experimental analysis of worker division of labor in bumblebee nest thermoregulation (Bombus huntii, Hymenoptera: Apidae)

Abstract

Bumblebee colonies experience daily and seasonal fluctuations in ambient temperature, but proper brood development requires a stable nest temperature. This study examined how adaptive colony responses to changing ambient temperature are achieved through the in-nest workers’ behavioral plasticity. We studied three Bombus huntii colonies in the laboratory. In the first experiment, we manipulated ambient temperature and recorded brood cell incubation and wing fanning by individually marked, known-age bees. The colonies maintained their nests closer to appropriate brood development temperatures (28 to 32°C) when exposed to a range of ambient temperatures from 10.3 to 38.6°C. Incubation activity was greater in cooler treatment conditions, whereas in the highest temperature treatment, some bees fanned and others moved off the brood. As the ambient temperature dropped, workers increased the duration of their incubating bouts, but, except at the highest temperature, the number of workers that incubated did not differ significantly among treatments. A subset of the bees incubated significantly more than their nest mates, some of which never incubated. Worker body size, but not age, was a good predictor of incubation rates, and smaller bees incubated at higher rates. In the second experiment, we removed the most actively incubating workers. Immediately after removals, the total colony incubation effort was lower than pre-removal levels, but incubation effort rebounded toward pre-removal levels after 24 h. The increased thermoregulatory demand after removals was met primarily by bees increasing their rates of incubation rather than by bees switching from a different task to incubation. We conclude that some B. huntii workers specialize on nest thermoregulation, and that changes in work rates are more important than task switching in meeting thermal challenges.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Backen SJ, Sendova-Franks AB, Franks NR (2000) Testing the limits of social resilience in ant colonies. Behav Ecol Sociobiol 48:125–131

    Article  Google Scholar 

  • Barrow DA, Pickard RS (1985) Larval temperature in brood clumps of Bombus pascuorum. J Apic Res 24:69–75

    Google Scholar 

  • Beshers SN, Fewell JH (2001) Models of the division of labor in social insects. Annu Rev Entomol 46:413–440

    PubMed  Article  CAS  Google Scholar 

  • Bishop JA, Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Funct Ecol 13:711–724

    Article  Google Scholar 

  • Breed MD, Williams DB, Queral A (2002) Demand for task performance and workforce replacement: undertakers in honeybee, Apis mellifera, colonies. J Insect Behav 15:319–329

    Article  Google Scholar 

  • Bujok B, Kleinhenz M, Fuchs S, Tautz J (2004) Hot spots in the bee hive. Naturwissenschaften 89:299–301

    Google Scholar 

  • Cameron SA (1989) Temporal patterns of division of labor among workers in the primitively eusocial bumble bee Bombus griseocollis (Hymenoptera: Apidae). Ethology 80:137–151

    Article  Google Scholar 

  • Cameron SA, Williams PH (2003) Phylogeny of bumble bees in the New World subgenus Fervidobombus (Hymenoptera: Apidae): congruence of molecular and morphological data. Mol Phylogenet Evol 28:552–563

    PubMed  Article  CAS  Google Scholar 

  • Cartar RV (1992) Adjustment of foraging efforts and task switching in energy manipulated wild bumblebee colonies. Anim Behav 44:75–87

    Article  Google Scholar 

  • Danks HV (2004) Seasonal adaptations in Arctic insects. Integr Comp Biol 44:85–94

    Article  Google Scholar 

  • Donahoe K, Lewis LA, Schneider SS (2003) The role of the vibration signal in the house-hunting process of honey bee (Apis mellifera) swarms. Behav Ecol Sociobiol 54:593–600

    Article  Google Scholar 

  • Engels W, Rosenkranz P, Engels E (1995) Thermoregulation in the nest of the neotropical stingless bee Scaptotrigona postica and a hypothesis on the evolution of temperature homeostasis in highly eusocial bees. Stud Neotrop Fauna Environ 30:193–205

    Article  Google Scholar 

  • Ferry C, Corbet SA (1996) Water collection by bumble bees. J Apic Res 35:120–122

    Google Scholar 

  • Foster RL (1992) Intraspecific recognition functions in bumble bees. Ph.D. Dissertation, University of Washington

  • Foster RL, Brunskill A, Verdirame D, O’Donnell S (2004) Reproductive physiology, dominance interactions, and division of labor among bumble bee workers. Physiol Entomol 29:327–334

    Article  Google Scholar 

  • Free JB (1955) The division of labor within bumblebee colonies. Insectes Soc 2:195–212

    Article  Google Scholar 

  • Goulson D, Peat J, Stout, JC, Tucker J, Darvill B, Derwent LC, Hughes WOH (2002) Can alloethism in workers of the bumblebee, Bombus terrestris be explained in terms of foraging efficiency? Anim Behav 64:123–130

    Article  Google Scholar 

  • Heinrich B (1974) Thermoregulation in endothermic insects. Science 135:747–756

    Article  Google Scholar 

  • Heinrich B (2004) Bumblebee economics. Harvard University Press

  • Heinrich B, Heinrich MJE (1983) Size and caste in temperature regulation by bumblebees. Physiol Zool 56:552–562

    Google Scholar 

  • Husband RW (1977) Observations on colony size in bumble bees (Bombus spp.). Great Lakes Entomol 10:83–85

    Google Scholar 

  • Jeanne RL, Morgan RC (1992) The influence of temperature on nest site choice and reproductive strategies in Polistes wasps. Ecol Entomol 17:135–141

    Google Scholar 

  • Jones JC, Helliwell P, Beekman M, Maleszka R, Oldroyd BP (2005) The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. J Comp Physiol A 191:1121–1129

    Article  Google Scholar 

  • Kawakita A, Sota T, Ito M, Ascher JS, Tanaka H, Kato M, Roubik DW (2004) Phylogeny, historical biogeography, and character evolution in bumble bees (Bombus: Apidae) based on simultaneous analysis of three nuclear gene sequences. Mol Phylogenet Evol 31:799–804

    PubMed  Article  CAS  Google Scholar 

  • Kleinhenz M, Bujok B, Fuchs S, Tautz J (2003) Hot bees in empty broodnest cells: heating from within. J Exp Biol 206:4217–4231

    PubMed  Article  Google Scholar 

  • Klingner R, Richter K, Schmolz E, Keller B (2005) The role of moisture in the nest thermoregulation of social wasps. Naturwissenschaften 92:427–430

    PubMed  Article  CAS  Google Scholar 

  • Kolmes SA, Winston ML (1988) Division of labor among worker honey bees in demographically manipulated colonies. Insectes Soc 35:262–270

    Article  Google Scholar 

  • Kronenberg F, Heller HC (1982) Colonial thermoregulation in honey bees (Apis mellifera). J Comp Physiol B 148:65–76

    Article  Google Scholar 

  • Kühnholz S, Seeley TD (1997) The control of water collection in honey bee colonies. Behav Ecol Sociobiol 41:407–422

    Article  Google Scholar 

  • McMullan JB, Brown MJF (2005) Brood pupation temperature affects the susceptibility of honeybees (Apis mellifera) to infestation by tracheal mites (Acarapis woodi). Apidologie 36:97–105

    Article  Google Scholar 

  • Mueller CB, Shykoff JA, Sutcliffe GH (1992) Life history patterns and opportunities for queen-worker conflict in bumblebees (Hymenoptera: Apidae). Oikos 65:242–248

    Article  Google Scholar 

  • O’Donnell S (1998) Effects of experimental forager removals on division of labor in the primitively eusocial wasp Polistes instabilis (Hymenoptera: Vespidae). Behavior 135:173–193

    Google Scholar 

  • O’Donnell S, Foster RL (2001) Thresholds of response in nest thermoregulation by worker bumble bees, Bombus bifarius nearcticus (Hymenoptera: Apidae). Ethology 107:387–399

    Article  Google Scholar 

  • Ott RL, Longnecker M (2001) Statistical methods and data analysis. Duxbury, Pacific Grove, CA

  • Pomeroy N, Plowright RC (1980) Maintenance of bumblebee colonies in observation hives (Hymenoptera: Apidae). Can Entomol 112:321–326

    Google Scholar 

  • Richards KW (1973) Biology of Bombus polaris Curtis and B. hyperboreus Schönherr at Lake Hazen, Northwest Territories (Hymenoptera: Bombini). Quaest Entomol 9:115–157

    Google Scholar 

  • Richards KW (1978) Nest site selection by bumble bees (Hymenoptera: Apidae) in southern Alberta. Can Entomol 110:301–318

    Article  Google Scholar 

  • Roberts SP, Harrison JF (1998) Mechanisms of thermoregulation in flying bees. Am Zool 38:492–502

    Google Scholar 

  • Seeley TD, Heinrich B (1981) Regulation of temperature in the nests of social insects. In: Heinrich B (ed) Insect thermoregulation. Wiley, New York, p 159–234

    Google Scholar 

  • Soemme L (1989) Adaptations in insects and other terrestrial arthropods to the alpine environment. Fauna Norv B:1–10

    Google Scholar 

  • Southwick EE, Moritz RFA (1987) Social control of air ventilation in colonies of honey bees (Apis mellifera). J Insect Physiol 33:623–626

    Article  Google Scholar 

  • Spaethe J, Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insectes Soc 49:142–146

    Article  Google Scholar 

  • Stabentheiner A, Pressl H, Papst T, Hrassnigg N, Crailsheim K (2003) Endothermic heat production in honeybee winter clusters. J Exp Biol 206:353–358

    PubMed  Article  Google Scholar 

  • Starks PT, Gilley DC (1999) Heat shielding: a novel method of colonial thermoregulation in honey bees. Naturwissenschaften 86:438–440

    PubMed  Article  CAS  Google Scholar 

  • Tautz J, Maier S, Groh C, Rossler W, Brockmann A (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. Proc Natl Acad Sci USA 100:7343–7347

    PubMed  Article  CAS  Google Scholar 

  • van Doorn A (1987) Investigation into the regulation of dominance behavior and of the division of labour in bumblebee colonies (Bombus terrestris). Neth J Zool 37:255–276

    Article  Google Scholar 

  • Visscher PK, Crailsheim K, Sherman G (1996) How do honey bees (Apis mellifera) fuel their water foraging flights? J Insect Physiol 42:1089–1094

    Article  CAS  Google Scholar 

  • Visscher PK, Shepardson J, McCart L, Camazine S (1999) Vibration signal modulates the behavior of house-hunting honey bees (Apis mellifera). Ethology 105:759–769

    Article  Google Scholar 

  • Vogt FD (1986a) Thermoregulation in bumblebee colonies. I. Thermoregulatory versus brood-maintenance behaviors during acute changes in ambient temperatures. Physiol Zool 59:55–59

    Google Scholar 

  • Vogt FD (1986b) Thermoregulation in bumblebee colonies. II. Demographic variation throughout the colony cycle. Physiol Zool 59:60–68

    Google Scholar 

  • Weidenmueller A (2004) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120–128

    Article  Google Scholar 

  • Weidenmueller A, Kleineidam C, Tautz J (2002) Collective control of nest climate parameters in bumblebee colonies. Anim Behav 63:1065–1071

    Article  Google Scholar 

  • Yoon HJ, Kim SE, Kim YS (2002) Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignitus. Appl Entomol Zool 37:419–423

    Article  Google Scholar 

Download references

Acknowledgment

Financial support was provided by NSF (IBN-9904885 and IBN-0347315 to S.O’D., and ROA-0119690 to R.L.F. and S.O’D.), the UEC-University of Puget Sound (to R.L.F); and Phi Sigma and the Murdock Charitable Trust (to K.E.G.). Special thanks to Tom Seeley for the assistance and advice on statistical analyses and thanks to Terry Mace, Tom Seeley, and two anonymous reviewers for the helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sean O’Donnell.

Additional information

Communicated by R.F.A. Moritz

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gardner, K.E., Foster, R.L. & O’Donnell, S. Experimental analysis of worker division of labor in bumblebee nest thermoregulation (Bombus huntii, Hymenoptera: Apidae). Behav Ecol Sociobiol 61, 783–792 (2007). https://doi.org/10.1007/s00265-006-0309-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0309-7

Keywords

  • Homeostasis
  • Polyethism
  • Specialization
  • Task performance
  • Temperature