Experimental analysis of worker division of labor in bumblebee nest thermoregulation (Bombus huntii, Hymenoptera: Apidae)
- 769 Downloads
- 14 Citations
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.
Keywords
Homeostasis Polyethism Specialization Task performance TemperatureNotes
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.
References
- Backen SJ, Sendova-Franks AB, Franks NR (2000) Testing the limits of social resilience in ant colonies. Behav Ecol Sociobiol 48:125–131CrossRefGoogle Scholar
- Barrow DA, Pickard RS (1985) Larval temperature in brood clumps of Bombus pascuorum. J Apic Res 24:69–75Google Scholar
- Beshers SN, Fewell JH (2001) Models of the division of labor in social insects. Annu Rev Entomol 46:413–440PubMedCrossRefGoogle Scholar
- Bishop JA, Armbruster WS (1999) Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology. Funct Ecol 13:711–724CrossRefGoogle Scholar
- Breed MD, Williams DB, Queral A (2002) Demand for task performance and workforce replacement: undertakers in honeybee, Apis mellifera, colonies. J Insect Behav 15:319–329CrossRefGoogle Scholar
- Bujok B, Kleinhenz M, Fuchs S, Tautz J (2004) Hot spots in the bee hive. Naturwissenschaften 89:299–301Google Scholar
- Cameron SA (1989) Temporal patterns of division of labor among workers in the primitively eusocial bumble bee Bombus griseocollis (Hymenoptera: Apidae). Ethology 80:137–151CrossRefGoogle 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 28:552–563PubMedCrossRefGoogle Scholar
- Cartar RV (1992) Adjustment of foraging efforts and task switching in energy manipulated wild bumblebee colonies. Anim Behav 44:75–87CrossRefGoogle Scholar
- Danks HV (2004) Seasonal adaptations in Arctic insects. Integr Comp Biol 44:85–94CrossRefGoogle 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 54:593–600CrossRefGoogle 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 30:193–205CrossRefGoogle Scholar
- Ferry C, Corbet SA (1996) Water collection by bumble bees. J Apic Res 35:120–122Google Scholar
- Foster RL (1992) Intraspecific recognition functions in bumble bees. Ph.D. Dissertation, University of WashingtonGoogle Scholar
- Foster RL, Brunskill A, Verdirame D, O’Donnell S (2004) Reproductive physiology, dominance interactions, and division of labor among bumble bee workers. Physiol Entomol 29:327–334CrossRefGoogle Scholar
- Free JB (1955) The division of labor within bumblebee colonies. Insectes Soc 2:195–212CrossRefGoogle 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 64:123–130CrossRefGoogle Scholar
- Heinrich B (1974) Thermoregulation in endothermic insects. Science 135:747–756CrossRefGoogle Scholar
- Heinrich B (2004) Bumblebee economics. Harvard University PressGoogle Scholar
- Heinrich B, Heinrich MJE (1983) Size and caste in temperature regulation by bumblebees. Physiol Zool 56:552–562Google Scholar
- Husband RW (1977) Observations on colony size in bumble bees (Bombus spp.). Great Lakes Entomol 10:83–85Google Scholar
- Jeanne RL, Morgan RC (1992) The influence of temperature on nest site choice and reproductive strategies in Polistes wasps. Ecol Entomol 17:135–141Google 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 191:1121–1129CrossRefGoogle 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 31:799–804PubMedCrossRefGoogle Scholar
- Kleinhenz M, Bujok B, Fuchs S, Tautz J (2003) Hot bees in empty broodnest cells: heating from within. J Exp Biol 206:4217–4231PubMedCrossRefGoogle Scholar
- Klingner R, Richter K, Schmolz E, Keller B (2005) The role of moisture in the nest thermoregulation of social wasps. Naturwissenschaften 92:427–430PubMedCrossRefGoogle Scholar
- Kolmes SA, Winston ML (1988) Division of labor among worker honey bees in demographically manipulated colonies. Insectes Soc 35:262–270CrossRefGoogle Scholar
- Kronenberg F, Heller HC (1982) Colonial thermoregulation in honey bees (Apis mellifera). J Comp Physiol B 148:65–76CrossRefGoogle Scholar
- Kühnholz S, Seeley TD (1997) The control of water collection in honey bee colonies. Behav Ecol Sociobiol 41:407–422CrossRefGoogle Scholar
- McMullan JB, Brown MJF (2005) Brood pupation temperature affects the susceptibility of honeybees (Apis mellifera) to infestation by tracheal mites (Acarapis woodi). Apidologie 36:97–105CrossRefGoogle Scholar
- Mueller CB, Shykoff JA, Sutcliffe GH (1992) Life history patterns and opportunities for queen-worker conflict in bumblebees (Hymenoptera: Apidae). Oikos 65:242–248CrossRefGoogle Scholar
- O’Donnell S (1998) Effects of experimental forager removals on division of labor in the primitively eusocial wasp Polistes instabilis (Hymenoptera: Vespidae). Behavior 135:173–193Google Scholar
- O’Donnell S, Foster RL (2001) Thresholds of response in nest thermoregulation by worker bumble bees, Bombus bifarius nearcticus (Hymenoptera: Apidae). Ethology 107:387–399CrossRefGoogle Scholar
- Ott RL, Longnecker M (2001) Statistical methods and data analysis. Duxbury, Pacific Grove, CAGoogle Scholar
- Pomeroy N, Plowright RC (1980) Maintenance of bumblebee colonies in observation hives (Hymenoptera: Apidae). Can Entomol 112:321–326Google Scholar
- Richards KW (1973) Biology of Bombus polaris Curtis and B. hyperboreus Schönherr at Lake Hazen, Northwest Territories (Hymenoptera: Bombini). Quaest Entomol 9:115–157Google Scholar
- Richards KW (1978) Nest site selection by bumble bees (Hymenoptera: Apidae) in southern Alberta. Can Entomol 110:301–318CrossRefGoogle Scholar
- Roberts SP, Harrison JF (1998) Mechanisms of thermoregulation in flying bees. Am Zool 38:492–502Google 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 159–234Google Scholar
- Soemme L (1989) Adaptations in insects and other terrestrial arthropods to the alpine environment. Fauna Norv B:1–10Google Scholar
- Southwick EE, Moritz RFA (1987) Social control of air ventilation in colonies of honey bees (Apis mellifera). J Insect Physiol 33:623–626CrossRefGoogle Scholar
- Spaethe J, Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insectes Soc 49:142–146CrossRefGoogle Scholar
- Stabentheiner A, Pressl H, Papst T, Hrassnigg N, Crailsheim K (2003) Endothermic heat production in honeybee winter clusters. J Exp Biol 206:353–358PubMedCrossRefGoogle Scholar
- Starks PT, Gilley DC (1999) Heat shielding: a novel method of colonial thermoregulation in honey bees. Naturwissenschaften 86:438–440PubMedCrossRefGoogle 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 100:7343–7347PubMedCrossRefGoogle 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 37:255–276CrossRefGoogle Scholar
- Visscher PK, Crailsheim K, Sherman G (1996) How do honey bees (Apis mellifera) fuel their water foraging flights? J Insect Physiol 42:1089–1094CrossRefGoogle Scholar
- Visscher PK, Shepardson J, McCart L, Camazine S (1999) Vibration signal modulates the behavior of house-hunting honey bees (Apis mellifera). Ethology 105:759–769CrossRefGoogle Scholar
- Vogt FD (1986a) Thermoregulation in bumblebee colonies. I. Thermoregulatory versus brood-maintenance behaviors during acute changes in ambient temperatures. Physiol Zool 59:55–59Google Scholar
- Vogt FD (1986b) Thermoregulation in bumblebee colonies. II. Demographic variation throughout the colony cycle. Physiol Zool 59:60–68Google Scholar
- Weidenmueller A (2004) The control of nest climate in bumblebee (Bombus terrestris) colonies: interindividual variability and self reinforcement in fanning response. Behav Ecol 15:120–128CrossRefGoogle Scholar
- Weidenmueller A, Kleineidam C, Tautz J (2002) Collective control of nest climate parameters in bumblebee colonies. Anim Behav 63:1065–1071CrossRefGoogle 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 37:419–423CrossRefGoogle Scholar