Sugar concentration influences decision making in Apis mellifera L. workers during early-stage honey storage behaviour

Mark K. Greco, Johann Lang, Peter Gallmann, Nicholas Priest, Edward Feil, Karl Crailsheim

Department für Klinische Veterin?rmedizin, Vetsuisse-Fakult?t, Universit?t Bern, Bern, Switzerland.
Department of Biology and Biochemistry, University of Bath, Bath, UK;.
Department of Biology and Biochemistry, University of Bath, Bath, UK;INVERT Group, Department of Electrical and Electronic Engineering, University of Bath, Bath, UK.
Institute for Zoology at the Karl-Franzens-Universit?t Graz, Austria.
Swiss Bee Research Institute, Agroscope Liebefeld-Posieux Research Station (ALP), Bern, Switzerland.

DOI: 10.4236/ojas.2013.33031                

Abstract

Decision making in honeybees is based on information which is acquired and processed in order to make choices between two or more alternatives. These choices lead to the expression of optimal behaviour strategies such as floral constancy. Optimal foraging strategies such as floral constancy improve a colony’s chances of survival, however to our knowledge, there has been no research on decision making based on optimal storage strategies. Here we show, using diagnostic radioentomology, that decision making in storer bees is influenced by nectar sugar concentrations and that, within 48 hours of collection, honeybees workers store carbohydrates in groups of cells with similar sugar concentrations in a nonrandom way. This behaviour, as evidenced by patchy spatial cell distributions, would help to hasten the ripening process by reducing the distance between cells of similar sugar concentrations. Thus, colonies which exhibit optimal storage strategies such as these would have an evolutionary advantage and im- prove colony survival expectations over less efficient colonies and it should be plausible to select colonies that exhibit these preferred traits.

Keywords

Honey; Floral Constancy; Nectar; Foraging Behaviour; Decision Making

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Emlen, J.M. (1966) The role of time and energy in food preference. American Naturalist, 100, 611-617. doi:10.1086/282455
[2]	MacArthur, R.H. and Pianka, E.R. (1966) On the optimal use of a patchy environment. The American Naturalist, 100, 603-609. doi:10.1086/282454
[3]	Waddington, K.D. and Holden, L.R. (1979) Optimal foraging: On flower selection by bees. The American Naturalist, 114, 179-196. doi:10.1086/283467
[4]	Charlton, N.L. and Houston, A.I. (2010) What currency do bumble bees maximize? PLoS ONE, 5, e12186. doi:10.1371/journal.pone.0012186
[5]	Betts, A.D. (1935) The constancy of the pollen-collecting bee. Bee World, 16, 111-113.
[6]	Wells, H. and Wells, P.H. (1983) Honey bee foraging ecology: Optimal diet, minimal uncertainty or individual constancy? Journal of Animal Ecology, 52, 829-836. doi:10.2307/4457
[7]	Slaa, E.J., van Nieuwstadt, M.G.L., Pisa, L.W. and Sommeijer, M.J. (1997) Foraging strategies of stingless bees (Apidae, Meliponinae): The relation between precision of recruitment, competition and communication. Acta Horticulturae, 437, 193-198.
[8]	Hassell, M.P. and Southwood, T.R.E. (1978) Foraging strategies of insects. Annual Review of Ecology and Systematics, 9, 75-98. doi:10.1146/annurev.es.09.110178.000451
[9]	Kobayashi-Kidokoro, M. and Higashi, S. (2010) Flower constancy in the generalist pollinator ceratina flavipes (Hymenoptera: Apidae): An evaluation by pollen analysis. Psyche, 2010, 891906. doi:10.1155/2010/891906
[10]	Eickwort, G. and Ginsberg, H. (1980) Foraging and mating behaviour in apoidea. Annual Reviews of Entomology, 25, 421-426. doi:10.1146/annurev.en.25.010180.002225
[11]	Gmeinbauer, R. and Crailsheim, K. (1993) Glucose utilisation during flight of honeybee workers, drones and queens. Journal of Insect Physiology, 39, 959-967. doi:10.1016/0022-1910(93)90005-C
[12]	Panzenbock, U. and Crailsheim, K. (1997) Glycogen in honeybee queens, workers and drones (Apis mellifera carnica). Journal of Insect Physiology, 34, 155-165. doi:10.1016/S0022-1910(96)00079-0
[13]	Romoser, W. S. and Stoffolano, J. G. (1998) The science of entomology. McGraw Hill, Singapore.
[14]	Suarez, R.K., Darveau, C.A., Welch, Jr., K.C., O’Brien, D.M., Roubik, D.W. and Hochachka, P.W. (2005) Energy metabolism in orchid bee flight muscles: Carbohydrate fuels all. Journal of Experimental Biology, 208, 3573-3579. doi:10.1242/jeb.01775
[15]	Standifer, L.N. (2007) Honeybee nutrition and supplemental feeding. Beekeeping in the United States.
[16]	Roubik, D.W. (1995) Pollination of cultivated plants in the tropics, FAO. Bulletin of Agricultural Services, 118, 1-194.
[17]	Somerville, D. (2005) Fat bees—Skinny bees. A manual on honey bee nutrition for beekeepers. Australian Government Rural Industries Research and Development Corporation, Goulburn, 1-142.
[18]	Brodschneider, R. and Crailsheim, K. (2010) Nutrition and health in the honeybee (Review). Apidologie, 41, 278-294. doi:10.1051/apido/2010012
[19]	Michener, C.D. (2000) The bees of the world. The John Hopkins University Press, Baltimore.
[20]	O’Toole, C. and Raw, A. (2004) Bees of the world. Cassell Illustrated, London.
[21]	Percival, M.S. (1961) Types of nectar in Angiosperms. New Phytologist, 60, 235-281. doi:10.1111/j.1469-8137.1961.tb06255.x
[22]	Bartareau, T. (1996) Foraging behaviour of Trigona carbonaria (Hymenoptera: Apidae) at multiple-choice feeding stations. Australian Journal of Zoology, 44, 143-153. doi:10.1071/ZO9960143
[23]	de Bruijn, L.L.M. and Sommeijer, M.J. (1997) Colony foraging in different species of stingless bees (Apidae, Meliponinae) and the regulation of individual nectar foraging. Insectes Sociaux, 44, 35-47. doi:10.1007/s000400050028
[24]	Waller, G.D. (1972) Evaluating responses of honey bees to sugar solutions using an artificial-flower feeder. Annual Review of Entomology, 65, 857-862.
[25]	Dress, W.J., Newell, S.J., Nastase, A.J. and Ford, J.C. (1997) Analysis of amino acids in nectar from pitchers of Sarracenia purpurea (Sarraceniaceae). American Journal of Botany, 84, 1701-1706. doi:10.2307/2446468
[26]	Inouye, D.W. and Waller, G.D. (1984) Responses of honey bees Apis mellifera to amino acid solutions mimicking nectars. Ecology, 65, 618-625. doi:10.2307/1941424
[27]	Alm, J., Ohnmeiss, T.E., Lanza, J. and Vriesenga, L. (1990) Preference of cabbage white butterflies and honey-bees for nectar that contains amino-acids. Oecologia, 84, 53-57. doi:10.1007/BF00665594
[28]	Williams, I.H. and Free, J.B. (1974) The pollination of onion (Allium cepa L.) to produce hybrid seed. Journal of Applied Ecology, 11, 409-418. doi:10.2307/2402194
[29]	Gary, N.E., Witherell, P.C., Lorenzen, K. and Marston, J.M. (1977) Area fidelity and intra field distribution of honey bees during the pollination of onions. Environmental Entomology, 6, 303-310.
[30]	Kumar, J. and Gupta, J.K. (1993) Nectar sugar production and honey bee foraging activity in three species of onion (Allium species). Apidologie, 24, 391-396. doi:10.1051/apido:19930405
[31]	Grant, V. (1950) The flower constancy of bees. The Botanical Review, 16, 379-398. doi:10.1007/BF02869992
[32]	Waser, N.M. (1986) Flower constancy: Definition, cause and measurement. The American Naturalist, 127, 596603. doi:10.1086/284507
[33]	Slaa, E.J., Tack, A.J.M. and Sommeijer, M.J. (2003) The effect of intrinsic and extrinsic factors on flower constancy of stingless bees. Apidologie, 34, 457-468. doi:10.1051/apido:2003046
[34]	Free, J.B. (1957) The transmission of food between worker honeybees. Brazilian Journal of Animal Behaviour, 5, 41-47. doi:10.1016/S0950-5601(57)80023-9
[35]	Free, J.B. (1959) The transfer of food between the adult members of a honeybee community. Bee World, 40, 193201.
[36]	Ribbands, C.R. (1953) Food sharing. In: Ribbands, C.R., Ed., The Behavior and Social Life of Honeybees, Bee Research Association, Ltd., London, 191-194.
[37]	Crailsheim, K. (1998) Trophallactic interactions in the adult honeybee (Apis mellifera L.). Apidologie, 29, 97112. doi:10.1051/apido:19980106
[38]	Park, W. (1925) The storing and ripening of honey by honeybees. Journal of Economic Entomology, 18, 405410.
[39]	Seeley, T.D. (1992) The tremble dance of the honey bee: Message and meanings. Behavioral Ecology and Sociobiology, 47, 311-316.
[40]	Grueter, C. and Farina, W.M. (2007) Nectar distribution and its relation to food quality in honeybee (Apis mellifera) colonies. Insectes Sociaux, 54, 87-94. doi:10.1007/s00040-007-0915-z
[41]	Johnson, B.R. and Baker, N. (2007) Adaptive spatial biases in nectar deposition in the nests of honey bees. Insectes Sociaux, 54, 351-355. doi:10.1007/s00040-007-0953-6
[42]	Schmickl, T. and Crailsheim, K. (2008) TaskSelSim: A model of the self-organization of the division of labour of honeybees. Mathematical and Computer Modelling of Dynamical Systems, 14, 101-125. doi:10.1080/13873950701846662
[43]	Thenius, R., Schmickl, T. and Crailsheim, K. (2008) Optimisation of a honeybee-colony’s energetics via social learning based on queuing delays. Connection Science, 20, 193-210. doi:10.1080/09540090802091982
[44]	Schmickl, T., Thenius, R. and Crailsheim, K. (2010) Swarm-intelligent foraging in honeybees: Benefits and costs of task-partitioning and environmental fluctuations. Neural Computing and Applications, 21, 251-268. doi:10.1007/s00521-010-0357-9
[45]	Nunez, J.A. (1966) Quantitative beziehungen zwischen den eigenschaften von futterquellen und dem verhalten von sammelbienen. Zeitschrift für Vergleichende Physiologie, 53, 142-164.
[46]	Farina, W.M. (1996) Food-exchange by foragers in the hive z—A means of communication among honey bees? Behavioral Ecology and Sociobiology, 38, 59-64. doi:10.1007/s002650050217
[47]	De Marco, R.J. and Farina, W.M. (2001) Changes in food source profitability affect the trophallactic and dance behavior of forager honeybees (Apis mellifera L.). Behavioral Ecology & Sociobiology, 50, 441-449. doi:10.1007/s002650100382
[48]	Pirez, N. and Farina, W.M. (2004) Nectar-receiver behavior in relation to the reward rate experienced by foraging honeybees. Behavioral Ecology & Sociobiology, 55, 574582. doi:10.1007/s00265-003-0749-2
[49]	Grüter, C. and Farina. W.M. (2007) Nectar distribution and its relation to food quality in honeybee (Apis mellifera) colonies. Insectes Sociaux, 54, 87-94. doi:10.1007/s00040-007-0915-z
[50]	Brodschneider, R., Hrassnigg, N., Vollmann, J., Petz, M., Riessberger-Gallé, U. and Crailsheim, K. (2007) Liquid nutrition within a honeybee colony—Who feeds? Apidologie, 38, 492.
[51]	Greco, M.K., Hoffmann, D., Dollin, A., Duncan, M., Spooner-Hart, R. and Neumann, P. (2009) The alternative pharaoh approach: Stingless bees mummify beetle parasites alive. Naturwissenschaften, 97, 319-323. doi:10.1007/s00114-009-0631-9
[52]	Greco, M., Spooner-Hart, R. and Holford, P. (2005) A new technique for monitoring Trigona carbonaria nest contents, brood and activity using X-ray computerized tomography. Journal of Apicultural Research, 44, 97-100.
[53]	Seeley, T.D. (1998) Thoughts on information and integration in honey bee colonies. Apidologie, 29, 67-80. doi:10.1051/apido:19980104
[54]	Camazine, S. (1991) Self-organizing pattern-formation on the combs of honey bee colonies. Behavioral Ecology & Sociobiology, 28, 61-76. doi:10.1007/BF00172140
[55]	Free, J.B. and Williams, I.H. (1974) Factors determining food storage and brood rearing in honeybee (Apis mellifera) comb. Journal of Entomology, 49, 47-63.
[56]	Johnson, B.R. and Baker, N. (2007) Adaptive spatial biases in nectar deposition in the nests of honey bees. Insectes Sociaux, 54, 351-355. doi:10.1007/s00040-007-0953-6
[57]	De Grandi-Hoffman, G. and Hagler, J. (2000) The flow of incoming nectar through a honey bee (Apis mellifera L.) colony as revealed by a protein marker. Insectes Socieux, 47, 302-306. doi:10.1007/PL00001720
[58]	Seeley, T.D. and Tovey, C.A. (1994) Why search time to find a food-storer bee accurately indicates the relatives rates of nectar collection and nectar processing in honey bee colonies. Animal Behaviour, 47, 311-316. doi:10.1006/anbe.1994.1044
[59]	Sur, R. and Stork, A. (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bulletin of Insectology, 56, 35-40.
[60]	Rogers, M.A., Krischik, V.A. and Martin, L.A. (2007) Effect of soil application of imidacloprid on survival of adult green lacewing, Chrysoperla carnea (Neuroptera: Chrysopidae), used for biological control in greenhouse. Biological Control, 42, 172-177. doi:10.1016/j.biocontrol.2007.05.006
[61]	Cloyd, R.A. and Bethke, J.A. (2010) Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. http://wileyonlinelibrary.com/
[62]	Seeley, T.D. (2010) Honeybee democracy. Princeton University Press, Princeton.
[63]	vanEngelsdorp, D., Evans, J.D., Donovall, L., Mullin, C., Frazier, M., Frazier, J., Tarpy, D.R., Hayes J. Jr. and Pettis, J.S. (2009) Entombed pollen: A new condition in honey bee colonies associated with increased risk of colony mortality. Journal of Invertebrate Pathology, 101, 147-149. doi:10.1016/j.jip.2009.03.008
[64]	Adler, L.S. (2001) The ecological significance of toxic nectar. Oikos, 91, 409-420. doi:10.1034/j.1600-0706.2000.910301.x
[65]	Robertson, L.M., Edlin, J.S. and Edwards, J.D. (2010) Investigating the importance of altitude and weather conditions for the production of toxic honey in New Zealand. New Zealand Journal of Crop and Horticultural Science, 38, 87-100. doi:10.1080/01140671003781702
[66]	Kevan, P.G. and Ebert, T. (2005) Can almond nectar and pollen poison honey bees? American Bee Journal, 145, 507-509.
[67]	Mesquita, L.X., Maracaja, P.G., Sakamoto, S.M. and Soto-Blanco, B. (2010) Toxic evaluation in honeybees (Apis mellifera) of pollen from selected plants from the semi-arid region of Brazil. Journal of Apicultural Research, 49, 265-269. doi:10.3896/IBRA.1.49.3.06