Learned olfactory cues affect pollen-foraging preferences in honeybees, Apis mellifera

Animal Behaviour

Volumn 83, Issue 4, 2012, Pages 1023-1033

  Arenas, A ^a   Farina, W M ^a  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

Author keywords

Apis mellifera; Decision making; Honeybee; Olfactory learning; Pollen

Indexed keywords

BIOASSAY; DECISION MAKING; FATTY ACID; FORAGING BEHAVIOR; HONEYBEE; NECTAR; ODOR; OLFACTORY CUE; PLANT-POLLINATOR INTERACTION; POLLEN; POLLINATION; SUCROSE;

APIS MELLIFERA; APOIDEA;

EID: 84858752755     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2012.01.026     Document Type: Article

References (52)

1. Arenas A., Fernández V.M., Farina W.M. Floral odor learning within the hive affects honeybees' foraging decisions. Naturwissenschaften 2007, 94:218-222.
2. Arenas A., Fernández V.M., Farina W.M. Floral scents experienced within the colony affect long-term foraging preferences in honeybees. Apidologie 2008, 39:714-722.
3. Baker H.G., Baker I. Starch in angiosperm pollen grains and its evolutionary significance. American Journal of Botany 1979, 66:591-600.
4. Barth F.G. Insects and Flowers: the Biology of a Partnership 1985, Princeton University Press, Princeton, New Jersey.
5. Bernays E.A., Chapman R.F. Host-Plant Selection by Phytophagous Insects 1994, Chapman & Hall, New York.
6. Bitterman M.E., Menzel R., Fietz A., Schaefer S. Classical conditioning of proboscis extension in honeybees. Journal of Comparative Physiology A 1983, 97:107-119.
7. Carcaud J., Roussel E., Giurfa M., Sandoz J.C. Odour aversion after olfactory conditioning of the sting extension reflex in honeybees. Journal of Experimental Biology 2009, 212:620-626.
8. Chaffiol A., Laloi D., Pham-Delègue M. Prior classical olfactory conditioning improves odour-cued flight orientation of honey bees in a wind tunnel. Journal of Experimental Biology 2005, 208:3731-3737.
9. Cook S.M., Awmack C.S., Murray D.A., Williams I.H. Are honey bees' foraging preferences affected by pollen amino acid composition?. Ecological Entomology 2003, 28:622-627.
10. Cook S.M., Sandoz J.C., Martin A.P., Murray D.A., Poppy G.M., Williams I.H. Could learning of pollen odours by honey bees (Apis mellifera) play a role in their foraging behaviour?. Physiological Entomology 2005, 30:164-174.
11. Dobson H.E.M., Groth I., Bergström G. Pollen advertisement: chemical contrasts between whole-flower and pollen odors. American Journal of Botany 1996, 83:877-885.
12. Dobson H.E.M., Danielson E.M., van Wesep D. Pollen odor chemicals as modulators of bumble bee foraging on Rosa rugosa Thunb. (Rosaceae). Plant Species Biology 1999, 14:153-166.
13. Dukas R. Evolutionary biology of insect learning. Annual Review of Entomology 2008, 53:145-160.
14. Free J.B. The flower constancy of honeybees. Journal of Animal Ecology 1963, 32:119-131.
15. Free J.B. Influence of the odour of a honeybee colony's food stores on the behaviour of its foragers. Nature 1969, 222:778.
16. Free J.B. Insect Pollination of Crops 1993, Academic Press, London. 2nd edn.
17. Gerber B., Geberzahn N., Hellstern F., Klein J., Kowalksy O., Wüstenberg D., Menzel R. Honey bees transfer olfactory memories established during flower visits to a proboscis extension paradigm in the laboratory. Animal Behaviour 1996, 52:1079-1085.
18. Giurfa M., Núñez J., Chittka L., Menzel R. Colour preferences of flower-naive honeybees. Journal of Comparative Physiology A 1995, 177:247-259.
19. Grüter C., Arenas A., Farina W.M. Does pollen function as a reward for honeybees in associative learning?. Insectes Sociaux 2008, 55:425-427.
20. Gumbert A. Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behavioral Ecology and Sociobiology 2000, 48:36-43.
21. Hanley M.E., Franco M., Pichon S., Darvill B., Goulson D. Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Functional Ecology 2008, 22:592-598.
22. Johnson D.L., Wenner A.M. A relationship between conditioning and communication in honeybees. Animal Behaviour 1966, 14:261-265.
23. Kim Y.S., Smith B.H. Effect of an amino acid on feeding preferences and learning behavior in the honey bee, Apis mellifera. Journal of Insect Physiology 2000, 46:793-801.
24. Knudsen J.T., Tollsten L., Bergstrom L.G. Floral scents: a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 1993, 33:253-280.
25. Koltermann R. Lern- und Vergessensprozesse bei der Honigbiene: aufgezeigt anhand von Duftdressuren. Zeitschrift für vergleichende Physiologie 1969, 63:310-334.
26. Menzel R. Memory dynamics in the honeybee. Journal of Comparative Physiology A 1999, 185:323-340.
27. Menzel R., Erber J. Learning and memory in honeybees. Scientific American 1978, 239:102-111.
28. National Institutes of Health Guide for the Care and Use of Laboratory Animals. A report of the Institute of Laboratory Animal Resources Committee on Care and Use of Laboratory Animals. No. 86-23 1985, U.S. Department of Health and Human Services, Washington D.C.
29. Nye W.P., Mackensen O. Preliminary report on selection and breeding of honeybees for alfalfa pollen collection. Journal of Apicultural Research 1965, 4:43-48.
30. Olsen L., Hoopingarner R., Martin E.C. Pollen preferences of honeybees sited on four cultivated crops. Journal of Apicultural Research 1979, 18:196-200.
31. Pacini E., Hesse M. Pollenkitt: its composition, forms and functions. Flora 2005, 200:399-415.
32. Page R.E., Erber J., Fondrk M.K. The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). Journal of Comparative Physiology A 1998, 182:489-500.
33. Pankiw T., Page R.E. Response thresholds to sucrose predict foraging division of labor in honeybees. Behavioral Ecology and Sociobiology 2000, 47:265-267.
34. Pernal S.F., Currie W. Discrimination and preferences for pollen-based cues by foraging honeybees, Apis mellifera L. Animal Behaviour 2002, 63:369-390.
35. Provecho Y., Josens R. Olfactory memory established during trophallaxis affects food search behaviour in ants. Journal of Experimental Biology 2009, 212:3221-3227.
36. Quinn G., Keough M. Experimental Design and Data Analysis for Biologists 2002, Cambridge University Press, Cambridge.
37. Reinhard J., Srinivasan M.V., Guez D., Zhang S.W. Floral scents induce recall of navigational and visual memories in honeybees. Journal of Experimental Biology 2004, 207:4371-4381.
38. Ribbands C.R. Communication between honeybees: the response of crop-attached bees to the scent of their crop. Proceedings of the Royal Entomological Society of London, Series A 1954, 29:141-144.
39. Ribbands C.R. The scent perception of the honeybee. Proceedings of the Royal Society B 1955, 143:367-379.
40. Roces F. Olfactory conditioning during the recruitment process in a leaf-cutting ant. Oecologia 1990, 83:261-262.
41. Roulston T.H., Cane J.H. The effect of diet breadth and nesting ecology on body size variation in bees (Apiformes). Journal of the Kansas Entomological Society 2000, 73:129-142.
42. Sandoz J.C., Laloi D., Odoux J.F., Pham-Delègue M.H. Olfactory information transfer in the honeybee: compared efficiency of classical conditioning and early exposure. Animal Behaviour 2000, 59:1025-1034.
43. Scheiner R., Erber J., Page R.E. Tactile learning and the individual evaluation of the reward in honey bees (Apis mellifera L.). Journal of Comparative Physiology A 1999, 185:1-10.
44. Scheiner R., Page R.E., Erber J. The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiology of Learning and Memory 2001, 76:138-150.
45. Scheiner R., Page R.E., Erber J. Sucrose responsiveness and behavioral plasticity in honey bees (Apis mellifera). Apidologie 2004, 35:133-142.
46. Simpson B.B., Neff J.L. Evolution and diversity of floral rewards. Handbook of Experimental Pollination Biology 1983, 142-159. Van Nostrand Reinhold, New York. C.E. Jones, R.J. Little (Eds.).
47. Sokal R.R., Rohlf F.J. Biometry: the Principles and Practice of Statistics in Biological Research 1995, W. H. Freeman, New York.
48. Takeda K. Classical conditioned response in the honey bee. Journal of Insect Physiology 1961, 6:168-179.
49. Vogel S. Ecophysiology of zoophilic pollination. Physiological Plant Ecology III 1983, 559-624. Springer, Berlin. O.L. Lange, P.S. Nobel, C.B. Osmond, H. Ziegier (Eds.).
50. Waddington K.D., Nelson C.M., Page R.E. Effects of pollen quality and genotype on the dance of foraging honey bees. Animal Behaviour 1998, 56:35-39.
51. Wehner R. The physiology of form vision in the honeybee. Zeitschrift für vergleichende Physiologie 1967, 55:145-166.
52. Wenner A.M., Wells P.H. Anatomy of a Controversy: the Question of a 'Language' among Bees 1990, Columbia University Press, New York.