The role of scents in honey bee foraging and recruitment

Food Exploitation by Social Insects: Ecological, Behavioral, and Theoretical Approaches

Volumn , Issue , 2009, Pages 165-182

  Reinhard, Judith ^a   Srinivasan, Mandyam V ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84893195997     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420075618     Document Type: Chapter

References (102)

1. Arenas A, Fernández VM, Farina WM. (2007). Floral odor learning within the hive affects honeybees’ foraging decisions. Naturwissenschaften 94:218-22.
2. Arnold G, Masson C, Budharugsa S. (1985). Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res 242:593-605.
3. Baker TC. (1986). Pheromone-modulated movements of flying moths. In Payne TL, Birch MC, Kennedy CEJ (eds.), Mechanisms in Insect Olfaction. Oxford: Claredon Press, pp. 39-48.
4. Beekman M. (2005). How long will honey bees (Apis mellifera L.) be stimulated by scent to revisit pastprofitable forage sites? J Comp Physiol A 191:1115-20.
5. Breed MD, Diaz PH, Lucero KD. (2004). Olfactory information processing in honeybee, Apis mellifera, nestmate recognition. Anim Behav 68:921-28.
6. Breer H. (2003). Olfactory receptors: Molecular basis for recognition and discrimination of odors. Anal Bioanal Chem 377:427-33.
7. Brockmann A, Brückner D. (1995). Projection pattern of poreplate sensory neurones in honey bee worker, Apis mellifera L. (Hymenoptera: Apidae). Int J Ins Morph Embryol 24:405-11.
8. Butler CG. (1966). Mandibular gland pheromone of worker honey bee. Nature 212:530.
9. Butler CG. (1967). Insect pheromones. Biol Res 42:42-87.
10. Chaffiol A, Laloi D, Pham-Delègue MH. (2005). Prior classical olfactory conditioning improves odour-cued orientation of honey bees in a wind tunnel. J Exp Biol 208:3731-37.
11. Deisig N, Giurfa M, Lachnit H, Sandoz JC. (2006). Neural representation of olfactory mixtures in the honeybee antennal lobe. Eur J Neurosci 24:1161-74.
12. Deisig N, Lachnit H, Giurfa M. (2002). The effect of similarity between elemental stimuli and compounds in olfactory patterning discriminations. Learn Mem 9:112-21.
13. Dudareva N, Piechersky E. (2006). Floral scent metabolic pathways: Their regulation and evolution. In Dudareva N, Pichersky E (eds.), Biology of Floral Scent. Boca Raton, FL: CRC Press, pp. 55-78.
14. Effmert U, Buss D, Rohrbeck D, Piechulla B. (2006). Localization of the synthesis and emission of scent compounds within the flower. In Dudareva N, Pichersky E (eds.), Biology of Floral Scent. Boca Raton, FL: CRC Press, pp. 105-124, pp. 105-24.
15. Esch HE, Burns JE. (1995). Honeybees use optic flow to measure the distance of a food source. Naturwissenschaften 82:38-40.
16. Esch HE, Burns JE. (1996). Distance estimation by foraging honeybees. J Exp Biol 199:155-62.
17. Esch HE, Zhang SW, Srinivasan MV, Tautz J. (2001). Honeybee dances communicate distances measured by optic flow. Nature 411:581-83.
18. Faber T, Joerges J, Menzel R. (1999). Associative learning modifies neural representation of odors in the insect brain. Nature Neurosci 2:74-78.
19. Faber T, Menzel R. (2001). Visualizing mushroom body response to a conditioned odor in honeybees. Naturwissenschaften 88:472-76.
20. Farina WM, Grüter C, Acosta L, McCabe S. (2007). Honeybees learn floral odors while receiving nectar from foragers within the hive. Naturwissenschaften 94:55-60.
21. Ferguson AW, Free JB. (1979). Production of a forage-marking pheromone by the honeybee. J Apic Res 18:128-35.
22. Fernández PC, Farina WM. (2001). Changes in food source profitability affect Nasonov gland exposure in honeybee foragers Apis mellifera L. Insect Soc 48:366-71.
23. Flanagan D, Mercer AR. (1989). An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 18:145-59.
24. Free JB. (1987). Pheromones of Social Bees. Ithaca, NY: Cornell University Press.
25. Friesen LJ. (1973). The search dynamics of recruited honeybees, Apis mellifera ligustica Spinola. Biol Bull 144:107-31.
26. von Frisch K. (1919). Über den Geruchssinn der Biene und seine blütenbiologische Bedeutung. Zool Jb Physiol 37:1-238.
27. von Frisch K. (1943). Versuche über die Lenkung des Bienenfluges durch Duftstoffe. Naturwissenschaften 31:445-60.
28. von Frisch K. (1993). The Dance Language and Orientation of Bees. Cambridge, MA: Harvard University Press.
29. Galizia CG, McIlwrath SL, Menzel R. (1999a). A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383-94.
30. Galizia CG, Menzel R. (2000). Odour perception in honeybees: Coding information in glomerular patterns. Curr Op Neurobiol 10:504-510.
31. Galizia CG, Sachse S, Rappert A, Menzel R. (1999b). The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2:473-78.
32. Gil M, De Marco RJ. (2005). Olfactory learning by means of trophallaxis in Apis mellifera. J Exp Biol 208:671-80.
33. Giurfa M. (1993). The repellent scent-mark of the honeybee Apis mellifera ligustica and its role as communication cue during foraging. Insect Soc 40:59-67.
34. Giurfa M. (2007). Behavioral and neural analysis of associative learning in the honeybee: A taste from the magic well. J Comp Physiol A 193:801-24.
35. Goodman L. (2003). Form and Function in the Honey Bee. Cardiff: IBRA.
36. Gould JL. (1993). Ethological and comparative perspectives on honey bee learning. In Papaj DR, Lewis AC (eds.), Insect Learning. New York: Chapman & Hall, pp. 18-50.
37. Greenfield MD. (2002). Signalers and Receivers: Mechanisms and Evolution of Arthropod Communication. Oxford: Oxford University Press.
38. Grüter C, Balbuena MS, Farina WM. (2008). Informational conflicts created by the waggle dance. Proc R Soc B 275:1321-27.
39. Hammer M, Menzel R. (1995). Learning and memory in the honeybee. J Neurosci 15:1617-30.
40. Hansson BS, Anton S. (2000). Function and morphology of the antennal lobe: New developments. Ann Rev Entomol 45:203-31.
41. Hildebrand JG, Shepherd GM. (1997). Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Ann Rev Neurosci 20:595-631.
42. Joerges J, Küttner A, Galizia CG, Menzel R. (1997). Representation of odours and odour mixtures visualized in the honeybee brain. Nature 387:285-88.
43. Keil TA. (1999). Morphology and development of the peripheral olfactory organs. In Hansson BS (ed.), Insect Olfaction. Berlin: Springer Verlag, pp. 5-47.
44. Kelber C, Rössler W, Kleineidam CJ. (2006). Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395-405.
45. Kirchner WH, Grasser A. (1998). The significance of odor cues and dance language information for the food search behavior of honeybees (Hymenoptera: Apidae). J Insect Behav 11:169-78.
46. Knudsen JT, Eriksson R, Gershenzon J, Ståhl B. (2006). Diversity and distribution of floral scent. Bot Rev 72:1-120.
47. Koltermann R. (1969). Lern- und Vergessensprozesse bei der Honigbiene - aufgezeigt anhand von Duftdressuren. Z vergl Phsyiol 63:310-34.
48. Kriston I. (1973). Die Bewertung von Duft- und Farbsignalen als Orientierungshilfen an der Futterquelle durch Apis mellifera L. J Comp Physiol 84:77-94.
49. Kuwabara M. (1957). Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J Fac Sci Hokkaido Univ Ser VI Zool 13:458-64.
50. Laloi D, Bailez O, Blight MM, Roger B, Pham-Delegue MH, Wadhams LJ. (2000). Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J Chem Ecol 26:2307-19.
51. Laska M, Galizia CG. (2001). Enantioselectivity of odor perception in honeybees (Apis mellifera carnica). Behav Neurosci 115:632-39.
52. Laska M, Galizia CG, Giurfa M, Menzel R. (1999). Olfactory discrimination ability and odor structure-Activity relationships in honeybees. Chem Senses 24:429-38.
53. Laurent G. (2002). Olfactory network dynamics and the coding of multidimensional signals. Nature Rev Neurosci 3:884-95.
54. Le Métayer M, Marion-Poll F, Sandoz JC, Pham-Delègue MH, Blight MM, Wadhams LJ, Masson C, Woodcock CM. (1997). Effect of conditioning on discrimination of oilseed rape volatiles by the honeybee: Use of a combined gas chromatography-proboscis extension behavioural assay. Chem Senses 22:391-98.
55. Lindauer M. (1948). Über die Einwirkung von Duft- und Geschmacksstoffen sowie anderer Faktoren auf die Tänze der Bienen. Z vergl Physiol 31:348-412.
56. Lindauer M. (1963). Kompassorientierung. Ergebn Biol 26:158-81.
57. Menzel R. (1990). Learning, memory, and cognition in honeybees. In Kesner RP, Olton DS (eds.), Neurobiology of Comparative Cognition. Hillsdale, NJ: Lawrence Erlbaum, pp. 237-92.
58. Menzel R. (1993). Associative learning in honey bees. Apidologie 24:157-68.
59. Menzel R, Erber J. (1978). Learning and memory in bees. Sci Am 239:102-9.
60. Menzel R, Giurfa M. (2001). Cognitive architecture of a mini-brain: The honeybee. Trends Cogn Sci 5: 62-71.
61. Menzel R, Greggers U, Hammer M. (1993). Functional organization of appetitive learning and memory in a generalist pollinator, the honey bee. In Papaj DR, Lewis AC (eds.), Insect Learning. New York: Chapman & Hall, pp. 79-125.
62. Mobbs PG. (1982). The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Phil Trans R Soc Lond B 298:309-54.
63. Müller D, Abel R, Brandt R, Zöckler M, Menzel R. (2002). Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188:359-70.
64. Nagnan-Le Meillour P, Jacquin-Joly E. (2003). Biochemistry and diversity of insect odorant-binding proteins. In Blomquist GJ, Vogt RG (eds.), Insect Pheromone Biochemistry and Molecular Biology. London: Elsevier, pp. 509-37.
65. Nieh JC. (2004). Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35:159-82.
66. Page RE Jr, Metcalf RA, Metcalf RL, Erickson JEH, Lampman RL. (1991). Extractable hydrocarbons and kin recognition in honeybees (Apis mellifera L.). J Chem Ecol 17: 745-56.
67. Pelosi P. (2001). The role of perireceptor events in vertebrate olfaction. CMLS 58:503-9.
68. Pflumm W. (1969). Beziehungen zwischen Putzverhalten und Sammelbereitschaft bei der Honigbiene. Z vergl Physiol 64:1-36.
69. Pham-Delègue MH, Bailez O, Blight MM, Picard-Nizou AL, Wadhams LJ. (1993). Behavioural discrimination of oilseed rape volatiles by the honeybee Apis mellifera L. Chem Senses 18:483-94.
70. Pham-Delègue MH, Roger B, Charles R, Masson C. (1990). Effet d’une pré-exposition olfactive sur un comportement d’orientation en olfactomètre dynamique à quatre voies chez l’abeille (Apis mellifera L.). Insect Soc 37:181-87.
71. Pickett JA, Williams IH, Smith MC, Martin AP. (1981). Nasonov pheromone of the honey bee, Apis melliferaL. (Hymenoptera, Apidae). Part III. Regulation of pheromone composition and production. J Chem Ecol 7:543-54.
72. Reinhard J, Srinivasan MV, Guez D, Zhang SW. (2004b). Floral scents induce recall of navigational and visual memories in honeybees. J Exp Biol 207:4371-81.
73. Reinhard J, Srinivasan MV, Zhang SW. (2004a). Scent-triggered navigation in honeybees. Nature 427:411.
74. Reinhard J, Srinivasan MV, Zhang SW. (2006). Complex memories in honeybees: Can there be more than two? J Comp Physiol A 192:409-16.
75. Robertson HM, Wanner KW. (2006). The chemoreceptor superfamily in the honey bee, Apis mellifera: Expansion of the odorant, but not gustatory, receptor family. Genome Res 16:1395-403.
76. Ruetzler M, Zwiebel LJ. (2005). Molecular biology of insect olfaction: Recent progress and conceptual models. J Comp Physiol A 191:777-90.
77. Sachse S, Galizia CG. (2002). Role of inhibition for temporal and spatial odor representation in olfactory output neurons: A calcium imaging study. J Neurophysiol 87:1106-17.
78. Sachse S, Rappert A, Galizia CG. (1999). The spatial representation of chemical structures in the antennal lobe of honeybees: Steps towards the olfactory code. Eur J Neurosci 11:3970-82.
79. Schade F, Legge RL, Thompson JE. (2001). Fragrance volatiles of developing and senescing carnation flowers. Phytochemistry 56:703-10.
80. Schmitt T, Herzner G, Weckerle B, Schreier P, Strohm E. (2007). Volatiles of foraging honeybees Apis melliferaL. (Hymenoptera: Apidae) and their potential role as semiochemicals. Apidologie 38:164-70.
81. Schneider D. (1964). Insect antennae. Annu Rev Entomol 9:103-22.
82. Schneider D, Steinbrecht RA. (1968). Checklist of insect olfactory sensilla. Symp Zool Soc Lond 23: 279-97.
83. Smith BH. (1991). The olfactory memory of the honeybee Apis mellifera: I. Odorant modulation of short- and intermediate-term memory after single-trial conditioning. J Exp Biol 161:367-82.
84. Smith BH, Wright GA, Daly KC. (2006). Learning-based recognition and discrimination of floral odors. In Dudareva N, Pichersky E (eds.), Biology of Floral Scent. Boca Raton, FL: CRC Press, pp. 263-95.
85. Srinivasan MV, Zhang SW, Altwein M, Tautz J. (2000). Honeybee navigation: Nature and calibration of the ‘odometer.’ Science 287:851-53.
86. Srinivasan MV, Zhang SW, Bidwell N. (1997). Visually mediated odometry in honeybees. J Exp Biol 200:2513-22.
87. Srinivasan MV, Zhang SW, Lehrer M, Collett TS. (1996). Honeybee navigation en route to the goal: Visual flight control and odometry. J Exp Biol 199:237-44.
88. Srinivasan MV, Zhang SW, Reinhard J. (2006). Small brains, smart minds: Vision, perception, navigation, and ‘cognition’ in insects. In Warrant E, Nilsson DA (eds.), Invertebrate Vision. Cambridge, MA: Cambridge University Press, pp. 462-93.
89. Stengl M, Ziegelberger G, Boekhoff I, Krieger J. (1999). Perireceptor events and transduction mechanisms in insect olfaction. In Hansson BS (ed.), Insect Olfaction. Berlin: Springer Verlag, pp. 49-66.
90. Stout JC, Goulson D. (2001). The use of conspecific and interspecific scent marks by foraging bumblebees and honeybees. Anim Behav 62:183-89.
91. Strausfeld NJ. (2002). Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450:4-33.
92. Strausfeld NJ, Hildebrand JG. (1999). Olfactory systems: Common design, uncommon origins. Curr Op Neurobiol 9:634-39.
93. Tautz J, Sandeman DC. (2003). Recruitment of honeybees to non-scented food sources. J Comp Physiol A 189:293-300.
94. Theis N, Raguso RA. (2005). The effect of pollination on floral fragrance in thistles. J Chem Ecol 31:2581-600.
95. Thom C, Gilley DC, Hooper J, Esch HE. (2007). The scent of the waggle dance. PloS Biology 5:e228.
96. Wadhams LH, Blight MM, Kerguelen V, Le Métayer M, Marion-Poll F, Masson C, Pham-Delègue MH, Woodcock CM. (1994). Discrimination of oilseed rape volatiles by honey bee: Novel combined gas chromatographic-electrophysiological behavioral assay. J Chem Ecol 20:3221-31.
97. Wehner R. (1982). Himmelsnavigation bei Insekten. Neurophysiologie und Verhalten. Neujahrsbl Naturforsch Ges Zürich 184:1-132.
98. Wehner R, Rossel S. (1985). The bee’s celestial compass-A case study in behavioral neurobiology. Fortschr Zool 31:11-53.
99. Wenner AM, Meade DE, Friesen LJ. (1991). Recruitment, search behavior, and flight ranges of honey bees. Am Zool 31:768-82.
100. Wenner AM, Wells PH, Johnson DJ. (1969). Honey bee recruitment to food sources: Olfaction or language? Science 164:84-86.
101. Winston ML. (1987). The Biology of the Honey Bee. Cambridge, MA: Harvard University Press.
102. Zwiebel LJ. (2003). The biochemistry of odor detection and its future prospects. In Blomquist GJ, Vogt RGm (eds.), Insect Pheromone Biochemistry and Molecular Biology. London: Elsevier, pp. 371-90.