Journal of Comparative Physiology A

, Volume 194, Issue 10, pp 861–869 | Cite as

Behavioral studies on tarsal gustation in honeybees: sucrose responsiveness and sucrose-mediated olfactory conditioning

  • Maria Gabriela de Brito SanchezEmail author
  • Chun Chen
  • Jianjun Li
  • Fanglin Liu
  • Monique Gauthier
  • Martin Giurfa
Original Paper


Although the forelegs of honeybees are one of their main gustatory appendages, tarsal gustation in bees has never been systematically studied. To provide a more extensive account on honeybee tarsal gustation, we performed a series of behavioral experiments aimed at characterizing (1) tarsal sucrose sensitivity under different experimental conditions and (2) the capacity of tarsal sucrose stimulation to support olfactory conditioning. We quantified the proboscis extension reflex to tarsal sucrose stimulation and to odors paired with tarsal sucrose stimulation, respectively. Our experiments show that tarsal sucrose sensitivity is lower than antennal sucrose sensitivity and can be increased by starvation time. In contrast, antennae amputation decreases tarsal sucrose sensitivity. Furthermore, we show that tarsal sucrose stimulation can support olfactory learning and memory even if the acquisition level reached is relatively low (40%).


Gustation Honeybee Tarsi Sucrose Olfactory learning 



Conditioned stimulus


Unconditioned stimulus


Molecular gustatory receptor


Gustatory receptor neuron


Proboscis extension reflex


Group experiencing olfactory stimulation


Group experiencing tarsal sucrose stimulation



We thank two anonymous reviewers and Jean-Christophe Sandoz for comments and suggestions on previous versions of the manuscript. We also thank Theo Mota and Edith Roussel for helping with the logistics of some experiments and Cyril Fresillon for Fig. 1. This work was supported by BEESHOP (European research grant “Bees in Europe and Sustainable Honey Production”), the French Research Council (CNRS), the University Paul-Sabatier and the Xishuangbanna Tropical Botanic Garden, Chinese Academy of Sciences.


  1. Adams MD et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195PubMedCrossRefGoogle Scholar
  2. Amrein H, Thorne N (2005) Gustatory perception and behavior in Drosophila melanogaster. Curr Biol 15:R673–R684PubMedCrossRefGoogle Scholar
  3. Bitterman ME, Menzel R, Fietz A, Schäfer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119PubMedCrossRefGoogle Scholar
  4. Chittka L, Brockmann A (2005) Perception space -The final frontier. PLoS Biol 3(4):e137PubMedCrossRefGoogle Scholar
  5. Chittka L, Raine N (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435PubMedCrossRefGoogle Scholar
  6. Chittka L, Dyer AG, Bock F, Dornhaus A (2003) Psychophysics: bees trade off foraging speed for accuracy. Nature 424:388PubMedCrossRefGoogle Scholar
  7. Chyb S, Dahanukar A, Wickens A, Carlson JR (2003) Drosophila Gr5a encodes a taste receptor tuned to trehalose. Proc Natl Acad Sci USA 100(Suppl 2):14526–14530PubMedCrossRefGoogle Scholar
  8. Clyne PJ, Warr CG, Carlson JR (2000) Candidate taste receptors in Drosophila. Science 287:1830–1834PubMedCrossRefGoogle Scholar
  9. Dahanukar A, Foster K, van Naters WM, Carlson JR (2001) A Gr receptor is required for response to the sugar trehalose in taste neurons of Drosophila. Nat Neurosci 4:1182–1186PubMedCrossRefGoogle Scholar
  10. Dahanukar A, Hallem EA, Carlson JR (2005) Insect chemoreception. Curr Opin Neurobiol 15:423–430PubMedCrossRefGoogle Scholar
  11. de Brito Sanchez MG, Giurfa M, de Paula Mota TR, Gauthier M (2005) Electrophysiological and behavioural characterization of gustatory responses to antennal ‘bitter’ taste in honeybees. Eur J Neurosci 22:3161–3170PubMedCrossRefGoogle Scholar
  12. de Brito Sanchez MG, Ortigao-Farias JR, Gauthier M, Liu F, Giurfa M (2007) Taste perception in honeybees: just a taste of honey? Arthropod Plant Interact 1:69–76CrossRefGoogle Scholar
  13. Dunipace L, Meister S, McNealy C, Amrein H (2001) Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr Biol 11:822–835PubMedCrossRefGoogle Scholar
  14. Dyer AG, Chittka L (2004a) Bumblebees (Bombus terrestris) sacrifice foraging speed to solve difficult colour discrimination tasks. J Comp Physiol A 190:759–763Google Scholar
  15. Dyer AG, Chittka L (2004b) Fine colour discrimination requires differential conditioning in bumblebees. Naturwissenschaften 91:224–227PubMedCrossRefGoogle Scholar
  16. Ebbs ML, Amrein H (2007) Taste and pheromone perception in the fruit fly Drosophila melanogaster. Pflugers Arch 454:735–747PubMedCrossRefGoogle Scholar
  17. Gaaboub I, Schuppe H, Newland PL (2005) Position-dependent sensitivity and density of taste receptors on the locust leg underlies behavioural effectiveness of chemosensory stimulation. J Comp Physiol A 191:281–289CrossRefGoogle Scholar
  18. Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193:801–824CrossRefGoogle Scholar
  19. Goodman L (2003) Form and function in the honey bee. International Bee Research Association, CardiffGoogle Scholar
  20. Guerrieri F, Schubert M, Sandoz JC, Giurfa M (2005) Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3(4):e60PubMedCrossRefGoogle Scholar
  21. Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113–135PubMedCrossRefGoogle Scholar
  22. Haupt SS (2004) Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology. J Comp Physiol A 190:735–745CrossRefGoogle Scholar
  23. Hori S, Takeuchi H, Arikawa K, Kinoshita M, Ichikawa N, Sasaki M, Kubo T (2006) Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J Comp Physiol A 192:691–700CrossRefGoogle Scholar
  24. Hori S, Takeuchi H, Kubo T (2007) Associative learning and discrimination of motion cues in the harnessed honeybee Apis mellifera L. J Comp Physiol A 193:825–833CrossRefGoogle Scholar
  25. Huber R (2005) Amines and motivated behaviors: a simpler systems approach to complex behavioral phenomena. J Comp Physiol A 191:231–239CrossRefGoogle Scholar
  26. Johnson SD, Hargreaves AL, Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87:2709–2716PubMedCrossRefGoogle Scholar
  27. Kuwabara M (1957) Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifera. J Fac Hokkaido Univ Serv VI Zool 13:458–464Google Scholar
  28. Libersat F, Pflüger HJ (2004) Monoamines and the orchestration of behavior. Bioscience 54:17–25CrossRefGoogle Scholar
  29. Lunney GH (1970) Using analysis of variance with a dichotomous dependent variable: an empirical study. J Educ Meas 7:263–269CrossRefGoogle Scholar
  30. Marella S, Fischler W, Kong P, Asgarian S, Rueckert E, Scott K (2006) Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49:285–295PubMedCrossRefGoogle Scholar
  31. Marshall J (1935) On the sensitivity of the chemoreceptors on the antenna and fore-tarsus of the honey-bee, Apis mellifica L. J Exp Biol 12:17–26Google Scholar
  32. Meunier N, Ferveur JF, Marion-Poll F (2000) Sex-specific non-pheromonal taste receptors in Drosophila. Curr Biol 10:1583–1586PubMedCrossRefGoogle Scholar
  33. Moon SJ, Kottgen M, Jiao Y, Xu H, Montell C (2006) A taste receptor required for the caffeine response in vivo. Curr Biol 16:1812–1817PubMedCrossRefGoogle Scholar
  34. Ono H, Kuwahara Y, Nishida R (2004) Hydroxybenzoic acid derivatives in a nonhost rutaceous plant, Orixa japonica, deter both oviposition and larval feeding in a rutaceae-feeding swallowtail butterfly, Papilio xuthus L. J Chem Ecol 30:287–301PubMedCrossRefGoogle Scholar
  35. Page RE Jr, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489–500PubMedCrossRefGoogle Scholar
  36. Page RE Jr, Scheiner R, Erber J, Amdam GV (2006) The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Top Dev Biol 74:253–286PubMedCrossRefGoogle Scholar
  37. 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 16:1395–1403PubMedCrossRefGoogle Scholar
  38. Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci USA 100:14537–14542PubMedCrossRefGoogle Scholar
  39. Rogers SMH, Newland PL (2000) Local movements evoked by chemical stimulation of the hind leg in the locust Schistocerca gregaria. J Exp Biol 203:423–433PubMedGoogle Scholar
  40. Sandoz JC, Hammer M, Menzel R (2002) Side-specificity of olfactory learning in the honeybee: US input side. Learn Mem 9:337–348PubMedCrossRefGoogle Scholar
  41. Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioral pharmacology of octopamine, tyramine and dopamine in honeybees. Behav Brain Res 136:545–553PubMedCrossRefGoogle Scholar
  42. Scheiner R, Kuritz-Kaiser A, Menzel R, Erber J (2005) Sensory responsiveness and the effects of equal subjective rewards on tactile learning and memory of honeybees. Learn Mem 12:626–635PubMedCrossRefGoogle Scholar
  43. Scheiner R, Sokolowski MB, Erber J (2008) Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster. Learn Mem 11:303–311CrossRefGoogle Scholar
  44. Scott K (2005) Taste recognition: food for thought. Neuron 48:455–464PubMedCrossRefGoogle Scholar
  45. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R (2001) A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104:661–673PubMedCrossRefGoogle Scholar
  46. Takeda K (1961) Classical conditioned response in the honeybee. J Insect Physiol 6:168–179CrossRefGoogle Scholar
  47. The Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–949CrossRefGoogle Scholar
  48. Ueno K, Ohta M, Morita H, Mikuni Y, Nakajima S, Yamamoto K, Isono K (2001) Trehalose sensitivity in Drosophila correlates with mutations in and expression of the gustatory receptor gene Gr5a. Curr Biol 11:1451–1455PubMedCrossRefGoogle Scholar
  49. Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533PubMedCrossRefGoogle Scholar
  50. Whitehead AT (1978) Electrophysiological response of honey bee labial palp contact chemoreceptors to sugars and electrolytes. Physiol Ent 3:241–248CrossRefGoogle Scholar
  51. Whitehead AT, Larsen J (1976a) Ultrastructure of the contact chemoreceptors of Apis mellifera l. (Hymenoptera, Apidae). Int J Insect Morphol Embryol 5:301–315CrossRefGoogle Scholar
  52. Whitehead AT, Larsen J (1976b) Electrophysiological responses of galeal contact chemoreceptors to selected sugars and electrolytes. J Insect Physiol 22:1609–1616PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Maria Gabriela de Brito Sanchez
    • 1
    Email author
  • Chun Chen
    • 2
  • Jianjun Li
    • 2
  • Fanglin Liu
    • 2
  • Monique Gauthier
    • 1
  • Martin Giurfa
    • 1
  1. 1.Centre de Recherches sur la Cognition Animale (CRCA)CNRS, Université Paul Sabatier Toulouse IIIToulouse Cedex 9France
  2. 2.Xishuangbanna Tropical Botanical GardenChinese Academy of SciencesKunmingThe People’s Republic of China

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