The tarsal taste of honey bees: Behavioral and electrophysiological analyses

Frontiers in Behavioral Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  de Brito Sanchez, Maria Gabriela ^a,b   Lorenzo, Esther ^a,b   Su, Songkun ^c   Liu, Fanglin ^d   Zhan, Yi ^c   Giurfa, Martin ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c ZHEJIANG UNIVERSITY   (China)

^d CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Electrophysiology; Gustation; Gustatory receptors; Honey bee; Insect; Proboscis extension reflex; Tarsi; Taste

Indexed keywords

EID: 84893606306     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00025     Document Type: Article

References (61)

1. Ayestaran, A., Giurfa, M., and De Brito Sanchez, M. G. (2010). Toxic but drank: gustatory aversive compounds induce post-ingestional malaise in harnessed honeybees. PLoS ONE 5:e15000. doi: 10.1371/journal.pone.0015000
2. Bernays, E. A., and Chapman, R. F. (2000). A neurophysiological study of sensitivity to a feeding deterrent in two sister species of Heliothis with different diet breadths. J. Insect Physiol. 46, 905-912. doi: 10.1016/S0022-1910(99)00197-3
3. Bernays, E. A., and Chapman, R. F. (2001). Electrophysiological responses of taste cells to nutrient mixtures in the polyphagous caterpillar of Grammia geneura. J. Comp. Physiol. A 187, 205-213. doi: 10.1007/s003590100191
4. Bonasio, R., Zhang, G., Ye, C., Mutti, N. S., Fang, X., Qin, N., et al. (2010). Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator. Science 329, 1068-1071. doi: 10.1126/science.1192428
5. Bowdan, E. (1995). The effects of a phagostimulant and a deterrent on the microstructure of feeding by Manduca sexta caterpillars. Entomol. Exp. Appl. 77 297-306. doi: 10.1111/j.1570-7458.1995.tb02327.x
6. Butler, C. G. (1940). The choice of drinking water by the honeybee. J. Exp. Biol. 17, 253-261.
7. Carleton, A., Accolla, R., and Simon, S. A. (2010). Coding in the mammalian gustatory system. Trends Neurosci. 33, 326-334. doi: 10.1016/j.tins.2010.04.002
8. Chapman, R. F., Ascoli-Christensen, A., and White, P. R. (1991). Sensory cording for feeding deterrence in the grasshopper Schistocerca americana. J. Exp. Biol. 158, 241-259.
9. Clyne, P. J., Warr, C. G., and Carlson, J. R. (2000). Candidate taste receptors in Drosophila. Science 287, 1830-1834. doi: 10.1126/science.287.5459.1830
10. Cobb, M., Scott, K., and Pankratz, M. (2009). Gustation in Drosophila melanogaster. SEB Exp. Biol. Ser. 63, 1-38.
11. Cocco, N., and Glendinning, J. I. (2012). Not all sugars are created equal: some mask aversive tastes better than others in an herbivorous insect. J. Exp. Biol. 215, 1412-1421. doi: 10.1242/jeb.059832
12. Dahanukar, A., Hallem, E. A., and Carlson, J. R. (2005). Insect chemoreception. Curr. Opin. Neurobiol. 15, 423-430. doi: 10.1016/j.conb.2005.06.001
13. De Brito Sanchez, M. G. (2011). Taste perception in honey bees. Chem. Senses 36, 675-692. doi: 10.1093/chemse/bjr040
14. De Brito Sanchez, M. G., Chen, C., Li, J., Liu, F., Gauthier, M., and Giurfa, M. (2008). Behavioral studies on tarsal gustation in honeybees: sucrose responsiveness and sucrose-mediated olfactory conditioning. J. Comp. Physiol. A 194, 861-869. doi: 10.1007/s00359-008-0357-8
15. De Brito Sanchez, M. G., and Giurfa, M. (2011). A comparative analysis of neural taste processing in animals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 2171-2180. doi: 10.1098/rstb.2010.0327
16. De Brito Sanchez, M. G., Giurfa, M., De Paula Mota, T. R., and Gauthier, M. (2005). Electrophysiological and behavioural characterization of gustatory responses to antennal 'bitter' taste in honeybees. Eur. J. Neurosci. 22, 3161-3170. doi: 10.1111/j.1460-9568.2005.04516.x
17. Dethier, V. G., and Bowdan, E. (1989). The effect of alkaloids on the sugar receptors of the blowfly. Physiol. Entomol. 14, 127-136. doi: 10.1111/j.1365-3032.1989.tb00944.x
18. Dethier, V. G., and Bowdan, E. (1992). Effects of alkaloids on feeding by Phormia regina confirm the critical role of sensory inhibition. Physiol. Entomol. 17, 325-330. doi: 10.1111/j.1365-3032.1992.tb01030.x
19. Dietz, A. (1971). Changes with age in some mineral constituents of worker honey bees, I. Phosphorus, potassium, calcium, magnesium, sodium and iron. J. Ga. Entomol. Soc. 6, 54-57.
20. Dunipace, L., Meister, S., McNealy, C., and Amrein, H. (2001). Spatially restricted expression of candidate taste receptors in the Drosophila gustatory system. Curr. Biol. 2001, 822-835. doi: 10.1016/S0960-9822(01)00258-5
21. Frings, H., and Frings, M. (1949). The loci of contact chemoreceptors in insects. A review with new evidence. Am. Mid. Nat. 41, 602-658. doi: 10.2307/2421776
22. Galizia, C., Eisenhardt, D., and Giurfa, M. (2011). Honeybee Neurobiology and Behavior: A Tribute to Randolf Menzel. Berlin: Springer.
23. Giurfa, M. (2007). Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J. Comp. Physiol. A 193, 801-824. doi: 10.1007/s00359-007-0235-9
24. Glendinning, J. I. (2002). How do herbivorous insects cope with noxious secondary plant compounds in their diet? Entomol. Exp. Appl. 104, 15-25. doi: 10.1046/j.1570-7458.2002.00986.x
25. Goodman, L. (2003). Form and Function in the Honey Bee. Cardiff: IBRA.
26. Hagler, J. R., and Buchmann, S. L. (1993). Honey-bee (Hymenoptera, Apidae) foraging responses to phenolic-rich nectars. J. Kansas Entomol. Soc. 66, 223-230.
27. Hallem, E. A., Dahanukar, A., and Carlson, J. R. (2006). Insect odor and taste receptors. Annu. Rev. Entomol. 51, 113-135. doi: 10.1146/annurev.ento.51.051705.113646
28. Haupt, S. S. (2004). Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology. J. Comp. Physiol. A 190, 735-745. doi: 10.1007/s00359-004-0532-5
29. Hiroi, M., Meunier, N., Marion-Poll, F., and Tanimura, T. (2004). Two antagonistic gustatory receptor neurons responding to sweet-salty and bitter taste in Drosophila. J. Neurobiol. 61, 333-342. doi: 10.1002/neu.20063
30. Ishimoto, H., and Tanimura, T. (2004). Molecular neurophysiology of taste in Drosophila. Cell. Mol. Life Sci. 61, 10-18. doi: 10.1007/s00018-003-3182-9
31. Jørgensen, K., Almaas, T. J., Marion-Poll, F., and Mustaparta, H. (2007). Electrophysiological characterization of responses from gustatory receptor neurons of sensilla chaetica in the moth Heliothis virescens. Chem. Senses 32, 863-879. doi: 10.1093/chemse/bjm057
32. Kessler, S., Vlimant, M., and Guerin, P. (2012). The sugar meal of the African malaria mosquito Anopheles gambiae and how deterrent compounds interfere with it: a behavioural and neurophysiological syudy. J. Exp. Biol. 216, 1292-1306. doi: 10.1242/jeb.076588
33. Kiechle, H. (1961). Die soziale Regulation der Wassersammeltatigkeit im Bienenstaat und deren physiologische Grundlage. Z. vergl. Physiol. 45, 154-192. doi: 10.1007/BF00297763
34. Kuwabara, M. (1957). Bildung des bedingten Reflexes von Pavlovs Typus bei der Honigbiene, Apis mellifica. J. Fac. Sci. Hokkaido Univ. Ser. VI Zool. 13, 458-464.
35. Liu, F., Chen, J., Chai, J., Zhang, X., Bai, X., He, D., et al. (2007). Adaptive functions of defensive plant phenolics and a non-linear bee response to nectar components. Funct. Ecol. 21, 96-100. doi: 10.1111/j.1365-2435.2006.01200.x
36. Liu, F., Fu, W. J., Yang, D. R., Peng, Y. Q., Zhang, X. W., and He, J. Z. (2004). Reinforcement of bee-plant interaction by phenolics in food. J. Apic. Res. 43, 155-157.
37. Marella, S., Fischler, W., Kong, P., Asgarian, S., Rueckert, E., and Scott, K. (2006). Imaging taste responses in the fly brain reveals a functional map of taste category and behavior. Neuron 49, 285-295. doi: 10.1016/j.neuron.2005.11.037
38. 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, 17-26.
39. Masek, P., and Scott, K. (2010). Limited taste discrimination in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 107, 14833-14838. doi: 10.1073/pnas.1009318107
40. Meunier, N., Marion-Poll, F., Rospars, J. P., and Tanimura, T. (2003). Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139-152. doi: 10.1002/neu.10235
41. Montell, C. (2009). A taste of the Drosophila gustatory receptors. Curr. Opin. Neurobiol. 19, 345-353. doi: 10.1016/j.conb.2009.07.001
42. Newland, P. L., Rogers, S. M., Gaaboub, I., and Matheson, T. (2000a). Parallel somatotopic maps of gustatory and mechanosensory neurons in the central nervous system of an insect. J. Comp. Neurol. 425, 82-96. doi: 10.1002/1096-9861(20000911)425:1<82::AID-CNE8>3.0.CO;2-5
43. Newland, P. L., Rogers, S. M., Matheson, T., and Gaaboub, I. (2000b). Overlapping chemosensory and mechanosensory maps in the thoracic ganglia of the locust. Eur. J. Neurosci. 12, 498.
44. Ramaswamy, S. B., Cohen, N. E., and Hanson, F. E. (1992). Deterrence of feeding and oviposition responses of adult Heliothis virescens by some compounds bitter-tasting to humans. Entomol. Exp. Appl. 65, 81-93. doi: 10.1111/j.1570-7458.1992.tb01630.x
45. Robertson, H. M., and Wanner, K. W. (2006). The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 16, 1395-1403. doi: 10.1101/gr.5057506
46. Robertson, H. M., Warr, C. G., and Carlson, J. R. (2003). Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 100, 14537-14542. doi: 10.1073/pnas.2335847100
47. Rogers, S. M., and Newland, P. L. (2002). Gustatory processing in thoracic local circuits of locusts. J. Neurosci. 22, 8324-8333.
48. Scott, K. (2004). The sweet and the bitter of mammalian taste. Curr. Opin. Neurobiol. 14, 423-427. doi: 10.1016/j.conb.2004.06.003
49. Scott, K. (2005). Taste recognition: food for thought. Neuron 48, 455-464. doi: 10.1016/j.neuron.2005.10.015
50. Scott, K., Brady, R., Cravchik, A., Morozov, P., Rzhetsky, A., Zuker, C., et al. (2001). A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104, 661-673. doi: 10.1016/S0092-8674(01)00263-X
51. Singaravelan, N., Inbar, M., Ne'eman, G., Distl, M., Wink, M., and Izhaki, I. (2006). The effects of nectar-nicotine on colony fitness of caged honeybees. J. Chem. Ecol. 32, 49-59. doi: 10.1007/s10886-006-9350-2
52. Snodgrass, R. E. (1956). Anatomy of the Honey Bee. New York, NY: Comstock Publishing Associates.
53. The Honeybee Genome Sequencing Consortium. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443, 931-949. doi: 10.1038/nature05260
54. Thorne, N., Chromey, C., Bray, S., and Amrein, H. (2004). Taste perception and coding in Drosophila. Curr. Biol. 14, 1065-1079. doi: 10.1016/j.cub.2004.05.019
55. Von Frisch, K. (1967). The Dance Language and Orientation of Bees. Cambridge: Harvard University Press.
56. Vosshall, L. B., and Stocker, R. E. (2007). Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505-533. doi: 10.1146/annurev.neuro.30.051606.094306
57. Wang, Z. R., Singhvi, A., Kong, P., and Scott, K. (2004). Taste representations in the Drosophila brain. Cell 117, 981-991. doi: 10.1016/j.cell.2004.06.011
58. Whitehead, A. T. (1978). Electrophysiological response of honey bee labial palp contact chemoreceptors to sugars and electrolytes. Physiol. Entomol. 3, 241-248. doi: 10.1111/j.1365-3032.1978.tb00153.x
59. Whitehead, A. T., and Larsen, J. R. (1976a). Electrophysiological responses of galeal contact chemoreceptors of Apis mellifera to selected sugars and electrolytes. J. Insect Physiol. 22, 1609-1616. doi: 10.1016/0022-1910(76)90052-4
60. Whitehead, A. T., and Larsen, J. R. (1976b). Ultrastructure of the contact chemoreceptors of Apis mellifera L. (Hymenoptera: Apidae). Int. J. Insect Morphol. Embryol. 5, 301-315. doi: 10.1016/0020-7322(76)90030-1
61. Yarmolinsky, D. A., Zuker, C. S., and Ryba, N. J. (2009). Common sense about taste: from mammals to insects. Cell 139, 234-244. doi: 10.1016/j.cell.2009.10.001