Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae

Multicellular electrophysiological responses from the dorsal organ on the cephalic lobes of third instar Drosophila melanogaster larvae (wild-type Canton S) stimulated with a cold-trapped banana volatile extract showed that this structure has an olfactory function in the fruit fly. Responses of the dorsal organ were also recorded to constituents of the banana volatile extract as they eluted from a gas chromatographic column (GC-coupled dorsal organ electrophysiology). The active chemostimulants were identified as 2-heptanone, isoamyl alcohol, hexyl acetate, hexanol and hexyl butyrate by gas chromatography-coupled mass spectrometry. Applying the same recording system to the terminal organ sensilla, no responses were obtained to either the banana volatile bouquet or its constituents. By contrast, high frequency multicellular responses were recorded in response to touching the terminal organ with the gustatory stimuli KCI and grapefruit juice; responses were absent on similar stimulation of the dorsal organ with either NaCl or KCI. This suggests a role for olfaction by the dorsal organ and for gustation by the terminal organ in Drosophila larvae. In a 7-mm high wind tunnel with a thin 1.2% agar floor, the Drosophila larvae showed odour-conditioned upwind responses in an air stream of 0.1-m/s bearing banana volatiles. Drosophila larvae responded best to the odour of cut bananas. A 1:1 mixture of the banana odour constituents 2-heptanone and hexanol (at either 50 or 100 mu g source dose each) proved as attractive as the known larval attractants propionic acid and isoamyl acetate on their own at 100 Gig, whereas hexanol and 2-heptanone on their own at a 100 mu g source dose were less attractive. The stronger behavioural response to the banana volatile bouquet and to the binary mixture serves to underline the multireceptor nature of the dorsal organ response to food odour in Drosophila. (C) 2000 Elsevier Science Ltd. All rights reserved.