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Specialized olfactory receptor neurons mediating intra- and interspecific chemical communication in leafminer moths Eriocrania spp. (Lepidoptera: Eriocraniidae)

Mattias C. Larsson^1,2,*, Eric Hallberg³, Mikhail V. Kozlov⁴, Wittko Francke⁵, Bill S. Hansson^1,2, and Christer Löfstedt¹

¹ Department of Ecology, Lund University, SE-223 62 Lund, Sweden
² Department of Crop Science, Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
³ Department of Zoology, Lund University, SE-223 62 Lund, Sweden
⁴ Section of Ecology, Biological Faculty, University of Turku, FIN-20014 Turku, Finland
⁵ Institute of Organic Chemistry, University of Hamburg, Martin Luther-King-Platz 6, D-20146, Hamburg, Germany
^* Present address: Department of Crop Science, Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden
Present address: Department of Crop Science, Chemical Ecology, Swedish University of Agricultural Sciences, PO Box 44, SE-230 53 Alnarp, Sweden

View larger version (115K): [in a new window]   Fig. 1. Electron micrographs of antennae of male Eriocrania semipurpurella. (A) Scanning electron micrograph showing two sensilla auricillica (arrows) and sockets from dislodged scales (arrowheads). The short hairs present on the antennal surface are non-innervated cuticular structures (compare C). Scale bar, 5 µm. (B) In addition to the auricillic sensilla, trichoid sensilla (arrows) occur basally on the flagellomeres. Stout chaetic sensilla (arrowhead) are found on the distal parts of the flagellomeres. Scale bar, 10 µm. (C) Transmission electron micrograph showing a transverse section of sensilla above the antennal surface (bottom) of a male E. semipurpurella. The auricillic sensillum (au) contains numerous branches of the dendritic outer segments, whereas the trichoid sensilla (tr) have moderately branched dendritic outer segments. Non-innervated hairs (arrowheads) are present between the sensilla. Scale bar, 1 µm.

View larger version (35K): [in a new window]   Fig. 2. Simultaneous recordings from three neurons with different spike amplitudes (marked with a, b and c; see Table 3) stimulated with four different compounds (source dose 1 ng). The a neuron (type 1) responded to (R,Z)-6-nonen-2-ol, the b neuron (type 2) to (S,Z)-6-nonen-2-ol and the c neuron (type 3) to both (R,Z)-4-hepten-2-ol and (R)-heptan-2-ol. The horizontal bar shows the duration of the stimulus period (0.5 s).

View larger version (25K): [in a new window]   Fig. 3. Dose/response relationships of four types of olfactory receptor neuron. Values are the number of spikes over 1 s (means ± S.E.M.). (A) Type 1 neurons responded to the pheromone component (R,Z)-6-nonen-2-ol, with the (S)-enantiomer having a 100-fold higher response threshold (N=13). (B) The response pattern of the type 2 neurons is a mirror image of that of the type 1 neurons; they responded to the pheromone component (S,Z)-6-nonen-2-ol (N-11). (C) Type 3 neurons responded to two compounds, (R)-heptan-2-ol and (R,Z)-4-hepten-2-ol, with the response threshold for the respective (S)-enantiomers being approximately 100 times higher (N=5). (D) Type 4 neurons responded to both nine-carbon ketones with a preference for (Z)-6-nonen-2-one over nonan-2-one (N=5). Dose/response curves are not shown for type 5 neurons because these neurons responded only to nonan-2-one and only at high concentrations.

View larger version (21K): [in a new window]   Fig. 4. Results from the first field-trapping experiment, 23-28 April. In each treatment, 5 µg of an electrophysiologically active compound was added to the pheromone blend of Eriocrania semipurpurella [reference blend (Ref.) 50 µg of (R,Z)-6-nonen-2-ol and 50 µg of (S,Z)-6-nonen-2-ol]. The graph shows the number of males of the two species E. semipurpurella and E. cicatricella caught per trap. Values are means + S.E.M. (N=15). *Significantly different from the reference blend (Ref.) (P<0.001) (Mann—Whitney U-test); NS, no significant difference from the reference blend.

View larger version (21K): [in a new window]   Fig. 5. Results from the second field-trapping experiment, 29 April to 7 May. Different amounts of potential semiochemicals were added to the pheromone blend of Eriocrania semipurpurella [50 µg of (R,Z)-6-nonen-2-ol and 50 µg of (S,Z)-6-nonen-2-ol]. The graph shows the number of males of the three species E. semipurpurella, E. sparrmannella and E. cicatricella caught per trap. Values are means + S.E.M. (N=15). One E. cicatricella male was caught in a trap containing 5 µg of (R)-heptan-2-ol (indicated with an asterisk). Columns labelled with the same letters are not significantly different (a,b,c refer to E. semipurpurella; a',b',c' refer to E. sparrmannella (Kruskal—Wallis analysis of variance followed by pairwise comparisons with a Mann—Whitney U-test; P<0.05).