Pharmacophagous feeding stimulant activity of neo-clerodane diterpenoids for the turnip sawfly, Athalia rosae ruficornis

Abstract

Adults of the turnip sawflies, Athalia rosae ruficornis (Jakovlev), are “pharmacophagously” stimulated to feed on glandular trichomes distributed on leaves of two specific plant genera, Clerodendron (Verbenaceae) and Ajuga (Labiatae). A series of neo-clerodane diterpenoids were responsible for the feeding activity in adults of both sexes. Twenty-one neo-clerodane diterpenes were obtained from various sawfly-attracting Clerodendron and Ajuga plants as well as from bodies of the sawflies which had sequestered the compounds from Clerodendron plants. Among them a new neo-clerodane analogue, named here as ajugareptone, was isolated from a cultivar of Ajuga reptans L. and characterized as 6α,19-diacetoxy-4α,18-epoxy-3β-hydroxy-12( S)-(2-methylbutanoyl)-oxy-1-oxoneoclerod-13-ene-15,16-olide. The feeding stimulant activity of each compound was tested on A. rosae ruficornis adults. The sawflies were found to respond strongly to a limited number of compounds (clerodendrins B, D, H, ajugachin A, athaliadiol, 3-epicaryoptin and clerodin) which possess a tetrahydrofurofuran moiety with a 7,8-saturated structure. Clerodendrin derivatives with a 7,8-unsaturation (A, E, F, G and I) showed a marginal activity only at high doses. Analogues with an α,β-unsaturated γ-lactone moiety were entirely inactive. These data indicate a fairly restricted structural requirement for induction of the specific feeding stimulant activity in the sawfly. The sawflies selectively incorporate specific neo-clerodanes (e.g. clerodendrin D) as defense substances, and the sequestered compounds play a role as a sex pheromone to stimulate male’s mating behavior. Thus, the selective chemosensory response of the sawfly to the specific molecules implies an ecological adaptation mechanism via pharmacophagy.