THE EFFECTS OF NATURAL TERPENOIDS ON BEHAVIOUR AND HOST PLANT ACCEPTANCE OF APHIDS

Paul HARREWIJN, Paul G.M. Piron and Johannes F.J.M. van den Heuvel
DLO Research Institute for Plant Protection (IPO-DLO), P.O. Box 9060, 6700 GW Wageningen, The Netherlands


Terpenoids are produced by lower organisms, plants and animals and have a wide range of functions. They consist of an integral number of five-carbon (isoprene) units that can be joined together to form relatively simple or complex structures with different biological activity: allelopathics, antimicrobials, repellents, semiochemicals and internal messengers on the cellular level and between organs.

Aphids can synthesize both monoterpenes and sesquiterpenes (1). The monoterpenes rx-pinene, B-pinene, limonene, nepetalactone and nepetalactol are sex pheromones of different aphid species. A wealth of monoterpenes is found in essential oils of plants, often stored in specific organs, especially in angiosperms of the mediterranean region. They are supposed to have defensive functions and some exert acute toxicity against insects. The aphid Acvrtosiphon pisumrefuses to penetrate into leaves of host plants treated with myrcene. Treatment of Mvzus persicaeand Menoura viciaewith menthol results in disturbed feeding behaviour and even in cannibalism. Pulegone has no effect on host plant acceptation but reduces reproduction in parthenogenetic individuals, stimulates the elate course of development and inhibits oviposition in sexuals of A. pisum. This may be caused by malfunction of the trophocytes that are dependent on amino acid homeostasis realized by the endosymbionts of the genus Buchnera (2). Pulegone has antimicrobial properties and destroys the symbionts in a dosage of 300 ng.mg-, of aphid.

(E)-ß-farnesene is a well-known alarm pheromone of aphids. The isomer (E,E)-a-farnesene and a mixture of farnesol isomers cause a high mortality among larvae of Aphis fabaeand M. nersicaewhen topically applied in a dosage equivalent to the amount of (E)-ß-farnesene present in the haemolymph. (E,E)-a-farnesene induces sexual characteristics, and the haemolymph of winged males and gynoparae contain an extraproportional amount of (E,E)-a-farnesene (3).

The essential oil of Matricaria matricaroideshas a high proportion of (E)-ß-farnesene and only a small amount of farnesene isomers (4). The vapour of plant extracts has a strong alarm effect on A. pisumand M. persicae. In contrast, the oil of M. chamomillacontains a considerable amount of (Z,E)-a-farnesene. It does not evoke an alarm effect, but increases mortality and reduces reproduction. Hexane extracts containing 0.01% (E)-ß-farnesene together with 0.05% pulegone strongly reduce fertility by initiating the birth of dead larvae, suggesting pathological effects on the reproductive system, comparable with inhibition of oviposition.

It is possible that the biosynthesis of mevalonic acid, the key substance to biologically active end products, takes more than one pathway in insects. In nonsterologenic cells as present in insects, the regulatory mechanism is not necessarily the same as in mammals (5). This would explain the additive or even synergistic effect of monoterpenes and sesquiterpenes on vital functions in aphids.

The triterpenoid azadirachtin is a feeding deterrent to M. persicae. It reduces the period of sustained phloem feeding from plants treated systemically with the compound. Thus it decreases the acquisition and transmission of phloem-limited and persistently transmitted viruses. Besides, studies on the brown planthopper have shown that the symbiont population declined after a treatment with azadirachtin-containing extracts (6). Azadirachtin presented in artificial diets to M. persicaehardly acts as a feeding deterrent but clearly influences the endosymbiont population. At dosages ranging from 100 to 2500 ppm the endosymbiotic bacteria become degenerate and development of the aphids is strongly inhibited. Also the synthesis of symbionin, a protein abundantly produced by the endosymbiont, and released into the haemolymph, is affected. As a consequence, the transmission of luteoviruses like potato leafroll virus (PLRV) was inhibited by more than 80% since symbionin is the key component in determining the persistent nature of these viruses in aphids (7). At dosages lower than 100 ppm, azadirachtin still causes a considerable reduction on PLRV transmission, although no allelopathic effects on the aphid were observed.

Aphids are equipped with a number of detoxifying enzymes such as esterases and oxidases that become active upon salivation or are secreted into the lumen of the intestinal tract. Aphids are not used to acquisition of high dosages of terpenoids because they feed on phloem sap. Volatile terpenoids which are toxic to herbivores of various insect taxa, act as allomones and repellents against aphids and have also reported antimicrobial properties (8).

Synthetic derivatives of monoterpenes can be produced with high yields and more complex terpenes can relatively easy be obtained from natural sources. Their combination could produce selective aphicides formulated to act on host plant acceptation, population development, dispersion and virus transmission.

Literature
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  2. Douglas A. E. : Proc. 8th Int. Symp. Insect-Plant Relationships, Dordrecht: Kluwer Acad. Publ., 329-336 (1992).
  3. Gut J., van Oosten A.M.: Acta Phyt. et Entomol. Hung. 25, 331-342 (1990).
  4. Harrewijn P., van Oosten A.M., Piron P.G.M.: Proc. Exper. & Appl. Entomol. N.E.V. Amsterdam 4, 21-26 (1993).
  5. Havel C.M., Rector II E.R., Watson J.A.: J.Biol. Chem. 262, 10150-10156 (1986).
  6. Raguraman S., Saxena R.C.: Phytoparasitica 22, 299-307 (1994)
  7. Van den Heuvel J.F.J.M., Verbeek M., van der Wilk F.: J. of Gen. Virol 75, 2559-2565 (1994).
  8. Harrewijn P., Minks A.K., Mollema C.: Chemoecology 5/6, 55-73 (1995).

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