Pieris butterfly anti-aphrodisiacs luring Trichogramma egg parasitoids: Their costs in a tritrophic perspective

Zusammenfassung der Projektergebnisse

The results of this project on the two-fold costs of anti-aphrodisiac compounds of Pieris butterflies in a tritrophic perspective show the following: (1) Besides the deposition of eggs in clutches (Pieris brassicae) also singly laid eggs (P. rapae), induce chemical changes in Brussels sprouts plants, which arrest Trichogramma wasps (T. brassicae and T. evanescens) three days after butterfly egg deposition. (2) Eliciting function was found in the accessory reproductive gland (ARG) secretion deposited with the eggs of mated butterfly females of both Pieris species, whereas the secretion of virgin females was inactive. (3) Traces of anti-aphrodisiac compounds were identified in the glands of mated female butterflies (benzyl cyanide in P. brassicae and indole in P. rapae), and were lacking in the gland secretion of virgin female butterflies. (4) Leaves treated with the synthetic compounds (with or without the ARG extract of virgin butterfly females) induced the plant and arrested the wasps three days after application. Evidently, these compounds derived from the seminal fluid of the butterfly males have changed the composition of the females’ ARG after mating and ultimately play a part in triggering the plants’ response. (5) The chemical differences between egg or BC/indole induced plants and clean palants are still unclear: we expect quantitative differences in the epicuticular leaf surface waxes, which are detected by the egg parasitoids. (6) A first whole genome analysis of P. brassicae egg-laden or BC treated Brussels sprouts plants provided molecular evidence that confirmed the oviposition- and BC-induced changes in the plant. (7) Recent studies on the wild crucifer showed that P. brassicae female butterflies were significantly repelled by volatiles of egg-laden B. nigra plants 24h after oviposition and preferred to oviposit on clean plants. Whether the anti-aphrodisiac elicits the ovipositioninduced volatile emission in B. nigra still needs to be evaluated. (8) No traces of BC were found when eggs were deposited. Probably, it evaporated too quickly when released onto a glass plate. (9) Different Trichogramma species were shown to employ phoretic behavior in nature, mainly on female butterfly hosts and mostly on solitary host species. Yet, the phoretic rates were relatively low, probably due to the catching mode. The new findings on the induction of oviposition-induced plant responses triggered by malederived butterfly anti-aphrodisiacs resulted in some public news articles, e.g. Nature Research Highlights, Die Presse, Trouw, Natuurbericht.nl, Resource (Wageningen University news).

Projektbezogene Publikationen (Auswahl)

• (2008). Foraging behavior of egg parasitoids exploiting chemical information. Behavioral Ecology, 19, 677-689
  Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. & Hilker, H.
  
• (2008). Male-derived butterfly antiaphrodisiac mediates induced indirect plant defense. Proceedings of the National Academy of Sciences of the USA, 105, 10033-1003
  Fatouros, N.E., Broekgaarden, C., Bukovinszkine’Kiss, G., van Loon, J.J.A., Mumm, R., Huigens, M.E., Dicke, M. & Hilker, M.
  
• (2009). Anti-aphrodisiac compounds of male butterflies increase the risk of egg parasitoid attack by inducing plant synomone production. Journal of Chemical Ecology, 35, 1373-1381
  Fatouros, N.E., Pashalidou, F.G., Aponte Cordero, W.V., van Loon, J.J.A., Mumm, R., Dicke, M., Hilker, M. &. Huigens, M.E.
  
• (2009). Hitch-hiking parasitic wasp learns to exploit butterfly antiaphrodisiac. Proceedings of the National Academy of Sciences of the USA, 106, 820-825
  Huigens, M.E., Pashalidou, F.G., Qian, M., Bukovinszky, T., Smid, H.M., van Loon, J.J.A., Dicke, M. & Fatouros, N.E.
  
• (2010). Chemical espionage on species-specific butterfly anti-aphrodisiac by hitch-hiking Trichogramma wasps. Behavioral Ecology, 21, 470-478
  Huigens, M.E., Woelke, J.F., Pashalidou, F.G., Smid, H.M., Bukovinszky, T. & Fatouros, N.E.
  
• (2010). Ooencyrtus marcelloi sp. nov. (Hymenoptera: Encyrtidae), an egg parasitoid of Heliconiini (Lepidoptera: Nymphalidae: Heliconiinae) on passion vines (Malpighiales: Passifloraceae) in Central America. Journal of Natural History, 44, 81-87
  Guerrieri, E., Huigens, M.E, Estrada, C., Woelke, J.F., De Rijk, M., Fatouros, N.E., Aiello, A. & Noyess, J.S.
  
• (2010). The use of oviposition-induced plant cues by Trichogramma egg parasitoids. Ecological Entomology, 35, 748-753
  Pashalidou, F.G., Huigens, M.E., Dicke, M. & Fatouros, N.E.