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The Effect of Root Volatiles on The The Effect of Root Volatiles on the Orientation Behaviour of Cockchafer Larvae in the Soil Dissertation In Partial Fulfilment of the Requirements for the Degree Doctor of Forest Sciences (Dr. forest.) of the Faculty of Forest Sciences and Forest Ecology Georg-August-University Göttingen submitted by Sonja Maria Weissteiner born in Brixen, Italy Göttingen, 2010 1st examiner: Prof. Dr. Stefan Schütz 2nd examiner: Prof. Dr. Friedrich Beese 3rd examiner: Prof. Dr. Dirk Hölscher Date of oral examination: 03.12.2010 The Effect of Root Volatiles on the Orientation Behaviour of Cockchafer Larvae in the Soil Summary The present study investigates the effect of root volatiles on the orientation behaviour of cockchafer larvae Melolontha hippocastani in the soil. Cockchafer larvae are known as severe pests in different crops and forests (e.g. reforestations of oaks), vineyards, orchards, grassland, pastures and meadows. In order to contribute to a better understanding of the mechanisms of food choice belowground, the present study adressed three relevant aspects of their chemical ecology. In the first part, volatile organic compounds (VOCs) of several potential host plant roots (Quercus sp. -Q. rubra and Q. petraea-, Aesculus hippocastanum, Daucus carota, Daucus carota ssp. sativus, Solanum tuberosum, Achillea millefolium, Cirsium arvense, Plantago lanceolata, Taraxacum officinale and Calamagrostis sp.) and shoots (Quercus sp., A. hippocastanum, Daucus carota ssp. sativus, and Solanum tuberosum) were investigated and analysed by using gas chromatography – mass spectrometry (GC-MS). Additionally, the roots of Quercus sp., A. hippocastanum, Daucus carota ssp. sativus and Solanum tuberosum were mechanically damaged by a pair of scissors, or damaged by larval feeding during several days. The obtained volatile patterns of the damaged roots differ clearly from the undamaged ones. In a second step, electrophysiological methods were employed to record sensory reactions of the detached larval antennae to several compounds identified in the first step. Volatile emissions of Quercus sp. (undamaged, mechanically damaged or damaged by larval feeding) were investigated in detail. By using electroantennography (EAG), changes in the receptor potential elicited by odour stimuli were recorded. However, reproducible results could be obtained only in the autumn- and winter-months. The following compounds elicited reproducible dose- response curves in 2007 and 2008 as a result of odour stimuli based on a silicon oil dilution series in concentrations ranging from 10-7 to 10-2: anisol, (1R)-camphor, (1S)-camphor, 1.8-cineol, β-caryophyllene, furanoid-trans-linalooloxide, 3-octanone and terpinolene. To identify biologically active compounds, the electro- antennographic detection (EAD) was applied as one appropriate method in chemical ecology. In the study presented here, this method did not provide any i reproducible results throughout one season. However, over some period of time, a small part of the tested antennae showed similar responses to special compounds, which were anisol, 1.8-cineol, (1R)-camphor, 3-octanone and furanoid trans- linalooloxid. The third part of this study tested the behavioural response of cockchafer larvae on selected compounds. A dual choice test setup was designed to study the behavioural orientation of the belowground living larvae. The compounds, which were able to attract the larvae of M. hippocastani were anisol, 1,8-cineol, and terpinolene. A repellent effect was elicited by acetone (as a representative of the compounds with a high vapour pressure) and β-caryophyllene. General results: The emitted shoot volatiles of Quercus sp. and A. hippocastanum differ clearly from the emitted root volatiles. Electrophysiologically active compounds could (in a reproducible manner) only be detected in special time periods during the season, which suggests that seasonal and maybe also circadian rhythms play an important role in the complex system of impulse processing in cockchafer larvae. Distinct orientation behaviour of the larvae of M. hippocastani could be observed in dual choice tests with several compounds found in root volatile samples of Quercus sp. damaged by larval feeding. Attractive and repellent compounds could be identified. The antennal lobes (ALs, first central processing unit for olfactory information processing in the insect brain) of 3rd instar of M. hippocastani contain a high number of glomeruli, which are regarded as the functional subunits of odour discrimination. Therefore, a highly developed odour discrimination ability of the cockchafer larvae is indicated. These findings are, to our knowledge, the first proof that larvae of M. hippocastani are able to perceive several volatiles emitted by roots of their host plants Quercus sp. in electrophysiological and behavioural tests. As a consequence, in dual choice tests they react with attractive or repellent behaviour. As a practical approach, these results could be used as a basis for semi-field studies towards pest control through attractive or repellent volatile compounds. However, in this context, additional investigations concerning the compatibility of the volatile composition (either single ii The Effect of Root Volatiles on the Orientation Behaviour of Cockchafer Larvae in the Soil compounds or volatile mixtures) and the carrier substance on floral and faunal organisms activity (especially on non-target organisms) are necessary. iii Zusammenfassung In der vorliegenden Dissertation wurde der Einfluss von Wurzelvolatilen auf das Verhalten von unterirdisch lebenden Waldmaikäferengerlingen Melolontha hippocastani untersucht. Diese Larven sind als ernstzunehmende Schadorganismen in Wäldern (z.B. Aufforstungsflächen von Eichenbeständen) sowie in verschiedenen Kulturen wie Wein-und Obstgärten, Wiesen und Weiden gefürchtet. Drei Aspekte der Chemischen Ökologie wurden näher beleuchtet, um zu einem besseren Verständnis der Verhaltensmechanismen bei der Wirtsfindung unterirdisch lebender Maikäferengerlinge beizutragen. Im ersten Teil wurden volatile Verbindungen (VOCs, Volatile Organic Compounds) von Wurzeln verschiedener potentieller Wirtspflanzen wie Quercus sp. (Q. rubra und Q. petraea), Aesculus hippocastanum, Daucus carota, Daucus carota ssp. sativus, Solanum tuberosum, Achillea millefolium, Cirsium arvense, Plantago lanceolata, Taraxacum officinale und Calamagrostis sp. sowie die Sprossvolatile von Quercus sp., A. hippocastanum, Daucus carota ssp. sativus und Solanum tuberosum gesammelt und mittels Gaschromatographie – Massenspektrometrie (GC-MS) analysiert und identifiziert. Zusätzlich wurden die Wurzeln von Quercus sp., A. hippocastanum, Daucus carota ssp. sativus und Solanum tuberosum mit einer Schere bzw. mit einem Messer zerschnitten oder den Maikäferengerlingen für mehrere Tage zum Fraß angeboten. Die Volatilenmuster der verletzten Wurzeln unterschieden sich deutlich von jenen der unverletzten. Im zweiten Teil wurde mittels elektrophysiologischer Methoden die Reaktion der isolierten Maikäfer-Engerlingsantenne auf die identifizierten Wurzelvolatile ermittelt. Die Duftmuster von Eichenwurzeln Quercus sp. (unverletzt, mechanisch verletzt, oder von den Engerlingen angefressen) wurden genauer untersucht. Mittels Elektroantennographie können olfaktorische Reaktionen der Insektenantenne durch Ableitung elektrischer Signale aufgezeichnet werden. Reproduzierbare Ergebnisse konnten jedoch ausschließlich in den Herbst- und Wintermonaten erzielt werden. Folgende Substanzen lieferten 2007 und 2008 in Verdünnungsreihen (10-7 to 10-2, als Lösungsmittel wurde Silikonöl verwendet) reproduzierbare Antennenreaktionen auf Duft-Stimuli: Anisol, (1R)-Campher, (1S)-Campher, 1,8-Cineol, β-Caryophyllen, die furanoide Form von trans-Linalooloxid, 3-Octanon und Terpinolen. Zur iv The Effect of Root Volatiles on the Orientation Behaviour of Cockchafer Larvae in the Soil Ermittlung biologisch aktiver Substanzen kann die Insektenantenne als elektroantennographischer Detektor (EAD) genutzt werden. Nur ein kleiner Teil der getesteten Maikäfer-Engerlingsantennen lieferte jedoch ähnliche Ergebnisse für Anisol, 1,8-Cineol, (1R)-Campher, 3-Octanon und für die furanoide Form von trans- Linalooloxid, und das jeweils nur ausschließlich während bestimmter Zeitfenster. Im dritten Teil wurde die Verhaltensreaktion der Maikäferengerlinge auf ausgewählte Substanzen untersucht. Ein dualer Versuchsaufbau wurde entwickelt um das Verhalten unterirdisch lebender Larven zu untersuchen. Anisol, 1,8-Cineol und Terpinolen übten eine anziehende Wirkung auf die Engerlinge aus, während Aceton und β-Caryophyllen abstoßend wirkten. Allgemeine Ergebnisse: Die emittierten Sprossvolatile von Quercus sp. und A. hippocastanum unterscheiden sich deutlich von den entsprechenden Wurzelvolatilen. Reproduzierbare Ergebnisse in elektrophysiologischen Versuchen konnten ausschließlich in den Herbst- und Wintermonaten erzielt werden. Diese Tatsache legt nahe, dass im komplexen neuronalen Reiz- Verarbeitungssystem der Maikäferlarven saisonale und vielleicht auch circadiane Rhythmen eine wichtige Rolle spielen könnten. In Verhaltensexperimenten konnte ein deutliches Orientierungsverhalten der Larven von M. hippocastani in Reaktion auf verschiedene Wurzelvolatile von angefressenen Quercus sp. beobachtet werden. Attraktive und repellente Substanzen konnten identifiziert werden. Die Antennalloben (ALs, erste zentrale Verarbeitungseinheiten für die olfaktorische Informationsverarbeitung im Insektengehirn) von M. hippocastani im
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