Electrophysiological and Behavioral Responses of an Ambrosia Beetle to Volatiles of its Nutritional Fungal Symbiont

Christopher M Ranger,Karla Addesso,Matthew Ethington,Michael E Reding,Marek Dzurenko,Jenny Barnett,Ruchika Geedi,Matthew Ginzel,Louela Castrillo

doi:10.1007/s10886-021-01263-0

Abstract

Ambrosia beetles (Coleoptera: Scolytinae) cultivate their fungal symbiont within host substrates as the sole source of nutrition on which the larvae and adults must feed. To investigate a possible role for semiochemicals in this interaction, we characterized electrophysiological and behavioral responses of Xylosandrus germanus to volatiles associated with its fungal symbiont Ambrosiella grosmanniae. During still-air walking bioassays, X. germanus exhibited an arrestment response to volatiles of A. grosmanniae, but not antagonistic fungi Beauveria bassiana, Metarhizium brunneum, Trichoderma harzianum, the plant pathogen Fusarium proliferatum, or malt extract agar. Solid phase microextraction-gas chromatography-mass spectrometry identified 2-ethyl-1-hexanol, 2-phenylethanol, methyl benzoate and 3-methyl-1-butanol in emissions from A. grosmanniae; the latter two compounds were also detected in emissions from B. bassiana. Concentration-responses using electroantennography documented weak depolarizations to A. grosmanniae fungal volatiles, unlike the comparatively strong response to ethanol. When tested singly in walking bioassays, volatiles identified from A. grosmanniae elicited relatively weak arrestment responses, unlike the responses to ethanol. Xylosandrus germanus also exhibited weak or no long-range attraction to the fungal volatiles when tested singly during field trials in 2016–2018. None of the fungal volatiles enhanced attraction of X. germanus to ethanol when tested singly; in contrast, 2-phenylethanol and 3-methyl-1-butanol consistently reduced attraction to ethanol. Volatiles emitted by A. grosmanniae may represent short-range olfactory cues that could aid in distinguishing their nutritional fungal symbiont from other fungi, but these compounds are not likely to be useful as long-range attractants for improving detection or mass trapping tactics.

Highlights

Ambrosia beetles (Curculionidae: Scolytinae and Platypodinae) are characterized by their obligate symbiosis with fungi (Hulcr et al 2015)
As X. germanus oriented along a walking platform towards a light source (Fig. 1a, b), individual beetles spent a significantly longer duration arrested over a culture of A. grosmanniae compared to B. bassiana, M. brunneum, T. harzianum, F. proliferatum, and a MEA control (Fig. 1c)
At 40 μg, X. germanus spent a longer duration of time over filter paper treated with 2-ethyl-1-hexanol and 2-phenylethanol compared to methyl benzoate; the shortest duration of time was spent over filter paper treated with mineral oil (Fig. 1d)

Summary

Introduction

Ambrosia beetles (Curculionidae: Scolytinae and Platypodinae) are characterized by their obligate symbiosis with fungi (Hulcr et al 2015). Dispersing female xyleborine beetles carry spores of their fungal symbiont(s) within mycetangia in the form of pits, grooves, sacs, or invaginated pouches (Hulcr et al 2015; Vega and Biedermann 2020). The fungal symbionts are mainly in the genera Ambrosiella, Fusarium, and Raffaelea and rely on ambrosia beetles for dispersal and propagation (Kostovcik et al 2015; Mayers et al 2015; Wingfield et al 2017). During tunnel excavation by female xyleborine beetles into host trees, spores are transferred to the tunnel walls for establishing fungal. Females begin ovipositing eggs after sowing the fungal symbiont that serves as the sole source of nourishment for developing larvae and maturing adults (Biedermann and Taborsky 2011)

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