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

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.

Microbial Biocontrol Strategies for Ambrosia Beetles and Their Associated Phytopathogenic Fungi

“…Compound βcaryophyllene, previously described as a potential biofumigant, was also dominantly emitted by the ambrosia fungus F. solani (Egonyu and Torto, 2018). In particular, ambrosia beetles exhibited a strong attraction to ethanol, which is also emitted by susceptible host trees (Ranger et al, 2021) and has been reported to promote the growth of fungal symbionts Ambrosiella spp. while reducing that of other competing fungi (Ranger et al, 2018).…”

“…Interestingly, the use of fungal VOCs has also been explored as lures for ambrosia beetles Egonyu and Torto, 2018;Ranger et al, 2021), as beetles showed to be particularly attracted to VOCs emitted by their fungal symbionts. Alcohols such as ethanol, 2-methyl-1-propanol and 3-methyl-1-butanol were detected in the volatile profiles of Ambrosiella sp., R. lauricola, and F. solani associated with Xylosandrus compactus (Kuhns et al, 2014;Egonyu and Torto, 2018).…”

“…Ambrosia beetles (Coleoptera: Platypodinae and Scolytinae) are a group of wood-boring insects that characteristically colonize stressed or recently dead trees, burrowing galleries into their hosts where they inoculate and culture their fungal symbionts as a food source for their larvae and maturing adults (Farrell et al, 2001;Biedermann and Taborsky, 2011;Huang et al, 2019). In turn, ambrosia fungi depend on their beetle vectors for dispersal (Ranger et al, 2021), as their spores are transported by the beetles in specialized sac-like structures named mycangia, thus facilitating fungal propagation among host trees (Batra, 1963). Fungi in the ambrosia symbiosis have been identified in at least seven families (Ophiostomataceae, Ceratocystidaceae, Nectriaceae, Bionectriaceae, Saccharomycetaceae, Peniophoraceae, and Meruliaceae) and dominantly belong to the genera Ambrosiella, Fusarium, and Raffaelea (Harrington et al, 2010;Huang et al, 2019;Ranger et al, 2021).…”

“…In turn, ambrosia fungi depend on their beetle vectors for dispersal (Ranger et al, 2021), as their spores are transported by the beetles in specialized sac-like structures named mycangia, thus facilitating fungal propagation among host trees (Batra, 1963). Fungi in the ambrosia symbiosis have been identified in at least seven families (Ophiostomataceae, Ceratocystidaceae, Nectriaceae, Bionectriaceae, Saccharomycetaceae, Peniophoraceae, and Meruliaceae) and dominantly belong to the genera Ambrosiella, Fusarium, and Raffaelea (Harrington et al, 2010;Huang et al, 2019;Ranger et al, 2021).…”

Characterization of olfactory sensory neurons in the striped ambrosia beetle Trypodendron lineatum

“…For example, fungi that release higher amounts of 3-methyl-1-butyl acetate, 2-methyl-1-butyl acetate and 2-phenetyl acetate are highly attractive ( Kandasamy et al, 2019 , 2023 ) . Other studies have shown that several species of ambrosia beetles in the Xylosandrus , Xyleborus , and Xyleborinus genera are attracted to their fungal symbiont odors and the response may be modulated by the addition of compounds such as ethanol ( Hulcr et al, 2011 ; Egonyu and Torto, 2018 ; Ranger et al, 2021 ). In addition, recent electrophysiological studies of the OSNs in I. typographus revealed several abundant OSN classes specifically tuned to odors derived from I. typographus fungal symbionts ( Kandasamy et al, 2019 , 2023 ).…”