Volatile-mediated location of mutualist host and toxic non-host microfungi by Drosophila larvae

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In analogy to herbivores, fungivorous animals may find suitable host fungi using fungal volatiles as infochemicals and to distinguish between fungi of varying suitability. This study tests the influence of volatiles emitted by micro-fungi, yeast and mould, on the foraging behaviour of facultative fungivorous Drosophila melanogaster larvae. We hypothesised that establishing or avoiding contact with edible yeast (host fungus) and inedible, toxic mould (non-host fungus) is regulated by fungus-specific variation in volatile production. In particular, we expected the non-host fungus to produce specific volatiles that repel fly larvae and thus contribute to signal inedibility. By quantifying innate variation in arrival of individual D. melanogaster larvae at colonies of the mutualist yeast Candida californica or of the antagonistic mould Penicillium expansum, we found the yeast to attract more rapidly a larger number of larvae than the mould did. The developmental stage (young, vegetative vs. old, sporulating) of P. expansum did not affect arrival of larvae at fungal colonies. We used gas chromatography coupled with mass spectrometry (GC–MS) to identify the composition of fungal volatiles. Four compounds appeared to be yeast-specific, twenty to be mould-specific volatiles. Eight volatiles were consistently produced by both young and old P. expansum. Two compounds, 3-methyl-1-butanol and 2-methyl-1-propanol, were released by P. expansum (young and old) as well as C. californica. Time-dependent behavioural response profiles of ~750 D. melanogaster larvae revealed innate attraction to three alcohols produced by yeast and/or moulds and to two yeast-specific organic acids. We found no indication of a repellent effect of mould-specific compounds, including terpenoids like geosmin known to elicit strong avoidance behaviour of adult D. melanogaster in response to harmful microbes. Also, synthetic mould and yeast-specific blends of attractive compounds were equally attractive to the larvae. With respect to the species combinations investigated in this study, we hypothesize that qualitative differences in fungal volatile profiles are of minor relevance in how Drosophila larvae locate and probably discriminate between fungi of varying suitability.