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Defense by Volatiles in Leaf-Mining Insect Larvae

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Abstract

The defense strategy of an insect toward natural enemies can include a trait that appears at first sight to contradict its defensive function. We explored phylogeny, chemistry, and defense efficiency of a peculiar group of hymenopteran sawfly larvae where this contradiction is obvious. Pseudodineurini larvae live in leaf mines that protect them from some enemies. Disturbed larvae also emit a clearly perceptible lemon-like odor produced by ventral glands, although the mine hampers the evaporation of the secretion. The mine could also lead to autointoxication of a larva by its own emitted volatiles. Citral was the major component in all Pseudodineurini species, and it efficiently repels ants. We conclude that full-grown larvae that leave their mine to pupate in the soil benefit from citral by avoiding attacks from ground-dwelling arthropods such as ants. In some species, we also detected biosynthetically related compounds, two 8-oxocitral diastereomers (i.e., (2E,6E)- and (2E,6Z)-2,6-dimethylocta-2,6-dienedial). Synthetic 8-oxocitral proved to be a potent fungicide, but not an ant repellent. The discrete distribution of 8-oxocitral was unrelated to species grouping in the phylogenetic tree. In contrast, we discovered that its presence was associated with species from humid and cold zones but absent in species favoring warm and dry environments. The former should be protected by 8-oxocitral when faced with a fungal infestation while crawling into the soil. Our work shows the importance of integrating knowledge about behavior, morphology, and life history stages for understanding the complex evolution of insects and especially their defense strategies.

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Acknowledgements

JLB performed the GC–MS analyses in the lab of Monika Hilker (Berlin, Germany), with the technical assistance of Frank Müller. Filip De Block provided JLB with ants. Many thanks, also, to the collectors of sawfly specimens used in the genetic analyses and to Tommi Nyman, Herbert R. Jacobson, and two anonymous reviewers for critical and helpful reading of the manuscript. For phylogenetic analyses, funding was provided by the Joint Experimental Molecular Unit (project ECES_PSEU) that is supported by the Belgian Science Policy Office.

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Correspondence to Jean-Luc Boevé.

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Boevé, JL., Sonet, G., Nagy, Z.T. et al. Defense by Volatiles in Leaf-Mining Insect Larvae. J Chem Ecol 35, 507–517 (2009). https://doi.org/10.1007/s10886-009-9627-3

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