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Plant virus infection influences bottom-up regulation of a plant-aphid-parasitoid system

Abstract

Plant viruses strongly influence the physiology of their host plants and phytophagous insect vectors, thereby affecting ecological interactions between them. Despite the important role of natural enemies on insect vector control and thus on virus dissemination, the influence of plant viruses on the third trophic level received little attention. We investigated how infection of the plant Camelina sativa (Brassicaceae) by the Turnip yellows virus (TuYV) influenced the host plant, an aphid vector (Myzus persicae) and an aphid parasitoid (Aphidius colemani) through bottom-up effects on the physiology of the three trophic levels. We also considered the behavioural responses of A. colemani towards infected and control (uninfected) plant-aphid complexes. Highlighting the importance of virus infection on bottom-up regulation of tri-trophic systems, TuYV infection resulted in (1) decreased photosynthetic activity and biomass in C. sativa, (2) an improvement of some aphid fitness parameters important for population dynamics and virus dissemination (i.e. better nymphal survival and shorter pre-reproductive period), but (3) a decrease in some other aphid parameters (i.e. lower body size and quantity of stored energetic resources), which probably explained (4) the decrease in several fitness-related traits (i.e. body size, fecundity and lipid content) in parasitoids developing in aphids reared on infected plants. Female parasitoids showed similar attraction towards control and infected plants, and similar attack and rejection rates towards control and virus-infected aphids. Our results suggest that in agroecosystems, virus presence may reduce parasitoid abundance and consequently biological control of aphid vectors, impacting virus dissemination and plant damage.

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Acknowledgements

We are grateful to Paul Abram, Suzi Claflin and Thomas Seth Davis for helpful comments on earlier drafts of this manuscript. This work was performed in partnership with the SAS PIVERT within the framework of the French Institute for the Energy Transition (Institut pour la Transition Energétique (ITE) P.I.V.E.R.T. (www.institut-pivert.com)), selected as an Investment for the Future (“Investissements d’Avenir”). This work was supported, as part of the Investments for the Future, by the French Government under the reference ANR-001-01.

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Correspondence to Moiroux Joffrey.

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Communicated by M. Jonsson.

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Joffrey, M., Chesnais, Q., Spicher, F. et al. Plant virus infection influences bottom-up regulation of a plant-aphid-parasitoid system. J Pest Sci 91, 361–372 (2018). https://doi.org/10.1007/s10340-017-0911-7

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Keywords

  • Insect physiology
  • Parasitoid behaviour
  • Plant physiology
  • Pathogen
  • Pest control
  • Tri-trophic system