, Volume 191, Issue 1, pp 113–125 | Cite as

Bottom-up regulation of a tritrophic system by Beet yellows virus infection: consequences for aphid-parasitoid foraging behaviour and development

  • Loulou AlbittarEmail author
  • Mohannad Ismail
  • Gertrud Lohaus
  • Arnaud Ameline
  • Bertanne Visser
  • Claude Bragard
  • Thierry Hance
Plant-microbe-animal interactions – original research


Effects of plants on herbivores can cascade up the food web and modulate the abundance of higher trophic levels. In agro-ecosystems, plant viruses can affect the interactions between crops, crop pests, and natural enemies. Little is known, however, about the effects of viruses on higher trophic levels, including parasitoids and their ability for pest regulation. We tested the hypothesis that a plant virus affects parasitoid foraging behaviour through cascading effects on higher trophic levels. We predicted that the semi-persistent Beet yellows virus (BYV) would influence plant (Beta vulgaris) quality, as well as aphid host (Aphis fabae) quality for a parasitoid Lysiphlebus fabarum. We determined amino acid and sugar content in healthy and infected plants (first trophic level), lipid content and body size of aphids (second trophic level) fed on both plants, as well as foraging behaviour and body size of parasitoids (third trophic level) that developed on aphids fed on both plants. Our results showed that virus infection increased sugars and decreased total amino acid content in B. vulgaris. We further observed an increase in aphid size without modification in host aphid quality (i.e., lipid content), and a slight effect on parasitoid behaviour through an increased number of antennal contacts with host aphids. Although the BYV virus clearly affected the first two trophic levels, it did not affect development or emergence of parasitoids. As the parasitoid L. fabarum does not seem to be affected by the virus, we discuss the possibility of using it for the development of targeted biological control against aphids.


Closterovirus Trophic interactions Semi-persistent virus Host suitability Plant quality Disease vector Cascading effect 



This study was supported by a PhD fellowship from the Université catholique de Louvain in Belgium. We thank Gwennaël Bataille for his helpful comments on the statistical analyses. We are grateful to Aude Couty (UPJV, France) for her critical comments on the manuscript and for revision of the English text. This publication is BRC 435 of the Biodiversity Research Centre.

Author contribution statement

LA, CB and TH conceived and designed the experiments. LA performed the experiments. LA and MI analysed the data. GL analysed amino acid and sugar content. LA, MI, and BV wrote the manuscript. TH, AA and CB reviewed and edited the paper.


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Loulou Albittar
    • 1
    Email author
  • Mohannad Ismail
    • 1
  • Gertrud Lohaus
    • 2
  • Arnaud Ameline
    • 3
  • Bertanne Visser
    • 1
  • Claude Bragard
    • 1
  • Thierry Hance
    • 1
  1. 1.Biodiversity Research Centre, Earth and Life InstituteUCLouvainLouvain-la-NeuveBelgium
  2. 2.Molecular Plant Science/Plant BiochemistryBergische Universität WuppertalWuppertalGermany
  3. 3.UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés)Université de Picardie Jules VerneAmiens CedexFrance

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