Impact of a shared sugar food source on biological control of Tuta absoluta by the parasitoid Necremnus tutae

  • Mateus Ribeiro de Campos
  • Lucie S. Monticelli
  • Philippe Béarez
  • Edwige Amiens-Desneux
  • Yusha Wang
  • Anne-Violette Lavoir
  • Lucia Zappalà
  • Antonio Biondi
  • Nicolas DesneuxEmail author
Original Paper


Honeydew is a sugar-rich food source produced by sap-feeding insects, notably by major pests such as aphids and whiteflies. It is an important alternative food source for the adult stage of various key natural enemies (e.g., parasitoids), but it may be used also as food by agricultural pests. Necremnus tutae is an idiobiont parasitoid, and it is the most abundant larval parasitoid associated with the South American tomato pinworm, Tuta absoluta, in recently invaded European areas. The impact of N. tutae on T. absoluta populations was evaluated under greenhouse conditions with and without the presence of a honeydew producer, the aphid Macrosiphum euphorbiae. In addition, laboratory experiments were performed to evaluate the longevity of N. tutae and T. absoluta adults when fed with water, honey or honeydew produced by the aphid. In the greenhouse, N. tutae effectively reduced T. absoluta population by the end of the experiment, and this independently of the presence of the aphid; still the presence of M. euphorbiae led to delayed and reduced T. absoluta population peak when controlled by the parasitoid (there was a fourfold increase in parasitoid density in presence of aphid). The longevity of both N. tutae and T. absoluta females increased in the presence of honeydew (when compared to water only) under laboratory conditions; it hinted that honeydew could be used by an herbivore as T. absoluta. The interactions between the two phytophagous species showed contrasting effects, and this mostly independently of parasitoid presence. Tuta absoluta had no impact on aphid population dynamics. By contrast, the production of T. absoluta larvae was higher in the first part of the experiment as the adults lived longer (feeding on aphid honeydew) and produced more larvae. In the second part of the experiment, there were fewer T. absoluta larvae in the presence of the aphid, likely owing to resource competition and/or negative plant-mediated indirect interactions. We demonstrated that honeydew producers could impact parasitoid-host population dynamics both through direct and indirect interactions and that potential positive effects of a sugar food source toward a pest can be nullified in the long term by other negative effects occurring simultaneously.


Eulophidae Biological control Solanaceae Gelechiidae Honeydew 



The authors thank the project ASCII (FP7 IRSES no. 318246) for funding to ND and MRC, the University of Catania (Project 2016–2018 “Emergent Pests and Pathogens and Relative Sustainable Strategies—5A722192113) and the Italian Ministry of Education, University and Research (MIUR) (PRIN project 2015 “BIOPIC” No. 2015BABFCF) for funding to AB and LZ, the project STomP (ARIMNET2 no. 618127) for funding to AB, AVL, LZ and ND, the IPM Innovation Lab (USAID Cooperative Agreement no. AID-OAA-L-15-00001) for funding to ND and MRC, and the EUCLID project (H2020-SFS-2014, no. 633999) for funding to PB, EAD and ND.

Author contributions statement

ND and MRC designed the experiment. MRC, PB, EAD and YW performed the bioassays. ND, AVL, AB and LZ provided technical and material supports. LSM and MRC analyzed the data. MRC, LSM and ND led the writing of the manuscript and all authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any studies with human participants or animals (others than insects) performed by any of the authors.


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Copyright information

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

Authors and Affiliations

  • Mateus Ribeiro de Campos
    • 1
  • Lucie S. Monticelli
    • 1
  • Philippe Béarez
    • 1
  • Edwige Amiens-Desneux
    • 1
  • Yusha Wang
    • 1
  • Anne-Violette Lavoir
    • 1
  • Lucia Zappalà
    • 2
  • Antonio Biondi
    • 2
  • Nicolas Desneux
    • 1
    Email author
  1. 1.Université Côte d’Azur, INRA, CNRSUMR ISANiceFrance
  2. 2.University of CataniaDepartment of Agriculture, Food and EnvironmentCataniaItaly

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