Title of M2 stage : Does intraguild predation challenge herbivore biocontrol ?
Stage supervisor : Enric Frago (UMR CBGP)
Duration : 6 months
Salary : based on « grille officielle ».
Location : UMR-CBGP, Montferrier-sur-Lez (à proximité de Montpellier).

General context
The success of biocontrol using natural enemies against pests relies on deep ecological knowledge of species interactions. Biocontrol is usually enhanced at higher natural enemy diversity, a relationship known as the biodiversity-biocontrol relationship (Dainese et al., 2019; Snyder & Tylianakis, 2012). This relationship emerges through the “complementarity effect” whereby assemblages of different enemies facilitate each other by exploiting prey of different stages, or at different spatio-temporal scales (Pekas et al., 2016; Perović et al., 2018; Snyder, 2019). The positive effect of natural enemy diversity on biocontrol, however, can be dampened by “antagonistic effects” among enemies (Frago, 2016; Polis & Holt, 1992; Snyder & Tylianakis, 2012). One of the antagonistic interactions that worries biocontrol stakeholders the most is intraguild predation, which occurs when two predators that share a prey also feed on each other. This belief is in contrast with some theoretical models (and some of our preliminary data) that suggest that over multiple generations (i.e. long-term dynamics), intraguild predation can stabilise the dynamics of multiple prey because it can prevent prey overexploitation by consumers (Frago, 2016; Polis & Holt, 1992). At the experimental level, however, the conditions under which intraguild predation enhance or impair biocontrol are little understood. Studies that explore the dynamics of communities over multiple generations are particularly important to understand the conditions leading to lasting biocontrol, and the long-term persistence of natural enemies engaging in intraguild predation. This MSc project is part of a larger ANR project entitled ENEMYCOCKTAIL « Designing natural enemy cocktails for a better biocontrol », which aims at finding out the best enemy combinations to control pest aphids and spider-mites.

Objective
The main objective of the project is to explore whether long-term biocontrol services will be stronger or weaker when enemies engage in intraguild predation.

The experimental system
We will work with an important polyphagous pest, the green peach aphid, Myzus persicae. We will use six natural enemies associated with this pest, all of them mass produced by our industrial partner Biobest (Biobest Group, 2021). We will manipulate two different communities and combine single vs dual enemy combinations, always including an intraguild prey (a predator that is eaten by another predator) and an intraguild predator (a predator that eats other predators). (1) The first community will be composed of the parasitic wasp Aphidius colemani, the ladybird Adalia bipunctata, and the lacewing Micromus angulatus. In this community the ladybird and the lacewing are the intraguild predators, and the parasitoid wasp is the intraguild prey. The parasitoid will suffer predation from the ladybird and the lacewing because parasitoid eggs and larvae inside aphids can be eaten when larger predators feed on aphids. (2) The second community will be composed of the gall midge Aphidoletes aphidimyza, and the predatory bugs Macrolophus pygmaeus and Orius laevigatus. In this community the larger-sized predatory bugs are the intraguild predators because they can feed on aphids, but also on the midge, which is the smaller-sized intraguild prey.

MSc plan, methods and techniques
For each community, we will test in the laboratory the effect of intraguild predation on biocontrol by testing the effect of each enemy independently, or in combination of two enemies (one intraguild prey and one intraguild predator). This will lead to a total of five different modalities per community, each replicated eight times in Bugdorm population cages of 40x40x40cm. We will monitor the long-term multi-generational dynamics of these communities [as we previously did in Sanders et al., 2016)]. Such dynamics will allow us to assess lasting biocontrol, and enemy persistence through time. The industrial partner will provide herbivores and natural enemies (Biobest Group, 2021). We will count the insects weekly during two months, and replace plants weekly. We will analyse aphid density through time as a proxy for biocontrol, and enemy persistence with a survival analysis (as in Sanders et al., 2016). These analyses will be performed using R. The student should be a keen entomologist, with good writing skills and interested in insect-plant and predator-prey interactions, and statistical analyses using mixed models. We will also use the R code editor RStudio and the reference manager Zotero. Getting mechanistic insights into the results obtained through Lotka-Volterra predator-prey simulations is also possible. All geographic origins, orientations and identities are welcome.

Keywords
Aphids, biocontrol, community ecology, microcosm experiments, predator-prey dynamics.

Partnership
This project will involve collaboration with all partners of the ANR project ENEMYCOCKTAIL, and particularly with Dr. Apostolos Pekas (Senior Scientist of R&D, Biobest Belgium) who will provide expertise in natural enemy biology, and will ensure access to the different enemies needed for the project.

References (references from the applicant are in bold):
– Biobest Group. (2021). Https://www.biobestgroup.com/fr/biobest/produits/lutte-biologique-contre-les-ravageurs-4459/.
– Dainese, M. et al (2019). A global synthesis reveals biodiversity-mediated benefits for crop production. Scientific Advances, 1–14.
– Frago, E. (2016). Interactions between parasitoids and higher order natural enemies: Intraguild predation and hyperparasitoids. Current Opinion in Insect Science, 14, 81–86.
– Hajek, A. E., & Eilenberg, J. (2018). Natural Enemies: An Introduction to Biological Control. Cambridge University Press.
– Pekas, A., Tena, A., Harvey, J. A., Garcia-Mari, F., & Frago, E. (2016). Host size and spatiotemporal patterns mediate the coexistence of specialist parasitoids. Ecology, 97(5), 1345–1356.
– Perović, D. J., Gámez-Virués, S., Landis, D. A., Wäckers, F., Gurr, G. M., Wratten, S. D., You, M. S., & Desneux, N. (2018). Managing biological control services through multi-trophic trait interactions: Review and guidelines for implementation at local and landscape scales. Biological Reviews, 93(1), 306–321.
– Polis, G. A., & Holt, R. D. (1992). Intraguild Predation—The Dynamics of Complex Trophic Interactions. Trends In Ecology & Evolution, 7(5), 151–154.
– Sanders, D., Kehoe, R., van Veen, F. F., McLean, A., Godfray, H. C. J., Dicke, M., Gols, R., & Frago, E. (2016). Defensive insect symbiont leads to cascading extinctions and community collapse. Ecology Letters, 19(7), 789–799.
– Snyder, W. E. (2019). Give predators a complement: Conserving natural enemy biodiversity to improve biocontrol. Biological Control, 135, 73–82.
– Snyder, W. E., & Tylianakis, J. M. (2012). The Ecology of Biodiversity-Biocontrol Relationships. In Biodiversity and Insect Pests: Key Issues for Sustainable Management (pp. 21–40).

Contact
If interested send an email to enric.frago@cirad.fr with a CV and a motivation letter (in English or French) including in the subject of the email « Candidature M2 Pucerons ».

Le contenu de cette offre est la responsabilité de ses auteurs. Pour toute question relative à cette offre en particulier (date, lieu, mode de candidature, etc.), merci de les contacter directement. Un email de contact est disponible: enric.frago@cirad.fr

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