Multitrophic Interactions and Biocontrol

The MIB team (resulting from the merger of the CEA and ESIM teams) produces fundamental and applied knowledge on multitrophic interactions including the physiology of the pests and the role of their symbionts, this of the biocontrol agents (BCA) and the effect of biotic (i.e. banker plants) and abiotic conditions (i.e. Fertilization, water…) on the pests-BCA interactions. This work is carried out with both a fundamental and applied goal aimed at optimizing and increasing the sustainability of integrated pest management (IPM) programs. The involvement in both mechanistic and finalized aspects gives the team an internationally recognized expertise. Our approach is part of the development of innovative and sustainable biocontrol approaches for the development of agroecology.

Diagram representing the different levels of trophic interactions taken into account in the approaches developed by the team.

The team's projects fall into four main themes:

1  Behavioural, physiological and ecological factors modulating the specialization of auxiliaries used in biological control

This concerns the study of the biology of parasitoid wasps, auxiliaries used in biological control, including behavioral ecology and the determinants of their specialization. Indeed, we lack knowledge about the factors that shape the host range of parasitoids (and more broadly of biological control agents), which limits the choice of the most effective auxiliaries and realistic risk assessments. The host/prey range test is a key selection criterion for biological control agents to identify the species with the best compromise between (a) efficacy against the pest and (b) specialization on this pest (Fig. 1).

Figure 1: Specificity index (STD*) values and classification of aphid parasitoids according to their degree of specialization. (Monticelli, L. S., et al. Evolutionary Applications 12, eva.12822-15 (2019).

The team studies 1) the determinants (behavioral, physiological, phylogenetic and ecological) of host specificity in biological control auxiliaries (aphid parasitoids, phytophagous, etc.); 2) the physiological host range of these auxiliaries that are (i) candidates in biological control programs for invasive pests and/or (ii) candidates in biological control programs by conservation (involving, for example, the use of service plants); (3) their effective host range and potential ecological filters (including the effect of bacterial endosymbionts). Knowledge of the behavioural, physiological and ecological basis of the host range can also help to assess the risk of potentially deleterious impacts on non-target species (an issue increasingly considered in conventional and augmentative biological control).

At the molecular level, we are interested in the venom injected by parasitoid wasps during oviposition, which inhibits the host's immune response, modifies its metabolism and behavior. Our work on parasitoid-Drosophila models and on other parasitoids has shown that the composition of parasitoid venom is complex and varies not only between taxa, but also between closely related species, as well as between strains and individuals of the same species. Between strains of the same species, most of these variations appear to be quantitative, although some may be due to the presence of different alleles. In addition, this venomous "cocktail" can evolve according to the resistance of the proposed host and be affected by geographical isolation conditions (Fig. 2) or by abiotic effects such as temperature. Ongoing work seeks to understand the mechanism underlying the of venom proteins effect in host and the adequacy between the venomous "cocktail" and the potential host spectrum of the parasitoid.

Figure 2. SDS-PAGE for venom analysis. Example of SDS-PAGE gels used to characterize the variation in the composition of the venoms of Leptopilina boulardi (A) and Leptopilina heterotoma (B), two drosophila parasitoids. Each lane contains the venom of a single wasp whose original population from France is indicated (Ey, Eyguières; Avignon; SFL, Ste Foy-Lès-Lyon; SLA, St Laurent d'Agny; Mo, Montbellet ; V, Vence; So, Sonnay; Ep, Epinouze; Uch, Uchizy). Reference bands that significantly discriminate populations are shown. According to Mathé-Hubert, H., et al. Frontiers in Ecology and Evolution 7, 318-17 (2019).

The team is also collaborating with the IGEPP-INRAE team in Rennes to evaluate, under natural conditions, the ability of the parasitoid Aphidius ervi to adapt to the protection conferred to the pea aphid Acyrthosiphon pisum by a secondary endosymbiont, the bacterium Hamiltonella defensa. As parasite success is linked to venom injection, we started the analysis of the protein profiles of the venoms of different A. ervi lines in order to identify possible variations associated with the virulence profiles. This project will allow us to better understand the role of venom in parasitic success against aphids and their endosymbionts.

All of this work is part of the understanding of the mechanisms of evolution of host resistance and parasitoid virulence. Understanding the evolutionary processes affecting the success and failure of biological control agents, and characterizing the genomic basis of the traits involved in such success/failure, are critical steps in developing innovative and sustainable approaches to managing pest species

2  How functional plant diversity can improve biocontrol services?

The necessary changes of agroecological practices to adapt to a low or no pesticide practices is often accompanied by a diversification of the agrosystems, with an increase in varietal diversity, the implementation of polyculture or rotational crops, or the enhancement of natural biodiversity for biological control through conservation. However, questions remain, particularly concerning the choice of plant species to be used and their management (spatial and temporal management with regard to the targeted crops, use of multi-service plants or simultaneous use of several service plants, etc.).

One of the team objectives is to define the biological, agronomic and ecological factors that condition the effectiveness of IPM levers based on service plants, and to formalize decision rules and indicators to effectively use these levers (Fig. 3). In the short and medium term, we aim to identify versatile biocontrol plants useful for controlling multiple pests, as well as to identify the underlying mechanism(s) that allow this. From a multi-service perspective (including multi-pest targeting), it remains to be determined whether a versatile plant is more interesting than a combination of plants.

Figure 3. Direct and indirect effects of biocontrol plants on crop pests (after Djian-Caporalino & Lavoir 2024).

3  Unintended impacts of biopesticides and more generally of biocontrol methods

Synthetic pesticides are now reaching their limits due to pest resistance, their high persistence in the environment, and also to their demostrated adverse impact on biodiversity and human health. For these reasons, botanical biopesticides are receiving a renewed attention. These biopesticides could be combined with biological control agents to implement more environmentally friendly IPM strategies (Fig. 4). However, the use of these biopesticides can also have some side effects on non-target organisms, including natural enemies that are beneficial to agroecosystems. In addition, the development of pest resistance to biopesticides must be considered in the same way as for synthetic pesticides. In this context, the design of a matrix listing the unintended effects of all biocontrol methods will provide a more global view of knowledge on the potential negative effects of these different control strategies and identify avenues to minimize undesirable effects (ENI, SUMCROP, INRAE network). As part of the European ADOPT-IPM project, which is based on our expertise in the toxicology of phytosanitary products of natural or conventional origin, we are studying the effects of botanical pesticides on target (pests) and non-target (predators, parasitoids) species in the laboratory, and we will look for the possible induction of resistance in pests (after exposure to a single substance and a mixture of molecules).

Figure 4. Use of concepts and tools from ecology and ecotoxicology to analyze the unintended effects of biocontrol solutions. From Amichot, M. et al, Environmental Science and Pollution Research, 34, (2018).

4  Playing on bottom-up effects to adapt biocontrol strategies

In the agroecological transition model, the first step to reduce chemical inputs is the demonstration that a similar productivity could be achieved. Our work has demonstrated that it is possible to reduce inorganic fertilizers (nitrogen) to an intermediate level while maintaining a good yield and also an efficient biocontrol service. We continue our efforts to identify general bottom-up effect patterns to facilitate the development of optimized IPM strategies (Fig. 5). The second step is to replace chemical inputs with biological inputs. We are thus testing the bottom-up effects of organic fertilizers on identified predator-prey interactions. In addition, in collaboration with the IRL team at ISA, we are studying the immune priming effect of the plant provided by root symbiosis against pea aphids. We seek to determine which immune and metabolic defense pathways are involved, and we will look at how plant symbiosis impacts the second and third trophic levels, for example by attracting aphid predators.

Figure 5. IPM strategies involving bottom-up effects on the "plant-herbivore-natural enemy" food chain. According to Han, P., et al., Annu. Rev. Entomol. 67, (2021).

Collaborations :

Local : équipes ISA RDLB, BES, IPN, BPI, IRL, M2P2, plateaux techniques de l’ISC PlantBIOs, UCA ICN…

National : IGEEP Rennes, DJIMI Montpelier, INSA Lyon, Université de Tours, INRAE Avignon, LAE Nancy, Agroecology Dijon, ASTRO Guadeloupe…

European : Université Catane, Naples et Pise, IRTA, IVIA, …

International : Chine, USA, Brésil, Mexique, …

Partnerships with private companies (Agrobio) and professional organizations (CTIFL, Astredhor, etc.).

Funding: INRAE (SPE, SumCrop), ARS, Ecophyto, PEPR, Parsada, Europe, etc.

Publications : > https://hal.inrae.fr/ISA-SOPHIA/?lang=en