title: Improving the efficiency of biological control with parasitoids for Tuta absoluta pest management
Creators: name: Gonthier, Jérémy
Publisher: name: Universität Bern
Year: 2024
Subjects: subject: 570 Life sciences; biology
subject: 580 Plants (Botany)

description: New sustainable strategies to control pest insects are required to reduce harmful effects on the environment and the rise of pesticide resistance. Tuta absoluta, also known as the tomato leafminer, is a major pest of tomato native to South America. It has since spread to other parts of the world, including Europe, Asia, Africa, and the Middle East, causing significant economic losses to tomato growers. The pest is highly destructive, with the potential to cause up to 100% loss in tomato crops if left untreated. It is extremely challenging to control due to its high population increase, wide host range, cryptic behavior, and pesticide resistance. Managing this pest requires an integrated approach that combines different control methods. Regarding biological control, parasitoids can be very effective agents; however, their use presents several challenges that remain to be addressed. 
Trichogramma spp. are generalist egg parasitoids widely used as biological control agents and have been proposed to control T. absoluta. Trichogramma wasps are commercially available and can be released in tomato fields at the early stages of crop development to prevent or reduce infestations. Nevertheless, their efficacy is limited, partially due to the low attraction to infested tomato plants. Studies demonstrated that female Trichogramma spp. could learn odor cues affecting their preference. In the first part of the project, we assessed whether learning increases the response to tomato odor and improves the parasitism rate of three species of Trichogramma. Associative learning with the tomato odor (leaves or extract) increased the searching time of T. achaeae and T. evanescens strongly. Rearing the parasitoids on T. absoluta for one generation increased the response of T. dendrolimi strongly and that of T. evanescens slightly. Concerning parasitism improvement, only associative learning with T. achaeae resulted in an increased parasitism rate in small-scale cage experiments. Therefore, the learning capacity of T. achaeae could be further explored to improve its biological control efficacy against T. absoluta.
Besides Trichogramma spp., several larval parasitoids have been found attacking T. absoluta, including Necremnus tutae in Europe and Dolichogenidea gelechiidivoris in South America. N. tutae is particularly abundant around the Mediterranean basin, and its role in naturally controlling the pest population is well studied. D. gelechiidivoris is an essential agent against T. absoluta in its native range and has recently been introduced intentionally into Kenya to help control T. absoluta. Recently, D. gelechiidivoris established unintentionally in Spain and Algeria.
Combining parasitoids with entomopathogen microorganisms such as baculoviruses is an emerging strategy to improve efficiency. Baculoviruses are a family of insect viruses successfully used as a biological control agent against several lepidopteran pests. Specifically, the Phthorimaea operculella granulovirus (PhopGV) has shown promising results in controlling T. absoluta populations in the field. Baculoviruses are highly specific to their target pests, killing the larvae of T. absoluta but not infecting other beneficial insects or non-target organisms. However, the efficacy of baculoviruses is highly dependent on the right timing and is sometimes limited, calling for complementary measures. Combining them with macroorganisms like parasitoids can improve the control efficiency, especially if each agent targets different host instars.
Therefore, in the second part of the project, we studied the interactions between larval parasitoids and baculoviruses. The aim was to evaluate the compatibility of PhopGV and the release of larval parasitoids to control T. absoluta. First, indirect non-target effects of baculoviruses on parasitoids can result from overlapping resource requirements and resource competition. Hence, we evaluated whether ovipositing parasitoid females avoided virus-treated hosts and the impact of within-host competition between two parasitoid species, N. tutae and D. gelechiidivoris, and PhopGV. The results showed that female D. gelechiidivoris avoided virus-treated hosts, but N. tutae did not discriminate. The virus had limited indirect effects on parasitoid offspring, with outcomes varying depending on the parasitoid species, sex, and timing of virus treatment. Overall, the virus had a low impact on parasitoid offspring, and the adverse effects detected are unlikely to reduce their fitness significantly. Therefore, both parasitoid species are compatible with the baculovirus as a control strategy for T. absoluta.
Large-scale experiments are crucial for evaluating the effectiveness of new control strategies and provide essential information to understand the effect over time at the population level. The importance of additive effects between parasitoids and baculovirus on pest population ─ and the relevance of such effects for pest control ─ remain largely unexplored. Therefore, we evaluated the efficacy of combining the baculovirus with the parasitoid N. tutae in greenhouse experiments. In term of pest reduction and plant damage, we found no significant reduction in the combination compared to each agent alone, although the combination constantly resulted in the the strongest absolute reduction. The parasitoid N. tutae alone or in combination with the baculovirus reduced the adult pest density equally, but less reduction was found for the baculovirus alone over the whole trial. Nevertheless, using the virus alone resulted in the strongest reduction of adult density in the third generation. Finally, each agent achieved the same plant damage reduction alone or in combination.
Modeling is an important tool for evaluating and improving biological control programs because it allows for predicting the outcome of different control strategies. Models can help to identify the most effective and sustainable approach by simulating the interactions between pests, natural enemies, and the environment. Parasitoids' efficiency is highly sensitive to the timing and amount of release. Thus, in the third part of this project, we developed a modeling framework to determine the optimal timing and frequency of interventions and the potential impact of baculovirus on pest populations and parasitoid efficiency. By integrating data from the greenhouse experiment, our model provides a comprehensive understanding of the dynamics of pest populations and the effectiveness of different control strategies. For instance, we demonstrate with our model that baculovirus application reduces the number of required parasitoids by almost 80%.
Finally, high host-specificity reduces the risk of ecological disturbance and enhances the parasitoid's efficiency in finding and attacking its host species. Thus, in the last chapter, we focused on understanding the trophic connections between the parasitoids D. gelechiidivoris and N. tutae, the target host T. absoluta and different non-target hosts. We evaluated the potential risks of using the parasitoid N. tutae and D. gelechiidivoris as biological control agents by conducting host-specificity testing in the laboratory. We also assess parasitization preference in the field. According to our findings, N. tutae is quite polyphagous, whereas D. gelechiidivoris is more specific. In the greenhouses, the parasitism rate for N. tutae was 27%, while for D. gelechiidivoris, it reached 35%. Our study highlights the significance of host affinity in comprehending the possible non-target impacts and underscores the potential value of these two parasitoids as a classical biological control.
Overall, this work provides promising ways for developing sustainable biological control of T. absoluta using parasitoids. We highlighted the importance of using multiple agents in the studied agroecosystem and clarified the role of each in the success or failure of biological control programs. The efficacy of these agents can be limited, but various strategies exist and have a large potential for improvement. In addition, a tool is provided that can aid future research: a modeling framework to test various combinations of micro and macroorganisms.