Alan Kergunteuil

Biological Control beneath the Feet: A Review of Crop Protection against Insect Root Herbivores

Sustainable agriculture is certainly one of the most important challenges at present, considering both human population demography and evidence showing that crop productivity based on chemical control is plateauing. While the environmental and health threats of conventional agriculture are increasing, ecological research is offering promising solutions for crop protection against herbivore pests. While most research has focused on aboveground systems, several major crop pests are uniquely feeding on roots. We here aim at documenting the current and potential use of several biological control agents, including micro-organisms (viruses, bacteria, fungi, and nematodes) and invertebrates included among the macrofauna of soils (arthropods and annelids) that are used against root herbivores. In addition, we discuss the synergistic action of different bio-control agents when co-inoculated in soil and how the induction and priming of plant chemical defense could be synergized with the use of the bio-control agents described above to optimize root pest control. Finally, we highlight the gaps in the research for optimizing a more sustainable management of root pests.

Selecting volatiles to protect brassicaceous crops against the cabbage root fly, Delia radicum

Volatiles resulting from plant–herbivore interactions play an important role in the behavioral decisions of phytophagous, predatory, and parasitoid insects and could be used for managing pest insects. However, to date and after about 40 years of research, documented studies on applications in the field remain extremely scarce. Delia radicum L. (Diptera: Anthomyiidae), the cabbage root fly, is a major pest of brassicaceous crops for which classical control strategies are currently lacking. Our previous studies showed that dimethyl disulfide (DMDS), a compound emitted by roots heavily infested by D. radicum larvae, was attractive for the fly’s main natural enemies and could lead to a reduction of 60% in number of eggs laid on treated plants in the field. As a follow‐up of this work, we conducted another field study to select additional volatiles that could be used in a push–pull approach. Several synthetic herbivore‐induced plant volatiles, selected on the basis of their potential action on the behavior of both the fly and its natural enemies, were placed in odor dispensers in experimental broccoli plots and their influence on oviposition by D. radicum and egg predation by ground‐dwelling predators was assessed. Our results confirmed the role of DMDS in reducing D. radicum egg numbers on broccoli plants and revealed that (Z)‐3‐hexenyl acetate, a green leaf volatile released by recently damaged plants, strongly stimulated fly oviposition. Also, two of the compounds tested slightly modified predation activity of ground‐dwelling predators: acetophenone decreased the proportion of predated patches, whereas methyl salicylate increased it. This study is a first step in designing a push–pull strategy to control the cabbage root fly.

Characterizing Volatiles and Attractiveness of Five Brassicaceous Plants with Potential for a ‘Push-Pull’ Strategy Toward the Cabbage Root Fly, Delia radicum

Volatile Organic Compounds (VOCs) released by plants are involved in various orientation processes of herbivorous insects and consequently play a crucial role in their reproductive success. In the context of developing new strategies for crop protection, several studies have previously demonstrated the possibility to limit insect density on crops using either host or non-host plants that release attractive or repellent VOCs, respectively. The cabbage root fly, Delia radicum, is an important pest of brassicaceous crops for which control methods have to be implemented. Several studies have shown that plant odors influence cabbage root fly behavior, but only few VOCs have been identified so far. The present study aimed at selecting both plants and olfactory stimuli that could be used in the development of a “push-pull” strategy against the cabbage root fly. Olfactometer results revealed that plants belonging to the same family, even to the same species, may exhibit different levels of attractiveness toward D. radicum. Plants that were found attractive in behavioral observations were characterized by high release rates of distinct terpenes, such as linalool, β-caryophyllene, humulene, and α-farnesene. This study represents a first step to identify both attractive plants of agronomic interest, and additional volatiles that could be used in the context of trap crops to protect broccoli fields against the cabbage root fly.

The Abundance, Diversity, and Metabolic Footprint of Soil Nematodes Is Highest in High Elevation Alpine Grasslands

Nematodes are key components of soil biodiversity and represent valuable bio-indicators of soil food webs. Numerous community indices have been developed in order to track variations in soil ecosystem processes, but their use is mainly restricted to anthropogenic stresses. In this study, we propose to expand the use of nematodes’ derived ecological indices in order to shed light on variations of soil food webs in natural systems distributed along elevation gradients. For this purpose, we aimed at determining how elevation affects the community structure and the trophic diversity by studying the abundance, the composition and the functional diversity of nematode communities. Nematode communities were sampled every 200 m across five transects that span about 2000 m in elevation in the Alps. To understand the underlying ecological parameters driving these patterns we studied both abiotic factors (soil properties) and biotic factors (trophic links, relationships with plant diversity). We found that (1) nematode abundance increases with elevation of lowland forests and alpine meadows; (2) differences in nematodes communities rely on habitat-specific functional diversity (e.g. tolerance to harsh environments, “colonizer/persister” status) while most trophic groups are ubiquitous; and (3) the metabolic footprint of the complete nematode community increases with elevation. We thus conclude that the contribution of soil dwelling nematodes to belowground ecosystem processes, including carbon and energy flow, is stronger at high elevation. The resulting cascading effects on the soil food web structure are discussed from an ecosystem functioning perspective. Overall, this study highlights the importance of nematodes in soil ecosystems and brings insights in their enhanced role along ecological gradients.

Field and laboratory selection of brassicaceous plants that differentially affect infestation levels by Delia radicum

Several plant traits control plant–insect interactions and shape host range of herbivorous insects according to their degree of dietary specialization. Understanding how plant species diversity influences herbivore infestations is of interest for the development of alternative crop protection strategies. In a pest management context, an appropriate selection of plants can modify pest distribution at the field scale. To develop a ‘push–pull’ strategy against the cabbage root fly, Delia radicum, we conducted a field study to both determine which plants exhibit contrasted pest infestation levels and to evaluate their influence on egg predation activity. Our field experiment reveals that infestation levels of brassicaceous plants by the cabbage root fly in the field can vary considerably according to plant genotype and species, while the number of predated eggs is only slightly affected by plant species. Olfactometry studies carried out under laboratory conditions revealed that plants harbouring the highest number of eggs in the field were also highly attractive, suggesting that olfactory stimuli are responsible, at least partially, for the differential infestation levels observed in the field. In a ‘push–pull’ context, this study demonstrates that different brassicaceous plants could be used to redistribute cabbage root flies in broccoli crops without compromising herbivore control by natural enemies. In addition, the importance of plant volatiles for infestation levels suggests a potential for developing a semiochemically assisted ‘push–pull’ system in which trap plants would be enhanced by synthetic release of attractive compounds.

Impact of Two Ant Species on Egg Parasitoids Released as Part of a Biological Control Program

Abstract Biological control using Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae), an egg parasitoid wasp, was tested in Uruguay to reduce populations of lepidopteran pests on soybeans. It was observed that the commercial parasitoid dispensers, which were made of cardboard, were vulnerable to small predators that succeeded in entering and emptying the containers of all the eggs parasitized by T. pretiosum. Observations in a soybean crop showed that the only small, common predators present were two ant species. The species responsible for the above mentioned predation was determined from the results of a laboratory experiment in which the behavior of the two common ants was tested. A modification of the dispensers to prevent introduction of this ant has been proposed and successfully tested in the laboratory and in the field.

Eco-evolutionary Factors Driving Plant-Mediated Above–Belowground Invertebrate Interactions Along Elevation Gradients

Plant-mediated aboveground (AG)–belowground (BG) interactions have received increasing interest over the past two decades. Despite several conceptual models to unravel AG–BG outcomes on plant-associated invertebrate communities, further efforts are required to apprehend eco-evolutionary factors driving such interactions. We here conducted an extensive literature review of the current knowledge about AG–BG interactions at the community level. We particularly highlighted the current shifts in AG–BG research towards a multi-trophic context, and we stressed the importance to consider these interactions under fluctuating environments. After presenting the main mechanisms involved in AG–BG plant-mediated effects on insect and nematode herbivore communities, we model how AG–BG interactions could be affected by environmental variations. We next develop a conceptual framework for predicting how the strength of AG–BG interactions could vary along steep elevation gradients. We suggest that the strengths of these interactions should be strongest at mid-range, where both the simultaneous AG–BG herbivore pressures and systemic defence induction should be strongest. Future tests of such model will allow disentangling the interactive effects of biotic and abiotic factors driving the ecology and evolution of AG–BG interactions.

Earthworms affect plant growth and resistance against herbivores: A meta-analysis

Subterranean detritivores such as earthworms can increase soil nutrient availability through their burrowing and casting activities. A number of recent studies have explored whether these changes caused by earthworms may in turn affect plant performance and resistance to herbivores, but no formal synthesis of this literature has been conducted to date. We tested for the effects of earthworms on plant growth, resistance and chemical defences against insect herbivores by performing a meta-analysis of the existing literature up to 2016. We also explored ecological factors that might explain among-studies variation in the magnitude of the earthworm effects on plant growth and resistance. We found that earthworm presence increases plant growth (by 20%) and nitrogen content (by 11%). Overall, earthworms did not affect plant resistance against chewing herbivores (caterpillars, slugs and rootworms), and even led to a 22% decrease in plant resistance against phloem-feeding herbivores (aphids). However, earthworm presence increased production of chemical defences by 31% when plants where attacked by cell-feeders (thrips), and resulted in an 81% increase in resistance against thrips. The magnitude of earthworm effects was stronger when earthworm inoculations consisted of a mix of species and ecological types, and when densities of earthworms were high. These results suggest that earthworm presence is an important factor underlying natural variation in plant defences against herbivores, and call for a better integration of the soil fauna in the studies of plant-herbivore interaction, both for applied and fundamental research. A plain language summary is available for this article.