**1. Introduction**

Agriculture is facing major challenges, i.e., global change and societal pressure to preserve the environment. Climate change may progressively alter the spatial distribution of species or their life cycle (e.g., voltinism), raising new concerns about crop protection against pests and pathogens. Societal awareness of the deleterious effects of chemical pesticides and fertilizers for both environmental and human health has increased with the publication and dissemination of studies reporting dramatic declines in animal populations and biodiversity (regarding entomofauna, see for example [1–3]), with change being called for in the agricultural production system, notably toward more environmentally friendly crop-managemen<sup>t</sup> practices. Such a demand sometimes spreads in the governmen<sup>t</sup> bodies. In this respect, the European Union introduced Directive 128/2009/EC, which made the implementation of Integrated Pest Management (IPM) principles compulsory, as described by the European network ENDURE (www.endure-network.eu, accessed on 9th of May 2021), and progressively banned various chemical products for which undesirable effects had been evidenced (e.g., neonicotinoids for their severe impact on pollinators [4,5]). New threats to crops concomitantly with a reduced availability of pesticides have put farmers in a difficult situation, and calls have come for alternative strategies to control pests and diseases, both preventative and curative.

**Citation:** Poggi, S.; Le Cointe, R.; Lehmhus, J.; Plantegenest, M.; Furlan, L. Alternative Strategies for Controlling Wireworms in Field Crops: A Review. *Agriculture* **2021**, *11*, 436. https://doi.org/10.3390/ agriculture11050436

Academic Editor: Eric Blanchart

Received: 3 April 2021 Accepted: 7 May 2021 Published: 11 May 2021

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The control of wireworms, the soil-dwelling larvae of click beetles (Coleoptera: Elateridae), is a remarkable illustration of this issue, and is the focus of this review. Wireworms, of which there are thousands of species but only a few harmful to agricultural crops, have been notorious as major pests worldwide for a long time. At the beginning of the 20th century, when chemicals were much less used, wireworms were considered the most harmful pests to arable crops [6]. Indeed, they can inflict severe economic damage on several major arable crops (e.g., potato, maize, and cereals) across Europe and North America [7], and the research effort into controlling these pests has risen considerably over the last few decades (Figure 1). Wireworms are extremely polyphagous pests and feed on nearly all cultivated (all cereals; all kinds of vegetables including onions, leek, and garlic; maize; potatoes; sweet potatoes; ornamentals, sugar beet and more) and wild plant species, including weeds. Additionally, most species relevant to agriculture are not only herbivorous but feed also on animal preys available in the soil (insect larvae and pupae or earthworms). Some crops are less susceptible to wireworm damage in terms of stand and yields because of agronomic characteristics (plant growth rate and density, tissues susceptibility, sowing date). This leads to the perception that some crops are specifically attacked while this is in general not the case. Elaterids exhibit a prolonged larval stage in the soil before pupation. Based on their life cycle, they fall into two groups: species overwintering as adults, and species not overwintering as adults [8]. The life cycles lasts 1–5 years [6,9–12], with only the adult stage dwelling outside the soil: a few days for species non-overwintering at the adult stage, and several months for species overwintering at the adult stage. Incidentally, the spatial distribution of species is changing probably due to climate change (e.g., *A. sordidus* is becoming a major pest in parts of Germany [13]). Meanwhile, moratoriums imposed by many countries on neonicotinoid seed treatments, as well as restrictions and deregistration of several active substances, have fostered the search for alternative environmentally friendly solutions for wireworm pest control.

**Figure 1.** Number of articles published annually from 1960 to 2020 (barplot) and their distribution across countries (world map), according to the Web of Science request formulated on 30 March 2021 as follows: (wireworm\* OR (click AND beetle\*) OR agriotes) AND (IPM OR biocontrol OR control OR managemen<sup>t</sup> OR regulation OR "risk assessment" OR "decision support" OR DSS). A total of 386 articles were published over the period under study, with a sharp rise around 2005.

Damage inflicted on crops results from the interaction between wireworm field abundance and host susceptibility under abiotic constraints. Alternative crop-protection strategies to the systematic use of chemicals should target one or both of these two components in order to contain damage under the economic threshold. Achieving this requires an in-depth understanding of pest biology and ecology and of host plant phenology, as well as of the main processes at stake in their interactions. While the sensitive phenological stages of the host crop are often well-known, knowledge of the biology and ecology of wireworms is still incomplete. As an example, while the duration of the feeding phase varies according to larval instar [9,10,14], the entire life cycle of some species still needs to be described (e.g., *A. lineatus*, *A. sputator*).

Strategies aiming at reducing wireworm densities below the economic threshold (when available) should integrate more than one practice with a partial impact and can be achieved through long-term managemen<sup>t</sup> along the crop rotation and at different spatial scales. Preventive practices include applying crop rotations unfavorable to oviposition and wireworm survival, tilling when edaphic conditions are conducive to destroying soildwelling life stages, incorporating plants or extracts with biofumigant and allelochemical properties into soil, the use of natural enemies for pest control, and the manipulation in space and time of favorable areas (e.g., managing grassland regimes). Practices targeting the containment of crop damage below an economic threshold (limitation of harmfulness) despite substantial larval densities rely on identifying optimal planting and harvest conditions, protecting the sensitive crop with attractive companion plants, increasing seeding rates, and planting more tolerant cultivars. Reaching a satisfactory level of crop protection requires a combination of agronomic practices, thereby designing an Integrated Pest Managemen<sup>t</sup> strategy (IPM) whose foundations are stated in Barzman et al. [15]. IPM faces the challenge of assessing which protection methods are compatible and how to set their combination so that the resulting crop protection has sufficient efficacy.

Our aim in this paper is to provide a comprehensive state-of-the-art of alternative wireworm managemen<sup>t</sup> practices to insecticide use and sugges<sup>t</sup> a holistic approach to exploiting them as IPM packages that include two or more alternative practices as replacements for insecticides. First, considering that any relevant managemen<sup>t</sup> strategy requires accurate risk assessment, we address the question of risk assessment in terms of wireworm infestation or crop damage and of wireworm population monitoring. Indeed, a basic efficient alternative to the preventive use of insecticides can be doing nothing when risk is low or waiving the planting of a susceptible crop where and when the risk is high. Then, we present the main pesticide-free methods for controlling wireworms and elaborate on their putative combinations within an IPM framework. Finally, we outline a future research avenue that will lead to reduced use of insecticides for controlling wireworms in field crops.

## **2. Risk Assessment**

Assessing the risk of wireworm infestation or crop damage is the first and most efficient alternative to the preventive use of insecticides, as it provides guidance on the selection of fields with low risk of economic damage. Risk assessment relies on the evaluation of factors that favor field infestation or crop damage and is a preventive tool. In its most advanced form, it consists of a decision-support system. It can also stem from the monitoring of pest populations, at different development stages, mainly at plot scale, and trigger the adoption of corrective tactics or the adaptation of preventive strategies.

#### *2.1. Evaluation of Risk Factors*
