Dose-dependent lethality of sulfuryl fluoride and transcriptomic insights into tolerance evolution on Cheyletus malaccensis (Oudemans) (Acari: Cheyletidae).

Stored grain pests are commonly found in human-made food facilities and bulk grain storage, leading to significant losses in both the quality and quantity of stored grains and related commodities (Arco et al., 2024; Dowdy and McGaughey, 1998). It is a serious issue that the agroindustry primarily addresses with pesticides and fumigants. However, a new approach is necessary due to the rising resistance of many common stored grain pests to fumigants and the increasing consumer interest in healthier products, along with concerns about the environmental impact of chemical residues (Benhalima et al., 2004; Feroz et al., 2020). Thus, biological control using natural enemies, as an environmentally friendly approach, presents a promising supplement to chemical methods (Jonsson et al., 2017; Ratto et al., 2022; Urbaneja-Bernat et al., 2024). Generalist predatory mites are widely used for the management of pests, typically as part of augmentative biological control strategies(Beretta et al., 2022; Duso et al., 2020).

Cheyletus malaccensis Oudemans (Arachnida, Acariformes, Prostigmata, Cheyletidae), is widely found in grain storage facilities and warehouses. It preys on various pests, including the harmful mite, the eggs or larvae of common grain storage pests such as Liposcelis bostrychophila (Badonnel), Cryptolestes ferrugineus (Stephens), Rhyzopertha dominica (Fabricius), and Lasioderma serricorne (Fabricius), making it a potential biological control agent for managing stored grain pests (He et al., 2016; Lan et al., 2020; Sun et al., 2020; Wu, 2023). C. malaccensis has a short developmental period, high fecundity, and rapid population growth under suitable conditions, along with a broad prey spectrum and substantial predation capacity (Wu, 2023). Additionally, storage facilities such as granaries offer controllable environmental factors, stable temperature and humidity, and confined spaces, making predatory mites an ideal biological control method for managing stored grain pests (Parsons et al., 2024). Sulfuryl fluoride has been registered for treating food commodities and food facilities. Sulfuryl fluoride (SO₂F₂) is a colorless, odorless, and non-flammable toxic gas at normal temperature and pressure. It kills pests by mechanisms such as inhibiting insect oxygen absorption, disrupting intracellular phosphate balance, and preventing the hydrolysis of fatty acids. Due to its broad insecticidal spectrum, strong diffusivity, and low residue characteristics, it is widely used in pest control (Hasan et al., 2021; Jagadeesan et al., 2018). Among the tested species, Tribolium castaneum had the lowest mortality in response to sulfuryl fluoride at 25 °C, across both eggs and adults (Jagadeesan and Nayak, 2017). To enhance the efficacy of predatory mites in pest management, we can be used in combination with fumigant agents for improved control of pests. The impact of sulfuryl fluoride on beneficial organisms, including predatory mites, emphasizes that proper fumigation management can minimize negative effects on these natural enemies, leading to more effective pest control.

Transcriptomics is an effective approach for analyzing the interactions between organisms and their environment. Gene expression analysis of predatory mites orally exposed to fenbutatin oxide and orange oil yielded only a limited xenobiotic stress response (Bajda et al., 2022). Transcriptome data indicated that Anisopteromalus calandrae can significantly upregulate the expression levels of abiotic related genes, such as the heat shock protein (Hsp 90) gene and cytochrome P450 to cope with cold stress (Guo et al., 2024). Zhao found that the metabolism and transporter pathways are associated with resistance to fenpropathrin in silkworm, and OCT6 is an effective and potential target (Zhao et al., 2023).

Currently, although there have been studies on the effectiveness of predatory mites in controlling stored grain pests, there are no reports on the combined treatment of C. malaccensis and sulfuryl fluoride fumigation, and little is known about the molecular mechanisms of C. malaccensis adaptation to sulfuryl fluoride. Therefore, the purpose of this study was to investigate the combined feasibility of C. malaccensis and sulfuryl fluoride fumigation for pest control and the molecular mechanisms of C. malaccensis adaptation to sulfuryl fluoride stress through transcriptome analysis. The research findings contribute to the promotion of application techniques for the use of predatory mites as biological control agents.