Cadmium (Cd), a ubiquitous heavy metal pollutant, threatens the ecological functions of the natural enemy insect Harmonia axyridis, though the molecular mechanisms of its toxicity remain poorly understood. Here, we first determined the 48-h median lethal concentration (LC₅₀) of Cd for third‑instar H. axyridis larvae as 7.667 mg/mL. Using a multi‑omics approach, we then analyzed larval responses to injected Cd stress at LC₂₅, LC₅₀, and LC₇₅ concentrations. Transcriptomics revealed 1986, 1471, and 1433 differentially expressed genes (DEGs) in the respective treatment groups, including down‑regulated genes encoding α,α‑trehalase (TRE) and maltase‑glucoamylase involved in carbohydrate metabolism. Metabolomics identified 907, 294, and 511 differential metabolites (DMs) across the three Cd exposures, with significant accumulation of sucrose and sucrose 6'‑phosphate in the LC₅₀ group. Integrated omics analysis showed that both DEGs and DMs were co‑enriched in starch and sucrose metabolism and galactose metabolism pathways. Furthermore, Cd transferred through the soil‑plant‑aphid‑ladybug food chain disrupted trehalose metabolism, leading to reduced carbohydrate levels, suppressed trehalase activity, and altered expression of key metabolic genes. Together, these results indicate that Cd‑induced downregulation of trehalose‑related genes causes upstream carbohydrate accumulation (e.g., sucrose) and disrupts the trehalose metabolic pathway, ultimately impairing energy homeostasis. This study uncovers a novel mechanism by which heavy metal pollution affects natural enemy insects via metabolic interference. Our findings highlight the potential disruption of pest control in agroecosystems under heavy metal stress and provide critical molecular targets for assessing the ecological risk of Cd pollution on beneficial insects.

Spodoptera frugiperda (J. E. Smith, 1797), an omnivorous crop pest worldwide, reproduces prolifically. Validamycin, a competitive natural inhibitor of trehalase, is regarded as an effective and safe insecticide. Pupae were injected with a validamycin gradient (0.5–10 µg/µL) to block trehalase; enzyme activity and the Vitellogenin gene (Vg)/its receptor gene (VgR) expression (rpL10 reference) were subsequently quantified to determine the compound’s impact on S. frugiperda ontogeny and fecundity. Validamycin directly inhibited pupal membrane-bound trehalase, sharply lowering glycogen. Both pupal and adult mortality rose with dose, yielding marked abnormalities versus the Control Check (CK) group. At 0.5 μg/μL validamycin, eggs blackened and clumped in the lateral oviduct, blocking release; treated females produced far fewer eggs by day 4, exhibited ovarian atrophy, shorter lifespan, and low hatchability. The expression levels of Vg and VgR in the ovaries of the fall armyworm were consistent with the changes in the ovarian developmental phenotype. Validamycin significantly inhibited the activity of trehalase in S. frugiperda, severely hindering their normal eclosion and lowering the potential reproductive capacity of S. frugiperda. Simultaneously, it directly affects ovarian development and the lifespan of female moths. The results provide data to support the development of new methods for controlling S. frugiperda.

The mass rearing of natural enemy insects is a cornerstone of effective green pest control, making the development of optimized artificial diets critical for sustaining large populations. However, existing artificial diets often have limitations, including inhibitory effects on the reproductive development of natural enemies. In this study, we innovatively incorporated 20% catalpol into the artificial diets for Harmonia axyridis, aiming to comprehensively assess the effects of such dietary regimens on larval development, reproductive performance, and the regulation of energy metabolism in H. axyridis. Our results demonstrated that catalpol supplementation significantly shortened the duration of the 4th instar larval and pupal stages and increased pupal weight. Furthermore, catalpol treatment enhanced reproductive capacity, as evidenced by increased fecundity, improved hatching rate stability, and enhanced ovarian development. This effect was directly correlated with the significant upregulation of the vitellogenin genes Vg1 and Vg2 and their receptor gene VgR at 3 days post-emergence. Regarding energy metabolism, catalpol supplementation led to increased glycogen reserves and glucose content. The expression of the membrane-bound trehalase enzyme gene TRE2 was significantly higher than that in the control group, and the expression level of the soluble trehalase enzyme gene TRE1 also showed a significant increase. These findings indicate that catalpol effectively optimized energy metabolism, thereby accelerating developmental processes and enhancing reproductive capacity. In this study, we elucidated the mechanism by which catalpol regulates physiological metabolism in predatory natural enemy insects. For the first time, catalpol was incorporated into the artificial diet of H. axyridis as a synergistic component, significantly enhancing its growth, reproductive capacity, and energy metabolism. These findings provide a scientific basis for developing efficient artificial feeding systems and improving the field adaptability of natural enemy insects.

Cadmium (Cd) is a pervasive heavy metal pollutant in agricultural ecosystems, posing toxic threats to crop productivity, food safety, and the efficacy of biological control programs. The Asian corn borer (ACB), Ostrinia furnacalis is a destructive lepidopteran pest of maize in East Asia, while Trichogramma ostriniae serves as the most widely applied egg parasitoid for the sustainable management of this pest in integrated pest management (IPM) programs. However, the cascading effects of sublethal Cd stress transmitted from herbivorous hosts to egg parasitoids remain poorly understood. Here, we investigated the sublethal effects of dietary Cd exposure (5.0 mg/kg) on the development and Cd bioaccumulation of ACB, and subsequently evaluated the parasitism performance of the egg parasitoid T. ostriniae reared on Cd-contaminated host eggs. Results showed that chronic Cd exposure did not significantly affect larval weight, male pupal weight, or female pupal weight of ACB, but significantly increased female adult body weight, indicating stage-specific stimulatory effects. Cd concentrations in larvae, female pupae, and female adults of ACB were markedly elevated following dietary exposure, with the highest Cd loads detected in female pupae (41.23 mg/kg). However, maternal Cd transfer to eggs did not result in a statistically significant increase in egg Cd concentration. Notably, parasitism by T. ostriniae on Cd-contaminated ACB eggs significantly increased the number of eggs parasitized, although offspring emergence rate and female progeny ratio remained unaffected. This study fills the research gap regarding the trophic transfer of Cd between ACB and T. ostriniae, clarifies the complex bottom-up effects of Cd pollution on host–parasitoid interactions, and provides empirical references for the rational deployment of T. ostriniae as a biocontrol agent in Cd-contaminated maize fields.