Sublethal effects of matrine and azadirachtin on the wolf spider Pardosa laura: no impairment of growth but marked suppression of reproduction

BACKGROUND Plant-derived pesticides (PDPs) are increasingly promoted as ‘eco-friendly’ alternatives to agrochemicals because of their low vertebrate toxicity, yet their safety for non-target arthropod natural enemies is rarely tested, especially the enrichment effect via trophic transfer. RESULTS We cultured fruit flies using media supplemented with two widely applied Chinese PDPs in tea plantations, matrine or azadirachtin, under commercial concentration, which were fed to newly emerged spiderlings of wolf spider Pardosa laura (Araneae: Lycosidae) throughout their entire life cycle. We examined the effect of these two PDPs on their survival, developmental parameters and reproduction. The results showed that developmental traits remained unaffected, but both PDPs markedly suppressed male mating success and female fecundity. Histological examination of paraffin sections revealed markedly impaired ovarian maturation. Microbiome profiling indicated that pesticide exposure disrupted ovarian microbial communities, with azadirachtin exerting the strongest effect, whereas gut and testicular communities remained largely unchanged. Transcriptomic analysis of ovaries showed significant enrichment of pathways related to ovarian development. Ten representative differentially expressed genes (DEGs) within these pathways were selected and validated by RT-qPCR. CONCLUSION PDPs may not compromise the development of spiders in the first generation, yet they can severely affect reproduction of the spiders, thereby precipitating substantial declines in population size of future generations. This result challenges the conventional wisdom of botanical pesticides, inspiring re-consideration of their rational use in integrated pest management. © 2025 Society of Chemical Industry.