Entomopathogenic nematodes impact the volatile profile of their insect hosts with a cascading effect on the behaviour of uninfected hosts

Abstract

Entomopathogenic nematodes (EPNs) are increasingly utilized as biological alternatives to insecticides for controlling pests. Infective juveniles release mutualistic bacteria that rapidly multiply and kill the host insect. Despite extensive research on EPN-insect interactions, it remains unclear if EPN infections alter the volatile organic compounds (VOC) emitted by the host, potentially influencing the behaviour of uninfected insects. This study tested two hypotheses: (1) entomopathogenic nematodes modify the emissions of volatile organic compounds of their insect host, and (2) these volatile emissions attract uninfected insects, therefore increasing EPN dispersal. Using Galleria mellonella larvae and two EPN species (Steinernema carpocapsae, Heterorhabditis bacteriophora), VOC were collected post-mortem using Hisorb methodology and analysed via gas chromatography-mass spectrometry. Behavioural tests, including pitfall, preference, and escape time assays, assessed the responses of uninfected insects to infected larvae. The results showed that EPN-infected larvae emit significantly different VOC profiles compared to larvae killed by other means, with a 100% success rate in distinguishing these profiles. Behavioural tests didn’t reveal an attraction effect but a significant reduction in escape time when uninfected insects were exposed to larvae infected early in the EPN life cycle. Sulphur compounds, typical of decomposition, were detected in the VOC profiles. The variation in VOC during the EPN reproductive cycle may stem from symbiotic bacteria. A correlation was found between the VOC profiles and the behavioural responses, supporting the study's hypotheses.