Transgenerational Effects of a Neonicotinoid and a Novel Sulfoximine Insecticide on the Harlequin Ladybird

SIMPLE SUMMARY: The coccinellid Harmonia axyridis is an important natural enemy of various agricultural pests, including aphids. Agrochemicals can negatively affect the performance of arthropod natural enemies and, thus, the ecological services they provide. In this context, we assessed the lethal and sublethal effects of two neuroactive compounds with different chemical structures: the long-established neonicotinoid insecticide, imidacloprid, and the novel, sulfoximine insecticide, sulfoxaflor, both of which act on nicotinic acetylcholine receptors against adult and developmental stages of H. axyridis. Estimated LC(20) and LC(50) doses of imidacloprid for a target pest species, Aphis gossypii, resulted in significantly greater mortality in contact bioassays against adult H. axyridis compared with equivalent LC(20) and LC(50) doses of sulfoxaflor. Both concentrations of imidacloprid and sulfoxaflor significantly reduced the proportion of ovipositing females of parental generation. LC(20) and LC(50) dose of imidacloprid and LC(50) dose of sulfoxaflor significantly reduced both the fecundity and fertility of parental generation. In progeny of parents exposed to both insecticides at LC(50) concentrations the juvenile survival rate was significantly reduced, and both concentrations of imidacloprid and sulfoxaflor, except LC(20) dose of sulfoxaflor, significantly prolonged the larval development time. These experimental results disclose the negative influence of sulfoxaflor and imidacloprid at low concentrations on the harlequin ladybird and its subsequent generation. Hence, actions should be taken to optimize imidacloprid and sulfoxaflor applications for the control of aphid pests, aiming at preserving the biocontrol services provided by this important predator. ABSTRACT: The harlequin ladybird, Harmonia axyridis Pallas (Coleoptera: Coccinellidae), is a generalist predator and an effective biocontrol agent of various insect pests that has been exploited for the control of aphid pests in the greenhouse and field. However, insecticides are widely used to control aphid pests worldwide and the potential non-target effects of sulfoxaflor and imidacloprid for controlling aphid pests towards this biocontrol agent are little known. Although both sulfoxaflor and imidacloprid act on nicotinic acetylcholine receptors of insects, sulfoxaflor has a novel chemical structure compared with neonicotinoids. We assessed the lethal, sublethal and transgenerational effects of sulfoxaflor and imidacloprid on H. axyridis simultaneously exposed via ingestion of contaminated prey and via residual contact on the host plant at LC(20) and LC(50) doses estimated for the cotton aphid. Imidacloprid significantly reduced the survival of H. axyridis adults compared to sulfoxaflor at the same lethal concentration against cotton aphid. Both concentrations of imidacloprid and sulfoxaflor reduced the proportion of ovipositing females, and both concentrations of imidacloprid and sulfoxaflor, except LC(20) dose of sulfoxaflor, reduced the fecundity and fertility of the parental generation. In the progeny of imidacloprid- and sulfoxaflor-exposed parents, both tested LC(50) concentrations significantly decreased the juvenile survival rate, and both concentrations of imidacloprid and sulfoxaflor, except LC(20) dose of sulfoxaflor, prolonged the development time. Our findings provide evidence of the negative influence of imidacloprid and sulfoxaflor at low lethal concentrations on the harlequin ladybird and on the progeny of exposed individuals, i.e., transgenerational effects. Hence, these findings stress the importance of optimizing the applications of imidacloprid and sulfoxaflor for the control of aphid pests, aiming at preserving the biocontrol services provided by H. axyridis throughout the integrated pest management approach.