An Insecticide Further Enhances Experience-Dependent Increased Behavioural Responses to Sex Pheromone in a Pest Insect

Abstract

Neonicotinoid insecticides are widely used to protect plants against pest insects, and insecticide residues remaining in the environment affect both target and non-target organisms. Whereas low doses of neonicotinoids have been shown to disturb the behaviour of pollinating insects, recent studies have revealed that a low dose of the neonicotinoid clothianidin can improve behavioural and neuronal sex pheromone responses in a pest insect, the male moth Agrotis ipsilon, and thus potentially improve reproduction. As male moth behaviour depends also on its physiological state and previous experience with sensory signals, we wondered if insecticide effects would be dependent on plasticity of olfactory-guided behaviour. We investigated, using wind tunnel experiments, whether a brief pre-exposure to the sex pheromone could enhance the behavioural response to this important signal in the moth A. ipsilon at different ages (sexually immature and mature males) and after different delays (2 h and 24 h), and if the insecticide clothianidin would interfere with age effects or the potential pre-exposure-effects. Brief pre-exposure to the pheromone induced an age-independent significant increase of sex pheromone responses 24 h later, whereas sex pheromone responses did not increase significantly 2 h after exposure. However, response delays were significantly shorter compared to naïve males already two hours after exposure. Oral treatment with clothianidin increased sex pheromone responses in sexually mature males, confirming previous results, but did not influence responses in young immature males. Males treated with clothianidin after pre-exposure at day 4 responded significantly more to the sex pheromone at day 5 than males treated with clothianidin only and than males pre-exposed only, revealing an additive effect of experience and the insecticide. Plasticity of sensory systems has thus to be taken into account when investigating the effects of sublethal doses of insecticides on behaviour.

Sublethal Exposure Effects of the Neonicotinoid Clothianidin Strongly Modify the Brain Transcriptome and Proteome in the Male Moth Agrotis ipsilon

“…However, we cannot conclude whether this large range of effects is due to a direct effect of clothianidin, or of its bio-transformed metabolites, or of a general response due to the stress induced by the insecticide exposure (i.e., oxidative stress, increase in metabolic cost…). Nevertheless, these neuronal changes could provide an explanatory element for the behavioral and neuronal sensitivity modifications that we observed previously in clothianidin-treated males [ 17 , 23 , 88 ].…”

Sublethal larval exposure to imidacloprid impacts adult behaviour in Drosophila melanogaster

“…A few notable exceptions have nonetheless been reported: in the pest moth Agrotis ipsilon, it was shown that a neonicotinoid insecticide enhanced the response to sex pheromones (Rabhi et al, ). Interestingly, an experience‐dependent response was also detected with re‐exposure leading to increased effect on pheromone sensitivity as measured through male orientation response assay (Abrieux et al, ). A similar impact on male reproductive behaviour was found for imidacloprid where a sublethal exposure of the neotropical brown stink bug Euschistus heros increased male reproductive fitness (Haddi et al, ).…”

Plasticity and modulation of olfactory circuits in insects

“…G, olfactory glomerulus; KC, Kenyon cell; LN, local interneuron; OSN, olfactory sensory neurons; MBON, mushroom body output neuron; PN, projection neuron another insecticide, deltamethrin, a widely used pyrethroid (Lalouette et al 2016). So far, it is, however, not known if the observed modulatory effects of insecticides are caused directly by receptor-ligand interactions, or if insecticides cause modifications of neuromodulator levels or expression of their receptors (Abrieux et al 2013(Abrieux et al , 2014(Abrieux et al , 2016. In addition, pyrethroid insecticides were shown to disturb the wiring of olfactory glomeruli during postembryonic metamorphic development in M. sexta (Wegerhoff et al 2001).…”