Pest Insect Olfaction in an Insecticide-Contaminated Environment: Info-Disruption or Hormesis Effect

Most animals, including pest insects, live in an “odor world” and depend strongly on chemical stimuli to get information on their biotic and abiotic environment. Although integrated pest management strategies including the use of insect growth regulators (IGRs) are increasingly developed, most insect pest treatments rely on neurotoxic chemicals. These molecules are known to disrupt synaptic transmission, affecting therefore sensory systems. The wide-spread use of neurotoxic insecticides and the growing use of IGRs result in residual accumulation of low concentrations in the environment. These insecticide residues could act as an “info-disruptor” by modifying the chemical communication system, and therefore decrease chances of reproduction in target insects. However, residues can also induce a non-expected hormesis effect by enhancing reproduction abilities. Low insecticide doses might thus induce adaptive processes in the olfactory pathway of target insects, favoring the development of resistance. The effect of sublethal doses of insecticides has mainly been studied in beneficial insects such as honeybees. We review here what is known on the effects of sublethal doses of insecticides on the olfactory system of insect pests

Mating-induced transient inhibition of responses to sex pheromone in a male moth is not mediated by octopamine or serotonin

In the male moth, Agrotis ipsilon, mating induces a transient inhibition of behavioural and central nervous responses to sex pheromone. Newly mated males are not attracted to sex pheromone, and the sensitivity of their antennal lobe (AL) neurons is lower than in virgin males. This rapid transient olfactory inhibition prevents them from re-mating unsuccessfully until they have refilled their sex glands. We hypothesized that this olfactory ‘switch off’ might be controlled by neuromodulators such as biogenic amines. To test our hypothesis, we studied the effects of octopamine (OA) and serotonin (5-hydroxytryptamine, 5-HT) on the coding properties of pheromone-sensitive AL neurons in virgin and newly mated males. We show that AL neuron sensitivity increased in newly mated males after injection of OA or 5-HT, but only OA treatment affected certain response characteristics of AL neurons in virgin males. Whereas all measured AL neuron response characteristics were different between virgin and newly mated males, amine treatment in newly mated males restored only the latency and spike frequency, but not the duration of excitatory and inhibitory phases, which were initially found in virgin males. Additionally, we investigated the behavioural effects of OA and 5-HT treatments in virgin and mated males. Although OA and 5-HT enhanced the general flight activity of newly mated males, amine treatments did not restore the behavioural pheromone response of mated moths. Altogether, these results show that, although biogenic amines modulate the olfactory system in moths, OA and 5-HT are probably not involved in the post-mating inhibition of responses to sex pheromone in A. ipsilon males.Fil: Barrozo, Romina. Institut National de la Recherche Agronomique; Francia. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Jarriault, David. Institut National de la Recherche Agronomique; FranciaFil: Simeone, Xenia. Institut National de la Recherche Agronomique; FranciaFil: Gaertner, Cyril. Institut National de la Recherche Agronomique; FranciaFil: Gadenne, Christophe. Institut National de la Recherche Agronomique; FranciaFil: Anton, Sylvia. Institut National de la Recherche Agronomique; Franci

Differential Interactions of Sex Pheromone and Plant Odour in the Olfactory Pathway of a Male Moth

Most animals rely on olfaction to find sexual partners, food or a habitat. The olfactory system faces the challenge of extracting meaningful information from a noisy odorous environment. In most moth species, males respond to sex pheromone emitted by females in an environment with abundant plant volatiles. Plant odours could either facilitate the localization of females (females calling on host plants), mask the female pheromone or they could be neutral without any effect on the pheromone. Here we studied how mixtures of a behaviourally-attractive floral odour, heptanal, and the sex pheromone are encoded at different levels of the olfactory pathway in males of the noctuid moth Agrotis ipsilon. In addition, we asked how interactions between the two odorants change as a function of the males' mating status. We investigated mixture detection in both the pheromone-specific and in the general odorant pathway. We used a) recordings from individual sensilla to study responses of olfactory receptor neurons, b) in vivo calcium imaging with a bath-applied dye to characterize the global input response in the primary olfactory centre, the antennal lobe and c) intracellular recordings of antennal lobe output neurons, projection neurons, in virgin and newly-mated males. Our results show that heptanal reduces pheromone sensitivity at the peripheral and central olfactory level independently of the mating status. Contrarily, heptanal-responding olfactory receptor neurons are not influenced by pheromone in a mixture, although some post-mating modulation occurs at the input of the sexually isomorphic ordinary glomeruli, where general odours are processed within the antennal lobe. The results are discussed in the context of mate localization

Brief Exposure to Sensory Cues Elicits Stimulus-Nonspecific General Sensitization in an Insect

The effect of repeated exposure to sensory stimuli, with or without reward is well known to induce stimulus-specific modifications of behaviour, described as different forms of learning. In recent studies we showed that a brief single pre-exposure to the female-produced sex pheromone or even a predator sound can increase the behavioural and central nervous responses to this pheromone in males of the noctuid moth Spodoptera littoralis. To investigate if this increase in sensitivity might be restricted to the pheromone system or is a form of general sensitization, we studied here if a brief pre-exposure to stimuli of different modalities can reciprocally change behavioural and physiological responses to olfactory and gustatory stimuli. Olfactory and gustatory pre-exposure and subsequent behavioural tests were carried out to reveal possible intra- and cross-modal effects. Attraction to pheromone, monitored with a locomotion compensator, increased after exposure to olfactory and gustatory stimuli. Behavioural responses to sucrose, investigated using the proboscis extension reflex, increased equally after pre-exposure to olfactory and gustatory cues. Pheromone-specific neurons in the brain and antennal gustatory neurons did, however, not change their sensitivity after sucrose exposure. The observed intra- and reciprocal cross-modal effects of pre-exposure may represent a new form of stimulus-nonspecific general sensitization originating from modifications at higher sensory processing levels

Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect

Behavioral sex pheromone responsiveness in the male moth Agrotis ipsilon was previously shown to be controlled by juvenile hormone (JH). However, this morphogenetic hormone did not change the sensitivity of antennae to sex pheromones. To analyze the possible involvement of JH in the central integration of the female-produced sex pheromone, we investigated the pheromone response of olfactory antennal lobe (AL) interneurons in male A. ipsilon as a function of age and JH status by using intracellular recordings. When the antennae were stimulated with the sex pheromone blend, the sensitivity of olfactory AL neurons increased with age, as does the JH-dependent behavioral and physiological development of A. ipsilon males. Furthermore, males surgically deprived of JH showed a significant decrease in the sensitivity of the AL neurons. JH injection in operated or in young males restored or induced, respectively, a high sensitivity of the AL neurons. JH seems likely to be involved in the plasticity of the adult insect brain by modulating the central nervous processing of olfactory information, thus allowing mate recognition and reproduction at the optimal time

Plasticity in the insect brain : why attractive odors are not always attractive

International audienc

Post-mating olfactory switch-off in a male moth: smell, sex, and stop!

National audienc

Central processing of plant volatiles in Agrotis ipsilon males is age-independent in contrast to sex pheromone processing.

Male moths rely on female sex pheromones to find their mating partner and on plant volatiles for the detection of food sources. In the noctuid moth, Agrotis ipsilon, plasticity of central sex pheromone processing has been shown previously in the antennal lobe. The sensitivity of antennal lobe interneurons increases with age and juvenile hormone level. Here we investigated whether age affects not only central sex pheromone processing, but also central processing of plant volatiles in A. ipsilon males. Intracellular recordings of antennal lobe interneurons were made in males of different ages after stimulation of the antennae with seven different plant volatiles. The sensitivity and specificity of the antennal lobe interneurons for any of the plant volatiles tested did not change with age. From these results we conclude that the sensitivity of the antennal lobe interneurons involved in central plant volatile processing is age-independent and that the action of juvenile hormone is specific for central sex pheromone processing in A. ipsilon males

Mimetique d'hormone juvenile et diapause chez Ostrinia nubilalis Hbn. (Lepidoptere, Pyralidae)

National audienc