Neural effects of insecticides in the honey bee

Abstract – During their foraging activity, honey bees are often exposed to direct and residual contacts with pesticides, especially insecticides, all substances specifically designed to kill, repel, attract or perturb the vital functions of insects. Insecticides may elicit lethal and sublethal effects of different natures that may affect various biological systems of the honey bee. The first step in the induction of toxicity by a chemical is the interaction between the toxic compound and its molecular target. The action on the molecular target can lead to the induction of observable or non-visible effects. The toxic substance may impair important processes involved in cognitive functions, behaviour or integrity of physiological functions. This review is focused on the neural effects of insecticides that have repercussions on (a) cognitive functions, including learning and memory, habituation, olfaction and gustation, navigation and orientation; (b) behaviour, including foraging and (c) physiological functions, including thermoregulation and muscle activity.

Here we cite the conclusions of this paper:

"Insecticides can induce more or less serious effects on neural functions that can lead to an impairment of behaviour and physiological functions. The mechanisms by which insecticides elicit their effects are not restricted to the exclusive interaction between the active substance and the molecular target responsible for the insecticidal action. The effects of a given insecticide involve multiple molecular targets of different affinities for the molecule that can be recruited at different exposure levels and that may induce various effects, some of which are opposite or can induce a feedback action. Time appears as an important factor in insecticide toxicity. The final action of the insecticides is strongly dependent on the circadian rhythms, the time following exposure, the age or the developmental stage of the bees and the season. The route and the mode of exposure (acute, subchronic or chronic) play a particularly determining role in the nature and the intensity of the effects induced, and are often involved in differential effects elicited by a given substance. Metabolic processes modulate the intrinsic toxicity and may lead to metabolites that exhibit toxicity levels higher or lower than that of the parent compound and may elicit completely different effects.

However, the simultaneous presence of several pesticides in a site or in food leads to interactions between substances that can drastically change the nature and the importance of the effects observed with one insecticide alone. Thus, investigations on pesticide combinations should take a more prevalent place in honey bee toxicology in the future. Because of the large number of pesticides, combinations to be studied will need to be prioritised. This could be based on the spatio-temporal occurrence of active substances.

The potential means to decrease the side effects of pesticides in the beneficial organisms, particularly the honey bees and pollinators, are of great concern. Different approaches involving highly repellent pesticides or genetic selection of pesticide-resistant bees have been proposed in the past. However, they were not considered fully satisfactory because of the unwanted impacts they can have on honey bees. Repellent substances with a long life span may elicit a drastic decrease in nectar and pollen gathering that could be damaging for both the honey bee colony and the beekeepers, and may prevent the proper pollination of crops. However, recent studies suggest that the combination of repellent and insecticide molecules can act synergistically on the insect pest (Pennetier et al. 2009). This type of action could be used advantageously to decrease the field dosages of pesticides, but it needs further investigation to assess the risk to the bees. The development of pesticide-resistant bees raises questions on food safety and genetic stability of colonies. It could be argued that pesticide-resistant bees could exhibit a higher survival rate after poisoning that enables them to harvest larger quantities of contaminated pollen or nectar. This could have harmful consequences for the human consumers of honey and pollen, and for honey bee colonies if the brood and the juveniles are more sensitive to pesticides than adult workers. Up to now, no pesticide-resistant bee populations have been reported. This is mainly due to the absence of strong selection pressure because the queen bee is not directly exposed to pesticides. Considering the variety and the complexity of the modes of action of the pesticides, it would not be possible to select bees that exhibit a multiple resistance due to biological targets that are less sensitive to pesticides. Multiple resistance based on an enhanced detoxification capacity should be more relevant but could create problems with pesticides having toxic metabolites such as organophosphates and neonicotinoids. However, in all cases of resistance, the problem of stabilising the resistant bee populations cannot be solved if the origin of queens and males in the apiary is not strictly controlled. A promising approach to preventing side effects of pesticides on beneficial organism has been derived from improved knowledge of the mode of action of pesticides in targeted pests and honey bees. Information on the mode of action can be used to develop substances that act selectively on pests. New substances might be designed to act preferentially on target subtypes of pests sensitive to insecticides such as neonicotinoids of phenylpyrazoles (Courjaret et al. 2003; Dupuis et al. 2010; Lavialle-Defaix et al. 2011; Bordereau-Dubois et al. 2012). A littleexplored way to act more selectively on pests consists in the designing of substances than act synergistically on the signalling pathways involved in the action of insecticides (Courjaret and Lapied 2001; Brandon et al. 2002; Es-Salah et al. 2008; Grünewald and Wersing 2008). This could improve the targeting of pesticides on pests and help to reduce the field dosages for decreasing the environmental impacts and the hazard to honey bees."

Full paper:
Luc P. BELZUNCES, Sylvie TCHAMITCHIAN, Jean-Luc BRUNET, 2012. Neural effects of insecticides in the honey bee. Apidologie.