Abstract
Neonicotinoids as thiamethoxam and thiacloprid are suspected to be implicated in the decline of honey bee populations. As nicotinic acetylcholine receptor agonists, they disturb acetylcholine receptor signaling in insects, leading to neurotoxicity and are therefore globally used as insecticides. Several behavioral studies have shown links between neonicotinoid exposure of bees and adverse effects on foraging activity, homing flight performance and reproduction, but the molecular aspects underlying these effects are not well-understood. In the last years, several studies through us and others showed the effects of exposure to neonicotinoids on gene expression in the brain of honey bees. Transcripts of acetylcholine receptors, hormonal regulation, stress markers, detoxification enzymes, immune system related genes and transcripts of the energy metabolism were altered after neonicotinoid exposure. To elucidate the link between homing flight performance and shifts in gene expression in the brain of honey bees after neonicotinoid exposure, we combined homing flight activity experiments applying RFID technology and gene expression analysis. We analyzed the expression of endocrine factors, stress genes, detoxification enzymes and genes linked to energy metabolism in forager bees after homing flight experiments. Three different experiments (experiment I: pilot study; experiment II: "worst-case" study and experiment III: laboratory study) were performed. In a pilot study, we wanted to investigate if we could see differences in gene expression between controls and exposed bees (experiment I). This first study was followed by a so-called "worst-case" study (experiment II), where we investigated mainly differences in the expression of transcripts linked to energy metabolism between fast and slow returning foragers. We found a correlation between homing flight duration and the expression of cytochrome c oxidase subunit 5A, one transcript linked to oxidative phosphorylation. In the third experiment (experiment III), foragers were exposed in the laboratory to 1 ng/bee thiamethoxam and 8 ng/bee thiacloprid followed by gene expression analysis without a subsequent flight experiment. We could partially confirm the induction of cytochrome c oxidase subunit 5A, which we detected in experiment II. In addition, we analyzed the effect of the feeding mode (group feeding vs. single bee feeding) on data scattering and demonstrated that single bee feeding is superior to group feeding as it significantly reduces variability in gene expression. Based on the data, we thus hypothesize that the disruption of energy metabolism may be one reason for a prolongation of homing flight duration in neonicotinoid treated bees.
Highlights
Over the last 50 years, the number of species of wild bees and other pollinating insects has declined [reviewed in: [1]]
Our results suggest that neonicotinoid exposure of forager bees disturbs their energy metabolism, and this disturbance might cause a reduced return rate or a prolonged flight time in neonicotinoid exposed bees in the radiofrequency identification (RFID) homing flight test
The homing flight return rates of honey bees treated with the highest tested dose of 1.5 ng thiamethoxam/bee, was considerably lower and significantly different to those return rates observed in non-treated control bees, or in the groups treated with the lower thiamethoxam doses at 0.3 and 1.0 ng thiamethoxam /bee (Figure 2A)
Summary
Over the last 50 years, the number of species of wild bees and other pollinating insects has declined [reviewed in: [1]]. The number of managed honey bee colonies has declined in North America and in many European countries [2]. In China and Argentina, on the other hand, the number of managed honey bee colonies has increased [3,4,5]. There are alarming reports of high colony losses in managed honey bees (colony collapse disorder CCD) from several areas of the world [6]. Several factors including CCD are suspected to cause the decline of bees. Diseases caused by bacterial and viral infections, and parasites e.g., the parasitic mite Varroa destructor contribute to the decline of bees [reviewed in: [1]]. The exposure to pesticides was suggested as driver of the bee decline worldwide [7,8,9]
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