From molecules to organisms: A multi-level approach shows negative effects of trace elements from sewage sludge used as soil improver on honeybees.

The use of sewage sludge as a soil improver has been promoted in agroecosystems. However, sludges can contain toxic trace elements because of suboptimal wastewater treatment. Nonetheless, field studies investigating the negative effects of these practices on pollinators are lacking. We collected honeybees from an area where sewage sludge use is widespread, and one where it is precluded. Trace elements in soils and bees were quantified. Cadmium, chromium, lead, mercury, and nickel were investigated because they were the least correlated elements to each other and are known to be toxic. Their levels were related to oxidative stress and energy biomarkers, midgut epithelial health, body size and wing asymmetry of honeybees. We found increased carbohydrate content in sites with higher cadmium levels, increased histological damage to the midgut epithelium in the sewage sludge area, and the presence of dark spherites in the epithelium of bees collected from the sites with the highest lead levels. Finally, we found that honeybees with the highest lead content were smaller, and that wing fluctuating asymmetry increased in sites with increasing levels of mercury. To the best of our knowledge, this is the first comprehensive study of the concentration and effects on honeybees of trace elements potentially deriving from soil amendment practices.

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Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.