Impact of sublethal concentrations of chemical pollutants on the gut microbiome of pollinators: a study on Osmia bicornis

In recent decades, significant declines in pollinator populations have been documented globally, leading to substantial environmental and economic damage due to impaired pollination services and loss of species diversity. One of the primary causes of this decline has been identified as the exposure of pollinators to chemical pollutants. This exposure to anthropogenic chemicals may, in turn, indirectly affect insect health by disrupting the gut microbiome, which plays essential roles for the host. In fact, the gut microbiome of insects is involved in various biological and evolutionary processes, including nutrition and development. Most research examining the impact of chemical pollutants on the microbiome of pollinators has focused on the honeybee (Apis mellifera) and on a few species of bumblebees. These studies have mainly considered a limited number of chemicals, mostly insecticides and herbicides, investigating their effect at typical field application dosage. Little is known about the impact of various chemicals on the gut microbial community of other pollinators, including wild bees, for which the structure and function of the microbiome are still poorly understood. Thus, this study aims to investigate the impact of various categories of chemical pollutants on the gut microbiome of the red mason bee Osmia bicornis, one of the most common wild pollinators. In this work, O. bicornis adults were subjected to chronic oral toxicity tests in two parallel laboratory trials using sublethal doses of four chemicals: boscalid, copper chloride, glyphosate and ivermectin, administered both singularly and in combination. These compounds have been previously found as residues in bee matrices (pollen, nectar), making them relevant for studying the impact on the gut microbiome of pollinators. The gut bacterial community of O. bicornis specimens was investigated by molecular analyses in terms of bacterial abundance and taxonomic composition, using quantitative PCR and high-throughput Illumina sequencing of the phylogenetic marker 16S rRNA, respectively. The results showed that gut bacterial abundance was significantly reduced when the insects were exposed to copper chloride and boscalid. Furthermore, the gut microbiome of O. bicornis was affected by all the different chemicals in terms of community composition and diversity. The knowledge acquired on the impact of chemicals on the gut microbiome of pollinators will be integrated with information on the effects of these compounds on pollinator health and survival, contributing to a better understanding of the chronic effects of sublethal doses of chemicals on pollinator populations.