4.2 Glyphosate exposure and mosquito susceptibility toPlasmodium infection
The impact of glyphosate on the susceptibility of mosquitoes to malaria parasite infection is unclear. While the probability of infection of females was 100% in the first experiment, we found that exposure to glyphosate in the larval stage reduced the prevalence ofPlasmodium infection by roughly one-third in the second experiment. Fluctuations in the prevalence of infection between experimental blocks are common (Pigeault et al., 2015). This might be due to the difference in parasite strains and parasite loads in infected canaries between the experiments. The observed effects in the second experiment may be due to an effect of glyphosate on mosquito immunity. Glyphosate can affect invertebrate immunity in several ways, including effects on haemocyte parameters (Hong et al., 2018, 2017; Matozzo et al., 2019; Monte et al., 2019), activity of immune enzymes (Hong et al., 2017) and on oxidative stress (de Melo Tarouco et al., 2017; Pala, 2019). The effects on invertebrate immunity were generally negative. For instance, the exposure of shrimps (Macrobrachium nipponensis ), Chinese mitten crabs (Eriocheir sinensisto ) and clams (Ruditapes philippinarumto ) to a sublethal concentrations of glyphosate caused a significant decrease in total haemocyte count (Hong et al., 2018, 2017; Matozzo et al., 2019). However, in the clam R. philippinarum , exposure to glyphosate increased significantly haemocyte proliferation and both diameter and volume of these immune cells (Matozzo et al., 2019). In the Chinese mitten crabs high concentrations of glyphosate increased the phenoloxidase (PO) activities. The phenoloxidase cascade is an important immune response of mosquitoes leading to encapsulation and death of a variety of parasites includingPlasmodium (Christensen et al., 2005; Yassine et al., 2012; Zhang et al., 2008).
Another non-exclusive reason that could explain lower prevalence of infection in mosquitoes exposed to glyphosate would be the effect of this molecule on their midgut (Gregorc and Ellis, 2011). Some other pesticides, such as imidacloprid, disrupt the development of mosquitoes’ midgut (Fernandes et al., 2015). Imidacloprid significantly reduced the number of digestive and endocrine cells, resulting in malformation of the midgut epithelium (Fernandes et al., 2015). The midgut epithelial membrane is the first barrier that parasites must cross to infect their vector. In addition, mosquito midgut produces large amounts of xanthurenic acid which is essential for the exflagellation ofPlasmodium transmissible stages (gametocytes, Billker et al., 1998), the secretion of digestive carboxypeptidase enzymes may also provide parasite with essential amino acids for its development (Lavazec and Bourgouin, 2008). An alteration of the midgut could therefore impact the parasite’s ability to invade this organ. It is important to note that while exposure to glyphosate did not affect the size of adult mosquitoes, females derived from larvae exposed to the highest concentrations of glyphosate (0.1mg/L) tended to excrete less haematin. This result may indicate an effect of glyphosate on their ability to digest blood potentially due to a midgut malformation.