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.