Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis

Background Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally. Methods/Principal findings We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae. Conclusions/Significance Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control. Author summary Over 800 million people are at risk of schistosomiasis and environmental factors that regulate densities of cercariae parasites that infect humans remain poorly understood. We sampled a spatially extensive area at 36 water-access points in northern Senegal, and quantified densities of snail intermediate hosts, snail predators, and aquatic vegetation in each sample, as well as cercariae released from snails after they were brought to the laboratory. We found that the quantity of submerged aquatic vegetation, particularlyCeratophyllumspp., was positively associated with schistosome cercariae released per infected snail, and total potential cercariae released by the collected snails per water access site. In contrast, the abundance of aquatic predators near infected snails (in the same sweep) was negatively associated with the per-capita cercarial release by infected snails, but positively associated with total snail abundance per site. Additionally, snail densities and potential cercarial densities (estimated as the sum of cercariae released by all collected, infected snails at a site) were only weakly correlated, suggesting that snail densities alone might not accurately reflect total potential of those snails to emit schistosome cercariae. Overall, a better understanding of aquatic factors that can influence the production of schistosome cercariae under field conditions, rather than snail host abundance alone, might facilitate improvements in schistosomiasis monitoring and control.