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

Abstract

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.

Schistosome infection in Senegal is associated with different spatial extents of risk and ecological drivers for Schistosoma haematobium and S. mansoni

“…This limited sampling to areas within ~10 m of shorelines, which is consistent with WHO guidelines recommending snail sampling within 10 m of shorelines [ 19 ] and with relevant literature suggesting that nearshore habitats pose the greatest risk for transmission to humans [ 32 ]. Even so, detailed drone mapping of village water access sites and surrounding aquatic areas revealed extensive snail habitat (defined as non-emergent vegetation, as determined through the snail–habitat association study described above and confirmed in the same study area in [ 20 ] and [ 45 ]) beyond the 10 meters sampling area from the shoreline (as shown in Fig 2A ). We hypothesized that, if non-emergent vegetation beyond nearshore areas supports dense snail populations, such areas might represent a source of unrecognized snail and schistosome exposure risk to humans ( Fig 1B ).…”

“…Parasitological data collection, ecological field sampling, and unmanned aerial vehicle (drone) imaging [ 42 ] took place between 2016 and 2018 at 16 villages in the lower Senegal River Basin, northwestern Senegal ( Fig 1C ). Data were collected as part of a longitudinal cohort study on regional schistosomiasis transmission ecology and potential for biological control using snail predators [ 20 , 43 – 45 ]. The criteria for which 16 villages were selected from among 701 candidate villages has been described previously [ 20 ].…”

Agricultural Innovations to Reduce the Health Impacts of Dams

“…Invasive aquatic species threaten biodiversity and productive use of river environments [43] while supporting the snails that transmit schistosomes [44,45]. Aquatic vegetation has been associated with both increased shedding of schistosome parasites from snails [46] and increased prevalence of infection in humans [47]. There is also evidence for a mutualistic relationship between snails that transmit schistosomes and submerged vegetation from the genus Ceratophyllum [46].…”

“…Aquatic vegetation has been associated with both increased shedding of schistosome parasites from snails [46] and increased prevalence of infection in humans [47]. There is also evidence for a mutualistic relationship between snails that transmit schistosomes and submerged vegetation from the genus Ceratophyllum [46]. The removal of aquatic vegetation from natural water bodies [48], reservoirs [49], and irrigation canals [50], thus, might be an important intervention for reducing snail abundance and disease transmission while maintaining agricultural productivity.…”

Identifying low risk insecticides that can enhance food production without increasing mortality of biocontrol agents for human schistosomiasis

“…Monosex M. rosenbergii that are unable to interbreed with M. vollenhovenii (Savaya-Alkalay et al, 2018) are being considered as biological control agents for schistosomiasis in Africa (Levy et al, 2019). Top-down effects of invertebrate snail predators have also been negatively associated with snail parasite production (Haggerty et al, 2020).…”