Dynamics of Host Snail Species and Associated Schistosoma/Fasciola Infections: Testing the Citizen Science Model in Lake Albert Region, Uganda

Abstract

Schistosomiasis is a snail-borne disease that affects over 200 million people globally, 90% living in Sub-Saharan Africa. Severe infections lead to morbidity and death. The disease is highly prevalent among the great lakes in Uganda. However, incomplete knowledge of the distribution patterns of the snail hosts, disease transmission sites, and a shortage of malacologists impede elimination of the disease. Hence, this study assessed the variation in the distribution of host snails of Schistosoma and Fasciola spp. in space and time within the schistosomiasis endemic Lake Albert region of Uganda. The study adopted a citizen science approach to snail monitoring. Snails were sampled from 73 sites monthly for 20 months by the PhD researcher (expert) starting from June 2020, while the citizen scientists (CSs) sampled the same sites weekly in the same period. A time-based snail scooping approach was followed while water physicochemical parameters were determined in situ and some in a field laboratory following standard protocols. Snail species determination followed analysis of the cytochrome c oxidase subunit 1 (COX1) and the nuclear internal transcribed spacer (ITS) markers. Phylogenetic and haplotype network analysis was conducted on the snail sequences to confirm species identity and study gene flow among populations. Logistical and generalised linear models were generated to compare the data generated by the expert and the CSs. Regression analyses were conducted between physicochemical parameters and snail abundance while spatial differences in snail abundance were analysed using the chi-square tests. In 1, 382 data reports (site visits), a total of 52,757 snails belonging to the three target genera (Bulinus (n = 6,123), Biomphalaria (n = 29,670) and Radix (n = 16,964)) were collected by the expert. Impressively, the CSs identified snail genera with over 99% accuracy (n = 4,034 data reports). In addition, the CS collected snail data agreed with the expert's data (70-90%) in snail presence but the degree of agreement varied between snail genera. Schistosoma mansoni was only recorded among Biomphalaria at lake sites despite superior snail numbers at sites away from the lake, thus highlighting the existence of transmission conditions at the lake. The upland Biomphalaria were dominated by B. cf. pfeifferi, which for the first time, this study provides evidence to be a subspecies of B. sudanica that tended to harbour Schistosoma rodhaini. Notably, the study found, for the first time in this area, Bulinus globosus and B. nasutus productus, the hosts of Schistosoma haematobium. However, shedding and PCR tests only revealed infections with the bovine parasite S. bovis. Increasing pH was significantly associated with Biomphalaria spp. abundance (R² = 0.388, p = 0.007) while site type was a predictor of Bulinus and Radix spp. abundance (p<0.05). Thus, this study highlights the actual and potential risk of both S. mansoni and S. haematobium respectively in the Albertine region and the high reliability of citizen-collected data for snail monitoring. This study recommends further research to resolve taxonomy gaps among Biomphalaria and Bulinus snails.