Spatio-temporal variability in transmission risk of human schistosomes and animal trematodes in a seasonally desiccating East African landscape

Abstract

Different populations of hosts and parasites experience distinct seasonality in environmental factors, depending on local-scale biotic and abiotic factors. This can lead to highly heterogeneous disease outcomes across host ranges. Variable seasonality characterizes urogenital schistosomiasis, a neglected tropical disease caused by parasitic trematodes (Schistosoma haematobium). Their intermediate hosts are aquatic Bulinus snails that are highly adapted to extreme rainfall seasonality, undergoing prolonged dormancy yearly. While Bulinus snails have a remarkable capacity for rebounding following dormancy, we investigated the extent to which parasite survival within snails is diminished. We conducted an investigation of seasonal snail schistosome dynamics in 109 ponds of variable ephemerality in Tanzania from August 2021 to July 2022. First, we found that ponds have two synchronized peaks of schistosome infection prevalence and observed cercariae, though of lower magnitude in the fully desiccating than non-desiccating ponds. Second, we evaluated total yearly schistosome prevalence across an ephemerality gradient, finding ponds with intermediate ephemerality to have the highest infection rates. We also investigated dynamics of non-schistosome trematodes, which lacked synonymity with schistosome patterns. We found peak schistosome transmission risk at intermediate pond ephemerality, thus the impacts of anticipated increases in landscape desiccation could result in increases or decreases in transmission risk with global change.

Keywords: Bulinus; Schistosoma haematobium; aestivation; ephemerality; schistosomiasis; seasonality.

Figure 1.

Map of localities of 109 ponds surveyed (red squares) across six districts of northwestern Tanzania, with inset of locality of sites within the continent of Africa.

Figure 2.

Change in area of (a) a desiccating pond in Misungwi district, Kisima cha Longo (reduction of pond area of 100%) and (b) a non-desiccating pond in Busega district, Lambo la Wachina (reduction of pond area of 79.78%) within a survey year.

Figure 3.

Generalized Additive Models (GAMMs) representing circannual (a) rainfall patterns (mm per day) in Mwanza, Tanzania of data from the airport weather station, and variability in (b) pond depth (m) and (c) Bulinus nasutus snail abundance (number collected in 30 min survey) in our 109 sites. The shaded region surrounding the line represents the best fit ± 1 s.e. Points represent monthly means and standard error. Depth and snail abundance were significantly nonlinear and different between the two ephemerality categories.

Figure 4.

GAMMs representing circannual (a) schistosome prevalence, (b) schistosome per capita cercariae observed, (c) schistosome total cercaria release per survey, (d) non-schistosome prevalence, (e) non-schistosome per capita cercariae observed, and (f) non-schistosome total cercaria observed per survey in desiccating and non-desiccating ponds. The shaded region surrounding the line represents the best fit ± 1 s.e. Points represent monthly means and standard error. All patterns were significantly nonlinear and different between the two ephemerality categories, except per capita cercariae observed was equivalent between two pond types.

Figure 5.

Overall yearly (a) schistosome and (b) non-schistosome trematode infection prevalence in across an ephemerality gradient (% decrease in pond area in the dry season). The shaded region surrounding the line represents the best fit with 95% CI. Points represent yearly prevalence in each pond and the size is indicative of the number of snails collected in each pond per year. Schistosome prevalence peaks at intermediate ephemerality (approx. 80% area decrease, binomial GLM, p < 0.01). Non-schistosome prevalence peaks at low ephemerality (approx. 50% area decrease, binomial GLM, p < 0.01).