Hydrology and density feedbacks control the ecology of intermediate hosts of schistosomiasis across habitats in seasonal climates

Abstract

We report about field and theoretical studies on the ecology of the aquatic snails (Bulinus spp. and Biomphalaria pfeifferi) that serve as obligate intermediate hosts in the complex life cycle of the parasites causing human schistosomiasis. Snail abundance fosters disease transmission, and thus the dynamics of snail populations are critically important for schistosomiasis modeling and control. Here, we single out hydrological drivers and density dependence (or lack of it) of ecological growth rates of local snail populations by contrasting novel ecological and environmental data with various models of host demography. Specifically, we study various natural and man-made habitats across Burkina Faso's highly seasonal climatic zones. Demographic models are ranked through formal model comparison and structural risk minimization. The latter allows us to evaluate the suitability of population models while clarifying the relevant covariates that explain empirical observations of snail abundance under the actual climatic forcings experienced by the various field sites. Our results link quantitatively hydrological drivers to distinct population dynamics through specific density feedbacks, and show that statistical methods based on model averaging provide reliable snail abundance projections. The consistency of our ranking results suggests the use of ad hoc models of snail demography depending on habitat type (e.g., natural vs. man-made) and hydrological characteristics (e.g., ephemeral vs. permanent). Implications for risk mapping and space-time allocation of control measures in schistosomiasis-endemic contexts are discussed.

Keywords: environmental monitoring; freshwater snails; infection controls; water-based disease.

Fig. 1.

Ecological and environmental field data. (A) Situation map of the field sites (black dots) chosen along the South/North climatic gradient in Burkina Faso, here highlighted by values of the normalized difference vegetation index (source in SI Appendix), and the state capital (Ouagadougou). (B–E) Illustrations of the ephemeral or permanent habitats chosen for snail sampling in the experimental sites of Tougou, Lioulgou, and Panamasso. (F–W) Ecological and environmental data time series. Weekly snail relative abundance data are given per species and habitat: Bulinus spp. in a canal in Tougou (solid line) (F) and in a pond (short dashed line) and a stream (long dashed line) in Lioulgou (G) and B. pfeifferi (dashed line) and Bulinus spp. (dotted line) in a stream in Panamasso (H). Periods during which the habitat dried out are indicated for Lioulgou and Tougou (canal closed for operational reasons). Their respective environmental data are given in columnar format. Environmental data consist of weekly cumulative precipitation (I–K) and daily averages of air temperature (L–N), water temperature (O–Q), conductivity (R–T), and water depth (U–W). Graphs containing the term “NA” indicate ephemeral habitats (S and V). Details on sampling and environmental monitoring methods are given in the SI Appendix.

Fig. 2.

Density feedbacks, environmental covariates, and snail population dynamics. The strength of density feedbacks (A–E) and of measured environmental covariate features (F–J) is given in terms of the frequency of appearance in the 500 best-selected models, summarized by decile (decile 10 corresponds to the top 10% of model outcomes). Results are shown in columnar format for Bulinus spp. in the irrigation canal (A–F), in the temporary pond (B–G), and in the ephemeral stream (C–H), and for B. pfeifferi (D–I) and Bulinus spp. (E–J) in the perennial stream.

Fig. 3.

Observed and predicted snail abundances. Abundance (dots), LOO-CV prediction of the 500 best models (gray lines, increasing transparency indicating lower SRM performance), and JMA of the set (red line) are given for Bulinus spp. in the irrigation canal (A), the temporary pond (B), and the ephemeral stream (C), and for B. pfeifferi (D) and Bulinus spp. (E) in the perennial stream. Average predictions in the case of partial model averages due to missing data are also shown (dash-dotted red line; SI Appendix).