Comparative analysis of time-based and quadrat sampling in seasonal population dynamics of intermediate hosts of human schistosomes

Abstract

Background: Despite their importance for designing and evaluating schistosomiasis control trials, little attention in the literature has been dedicated to sampling protocols for the parasite's snail intermediate hosts since their first development. We propose a comparative analysis of time-based and quadrat sampling protocols to quantify the seasonal variations in the abundance of these aquatic snail species of medical importance.

Methodology/principal findings: Snail populations were monitored during 42 consecutive months in three types of habitats (ephemeral pond, ephemeral river and permanent stream) in two sites covering different climatic zones in Burkina Faso. We employed both a widely used time-based protocol of 30min of systematic collection at a weekly interval, and a quadrat protocol of 8 replicates per sample at a monthly interval. The correspondence between the two protocols was evaluated using an ensemble of statistical models including linear and saturating-type functional forms as well as allowing for count zero-inflation. The quadrat protocol yielded on average a relative standard error of 40%, for a mean snail density of 16.7 snails/m2 and index of dispersion of 1.51. Both protocols yielded similar seasonal patterns in snail abundance, confirming the asynchrony between permanent and ephemeral habitats with respect to the country's seasonal rainfall patterns. Formal model comparison of the link between time vs. quadrat counts showed strong support of saturation for the latter and measurement zero-inflation, providing important evidence for the presence of density feedbacks in the snail's population dynamics, as well as for spatial clustering.

Conclusions/significance: In addition to the agreement with the time-based method, quadrat sampling provided insight into snail population dynamics and comparable density estimates across sites. The re-evaluation of these "traditional" sampling protocols, as well as the correspondence between their outputs, is of practical importance for the design and evaluation of schistosomiasis control trials.

Fig 1. Situation map of field sites and habitats.

a. Burkina Faso with its capital (Ouagadougou) and the location of the two field sites (in red) along the precipitation gradient (2014-2017 average, CHIRPS data [51]). The map was produced with QGIS (version 3.6) with country boundaries provided by GADM (version 3.4). Sampled habitats in Lioulgou included an ephemeral pond (b) and a river (c), and a permanent stream in Panamasso (d).

Fig 2. Quadrat sampling scheme performance.

Reported are the distribution of standard errors ($SE=\sigma /\sqrt{n}\left[{\text{snails}}^{\frac{1}{2}}/\text{m}\right]$), relative standard errors (SE/μ [-]), the index of dispersion (I_D = σ²/μ [-]) and the mean density (μ [snails/m²]) by habitat and intermediate host species.

Fig 3. Ecological monitoring data of intermediate hosts of schistosomiasis in Burkina Faso.

Data was collected in three different habitats in two distinct sites, one in the Sudano-Sahelian climatic zone (pond and river, village of Lioulgou), and one in the Sudanian climatic zone (stream, village of Panamasso). Data are presented in terms of the number of observed counts (grey points) by intermediate host genera for the quadrat (top row) and time-based method (bottom row) protocols with blue rectangles indicating timing of the rainy season (July-September). Monthly means (red points) for the quadrat method consist of the average of the 8 quadrat replicates on the sampling date, and the mean of the weekly time-based counts grouped to the closest month start, along with their 95% CI (red errorbars, mean ±1.96 SE). Note that quadrat data in the months of June-October of 2016 were not collected in the permanent stream in Panamasso due to logistical constraints.

Fig 4. Comparison of monthly mean densities from the quadrat and time-based sampling schemes.

Horizontal and vertical errorbars give the 95% CI of the time-based and quadrat-based means respectively.

Fig 5. Model simulations of the relations between time-based and quadrat sampling strategies.

Simulations were performed using the 95% credible model set (S1 Table) for each species-habitat configuration. Simulations are shown in terms of the mean (black line) as well as the 95% (light gray ribbon) and 50% (dark gray ribbon) simulation envelops for 5000 simulations per time-based count. Quadrat counts (gray dots) are given as in the first row of Fig 3 along with monthly means (red dots).