Nutritional effects of invasive macrophyte detritus on Schistosoma mansoni infections in snail intermediate hosts

Abstract

Schistosomes are parasitic flatworms that cycle between humans and freshwater snails, infecting more than 200 million humans. Many schistosome-endemic sites are invaded by non-native plants that snails cannot consume. Inedible plants could suppress snail growth, reproduction, and schistosome production by outcompeting edible resources. Alternatively, their decomposition could create edible detritus that fuels snail growth, reproduction, or schistosome production. We evaluated the nutritional effects of detritus from four widespread invasive plants on human schistosomes, Schistosoma mansoni, and snail intermediate hosts, Biomphalaria glabrata. We predicted that water hyacinth, which is fibrous and waxy, would cause poor growth, reproduction, and parasite production. In contrast, we predicted water lettuce, water fern, and duckweed would enable rapid growth, reproduction, and parasite production via better nutrient content and digestibility. Infected snails consuming water fern and water lettuce grew ~100% larger and produced ~9-fold more cercariae than those consuming water hyacinth or duckweed. We then tested whether extended decomposition of water hyacinth could improve snail and schistosome performance but found negligible effects. Managers should prioritize removal of plants that produce nutritious detritus, because in situ destruction could increase schistosome transmission. Characterizing interactions among plant invasions, management, and parasites could facilitate solutions that improve human and environmental health.

Keywords: Resource ecology; food quality; infection; intermediate host; invasive plants; schistosomes.

Figure 1.

Effects of laboratory food and detritus from four invasive macrophytes (x-axis) and infections status (column) on (A, B) snail growth, (C, D) snail reproduction, (E, F) snail survival, and (G) parasite production. For survival points represent treatment means ± SE and all other panels are represented with boxplots indicating median, interquartile range, and outliers. In each panel, treatment pairs with no letters in common significantly differ. (A) Infected snails consuming laboratory (N = 18) food grew largest, and snails consuming water lettuce (N = 15) and water fern (N = 18) grew significantly larger than snails consuming water hyacinth (N = 8) and duckweed (N = 9). (B) Uninfected snails consuming water lettuce (N = 8) and water fern (N = 8) grew comparably to those eating lab food (N = 6) and significantly larger than snails consuming water hyacinth (N = 8) and duckweed (N = 8). (C) Infected snails produced essentially no eggs. (D) Uninfected snails consuming water lettuce reproduced significantly more than snails consuming any other macrophyte. (E) There were no differences in survival of infected snails across macrophytes, but those consuming duckweed and water hyacinth died faster than snails consuming lab food. (F) Survival was high for all uninfected snails (G) Infected snails consuming water lettuce, laboratory food and water fern produced more cercariae than snails consuming water hyacinth and duckweed.

Figure 2.

Effects of water hyacinth decomposition time (2, 21, or 49 days) vs high-quality laboratory food (x-axis) and infections status (column) on (A, B) snail growth, (C, D) snail reproduction, (E, F) snail survival , and (G) parasite production. For survival points represent treatment means ± SE and all other panels are represented with boxplots indicating median, interquartile range, and outliers. Each treatment contained 8 uninfected snails. Laboratory food had N = 14 infected snails while the 2-, 21-, and 49-day decomposition treatments had N = 6, 17, and 13 infected snails, respectively. In each panel, treatment pairs with no letters in common significantly differ. In general, decomposition time had small effects on the size of (A) infected and (B) uninfected snails. Snails consuming laboratory food were significantly larger than all hyacinth treatments. Regardless of decomposition time, (C, D) all snails consuming water hyacinth failed to reproduce, whereas snails consuming laboratory food successfully reproduced. There were no differences in survival across any food treatments for (E) infected or (F) uninfected snails. (G) All decomposition treatments yielded similarly poor parasite production, which was significantly lower than for snails consuming laboratory food.