Experimental water hyacinth invasion and destructive management increase human schistosome transmission potential

Abstract

Invasive species cause environmental degradation, decrease biodiversity, and alter ecosystem function. Invasions can also drive changes in vector-borne and zoonotic diseases by altering important traits of wildlife hosts or disease vectors. Managing invasive species can restore biodiversity and ecosystem function, but it may have cascading effects on hosts, parasites, and human risk of infection. Water hyacinth, Eichhornia crassipes, is an extremely detrimental invader in many sites of human schistosome transmission, especially in Lake Victoria, where hyacinth is correlated with high snail abundance and hotspots of human schistosome infection. Hyacinth is often managed via removal or in situ destruction, but the effects of these strategies on snail intermediate hosts and schistosomes are not known. We evaluated the effects of water hyacinth invasion and these management strategies on the dynamics of human schistosomes, Schistosoma mansoni, and snails, Biomphalaria glabrata, in experimental mesocosms over 17 weeks. We hypothesized that hyacinth, which is inedible to snails, would affect snail growth, reproduction, and cercariae production through the balance of its competitive effects on edible algae and its production of edible detritus. We predicted that destruction would create a pulse of edible detrital resources, thereby increasing snail growth, reproduction, and parasite production. Conversely, we predicted that removal would have small or negligible effects on snails and schistosomes, because it would alleviate competition on edible algae without generating a resource pulse. We found that hyacinth invasion suppressed algae, changed the timing of peak snail abundance, and increased total production of human-infectious cercariae ~6-fold relative to uninvaded controls. Hyacinth management had complex effects on algae, snails, and schistosomes. Removal increased algal growth and snail abundance (but not biomass), and slightly reduced schistosome production. In contrast, destruction increased snail biomass (but not abundance), indicating increases in body size. Destruction caused the greatest schistosome production (10-fold more than the control), consistent with evidence that larger snails with greater access to food are most infectious. Our results highlight the dynamic effects of invasion and management on a globally impactful human parasite and its intermediate host. Ultimately, preventing or removing hyacinth invasions would simultaneously benefit human and environmental health outcomes.

Keywords: inedible plant; intermediate host; invasive species management; population dynamics; resource competition; schistosomes.

Figure 1.

Growth of water hyacinth (wet mass, g ± SE) over 17 weeks. Shapes and lines indicate management strategy implemented on week 7. Water hyacinth steadily increased in biomass after a slight decrease when the populations were established.

Figure 2.

Effects of water hyacinth invasion (green) compared to uninvaded control mesocosms (black) on (A) periphyton productivity measured in arbitrary fluorescence units, AU, (B) snail abundance, and (C) snail population biomass, as well as (D) reproduction and (E) cercarial production. Points and error bars are treatment means ± SE. Lines and shaded regions are model fits ± SE. (A) As predicted, hyacinth invasion suppressed algal production. It also caused an earlier, smaller peak in (B) snail abundance and (C) biomass. Invasion also (D) reduced reproduction, especially in weeks 6–10. Despite this, invasion caused substantial increases in (E) cercarial production, especially during peaks in cercariae during weeks 4–6 and 13–15.

Figure 3.

Effects of water hyacinth management (in situ destruction: brown, removal: blue) vs unmanaged invasions (green) on (A) periphyton productivity measured in arbitrary fluorescence units, AU, (B) snail abundance, and (C) snail population biomass, as well as (D) reproduction and (E) cercarial production compared to uninvaded control mesocosms (black). Points and error bars are treatment means ± SE. Lines and shaded regions are model fits ± SE. Given invasion, hyacinth destruction caused (A) a marginally significant transient increase in algal productivity, whereas removal permanently increased algal growth. (B) Neither intervention significantly affected snail abundance. However, hyacinth destruction substantially increased (C) the biomass of snail populations. It also stimulated abundant (D) snail reproduction – although (B) the resulting juveniles were never observed in these populations Lastly, (E) destruction caused a shift in the timing of cercarial production and resulted in a large pulse of cercarial production on week 12, whereas removal caused a slight but significant reduction in cercarial production throughout the post-intervention period.

Figure 4:

Boxplot comparison of cumulative cercarial production across the 17-week experiment for all treatments. The thick line represents the median value, the extent of the box represents the interquartile range (IQR; 25^th – 75^th percentiles), the error bars indicate a range 1.5-fold beyond the IQR and points represent observations beyond that span. Unmanaged hyacinth invasion and in situ destruction caused significant increases in cumulative cercarial production when compared against the uninvaded control (indicated with asterisks). No other treatments significantly differed from the uninvaded treatment.