Regulation of laboratory populations of snails (Biomphalaria and Bulinus spp.) by river prawns, Macrobrachium spp. (Decapoda, Palaemonidae): implications for control of schistosomiasis

Abstract

Human schistosomiasis is a common parasitic disease endemic in many tropical and subtropical countries. One barrier to achieving long-term control of this disease has been re-infection of treated patients when they swim, bathe, or wade in surface fresh water infested with snails that harbor and release larval parasites. Because some snail species are obligate intermediate hosts of schistosome parasites, removing snails may reduce parasitic larvae in the water, reducing re-infection risk. Here, we evaluate the potential for snail control by predatory freshwater prawns, Macrobrachium rosenbergii and M. vollenhovenii, native to Asia and Africa, respectively. Both prawn species are high value, protein-rich human food commodities, suggesting their cultivation may be beneficial in resource-poor settings where few other disease control options exist. In a series of predation trials in laboratory aquaria, we found both species to be voracious predators of schistosome-susceptible snails, hatchlings, and eggs, even in the presence of alternative food, with sustained average consumption rates of 12% of their body weight per day. Prawns showed a weak preference for Bulinus truncatus over Biomphalaria glabrata snails. Consumption rates were highly predictable based on the ratio of prawn: snail body mass, suggesting satiation-limited predation. Even the smallest prawns tested (0.5-2g) caused snail recruitment failure, despite high snail fecundity. With the World Health Organization turning attention toward schistosomiasis elimination, native prawn cultivation may be a viable snail control strategy that offers a win-win for public health and economic development.

Keywords: Biological control; Functional response; Predation; Predator; Schistosoma haematobium; Schistosoma mansoni.

Figure 1

Comparing consumption rates for two prawn species: M. rosenbergii (filled circles) and M. vollenhovenii (open triangles). The dashed line represents the “line of equivalence,” or a constant 12% consumption rate over all body sizes which was the average overall consumption rate (it is not a regression line). Points above the line represent trials in which prawns ate more than the average of 12% of their body weight daily and those falling below the line ate less than 12%. Each point and vertical bar represents the average and standard error of multiple consecutive consumption trials with a single prawn. Trials where prawns were offered single-species populations of either B. glabrata (three size classes) or Bu. truncatus (one size class) were combined to generate this figure.

Figure 2

Consumption and elimination of high-density mixed-sized populations of B. glabrata snails (80 snails/tank) by small M. rosenbergii prawns (2–3g; circles), medium M. rosenbergii prawns (7–12g, triangles) and very large M. rosenbergii prawns (>30g, squares). Data for small and medium prawns are from Roberts and Kuris (1990); data for very large prawns are from this study.

Figure 3

The effect of (A) snail size and (B) prawn size on snail consumption rates by prawns. XS = <1g prawns; S= 1–3g prawns; M= 3–10g prawns; L=10–30g prawns; Market = >30g prawns. Data from both M. rosenbergii and M. vollenhovenii preying on snails of either B. glabrata or B. truncatus were combined to generate this figure.

Figure 4

Results of preference trials for Small (<3g) and Market sized (>30g) M. rosenbergii prawns when offered either single species populations of B. glabrata snails of three size classes (S = 4mm ± 2mm, M = 8mm ± 2mm, L = 12mm ± 2mm) or two snail species (BT = B. truncatus, BG = B. glabrata) in equal ratios. Outcomes are similar whether expressed in terms of biomass of snails consumed (top graph) or the number of snails consumed (bottom graph).

Figure 5

(A) A subset of best fit functional response curves, based on least squares fitting of Holling’s disc equation for prawns of different size (Small = 1–3g prawns, Medium = 3–10g prawns, Market = >30g prawns) consuming B. glabrata snails of different size classes (8mm or 12mm ± 2mm shell length). (B) The relationship between the parameters governing the attack rate and handling time and prawn:snail body mass ratio, showing a predictable functional response. Data for M. vollenhovenii and M. rosenbergii preying on either B. glabrata or B. truncatus were combined to generate this figure.

Figure 6

Results of 90-day population regulation experiments using very small M. vollenhovenii (0.5–2g) prawns. Shown are the trajectories over time for snail eggs (A,E), hatchlings (B, F), juveniles (C, G), and new adults, not including the founding population (D,H) in prawn-treatment (solid lines) and control tanks (dashed lines). Small prawns strongly suppressed recruitment, despite their inability to consume adult snails, even with an increased standing biomass of snail eggs. Snails began to hatch at day 10 and then passed through successive size cohorts until they reached adult size by day 40–50.

Figure 7

Effect of five treatments on (A) snail fecundity (egg masses/adult snail) and (B) recruitment (new snail recruits/adult snail) in laboratory populations of Biomphalaria pfeifferi snails. “Removal” = manual snail recruit removal (by crushing weekly) plus 0.15g shrimp diet added daily; “3 prawns” = 3 M. vollenhovenii prawns (0.5–2g each) housed/tank plus 0.15g shrimp diet added daily, “single prawn” = 1 M. vollenhovenii prawn (0.5–2g) housed/tank plus 0.15g of shrimp diet added daily, food only = 0.15g shrimp diet added daily (no prawns or recruit removal), and neg control = a negative control whereby snails were only fed lettuce ad libitum. Bars sharing a letter are not significantly different.

Figure 8

Proposed trophic interactions between large or small prawns and adult snails, snail recruits, and snail eggs. Large prawns have negative direct and indirect effects on all snail life stages. On the other hand, small prawns (<2g) are limited in their ability to kill adult snails. A negative effect of juvenile recruit snails on eggs (due to competitive or egg-cannibalistic effects) led to positive indirect effects of small prawns on snail eggs, despite a strong negative effect on snail recruitment.