Molluscicidal effectiveness of Luo-Wei, a novel plant-derived molluscicide, against Oncomelania hupensis, Biomphalaria alexandrina and Bulinus truncatus

Abstract

Background: Control of snail intermediate hosts has been proved to be a fast and efficient approach for interrupting the transmission of schistosomiasis. Some plant extracts have shown obvious molluscicidal activity, and a new compound Luo-Wei, also named tea-seed distilled saponin (TDS), was developed based on the saponins extracted from Camellia oleifera seeds. We aimed to test the molluscicidal activity of 4% TDS against the intermediate host snails in China and Egypt, and evaluate its environmental safety to non-target organisms.

Methods: In the laboratory, Oncomelania hupensis, Biomphalaria alexandrina and Bulinus truncatus were exposed to 4% TDS, and the median lethal concentration (LC₅₀) was estimated at 24, 48 and 72 h. In the field, snail mortalities were assessed 1, 2, 3 and 7 d post-immersion with 2.5 g/m³ 4% TDS and 1, 3, 7 and 15 d post-spraying with 5 g/m² 4% TDS. In addition, the acute toxicity of 4% TDS to Japanese quail (Coturnix japonica), zebrafish (Brachydanio rerio) and freshwater shrimp (Macrobrachium nipponense) was assessed by estimations of LC₅₀ or median lethal dose (LD₅₀).

Results: In the laboratory, the LC₅₀ values of 4% TDS for O. hupensis were 0.701, 0.371 and 0.33 mg/L at 24, 48 and 72 h, respectively, and 4% TDS showed a 1.975 mg/L [corrected] 24 h LC₅₀ against B. alexandrina, and a 1.396 mg/L 24 h LC₅₀ against B. truncatus. Across all study regions, the pooled mortalities of O. hupensis were 72, 86, 94 and 98% at 1, 2, 3 and 7 d, following field immersion of 4% TDS at a dose of 2.5 g/m³, and were 69, 77, 85 and 88% at 1, 3, 7 and 15 d, following field spraying at 5 g/m², respectively. 4% TDS had moderate toxicity to Japanese quail (7 d LD₅₀ > 60 mg/kg) and to shrimp (96 h LC₅₀ = 6.28 mg/L; 95% CI: 3.53-11.2 mg/L), whereas its toxicity to zebrafish was high (96 h LC₅₀ = 0.15 mg/L; 95% CI: 0.14-0.17 mg/L).

Conclusions: 4% TDS is active against O. hupensis, B. alexandrina and B. truncatus under laboratory and field conditions, and it may be a candidate molluscicide of plant origin.

Keywords: Biomphalaria alexandrina; Bulinus truncatus; Luo-Wei; Molluscicidal activity; Oncomelania hupensis; Plant-derived molluscicide; Schistosomiasis.

Fig. 1

Structural formula of TDS (Luo-Wei) and its chemical name. TDS (C₅₂H₈₄O₂₄, molecular weight 1093.23) is a pentacyclic triterpenoid saponin extracted from the tea seed pomace (Camellia oleifera) that is left after commercial pressing of seeds for tea oil. Its chemical name listed at the International Union of Pure and Applied Chemistry (IUPAC) is(3β, 16α)-28-oxo-D-xylopyranose-(1 → 3)-O -β-D-pyran-(1 → 4)-O-6-deoxy-α-L-mannopyranosyl-(1 → 2)-β-D-xylopyranose-17 -hydroxymethyl-16, 21, 22-trihydroxyoleanolic-12-alkene

Fig. 2

Distribution of the study areas to test the field molluscicidal efficacy of 4% TDS against Oncomelania hupensis in China. During the period between 2011 and 2014, field assessment of 4% TDS against O. hupensis was conducted in provinces that were endemic for S. japonicum in China, including Hunan, Hubei, Jiangxi, Anhui, Jiangsu, Sichuan, and Yunnan

Fig. 3

Dose-response curves of Oncomelania hupensis, Biomphalaria alexandrina, and Bulinus truncatus snails subjected to aqueous dilutions of 4% TDS for 24 h. a Oncomelania hupensis; b Biomphalaria alexandrina; c Bulinus truncatus; d The equality and parallelism of the regression lines of different snail species after 24 h exposure, tested by LR. O. h., Oncomelania hupensis; B. a., Biomphalaria alexandrina; B. t., Bulinus truncatus. The equality of the regression lines were tested using the likelihood ratio (LR). In general, there are significant differences between slopes and intercepts of lines (χ² = 206, P < 0.05). The parallelism of slopes is tested by the LR. In general, there are significant differences between the regression lines (χ² = 39.6, P < 0.05)

Fig. 4

Molluscicidal effect of 4% TDS by immersion in the field. a Mortality of Oncomelania hupensis post-exposure to 4% TDS by immersion in the field. Danling_1, conducted in the ditch; Danling_2, conducted in the paddy field. b–e Comparison of Oncomelania hupensis mortalities (individual and pooled results) between TDS (2.5 g/m³) and WPN (2 g/m³) 1 (b), 2 (c), 3 (d) and 7 d (e) post-immersion in the field, studies performed 2011 to 2013. There is no significant difference in the pooled effects between TDS and WPN 7 d post-immersion (e), of which the relative risk values (TDS/WPN) for snail mortality was 0.991 (95% CI: 0.975–1.006)

Fig. 5

Molluscicidal effect of 4% TDS by spraying in the field. a, Mortalities of Oncomelania hupensis post-exposure by ground spraying of 4% TDS in the field. b–e Comparison of Oncomelania hupensis mortalities (individual and pooled results) between TDS (5 g/m²) and WPN (2 g/m²) 1 (b), 3 (c), 7 (d) and 15 d (e) post-spraying in the field, studies performed 2011 to 2013. There is no significant difference in the pooled effects between TDS and WPN at 7 d (d) and 15 d (e) post-spraying, of which the relative risk values (TDS/WPN) for snail mortality are 0.968 (95% CI: 0.917–1.021) at 7 d and 0.99 (95% CI: 0.952–1.030) at 15 d, respectively