Hostname: page-component-6898cfcb55-zsp5v Total loading time: 0 Render date: 2026-11-11T10:24:37.324Z Has data issue: false hasContentIssue false
  • English
  • Français

Molluscicidal and ovicidal activities of plant extracts of the Piperaceae on Biomphalaria glabrata (Say, 1818)

Published online by Cambridge University Press:  06 May 2010

L.N. Rapado,
E. Nakano,
F.P. Ohlweiler,
M.J. Kato,
L.F. Yamaguchi,
C.A.B. Pereira and
T. Kawano
L.N. Rapado*
Affiliation:
Instituto de Ciências Biomédicas, Universidade de São Paulo, BrazilLab. Parasitologia e Malacologia, Instituto Butantan, São Paulo, Brazil
E. Nakano
Affiliation:
Lab. Parasitologia e Malacologia, Instituto Butantan, São Paulo, Brazil
F.P. Ohlweiler
Affiliation:
Superintendência de Controle de Endemias (SUCEN), São Paulo, Brazil
M.J. Kato
Affiliation:
Lab. Química de Produtos Naturais, Universidade de São Paulo, Brazil
L.F. Yamaguchi
Affiliation:
Lab. Química de Produtos Naturais, Universidade de São Paulo, Brazil
C.A.B. Pereira
Affiliation:
Depto de Estatística, Núcleo de Bioinformática, Instituto de Matemática, Universidade de São Paulo, São Paulo, SP, Brazil
T. Kawano
Affiliation:
Lab. Parasitologia e Malacologia, Instituto Butantan, São Paulo, Brazil
*
*E-mail: ludmilanr@usp.br
Rights & Permissions [Opens in a new window]

Abstract

Schistosomiasis is a tropical disease caused by Schistosoma and occurs in 54 countries, mainly in South America, the Caribbean region, Africa and the eastern Mediterranean. Currently, 5 to 6 million Brazilian people are infected and 30,000 are under infection risk. Typical of poor regions, this disease is associated with the lack of basic sanitation and very frequently to the use of contaminated water in agriculture, housework and leisure. One of the most efficient methods of controlling the disease is application of molluscicides to eliminate or to reduce the population of the intermediate host snail Biomphalaria glabrata. Studies on molluscicidal activity of plant extracts have been stimulated by issues such as environmental preservation, high cost and recurrent resistance of snails to synthetic molluscicides. The aim of this study was to determine the molluscicide action of extracts from Piperaceae species on adult and embryonic stages of B. glabrata. Fifteen extracts from 13 Piperaceae species were obtained from stems, leaves and roots. Toxicity of extracts was evaluated against snails at two different concentrations (500 and 100 ppm) and those causing 100% mortality at 100 ppm concentration were selected to obtain the LC90 (lethal concentration of 90% mortality). Piper aduncum, P. crassinervium, P. cuyabanum, P. diospyrifolium and P. hostmannianum gave 100% mortality of adult snails at concentrations ranging from 10 to 60 ppm. These extracts were also assayed on embryonic stages of B. glabrata and those from P. cuyabanum and P. hostmannianum showed 100% ovicidal action at 20 ppm.

Information

Type
Research Papers
Information
Journal of Helminthology , Volume 85 , Issue 1 , March 2011, pp. 66 - 72
Copyright
Copyright © Cambridge University Press 2010

Introduction

Schistosomiasis remains one of the most prevalent parasitic infections in the world and has significant economic and public health consequences. It is estimated that 200 million people are infected and 600 million people are at risk of infection (WHO, 1993; Chitsulo et al., Reference Chitsulo, Engels, Montresor and Savioli2000).

Three main schistosome species infect humans: Schistosoma mansoni, present mainly in Africa and South America; S. haematobium, found in Africa and the Middle East; and S. japonicum, which is endemic in Asia. Freshwater snails of the genus Biomphalaria play a major role as intermediate hosts in the transmission of S. mansoni. An intense multiplication of parasites occurs in these snails, making strategies to control snail populations a high priority for reduction of schistosomiasis transmission in endemic regions (WHO, 1984; Rey, Reference Rey2008).

At present, niclosamide (Bayluscide®, Bayer, Leverkusen, Germany) is the only commercially available molluscicide recommended by the World Health Organization (WHO) for large-scale use in schistosomiasis control programmes (WHO, 1993). Niclosamide is not toxic to humans, domestic animals or crops, although it is costly and ictiotoxic (WHO, 1973; McCullough & Mott, Reference McCullough and Mott1983). Moreover, it is rapidly decomposed by sunlight and its application does not prevent recolonization of sites by surviving snails, which could lead to selection of molluscicide-resistant populations. Thus, novel natural molluscicidal compounds from plants should be investigated as possible alternatives to synthetic products (Luna et al., Reference Luna, Santos, Lima, Omena, Mendonça, Bieber and Sant'Ana2005).

Members of the Piperaceae family are among a wide variety of species under study. The family comprises 14 genera and 1950 species (Mabberley, Reference Mabberley1997); Piper and Peperomia are the most abundant genera, with approximately 700 and 600 species, respectively (Joly, Reference Joly1993). Plants from the genus Piper are widely distributed throughout tropical and subtropical regions. Brazil has several species and promising studies on biological properties of plants of the Piperaceae family have been published (Navickiene et al., Reference Navickiene, Alécio, Kato, Bolzani, Young, Cavalheiro and Furlan2000; Danelutte et al., Reference Danelutte, Lago, Young and Kato2003, Reference Danelutte, Constantin, Delgado, Braz-Filho and Kato2005; Cysne et al., Reference Cysne, Canuto, Pessoa, Nunes and Silveira2005; Yamaguchi et al., Reference Yamaguchi, Lago, Tanizaki, Masuo and Kato2006).

Phytochemical investigations on Piper species have revealed many bioactive compounds such as amides, alkaloids, lignans, benzoic acids and chromenes (Parmar et al., Reference Parmar, Jain, Bisht, Jain, Taneja, Jha, Tyagi, Prasad, Wengel, Olsen and Boll1997; Alécio et al., Reference Alécio, Bolzani, Young, Kato and Furlan1998; Navickiene et al., Reference Navickiene, Alécio, Kato, Bolzani, Young, Cavalheiro and Furlan2000; Silva et al., Reference Silva, Navickiene, Kato, Bolzani, Meda, Young and Furlan2002). Chromenes and benzoic acid derivatives are frequently isolated from Piper species showing antimicrobial, antitumoral, germination inhibition, fungicidal (Nair & Burke, Reference Nair and Burke1990), insecticidal (Miranda et al., Reference Miranda, Oliveira, Rocha, Bortoli, Navickiene, Kato and Furlan2002) and anti-leishmania activities (Torres-Santos et al., Reference Torres-Santos, Moreira, Kaplan, Meirelles and Rossi-Bergmann1999). In the case of molluscicidal activity, only a few reports have addressed Piper species, including essential oil from P. marginatum (Rouquayrol et al., Reference Rouquayrol, Fonteles, Alencar, Matos and Craveiro1980) and P. tuberculatum (Sousa & Rouquayrol, Reference Sousa and Rouquayrol1974), chromenes and benzoic acid from P. aduncum (Orjala et al., Reference Orjala, Erdelmeier, Wright and Sticher1993a, Reference Orjala, Erdelmeier, Wright, Rali and Sticherb) and extracts from P. cubeba (Pandey & Singh, Reference Pandey and Singh2009).

In spite of the variety of secondary compounds described, no systematic evaluation of molluscicidal activity of Piperaceae extracts has been carried out. Thus, in this work, several crude extracts were assessed regarding molluscicidal and ovicidal properties.

Materials and methods

Molluscicidal and ovicidal assays were performed according to the methodology recommended by World Health Organization (WHO, 1965, 1983) and experimental procedures were employed according to accepted principles of animal welfare in experimental science.

Adults and egg masses were obtained from the population of Biomphalaria glabrata (Say, 1818) originally from Belo Horizonte, MG, Brazil and reared under laboratory conditions for several years, fed with fresh lettuce ad libitum and a balanced ration.

Plant material

Fresh material of each species (table 1) was collected by Dr Massuo Jorge Kato and identified by Dr Elsie F. Guimarães from Instituto de Pesquisas Jardim Botânico do Rio de Janeiro and vouchers were deposited in the Herbarium of Jardim Botânico do Rio de Janeiro.

Table 1

Piperaceae species screened for molluscicidal activity in B. glabrata.

Selected part for all species, leaves; * stem, leaves and roots. S, São Paulo; RJ, Rio de Janeiro, AM, Amazonas.

Preparation of plant extracts

Selected parts (table 1) of freshly collected plant material were separated, immediately air dried and finally dried in an oven at 45°C. Material was ground and powdered materials were extracted with dichloromethane:methanol (2:1) at room temperature (25–27°C) three times and filtered. Extracts were evaporated to dryness under vacuum in a rotoevaporator and stored at − 20°C.

A stock solution containing 1000 ppm of each extract was prepared by suspending 10 mg of extract in 0.1 ml of 99.9% dimethylsulphoxide (DMSO; Aldrich, Milwaukee, Wisconsin, USA) and making up to 10 ml with dechlorinated water. Stock solutions were diluted with dechlorinated water in order to provide assay solutions.

Assays for molluscicidal/ovicidal activities of plant extracts

Molluscicidal activities of extracts against adults of B. glabrata were determined according to previously described procedures (WHO, 1965, 1983). Snails with 10–18 mm shell diameter were exposed to test compounds for 24 h. After exposure, snails were washed and observed daily for 10 days to record the death rate. A negative control group was maintained in dechlorinated tap water containing 1% DMSO under the same experimental conditions. Bayluscide WP70® was used as a positive control. Extracts were tested first at concentrations of 500 and 100 ppm and those inactive were not investigated further. LC90 was determined for all selected extracts with ten animals per dose group, and experiments were repeated three times.

Based on values of LC90 for adults, egg masses with embryos at blastula stage (Camey & Verdonk, Reference Camey and Verdonk1970) were exposed to lethal concentrations of extracts for 24 h. At the end of exposure, egg masses were washed and observed for mortality daily for 7 days. Assays were repeated three times with about 100 embryos for each concentration. A control group was maintained in dechlorinated water containing 1% DMSO under the same experimental conditions.

Data analysis

LC90 was obtained from the logistic regression adjustment using a log-dose transformation. This corresponds to a maximum likelihood estimated for the logodds in a multinomial probability model.

Results

All extracts were 100% lethal to B. glabrata at 500 ppm but at 100 ppm, only leaf extracts of P. aduncum, P. crassinervium, P. cuyabanum, P. diospyrifolium and P. hostmannianum showed 100% lethality during 24 h of exposure, so the LC90 (table 2, figs 1–3) and ovicidal activity (table 3 and fig. 4) of these extracts were determined. Leaf extracts of Pep. macrostachya, P. hoffmanseggianum, P. macedoi and P. solmsianum did not show molluscicidal activity at 100 ppm; but mortality obtained with extracts of P. corcovadensis (stem, leaf and root), P. amplum (leaf), P. callosum (leaf) and P. tuberculatum (stem) reached a maximum of 90% at 100 ppm (table 2). The percentage of dead snails in the control group over 10 days of observation was 3.3% while dead embryos in control groups over 7 days were 1.6%.

Table 2

Molluscicidal activity of Piperaceae extracts in adult B. glabrata.

n = 30 adult snails; Pep., Peperomia.

a n = 10 adult snails.

Fig. 1

Estimated mortality of B. glabrata exposed to (a) P. aduncum leaf extract; (b) P. crassinervium leaf extract; logistic tendency function.

Fig. 2

Estimated mortality of B. glabrata exposed to (a) P. cuyabanum leaf extract; (b) P. diospyrifolium leaf extract; logistic tendency function.

Fig. 3

Estimated mortality of B. glabrata exposed to P. hostmannianum leaf extract; logistic tendency function.

Table 3

Effect of leaf extracts from P. aduncum, P. cuyabanum, P. crassinervium, P. diospyrifolium and P. hostmannianum on B. glabrata embryos.

Fig. 4

Embryos of B. glabrata after exposure at blastula stage to 10 ppm of P. cuyabanum leaf extract. 1, Dead embryo; 2, normal embryo at veliger stage.

Discussion

All 15 extracts from Piperaceae species were active with 100% mortality at 500 ppm. WHO (1983) recommends that a crude preparation of plant material should be active at 100 ppm or less and kill 90% of snails exposed for 24 h. Leaf extracts of P. aduncum, P. crassinervium, P. cuyabanum, P. diospyrifolium and P. hostmannianum were active at concentrations of less than 100 ppm, which make them good candidates for natural molluscicides (WHO, 1965, 1983).

Adult snails showed a similar response to extracts with molluscicidal action. A common feature was low values of LC90 associated with death during 24 h of exposure. At the highest concentrations, death occurred in the first hours of exposure. Release of haemolymph was also frequently observed and occurred in a dose–response manner. It is quite often associated with rupture of external membranes, but haemolymph could also be liberated through the haemal pore (Duncan, Reference Duncan1985). At present, information on the mode of action of molluscicides is scarce. As is true for most insecticides, the action of a molluscicide may conceivably be a multi-component process affecting more than one system. Several such responses indicative of this have been reported in the literature, for example a reduction in heart rate, swelling of tissues and alteration of water balance have been described (WHO, 1983). In our work, active extracts caused death after around 4 h of exposure, differing significantly from the action of the molluscicide Bayluscide WP70® which induces death only after 24 h, even at 100% lethal concentrations. The efficient molluscicide action observed in our study requires further investigation in order to unravel the possible mechanism of action for toxicity against B. glabrata.

Among the five selected Piperaceae extracts, P. crassinervium, P. cuyabanum and P. hostmannianum showed similar activity in adults and embryos. Sensitivity was inversely proportional to developmental stage. Mortality was highest in embryos at blastula stage, followed by gastrula, trocophore and veliger stages. This higher sensitivity could be attributed to intense cell proliferation activity at early stages; previous studies also showed a differential sensitivity according to developmental stages (Kawano et al., Reference Kawano, Chaves and Simões1979; Kawano & Simões, Reference Kawano and Simões1987; Kawano et al., Reference Kawano, Simões and Marques1991; Yamamoto et al., Reference Yamamoto, Kawano, Young, Haraguchi and Hiroki1996).

Piper aduncum was more active in adults than in embryos. A similar profile was observed with crude extracts and steroidal glycoalkaloid fraction of Lycopersicon esculentum, which showed high activity in adults and low effect in embryos (Leyton et al., Reference Leyton, Henderson, Mascara and Kawano2005). Similar results were obtained in B. glabrata, B. alexandrina and Bulinus truncatus in a study of the molluscicidal effect of Phytolacca dodecandra (Lemma et al., Reference Lemma, Goll, Newell, Parkhurst and Skinner1972). Pereira et al. (Reference Pereira, Souza and Mendes1978) evaluated a leaf extract of Euphorbia cotinifolia and observed an effect in B. glabrata embryos with 48 ppm, a concentration about 20 times higher than the 2.4 ppm observed to have an effect on adult specimens.

Piper diospyrifolium did not show molluscicidal activity in embryos at concentrations evaluated in adults. On the other hand, P. amplum was highly effective in embryos (LC90 of 8.8 ppm) despite its low activiy in adults (Teixeira, Reference Teixeira2004).

In a comprehensive screening, the highest proportions of molluscicidal species were detected in Euphorbiaceae, Asteraceae, Leguminosae, Phytolaccaceae, Polygonaceae, Rubiaceae and Rutaceae species (WHO, 1983; Kloos & McCullough, 1987). Jurberg et al. (Reference Jurberg, Vasconcellos and Mendes1989) describe active extracts from two species of Euphorbiaceae. In our study, five out of 13 Piperaceae species fulfilled the practical criterion for activity against B. glabrata. Based on results obtained with Piper extracts, further studies with P. aduncum, P. crassinervium, P. cuyabanum, P. diospyrifolium and P. hostmannianum should be carried out, looking at the isolation of bioactive compounds. At present, molluscicidal activity of P. aduncum and P. diospyrifolium fractions are being assessed. Concomitantly, we are perfoming bioassays with Daphnia similis and Ceridaphnia dubia to evaluate acute and chronic toxicity of bioactive compounds isolated from the selected Piper extracts. Cladoceran species have been used extensively; they have several advantages, such as high sensitivity and short reproductive cycles (Farre & Barcelo, Reference Farre and Barcelo2003). Inclusion of safety testing will ascertain whether toxic effects on non-target organisms are at acceptable levels.

Acknowledgements

This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

References

Alécio, A.C., Bolzani, V.S., Young, M.C.M., Kato, M.J. & Furlan, M. (1998) Antifungal amide from leaves of Piper hispidum. Journal of Natural Products 61, 637–639.CrossRefGoogle ScholarPubMed
Camey, T. & Verdonk, N.H. (1970) The early development of the snail Biomphalaria glabrata (Say, 1818) and the origin of the head organs. Netherlands Journal of Zoology 20, 93–121.CrossRefGoogle Scholar
Chitsulo, L., Engels, D., Montresor, A. & Savioli, L. (2000) The global status of schistosomiasis and its control. Acta Tropica 77, 41–51.CrossRefGoogle ScholarPubMed
Cysne, J.B., Canuto, K.M., Pessoa, O.D., Nunes, E.P. & Silveira, E.R. (2005) Leaf essential oils of four Piper species from the state of Ceará – Northeast of Brazil. Journal of Brazilian Chemical Society 16, 1378–1381.CrossRefGoogle Scholar
Danelutte, A.P., Lago, J.H.G., Young, M.C.M. & Kato, M.J. (2003) Antifungal flavanones and prenylated hydroquinones from Piper crassinervium Kunth. Phytochemistry 64, 555–559.CrossRefGoogle ScholarPubMed
Danelutte, A.P., Constantin, M.B., Delgado, G.E., Braz-Filho, R. & Kato, M.J. (2005) Divergency of secondary metabolism in cell suspension cultures and differentiated plants of Piper cernuum and Piper crassinervium. Journal of Brazilian Chemical Society 16, 1425–1430.CrossRefGoogle Scholar
Duncan, J. (1985) The toxicology of plant molluscicides. Pharmacology & Therapeutics 27, 243–264.CrossRefGoogle ScholarPubMed
Farre, M. & Barcelo, D. (2003) Toxicity testing of wastewater and sewage sludge by biosensors, bioassays and chemical analysis. Trends in Analytical Chemistry 22, 299–310.CrossRefGoogle Scholar
Joly, A.B. (1993) Botânica: introdução à taxonomia vegetal. 11th edn.777 pp. São Paulo, Nacional.Google Scholar
Jurberg, P., Vasconcellos, M.C. & Mendes, N.M. (1989) Plantas empregadas como moluscicidas: Uma visão crítica. Memórias do Instituto Oswaldo Cruz 84 (Suppl. I), 76–83.CrossRefGoogle Scholar
Kawano, T. & Simões, L.C.G. (1987) Morphogenetic effects of caffeine on Biomphalaria glabrata (Pulmonata, Planorbidae). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen 90, 281–302.Google Scholar
Kawano, T., Chaves, W.R. & Simões, L.C.G. (1979) Effects of caffeine on embryonic development of Biomphalaria glabrata. Ciência e Cultura 31, 1265–1273.Google Scholar
Kawano, T., Simões, L.C. & Marques, J. (1991) Biomphalaria glabrata (Say, 1818): Efeitos morfogenéticos do sulfato de nicotina. Revista Brasileira de Biologia 53, 539–547.Google Scholar
Kloos, H. & McCullough, F.S. (1987) Plants with recognized molluscicidal activity. pp. 45–108in Mott, K.E. (Ed.) Plant molluscicides. Chichester, UK, John Wiley & Sons.Google Scholar
Lemma, A., Goll, P., Newell, G.W., Parkhurst, R.M. & Skinner, W.A. (1972) Studies on the molluscicidal properties of endod (Phytolaca dodecandra): I. Increased potency with butanol extraction. The Journal of Parasitology 58, 104–107.CrossRefGoogle Scholar
Leyton, V., Henderson, T.O., Mascara, D. & Kawano, T. (2005) Atividade moluscicida de principios ativos de folhas de Lycopersicon esculentum (Solanales, Solanaceae) em Biomphalaria glabrata (Gastropoda, Planorbidae). Iheringia Serie Zoologia 95, 213–216.CrossRefGoogle Scholar
Luna, J.S., Santos, A.F., Lima, M.R.F., Omena, M.C., Mendonça, F.A.C., Bieber, L.W. & Sant'Ana, A.E.G. (2005) A study of the larvicidal and molluscicidal activities of some medicinal plants from northeast Brazil. Journal of Ethnopharmacology 97, 199–206.CrossRefGoogle Scholar
Mabberley, D.J. (1997) The plant book: a portable dictionary of the vascular plants. 2nd edn.858 pp. Cambridge, Cambridge University Press.Google Scholar
McCullough, F. & Mott, K.E. (1983) The role of molluscicides in schistosomiasis control. Bulletin of the World Health Organization 83, 1–13.Google Scholar
Miranda, J.E., Oliveira, J.E.M., Rocha, K.C.G., Bortoli, S.A., Navickiene, H.M.D., Kato, M.J. & Furlan, M. (2002) Potencial inseticida do extrato de Piper tuberculatum sobre Alabama agillacea (Huebner, 1818) (Lepidoptera: Noctuidae). Revista Brasileira de Oleaginosas e Fibrosas 6, 557–563.Google Scholar
Nair, M.G. & Burke, B.A. (1990) Antimicrobial Piper metabolite and related compounds. Journal of Agriculture and Food Chemistry 38, 1093–1096.CrossRefGoogle Scholar
Navickiene, H.M.D., Alécio, A.C., Kato, M.J., Bolzani, V.S., Young, M.C.M., Cavalheiro, A.J. & Furlan, M. (2000) Antifungal amides from Piper hispidum and Piper tuberculatum. Phytochemistry 6, 621–626.CrossRefGoogle Scholar
Orjala, J., Erdelmeier, C.A.J., Wright, A.D. & Sticher, O. (1993a) Two chromenes and a prenylated benzoic acid derivate from Piper aduncum. Phytochemistry 34, 813–818.CrossRefGoogle Scholar
Orjala, J., Erdelmeier, C.A.J., Wright, A.D., Rali, T. & Sticher, O. (1993b) Five new prenylated p-hydroxybenzoic acid-derivatives with antimicrobial and molluscicidal activity from Piper aduncum leaves. Planta Medica 59, 546–551.CrossRefGoogle ScholarPubMed
Pandey, J.K. & Singh, D. (2009) Molluscicidal activity of Piper cubeba Linn., Piper longum Linn. and Tribulus terrestris Linn. and their combinations against snail Indoplanorbis exustus Desh. Indian Journal of Experimental Biology 47, 643–648.Google ScholarPubMed
Parmar, V.S., Jain, S.C., Bisht, K.S., Jain, R., Taneja, P., Jha, A., Tyagi, O.D., Prasad, A.K., Wengel, J., Olsen, C.E. & Boll, P.M. (1997) Phytochemistry of the genus Piper. Phytochemistry 46, 597–673.CrossRefGoogle Scholar
Pereira, J.P., Souza, C.P. & Mendes, N.M. (1978) Propriedades moluscicidas da Euphorbia cotinifolia L. Revista Brasileira de Pesquisas Medicas e Biológicas 11, 345–351.Google ScholarPubMed
Rey, L. (2008) Parasitologia. 3rd edn.930 pp. Rio de Janeiro, Guanabara Koogan S.A.Google Scholar
Rouquayrol, M.Z., Fonteles, M.C., Alencar, J.E., Matos, J.A. & Craveiro, A.A. (1980) Molluscicidal activity of essential oils from Northeastern Brazilian plants. Revista Brasileira de Pesquisas Medicas e Biológicas 13, 135–143.Google Scholar
Silva, R.V., Navickiene, H.M.D., Kato, M.J., Bolzani, V.S., Meda, C.I., Young, M.C. & Furlan, M. (2002) Antifungal amides from Piper arboreum and Piper tuberculatum. Phytochemistry 59, 521–527.CrossRefGoogle Scholar
Sousa, M.P. & Rouquayrol, M.Z. (1974) Atividade moluscicida de plantas do Nordeste brasileiro. Revista Brasileira de Pesquisas Medicas e Biológicas 7, 388–393.Google Scholar
Teixeira, E. (2004) Estudo do efeito moluscicida de extratos de Piperaceae em Biomphalaria glabrata (Say, 1818). Dissertação de mestrado. Coordenadoria dos Institutos de Pesquisa da Secretaria de Estado da Saúde de São Paulo.Google Scholar
Torres-Santos, E.C., Moreira, D.L., Kaplan, M.A.C., Meirelles, M.N. & Rossi-Bergmann, B. (1999) Selective effect of 2′,6′-dihydroxy-4′-methoxychalcone isolated from Piper aduncum on Leishmania amazonensis. Antimicrobial Agents and Chemotherapy 5, 1234–1241.CrossRefGoogle Scholar
WHO (1965) Molluscicide screening and evaluation. Bulletin of the World Health Organization 33, 567–581. Geneva, WHO.Google Scholar
WHO (1973) Schistosomiasis control. pp. 1–47. Geneva, WHO.Google Scholar
WHO (1983) Report of the scientific working group on plant molluscicides, vol. 12, pp. 1–11. Geneva, WHO.Google Scholar
WHO (1984) Report of informal consultation on research on the biological control of snail intermediated hosts. pp. 1–41. Geneva, WHO.Google Scholar
WHO (1993) The control of Schistosomiasis: second report of the WHO Expert Committee. 86 pp. Geneva, WHO.Google Scholar
Yamaguchi, L.F., Lago, H.J.G., Tanizaki, T.M., Masuo, P. & Kato, M.J. (2006) Antioxidant activity of prenylated hydroquinone and benzoic derivates from Piper crassinervium Kunt. Phytochemistry 67, 1838–1843.CrossRefGoogle Scholar
Yamamoto, M.M., Kawano, T., Young, M.C.M., Haraguchi, M. & Hiroki, K. (1996) Molluscicidal activity of three Brazilian plant species. Fitoterapia 57, 59–62.Google Scholar
Figure 0

Table 1Piperaceae species screened for molluscicidal activity in B. glabrata.

Figure 1

Table 2Molluscicidal activity of Piperaceae extracts in adult B. glabrata.

Figure 2

Fig. 1Estimated mortality of B. glabrata exposed to (a) P. aduncum leaf extract; (b) P. crassinervium leaf extract; logistic tendency function.

Figure 3

Fig. 2Estimated mortality of B. glabrata exposed to (a) P. cuyabanum leaf extract; (b) P. diospyrifolium leaf extract; logistic tendency function.

Figure 4

Fig. 3Estimated mortality of B. glabrata exposed to P. hostmannianum leaf extract; logistic tendency function.

Figure 5

Table 3Effect of leaf extracts from P. aduncum, P. cuyabanum, P. crassinervium, P. diospyrifolium and P. hostmannianum on B. glabrata embryos.

Figure 6

Fig. 4Embryos of B. glabrata after exposure at blastula stage to 10 ppm of P. cuyabanum leaf extract. 1, Dead embryo; 2, normal embryo at veliger stage.