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Acute Toxicity of Metaldehyde in the Invasive Rice Snail Pomacea canaliculata and Sublethal Effects on Tadpoles of a Non-target Species (Rhinella arenarum)

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Abstract

We investigated the effects of exposure to molluscicidal metaldehyde (MET) on golden apple snail (GAS) Pomacea canaliculata and Rhinella arenarum tadpoles by assessing mortality and/or other effects via: acute toxicity assays; B-esterase activities (acetilcholinesterase (AChE) and carboxilesterase (CbE)) and oxidative responses (glutathione-S-transferase (GST) and catalase (CAT)). The effect of sublethal concentrations of MET was also analysed by assessing biochemical changes and swimming parameters in tadpoles. The LC50 value in P. canaliculata was as 0.50 mg L−1 and in R. arenarun tadpoles, 229.7 mg L−1 at 48 h. The intestine of MET-exposed P. canaliculata exhibited a significant reduction in CbE and CAT activities, but not in AChE activity; hepatopancreas of GAS showed a decreased GST activity decreased with respect to control individuals. In addition, a significant reduction of CbE activities was detected in R. arenarum tadpoles exposed to MET, and AChE presented lower values than the control but without statistical differences. Antioxidant enzymes (GST and CAT) were significantly reduced in tadpoles exposed to MET compared with the control group. In addition, MET had a significant effect on the swimming behaviour of R. arenarum. Finally, since amphibian tadpoles and P. canaliculata often co-occur, other native amphibian species should be studied to elucidate the ecological risk of MET to amphibian populations.

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References

  • Aebi, H. (1984). Catalase in vitro. Metods Enzymology, 105, 121–126.

    Article  CAS  Google Scholar 

  • Aldridge, W. N. (1953). Serum esterases. (1) Two types of esterases (A and B) hydrolyzing p- nitrophenyl acetate, propionate and butyrate, and a method for their determination. Biochemistry Journal, 52, 110–117.

    Article  Google Scholar 

  • Almeida, J. R., Oliveira, C., Gravato, C., & Guilhermino, L. (2010). Linking behavioural alterations with biomarkers responses in the European sea bass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion. Ecotoxicology, 19, 1369–1381.

    Article  CAS  Google Scholar 

  • APHA. (1989). Standard Methods for the Examination of Water and Wastewater (17th ed., p. 1,268). Washington D.C: American Public Health Association.

    Google Scholar 

  • ASIH, HL, & SSAR. (2011). Guidelines for use of live amphibians and reptiles in field and laboratory research, Herpetological Animal Care and Use Committee (HACC) of the American Society of Ichthyologists and Herpetologists. Washington, DC, USA

  • Attademo, A. M., Peltzer, P. M., Lajmanovich, R. C., Cabagna-Zenklusen, M., Junges, C. M., Lorenzatti, E., Aró, C., & Grenón, P. (2015). Biochemical changes in certain enzymes of Lysapsus limellium (Anura: Hylidae) exposed to chlorpyrifos. Ecotoxicology and Environmental Safety, 113, 287–294.

    Article  CAS  Google Scholar 

  • Attademo, A. M., Peltzer, P. M., Lajmanovich, R. C., Cabagna-Zenklusen, M. C., Junges, C. M., & Basso, A. (2014a). Biological endpoints, enzyme activities, and blood cell parameters in two anuran tadpole species in rice agroecosystems of mid-eastern Argentina. Environmental Monitoring and Assessment, 186, 635–649.

    Article  CAS  Google Scholar 

  • Attademo, A. M., Peltzer, P. M., Lajmanovich, R. C., Basso, A., & Junges, C. (2014b). Tissue-specific variations of esterase activities in the tadpoles and adults of Pseudis paradoxa (Anura: Hylidae). Water Air Soil and Pollution, 225, 1903.

    Article  Google Scholar 

  • Bambaradeniya, C. N. B., Edirisinghe, J. P., De Silva, D. N., Gunatilleke, C. V. S., Ranawana, K. B., & Wijekoon, S. (2004). Biodiversity associated with an irrigated rice agroecosystem in Sri Lanka. Biodiversity and Conservation, 13, 1715–1753.

    Article  Google Scholar 

  • Basack, S. B., Oneto, M. L., Fuchs, J. S., Wood, E. J., & Kestenm, E. M. (1998). Esterases of Corbicula fluminea as biomarkers of exposure to organophosphorous pesticides. Bulletin of Environmental Contamination and Toxicology, 61, 569–576.

    Article  CAS  Google Scholar 

  • Berrill, M., Bertrama, S., Wilson, A., Louis, S., Brighaman, D., & Stromberg, C. (1993). Lethal and sublethal impacts of pyrethroid insecticides on amphibian embryos and tadpoles. Environmental Toxicology and Chemistry, 12, 525–539.

    Article  CAS  Google Scholar 

  • Boland, B. B., Meerhoff, M., Fosalba, C., Mazzeo, N., Barnes, M. A., & Burks, R. L. (2008). Juvenile snails, adult appetites: contrasting resource consumption between two species of applesnails (Pomacea). Journal of Molluscan Studies, 74(1), 47–54.

    Article  Google Scholar 

  • Booze, T. F., & Oehme, F. W. (1985). Metaldehyde toxicity—a review. Vet. Hum. Tox., 27(I), 11–19.

    CAS  Google Scholar 

  • Borlogan, I. G., Coloso, R. M., & Blum, R. A. (1996). Use of metaldehyde as molluscicide in milkfish ponds. In I. F. Henderson (Ed.), Slug & snail pests in agriculture (pp. 205–212). BCPC Monograph no. 66.

    Google Scholar 

  • Brunelli, E., Bernabó, I., Berg, C., Lundstedt-Enkel, K., Bonacci, A., & Tripepi, S. (2009). Environmentally relevant concentrations of endosulfan impair development, metamorphosis and behaviour in Bufo bufo tadpoles. Aquatic Toxicology, 91, 135–142.

    Article  CAS  Google Scholar 

  • Bunyan, P. J., & Jennings, D. M. (1968). Organophosphorus poisoning; some properties of avian esterase. Journal of Agricultural and Food Chemistry, 16, 326–331.

    Article  CAS  Google Scholar 

  • Cagauan, A. G., & Joshi, R. C. (2002). Golden Apple Snail Pomacea spp. in the Philippines. 7th ICMAM Special Working Group on Golden Apple Snail, 22 October, 2002

  • Calabrese, E. J. (2004). Hormesis: from marginalization to mainstream a case for hormesis as the default dose-response model in risk assessment. Toxicology and Applied Pharmacology, 197, 125–136.

    Article  CAS  Google Scholar 

  • Carlsson, N., Kestrup, A., Martensson, M., & Nyström, P. (2004). Lethal and non-lethal effects of multiple indigenous predators on the invasive golden apple snail (Pomacea canaliculata). Freshwater Biology, 49(10), 1269–1279.

    Article  Google Scholar 

  • Cheng, E. Y. (1989). Control strategy for the introduced snail, Pomacea lineate, in rice paddy. In I. F. Henderson (Ed.), Slugs and snails in world agriculture (pp. 69–75). BCPC Monograph no. 41.

    Google Scholar 

  • Cnubben, N. H. P., Rietjens, I. M., Wortelboer, H., van Zanden, J., & van Bladeren, P. J. (2001). The interplay of glutathione-related processes in antioxidant defense. Environomental Toxicology and Pharmacology, 10, 141–152.

    Article  CAS  Google Scholar 

  • Cserháti, T., Forgacs, E., & Oros, G. (2002). Biological activity and environmental impact of anionic surfactants. Environment International, 28(5), 337–348.

    Article  Google Scholar 

  • Cohn, J., & MacPhail, R. C. (1996). Ethological and experimental approaches to behavior analysis: implications for ecotoxicology. Environmental Health Perspectives, 104, 305.

    Article  Google Scholar 

  • Cowie, R. H. (2002). Apple snails (Ampullariidae) as agricultural pests: their biology, impacts and management. Molluscs as crop pests, , 145–192.

  • Denoël, M., D’Hooghe, B., Ficetola, G. F., Brasseur, C., De Pauw, E., Thomé, J. P., & Kestemont, P. (2012). Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles. Ecotoxicology, 21, 1240–1250.

    Article  Google Scholar 

  • Drobne, D., Blazic, M., Van Gestel, C. A. M., Leser, V., Zidar, P., Jemec, A., & Trebse, P. (2008). Toxicity of imidacloprid to the terrestrial isopod Porcellio scaber (Isopoda, Crustacea). Chemosphere, 71, 1326–1334.

    Article  CAS  Google Scholar 

  • El-Wakil, H. B., & Radwan, M. A. (1991). Biochemical studies on the terrestrial snail, Eobania vemiculala (Muller) treated with some pesticides. Journal of Environmental Science and Health, B26(5-6), 479–489.

    Article  CAS  Google Scholar 

  • Ellman, G. L., Courtney, K. D., Andreas, V., Jr., & Featherstone, R. M. (1961). A new and rapid calorimetric determination of cholinesterase activity. Biochemistry Pharmacology, 7, 88–95.

    Article  CAS  Google Scholar 

  • Ferrari, A., Lascano, C., Pechen de D’Angelo, A. M., & Venturino, A. (2011). Effects of azinphos methyl and carbaryl on Rhinella arenarum tadpoles esterases and antioxidant enzymes. Comparative Biochemistry and Physiology, 153, 34–39.

    Google Scholar 

  • Geiger, F., Bengtssonb, J., Berendse, F., Weisser, W. W., Emmersond, M., & Morales, M. B. (2010). Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic and Applied Ecology, 11, 97–105.

    Article  CAS  Google Scholar 

  • Gomori, G. (1953). Human esterases. Journal of Laboratory and Clinical Medicine, 142, 445–453.

    Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and tadpoles with notes on identification. Herpetologica, 16, 183–190.

    Google Scholar 

  • Habdous, M., Visvikis, S., & Visvikis, S. (2002). Rapid spectrophotometric method for serum glutathione S-transferases activity. Clinical and Chemistry Acta, 326, 131–142.

    Article  CAS  Google Scholar 

  • Habig, W. H., Pabst, M. J., & Jakoby, W. (1974). Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249, 7130–7139.

    CAS  Google Scholar 

  • Hamilton, M. A., Russo, R. C., & Thurston, R. V. (1977). Trimmed Spearman-Karber method for estimating median lethal concentrations in toxicity bioassays. Environmental and Science Technology, 11, 714–719.

    Article  CAS  Google Scholar 

  • Halliwell, B., & Gutteridge, J. M. C. (2007). Free radicals in biology and medicine. New York, USA: Oxford University Press.

    Google Scholar 

  • Hayes, K. A., Joshi, R. C., Thiengo, S. C., & Cowie, R. H. (2008). Out of South America: multiple origins of non-native apple snails in Asia. Diversity and Distributions, 14(4), 701–712.

    Article  Google Scholar 

  • Henderson, I., & Triebskorn, R. (2002). Chemical control of terrestrial gastropods. In G. M. Barker (Ed.), Molluscs as crop pests (pp. 1–31). Wallingford, .K: CABI Publishing.

    Chapter  Google Scholar 

  • Joshi, R., Meepagala, K., Sturtz, G., Cagauan, A., Mendoza, C., Dayan, F., & Duke, S. (2005). Molluscicidal activity of vulgarone B from Artemisia douglasiana (Besser) against the invasive, alien, mollusk pest, Pomacea canaliculata (Lamarck). International Journal of Pest Management, 51(3), 175–180.

    Article  CAS  Google Scholar 

  • Joshi, R. C., De La Cruz, M. S., & Duca, A. V. (2002). Ovicidal effect of a molluscicide on golden apple snail in the Philippines. International Rice Research Notes, 27, 26–27.

    Google Scholar 

  • Kingbley, G. R. (1942). The direct Biuret method for the determination of serum proteins as applied to photoelectric and visual colorimetry. Journal of Laboratory and Clinical Medicine, 27, 840–845.

    Google Scholar 

  • Kristoff, G., Barrionuevo, D. C., Cacciatore, L., Verrengia Guerrero, N. R., & Cochón, A. C. (2012). In vivo studies on inhibition and recovery of B-esterase activities in Biomphalaria glabrata exposed to azinphos-methyl: Analysis of enzyme, substrate and tissue dependence. Aquatic Toxicology, 112–113, 19–26.

    Article  Google Scholar 

  • Lach, L., Britton, D. K., Rundell, R. J., & Cowie, R. H. (2000). Food preference and reproductive plasticity in an invasive freshwater snail. Biological Invasions, 2, 279–288.

    Article  Google Scholar 

  • Lajmanovich, R. C., Junges, C. M., Cabagna-Zenklusen, M. C., Attademo, A. M., Peltzer, P. M., Maglianese, M., Márquez, V. E., & Beccaria, A. J. (2015). Toxicity of Bacillus thuringiensis var. israelensis in aqueous suspension on the South American common frog Leptodactylus latrans (Anura: Leptodactylidae) tadpoles. Enviromental Research, 136, 205–212.

    Article  CAS  Google Scholar 

  • Lajmanovich, R. C., Junges, C. M., Attademo, A. M., Peltzer, P. M., Cabagna Zenklusen, M., & Bassó, A. (2013). Individual and mixture toxicity of commercial formulations containing glyphosate, metsulfuron-methyl, bispyribac-sodium, and picloram on Rhinella arenarum tadpoles. Water, Air, & Soil Pollution, 224, 1404.

    Article  Google Scholar 

  • Lazartigues, A., Banas, D., Feidt, C., Brun-Bellut, J., & Thomas, M. (2012). Pesticide pressure and fish farming in barrage pond in Northeastern France. Part I: site characterization and water quality. Environmental Sciences and Pollution Research, 19(7), 2802–2812.

    Article  CAS  Google Scholar 

  • Lee, R. F. (1988). Glutathione S-transferase in marine invertebrates from Langesundfjord. Marine Ecology, 46, 33–36.

    Article  CAS  Google Scholar 

  • Mandrillon, A., & Saglio, P. (2007). Herbicide exposure affects the chemical recognition of a non native predator in common toad tadpoles (Bufo bufo). Chemoecology, 17, 31–36.

    Article  CAS  Google Scholar 

  • Mann, R., Harding, J. M., & Southworth, M. J. (2009). Reconstructing pre-colonial oyster demographics in the Chesapeake Bay, USA. Estuarine, Coastal and Shelf Science, 85, 217–222.

    Article  Google Scholar 

  • Martínez-Álvarez, R. M., Morales, A. E., & Sanz, A. (2005). Antioxidant defenses in fish: biotic and abiotic factors. Reviews Fish Biology Fisheries, 15, 75–88.

    Article  Google Scholar 

  • Maxwell, D. M., & Brecht, K. M. (2001). Carboxylesterase: specific and spontaneous reactivation of an endogenous scavenger for organophosphorus compounds. Journal of Applied Toxicology, 21, 103–107.

    Article  Google Scholar 

  • Mills, J. D., Bailey, S. E. R., & McCrohan, C. R. (1989). Effects of molluscicides on feeding behavior and neuronal activity. In: I. Henderson (Ed.), British Crop Protection Council Monograph, no. 41. Slugs and snails in world agriculture; Symposium, Surrey, England, UK, April 10–12 (pp. 77–84). Thornton Heath, England, UK.

  • Ossana, N. A., Castañé, P. M., & Salibián, A. (2013). Use of Lithobates catesbeianus tadpoles in a multiple biomarker approach for the assessment of water quality of the Reconquista river (Argentina). Archives of Environmental Contamination and Toxicology, 65, 486–497.

    Article  CAS  Google Scholar 

  • Peltzer, P. M., Junges, C. M., Attademo, A. M., Bassó, A., Grenón, P., & Lajmanovich, R. C. (2013). Cholinesterase activities and behavioral changes in Hypsiboas pulchellus (Anura: Hylidae) tadpoles exposed to glufosinate ammonium herbicide. Ecotoxicology, 22, 1165–1173.

    Article  CAS  Google Scholar 

  • Peltzer, P. M., Lajmanovich, R. C., Attademo, A. M., & Beltzer, A. H. (2006). Diversity of anurans across agricultural ponds in Argentina. Biodiversity and Conservation, 15, 3499–3513.

    Article  Google Scholar 

  • Putchakayala, S. M., & Ram, J. L. (2000). Toxic and excitatory effects of the molluscicide metaldehyde on the biofouling bivalve Dreissena polymorpha Pallas. Pest Management Science, 56, 39–42.

    Article  CAS  Google Scholar 

  • Relyea, R. A., & Jones, D. K. (2009). The toxicity of Roundup Original Max to 13 species of larval amphibians. Environmental Toxicology and Chemistry. doi:10.1897/09-021.1.

    Google Scholar 

  • Robles-Mendoza, C., Zúñiga-Lagunes, S. R., Ponce de León-Hill, C. A., Hernández-Soto, J., & Vanegas-Pérez, C. (2011). Esterases activity in the axolotl Ambystoma mexicanum exposed to chlorpyrifos and its implication to motor activity. Aquatic Toxicology, 105, 728–734.

    Article  CAS  Google Scholar 

  • Sánchez-Bayo, F. (2012). Insecticides mode of action in relation to their toxicity to non-target organisms. Journal of Environmental and Analytical Toxicology, S4, 002.

    Google Scholar 

  • Schnorbach, H. J., Rauen, H. W., Bieri, M., Joshi, R., & Sebastian, L. (2006). Chemical control of the golden apple snail, Pomacea canaliculata. In R. C. Joshi & L. S. Sebastian (Eds.), Global advances in ecology and management of golden apple snails (pp. 419–438). Nueva Ecija: Philippine Rice Research Institute.

    Google Scholar 

  • Scott, G., & Sloman, K. (2004). The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquatic Toxicology, 68, 369–392.

    Article  CAS  Google Scholar 

  • Solé, M., & Sanchez-Hernandez, J. C. (2015). An in vitro screening with emerging contaminants reveals inhibition of carboxylesterase activity in aquatic organisms. Aquatic Toxicology, 169, 215–222.

    Article  Google Scholar 

  • Sparling, D. W., & Fellers, G. M. (2009). Toxicity of two insecticides to California, USA, anurans and its relevance to declining amphibian populations. Environmental and Toxicology Chemistry, 28, 1696–1703.

    Article  CAS  Google Scholar 

  • Stark, J. D., Vargas, R., & Banks, J. E. (2007). Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. Journal of Economic Entomology, 100, 1027–1032.

    Article  Google Scholar 

  • Stenersen, J. (2004). Chemical pesticides: mode of action and toxicology. Boca Raton, FL: CRC Press LLC.

    Book  Google Scholar 

  • Tiwari, F., Singh, K., & Singh, D. K. (2008). Enzyme inhibition by different bait formulations in the nervous system of the snail Lymnaea acuminate. In B. D. Joshi, P. C. Joshi, & N. Joshi (Eds.), Environmental Pollution and Toxicology (pp. 115–128). New Dehli, India

  • Triebskorn, R. (1991). The impact of molluscicides on enzyme activities in the hepatopancreas of Deroceras reticulatum (Miiller). Malacologia, 33, 255–272.

    Google Scholar 

  • Triebskorn, R., Christensen, K., & Heim, I. (1998). Effects of orally and dermally applied metaldehyde on mucus cells of slugs (Deroceras reticulatum) depending on temperature and duration of exposure. Journal of Molluscan Studies, 64, 467–487.

    Article  Google Scholar 

  • US EPA. (1992). EPA probit analysis program, version 1.5 (Ecological Monitoring Research). Cincinnati, OH: Division Environmental Monitoring Systems Laboratory.

    Google Scholar 

  • Vaira, M., Akmentins, M., Attademo, A., Baldo, D., Barrasso, D., et al. (2012). Categorización del estado de conservación de los Anfibios de la República Argentina. Cuadernos de Herpetologia, 26, 131–159.

    Google Scholar 

  • Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64, 178–189.

    Article  CAS  Google Scholar 

  • Van Buskirk, J., & McCollum, S. A. (2000). Influence of tail shape on tadpole swimming performance. Journal of Experimental Biology, 203, 2149–2158.

    Google Scholar 

  • Venturino, A., & Pechen de D’Angelo, A. M. (2005). Biochemical targets of xenobiotics: biomarkers in amphibian ecotoxicology. Applied Herpetology, 2, 335–353.

    Article  Google Scholar 

  • Weis, J. S., & Candelmo, A. (2012). Pollutants and fish predator/prey behaviour: a review of laboratory and field approaches. Current Zoology, 58, 9–20.

    Article  Google Scholar 

  • Wheelock, C. E., Phillips, B. M., Anderson, B. S., Miller, J. L., Miller, M. J., & Hammock, B. D. (2008). Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Reviews of Environmental Contamination and Toxicology, 195, 117–178.

    Article  CAS  Google Scholar 

  • Wu, J. Y., Meng, P. J., Liu, M. Y., Chiu, Y. W., & Liu, L. L. (2010). A high incidence of imposex in Pomacea apple snails in Taiwan: a decade after triphenyltin was banned. Zoological Studies, 49, 85–93.

    Google Scholar 

  • Zhang, J., Li, D., Ge, P., Guo, Y., Zhu, K. Y., Ma, E., & Zhang, J. (2014). Molecular and functional characterization of cDNAs putatively encoding carboxylesterases from the migratory locust, Locusta migratoria. PlosOne, 9, e94809.

    Article  Google Scholar 

  • Zar, J. H. (1999). Biostatistical analysis (4th ed.). New Jersey: Prentice Hall.

    Google Scholar 

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Acknowledgements

This study was supported in part by Secretaría de Ciencia y Tecnología (SECYT), Curso de Acción para la Investigación y Desarrollo (Programa de I+D Orientado a Problemas Sociales y Productivos, UNL) and Agencia Santafesina de Ciencia, Tecnología e Innovación (ASaCTeI).

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Correspondence to Andrés Maximiliano Attademo.

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Animals used in this research have been treated according to ASIH et al. (2011) criteria and with approval from the animal ethics committee of the Faculty of Biochemistry and Biological Sciences. http://www.fbcb.unl.edu.ar/pages/investigacion/comite-deetica.php.

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Attademo, A.M., Lajmanovich, R.C., Peltzer, P.M. et al. Acute Toxicity of Metaldehyde in the Invasive Rice Snail Pomacea canaliculata and Sublethal Effects on Tadpoles of a Non-target Species (Rhinella arenarum). Water Air Soil Pollut 227, 400 (2016). https://doi.org/10.1007/s11270-016-3083-9

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