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Acute Toxicity and Etho-toxicity of Three Insecticides Used for Mosquito Control on Amphibian Tadpoles

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Abstract

Among the measures used to manage mosquito populations and prevent human diseases, the application of pesticides is the global strategy mostly employed. To investigate the lethal and sublethal effects of insecticides used to control mosquitoes on amphibians (Rhinella arenarum, Rhinella fernandezae, and Physalaemus albonotatus), tadpoles were exposed to commercial formulations of temephos (Abate®), Bacillus thuringiensis var. israelensis (Introban®), and permethrin (Depe®). Their acute toxicity in terms of median lethal concentration (LC50) and no- (NOEC) and lowest-observed-effect concentrations (LOEC) was evaluated. To assess the sublethal effects on behavioral endpoints, tadpoles were exposed to the NOEC-24-h value of each insecticide. After that, tadpoles were recorded and video-streaming data were processed by Smart® software. Based on LC50, permethrin was the most toxic insecticide, followed by temephos and B. thuringiensis var. israelensis. Also, intraspecific and interspecific susceptibilities of tadpoles to insecticides were observed. Regarding behavior, the exposure of R. arenarum to the three insecticides had a significant effect on all behavioral endpoints. Two of the three swimming parameters evaluated for R. fernandezae were affected by permethrin, and in the end, only one behavioral pattern was altered in P. albonotatus after exposure to temephos. These results showed that tadpoles’ species were affected differently depending on the chemical properties of the pesticide and on a dose-response effect of the insecticides. Overall, our study suggests that further research is needed to quantify the potential damage of pyrethroid insecticides used for mosquito control on non-target aquatic organisms, mainly due to etho-toxic effects.

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References

  • Agnelli, P., Bellucci, V., Bianco, P. M., Jacomini, C., Modonesi, C. M., Panizza, C., & Tamino, G. (2015). Impatto sugli ecosistemi e sugli esseri viventi delle sostanze sintetiche utilizzate nella profilassi antizanzara. In: D. Mazzella (Ed.). Roma: Istituto Superiore per la Protezione e la Ricerca Ambientale Via-Ambiente e Societá.

    Google Scholar 

  • ASIH: American Society of Ichthyologists and Herpetologists. (2004). Guidelines for use of live amphibians and reptiles in field and laboratory research, 2nd edn. Washington, D.C.: Herpetological Animal Care and Use Committee (HACC) of the American Society of Ichthyologists and Herpetologists.

  • ASTM: American Society for Testing and Materials (2007). Standard guide for conducting whole sediment toxicity tests with amphibians, E. 2591-07. In: ASTM book of standards, biological effects and environmental fate; biotechnology, vol. 11.06, pp. 776–791.

  • Attademo, A. M., Peltzer, P. M., Lajmanovich, R. C., Cabagna-Zenklusen, M. C., Junges, C. M., & Basso, A. (2014). 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(1), 635–649.

    Article  CAS  Google Scholar 

  • Biber, P. A., Dueñas, J. R., Almeida, F. L., Gardenal, C. N., & Almirón, W. R. (2006). Laboratory evaluation of susceptibility of natural subpopulations of Aedes aegypti larvae to temephos. Journal of the American Mosquito Control Association, 22(3), 408–411.

    Article  CAS  Google Scholar 

  • Boisvert, M., & Boisvert, J. (2000). Effects of Bacillus thuringiensis var. israelensis on target and nontarget organisms: a review of laboratory and field experiments. Biocontrol Science and Technology, 10(5), 517–561.

    Article  Google Scholar 

  • Bowatte, G., Perera, P., Senevirathne, G., Meegaskumbura, S., & Meegaskumbura, M. (2013). Tadpoles as dengue mosquito (Aedes aegypti) egg predators. Biological Control, 67(3), 469–474.

    Article  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 

  • Caquet, T., Roucaute, M., Le Goff, P., & Lagadic, L. (2011). Effects of repeated field applications of two formulations of Bacillus thuringiensis var. israelensis on non-target saltmarsh invertebrates in Atlantic coastal wetlands. Ecotoxicology and Environmental Safety, 74(5), 1122–1130.

    Article  CAS  Google Scholar 

  • Crivelenti, L. Z., Guilherme, L. C., Morelli, S., & Borin, S. (2010). Toxicidade do inseticida organofosforado Abate® em alevinos de Poecilia reticulata. Journal of the Brazilian Society of Ecotoxicology, 5(2–3), 1–4.

    Google Scholar 

  • Davies, T. G. E., Field, L. M., Usherwood, P. N. R., & Williamson, M. S. (2007). DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life, 59(3), 151–162.

    Article  CAS  Google Scholar 

  • Denoël, M., Bichot, M., Ficetola, G. F., Delcourt, J., Ylieff, M., Kestemont, P., & Poncin, P. (2010). Cumulative effects of road de-icing salt on amphibian behavior. Aquatic Toxicology, 99(2), 275–280.

    Article  Google Scholar 

  • 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(4), 1240–1250.

    Article  Google Scholar 

  • Denoël, M., Libon, S., Kestemont, P., Brasseur, C., Focant, J.-F., & De Pauw, E. (2013). Effects of a sublethal pesticide exposure on locomotor behavior: a video-tracking analysis in larval amphibians. Chemosphere, 90(3), 945–951.

    Article  Google Scholar 

  • Fort, D. J., Propst, T. L., Stover, E. L., Helgen, J. C., Levey, R. B., Gallagher, K., & Burkhart, J. G. (1999). Effects of pond water, sediment, and sediment extracts from Minnesota and Vermont, USA, on early development and metamorphosis of Xenopus. Environmental Toxicology and Chemistry, 18(10), 2305–2315.

    Article  CAS  Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3), 183–190.

    Google Scholar 

  • Hagman, M., & Shine, R. (2007). Effects of invasive cane toads on Australian mosquitoes: does the dark cloud have a silver lining? Biological Invasions, 9(4), 445–452.

    Article  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 Science & Technology, 11, 714–719.

    Article  CAS  Google Scholar 

  • Harischandra, H. K. S. P., Karunaratne, S. H. P. P., & Rajakaruna, R. S. (2011). Effect of mosquito larvicide Abate® on the developmental stages of the Asian common toad, Bufo melanostictus. Ceylon Journal of Science, 40(2), 133–140.

    Google Scholar 

  • Hilbert, J. (2016). Argentina battles major outbreak of dengue as mosquito population swells–the New York Times. New York: New York Times http://www.nytimes.com/2016/02/18/world/americas/argentina-battles-major-outbreak-of-dengue-as-mosquito-population-swells.html?_r=0. Accessed 22 July 2016.

    Google Scholar 

  • IUCN (2015). An analysis of amphibians on the 2015. The IUCN Red List of Threatened Species. Version 2015-4. >. Accessed 11 June 2015.

  • Jager, T. (2012). Bad habits die hard: the NOEC’s persistence reflects poorly on ecotoxicology. Environmental Toxicology and Chemistry, 31(2), 228–229.

    Article  CAS  Google Scholar 

  • Johansson, M., Piha, H., Kylin, H., & Merilä, J. (2006). Toxicity of six pesticides to common frog (Rana temporaria) tadpoles. Environmental Toxicology, 25(12), 3164–3170.

    Article  CAS  Google Scholar 

  • Lagadic, L., Roucaute, M., & Caquet, T. (2014). Bti sprays do not adversely affect non-target aquatic invertebrates in French Atlantic coastal wetlands. Journal of Applied Ecology, 51, 102–113.

    Article  Google Scholar 

  • Lajmanovich, R. C., Peltzer, P. M., Junges, C. M., Attademo, A. M., Sanchez, L. C., & Bassó, A. (2010). Activity levels of B-esterases in the tadpoles of 11 species of frogs in the middle Paraná River floodplain: Implication for ecological risk assessment of soybean crops. Ecotoxicology and Environmental Safety, 73(7), 1517–1524.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lavorato, M., Bernabò, I., Crescente, A., Denoël, M., Tripepi, S., & Brunelli, E. (2013). Endosulfan effects on Rana dalmatina tadpoles: Quantitative developmental and behavioural analysis. Archives of Environmental Contamination and Toxicology, 64(2), 253–262.

    Article  CAS  Google Scholar 

  • Maletz, S., Wollenweber, M., Kubiak, K., Müller, A., Schmitz, S., Maier, D., et al. (2015). Investigation of potential endocrine disrupting effects of mosquito larvicidal Bacillus thuringiensis israelensis (Bti) formulations. Science of the Total Environment Journal, 536, 729–738.

    Article  CAS  Google Scholar 

  • Mandrillon, A., & Saglio, P. (2007). Waterborne amitrole affects the predator–prey relationship between common frog tadpoles (Rana temporaria) and larval spotted salamander (Salamandra salamandra). Environmental Toxicology, 53, 233–240.

    CAS  Google Scholar 

  • McDiarmid, R. W., & Altig, R. (1999). Tadpoles: the biology of anuran larvae. Chicago: University of Chicago Press.

    Google Scholar 

  • Ministerio de Salud de la Nación (2011). Directrices para la prevención y control de Aedes aegypti. Dirección de Enfermedades Transmisibles por Vectores-Cdad. Autónoma de Bs. As., República Argentina.Web: www.msal.gov.ar

  • Miyamoto, M., Saito, S., Fujisawa, T., & Katagi, T. (2015). Bioconcentration and metabolism of trans-tetramethrin in fish. Journal of Pesticide Science, 40(3), 1–8.

    Article  Google Scholar 

  • Moore, L. J., Fuentes, L., Rodgers, J. H., Bowerman, W. W., Yarrow, G. K., Chao, W. Y., & Bridges, W. C. (2012). Relative toxicity of the components of the original formulation of Roundup® to five North American anurans. Ecotoxicology and Environmental Safety, 78, 128–133.

    Article  CAS  Google Scholar 

  • Nkya, T. E., Akhouayri, I., Kisinza, W., & David, J.-P. (2013). Impact of environment on mosquito response to pyrethroid insecticides: facts, evidences and prospects. Insect Biochemistry and Molecular Biology, 43(4), 407–416.

    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 

  • 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(7), 1165–1173.

    Article  CAS  Google Scholar 

  • Preud’homme, V., Milla, S., Gillardin, V., De Pauw, E., Denoël, M., & Kestemont, P. (2015). Effects of low dose endosulfan exposure on brain neurotransmitter levels in the African clawed frog Xenopus laevis. Chemosphere, 120, 357–364.

    Article  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, 28(9), 2004–2008.

    Article  CAS  Google Scholar 

  • Rubbo, M. J., Lanterman, J. L., Falco, R. C., & Daniels, T. J. (2011). The influence of amphibians on mosquitoes in seasonal pools: Can wetlands protection help to minimize disease risk? Wetlands, 31(4), 799–804.

    Article  Google Scholar 

  • Sarwar, M. (2015). Controlling dengue spreading Aedes mosquitoes (Diptera: Culicidae) using ecological services by frogs, toads and tadpoles (Anura) as predators. American Journal of Clinical Neurology and Neurosurgery, 1(1), 18–24.

    Google Scholar 

  • Schleier, J. J., & Peterson, R. K. D. (2010). Toxicity and risk of permethrin and naled to non-target insects after adult mosquito management. Ecotoxicology, 19(6), 1140–1146.

    Article  CAS  Google Scholar 

  • Scott, G. R., & Sloman, K. A. (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 

  • Seccacini, E., Lucia, A., Zerba, E., Licastro, S., & Masuh, H. (2008). Aedes aegypti resistance to temephos in Argentina. Journal of the American Mosquito Control Association, 24(4), 608–609.

    Article  Google Scholar 

  • Selvi, M., Sarikaya, R., & Erkoç, F. (2004). Acute behavioral changes in the guppy (Poecilia reticulata) exposed to temephos. Gazi University Journal of Science, 17(4), 15–19.

    Google Scholar 

  • Shao, Q. (2000). Estimation for hazardous concentrations based on NOEC toxicity data: an alternative approach. Environmetrics, 11(5), 583–595.

    Article  CAS  Google Scholar 

  • Smetanová, S., Bláha, L., Liess, M., Schäfer, R. B., & Beketov, M. A. (2014). Do predictions from species sensitivity distributions match with field data? Environmental Pollution, 189, 126–133.

    Article  Google Scholar 

  • Sparling, D. W., Lowe, T. P., & Pinkney, A. E. (1997). Toxicity of abate to green frog tadpoles. Bulletin of Environmental Contamination and Toxicology, 58, 475–481.

    Article  CAS  Google Scholar 

  • Tarragona, S., Monteverde, M., Marchioni, S., Caporale, J., Pereiro, A., & Palacios, J. (2012). Dengue in Argentina: an economic analysis of the impact of the 2009 epidemic. Salud Colectiva (English Edition), 8(2), 151–162.

    Article  Google Scholar 

  • USEPA (1975). Methods for acute toxicity tests with fish, macroinvertebrates, and amphibians. USEPA660/3-75-009, p. 62.

  • USEPA (2002). Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Fifth edition, USEPA 821-R-02-012.

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

    CAS  Google Scholar 

  • Wagner, C., & Løkke, H. (1991). Estimation of ecotoxicological protection levels from NOEC toxicity data. Water Research, 25(10), 1237–1242.

    Article  CAS  Google Scholar 

  • Wheeler, M. W., Park, R. M., & Bailer, A. J. (2006). Comparing median lethal concentration values using confidence interval overlap or ratio tests. Environmental Toxicology and Chemistry, 25(5), 1441–1444.

    Article  CAS  Google Scholar 

  • WHO. (2008). WHO specifications and evaluations for public health pesticides—temephos. Geneva: World Health Organization Accessed 20 October 2015.

    Google Scholar 

  • WHO (2009). Bacillus thuringiensis israelensis (Bti) in drinking-water. WHO Guidelines for drinking-water quality. Switzerland. http://www.who.int/water_sanitation_health/gdwqrevision/RevisedFourthEditionBacillusthuringiensis_Bti_July272009_2.pdf. Accessed 15 Oct 2015.

  • Winandy, L., & Denoël, M. (2011). The use of visual and automatized behavioral markers to assess methodologies: a study case on PIT-tagging in the Alpine newt. Behavior Research Methods, 43(2), 568–576.

    Article  Google Scholar 

  • Zambrini, D. A. B. (2011). Neglected lessons from the 2009 dengue epidemic in Argentina. Revista de Saúde Pública, 45(2), 428–431.

    Article  Google Scholar 

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Acknowledgements

This study was supported in part by the National Agency for Promotion of Science and Technology (ANPCyT-FONCyT PICT) and the Course of Action for Research and Science Promotion (CAI + D-UNL).

Author Contributions

Celina M. Junges, Mariana I. Maglianese, and Rafael C. Lajmanovich conceived and designed the experiments. Rafael C. Lajmanovich and Andrés M. Attademo collected the amphibian species. Celina M. Junges and Paola M. Peltzer contributed writing and revising the paper. All authors reviewed the manuscript and approved the final version.

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Correspondence to C. M. Junges.

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All procedures performed in this study involving animals were in accordance with the ASIH (2004) criteria and ethical standards of the animal ethics committee of the Facultad de Bioquímica y Ciencias Biológicas, FBCB Res. CD no. 388/06.

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Junges, C.M., Maglianese, M.I., Lajmanovich, R.C. et al. Acute Toxicity and Etho-toxicity of Three Insecticides Used for Mosquito Control on Amphibian Tadpoles. Water Air Soil Pollut 228, 143 (2017). https://doi.org/10.1007/s11270-017-3324-6

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