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B-esterases and Behavioral Biomarkers in Tadpoles Exposed to Pesticide Pyrethroid-TRISADA®

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Abstract

Objective

The ecotoxic effects of pesticide used for mosquito’s control TRISADA® (TRI) [deltamethrin (D) 1%+tetramethrin (T) 0.33%, and piperonyl butoxide (PB) 0.29%] on amphibian larvae were investigated.

Methods

In the laboratory, Rhinella arenarum tadpoles were exposed to nominal concentrations of 0.0000 (control; CO), 0.0003125% (C1); 0.000625% (C2); 0.00125% (C3); 0.0025% (C4); 0.005% (C5) (v/v) of formulated TRI. Median lethal concentration (LC50) (%) and 95% confidence limits (CL), the no-observedeffect concentration (NOEC), and the lowest-observedeffect concentration (LOEC) were quantified. The possible effects of TRI on B-esterases, evaluated through acetylcholinesterase (AChE) and carboxylesterase (CbE) activities, in addition to swimming performance (distance moved, mean speed, maximum speed, global activity, and resting time or immobility) were measured in tadpoles whose concentrations displayed survival rates higher than 50%.

Results

The 48 h LC50 of TRI was 0.00125% (v/v) [12.5 (D)+4.1 (T)+3.6 (PB); μg L-1] (CL: 0.000811- 0.001926%). The 48 h NOEC and LOEC values were 0.0003125% (v/v) [3.1 (D)+1 (T)+0.9 (PB); μg L-1] and 0.000625% (v/v) [6.2 (D) +2 (T) +1.8 (PB); μg L-1], respectively. At 48 h of exposure to upper sublethal TRI concentration assay (C3), AChE and CbE activities were significantly inhibited (68 and 84%, respectively) with respect to controls. Also, all the sublethal TRI concentrations caused significantly alterations of all swimming endpoints evaluated.

Conclusion

The current study established that pesticide TRI is toxic to R. arenarum tadpoles and had detrimental effects on the B-sterases activities and swimming activity at TRI sublethal concentrations.

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References

  1. Hayes, T. B., Falso, P., Gallipeau, S. & Stice, M. The cause of global amphibian declines: a developmental endocrinologist’s perspective. J. Exp. Biol. 213, 921–933 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Sparling, D. W., Linder, G., Bishop, C. A. & Krest, S. K. in Ecotoxicology of Amphibians and Reptiles, 2nd edn (eds Sparling, D. W., Linder, G., Bishop, C. A. & Krest, S. K.) 1–11 (CRC Press, Taylor & Francis Group, New York, 2010).

  3. Hemingway, J. The role of vector control in stop** the transmission of malaria: threats and opportunities. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 369, doi: 10.1098/ rstb.2013.0431 (2014).

  4. WHO. Fifteenth report of the WHO Expert Committee on Vector Biology and Control, http://apps.who.int/ iris/bitstream/handle/10665/37432/WHO_TRS_818. pdf?sequence=1&isAllowed=y (1992).

    Google Scholar 

  5. Rehman, H. et al. Systematic review on pyrethroid toxicity with special reference to deltamethrin. J. Entomol. Zool. Stud. 2, 60–70 (2014).

    Google Scholar 

  6. Cakir, G., Yavuz, O. & Kocak, O. Effects of piperonyl butoxide and tetramethrin combinations on biological activities of selected synthetic pyrethroid insecticides against different Housefly (Musca domestica L., Diptera: Muscidae) populations. Acta. Vet. Brno. 77, 467–474 (2008).

    Article  CAS  Google Scholar 

  7. Merivee, E. et al. Low doses of the common alpha–cypermethrin insecticide affect behavioural thermoregulation of the non–targeted, beneficial carabid beetle Platynus assimilis (Coleoptera: Carabidae). Ecotoxicol. Environ. Saf. 120, 286–294 (2015).

    Article  CAS  PubMed  Google Scholar 

  8. Berrill, M. et al. Lethal and sublethal impacts of pyrethroid insecticides on amphibian embryos and tadpoles. Environ. Toxicol. Chem. 12, 525–539 (1993).

    Article  CAS  Google Scholar 

  9. Sánchez–Hernández, J. C. in Environmental pollution: new research (eds Plattenberg, R. H.) 1–45 (Nova, New York, 2006).

  10. Freitas, J. S., Felício, A. A., Teresa, F. B. & Alves de Almeida, E. Combined effects of temperature and clomazone (Gamit®) on oxidative stress responses and B–esterase activity of Physalaemus nattereri (Leiuperidae) and Rhinella schneideri (Bufonidae) tadpoles. Chemospher. 185, 548–562 (2017).

    Article  CAS  Google Scholar 

  11. Wheelock, C. E. et al. Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Rev. Environ. Contam. Toxicol. 195, 117–178 (2008).

    CAS  PubMed  Google Scholar 

  12. Peltzer, P. et al. Effect of exposure to contaminated pond sediments on survival, development, and enzyme and blood biomarkers in veined treefrog (Trachycephalus typhonius) tadpoles. Ecotoxicol. Environ. Saf. 98, 142–151 (2013).

    Article  CAS  PubMed  Google Scholar 

  13. Attademo, A. M., Lajmanovich, R. C., Peltzer, P. M. & Junges, C. 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, 1–12 (2016).

    Article  CAS  Google Scholar 

  14. Robles–Mendoza, C. et al. Esterases activity in the axolotl Ambystoma mexicanum exposed to chlorpyrifos and its implication to motor activity. Aquat. Toxicol. 105, 728–734 (2011).

    Article  CAS  PubMed  Google Scholar 

  15. Denoël, M. et al. Effects of a sublethal pesticide exposure on locomotor behavior: a video–tracking analysis in larval amphibians. Chemospher. 90, 945–951 (2013).

    Article  CAS  Google Scholar 

  16. Egea–Serrano, A. & Tejedo, M. Contrasting effects of nitrogenous pollution on fitness and swimming performance of Iberian water frog, Pelophylax perezi (Seoane, 1885), larvae in mesocosms and field enclosures. Aquat. Toxicol. 146, 144–153 (2014).

    Article  CAS  PubMed  Google Scholar 

  17. Junges, C. M. et al. Acute toxicity and etho–toxicity of three insecticides used for mosquitoes control on amphibian tadpoles. Water. Air. Soil. Pollut. 228, 143–153 (2017).

    Article  CAS  Google Scholar 

  18. Hemingway, J. & Ranson, H. Insecticide resistance in insect vectors of human disease. Annu. Rev. Entomol. 45, 371–391 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. Wu, X. M. et al. Identification of carboxylesterase genes associated with pyrethroid resistance in the malaria vector Anopheles sinensis (Diptera: Culicidae). Pest. Manag. Sci. 74, 159–169 (2018).

    Article  CAS  PubMed  Google Scholar 

  20. Salibián, A. Effects of deltametrhin on the south american toad (Bufo arenarum). Bull. Environ. Contam. Toxicol. 48, 616–621 (1992).

    Article  PubMed  Google Scholar 

  21. de Knecht, J. A. & van Herwijnen, R. Environmental risk limits for deltamethrin. https://www.researchgate. net/publication/237125551_Environmental_risk_limits_ for_deltamethrin.pdf (2008).

    Google Scholar 

  22. Aydin–Sinan, H., Güngördü, A. & Ozmen, M. Toxic effects of deltamethrin and ë–cyhalothrin on Xenopus laevis tadpoles. J. Environ. Sci. Health B. 47, 397–402 (2012).

    Article  CAS  PubMed  Google Scholar 

  23. Macagnan, N. et al. Toxicity of cypermethrin and deltamethrin insecticides on embryos and larvae of Physalaemus gracilis (Anura: Leptodactylidae). Environ. Sci. Pollut. Res. Int. 24, 20699–20704 (2017).

    Article  CAS  PubMed  Google Scholar 

  24. Zhang, Z. Y. et al. Acute toxicity to zebrafish of two organophosphates and four pyrethroids and their binary mixtures. Pest. Manag. Sci. 66, 84–89 (2010).

    Article  CAS  PubMed  Google Scholar 

  25. Conney, A. H. et al. Effects of piperonyl butoxide on drug metabolism in rodents and man. Arch. Environ. Occup. Healt. 24, 97–106 (1972).

    Article  CAS  Google Scholar 

  26. Wickham, J. in Piperonyl Butoxide: the insecticide synergist (eds Jones, D. G.) 239–260 (Academic Press, London, 1998).

  27. Sánchez–Bayo, F. Insecticides Mode of Action in Relation to Their Toxicity to Non–Target Organisms. J. Environment. Analytic. Toxicol. S4, doi:10.4172/2161–0525. S4–002 (2012).

  28. Schleier, J. J. & Peterson R. K. D. The Joint Toxicity of Type I, II,and Nonester Pyrethroid Insecticides. J. Econ. Entomol. 105, 85–91 (2012).

    Article  CAS  PubMed  Google Scholar 

  29. Spitzer, N. C. & Borodinsky, L. N. Implications of activity–dependent neurotransmitter—receptor matching. Philos. Trans. R. Soc. Lond., B., Biol. Sci. 363, doi: 10. 1098/rstb.2007.2257 (2008).

  30. Das, B. K. & Mukherjee, S. C. Chronic toxic effects of quinalphos on some biochemical parameters in Labeo rohita (Ham.). Toxicol. Lett. 114, 11–18 (2000).

    Article  CAS  PubMed  Google Scholar 

  31. Velisek, J. et al. Effects of deltamethrin on rainbow trout (Oncorhynchus mykiss). Environ. Toxicol. Pharmacol. 23, 297–301 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Tu, H. T. et al. Combined effects of deltamethrin, tem perature and salinity on oxidative stress biomarkers and acetylcholinesterase activity in the black tiger shrimp (Penaeus monodon). Chemospher. 86, 83–91 (2012).

    Article  CAS  Google Scholar 

  33. Üner, N., Piner, P. & Temiz, Ö. Piperonyl butoxide increases oxidative toxicity of fenthion in the brain of Oreochromis niloticus. J. Biochem. Mol. Toxicol. 28, 84–90 (2014).

    Article  CAS  PubMed  Google Scholar 

  34. Maxwell, D. M. The specificity of carboxylesterase protection against the toxicity of organophosphate compounds. Toxicol. Appl. Pharmacol. 114, 306–312 (1992).

    Article  CAS  PubMed  Google Scholar 

  35. Denton, D. L. Joint acute toxicity of esfenvalerate and diazinon to fathead minnow (Pimephales promelas) larvae. Environ. Toxicol. Chem. 22, 336–341 (2003).

    Article  CAS  PubMed  Google Scholar 

  36. David, M., Marigoudar, S. R., Patil, V. K. & Halappa, R. Behavioral, morphological deformities and biomarkers of oxidative damage as indicators of sublethal cypermethrin intoxication on the tadpoles of D. melanostictus (Schneider, 1799). Pest. Biochem. Physiol. 103, 127–134 (2012).

    Article  CAS  Google Scholar 

  37. Materna, E. J., Rabeni, C. F. & Lapoint, T. W. Effects of the synthetic pyrethroid insecticide, esfenvalerate, on larval leopard frogs (Rana spp.). Environ. Toxicol. Chem. 14, 613–622 (1995).

    CAS  Google Scholar 

  38. Agostini, M. G., Natale, G. S. & Ronco, A. E. Lethal and sublethal effects of cypermethrin to Hypsiboas pulchellus tadpoles. Ecotoxicolog. 19, 1545–1550 (2010).

    Article  CAS  Google Scholar 

  39. Casco, V. et al. Apoptotic cell death in the central nervous system of Bufo arenarum tadpoles induced by cypermethrin. Cell Biol. Toxicol. 22, 199–211 (2006).

    Article  CAS  PubMed  Google Scholar 

  40. Mushigeri, S. & David, M. Fenvalerate induced changes in the Ach and associated AchE activity in different tissues of fish Cirrhinus mrigala (Hamilton) under lethal and sub–lethal exposure period. Environ. Toxicol. Pharmacol. 20, 65–72 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Marigoudar, S. R., Nazeer Ahmed, R. & David, M. Impact of cypermethrin on Behavioural responses in the fresh water teleost, Labeo rohita (Hamilton). World. J. Zool. 4, 19–23 (2009).

    Google Scholar 

  42. Gan, J. et al. Distribution and persistence of pyrethroids in runoff sediments. J. Environ. Qual. 34, 836–841 (2005).

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  46. Kingsley, G. R. The direct biuret method for the determination of serum proteins as applied to photoelectric and visual colorimetry. J. Lab. Clin. Med. 27, 840–845 (1942).

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  48. Bunyan, P. J. & Jennings, D. M. Organophosphorus poisoning; some properties of avian esterase. J. Lab. Clin. Med. 16, 326–331 (1968).

    CAS  Google Scholar 

  49. Hamilton, M. A., Russo, R. C. & Thurston, R. V. Trimmed Spearman–Karber method for estimating median lethal concentrations in toxicity bioassays. Environ. Sci. Tech. 11, 714–719 (1977).

    Article  CAS  Google Scholar 

  50. Ayres, M. Jr., Ayres, D. & Santos, A. BioEstat, Versao 5.0. Sociedade Civil Mamirauá, MCT–CNPq, https:// www.mamiraua.org.br/pt–br/downloads/programas/ bioestat–versao–53/ (2008).

    Google Scholar 

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Authors and Affiliations

  1. Ecotoxicology Laboratory, Faculty of Biochemistry and Biological Sciences, FBCB-UNL, Ciudad Universitaria, Paraje el Pozo s/n (3000), Santa Fe, Argentina

    Rafael C. Lajmanovich, Paola M. Peltzer, Candela S. Martinuzzi, Andrés M. Attademo, Agustín Bassó, Mariana I. Maglianese & Carlina L. Colussi

  2. National Council for Scientific and Technical Research (CONICET), Buenos Aires, Argentina

    Rafael C. Lajmanovich, Paola M. Peltzer, Candela S. Martinuzzi & Andrés M. Attademo

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  1. Rafael C. Lajmanovich
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Correspondence to Rafael C. Lajmanovich.

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Lajmanovich, R.C., Peltzer, P.M., Martinuzzi, C.S. et al. B-esterases and Behavioral Biomarkers in Tadpoles Exposed to Pesticide Pyrethroid-TRISADA®. Toxicol. Environ. Health Sci. 10, 237–244 (2018). https://doi.org/10.1007/s13530-018-0371-3

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