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Recovery of Ceratophrys ornata tadpoles exposed to environmental concentrations of chlorpyrifos: evaluation of biomarkers of exposure

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Abstract

Chlorpyrifos (CPF) is one of the most widely used insecticides worldwide despite the fact that many authors have warned about its effects in non-target biota. The effects of CPF on anurans are well known, but the process of recovery from these effects after exposure is less explored. The aim of this study was to evaluate the duration of sublethal effects induced by environmental concentrations of CPF on Ceratophrys ornata tadpoles after exposure. The experimental design consisted of an exposure phase (96 h) in which tadpoles were individually exposed to three concentrations of CPF (0, 0.01 and 0.02 mg CPF/L) and a post-exposure phase (72 h) in which exposed tadpoles were transferred to CPF-free media. Individuals that survived the exposure phase to CPF showed neither long-term lethal effects nor long-term swimming alterations and altered prey consumption after being transferred to CPF-free media. No morphological abnormalities were observed either. However, at the end of both phases, tadpoles emitted shorter sounds with a higher dominant frequency than the tadpoles in the control group, i.e., the tadpoles did not recover their normal sounds. Thus, for the first time in this species, we have shown that effects on sounds should be prioritized as biomarkers of exposure, as they not only provide longer detection times after cessation of exposure, but also involve non-destructive methods. The following order of priority could be established for the selection of biomarkers that diagnose the health status of individuals and precede irreversible responses such as mortality: alterations in sounds > swimming alterations > prey consumption.

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References

  • Alvarez M, Du Mortier C, Jaureguiberry S, Venturino A (2019) Joint probabilistic analysis of risk for aquatic species and exceedence frequency for the agricultural use of chlorpyrifos in the pampean region, argentina. Environ Toxicol Chem 38(80):1748–1755

    Article  CAS  Google Scholar 

  • Ashauer R, O’Connor I, Hintermeister A, Escher BI (2015) Death dilemma and organism recovery in ecotoxicology. Environ Sci Technol 49(16):10136–10146

    Article  CAS  Google Scholar 

  • Attademo AM, Peltzer PM, Lajmanovich RC, Cabagna-Zenklusen M, Junges CM, Lorenzatti E, Aró C, Grenón P (2015) Biochemical changes in certain enzymes of Lysapsus limellium (Anura: Hylidae) exposed to chlorpyrifos. Ecotoxicol Environ Saf 113:287–294

    Article  CAS  Google Scholar 

  • Bahl MF, Brodeur JC, Salgado Costa C, D’Andrea MF, Sansiñena JA, Marino DJ, Natale GS (2021) Lethal and sublethal effects of the natural and healthy spinosad-based formulation tracer™ on tadpoles of two neotropical species. Environ Sci Pollut Res 28:13524–13535

    Article  CAS  Google Scholar 

  • Bantle JA, Dumont JN, Finch RA, Linder G (1996) Atlas of abnormalities: a guide for the performance of fetax. Oklahoma State University, Stillwater

  • Barreto E, Salgado Costa C, Demetrio P, Lascano C, Venturino A, Natale GS (2020) Sensitivity of Boana pulchella (Anura: Hylidae) tadpoles to environmentally relevant concentrations of chlorpyrifos: Effects at the individual and biochemical level. Environ Toxicol Chem 39(4):834–841

    Article  CAS  Google Scholar 

  • Bernabò I, Sperone E, Tripepi S, Brunelli E (2011) Toxicity of chlorpyrifos to larval Rana dalmatina: acute and chronic effects on survival, development, growth and gill apparatus. Arch Environental Contam Toxicol 61(4):704–718

    Article  Google Scholar 

  • Brent RN, Herricks EE (1998) Postexposure effects of brief cadmium, zinc, and phenol exposures on freshwater organisms. Environ Toxicol Chem: Int J 17(10):2091–2099

    Article  CAS  Google Scholar 

  • Brodeur JC, Damonte MJ, Rojas DE, Cristos D, Vargas C, Poliserpi MB, Andriulo AE (2022) Concentration of current-use pesticides in frogs from the pampa region and correlation of a mixture toxicity index with biological effects. Environ Res 204:112354

    Article  CAS  Google Scholar 

  • Brunelli E, Bernabò 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. Aquat Toxicol 91(2):135–142

    Article  CAS  Google Scholar 

  • CASAFE (2016) Cámara argentina de fitosanitarios. Guía de productos fitosanitarios para la república argentina. Buenos Aires

  • Cowman D, Mazanti L (2000) Ecotoxicology of “new generation” pesticides to amphibians. Ecotoxicology of Amphibians and Reptiles. 233–268

  • Deb N, Das S (2013) Chlorpyrifos toxicity in fish: a review. Curr World Environ 8(1):77

    Article  CAS  Google Scholar 

  • Denoël M, D’Hooghe B, Ficetola GF, 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 

  • Duellman WE, Trueb L (1994) Biology of amphibians. Johns Hopkins University Press, Baltimore

    Book  Google Scholar 

  • El-Merhibi A, Kumar A, Smeaton T (2004) Role of piperonyl butoxide in the toxicity of chlorpyrifos to Ceriodaphnia dubia and Xenopus laevis. Ecotoxicol Environ Saf 57(2):202–212

    Article  CAS  Google Scholar 

  • Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25(1):272–280

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Greulich K, Pflugmacher S (2003) Differences in susceptibility of various life stages of amphibians to pesticide exposure. Aquat Toxicol 65(3):329–336

    Article  CAS  Google Scholar 

  • Islam MA, Amin SN, Rahman MA, Juraimi AS, Uddin MK, Brown CL and Arshad A (2022) Chronic effects of organic pesticides on the aquatic environment and human health: a review. Environ Nanotechnol, Monit Manag 18:100740

  • IUCN (2022) International union for conservation of nature. The IUCN red list of threatened species

  • Jacobson B, Cedeno-Vazquez JR, Espinoza-Avalos J, Gonzalez-Solis D (2019) The effect of diet on growth and metamorphosis of Triprion petasatus (Anura: Hylidae) tadpoles. Herpetological Conservation and Biology 14(2):308–324

    Google Scholar 

  • Kerby JL (2006) Pesticide effects on amphibians: a community ecology perspective. University of California, Davis

    Google Scholar 

  • Koshlukova S, Reed N (2014) Chlorpyrifos. Elsevier

  • Krüger HS, Hanganu‐Opatz IL (2013) Neonatal cholinergic lesion alters the acoustic structure of infant rat vocalization but not the early cognitive development. Dev Psychobiol 55(3):294–308

    Article  Google Scholar 

  • Lajmanovich RC, Attademo AM, Peltzer P, Junges CM (2009) Inhibition and recovery of cholinesterases in Odontophrynus americanus tadpoles exposed to fenitrothion. J Environ Biol 30(5):923–926

    CAS  Google Scholar 

  • Mac Loughlin TM, Peluso L, Marino DJG (2017) Pesticide impact study in the peri-urban horticultural area of Gran La Plata, Argentina. Sci Total Environ 598:572–580

    Article  Google Scholar 

  • McCarthy JF, Shugart LR (1990) Biomarkers of environmental contamination. Lewis Publishers, Boca Raton

    Google Scholar 

  • McClelland SJ, Woodley SK (2022) Developmental exposure to trace concentrations of chlorpyrifos results in nonmonotonic changes in brain shape and behavior in amphibians. Environ Sci Technol 56(13):9379–9386

    Article  CAS  Google Scholar 

  • Nagai T (2016) Ecological effect assessment by species sensitivity distribution for 68 pesticides used in japanese paddy fields. J Pesti Sci 41(1):6–14

    Article  CAS  Google Scholar 

  • Natale GS, Alcalde L, Herrera R, Cajade R, Schaefer EF, Marangoni F, Trudeau VL (2011) Underwater acoustic communication in the macrophagic carnivorous larvae of Ceratophrys ornata (Anura: Ceratophryidae). Acta Zool 92(1):46–53

    Article  Google Scholar 

  • Natale GS, Vera-Candioti J, Ruiz de Arcaute C, Soloneski S, Larramendy ML, Ronco AE (2018) Lethal and sublethal effects of the pirimicarb-based formulation aficida® on Boana pulchella (Duméril and Bibron, 1841) tadpoles (Anura, Hylidae). Ecotoxicol Environ Saf 147:471–479

    Article  CAS  Google Scholar 

  • Newman MC, Unger MA (2003) Fundamentals of ecotoxicology. Florida: CRC/Lewis Press, Boca Raton

  • Nikinmaa M (2014) Bioindicators and biomarkers. Elsevier

  • Nowell LH, Norman JE, Moran PW, Martin JD, Stone WW (2014) Pesticide toxicity index—a tool for assessing potential toxicity of pesticide mixtures to freshwater aquatic organisms. Science of the Total Environment 476:144–157

    Article  Google Scholar 

  • OECD (1996) Guidelines for testing of chemicals: bioconcentration flow-through fish test. Organisation for Economic Co-operation and Development

  • Pérez-Iglesias JM, Natale GS, Soloneski S, Larramendy ML (2018) Are the damaging effects induced by the imazethapyr formulation pivot® h in Boana pulchella (Anura) reversible upon ceasing exposure? Ecotoxicol Environ Saf 148:1–10

    Article  Google Scholar 

  • Quiroga LB, Sanabria EA, Fornés MW, Bustos DA, Tejedo M (2019) Sublethal concentrations of chlorpyrifos induce changes in the thermal sensitivity and tolerance of anuran tadpoles in the toad Rhinella arenarum? Chemosphere. 219:671–677

    Article  CAS  Google Scholar 

  • Reeve E, Ndriantsoa SH, Strauß A, Randrianiaina R-D, Hiobiarilanto TR, Glaw F, Glos J, Vences M (2011) Acoustic underwater signals with a probable function during competitive feeding in a tadpole. Naturwissenschaften. 98(2):135–143

    Article  CAS  Google Scholar 

  • Richards SM, Kendall RJ (2002) Biochemical effects of chlorpyrifos on two developmental stages of Xenopus laevis. Environ Toxicol Chem 21(9):1826–1835

    Article  CAS  Google Scholar 

  • Rimoldi F, Fogel MN, Ronco A, Schneider M (2017) Comparative susceptibility of two neotropical predators, Eriopis connexa and Chrysoperla externa, to acetamiprid and pyriproxyfen: Short and long- term effects after egg exposure. Environ Pollut 231:1042–1050

    Article  CAS  Google Scholar 

  • Rimoldi F, Schneider MI, Ronco AE (2008) Susceptibility of Chrysoperla externa eggs (Neuroptera: Chrisopidae) to conventional and biorational insecticides. Environ Entomol 37(5):1252–1257

    Article  Google Scholar 

  • Rosenbaum EA, Duboscq L, Soleño J, Montagna CM, Ferrari A, Venturino A (2012) Response of biomarkers in amphibian larvae to in situ exposures in a fruit‐producing region in North Patagonia, Argentina. Environ Toxicol Chem 31(10):2311–2317

    Article  CAS  Google Scholar 

  • Ruiz de Arcaute C, Salgado Costa C, Demetrio PM, Natale GS, Ronco AE (2012) Influence of existing site contamination on sensitivity of Rhinella fernandezae (Anura, Bufonidae) tadpoles to lorsban®48e formulation of chlorpyrifos. Ecotoxicology. 21(8):2338–2348

    CAS  Google Scholar 

  • Rutkoski CF, Macagnan N, Folador A, Skovronski VJ, do Amaral AM, Leitemperger J, Costa MD, Hartmann PA, Müller C, Loro VL (2020) Morphological and biochemical traits and mortality in Physalaemus gracilis (Anura: Leptodactylidae) tadpoles exposed to the insecticide chlorpyrifos. Chemosphere. 250:126162

    Article  CAS  Google Scholar 

  • Salgado Costa C, Chuliver, Pereyra M, Alcalde L, Herrera R, Trudeau VL, Natale GS (2014) Underwater sound emission as part of an antipredator mechanism in Ceratophrys cranwelli tadpoles. Acta Zool 95(3):367–374

    Article  Google Scholar 

  • Salgado Costa C, Rimoldi F, Pantucci Saralegui MJ, Rubio Puzzo ML, Trudeau VL, Natale GS (2021) Disruptive effects of chlorpyrifos on predator-prey interactions of Ceratophrys ornata tadpoles: Consequences at the population level using computational modeling. Environ Pollut 285:117344

    Article  CAS  Google Scholar 

  • Salgado Costa C, Ronco AE, Trudeau VL, Marino D, Natale GS (2018) Tadpoles of the horned frog Ceratophrys ornata exhibit high sensitivity to chlorpyrifos for conventional ecotoxicological and novel bioacoustic variables. Environ Pollut 235:938–947

    Article  CAS  Google Scholar 

  • Salgado Costa C, Trudeau VL, Ronco AE, Natale GS (2016) Exploring antipredator mechanisms: New findings in ceratophryid tadpoles. J Herpetol 50(2):233–238

    Article  Google Scholar 

  • Salgado Costa C (2016) Desarrollo de un modelo experimental con larvas de Ceratophrys spp. (Anura: Ceratophryidae) para su aplicación en estudios ecotoxicológicos de plaguicidas: efectos sobre variables convencionales y bioacústicas. Sedici: Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata

  • Sharma A, Kumar V, Shahzad B, Tanveer M, Sidhu GPS, Handa N, Kohli SK, Yadav P, Bali AS, Parihar RD (2019) Worldwide pesticide usage and its impacts on ecosystem. SN Appl Sci 1:1–16

    Article  Google Scholar 

  • Shugart LR, McCarthy JF, Halbrook RS (1992) Biological markers of environmental and ecological contamination: an overview. Risk Anal 12(3):353–360

    Article  CAS  Google Scholar 

  • Sobrero M, Rimoldi F, Ronco A (2007) Effects of the glyphosate active ingredient and a formulation on Lemna gibba l. At different exposure levels and assessment end-points. Bull Environ Contam Toxicol 79(5):537–543

    Article  CAS  Google Scholar 

  • Sotomayor V, Chiriotto TS, Pechen AM, Venturino A (2015) Biochemical biomarkers of sublethal effects in Rhinella arenarum late gastrula exposed to the organophosphate chlorpyrifos. Pestic Biochem Physiol 119:48–53

    Article  CAS  Google Scholar 

  • Trudeau VL, Schueler FW, Navarro-Martin L, Hamilton CK, Bulaeva E, Bennett A, Fletcher W, Taylor L (2013) Efficient induction of spawning of northern leopard frogs (Lithobates pipiens) during and outside the natural breeding season. Reprod Biol Endocrinol 11(1):14

    Article  CAS  Google Scholar 

  • Trudeau VL, Somoza GM, Natale GS, Pauli B, Wignall J, Jackman P, Doe K, Schueler FW (2010) Hormonal induction of spawning in 4 species of frogs by coinjection with a gonadotropin-releasing hormone agonist and a dopamine antagonist. Reprod Biol Endocrinol 8(1):36

    Article  Google Scholar 

  • ur Rahman HU, Asghar W, Nazir W, Sandhu MA, Ahmed A, Khalid N (2021) A comprehensive review on chlorpyrifos toxicity with special reference to endocrine disruption: Evidence of mechanisms, exposures and mitigation strategies. Sci Total Environ 755:142649

    Article  Google Scholar 

  • USEPA (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Washington, DC: U.S. Environmental Protection Agency, Office of Water

  • Walker C, Hopkin S, Sibly R, Peakall D (2006) Principles of ecotoxicology

  • Wołejko E, Łozowicka B, Jabłońska-Trypuć A, Pietruszyńska M, Wydro U (2022) Chlorpyrifos occurrence and toxicological risk assessment: a review. International Journal of Environmental Research and Public Health 19(19):12209

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5 th edition

  • Zippel K, Lacy R, Byers O (2006) Cbsg/waza amphibian ex situ conservation planning workshop final report. USA

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Acknowledgements

This research was funded by PICT 2015–3137 and the projects X865 from National University of La Plata. MJPS acknowledges Consejo Interuniversitario Nacional (CIN) for a scholarship for scientific vocations. The support of the National Council of Scientific and Technical Research (CONICET) is also acknowledged.

Author contributions

FR: Conceptualization, Methodology, Formal Analysis, Writing - Original Draft. CSC: Conceptualization, Methodology, Formal Analysis, Writing - Original Draft. Pantucci MJPS: Conceptualization, Investigation. MFB: Writing- Reviewing and Editing, GSN: Conceptualization, Supervision.

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Author notes

  1. These authors contributed equally: Federico Rimoldi, Carolina Salgado Costa

Authors and Affiliations

  1. Centro de Investigaciones del Medio Ambiente (CIM), Universidad Nacional de La Plata (UNLP)-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Bv. 120 n° 1489 (1900), La Plata, Buenos Aires, Argentina

    Federico Rimoldi, Carolina Salgado Costa, María Florencia Bahl & Guillermo Sebastián Natale

  2. Instituto de Limnología Dr. Raúl A. Ringuelet (ILPLA), CONICET- UNLP, Boulevard 120 y 62 (1900), La Plata, Buenos Aires, Argentina

    Morena Johana Pantucci Saralegui

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  1. Federico Rimoldi
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Correspondence to Guillermo Sebastián Natale.

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Rimoldi, F., Salgado Costa, C., Pantucci Saralegui, M.J. et al. Recovery of Ceratophrys ornata tadpoles exposed to environmental concentrations of chlorpyrifos: evaluation of biomarkers of exposure. Ecotoxicology 32, 638–645 (2023). https://doi.org/10.1007/s10646-023-02670-7

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