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Ecotoxicological assessment of Fluazuron: effects on Folsomia candida and Eisenia andrei

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Abstract

The cattle production in Brazil has increased considerably in the last years, mainly due to the control of parasite infestation of the animals, which cause loss of productivity to the sector. Fluazuron is an active ingredient (a.i.) of the benzoylurea class used to control ticks in cattle. As this a.i. has been found unchanged in animal feces, which may present a risk to edaphic organisms, this study aimed to assess the effects of fluazuron on survival, reproduction, and behavior of the soil invertebrates Folsomia candida and Eisenia andrei, through ecotoxicological assays. We carried out bioassays in a tropical artificial soil (TAS) spiked with increasing doses of the insecticide. Earthworm mortality was found only at the highest tested fluazuron concentration (LOEC = 160 mg a.i. kg−1 dry soil and NOEC = 80 mg kg−1), while the reproduction of F. candida and E. andrei was reduced at lower fluazuron concentrations (EC50 = 4.48 mg kg−1 and EC50 = 20.8 mg kg−1, respectively). Avoidance behavior was detected for both species at lower concentrations than those that caused impacts on reproduction, indicating that the substance may affect the soil habitat function. Since the possible adverse effects of fluazuron on edaphic fauna are still unknown or neglected, this study also warns about the possible harmful effect of veterinary pharmaceutical products on edaphic fauna.

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References

  • Adhikari K, Hartemink AE (2016) Linking soils to ecosystem services - a global review. Geoderma 262:101–111

    Article  CAS  Google Scholar 

  • Alves PRL, Cardoso EJBN, Martines AM, Sousa JP, Pasini A (2014) Seed dressing pesticides on springtails in two ecotoxicological laboratory tests. Ecotoxicol Environ Saf 105:65–71

    Article  CAS  Google Scholar 

  • Alves PRL, Natal-Da-Luz T, Sousa JP, Cardoso EJBN (2015) Ecotoxicological characterization of sugarcane vinasses when applied to tropical soils. Sci Total Environ 526:222–232

    Article  CAS  Google Scholar 

  • Araya-Anchetta A, Busch JD, Scoles GA, Wagner DM (2015) Thirty years of tick population genetics: a comprehensive review. Infect Genet Evol 29:164–179

    Article  Google Scholar 

  • Campiche S, Becker-Van SK, Ridreau C, Tarradellas J (2006) Effects of insect growth regulators on the nontarget soil arthropod Folsomia candida (Collembola). Ecotoxicol Environ Saf 63:216–225

    Article  CAS  Google Scholar 

  • Campiche S, L’Ambert G, Tarradellas J, Becker-van SK (2007) Multigeneration effects of insect growth regulators on the springtail Folsomia candida. Ecotoxicol Environ Saf 67:180–189

    Article  CAS  Google Scholar 

  • CQFS RS/SC - Comissão de Química e Fertilidade do Solo (2004) Manual de adubação e de calagem para os Estados do Rio Grande do Sul e de Santa Catarina, 10th edn. Sociedade Brasileira de Ciência do Solo, Porto Alegre 400p

    Google Scholar 

  • Daam MA, Leitão S, Cerejeira MJ, Sousa JP (2011) Comparing the sensitivity of soil invertebrates to pesticides with that of Eisenia fetida. Chemosphere 85:1040–1047

    Article  CAS  Google Scholar 

  • De Silva PMCS, Van Gestel CAM (2009) Comparative sensitivity of Eisenia andrei and Perionyx excavatus in earthworm avoidance tests using two soil types in the tropics. Chemosphere 77:1609–1613

    Article  CAS  Google Scholar 

  • Dourmishev AL, Schwartz RA (2005) Ivermectin: pharmacology and application in dermatology. Int J Dermatol 44:981–988

    Article  CAS  Google Scholar 

  • EC (2003) Technical guidance document on risk assessment, in support of commission directive 93/67/EEC, commission regulation (EC) no 1488/94 and directive 98/8/EC. European Commission Joint Research Center

  • Environmental Canada (2007) Guidance document on statistical methods for environmental toxicity test. Environmental Protection Series, EPS 1/RM/46, 2005 with 2007 updates. Environmental Canada, Ottawa

  • FAO - Food and Agriculture Organization of the United Nations (1998) Residues of some veterinary drugs in animals and foods. Available at: <http://www.fao.org/docrep/w8338e/w8338e00.htm#Contents >. Accessed 15 August 2018

  • Frampton GK, Jänsch S, Scott-Fordsmand JJ, Römbke J, Van der Brink P (2006) Effects of pesticides on soil invertebrates in laboratory studies: a review and analysis using species sensitivity distributions. Environ Toxicol Chem 25:2480–2489

    Article  CAS  Google Scholar 

  • Franco FC, Alves AA, Godoy FR, Avelar JB, Rodrigues DD, Pedroso TMA, deCruz AD, Nomura F, de Melo e Silva D (2016) Evaluating genotoxic risks in Brazilian public health agents occupationally exposed to pesticides: a multi-biomarker approach. Environ Sci Pollut Res 23(19):19723–19734

    Article  CAS  Google Scholar 

  • Furlong J (2005) Carrapato: problemas e soluções. Embrapa Gado de Leite. Juiz de Fora – MG, 65 p. Avaliable at: <http://ainfo.cnptia.embrapa.br/digital/bitstream/item/132467/1/Livro-Carrapatos-problemas-e-solucoes.pdf>. Accessed 15 August 2018

  • Gangishetti U, Breitenbach S, Zander M, Saheb SK, Müller U, Schwarz H, Moussian B (2009) Effects of benzoylphenylurea on chitin synthesis and orientation in the cuticle of the Drosophila larva. Eur J Cell Biol 88:167–180

    Article  CAS  Google Scholar 

  • Garcia MVB (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. Ecology and Development Series, vol. 19. University of Bonn, Germany

    Google Scholar 

  • Hsiao Y, Ho W, Yen J (2013) Vertical distribution in soil column and dissipation in soil of benzoylurea insecticides diflubenzuron, flufenoxuron and novaluron and effect on the bacterial community. Chemosphere 90:380–386

    Article  CAS  Google Scholar 

  • ISO (1993) International organization for standardization - 11268-1. Soil quality - effects of pollutants on earthworms (Eisenia fetida) - Part 1: Determination of acute toxicity using soil substrate. Genève, 26 p

  • ISO (2008) International organization for standardization - 17512-1. Soil quality - avoidance test for determining the quality of soils and effects of chemicals on behavior – Part 1: test with earthworms (Eisenia fetida and Eisenia andrei). Genève, 26 p

  • ISO (2011) International organization for standardization - 17512-2. Soil quality - avoidance test for determining the quality of soils and effects of chemicals on behavior – Part 2: test with collembolans (Folsomia candida). Genève, 13 p

  • ISO (2012) International standardization organization - 11268-2. Soil quality - effects of pollutants on earthworms - Part 2: Determination of effects on reproduction of Eisenia fetida/Eisenia andrei. Genève, 24 p

  • ISO (2014) International standardization organization – 11267. Soil quality - inhibition of reproduction of Collembola (Folsomia candida) by soil contaminants. Genève, 27 p

  • Kryger U, Deschodt C, Scholtz CH (2005) Effects of fluazuron and ivermectin treatment of cattle on the structure of dung beetle communities. Agric Ecosyst Environ 105:649–656

    Article  CAS  Google Scholar 

  • Kryger U, Deschodt C, Davis ALV, Scholtz CH (2007) Effects of cattle treatment with a fluazuron pour-on on survival and reproduction of the dung beetle species Onthophagus gazella (Fabricius). Vet Parasitol 143:380–384

    Article  CAS  Google Scholar 

  • Maccari AP, Baretta D, Paiano D, Leston S, Freitas A, Ramos F, Sousa JP, Klauberg-Filho O (2016) Ecotoxicological effects of pig manure on Folsomia candida in subtropical Brazilian soils. J Hazard Mater 314:113–120

    Article  CAS  Google Scholar 

  • Mapholi NO, Marufu MC, Maiwashe A, Banga CB, Muchenje V, MacNeil MD, Chimonyo M, Dzama K (2014) Towards a genomics approach to tick (Acari: Ixodidae) control in cattle. Ticks Tick-Borne Dis 5:475–483

    Article  Google Scholar 

  • Nasr HM, Badawy ME (2015) Biomarker response and biomass toxicity of earthworms Aporrectodea caliginosa exposed to IGRs pesticides. J Environ Anal Toxicol 5:332

    Article  Google Scholar 

  • National Registration Authority for Agricultural and Veterinary Chemicals (NRA) (1994) Fluazuron in the product Acatak pouron tick development inhibitor. Public Release Summary. NRA, Canberra

    Google Scholar 

  • Niva CC, Niemeyer JC, Da Silva Junior FMR, Nunes MET, De Sousa DL, Aragão CWS, Sautter KD, Espindola EG, Sousa JP, Römbke J (2016) Soil ecotoxicology in Brazil is taking its course. Environ Sci Pollut Res 23:11363–11378

    Article  CAS  Google Scholar 

  • OECD (1984) Guideline for testing chemicals, no. 207. Earthworm acute toxicity test. OECD Document, Organisation for Economic Co-Operation and Development. Paris, 9 p

  • Oliveira PR, Calligaris IB, Roma GC, Bechara GH, Pizano MA, Mathias MIC (2012) Potential of the insect growth regulator, fluazuron, in the control of Rhipicephalus sanguineus nymphs (Latreille, 1806) (Acari: Ixodidae). Exp Parasitol 131:35–39

    Article  CAS  Google Scholar 

  • Oliveira PR, Calligaris IB, Nunes PH, Bechara GH, Camargo-Mathias MI (2014) Fluazuron-induced morphological changes in Rhipicephalus sanguineus Latreille, 1806 (Acari: Ixodidae) nymphs. Acta Trop 133:45–55

    Article  CAS  Google Scholar 

  • Peijnenburg W, Capri E, Kula C, Liess M, Luttik R, Montforts M, Nienstedt K, Römbke J, Sousa JP, Jensen J (2012) Evaluation of exposure metrics for effect assessment of soil invertebrates. Crit Rev Env Sci Tec 42:1862–1893

    Article  CAS  Google Scholar 

  • Pereira CMS, Novais SC, Soares AMVM, Amorim MJB (2013) Dimethoate affects cholinesterases in Folsomia candida and their locomotion - false negative results of an avoidance behaviour test. Sci Total Environ 443:821–827

    Article  CAS  Google Scholar 

  • Piwoni M, Keeley J (1990) Basic concepts of contaminant sorption at hazardous waste sites. US Environ Prot Agency Document EPA/540/4-90/053, 7 p

  • Roberts TR, Hutson DH (1999) Metabolic pathways of agrochemicals: part 2: insecticides and fungicides. Royal Society of Chemistry, Cambridge, 1475 p

    Google Scholar 

  • Rugno GR, Zanardi OZ, Cuervo JB, Morais MR, Yamamoto PT (2016) Impact of insect growth regulators on the predator Ceraeochrysa cincta (Schneider) (Neuroptera: Chrysopidae). Ecotoxicology 25:940–949

    Article  CAS  Google Scholar 

  • Sakuma M (1999) Probit analisys of preference data. Appl Entomol Zool 8:339–347

    Google Scholar 

  • Segat JC, Alves PRL, Baretta D, Cardoso EJBN (2015) Ecotoxicological evaluation of swine manure disposal on tropical soils in Brazil. Ecotoxicol Environ Saf 122:91–97

    Article  CAS  Google Scholar 

  • Sousa A, Pereira R, Antunes SC, Cachada A, Pereira E, Duarte AC, Gonçalves F (2008) Validation of assays for the screening assessment of soils under different anthropogenic disturbances. Ecotoxicol Environ Saf 71:661–670

    Article  CAS  Google Scholar 

  • Wang Y, Cang T, Zhao X, Yu R, Chen L, Wu C, Wang Q (2012) Comparative acute toxicity of twenty-four insecticides to earthworm, Eisenia fetida. Ecotoxicol Environ Saf 79:122–128

    Article  CAS  Google Scholar 

  • Willers CD, Maranduba HL, de Almeida Neto JA, Rodrigues LB (2017) Environmental impact assessment of a semi-intensive beef cattle production in Brazil’s northeast. Int J Life Cycle Assess 22:516–524

    Article  CAS  Google Scholar 

  • Wolstenholme AJ, Rogers AT (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131:85–95

    Article  CAS  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall International, London, 663 p

    Google Scholar 

  • Zortéa T, Segat JC, Maccari AP, Sousa JP, Da Silva AS, Baretta D (2017) Toxicity of four veterinary pharmaceuticals on the survival and reproduction of Folsomia candida in tropical soils. Chemosphere 173:460–465

    Article  CAS  Google Scholar 

  • Zortéa T, Da Silva AF, Dos Reis TR, Segat JC, Paulino AT, Sousa JP, Baretta D (2018) Ecotoxicological effects of fipronil, neem cake and neem extract in edaphic organisms from tropical soil. Ecotoxicol Environ Saf 166:207–214

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank the anonymous ESPR reviewers for their helpful and constructive comments that greatly contributed to improving the final version of this paper. The authors also thank the Centro de Educação Superior do Oeste of the Santa Catarina State University for the research opportunity.

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Authors and Affiliations

  1. Federal University of Fronteira Sul, Av. Fernando Machado 108 E, Chapecó, SC, 89802-112, Brazil

    Paulo Roger Lopes Alves, Maicon Giraldi & Rosicler Presotto

  2. Department of Soil Science, Santa Catarina State University, Av. Luis de Camões, 2090, Lages, SC, 88520-000, Brazil

    Felipe Ogliari Bandeira

  3. Centro de Educação Superior do Oeste, Santa Catarina State University, Beloni Trombeta Zanin, 680-E, Chapecó, SC, 89815-630, Brazil

    Julia Corá Segat & Dilmar Baretta

  4. Department of Soil Science, University of São Paulo, Avenida Pádua Dias, 11, Piracicaba, 13416-900, Brazil

    Elke Jurandy Bran Nogueira Cardoso

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  1. Paulo Roger Lopes Alves
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Correspondence to Paulo Roger Lopes Alves.

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Alves, P.R.L., Bandeira, F.O., Giraldi, M. et al. Ecotoxicological assessment of Fluazuron: effects on Folsomia candida and Eisenia andrei. Environ Sci Pollut Res 26, 5842–5850 (2019). https://doi.org/10.1007/s11356-018-4022-7

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