Skip to main content
SpringerLink
Log in

An alternative approach to assess ecotoxicological effects of agrochemical combinations used in Brazilian aquaculture farms

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Agrochemicals used for treating and preventing aquaculture diseases are usually present in combination with other compounds, and the toxicity resulting from their chemical interactions presents an important reason to assess the ecotoxicity of compound mixtures in view to better understanding the joint action of chemicals and avoiding their environmental impacts. In this study, we evaluated the acute aquatic ecotoxicity of several compounds used in Brazilian fish farming (Oxytetracycline [OXT], Trichlorfon [TRC], and BioFish® [BIO]), both individually and in binary and ternary mixtures. Initial test concentrations were prepared according to the recommended concentrations for aquaculture application, and from these, a geometric dilution series was tested on two important fresh water quality indicator species, the microcrustacean Daphnia magna and the bacterium Aliivibrio fischeri. At the recommended pond application rate, TRC and BIO applied individually showed toxicity to the tested organisms in terms of the lowest-observed-effect concentration (LOEC), and D. magna was always more sensitive than A. fischeri. For the two test organisms, the results obtained with the binary mixtures showed that the TRC and BIO mixture was more toxic than TRC and OXT, which in turn was more toxic than OXT and BIO. The toxicity from all agrochemicals in the ternary mixture was more than that of the agrochemical combinations in the binary mixtures. Given the results presented in this study, it is evident that the mode of action and availability of the tested compounds undergo changes that increase toxicity when they are present in combination, and therefore, aquaculture wastewater treatment should be adopted to ensure decontamination of agrochemical residues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • ABNT (2007) NBR 15411-3 aquatic ecotoxicology — determination of the inhibitory effect of aqueous samples on bioluminescence emission from Vibrio fischeri (luminescent bacteria assay). Part 3: Method using lyophilized bacteria. Associação Brasileira de Normas Técnicas, Rio de Janeiro, RJ, Brazil

    Google Scholar 

  • ABNT (2009) NBR 12713 aquatic ecotoxicology — acute toxicity — test method with Daphnia spp. (Crustacea, Cladocera). Associação Brasileira de Normas Técnicas, Rio de Janeiro, RJ, Brazil

    Google Scholar 

  • Altenburger R, Boedeker W, Faust M, Grimme LH (1996) Regulations for combined effects of pollutants: consequences from risk assessment in aquatic toxicology. Food Chem Toxicol 34:1155–1157. https://doi.org/10.1016/S0278-6915(97)00088-4

    Article  CAS  Google Scholar 

  • Amaral Junior H, Garcia S, Liebl F, Rocha DJ, Boanini A (2018) Effect of Biogermex® phytotherapeutic incorporated into the feed on the survival of catfish larvae Rhamdia quelen. Camboriú. Available in: http://intranetdoc.epagri.sc.gov.br/producao_tecnico_cientifica/DOC_23166.pdf. Access: 09 March, 2020.

  • Backhaus T, Altenburger R, Arrhenius A, Blanck H, Faust M, Finizio A, Gramatica P, Grote M, Junghans M, Meyer W, Pavan M, Porsbring T, Scholze M, Todeschini R, Vighi M, Walter H, Grimme LH (2003) The BEAM-project: prediction and assessment of mixture toxicities in the aquatic environment. Cont Shelf Res 23:1757–1769. https://doi.org/10.1016/j.csr.2003.06.002

    Article  Google Scholar 

  • Backhaus T, Froehner K, Altenburger R, Grimme LH (1997) Toxicity testing with Vibrio fischeri: a comparison between the long-term (24 h) and the short-term (30 min) bioassay. Chemosphere 35:2925–2938. https://doi.org/10.1016/S0045-6535(97)00340-8

    Article  CAS  Google Scholar 

  • Barata C, Baird DJ, Nogueira AJA, Soares AMVM, Riva MC (2006) Toxicity of binary mixtures of metals and pyrethroid insecticides to Daphnia magna Straus. Implications for multi-substance risks assessment. Aquat Toxicol 78:1–14. https://doi.org/10.1016/j.aquatox.2006.01.013

    Article  CAS  Google Scholar 

  • Bebak-Williams J, Bullock G, Carson MC (2002) Oxytetracycline residues in a freshwater recirculating system. Aquaculture 205:221–230

    Article  CAS  Google Scholar 

  • Belden JB, Brainz RA (2018) Incorporating the joint toxicity of co-applied pesticides intothe ecological risk assessment process. Integr Environ Assess Manag 14:79–91. https://doi.org/10.1002/ieam.1957

    Article  CAS  Google Scholar 

  • BioGermex (2019) BioFish. Itajaí. Available in: http://www.biogermex.com.br. Access in: 09 Mar. 2021.

  • Bjergager M-BA, Hanson ML, Solomon KR, Cedergreen N (2012) Synergy between prochloraz and esfenvalerate in Daphnia magna from acute and subchronic exposures in the laboratory and microcosms. Aquat Toxicol 110–111:17–24. https://doi.org/10.1016/j.aquatox.2011.12.001

    Article  CAS  Google Scholar 

  • Bliss CI (1939) The toxicity of poisons applied jointly. Ann Appl Biol 26:585–615

    Article  CAS  Google Scholar 

  • Cedergreen N, Nazir A (2014) Quantifying synergy: a systematic review of mixture toxicity studies within environmental toxicology. PloS One 9:e96580. https://doi.org/10.1371/journal.pone.0096580

    Article  CAS  Google Scholar 

  • Chèvre N, Gregorio V (2013) Mixture effects in ecotoxicology. In: Blaise C (ed) Férard JF. Encyclopedia of Aquatic Ecotoxicology, Springer, pp 729–731

    Google Scholar 

  • Coelho S, Oliveira R, Pereira S, Musso C, Domingues I, Bhujel RC, Soares AMVM, Nogueira JA (2011) Assessing lethal and sub-lethal effects of Trichlorfon on different trophic levels. Aquat Toxicol 103:191–198

    Article  CAS  Google Scholar 

  • Czeizel AE, Elek C, Gundy S, Métneki J, Nemes E, Reis A, Sperling K, Tímár L, Tusnády G, Virágh Z (1993) Environmental Trichlorfon and cluster of congenital abnormalities. Lancet 27:539–542

    Article  Google Scholar 

  • Da Silva LFBA, Yang Z, Pires NMM, Dong T, Teien H-C, Storebakken T, Salbu B (2018) Monitoring aquaculture water quality: design of an early warning sensor with Aliivibrio fischeri and predictive models. Sensors 18:1–16. https://doi.org/10.3390/s18092848

    Article  Google Scholar 

  • FAO (2018) The state of world fisheries and aquaculture 2018 — meeting the sustainable development goals. Food and Agriculture Organization of the United Nations, Rome Licence: CC BY-NC-SA 3.0 IGO

  • Feng T, Li ZB, Guo XQ, Guo JP (2008) Effects of Trichlorfon and sodium dodecyl sulphate on antioxidant defense system and acetylcholinesterase of Tilapia nilotica in vitro. Pest Biochem Physiol 92:107–113

    Article  CAS  Google Scholar 

  • Fox DR, Landis WG (2016) Don’t be fooled—a no-observed-effect concentration is no substitute for a poor concentration–response experiment. Environ Toxicol Chem 35:2141–2148. https://doi.org/10.1002/etc.3459

    Article  CAS  Google Scholar 

  • Froehner K, Meyer W, Grimme LH (2002) Time-dependent toxicity in the long-term inhibition assay with Vibrio fischeri. Chemosphere 46:987–997

    Article  CAS  Google Scholar 

  • Garcia S, Amaral Júnior H, Mello GL, Silva FM, Graeff A, Serafini RL, Liebl F, Bernardes Júnior JJ (2018a) Evaluation of the lethal concentration in 96 hours (LC50-96 h) for Biogermex® in tilapia GIFT fingerlings (Oreochromis niloticus) in southern Brazil, Camboriú. Available in: http://intranetdoc.epagri.sc.gov.br/producao_tecnico_cientifica/DOC_6951.pdf. Access in: 09 Mar. 2018

  • Garcia S, Amaral Júnior H, Mello GL, Silva FM Graeff A, Serafini RL, Liebl F, Bernardes Júnior JJ (2018b) Lethal concentration in 24 hours (Cl50-24 h) of Biogermex® for grass carp fingerlings (Ctenopharyngodon idella), Camboriú. Available in: http://intranetdoc.epagri.sc.gov.br/producao_tecnico_cientifica/DOC_26839.pdf. Access in: 09 Mar. 2018.b

  • González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five agrochemicals and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064

    Article  Google Scholar 

  • Gupta RC (2005) Trichlorfon. In: Wexler P (ed) Encyclopedia of Toxicology (Second Edition). Elsevier, pp 377–379. https://doi.org/10.1016/B0-12-369400-0/00983-2

    Chapter  Google Scholar 

  • Hem L, Khay S, Choi JH, Morgan ED, Abd El-Aty AM, Shim JH (2010) Determination of Trichlorfon pesticide residues in milk via gas chromatography with μ-electron capture detection and GC-MS. Toxicol Res 26:149–155. https://doi.org/10.5487/TR.2010.26.2.149

    Article  CAS  Google Scholar 

  • Hernando MD, Vettori S, Bueno MJM, Fernández-Alba AR (2007) Toxicity evaluation with Vibrio fischeri test of organic chemicals used in aquaculture. Chemosphere 68:724–730. https://doi.org/10.1016/j.chemosphere.2006.12.097

    Article  CAS  Google Scholar 

  • Hoel DG (1987) Statistical aspects of chemical mixtures. In: Vouk VB, Butler GC, Upton AC, Parke DV, Casher S (eds) Methods for Assessing the Effects of Mixtures of Chemicals. SCOPE Report, Chichester, Willey, pp 369–377

    Google Scholar 

  • Isidori M, Lavorgna M, Nardelli Â, Pascarella L, Parrella A (2005) Toxic and genotoxic evaluation of six agrochemicals on non-target organisms. Sci Total Environ 346:87–98

    Article  CAS  Google Scholar 

  • Kaiser KLE (1998) Correlation of Vibrio fischeri bacteria test data with bioassay data for other organisms. Environ Health Prospect 106:583–591

    CAS  Google Scholar 

  • Kay P, Blackwell PA, Boxall ABA (2005) Transport of veterinary agrochemicals in overland flow following the application of slurry to arable land. Chemosphere 59:951–959

    Article  CAS  Google Scholar 

  • Kemper N (2008) Veterinary agrochemicals in the aquatic and terrestrial environment. Ecol Indic 8:1–13

    Article  CAS  Google Scholar 

  • Kołodziejska M, Maszkowska J, Białk-Bielińska A, Steudte S, Kumirska J, Stepnowski P, Stolte S (2013) Aquatic toxicity of four veterinary drugs commonly applied in fish farming and animal husbandry. Chemosphere 92:1253–1259

    Article  Google Scholar 

  • Lalumera GM (2004) Preliminary investigation on the environmental occurrence and effects of agrochemicals used in aquaculture in Italy. Chemosphere 54:661–668

    Article  CAS  Google Scholar 

  • Loewe S, Muischnek H (1926) Über combinations wirkungen 1. Mitteilung: Hilfsmittel der Frage-stellungNaunyn-Schmiedebergs. Arch Exp Pathol Pharmakol 114:313–326

    Article  CAS  Google Scholar 

  • Masoten®. Aqua Cultura. Available in: http://www.aquasem.com.br/images/masoten.pdf. Access in: 09 Mar. 2018.

  • Maximiano AA, Fernandes RO, Nunes FP, Assis MP, Matos RV, Barbosa CGS, Oliveira-Filho EC (2005) Use of veterinary drugs, pesticides and similars in water environments: demands, regulations and considerations about risks to human and environmental health. Ciência e Saúde Coletiva 10:483–491. https://doi.org/10.1590/S1413-81232005000200026

    Article  Google Scholar 

  • Okocha RC, Olatoye IO, Alabi PI, Ogunnoiki MG, Adedeji OB (2021) Aquaculture management practices associated with antimicrobial residues in Southwestern Nigeria. Aquaculture 533:736195. https://doi.org/10.1016/j.aquaculture.2020.736195

    Article  CAS  Google Scholar 

  • Papadoyannis IN, Samanidou VF, Kovatsi LA (2000) A rapid high performance liquid chromatographic (HPLC) assay for the determination of Oxytetracycline in commercial pharmaceuticals. J Pharm Biomed Anal 15:275–280. https://doi.org/10.1016/s0731-7085(00)00300-9

    Article  Google Scholar 

  • Park S, Choi K (2008) Hazard assessment of commonly used agricultural agrochemicals on aquatic ecosystems. Ecotoxicology 7:526–538

    Article  Google Scholar 

  • PhibroTM ® 700. Technical datasheet. http://phibro.com.br/uploads/produtos/1441190547-Ficha%20Tecnica%20-%20TM%20700.pdf. Access in: 09 Mar. 2020.

  • Qin LT, Wu J, Mo LY, Zeng HH, Liang YP (2015) Linear regression model for predicting vinteractive mixture toxicity of pesticide and ionic liquid. Environ Sci Pollut Res 22:12759–12768

    Article  CAS  Google Scholar 

  • Rico A, Oliveira R, Mcdonough S, Matser A, Khatikarn J, Satapornvanit K, Nogueira A, Soares A, Domingues I, Brink P (2014) Use, fate and ecological risks of agrochemicals applied in tilápia cage farming in Thailand. EnvironPollut 191:8–16

    CAS  Google Scholar 

  • Rigos G, Troisi GM (2005) Antibacterial agents in Mediterranean finfish farming: a synopsis of drug pharmacokinetics in important euryhaline fish species and possible environmental implications. Rev Fish Biol Fish 15:53–73

    Article  Google Scholar 

  • Rodea-Palomares I, González-Pleiter M, Martín-Betancor K, Rosal R, Fernández-Piñas F (2015) Additivity and interactions in ecotoxicity of pollutant mixtures: some patterns, conclusions and open questions. Toxics 25:342–369. https://doi.org/10.3390/toxics3040342

    Article  CAS  Google Scholar 

  • Subasinghe R, Soto D, Jia J (2009) Global aquaculture and its role in sustainable development. Rev Aquac 1:2–9

    Article  Google Scholar 

  • Tanaka Y, Tada M (2017) Generalized concentration addition approach for predicting mixture toxicity. Environ Toxicol Chem 36:265–275

    Article  CAS  Google Scholar 

  • Thomulka KW, Kriebel JR, Schroeder JA, Lange JH (1993) Toxicity of various chemicals in a sand and water mixture using the marine bacterium Vibrio harveyi in a direct bioluminescence-reduction bioassay. J Clean Technol Environ 3:217–226

    CAS  Google Scholar 

  • Tkaczyk A, Bownik A, Dudka J, Kowal K, Ślaska B (2021) Daphnia magna model in the toxicity assessment of pharmaceuticals: a review. Sci Total Environ 763:143038. https://doi.org/10.1016/j.scitotenv.2020.143038

    Article  CAS  Google Scholar 

  • Toumi H, Boumaiza M, Millet M, Radetski CM, Camara B, Felten V, Masfaraud J-F, Férard J-F (2018) Joint acute ecotoxicity of malathion and deltamethrin to Daphnia magna (Crustacea, Cladocera). Environ Sci Pollut Res 25:17781–17788

    Article  CAS  Google Scholar 

  • Toussaint MW, Shedd TR, van der Schalie WH, Leather GR (1995) A comparison of standard acute toxicity tests with rapid-screening toxicity tests. Environ Toxicol Chem 14:907–915. https://doi.org/10.1002/etc.5620140524

    Article  CAS  Google Scholar 

  • Valenti WC, Barros HP, Moraes-Valenti P, Bueno GW, Cavalli RO (2021) Aquaculture in Brazil: past, present and future. Aquac Rep 19:100611. https://doi.org/10.1016/j.aqrep.2021.100611

    Article  Google Scholar 

  • Valladão GMR, Gallani SU, Jerônimo GT, Seixas AT (2020) Challenges in the control of acanthocephalosis in aquaculture: special emphasis on Neoechinorhynchus buttnerae. Rev Aquacult 12:1360–1372. https://doi.org/10.1111/raq.12386

    Article  Google Scholar 

  • Wang X, Lin Y, Zheng Y, Meng F (2022) Antibiotics in mariculture systems: a review of occurrence, environmental behavior, and ecological effects. Environ Pollut 293:118541. https://doi.org/10.1016/j.envpol.2021.118541

    Article  CAS  Google Scholar 

  • Wei S, Wang F, Chen Y, Lan T, Zhang S (2018) The joint toxicity effect of five agrochemicals and dibutyl phthalate to luminescent bacteria (Vibrio fischeri). Environ Sci Pollut Res 25:26504–26511. https://doi.org/10.1007/s11356-018-2720-9

    Article  CAS  Google Scholar 

  • Williams DA (1972) The comparison of several dose levels with a zero-dose control. Biometrics 28:519–531

    Article  CAS  Google Scholar 

  • Wollenberger L, Halling-Sorensen B, Kusk KO (2000) Acute and chronic toxicity of veterinary agrochemicals to Daphnia magna. Chemosphere 40:723–730

    Article  CAS  Google Scholar 

  • Yoshimura H, Endoh YS (2005) Acute toxicity to freshwater organisms of antiparasitic drugs for veterinary use. Environ Toxicol 20:60–66

    Article  CAS  Google Scholar 

  • Zhang Y-H, Liu S-S, Liu H-L, Liu Z-Z (2010) Evaluation of the combined toxicity of 15 pesticides by uniform design. Pest Manag Sci 66:879–887

    Article  CAS  Google Scholar 

  • Zounková R, Klimešová Z, Nepejchalová L, Hilscherová K, Bláha L (2011) Complex evaluation of ecotoxicity and genotoxicity of antimicrobials Oxytetracycline and flumequine used in aquaculture. Environ Toxicol Chem 30:1184–1189

    Article  Google Scholar 

Download references

Acknowledgements

We thank EPAGRI Camboriú and UNIVALI for the technical support, Ingelvet for supplying the Oxytetracycline compound, and Biogermex for supplying the BioFish® compound.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

Support was provided by FAPESC (Project # 2021TR000549) to C. M. Radetski.

Author information

Authors and Affiliations

  1. Laboratório de Química Analítica e Ambiental, Instituto Federal Catarinense – Campus Araquari, Araquari, SC, 89245-000, Brazil

    Vanessa A. Matias, Juliano S. Gueretz & Cleder A. Somensi

  2. Laboratório de Fisiologia, Universidade do Vale do Itajaí, Itajaí, SC, 88302-202, Brazil

    Vanessa A. Matias & Ariana G. Weber

  3. Curso de Mestrado em Tecnologia e Ambiente, Instituto Federal Catarinense – Campus Araquari, Araquari, SC, 89245-000, Brazil

    Gabriel C. Walz, Cristiane V. Tagliari-Corrêa & Cleder A. Somensi

  4. Faculté des Sciences de Bizerte, Laboratoire de Bio-surveillance de l’Environnement (LBE), Université de Carthage, 7021, Zarzouna, Bizerte, Tunisia

    Héla Toumi

  5. Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), Université de Lorraine, F-57070, Metz, France

    Jean-François Férard & Sylvie Cotelle

  6. Programa de Pós-Graduação em Ciência e Tecnologia Ambiental, Universidade do Vale do Itajaí, Itajaí, SC, 88302-202, Brazil

    Claudemir M. Radetski

Authors
  1. Vanessa A. Matias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ariana G. Weber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Juliano S. Gueretz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriel C. Walz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristiane V. Tagliari-Corrêa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Héla Toumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jean-François Férard
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Claudemir M. Radetski
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Cleder A. Somensi
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sylvie Cotelle
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

V. A. Matias, A. G. Weber, J. S. Gueretz, G. Walz, C. V. Tagliari-Corrêa, H. Toumi: investigation, formal analysis, resources, funding acquisition. J.-F. Férard, C. M. Radetski, C. A. Somensi, S. Cotelle: resources, writing — review and editing, supervision.

Corresponding author

Correspondence to Sylvie Cotelle.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Matias, V.A., Weber, A.G., Gueretz, J.S. et al. An alternative approach to assess ecotoxicological effects of agrochemical combinations used in Brazilian aquaculture farms. Environ Sci Pollut Res 30, 70713–70721 (2023). https://doi.org/10.1007/s11356-023-27414-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-27414-2

Keywords

Search

Navigation