Skip to main content
SpringerLink
Log in

Ecotoxicological and biochemical mixture effects of an herbicide and a metal at the marine primary producer diatom Thalassiosira weissflogii and the primary consumer copepod Acartia tonsa

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

Abstract

Mixture effects of chemicals and their potential synergistic interactions are of great concern to the public and regulatory authorities worldwide. Intensive agricultural activities are leading to discharges of chemical mixtures to nearby estuarine and marine waters with possible adverse effects on the aquatic communities and for the trophic food web interlinking these communities. Further information about the impacts of these stressors on aquatic organisms is needed. This study addresses ecotoxicological and biochemical effects of single and mixtures of the metal copper and the herbicide Primextra® Gold TZ on the marine diatom Thalassiosira weissflogii and on the estuarine calanoid copepod Acartia tonsa by determining growth rate and survival, respectively, and changes on fatty acid(FA) profiles in both species. Mixture effects on diatom species revealed that copper and Primextra® acted most likely additively with respect to the concentration addition (CA) and independent action (IA) models with model deviation ratios (MDR), 0.752 and 1.063, respectively. For the copepod species, copper and Primextra® were most likely non-interactive with respect to the CA model (MDR = 1.521) but acted most likely synergistically with respect to the IA model (MDR = 2.026). A significant decline in the absolute FA concentration was observed for copepod species after mixture exposure including a considerable decrease of essential FAs that cannot be synthesized de novo by these grazers. We concluded that the mixture effects are more hazardous for primary consumer than for primary producer species in terms of both abundance and biomass quality, suggesting a potential for harmful effects for higher trophic levels and thus a decrease in energy flow through the ecosystem.

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
Fig. 2

Similar content being viewed by others

References

  • Ahsanullah M, Florence T (1984) Toxicity of copper to the marine amphipod Allorchestes compressa in the presence of water- and lipid-soluble ligands. Mar Biol 84:41–45

    Article  CAS  Google Scholar 

  • Aoyama I, Okamura H, Yagi M (1987) The interaction effects of toxic chemical combinations on Chlorella ellipsoidea. Toxic Assess An Int Q 2:341–355

    CAS  Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Araújo CFC, Souza-Santos LP (2013) Use of the microalgae Thalassiosira weissflogii to assess water toxicity in the Suape industrial-port complex of Pernambuco, Brazil. Ecotoxicol Environ Saf 89:212–221. https://doi.org/10.1016/j.ecoenv.2012.11.032

    Article  CAS  Google Scholar 

  • Backhaus T, Faust M (2012) Predictive environmental risk assessment of chemical mixtures: a conceptual framework. Environ Sci Technol 46:2564–2573

    Article  CAS  Google Scholar 

  • Bae JH, Lim SY (2012) Heavy metals and biochemical composition of four sea bream species (Acanthopagrus schlegelii Bleeker, Pagrus major Temminck & Schlegel, Oplegnathus fasciatus Krøyer and Girella punctata Gray). Philipp Agric Sci 95:185–191

    Google Scholar 

  • Baker LF, Mudge JF, Thompson DG, Houlahan JE, Kidd KA (2016) The combined influence of two agricultural contaminants on natural communities of phytoplankton and zooplankton. Ecotoxicology 25:1021–1032. https://doi.org/10.1007/s10646-016-1659-1

    Article  CAS  Google Scholar 

  • Belden JB, Gilliom R, Lydy MJ (2007) How well can we predict the aquatic toxicity of pesticide mixtures. Integr Environ Assess Manag 3:364–372

    Article  CAS  Google Scholar 

  • Binderup ML, Dalgaard M, Dragsted LO et al (2003) Combined actions and interactions of Chemicals in Mixtures: the toxicological effects of exposure to mixtures of industrial and environmental chemicals, 1st edn. FödevareRapport, Miljøstyrelsen

    Google Scholar 

  • Bliss C (1939) The toxicity of poisons applied jointly. Ann Appl Biol 26:585–615. https://doi.org/10.1111/j.1744-7348.1939.tb06990.x

    Article  CAS  Google Scholar 

  • Brett MT, Dörthe CM-N, Persson J (2009) Crustacean zooplankton fatty acid composition. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 115–146

    Chapter  Google Scholar 

  • Brett MT, Müller-Navarra DC (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshw Biol 38:483–499. https://doi.org/10.1046/j.1365-2427.1997.00220.x

    Article  CAS  Google Scholar 

  • Brix KV, Gerdes RM, Adams WJ, Grosell M (2006) Effects of copper, cadmium, and zinc on the hatching success of brine shrimp (Artemia franciscana). Arch Environ Contam Toxicol 51:580–583. https://doi.org/10.1007/s00244-005-0244-z

    Article  CAS  Google Scholar 

  • Castro M, Ojeda C, Cirelli AF (2013) Surfactants in agriculture. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) green materials for energy, products and depollution. Environmental chemistry for a sustainable world. Vol. 3. Springer, Dordrecht

  • Cedergreen N (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 

  • Cerejeira MJ, Viana P, Batista S, Pereira T, Silva E, Valério MJ, Silva A, Ferreira M, Silva-Fernandes AM (2003) Pesticides in Portuguese surface and ground waters. Water Res 37:1055–1063. https://doi.org/10.1016/S0043-1354(01)00462-6

    Article  CAS  Google Scholar 

  • Chen C, Wang Y, Qian Y, Zhao X, Wang Q (2015) The synergistic toxicity of the multiple chemical mixtures: implications for risk assessment in the terrestrial environment. Environ Int 77:95–105. https://doi.org/10.1016/j.envint.2015.01.014

    Article  CAS  Google Scholar 

  • Chen H, Sheng X, Wen Y, Zhang L, Bao H, Li L, Liu W (2013) New insights into the effects of the herbicide imazethapyr on Cu(II) ecotoxicity to the aquatic unicellular alga Scenedesmus obliquus. Aquat Toxicol 140–141:407–414. https://doi.org/10.1016/j.aquatox.2013.06.017

    Article  CAS  Google Scholar 

  • CMA/3/H (2002) Organofosorpesticiden en triazine-type herbiciden met GC/MS ontwerp

  • Cook ME, Moore PA (2008) The effects of the herbicide metolachlor on agonistic behavior in the crayfish, Orconectes rusticus. Arch Environ Contam Toxicol 55:94–102. https://doi.org/10.1007/s00244-007-9088-z

    Article  CAS  Google Scholar 

  • Coors A, Löffler I, Noronha-Jänsch P et al (2013) Ecotoxicological combined effects from chemical mixtures. Part 2: development of ecotoxicological tests with biocidal products and eluates: investigating the suitability of biotests with algae and daphnids to estimate mixture toxicity. Dessau-Roßlau, Germany

    Google Scholar 

  • Cruzeiro C, Rocha E, Pardal MA, Rocha MJ (2016) Environmental assessment of pesticides in the Mondego River Estuary (Portugal). Mar Pollut Bull 103:240–246. https://doi.org/10.1016/j.marpolbul.2015.12.013

    Article  CAS  Google Scholar 

  • De Coninck DIM, De Schamphelaere KAC, Jansen M et al (2013) Interactive effects of a bacterial parasite and the insecticide carbaryl to life-history and physiology of two Daphnia magna clones differing in carbaryl sensitivity. Aquat Toxicol 130–131:149–159. https://doi.org/10.1016/j.aquatox.2013.01.008

    Article  CAS  Google Scholar 

  • De Troch M, Boeckx P, Cnudde C et al (2012) Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Mar Ecol Prog Ser 465:53–67. https://doi.org/10.3354/meps09920

    Article  CAS  Google Scholar 

  • Debenest T, Silvestre J, Coste M, Pinelli E (2010) Effects of pesticides on freshwater diatoms. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology. Springer Science+Business Media, LLC, pp 87–103

  • DeLorenzo ME, Serrano L (2003) Individual and mixture toxicity of three pesticides; atrazine, chlorpyrifos, and chlorothalonil to the marine phytoplankton species Dunaliella tertiolecta. J Environ Sci Health B 38:529–538. https://doi.org/10.1081/PFC-120023511

    Article  CAS  Google Scholar 

  • Diz FR, Araújo CVM, Moreno-Garrido I, Hampel M, Blasco J (2009) Short-term toxicity tests on the harpacticoid copepod Tisbe battagliai: lethal and reproductive endpoints. Ecotoxicol Environ Saf 72:1881–1886. https://doi.org/10.1016/j.ecoenv.2009.03.004

    Article  CAS  Google Scholar 

  • Dores EFGC, Spadotto CA, Weber OLS, Carbo L, Vecchiato AB, Pinto AA (2009) Environmental behaviour of metolachlor and diuron in a tropical soil in the central region of Brazil. Water Air Soil Pollut 197:175–183. https://doi.org/10.1007/s11270-008-9801-1

    Article  CAS  Google Scholar 

  • EPA (2008) EPA Report 815-R-08-012: regulatory determinations support documnet for selected contaminants from the second drinking water contaminant candidate list (CCL 2). Part III: what about the remaining CCL 2 contaminants? Chapter 12: metolachlor

  • Ferreira JG, Simas T, Nobre A, et al (2003) Identification of sensitive areas and vulnerable zones in transitional and coastal Portuguese systems. INAG—Instituto da Agua—Institute of Marine Research

  • Filimonova V, Gonçalves F, Marques J et al (2016a) Biochemical and toxicological effects of organic (herbicide Primextra® Gold TZ) and inorganic (copper) compounds on zooplankton and phytoplankton species. Aquat Toxicol 177:33–43. https://doi.org/10.1016/j.aquatox.2016.05.008

    Article  CAS  Google Scholar 

  • Filimonova V, Gonçalves F, Marques J et al (2016b) Fatty acid profiling as bioindicator of chemical stress in marine organisms: a review. Ecol Indic 67:657–672. https://doi.org/10.1016/j.ecolind.2016.03.044

    Article  CAS  Google Scholar 

  • Finney DJ (1971) Probit analysis. WILEY-VCH Verlag, Cambridge

    Google Scholar 

  • Fiori E, Mazzotti M, Guerrini F, Pistocchi R (2013) Combined effects of the herbicide terbuthylazine and temperature on different flagellates from the northern Adriatic Sea. Aquat Toxicol 128–129:79–90. https://doi.org/10.1016/j.aquatox.2012.12.001

    Article  CAS  Google Scholar 

  • Flindt MR, Kamp-Nielsen L, Marques JC, Pardal MA, Bocci M, Bendoricchio G, Salomonsen J, Nielsen SN, Jørgensen SE (1997) Description of the three shallow estuaries: Mondego River (Portugal), Roskilde Fjord (Denmark) and the Lagoon of Venice. Ecol Model 102:17–31

    Article  CAS  Google Scholar 

  • Forget J, Pavillon JF, Beliaeff B, Bocquené G (1999) Joint action of pollutant combinations (pesticides and metals) on survival (LC50 values) and acetylcholinesterase activity of Tigriopus brevicornis (Copepoda, Harpacticoida). Environ Toxicol Chem 18:912–918. https://doi.org/10.1897/1551-5028(1999)018<0912:jaopcp>2.3.co;2

    Article  CAS  Google Scholar 

  • Franklin NM, Stauber JL, Lim RP, Petocz P (2002) Toxicity of metal mixtures to a tropical freshwater alga (Chlorella sp): the effect of interactions between copper, cadmium, and zinc on metal cell binding and uptake. Environ Toxicol Chem 21:2412–2422. https://doi.org/10.1002/etc.5620211121

    Article  CAS  Google Scholar 

  • Gabrielides GP (1995) Pollution of the Mediterranean Sea. Water Sci Technol 32:1–10. https://doi.org/10.1016/0273-1223(96)00070-4

    Article  CAS  Google Scholar 

  • Gabryelak T, Filipiak A, Brichon G (2000) Effects of zinc on lipids of erythrocytes from carp (Cyprinus carpio L.) acclimated to different temperatures. Comp Biochem Physiol-C Pharmacol Toxicol Endocrinol 127:335–343. https://doi.org/10.1016/S0742-8413(00)00161-4

    Article  CAS  Google Scholar 

  • Geret F, Burgeot T, Haure J et al (2011) Effects of low-dose exposure to pesticide mixture on physiological responses of the pacific oyster, Crassostrea gigas. Environ Toxicol 28:689–699. https://doi.org/10.1002/tox

    Article  CAS  Google Scholar 

  • Gonçalves A, Azeiteiro U, Pardal M, De Troch M (2012a) Fatty acid profiling reveals seasonal and spatial shifts in zooplankton diet in a temperate estuary. Estuar Coast Shelf Sci 109:70–80. https://doi.org/10.1016/j.ecss.2012.05.020

    Article  CAS  Google Scholar 

  • Gonçalves A, Mesquita A, Verdelhos T et al (2016) Fatty acids’ profiles as indicator of stress induced by of a common herbicide on two marine bivalves species: Cerastoderma edule (Linnaeus, 1758) and Scrobicularia plana (da Costa, 1778). Ecol Indic 63:209–218. https://doi.org/10.1016/j.ecolind.2015.12.006

    Article  CAS  Google Scholar 

  • Gonçalves A, Pardal MA, Marques SC et al (2010) Distribution and composition of small-size zooplankton fraction in a temperate shallow estuary (Western Portugal). Fresenius Environ Bull 19:3160–3176

    Google Scholar 

  • Gonçalves A, Pardal M, Marques S et al (2012b) Diel vertical behavior of Copepoda community (naupliar, copepodites and adults) at the boundary of a temperate estuary and coastal waters. Estuar Coast Shelf Sci 98:16–30. https://doi.org/10.1016/j.ecss.2011.11.018

    Article  Google Scholar 

  • Gonçalves A, Pardal M, Marques S et al (2012c) Responses of Copepoda life-history stages to climatic variability in a southern-European temperate estuary. Zool Stud 51:321–335

    Google Scholar 

  • Hack LA, Tremblay LA, Wratten SD et al (2008) Zinc sulfate and atrazine toxicity to the marine harpacticoid copepod Robertsonia propinqua. New Zeal J Mar Freshw Res 42:93–98. https://doi.org/10.1080/00288330809509939

    Article  CAS  Google Scholar 

  • Henderson RJ, Mackinlay EE, Hodgson P, Harwood JL (1990) Differential effects of the substituted pyridazinone herbicide Sandoz 9785 on lipid composition and biosynthesis in photosynthetic and non-photosynthetic marine microalgae. Fatty acid composition. J Exp Bot 41:729–736. https://doi.org/10.1093/jxb/41.6.723

    Article  CAS  Google Scholar 

  • Hochmuth JD, Asselman J, De Schamphelaere KAC (2014) Are interactive effects of harmful algal blooms and copper pollution a concern for water quality management? Water Res 60:41–53. Doi: https://doi.org/10.1016/j.watres.2014.03.041 http://www.fao.org/faostat. Accessed 29 Jan 2018

  • Hunting ER, Vonk JA, Musters CJM, Kraak MHS, Vijver MG (2016) Effects of agricultural practices on organic matter degradation in ditches. Sci Rep 6

  • ISO 10695 (2000) Water quality—determination of selected organic nitrogen and phosphorus compounds—gas chromatographic methods

  • Jonker MJ, Svendsen C, Bedaux JJM, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environ Toxicol Chem 24:2701–2713. https://doi.org/10.1897/04-431r.1

    Article  CAS  Google Scholar 

  • Keegstra K (2010) Plant cell walls. Futur Perspect Plant Biol 154:483–486. https://doi.org/10.1038/npg.els.0001682

    Article  CAS  Google Scholar 

  • Köck M, Farré M, Martínez E, Gajda-Schrantz K, Ginebreda A, Navarro A, Alda ML, Barceló D (2010) Integrated ecotoxicological and chemical approach for the assessment of pesticide pollution in the Ebro River delta (Spain). J Hydrol 383:73–82. https://doi.org/10.1016/j.jhydrol.2009.12.029

    Article  CAS  Google Scholar 

  • Kumar V, Kumar V, Upadhyay N, Sharma S (2015) Interactions of atrazine with transition metal ions in aqueous media: experimental and computational approach. 3 Biotech 5:791–798. https://doi.org/10.1007/s13205-015-0281-x

    Article  Google Scholar 

  • Lavens P, Sorgeloos P (1996) Manual on the production and use of live food for aquaculture. FAO Fish Tech Pap 361:295

    Google Scholar 

  • Lekkas T, Kolokythas G, Nikolaou A, Kostopoulou M, Kotrikla A, Gatidou G, Thomaidis NS, Golfinopoulos S, Makri C, Babos D, Vagi M, Stasinakis A, Petsas A, Lekkas DF (2004) Evaluation of the pollution of the surface waters of Greece from the priority compounds of list II, 76/464/EEC directive, and other toxic compounds. Environ Int 30:995–1007. https://doi.org/10.1016/j.envint.2004.04.001

    Article  CAS  Google Scholar 

  • Lepp N (1981) Effect of heavy metal pollution on plants: metals in the environment. In: MeIIanby K (ed) Pollution monitoring series. Applied Science Publishers, London, pp 1–33

    Google Scholar 

  • Letelier ME, Lepe AM, Faúndez M, Salazar J, Marín R, Aracena P, Speisky H (2005) Possible mechanisms underlying copper-induced damage in biological membranes leading to cellular toxicity. Chem Biol Interact 151:71–82. https://doi.org/10.1016/j.cbi.2004.12.004

    Article  CAS  Google Scholar 

  • Liebl (1995) Cell growth inhibitors (Chloroacetamides, Cabomothioates, Napropamide, Bensulide). In: Herbicide Action, vol 1. Purdue University, West Lafayette, pp 200–224

    Google Scholar 

  • Lister LJ, Svendsen C, Wright J, Hooper HL, Spurgeon DJ (2011) Modelling the joint effects of a metal and a pesticide on reproduction and toxicokinetics in Lumbricid earthworms. Environ Int 37:663–670. https://doi.org/10.1016/j.envint.2011.01.006

    Article  CAS  Google Scholar 

  • Liu H, Xiong M (2009) Comparative toxicity of racemic metolachlor and S-metolachlor to Chlorella pyrenoidosa. Aquat Toxicol 93:100–106. https://doi.org/10.1016/j.aquatox.2009.04.006

    Article  CAS  Google Scholar 

  • Loewe S, Muischnek H (1926) Effect of combinations: mathematical basis of the problem. Arch Für Exp Pathol und Pharmakologie 114

  • Lopez-Roldan R, Jubany I, Marti V et al (2013) Ecological screening indicators of stress and risk for the Llobregat river water. J Hazard Mater 263P:239–247. https://doi.org/10.1016/j.jhazmat.2013.07.008

    Article  CAS  Google Scholar 

  • Mahar AM, Watzin MC (2005) Effects of metal and organophospate mixtures on Ceriodaphia dubia survival and reproduction. Environ Toxicol Chem 24:1579–1586

    Article  CAS  Google Scholar 

  • Mai H, Cachot J, Brune J, Geffard O, Belles A, Budzinski H, Morin B (2012) Embryotoxic and genotoxic effects of heavy metals and pesticides on early life stages of Pacific oyster (Crassostrea gigas). Mar Pollut Bull 64:2663–2670. https://doi.org/10.1016/j.marpolbul.2012.10.009

    Article  CAS  Google Scholar 

  • Manimaran K, Karthikeyan P, Ashokkumar S, Ashok Prabu V, Sampathkumar P (2012) Effect of copper on growth and enzyme activities of marine diatom, Odontella mobiliensis. Bull Environ Contam Toxicol 88:30–37. https://doi.org/10.1007/s00128-011-0427-4

    Article  CAS  Google Scholar 

  • Martins M, Costa PM (2014) The comet assay in environmental risk assessment of marine pollutants: applications, assets and handicaps of surveying genotoxicity in non-model organisms. Mutagenesis 30:89–106. https://doi.org/10.1093/mutage/geu037

    Article  CAS  Google Scholar 

  • Mehler WT, Du J, Lydy MJ, You J (2011) Joint toxicity of a pyrethroid insecticide, cypermethrin, and a heavy metal, lead, to the benthic invertebrate Chironomus dilutus. Environ Toxicol Chem 30:2838–2845. https://doi.org/10.1002/etc.689

    Article  CAS  Google Scholar 

  • Neves M, Castro B, Vidal T et al (2015) Biochemical and populational responses of an aquatic bioindicator species, Daphnia longispina, to a commercial formulation of a herbicide (Primextra® Gold TZ) and its active ingredient (S-metolachlor). Ecol Indic 53:220–230. https://doi.org/10.1016/j.ecolind.2015.01.031

    Article  CAS  Google Scholar 

  • Nguyen-Ngoc H, Durrieu C, Tran-Minh C (2009) Synchronous-scan fluorescence of algal cells for toxicity assessment of heavy metals and herbicides. Ecotoxicol Environ Saf 72:316–320. https://doi.org/10.1016/j.ecoenv.2008.04.016

    Article  CAS  Google Scholar 

  • Nödler K, Licha T, Voutsa D (2013) Twenty years later—atrazine concentrations in selected coastal waters of the Mediterranean and the Baltic Sea. Mar Pollut Bull 70:112–118. https://doi.org/10.1016/j.marpolbul.2013.02.018

    Article  CAS  Google Scholar 

  • Nwani CD, Ifo CT, Nwamba HO, Ejere VC, Onyishi GC, Oluah SN, Ikwuagwu OE, Odo GE (2014) Oxidative stress and biochemical responses in the tissues of African catfish Clarias gariepinus juvenile following exposure to primextra herbicide. Drug Chem Toxicol 545:1–8. https://doi.org/10.3109/01480545.2014.947503

    Article  CAS  Google Scholar 

  • Nweke CO, Orji JC, Ahumibe NC (2015) Prediction of phenolic compounds and formulated glyphosate toxicity in binary mixtures using rhizobium species dehydrogenase activity. Adv Life Sci 5:27–38. https://doi.org/10.5923/j.als.20150502.01

    Article  Google Scholar 

  • Nys C, Asselman J, Hochmuth JD, Janssen CR, Blust R, Smolders E, de Schamphelaere KAC (2015) Mixture toxicity of nickel and zinc to Daphnia magna is noninteractive at low effect sizes but becomes synergistic at high effect sizes. Environ Toxicol Chem 34:1091–1102. https://doi.org/10.1002/etc.2902

    Article  CAS  Google Scholar 

  • OECD (2004) OECD Guidelines for testing of chemicals. OECD/OCDE 202. Daphnia sp. acute immobilisation test

  • Otto S, Vighi N, Zanin G et al (1999) Losses of terbuthylazine and alachlor from agricultural fields. Part II: mass balance and modelling. Fresenius Environ Bull 8:405–415

    CAS  Google Scholar 

  • Palma P, Köck-Schulmeyer M, Alvarenga P, Ledo L, Barbosa IR, López de Alda M, Barceló D (2014) Risk assessment of pesticides detected in surface water of the Alqueva reservoir (Guadiana basin, southern of Portugal). Sci Total Environ 488-489:208–219

    Article  CAS  Google Scholar 

  • Pantani C, Ghetti PF, Cavacini A, Muccioni P (1990) Acute toxicity of equitoxic binary-mixtures of some metals, surfactants and pesticides to the freshwater amphipod Gammarus italicus Goedm. Environ Technol 11:1143–1146

    Article  CAS  Google Scholar 

  • Pereira AS, Cerejeira MJ, Daam MA (2017) Toxicity of environmentally realistic concentrations of chlorpyrifos and terbuthylazine in indoor microcosms. Chemosphere 182:348–355. https://doi.org/10.1016/j.chemosphere.2017.05.032

    Article  CAS  Google Scholar 

  • Pinho GLL, Bianchini A (2010) Acute copper toxicity in the euryhaline copepod Acartia tonsa: implications for the development of an estuarine and marine biotic ligand model. Environ Toxicol Chem 29:1834–1840. https://doi.org/10.1002/etc.212

    Article  CAS  Google Scholar 

  • Rael LT, Thomas GW, Craun ML, Curtis CG, Bar-Or R, Bar-Or D (2004) Lipid peroxidation and the thiobarbituric acid assay: standardization of the assay when using saturated and unsaturated fatty acids. J Biochem Mol Biol 37:749–752. https://doi.org/10.5483/BMBRep.2004.37.6.749

    Article  CAS  Google Scholar 

  • Rippingale RJ, Payne MF (2001) Intensive cultivation of the calanoid copepod Gladioferens imparipes. Aquaculture 201:329–342. https://doi.org/10.1016/S0044-8486(01)00608-1

    Article  Google Scholar 

  • Ruas CBG, Carvalho C dos S, De Araújo HSS et al (2008) Oxidative stress biomarkers of exposure in the blood of cichlid species from a metal-contaminated river. Ecotoxicol Environ Saf 71:86–93. https://doi.org/10.1016/j.ecoenv.2007.08.018

    Article  CAS  Google Scholar 

  • Sibi G, Anuraag TS, Bafila G (2014) Copper stress on cellular contents and fatty acid profiles in Chlorella species. Online J Biol Sci 14:209–217. https://doi.org/10.3844/ojbssp.2014.209.217

    Article  Google Scholar 

  • Sicko-Goad L, Evans M, Lazinsky D et al (1989a) Effects of chlorinated benzenes on diatom fatty acid composition and quantitative morphology. IV. Pentachlorobenzene and comparison with trichlorobenzene isomers. Arch Environ Contam Toxicol 18:656–668

    Article  CAS  Google Scholar 

  • Sicko-Goad L, Hall J, Lazinsky D, Simmons MS (1989b) Effects of chlorinated benzenes on diatom fatty acid composition and quantitative morphology. II. 1,3,5-Trichlorobenzene. Arch Environ Contam Toxicol 18:638–646

    Article  CAS  Google Scholar 

  • Sicko-Goad L, Hall J, Lazinsky D, Simmons MS (1989c) Effects of chlorinated benzenes on diatom fatty acid composition and quantitative morphology. III. 1,2,3-Trichlorobenzene. Arch Environ Contam Toxicol 18:647–655

    Article  CAS  Google Scholar 

  • Sicko-Goad L, Lazinsky D, Hall J, Simmons MS (1989d) Effects of chlorinated benzenes on diatom fatty acid composition and quantitative morphology. I. 1,2,4-Trichlorobenzene. Arch Environ Contam Toxicol 18:629–637

    Article  CAS  Google Scholar 

  • Spoljaric D, Cipak A, Horvatic J, Andrisic L, Waeg G, Zarkovic N, Jaganjac M (2011) Endogenous 4-hydroxy-2-nonenal in microalga Chlorella kessleri acts as a bioactive indicator of pollution with common herbicides and growth regulating factor of hormesis. Aquat Toxicol 105:552–558. https://doi.org/10.1016/j.aquatox.2011.08.007

    Article  CAS  Google Scholar 

  • Steinback KE, Mcintoshtt LEE, Bogoradt L, Arntzen CJ (1981) Gene product. Proc Natl Acad Sci U S A 78:7463–7467

    Article  CAS  Google Scholar 

  • Stringer TJ, Glover CN, Keesing V, Northcott GL, Tremblay LA (2012) Development of a harpacticoid copepod bioassay: selection of species and relative sensitivity to zinc, atrazine and phenanthrene. Ecotoxicol Environ Saf 80:363–371. https://doi.org/10.1016/j.ecoenv.2012.04.008

    Article  CAS  Google Scholar 

  • Sun L, Zha J, Wang Z (2009) Interactions between estrogenic chemicals in binary mixtures investigated using vitellogenin induction and factorial analysis. Chemosphere 75:410–415. https://doi.org/10.1016/j.chemosphere.2008.11.083

    Article  CAS  Google Scholar 

  • Teisseire H, Couderchet M, Vernet G (1999) Phytotoxicity of diuron alone and in combination with copper or folpet on duckweed (Lemna minor). Environ Pollut 106:39–45. https://doi.org/10.1016/S0269-7491(99)00066-4

    Article  CAS  Google Scholar 

  • Thakkar M, Randhawa V, Wei L (2013) Comparative responses of two species of marine phytoplankton to metolachlor exposure. Aquat Toxicol 126:198–206. https://doi.org/10.1016/j.aquatox.2012.10.002

    Article  CAS  Google Scholar 

  • Undabeytia T, Cheshire MV, McPhail D (1996) Interaction of the herbicide glyphosate with copper in humic complexes. Chemosphere 32:1245–1250. https://doi.org/10.1016/0045-6535(96)00036-7

    Article  CAS  Google Scholar 

  • Uwizeyimana H, Wang M, Chen W, Khan K (2017) The eco-toxic effects of pesticide and heavy metal mixtures towards earthworms in soil. Environ Toxicol Pharmacol 55:20–29. https://doi.org/10.1016/j.etap.2017.08.001

    Article  CAS  Google Scholar 

  • Vasconcelos RP, Reis-Santos P, Maia A, Ruano M, Costa MJ, Cabral HN (2011) Trace metals (Cu, Zn, Cd and Pb) in juvenile fish from estuarine nurseries along the Portuguese coast. Sci Mar 75:155–162. https://doi.org/10.3989/scimar.2011.75n1155

    Article  CAS  Google Scholar 

  • Waters Corporation (2002) Environmental and agrochemical applications notebook. Waters Corporation. 720000421 EN, Rev. 3, 02/02

  • Weed Science Society of America (1994) Herbicide handbook, 7th edn. Weed Science Society of America, Champaign

    Google Scholar 

  • Wenneker M, Beltman WHJ, De Werd H et al (2010) Quantifying point source entries of pesticides in surface waters. Asp Appl Biol 99:69–74

    Google Scholar 

  • WHO (2003) Terbuthylazine (TBA) in drinking-water: background document for development of WHO guidelines for drinking-water quality. In: World Health Organization, Geneva (ed) Health criteria and other supporting information, pp. 1–8

Download references

Acknowledgements

We thank A. C. Garcia and P. Barría for the significant assistance during sampling campaigns, N. De Saeyer for performing the atomic absorption spectrophotometric and gas-liquid chromatography-mass spectrometric analyses, and D. Van Gansbeke for his assistance with the FA analyses.

Funding

This work was funded through a MARES Grant. MARES is a Joint Doctoral program selected under Erasmus Mundus coordinated by Ghent University (FPA 2011-0016) (www.mares-eu.org). This study had also the support of Portuguese Foundation for Science and Technology (FCT, Portugal), through the strategic project UID/MAR/04292/2013, granted to MARE, and UID/AMB//50017/2013, granted to CESAM. A. M. M. Gonçalves also thanks FCT for financial support through the post-doctoral grant SFRH/BPD/97210/2013, co-funded by the Human Potential Operational Programme (National Strategic Reference Framework 2007-2013), European Social Fund (EU), and the program POPH/FSE. The FA analyses were supported by FWO-Flanders and the Special Research Fund—Ghent University in the form of research grant 31523814 “Fatty acids as dietary tracers in benthic food webs” and research project 01N2816 “Energy transfer at the basis of marine food webs in a changing world” awarded to M. De Troch.

Author information

Authors and Affiliations

  1. IMAR-CMA and MARE, Faculty of Science and Technology, University of Coimbra, 3004-517, Coimbra, Portugal

    Valentina Filimonova, João C. Marques & Ana M. M. Gonçalves

  2. Department of Biology and CESAM, University of Aveiro, 3810-193, Aveiro, Portugal

    Valentina Filimonova, Fernando Gonçalves & Ana M. M. Gonçalves

  3. Faculty of Science, Biology Department, Marine Biology, Ghent University, Krijgslaan 281-S8, 9000, Ghent, Belgium

    Valentina Filimonova & Marleen De Troch

  4. Faculty of Bioscience Engineering, GhenToxLab, Ghent University, Jozef Plateaustraat 22, 9000, Ghent, Belgium

    Charlotte Nys & Karel A. C. De Schamphelaere

Authors
  1. Valentina Filimonova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charlotte Nys
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karel A. C. De Schamphelaere
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fernando Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. João C. Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana M. M. Gonçalves
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marleen De Troch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valentina Filimonova.

Additional information

Responsible editor: Cinta Porte

Electronic supplementary material

ESM 1

(DOC 583 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Filimonova, V., Nys, C., De Schamphelaere, K.A.C. et al. Ecotoxicological and biochemical mixture effects of an herbicide and a metal at the marine primary producer diatom Thalassiosira weissflogii and the primary consumer copepod Acartia tonsa. Environ Sci Pollut Res 25, 22180–22195 (2018). https://doi.org/10.1007/s11356-018-2302-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-2302-x

Keywords

Search

Navigation