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Pacific oyster (Crassostrea gigas) hemocyte are not affected by a mixture of pesticides in short-term in vitro assays

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Abstract

Pesticides are frequently detected in estuaries among the pollutants found in estuarine and coastal areas and may have major ecological consequences. They could endanger organism growth, reproduction, or survival. In the context of high-mortality outbreaks affecting Pacific oysters, Crassostrea gigas, in France since 2008, it appears of importance to determine the putative effects of pesticides on oyster susceptibility to infectious agents. Massive mortality outbreaks reported in this species, mainly in spring and summer, may suggest an important role played by the seasonal use of pesticides and freshwater input in estuarine areas where oyster farms are frequently located. To understand the impact of some pesticides detected in French waters, their effects on Pacific oyster hemocytes were studied through short-term in vitro experiments. Bivalve immunity is mainly supported by hemocytes eliminating pathogens by phagocytosis and producing compounds including lysosomal enzymes and antimicrobial molecules. In this study, oyster hemocytes were incubated with a mixture of 14 pesticides and metaldehyde alone, a molecule used to eliminate land mollusks. Hemocyte parameters including dead/alive cells, nonspecific esterase activities, intracytoplasmic calcium, lysosome number and activity, and phagocytosis were monitored by flow cytometry. No significant effect of pesticides tested at different concentrations was reported on oyster hemocytes maintained in vitro for short-term periods in the present study. It could be assumed that these oyster cells were resistant to pesticide exposure in tested conditions and developing in vivo assays appears as necessary to better understand the effects of pollutants on immune system in mollusks.

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References

  • Alvarez MR, Friedl FE (1992) Effects of a fungicide on in vitro hemocyte viability, phagocytosis and attachment in the American oyster, Crassostrea virginica. Aquaculture 107:135–140

    Article  CAS  Google Scholar 

  • Anguiano G, Llera-Herrera R, Rojas E, Vazquez-Boucard C (2007) Subchronic organismal toxicity, cytotoxicity, genotoxicity, and feeding response of Pacific oyster (Crassostrea gigas) to lindane (gamma-HCH) exposure under experimental conditions. Environ Toxicol Chem 26:2192–2197

    Article  CAS  Google Scholar 

  • Aton E, Renault T, Gagnaire B, Thomas-Guyon H, Cognard C, Imbert N (2006) A flow cytometric approach to study intracellular-free Ca2+ in Crassostrea gigas haemocytes. Fish Shellfish Immunol 20:493–502

    Article  CAS  Google Scholar 

  • Baier-Anderson C, Anderson RS (2000) The effects of chlorothalonil on oyster hemocyte activation: phagocytosis, reduced pyridine nucleotides, and reactive oxygen species production. Environ Res 83:72–78

    Article  CAS  Google Scholar 

  • Banerjee BD, Koner BC, Ray A (1996) Immunotoxicity of pesticides: perspectives and trends. Indian J Exp Biol 34:723–733

    CAS  Google Scholar 

  • Banerjee BD, Seth V, Ahmed RS (2001) Pesticide-induced oxidative stress: perspectives and trends. Rev Environ Health 16:1–40

    Article  CAS  Google Scholar 

  • Bretaud S, Toutant JP, Saglio P (2000) Effects of carbofuran, diuron, and nicosulfuron on acetylcholinesterase activity in goldfish (Carassius auratus). Ecotoxicol Environ Saf 47:117–124

    Article  CAS  Google Scholar 

  • Cajaraville MP, Olabarrieta I, Marigomez I (1996) In vitro activities in mussel hemocytes as biomarkers of environmental quality: a case study in the Abra Estuary (Biscay Bay). Ecotoxicol Environ Saf 35:253–260

    Article  CAS  Google Scholar 

  • Canty MN, Hagger JA, Moore RTB, Cooper L, Galloway TS (2007) Sublethal impact of short term exposure to the organophosphate pesticide azamethiphos in the marine mollusc Mytilus edulis. Mar Pollut Bull 54:396–402

    Article  CAS  Google Scholar 

  • Cheng TC (1981) Bivalves. In: Ratcliffe A, Rowley AF (eds) Invertebrate blood cells. Academic, London, pp 233–299

    Google Scholar 

  • Coles JA, Pipe RK (1994) Phenoloxidase activity in the haemolymph and haemocytes of the marine mussel Mytilus edulis. Fish Shellfish Immunol 4:337–352

    Article  Google Scholar 

  • Collin H, Meistertzheim A-L, David E, Moraga D, Boutet I (2010) Response of the Pacific oyster Crassostrea gigas, Thunberg 1793, to pesticide exposure under experimental conditions. J Exp Biol 213:4010–4017

    Article  Google Scholar 

  • Dai L, Wang W, Dong X, Hu R, Nan X (2011) Molluscicidal activity of cardiac glycosides from Nerium indicum against Pomacea canaliculata and its implications for the mechanisms of toxicity. Environ Toxicol Pharmacol 32:226–232

    CAS  Google Scholar 

  • EFSA (European Food Safety Authority) (2010) Scientific Opinion on the increased mortality events in Pacific oysters, Crassostrea gigas. EFSA J 8(11):1894

    Google Scholar 

  • Feng SY (1988) Cellular defense mechanisms of oysters and mussels. Am Fish Soc Spec Publ 18:153–168

    Google Scholar 

  • Ford SE, Paillard C (2007) Repeated sampling of individual bivalve mollusks I: intraindividual variability and consequences for haemolymph constituents of the Manila clam, Ruditapes philippinarum. Fish Shellfish Immunol 23:280–291

    Article  CAS  Google Scholar 

  • Fournier M, Chevalier G, Nadeau D, Trottier B, Krzystyniak K (1988) Virus-pesticide interactions with murine cellular immunity after sublethal exposure to dieldrin and aminocarb. J Toxicol Environ Health 25:103–118

    Article  CAS  Google Scholar 

  • Fournier M, Cyr D, Blakley B, Boermans H, Brousseau P (2000) Phagocytosis as a biomarker of immunotoxicity in wildlife species exposed to environmental xenobiotics. Amer Zool 40:412–420

    Article  CAS  Google Scholar 

  • Gagnaire B, Renault T, Bouilly K, Lapegue S, Thomas-Guyon H (2003) Study of atrazine effects on Pacific oyster, Crassostrea gigas, haemocytes. Curr Pharm Des 9:193–199

    Article  CAS  Google Scholar 

  • Gagnaire B, Thomas-Guyon H, Burgeot T, Renault T (2006a) Pollutant effects on Pacific oyster, Crassostrea gigas (Thunberg), hemocytes: screening of 23 molecules using flow cytometry. Cell Biol Toxicol 22:1–14

    Article  CAS  Google Scholar 

  • Gagnaire B, Frouin H, Moreau K, Thomas-Guyon H, Renault T (2006b) Effects of temperature and salinity on haemocyte activities of the Pacific oyster, Crassostrea gigas (Thunberg). Fish Shellfish Immunol 20:536–547

    Article  CAS  Google Scholar 

  • Gagnaire B, Gay M, Huvet A, Daniel J-Y, Saulnier D, Renault T (2007) Combination of a pesticide exposure and a bacterial challenge: in vivo effects on immune response of Pacific oyster, Crassostrea gigas (Thunberg). Aquat Toxicol 84:92–102

    Article  CAS  Google Scholar 

  • Galloway TS, Depledge MH (2001) Immunotoxicity in invertebrates: measurement and ecotoxicological relevance. Ecotoxicology 10:5–23

    Article  CAS  Google Scholar 

  • Galloway T, Handy R (2003) Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12:345–363

    Article  CAS  Google Scholar 

  • Greco L, Pellerin J, Capri E, Garnerot F, Louis S, Fournier M, Sacchi A, Fusi M, Lapointe D, Couture P (2011) Physiological effects of temperature and a herbicide mixture on the soft-shell clam Mya arenaria (Mollusca, Bivalvia). Environ Toxicol Chem 30:132–141

    Article  CAS  Google Scholar 

  • Hyne RV, Aistrope M (2008) Calibration and field application of a solvent-based cellulose membrane passive sampling device for the monitoring of polar herbicides. Chemosphere 71:611–620

    Article  CAS  Google Scholar 

  • Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ (2005) Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environ Toxicol Chem 24:238–248

    Article  CAS  Google Scholar 

  • Kim Y, Powell EN, Wade TL, Presley BJ (2008) Relationship of parasites and pathologies to contaminant body burden in sentinel bivalves: NOAA Status and Trends “Mussel Watch” Program. Mar Environ Res 65:101–127

    Article  CAS  Google Scholar 

  • Knauert S, Escher B, Singer H, Hollender J, Knauer K (2008) Mixture toxicity of three photosystem II inhibitors (atrazine, isoproturon, and diuron) toward photosynthesis of freshwater phytoplankton studied in outdoor mesocosms. Environ Sci Technol 42:6424–6430

    Article  CAS  Google Scholar 

  • Kouassi, Edouard, Ayotte, Pierre, Roy, Raynald, Fournier, Michel, Revillard, Jean-Pierre (2001) BISE, Effets des contaminants de l’environnement sur le système immunitaire. http://www.inspq.qc.ca/bise/post/2001/04/20/Effets-des-contaminants-de-le28099environnement-sur-le-systeme-immunitaire.aspx

  • Lanyi K, Dinya Z (2003) Photodegradation study of some triazine-type herbicides. Microchem J 75:1–13

    Article  CAS  Google Scholar 

  • Larson KG, Roberson BS, Hetrick FM (1989) Effect of environmental pollutants on the chemiluminescence of hemocytes from the American oyster Crassostrea virginica. Dis Aquat Org 6:131–136

    Article  Google Scholar 

  • Luna-Acosta A, Kanan R, Le Floch S, Huet V, Pineau P, Bustamante P, Thomas-Guyon H (2011) Enhanced immunological and detoxification responses in Pacific oysters, Crassostrea gigas, exposed to chemically dispersed oil. Water Res 45:4103–4118

    CAS  Google Scholar 

  • Masuda M, Satsuma K, Sato K (2012) An environmental fate study of methoxychlor using water-sediment model system. Biosci Biotechnol Biochem 76:73–77

    Article  CAS  Google Scholar 

  • Menin A, Ballarin L, Bragadin M, Cima F (2008) Immunotoxicity in ascidians: antifouling compounds alternative to organotins—II. The case of Diuron and TCMS pyridine. J Environ Sci Health B 43:644–654

    Article  CAS  Google Scholar 

  • Munaron D, Dubernet JF, Delmas F, Stanisière JY, Scribe P (2006) Assessment of the quantities of herbicides and nutrients brought down by the river Charente to the coast and modelling of the dispersion of atrazine in the Marennes-Oléron bay. http://cemadoc.irstea.fr/cemoa/PUB00022983

  • Neuwoehner J, Zilberman T, Fenner K, Escher BI (2010) QSAR-analysis and mixture toxicity as diagnostic tools: influence of degradation on the toxicity and mode of action of diuron in algae and daphnids. Aquat Toxicol 97:58–67

    Article  CAS  Google Scholar 

  • Ordás MC, Ordás A, Beloso C, Figueras A (2000) Immune parameters in carpet shell clams naturally infected with Perkinsus atlanticus. Fish Shellfish Immunol 10:597–609

    Article  Google Scholar 

  • Patetsini E, Dimitriadis VK, Kaloyianni M (2013) Biomarkers in marine mussels, Mytilus galloprovincialis, exposed to environmentally relevant levels of the pesticides, chlorpyrifos and penoxsulam. Aquat Toxicol 126:338–345

    Article  CAS  Google Scholar 

  • Pesce S, Lissalde S, Lavieille D, Margoum C, Mazzella N, Roubeix V, Montuelle B (2010) Evaluation of single and joint toxic effects of diuron and its main metabolites on natural phototrophic biofilms using a pollution-induced community tolerance (PICT) approach. Aquat Toxicol 99:492–499

    Article  CAS  Google Scholar 

  • Renault T (2011) Effects of pesticides on marine bivalves: what do we know and what do we need to know? In: Stoytcheva M (ed) Pesticides in the modern world—risks and benefits. InTech; October 3, 2011

  • Ross MW, Managing HIV (1996) Part 3: mechanisms of disease. 3.8 How psychosocial aspects of HIV infection can affect health. Med J Aust 164:235–237

    CAS  Google Scholar 

  • Saglio P, Bretaud S, Rivot E, Olsén KH (2003) Chemobehavioral changes induced by short-term exposures to prochloraz, nicosulfuron, and carbofuran in goldfish. Arch Environ Contam Toxicol 45:515–524

    Article  CAS  Google Scholar 

  • Savage C, Thrush SF, Lohrer AM, Hewitt JE (2012) Ecosystem services transcend boundaries: estuaries provide resource subsidies and influence functional diversity in coastal benthic communities. PLoS One 7:e42708

    Article  CAS  Google Scholar 

  • Segarra A, Pépin JF, Arzul I, Morga B, Faury N, Renault T (2010) Detection and description of a particular Ostreid herpes virus 1 genotype associated with massive mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus Res 153:92–99

    Article  CAS  Google Scholar 

  • Sørensen SR, Bending GD, Jacobsen CS, Walker A, Aamand J (2003) Microbial degradation of isoproturon and related phenyl urea herbicides in and below agricultural fields. FEMS Microbiol Ecol 45:1–11

    Article  Google Scholar 

  • Tanguy A, Boutet I, Laroche J, Moraga D (2005) Molecular identification and expression study of differentially regulated genes in the Pacific oyster Crassostrea gigas in response to pesticide exposure. FEBS J 272:390–403

    Article  CAS  Google Scholar 

  • Van Loveren H, Ross PS, Osterhaus AD, Vos JG (2000) Contaminant-induced immunosuppression and mass mortalities among harbor seals. Toxicol Lett 112–113:319–324

    Article  Google Scholar 

  • Vargha M, Takáts Z, Márialigeti K (2005) Degradation of atrazine in a laboratory scale model system with Danube river sediment. Water Res 39:1560–1568

    Article  CAS  Google Scholar 

  • Vial T, Nicolas B, Descotes J (1996) Clinical immunotoxicity of pesticides. J Toxicol Environ Health 48:215–229

    Article  CAS  Google Scholar 

  • Zhang G, Fang X, Guo X, Li L, Luo R, Xu F et al (2012) The oyster genome reveals stress adaptation and complexity of shell formation. Nature 490:49–54

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partially funded through the EU project BIVALIFE (26 61 57) and the Poitou Charentes Region. Thank you to Valerie Barbosa-Solomieu for English editing.

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Authors and Affiliations

  1. Ifremer (Institut Français pour la Recherche et l’Exploitation de la Mer), Unité Santé Génétique et Microbiologie des Mollusques, Laboratoire de Génétique et Pathologie des Mollusques Marins, 17390, La Tremblade, France

    Pierrick Moreau & Tristan Renault

  2. Ifremer (Institut Français pour la Recherche et l’Exploitation de la Mer), Unité Biogéochemie et Ecotoxicologie, rue de l’Ile d’Yeu, 21105, 44311, Nantes, France

    Thierry Burgeot

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  1. Pierrick Moreau
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  2. Thierry Burgeot
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Correspondence to Pierrick Moreau.

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Responsible editor: Philippe Garrigues

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Moreau, P., Burgeot, T. & Renault, T. Pacific oyster (Crassostrea gigas) hemocyte are not affected by a mixture of pesticides in short-term in vitro assays. Environ Sci Pollut Res 21, 4940–4949 (2014). https://doi.org/10.1007/s11356-013-1931-3

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  • DOI: https://doi.org/10.1007/s11356-013-1931-3

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