Skip to main content

Advertisement

SpringerLink
Log in

Continuous Exposure to Microplastics Does Not Cause Physiological Effects in the Cultivated Mussel Perna perna

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The environmental impact of microplastics is a challenging theme, especially under realistic experimental conditions. We investigated physiological responses to 0.1–1.0 μm PVC particles intake by the mussel Perna perna after a relative long-term exposure (90 days) at a less extreme concentration compared with previous studies (0.125 g/L). Microplastic intake was inferred by the presence of PVC in the feces of mussels, and physiological damages were assessed through ingestion rate, assimilation efficiency, growth rate, cellular and molecular biomarkers (lysosomal integrity, lipid peroxidation, and DNA damage), and condition index. All physiological responses showed nonsignificant effects of the microplastics on the exposed mussels. We suggest that, despite the experimental concentration of microplastics, mussels were able to acclimate to the exposure through their abilities for long-term recovery and tolerance to stresses. These data have positive implications for environmental health and in terms of human food resource because mussel farming is a worldwide practice that heavily relies on plastic materials, increasing the chances of microplastic exposure and mussels contamination.

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

  • ABIPLAST. Associação brasileira da indústria do plástico (2012). http://abiplast.org.br. Accessed 15 Jan 2013

  • Andrady AL (2011) Microplastics in the marine environment. Mar Pollut Bull 62:1596–1605

    Article  CAS  Google Scholar 

  • Arthur C, Baker J, Bamford H (eds) (2009) Proceedings of the international research workshop on the occurrence, effects and fate of microplastic marine debris (NOAA Technical Memorandum NOS-OR&R-30). NOAA, Silver Spring

  • Avio CG, Gorbi S, Milan M, Benedetti M, Fattorini D, d’Errico G, Pauletto M, Bargelloni L, Regoli F (2015) Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut 198:211–222

    Article  CAS  Google Scholar 

  • Baird RH (1958) Measurement of condition in mussels and oysters. J Cons Perm Inter Explor Mer 23:249–257

    Article  Google Scholar 

  • Barnes DKA, Galgani F, Thompson RC, Barlaz M (2009) Accumulation and fragmentation of plastic debris in global environments. Philos Trans R Soc Lond 364:1985–1998

    Article  CAS  Google Scholar 

  • Bayne BL, Hawkins AJS, Navarro E (1987) Feeding and digestion by mussel Mytilus edulis L. (Bivalvia: Mollusca) in mixtures of silt and algal cells at low concentrations. J Exp Mar Biol Ecol 111:1–22

    Article  Google Scholar 

  • Bayne BL, Iglesias JIP, Hawkins AJS, Navarro E, Heral M, Deslous-Paoli JM (1993) Feeding behaviour of the mussel, Mytilus edulis: responses to variations in quality and organic content of the séston. J Mar Biol Assoc 73:813–829

    Article  Google Scholar 

  • Besseling E, Wegner A, Foekema EM, Heuvel-Greve MJ, Koelmans AA (2013) Effects of microplastic on fitness and PCB bioaccumulation by the lugworm Arenicola marina (L.). Environ Sci Technol 47:593–600

    Article  CAS  Google Scholar 

  • Blakley BR (1985) The effect of cadmium chloride on the immune response in mice. Can J Comp Med 49:104–108

    CAS  Google Scholar 

  • Bocchetti R, Regoli F (2006) Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65:913–921

    Article  CAS  Google Scholar 

  • Boerger CM, Lattin GL, Moore SL, Moore CJ (2010) Plastic ingestion by planktivorous fishes in the North Pacific Central Gyre. Mar Pollut Bull 60:2275–2278

    Article  CAS  Google Scholar 

  • Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC (2008) Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L.). Environ Sci Technol 42:5026–5031

    Article  CAS  Google Scholar 

  • Browne MA, Crump P, Niven SJ, Teuten E, Tonkin A, Galloway T, Thompson R (2011) Accumulation of microplastics on shorelines worldwide: sources and sinks. Environ Sci Technol 45:9175–9179

    Article  CAS  Google Scholar 

  • Browne MA, Niven SJ, Galloway TS, Rowland SJ, Thompson RC (2013) Microplastic moves pollutants and additives to worms, reducing functions linked to health and biodiversity. Curr Biol 23:2388–2392

    Article  CAS  Google Scholar 

  • Cole M, Lindeque P, Halsband C, Galloway T (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bull 62:2588–2597

    Article  CAS  Google Scholar 

  • Cole M, Lindeque P, Fileman E, Halsband C, Goodhead RM, Morger J, Galloway T (2013) Microplastic ingestion by zooplankton. Environ Sci Technol 47:6646–6655

    Article  CAS  Google Scholar 

  • Cole M, Lindeque P, Fileman E, Halsband C, Galloway TS (2015) The impact of polystyrene microplastics on feeding, function and fecundity in the marine copepod Calanus helgolandicus. Environ Sci Technol 49:1130–1137

    Article  CAS  Google Scholar 

  • Conover RJ (1996) Assimilation of organic matter by zooplâncton. Limnol Oceanogr 11:338–345

    Article  Google Scholar 

  • Di Giulio RT, Scanlon PF (1985) Effects of cadmium ingestion and food restriction on energy metabolism and tissue metal concentrations in mallard ducks (Arias platyrhynchos). Environ Res 37:433–444

    Article  Google Scholar 

  • Eriksen M, Lebreton LCM, Carson HS, Thiel M, Moore CJ, Borerro JC, Galgani F, Ryan PG, Reisser J (2014) Plastic pollution in the world’s oceans: more than 5 trillion plastic pieces weighing over 250,000 tons float at sea. PLoS ONE 9:e1111913

    Google Scholar 

  • Erikson C, Burton H (2003) Origins and biological accumulation of plastic particles in fur seals from Macquarie Island. Ambio 32:380–384

    Article  Google Scholar 

  • FAO (Food and Agriculture Organization of the United Nations) (2011) World aquaculture 2010. Technical Paper. No. 500/1 2011. FAO, Rome

  • FAO (Food and Agriculture Organization of the United Nations) (2014) The state of world fisheries and aquaculture. FAO, Rome

    Google Scholar 

  • Fernandes FC, Souza RCCL, Junqueira AOR, Rapagnã LC, Ramos AB (2008) Distribuição Mundial e o Impacto de sua Introdução no Brasil. In: Junior CR, Weber LI, Conceição MB (eds) O mexilhão Perna perna (L.) biologia, ecologia e aplicações, 1st edn. Interciência, Rio de Janeiro, pp 25–30

    Google Scholar 

  • Ferreira JF, Magalhães ARM (2010) Cultivo de Mexilhões, Instruções e Ajuda. http://www.cca.ufsc.br/~jff/disciplinas/cultivodemoluscos/pdf/Cultivo%20de%20Mexilhoes%202003-1.pdf. Accessed 28 Feb 2010

  • Fisner M, Taniguchi S, Majer AP, Bícego MC, Turra A (2013) Concentration and composition of polycyclic aromatic hydrocarbons (PAHs) in plastic pellets: implications for small-scale diagnostic and environmental monitoring. Mar Pollut Bull 76:349–354

    Article  CAS  Google Scholar 

  • Foekma EM, Gruijter C, Mergia MT, van Franeker JA, Murk TJ, Koelmans AA (2013) Plastic in North Sea fish. Environ Sci Technol 47:8818–8824

    Article  Google Scholar 

  • Foster-Smith RL (1975) The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderrna edule (L.) and Venerupis pullastra (Montagu). J Exp Mar Biol Ecol 7:1–22

    Article  Google Scholar 

  • Gagné F, Trottier S, Blaise C, Sproull J, Ernst B (1995) Genotoxicity of sediment extracts obtained in the vicinity creosote-treated wharf to rainbow trout hapocyties. Toxicol Lett 78:175–182

    Article  Google Scholar 

  • Gallagher A, Rees A, Rowe R, Stevens J, Wright P (2015) Microplastics in the Solent estuarine complex, UK: an initial assessment. Mar Pollut Bull 102:243–249

    Article  Google Scholar 

  • GESAMP (IMO/FAO/UNESCO-IOC/UNIDO/WMO/IAEA/UN/UNEP/UNDP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection) (2015) Sources, fate and effects of microplastics in the marine environment: a global assessment (Rep. Stud. GESAMP No. 90.). International Maritime Organization, London

  • GESAMP (IMO/FAO/UNESCO-IOC/UNIDO/WMO/IAEA/UN/UNEP/UNDP Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection) (2016) Sources, fate and effects of microplastics in the marine environment: Part 2 of a global assessment (Rep. Stud. GESAMP No. 93.). International Maritime Organization, London

  • Graham ER, Thompson JT (2009) Deposit- and suspension-feeding sea cucumbers (Echinodermata) ingest plastic fragments. J Exp Mar Biol Ecol 368:22–29

    Article  Google Scholar 

  • Green DS (2016) Effects of microplastics on European flat oysters, Ostrea edulis and their associated benthic communities. Environ Pollut 216:95–103

    Article  CAS  Google Scholar 

  • Gregory MR, Andrady AL (2003) Plastics in the marine environment. In: Andrady AL (ed) Plastics and the environment. Wiley, New Jersey, pp 379–401

    Google Scholar 

  • Hamdoun AM, Cheney DP, Cherr GN (2003) Phenotypic plasticity of Hsp70 and Hsp70 gene expression in the pacific oyster (Crassostrea gigas): implications for thermal limits and induction of thermal tolerance. Biol Null 205:160–169

    CAS  Google Scholar 

  • Hämer J, Gutow L, Köhler A, Saborowski R (2014) Fate of microplastics in the marine isopod Idotea emarginata. Environ Sci Technol 48:13451–13458

    Article  Google Scholar 

  • Held P (2015) An introduction to reactive oxygen species: Measurement of ROS in cells. Biotek, Vermont

    Google Scholar 

  • Helmuth B (2009) From cells to coastlines: how can we use physiology to forecast the impacts of climate change? J Exp Biol 212:753–760

    Article  Google Scholar 

  • Helmuth BST, Hofmann GE (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Bio Bull 201:374–384

    Article  CAS  Google Scholar 

  • Henriques MB (2004) Resistência do mexilhão Perna perna (Linnaeus, 1758) proveniente de bancos naturais da baixada santista, a variação de temperatura, salinidade, tempo de exposição ao ar e determinação da incidência de parasitismo. Dissertation, São Paulo State University

  • Hirai H, Takada H, Ogata Y, Yamashita R, Mizukawa K, Saha M, Kwan C, Moore C, Gray H, Laursen D, Zettler ER, Farrington JW, Reddy CM, Peacock EE, Ward M (2011) Organic micropollutants in marine plastics from the open ocean and remote and urban beaches. Mar Pollut Bull 62:1683–1692

    Article  CAS  Google Scholar 

  • Hunt HL, Scheibling RE (2001) Predicting wave dislodgement of mussels: variation in attachment strength with body size, habitat, and season. Mar Ecol Prog Ser 213:157–164

    Article  Google Scholar 

  • Imhof HK, Laforsch C (2016) Hazardous or not—are adult and juvenile individuals of Potamopyrgus antipodarum affected by non-buoyant microplastic particles? Environ Pollut 218:383–391

    Article  CAS  Google Scholar 

  • Itziou A, Kaloyianni M, Dimitriadis VK (2011) Effects of organic contaminants in reactive oxygen species, protein carbonylation and DNA damage on digestive gland and heamolymph of land snails. Chemosphere 85:1101–1107

    Article  CAS  Google Scholar 

  • Jena NR (2012) DNA damage by reactive species: mechanisms, mutation and repair. J Biosci 37:503–517

    Article  CAS  Google Scholar 

  • Jørgensen CB (1981) Feeding and cleaning mechanisms in the suspension feeding bivalve Mytilus edulis. Mar Biol 65:159–163

    Article  Google Scholar 

  • Li J, Qu X, Su L, Zhang W, Yang D, Kolandhasamy P, Li D, Shi H (2016) Microplastics in mussels along the coastal waters of China. Environ Pollut 214:177–184

    Article  CAS  Google Scholar 

  • Lithner D, Damberg J, Dave G, Larsson A (2009) Leachates from plastic consumer products—screening for toxicity with Daphnia magna. Chemosphere 74:1195–1200

    Article  CAS  Google Scholar 

  • Lithner D, Larsson A, Dave G (2011) Environmental and health hazard ranking and assessment of plastic polymers based on chemical composition. Sci Total Environ 409:3309–3324

    Article  CAS  Google Scholar 

  • Lowe DM, Fossato VU, Depledge MH (1995) Contaminant-induced lysosomal membrane damage in blood cells of mussels Mytilus galloprovincialis from Venice lagoon: as in vitro study. Mar Ecol Prog Ser 129:189–196

    Article  Google Scholar 

  • Lu Y, Zhang Y, Deng Y, Jiang W, Zhao Y, Geng J, Ding L, Ren H (2016) Uptake and accumulation of polystyrene microplastics in zebrafish (Danio rerio) and toxic effects in liver. Environ Sci Technol 50:4054–4060

    Article  CAS  Google Scholar 

  • Lushchak VI (2016) Contaminant-induced oxidative stress in fish: a mechanism approach. Fish Physiol Biochem 42:711–747

    Article  CAS  Google Scholar 

  • Marques HLA (1988) Considerações ecológicas sobre o mexilhão Perna perna (Linnaeus, 1758) em bancos naturais da região de Ubatuba, São Paulo, Brasil. Dissertation, University of Campinas, Campinas

  • Mathalon A, Hill P (2014) Microplastic fibers in the intertidal ecosystem surrounding Halifax Harbor, Nova Scotia. Mar Pollut Bull 81:69–79

    Article  CAS  Google Scholar 

  • Moore MN, Allen JI, McVeigh A (2006) Environmental prognostics: an integrated model supporting lysosomal stress responses as predictive biomarkers of animal health status. Mar Environ Res 61:278–304

    Article  CAS  Google Scholar 

  • Moreira FT (2011) Ecotoxicological consequences of novel biocides in the discharge of seawater used in cooling systems from coastal buildings, Dissertation, University of Sydney

  • Murray F, Cowie PR (2011) Plastic contamination in the decapod crustacean Nephrops norvegicus (Linnaeus, 1758). Mar Pollut Bull 62:1207–1217

    Article  CAS  Google Scholar 

  • Navarro E, Iglesias JIP, Camacho AP, Labarta U (1996) The effect of the diets of phytoplankton and suspended bottom material on feeding and absorption of raft mussel (Mytilus galloprovincialis Lmk). J Exp Mar Biol Ecol 198:175–189

    Article  Google Scholar 

  • OECD (The Organisation for Economic Cooperation and Development) (2004) Emission Scenario Document on Plastic Additives. Series on Emission Scenario Documents, No. 3. OECD Environmental Health and Safety Publications. Environment Directorate, Paris

  • Oehlmann J, Schulte-Oehlmann U, Kloas W, Jagnytsch O, Lutz I, Kusk KO, Wollenberger L, Santos EM, Paull GC, Van Look KJW, Tyler CR (2009) A critical analysis of the biological impacts of plasticizers on wildlife. Philos Trans R Soc B 364:2047–2062

    Article  CAS  Google Scholar 

  • Olive PL (1998) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11:487–495

    Article  Google Scholar 

  • Omory M, Ikeda T (1984) Methods in marine zooplancton ecology. Wiley, New York

    Google Scholar 

  • Pereira CDS, Martín-Díaz ML, Zanette J, Cesar A, Choueri RB, Abessa DMS, Catharino MGM, Vasconcellos MBA, Bainy ACD, Sousa ECPM, DelValls TA (2011) Integrated biomarker responses as environmental status descriptors of a coastal zone (São Paulo, Brazil). Ecotoxicol Environ Saf 74:1257–1264

    Article  CAS  Google Scholar 

  • Peterson CH, Rice SD, Short JW, Esler D, Bodkin JL, Ballachey BE, Irons DB (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302:2082–2086

    Article  CAS  Google Scholar 

  • Resgalla C Jr, Manzoni G, Kuroshima KN, Reis FO, Laitano RW, Laitano KS (1999) Variabilidade nas taxas fisiológicas do mexilhão Perna perna em dois sítios de cultivo do litoral norte de Santa Catarina. Facimar 3:33–40

    Google Scholar 

  • Resgalla C Jr, Brasil ES, Salomão LC (2007) The effect of temperature and salinity on the physiological rates of the mussel Perna perna (Linnaeus 1758). Braz Arch Biol technol 50:543–556

    Article  CAS  Google Scholar 

  • Rodolfo A, Nunes LR, Ormanji W (2006) Tecnologia do PVC. BRASKEM, São Paulo

    Google Scholar 

  • Santana MFM (2015) Effects of microplastic contamination on marine biota. Dissertation, University of São Paulo

  • Santana MFM, Ascer LG, Custódio MR, Pereira CDS, Moreira F, Turra A (2016) Microplastics contamination in mussels’ natural beds from a Brazilian urbanized coastal region: an initial evaluation for further bioassessments. Mar Pollut Bull 106:183–189

    Article  CAS  Google Scholar 

  • Sussarellu R, Suquet M, Thomas Y, Lambert C, Fabioux C, Pernet MEJ, Goïc NL, Quillien V, Mingant C, Epelboin Y, Corporeau C, Guyomarch J, Robbens J, Paul-Pont I, Soudant P, Huvet A (2016) Oyster reproduction is affected by exposure to polystyrene microplastics. PNAS 113:2430–2435

    Article  CAS  Google Scholar 

  • Syberg K, Khan FR, Selck H, Palmqvist A, Banta GT, Daley J, Sano L, Duhaime MB (2015) Microplastics: addressing ecological risk through lessons learned. Environ Toxicol Chem 34:945–953

    Article  CAS  Google Scholar 

  • Underwood AJ, Peterson CH (1988) Towards an ecological framework for investigating pollution. Mar Ecol Prog Ser 46:227–234

    Article  Google Scholar 

  • Van Cauwenberghe L, Janssen CR (2014) Microplastics in bivalves cultured for human consumption. Environ Pollut 193:65–70

    Article  Google Scholar 

  • Van Cauwenberghe L, Vanreusel A, Mees J, Janssen CR (2013) Microplastic pollution in deep-sea sediments. Environ Pollut 182:495–499

    Article  Google Scholar 

  • Von Moos N, Burkhardt-Holm P, Kohler A (2012) Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environ Sci Technol 46:11327–11335

    Article  Google Scholar 

  • Ward JE, Shumway SE (2004) Separating the grain from the chaff: particle selection in suspension- and deposit-feeding bivalves. J Exp Mar Biol Ecol 300:83–130

    Article  Google Scholar 

  • Wegner A, Besseling E, Foekema EM, Kamermans P, Koelmans AA (2012) Effects of nanopolystyrene on the feeding behaviour of the blue mussel (Mytilus edulis L.). Environ Toxicol Chem 31:2490–2497

    Article  CAS  Google Scholar 

  • Welden NAC, Cowie PR (2016) Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ Pollut 218:895–900

    Article  CAS  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Widdows J, Bayne BL (1971) Temperature acclimation of Mytilus edulis with reference to its energy budget. J Mar Biol Assoc UK 51:827–843

    Article  Google Scholar 

  • Wills ED (1987) Evaluation of lipid peroxidation in lipids and biological membranes. In: Snell K, Mullock B (eds) Biochemical toxicology: a practical approach, 1st edn. IRL Press, Washington, pp 127–152

    Google Scholar 

  • Ye S, Andrady AL (1991) Fouling of floating plastic debris under Biscayne Bay exposure conditions. Mar Pollut Bull 22:608–613

    Article  Google Scholar 

  • Zilberberg C, Sereno D, Lima G, Custódio MR, Lôbo-Hajdu G (2011) Effect of mussel’s gender and size on a stress response biomarker. Water Air Soil Pollut 217:317–320

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank CAPES for the student grants, CNPq for the research grant of Denis Abessa (CNPq, 311609/2014-7), Plastivida (Plastics Socio-environmental Institute) for the fellowship to Fabiana Tavares Moreira the technical staff of IOUSP, Liv Ascer and Elisa V. S. Menck for the support throughout the experiment, Prof. Dr. Márcio Reis Custódio for content revision, and Ian McCarthy (FAPESP, 14/21804-3) and Linda Gwen Waters for the language and structure revision.

Author information

Authors and Affiliations

  1. Department of Biological Oceanography, Oceanographic Institute (IO), University of São Paulo (USP), São Paulo, São Paulo, 05508-120, Brazil

    Marina F. M. Santana, Fabiana T. Moreira & Alexander Turra

  2. College of Science and Engineering, Australian Tropical Science and Innovation Precinct (ATSIP), James Cook University (JCU), Townsville, QLD, 4811, Australia

    Marina F. M. Santana

  3. Australian Institute of Marine Science (AIMS), Townsville, Cape Cleveland, QLD, 4810, Australia

    Marina F. M. Santana

  4. Department of Marine Science, Federal University of São Paulo (UNIFESP), Santos, São Paulo, 11030-490, Brazil

    Camilo D. S. Pereira

  5. Paulista State University (UNESP), São Vicente, São Paulo, 11380-972, Brazil

    Denis M. S. Abessa

Authors
  1. Marina F. M. Santana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fabiana T. Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Camilo D. S. Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Denis M. S. Abessa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander Turra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina F. M. Santana.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest. The founding sponsors had no role in the design of the study, in the collection, analyses, or interpretation of data, in the writing of the manuscript, or in the decision to publish the results.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 23 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santana, M.F.M., Moreira, F.T., Pereira, C.D.S. et al. Continuous Exposure to Microplastics Does Not Cause Physiological Effects in the Cultivated Mussel Perna perna. Arch Environ Contam Toxicol 74, 594–604 (2018). https://doi.org/10.1007/s00244-018-0504-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-018-0504-3

Search

Navigation