Skip to main content

Advertisement

SpringerLink
Log in

Bioaccumulation of PAHs in marine zooplankton: an experimental study in the copepod Pseudodiaptomus marinus

  • Thematic Issue
  • Published:
Environmental Earth Sciences Aims and scope Submit manuscript

Abstract

Laboratory exposure experiments were performed on the marine coastal zooplankton species Pseudodiaptomus marinus—a keystone species of vast Atlantic and Pacific marine ecosystems, tracing the accumulation of three polycyclic aromatic hydrocarbons (PAHs): phenanthrene, anthracene and pyrene. The experiment was designed to study the bioconcentration of PAHs in phytoplankton (Rhodomonas baltica) and accumulation in copepods (P. marinus), through two different pathways: food and water uptake. For this purpose, water and organism subsamples were collected, ASE (accelerated solvent extraction) extracted, and analyzed for PAHs by GC/MS technique. As a result, experimental bioconcentration (BCF) and bioaccumulation (BAF) factors which showed a significant correlation with the octanol–water partition coefficient (K ow) were presented for P. marinus. The active feeding route of exposure showed no significant differences versus passive uptake, highlighting the importance of dietary exposure as a major pathway for POPs accumulation in zooplankton; in particular for those which cannot be metabolized.

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
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bajt O (2014) Aliphatic and polycyclic aromatic hydrocarbons in gulf of Trieste sediments (Northern Adriatic): potential impacts of maritime traffic. Bull Environ Contam Toxicol 93(3):299–305

    Article  Google Scholar 

  • Barceló D (1993) Environmental Protection Agency and other methods for the determination of priority pesticides and their transformation products in water. J Chromatogr A 643(1):117–143

    Article  Google Scholar 

  • Barron MG (1990) Bioconcentration will water-borne organic chemicals accumulate in aquatic animals. Environ Sci Technol 24:1612–1618

    Article  Google Scholar 

  • Berrojalbiz N, Lacorte S, Calbet A, Saiz E, Barata C, Dachs J (2009) Accumulation and cycling of polycyclic aromatic hydrocarbons in zooplankton. Environ Sci Technol 43(7):2295–2301

    Article  Google Scholar 

  • Brylinski JM, Antajan E, Raud T, Vincent D (2012) First record of the Asian copepod Pseudodiaptomus marinus Sato, 1913 (Copepoda: Calanoida: Pseudodiaptomidae) in the southern bight of the North Sea along the coast of France. Aquat Invasions 7(4):577–584

    Article  Google Scholar 

  • Burgess RM, Ahrens MJ, Hickey CW, Den Besten PJ, Ten Hulscher D, Van Hattum Meador J, Douben PE (2003) An overview of the partitioning and bioavailability of PAHs in sediments and soils. In: Douben PE (ed) PAHs: an ecotoxicological perspective, Ecological and Environmental Toxicology Series. Wiley, West Sussex, p 99

    Google Scholar 

  • Cailleaud K, Forget-Leray J, Souissi S, Lardy S, Augagneur S, Budzinski H (2007) Seasonal variation of hydrophobic organic contaminant concentrations in the water-column of the Seine Estuary and their transfer to a planktonic species Eurytemora affinis (Calanoïd, Copepod) Part 2: alkylphenol-polyethoxylates. Chemosphere 70(2):281–287

    Article  Google Scholar 

  • Cailleaud K, Forget-Leray J, Peluhet L, LeMenach K, Souissi S, Budzinski H (2009) Tidal influence on the distribution of hydrophobic organic contaminants in the Seine Estuary and biomarker responses on the copepod (Eurytemora affinis). Environ Pollut 157(1):64–71

    Article  Google Scholar 

  • Chan SMN, Luan T, Wong MH, Tam NFY (2006) Removal and biodegradation of polycyclic aromatic hydrocarbons by Selenastrum capricornutum. Environ Toxicol Chem 25(7):1772–1779

    Article  Google Scholar 

  • Chiou CT, McGroddy SE, Kile DE (1998) Partition characteristics of polycyclic aromatic hydrocarbons on soils and sediments. Environ Sci Technol 32(2):264–269

    Article  Google Scholar 

  • Fisk AT, Stern GA, Hobson KA, Strachan WJ, Loewen MD, Norstrom RJ (2001) Persistent organic pollutants (POPs) in a small, herbivorous, Arctic marine zooplankton (Calanus hyperboreus): trends from April to July and the influence of lipids and trophic transfer. Mar Pollut Bull 43(1):93–101

    Article  Google Scholar 

  • Fleminger A, Kramer SH (1988) Recent introduction of an Asian estuarine copepod, Pseudodiaptomus marinus (Copepoda: Calanoida), into southern California embayments. Mar Biol 98(4):535–541

    Article  Google Scholar 

  • Gerofke A, Kömp P, McLachlan MS (2005) Bioconcentration of persistent organic pollutants in four species of marine phytoplankton. Environ Toxicol Chem 24(11):2908–2917

    Article  Google Scholar 

  • Gobas FA, Morrison HA (2000) Bioconcentration and biomagnification in the aquatic environment handbook of property estimation methods for chemicals: environmental and health sciences. Lewis, Boca Raton, pp 189–231

    Google Scholar 

  • Grindley JR and Grice GD (1969) A redescription of Pseudodiaptomus marinus Sato (Copepoda, Calanoida) and its occurrence at the Island of Mauritius Crustaceana, p 125–134

  • Guillard RRL, Sieracki MS (2005) Counting cells in cultures with the light microscope. In: Anderson RA (ed) Algal Culturing Techniques. Elsevier, New York, pp 239–252

    Google Scholar 

  • Hamelink JL, Waybrant RC, Ball RC (1971) A proposal: exchange equilibria control the degree chlorinated hydrocarbons are biologically magnified in lentic environments. Trans Am Fish Soc 100(2):207–214

    Article  Google Scholar 

  • Hamelink J, Landrum PF, Bergman H, Benson WH (1994) Bioavailability: physical, chemical, and biological interactions. CRC Press, Boca Raton

    Google Scholar 

  • Hoekstra PF, O’Hara TM, Teixeira C, Backus S, Fisk AT, Muir DCG (2002) Spatial trends and bioaccumulation of organochlorine pollutants in marine zooplankton from the Alaskan and Canadian Arctic. Environ Toxicol Chem 21:575–583

    Article  Google Scholar 

  • Hubert A, Wenzel KD, Engewald W, Schürmann G (2001) Accelerated solvent extraction—More efficient extraction of POPs and PAHs from real contaminated plant and soil samples. Rev Anal Chem 20(2):101–144

    Article  Google Scholar 

  • Islam MS, Tanaka M (2009) Diet and prey selection in larval and juvenile Japanese anchovy Engraulis japonicus in Ariake Bay, Japan. Aquatic Ecology 43(2):549–558

    Article  Google Scholar 

  • Iwasawa K, Murata A, Taguchi S (2009) Cell shrinkage of Isochrysis galbana (Prymneshiophyceae) during storage with preservatives. Plankton Benthos Res 4(3):120–121

    Article  Google Scholar 

  • Jensen LK, Honkanen JO, Jæger I, Carroll J (2012) Bioaccumulation of phenanthrene and benzo [a] pyrene in Calanus finmarchicus. Ecotox Environ Safe 78:225–231

    Article  Google Scholar 

  • Kowalewska G, Konat J (1997) Distribution of polynuclear aromatic hydrocarbons (PAHs) in sediments of the southern Baltic Sea. Oceanologia 39:83–104

    Google Scholar 

  • Landrum PF (1989) Bioavailability and toxicokinetics of polycyclic aromatic hydrocarbons sorbed to sediments for the amphipod Pontoporeia hoyi. Environ Sci Technol 23:588–595

    Article  Google Scholar 

  • Landrum PF, Frez WA, Simmons MS (1992) The effect of food consumption on the toxicokinetics of benzo(a)pyrene and 2,2′,4,4′,5,5′-hexachlorobiphenyl in Mysis relicta. Chemosphere 25:397–415

    Article  Google Scholar 

  • Liang D, Uye S (1997) Seasonal reproductive biology of the egg-carrying calanoid copepod Pseudodiaptomus marinus in a eutrophic inlet of the Inland Sea of Japan. Mar Biol 128(3):409–414

    Article  Google Scholar 

  • Lotufo GR (1998) Lethal and sublethal toxicity of sediment-associated fluoranthene to benthic copepods: application of the critical-body-residue approach. Aquat Toxicol 44(1):17–30

    Article  Google Scholar 

  • Mackay D (1982) Correlation of bioconcentration factors. Environ Sci Technol 16:274–278

    Article  Google Scholar 

  • Mackay D, Fraser A (2000) Bioaccumulation of persistent organic chemicals: mechanisms and models. Environ Pollut 110(3):375–391

    Article  Google Scholar 

  • Mackie and Adron (1978) Identification of inosine and inosine 5′-monophosphate as the gustatory feeding stimulants for the turbot, Scophthalmus maximus. Comp Biochem Physiol 60A:79–83

    Article  Google Scholar 

  • Magnusson K, Tiselius P (2010) The importance of uptake from food for the bioaccumulation of PCB and PBDE in the marine planktonic copepod Acartía clausí. Aquat Toxicol 98(4):374–380

    Article  Google Scholar 

  • Magnusson K, Magnusson M, Ostberg P, Granberg M, Tiselius P (2007) Bioaccumulation of C-14-PCB 101 and C-14-PBDE 99 in the marine planktonic copepod Calanus finmarchicus under different food regimes. Mar Environ Res 63:67–81

    Article  Google Scholar 

  • Mandalakis M, Gustafsson O, Alsberg T, Egeback AL, Reddy CM, Xu L, Klanova J, Holoubek I, Stephanou EG (2005) Contribution of biomass burning to atmospheric polycyclic aromatic hydrocarbons at three European background sites. Environ Sci Technol 39:2976–2982

    Article  Google Scholar 

  • McCready S, Birch GF, Long ER (2006) Metallic and organic contaminants in sediments of Sydney harbour, Australia and vicinity—a chemical dataset for evaluating sediment quality guidelines. Environ Int 32(4):455–465

    Article  Google Scholar 

  • Meador JP, Stein JE, Reichert WL, Varanasi U (1995) Bioaccumulation of polycyclic aromatic hydrocarbons by marine organisms. In: Whitacre DM (ed) Reviews of environmental contamination and toxicology. Springer, New York, pp 79–165

    Chapter  Google Scholar 

  • Means JC, Wood SG, Hassett JJ, Banwart WL (1980) Sorption of polynuclear aromatic hydrocarbons by sediments and soils. Environ Sci Technol 14:1524–1528

    Article  Google Scholar 

  • Middleditch BS, Missler SR, Ward DG, McVey JB, Brown A, Lawrence AL (1979) Maturation of penaeid shrimp: dietary fatty acids. In: Proceedings of the World Mariculture Society (Vol 10, No 1–4, pp 472–476) Blackwell Publishing Ltd

  • Riccardi C, Di Filippo P, Pomata D, Di Basilio M, Spicaglia S, Buiarelli F (2013) Identification of hydrocarbon sources in contaminated soils of three industrial areas. Sci Total Environ 450:13–21

    Article  Google Scholar 

  • Sabia L, Uttieri M, Schmitt FG, Zagami G, Zambianchi E, Souissi S (2014) Pseudodiaptomus marinus Sato, 1913, a new invasive copepod in Lake Faro (Sicily): observations on the swimming behaviour and the sex-dependent responses to food. Zoological Studies 53(1):49

    Article  Google Scholar 

  • Sabia L, Zagami G, Mazzocchi MG, Zambianchi E, Uttieri M (2015) Spreading factors of a globally invading coastal copepod. Medit. Mar. Sci. 16:460–471

    Google Scholar 

  • Schantz MM (2006) Pressurized liquid extraction in environmental analysis. Anal Bioanal Chem 386(4):1043–1047

    Article  Google Scholar 

  • Serrazanetti GP, Conte LS, Cortesi P, Totti C, Viviani R (1991) Seasonal variations of aliphatic hydrocarbons in Sardina pilchardus (Walb) (Teleostei: Clupeidae) tissues. Mar Chem 32:9–18

    Article  Google Scholar 

  • Sibley PK, Harris ML, Bestari KT, Steele TA, Robinson RD, Gensemer RW, Solomon KR (2004) Response of zooplankton and phytoplankton communities to creosote—impregnated Douglas fir pilings in freshwater microcosms. Arch Environ Contam Toxicol 47(1):56–66

    Article  Google Scholar 

  • Skjoldal HR, Dale T, Haldorsen H, Pengerud B, Thingstad TF, Tjessem K, Aaberg A (1982) Oil pollution and plankton dynamics 1. Controlled ecosystem experiments during the 1980 spring bloom in lindåspollene, Norway. Neth J Sea Res 16:511–523

    Article  Google Scholar 

  • Souissi S, Michalec FG, Dur G, Mahjoub MS, Schmitt FG, Hwang JS (2010) How does salinity influence the swimming speed of the estuarine calanoid copepod Eurytemora affinis? Reply. J Plankton Res 32:1227

    Article  Google Scholar 

  • Souissi A, Souissi S, Hansen BW (2015) Physiological improvement in the copepod Eurytemora affinis through thermal and multigenerational selection. Aquac Res. doi:10.1111/are.12675

    Google Scholar 

  • Stange K, Swackhamer DL (1994) Factors affecting phytoplankton species-specific differences in accumulation of 40 polychlorinated biphenyls (PCBs). Environ Toxicol Chem 13(11):1849–1860

    Article  Google Scholar 

  • Tlili S, Ovaert J, Souissi A, Ouddane B, Souissi S (2016) Acute toxicity, uptake and accumulation kinetics of nickel in an invasive copepod species: Pseudodiaptomus marinus. Chemosphere 144:1729–1737

    Article  Google Scholar 

  • USEPA (2007) Method 3500C. Organic extraction and sample preparation. United States of America Environmental Protection Agency (USEPA). http://www.3.epa.gov/epawaste/hazard/testmethods/sw846/pdfs/3500c.pdf

  • Uye SI, Kasahara S (1983) Grazing of Various Developmental Stages of Pseudodiaptomus marinus (Copepoda: Calanoida) on Naturally Occurring Particles. Bull Plankton Soc Japan 30(2):147–158

    Google Scholar 

  • Valbonesi A, Harada E (1980) The vertical distributions of some copepods and a mysid in a near-shore water of Tanabe Bay. Publications of the Seto Marine Biological Laboratory. Kyoto University. vol. 25 No. 5–6

  • Van Hattum B, Pons MJC, Montanes JFC (1998) Polycyclic aromatic hydrocarbons in freshwater isopods and field-partitioning between abiotic phases. Arch Environ Contam Toxicol 35:257–267

    Article  Google Scholar 

  • Wang Z, Fingas M, Shu YY, Sigouin L, Landriaut M, Lambert P et al (1999) Quantitative characterization of PAHs in burn residue and soot samples and differentiation of pyrogenic PAHs from petrogenic PAHs- the 1994 mobile burn study. Environ Sci Technol 33(18):3100–3109

    Article  Google Scholar 

  • Weber WJ, Gould JP (1966) Sorption of organic pesticides from aqueous solution. Adv Chem Ser 60, American Chemical Society, Washington

  • Wetzel DL, Van Vleet ES (2004) Accumulation and distribution of petroleum hydrocarbons found in mussels (Mytilus galloprovincialis) in the canals of Venice, Italy. Marine Pollut Bull 48(9):927–936

    Article  Google Scholar 

  • Zhang Q, Yang L, Wang WX (2011) Bioaccumulation and trophic transfer of dioxins in marine copepods and fish. Environ Pollut 159(12):3390–3397

    Article  Google Scholar 

  • Zhu LZ, Cai XF, Wang J (2005) PAHs in aquatic sediment in Hangzhou, China: analytical methods, pollution pattern, risk assessment and sources. J Environ Sci 17(5):748–755

    Google Scholar 

Download references

Acknowledgments

Our sincere gratitude to Dr. Sopheak Net and David Dumoulin for their invaluable support throughout the research phase in France. We also thanks gratefully to the Erasmus Mundus mobility program staff (UE). We thank Olivier Glippa and Damien Bocahu for the discussions and help during these experiments. Special thanks to past and present members of Sami Souissi’s team for their contribution in maintaining continuously strains and mass culture of several species of copepods, including P. marinus used in this study. We particularly thank the LOG COPEFISH team for their help in keeping P. marinus cultures in the laboratory since 2011 in the framework of the COPEFISH project (Young Researcher (A.S.). Emerging Project of the Nord-Pas de Calais Regional Council). We thank Hans-U. Dahms (Kaohsiung) for critical remarks on an earlier version of the MS.

Financial support

This work was carried out with the financial support of Lille-1 University and its Interdisciplinary Institute IREPSE (S.Souissi and B. Oudanne), the National Council of Scientific and Technological Research of Argentina (CONICET) and the Argentinean Agency of Science and Technology Promotion (ANPYCT) through PICT 2010-1302 (granted to A. Arias).

Author information

Authors and Affiliations

  1. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Rivadavia 1917, C1033AAJ, Buenos Aires, Argentina

    Andrés H. Arias

  2. Área de Oceanografía Química, Instituto Argentino de Oceanografía (IADO-CONICET-UNS), Florida 8000 (Camino La Carrindanga km 7,5), B8000FWB, Bahía Blanca, Argentina

    Andrés H. Arias

  3. Departamento de Química, Area III, Universidad Nacional del Sur, Alem 1253, 8000, Bahía Blanca, Argentina

    Andrés H. Arias

  4. Univ. Lille, CNRS, UMR 8187 LOG, Laboratoire d’Océanologie et de Géosciences, Univ. Littoral Cote d’Opale, 62930, Wimereux, France

    Anissa Souissi, Marion Roussin & Sami Souissi

  5. Laboratoire LASIR, UMR CNRS 8516, Equipe Physico-Chimie de l’Environnement, Université de Lille1, 59655, Villeneuve d’Ascq Cedex, France

    Baghdad Ouddane

Authors
  1. Andrés H. Arias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anissa Souissi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marion Roussin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Baghdad Ouddane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sami Souissi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrés H. Arias.

Additional information

This article is part of a Topical Collection in Environmental Earth Sciences on “3RAGSU”, guest edited by Daniel Emilio Martinez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arias, A.H., Souissi, A., Roussin, M. et al. Bioaccumulation of PAHs in marine zooplankton: an experimental study in the copepod Pseudodiaptomus marinus . Environ Earth Sci 75, 691 (2016). https://doi.org/10.1007/s12665-016-5472-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12665-016-5472-1

Keywords

Search

Navigation