Environmental Science and Pollution Research

, Volume 24, Issue 23, pp 19114–19125 | Cite as

Monitoring of organic pollutants in marine environment by semipermeable membrane devices and mussels: accumulation and biochemical responses

  • Oya S. Okay
  • Burak Karacık
  • Abbas Güngördü
  • Atilla Yılmaz
  • Nazmi C. Koyunbaba
  • Sevil D. Yakan
  • Bernhard Henkelmann
  • Karl-Werner Schramm
  • Murat Ozmen
Research Article


This study involves the monitoring of organic pollutants using transplanted mussels (Mytilus galloprovincialis) as bioindicator organisms and semipermeable membrane devices (SPMDs) as passive samplers. Mussels and SPMDs were deployed to marinas, shipyards and shipbreaking yards on the coastal area of Turkey and retrieved after 60 days. Polycyclic aromatic hydrocarbons (PAH), polychlorinated biphenyls (PCB) and organochlorine pesticide (OCP) compounds were analysed with high-resolution GC-MS. Total PAH concentrations in SPMDs and mussels ranged from 200 to 4740 ng g sampler−1 and from 7.0 to 1130 ng g−1 in wet weight (ww). PCB and OCP concentrations in SPMDs changed between 0.04–200 and 4.0–26 ng g sampler−1, respectively. The highest PCB (190 ng g−1 ww) and OCP (200 ng g−1 ww) concentrations in mussels were measured at shipyard stations. A strong correlation was observed between the PAH and PCB concentrations in SPMDs and mussels. Enzyme assays (acetylcholinesterase, ethoxyresorufin-O-deethylase, glutathione S-transferase, glutathion reductase and carboxylesterase activities) were performed as biomarkers to reveal the effects of pollution on the mussels. There was no clear relationship found between the enzyme levels and the pollutant concentrations in mussels. Integrated biomarker responses were calculated to interpret the overall effect of pollutants.


Passive sampling SPMDs Mussel transplantation Organic pollutants, enzymes Integrated biomarker response 



This research has been supported via Joint Research Projects between The Scientific and Technological Research Council of Turkey (TÜBİTAK), International Bureau of the Federal Ministry of Education and Research, Germany (project numbers: 110Y194 in Turkey and PT-DLR 01DL12016 in Germany).

Supplementary material

11356_2017_9594_MOESM1_ESM.docx (30 kb)
Table S1 (DOCX 29 kb)
11356_2017_9594_MOESM2_ESM.docx (21 kb)
Table S2 (DOCX 21 kb)
11356_2017_9594_MOESM3_ESM.docx (18 kb)
Table S3 (DOCX 17 kb)
11356_2017_9594_MOESM4_ESM.docx (30 kb)
Table S4 (DOCX 30 kb)
11356_2017_9594_MOESM5_ESM.docx (34 kb)
Table S5 (DOCX 33 kb)
11356_2017_9594_MOESM6_ESM.docx (19 kb)
Table S6 (DOCX 18 kb)
11356_2017_9594_MOESM7_ESM.docx (333 kb)
Figure S1 (DOCX 332 kb)
11356_2017_9594_MOESM8_ESM.docx (200 kb)
Figure S2 (DOCX 199 kb)


  1. Adams RG, Lohmann R, Fernandez LA et al (2007) Polyethylene devices: passive samplers for measuring dissolved hydrophobic organic compounds in aquatic environments. Environ Sci Technol 41:1317–1323. doi: 10.1021/es0621593 CrossRefGoogle Scholar
  2. Alvarez DA, Maruya KA, Dodder NG et al (2014) Occurrence of contaminants of emerging concern along the California coast (2009–10) using passive sampling devices. Mar Pollut Bull 81:347–354. doi: 10.1016/j.marpolbul.2013.04.022 CrossRefGoogle Scholar
  3. Alvarez DA, Petty JD, Huckins JN et al (2004) Development of a passive, in situ, integrative sampler for hydrophilic organic contaminants in aquatic environments. Environ Toxicol Chem 23:1640–1648. doi: 10.1897/03-603 CrossRefGoogle Scholar
  4. Andersson T, Förlin L (1992) Regulation of the cytochrome P450 enzyme system in fish. Aquat Toxicol 24:1–19. doi: 10.1016/0166-445X(92)90014-E CrossRefGoogle Scholar
  5. Axelman J, Naes K, Näf C, Broman D (1999) Accumulation of polycyclic aromatic hydrocarbons in semipermeable membrane devices and caged mussels (Mytilus edulis L.) in relation to water column phase distribution. Environ Toxicol Chem 18:2454–2461. doi: 10.1002/etc.5620181111 CrossRefGoogle Scholar
  6. Barsiene J, Lehtonen KK, Koehler A et al (2006) Biomarker responses in flounder (Platichthys flesus) and mussel (Mytilus edulis) in the Klaipeda-Būtinge area (Baltic Sea). Mar Pollut Bull 53:422–436. doi: 10.1016/j.marpolbul.2006.03.009 CrossRefGoogle Scholar
  7. Baussant T, Sanni S, Jonsson G et al (2001) Bioaccumulation of polycyclic aromatic compounds: 1. Bioconcentration in two marine species and in semipermeable membrane devices during chronic exposure to dispersed crude oil. Environ Toxicol Chem 20:1175–1184. doi: 10.1002/etc.5620200606 CrossRefGoogle Scholar
  8. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322. doi: 10.1002/etc.5620210629 CrossRefGoogle Scholar
  9. Bergqvist PA, Strandberg BO, Ekelund R et al (1998) Temporal monitoring of organochlorine compounds in seawater by semipermeable membranes following a flooding episode in western Europe. Environ Sci Technol 32:3887–3892. doi: 10.1021/es980146m CrossRefGoogle Scholar
  10. Bodin N, Burgeot T, Stanisière JY et al (2004) Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp Biochem Physiol Part C Toxicol Pharmacol 138:411–427. doi: 10.1016/j.cca.2004.04.009 CrossRefGoogle Scholar
  11. Boehm PD, Page DS, Brown JS et al (2005) Comparison of mussels and semi-permeable membrane devices as intertidal monitors of polycyclic aromatic hydrocarbons at oil spill sites. Mar Pollut Bull 50:740–750. doi: 10.1016/j.marpolbul.2005.02.002 CrossRefGoogle Scholar
  12. Booij K, Hoedemaker JR, Bakker JF (2003) Dissolved PCBs, PAHs, and HCB in pore waters and overlying waters of contaminated harbor sediments. Environ Sci Technol 37:4213–4220. doi: 10.1021/es034147c CrossRefGoogle Scholar
  13. Booij K, Sleiderink HM, Smedes F (1998) Calibrating the uptake kinetics of semipermeable membrane devices using exposure standards. Environ Toxicol Chem 17:1236–1245. doi: 10.1002/etc.5620170707 CrossRefGoogle Scholar
  14. Booij K, Smedes F (2010) An improved method for estimating in situ sampling rates of nonpolar passive samplers. Environ Sci Technol 44:6789–6794. doi: 10.1021/es101321v CrossRefGoogle Scholar
  15. Booij K, Smedes F, Van Weerlee EM, Honkoop PJC (2006) Environmental monitoring of hydrophobic organic contaminants: the case of mussels versus semipermeable membrane devices. Environ Sci Technol 40:3893–3900. doi: 10.1021/es052492r CrossRefGoogle Scholar
  16. Booij K, van Drooge BL (2001) Polychlorinated biphenyls and hexachlorobenzene in atmosphere, sea-surface microlayer, and water measured with semi-permeable membrane devices (SPMDs). Chemosphere 44:91–98. doi: 10.1016/S0045-6535(00)00303-9 CrossRefGoogle Scholar
  17. Booij K, Zegers BN, Boon JP (2002) Levels of some polybrominated diphenyl ether (PBDE) flame retardants along the Dutch coast as derived from their accumulation in SPMDs and blue mussels (Mytilus edulis). Chemosphere 46:683–688. doi: 10.1016/S0045-6535(01)00232-6 CrossRefGoogle Scholar
  18. Bourgeault A, Gourlay-Francé C (2013) Monitoring PAH contamination in water: comparison of biological and physico-chemical tools. Sci Total Environ 454:328–336. doi: 10.1016/j.scitotenv.2013.03.021 CrossRefGoogle Scholar
  19. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi: 10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  20. Bucheli TD, Fent K (1995) Induction of cytochrome P450 as a biomarker for environmental contamination in aquatic ecosystems. Crit Rev Environ Sci Technol 25:201–268CrossRefGoogle Scholar
  21. Burgess RM, Lohmann R, Schubauer-Berigan JP et al (2015) Application of passive sampling for measuring dissolved concentrations of organic contaminants in the water column at three marine superfund sites. Environ Toxicol Chem 34:1720–1733. doi: 10.1002/etc.2995 CrossRefGoogle Scholar
  22. Carls MG, Holland LG, Short JW et al (2004) Monitoring polynuclear aromatic hydrocarbons in aqueous environments with passive low-density polyethylene membrane devices. Environ Toxicol Chem 23:1416. doi: 10.1897/03-395 CrossRefGoogle Scholar
  23. Casida JE, Quistad GB (2004) Organophosphate toxicology: safety aspects of nonacetylcholinesterase secondary targets. Chem Res Toxicol 17:983–998. doi: 10.1021/tx0499259 CrossRefGoogle Scholar
  24. Chen L, Lam JCW, Zhang X et al (2015) Relationship between metal and polybrominated diphenyl ether (PBDE) body burden and health risks in the barnacle Balanus amphitrite. Mar Pollut Bull 100:383–392. doi: 10.1016/j.marpolbul.2015.08.020 CrossRefGoogle Scholar
  25. Connolly JP, Pedersen CJ (1988) A thermodynamic-based evaluation of organic chemical accumulation in aquatic organisms. Environ Sci Technol 22:99–103. doi: 10.1021/es00166a011 CrossRefGoogle Scholar
  26. Di Leo A, Annicchiarico C, Cardellicchio N et al (2014) Monitoring of PCDD/Fs and dioxin-like PCBs and seasonal variations in mussels from the Mar Grande and the Mar Piccolo of Taranto (Ionian Sea, Southern Italy). Environ Sci Pollut Res Int 21:13196–13207. doi: 10.1007/s11356-014-2495-6 CrossRefGoogle Scholar
  27. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. doi: 10.1016/0006-2952(61)90145-9 CrossRefGoogle Scholar
  28. Fernandez LA, Gschwend PM (2015) Predicting bioaccumulation of polycyclic aromatic hydrocarbons in soft-shelled clams (Mya arenaria) using field deployments of polyethylene passive samplers. Environ Toxicol Chem 34:993–1000. doi: 10.1002/etc.2892 CrossRefGoogle Scholar
  29. Flammarion P, Migeon B, Urios S et al (1998) Effect of methidathion on the cytochrome P-450 1A in the cyprinid fish gudgeon (Gobio gobio). Aquat Toxicol 42:93–102. doi: 10.1016/S0166-445X(98)00046-0 CrossRefGoogle Scholar
  30. Forsberg ND, Smith BW, Sower GJ, Anderson KA (2014) Predicting polycyclic aromatic hydrocarbon concentrations in resident aquatic organisms using passive samplers and partial least-squares calibration. Environ Sci Technol 48:6291–6299. doi: 10.1021/es5000534 CrossRefGoogle Scholar
  31. Galvao P, Henkelmann B, Longo R et al (2015) The brown mussel Perna perna (L., 1758) as a sentinel species for chlorinated pesticide and dioxin-like compounds. Environ Sci Pollut Res Int 22:13522–13533. doi: 10.1007/s11356-015-4607-3 CrossRefGoogle Scholar
  32. González-Fernández C, Albentosa M, Campillo JA et al (2015) Influence of mussel biological variability on pollution biomarkers. Environ Res 137:14–31. doi: 10.1016/j.envres.2014.11.015 CrossRefGoogle Scholar
  33. Gooch JW, Elskus AA, Kloepper-Sams PJ et al (1989) Effects of ortho- and non-ortho-substituted polychlorinated biphenyl congeners on the hepatic monooxygenase system in scup (Stenotomus chrysops). Toxicol Appl Pharmacol 98:422–433. doi: 10.1016/0041-008X(89)90171-3 CrossRefGoogle Scholar
  34. Gorbi S, Virno Lamberti C, Notti A et al (2008) An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoring the impact of an offshore platform in the Adriatic sea. Mar Environ Res 65:34–49. doi: 10.1016/j.marenvres.2007.07.006 CrossRefGoogle Scholar
  35. Gowland BTG, McIntosh AD, Davies IM et al (2002) Implications from a field study regarding the relationship between polycyclic aromatic hydrocarbons and glutathione S-transferase activity in mussels. Mar Environ Res 54:231–235. doi: 10.1016/S0141-1136(02)00129-0 CrossRefGoogle Scholar
  36. Greenwood R, Mills G, Vrana B (2007) Passive sampling techniques in environmental monitoring. Elsevier, AmsterdamGoogle Scholar
  37. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  38. Hale SE, Oen AMP, Cornelissen G et al (2016) The role of passive sampling in monitoring the environmental impacts of produced water discharges from the Norwegian oil and gas industry. Mar Pollut Bull 111:33–40. doi: 10.1016/j.marpolbul.2016.07.051 CrossRefGoogle Scholar
  39. Hofelt CS, Shea D (1997) Accumulation of organochlorine pesticides and pcbs by semipermeable membrane devices and Mytilus edulis in New Bedford Harbor. Environ Sci Technol 31:154–159. doi: 10.1021/es9602509 CrossRefGoogle Scholar
  40. Hong Y, Wetzel D, Pulster EL et al (2015) Significant spatial variability of bioavailable PAHs in water column and sediment porewater in the Gulf of Mexico 1 year after the Deepwater Horizon oil spill. Environ Monit Assess 187:646. doi: 10.1007/s10661-015-4867-x CrossRefGoogle Scholar
  41. Huckins JN, Manuweera GK, Petty JD et al (1993) Lipid-containing semipermeable membrane devices for monitoring organic contaminants in water. Environ Sci Technol 27:2489–2496. doi: 10.1021/es00048a028 CrossRefGoogle Scholar
  42. Huckins JN, Petty JD, Booij K (2006) Monitors of organic chemicals in the environment. Springer US, Boston, MAGoogle Scholar
  43. Huckins JN, Petty JD, Lebo JA et al (2002) Development of the permeability/performance reference compound approach for in situ calibration of semipermeable membrane devices. Environ Sci Technol 36:85–91. doi: 10.1021/es010991w CrossRefGoogle Scholar
  44. Joyce AS, Pirogovsky MS, Adams RG et al (2015) Using performance reference compound-corrected polyethylene passive samplers and caged bivalves to measure hydrophobic contaminants of concern in urban coastal seawaters. Chemosphere 127:10–17. doi: 10.1016/j.chemosphere.2014.12.067 CrossRefGoogle Scholar
  45. Jönsson ME, Brunström B, Brandt I (2009) The zebrafish gill model: induction of CYP1A, EROD and PAH adduct formation. Aquat Toxicol 91:62–70. doi: 10.1016/j.aquatox.2008.10.010 CrossRefGoogle Scholar
  46. Karacık B, Okay OS, Henkelmann B et al (2013) Water concentrations of PAH, PCB and OCP by using semipermeable membrane devices and sediments. Mar Pollut Bull 70:258–265. doi: 10.1016/j.marpolbul.2013.02.031 CrossRefGoogle Scholar
  47. Kauneliene V, Krugly E, Kliucininkas L et al (2016) PAHs in indoor and outdoor air from decentralized heating energy production: comparison of active and passive sampling. Polycycl Aromat Compd 36:410–428. doi: 10.1080/10406638.2014.999949 CrossRefGoogle Scholar
  48. Kopp J, Cornette F, Simonne C (2005) A comparison of growth and biochemical composition of Mytilus galloprovincialis (Lmk.) and Mytilus edulis (L.) on the West coast of Cotentin, Normandy, France 1999–2000. Aquac Int 13:327–340. doi: 10.1007/s10499-004-6548-6 CrossRefGoogle Scholar
  49. Li H, Ran Y (2012) Distribution and bioconcentration of polycyclic aromatic hydrocarbons in surface water and fishes. Sci World J 2012:632910. doi: 10.1100/2012/632910 Google Scholar
  50. Liscio C, Magi E, Di Carro M et al (2009) Combining passive samplers and biomonitors to evaluate endocrine disrupting compounds in a wastewater treatment plant by LC/MS/MS and bioassay analyses. Environ Pollut 157:2716–2721. doi: 10.1016/j.envpol.2009.04.034 CrossRefGoogle Scholar
  51. Lohmann R, Muir D, Zeng EY et al (2017) Aquatic Global Passive Sampling (AQUA-GAPS) revisited: first steps toward a network of networks for monitoring organic contaminants in the aquatic environment. Environ Sci Technol 51:1060–1067. doi: 10.1021/acs.est.6b05159 CrossRefGoogle Scholar
  52. Lourenço RA, de Oliveira FF, de Souza JM et al (2016) Monitoring of polycyclic aromatic hydrocarbons in a produced water disposal area in the Potiguar Basin, Brazilian equatorial margin. Environ Sci Pollut Res 23:17113–17122. doi: 10.1007/s11356-016-6903-y CrossRefGoogle Scholar
  53. Luellen DR, Shea D (2003) Semipermeable membrane devices accumulate conserved ratios of sterane and hopane petroleum biomarkers. Chemosphere 53:705–713. doi: 10.1016/S0045-6535(03)00576-9 CrossRefGoogle Scholar
  54. Luellen DR, Shea D (2002) Calibration and field verification of semipermeable membrane devices for measuring polycyclic aromatic hydrocarbons in water. Environ Sci Technol 36:1791–1797. doi: 10.1021/es0113504 CrossRefGoogle Scholar
  55. Newsted JL, Jones PD, Giesy JP et al (1995) Development of toxic equivalency factors for PCB congeners and the assessment of TCDD and PCB mixtures in rainbow trout. Environ Toxicol Chem 14:861–871. doi: 10.1002/etc.5620140518 CrossRefGoogle Scholar
  56. Okay OS, Karacik B, Güngördü A et al (2014) Micro-organic pollutants and biological response of mussels in marinas and ship building/breaking yards in Turkey. Sci Total Environ 496:165–178. doi: 10.1016/j.scitotenv.2014.07.035 CrossRefGoogle Scholar
  57. Pauka LM, Maceno M, Rossi SC, Silva de Assis HC (2011) Embryotoxicity and biotransformation responses in zebrafish exposed to water-soluble fraction of crude oil. Bull Environ Contam Toxicol 86:389–393. doi: 10.1007/s00128-011-0235-x CrossRefGoogle Scholar
  58. Paulik LB, Smith BW, Bergmann AJ et al (2016) Passive samplers accurately predict PAH levels in resident crayfish. Sci Total Environ 544:782–791. doi: 10.1016/j.scitotenv.2015.11.142 CrossRefGoogle Scholar
  59. Petty JD, Huckins JN, Alvarez DA et al (2004) A holistic passive integrative sampling approach for assessing the presence and potential impacts of waterborne environmental contaminants. Chemosphere 54:695–705. doi: 10.1016/j.chemosphere.2003.08.015 CrossRefGoogle Scholar
  60. Petty JD, Huckins JN, Zajicek JL (1993) Application of semipermeable membrane devices (SPMDs) as passive air samplers. Chemosphere 27:1609–1624. doi: 10.1016/0045-6535(93)90143-S CrossRefGoogle Scholar
  61. Petty JD, Poulton BC, Charbonneau CS et al (1998) Determination of bioavailable contaminants in the lower Missouri River following the flood of 1993. Environ Sci Technol 32:837–842. doi: 10.1021/es9707320 CrossRefGoogle Scholar
  62. Peven CS, Uhler AD, Querzoli FJ (1996) Caged mussels and semipermeable membrane devices as indicators of organic contaminant uptake in dorchester and duxbury bays, Massachusetts. Environ Toxicol Chem 15:144–149. doi: 10.1002/etc.5620150212 CrossRefGoogle Scholar
  63. Piccardo MT, Stella A, Pala M et al (2010) Field use of semipermeable membrane devices (SPMDs) for passive air sampling of polycyclic aromatic hydrocarbons: opportunities and limitations. Atmos Environ 44:1947–1951. doi: 10.1016/j.atmosenv.2010.03.003 CrossRefGoogle Scholar
  64. Poma G, Binelli A, Volta P et al (2014) Evaluation of spatial distribution and accumulation of novel brominated flame retardants, HBCD and PBDEs in an Italian subalpine lake using zebra mussel (Dreissena polymorpha). Environ Sci Pollut Res 21:9655–9664. doi: 10.1007/s11356-014-2826-7 CrossRefGoogle Scholar
  65. Prato E, Danieli A, Maffia M, Biandolino F (2010) Lipid and fatty acid compositions of Mytilus galloprovincialis cultured in the Mar Grande of Taranto (Southern Italy): feeding strategies and trophic relationships. Zool Stud 49:211–219Google Scholar
  66. Rantalainen A-L, Cretney WJ, Ikonomou MG (2000) Uptake rates of semipermeable membrane devices (SPMDs) for PCDDs, PCDFs and PCBs in water and sediment. Chemosphere 40:147–158. doi: 10.1016/S0045-6535(99)00220-9 CrossRefGoogle Scholar
  67. Richardson BJ, Tse ES-C, De Luca-Abbott SB et al (2005) Uptake and depuration of PAHs and chlorinated pesticides by semi-permeable membrane devices (SPMDs) and green-lipped mussels (Perna viridis). Mar Pollut Bull 51:975–993. doi: 10.1016/j.marpolbul.2005.04.028 CrossRefGoogle Scholar
  68. Richardson BJ, Zheng GJ, Tse ESC et al (2003) A comparison of polycyclic aromatic hydrocarbon and petroleum hydrocarbon uptake by mussels (Perna viridis) and semi-permeable membrane devices (SPMDs) in Hong Kong coastal waters. Environ Pollut 122:223–227. doi: 10.1016/S0269-7491(02)00301-9 CrossRefGoogle Scholar
  69. Rusina TP, Smedes F, Koblizkova M, Klanova J (2010) Calibration of silicone rubber passive samplers: experimental and modeled relations between sampling rate and compound properties. Environ Sci Technol 44:362–367. doi: 10.1021/es900938r CrossRefGoogle Scholar
  70. Santhoshkumar P, Shivanandappa T (1999) In vitro sequestration of two organophosphorus homologs by the rat liver. Chem Biol Interact 119-120:277–282. doi: 10.1016/S0009-2797(99)00037-X CrossRefGoogle Scholar
  71. Schiedek D, Broeg K, Barsiene J et al (2006) Biomarker responses as indication of contaminant effects in blue mussel (Mytilus edulis) and female eelpout (Zoarces viviparus) from the southwestern Baltic Sea. Mar Pollut Bull 53:387–405. doi: 10.1016/j.marpolbul.2005.11.013 CrossRefGoogle Scholar
  72. Seethapathy S, Górecki T, Li X (2008) Passive sampling in environmental analysis. J Chromatogr A 1184:234–253. doi: 10.1016/j.chroma.2007.07.070 CrossRefGoogle Scholar
  73. Sogorb MA, Vilanova E (2002) Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215–228. doi: 10.1016/S0378-4274(01)00543-4 CrossRefGoogle Scholar
  74. Stephensen E (2000) Biochemical indicators of pollution exposure in shorthorn sculpin (Myoxocephalus scorpius), caught in four harbours on the southwest coast of Iceland. Aquat Toxicol 48:431–442. doi: 10.1016/S0166-445X(99)00062-4 CrossRefGoogle Scholar
  75. Stok JE, Huang H, Jones PD et al (2004) Identification, expression, and purification of a pyrethroid-hydrolyzing carboxylesterase from mouse liver microsomes. J Biol Chem 279:29863–29869. doi: 10.1074/jbc.M403673200 CrossRefGoogle Scholar
  76. Sureda A, Box A, Tejada S et al (2011) Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Eivissa Island, Spain). Aquat Toxicol 101:540–549. doi: 10.1016/j.aquatox.2010.12.011 CrossRefGoogle Scholar
  77. Tsangaris C, Kormas K, Strogyloudi E et al (2010) Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. Comp Biochem Physiol Toxicol Pharmacol 151:369–378. doi: 10.1016/j.cbpc.2009.12.009 CrossRefGoogle Scholar
  78. van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. doi: 10.1016/S1382-6689(02)00126-6 CrossRefGoogle Scholar
  79. Verweij F, Booij K, Satumalay K et al (2004) Assessment of bioavailable PAH, PCB and OCP concentrations in water, using semipermeable membrane devices (SPMDs), sediments and caged carp. Chemosphere 54:1675–1689. doi: 10.1016/j.chemosphere.2003.10.002 CrossRefGoogle Scholar
  80. Vidal-Liñán L, Bellas J, Etxebarria N et al (2014) Glutathione S-transferase, glutathione peroxidase and acetylcholinesterase activities in mussels transplanted to harbour areas. Sci Total Environ 470-471:107–116. doi: 10.1016/j.scitotenv.2013.09.073 CrossRefGoogle Scholar
  81. Vrana B, Mills GA, Dominiak E, Greenwood R (2006) Calibration of the Chemcatcher passive sampler for the monitoring of priority organic pollutants in water. Environ Pollut 142:333–343. doi: 10.1016/j.envpol.2005.10.033 CrossRefGoogle Scholar
  82. Vrana B, Mills GA, Kotterman M et al (2007) Modelling and field application of the Chemcatcher passive sampler calibration data for the monitoring of hydrophobic organic pollutants in water. Environ Pollut 145:895–904. doi: 10.1016/j.envpol.2006.04.030 CrossRefGoogle Scholar
  83. Vrana B, Paschke A, Popp P, Schüürmann G (2001) Use of semipermeable membrane devices (SPMDs). Environ Sci Pollut Res 8:27–34. doi: 10.1007/BF02987292 CrossRefGoogle Scholar
  84. Wang J, Henkelmann B, Bi Y et al (2013) Temporal variation and spatial distribution of PAH in water of Three Gorges Reservoir during the complete impoundment period. Environ Sci Pollut Res 20:7071–7079. doi: 10.1007/s11356-012-1427-6 CrossRefGoogle Scholar
  85. Wheelock CE, Phillips BM, Anderson BS et al (2008) Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). Springer, New York, pp 117–178Google Scholar
  86. Williamson KS, Petty JD, Huckins JN et al (2002) Sequestration of priority pollutant PAHs from sediment pore water employing semipermeable membrane devices. Chemosphere 49:717–729. doi: 10.1016/S0045-6535(02)00393-4 CrossRefGoogle Scholar
  87. Xue W, Warshawsky D (2005) Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol Appl Pharmacol 206:73–93. doi: 10.1016/j.taap.2004.11.006 CrossRefGoogle Scholar
  88. Yılmaz A, Karacık B, Henkelmann B et al (2014) Use of passive samplers in pollution monitoring: a numerical approach for marinas. Environ Int 73:85–93. doi: 10.1016/j.envint.2014.07.013 CrossRefGoogle Scholar
  89. Zhang H, Davison W (1995) Performance characteristics of diffusion gradients in thin films for the in situ measurement of trace metals in aqueous solution. Anal Chem 67:3391–3400. doi: 10.1021/ac00115a005 CrossRefGoogle Scholar
  90. Zhu X, Zhou C, Henkelmann B et al (2013) Monitoring of PAHs profiles in the urban air of Dalian, China with active high-volume sampler and semipermeable membrane devices. Polycycl Aromat Compd 33:265–288. doi: 10.1080/10406638.2013.777672 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Oya S. Okay
    • 1
  • Burak Karacık
    • 1
  • Abbas Güngördü
    • 2
  • Atilla Yılmaz
    • 1
  • Nazmi C. Koyunbaba
    • 1
  • Sevil D. Yakan
    • 1
  • Bernhard Henkelmann
    • 3
  • Karl-Werner Schramm
    • 3
    • 4
  • Murat Ozmen
    • 2
  1. 1.Faculty of Naval Architecture and Ocean EngineeringIstanbul Technical UniversityIstanbulTurkey
  2. 2.Arts and Sciences Faculty, Department of Biology, Laboratory of Environmental ToxicologyInönü UniversityMalatyaTurkey
  3. 3.Helmholtz Zentrum München, German Research Center for Environmental HealthInstitute of Ecological ChemistryNeuherbergGermany
  4. 4.Department für BiowissenschaftenTUM, Wissenschaftszentrum Weihenstephan für Ernährung und LandnutzungFreisingGermany

Personalised recommendations