ARTICLE pubs.acs.org/est
Persistent Organic Pollutants in Mediterranean Seawater and Processes Affecting Their Accumulation in Plankton Naiara Berrojalbiz,† Jordi Dachs,*,† Sabino Del Vento,† María Jose Ojeda,† María Carmen Valle,† Javier Castro-Jimenez,†,‡ Giulio Mariani,‡ Jan Wollgast,‡ and Georg Hanke‡ †
Department of Environmental Chemistry, Institute of Environmental Assessment and Water Research (IDAEA - CSIC), Barcelona, Catalunya, Spain ‡ European Commission-DG Joint Research Centre, Institute for Environment and Sustainability, Ispra, Italy
bS Supporting Information ABSTRACT: The Mediterranean and Black Seas are unique marine environments subject to important anthropogenic pressures due to riverine and atmospheric inputs of organic pollutants. Here, we report the results obtained during two eastwest sampling cruises in June 2006 and May 2007 from Barcelona to Istanbul and Alexandria, respectively, where water and plankton samples were collected simultaneously. Both matrixes were analyzed for hexaclorochyclohexanes (HCHs), hexachlorobenzene (HCB), and 41 polychlorinated biphenyl (PCB) congeners. The comparison of the measured HCB and HCHs concentrations with previously reported dissolved phase concentrations suggests a temporal decline in their concentrations since the 1990s. On the contrary, PCB seawater concentrations did not exhibit such a decline, but show a significant spatial variability in dissolved concentrations with lower levels in the open Western and South Eastern Mediterranean, and higher concentrations in the Black, Marmara, and Aegean Seas and Sicilian Strait. PCB and OCPs (organochlorine pesticides) concentrations in plankton were higher at lower plankton biomass, but the intensity of this trend depended on the compound hydrophobicity (KOW). For the more persistent PCBs and HCB, the observed dependence of POP concentrations in plankton versus biomass can be explained by interactions between airwater exchange, particle settling, and/or bioaccumulation processes, whereas degradation processes occurring in the photic zone drive the trends shown by the more labile HCHs. The results presented here provide clear evidence of the important physical and biogeochemical controls on POP occurrence in the marine environment.
’ INTRODUCTION Surrounded by land, the Mediterranean Sea has historicaly been subject to high anthropogenic pressures of direct and indirect loads of persistent organic pollutants (POPs) from intensive industrial and agricultural activities. Although international regulations have banned or restricted the global use of some of these chemicals, the presence of ubiquitous POP in the Mediterranean environment is still of concern. Organochlorine compounds (OCl) such as polychlorinated biphenyls (PCBs), hexachlorocyclohexanes (HCHs), and hexachlorobenzene (HCB) are of particular interest due to their bioacumulation potential and proved toxic effects.1 The Mediterranean Sea receives POPs as a result of river/ runoff inflow and atmospheric deposition.2 The behavior and occurrence of POPs in the different aquatic media is driven by dynamic oceanic biogeochemical cycles, especially the biological pump, which comprises several biologically mediated processes such as bioacumulation, particle settling, or, for some compounds, biodegradation. Previous work has already pointed out the importance of the trophic status in the occurrence of POPs in r 2011 American Chemical Society
aquatic environments.37 In fact, several studies carried out in lacustrine eutrophic systems revealed that POP concentration in plankton decreased with increasing biomass.812 Nevertheless, field evidence of this process is lacking in the marine environment. Thus, the oligotrophic conditions of Mediterranean waters with its particular biogeochemical characteristics provide a good scenario for this study and are representative of the processes occurring in other oceanic regions. The main objectives of this work are: (i) to provide a large data set of PCB, HCB, and HCHs concentrations in the Mediterranean and SW Black Sea seawater and plankton, (ii) to evaluate the physical and trophic controls affecting the accumulation of OCls in oceanic plankton, and (iii) to assess the influence of POP` physical-chemical properties on their cycling in the marine environment. Received: November 13, 2010 Accepted: April 11, 2011 Revised: April 8, 2011 Published: April 28, 2011 4315
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’ MATERIALS AND METHODS Site Description and Sample Collection. The Mediterranean Sea is a semienclosed sea surrounded by populated coastal areas and with evaporation exceeding precipitation and river runoff. This is compensated with the exchange of water through the Gibraltar Strait in the form of incoming less saline Atlantic surface waters. The Mediterranean Sea is oligotrophic with a dominant gradient of increasing oligotrophy from West to East in terms of primary productivity13 and autotrophic biomass14 (see Annex I of the Supporting Information for additional details of site description). Water (W) and plankton (P) samples were collected on board of the R/V Garcia del Cid during the two THRESHOLDS sampling cruises made in June 2006 and May 2007. In both transects, Barcelona was the initial and final port, with Istanbul and Alexandria being the intermediate stops, respectively. The transects covered an extensive area within a 1-year time span allowing a good spatial coverage of different regions (see Annex I). Surface seawater was collected continuously during transects from 2 m depth and pumped from a tow-fish to an online system placed on board of the ship composed of a GF/F filter and a XAD column to separate particulate and dissolved phases, respectively. The total volume of the different samples filtered through the system at 150200 mL min1 flow rate ranged from 90 to 350 L. 180200 L water samples from 200 m depth (WD) were taken with a 20 L stainless steel sampling device (Duncan & Associates, Grange-over-Sands, Cumbria, UK) into a precleaned 200 L stainless steel container and processed as above. XAD columns were kept at 4 °C and were processed within 20 days after the ending of each sampling cruise. Filters were preserved frozen (20 °C) until chemical analysis. Plankton samples were taken at sampling stations (Figure 1b) using a 50 μm mesh vertical plankton net and by performing vertical tows from a depth located 10 m below the maximum chlorophyll depth to surface. The collected material was filtered with GF/D glass fiber Whatman filters (2.7 μm) to remove the excess water. Filters were frozen (18 °C) until the extraction process. Biomass (mg L1) for each sample was determined using the dry weight of the filters over the volume of filtered water by vertical tows of plankton net. In some cases, due to the small biomass, samples from geographically close stations were combined to get levels above the method detection limits. Organic carbon (OC) determination of five plankton samples representative of different basins was performed, giving an average OC content of 44% and ranging from 32.5% to 49.9% (Annex I). Concurrent determinations of phytoplankton productivity and water column metabolism do not show a significant eastwest trend15 due to the observed variability. Chemical Analysis. Briefly, two analogous methodologies (A and B) were used to analyze water samples (dissolved and particle samples) following the procedures proposed by Berrojalbiz et al.16 and Castro et al.,2 respectively. Plankton filters were freeze-dried for 24 h, weighed, and processed as described by Berrojalbiz et al.16 Further details on analytical methods are described in Annex II. Water samples and plankton extracts were analyzed for 41 PCB congeners, R-HCH, β-HCH, γ-HCH, and HCB by gas chromatography coupled to a electron capture detector. Compounds were quantified by the internal standard procedure (see Annex II for instrumental detection limits). In addition,
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a selected group of samples with higher sampled volumes was also used to quantify eight Mono-Ortho PCB. The analysis of this group of samples containing six surface waters and all of the samples collected at 200 m was performed by isotope dilution high resolution gas chromatographyhigh resolution mass spectrometry (HRGCHRMS) on the basis of the EPA 1668 method2 (see Annex II). The analytical procedure for all matrices was validated by determining the recovery rates of the surrogates of each sample, and analytical and field blanks were analyzed in parallel to XADs and filter samples (Annex II). Results were corrected by the obtained recoveries and the mean value of the blanks. Particle samples collected in the 2006 sampling cruise were discarded due to field levels close to blank levels.
’ RESULTS AND DISCUSSION Organochlorine Compounds Occurrence in Water and Plankton. PCB Concentrations in the Dissolved Phase of Surface Water Samples (CW). Levels of ∑41 PCBs in dissolved phase of
surface waters ranged from 2.2 to 82.4 pg L1, with a median of 24.1 pg L1, and the distribution pattern was dominated by penta- and hexachloro-congeners in all of the sampling locations (Figure 1a) (Annex III). The highest CW values were found in the Western part of the Ionian Sea (samples B1, B2, W19) and in the Aegean and Black Sea. Conversely, CW values in the Western Mediterranean are close to the median of the whole Mediterranean Sea. In general, CW in Mediterranean open sea waters exhibited lower mean and variability than those reported by previous studies in Mediterranean open sea sites17,18 and comparable to other marine temperate regions.19,20 Black sea CW values are consistent with those of Maldonado et al.21 Conversely, the CW values are significantly lower than those reported at coastal sites, at a few miles from coast and shallow waters.2225 This is due to the general circulation pattern in the Mediterranean coastal areas, which is parallel to the coast line with little mixing between coastal and open sea waters. CW values for nonortho-substituted PCB congeners in surface waters are shown in Annex III. In general, the samples collected in the Eastern basin showed lower concentrations for all of the individual congeners in comparison to the Western basin. This is the first time that concentrations of coplanar PCBs are reported for the open Mediterranean seawater. PCBs in Particulate Phase of Surface Water Samples (CWP). CWP of ∑41 PCBs ranged from 1 to 25.6 pg L1 (Annex III) and accounted for 570% of the total amount of PCBs in the dissolved phase. The fraction of PCBs in the particle phase is significantly correlated to total suspended particles (R2 = 0.56, p < 0.05). The relative abundance in terms of individual compounds is dominated by tri- and penta-congeners in all of the sampling locations. These results are in the range of those found in the open waters of the NW Mediterranean Sea.18 PCB Concentrations in the 200 m Depth Dissolved (CWD) and Particulate Phases (CWP). In samples collected at 200 m depth, the sum of the seven ICES PCB congeners ranged from 7.53 to 86.9 pg L1 (Annex III). With the exception of sample WD1 (near Mallorca), the rest of the samples showed lower PCB concentrations for all of the congeners than in surface waters, which is in agreement with the vertical profiles described for the Mediterranean and Atlantic ocean.18,26 Likewise, the particle associated ∑7PCBs concentration range at 200 m was 4316
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Figure 1. (A) Map showing the sampling transects of dissolved and particulate phase samples and the corresponding spatial variation of the concentrations of PCBs in the water dissolved phase samples. Samples indicated in dark and light blue were processed using methodologies A and B, respetively (see chemical analysis). (B) Map showing the sampling sites of plankton samples and spatial variation of the concentrations of PCBs in plankton. 4317
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Figure 2. Influence of plankton biomass (B [mg L1]) on the concentrations of PCBs in plankton (CP [ng gdw1]) as given by log CP = a m log[B] (eq 2). The central panel shows the dependence of m on the chemical hydrophobicity (KOW) for plankton samples from the Mediterranean.
2.38.7 pg L1 (Annex III) and in the range of what has been reported elsewhere.18 OCPs (Organochlorine Pesticides) in Surface Waters (CW). γ-HCH dissolved concentrations varied from nondetected values to 3.5 pg L1. Levels of δ-HCH ranged from values near detection limit to 15.5 pg L1. For both compounds, highest values were detected in the samples taken between Barcelona and Mallorca (W1 and W3), while Aegean Sea and Black Sea regions were the areas with the lowest concentrations. All samples in which the presence of β-HCH was detected in dissolved phase were located in the Libyan and Ionian seas with a maximum value of 0.7 pg L1 in the sample W17 taken near the Alexandria and Nile river mouth. Levels of HCB in the dissolved phase ranged from nondetected to 1.7 pg L1 for the Mediterranean Sea with a maximum value of 4.3 pg L1 in a Black Sea transect (WB3) (Annex III). OCP levels found in this study are much lower than those reported in the Mediterranean Sea two decades ago.27,28 Lakaschus and co-workers also reported a strong decline in HCHs concentrations in the North Atlantic Ocean during the 1990s.29 This decrease may be due to in situ degradation and/or volatilization30 and other sinks such as settling.3132 OCls in Plankton Samples (CP, ng g1 per Dry Weight Biomass). CP of ∑41 PCBs in plankton samples ranged from 0.76 to 353 ng g1dwb (on dry weight basis) (Annex III). The relative abundance in terms of individual compounds is dominated by penta to hepta chloro-congeners (Figure 1b). The sum of HCH isomers ranged from 0.3 to 346 ng g1dwb in plankton samples. γ-HCH was detected in most of the samples. HCB concentrations in plankton ranged from nondetected values to 2.5 ng g1dwb (Annex III). There is a scarcity of previous reports of plankton OCl concentration in marine regions.27,3336 OCls levels in photic zone plankton showed neither no significant eastwest distribution pattern, nor any dependence
on distance from coast, nor with the maximum chlorophyll depth, nor a relationship with surface water concentrations. However, previous studies in lakes have shown the influence of biomass and airwaterplankton exchange on PCB concentrations in plankton.3,4,912 For the Mediterranean Sea, when ∑PCBs and ∑HCHs concentrations in plankton are plotted against biomass, highly significant correlations (R2 = 0.58, p < 0.01 and R2 = 0.61, p < 0.01 respectively) are also found (Anex IV, and Figures 2 and 3). Organochlorine Compound Concentration Dependence on the Plankton Biomass. CP values for many OCl are significantly correlated with plankton biomass (Figures 2 and 3). The relationship between CP and the biomass (B, [kg L1]) has been hypothesized to be driven by the named “biomass dilution effect”.5 The “biomass dilution” hypothesis assumes that given the same amount of pollutants (Ctotal [ng L1]) in a water volume, a dilution of OCls will occur in planktonic organisms when a larger biomass is present in the system. In an hypothetical water volume, the relationship between CP and B could be described as BCF CP ¼ Ctotal ð1Þ 1 þ BBCF where BCF (L kg1) is the bioconcentration factor. Therefore, depending on whether the factor (B BCF) is higher than unity, the dry weight concentrations will be inversely correlated to biomass or, on the contrary, will be constant. If the dilution effect is a process controlling POP concentrations in plankton, then the trend should be observed for all compounds regardless of their physicochemical properties (for the B values found in Mediterranean waters). By fitting by least-squares the concentrations in plankton versus the biomass, it is found that, in general, 4318
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Figure 3. Influence of plankton biomass (B [mg L1]) on the concentrations of R-HCH, β-HCH, γ-HCH, and HCB in plankton (CP [ng gdw1]) as given by log CP = la m log[B] (eq 2). The central panel shows the dependence of m on the chemical hydrophobicity (KOW) for plankton samples from the Mediterranean (blue b) and Black Sea (red b).
CP for OCl decreased with increasing B following a power function: log½CP ¼ a mlog½B
ð2Þ
where a and m are the independent term and slope, respectively (Figures 2 and 3). These results are in agreement with the findings of Taylor and co-workers in Lakes of Canada,9 who described a similar OCl concentration decrease at high biomass. However, the slope m depends on the compound physicalchemical properties. This is reflected in the different values of m fitted for different PCB congeners, which are proportional to the influence of B on CP for a particular compound. Hence, higher m values would suggest a higher control of CP by plankton biomass, while lower values of m denote an independence of CP on B. To assess the influence of the OCl affinity to organic matter on these processes, m was plotted against the corresponding octanolwater partition coefficient (KOW) for PCBs (Figure 2) and HCHs and HCB (Figure 3). While Figure 2 shows increasing m values for the more hydrophobic PCB congeners, Figure 3 indicates a decrease of m with increasing KOW for HCHs and HCB. These trends show that the observed dependence on biomass is compound dependent and thus is not consistent with the “biomass dilution” hypothesis [eq 1], because under this scenario the m dependence on KOW should be the same for all chemicals. As shown in Figures 2 and 3, for high chlorinated PCBs and HCHs m is significantly different from zero, while for low chlorinated PCBs and HCB m is not statistically different from zero. The traditional approach of “biomass dilution” is based on the assumption of a constant amount of chemical (Ctotal) in the
Figure 4. Schematics of the processes affecting surface concentrations of dissolved and particle phase organochlorine compounds (OCs) and plankton OCs in the photic zone.
system, with no inputs and losses. In the oceanic compartment, however, there are inputs and/or outputs of chemicals. Figure 4 shows some of the dominant processes affecting the occurrence of OCl in plankton from the photic zone and provides the basis for explaining the trends observed in Figures 2 and 3. Therefore, CP values can be explained by considering atmospheric inputs and loss by settling particles and/or accumulation processes in the system. Advective inputs are neglected because in the open 4319
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Figure 5. Comparison of predicted and measured concentrations in plankton for PCB 52 and PCB 151 (left) and R-HCH and HCB concentrations (right) in plankton.
Mediterranean sea, atmospheric inputs are dominant due to direct inputs to coastal waters do not reach effectively the open sea due to limited mixing of coastal and open seawater masses. Under this scenario (Figure 4), the predicted relationship between CP and B would lie between a constant value of CP and a decrease of CP with biomass.4,37 Dachs and co-workers (2002) proposed an airwaterphytoplankton coupled model to account for atmospherewaterplankton interactions of POPs in the mixed surface ocean layer.37 Using this approach, airwater (FAW [ng m2 d1], waterphytoplankton (FWP [ng m2 d1]), and settling fluxes (FSETTL [ng m2 d1]) can be predicted by (see Annex IV in the Supporting Information for detailed information about the model): CA CW ð3Þ FAW ¼ kAW H0 kd FWP ¼ kWP CW CP ku FSETTL ¼ kSETTL
kd CP ku
ð4Þ ð5Þ
where CA and CW are the gas phase and surface dissolved POP concentrations (ng m3), respectively, H0 is the temperature corrected and dimensionless Henry’s law constant, kAW (m d1) is the airwater mass transfer rate, ku (m d1), kd (d1) are the plankton’s uptake and depuration rate constants, respectively, kWP (m d1) is the mass transfer coefficient between water and plankton, and kSETTL (m d1) is the mass transfer rate coefficient for sinking of POPs. Hence, in this scenario, plankton concentrations will be driven by the relative importance of both air concentrations and settling fluxes. Higher biomass and associated settling fluxes will lower the concentrations, while higher inputs from the atmosphere will increase the concentrations. Drivers of PCBs Occurrence in Plankton. Airwater exchange is the main pathway for entry and loss of PCBs in
the marine environment.38 Atmosphereocean diffusive exchange supports the dissolved POP concentrations in the surface ocean mixed layer, which is likewise affecting waterplankton equilibria of POPs. Consequently, when POPs in the gas phase are equilibrated with the dissolved phase, which in turn is equilibrated with plankton, CP will be independent of biomass for a given gas-phase concentration. This process gains importance for less hydrophobic compounds for which the fast dynamic coupling between air and water compensates any potential depletion of CW that could be reflected in changes in CP due to high biomass.4,37 Therefore, CP is independent of biomass as observed for the less hydrophobic PCB congeners in this work. For the more hydrophobic congeners, airwater exchange is a much slower process, and settling of particle associated POPs is more relevant.4 The partitioning between plankton and the dissolved phase for PCBs (BCF = CP/CW) shows a significant correlation (R2 = 0.69, p < 0.01) with Kow, which means that the more hydrophobic compounds have higher fractions of sorbed chemical (Annex IV). Thus, settling could be an important loss for POPs preferentially associated to sinking organic matter. When the amount of particles is higher, enhanced settling flux induces a depletion of PCBs in the water column by scavenging and thus lowering the water concentrations. Therefore, CP will decrease at higher biomass due to airwater dis-equilibria driven by bioaccumulation and settling particles. Indeed, for hydrophobic chemicals, airwater exchange is not fast enough to support phytoplankton uptake and settling, leading to a decrease of concentrations for the more hydrophobic chemicals. This trend is consistent with observations made by previous studies of PCBs in lakes.3,8 The decrease in CP concentrations at higher biomass due to airwaterplankton interactions is also in agreement with Figure 2 that shows an increasing m value as PCB congener hydrophobicity increases (R2 = 0.78; p < 0.05), while CP values for the less hydrophobic congeners are less influenced by B. Using eqs 35, and assuming steady-state conditions where FAW = FWP = FSETTL = FADW, where FADW is the air-deep water 4320
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flux, it is given by: FADW ¼ kADW
CA H0
ð6Þ
where kADW is the air-deep water mass transfer coefficient (Annex IV). Once FAW is known, concentration in the dissolved phase can be predicted from gas-phase concentrations by eq 3 (see Annex IV). Finally, CP values can be predicted from the predicted dissolved concentrations using eq 4. Concentrations in plankton were predicted from the measured gas-phase concentrations during the two sampling cruises (Annex IV). Figure 5 shows the CP predictions made for two PCB congeneres (see Annex IV for a detailed description of the estimations) in relation to real measured CP and their relationship with B. The approach used predicted not only the concentrations with a reasonable degree of accuracy, errors of a factor of 3 similar to those described when applying the model to lakes,3,4 but also the observed dilution trend in measured CP, confirming that airwater exchange and settling processes are two significant drivers controlling the PCB occurrence in plankton. Drivers of OCP Occurrence in Plankton. The dependence of HCHs concentrations on biomass is different from that for PCBs, with lower values of m when increasing KOW (Figure 3). As a result, the effect of apparent “biomass dilution” is more pronounced for the less hydrophobic compounds. In fact, looking at the calculated CP using eqs 36 from measured gasphase concentrations for HCHs, a disagreement can be seen between the trend of measured and predicted CP concentrations (Figure 5). HCHs are less hydrophobic than PCBs, so airwater exchange can, in principle, support and sustain water and plankton concentrations in most environments, which would lead to m values close to unity similar to the less hydrophobic PCB congeners, Conversely, the measured trend leads to m values significantly different from unity (Figures 3 and 5). This suggests that there is a process, different from settling fluxes, leading to airwater-plankton disequilibria at higher biomass. While PCBs are persistent compounds in the marine environment, HCHs are known to be less persistent, and subject to degradation processes in the natural environment.39,40 Therefore, the decrease of concentrations at higher biomass may be linked to degradation processes that lower the concentrations in the system, such as biological degradation, hydrolysis, or photodegradation.41 Among these, microbial degradation has been suggested to be the major removal process of HCHs in the Arctic Ocean,42 and presumably also for the Mediterranean. Therefore, for HCH, the airwaterplankton interactions captured by eqs 24 cannot predict the observed trends of HCH concentrations in plankton versus biomass because the model does not account for biodegradation processes. In contrast, HCB is a persistent compound,43 with a persistence comparable to PCB congeners and the same degree of hydrophobicity. In fact, the m value for HCB is comparable to the m values for PCB congeners with similar KOW values (Figure 4). Predictions of HCB concentrations from measured gas-phase concentrations using eqs 35 can reproduce the observed independence of HCB’s CP on B (Figure 5), consistent with airwaterplankton equilibria driving HCB concentrations in the photic zone, without any evidence of a significant degradation process. The present study provides a clear evidence of the importance of the coupling of airwater exchange and biogeochemical processes as a key control driving OCl occurrence in the marine
water column. More research is needed to determine the relative importance of settling and degradation processes on local, regional, and global cycling of different POPs, transfer to the food web, and the role of the microbial loop.
’ ASSOCIATED CONTENT
bS
Supporting Information. Sampling-sites descriptions, sample collection, and CTD vertical profiles. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT This work was funded by the European Union and Spanish Ministry of Science and Innovation through the THRESHOLDS projects (FP6 Integrated Project Contract No. 003933). N.B. acknowledges a predoctoral fellowship from the Basque Government. ’ REFERENCES (1) Stockholm Convention on Persistent Organic Pollutants; http://www.pops.int/. (2) Castro-Jimenez, J.; Eisenreich, S. J.; Ghiani, M.; Mariani, G.; Skejo, H.; Umlauf, G.; Wollgast, J.; Zaldívar, J. M.; Berrojalbiz, N.; Dachs, J.; Reuter, H. I. Atmospheric occurrence and deposition of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) in the open Mediterranean Sea. Environ. Sci. Technol. 2010, 44, 5456–5463. (3) Dachs, J.; Eisenreich, S. J.; Baker, J.; Ko, F. C.; Jeremiason, J. D. Coupling of phytoplankton uptake and air-water exchange of persistent organic pollutants. Environ. Sci. Technol. 1999, 33, 3653–3660. (4) Dachs, J.; Eisenreich, S.; Hoff, R. M. Influence of euthrophication on air-water exchange, vertical fluxes and phytoplankton concentrations of persistent organic pollutants. Environ. Sci. Technol. 2000, 34, 1095–1102. (5) Larsson, P.; Andersson, A.; Broman, D.; Nordb€ack, J.; Lundberg, E. Persistent organic pollutants (POPs) in pelagic systems. Ambio 2000, 29, 202–209. (6) Berglund, O.; Larsson, P.; Ewald, G.; Okla, L. Influence of trophic status on PCB distribution in lake sediments and biota. Environ. Pollut. 2001, 113, 199–210. (7) Kuzyk, Z. Z. A.; MacDonald, R. W.; Johannessen, S. C.; Stern, G. A. Biogeochemical controls on PCB deposition in Hudson Bay. Environ. Sci. Technol. 2010, 44, 3280–3285. (8) Larsson, P. Atmospheric deposition of persistent pollutants governs uptake by zooplankton in a pond in southern Sweden. Atmos. Environ. 1989, 23, 2151–2158. (9) Taylor, W. D.; Carey, J. H.; Lean, D. R. S.; McQueen, D. J. Organochlorine concentrations in the plankton of lakes in Southern Ontario and their relationship to plankton biomass. Can. J. Fish. Aquat. Sci. 1991, 48, 1960–1966. (10) Jeremiasson, J. D.; Eisenreich, S. J.; Paterson, M. J.; Besty, K. G.; Hecky, R.; Elser, J. J. Biogeochemical cycling of PCBs in lakes of variable trophic status: a paired-lake experiment. Limnol. Oceanogr. 1999, 44, 889–902. (11) Skei, J.; Larsson, P.; Rosenberg, R.; Jonsson, P.; Olsson, M.; Broman, D. Euthrophication and contaminants in aquatic ecosystems. Ambio 2000, 29, 184–194. (12) Berglund, O.; Larsson, P.; Ewald, G.; Okla, L. The effect of lake trophy on lipid content and PCB concentrations in planktonic food webs. Ecology 2001, 82, 1078–1008. 4321
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