Environ. Sci. Technol. 2006, 40, 3893-3900
Environmental Monitoring of Hydrophobic Organic Contaminants: The Case of Mussels versus Semipermeable Membrane Devices K E E S B O O I J , * ,† F O P P E S M E D E S , ‡ EVALINE M. VAN WEERLEE,† AND PIETER J. C. HONKOOP† Royal Netherlands Institute for Sea Research, P.O. Box 59, 1790 AB Texel, and Ministry of Transport, Public Works and Water Management, National Institute for Coastal and Marine Management/RIKZ, P.O. Box 207, 9750 AE Haren, The Netherlands
Concentrations of hydrophobic chemicals in mussels and semipermeable membrane devices (SPMDs) from nine studies published over the past decade, amended with new data obtained in the Scheldt-North Sea area, were assessed to understand the similarities and differences between these sampling matrixes. A model was developed to describe the concentration ratios, using literature values of elimination rate constants and steady-state accumulation factors of both samplers as key parameters. The model could successfully describe the results of seven studies. Differences in concentration ratios among these studies were related to the variability of mussel bioaccumulation factors (BAFs) and water sampling rates of SPMDs. For two studies, the model could only describe the data by adopting unrealistically high water sampling rates, and for one study there were not enough data to test the model. We argue that SPMDs will generally yield more reliable estimates of exposure concentrations than mussels, because in situ BAF values are difficult to estimate, whereas the in situ exchange kinetics of SPMDs can be quantified by measuring the dissipation rates of performance reference compounds. The implications of the results for future and existing monitoring programs are discussed.
Introduction The relative merits of mussels and semipermeable membrane devices (SPMDs) for assessing the fate of hydrophobic organic contaminants have been extensively studied over the past decade. Some general conclusions can be drawn from these studies. First, similar geographical trends are identified by SPMDs and mussels (1-6). Second, the relative abundance of more hydrophobic contaminants is higher in mussels than in SPMDs (1, 7). Third, substantial differences in SPMD/ mussel concentration ratios exist among studies (see the Results and Discussion). Mussels have been deployed over the past few decades for identifying pollution sources (8, 9) and for monitoring the effectiveness of site remediation and emission reduction policies (10-13). The identification of geographical and * Corresponding author phone: +31 222 369 463; fax: +31 222 319 674; e-mail:
[email protected]. † Royal Netherlands Institute for Sea Research. ‡ National Institute for Coastal and Marine Management/RIKZ. 10.1021/es052492r CCC: $33.50 Published on Web 05/18/2006
2006 American Chemical Society
temporal trends is hampered by a number of factors inherent to the use of biomonitoring organisms (BMOs). First, not all bivalve species can be found in all environments, and multiple bivalve species are used in the programs that cover larger geographical areas (e.g., 4 mussel species and 3 oyster species in NOAA’s National Status and Trends program (12, 13) and 5 oyster species, 13 mussels species, and 11 other bivalve species in the International Mussel Watch program in Central and South America, the Caribbean, and Mexico (14)). Variation of hydrophobic contaminant levels among bivalve species was minor in some studies (12, 15, 16), but Gunther et al. (17) observed higher organic contaminant accumulation in oysters than in mussels and clams, and Tavares et al. (18) reported organic contaminant concentrations that differed among eight bivalve species by a factor of 4-40. The second problem that is inherent to the use of BMOs is that contaminant accumulation may depend on environmental conditions, such as temperature, salinity, food availability, and levels of oxygen and toxins, as well as on physiological parameters of the organisms, such as feeding rate, reproductive status, and handling stress (17, 19-28). The use of semipermeable membrane devices in monitoring programs for organics eliminates many, but not all, of these difficulties. Uptake rates by SPMDs increase by a factor of ∼2 for each 10 °C temperature increase (29-31), and also increase with increasing flow rates (32, 33). Furthermore, the development of biofilms on the SPMD surface may impede the uptake of contaminants (34, 35). Huckins et al. (35) showed that the effect of environmental factors on the uptake kinetics can be accounted for by measuring the dissipation rate of performance reference compounds (PRCs), but additional evidence has been scarce. The simpler design of SPMDs and the fewer environmental factors that influence contaminant uptake seem to be attractive, but the choice for either mussels or SPMDs in monitoring programs should be based on a thorough understanding of the capabilities and limitations of either sampling matrix. In view of the wide range of SPMD/mussel concentration ratios that have been observed, SPMDs cannot simply be regarded as artificial mussels, nor can mussels simply be treated as living passive samplers. The purpose of this study was to quantitatively understand SPMD/mussel concentration ratios, to provide a tool for linking bivalve data to SPMD data, and to assess the usefulness of PRCs to identify intersite differences in SPMD uptake kinetics. The methods involved include the collection of literature data (kinetic and steady-state) both for mussels and for SPMDs, modeling of observed SPMD/mussel concentration ratios, and the analysis of an additional musselSPMD comparison made in the Western Scheldt and North Sea area.
Materials and Methods Literature Data. Ratios of concentrations in SPMDs (whole weight basis) and mussels (dry weight basis) were calculated for nine studies (1, 3-5, 7, 36-40) (Tables A and B, Supporting Information). The data reported by Richardson et al. (38, 40) were treated as one study. For this study and for the study by Herve et al. (1), the concentrations in SPMDs were assumed to be equal to the concentration in the triolein phase, because the membrane was not analyzed. A triolein/SPMD mass ratio of 0.20 was adopted when necessary (Table A, Supporting Information). Bioaccumulation factors (BAFs) of nonpolar organic contaminants were collected for the zebra mussel, Dreissena polymorpha (23, 24), the blue mussel, Mytilus edulis (4, 10, VOL. 40, NO. 12, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3893
FIGURE 1. Ratio of concentrations in SPMDs (whole weight basis) and mussels (dry weight basis) for the present study (a) and for literature data that do (b) or do not (c) follow the model (eq 5). Lines represent the model calculations with zero (drawn) and two (dotted and dashed) adjustable parameters (Table 1). 41-43), the Californian mussel, Mytilus californianus (44), and the freshwater mussel, Elliptio complanata (45) (Table C, Supporting Information). Where applicable, BAF values were converted to a wet weight basis, using the reported dry weight fraction and/or the lipid content. If no such information was supplied, a dry to wet weight ratio of 0.2 and a lipid to dry weight ratio of 0.1 were adopted. Elimination rate constants (k2) were collected for D. polymorpha (46), E. complanata (45, 47, 48), the green-lipped mussel, Perna viridis (49), and M. edulis (11, 42, 50) (Table D, Supporting Information). Elimination rate constants and BAFs that were based on short-term ( 5.5, the ratios steadily decrease to values of ∼0.1 at log Kow ) 7. Concentration ratios for site 1 are up to a factor of 6.8 larger than for the other sites. Literature values of SPMD/mussel concentration ratios are shown in Figure 1b,c. Where Cm/Cs ratios were reported for multiple sites, the geometric means per study are shown. The reported ratios span 4 orders of magnitude. At similar log Kow values, the ratios show a scatter of (1 order of magnitude. Cs/Cm ratios are fairly constant in the low-Kow range and decrease sharply with increasing log Kow for most studies. By contrast, ratios for two studies (3, 38, 40) remain fairly constant over the whole log Kow range. Exceptionally high ratios (∼100) were found for R-HCH and HCB in two studies (1, 36), but in other studies, much lower ratios (1-6) were reported for these compounds (3, 36-38). SPMD/Mussel Concentration Ratio Model. Literature data on contaminant uptake by mussels and SPMDs may 3894
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 12, 2006
help to better understand the observed ratios. The evolution of (volume-based) concentrations in SPMDs (C′s) is governed by (30, 52)
C′s ) CwKsw(1 - exp[-ket])
(1)
where Ksw is the SPMD-water partition coefficient, Cw is the aqueous concentration, t is the exposure time, and ke is the first-order elimination rate constant. The rate of change of concentrations in mussels (C′m, wet weight basis) can be described by (22, 53, 54)
dC′m/dt ) kuCw + RFCf - (kd + kb + G)C′m
(2)
where Cf is the concentration in food, ku is the uptake rate constant from water (L g-1 d-1), F is the food ingestion rate per unit mussel weight (g g-1 d-1), R is the food assimilation efficiency, kd is the rate constant for depuration via gills and feces (d-1), kb is the first-order biotransformation constant (d-1), and G is the specific growth rate (g g-1 d-1). Assuming that contaminants in food and water are in equilibrium (i.e., Cf ) CwKfw, where Kfw is the food-water partition coefficient), eq 2 reduces to
dC′m/dt ) (ku + RFKfw)Cw - (kd + kb + G)C′m ) k1Cw - k2C′m
(3)
where k1 and k2 are the lumped rate constants for the uptake and the elimination processes. The solution to eq 3 is given by
C′m ) Cw(BAF)(1 - exp[-k2t])
(4)
where the (wet-weight-based) BAF equals k1/k2. Contaminant concentrations in mussel-SPMD comparison studies typically are expressed on a dry weight basis for mussels (Cm) and a whole weight basis for SPMDs (Cs). Combining eqs 1 and 4, and using the dry weight fraction of mussels (fdw) and the SPMD density (Fs ) 0.91 g mL-1) for the conversion of concentration units, yields an expression for the evolution of SPMD/mussel concentration ratios (g g-1):
Cs fdwKsw[1 - exp(-ket)] ) Cm Fs(BAF)[1 - exp(-k2t)]
(5)
Mussel k2 Values. Elimination rate constants for four mussel species are shown as a function of log Kow in Figure 2. Values range between 0.27 d-1 for 2,6-dimethylnaphthalene in E. complanata (47) to 0.015 d-1 for PCB153 in M. edulis (42), corresponding to a half-life time of 3-46 d. Values for
FIGURE 2. First-order elimination rate constants for M. edulis (filled and open triangles, filled squares) and D. polymorpha, E. complanata, and P. viridis (other symbols). The drawn and dashed lines represent the linear regression equation (log k2 vs log Kow) for M. edulis and other mussels, respectively.
FIGURE 3. Mussel bioaccumulation factors (wet weight) as a function of log Kow. The drawn line shows the linear regression equation after exclusion of the data from ref 10 and the smelter-site data from ref 4 for reasons explained in the text. M. edulis are lower than k2 values of the other mussels by a factor of ∼3. The data could be modeled by
log k2 ) -0.149 log Kow + a0
(6)
M. edulis: a0 ) -0.58 E. complanata, D. polymorpha, P. viridis: a0 ) -0.08 R2 ) 0.73, s ) 0.12, n ) 165 where a0 is a species-dependent constant and k2 is given in units of d-1. Bioaccumulation Factors. BAF values (wet weight basis) for M. edulis, E. complanata, and M. californianus are shown as a function of log Kow in Figure 3. The smelter-site BAF data reported by Axelman et al. (4) are about 2 orders of magnitude higher than the BAF data obtained from other studies. These values must be regarded as excessive, and were therefore excluded from further analysis. The BAF values reported by Bergen et al. (10) are 0.8 log unit higher than the BAFs reported in an earlier study (43) of the same laboratory at the same site and were excluded as well. The log BAF-log Kow relations
FIGURE 4. SPMD-water partition coefficients of PCBs, PAHs, and chlorobenzenes.
FIGURE 5. Elimination rate constants for SPMDs, based on reported sampling rates. Equation 11 is shown as a drawn line. for the various studies are characterized by a common slope and an intercept that differs among studies:
log BAF ) 0.840 log Kow + a0,i
(7)
R2 ) 0.89, s ) 0.36, n ) 68 The intercepts (a0,i) observed for the six studies ranged between -1.06 and +0.22, with an average value of -0.49 and a standard deviation of 0.41. SPMD-Water Partition Coefficients. Reported Ksw values from three studies (29, 30, 35) are shown as a function of log Kow in Figure 4. The drawn line is given by
log Ksw ) 0.788 log Kow + 0.91
(8)
R2 ) 0.94, s ) 0.16, n ) 41 Ksw values are larger than the (wet-weight-based) BAFs by about 1 order of magnitude, as a result of the more nonpolar nature of SPMDs compared to mussels. SPMD ke Values. Elimination rate constants for SPMDs were calculated from reported sampling rates (29, 31, 33, 51) and Ksw values (eq 8) according to (29)
ke ) Rs/(KswVs) ) (koA)/(KswVs) VOL. 40, NO. 12, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
(9) 9
3895
FIGURE 6. Model estimates (eq 5) of SPMD/mussel concentration ratios (Cs/Cm): (a) time evolution of Cs/Cm using the model parameters given in eqs 6 (M. edulis), 7, 8, and 10; (b) effect of decreasing the log BAF-log Kow intercept on Cs/Cm at 30 d exposure; (c) effect of increasing the log ke-log Kow intercept on Cs/Cm at 30 d exposure. where Rs is the sampling rate, Vs is the SPMD volume, A is the SPMD surface area, and ko is the overall mass transfer coefficient. The resulting log ke values were modeled as a quadratic function of log Kow (Figure 5):
log ke ) -0.1166(log Kow)2 + 0.508 log Kow - 1.51 (10) 2
R ) 0.96, s ) 0.20, n ) 184 Three issues regarding Figure 5 and eqs 9 and 10 are worth noting. First, part of the scatter originates from differences in the experimental temperature. The high-temperature data reported by Rantalainen et al. (31) and Huckins et al. (29) generally fall above the regression curve in Figure 5, and their low-temperature data fall below this curve. Second, ke is larger (and equilibration times are shorter) at high surface areas and small SPMD volumes (eq 9). For the SPMD-mussel comparison studies, V/A ratios of SPMDs range from 107 µm for the standard-design SPMD (52) to a lowest value of 31 µm (3). Third, the ke values of SPMDs and the k2 values of mussels are of similar magnitude (∼0.1 d-1) in the range 3 < log Kow < 4.5, but the ke values for SPMDs decrease stronger with increasing log Kow than the k2 values of mussels. The slope of the log k versus log Kow plot can be expected to be ∼-1 when the aqueous boundary layer controls the mass transfer rates (32, 55). For SPMDs, a log ke-log Kow slope of -1 is observed for the range log Kow > 5 (Figure 5), whereas for mussels the log k2-log Kow slope attains a value of only -0.15 (eq 6). The small slope value for mussels is in contrast with the more negative slopes (-0.4 to -0.8) observed for halogenated hydrocarbons in fish (55-58), indicating that food-mediated transport significantly contributes to the mussel-water exchange rates of hydrophobic contaminants. Model Results. Modeled SPMD/mussel concentration ratios (eq 5) are shown as a function of log Kow in Figure 6a, using the parameter estimates for k2, BAF, Ksw, and ke from eqs 6 (M. edulis), 7, 8, and 10, respectively. For short exposure times (t , 1/ke and t , 1/k2), the model reduces to
Cs fdwKswke ) Cm Fs(BAF)k2
(11)
which is shown as a thick drawn line in Figure 6a. The numerator in eq 11 is not strongly Kow dependent, because Ksw and ke have an opposing dependency on Kow (log-log slopes of 0.8 and ∼-1, respectively; Figures 4 and 5). The denominator is strongly Kow dependent, because BAF strongly increases with Kow and k2 is nearly independent of Kow (loglog slopes of 0.84 and -0.15, respectively; Figures 2 and 3). After an infinitely long exposure time, both mussels and 3896
9
ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 40, NO. 12, 2006
SPMDs attain equilibrium, and the model reduces to
fdwKsw Cs ) Cm Fs(BAF)
(12)
which is shown as a dashed line in Figure 6a. SPMD/mussel concentration ratios are nearly independent of Kow in this case, because the slopes of both log BAF-log Kow and log Ksw-log Kow are similar (0.84 versus 0.79). At intermediate times, the Cs/Cm ratios are positioned between the model curves for t f 0 and t f ∞. At low Kow values, the model lines are folded along the steady-state line, because a steady state is more quickly attained for low-Kow compounds in both samplers. At high Kow values, the concentration ratios increase toward their steady-state values. The intersection of the model curves for t f 0 and t f ∞ at log Kow ≈ 3 is coincidental. With a different choice of parameters, either curve can move upward or downward, and the curves may even cross. For any choice of parameters, however, the time evolution of the Cs/Cm curves is characterized by an initial attachment to the t f 0 curve, followed by an attachment to the t f ∞ curve, starting at the low log Kow end. The model results are compared to the experimental data in Figure 1b, for a commonly used 30 d exposure time. Although the model correctly describes the shape of the Cs/Cm data for eight studies, the model results are too low by a factor of ∼4, on average. Considering that the model calculation was based on independent estimates of the model parameters Ksw, BAF, ke, and k2 (i.e., without curve fitting), the results are satisfying. The experimental Cs/Cm ratios for two studies are poorly described by the model, particularly in the high log Kow range, where the slope of the model curve is too steep. It is tempting to apply curve fitting of the model to the data, with slopes and intercepts of the relation between log Kow and log Ksw/ log BAF/log ke/log k2 as adjustable parameters. However, the total number of adjustable parameters would be rather large: 3 (log ke) + 2 (log k2) + 2 (log[Ksw/BAF]) ) 7, and this would not yield meaningful results. Therefore, basic reasoning should be applied to select the most promising parameters for curve fitting. The first candidate is the intercept of the log BAF-log Kow relation, which may vary among studies by an order of magnitude (Figure 3, eq 7). The effect of decreasing the intercept of the log BAF - log Kow relation by 0.5 and 1.0 log unit is to shift the Cs/Cm curve upward by the same amount (Figure 6b), due to the fact that Cs/Cm is inversely proportional to BAF (eq 5). The second factor that may vary among studies is the sampling rate of SPMDs. Huckins et al. (35) have shown that sampling rates for field-exposed SPMDs (Rs,field) may differ
TABLE 1. Results of Fitting the Model to the Logarithm-Transformed Cs/Cm Ratios, Using the log BAF-log Kow Intercept (a0,BAF) and the log ke-log Kow Intercept (a0,ke) as Adjustable Parameters
a
study
a0,BAF ( s
a0,ke ( s
residual error
Axelman et al. (4) Baussant et al. (39) present study Granmo et al. (37)a Herve et al. (1) Hofelt and Shea (3)b Peven et al. (7) (24 d data) Peven et al. (7) (64 d data) Prest et al. (36) Richardson et al. (38, 40) Utvik et al. (5) all data from Figure 1b
0.50 ( 0.16 0.06 ( 0.09 -0.44 ( 0.15 -1.94 ( 4.25 -0.92 ( 0.09 -1.74 ( 0.86 -0.32 ( 0.15 -0.47 ( 0.09 -0.92 ( 0.17 -0.63 ( -0.09
-0.94 ( 0.22 -0.46 ( 0.18 -0.89 ( 0.18 -2.09 ( 4.55 -0.84 ( 0.14 -1.67 ( 0.91 -0.65 ( 0.21 0.35 ( 0.35 -1.10 ( 0.22 -0.96 ( 0.12
0.21 0.23 0.24 0.98 0.26 0.25 0.47 0.40 0.40 0.55
No parameters estimated, only four compounds.
b
No convergence.
TABLE 2. Dissipation Rate Constants (ke, d-1) of Performance Reference Compounds in SPMDsa site 1
phenanthrene-d10 PCB4 PCB29 chrysene-d12 a
site 2
site 3
site 4
site 5
all sites
ke (d-1)
CV (%)
ke (d-1)
CV (%)
ke (d-1)
CV (%)
ke (d-1)
CV (%)
ke (d-1)
CV (%)
ke (d-1)
CV (%)
0.090 0.048 0.010 0.0056
6 13 10 8
0.092 0.051 0.011 0.0051
2 2 1 4
0.084 0.049 0.009 0.0036
-
0.086 (0.112) 0.011 0.0052
-
0.096 0.056 0.012 0.0073
7 2 1 10
0.090 0.051 0.011 0.0054
5 7 11 25
Coefficients of variation (CVs, %) of the ke estimates are based on the analysis of duplicate samplers.
from the values observed in calibration studies (Rs,cal) by a constant factor, the exposure adjustment factor (EAF), that is relatively independent of Kow:
Rs,field ) (EAF)Rs,cal
(13)
Since the elimination rate constant (ke) is linearly proportional to Rs (eq 9), the same EAF applies to differences in ke values for field-deployed SPMDs (ke,field) and ke values observed in calibration studies (ke,cal), which gives after logarithm transformation
log ke,field ) log ke,cal + log EAF
(14)
This effect therefore results in an intercept of the log ke-log Kow curve (eq 10) that varies among studies. Increasing this intercept by 0.5 and 1.0 log unit causes a broader range of compounds to attain their steady-state Cs/Cm ratio (Figure 6c). In the high log Kow range, increasing the log ke-log Kow intercept results in an increase of the Cs/Cm ratios by 0.5 and 1.0 log unit, because these compounds will be in the linear uptake stage, where Cs is linearly proportional to Rs, and hence to ke (eq 9). The logarithm-transformed concentration ratios for the individual studies were fitted to the model, using the two intercepts mentioned above as adjustable parameters (Table 1). The log BAF-log Kow intercepts attain values of -0.69 ( 0.79, which are similar to the values found in bioaccumulation studies (-0.49 ( 0.41, eq 8). The a0,ke estimates, excluding the extremely high value obtained for the data reported by Richardson et al. (38, 40), range from -2.09 to -0.46, suggesting that the water sampling rates in the field were 3 times lower to 10 times higher (1-40 L d-1) than for the laboratory calibration studies. The deviations observed for the data from Richardson et al. (38, 40) and Hofelt and Shea (3) may be explained by assuming that all compounds attained their equilibrium concentration in SPMDs (3). However, >90% equilibrium attainment in 30 days requires ke values in excess of 0.077 d-1. Compounds with log Kow )
7 (log Ksw ) 6.4, eq 8) absorbed by standard-design SPMDs (Vs ) 5.0 mL) would have to be sampled at a rate >970 L d-1 (eq 9). Although Rs values up to 100 L d-1 have been reported in calibration studies with unshielded SPMDs at flows of 90 cm s-1 (30), these values are not likely to be encountered for caged SPMDs at moderate flows. The small log(Cs/Cm)-log Kow slopes observed for these two studies may also be caused by slow uptake kinetics by mussels, resulting in concentrations that are smaller than their equilibrium values, particularly for highly hydrophobic compounds. Data from depuration studies (Figure 2) suggest that half-life times in mussels are between 3 and 46 d. On some occasions, much longer equilibration times are reported: >90 d (8), .130 d (59), .60 d (60). Although it is well established that bivalves can adjust their ventilation rates in response to changes in environmental conditions (see the Introduction), the in situ monitoring of mussel-water exchange kinetics is difficult to monitor in situ. Finally, incomplete removal of particles that are attached to the SPMD surface may also result in smaller slopes of log(Cs/Cm) versus log Kow. However, the amount of attached particles would have to be larger than about 30 mg of organic carbon/SPMD to have a noticeable impact (section H, Supporting Information). Control of Critical Factors. The BAF largely controls organic contaminant accumulation in mussels for exposure times larger than 2-3 half-lives. The scatter in experimental BAF values is large (∼0.4 log unit), even when evidently anomalous BAFs are excluded (Figure 3). Moreover, interannual differences in BAF values may amount to about 1 order of magnitude (23). Although part of the variation in BAF values may originate from the difficulty of reliably measuring aqueous concentrations, a substantial contribution originating from differential responses of mussels to differences in exposure conditions (on temporal, vertical, and horizontal scales) cannot be excluded. The in situ sampling rate is the critical factor for contaminant sampling by SPMDs. Information on this parameter can be obtained from the dissipation of the PRCs VOL. 40, NO. 12, 2006 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
9
3897
(32, 34, 35, 52). PRC-based dissipation rate constants (ke) can be estimated from (35)
ke ) -[ln(N/N0)]/t
(15)
where N0 is the PRC amount spiked into the SPMDs prior to exposure and N is the amount detected after the exposure. For the present study, ke estimates could be obtained for four PRCs at all sites (Table 2). The dissipation of PCB155 and PCB204 was insignificant (>90% retained), and the amounts of acenaphthene-d10 detected in the exposed samplers were below the quantitation limit (
