Article pubs.acs.org/est
Two-Compartment Kinetic Modeling of Radiocesium Accumulation in Marine Bivalves under Hypothetical Exposure Regimes Pan Ke,†,‡ Qiao-Guo Tan,§ and Wen-Xiong Wang*,†,‡ †
Division of Life Science, The Hong Kong University of Science and Technology (HKUST), Clear Water Bay, Kowloon, Hong Kong HKUST Shenzhen Research Institute, Shenzhen 518057, China § Key Laboratory of the Coastal & Wetland Ecosystems, Ministry of Education, College of the Environment & Ecology, Xiamen University, Xiamen, Fujian 361102, China ‡
S Supporting Information *
ABSTRACT: Interpreting the variable concentrations of 137Cs in the field biological samples requires mechanistic understanding of both environmental and biological behavior of 137Cs. In this study, we used a two-compartment model to estimate and compare the 137Cs biokinetics in three species of subtropical marine bivalves. Significant interspecific difference of 137Cs biokinetics was observed among oysters, mussels, and scallops. There was considerable 137Cs assimilation from phytoplankton in the bivalves, but the calculated trophic transfer factors were generally between 0.04 and 0.4. We demonstrated a major efflux of radiocesium in the scallops (with a rate constant of 0.207 d−1), whereas the efflux was comparable between oysters and mussels (0.035−0.038 d−1). A two-compartment kinetic model was developed to simulate the 137Cs accumulation in the three bivalves under four hypothetical exposure regimes. We showed that the bivalves respond differently to the exposure regimes in terms of time to reach equilibrium, equilibrium concentration, and maximum concentration. Bivalves suffering more frequent intermittent exposure may have higher maximum concentrations than those receiving less frequent exposure. The interspecific difference of 137Cs accumulation in bivalves has important implications for biomonitoring and implementing management techniques. This study represents one of the first attempts to combine both dissolved and dietary pathways to give a realistic simulation of 137Cs accumulation in marine bivalves under dynamic exposure regimes.
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and season.9−11 For example, the decrease of 137Cs in marine invertebrates after Fukushima accident varied greatly in different mollusc species.12,13 Interpreting the concentration data requires a mechanic understanding of both environmental and biological behavior of 137Cs. Moreover, understanding the interspecific difference of 137Cs bioaccumulation in bivalves is very useful for choosing the best candidate species for biomonitoring of 137Cs contamination. Bivalves in field environments are subjected to dynamic exposure regimes, for example, long-term stable exposure in pristine areas or exponential exposure during accidental release of 137Cs. With the repeated releases that occurred over months, the Fukushima accident has brought up the urgent need of models that can deal with complex source terms.14,15 Predicting the radionuclide concentration in aquatic organisms is usually based on the steady-state approach, in which equilibrium is assumed between organism and ambient 137Cs.16−18 The equilibrium modeling may be appropriate for the situations where organisms are subjected to long-term stable exposure.
INTRODUCTION On 11 March, 2011, catastrophic earthquake resulting in the failure of Fukushima Dai-ichi nuclear power plant and the massive release of radionuclides into marine environments rekindled the considerable interest to investigate the ecological impacts of radionuclide releases on marine biota.1−4 Among the many artificial radionuclides, radiocesium (137Cs and 134Cs) has drawn the utmost attention because of their long physical halflives and residence times in the water column. Being a highly soluble radionuclide, radiocesium also raises a major concern about its potential biomagnification at higher trophic levels in aquatic food chains.5 Understanding the transfer of radiocesium from radioactive effluent to biota is therefore critical for a realistic assessment of its potential detrimental effects on human health. Much work has been conducted regarding the 137Cs concentrations in field-collected marine organisms. Bivalves are of particular interests in this regard since they serve as important seafood for human consumption and bioindicators of contaminant exposure. Previous studies have indicated that the 137 Cs bioaccumulation varies among different taxonomic groups of bivalves.6−8 Field evidence have also showed that bivalves carry highly variable 137Cs concentrations which are influenced by factors such as geographical origin, exposure regime, species, © XXXX American Chemical Society
Received: November 5, 2015 Revised: January 27, 2016 Accepted: January 29, 2016
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DOI: 10.1021/acs.est.5b05445 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology However, routine releases from nuclear power plants (NPP) may not be stable because they depend on specific operations within the reactors. Also, radionuclide concentrations in water change rapidly in the accidental release of radioactive contaminant. As a result, equilibrium does not exist between organisms and water, and kinetic modeling approach is more suitable for the prediction of 137Cs bioaccumulation in these scenarios. There have been many studies on the kinetic modeling of 137Cs accumulation in fish, but most of these studies are restricted to single pulse inputs.15,19−21 Moreover, less attention has been given to the biota comprising the food chains that lead to fish, such as marine bivalves.22,23 To model the 137Cs accumulation in marine bivalves, rate constants including uptake rate from seawater, assimilation efficiency for phytoplankton, and efflux rate are required to make the predictions. 137Cs bioaccumulation is a dynamic balance between the uptake and elimination of the metal. It is important to link the two processes to give rigorous and realistic measurements of kinetic parameters. Previous studies assumed minor effects of efflux process in the estimation of the dissolved uptake constant and assimilation efficiency for metals.24,25 Such assumption may underestimate the accumulation of metals, especially for those metals with high turnover rates such as 137Cs. It has been shown that the biological halflives of 137Cs in mussels were between 4 and 8 days,26,27 indicating that it is necessary to consider the effects of 137Cs efflux when measuring 137Cs uptake and assimilation. However, few studies have attempted to incorporate efflux rate constant in the estimation of 137Cs uptake and assimilation.11,28 In this study, we quantified the biokinetics of 137Cs in three different marine bivalves, including the oyster Saccostrea cucullata, the mussel Septifer virgatus, and the scallop Chlamys nobilis, all of which have been suggested to be useful biomonitors for radionuclides.7,10 The 137Cs uptake from seawater, assimilation from phytoplankton, and elimination rates in the bivalves were measured at first. A two-compartment kinetic model was then developed accordingly to couple the influx and efflux processes for parameter estimations. Finally, the model with the estimated parameters was used to predict 137 Cs accumulation in the bivalves under different exposure scenarios, with an aim to improve our knowledge of the interspecific variations of the 137Cs bioaccumulation and its causes.
Figure 1. Schematic of a two-compartment model to simulate accumulation in marine bivalves.
Jin (t ) = k u × Cw(t ) + AE × IR × Cf (t )
dC1(t ) = Jin (t ) − (ke1 + g + k12) × C1(t ) dt
(2)
dC2(t ) = C1(t ) × k12 − (ke2 + g ) × C2(t ) dt
(3)
(4)
where ku is the uptake rate constant of 137Cs from the dissolved phase (L dry g−1 d−1). AE is the assimilation efficiency of dietary 137Cs. IR is the ingestion rate (dry g g−1 d−1); Cf is the 137 Cs concentration in the ingested phytoplankton (Bq dry g−1), which is the product of Cw and concentration factor (CF) for the ingested particles. CF is applied assuming that the equilibrium between dissolved 137Cs and its sorption onto phytoplankton is generally rapidly attained. g is the bivalve specific growth rate constant (d−1). k12 is the rate constant for 137 Cs being transferred from compartment one to two (d−1). Under steady-state, dC1(t)/dt = 0 and dC2(t)/dt = 0, the 137Cs concentration in bivalves can be calculated from eqs 1−3: ⎛ k12 C int,ss = ⎜1 + k ⎝ e2 +
⎞ Jin (t ) ⎟ g ⎠ k12 + ke1 + g
(5)
137
The trophic transfer factor (TTF) for Cs is the ratio of the steady-state tissue 137Cs concentration in a predator relative to that in its prey. Calculation of TTF only considers the fraction of the 137Cs accumulated from dietary pathway, that is, Jin(t) = AE × IR × Cf(t). TTF can be calculated using eq 5 as followed: TTF =
⎛ k12 ⎞ AE × IR = ⎜1 + ⎟ Cf (t ) ke2 + g ⎠ k12 + ke1 + g ⎝
C int,ss
(6)
137
MATERIALS AND METHODS Two-Compartment Model to Predict 137Cs Bioaccumulation in Bivalves. The accumulation of 137Cs in bivalves can be simulated using a two-compartment kinetic model.29,30 The kinetic processes include 137Cs influx from water and food, the transfer of 137Cs between water and food, 137Cs efflux, and growth dilution of 137Cs. 137Cs is assumed to be first accumulated into compartment one from seawater or food, and is then transferred to compartment two. Efflux of 137Cs occurs in both compartments (Figure 1). (1)
Cs
Cint(t) is the weight-specific radioactivity of 137Cs remaining in bivalves on dry weight basis (Bq g−1). C1(t) and C2(t) are the weight-specific radioactivity distributed in compartment one and two (Bq g−1), both of which were also normalized to the dry weight of the whole bivalves. Jin(t) is the 137Cs influx rate from dissolved and dietary pathways (Bq dry g−1 d−1). The influx rate of 137Cs in bivalves can be expressed as
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C int(t ) = C1(t ) + C2(t )
137
Bivalves and the Radioisotope Cs. The scallops Chlamys nobilis were obtained from the Dapeng Bay of Hong Kong. The oysters Saccostrea cucullata and black mussels Septifer virgatus were collected from a rocky shore in the Clear Water Bay, Hong Kong. Bivalves with relatively uniform size of 3−4 cm shell height were collected for our experiments. After collection the bivalves were carefully cleaned of their epibionts and acclimated in aerated natural seawater (33 psu, 25 ± 0.5 °C, pH: 8.0 ± 0.2) for at least 1 week, during which the bivalves were fed with the diatom cultures of Chaetoceros gracilis. The radioisotope 137Cs (137CsCl in 0.1 M HCl, radionuclidic purity> 99.5%) was used to quantify the Cs kinetics in bivalves, which was purchased from National Centre for Nuclear Research Radioisotope Centre, Otwock, Poland. Experimental Procedure for Measuring 137Cs Kinetics in Bivalves. The ku, AE, and ke were measured using well established methods. To measure the ku of 137Cs in bivalves, 25 bivalves of each species were placed individually into beakers filled with 200 mL of 0.22 μm filtered seawater spiked with 74 B
DOI: 10.1021/acs.est.5b05445 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology
Figure 2. Accumulation of 137Cs from seawater (A), 48 h depuration of 137Cs after ingestion of radiolabeled algae (B), and loss of 137Cs after 7 day combined exposure of 137Cs (C) in marine bivalves. The dots are measured values and the lines are modeled values. C1(t), C2(t), and Cint(t) are the radioactivity (or its percentage) remained in compartment one, two, and whole body. Data are mean ± SD (n = 5 for A, B, and 10 for C).
kBq L−1 of 137Cs. The aqueous exposure experiment was conducted under 25 °C and last for 10 h. Five replicated animals were randomly sampled at every 2 h interval. Aliquots of the seawater (3 mL) were sampled to measure the variations of radioactivity in the water before and after exposure. Only minor decrease of radioactivity in seawater was observed (300 days).13,37 Our results also suggest that oysters are more appropriate to be used as biomonitor of 137Cs contamination than mussels and scallops, as oysters are more readily to accumulate 137Cs from ambient environment. Figure 5C and D shows the Cs accumulation in the bivalves when receiving intermittent exposure of 137Cs. The bivalve 137 Cs concentrations at first fluctuate with the seawater 137Cs and finally reach a dynamic equilibrium. Figure 5C also illustrates that the 137Cs concentrations in the bivalves actually drop quickly with the decrease of 137Cs level in seawater. This generates important implications for sampling practice in biomonitoring. When using bivalves to monitor 137Cs contamination, the sampling interval should be short enough in order to capture the discharge pattern or magnitude of 137Cs release from NPP, especially in the monitoring activities of an accident release. The simulated results also show that the interval of 137Cs pulses affects the maximum 137Cs concentrations in bivalves. When 137Cs concentration in seawater is kept under a certain level (i.e., 100 Bq L−1), bivalves suffering more frequent intermittent exposure may have higher maximum concentrations (or BAF) than those received less frequent exposure. Our results also have implications for environmental management of discharges of radionuclides in the operation of NPP in which routine release of radionuclides occurs. One of the basic tenets of the philosophy in radioecological management is that all exposures to manmade sources of radiation should be reduced as far as possible to be well below the maximum limits. Our study suggest that, in order to keep the 137Cs levels under safety limit (i.e., 100 Bq wet kg−1), attention may be paid to the manner of discharge and the biological response of 137Cs when implementing management techniques. In our study, significant interspecific difference of 137Cs biokinetics was observed in oysters, mussels, and scallops. Our model estimation indicates that there is considerable 137Cs assimilated from phytoplankton in the bivalves. However, no evidence supports biomagnification of 137Cs in the phytoplankton-bivalve food chain. The dissolved and dietary pathway can be similarly important for the bioaccumulation of 137Cs, which largely depends on the partitioning of 137Cs between seawater and the ingested particles. High efflux rates were observed in the bivalves, indicating fast turnover of 137Cs in the subtropical bivalves. The three bivalves responded differently to the exposure regimes, in terms of the time to reach equilibrium, the equilibrium concentration, and the maximum concentration. The interspecific difference of 137Cs bioaccumulation in bivalves should be considered in biomonitoring and risk management.
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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.5b05445.
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AUTHOR INFORMATION
Corresponding Author
*Phone: (852) 23587346; fax: (852) 23581559; e-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank Gao Shi for his help with the experiments, and the anonymous reviewers for their comments on this work. This study was supported by an Environment and Conservation Fund (ECWW11SC03) and a Key Project from the National Natural Science Foundation (21237004).
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