Temporal changes in 137Cs concentrations in fish, sediments, and

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Temporal changes in Cs concentrations in fish, sediments, and seawater off Fukushima Japan Cuiyu Wang, Robert M. Cerrato, and Nicholas S. Fisher Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b03294 • Publication Date (Web): 15 Oct 2018 Downloaded from http://pubs.acs.org on October 19, 2018

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Environmental Science & Technology

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Main text of Temporal changes in 137Cs concentrations in fish,

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sediments, and seawater off Fukushima Japan.

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Cuiyu Wang, Robert M. Cerrato, and Nicholas S. Fisher

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1 ACS Paragon Plus Environment


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Temporal changes in 137Cs concentrations in fish,

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sediments, and seawater off Fukushima Japan

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Cuiyu Wang*, Robert M. Cerrato, and Nicholas S. Fisher

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School of Marine and Atmospheric Sciences, Stony Brook University

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Stony Brook, New York 11794-5000

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Abstract

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We analyzed publicly-available data of Fukushima 137Cs concentrations in coastal fish, in surface

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and bottom waters, and in surface marine sediments and found that within the first year of the

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accident pelagic fish lost 137Cs at much faster rates (mean of ~1.3% d-1) than benthic fish (mean

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of ~0.1% d-1), with benthopelagic fish having intermediate loss rates (mean of ~0.2% d-1). The

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loss rates of 137Cs in benthic fish in the first year were more comparable to the decline of 137Cs

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concentrations in sediments (0.03% d-1), and the declines in pelagic fish were more comparable

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to the declines in seawater. Retention patterns of 137Cs in pelagic fish were comparable to that in

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laboratory studies of fish in which there were no sustained 137Cs sources, whereas the

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benthopelagic and benthic fish species retained 137Cs to a greater extent, consistent with the idea

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that there is a sustained additional 137Cs source for these fish. These field data, based on 13,511

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data points in which 137Cs was above the detection limit, are consistent with conclusions from

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laboratory experiments that demonstrate that benthic fish can acquire 137Cs from sediments,

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primarily through benthic invertebrates that contribute to the diet of these fish.

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Key words

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cesium; radioactivity; Fukushima

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Abstract art

First year after Fukushima accident March 2011- March 2012

Surface Water

Bottom Water

Sediments

Pelagic Fish

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Benthopelagic Benthic Fish Fish


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Introduction

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Damage to the Fukushima Dai-ichi nuclear power plant (FDNPP) in March 2011 resulted in a

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massive release of radionuclides into Japanese coastal waters. Immediately after the accident,

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various governmental agencies launched coordinated activities to comprehensively monitor the

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fate of the released radionuclides from FDNPP to the marine environment and fishery products.

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Until January 2017, over 3000 seawater samples, nearly 2000 sediment samples, and more than

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10,000 marine fish collected off Fukushima prefecture were analyzed for Fukushima-derived

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radionuclides. These data are generally available online to the public.

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Surface seawater1, subsurface seawater2, marine sediments3-5 and biota in local5, 6 and distant

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waters7 were found to be contaminated with cesium isotopes (134Cs and 137Cs). In marine fish, Cs

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mainly concentrates in muscle8-10 which is the principal part consumed by seafood eaters.

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Therefore, the relatively long half-life of 137Cs (t1/2 = 30.17 y) has led to continuing concern

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about public health implications of these released nuclear fission products for seafood

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consumers11. Fishery activities were restricted in the areas off the shore of Fukushima Prefecture,

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many fish species were listed as restricted foodstuffs for shipment by the Japan Ministry of

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Health, Labor and Welfare, and fish exports faced the restriction of foreign governments12. The

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fishery industry consequently experienced a serious decline after the accident13.

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Buesseler, citing the monitoring results within the first year after the accident, reported that

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radiocesium concentrations were higher in benthic fish than in pelagic fish14. The Fisheries

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Agency of Japan15 and several other independent studies6, 16 reported similar findings. A central


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hypothesis to help explain this pattern of fish contamination has been that marine sediments

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serve as a continuous source of radiocesium for benthic animals, and benthic fish assimilate Cs

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through a diet of invertebrates associated with the sediment17. This hypothesis is consistent with

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the persistent radiocesium contamination in the sediments in the region18 and over 40 species of

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benthic invertebrates caught in the region19.

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The ocean discharge of radioisotopes from FDNPP peaked on April 6, 2011. In May 2011, the

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levels of 137Cs in seawater immediately offshore of the power plant had declined by 3 orders of

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magnitude20, likely due to dilution and dispersal by ocean currents and mixing processes21.

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About six months after the accident, it was estimated that more than 90% of the radiocesium in

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sediment had accumulated in regions shallower than 200m4. The concentration of 137Cs in marine

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sediment was highly heterogeneous22. Most of these studies focused on biota or seawater or

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sediment contamination separately. For example, spatial and temporal distributions of 137Cs were

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reported only in sediment3, 4 or only in seawater1, 2, 20. Wada et al. reported the 134+137Cs decline

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rates in pooled pelagic and benthic fish, and some representative species from both ecological

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groups6. Iwata et al. compared the biological half-lives of 137Cs in 16 species of benthic

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invertebrates and fish23. However, only a few studies evaluated the 137Cs contamination in

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different matrices simultaneously and related 137Cs concentrations in these different components

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of the marine ecosystem to one another. Sohtome et al. reported similar decline rates of 137Cs in

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marine benthic invertebrates and sediments5. Tagami and Uchida estimated the contribution of

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137Cs

in contaminated sediment and seawater to Japanese rockfish Sebastes cheni24.

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No studies have evaluated 137Cs patterns in marine fish of different ecological groups and related

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them to contamination in ambient water and sediment. Thus, this study explores the patterns of

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137Cs

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contamination in surface, bottom seawater and in sediments.

contamination in different groups of fish and compares them with patterns of 137Cs

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In general, marine animals acquire Cs from both aqueous and dietary sources17, 25-28. Depending

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on prey selection, ingestion rate and contamination levels in water and diet, both aqueous25 and

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dietary sources17, 25, 26 can contribute a significant portion of Cs to the overall body burden in an

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animal28. Benthic invertebrates, many being the prey of benthic fish, live in or on marine

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sediments, and have feeding behaviors tightly associated with sediment exposure. They may

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serve as important conduits for radiocesium from sediment to benthic fish that feed on them17, 28.

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Apart from acquiring 137Cs from their diet, bottom-dwelling fish may also acquire 137Cs from the

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dissolved phase in bottom waters, which is derived from desorbed 137Cs from contaminated

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sediment. Such routes of metal uptake in benthic animals have been described for a wide variety

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of other contaminant metals in coastal ecosystems29, 30. However, the degree to which this occurs

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with 137Cs in marine ecosystems remains poorly understood. Regardless of diet or aqueous

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pathways, the sediments can potentially serve as the ultimate source of 137Cs for these bottom-

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dwelling fish in waters off the east coast of Japan.

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The data of 137Cs contamination in fish off Fukushima collected by Japanese authorities are the

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most comprehensive datasets of radionuclide contamination in marine ecosystems. The goal of

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this study was to use these valuable data to describe the patterns of 137Cs contamination in

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individual fish species and in different ecological groups (pelagic, benthopelagic and benthic


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species) in eastern Japanese coastal waters. Further, it was envisioned that comparing the

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temporal trends in 137Cs contamination in fish, seawater and sediment could provide important

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inferences about key sources of 137Cs in fish of different ecological groups. As noted above, prior

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studies reported declines of 137Cs levels over time in fish23. However, only for benthic

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invertebrates5 and one species of benthic fish24 were 137Cs declines related to water and sediment

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concentrations. Our study is the first to relate temporal declines of 137Cs concentrations in marine

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fish with those in sediments and water in the field, and used a comprehensive field data set to test

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the hypothesis that contaminated marine sediments have provided an ongoing source of

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radiocesium for benthic biota. Our statistical analyses focused primarily on field data obtained

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during the first year after the accident during which time all fish samples had radiocesium levels

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above reported detection limits.

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Materials and Methods

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137Cs

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from data available on the websites of the Fisheries Agency of Japan and Nuclear Regulation

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Authority of Japan. Both 134Cs and 137Cs were decay-corrected to the time of the accident and

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provided in these databases32,33 . As fish caught off Fukushima had higher 137Cs concentrations

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than those from the prefectures to the north and the south14, we chose to analyze data only from

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fish that were landed off Fukushima and from seawater and sediment stations from comparable

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locations (Fig. 1). 137Cs concentrations were expressed in Bq kg-1 (on a wet weight basis) in both

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fish and sediment, or in Bq L-1 in seawater32,33.

concentration data in fish, surface seawater, bottom seawater and sediment were collected

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While both Cs isotopes behave similarly, we only analyzed 137Cs because its radiological half-

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life (30.1 years) is longer than that of 134Cs (2.1 years); consequently, radioactivity levels in biota,

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seawater and sediment are less subject to radioactive decay during our study period (2011-2016).

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As Cs mainly concentrates in the muscle of marine organisms8-10, we used muscle tissue

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concentrations to represent the Cs concentration in fish. We quantified 137Cs loss patterns for the

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first year after the accident to follow the initial 137Cs contamination in fish directly from the

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power plant discharge, rather than 137Cs that may have undergone cycling within the marine

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environment (including seawater and sediments). For analyses that reported lower limits of

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detection, the 137Cs activities were greater than the detection limit for this radionuclide in all fish

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captured within one year of the accident. That is, none of the fish samples had 137Cs

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radioactivities below the detection limits, including for all 36 fish species (regardless of pelagic

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or benthic habitats) considered in this study within the first year. The first 137Cs non-detects in

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fish were observed at 381 days after the accident.

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Over the 5-year period following the accident, 137Cs concentrations were analyzed in 102

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samples of 3 selected species of pelagic fish, 963 samples of 7 selected species of benthopelagic

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fish, and 7400 samples of 26 selected species of benthic fish. Seawater samples analyzed

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included 2042 surface and 2104 bottom samples. Over this 5-year period, 91% of pelagic fish

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samples, 70% of benthopelagic fish, and 60% of benthic fish had 137Cs activities below detection

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limits; 28% of surface seawater samples and 25% of bottom seawater samples had 137Cs below

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detection limits. It is recognized that the fish that had 137Cs concentrations below the detection

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limit may have migrated into the sampling area from relatively uncontaminated regions and may

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never have been contaminated with 137Cs; thus including them in regression analyses could


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complicate interpretation of the temporal trends in the 137Cs concentrations, so they were not

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included in the regression analyses.

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Fish were categorized as pelagic, benthopelagic and benthic fish based on their diet and

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information provided by Fishbase34. Diet studies of the species of interest are listed in Table S1.

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Sandlance is placed into the pelagic grouping since it feeds primarily in the water column,

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although it is recognized that it burrows into marine sediments (Table S1). Species with more

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than 10 observations were selected to ensure enough data for analysis. A total of 3 pelagic, 7

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benthopelagic, and 26 benthic fish species were selected.

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To analyze the temporal trend of 137Cs concentrations in fish, seawater and sediment, we used

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log transformed linear regression analysis. We chose this regression function because

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exploratory data analysis indicated that 137Cs concentrations in pelagic fish, surface seawater and

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bottom seawater decreased exponentially over time and had highly skewed residual distributions.

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To compare the loss coefficients in fish, seawater, and sediments, 137Cs concentrations were

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natural log transformed and fit to a linear function of time:

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ln(137Cs) = a + bt + 

(Equation 1)

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where b is the loss coefficient (d-1) of the ln(137Cs) concentrations in samples, t represents the

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time in days since the date of the FDNPP accident on 11 March 2011, and  is the residual,

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which is assumed to be normally distributed with a mean of 0 and an unknown standard

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deviation. In order to distinguish interspecific 137Cs depuration patterns within each ecological



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group, regression analysis was conducted for individual fish species. Additionally, regression

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analyses of pooled species of the three ecological groups were performed to compare differences

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among these groups.

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To better understand the loss of 137Cs in fish off Fukushima over the first year after the accident,

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we compared the estimated loss coefficients for different marine fish to depuration estimates

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from various laboratory studies (Table S2). Published loss coefficients range from 0.008 to 0.05

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d-1, therefore we considered a range of 0.01 and 0.05 d-1 in the present study.

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Dunnett’s test35, 36 with adjusted degrees of freedom was used to compare the 137Cs loss

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coefficients in benthic fish with sediments, in benthopelagic fish with surface seawater, bottom

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seawater and sediments, and pelagic fish with surface seawater. The minimum significant

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difference between the estimated loss coefficient 𝑏𝑖 of species 𝑖 (𝑖 = 1,…,𝑘) and the coefficient 𝑏𝑠

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for sediment or seawater is given by

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1/2

𝑀𝑆𝐷𝑖 = 𝑞𝛼,𝑘,𝑣(𝑠2𝑏𝑖 + 𝑠2𝑏𝑠)

(Equation 2)

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where 𝑠𝑏𝑖 is the standard error of the loss coefficient of species i from a group of k species, 𝑠𝑏𝑠 is

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the standard error of the loss coefficient in sediment or seawater, and 𝑞𝛼,𝑘,𝑣 is the critical value of

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the Dunnett test with family error rate 𝛼, number of comparisons 𝑘, and degrees of freedom 𝑣37.

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To account for heterogeneous residual error variances between fish, sediment, and seawater, the

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degrees of freedom in the tests were adjusted to

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𝑣=

(𝑠2𝑏𝑖 + 𝑠2𝑏𝑠)2 2

2

(𝑠2𝑏𝑖) (𝑛𝑖

(𝑠2𝑏𝑠)

― 2)

+ (𝑛 𝑠

(Equation 3)

― 2)

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as suggested by Games and Howell38. In this equation, 𝑛𝑖 is the number of individuals of species

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𝑖 and 𝑛𝑠 is the number of sediment or seawater samples. All analyses were carried out at a

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family error rate of 0.05. Critical values for Dunnett’s test were obtained from the qNCDun()

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function in the nCDunnett library of R39.

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Results and Discussion

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By analyzing the 137Cs concentrations in marine fish, seawater and sediment off Fukushima from

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2011 to 2016, we gained an overview of 137Cs contamination and attenuation in the ecosystem

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off Fukushima after the nuclear accident. Long-term contamination of 137Cs in many marine fish

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species, seawater and marine sediment was observed, but the rate of decline of 137Cs

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concentrations in fish varied among ecological groups and species during the first year after the

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FDNPP accident. Generally, benthic fish were shown to have a lower rate of loss of 137Cs over

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time than other fish.

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Relating 137Cs declines in fish with water and sediment in the first year

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When data for species in an ecological group were pooled, 137Cs concentrations in pelagic and

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benthopelagic fish but not benthic fish declined more slowly over the first year than the seawater

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they contacted (Fig. 2). The loss coefficient in 137Cs concentrations was -1.2% d-1 for the pelagic

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group (p < 0.001) compared to -2.3% d-1 for surface seawater (p < 0.001) (Fig. 3). The loss

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coefficient in 137Cs concentrations was -0.2% d-1 for the benthopelagic group (p < 0.05) and -0.9% 11 ACS Paragon Plus Environment


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d-1 in bottom seawater (p < 0.001). There was little difference in the loss coefficient for benthic

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fish (-0.1% d-1, p < 0.01) and sediments (0.03% d-1), and notably the loss coefficient for

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sediments was not significant (p = 0.78).

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Loss coefficients were heterogeneous among species within an ecological group, probably

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reflecting life history and habitat variability (Fig. 3), and while individual pelagic and benthic

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species tended to reflect the pooled results, differences between individual and pooled species

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were evident for benthopelagic fish. The loss coefficients in 137Cs concentrations ranged from -

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0.9 to -1.5% d-1 in pelagic species and all were significantly different from surface seawater at a

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family error rate of 0.05 (Table S3). Loss coefficients ranged from -0.8 to 0.4% d-1 in benthic

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species and significantly differed from sediments in only 2 of 26 species (Table S4). In contrast

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to these two ecological groups, the analysis of individual benthopelagic species did not reinforce

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the pooled result. Only 1 of 7 species differed significantly from that of sediment, and only 3 of

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7 species differed significantly from the loss coefficient for bottom seawater (Table S5). Loss

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coefficients ranged from -0.07 to -0.63% d-1 in benthopelagic species.

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The higher 137Cs concentrations typically observed in benthic fish might be caused by higher

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initial 137Cs contamination following the accident, or slower depuration of the 137Cs. Most

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studies focused on the depuration rates6, 24, 40 rather than the initial contamination levels. Our

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analysis of the data (Figs. S1, S2) showed that, among the fish of the 3 ecological groups

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considered here, the initial contamination of 137Cs was highest in the pelagic species Japanese

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sandlance A. personatus (7200 Bq kg-1), followed by the benthic species olive flounder P.

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olivaceus (2250 Bq kg-1) and the benthopelagic species brown hakeling P. maximowiczi (885 Bq


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kg-1). This comparison highlighted that the generally higher 137Cs concentrations found in

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benthic fish was not due to the higher initial 137Cs contamination; therefore, slower net loss of

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137Cs

is more likely to be the reason. This may be due to the proximity to a sustained source of

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137Cs

(sediments) for the benthic fish, either through dermal contact, exposure to bottom waters

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that remain contaminated because of 137Cs desorption from contaminated sediments, or

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invertebrate prey contaminated from sediment exposure17.

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The average 137Cs concentration in 2011 was highest in pooled pelagic fish, as the initial

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contamination levels in the Japanese sandlance is very high and the sample size (n=102) is

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smaller compared to that of the pooled benthopelagic (n=963) and benthic fish (n=7400) groups

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(Fig. S1). However, in 2012 the average 137Cs concentration in pooled pelagic fish was lower

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than that in both pooled benthopelagic and benthic species. There were no reports comparing the

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contamination of 137Cs in pelagic or benthic fish to that in benthopelagic fish, which includes

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many important commercial species, such as Pacific cod G. macrocephalus, nibe croaker N.

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mitsukurii, John dory Z. faber, flounder P. japonicus, drum A. argentatus, dory Z. nebulosa and

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brown hakeling P. maximowiczi. Many studies considered them as benthic species; however,

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these species have significant portions of their diet from both the pelagic and benthic habitat,

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thus they should be grouped independently. The average 137Cs concentration was lower in pooled

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benthopelagic fish than that in benthic fish from 2011 to 2016 (Fig. S1).

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Our analysis showed that during the first year after the accident, the loss coefficients of 137Cs

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concentrations in marine fish were species-specific and ecological group-specific. While there

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was considerable interspecific variability, regression analysis showed that within the first year of



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the accident, pelagic fish lost 137Cs at much faster rates (mean of ~1.3% d-1) than benthic fish

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(mean of ~0.1% d-1), with benthopelagic fish having intermediate loss rates (mean of ~0.2% d-1).

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Wada et al. reported radiocesium concentrations in field populations of several species of marine

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fish in the region for which we calculated loss coefficients.6 These concentrations were similar to

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those found in this study (Table S6), except for sandlance, possibly because their dataset did not

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contain samples with extremely high Cs contamination levels. In this study, the decline rate (SE)

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of 137Cs in Japanese rockfish S. cheni caught off Fukushima was 0.20.3% d-1 (Fig. 3). It was

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around 0.2% d-1 in the same species caught off two stations that were within 10 km of the

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FDNPP24. Matsumoto et al. reared 23 individuals of the same species contaminated by the

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FDNPP accident and caught off Fukushima prefecture, and they reported40 a decline rate (SE)

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of 0.30.02% d-1. Although the standard errors of the decline rates in our analyses were large

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(0.3% d-1), the mean value (0.2% d-1) was comparable to that derived from field observations

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reported by Tagami and Uchida24 and the laboratory study of Matsumoto et al.40

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The rates of decline in 137Cs concentrations in benthic fish off Fukushima were lower than the

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lower range of those found in laboratory studies (0.8 to 5% d-1, Table S2, Figs. 4, S3, S4),

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possibly because of a sustained source of radiocesium in Japanese coastal waters and possibly

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because most of the lab studies used juvenile rather than adult fish, and juveniles with higher

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metabolic activities41 may be expected to have higher loss rates of 137Cs. Sustained sources could

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be 137Cs runoff from the land, desorption from contaminated sediments, and consumption of

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benthic prey contaminated from sediment. Pooling data for many species (especially true for

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benthic fish species), greatly reduced the confidence intervals for the 137Cs loss rates due to the

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increase in sample size. Therefore, it is important to acknowledge the wider ranges of the 137Cs 14 ACS Paragon Plus Environment

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loss rates in individual fish of the same ecological group while discussing the different patterns

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of 137Cs concentrations in the three ecological groups. Thus, pooled data weigh each individual

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fish of an ecological group equally, regardless of species, and this accounts for differences

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between mean values among species within an ecological group and pooled values from that

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group. For example, for benthopelagic species, the loss coefficient of 137Cs from pooled data is

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0.2% d-1, whereas the average loss coefficient for individual species within this ecological group

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is 0.37% d-1; similarly, the pooled benthic species had a loss coefficient of 0.1% d-1 and that of

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individual species is 0.20% d-1 (Fig. 3).

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All but one fish species had estimated loss coefficients that were less than the -1 to -5% d-1 range

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observed in laboratory studies which primarily used juveniles (Figs. 3, 4); there is a relative

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paucity of experimental data using adult fish. Of the 36 species analyzed only whitebait, a

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pelagic fish, had an estimated loss coefficient that exceeded -1% d-1. The remaining species had

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loss coefficients that ranged from -1 to 0.4% d-1. The loss rates of 137Cs were either larger than or

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very close to 1% d-1 in pelagic fish (all p < 0.05); in contrast, 137Cs loss rates were all below 1%

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d-1 in benthopelagic and benthic species (Figs. 3, 4, S3, S4).

299 300

137Cs

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The 137Cs concentrations in fish, sediments, and seawater that were contaminated over the five

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years following the March 2011 accident are shown in Fig. S1. Unlike the fish, most of the

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sediment samples (99.9%) were above detection limits (n = 1978). Detection limits varied

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considerably among datasets for fish, typically ranging between 5 and 10 Bq kg-1 wet wt, and for

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water between 1 and 25 Bq L-1; the detection limit was 2 Bq kg-1 wet wt for sediments.

in fish and sediments after the first year



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The average concentration of 137Cs (SD) in pelagic fish whose 137Cs concentrations were above

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the detection limit was 3041095 Bq kg-1 in 2011 and 1815 Bq kg-1 in 2012.

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concentrations above 100 Bq kg-1 were found throughout the first 2.5 years following the

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accident in benthopelagic fish. Average concentrations of 137Cs (SD) in those benthopelagic

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fish whose 137Cs concentrations exceeded the detection limit were 69115 Bq kg-1, 3952 Bq kg-

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1,

313

and 2016, respectively.

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4 years following the accident in benthic fish. The average concentration of 137Cs (SD) in

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pooled benthic fish (above the detection limit) was 103169 Bq kg-1, 78 128 Bq kg-1, 3960 Bq

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kg-1, 2734 Bq kg-1, 1714 Bq kg-1, and 1510 Bq kg-1 in 2011, 2012, 2013, 2014, 2015, and

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2016, respectively. 137Cs concentrations in representative individual species of the three

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ecological groups are presented in Fig. S2.

137Cs

2227 Bq kg-1, 1311 Bq kg-1, 114 Bq kg-1, and 71 Bq kg-1 in 2011, 2012, 2013, 2014, 2015, 137Cs

concentrations above 100 Bq kg-1 were found throughout the first

319 320

In the seawater samples above the detection limit, average monthly concentrations decreased by

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one to two orders of magnitude within the first year after the accident and then declined more

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gradually thereafter. The average monthly 137Cs concentrations decreased from 12 to 0.08 Bq L-1

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in surface seawater and from 9 to 1 Bq L-1 in bottom seawater during the first year (Fig. S1).

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From 2012 to 2015, concentrations gradually decreased from 0.08 to 0.02 Bq L-1 in surface

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seawater and from 0.1 to 0.01 Bq L-1 in bottom seawater (Fig. S1).

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In contrast to fish and seawater, the decline in the average 137Cs in sediment samples above the

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detection limit was gradual, but as expected, coastal sediments had much higher (up to 6-fold) 16 ACS Paragon Plus Environment

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average concentrations and variability of 137Cs than offshore stations (Fig. S1). The average

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137Cs

331

kg-1, 184295 Bq kg-1, 137188 Bq kg-1, and 111194 Bq kg-1 in 2011, 2012, 2013, 2014, and

332

2015, respectively. In sediments of offshore stations, the average 137Cs concentrations (SD)

333

were 8263 Bq kg-1, 7662 Bq kg-1, 6478 Bq kg-1, and 4539 Bq kg-1 in 2011, 2012, 2013, and

334

2014, respectively.

concentrations (SD) in sediments of coastal stations were 502611 Bq kg-1, 309362 Bq

335 336

Factors affecting 137Cs bioaccumulation

337

Benthic invertebrates living in marine sediments constitute the diet of many benthic fish species

338

and can serve as a conduit of radiocesium from sediment to fish17. The decline rates in

339

radiocesium concentrations over the first 2 years after the accident in invertebrates in the coastal

340

benthic food web off Fukushima were very similar to those in the sediments in the same region,

341

suggesting that sediments were a likely source of radiocesium for these benthic invertebrates5.

342

Our analysis showed that the change in 137Cs concentrations in most of the benthic and

343

benthopelagic species was comparable to that in the sediments, indicating that sediment could

344

have been the source of 137Cs for these benthic and benthopelagic fish. Sediments are major

345

repositories30 as well as possible sources42-44 of many metals and radionuclides in aquatic

346

ecosystems. When contaminants are present in a bioavailable form42-44, they can be assimilated

347

by deposit-feeding animals such as polychaetes, clams and fish ingesting sediment and

348

transferred to predators in demersal food chains17. The sediment-water distribution coefficient

349

(Kd) of Cs, which reflects Cs enrichment in sediment relative to water, is 2103 in the marine

350

environment45. Given this moderate Kd value of Cs, some of the 137Cs in the sediment may

351

desorb from sediment particles into overlying seawater and porewater, from which it can 17 ACS Paragon Plus Environment


352

presumably be taken up by marine fish. Through these two routes (dietary and aqueous), marine

353

sediments can serve as the ultimate source of 137Cs for marine fish.

354 355

The concentration of 137Cs in fish can be affected by many ecological and biological factors,

356

such as the ambient K+ concentration46, temperature46, 47, trophic level48, animal size47, 48, and

357

diet48. Another hypothesis to explain the slower decline of 137Cs in benthopelagic and benthic

358

fish than in pelagic fish, in addition to sediments serving as a continuous source of 137Cs, is that

359

colder bottom waters (compared to surface waters) leads to slower depuration of 137Cs in

360

benthopelagic and benthic fish. The excretion of elements in animals is a basic metabolic

361

process49, on which temperature could have a profound effect. Many studies have shown that the

362

depuration rate of 137Cs in fish increases with temperature10, 27, 40, 46, 47, 50. Recent and previous

363

Q10 determinations, ranging from 1 to 4 for 137Cs loss from fish, indicate that although 137Cs loss

364

is inversely related to temperature, the influence of temperature is not sufficient to account for

365

the retention of this radionuclide in benthic fish for longer than 2 years (Wang et al. submitted).

366

This highlights the importance of an ongoing source of 137Cs contamination in the fish such as

367

acquisition from contaminated sediments.

368


Page 18 of 29

Page 19 of 29

369


Acknowledgements

370 371

We thank J. Nishikawa and H. Kaeriyama for helping to compile the data on Cs concentrations

372

in fish and two anonymous reviewers for helpful comments on the manuscript. This study was

373

supported by Grants 3423 from the Gordon and Betty Moore Foundation and 269672 from the

374

European Commission to N. Fisher.

375



376

Figure 1. Study area. The circle indicates the location of the Fukushima Daiichi Nuclear Power

377

Plant. The triangles denote the sample locations of sediment and seawater samples.

378

379


Page 20 of 29

Page 21 of 29


380

Figure 2. 137Cs concentrations in pooled pelagic, pooled benthopelagic, pooled benthic fish,

381

surface seawater, bottom seawater and sediment during the first year after the accident, and their

382

fit to a linear function of time. Data below the detection limit were excluded. Equations are for

383

regressions of log-transformed data.

384 Pelagic species

Surface seawater

10000 Cs-137 concentration (Bq/L) (Bq L -1)

100.000

y = 305.51e-0.012x R! = 0.44842

1000 100 10 1

0

100

200

300

10.000 1.000 0.100 0.010 0.001

400

y = 53.442e-0.023x R! = 0.92123

!

"! !

Cs-137 concentration (Bq (Bq/L) L-1)

kg-1) (Bq/kg) Cs-137 concentration (Bq

100.000

y = 54.137e-0.002x R! = 0.01751 1000 100 10

!

"! !

#! !

$! !

kg-1) Cs-137 concentration (Bq (Bq/kg)

100 10 1

385

200

0.100 0.010

!

"! !

#! !

$! !

%! !

300

400

10,000

1000

100

1.000

Sediment

y = 66.017e-0.001x R! = 0.00505

0

%! !

y = 18.855e-0.009x R! = 0.87764

10.000

0.001

%! !

Benthic species 10000

$! !

Bottom seawater

Benthopelagic species 10000

1

#! !

300

400

1,000 100 10

y = 113.39e0.0003x R! = 0.0004

1 0

100

200

Time since accident (d)




Page 22 of 29

386

Figure 3. Rates of change (% d-1) of 137Cs concentrations in individual species of pelagic,

387

benthopelagic, and pelagic fish, each fish ecological group, surface seawater, bottom seawater,

388

and sediments off Fukushima during the first year after the accident. Data points are means + 95%

389

confidence intervals.

390 22 ACS Paragon Plus Environment

Page 23 of 29


391

Figure 4. 137Cs concentrations in representative pelagic, benthopelagic and benthic fish during

392

the first year after the accident. Solid lines indicate regressions of measured values for each

393

species. The dashed lines are the depuration curves of 137Cs in the fish with the y-intercept the

394

same as that derived from the observations off Fukushima, and the lower limit of the loss rates (1%

395

d-1) found in laboratory studies. The dotted lines represent the depuration curves of 137Cs with the

396

y-intercept the same as that derived from the observations off Fukushima, and the upper limit of

397

the loss rates (5% d-1) found in laboratory studies. Anchovy (Engraulis japonicus)

Whitebait

100

Japanese sandlance (Ammodytes personatus)

1000

10000 y = 269.89e-0.015x R! = 0.52987

84.097e -0.009x

y= R! = 0.46531

Pelagic

y = 552.47e-0.01x R! = 0.47517

1000

100 100

10 10

10 1

Benthopelagic

(Bq/kg) Cs-137 concentration (Bq kg-1)

1

!

"! !

#! !

$! !

%! !

Pacific cod (Gadus macrocephalus)

!

"! !

#! !

$! !

Nibe croaker (Nibea mitsukurii)

%! !

1000

1000

100

100

10

10

!

"! !

#! !

$! !

%! !

Brown hakeling (Physiculus maximowiczi)

10000

y = 351.05e-0.006x R! = 0.34513

y = 74.644e-0.003x R! = 0.0561

1

y = 143.73e-0.004x R! = 0.07038

1000 100

1

!

"! !

#! !

$! !

%! !

1

Flathead flounder (Hippoglossoides dubius)

100

10 1 !

"! !

#! !

$! !

%! !

Littlemouth flounder (Pleuronectes herzensteini)

1000

y = 42.242e-0.004x R! = 0.05236

!

"! !

y = 81.605e-0.004x R! = 0.18212

#! !

$! !

Fat greenling (Hexagrammos otakii)

10000

%! !

y = 129.85e-0.001x R! = 0.00482

1000

100

Benthic

100

10 10

1 0

100

200

300

400

10 1

1 0

100

200

300

400

0

100

200

300


398

Exponential regression

1% loss rate

399


5% loss rate

400


400

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Temporal changes in 137Cs concentrations in fish, sediments, and

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