Impacts of the fukushima nuclear accident on fish and fishing grounds

Nakata, Kaoru

Sugisaki,Hiroya

2015

Springer

This book presents the results from the Japanese Fisheries Research Agency’s 3-year intensive monitoring of radionuclides in a variety of fish, plankton, benthos, and their living environments after the Fukushima Daiichi Nuclear Power Plant (FNPP) accident in March 2011. The book reveals the dynamics of contamination processes in marine and freshwater fish, mediated by the contamination of water, sediments, and food organisms; it also clarifies the mechanisms by which large variations in the level of contamination occurs among individual fish. Most importantly, the book includes a large amount of original measurement data collected in situ and for the first time assesses diffusion of radiocesium across the Pacific using both in situ data and a numerical simulation model. Also introduced are several new approaches to evaluate the impact of the release of radionuclides, including the measurement of radiation emission from an otolith section to identify the main period of contamination in fish. The FNPP accident represents a rare instance where the environmental radioactivity level was elevated steeply through atmospheric fallout and direct discharge of radioactive water into the sea over a short period of time. Replete with precise scientific data, this book will serve as an important resource for research in fields such as fishery science, oceanography, ecology, and environmentology, and also as a solid basis for protecting fisheries from damage resulting from harmful rumors among the general public.

Aquaculture and Fisheries

Business and Management

Chemical Engineering

English

978-4-431-55536-0 (prints)

978-4-431-55537-7 (eBook)

Kaoru Nakata · Hiroya Sugisaki Editors

Impacts of the
Fukushima
Nuclear Accident
on Fish and
Fishing Grounds

Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds

Kaoru Nakata • Hiroya Sugisaki
Editors

Impacts of the Fukushima
Nuclear Accident on Fish
and Fishing Grounds

Editors
Kaoru Nakata
Research Management Department
Fisheries Research Agency
Yokohama, Kanagawa, Japan

Hiroya Sugisaki
National Research Institute of Fisheries
Sciences
Fisheries Research Agency
Yokohama, Kanagawa, Japan

ISBN 978-4-431-55536-0
ISBN 978-4-431-55537-7
DOI 10.1007/978-4-431-55537-7

(eBook)

Library of Congress Control Number: 2015939907
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Foreword

On March 11, 2011, the most disastrous earthquake and tsunami in modern Japanese
history occurred in northeast Japan. They caused a great calamity for the people
and industries on the Pacific coast of the Tohoku region of Japan, one of the most
important regions for Japanese fisheries. The Fukushima Dai-ichi Nuclear Power
Plant (FNPP) was covered by a 15-m-high tsunami, and the electric power supply to
its four nuclear reactors was severed, resulting in hydrogen explosions and the meltdown of the core. This accident caused the elevation of the level of anthropogenic
radioactivity in the marine environment in the western North Pacific from atmospheric fallout and direct discharges of highly radioactive waters. Security of food
safety of marine products is a great concern for the people in the world and especially for the people involved in the fisheries industry.
The Fisheries Research Agency (FRA) has been conducting research and monitoring
the radioactivity of fish and shellfish since the 1950s, when we were worried about the
effect of nuclear arms tests in the ocean to marine environments and products. Because
the FRA has enough experience and knowledge of research on the radioactivity of large
quantities of specimens, we accepted the requests from the national government to
analyze the radioactivity of marine products fished all over Japan and started to make a
plan to monitor radioactivity of various marine products fished around Japan in cooperation with local governmental institutes just after the accident.
This book describes the results of the research on the effect of radioactivity to
ocean and coastal ecosystems and various marine and freshwater fish caused by the
FNPP accident of the huge magnitude of radioactivity on the ecosystems around
Japan. This is the first report on the effect on the hydrosphere ecosystem from the
point of view of marine ecology and fisheries oceanography. A scientifically precise
description of the distribution and variation of radioactive elements in the ecosystem
is presented in detail in this publication. Of course, this is the first step in revealing

v

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Foreword

the anthropological effect of radioactivity on the ecosystem, and we should continue the research. I trust that this book will contribute to overcoming the tragedy
and enhance the culture of human beings in the world.
President of the Fisheries Research Agency
Yokohama, Japan

Masanori Miyahara

Preface

On March 11, 2011, the Great East Japan Earthquake occurred. The earthquake
itself and the resulting tsunami caused the Fukushima Daiichi Nuclear Power Plant
(FNPP) accident. As a result, a large volume of radionuclides was released into the
environment as fallout, which contaminated both freshwater and marine systems.
On April 2, heavily contaminated water was released around the No. 2 reactor into
the ocean. Several further leakages of water contaminated with radionuclides, as
well as a release of low-level contaminated water by the Tokyo Electric Power
Company (TEPCO), occurred around FNPP up until May 2011. This was the first
time that heavily contaminated water originating from a nuclear power plant accident had been directly released into the ocean over a relatively short period. Since
then, contaminated fish with relatively high radiocesium concentrations (higher
than ca. 100 Bq/kg-wet) have often been caught in the coastal areas of Fukushima
and in adjacent prefectures.
The Fisheries Research Agency (FRA) has monitored radioactive substances in
marine organisms around Japan since 1954, when the H-bomb test was carried out
on Bikini Atoll. Soon after the FNPP accident, the FRA began monitoring radionuclides in fisheries resources and their habitats. Decreasing trends of radiocesium
concentration in small pelagic fish and demersal fish have been obvious since summer 2011 and winter 2012, respectively, based on intensive monitoring of radioactivity in fisheries products by local governments and the FRA (http://www.jfa.maff.
go.jp/j/housyanou/kekka.html).
However, incidents that have worried the general public, including fishermen,
have often occurred, including catches of cod with relatively high radiocesium concentrations in areas distant from Fukushima Prefecture, a catch of extremely highly
contaminated fat greenlings, and continuing contamination of fish in some freshwater systems. Various questions have therefore been raised by the public, such as:
When will the radiocesium concentrations of fish and fishing grounds recover to the
level before the accident? Will the radiocesium in fish continue to be accumulated
in fish via the food chain, like heavy metals and some kinds of chemicals? What is

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Preface

the mechanism for the occurrence of extremely highly contaminated fish? Is the
contamination of fish with radiocesium an ongoing phenomenon?
In order to restore trust in fisheries products from the Tohoku district, both abroad
and among the Japanese people, it is important to answer these questions based on
scientific data. Accordingly, the FRA has conducted research to clarify the impacts
of the FNPP accident on fish and fishing grounds, and the dynamics of radionuclides through both marine and freshwater systems by in situ investigation, rearing
experiments, and the use of simulation models.
Although our research is ongoing, the main body of our investigations was conducted from 2011 to 2013.
Yokohama, Japan

Tokio Wada
Kaoru Nakata
Hiroya Sugisaki

Contents

1

Introduction: Overview of Our Research on Impacts
of the Fukushima Dai-ichi Nuclear Power Plant
Accident on Fish and Fishing Grounds .................................................
Kaoru Nakata and Hiroya Sugisaki

Part I
2

3

5

Seawater and Plankton

134

Cs and 137Cs in the Seawater Around
Japan and in the North Pacific ..............................................................
Hideki Kaeriyama
Temporal Changes in 137Cs Concentration in Zooplankton
and Seawater off the Joban–Sanriku Coast, and in Sendai
Bay, After the Fukushima Dai-ichi Nuclear Accident..........................
Hideki Kaeriyama

Part II
4

1

11

33

Sediments and Benthos

Three-Dimensional Distribution of Radiocesium
in Sea Sediment Derived from the Fukushima Dai-ichi
Nuclear Power Plant ...............................................................................
Daisuke Ambe, Hideki Kaeriyama, Yuya Shigenobu, Ken Fujimoto,
Tsuneo Ono, Hideki Sawada, Hajime Saito, Mikiko Tanaka,
Shizuho Miki, Takashi Setou, Takami Morita, and Tomowo Watanabe
Radiocesium Concentrations in the Organic
Fraction of Sea Sediments ......................................................................
Tsuneo Ono, Daisuke Ambe, Hideki Kaeriyama, Yuya Shigenobu,
Ken Fujimoto, Kiyoshi Sogame, Nobuya Nishiura, Takashi Fujikawa,
Takami Morita, and Tomowo Watanabe

53

67

ix

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6

7

Contents

Bottom Turbidity, Boundary Layer Dynamics,
and Associated Transport of Suspended Particulate
Materials off the Fukushima Coast .......................................................
Hiroshi Yagi, Kouichi Sugimatsu, Shigeru Kawamata,
Akiyoshi Nakayama, and Toru Udagawa
Investigation of Radiocesium Translation
from Contaminated Sediment to Benthic Organisms..........................
Yuya Shigenobu, Daisuke Ambe, Hideki Kaeriyama,
Tadahiro Sohtome, Takuji Mizuno, Yuichi Koshiishi,
Shintaro Yamasaki, and Tsuneo Ono

Part III

77

91

Marine Fish

8

Detection of 131I, 134Cs, and 137Cs Released into the Atmosphere
from FNPP in Small Epipelagic Fishes, Japanese Sardine
and Japanese Anchovy, off the Kanto Area, Japan .............................. 101
Takami Morita, Kaori Takagi, Ken Fujimoto, Daisuke Ambe,
Hideki Kaeriyama, Yuya Shigenobu, Shizuho Miki,
Tsuneo Ono, and Tomowo Watanabe

9

Radiocesium Concentration of Small Epipelagic Fishes
(Sardine and Japanese Anchovy) off the Kashima-Boso Area ............ 111
Kaori Takagi, Ken Fujimoto, Tomowo Watanabe, Hideki Kaeriyama,
Yuya Shigenobu, Shizuho Miki, Tsuneo Ono, Kenji Morinaga,
Kaoru Nakata, and Takami Morita

10

Why Do the Radionuclide Concentrations
of Pacific Cod Depend on the Body Size? ............................................. 123
Yoji Narimatsu, Tadahiro Sohtome, Manabu Yamada, Yuya Shigenobu,
Yutaka Kurita, Tsutomu Hattori, and Ryo Inagawa

11

Radiocesium Contamination Histories of Japanese
Flounder (Paralichthys olivaceus) After the 2011 Fukushima
Nuclear Power Plant Accident ............................................................... 139
Yutaka Kurita, Yuya Shigenobu, Toru Sakuma, and Shin-ichi Ito

Part IV
12

Mechanisms of Severe Contamination in Fish

Evaluating the Probability of Catching Fat Greenlings
(Hexagrammos otakii) Highly Contaminated
with Radiocesium off the Coast of Fukushima..................................... 155
Yuya Shigenobu, Ken Fujimoto, Daisuke Ambe, Hideki Kaeriyama,
Tsuneo Ono, Takami Morita, and Tomowo Watanabe

Contents

xi

13

Analysis of the Contamination Process of the Extremely
Contaminated Fat Greenling by Fukushima-Derived
Radioactive Material............................................................................... 163
Tomowo Watanabe, Ken Fujimoto, Yuya Shigenobu,
Hideki Kaeriyama, and Takami Morita

14

Contamination Levels of Radioactive Cesium
in Fat Greenling Caught at the Main Port
of the Fukushima Dai-ichi Nuclear Power Plant.................................. 177
Ken Fujimoto, Shizuho Miki, and Tamaki Morita

Part V

Freshwater Systems

15

Comparison of the Radioactive Cesium Contamination Level
of Fish and their Habitat Among Three Lakes in Fukushima
Prefecture, Japan, After the Fukushima Fallout.................................. 187
Keishi Matsuda, Kaori Takagi, Atsushi Tomiya, Masahiro Enomoto,
Jun-ichi Tsuboi, Hideki Kaeriyama, Daisuke Ambe, Ken Fujimoto,
Tsuneo Ono, Kazuo Uchida, and Shoichiro Yamamoto

16

Radiocesium Concentrations and Body Size of Freshwater
Fish in Lake Hayama 1 Year After the Fukushima
Dai-Ichi Nuclear Power Plant Accident ................................................ 201
Kaori Takagi, Shoichiro Yamamoto, Keishi Matsuda, Atsushi Tomiya,
Masahiro Enomoto, Yuya Shigenobu, Ken Fujimoto, Tsuneo Ono,
Takami Morita, Kazuo Uchida, and Tomowo Watanabe

17

Spatiotemporal Monitoring of 134Cs and 137Cs in Ayu,
Plecoglossus altivelis, a Microalgae-Grazing Fish,
and in Their Freshwater Habitats in Fukushima................................. 211
Jun-ichi Tsuboi, Shin-ichiro Abe, Ken Fujimoto,
Hideki Kaeriyama, Daisuke Ambe, Keishi Matsuda,
Masahiro Enomoto, Atsushi Tomiya, Takami Morita,
Tsuneo Ono, Shoichiro Yamamoto, and Kei’ichiro Iguchi

18

Radiocesium Concentrations in the Muscle
and Eggs of Salmonids from Lake Chuzenji, Japan,
After the Fukushima Fallout.................................................................. 221
Shoichiro Yamamoto, Tetsuya Yokoduka, Ken Fujimoto,
Kaori Takagi, and Tsuneo Ono

19

Assessment of Radiocesium Accumulation
by Hatchery-Reared Salmonids After
the Fukushima Nuclear Accident .......................................................... 231
Shoichiro Yamamoto, Kouji Mutou, Hidefumi Nakamura,
Kouta Miyamoto, Kazuo Uchida, Kaori Takagi, Ken Fujimoto,
Hideki Kaeriyama, and Tsuneo Ono

Chapter 1

Introduction: Overview of Our Research
on Impacts of the Fukushima Dai-ichi Nuclear
Power Plant Accident on Fish and Fishing
Grounds
Kaoru Nakata and Hiroya Sugisaki
Abstract As a result of the Fukushima Dai-Ichi Nuclear Power Plant accident in
March 2011, a large volume of radionuclides was released into the environment,
thus contaminating marine and freshwater systems. The Fisheries Research Agency
has conducted research beginning soon after the accident. Our research addressed
the contamination processes of radionuclides (mainly radiocesium) through water,
sediments, and food chains, in both marine and freshwater systems, based on a large
volume of original in situ data. Our research has also provided important information on when and how marine fish have been contaminated. This chapter gives an
overview of our research.
Keywords Fukushima • Radionuclides • Radiocesium • Marine and freshwater
systems • Contamination process

1.1

Objectives of Our Research

As a result of the Great East Japan Earthquake on March 11, 2011, and the resulting
tsunami, all power supplies to the No. 1 through No. 4 nuclear reactors at Tokyo
Electric Power’s Fukushima I Nuclear Power Plant (FNPP) were lost because of
submergence and electrical discharge. As a result, core meltdowns occurred in the
No. 1 to No. 3 reactors and hydrogen explosions sequentially occurred in No. 1, No.
3, and No. 4 nuclear reactors. By March 15, a large amount of radioactive materials
had been released into the environment as fallout, which contaminated both marine
K. Nakata (*)
Fisheries Research Agency, Queen’s Tower B 15F, 2-3-3 Minato Mirai,
Nishi-ku, Yokohama, Kanagawa 220-6115, Japan
e-mail: may31@affrc.go.jp
H. Sugisaki
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Yokohama, Kanagawa 236-8648, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_1

1

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K. Nakata and H. Sugisaki

and freshwater systems. On April 2, heavily contaminated water was found at an
intake of the No. 2 reactor. In addition, several leakages of contaminated water
around FNPP, as well as a release of low-level contaminated water by Tokyo Electric
Power Company (TEPCO), had occurred by May 2011.
The Fisheries Research Agency (FRA) has conducted research to clarify the
impacts of the FNPP accident on fish and fishing grounds since soon after the accident. Our research has mainly involved monitoring radionuclides in fish and their
habitats and conducting studies to clarify the dynamics of radionuclides in both
marine and freshwater systems. This book aims to introduce the results of our
research, the bulk of which was conducted from 2011 to 2013. An overview of our
results is given next.

1.2

Seawater and Plankton (Part I)

FNPP-derived radiocesium has accumulated in marine food webs via seawater
intake and predator–prey interactions. Information on the spatiotemporal distribution of radiocesium concentration in seawater and plankters is therefore important
for comprehending the accumulation and dynamics of radiocesium in pelagic ecosystems. Although a large amount of contaminated water was released into the
ocean, by 2012 the 137Cs concentrations in the surface seawater around Japan
(Fig. 1.1), except for the waters off the Pacific coast of Tohoku district (Fig. 1.1),
had dropped to levels seen before the accident (Table 1.1). The concentrations off
the Pacific coast of Tohoku district in 2012 were still about ten times higher than
those before the accident, but they had decreased to the level seen before the accident by late 2013 (FRA 2014).
Chapter 2 summarizes the dispersion process of FNPP-derived radioactive
cesium (Cs) in seawater, based on observatory data and numerical simulation. A
considerable amount of radioactive Cs from FNPP dispersed from the western
North Pacific eastward to the central North Pacific during the first year after the
accident. It then dispersed not only eastward but also northward and southward in
the central North Pacific in the subsequent second and third years. Research by the
FRA also shows transportation of the contaminated water into the subtropical zone
beneath the Kuroshio Extension.
Chapter 3 shows the temporal variability of 137Cs concentrations in zooplankters
off the Joban coast and Sendai Bay, on the Pacific coast of the middle to southern
Tohoku district. 137Cs concentrations in both seawater and zooplankton have
decreased during our research period since June 2011. However, the rate decrease in
seawater was faster than in zooplankton, which resulted in a high apparent concentration ratio (aCR) for zooplankton (Chap. 3). We also show that the aCR value
measured in zooplankton accurately describes the progress of 137Cs contamination
in zooplankton, from the beginning of the FNPP accident (dynamic nonequilibrium
state) to the restoration phase (dynamic equilibrium state).

1

Introduction: Overview of Our Research on Impacts of the Fukushima…

3

Fig. 1.1 Sampling points of surface water for analyzing the radiocesium concentrations
around Japan

Table 1.1 Comparisons of 137Cs concentration in surface waters around Japan between 2012 and
periods before the accident at Fukushima Dai-ichi Nuclear Power Plant in March 2011
137

Cs concentration (mBq/kg)
Sea area
Month surveyed (2012)
2012
2001–2010
Sea of Okhotsk
Jun
1.9 ± 0.37
2.2–ND
Sea of Japan
Jun–Nov
2.4–2.0
2.9–ND
East China Sea
Jun–Oct
2.0–1.4
2.4–1.4
(Kuroshio)
Jan–Aug
2.7–1.2
3.8–ND
Source: http://www.fra.affrc.go.jp/eq/Nuclear_accident_effects/H24seika.pdf (in Japanese)

• Chapter 2. 134Cs and 137Cs in the Seawater Around Japan and in the North Pacific
(H. Kaeriyama)
• Chapter 3. Temporal Changes in 137Cs Concentration in Zooplankton and
Seawater off the Joban–Sanriku Coast, and in Sendai Bay, After the Fukushima
Dai-ichi Nuclear Accident (H. Kaeriyama)

4

1.3

K. Nakata and H. Sugisaki

Sediments and Benthos (Part II)

Intensive monitoring of radiocesium in marine organisms by the Fukushima
Prefectural Fisheries Experimental Station showed that the radiocesium concentration in demersal fish was higher, and showed slower decline, compared with pelagic
fish (Wada et al. 2013). This phenomenon might have been largely influenced by the
distribution and dynamics of radiocesium in sediment. The FRA has investigated
the spatial and temporal distribution of radiocesium concentrations in marine sediment, its translation from contaminated sediment to benthos, and the probable food
of demersal fish. The results are summarized in Part II.
Chapter 4 shows the spatial distribution of the radiocesium concentration in the
top 14 cm of sea sediment off the coast of northern Ibaraki to Fukushima, with
5-min horizontal resolution. There was a high concentration band along 100-m isobaths, where the concentration of 137Cs reached a maximum of 1,240 Bq/kg-dry.
When assessing radiocesium transportation from sea sediments to a marine demersal ecosystem, information is required not only on the concentration but also on the
biological ingestibility of sea sediment radiocesium. To assess radiocesium transportation from sea sediments to a benthic ecosystem, radiocesium concentration in
the organic fraction of sea sediments (Csorg) was analyzed (Chap. 5), and showed
horizontal distribution of Csorg off the coast of northern Ibaraki to Fukushima and
Sendai Bay. Csorg of sea sediments was significantly higher than that of bulk sediments (Csbulk). We suggest that Csorg can be used as an indicator of the potential
effects of sediment radiocesium on the demersal ecosystem.
The FRA also monitored the behavior of particulate matter, which is closely
related to that of sediment radiocesium, at a depth of 32 m off Iwaki, Fukushima, by
automated observatory systems (Chap. 6). The behavior was largely influenced by
waves, and particulate matter was resuspended and transported with water movement during high waves. We show that the combination of waves and currents
resulting from meteorological disturbance is one of the important processes in the
transport of suspended particle material off the Fukushima coast.
On the basis of the results from field investigations and rearing experiments
using a benthic polychaete (Perinereis aibuhitensis) with highly contaminated sediment collected at the station 1 km off FNPP, the FRA estimated the transport of
radiocesium from contaminated sediment to benthic organisms off the coast of
Fukushima (Chap. 7). These results suggest that the intake of radiocesium through
the benthic food web is limited for benthic organisms, even if the sediments are
highly contaminated.
• Chapter 4. Three-Dimensional Distribution of Radiocesium in Sea Sediment
derived from the Fukushima Dai-ichi Nuclear Power Plant (D. Ambe et al.)
• Chapter 5. Radiocesium Concentrations in the Organic Fraction of Sea Sediments
(T. Ono et al.)
• Chapter 6. Bottom Turbidity, Boundary Layer Dynamics, and Associated
Transport of Suspended Particulate Materials off the Fukushima Coast (H. Yagi
et al.)

1

Introduction: Overview of Our Research on Impacts of the Fukushima…

5

• Chapter 7. Investigation of Radiocesium Translation from Contaminated
Sediment to Benthic Organisms (Y. Shigenobu et al.)

1.4

Marine Fish (Part III)

Off the Fukushima coast, the percentage of fish with a radiocesium concentration
higher than 100 Bq/kg-wet (the standard value of radiocesium in foods) accounted
for more than 90 % of the fish caught off Fukushima in April 2011. The percentage
had declined to 0.6 % by October 2014, according to the Fukushima Prefectural
Fisheries Experimental Station (2014). The concentration trend was different
between pelagic and demersal fish. Part III describes the characteristics of the temporal variations of the concentration and their background mechanisms for small
epipelagic fish (sardine and anchovy) and demersal fish (cod and flatfish).
In addition to the intrusion of the contaminated waters from FNPP, some radionuclides were delivered to marine fish and their habitat through the atmospheric
pathway. Chapter 8 describes evidence of impacts via the atmospheric pathway on
small epipelagic fish off the coast of southern Ibaraki and Chiba Prefectures, before
the direct release of contaminated water into the ocean. After the release, fluctuations in the radiocesium concentration in fish muscles were synchronized with the
decreasing concentration in the seawater near the fishing ground; the radiocesium
concentration in fish muscles reached a maximum of 31 Bq/kg-wet in July 2011,
after which it declined gradually (Chap. 9).
Decline of the radiocesium concentration in demersal fish seemed to be slower
compared with pelagic fish, but this varied individually and across species. It is still
unclear which species or individuals of demersal fish showed high radiocesium concentrations. Chapter 10 shows differences in radiocesium concentration in the
Pacific cod (Gadus microcephalus) across year-classes and also suggests that the
difference could be explained by ontogenetic changes in diet and seasonal changes
in vertical distribution.
Chapter 11 describes three features of the contamination histories of the Japanese
flounder (Paralichthys olivaceus) after the accident by analyzing the observed spatiotemporal changes in Cs concentration, a comparison of the dynamics of Cs concentration across year-classes, and simulation studies: (1) high Cs values with high
variation in the first year after the accident, (2) low Cs values with their minimum
values peaking around autumn 2011, and (3) lower Cs values observed for 2011
year-class and younger than 2010 year-class and older. A hypothesis on the background mechanisms is also discussed.
• Chapter 8. Detection of 131I, 134Cs, and 137Cs Released into the Atmosphere from
FNPP in Small Epipelagic Fishes, Japanese Sardine, and Japanese Anchovy, off
the Kanto Area, Japan (T. Morita et al.)
• Chapter 9. Radiocesium Concentration of Small Epipelagic Fishes (Sardine and
Japanese Anchovy) off the Kashima-Boso Area (K. Takagi et al.)

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K. Nakata and H. Sugisaki

• Chapter 10. Why Do the Radionuclide Concentrations of Pacific Cod Depend on
Body Size? (Y. Narimatsu et al.)
• Chapter 11. Radiocesium Contamination Histories of Japanese Flounder
(Paralichthys olivaceus) after the 2011 Fukushima Nuclear Power Plant Accident
(Y. Kurita et al.)

1.5

Mechanisms of Severe Contamination in Fish (Part IV)

Decreasing trends of radiocesium have generally been found for pelagic fish since
summer 2011 and for demersal fish since winter 2012 (http://www.fra.affrc.go.jp/
eq/Nuclear_accident_effects/H24seika.pdf). However, extremely contaminated fat
greenlings (Hexagrammos otakii), with 25,800 Bq/kg-wet of radiocesium, which is
the highest value except for fish collected in the FNPP port (Chap. 14), were caught
off Ota River within a 20-km radius of FNPP. The FRA investigated the causes and
mechanisms for the occurrence of the extremely contaminated fat greenlings.
Based on the radiocesium concentrations in 236 greenlings that had been collected off the coast of Fukushima after the accident, the probability of the occurrence of extremely contaminated fat greenlings was calculated assuming a normal
distribution (Chap. 12). The probability was exceedingly low, at less than
2.794 × 10−6, yet the concentration found was almost equivalent to that frequently
observed for the greenlings caught in the FNPP port.
The contamination process for the extremely contaminated fat greenlings was
also investigated by analyses of beta-ray emission from otoliths and using a biokinetic model; the results are shown in Chap. 13. Analyses of the beta-ray emission
from the otoliths showed that the fat greenlings were in the highly contaminated
environment in the period just after the FNPP accident. Simulation of the 137Cs concentration in fat greenlings using the biokinetic model showed that the fat greenlings had their origin in the FNPP port just after the accident.
Contamination levels of fish caught in the FNPP port are summarized in Chap. 14,
and radiocesium concentrations in fat greenlings, Japanese rockfish, and spotbelly
rockfish are shown to be higher than in other species. Relationships among beta rays
emitted from otoliths, 90Sr, and radiocesium in the whole body without internal
organs were confirmed for Japanese rockfish.
• Chapter 12. Evaluating the Probability of Catching Fat Greenlings (Hexagrammos
otakii) Highly Contaminated with Radiocesium off the Coast of Fukushima
(Y. Shigenobu et al.)
• Chapter 13. Analysis of the Contamination Process of the Extremely
Contaminated Fat Greenling by Fukushima-Derived Radioactive Material
(T. Watanabe et al.)
• Chapter 14. Contamination Levels of Radioactive Cesium in Fat Greenling
Caught at the Main Port of the Fukushima Dai-ichi Nuclear Power Plant
(K. Fujimoto et al.)

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Introduction: Overview of Our Research on Impacts of the Fukushima…

1.6

7

Freshwater Systems (Part V)

Contamination of freshwater systems by the FNPP accident was primarily caused
by fallout from the FNPP. Part V describes factors affecting variation among freshwater systems, fish species, and individuals.
Contamination levels were compared across Lake Hayama, Lake Akimoto, and
Lake Tagokura in Fukushima Prefecture (Chap. 15). Radiocesium concentrations of
the lake water, bottom sediment, plankton, and fish were significantly correlated
with the surface soil radiocesium content near the lake sites. In Lake Hayama, with
the highest contamination level of the three lakes, factors affecting the radiocesium
concentration level in several fish species were considered (Chap. 16). Body
size and feeding habit seemed to influence the variation among fish species in
Lake Hayama.
The radiocesium concentration level in ayu (Plecoglossus altivelis) was analyzed
in five rivers in Fukushima Prefecture between summer 2011 and autumn 2013
(Chap. 17). The concentrations of radiocesium in ayu were shown to have decreased
during the study period. Our research also shows a positive correlation between the
concentrations of radiocesium in the internal organs and the muscle of ayu (r = 0.746,
p = 0.006). However, the median concentration in the muscle was 14.5 % that of
the median concentration in the internal organs, which shows that a small proportion (about 15 %) of the ingested food from the riverbed appears to be transferred to
the muscle.
The contamination levels in salmonid fish were also investigated in Lake
Chuzenji, central Honshu Island, Japan, in Tochigi Prefecture (160 km from the station) (Chap. 18). In Lake Chuzenji, substantial accumulations of radiocesium were
confirmed in the muscle of hatchery-reared kokanee (Oncorhynchus nerka) and
masu salmon (Oncorhynchus masou). Rearing experiments controlling for water
and food radiocesium levels revealed that radiocesium contamination of fish is an
ongoing process, and that radiocesium is accumulated in fish via the food chain
(Chap. 19).
• Chapter 15. Comparison of the Radioactive Cesium Contamination Level of Fish
and their Habitat Among Three Lakes in Fukushima Prefecture, Japan, After the
Fukushima Fallout (K. Matsuda et al.)
• Chapter 16. Radiocesium Concentrations and Body Size of Freshwater Fish in
Lake Hayama 1 Year After the Fukushima Dai-ichi Nuclear Power Plant Accident
(K. Takagi et al.)
• Chapter 17. Spatiotemporal Monitoring of 134Cs and 137Cs in Ayu, Plecoglossus
altivelis, a Microalgae-Grazing Fish, and in Their Freshwater Habitats in
Fukushima (J. Tsuboi et al.)
• Chapter 18. Radiocesium Concentrations in the Muscle and Eggs of Salmonids
from Lake Chuzenji, Japan, After the Fukushima Fallout (S. Yamamoto et al.)
• Chapter 19. Assessment of Radiocesium Accumulation by Hatchery-Reared
Salmonids After the Fukushima Nuclear Accident (S. Yamamoto et al.)

8

K. Nakata and H. Sugisaki

Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
Fukushima Prefectural Fisheries Experimental Station (2014) http://www.pref.fukushima.lg.jp/
uploaded/attachment/930000.pdf. Accessed 27 Dec 2014. [in Japanese]
FRA (2014) http://www.fra.affrc.go.jp/eq/Nuclear_accident_effects/H25seika.pdf. Accessed 20
Nov 2014. [in Japanese]
Wada T, Nemoto Y, Shimamura S, Fujita T, Mizuno T, Sohtome T, Kamiyama K, Morita T, Igarashi
S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ Radioact
124:246–254

Part I

Seawater and Plankton

Chapter 2
134

Cs and 137Cs in the Seawater Around
Japan and in the North Pacific
Hideki Kaeriyama

Abstract Enormous quantities of radionuclides were released into the ocean via
both atmospheric deposition and direct release as a result of the Fukushima Dai-ichi
Nuclear Power Plant (FNPP) accident. The evaluation of FNPP-derived radioactive
cesium (Cs) in the marine environment is important in addressing risks to both
marine ecosystems and public health through consumption of fisheries products.
Understanding the distribution patterns of radioactive Cs in the ocean throughout
the water column is key in assessing its effects on marine ecosystems. This chapter
summarizes the dispersion pattern of FNPP-derived radioactive Cs in the North
Pacific and around Japan, based on our observational studies as follows: (1) eastward dispersion in surface seawater; (2) southwestward intrusion with mode water;
and (3) background level 137Cs without any detectable 134Cs in the Japan Sea, East
China Sea, Seto Inland Sea, and Bering Sea, along with highly radioactive Cs off the
coast of East Japan.
Keywords Fukushima Dai-ichi Nuclear Power Plant accident • 134Cs • 137Cs • North
Pacific • Kuroshio • Mode water

2.1

Fukushima Dai-ichi Nuclear Power Plant Accident

After the 9.0-magnitude Tohoku earthquake and the subsequent tsunami on March
11, 2011, loss of electric power at the Fukushima Dai-ichi Nuclear Power Plant
(hereafter FNPP) resulted in overheated reactors and hydrogen explosions.
Radioactive materials were then released into the ocean through atmospheric fallout
as well as by direct release and leaking of the heavily contaminated coolant water
(Chino et al. 2011; Buesseler et al. 2011). Because of its relatively long half-life
(2.07 years for 134Cs and 30.07 years for 137Cs), evaluation of this radioactive Cs in
the marine environment is important for addressing risks to both marine ecosystems

H. Kaeriyama (*)
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: kaeriyama@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_2

11

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H. Kaeriyama

and public health through consumption of fisheries products. The Japanese
government conducted intensive monitoring of 131I, 134Cs, and 137Cs in the seawater
offshore near the FNPP (Nuclear Regulation Authority 2014) and in fisheries products from a wide area around Japan (Fisheries Agency 2014). Although information
on radioactive contamination covering a broad area of the North Pacific is still quite
limited (Aoyama et al. 2013a, b), some model experiments have addressed the dispersion of FNPP-derived radioactive Cs (Kawamura et al. 2011; Bailly du Bois
et al. 2012; Dietze and Kriest 2012; Tsumune et al. 2012; Miyazawa et al. 2012),
and estimated amounts of 137Cs discharged directly into the ocean ranged from 2.3
to 14.8 PBq, with considerable uncertainties (Masumoto et al. 2012). Although
most studies have discussed the surface dispersion patterns of FNPP-derived radioactive Cs, understanding the ocean distribution patterns of radioactive Cs throughout the water column is key to assessing its effects on marine ecosystems.

2.2

Oceanic Background and 137Cs in the North Pacific
Before the FNPP Accident

The Kuroshio Current (KC) and its extension, Kuroshio Extension (KE), are the
strongest eastward currents off the south and east coasts of Japan (Mizuno and
White 1983). The KC and KE are important in the reproduction, dispersal, and
migration of pelagic fish species (Sugisaki et al. 2010). Because the FNPP was
located at 37°25.28′N, 141°02.02′E (north of KE), most of the radioactive Cs
released directly to the ocean was believed to be dispersed eastward in the North
Pacific by the KE because the KE is thought to act as a transport barrier against
southward dispersion (Buesseler et al. 2011, 2012; Aoyama et al. 2013a, b;
Kaeriyama et al. 2013). In the northern area off the coast near the FNPP, the subarctic Oyashio water flows southwardly, and the water masses off the coast of East
Japan, including off the FNPP, revealed complex features with meso-scale eddies as
a result of the mixing of the subarctic Oyashio water and subtropical Kuroshio
water (Yasuda 2003). The largest 137Cs deposition in the Pacific Ocean before the
FNPP accident occurred in the early 1960s as a part of global fallout from atmospheric nuclear weapons testing (Povinec et al. 2004; Hirose and Aoyama 2003). In
the North Pacific, the concentration of 137Cs in surface water ranged from 1.5 to
2.0 Bq m−3, decay-corrected in 2011, and displayed a horizontally homogeneous
distribution (Hirose and Aoyama 2003). Southward transport of 137Cs from the subarctic region (north of KE) to subtropical and tropical regions (south of KE) was
observed at 20°N–165°E in 2002 (Aoyama et al. 2008). There were two 137Cs concentration maxima, located at the density range of North Pacific Subtropical Mode
Water (NPSTMW) and Lighter Central Mode Water (Aoyama et al. 2008). The
winter mixed layer south of the KE, which forms the NPSTMW core layer, develops and reaches its deepest depth from February to March, and the newly formed
NPSTMW south of the KE is subducted and advected southwestward by the
Kuroshio recirculation (Aoyama et al. 2008). The NPSTMW then begins to appear

2

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

13

Fig. 2.1 Sampling locations of seawater for measurement of 134Cs and 137Cs described in Sect. 2.3
(red open circles), in Sect. 2.4 (black open circles), and in Sect. 2.5 (blue open diamonds).
Schematic flows of Kuroshio and Oyashio are indicated as green broken lines

at the southernmost Japanese islands within a few months (Oka et al. 2007). The
137
Cs core waters observed at 20°N–165°E in 2002 were formed by the movement
of mode waters between the 1960s and the 2000s (Aoyama et al. 2008).
This chapter consists of the following three descriptions concerning the distribution of 134Cs and 137Cs in seawater, based on our field observations after the FNPP
accident (Fig. 2.1):
• Eastward dispersion of 134Cs and 137Cs in the western and central North Pacific
(Kaeriyama et al. 2013, 2014c)
• Southwest intrusion of 134Cs and 137Cs with mode water (Kaeriyama et al. 2014a, c)
• 134Cs and 137Cs around the Japanese Islands (Kaeriyama et al. 2014b, d)

2.3

Eastward Dispersion in Surface Seawater

During the summer season, 3-year repeated observations were conducted along
three north–south transects at 144°E, 155°E, and 175°30′E in 2011 and 2013. In
October 2011, additional sampling was conducted around the area covering summer
season observations.

14

H. Kaeriyama

In July 2011, the concentrations of 134Cs and 137Cs in surface seawater were
highly elevated, with values exceeding 10 Bq m−3 and up to 140 Bq m−3 and
153 Bq m−3 at the northern end of the Kuroshio Extension (KE) along with 144°E
and at all stations at 155°E (Fig. 2.2a). At 38°30′N–144°00′E, 134Cs was not detected
(<1.4 Bq m−3), and 137Cs concentration was lower than that detected at adjacent stations, despite being located at the north of the KE (Fig. 2.3). The concentrations of
137
Cs in the central North Pacific (175°30′E transect) ranged from 3.2 to 9.3 Bq m−3
and were lower than those in the western part of the studied area (144°E and 155°E
transects) but still higher than background level (~2.0 Bq m−3; Hirose and Aoyama
2003). In the northern section of the KE, an east–west gradient of 134Cs and 137Cs
was observed in the surface water at the stations around 40°N in October 2011
(Fig. 2.2b). More than 10 Bq m−3 of 134Cs and 137Cs was observed between 147°E
and 175°05′E, and the highest concentrations were observed at 152°31′E. On the
other hand, in the southern area of the KE, concentrations of 137Cs were relatively
lower than those in the northern KE. A slight increase in 137Cs was observed at the
eastern stations (31°N–34°N, around 175°30′E). 134Cs was not detected at almost
any station located in the southern KE, mainly because of the short measurement
time; the detection limit for 134Cs was 3–4 Bq m−3 with 7,200 s counting. After 1
year from the observation in July 2011, 134Cs and 137Cs were drastically decreased at
the 144°E and 155°E transects (Fig. 2.2c), and the concentrations of 134Cs and 137Cs
at the 175°E transect between the 2 years were similar or slightly increased in July
2012 compared to July 2011. In July 2013, the concentrations of 137Cs were almost
the same as background level at the 144°E and 155°E transects, and 134Cs was only
detected at 41°30′N–155°E (1.9 Bq m−3). On the other hand, 134Cs was still detected
at most stations (1.5–5.8 Bq m−3), and the concentrations of 137Cs were slightly
higher than those measured before the FNPP accident at the 175°30′E transect
(Fig. 2.2d).
During the 3-year observations, FNPP-derived Cs was high in the northern KE
and low in the southern KE. The low concentration of radioactive Cs in the southern
KE was also confirmed by field observations of seawater (Buesseler et al. 2011,
2012; Aoyama et al. 2012) and simulation models (Masumoto et al. 2012). Thus,
the majority of radioactive Cs directly released to the ocean from the FNPP was not
dispersed south of the KE near the east coast of Japan in 2011; rather, the detection
of 134Cs at three stations along with the 175°30′E transect and station located south
of the KE (35°N–144°E) in July 2011 and stations around 30°N in October 2011
may indicate the effect of atmospheric deposition. Atmospheric deposition occurred
mostly in March 2011 (Chino et al. 2011), and most of the direct discharge occurred
during late March and early April 2011 (Tsumune et al. 2012). Aoyama et al.
(2013b) reported a high radioactive Cs concentration area around the International
Date Line in April–July 2011. The eastward speed of the radioactive plume was
estimated to be 8 cm s−1. Moreover, atmospheric deposition of radioactive Cs and
131
I south of the KE near the east coast of Japan was strongly indicated by numerical
simulations (Kawamura et al. 2011; Kobayashi et al. 2013). Thus, the highly radioactive Cs area observed in the central North Pacific in July 2011 and south of the KE
near the east coast of Japan may have originated from atmospheric deposition.

Fig. 2.2 Sampling locations for surface seawater in the western and central North Pacific. Closed
circles indicate the sampling stations. Color of the closed circles indicates the concentration of
137
Cs in the surface seawater. Gray arrows indicate the estimated temporal mean velocity vectors
for the period between June 30 and July 29, 2011 (a), October 14 and November 7, 2011 (b), July
2 and August 1, 2012 (c), and July 2–31, 2013 (d). (Modified from Kaeriyama et al. 2013)

16

H. Kaeriyama

Fig. 2.3 Sampling locations for surface seawater around the anti-cyclonic eddy observed in July
2011. Color of the closed circles indicates concentration of 137Cs in the surface seawater. Gray
arrows indicate the estimated temporal mean velocity vectors for the period between June 30 and
July 29, 2011 (Modified from Kaeriyama et al. 2013)

Some patchy distribution of radioactive Cs was also observed; local minima of
Cs and 134Cs were observed at 38°30′N–144°E, whereas the adjacent stations had
higher concentrations in July 2011 (Fig. 2.3). Judging from the sea surface velocity
field, 38°30′N–144°E was located at the edge of an anti-cyclonic eddy (Fig. 2.3).
Because the surface water of anti-cyclonic eddies originates from the KE (Itoh and
Yasuda 2010a; Yasuda et al. 1992), the water at 38°30′N–144°E would not contain
much water derived from the FNPP. As there are many meso-scale eddies that originate from both the KE and Oyashio in the western Kuroshio–Oyashio transition
area (Itoh and Yasuda 2010b), the concentration of radioactive Cs should be patchy
corresponding to eddies there. An area with high concentration (more than
50 Bq m−3) of 137Cs was distributed around 40°N between 150°E and 170°E in
October 2011 (Fig. 2.2b). As Isoguchi et al. (2006) showed the existence of two
quasi-stationary jets that flow northeastward from the KE to the subarctic front
between 150°E and 170°E, radioactive Cs from the FNPP might have dispersed
along these jets around the time of this observation period.
137

2

134

Cs and 137Cs in the Seawater Around Japan and in the North Pacific

17

The concentrations of radioactive Cs at the 144°E and 155°E transects in July
2012 were much less than those in the previous year (July 2011). These differences
strongly suggest that the water with a high concentration of radioactive Cs had been
transported eastward by 16 months after the FNPP accident. In contrast, the concentrations of radioactive Cs at the 175°30′E transect were similar between the 2 years.
The concentration of radioactive Cs observed at the 175°30′E transect in July 2012
would have been a result of dilution processes that occurred in the western North
Pacific during the 16 months since the FNPP accident. Because the KE jet weakens
eastward and its streamline spreads northward or southward by 175°E (see fig. 1 of
Qiu and Chen 2011), the highly radioactive Cs waters would be stagnant around the
central Pacific and would disperse not only eastward but also slowly northward and
southward. Actually, 134Cs was still detected at the 175°30′E transect, but it was not
detected at the 144°E and 155°E transects, except for that at 41°30′N, 155°E in
2013.
A considerable amount of radioactive Cs from the FNPP was dispersed eastward
from the western North Pacific to the central North Pacific during the first year after
the FNPP accident. In addition, it dispersed not only eastward but also northward
and southward in the central North Pacific for 2 to 3 years after the FNPP accident
(Kaeriyama et al. 2013).

2.4

Southwest Intrusion with Mode Water

A repeat observation was conducted four to five times per year between 27°N and
34°N along 138°E during August 2011 and March 2013. As the 138°E transect lies
across the Kuroshio Current (KC), the water samples were collected north of the
KC, in the KC, and south of the KC. In September 2012, additional sampling was
conducted at five stations located far south of Japan between 13°N and 26°50′N
around 135°E. In October 2011 and November 2012, seawater samples were also
collected between 30°30′N and 36°30′N along 147°E near the Kuroshio Extension
(KE) (Fig. 2.1).

2.4.1

Transect Across the Kuroshio Current

For the nine observations along the 138°E transect, the concentration of 137Cs at all
sampling depths ranged from 1.3 to 3.7 Bq m−3 at 34°N (north of the KC), and from
1.2 to 2.6 Bq m−3 in the KC. No 134Cs was detected except at 100 m in the KC in
January 2012. The vertical distribution pattern of 137Cs at the stations north of and
in the KC was relatively uniform throughout the water column between 0 and
500 m, whereas 137Cs concentrations south of the KC had significant peaks (2.3–
12 Bq m−3) at subsurface depths (100–500 m), especially after April 2012 (Fig. 2.4).
We also detected 134Cs at the subsurface peak of 137Cs (mostly at 300 m), which

18

H. Kaeriyama

Fig. 2.4 Vertical profiles of 137Cs at three to four stations along the 138°E line during August 2011
and March 2013. Arrows indicate the detection of 134Cs. Error bars indicate counting error (±1σ).
When 137Cs was under the detection limit (<3σ), the detection limit was plotted (Adopted with
permission from Kaeriyama et al. 2014a. Copyright (2014) American Chemical Society)

varied from 1.8 to 6.8 Bq m−3 south of the KC. The concentration of 137Cs in deeper
water (≥750 m) was lower than 1.6 Bq m−3, and no 134Cs was detected. Thus, the
subsurface peak of 134Cs and 137Cs was observed between 100 and 500 m south of
the KC. Further south of the 138°E transect, 134Cs was also detected at 300 m, and
137
Cs ranged from 1.2 to 14 Bq m−3 between 0 and 500 m in September 2012 between
18°N and 26°49′N around 135°E. The 137Cs concentration was relatively low and
vertically homogenized, and 134Cs was not detectable at 14°59′N or 13°N on the
same cruise (Fig. 2.5). The 137Cs inventories were nearly the same level, between
630 ± 180 and 1,160 ± 190 Bq m−2, both north of the KC and in the KC during the
entire study period (Fig. 2.6a). South of the KC, the inventories were comparable
with those found north of the KC and in the KC during August 2011 and February
2012 (1,000–1,350 Bq m−2) and then markedly increased to 3,260 ± 410 Bq m−2 after
April 2012 (Fig. 2.6a). The inventories of 137Cs ranged from 800 ± 300 to
3,460 ± 560 Bq m−2 and decreased traveling southward between 13°00′N and
26°49′N around 135°E in September 2012 (Fig. 2.6b).
Because water usually circulates along the isopycnal layer below the subsurface,
the density range of the subsurface peak of 134Cs and 137Cs gives information about
what water mass transported FNPP-derived radioactive Cs. Although the subsurface
peaks were found at the isopycnals from 25.0 to 25.5 σθ and from 26.0 to 26.5 σθ at
34°46′N, 148°52′E in February 2012 (Kumamoto et al. 2013), the present study

2

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

19

Fig. 2.5 Vertical profiles of
137
Cs at five stations around
135°E in September 2012.
Arrows indicate the detection
of 134Cs. Error bars indicate
counting error (±1σ). When
137
Cs was below the detection
limit (<3σ), the detection
limit was plotted (Adopted
with permission from
Kaeriyama et al. 2014a.
Copyright (2014) American
Chemical Society)

shows that 134Cs south of the KC along 138°E and around 135°E was observed at a
density range from 23.9 to 25.7 σθ, with a sharp peak around 25.3 σθ (Fig. 2.7). The
134
Cs peak at 25.3 σθ suggests that core waters with high 134Cs and 137Cs levels
derived from the FNPP accident are distributed in the North Pacific Subtropical
Mode Water (NPSTMW). The predominant temperature (16.4 °–17.9 °C) and salinity (34.6–34.7 psu) ranges of 134Cs and 137Cs are present within the NPSTMW (Oka
2009). In the present study, the radioactive Cs detected in the southern region was
thought to contain the atmospheric fallout from the FNPP to the sea surface south of
the KE during mid-March and early April 2011 (Sect. 2.3; Chino et al. 2011; Rypina
et al. 2013; Honda et al. 2012; Kobayashi et al. 2013).
Using dissolved oxygen data (apparent oxygen utilization, AOU) (Ebbesmeyer
and Lindstrom 1986), we examined whether the subsurface water was ventilated
with highly radioactive Cs at the surface in March 2011 as oxygen in the NPSTMW
gradually decreases after its subduction (Suga and Hanawa 1995). The detected
134
Cs south of the KC in April 2012 and in January 2013 did in fact originate from
atmospheric deposition and was ventilated in March 2011 (Kaeriyama et al. 2014a).
The inventory of 137Cs south of the KC along the 138°E transect increased from
1,100 to 3,210 Bq m−2 between February and August 2012 (Fig. 2.6a), suggesting
that the newly formed NPSTMW brought more FNPP-derived radioactive Cs to the
south of the KC. Alternatively, the inventories of 137Cs north of the KC and in the
KC along the 138°E transect varied from 650 to 1,410 Bq m−2 throughout the study
period (Fig. 2.6a), which is almost comparable with the water column inventories of
137
Cs detected in the North Pacific before the FNPP accident (almost 1,000 Bq m−2)
Aoyama et al. 2008; Povinec et al. 2004). These data may indicate that the water
north of and in the KC was mostly unaffected by the FNPP-derived radioactive Cs.
In September 2012, 134Cs was detected at 18°N, but not at 14°59′N (Fig. 2.5). The
inventories of 137Cs at 13°N and 14°59′N (Fig. 2.6b) were comparable with those in

20

H. Kaeriyama

Fig. 2.6 Water column inventories of 137Cs between 0- and 500-m depth along the 138°E transect
from August 2011 to March 2013 (a), around 135°E in September 2012 (b), and along l47°E in
October 2011 (open bars) and November 2012 (closed bars) (c). When 137Cs was under the detection limit (<3σ), the detection limit was used for calculation (Adopted with permission from
Kaeriyama et al. 2014a. Copyright (2014) American Chemical Society)

2

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

21

Fig. 2.7 Relationship
between subsurface (≥100 m
depth) 134Cs concentration
and potential density (σθ)
south of the Kuroshio Current
(KC) along the 138°E
transect (Adopted with
permission from Kaeriyama
et al. 2014a. Copyright
(2014) American Chemical
Society)

the North Pacific before the FNPP accident (Aoyama et al. 2008; Povinec et al.
2004). These results suggest the FNPP-derived radioactive Cs core water had dispersed southward to at least 18°N by 19 months after the FNPP accident. Nakano
and Povinec (2012) reported long-term simulations of FNPP-derived 137Cs dispersion in the global oceans with a grid size of 2 × 2 and 15 layers of vertical direction.
The vertical distribution pattern of FNPP-derived 137Cs with subsurface peaks
between 100 and 300 m at 20°N–130°E is in agreement with our results at
21°N–134°E from September 2012 (Fig. 2.5). However, the timing of the appearances and concentrations of subsurface 137Cs peaks are very different from our
results. Their model results revealed the first appearance of a subsurface peak of
FNPP-derived 137Cs was in 2014 and the peak depth concentration was estimated as
0.5 Bq m−3. However, our results showed a subsurface peak concentration of
2.1 Bq m−3 for FNPP-derived 134Cs at 20°N–130°E in September 2012, that is, 2
years earlier than the model result. These differences between the modeled result of
Nakano and Povinec (2012) and our direct observation may be the result of limitations such as uncertainties regarding the amount of 137Cs released from the FNPP
and the resolution of the velocity field. Nakano and Povinec (2012) mentioned that
the KC and the KE were weaker in their model than the ARGO drifters predicted.

2.4.2

Transect Across the Kuroshio Extension

In October 2011, concentrations of 134Cs and 137Cs in excess of 20 Bq m−3 were
observed in surface waters and at 50-m depth north of the KE at 147°E (Fig. 2.8).
Alternatively, the subsurface peak of radioactive Cs was observed in the KE and south
of the KE (Fig. 2.8). The concentrations of 137Cs drastically decreased after 1 year at
all three stations and were distributed uniformly between 1.3 and 4.3 Bq m−3, which
were observed north of and in the KE in November 2012 (Fig. 2.8). In contrast, the
subsurface peak of 137Cs was observed at 9 to 12 Bq m−3 south of the KE, with 134Cs
detected in the KE and south of the KE in November 2012 (Fig. 2.8). Southeast of the
FNPP, 137Cs inventories north of the KE, in the KE, and south of the KE in October
2011 were calculated to be 3,840 ± 660, 6,370 ± 2,060, and 10,990 ± 3,870 Bq m−2,

22

H. Kaeriyama

Fig. 2.8 Vertical profiles of 137Cs north of the Kuroshio Extension (KE) (36°30′N), in the KE
(35°30′N), and south of KE (30°00′N-34°30′N). Open circles represent values recorded in October
2011. Closed circles represent values recorded in November 2012. Arrows indicate the detection
of 134Cs. Error bars indicate counting error (±1σ). When 137Cs was under the detection limit (<3σ),
the detection limit was plotted

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

23

respectively (Fig. 2.6c); those from November 2012 were 1,030 ± 280, 1,150 ± 370,
and between 2,440 and 3,300 Bq m−2, respectively (Fig. 2.6c).
In shallow water (0 and 50-m depth), high concentrations of 134Cs and 137Cs were
observed north of the KE, but low concentrations were observed in the KE and south
of the KE, which is consistent with previous studies showing that the KE prevented
the southward dispersion of radioactive Cs from the FNPP in the surface water
(Sect. 2.3; Aoyama et al. 2013a, b; Buesseler et al. 2012). Our results showed that
deeper intrusion of FNPP-derived radioactive Cs occurred at 34°30′N and 35°30′N
in October 2011 before the first winter after the FNPP accident. In October 2011, the
subsurface peak of 134Cs was observed from 24.0 to 26.5 σθ. Observations at 34°30′N
in November 2012 were between 25.1 and 26.1 σθ with a peak at 25.3 σθ. The difference in the density of subsurface 134Cs waters may indicate that different water
masses of FNPP-derived radioactive Cs existed during these 2 years. The large spatial variation of the FNPP-derived radioactive Cs around the KE was also discussed
with data obtained at 34°46′N–148°52′E in February 2012 (Kumamoto et al. 2013).
Rypina et al. (2013) reported model results of FNPP-derived radioactive Cs in the
area of 34°N–37°N, 142°E–147°E during March and June 2011. The three-dimensional (3-D) model results (fig. 9 of Rypina et al. 2013) suggested that FNPP-derived
137
Cs occasionally penetrated to 300–400 m in depth north of the KE during April
and June 2011 as a consequence of the spatial heterogeneity of mixed-layer depth
and the existence of strong downwelling regions. Furthermore, Oikawa et al. (2013)
showed data obtained near the FNPP during March 2011 and February 2012, which
were part of the monitoring program initiated by the Ministry of Education, Culture,
Sports, Science and Technology (MEXT). They concluded that the depth of σt isopycnals of 25.5–26.5 waters increased with time and transported the FNPP-derived
radioactive Cs to deep water from the FNPP-proximal coastal waters between May
and December 2011. Taking into account the monitoring data of MEXT (Oikawa
et al. 2013), the observational data from February 2012 (Kumamoto et al. 2013), and
model results (Rypina et al. 2013), it has been suggested that the subsurface peak of
radioactive Cs observed south of and in the KE in October 2011 may have been
transported from the coastal area off the FNPP without subduction.

2.4.3

Amount of 134Cs in Subsurface Core
Waters in the Southern Area

We estimated the amount of 134Cs in subsurface core waters south of both the KC
and the KE from our observational data collected in September 2012, when the
southernmost detection of 134Cs was observed at 18°N–135°E (Fig. 2.5). Results
suggest that the FNPP-derived radioactive Cs was taken into the NPSTMW and
then transported southwestward by the Kuroshio recirculation (Suga and Hanawa
1995). As a first step, the amount of 134Cs in the entire area of the NPSTMW was
estimated. The average concentration of 134Cs in the NPSTMW (26°49′N–34°30′N),
decay-corrected on March 11, 2011, was 11 ± 1.7 Bq m−3. Suga et al. (2008) estimated the total volume of the NPSTMW as 1 × 106 km3. Therefore, the amount of

24

H. Kaeriyama

134

Cs in the entire area of the NPSTMW would be estimated as 11 ± 1.7 PBq.
Kumamoto et al. (2014) reported 134Cs in the area around the center of the NPSTMW
during January and February 2012, estimating the total inventory of 134Cs in the
NPSTMW to be 6 PBq. These estimates may indicate that 6 PBq of 134Cs intruded
into the NPSTMW during March and April 2011, as observed in January and
February 2012 (Kumamoto et al. 2014), and 3.3–6.7 PBq additional 134Cs had
intruded into the NPSTMW during the 2011–2012 winter season, observed in
September 2012 (this study). Because the vertical resolution of this study was low
(seven layers between the surface and 1,000 m), and the study area was limited to
the western part of the NPSTMW, considerable uncertainty should have been taken
into account. The second estimate was limited to the peak depth of radioactive Cs
around the western part of the NPSTMW. Contours of acceleration potential on an
isopycnal surface indicate isopycnal streamlining in September 2012 based on
ARGO float data. The shape of the closed contour line of 19 m2 s−2 is similar to the
Kuroshio recirculation as described by Suga and Hanawa (1995), and the area was
defined as the western part of the NPSTMW (Fig. 2.9a).
The 134Cs concentration was estimated for the observationally sparse area in the
western part of the NPSTMW by Gaussian averaging (Fig. 2.9b). The thickness of
the NPSTMW core was estimated as the difference between the depths of isopycnal
surfaces 25.2 σθ and 25.4 σθ (Fig. 2.9c). The horizontal inventory of 134Cs in the
western part of the NPSTMW core was estimated using the product of the concentration and thickness listed above (Fig. 2.9d). Then, the amount of 134Cs in the core
of the western part of the NPSTMW in September 2012 was estimated to be 1.07
PBq, which accounts for 7–47 % of the total amount of 134Cs released directly into
the ocean from the FNPP (2.3–14.8 PBq of 137Cs; 134Cs/137Cs ratio assumed to be 1.0
Masumoto et al. 2012), or 10 % of the total deposition including direct release and
atmospheric surface deposition (11 PBq 134Cs; Kobayashi et al. 2013). Although the
estimation includes enormous uncertainties, it should be noted that a considerable
amount of the FNPP-derived radioactive Cs had been dispersed in the southwestern
portion of the North Pacific across the KC, which was considered to act as a barrier
against the southward dispersion of FNPP-derived radionuclides (Sect. 2.3, Aoyama
et al. 2013a, b; Buesseler et al. 2012). To clarify and improve the amount of FNPPderived radioactive Cs in the southwestern portion of the North Pacific, future studies should include not only collection of observational data, but also an improved
model with a comprehensive understanding of FNPP-derived Cs dispersion in the
oceanic environment.

Fig. 2.9 (continued) (b) Estimated spatial distribution of 134Cs concentration (Bq m−3) at the core
water of the western part of the NPSTMW, which is estimated by Gaussian averaging with a 1,000km e-folding scale applied to the 134Cs data collected during September and November 2012 and
decay-corrected on March 11, 2011. The black line indicates acceleration potential of 19 m2 s−2.
(c) Spatial distribution of water thickness between the isopycnal surfaces 25.2 σθ and 25.4 σθ based
on the Argo data. (d) Estimated inventory of 134Cs in the core water of the western part of the
NPSTMW in September 2012, which is estimated by the 134Cs concentration (Bq m−3) and the
water column thickness. The black line indicates acceleration potential of 19 m2 s−2

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

35°N

25

a

30°N

25°N

20°N

15°N
35°N

b

30°N

25°N

20°N

15°N
35°N

c

30°N

25°N

20°N

15°N
35°N

d

30°N

25°N

20°N

15°N
120°E

125°E

130°E

135°E

140°E

145°E

150°E

155°E

160°E

Fig. 2.9 (a) Acceleration potential on isopycnal surface 25.3 σθ referred to 1,000 dbar based on the
quality-checked Argo data (resolutions: horizontal 1° × 1°, vertical 25 layers from surface to 2,000-m
depth) during September 2012, which were obtained from http://www.jamstec.go.jp/ARGO/argo_
web/argo/index.html. The area with acceleration potential >19 m2 s−2 is colored in yellow.

26

2.5

H. Kaeriyama
134

Cs and 137Cs Around Japan Islands

The seawater samples for measurement of 134Cs and 137Cs were collected between
May 2011, 2 months after the FNPP accident, and March 2014 (Fig. 2.1). In the
Japan Sea, the East China Sea, the Seto Inland Sea, and the Bering Sea, only 137Cs
was detected at background levels (<2.0 Bq m−3), without any detectable 134Cs
(Fig. 2.10). Inoue et al. (2012), Wu et al. (2012), and Kim et al. (2012) reported
134
Cs at trace levels in the Japan Sea, the East China Sea, and around the Korean

Fig. 2.10 Sampling locations of surface seawater (a), and temporal variations of 137Cs in the western North Pacific (b), in the area north of 38°N (open circles), 37°N–38°N (open squares), south
of 37°N (open triangles), and in other areas, including the Japan Sea, the Seto Inland Sea, the East
China Sea, and the Bering Sea (cross) (Modified from Kaeriyama et al. 2014b)

2

134

Cs and 137Cs in the Seawater Around Japan and in the North Pacific

27

Peninsula, respectively. These results demonstrated that FNPP-derived radioactive
Cs slightly affected the Japan Sea, the East China Sea, the Seto Inland Sea, and the
Bering Sea.
In contrast, a high level of radioactive Cs was observed off the coast of East
Japan in the western North Pacific (Fig. 2.10). In May 2011, a high concentration of
137
Cs, in excess of 200 Bq m−3, was observed in the area 36°20′N–38°N, but concentrations were lower than 100 Bq m−3 south of 36°20′N (Fig. 2.11). In the area south
of 36°20′N, more than 500 Bq m−3 137Cs was observed in June 2011, 1 month after
our observation (Buesseler et al. 2012). Aoyama et al. (2012) reported temporal
variation of radioactive Cs at Hasaki (35°50.4′N–140°45.6′E), 180 km south of the
FNPP site, during April and December 2011. The peak of radioactive Cs at Hasaki
observed in June 2011 represented a delay of 2 months from the appearance of the
peak of radioactive Cs at the FNPP site in April 2011. The meso-scale eddy existed
in mid-latitudes between FNPP and Hasaki, and its center is located at
36°30′N–141°24′E. This eddy may have prevented the southward transport of
FNPP-derived radioactive Cs to Hasaki until the end of May 2011 (Aoyama et al.
2012). The difference in the horizontal distribution of 137Cs between May and June
2011 (Fig. 2.11) also clearly indicates that the warm core eddy inhibited the southward dispersion of FNPP-derived radioactive Cs along the east Japan coast until the
end of May 2011. North of the FNPP, the meso-scale eddy also affected the local

Fig. 2.11 Sampling locations of surface seawater and 137Cs concentration in May (circles) and
June (triangles) 2011. The data for June 2011 were obtained from Buesseler et al. (2012). Colors
of the closed and open symbols indicate the concentrations of 137Cs (Modified from Kaeriyama
et al. 2014b)

28

H. Kaeriyama

distribution of FNPP-derived Cs (Kofuji and Inoue 2013). The patchy distribution
of radioactive Cs was also observed around the meso-scale eddy just north of the
KE (as shown in Sect. 2.3). To comprehensively understand the patchy distribution
of radioactive Cs released from the FNPP, meso-scale-resolved models should be
developed.
Figure 2.12 shows temporal variations of 137Cs off the coast of East Japan based
on selected data sets (Aoyama et al. 2012; Buesseler et al. 2011; Kaeriyama et al.
2014b, d; Kaeriyama, unpublished data). To compare the decreasing trend of FNPPderived radioactive Cs within these data sets, the data of Aoyama et al. (2012) and
Buesseler et al. (2011) were plotted from the timing of the observed peak concentration. Exponential decrease was observed in each data set. During the first year from
the FNPP accident, drastic decreases of 137Cs were observed off the east coast of
Japan. On the other hand, after 1 year from the FNPP accident, the decay rate
seemed to be slower than that of the first year (Fig. 2.12), which may imply that the
extremely high radioactive Cs released during March and April 2011 was quickly
dispersed from the coastal area to the open ocean within 1 year from the FNPP
accident in this area. The weakened decreasing trend apparent after 1 year from the
FNPP accident would be affected by new inputs of FNPP-derived radioactive Cs,
such as continuing release from the FNPP site, even though continued release was
more than four orders of magnitude less than the direct discharge that occurred during March and April 2011 (Kanda 2013). Furthermore, river-borne waters and sediments should have been considered as a long-term source of FNPP-derived
radioactive Cs to the ocean. The concentration of 137Cs obtained from very near
coast (off the coast of Onahama; Fig. 2.12) were higher than that of offshore stations
(off the east Japan coast and Sendai Bay; Fig. 2.12), possibly caused by the fluvial
input of terrestrial FNPP-derived radioactive Cs. Nagao et al. (2013) reported the
transport of FNPP-derived radioactive Cs from a contaminated watershed in
Fukushima Prefecture to the coastal ocean area during July and December 2011;
they estimated the export flux of 134Cs and 137Cs after the heavy rain event (Typhoon
Roke in September 2011) as roughly 0.74–2.6 × 1010 Bq day−1 for the rivers of
Fukushima Prefecture. These values account for 30–50 % of the export of radioactive Cs for the 10 months of March 11–December 31, 2011 in these rivers (Nagao
et al. 2013). In the future, secondary dispersion of FNPP-derived radioactive Cs
through rivers, as considered in Nagao et al. (2013), and through groundwater
should be studied to understand the long-term effects of the FNPP accident in the
coastal area of East Japan.

Fig. 2.12 (continued) (Kaeriyama et al. 2014b), near the coast of Onahama (open triangles)
(Kaeriyama, unpublished data), near the coast of Hasaki (purple open diamonds) (Aoyama et al.
2012), and near the coast of Iwasawa (blue open diamonds) (Buesseler et al. 2011)

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Cs and 137Cs in the Seawater Around Japan and in the North Pacific

29

Fig. 2.12 Sampling locations of surface seawater (a) and temporal variations of 137Cs (b) in
Sendai Bay (open squares) (Kaeriyama et al. 2014d), off the coast of east Japan (open circles)

30

H. Kaeriyama

Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Chapter 3

Temporal Changes in 137Cs Concentration
in Zooplankton and Seawater off the
Joban–Sanriku Coast, and in Sendai
Bay, After the Fukushima Dai-ichi
Nuclear Accident
Hideki Kaeriyama

Abstract The Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident following
the Great East Japan Earthquake in 2011 resulted in the release of enormous
quantities of anthropogenic radionuclides into the ocean off the east Japanese coast,
especially radioactive cesium (134Cs and 137Cs). FNPP-derived radioactive Cs might
have consequently accumulated within marine food webs via seawater intake and
predator–prey interactions. This study provides evidence of temporal variability in
137
Cs concentrations in seawater and zooplankton samples collected off the Joban–
Sanriku coast and in Sendai Bay between June 2011 and December 2013. In Sendai
Bay, seawater 137Cs concentration was more than 1 Bq/kg in June 2011 and rapidly
decreased over the study period. 137Cs concentration in zooplankton was also
measured to be as high as high 23 Bq/kg-wet in June 2011, and this concentration
decreased at a slower rate than seawater concentrations. The difference in the rate of
decrease of 137Cs concentration between seawater and zooplankton resulted in an
elevated apparent concentration ratio (aCR) for zooplankton. The observed relationship between 137Cs in seawater and the aCR of zooplankton reflected the progression
of 137Cs contamination in zooplankton from the beginning of the FNPP accident to
the restoration phase.
Keywords Fukushima Dai-ichi Nuclear Power Plant accident • 134Cs •
Zooplankton • Seawater • Dynamic equilibrium • Concentration ratio

137

Cs •

H. Kaeriyama (*)
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: kaeriyama@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_3

33

34

3.1

H. Kaeriyama

Introduction

After the magnitude 9.0 Great East Japan Earthquake and subsequent tsunami on
March 11, 2011, a loss of electric power at the Fukushima Dai-ichi Nuclear Power
Plant (hereafter FNPP) resulted in an overheated reactor and hydrogen explosions.
Enormous quantities of radionuclides were then released into the ocean through
atmospheric fallout as well as direct release and leaking of the heavily contaminated
coolant water (Chino et al. 2011; Buesseler et al. 2011). Because of its relatively
long half-life (2.07 years for 134Cs and 30.07 years for 137Cs), evaluation of this
radioactive Cs in the marine environment is important for addressing risks both to
marine ecosystems and to public health through consumption of fisheries products.
The Japanese government conducted intensive monitoring of 131I, 134Cs, and 137Cs
concentrations in seawater offshore near the FNPP (Nuclear Regulation Authority
2014) and in fisheries products in a wide area around Japan to ensure the safety of
fishery products (Fisheries Agency 2014). In the western North Pacific, the dispersion pattern of FNPP-derived radioactive cesium from just after the FNPP accident
was studied by means of direct observations and simulation models (see Chap. 2).
The FNPP-derived radioactive Cs was dispersed eastward in the surface seawater in
a wide area of the northern Kuroshio Extension, and a part of the FNPP-derived
radioactive Cs contamination intruded into the southern area of the Kuroshio
Extension with mode water and was transported westward far south of the Japan
Islands (see Chap. 2).
Wada et al. (2013) demonstrated the temporal change in 134Cs and 137Cs concentrations as total radioactive cesium (134Cs + 137Cs), which is limited to 100 Bq/kg-wet
by Japanese authorities, in numerous species of marine organisms collected around
Fukushima Prefecture and clarified the difference in the decrease rate of radioactive
cesium among species. The decrease in rates of radioactive Cs in demersal fish was
slower than that of pelagic fish (Wada et al. 2013; Iwata et al. 2013; Buesseler
2012), mainly because of a high concentration of FNPP-derived radioactive cesium
in the marine sediments offshore near the FNPP (Kusakabe et al. 2013; Chap. 4).
Even though temporal changes of many fisheries products were clarified from the
monitoring data, the mechanism controlling the concentrations of radioactive Cs in
each marine organism is still unknown (Wada et al. 2013; Iwata et al. 2013; Buesseler
2012). One of the most important factors controlling the amount of radioactive Cs
in marine organisms is the uptake of radioactive Cs through food (Yoshida and
Kanda 2012). Unfortunately, information concerning FNPP-derived radioactive Cs
in the prey of fisheries products such as zooplankton and benthos is limited to those
of zooplankton collected from the open ocean after the FNPP accident (Buesseler
et al. 2012; Kitamura et al. 2013). Before the FNPP accident, several studies reported
the concentration of 137Cs in zooplankton around the Japanese coast (Tateda 1998;
Kaeriyama et al. 2008a). Kaeriyama et al. (2008a) reported that the concentration of
137
Cs in zooplankton collected before the FNPP accident off the coast of Aomori
Prefecture ranged from 0.01 to 0.02 Bq/kg-wet.
The concentration ratio (CR) (concentration in organisms relative to that in
media) under equilibrium conditions is a useful environmental parameter, used in

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

35

mathematical models to estimate the level of radionuclides present in the organisms
in comparison to the surrounding environment such as soil, sediments, water, or air
(IAEA 2004; Tagami and Uchida 2013; Howard et al. 2013). The recommended CR
values for 137Cs in marine zooplankton, fish, and crustaceans are 40, 100, and 50,
respectively (IAEA 2004). In this chapter, we did not calculate CR under equilibrium conditions; therefore, the CR value was referred to as the “apparent CR (aCR)”
and was compared to the pre-FNPP CR.
In June 2011, only 3 months after the FNPP accident, the Fisheries Research
Agency initiated a monitoring program to measure the environmental concentration
of FNPP-derived radioactive Cs in different marine ecosystems, such as seawater,
sediments, zooplankton, benthos, and fishes, in the most severely affected area off
the coasts of Fukushima, Miyagi, and Ibaraki Prefectures (hereafter Joban–Sanriku
coast) and in Sendai Bay (Fig. 3.1). In this chapter, we describe temporal changes in
the concentrations of 137Cs in seawater and zooplankton off the Joban–Sanriku
coast and in Sendai Bay that occurred from June 2011 to December 2013 based on
data from Kaeriyama et al. (2014). Although 134Cs was also determined, the
decreasing trend of 134Cs during more than 2 years was strongly affected by the
physical decay of 134Cs. Thus, only 137Cs is presented (134Cs data were reported in

Fig. 3.1 Seawater and zooplankton sampling locations. Filled and open circles indicate sampling
locations off the Joban–Sanriku coast in 2011 and in 2012, respectively. Filled and open squares
indicate the repeated sampling stations (E1, E4, C5, C12) and other stations, mostly observed in
June 2011 in Sendai Bay. The Fukushima Dai-ichi Nuclear Power Plant is shown as an open triangle in the right panel (Modified from Kaeriyama et al. 2014)

36

H. Kaeriyama

Kaeriyama et al. 2014). The fate of FNPP-derived radioactive Cs in seawater and
zooplankton is also discussed in regard to the atomic 137Cs/stable Cs ratio and the
relationship between 137Cs in seawater and 137Cs aCR of zooplankton.

3.2

Temporal Changes of 137Cs in Seawater and Zooplankton

After the FNPP accident, environmental 137Cs concentrations increased in seawater
and zooplankton in the area off the Joban–Sanriku coast and in Sendai Bay. Off the
Joban–Sanriku coast, the concentration of 137Cs decreased drastically by one order
of magnitude between 2011 and 2012 (Fig. 3.2a). Generally, the behavior of cesium
is thought to be conservative. Cesium is a soluble substance (<1 % is attached to
marine particles) (Buesseler et al. 2011), and it is dispersed primarily by ocean currents. In fact, FNPP-derived radioactive Cs was dispersed eastward rapidly in the
North Pacific, with an estimated speed of 8 cm/s, following predominant water currents (Aoyama et al. 2013). According to Kaeriyama et al. (2013), 134Cs and 137Cs
concentrations in surface seawaters at 144°E decreased by one or two orders of
magnitude between July 2011 and July 2012. The fate of 137Cs off the Joban–Sanriku
coast also mainly depends on seawater dilution. In Sendai Bay, the 137Cs monthly
average value measured in seawater drastically decreased from 770 mBq/kg in June
to 30 mBq/kg in December 2011. Subsequently, the decreasing trend continued,
although moderately, until the concentration reached 7 mBq/kg in November–
December 2013 (Fig. 3.2a). The residence time of seawater in Sendai Bay has been
estimated to be 40 days (Kakehi et al. 2012) even for calm ocean conditions; therefore, the rapid decrease in 137Cs observed during the first year following the FNPP
accident might have been influenced by the level of water exchange in this bay. 137Cs
peaked in surface waters between June and September 2011 at the E1, E4, and C5
sampling stations, although the vertical differences in 137Cs concentrations were not
obvious in December 2011 for the same stations (Fig. 3.3). The depth of the seasonal mixed layer may also influence the seasonal variation observed in the seawater 137Cs vertical profile. In April 2012, the differences observed in 137Cs
concentrations between the surface and the middle or bottom waters were reduced
in comparison with the differences observed during June and September 2011.
During 2011–2012, winter mixing led to a homogeneous vertical distribution of
137
Cs in this bay.
In contrast to the rapid decrease of FNPP-derived radioactive Cs measured in
seawater, the concentration of 137Cs in zooplankton showed only a gradual decrease
over the course of this study. 137Cs concentration in zooplankton ranged from 0.21
to 23 Bq/kg-wet (Fig. 3.2b). Off the Joban–Sanriku coast, the median 137Cs concentration in zooplankton decreased from 1.4 to 0.39 Bq/kg-wet between July–August
2011 and August 2012 (Fig. 3.2b). Although these data varied considerably among
stations, the 137Cs concentrations in zooplankton differed significantly between
July–August 2011 and August 2012 (Wilcoxon rank-sum test, p < 0.05). In Sendai
Bay, 137Cs concentrations in zooplankton did not differ significantly between zoo-

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

37

Fig. 3.2 Temporal changes in the concentration of 137Cs in seawater (average value of two or three
depth strata) (a) and in zooplankton (b), and the apparent concentration ratio (aCR) for zooplankton (c). Black open circles and red squares indicate data obtained off the Joban–Sanriku coast and
in Sendai Bay, respectively (Modified from Kaeriyama et al. 2014)

38
Fig. 3.3 Temporal changes
in 137Cs concentration in
seawater at E1 (a), E4 (b), C5
(c), and C12 (d) in Sendai
Bay. Open circles, filled
diamonds, and crosses
indicate the concentration of
137
Cs in surface, middle, and
bottom waters, respectively
(Modified from Kaeriyama
et al. 2014)

H. Kaeriyama

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

39

plankton collected using a Bongo net and a sledge net (Wilcoxon rank-sum test,
p > 0.05). The temporal change in the 137Cs concentration of zooplankton, in terms
of the median value calculated for each sampling period, clearly decreased from
June 2011 to April 2012, slightly increased and fluctuated between June and
September 2012, and then decreased again between September 2012 and June 2013
(Fig. 3.2b). The median 137Cs value measured in zooplankton in November 2013
was 13 % of that measured in June 2011.
The concentration of radioactive Cs in marine organisms is mainly influenced by
the rate of excretion of the organism and its intake of radioactive Cs from the prey
and the surrounding seawater. Iwata et al. (2013) estimated the “ecological halflife” (Teco) for marine organisms collected off the Fukushima prefecture. Teco is
defined as the time required for the radionuclides concentration to decline by 50 %
in a natural population. This value is influenced by both abiotic factors (such as
temporal changes in the concentration of radioactive Cs in seawater, extension of
the contaminated area, temperature, and salinity) and biotic factors (such as life
stages, feeding habitat, and population migration range). The Teco for the zooplankton samples collected in Sendai Bay and off the Joban–Sanriku coast was estimated
to be 263 ± 48 days (Teco ± SE, p < 0.0001) and 178 ± 31 days (p < 0.0001), respectively. The difference in Teco values between Sendai Bay and the Joban–Sanriku
coast may result from the difference in the decreasing rate of 137Cs in the surrounding seawater. The time required for a 50 % decline of 137Cs in seawater in Sendai
Bay (122 ± 10 days, p < 0.0001) was longer than that of the Joban–Sanriku coast
(85 ± 8 days, p < 0.0001). The ratios of Teco of zooplankton to the time required for
50 % decline in seawater in Sendai Bay and off the Joban–Sanriku coast are almost
comparable (2.2 vs. 2.1), suggesting that the decreasing rate of 137Cs in zooplankton
was strongly affected by the decreasing rate of 137Cs in ambient seawater.

3.3

Dynamic Equilibrium of Radioactive Cs
Between Zooplankton and Seawater

The concentration of radioactive Cs in marine organisms is mainly influenced by
the rate of uptake of radioactive Cs from prey and the surrounding seawater and the
excretion rate from the organism, which comes down to the dynamic equilibrium of
radioactive Cs between organisms and the surrounding seawater. The atomic ratio
of radioactive Cs and stable Cs in organisms and seawater is a good indicator of
whether dynamic equilibrium between the organism and seawater has been reached
(Tateda and Koyanagi 1994, 1996; Tateda 1998). The range of stable Cs concentrations in this study (16–190 ng/g-dry; Table 3.1) is comparable to the reported values
of zooplankton collected around the Japan Islands before the FNPP accident (12–
447 ng/g dry; Kaeriyama et al. 2008b; Masuzawa et al. 1988; Marumo et al. 1998;
Tateda 1998). The atomic 137Cs/Cs ratio in zooplankton (0.063–5.1 × 10−7; Table 3.1)
was one or two order of magnitudes higher than previously reported (2.7 ± 2.0 × 10−9
(Tateda 1998). Furthermore, the atomic 137Cs/Cs ratio fluctuated with time, and high

Station ID
Latitude
Off Joban–Sanriku coast
F250
37°34.8′N
F250
37°34.8′N
SY20
37°00.0′N
SY21
37°00.0′N
SY22
37°00.0′N
SY16
36°15.0′N
SY17
36°15.0′N
F250
37°34.8′N
Sendai Bay
C16
37°56.6′N
C10
37°59.5′N
E1
38°13.1′N
E4
38°09.9′N
C5
38°01.8′N

Sampling date

2012/4/19
2012/6/16
2012/8/3
2012/8/3
2012/8/4
2012/8/6
2012/8/6
2012/8/7

2011/7/22
2011/12/3
2012/4/22
2012/6/15
2012/6/18

Longitude

141°38.37′E
141°38.37′E
141°30.0′E
141°50.0′E
143°50.0′E
141°00.0′E
141°30.0′E
141°38.37′E

141°26.9′E
141°15.0′E
141°13.1′E
141°26.0′E
141°05.2′E

133
267
408
462
465

405
463
511
511
512
514
514
515

Days from
March 11 2011

0.28
1.7
0.95
2.3
6.2

0.47
0.21
1.8
0.79
0.30
0.29
0.49
0.24

Cs
(Bq/kg-wet)

137

34
53
54
16
126

154
63
34
34
27
34
79
41

Stable Cs
(ng/g-dry)

0.18
0.62
0.25
5.1
2.0

0.063
0.10
1.1
0.66
0.45
0.17
0.18
0.092

Atomic 137Cs/Cs ratio
Zooplankton (×10−7)

Table 3.1 Concentrations of 137Cs and stable Cs in zooplankton and the atomic 137Cs/Cs ratios in zooplankton and seawater

NSb
NS
13
8.5
29

3.5
6.6
3.4
6.9
5.1
3
7.7
5.3

Seawatera (×10−9)

40
H. Kaeriyama

C5
38°01.8′N
141°05.2′E
2012/7/14
491
4.3
64
C10
37°59.5′N
141°15.0′E
2012/7/14
491
2.4
42
C16
37°56.6′N
141°26.9′E
2012/7/15
492
4.1
35
C22
37°53.6′N
141°39.0′E
2012/7/15
492
2.0
30
E4
38°09.9′N
141°26.0′E
2012/8/10
518
1.7
127
C5
38°01.8′N
141°05.2′E
2012/9/9
548
1.4
33
C5
38°01.8′N
141°05.2′E
2012/9/10
549
9.7
77
E1
38°13.1′N
141°13.1′E
2012/11/10
610
3.0
71
E4
38°09.9′N
141°26.0′E
2012/11/10
610
1.9
179
C5
38°01.8′N
141°05.2′E
2012/11/10
610
1.0
69
C5
38°01.8′N
141°05.2′E
2012/11/10
610
0.46
72
E1
38°13.1′N
141°13.1′E
2013/6/15
827
0.68
58
C5
38°01.8′N
141°05.2′E
2013/6/15
827
1.1
75
C5
38°01.8′N
141°05.2′E
2013/6/15
827
0.22
42
E1
38°13.1′N
141°13.1′E
2013/11/15
980
2.9
189
C5
38°01.8′N
141°05.2′E
2013/11/15
980
0.32
49
Source: Modified from Kaeriyama et al. (2014)
a
The concentration of stable Cs in seawater was assumed to be 0.29 μg/l (Tateda and Koyanagi 1996)
b
NS no sample

1.8
2.1
3.1
1.6
0.32
1.3
3.4
1.8
0.37
0.65
0.28
0.28
0.35
0.12
0.50
0.26

NS
NS
NS
NS
2.2
7.9
7.9
1.8
1.8
11
5.3
4.4
4.4
7.6
7.3
6.3

3
Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…
41

42

H. Kaeriyama

values were observed between June and November 2012 (Table 3.1). According to
Tateda and Koyanagi (1996), the mean concentration of stable Cs in Japanese
coastal waters was 0.29 μg/l. From this value and the 137Cs concentration in seawater obtained in this study, the atomic 137Cs/Cs ratio of seawater was also calculated
(Table 3.1). The geometric mean of the atomic 137Cs/Cs ratio in seawater was
5.6 × 10−9 with a range of 2.2–29 × 10−9. The geometric mean is comparable with that
obtained before the FNPP accident (3.5–6.9 × 10−9; Tateda and Koyanagi 1996). A
high atomic 137Cs/Cs ratio of seawater (11–29 × 10−9) was observed at station E1 in
April 2012 and at station C5 in June and November 2012. One of the possible explanations for the temporal and spatial variations in the atomic 137Cs/Cs ratios of seawater and zooplankton may be the pulse input of FNPP-derived 137Cs from land to
ocean caused by heavy rain during the typhoon season or ice melt during thaw
season. Actually, Nagao et al. (2013) reported that the export flux of 137Cs from land
to ocean during the heavy rain season (September 2011) through rivers located in
the Fukushima Prefecture contributed 50 % of their annual export flux in 2011 (see
also Sect. 2.5). The input of FNPP-derived 137Cs from land to ocean is one of the
most important processes affecting the coastal environment and needs further investigation to understand the long-term effects of the FNPP accident on the coastal
region. Another possible input source of FNPP-derived radioactive Cs is continuing
release from the FNPP harbor; the estimated average release rate of 137Cs was
93 GBq day−1 in the summer of 2011 and 8.1 GBq day−1 in the summer of 2012
(Kanda 2013). However, as this radioactive Cs would be diluted offshore near the
FNPP harbor, the elevation of radioactive Cs concentration in seawater and zooplankton would be almost negligible within the present study area. Judging from the
atomic 137Cs/Cs ratio, which was higher than before the FNPP accident in zooplankton but constant in seawater, 137Cs dynamic equilibrium between zooplankton and
the surrounding seawater was not attained during the study period.
In contrast to Teco (see Sect. 3.2), the biological half-life (Tb) of zooplankton was
reported as 13 days (Vives i Batlle et al. 2007). The Tb of zooplankton strongly suggests that dynamic equilibrium should have been attained during this study. Because
the zooplankton samples contained multiple species (such as copepods, euphausiids, amphipods, chaetognath), including those with gut contents, the concentration
of radioactive Cs in zooplankton may have been affected by interspecies variability
in radioactive Cs concentrations in this study. The species-specific difference in
stable Cs content was less than one order of magnitude (Kaeriyama et al. 2008b;
Masuzawa et al. 1988; Marumo et al. 1998). Thus, the difference in species composition should not be a major factor influencing radioactive Cs in zooplankton. The
gut contents of zooplankton may contain suspended particles and/or clay particles;
clay particles have higher radioactive Cs than organic particles such as phytoplankton (Kusakabe et al. 2013). In addition, high concentrations of 134Cs and 137Cs were
observed in fecal pellets of zooplankton soon after the Chernobyl accident (Fowler
et al. 1987). The stable Cs contents in this study were almost comparable with previous studies based on samples containing gut contents (Kaeriyama et al. 2008b).
Thus, the high radioactive Cs in gut contents likely did not affect the concentration
of radioactive Cs in zooplankton. At present, it is difficult to determine the reason

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

43

for the slow decrease in the rate of 137Cs in zooplankton observed in this study.
Laboratory experiments on the uptake and excretion of radioactive Cs by zooplankton
under unstable conditions, such as radioactive Cs in seawater/prey that increases/
decreases with time, would provide insights on the time-dependent concentration of
radioactive Cs in seawater and the corresponding time-dependent concentration of
radioactive Cs in zooplankton.

3.4

Temporal Changes of the 137Cs Apparent Concentration
Ratio (aCR) of Zooplankton

The 137Cs aCR in zooplankton collected off the Joban–Sanriku coast varied from 5
to 276, and the median value increased with time from 12, measured in July 2011,
to 29, measured in August 2011, and to 115, measured in August 2012 (Fig. 3.2c).
In Sendai Bay, the aCR varied between 5 and 1,280 throughout the study period.
Because of the large variation in 137Cs concentrations among zooplankton samples,
aCR also varied within each sampling period in Sendai Bay. The aCR monthly
median value increased from 16, measured in June 2011, to 335 in December 2011
and fluctuated by more than 80, up to 854 in August 2012 and 730 in September
2012. The 137Cs aCR of zooplankton increased over time, although it varied significantly between months (Fig. 3.2c). In November–December 2013, the median aCR
value (262) was more than one order of magnitude higher than CR values obtained
before the FNPP accident, which ranged from 6 to 14 (Kaeriyama et al. 2008a). The
increase in aCR was mainly associated with differences in the rate of decrease of
137
Cs in seawater and zooplankton, as was clearly observed in Sendai Bay. The continuous uptake of 137Cs by zooplankton may lead to a slow rate of decrease of 137Cs
in zooplankton.
Figure 3.4a conceptually shows the temporal change in 137Cs expected in seawater and zooplankton following a release of large quantities of 137Cs, similar to the
FNPP accident. The concentration of 137Cs in seawater is expected to increase soon
after the release, and the increase in 137Cs in zooplankton is observed after that
(phase I). A sharp peak of 137Cs is observed in seawater samples, followed by an
exponential decrease with time (phase II). On the other hand, the maximum concentration of 137Cs in zooplankton is expected to be delayed from the peak of 137Cs
concentration in seawater and to gradually decrease with time (phase III). A time
lag in the 137Cs concentration between seawater and zooplankton leads to temporal
changes in aCR observed in zooplankton (Fig. 3.4b). Eventually, the rate of decrease
of 137Cs in seawater and zooplankton equalizes, and the zooplankton aCR reaches
the same level as the CR before the release of 137Cs to the environment (phase IV).
The dynamic equilibrium of 137Cs between zooplankton and the surrounding seawater is attained during phase IV. Figure 3.4c shows the relationship between seawater
137
Cs and aCR in zooplankton resulting from the temporal changes shown in
Fig. 3.4a, b. The relationship between seawater 137Cs concentration and 137Cs zooplankton aCR in this study along with those obtained from previous studies con-

44
Fig. 3.4 Conceptual
temporal variation in 137Cs
concentration in seawater
(thin lines) and in
zooplankton (bold lines) (a),
aCR for zooplankton (b), and
a scatter plot between 137Cs
concentrations in seawater
and aCR for zooplankton (c).
The temporal variation of
137
Cs is defined as the
time-course phase from I to
IV (Modified from
Kaeriyama et al. 2014)

H. Kaeriyama

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

45

Fig. 3.5 Scatter plot between 137Cs concentration in seawater and aCR for zooplankton off the
Joban–Sanriku coast (black open circles) and in Sendai Bay (red open squares) from this study
compared to those obtained in June 2011 in the western North Pacific (wNP) (green open triangles; Buesseler et al. 2012). The scatter plot between 137Cs concentrations in seawater and the
concentration ratio (CR) for zooplankton collected off Aomori Prefecture during October 2005 and
June 2006, before the FNPP accident, is shown as black filled diamonds (data from Kaeriyama
et al. 2008a). Arrows indicate flow of time (Modified from Kaeriyama et al. 2014)

ducted off the east of Japan in June 2011 (Buesseler et al. 2012) revealed that the
pattern observed in Fig. 3.4c corresponds with the aCR increasing phase under
dynamic nonequilibrium conditions (phase III; Fig. 3.5). Figure 3.5 also shows data
obtained under dynamic equilibrium conditions before the FNPP accident
(Kaeriyama et al. 2008a). The time lag expected during the elevation phase (phase I
and II) should have occurred during the few months following the FNPP accident;
however, this phase is not shown in Fig. 3.5 because these data were not available.
On the other hand, the fate of the FNPP-derived 137Cs in seawater and zooplankton
varied throughout the 3 years between the FNPP accident and this study, which
resulted in the negative correlation shown in Fig. 3.5. Although the 137Cs aCR in
zooplankton has steadily increased, the concentration of 137Cs in seawater has
remained nearly constant since before the FNPP accident (Fig. 3.5; 1–2 mBq/kg). If
no more 137Cs is added to the environment, the aCR in zooplankton would reach the
decreasing phase (phase IV), and 137Cs concentration in zooplankton would reach
pre-FNPP accident levels in the near future. Based on the Teco of zooplankton off the
Joban–Sanriku coast, the 137Cs concentration in zooplankton will reach the preFNPP accident level (0.015 Bq/kg-wet) after 2.6 years. Although the data were limited, the observed relationship between 137Cs concentration in seawater and the aCR
value measured in zooplankton accurately describes the progression of 137Cs contamination in zooplankton from the beginning of the FNPP accident (dynamic nonequilibrium state) to the restoration phase (dynamic equilibrium state).

46

3.5

H. Kaeriyama

Possible Application of the Relationship Between
Seawater 137Cs and aCR to Pelagic Fishes

The concept just mentioned could also be applicable to other marine organisms, in
particular to pelagic fishes that prey on zooplankton. Figure 3.6a shows the temporal changes in 137Cs concentration in pelagic fish collected from Sendai Bay and off
the Miyagi Prefecture (Fisheries Agency 2014) compared to the seawater and zooplankton concentrations in Sendai Bay shown in Fig. 3.2a, b. The two planktivorous
fishes, the sand lance Ammodytes personatus and the Japanese anchovy Engraulis
japonica, together with two carnivorous fishes, the chub mackerel Scomber japonicus and the Japanese sea bass Lateolabrax japonicas, were selected for this analysis. Figure 3.6b shows the scatter plots between 137Cs in seawater and the aCRs of
four fish species in relationship to the 137Cs concentrations measured in zooplankton
from Sendai Bay. The concentrations of radioactive Cs in fish published by the
Fisheries Agency in 2011 were the total of two radionuclides, 134Cs and 137Cs. The
activity ratio of 134Cs to 137Cs just after the FNPP accident is considered to be
approximately 1.0 (Chino et al. 2011; Buesseler et al. 2011), and the concentrations
of 137Cs, including physical decay, in fish in 2011 were estimated from this ratio. To
calculate the 137Cs aCR in fish, the concentration of 137Cs in seawater was estimated
from the exponential relationship between the concentrations of 137Cs measured in
Sendai Bay and the days since March 11, 2011 (Fig. 3.6a).
The concentration of 137Cs and aCR of planktivorous fishes, sand lance, and
Japanese anchovy were similar to those measured for zooplankton. On the other
hand, Japanese sea bass showed a higher concentration of 137Cs and aCR than other
fish and zooplankton. The species-specific difference in utilization of the environment, both for pelagic and benthic food webs and those from brackish environments
in the case of the Japanese sea bass (Kosaka 1969), may have led to the observed
difference in 137Cs concentrations and aCRs for the Japanese sea bass and other fish
and zooplankton. At present, understanding of the relationship between 137Cs in
seawater and the aCR in fish and their change with time is limited. Further analysis
that includes 137Cs data from prey items such as benthic organisms and seawater
samples covering broader areas is required to completely understand the evolution
of 137Cs concentrations in food webs. In addition, ecological/biological features of
target fish species, including spatiotemporal distribution, life cycles, and feeding
habitats, would provide further insights regarding the effect of the FNPP accident
on pelagic ecosystems in coastal areas off the FNPP.

3

Temporal Changes in 137Cs Concentration in Zooplankton and Seawater…

47

Fig. 3.6 (a) Temporal changes in 137Cs concentrations in seawater (red open triangles), zooplankton
(red open circles), sand lance (black crosses), Japanese anchovy (black plus symbols), chub mackerel
(black open diamonds), and Japanese sea bass (open squares) in Sendai Bay and off the coast of the
Miyagi prefecture (Fisheries Agency 2014). (b) Scatter plots showing the relationship between 137Cs
concentration in Sendai Bay seawater and the aCR in zooplankton (red open circles), sand lance
(black crosses), Japanese anchovy (black plus symbols), chub mackerel (black open diamonds), and
Japanese sea bass (black open squares) in Sendai Bay and off the coast of Miyagi Prefecture. The
scatter plot between 137Cs concentration in seawater and the CR for zooplankton off Aomori
Prefecture, obtained during October 2005 and June 2006 before the FNPP accident, is also shown as
filled circles (data from Kaeriyama et al. 2008a) (Modified from Kaeriyama et al. 2014)

48

H. Kaeriyama

Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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99:1838–1845
Kaeriyama H, Watabe T, Kusakabe M (2008b) The concentration of 137Cs and stable Cs in zooplankton in the western North Pacific in relation to their taxonomic composition. In: Proceedings
of the 16th Pacific Basin Nuclear Conference, paper ID P16P1197, Aomori, Japan, October
2008
Kaeriyama H, Ambe D, Shimizu Y, Fujimoto K, Ono T, Yonezaki S, Kato Y, Matsunaga H, Minami
H, Nakatsuka S, Watanabe T (2013) Direct observation of 134Cs and 137Cs in the western and
central North Pacific after the Fukushima Dai-ichi Nuclear Power Plant accident. Biogeosciences
10:4287–7295
Kaeriyama H, Fujimoto K, Ambe D, Shigenobu Y, Ono T, Tadokoro K, Okazaki Y, Kakehi S, Ito
S, Narimatsu Y, Nakata K, Morita T, Watanabe T (2014) Fukushima-derived radionuclides
134
Cs and 137Cs in zooplankton and seawater samples collected off the Joban-Sanriku coast, in
Sendai Bay, and in the Oyashio region. Fish Sci. doi:10.1007/s12562-014-0827-6

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49

Kakehi S, Ito S, Yagi H, T Wagawa (2012) Estimation of the residence time of fresh and brackish
water in Sendai Bay. J Jpn Soc Civ Eng Ser B2 (Coastal Engineering) 68:951–955 (in Japanese
with English abstract)
Kanda J (2013) Continuing 137Cs release to the sea from the Fukushima Dai-ichi Nuclear Power
Plant through 2012. Biogeosciences 10:6107–6113
Kitamura M, Kumamoto Y, Kawakami H, Cruz EC, Fujioka K (2013) Horizontal distribution of
Fukushima-derived radiocesium in zooplankton in the northwestern Pacific Ocean.
Biogeosciences 10:5729–5738
Kosaka M (1969) Ecology of the common sea bass, Lateolabrax japonicas in Sendai Bay. J Coll
Mar Sci Technol Tokai Univ 3:67–85 (in Japanese with English abstract)
Kusakabe M, Oikawa S, Takata H, Misono J (2013) Spatiotemporal distributions of
Fukushima-derived radionuclides in nearby marine surface sediments. Biogeosciences
10:5019–5030
Marumo K, Ishii T, Ishikawa Y, Ueda T (1998) Concentration of elements in marine zooplankton
from coastal waters of Boso Peninsula, Japan. Fish Sci 64:185–190
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zooplankton species. Mar Biol 97:587–591
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Japanese data. J Environ Radioact 126:420–426
Tateda Y (1998) Concentration factor of 137Cs for zooplankton collected from the Misaki coastal
water. Fish Sci 64:176–177
Tateda Y, Koyanagi T (1994) Concentration factors for 137Cs in marine algae from Japanese coastal
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biokinetic parameters for marine biota. Sci Total Environ 388:256–269
Wada T, Nemoto Y, Shimamura S, Fujita T, Mizuno T, Sohtome T, Kamiyama K, Morita T,
Igarashi S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ
Radioact 124:246–254
Yoshida N, Kanda J (2012) Tracking the Fukushima radionuclides. Science 336:1115–1116

Part II

Sediments and Benthos

Chapter 4

Three-Dimensional Distribution
of Radiocesium in Sea Sediment
Derived from the Fukushima
Dai-ichi Nuclear Power Plant
Daisuke Ambe, Hideki Kaeriyama, Yuya Shigenobu, Ken Fujimoto,
Tsuneo Ono, Hideki Sawada, Hajime Saito, Mikiko Tanaka, Shizuho Miki,
Takashi Setou, Takami Morita, and Tomowo Watanabe

Abstract This section introduces results of an investigation for radiocesium (134Cs and
137
Cs) in sea sediment. The three-dimensional spatial distributions of radiocesium in sea
sediment to a 14-cm core depth were surveyed from off the northern part of Ibaraki
Prefecture to off Fukushima Prefecture with 5-min horizontal resolution in July 2012,
approximately 16 months after the Fukushima Dai-ichi Nuclear Power Plant (FNPP)
accident. A high concentration band was observed along the 100-m isobaths where the
D. Ambe (*) • H. Kaeriyama • Y. Shigenobu • K. Fujimoto • T. Ono
M. Tanaka • S. Miki • T. Setou
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: Ambe@affrc.go.jp
H. Sawada
National Research Institute of Fisheries Engineering, Fisheries Research Agency,
7620-7, Hasaki, Kamisu, Ibaraki 314-0408, Japan
Maizuru Fisheries Research Station, Field Science Education and Research Center,
Kyoto University, Nagahama, Maizuru, Kyoto 625-0086, Japan
H. Saito
National Research Institute of Fisheries Engineering, Fisheries Research Agency,
7620-7, Hasaki, Kamisu, Ibaraki 314-0408, Japan
Agriculture, Forestry, and Fisheries Council, Agriculture, Forestry and Fisheries Research
Council, 1-2-1, Kasumigaseki, Chiyoda-ward, Tokyo 100-8907, Japan
T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
Fisheries Agency, 1-2-1, Kasumigaseki, Chiyoda-ward, Tokyo 100-8907, Japan
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_4

53

54

D. Ambe et al.

concentration of the 137Cs reached 1,240 Bq/kg-dry at the maximum and where vertical
profiles of the concentration generally had an exponential-type decline with depth. The
concentrations were very low at the area shallower than 100 m of depth north from the
FNPP, where vertical concentration peaks often occurred in deeper layers. These horizontal and vertical distribution patterns are suggested to be mainly determined by the supplied amount of radiocesium from the radiocesium-contaminated bottom seawater and
the ability of radiocesium adsorption as dependent on the grain size of the sediment.
Keywords Radiocesium • Sea sediment • Grain size • Organic matter • Bottom
seawater

4.1

Introduction

The Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident associated with the
Great Earthquake and ensuing tsunami that occurred east of Japan on March 11,
2011 caused a serious discharge of anthropogenic radionuclides directly into the sea
environment from that site. Although a large part of the FNPP-derived radiocesium
(134Cs and 137Cs) released directly into the ocean, which was one of the main discharged radionuclides (TEPCO 2012), was transported and diffused to the open
ocean by ocean currents (Buesseler et al. 2011; Aoyama et al. 2012; Tsumune et al.
2012; Kaeriyama et al. 2013, 2014), the radiocesium remained with relatively high
concentration levels in sea sediment off East Japan (Kusakabe et al. 2013).
Because 134Cs and 137Cs have long half-lives, about 2.06 years and 30.17 years,
respectively, these isotopes are of concern about their affects on the marine benthic
ecosystems. A report of marine organism monitoring (Wada et al. 2013) indicated that
the radiocesium concentrations in demersal fishes tended to have a higher and slower
decline than those in pelagic fish. Therefore, evaluation of the impact of the radiocesium in the sea bottom environment on marine benthic ecosystems is strongly and
socially required, but detailed distribution of the radiocesium on the sea bottom and its
features had been unclear. In this chapter, the three-dimensional distribution of the radiocesium concentration in sea sediment on July 2012, which was reported by Ambe
et al. (2014), is introduced. They revealed the detailed spatial distribution of radiocesium in sediments off the northern part of Ibraki Prefecture to Fukushima Prefecture,
with 5-min horizontal resolution (Fig. 4.1). Furthermore, they also obtained the vertical
structures of radiocesium in sediment to a 14-cm depth from the sea bottom by tubetype sediment core sampling (Fig. 4.2). (For details of the collecting and analyses for
the sediment samples, please see the original article.) The discussion by Amber et al. for
formative factors of the distribution of radiocesium in sediment is also introduced here.

4.2

Horizontal Distribution of Radiocesium

Figure 4.3 shows the obtained distributions of 134Cs and 137Cs concentrations in the
0–1, 1–2, 2–4, 4–6, 6–10, and 10–14 cm layers on July 2012 by Ambe et al. (2014).
The 134Cs concentrations were detected at all sampled locations to the 2–4 cm layer,

4

Three-Dimensional Distribution of Radiocesium in Sea Sediment Derived…

55

Fig. 4.1 Location of survey for radiocesium concentration in sea sediment in July 2012. Sediments
were sampled with a tube-type core sampler (squares) and a Smith–McIntyre grab sampler (triangles). Contour lines indicate water depth at an interval of 100 m. Cross indicates the location of
the Fukushima Dai-ichi Nuclear Power Plant (FNPP). Dotted line indicates a caution zone that had
been established during the survey period by the Japanese government

Fig. 4.2 Photographs of collecting sea sediment by a tube-type core sampler

56

D. Ambe et al.

indicating that radioactive contamination reached this depth by 16 months after the
FNPP accident. Although the obtained data were sparse in the deeper layer because
of the absence of sediment samplings, they indicated some interesting features of
horizontal patterns of radiocesium concentration throughout those sediment layers.
One point is that sediments with relatively high concentrations were distributed
along and near the coast and and in 100-m isobaths. For example, concerning the
137
Cs concentrations in the 0–1 cm sediment layer (Fig. 4.3g), where the geometric
mean of the concentration value was 100 Bq/kg-dry in the whole area with a value

Fig. 4.3 Spatial distributions of 134Cs (a–f) and 137Cs (g–l) concentrations in sediment in July
2012. The respective nuclide and layer are indicated at the upper left side of each map. “X” mean
that radiocesium was not detected (concentration was less than the lower limit of detection, which
was from 0.63 to 3.0 Bq/kg-dry). Blank tiles mean data missing where no sample was collected.
Contour lines indicate water depth at an interval of 100 m. Cross indicates the location of the FNPP

4

Three-Dimensional Distribution of Radiocesium in Sea Sediment Derived…

57

Fig. 4.3 (continued)

range from 8.8 to 1,240 Bq/kg-dry, most of the concentrations higher than 150 Bq/
kg-dry were distributed in these areas. It can be also seen that the high-concentration
bands were divided into two in the northern part of Fukushima Prefecture, associated with the 100-m isobath that goes away from the coast there.
Another significant feature is that sediments with relatively low concentrations
were found between the two high-concentration bands in the northern part of
Fukushima Prefecture. The concentration value less than approximately 20 Bq/kgdry was locally concentrated in this area. Furthermore, a narrow minimal concentration band of 30–60 Bq/kg-dry in the 0–1 cm sediment layer also seemed to exist
near the 200-m isobaths in about 20–30 km east from the high-concentration band
in the south of the FNPP. Because this low band did not quite range over plural grid
points from east to west, the band width was probably less than 15 km (for instance,

58

D. Ambe et al.

a longitudinal 5-min grid interval is approximately 7.4 km at 37°N). These results
indicate that radiocesium concentration does not simply decrease toward offshore.

4.3

Vertical Distribution of Radiocesium

Figure 4.4 shows all the acquired vertical profiles of the 137Cs concentrations in the
sea sediment in July 2012. Although the 137Cs concentration values ranged widely
over two orders of magnitude in each layer, the values from the 25 to 75 percentiles
ranged less than one order of magnitude. The median value was the highest in the
uppermost layer from the surface (0–1 cm), and generally exponentially decreased
in deeper layers; the median values were 102, 78.3, 46.8, 19.3, 13.1, and 6.54 Bq/
kg-dry in the 0–1, 1–2, 2–4, 4–6, 6–10, and 10–14 cm layers, respectively. Cases
wherein the highest concentration was found in the surfacemost layer occupied
53 % of all the profiles. In the remaining cases, the concentration peaks were found
in layers deeper than 0–1 cm.
To detect areas with concentration peaks in the deeper layers, all the 137Cs concentration data were converted to relative ratios to 137Cs concentration in the 0–1 cm
layer at each location (Fig. 4.5). It can be seen that relatively high ratios were found
near the coast. Ambe et al. (2014) suggested resuspension and redeposition pro-

Fig. 4.4 All obtained vertical
profiles (gray lines with
circles) of 137Cs concentration
in July 2012. The box-andwhisker plot shows the
minimum value, the 25th,
50th, and 75th percentiles,
and the maximum value,
respectively, in each layer

4

Three-Dimensional Distribution of Radiocesium in Sea Sediment Derived…

59

cesses of sediment as possible causes for this factor; that is, in the coastal region, the
sea bottom is easily disturbed by ocean waves and bottom currents in general.
Therefore, sediment contaminated by radiocesium at the surface and that uncontaminated in deep layers can be mixed or overturned. However, they also suggested
another process can operate at the area north of the FNPP where the radiocesium
concentrations were very low (Fig. 4.3); the relative ratios were especially high in
the deeper layers there. In this regard, a possible factor is introduced with the grain
size of sea sediment in the following section.

Fig. 4.5 Relative magnitude of 134Cs (a–f) and 137Cs (g–l) concentration compared with in the
surface-most (0–1 cm) sediment at each location in July 2012. The respective layer is indicated at
the side of each map

D. Ambe et al.

60

Fig. 4.5 (continued)

4.4

Grain-Size Distribution and Relationship
with Radiocesium Concentrations in Sediment

Figure 4.6 shows the horizontal distribution of the median grain sizes of sediments
in the surface layer (0–1 cm). Relatively large grain sizes were distributed in the
north of the FNPP where the radiocesium concentrations were very low (Fig. 4.3),
whereas a band of very small grain sizes, less than 100 μm diameter, was found
around the 100-m isobaths where the radiocesium concentrations were high
(Fig. 4.3). Ambe et al. (2014) further showed a significant correlation between 137Cs

4

Three-Dimensional Distribution of Radiocesium in Sea Sediment Derived…

61

Fig. 4.6 Spatial distribution of median particle grain size of the surface-most sediment in July
2012

concentration and median grain size: the correlation coefficient is −0.38 (p < 0.01)
(Fig. 4.7a). It is well known that Cs has strong affinity with fine minerals, especially
illite minerals (Børrentzen and Salbu 2012; Comans et al. 1991; Comans and
Hockley 1992; Sakuma and Kawamura 2011). Indeed, by sieving and dividing the
surface sediment samples into three grain-size fractions (<106, 106–250,
and > 250 μm), we also obtained similar results, that is, the finer-size fraction of the
sediment samples had higher radiocesium concentrations than the bulk sediment in
most cases (Fig. 4.8). Thus, the probable grain size-dependent adsorption capability
of cesium is strongly suggested as one of the factors that determines the spatial
distribution pattern of radiocesium concentration. In addition, as the proportional
relationship between the permeability and grain size of sediment is also well known
(Shepherd 1989), dissolved radiocesium can migrate downward with seawater
through large-grained sediments. Therefore, it can be considered that higher radiocesium concentrations than those in the surface sediment existed in deeper layers at
the area north from the FNPP, as indicated in the previous section.

D. Ambe et al.

62

Fig. 4.7 (a) Comparison between 137Cs concentration and median grain size in the most-surface
sediment. The symbols for the scatter plot show the clusters segmented into five types by the group
average method; the corresponding locations of those types are projected in (b)

50

< 106 µm

40

Frequency

106-250 µm
30

> 250 µm

20

10

0

Relative Proportion of

137Cs

Concentration

Fig. 4.8 Histograms of relative magnitude of 137Cs concentration in each diameter class of the
surface-most sediment compared with the concentration in bulk sediment. Diameter classes are
indicated at upper right

4

Three-Dimensional Distribution of Radiocesium in Sea Sediment Derived…

63

Ambe et al. (2014) also indicated that the quantity of radiocesium supplied to the
sea bottom from seawater is another factor to determine the distribution of the radiocesium concentration in sea sediment. The concentrations ranged over more than
one order of magnitude in each similar grain-size class, but the samples could be
divided into five clusters (symbols in Fig. 4.7a) by cluster analysis based on the
group average method (Romesburg 2004), using the distance on the coordinate
between the median grain size and 137Cs concentration. Accordingly, three types of
clusters by geographic dependence were detected (Fig. 4.7b): (1) large grain sizes
and low radiocesium concentrations, distributed at depths shallower than 100 m in
the region north from the FNPP (indicated by filled triangles in the figure); (2) small
grain sizes with high radiocesium concentrations, distributed mainly at depths
shallower than 100 m, excepting the area of cluster (1) (indicated by filled squares);
and (3) small grain sizes with low radiocesium concentrations, mainly in the area
deeper than 100 m (filled circles). The division of cluster (1) from others can be
attributed mainly to the low adsorption capability of large-grain-size sediment for
cesium, as already mentioned. On the other hand, the radiocesium concentration in
bottom seawater could be more than twice or one order higher in the area shallower
than 100 m than in the area at 100–300 m depth by monitoring data (Oikawa et al.
2013) and numerical study (Bailly du Bois et al. 2014), for division between the
clusters (2) and (3).

4.5

Organic Matter Content and Relationship
with Radiocesium Concentration in Sediment

Ambe et al. (2014) also investigated the horizontal distribution of the organic matter
content in the surface sediment (as shown in Fig. 4.9a). Although notably higher
values, up to almost 10 %, existed along the 100-m isobaths where the radiocesium
concentrations were very low, the content was relatively low north of the FNPP
where the radiocesium concentrations were high. These patterns highly corresponded to those of the median grain size. Therefore, the organic matter content
also was correlated with the 137Cs concentration (r = 0.38, p < 0.01) and the median
grain size (r = −0.76, p < 0.01) (Fig. 4.9b). This result seems superficially to indicate
that organic content also can determine radiocesium concentration. However, a
report for radiocesium concentration in the coastal area of Ibaraki Prefecture after
the FNPP accident (Otosaka and Kobayashi 2013) indicated that the lithogenic fraction contained most of the 137Cs in the sediment. The contribution of organic matter
to the radiocesium concentration in sea sediment is also small by chemical leaching
for the samples of Ambe et al. (2014) (as seen in the next chapter). Thus, the organic
matter might not be the constitutive factor that determines radiocesium concentration in sea sediment more than 1 year after the FNPP accident. The grain size of
sediment could determine the distributions of both the 137Cs concentration and the
organic matter content in sediment.

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D. Ambe et al.

Fig. 4.9 (a) Spatial distribution of organic matter content of the surface-most sediment in July
2012. (b) Comparison between 137Cs concentration and organic matter content in the surface sediment. Symbols correspond to the result of cluster analysis in Fig. 4.7a

Acknowledgments This study was supported by the Fisheries Agency, Ministry of Agriculture,
Forestry and Fisheries, Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
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Morita T, Watanabe T (2014) Five-minute resolved spatial distribution of radiocesium in sea
sediment derived from the Fukushima Dai-ichi Nuclear Power Plant. J Environ Radioact
138:264–275. doi:10.1016/j.jenvrad.2014.09.007
Aoyama M, Tsumune D, Uematsu M, Kondo F, Hamajima Y (2012) Temporal variation of 134Cs
and 137Cs activities in surface water at stations along the coastline near the Fukushima Dai-ichi
Nuclear Power Plant accident site, Japan. Geochem J 46(4):321–325
Bailly du Bois P, Garreau P, Laguionie P, Korsakissok I (2014) Comparison between modelling
and measurement of marine dispersion, environmental half-time and 137Cs inventories after the
Fukushima Daiichi accident. Ocean Dyn 64(3):361–383. doi:10.1007/s10236-013-0682-5
Børrentzen P, Salbu B (2012) Fixation of Cs to marine sediments estimated by a stochastic modeling approach. J Environ Radioact 61:1–20

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56:1157–1164
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Kaeriyama H, Ambe D, Shimizu Y, Fujimoto K, Ono T, Yonezaki S, Kato Y, Matsunaga H, Minami
H, Nakatsuka S, Watanabe T (2013) Direct observation of 134Cs and 137Cs in the western and
central North Pacific after the Fukushima Dai-ichi Nuclear Power Plant accident. Biogeosciences
10:4287–7295
Kaeriyama H, Shimizu Y, Ambe D, Masujima M, Shigenobu Y, Fujimoto K, Ono T, Nishiuchi K,
Taneda T, Kurogi H, Setou T, Sugisaki H, Ichikawa T, Hidaka K, Hiroe Y, Kusaka A, Kodama
T, Kuriyama M, Morita H, Nakata K, Morinaga K, Morita T, Watanabe T (2014) Southwest
intrusion of 134Cs and 137Cs derived from the Fukushima Dai-ichi Nuclear Power Plant accident
in the western North Pacific. Environ Sci Technol 48:3120–3127
Kusakabe M, Oikawa S, Takata H, Misonoo J (2013) Spatiotemporal distributions of Fukushimaderived radionuclides in nearby marine surface sediments. Biogeosciences 10:5019–5030.
doi:10.5194/bg-10-5019-2013
Oikawa S, Takata H, Watabe T, Misonoo J, Kusakabe M (2013) Distribution of the Fukushimaderived radionuclides in seawater in the Pacific off the coast of Miyagi, Fukushima, and Ibaraki
prefectures, Japan. Biogeosciences 10:5031–5047. doi:10.5194/bgd-10-4851-2013
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S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ Radioact
124:246–254. doi:10.1016/j.jenvrad.2013.05.008

Chapter 5

Radiocesium Concentrations in the Organic
Fraction of Sea Sediments
Tsuneo Ono, Daisuke Ambe, Hideki Kaeriyama, Yuya Shigenobu,
Ken Fujimoto, Kiyoshi Sogame, Nobuya Nishiura, Takashi Fujikawa,
Takami Morita, and Tomowo Watanabe
Abstract  Sequential chemical extraction of radiocesium was performed on 22
­surface sediment samples to assess radiocesium concentration in the organic fraction of sea sediments (Csorg). Our results showed that Csorg of sea sediments was
significantly larger than that of bulk sediments (Csbulk). The concentration factor
of radiocesium in organic fraction against the bulk concentration (CF) varied
from 3 to 50 off the Fukushima continental margin and showed a proportional
relationship with median grain size and an inversely proportional relationship
with organic content (OC) of the sediment. By using these relationships, the
regression equation of Csorg based on median grain size, organic content, and
Csbulk was determined to construct a two-dimensional (2-D) distribution of Csorg
along the continental margin off the Fukushima region. The resultant map showed
that the continental margin north of Fukushima Dai-ichi Nuclear Power Plant
(FNPP) had moderate Csorg values despite very low Csbulk. On the other hand,
sediments sampled at the mouth of Abukuma River showed extremely low CF,
which might have been caused by the existence of river-derived sediment
particles.
Keywords Sediment • Radiocesium • Organic fraction

T. Ono (*) • D. Ambe • H. Kaeriyama • Y. Shigenobu
K. Fujimoto • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: tono@affrc.go.jp
K. Sogame • N. Nishiura • T. Fujikawa
KANSO Technos, 3-1-1 Higashikuraji, Katano, Osaka 576-0061, Japan
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_5

67

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T. Ono et al.

5.1  Introduction
In the assessment of radiocesium transportation from sea sediments to a marine demersal ecosystem, information is required not only on the concentration but also on biological ingestibility of sea sediment radiocesium. Although IAEA has provided a
standard concentration factor of radiocesium from sea sediments in marine organisms
(e.g., 1 × 102 for fish; IAEA 2004), its actual value may vary according to sediment
properties such as grain size and chemical composition. Radiocesium concentration in
the organic fraction of sediments (Csorg) is an important factor because the transport of
radiocesium from sediment to demersal ecosystem occurs primarily through the feeding/ingestion of carbon sediments by benthos. With regard to the FNPP accident, a
large amount of data is available on the spatiotemporal distribution of radiocesium
concentration in sea sediments (Csbulk) off the Fukushima Prefecture (Otosaka and
Kobayashi 2012; Kusakabe et al. 2013; Otosaka and Kato 2014; Ambe et al. 2014).
Unfortunately, insufficient data are available on the spatiotemporal distribution of Csorg.
To address this issue, we conducted sequential chemical leaching experiments for 21
sea sediments sampled in July 2012 at 5′ × 5′ grid stations off Fukushima Prefecture
(Ambe et al. 2014; see Fig. 5.1 for station map) to measure Csorg of these sediments. For
details of sampling stations and experimental procedures, see Ono et al. (2015).

5.2  Csorg and Its Relationship with Csbulk
Estimated radiocesium concentrations in organic fraction (Csorg) and bulk sediment
(Csbulk) in 21 grid samples are listed in Table 5.1. Csbulk ranged from 31 to 910 Bq/
kg-dry and Csorg ranged from 345 to 3,390 Bq/kg-org-dry. Concentration factor
(CF) and inventory ratio (IR) of radiocesium in organic fraction against bulk sediment were then calculated by the following equation:


CF = Csorg / Csbulk



IR = ( Csorg × OC ) / Csbulk

(5.1)




(5.2)

where OC represents the organic content of the sediment (Table 5.1).
CF values vary from 3 to 50, clearly illustrating that radiocesium concentration
in the organic fraction of sea sediments is always several times larger than that of
bulk sediment in areas off Fukushima. Despite these high CF values, IR showed
relatively low values, ranging from 2.4 % to 13.9 %, reflecting low organic content
in open ocean sediments.
Land sediments and soils have highly selective, nonexchangeable cesium adsorption capacity, up to 1 × 10−11 mol/kg-dry, because of the frayed edge sites in illite
particles (Nakao et al. 2012). In marine environments, however, such
­nonexchangeable adsorption sites are occupied by stable cesium (~2 × 10−9 mol/l in
seawater) and potassium (~1 × 10−2 mol/l in seawater). Newly supplied radiocesium
from the accident, therefore, can only be bound to nonselective, exchangeable
­sorption sites, with the distribution coefficient of radiocesium estimated to be

5  Radiocesium Concentrations in the Organic Fraction of Sea Sediments

69

Fig. 5.1 Map of the location of the samples used in this study. Thick gray line denotes Abukuma
River (only lower reaches are shown). Open squares denote the samples used for the bulk extraction experiment (Table 5.1), and open triangles denote the location of the off-Abukuma station
(Table 5.2). Sampling stations of Ambe et al. (2014) are overlaid as solid squares

300–4,000 l/kg-dry (IAEA 2004). Organic substances in the sediments also have
nonselective sorption sites for cesium, but so far little is known about the distribution coefficient of cesium between marine organic matter and seawater. On land,
several observations have indicated that the distribution coefficient of cesium for
organic substances in soils is of the order of 102–103 l/kg-dry (Bunzl and Schimmack
1991; Nakamaru et al. 2007). If we assume that marine organic substances have the
same distribution coefficient of cesium as land soils, we can consider that mineral
and organic substances in the off-Fukushima sediments have the same order of preference as FNPP-derived radiocesium. The apparent preference of radiocesium in
organic substances further increases when the surface of mineral particles is covered by organic substances (Keil et al. 1994; Mayer 1994; 1999). Mayer (1999), for
example, found that even 0.5 % (w/w) of organic carbon can cover more than 10 %
of total sediment surface area. In this case, with the assumption that organic carbon
and mineral surfaces have the same preference with cesium, the observed CF of
radiocesium increases to more than 20.

Station no. Sampling date Latitude [N] Longitude [E]
S1
2012.7.11
36° 20′
140° 55′
S2
2012.7.11
36° 20′
140° 50′
S3
2012.7.11
36° 20′
140° 45′
S4
2012.7.11
36° 20′
140° 40′
S20
2012.7.12
36° 40′
141° 10′
S21
2012.7.12
36° 40′
141° 05′
S22
2012.7.12
36° 40′
141° 00′
S23
2012.7.12
36° 40′
140° 55′
S24
2012.7.12
36° 40′
140° 50′
S25
2012.7.12
36° 40′
140° 45′
S59
2012.7.13
37° 05′
141° 25′
S60
2012.7.13
37° 05′
141° 20′
S61
2012.7.13
37° 05′
141° 15′
S62
2012.7.13
37° 05′
141° 10′
S63
2012.7.12
37° 05′
141° 05′
S64
2012.7.12
37° 05′
141° 01′
S92
2012.7.15
37° 40′
141° 03.5′
S93
2012.7.15
37° 40′
141° 05′
S94
2012.7.15
37° 40′
141° 10′
S95
2012.7.15
37° 40′
141° 15′
S96
2012.7.15
37° 40′
141° 20′
All data are reproduced from Ono et al. (2015)
Note: For definitions of Csbulk, Csorg, OC, CF, and IR, see the text

Bottom
depth (m)
257
120
59
33
261
144
133
111
70
33
177
151
140
120
72
25
24
28
37
59
100

Table 5.1  Specifications and measurement results of grid samples
Median grain
size (μm)
142
136
889
201
233
265
161
87
116
no data
247
225
85
87
158
167
118
407
723
1,240
146
OC (%)
0.8
0.7
0.4
1.0
0.6
0.5
1.0
1.6
1.0
0.3
0.6
0.6
1.3
1.6
1.6
0.9
1.0
0.2
0.1
0.1
0.7

Csbulk
(Bq/kg-dry)
49 ± 5.5
78 ± 6.6
153 ± 9.7
310 ± 20
103 ± 6.3
60 ± 4.7
180 ± 13
180 ± 14
270 ± 21
69 ± 5.9
83 ± 5.4
104 ± 6.3
101 ± 7.6
440 ± 27
690 ± 32
910 ± 32
710 ± 28
82 ± 5.9
31 ± 3.4
47 ± 4.1
230 ± 16

Csorg
[Bq/kg-org-dry]
350
1,440
2,440
1,090
520
850
1,330
960
1,300
490
470
2,360
600
1,200
1,840
3,120
3,390
1,270
780
2,330
2,080
CF
7
19
16
4
5
14
7
6
5
7
6
23
6
3
3
3
5
16
25
50
9

IR [%]
5.8
12.0
5.9
3.4
3.0
7.0
7.3
8.9
4.9
2.4
3.2
13.9
7.4
4.5
4.2
3.2
4.9
4.0
3.2
5.0
6.5

70
T. Ono et al.

71

5  Radiocesium Concentrations in the Organic Fraction of Sea Sediments

5.3  H
 orizontal Distribution of Csorg in off-Fukushima
Continental Margin
CF is roughly proportional to median grain size and inversely proportional to OC
(Fig. 5.2), suggesting that either or both of these properties are the main control factors of CF, although detailed analysis by Ono et al. (2015) concluded that OC is a
major control factor and median grain size is minor. Using this information, we
applied dual-parameter regression, appropriate for CF, against median grain size
and combustion loss as follows:


(

)

CF = 0.0255m + 20.08 / IL - 0.69 r 2 = 0.736, r < 0.01

(5.3)

where μ and IL represent median grain size in μm (micrometers) and ignition loss
in percentage, respectively. We chose IL instead of OC as an explanatory variable
because the latter parameter was not measured for all samples reported by Ambe
et al. (2014). Although IL somewhat overestimated the actual OC, we confirmed the
linearity of IL against OC before the derivation of Eq. (5.3). We applied this equation to 113 surface stations observed by Ambe et al. (2014), and the calculated CF
was multiplied by Csbulk in each station (Fig. 4.3 in Chap. 4) to obtain Csorg. The
results are shown in Fig. 5.3. A high Csorg band exists just offshore south of FNPP,
within which the highest Csorg value of 10,300 Bq/kg-org-dry was obtained. In this
area, the typical range of Csbulk south of FNPP was 2,000–7,000 Bq/kg-org-dry for
the area with a bottom depth shallower than 100 m, and 500–1,500 Bq/kg-org-dry
Fig. 5.2  Plot of
concentration factor (CF)
versus median grain size
(solid circles) and 1/organic
content (OC) (open circles)
for 21 off-Fukushima
samples

72

T. Ono et al.

Fig. 5.3  Distribution of calculated Csorg (organic cesium) in the off-Fukushima continental margin
area. Contours are drawn from the Csorg value estimated by Eq. (5.3) for each station of Ambe et al.
(2014)

for the area with bottom depth ranging from 100 to 200 m. In the station north of
FNPP, Csorg showed medium concentrations (~300–3,600 Bq/kg-org-dry) for the
area with a bottom depth shallower than 100 m, and Csbulk values were extremely
low (~10–100 Bq/kg-dry; see Ambe et al. 2014 and previous chapter); this is because
the sediments of the mid-depth area (~30–100 m) north of FNPP consist mainly of
large particles with low organic carbon content, which, using Eq. 5.3, leads to very
high CF values. This result implies that the potential effect of sea sediment radiocesium on benthos would not be too different between the area south of FNPP with a
bottom depth ranging from 100 to 200 m and north of FNPP with a bottom depth
shallower than 100 m, despite a significant Csbulk difference between these areas.
Wada et al. (2013) detected similar radiocesium level of demersal fishes between
these two areas after 2012. These findings suggest that Csorg can be used as an indicator of the potential effect of sediment radiocesium on the demersal ecosystem.

5  Radiocesium Concentrations in the Organic Fraction of Sea Sediments

73

Table 5.2  Specifications and measurement results of off-Abukuma patch
Bottom
Station Sampling Latitude Longitude depth
(m)
no.
date
[N]
[E]
ABK-A 2013.8.22 38° 2.4′ 140° 56.4′ 13

Csbulk
Median
grain
OC (Bq/
size (μm) (%) kg-dry)
No data 16 5,600 ± 75

Csorg (Bq/
kg-orgIR
dry)
CF (%)
7,882
1.4 23

5.4  Csorg and CF in off-Abukuma River Sediments
As the sediments described in the former sections are sampled from the continental
margin, organic materials contained in these sediments are thought to be produced
in the ocean. However, sediments in some local areas such as river mouths contain
lithogenic particles, which were produced within freshwater or on land and then
transported to the seafloor after the FNPP accident. For such sediments, CF can be
considerably low because the nonexchangeable adsorption sites of mineral particles
were not occupied by stable cesium or potassium at the time of the accident. To
assess the CF value for such sediments, we performed additional Csorg measurements for sediments taken from the local high radiocesium patch recently discovered by the Nuclear Regulation Office (NRA 2014), located just outside of the
Abukuma River mouth, with a horizontal scale of about 900 × 400 m width.
Differing from the foregoing grid samples, Csorg in the off-Abukuma patch
showed significantly low CF values (~1.4; Table 5.2), possibly because of the significantly high OC value in the sample. Hence, a high-OC sediment tends to have a
low CF value (Fig. 5.2). Another reason might be that the sediments in this patch
contain a significant amount of lithogenic particles derived from the Abukuma
River (Yamashiki et al. 2014). Although the observed Csbulk in this patch is the highest among the oceanic stations we observed, a low CF in the sediments causes the
Csorg value to be at the same level as the average value of off-Fukushima sediments.
The monitoring results for marine products for the off-Miyagi prefecture region did
not detect any local increase in the occurrence of high-Cs fishes in off-Abukuma
regions (JFA 2014), despite the existence of a high-Cs patch in sediments. A significantly low CF in the off-Abukuma sediment patch may explain these observation
results. Again, our results showed that not only Csbulk but also Csorg are essential for
accurately assessing the potential effect of sediment radiocesium on the demersal
ecosystem in each region.

5.5  Summary
Our study clarifies that radiocesium concentration in the organic fraction of sea
sediments is always larger than that in the organic fraction of bulk sediments. This
result indicates that the transport efficiency of radiocesium from the organic fraction
of sediments to the marine benthos is extremely low, because the radiocesium

74

T. Ono et al.

concentration in marine benthos is of the order of 101 Bq/kg-wet (see Chap. 7). The
details of the physiological mechanism that results in such low transport efficiency
is an important topic for future study.
Based on Csorg, we assessed that the sediments in the off-Fukushima continental
margin north of the FNPP have moderate potential to transport radiocesium to benthic ecosystems, despite the low Csbulk observed in this region. However, sediments
off Abukuma River have less potential to transport radiocesium than the level
inferred from its Csbulk value.
Open Access  This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
Ambe D, Kaeriyama H, Shigenobu Y, Fujimoto K, Ono T, Sawada H, Saito H, Miki S, Setou T,
Morita T, Watanabe T (2014) A high-resolved spatial distribution of radiocesium in sea sediment derived from Fukushima Dai-ichi Nuclear Power Plant. J Environ Radioact
138:264–275
Bunzl K, Schimmack W (1991) Kinetics of the sorption of 137Cs, 85Sr, 57Co, 65Zn, and 109Cd by the
organic horizons of a forest soil. Radiochim Acta 54:97–102
IAEA (2004) Sediment distribution coefficients and concentration factors for biota in the marine
environment. IAEA technical reports series No.422. IAEA, Vienna
JFA (2014) Results of the monitoring on radioactivity level in fisheries products. http://www.jfa.
maff.go.jp/e/inspection/index.html
Keil RG, Montlucon DB, Prahl FG, Hedges JI (1994) Sorptive preservation of labile organic matter in marine sediments. Nature (Lond) 370:549–552
Kusakabe M, Oikawa S, Takata H, Misonoo J (2013) Spatiotemporal distributions of Fukushimaderived radionuclides in nearby marine surface sediments. Biogeosciences 10:5019–5030.
doi:10.5194/bg-10-5019-2013
Mayer LM (1994) Surface area control of organic carbon accumulation in continental shelf sediments. Geochim Cosmochim Acta 58:1271–1284
Mayer LM (1999) Extent of coverage of mineral surfaces by organic matter in marine sediments.
Geochim Cosmochim Acta 63:207–215
Nakamaru Y, Ishikawa N, Tagami K, Uchida S (2007) Role of soil organic matter in the mobility
of radiocesium in agricultural soils common in Japan. Colloid Surf A 306:111–117.
doi:10.1016/j.colsurfa.2007.01.014
Nakao A, Funakawa S, Takeda A, Tsukada H, Kosaki T (2012) The distribution coefficient for
cesium in different clay fractions in soils developed from granite and Paleozoic shales in Japan.
Soil Sci Plant Nutr 58:397–403. doi:10.1080/00380768.2012.698595
NRA (2014) FY2013 Report of NRA survey for distribution of radioactive nuclides in marine
environment
(in
Japanese)
http://radioactivity.nsr.go.jp/ja/contents/10000/9423/24/
report_20140613.pdf
Ono T, Ambe D, Kaeriyama H, Shigenobu Y, Fujimoto K, Sogame K, Nishiura N, Fujikawa T,
Morita T, Watanabe T (2015) Concentration of radiocesium bonded to organic fraction of sediment off Fukushima, Japan. Geochem J 49. doi: 10.2343/geochemj.2.0351

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Otosaka S, Kato Y (2014) Radiocesium derived from the Fukushima Daiichi Nuclear Power Plant
accident in seabed sediments: initial deposition and inventories. Environ Sci Processes Impacts
16:978–990. doi:10.1039/C4EM00016A
Otosaka S, Kobayashi T (2012) Sedimentation and remobilization of radiocesium in the coastal
area of Ibaraki, 70 km south of the Fukushima Dai-ichi Nuclear Power Plant. Environ Monit
Assess 185:5419–5433. doi:10.1007/s10661-012-2956-7
Wada T, Nemoto Y, Shimamura S, Fujita T, Mizuno T, Sahtome T, Kamiyama K, Morita T, Igarashi
S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ Radioact
124:246–254. doi:10.1016/j.jenvrad.2013.05.008
Yamashiki Y, Onda Y, Smith HG, Blake WH, Wakahara T, Igarashi Y, Matsuura Y, Yoshimura K
(2014) Initial flux of sediment-associated radiocesium to the ocean from the largest river
impacted by Fukushima Daiichi Nuclear Power Plant. Sci Rep 4:3714. doi:10.1038/srep03714

Chapter 6

Bottom Turbidity, Boundary Layer Dynamics,
and Associated Transport of Suspended
Particulate Materials off the Fukushima Coast
Hiroshi Yagi, Kouichi Sugimatsu, Shigeru Kawamata, Akiyoshi Nakayama,
and Toru Udagawa
Abstract Long-term monitoring and intensive field experiments for the bottom
layer off the Fukushima coast were performed from October 2012 to November
2014 to understand the bottom processes, which are closely related to the spatial
distribution and temporal variations of radiocesium in sea sediment. In this section,
focusing on autumn 2012, we examine the bottom processes for a 32-m depth site
(Sta. B) off Iwaki, Fukushima. Observational results showed that the bottom shear
stresses from waves generally dominated over those from currents in this depth
region, and the bottom turbidity increased in high wave conditions. Stepwise and
significant southward cumulative transports of bottom turbidity were observed
when high waves with long periods (LPW) coming from an E–ENE direction were
superimposed on the southward current flow that has a periodicity of 5 days; both
phenomena are influenced by successive passages of low pressure systems and the
associated spatial distribution of atmospheric pressure. The combination of waves
and currents caused by meteorological disturbance is a key process in the transport
of suspended particulate material off the Fukushima coast.
Keywords Turbidity • Bottom boundary layer • Low period waves • Low pressure
system

H. Yagi (*)
Department of Civil and Environmental Engineering, National Defense Academy,
1-10-20, Hashirimizu, Yokosuka, Kanagawa 239-8686, Japan
e-mail: yagih@nda.ac.jp
K. Sugimatsu • S. Kawamata • A. Nakayama • T. Udagawa
National Research Institute of Fisheries Engineering, Fisheries Research Agency,
7620-7, Hasaki, Kamisu, Ibaraki 314-0408, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_6

77

78

H. Yagi et al.

6.1  Introduction
More than 3 years have passed since the accident at the Fukushima Dai-ichi Nuclear
Power Plant (FNPP) associated with the Great Earthquake east of Japan on March
11, 2011. Concentrations of seawater radionuclides are decreasing, but the bottom
sediment still has appreciable levels of radionuclides that could be incorporated in
the benthic ecosystem. Therefore, it is important to understand the details of the
spatial distribution and temporal variations of radionuclide concentrations included
in the bottom sediment. Several studies have investigated the spatial distribution of
radiocesium in the seabed (Otosaka and Kobayashi 2013; Kusakabe et al. 2013;
Thornton et al. 2013; Ambe et al 2014); however, to understand the formation
mechanism of the measured spatial distributions and temporal variations of sea bottom radiocesium, the characteristics of suspended sediment transport in the
Fukushima coastal sea area must be known. These characteristics are closely related
to the movement of sediment and suspended particulate radiocesium. In this section, we introduce the characteristics of bottom turbidity, boundary layer dynamics,
and associated bottom turbidity transport off the Fukushima coast, based on the
field measurement results reported by Yagi et al. (2013).

6.2  O
 utline of Field Measurements for Bottom Processes off
the Fukushima Coast
We performed two kinds of field measurements to understand the bottom processes
off the Fukushima coast: one was the long-term monitoring of coastal bottom environments focusing on basic parameters (current, wave, turbidity, temperature, salinity), and the other was an intensive field survey aimed at understanding the details of
bottom boundary layer dynamics and associated sediment transport processes. For
long-term monitoring, three monitoring sites were deployed off Iwaki, the southern
part of the Fukushima coast (stations B, C, and D at depths of 32, 80, and 130 m,
respectively), and one site (Sta. A at a depth of 30 m) off Ooarai on the Ibaraki coast
(see Fig. 6.1). Bottom-mounted and bottom-moored instrument platforms were
installed with an ADCP (acoustic Doppler current profiler, Telendy RDI), OBS
(optical back-scatter sensor for turbidity, Infinity-CLW, JEF-advantec), and salinity–temperature sensors (Infinity-CTW, JEF-advantec) (Fig. 6.2a); mooring systems
to measure the surface and middle layer conditions (temperature, salinity, and turbidity) were also deployed for stations A and B. Measurements began in mid-October 2012 and continued for 2 years until early November 2014. The intensive survey
focusing on the bottom boundary layer involved the installation of a bottom tripod
(Fig. 6.2b) equipped with a vertical array of OBSs, a 3-D acoustic Doppler velocimeter (ADV-Vector, Nortec), and an in-situ laser particle size analyzer (LISST-100x,
Sequoia Sci) at Sta. B (32 m depth) (Fig. 6.1). Three field campaigns were conducted: BBL-Exp. I (15 October to 20 November 2012), BBL-Exp. II (13 February
to 25 March 2013), and BBL-Exp. III (1 November to 15 December 2013).

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

79

a
45∞ N

FNPP
40∞ N

Sea of Japan

Fukushima
Prefecture

35∞ N

Iwaki

Pacific Ocean
30∞ N
145∞ E

130∞ E 135∞ E 140∞ E

Meteorological
Observatory
(JMA)

Ibaraki
Prefecture

Oarai

Monitoring sites
(Sta. A –D)

Distance (km)

b

0

5

C

20

25

D

50

0

B

15

Bottom moored
type platform
Bottom mounted
type platform

100

Depth (m)

10

150

Mooring system
141∞ 00'

141∞ 10'

Fig. 6.1 (a) Map of study area. Topography and locations of monitoring station A off Oarai of
Ibaraki Prefecture, and stations B, C, and D off Iwaki of Fukushima Prefecture. FNPP marks the
location of the Fukushima Dai-ichi Nuclear Power Plant. (b) On- to offshore topography changes
around the monitoring sites off Iwaki and locations of stations B, C, and D

80

H. Yagi et al.

a

Sta. A (off Oarai)
Sta. B (off Iwaki)

Sta. C, D (off Iwaki)

Surface layer
CTW

Middle
layer

CLW
ADCP300kHz
CLW, CTW

ADCP600kHz
CLW, CTW

Bottom mounted
type platform

1 m above
sea bed

Bottom moored
type platform

Mooring system

b

(Unit: m)

0.8

CLW

0.5

0.15

0.25

Sea bed

0.35

0.5

CLW

0.6

1.0

CLW

LISST
-100X

1.4

ADV
-Vector

Fig. 6.2  Schematics of the monitoring systems. (a) Deployed experimental setup of the instrument platform (bottom-mounted and -moored types) and mooring system at stations A–D. (b)
Bottom tripod for bottom boundary layer experiment and instrumentation layout. CLW shows
OBS (optical back-scatter sensor for turbidity) and CTW shows a salinity-temperature sensor

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

81

Of all the data from these measurements, we focused first on the bottom boundary
layer experiment for the 32-m depth site (Sta. B) and the corresponding long-­term
monitoring in autumn 2011. The fundamental characteristics of bottom processes off
the Fukushima coast for this period are discussed in the following subsections.

6.3  B
 ottom Turbidities and Boundary Layer Characteristics
off the Fukushima Coast in Autumn 2012
Measurement results in autumn 2012 revealed that temporal variations in turbidity
in the inner-shelf and mid-shelf bottom layers off the Fukushima coast have
different characteristics (Fig. 6.3). The bottom turbidities at the inner-shelf site

Tide level (m)

0.8
0.4
0
-0.4
-0.8
-1.2

17-Oct

1-Nov

16-Nov

1-Dec

Boundary layer experiment I
Turbidity (FTU)

30

Sta. B (depth 32 m)

20
10
0
17-Oct

1-Nov

15-Nov

1-Dec

Turbidity (FTU)

Turbidity (FTU)

30

Sta. C (depth 80 m)
20
10
0
17-Oct
30

1-Nov

15-Nov

1-Dec

Sta. D (depth 130 m)

20
10
0
17-Oct

1-Nov

15-Nov

1-Dec

Fig. 6.3  Bottom turbidities at stations B, C, and D with tidal elevations in autumn 2012. The turbidity data are given in FTUs (Formazin turbidity units)

82

H. Yagi et al.

a

Bottom currents Uc
Atmospheric pressure P

Moving average of Uc

1040

1020
0
1000

-0.3
South 16-Oct

21-Oct

26-Oct

31-Oct

5-Nov

10-Nov

15-Nov

980
20-Nov

21-Oct

26-Oct

31-Oct

5-Nov

10-Nov

15-Nov

20-Nov

Pressure P (hPa)

Bottom currents Uc (m/s)

North
0.3

Wave direction θ (deg.)

b
S 180
SE 135
E

90

NE 45
N

Wave height Hs [m]

0.4

4
3

HW3
HW1

Turbidity [FTU]

HW5

HW2

HW6

0.3

2

0.2

1

0.1

0
16-Oct

d

HW4

30

20

21-Oct

26-Oct

31-Oct

5-Nov

10-Nov

15-Nov

0
20-Nov

Wave orbital velocity Uwb [m/s)]

c

0
16-Oct

mab: meters above the sea bed
0.25 mab
0.5 mab
1.0 mab

10

0
16-Oct

21-Oct

26-Oct

31-Oct

5-Nov

10-Nov

15-Nov

20-Nov

Fig. 6.4  Measurement results for the bottom boundary experiment: bottom currents and atmospheric pressure (a), wave direction (b), significant wave heights (Hs, black trace) and wave orbital

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

83

(32-m depth; Sta. B) were generally larger than those at the mid-shelf site (130-m
depth; Sta. D), and Sta. B saw high turbidity conditions over several days. In contrast, turbidity at the mid-shelf site (Sta. D) showed temporal variations with high
frequencies. The intermediate depth site (80-m depth; Sta. C) combined the bottom
turbidity features observed at the inner- and mid-shelf sites.
Focusing on the inner-shelf bottom layer, we examined the details of boundary
layer characteristics (currents, waves, bottom shear stress) and the relationships
with bottom turbidities (Fig. 6.4). The bottom currents (Fig. 6.4a) showed temporal
variations with a period of around 5 days, which were well correlated with low pressure system passages over the study area (shown by the gray hatching in this figure)
associated with temporal variations of local atmospheric pressure. These periodic
and subtidal current fluctuations off the Fukushima coast were also observed by
Kubota et al. (1981) and were thought to be shelf waves in the forcing region caused
by periodic meteorological disturbances (Kubota 1982). In contrast, waves observed
in high wave conditions showed two distinct sets of characteristics. (1) High waves
during low pressure passages had relatively shorter wave periods and an ESE–SSE
wave direction (type 1: corresponding to the high wave periods HW1, HW2, HW4,
and HW6 in Fig. 6.4c, and indicated as type 1 in Fig. 6.5a). (2) High waves occurring in the intervals between low pressure passages had longer wave periods and an
E–ENE wave direction (type 2: corresponding to the high wave periods HW3 and
HW5 in Fig. 6.4c, and indicated as type 2 in Fig. 6.5a). These different characteristics were the result of the different wave generation systems, in that type 1 was
induced by the passage of a low pressure system over the study area (Fig. 6.5b, left
panel) and type 2 developed off the east part of the main island of Japan (Fig. 6.5b,
right panel) and propagated into the study region from an E–ENE direction with
longer periods.
Bottom shear stress from currents and waves (τc and τw) can be evaluated by the
following equations (Soulsby 1997):
2

t c = rU c2



1  z 
 ln    and
 k  z0  

τw = ρ

1
fwU w2 ,
2


(6.1)

(6.2)

where Uc is the current velocity at z (elevation above the sea bed), κ is the von
Karman constant, ρ is the density of seawater, z0 is the bed roughness length, Uw is

Fig. 6.4  (continued) velocities (Uwb, gray trace) (c), and turbidities (d) at 0.25, 0.5, and 1 m above
the seabed. Timing of low pressure passages over the study area, which were defined from local
atmospheric pressure data and synoptic-scale information on atmospheric pressure (weather map)
from the JMA (Japan Meteorological Agency), is shown by the gray hatching in (a) and (b). (c)
HW 1–6 are high wave periods during the observation period. HW1, -2, -4, and -6 occurred during
the low pressure passage; HW3 and -5 in intervals between low pressure passages are shown by
dotted arrows

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H. Yagi et al.

Fig. 6.5 (a) Relationship between wave direction, significant wave heights, and wave periods for
autumn 2012. (b) Weather map by the JMA for two high wave periods: left, high wave period HW2
(type 1); right, high wave period HW5 (type 2). Wave directions are illustrated based on the wave
map by the JMA

the bottom wave orbital velocity, and fw is the bottom friction coefficient caused by
waves (Soulsby 1997). By substituting the measured ADCP velocity at the lowest
layer (z = 2.12  m) for Uc, and RMS wave orbital velocities by the ADV-Vector for
Uw, we can obtain the bottom shear stresses.
The estimated bottom shear stress caused by waves (τw) generally dominated
over that caused by currents (τc) in autumn 2012 and showed larger values in type 2
high wave conditions (HW3 and HW5 in Fig. 6.6a). Furthermore, τw correlates well

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

τw & τc [Pa]

a

4

τw : wave

3

τc : current

2

HW2

85

HW5
HW3
HW6
HW4

HW1
1

0
16-Oct
20
15
10

26-Oct

31-Oct

5-Nov

12

τwc : wave & current
HW5

Turbidity 0.5mab

8
HW1

HW2

HW3

HW4

HW6
4

5
0
16-Oct

10-Nov 15-Nov 20-Nov

τw [Pa]

Turbidity [FTU]

b

21-Oct

21-Oct

26-Oct

31-Oct

5-Nov

0
10-Nov 15-Nov 20-Nov

Fig. 6.6 (a) Temporal variations in estimated bottom shear stresses caused by waves (τw) and currents (τc). (b) Temporal variations in bottom turbidities (0.5 mab) and τw for autumn 2012. HW
1–6 in the figure are as defined for Fig. 6.4c

with the observed turbidities, meaning high turbidity conditions occurred simultaneously with the larger bottom shear stresses (Fig. 6.6b). These observational results
demonstrate that the larger bottom turbidities are induced by the high wave conditions in the intervals between low pressure passages (type 2), which showed longer
wave periods and larger bottom shear stresses.

6.4  N
 ear-Bottom Turbidity Transport off Fukushima Coast
Under the Condition of Successive Low Pressure
Passages
To understand the characteristics of near-bottom turbidity transport off the
Fukushima coast, which are closely related to the movement of suspended sediment
and particulate radiocesium, we evaluated the turbidity transport rates from the estimated vertical distributions of turbidity and velocity in the bottom layer. Measured

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H. Yagi et al.

bottom turbidities at three different depths (0.25, 0.5, and 1 m above the seabed)
were approximated with the exponential function


C ( z ) = C be ⋅ exp [ −α ⋅ z ]

(6.3)



where C(z) is estimated turbidity and z is the distance above the seabed. Cbe (reference bottom turbidity) and α (shape factor) are time-varying parameters decided by
regression analysis of the measured bottom turbidities. Additionally, the vertical
profile of bottom current velocities can be approximated using a well-known logarithmic law of the wall for a sea bottom boundary layer (Soulsby 1997) as follows:
u (z ) =


ln z − ln z 0
uADCP
ln z ADCP − ln z 0

(6.4)


where u(z) is estimated bottom velocity (north–south or east–west component),
uADCP is the velocity of the lowest layer of ADCP (north–south or east–west component), and zADCP is the distance above the seabed for the lowest layer of ADCP
(2.12 m above the seabed). Horizontal turbidity flux is calculated as the product of
Eqs. (6.3) and (6.4) and integrated over the bottom layer to evaluate the bottom
turbidity transport rate qb as follows:
zb



qb = ∫ C ( z ) ⋅ u ( z ) ⋅ dz
0

(6.5)


where zb is the thickness of the bottom layer. defined here as 2 m.
The estimated temporal and vertical distribution of bottom turbidity (Fig. 6.7a)
shows that significant turbidity variation occurred predominantly below 2 m above
the seabed in autumn 2012. The cumulative transport rate qb (Fig. 6.7b) demonstrates that southward transport dominated and occurred stepwise during type 2
high wave periods (HW3 and HW5 in Fig. 6.7b), which have longer wave periods
and larger bottom shear stresses, as shown in Figs. 6.5a and 6.6a. In contrast, as
discussed, the bottom currents represent temporal variations with a periodicity
around 5 days, and southward currents occurred in the intervals between low pressure atmospheric events. As a result, significant southward bottom turbidity transport was induced during high wave periods HW3 and HW5 (Fig. 6.7b), in the
interval between low pressure events when higher bottom turbidities and southward
bottom currents co-occurred. From these observational results, it is revealed that
successive low pressure passages and the associated spatial distributions of atmospheric pressure influenced both the current and wave fields, and that significant
southward bottom turbidity transports were induced by the co-occurrence of high
waves coming from E–ENE with longer periods (favorable for high bottom turbidity) and southward bottom currents in the interval between low pressure passages
(Fig. 6.8). The relationship between waves and currents through atmospheric conditions is an important influence on bottom processes off the Fukushima coast.

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

a
distance above sea bed(m)

FTU

0

10 20 30 40

1.5
1
0.5

North

cumulative bottom turbidity
transport rate ( x 104 FTU • m/s)

b

2

87

4

HW1

HW2

HW3

HW4

HW5

HW6

0
-4
-8
-12

South

Fig. 6.7 (a) Temporal and vertical distribution of turbidity estimated by Eq. (6.3). (b) Temporal
variation of the cumulative value of the bottom turbidity transport rate found by Eq. (6.5) (north–
south direction). HW1–6 in b as defined for Fig. 6.4c

In the bottom boundary layer experiment in autumn 2012, a sediment trap was
also installed at the inner-shelf site (32-m depth, Sta. B) to measure the sinking flux
and radiocesium concentration of suspended particulate material in the bottom layer
(Kaeriyama et al. 2013). The measurement results showed a significant correlation
between bottom turbidities and the sinking fluxes of particulate radiocesium (Yagi
et al. 2014), which fact suggests that sediment or particulate radiocesium movements
are closely related to the transport processes of the bottom turbidity examined here.

6.5  Conclusions
In this section, fundamental characteristics of bottom turbidity, bottom boundary
layer dynamics, and associated bottom turbidity transport off the Fukushima coast
were examined based on field measurement results in autumn 2012, focusing on the
inner-shelf bottom layer (32-m depth, Sta. B). Observational results showed that the
bottom shear stresses from waves generally dominated those caused by currents,
and the bottom turbidity increased in high wave conditions. In particular, significant

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H. Yagi et al.

During low pressure passage

FNPP

Interval between low pressure passages

Northward
currents

LPW (Long period waves)
from E - ENE

FNPP

lower
bottom turbidity
induced
higher
bottom turbidity
induced
Waves from ESE-SSE

Southward
currents
Relatively large southward
sediment transport

High wave Type 1
(Periods: HW1, 2, 4, and 6)

High wave Type 2
(Periods: HW3 and 5)

Fig. 6.8  Schematic illustrations of bottom turbidity transport processes for type 1 and type 2 high
wave events

and stepwise southward cumulative transport of bottom turbidity was observed
when southward currents and high waves coming from an E–ENE direction with
longer periods co-occurred. This combination of bottom current variations with a
periodicity of several days and high wave conditions with longer wave periods
(LPW), both of which are influenced by the successive passage of periodic low
pressure systems and the associated spatial distribution of atmospheric pressure,
affects the transport of suspended particulate material in the bottom layer. The
results of this study highlight the importance of the relationship between atmospheric conditions and trends in waves and currents in understanding the bottom
processes off the Fukushima coast.
Acknowledgments  We appreciate the extensive support from Mr. A. Suzuki, Mr. M. Hosono, and
Mr. M. Kobayashi of International Meteorological & Oceanographic Consultants Co. Ltd, and
from Mr. Y. Nishi of Alpha Hydraulic Engineering Consultants Co., Ltd. This study was financially supported by the Fisheries Research Agency of Japan.
Open Access  This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

6  Bottom Turbidity, Boundary Layer Dynamics, and Associated Transport…

89

References
Ambe D, Kaeriyama H, Shigenobu Y, Fujimono K, Ono T, Sawada H, Saito H, Miki S, Setou T,
Morita T, Watanabe T (2014) A high-resolved spatial distribution of radiocesium in sea sediment derived from Fukushima Dai-ichi nuclear power plant. J Environ Radioact 136:218–228
Kaeriyama H, Ambe D, Ono T, Yagi H, Sugimatsu K, Kawamata S, Udagawa T, Nakayama T,
Watanabe T (2013) Sinking flux of particle radioactive cesium near sea bottom off the coast of
Fukushima prefecture. In: Fall Meeting of the Oceanographic Society of Japan, Sapporo,
Hokkaido, Japan, 17–21 Sept 2013, 316, p. 162 (in Japanese)
Kubota M (1982) Continental shelf waves off the Fukushima coast. Part II: theory of their generation. J Oceanogr Soc Jpn 38:323–330
Kubota M, Nakata K, Nakamura Y (1981) Continental shelf waves off the Fukushima coast. Part
I: observations. J Oceanogr Soc Jpn 37:267–278
Kusakabe M, Oikawa S, Takata H, Misonoo J (2013) Spatiotemporal distributions of Fukushima-­
derived radionuclides in nearby marine surface sediments. Biogeosciences 10:5019–5030
Otosaka S, Kobayashi T (2013) Sedimentation and remobilization of radiocesium in the coastal
area of Ibaraki, 70 km south of the Fukushima Dai-ichi Nuclear Power Plant. Environ Monit
Assess 185(7):5419–5433
Soulsby R (1997) Dynamics of marine sands. Thomas Telford, London, p 249
Thornton B, Ohnishi S, Ura T, Odano N, Fujita T (2013) Continuous measurement of radionuclide
distribution off Fukushima using a towed sea-bed gamma ray spectrometer. Deep-Sea Res I
79:10–19
Yagi H, Sugimatsu K, Nishi Y, Kawamata S, Nakayama A, Udagawa T, Suzuki A (2013) Field
measurements of bottom boundary layer and suspend particle materials on Jyoban coast in
Japan. Journal of Japan Society of Civil Engineers, Ser B2 (Coastal Engineering) 69(2):
1046–1050 (in Japanese)
Yagi H, Sugimatsu K, Kawamata S, Nakayama A, Udagawa T, Kaeriyama H, Ono T, Ambe D
(2014) Estimation of horizontal flux of particulate radiocesium in the bottom layer off Joban
coast. In: Spring Meeting of the Oceanographic Society of Japan, Tokyo, Japan, 26–30 March
2014, 201, p. 59 (in Japanese)

Chapter 7

Investigation of Radiocesium Translation
from Contaminated Sediment to Benthic
Organisms
Yuya Shigenobu, Daisuke Ambe, Hideki Kaeriyama, Tadahiro Sohtome,
Takuji Mizuno, Yuichi Koshiishi, Shintaro Yamasaki, and Tsuneo Ono

Abstract We estimated the radiocesium translation from contaminated sediments
to benthic organisms off the coast of Fukushima. We conducted field investigations
and an experiment with a benthic polychaete (Perinereis aibuhitensis) reared on
highly contaminated sediments collected from a station 1 km off the Fukushima
Dai-ichi Nuclear Power Plant. Results of the field investigations revealed that radiocesium contamination in benthic organisms depended on their feeding habitat. The
radiocesium concentration in carnivore or herbivore feeder polychaetes was higher
than that in deposit feeders. Radiocesium concentrations of all benthic organism
specimens were lower than that in sediments collected from the same sampling
point. Results of the rearing experiment showed that the concentration ratio (CR) of
137
Cs for P. aibuhitensis and contaminated sediments (wet/wet) was less than 0.10.
Moreover, 4 days after separation from the contaminated sediments, the 137Cs concentrations in P. aibuhitensis rapidly decreased. Based on the results of our field
investigations and rearing experiment, we conclude that the intake of radiocesium
through the benthic food web is limited for benthic organisms, despite the high
contamination of the surrounding sediments.

Y. Shigenobu (*) • D. Ambe • H. Kaeriyama • Y. Koshiishi • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: yshig@affrc.go.jp
T. Sohtome • T. Mizuno
Fukushima Prefectural Fisheries Experimental Station,
13-2, Matsushita, Onahama, Iwaki, Fukushima 970-0316, Japan
S. Yamasaki
National Research Institute of Fisheries Engineering, Fisheries Research Agency,
7620-7, Hasaki, Kamisu, Ibaraki 314-0408, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_7

91

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Y. Shigenobu et al.

Keywords Benthic organisms • Contaminated sediment • Rearing experiment •
Concentration ratio (CR)

7.1

Introduction

The Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident in March 2011
released a large amount of anthropogenic radionuclides into the marine environment. Although most of the short-lived radionuclides soon decayed to a level below
the detection limit, two isotopes of radiocesium (134Cs and 137Cs), which have relatively long half-lives (2.07 years and 30.1 years, respectively), have been continually detected in the environment. Tsumune et al. (2012) estimated that
3.5 ± 0.7 × 1015 Bq of 137Cs was released directly into the ocean from 26 March 2011
to the end of May 2011. The discharged radiocesium from the FNPP gradually
associated with suspended material and settled to the sea bottom around Fukushima.
Ambe et al. (2014) reported that the radiocesium concentrations in the surface sediment layer (0–1 cm) collected off the coast of Fukushima in 2012 and 2013 were
mainly in the range of dozens to several hundred Bq/kg-dry (see Sect. 2.1).
Moreover, the particularly highly contaminated (137Cs concentration = 40,152 ± 3,998 Bq/kg-wet) area that is extremely small, encompassing only a
few square meters of the seafloor, was confirmed near the FNPP in February 2013
(Thornton et al. 2013). It is thought that demersal fish and benthic organisms take in
radiocesium from highly contaminated sediments through the benthic food web
(Buesseler 2012; Tateda et al. 2013; Sohtome et al. 2014). High radiocesium concentrations were detected from some sedentary demersal fish species, such as fat
greenling (Hexagrammos otakii), marbled flounder (Pseudopleuronectes yokohamae), slime flounder (Microstomus achne), and Japanese rockfish (Sebastes cheni),
off the coast of Fukushima (Wada et al. 2013).
The radiocesium concentrations in benthic organisms off the coast of Fukushima
range from several to dozens Bq/kg-wet (Sohtome et al. 2014). According to a previous experimental study on the concentration ratio (CR) of 137Cs between contaminated sediments and marine polychaetes (CR = 0.179) (Ueda et al. 1977), this level
of contamination in benthic organisms off the coast of Fukushima is reasonable.
However, the current transfer efficiency of radiocesium from contaminated sediments to the benthic organisms along the sea bottom off the coast of Fukushima is
unclear. In this section, we discuss the results of our measurements of radiocesium
concentrations in benthic organisms caught off the coast of Fukushima in October
2013 and the results of experiments rearing a benthic polychaete (Perinereis aibuhitensis) on highly contaminated sediments collected at the station 1 km off the FNPP
in August 2013 (Fig. 7.1). Through our field investigations and the rearing experiment, we estimated the radiocesium translation from contaminated sediments to
benthic organisms off the coast of Fukushima.

7 Investigation of Radiocesium Translation from Contaminated Sediment to Benthic…

93

Fig. 7.1 Sampling point
(black spot) of benthic
organisms off the coast of
Fukushima in October 2013.
Gray circle indicates a 20-km
radius around the Fukushima
Dai-ichi Nuclear Power Plant

7.2

Radiocesium Concentrations in Benthic
Organisms off the Coast of Fukushima

Benthic organisms in the southern coastal waters of Fukushima were collected using
a dredge on the R/V Taka-maru of the Fisheries Research Institute of Fisheries
Engineering in October 2013 (Fig. 7.1). We sorted benthic organisms into major
taxonomic groups and measured radiocesium concentrations of whole-body specimens, which included digestive system contents (Fig. 7.2). The specimens were
packed tightly in plastic cylindrical containers, and specific gamma rays of 134Cs (605
and 796 keV) and 137Cs (662 keV) were measured with a high-purity germanium
(HPGe) semiconductor detector (ORTEC, GEM30-70-LB-C, 1.85 Kev/1.33 MeV of
resolution) with a multichannel analyzer.
Radiocesium concentrations in all benthic organisms were lower than that in the
sediments (216 Bq/kg-wet) collected from the same sampling point. Radiocesium
concentrations in benthic organisms ranged from not-detected (N.D.) to 99.4 Bq/
kg-wet. Although a low level of radiocesium contamination was detected in crustacean specimens, radiocesium concentrations in polychaete specimens varied among
taxonomic groups (Table 7.1).
The radiocesium concentrations in benthic organisms were typically measured
for whole-body specimens, which contained the contaminated sediments within and

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Y. Shigenobu et al.

Fig. 7.2 Polychaetes collected off the coast of Fukushima in October 2013. We selected several
species of polychaetes from sea sediments (a, b and c). White oval in d indicates the internal sediments in Flabelligeridae specimens

Table 7.1 Radiocesium concentrations in benthic organisms off the coast of Fukushima in
October 2013
Taxonomic group
of benthic organisms
Polychaeta
Glyceridae
Eunicidae
Flabelligeridae
Terebellidae
Opheliidae
Polynoidae
Crustacea
Crangonidae
Paradorippe granulata
Asteroidea
Philyra syndactyla
Luidia quinaria
Asterias amurensis
a

134
Cs + 137Cs
concentrations
(Bq/kg-wet)
N.D. (<2.89)
11.2
99.4
30.2
N.D. (<6.56)
12.1
1.09
4.37
3.58
2.65
N.D. (<2.47)

Concentration ratios
between sea sedimentsa
and benthic organisms
—
0.0519
0.460
0.140
—
0.0560
0.00505
0.0202
0.0166
0.0123
—

Radiocesium concentration of sea sediment at the sampling point was 216 Bq/kg-wet

7 Investigation of Radiocesium Translation from Contaminated Sediment to Benthic…

95

around their body. Ono et al. (in press, 2015) reported that organic matter in marine
sediments had a higher radiocesium concentration than did mineral substances.
Therefore, it is thought that the feeding habitats of benthic organisms influence
radiocesium concentrations within the organisms. In this investigation, we observed
internal sediments in the Flabelligeridae specimens, which had the highest
radiocesium concentration. Species belonging to Flabelligeridae, Terebellidae, and
Opheliidae are categorized as filter feeders or surface deposit feeders (Fauchald and
Jumars 1979). Except for the Opheliidae specimens, radiocesium concentrations in
deposit feeder polychaetes were comparatively higher than in other benthic organisms. In contrast, species with low radiocesium concentration (Glyceridae,
Eunicidae, and Polynoidae) are categorized as carnivore or herbivore feeders. The
reason for low contamination levels in Opheliidae specimens was unclear. Additional
and continuous investigations are required to reveal the relationship between radiocesium contamination and feeding habitats of benthic organisms off the coast of
Fukushima.

7.3

Rearing Experiments of the Marine Polychaete
(Perinereis aibuhitensis) Using Highly Contaminated
Sediment from Near the FNPP

Contaminated sediments from near the FNPP (37°24.850′N–141°02.330′E) were
collected using a Smith-Mclntyre grab sampler on the R/V Takusui of the Fukushima
Prefectural Fisheries Experimental Station in August 2013. After removing impurity particles using a 2-mm sieve, we agitated the contaminated sediment for equalization. Before initiating the rearing experiments, we confirmed noncontamination
of the marine polychaete (Perinereis aibuhitensis) specimens with an HPGe semiconductor detector. The specimens of P. aibuhitensis were reared for 5 weeks in four
tanks (450 mm × 300 mm × 330 mm) with the contaminated sediments, and then P.
aibuhitensis were reared for 2 weeks without sediments (seawater only). The 137Cs
concentrations of living P. aibuhitensis in plastic cylindrical containers were measured with an HPGe semiconductor detector, and then the specimens were returned
to the rearing tank. The sediment samples were dried at 60 °C for 7 days, and the
dry weight was converted into wet weight concentrations using the percentage of
lost water content. Because organic matter in contaminated sediments has a high
preference for radiocesium (Ono et al. in press, 2015), an ignition loss test was
employed to determine the sediment content in each of the four tanks. The sediment
samples were heated in a muffle furnace at 750 °C for 1 h.
Figure 7.3 shows the time-series trends of 137Cs concentrations for contaminated
sediments and P. aibuhitensis in each tank. At the start of the rearing experiment, the
137
Cs concentration in the contaminated sediments was 1,250 Bq/kg-wet. However,
137
Cs concentrations in the contaminated sediments fluctuated with time. During the
rearing period with contaminated sediments, the geometric mean of 137Cs concentration for sediments in tank 1, tank 2, tank 3, and tank 4 were 1,500 Bq/kg-wet,

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Y. Shigenobu et al.

Fig. 7.3 Temporal trends of 137Cs concentrations in Perinereis aibuhitensis and sediments
Table 7.2 Temporal trend of organic matter contents (%) in sediments for each rearing tank
Tank
Rearing tank-①
Rearing tank-②
Rearing tank-③
Rearing tank-④

Initial value 5.9

Days after the start of rearing experiment
7 days
14 days
21 days
28 days
5.1
5.1
4.9
4.5
4.2
4.8
4.7
4.6
5.3
5.4
5.8
4.4
4.9
4.7
5.5
4.4

35 days
5.1
4.5
4.3
4.9

1,250 Bq/kg-wet, 1,210 Bq/kg-we,t and 1,180 Bq/kg-wet, respectively. Insufficient
agitation of the initial contaminated sediments and the burrowing activity of P.
aibuhitensis could have caused the variation of 137Cs concentration among the tanks.
In contrast, the organic matter content in the contaminated sediments for each tank
was approximately equal during the rearing period (Table 7.2).
The 137Cs concentrations of P. aibuhitensis reached the maximum value after
approximately 2 weeks, and conspicuous fluctuations were not observed during the
next 3 weeks. On the 35th day after the start of the experiment, the CR for 137Cs
between P. aibuhitensis and sediments (wet/wet) was less than 0.10 (tank 1 = 0.087,
tank 2 = 0.056, tank 3 = 0.057, tank 4 = 0.060). Meanwhile, the 137Cs concentrations
in P. aibuhitensis varied among the tanks. On the 14th day after the start of the
experiment, the 137Cs concentrations in tank 1, tank 2, tank 3, and tank 4 were
116 Bq/kg-wet, 72.5 Bq/kg-wet, 45.1 Bq/kg-wet, and 56.8 Bq/kg-wet, respectively.
Four days after separation from the contaminated sediments, the 137Cs concentration

7 Investigation of Radiocesium Translation from Contaminated Sediment to Benthic…

97

in P. aibuhitensis rapidly decreased, to 23–34 % of the concentration on the 35th
day. The 137Cs concentration in P. aibuhitensis eventually decreased to less than
20 Bq/kg-wet in all tanks. These results suggest that the 137Cs concentrations in P.
aibuhitensis are associated with the sediment contamination level in each tank. We
assumed that the observed radiocesium concentration in P. aibuhitensis include
measurements of contaminated sediments in their digestive systems.
Our rearing experiments determined that the CR for radiocesium between P.
aibuhitensis and contaminated sediments (wet/wet) was less than 0.10. Otosaka and
Kobayashi (2013) calculated that the amount of bioavailable 137Cs in the surface
sediment layer (0–3 cm) off the coast of Ibaraki Prefecture (approximately 70 km
south of the FNPP) was only about 20 % of the total sedimentary 137Cs because
more than 75 % of the 137Cs was incorporated into lithogenic fractions that were not
bioavailable to marine products. Therefore, most of the sedimentary radiocesium in
the digestive system of benthic organisms would be excreted with their wastes.
Moreover, the ability of osmoconformation in invertebrates would influence the
rapid excretion of internally absorbed radiocesium. The results of our study indicate
that the intake of radiocesium through the benthic food web is limited for benthic
organisms and demersal fish species, despite high contamination of the surrounding
sediments.
Acknowledgments We are grateful to Satoshi Igarashi for the sorting of benthic organisms. We
also thank Takami Morita and Ken Fujimoto for their valuable discussions and information. We
appreciate the captains and crews of the R/V Takusui and Taka-maru for sampling contaminated
sediments and benthic organisms.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
Ambe D, Kaeriyama H, Shigenobu Y, Fujimoto K, Ono T, Sawada H, Saito H, Miki S, Setou T,
Morita T, Watanabe T (2014) Five-minute resolved spatial distribution of radiocesium in sea
sediment derived from the Fukushima Dai-ichi Nuclear Power Plant. J Environ Radioact
138:264–275
Buesseler KO (2012) Fishing for answers off Fukushima. Science 338:480–482
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S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ Radioact
124:246–254

Part III

Marine Fish

Chapter 8

Detection of 131I, 134Cs, and 137Cs Released into
the Atmosphere from FNPP in Small
Epipelagic Fishes, Japanese Sardine
and Japanese Anchovy, off the Kanto
Area, Japan
Takami Morita, Kaori Takagi, Ken Fujimoto, Daisuke Ambe,
Hideki Kaeriyama, Yuya Shigenobu, Shizuho Miki, Tsuneo Ono,
and Tomowo Watanabe

Abstract The artificial radionuclides 131I, 134Cs, and 137Cs released from FNPP
were detected in Japanese sardine (Sadinopes melanostictus) and Japanese anchovy
(Engraulis japonicus) off the Kanto area of Japan. In the research period from 24
March 2011 to 13 July 2011, the maximum concentrations of 131I, 134Cs, and 137Cs
were detected in the internal organs of Japanese anchovy collected on 24 March
2011. The concentration of 131I in the internal organs tended to be higher than that
in muscle and the whole body, although no clear tendency was observed for 134Cs
and 137Cs; it was thought that that was caused by 131I of the planktonic contents in
the internal organs. These radionuclides detected in sardine and anchovy would be
derived through the atmospheric pathway from FNPP to off the Kanto area, because
these radionuclides were detected before the direct release of contaminated water
into the ocean from FNPP.
Keywords Radioiodine • Diocesium • Epipelagic fish • Atmosphere

T. Morita (*) • K. Fujimoto • D. Ambe • H. Kaeriyama
Y. Shigenobu • S. Miki • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: takam@affrc.go.jp
K. Takagi
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_8

101

102

8.1

T. Morita et al.

Introduction

Large amounts of artificial radionuclides such as 131I, 134Cs, and 137Cs, were released
into the environment by the Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident, which was caused by the Great East Japan Earthquake and tsunami on 11
March 2011. Tokyo Electric Power Company (TEPCO) estimated that 4.7 × 1015 Bq
of radioactive materials including 131I, 134Cs, and 137Cs were released directly into
the ocean from the FNPP Unit 2 reactor during April 1–6 in 2011 (Nuclear
Emergency Response Headquarters 2011), although it was reported that the direct
release to the ocean had already occurred on 26 March 2011, and showed the estimation that the total amount of 137Cs directly released was 3.5 ± 0.7 × 1015 Bq from
March 26 to the end of May 2011 (Tsumune et al. 2012). The total quantity of 131I
and 137Cs released into the atmosphere between 12 March 2011 and 1 May 2011 was
estimated to be approximately 2.0 × 1017 Bq and 1.3 × 1016 Bq, respectively.
Furthermore, the quantities of 131I and 137Cs deposited on the ocean surface from the
atmosphere were estimated as 9.9 × 1016 Bq and 7.6 × 1015 Bq, respectively
(Kobayashi et al. 2013).
Monitoring research detected 131I, 134Cs, and 137Cs in marine organisms (Fisheries
Agency 2014). The source of the 131I and 134Cs detected in marine organisms clearly
originated from FNPP because of the short physical half-lives, 8.02 days for 131I and
about 2.06 years for 134Cs. However, it has been unclear whether the radionuclides
were released into the atmosphere or directly into the ocean from FNPP. In this
report, we focus on the detection of 131I, 134Cs, and 137Cs in small epipelagic fishes,
sardine and anchovy, off the Kanto area of Japan. Our results indicate that the 131I,
134
Cs, and 137Cs detected in small epipelagic fishes was released into the atmosphere
from FNPP.

8.2

Experimental Procedure

Fish samples were commercially collected from 24 March 2011 to 13 July 2011 at
regions shown in Fig. 8.1. An individual fish sample contain only small amounts of
131 134
I, Cs, and 137Cs, so to determine the concentrations we used multiple fish samples for each measurement specimen. Therefore, we prepared the specimen for
measurement consisting of muscle, internal organs, and whole body from multiple
samples, a total of 5–10 kg individuals. The previous report showed 134Cs and 137Cs
concentrations in most of the fish samples obtained from raw measurement specimens (Takagi et al. 2014). In this report, those samples were re-measured after ashing. On the other hand, 131I concentrations were obtained from the measurement
using a raw measurement specimen. For preparation of the ashed measurement
specimen, raw samples were dried in an oven at 105 °C for 72–120 h, carbonized in
a gas furnace at 350–400 °C for approximately 6 h, and ashed in an electric furnace
at 450 °C for 48–72 h. The ashed samples were ground to a fine powder, transferred
to a plastic cup, and pressed using a hand press. The concentrations of 131I, 134Cs,
and 137Cs were measured using a high-purity germanium (HpGe) semiconductor

8

Detection of 131I, 134Cs, and 137Cs Released into the Atmosphere from FNPP…

103

Fig. 8.1 Location of the Fukushima Dai-ichi Nuclear Power Plant (FNPP) and sampling regions
(A and B). Respective sampling regions are surrounded by dashed lines indicating shorelines

detector with a multichannel analyzer (Seiko EG & G; ORTEC, Oak Ridge, TN,
USA). This HpGe semiconductor detector has a resolution of 1.44 keV at a peak of
662.15 keV (137Cs). The counting efficiency of the Ge semiconductor detector was
calibrated using volume standard sources (MX033U8PP; Japan Radioisotope
Association, Tokyo, Japan). Coincidence summing effects of 134Cs were corrected
with 134Cs standard solutions (CZ005; Japan Radioisotope Association, Tokyo,
Japan). The counting times were about 7,200 s for the raw specimen and from about
3,000 s to about 7,200 s for ashed specimens. All radionuclide concentrations were
corrected for decay from the respective sampling date. The concentration of three
standard deviations (σ) from counting error was defined as the detection limit.

8.3

Concentrations of 131I, 134Cs, and 137Cs in Sardine
and Anchovy

There was no difference in the 134Cs/137Cs concentration ratio between sardine and
anchovy and among the respective measurement specimens. Considering that the
half-life for 134Cs is 2.1 years, the 134Cs/137Cs concentration ratio in these small

104

T. Morita et al.

Fig. 8.2 Relationship between 134Cs/137Cs concentration ratio and concentration of 137Cs detected
in this study. The 134Cs/137Cs concentration ratio was calculated from the data decay corrected on
11 March 2011

epipelagic fishes was close to 1.0 (Fig. 8.2, Table 8.1). This ratio is consistent with
the 134Cs/137Cs concentration ratio already reported in seawater and marine organisms (Aoyama et al. 2012; Wada et al. 2013). The ratio indicated that the 134Cs and
most of the 137Cs detected in these small epipelagic fishes originated from the FNPP
accident. The concentration of 137Cs in muscle and whole bodies without internal
organs of sardines collected off the Kanto area in 2010, before the FNPP accident,
was 0.052 ± 0.0038 Bq/kg-wet and 0.030 ± 0.0044 Bq/kg-wet, respectively (Fisheries
Research Agency 2012).
The previous report showed the summed concentration of 134Cs and 137Cs in raw
measurement specimens for muscle of sardine and anchovy (Takagi et al. 2014).
These concentrations were 61.0 % to 155.9 % of the sum concentration of 134Cs and
137
Cs in the ashed measurement specimen consisting of the same samples as the raw
measurement specimen. Figure 8.3 shows the temporal variation of 131I and 137Cs
concentrations in the internal organs of sardine and anchovy. The maximum concentrations of 131I, 134Cs, and 137Cs were 309.08 ± 2.06 Bq/kg-wet, 61.01 ± 0.52 Bq/
kg-wet, and 59.63 ± 0.39 Bq/kg-wet, respectively, in the internal organs of anchovy
collected 24 March 2011 (Fig. 8.3, Table 8.1). There was no detection of 131I on 26
April 2011 because of the short physical half-life, 8.02 days. The concentrations of
131
I in the internal organs of sardine and anchovy until 26 April 2011 decreased to
half by 4.4 and 4.6 days, respectively.
The respective concentrations in fishes collected in region B were obviously
lower than those in region A. It was clear that the reason was the distance from
FNPP to each sampling region. The concentration of 131I in the internal organs
tended to be higher than those in other measurement specimens, although no clear
tendency was observed for 134Cs and 137Cs (Table 8.1). Although the concentration
factor of iodine in fish is from 9 to 10, the factor of iodine in phytoplankton and
zooplankton is from 800 to 1,000 (IAEA 2004). The measurement specimen from
the internal organs of sardine and anchovy, which are plankton feeders, could
include some plankton. Therefore, the higher concentrations of 131I would be
detected in the internal organ specimens from sardine and anchovy.

Sampling
Region Date
Sardine
A
2011/3/28
A
2011/4/6
A
2011/4/11
A
2011/4/13
A
2011/4/25
A
2011/4/26
A
2011/5/5
A
2011/5/9
A
2011/5/16
A
2011/5/20
A
2011/5/25
A
2011/6/2
A
2011/6/4
A
2011/6/22
A
2011/6/29
B
2011/4/11
B
2011/6/6
Japanese anchovy
A
2011/3/24
A
2011/4/7
A
2011/4/14
A
2011/4/18

309.08 ± 2.06
12.05 ± 0.40
3.61 ± 0.39
1.75 ± 0.09

13.22 ± 0.20
6.73 ± 0.29
1.78 ± 0.30
0.86 ± 0.25
<0.79
<0.69
<0.60
<0.64
<0.61
2.19 ± 0.48
1.16 ± 0.25
<0.85
<0.77
2.39 ± 0.33
<0.58

84.06 ± 1.55a

131

Internal organs
I

59.63 ± 0.39
8.72 ± 0.13
5.95 ± 0.08

61.01 ± 0.52
8.80 ± 0.18

6.22 ± 0.11

1.52 ± 0.04
2.11 ± 0.06
1.12 ± 0.05
44.78 ± 0.20
8.14 ± 0.12
12.57 ± 0.12
12.01 ± 0.13
1.07 ± 0.03
2.07 ± 0.05

<0.79
<0.69
1.66 ± 0.05
2.25 ± 0.07
1.33 ± 0.07
50.20 ± 0.28
8.64 ± 0.16
13.37 ± 0.15
12.92 ± 0.17
1.15 ± 0.05
2.29 ± 0.07

Cs

13.34 ± 0.09
6.53 ± 0.08
3.58 ± 0.07
3.23 ± 0.07
2.12 ± 0.05

134

13.75 ± 0.12
6.96 ± 0.11
3.69 ± 0.09
3.43 ± 0.09
2.28 ± 0.07

Cs

137

14.30 ± 0.35
2.20 ± 0.35
<0.67
<0.54

7.90 ± 0.42
5.77 ± 0.35
2.00 ± 0.22
0.99 ± 0.17
<0.75
0.74 ± 0.21
<0.53
<0.52
<0.56
<0.56
<0.60
<0.72
<0.68
<0.63
<0.81
<0.57
<0.65

Muscle
I

131

Table 8.1 Concentrations of 131I, 134Cs and 137Cs in sardine and Japanese anchovy
Cs

4.01 ± 0.05

3.77 ± 0.04

2.34 ± 0.03

11.80 ± 0.07
3.84 ± 0.05
12.64 ± 0.08
13.22 ± 0.08
0.86 ± 0.02

12.86 ± 0.10
4.25 ± 0.06
13.42 ± 0.10
13.78 ± 0.10
0.94 ± 0.02

2.38 ± 0.04

3.64 ± 0.03
5.67 ± 0.06

2.88 ± 0.04
3.37 ± 0.04
3.32 ± 0.04
3.29 ± 0.04
3.99 ± 0.04

Cs

134

3.91 ± 0.04
5.70 ± 0.08

3.04 ± 0.05
3.55 ± 0.05
3.36 ± 0.06
3.41 ± 0.06
4.28 ± 0.06

137

2.34 ± 0.28
1.20 ± 0.16

117.46 ± 1.27

24.47 ± 0.77
3.50 ± 0.16
6.20 ± 0.28
3.25 ± 0.23
<0.73
0.57 ± 0.15
<0.59
<0.56
<0.59
<0.54
<0.61
<0.82
<0.59
<0.61
<0.70
0.89 ± 0.24
<0.62

Whole body
I

131

Cs

Cs

2.74 ± 0.05
(continued)

12.96 ± 0.08
0.85 ± 0.02
1.13 ± 0.02

13.76 ± 0.11
0.92 ± 0.03
1.26 ± 0.03

2.95 ± 0.07

3.00 ± 0.06
3.83 ± 0.03
2.88 ± 0.03
11.12 ± 0.08
4.04 ± 0.05

3.93 ± 0.07
2.88 ± 0.05
5.10 ± 0.06
2.62 ± 0.04
3.13 ± 0.04

134

3.23 ± 0.09
3.88 ± 0.04
3.15 ± 0.05
12.09 ± 0.11
4.44 ± 0.07

3.96 ± 0.09
2.90 ± 0.06
5.24 ± 0.08
2.75 ± 0.06
3.39 ± 0.06

137

Internal organs
Sampling
131
Region Date
I
A
2011/4/26
2.42 ± 0.38
A
2011/5/12
<0.72
A
2011/5/18
<0.65
A
2011/5/26
<0.58
A
2011/5/26
<0.68
A
2011/7/13
<0.57
B
2011/3/16
18.56 ± 0.60
B
2011/3/29
13.65 ± 0.70
B
2011/6/6
<0.77
a
Value shows 1 σ counting error

Table 8.1 (continued)

13.31 ± 0.20
8.29 ± 0.11
8.92 ± 0.11
8.51 ± 0.12
3.49 ± 0.05
2.37 ± 0.16
3.25 ± 0.08
2.34 ± 0.13

Cs

137

Cs

13.16 ± 0.15
7.60 ± 0.08
8.59 ± 0.08
7.79 ± 0.08
3.06 ± 0.04
2.37 ± 0.12
3.23 ± 0.06
2.11 ± 0.11

134

<0.67
<0.59
<0.70
2.62 ± 0.13
1.46 ± 0.35
<0.50

Muscle
I
<0.51
<0.79
131

16.54 ± 0.06
12.82 ± 0.05
10.06 ± 0.04
6.52 ± 0.04
1.00 ± 0.04
1.35 ± 0.02
5.38 ± 0.07

7.18 ± 0.05
1.07 ± 0.05
1.39 ± 0.03
5.87 ± 0.09

Cs

134

16.96 ± 0.08
13.61 ± 0.07
10.84 ± 0.06

Cs

137

Whole body
I
1.10 ± 0.17
<0.75
<0.61
<0.55
<0.69
<0.57
4.88 ± 0.22
4.82 ± 0.34
131

Cs

7.88 ± 0.07
6.93 ± 0.07
5.31 ± 0.06
0.40 ± 0.04
1.56 ± 0.05

137

Cs

7.34 ± 0.05
6.34 ± 0.05
4.77 ± 0.05
0.37 ± 0.03
1.52 ± 0.04

134

8

Detection of 131I, 134Cs, and 137Cs Released into the Atmosphere from FNPP…

107

Fig. 8.3 Temporal variation in the concentration of 131I (a) and 137Cs (b) in internal organs of sardine and anchovy. Circles and square symbols indicate data for sardine and anchovy, respectively.
Open and closed symbols indicate data for samples collected in regions A and B, respectively.
Error bar shows 1 σ value derived from counting statistics. Errors for many of the data are too
small to show an error bar

8.4

Detection of 131I, 134Cs, and 137Cs Released into
the Atmosphere from FNPP

The 137Cs concentration in sardine gradually decreased until the end of May in 2011,
but the concentration suddenly increased in the first week of June in 2011 (Fig. 8.3b,
Table 8.1). It was considered that this sudden increase was caused by the disappearance on 30 May 2011 of a warm water eddy, the center of which was located off
Iwaki between Onahama and Hasaki from the middle of May (Takagi et al. 2014;
Fig. 9.4 in Chap. 9). The warm water eddy prevented the seawater, including 131I,
134
Cs, and 137Cs, from moving southward to sampling region A (Aoyama et al. 2012).
In this time, 131I was again detected in the internal organs of sardine, although there
had come to be no detection of 131I on 26 April 2011. This detection of 131I also could
indicate the southward movement of contaminated seawater.

108

T. Morita et al.

134

Cs and 137Cs were detected in sardine and anchovy collected in sampling
region A before the southward movement of contaminated seawater. According to
the previous report, the reason for these detections was considered to be that the
contaminated sardine and anchovy migrated southward to the region earlier than the
southward movement of contaminated seawater (Takagi et al. 2014). It is well
known that the radioactively contaminated fishes are able to migrate from a contaminated area to a noncontaminated area. Radionuclides were transported from
Russia to Japan by walleye pollock and from Japan to the United States of America
by Pacific bluefin tuna (Morita et al. 2007; Madigan et al. 2012). However, in the
large amount of 131I, 134Cs, and 137Cs deposited on the ocean surface off the Kanto
area (Kobayashi et al. 2013), it would be difficult to distinguish between directly
released and atmospheric pathway radionuclides.
The 131I/137Cs concentration ratio in the internal organs of sardine and anchovy
that were collected during from 16 March 2011 to 29 March 2011 in regions A and
B was from 4.2 to 7.8. The 131I/137Cs concentration ratio of the radionuclides that
were released directly from FNPP to 30 km offshore from 26 March to 6 April 2011
agreed with the radioactive decay curve of 131I (Tsumune et al. 2012). However, it
was unclear whether this agreement applied to the region A. In addition, the 131I/137Cs
concentration ratio shows variations during atmospheric transport (Kinoshita et al.
2011) because of differences in the wet deposition rate depending on the size of
particles (Hirose et al. 1993), whereas the simulation estimated that the 131I/137Cs
ratio deposited in the ocean during 22 March 2011 to 24 March 2011 around region
A was 6.7–40.4 (T. Kobayashi, personal communication). Therefore, it was also
difficult to determine the route (as direct release or via the atmospheric pathway) of
these radionuclides by the 131I/137Cs concentration ratio because of the range variation in the estimated ratio and the difference in incorporation rate into the internal
organs between 131I and 137Cs. On the other hand, it was estimated that the direct
release of the contaminated water from FNPP into the ocean occurred from 26
March 2011 (Tsumune et al. 2012). We detected 134Cs and 137Cs in Japanese anchovy
collected on 24 March 2011 in region A and on 16 March 2011 in region
B. Consequently, it was clear that these radionuclides were released into the atmosphere from FNPP; these would deposit on the surface water in this region through
the atmospheric pathway. In addition, we also detected 134Cs and 137Cs in sardines
collected on 28 March 2011 in region A and in both sardine and anchovy collected
on 29 March 2011 in region B. Considering the distance between the FNPP and
these sampling regions, these radionuclides were clearly released into the atmosphere from FNPP.
Acknowledgments We thank Dr. Takuya Kobayashi of the Japan Atomic Energy Agency (JAEA)
for helpful discussion. We appreciate the great help from the staff members of the radioecology
group, research center for fisheries oceanography and marine ecosystem, National Research
Institute of Fisheries Science. This study was supported financially by the Fisheries Agency of
Japan.

8

Detection of 131I, 134Cs, and 137Cs Released into the Atmosphere from FNPP…

109

Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Nakata K, Morita T (2014) Radiocesium concentration of small epipelagic fishes (sardine and
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Chapter 9

Radiocesium Concentration of Small
Epipelagic Fishes (Sardine and Japanese
Anchovy) off the Kashima-Boso Area
Kaori Takagi, Ken Fujimoto, Tomowo Watanabe, Hideki Kaeriyama,
Yuya Shigenobu, Shizuho Miki, Tsuneo Ono, Kenji Morinaga,
Kaoru Nakata, and Takami Morita

Abstract After the Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident,
which occurred in March of 2011, the National Research Institute of Fisheries
Science (NRIFS) undertook emergent radioactivity monitoring of 63 samples of
small epipelagic fishes (such as sardine and Japanese anchovy) collected by commercial fishery boats off the Kashima-Boso area (located to the south of the
Fukushima coast) from 24 March 2011 to 21 March 2013. Fluctuations in the radiocesium concentration in fish muscles synchronized with the decreasing concentration from seawater near the fishing ground; the radiocesium concentration in fish
muscles reached a maximum of 31 Bq/kg-wet in July 2011, after which it declined
gradually. From 2012 to 2013, the radiocesium concentrations in fish muscles were
low (0.58–0.63 Bq/kg-wet). Compared to the 137Cs concentration before the FNPP
accident, 137Cs concentration in fish muscles in 2013 was still about 10 times higher,
whereas it was about 4.5 times higher in seawater near the fishing ground in 2012.

K. Takagi (*)
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
K. Fujimoto • H. Kaeriyama • Y. Shigenobu
S. Miki • T. Ono • K. Morinaga • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: takam@affrc.go.jp
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
K. Nakata
Fisheries Research Agency Headquarters,
2-3-3, Minatomirai, Nishi, Yokohama, Kanagawa 220-6115, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_9

111

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K. Takagi et al.

Keywords Japanese anchovy • Off the Kashima-Boso area • Pacific Ocean •
Radiocesium • Sardine • Seawater

9.1

Introduction

Artificial radionuclides were released into the environment as a result of the Tokyo
Electric Power Company (TEPCO) Fukushima Dai-ichi Nuclear Power Plant (FNPP)
accident that occurred in March of 2011. TEPCO (2012) has estimated that radiocesium (134Cs and 137Cs) at approximately 10 PBq for both 134Cs and 137Cs was released
into the atmosphere in March 2011. In addition, it was estimated that 134Cs was
released into the atmosphere and the ocean from the port of the nuclear power plant
from March to September 2011 at a level of 3.5 PBq and that the level of 137Cs was
3.6 PBq. Some of the released radiocesium was taken into the bodies of marine
organisms through the surrounding water and their prey, and an investigation into
radioactive substances in marine products, conducted by Fisheries Agency (FA),
showed that a relatively high radiocesium concentration (compared to the concentration before the FNPP accident) was detected in some of the fish of the northwest
Pacific Ocean (Fisheries Agency 2012, 2013). These results indicate that there is a
possibility of long-term residual radiocesium in organisms with strong regional characteristics, including bottom fish (Buesseler 2012). The mechanisms of radioactive
substance migration in marine ecosystems need to be understood (Yoshida and
Kanda 2012), but this would entail an analysis of the radioactive substance transfer
mechanism corresponding to ecological characteristics related to each component of
the marine ecosystem. The National Research Institute of Fisheries Science (NRIFS),
Fisheries Research Agency (FRA) cooperated with the radioactive substance investigation and conducted an intensive survey of marine products caught in the Kanto
region for approximately 6 months immediately after the FNPP accident.
Some of the species of fish that were present during the high fishing season off the
Pacific Ocean coast after the FNPP accident included small migratory epipelagic fishes,
namely, sardine (Sardinops melanostictus) and Japanese anchovy (Engraulis japonicus). Sardine and Japanese anchovy actively eat plankton, and they are preyed upon by
whales and large fishes, which gives them an important ecological niche in the Pacific
Ocean coastal areas of the Tohoku region. Each year, from winter/spring to summer,
sardine and Japanese anchovy migrate to Kashima-Boso, temporarily remaining in the
area to create a fishing ground, and they are fished in large- to medium-scale roundhaul fisheries (Uchiyama 1998; Yasumi 2008; Kubota 2012). Thus, this chapter contains an analysis of fluctuations in the radiocesium concentration of these small
epipelagic fishes caught in the fishing grounds off the Kashima-Boso area.

9.2

Collection of Fish and Radioactivity Measurement

NRIFS prepared 63 specimens for radioactivity measurement for each fish species
for each sampling date for adult sardine and Japanese anchovy caught mainly in a
large- to medium-scale round-haul fishery off the Kashima-Boso area (Fig. 9.1)

Radiocesium Concentration of Small Epipelagic Fishes (Sardine and Japanese…

Fig. 9.1 Locations of the
Fukushima Dai-ichi Nuclear
Power Plant (FNPP), and
fishing grounds of fish
sampled (sardine and
Japanese anchovy) in this
chapter (shaded area)

113
37

a

m
ha

50

a

On

FNPP

40

hi
ac
Hit aka
-n

30
130

140

150

Latitude (°N)

9

hi

os

Ch

Fishing ground

Pacific Ocean
35
140

142
Longitude (°E)

from 24 March to 3 November 2011; 27 June and 20 August 2012; and 18 February
2013. Muscles were chosen as the measurement sample for this study. For small
epipelagic fishes collected in 2011, 60 raw specimens were prepared, and for small
epipelagic fishes collected in 2012 and 2013, 3 ashed specimens were prepared,
assuming that the radiocesium concentration would be quite low.
To measure radiocesium concentrations, a germanium semiconductor detector
(EG ORTEC Solid-State Photon Detector) and a pulse-height analyzer (SEIKO EG
MCA 7600 Multichannel Analyzer) were used. The resolution of the germanium
semiconductor detector [full width at half-maximum (FWHM)] was 1.80 keV (60Co,
1,333 keV), and the relative efficiency was 33.0 %. The standard source was the
quasi-gamma-ray volume source standard MX033SPS prepared by Japan
Radioisotope Association (a special order was placed to obtain source heights of 5,
10, 20, 30, and 50 mm), and the MX033U8PP type prepared by the Association.
Nuclides that were objects of measurement were 134Cs (605, 796 keV; without summing the effect correction) and 137Cs (662 keV). For calculation of the targeted
nuclide concentrations, we followed the directive ‘The gamma-ray spectrometry by
germanium semiconductor detector’ (Ministry of Education, Culture, Sports,
Science and Technology 1992), and we calculated using the Covell method. Sixty
specimens of epipelagic fishes collected in 2011 were used as raw samples for
7,200-s measurements, and three specimens of epipelagic fishes collected in 2012
and 2013 were ashed under the assumption that the radiocesium concentration is

K. Takagi et al.

114

quite low; they were analyzed by carrying out 40,000-s measurements or longer.
Radiocesium data (both 134Cs and 137Cs) were obtained by making attenuation corrections to the sample of small epipelagic fishes for the sampling date.

9.3

Tracking the 2010 Year-Class Fish

We first introduce the distribution ecology based on the fluctuation in catch
volumes for both sardine and Japanese anchovy. From March to August 2011,
the sardine haul was more than that of Japanese anchovy, and the sardine haul
in Chiba Prefecture during this period (66,000 tons) was twice that of Japanese
anchovy (33,000 tons) (National Research Institute of Fisheries Science 2011).
As for which sardine haul is relatively larger, the main target of the round-haul
fishery is the southward migrating group of sardine during winter and spring,
but during summer, the target changes to the northward migrating group composed of age 2 fish and older as usual (Fisheries Agency and Fisheries Research
Agency 2011). However, in the fishing season of 2011, the 2010 year-class had
the highest amount of recruitment to the sardine stock since 2002 (Kawabata
et al. 2012). Furthermore, during the fishing seasons from winter/spring to the
summer of 2011, the 2010 year-class was widespread in the Boso area. Thus,
only a small number of age 2 fish and older (which are older than the 2010 year
class) were mixed among the catch (Fisheries Agency and Fisheries Research
Agency 2011).
Before preparing the radioactivity measurement samples, ten specimens were
randomly selected, and the standard length (SL, mm) was measured to calculate
the average length of each sample. The average values of SL of small epipelagic
fish samples were 132–200 and 99–124 mm for sardine and Japanese anchovy,
respectively (Fig. 9.2). The average length of fishes used as samples generally
matched the mode of length composition of the catch in the Joban-Boso area from
March to August 2011 (National Research Institute of Fisheries Science 2011).
Thus, it was determined that both the sardine and Japanese anchovy used for this
study were the results of continuously tracking the temporal fluctuations in radiocesium concentration of age 1 fish (the 2010 year-class) in the surveyed area in
the ocean. It was also determined from the average length of the sample that we
tracked the 2010 year-class until August 2012, and the February 2013 sample was
the result of tracking age 1 fish from the 2012 year-class. Whitebait (Japanese
anchovy) of coastal areas off Fukushima Prefecture is known as an example of the
turnover of fish schools affecting the fluctuations of radiocesium concentration in
fish (Wada et al. 2013), but it was considered to be fluctuation of radiocesium
concentration in the 2010 year-class sardine that was tracked during 2011 in this
chapter. Subsequently, the main catch for Japanese anchovy during April to June
was age 1 fish (the 2010 year-class) (Fisheries Agency and Fisheries Research
Agency 2011), similar to sardine.

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Radiocesium Concentration of Small Epipelagic Fishes (Sardine and Japanese…

115

Fig. 9.2 Mean standard length of fish samples (sardine and Japanese anchovy) used in this chapter. Vertical bar indicates standard deviation

9.4

Temporal Fluctuations in Radiocesium Concentration
of Small Epipelagic Fishes

Because there was no significant difference between radiocesium concentrations of
sardine and Japanese anchovy collected during the research period (Fig. 9.3), these two
species were considered together as ‘small epipelagic fishes’ for the analysis. From
March to May 2011, the radiocesium concentration in the muscle of small epipelagic
fishes exhibited relatively high concentrations on certain occasions, such as 13 Bq/

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K. Takagi et al.

Fig. 9.3 Temporal variations of radiocesium (134Cs + 137Cs) concentration in small epipelagic fish
(sardine and Japanese anchovy) caught off the Kashima-Boso area

kg-wet on 25 April, 21 Bq/kg-wet on 26 April, and 27 Bq/kg-wet on 12 May; however,
the concentrations generally remained at 9 Bq/kg-wet or lower (Fig. 9.3). Concentrations
mostly ranged from 9 to 22 Bq/kg-wet from June to August (Fig. 9.3), and these values
were significantly higher than the concentrations detected from March to May (Mann–
Whitney U test, p < 0.01). After detecting the maximum value of 31 Bq/kg-wet in early
July, none of the specimens had a value greater than 20 Bq/kg-wet in August, and 6 and
5.5 Bq/kg-wet were recorded on 25 October and 3 November, respectively, which was
after the summer fishing season (Fig. 9.3). Concentrations have continued to decrease
since 2012, and levels as low as 0.58–0.63 Bq/kg-wet were detected (Fig. 9.3).

9.5

Decreasing Trend of Radiocesium Concentration
of Small Epipelagic Fishes

Measurement results of small epipelagic fishes by NRIFS used in this research were
mainly conducted until August 2011. To complete the time-series data, data for 200
specimens collected in the same area (Fig. 9.4a) as this study were referenced from
radiocesium concentration data (for both 134Cs and 137Cs) of sardine and Japanese
anchovy reported on the FA website from 24 March 2011 to 21 March 2013
(Fig. 9.4b) (Fisheries Agency 2012, 2013). These data were mostly obtained as raw
samples through 7,200-s measurements by local municipalities in the same manner
as the NRIFS data. However, information regarding the length of fish from which
samples were taken was not made public. In addition to muscle samples, samples
prepared from the whole fish are included in the measurement samples (in this chapter, whitebait and samples that are labeled as processed goods were excluded).

37

a
am
ah
On
hi
ac
Hit aka
-n

Latitude (°N)

a

Current of
warm water eddy

ki
sa
Ha shi
o
Ch

Fishing ground
Sampling site of sea water

35
143

140
Longitude (°E)
35

7
Fish muscle data measured by NRIFS

Radiocesium concentration
in fish (Bq/kg-wet)

30

6

Fish data published by FA

25
Sea water data after Aoyama et al. (2012)

5

20

4

15

3

10

2

5

1

0

0

Radiocesium concentration
in sea water (Bq/L)

b

2011

2012

1- Feb.

1- Dec.

1- Oct.

1- Aug.

1- Jun.

1- Apr.

1- Feb.

1- Dec.

1- Oct.

1- Aug.

1- Jun.

1- Apr.

Below the detection limit

2013

Date

Fig. 9.4 (a) Locations of fishing grounds of fish sampled (sardine and Japanese anchovy) in this
chapter (shaded area), and sampling site of seawater (star) (after Aoyama et al. 2012). Thin curved
arrows indicate current of warm water eddy (after Aoyama et al. 2012). (b) Temporal variations of
radiocesium (134Cs + 137Cs) concentration in small epipelagic fish (sardine and Japanese anchovy)
caught off the Kashima-Boso area and seawater (after Aoyama et al. 2012). The National Research
Institute of Fisheries Science (NRIFS) measured radiocesium concentration of fish muscle. Data
from the Fisheries Agency (FA) indicate radiocesium concentrations of both muscle and whole
body in fish. Plot below the x-axis indicates the existence of data indicating a radiocesium concentration below the detection limit

118

K. Takagi et al.

The published data on the aforementioned FA website do not state the collection
date; thus, in this study we substituted the published date as the collection date for
each datum. According to this, even after August 2011, the gradual decreasing trend
of the concentration continued. After December 2011, the concentration decreased
below 5.0 Bq/kg-wet, and by April 2012, many specimens had concentrations below
the lower limit of detection. The detection limit value since April 2012 was 0.54 Bq/
kg-wet on average for 137Cs (range, 0.29–0.76). The concentrations of 137Cs obtained
from the measurement of ashed samples by NRIFS in June 2012, August 2012, and
February 2013 were 0.38, 0.42, and 0.42 Bq/kg-wet, respectively, which were lower
than the aforementioned average detection limit values.

9.6

Radiocesium Concentration in Seawater
of the Fishing Ground

Aoyama et al. (2012) measured the radiocesium concentration (Fig. 9.4b) of the
seawater collected in Hasaki (Fig. 9.4a) near the fishing ground from 25 April to 5
December 2011 after the FNPP accident. According to these results, the radiocesium concentration of seawater was less than 1.0 Bq/l from April to May 2011, and
then it suddenly increased in June, reaching an average of 3.9 Bq/l in early June.
After attaining the maximum value of 4.4 Bq/l in mid-June, concentration gradually
decreased in late June to an average of 3.4 Bq/l. The concentration continued to
decrease and reached an average of 1.1 Bq/l in late July, and in late August the average concentration was less than 1.0 Bq/l (Fig. 9.4b) (Aoyama et al. 2012). Differing
from the fluctuations in the radiocesium concentration of small epipelagic fishes in
the same marine area (Figs. 9.3 and 9.4b), the radiocesium concentration of seawater spiked in June, showing values significantly higher than the concentrations in
April to May and July to August (Mann–Whitney U test, p < 0.05). Aoyama et al.
(2012) analyzed this situation as a reflection of the temporary inhibition of southward flow of the seawater (strongly affected by the FNPP accident) because of the
presence of a warm eddy (Fig. 9.4a) and its arrival to Hasaki in early June. According
to the survey conducted by FRA in August 2012, it has been found that the radiocesium concentration near the fishing ground (36°15′N–141°00′E) has decreased to
16 mBq/l (10 mBq/l for 137Cs only) (Fisheries Research Agency 2013).

9.7

Fluctuations of Radiocesium Concentration of Small
Epipelagic Fishes Associated with Their Migration
Patterns

Compared to spiking fluctuations of the radiocesium concentration of the seawater,
the radiocesium concentration in the muscle of small epipelagic fishes showed a
relatively mild increase and decrease (Fig. 9.4b). Because radiocesium is

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Radiocesium Concentration of Small Epipelagic Fishes (Sardine and Japanese…

119

incorporated into the bodies of fish from the environment and remains there for
some time, the radiocesium concentration of small epipelagic fishes gradually
decreased following the fluctuations of radiocesium concentration in seawater.
However, because samples were prepared from the catch for this study, fluctuations
in concentration in the bodies of fish might be affected by the distribution condition
of small epipelagic fishes in the fishing ground. Sardine and Japanese anchovy are
widespread in the Sanriku-Boso area during winter and spring, and wintering age 0
fish are known to migrate southward from Sanriku to Boso (Uchiyama 1998; Yasumi
2008; Kubota 2012). From the coast off Hokota City, which is located just to the
north of Kashima City, to the coast off Kitaibaraki City, the concentrations detected
from April to May 2011 for sardine and Japanese anchovy were 40 and 30–170 Bq/
kg-wet, respectively (Fisheries Agency 2012). Based on these results, the reason
that the radiocesium concentration of small epipelagic fishes increased before the
concentration in the seawater of Hasaki increased, and showed some variability,
may be that the school of fish from the northern ocean with a radiocesium concentration higher than that of Hasaki has migrated into the fishing ground off the
Kashima-Boso area.

9.8

Comparison of Situations Before and After
the FNPP Accident

From 134Cs and 137Cs released as a result of the FNPP accident, we will use the 137Cs
nuclide with a relatively long half-life (30.1 years), which can be compared to the
pre-FNPP accident conditions, to continue this discussion.
Measurement values from May to November 2011 (for which radiocesium concentration data of seawater in Hasaki are complete from the early part of a month to
the later part) were used to compare the fluctuations in 137Cs concentration of seawater and small epipelagic fishes in 2011 for monthly average values (Fig. 9.5). The
average concentrations in small epipelagic fishes were 6.1 ± 4.3, 8.8 ± 3.8, 8.9 ± 3.9,
and 7.9 ± 2.0 Bq/kg-wet for May, June, July, and August, respectively; the August
average value was close to those of June and July, but it had relatively small deviations (Fig. 9.5). The values decreased to approximately half the value recorded in
May by October and November at 3.2–3.4 Bq/kg-wet. In comparison, the concentrations in seawater were 0.07 ± 0.02 Bq/l in May, with a maximum value of
1.65 ± 0.77 Bq/l in June. It then decreased to 0.95 ± 0.30 Bq/l in July, and the
decreasing trend continued; by November, the value was similar to that from May
at 0.07 ± 0.01 Bq/l. As these results show, seawater concentrations quickly decreased
after peaking in June, but the concentrations of small epipelagic fishes remained
relatively high until August. Thus, this clearly indicates a delayed decreasing trend
compared to the seawater. Assuming that the small epipelagic fishes and environmental water are in equilibrium, we calculated the concentration coefficient (biological concentration/seawater concentration) of 137Cs in the muscle of small pelagic
fish from the average monthly values of radiocesium concentration already

Fig. 9.5 Relationship in
mean 137Cs concentration per
month between seawater
(after Aoyama et al. 2012)
and small epipelagic fish
(sardine and Japanese
anchovy) measured by
National Research Institute of
Fisheries Science (NRIFS)
during May to November
2011. Horizontal and vertical
bars indicate standard
deviation

K. Takagi et al.
Mean137Cs concentration in fish muscle
(Bq/kg-wet)

120
15

Jul. Jun.
May
10

5

Aug.

Nov. Oct.

0
0

0.1

1

3

Mean137Cs concentration in sea water
(Bq/L)

described. The results showed that the coefficient varied from 5 to 94 in 2011, with
October and November having values of 34 and 46, respectively. Based on the survey results by FRA (2013), the concentration coefficient of 137Cs of seawater concentration near the fishing ground in August 2012 was obtained, and the result was
42. The concentration coefficient of 137Cs before the FNPP accident was 10–100 for
all types of fishes, but 20–40 for sardine (Yoshida 1999); thus, the concentration
coefficient of small epipelagic fishes collected in the target marine area since the fall
of 2011 appears to be returning to this range. In contrast to the 137Cs concentration
in the muscles of sardine collected in the same marine area in June 2009, 0.038 Bq/
kg-wet (Ministry of Agriculture, Forestry and Fisheries Agriculture 2011), concentrations approximately 10 times higher than those from before the FNPP accident
(0.42 Bq/kg-wet) were detected in August 2012 and February 2013 during the
course of this study. Meanwhile, as the 137Cs concentration in seawater was
2.2 mBq/l in June 2009 (Japan Coastal Guard 2010), the value in August 2012 was
approximately 4.5 times higher than that from before the FNPP accident. Therefore,
it has been indicated that the seawater concentration decreases before the radiocesium concentration of small epipelagic fishes decreases. Based on these results,
although the rapid fluctuations in radiocesium concentrations are decreasing, the
radiocesium concentration still remains higher than that before the FNPP accident.
It is necessary to continue long-term monitoring to track the decreasing process of
radiocesium in small epipelagic fishes and analyze the behaviour of radiocesium in
marine ecosystems.
Acknowledgments This chapter was written based on Takagi et al. (2014). As emergent radioactivity monitoring of marine organisms immediately after the Tohoku Region Pacific Coast
Earthquake, fishes were dissected with great cooperation from everyone at National Research
Institute of Fisheries Science, for which we hereby express our sincere gratitude. In particular, the
contract staffs from Radioecology Group of the Marine Ecology Research Centre have continued
to dissect and measure the fishes for radioactive content. We wish to extend our most sincere

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121

thanks to Dr. Satoshi Honda of Fisheries Research Agency headquarters, who gave us valuable
advice on the fishing situations and resource conditions of the Pacific stock of sardine. In addition,
this study was conducted under the 2011–2013 Fisheries Agency Commissioned Project
‘Radioactive Material Impact Investigation Research Project.’
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Agency, Tokyo, pp 15–44 (in Japanese)
Kubota H (2012) Ecological characteristics estimated by long-term resource fluctuations in the
Pacific group of Japanese anchovy. Fish Biol Oceanogr Kuroshio 13:27–32 (in Japanese)
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Forestry and Fisheries related radioactivity survey research annual report, Tokyo (in Japanese)
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series 7 Gamma-ray spectrometry by germanium semiconductor detector (1992 revised edition). Tokyo
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Spotted Mackerel — fishing condition related materials. National Research Institute of
Fisheries Science, Fisheries Research Agency, Yokohama, 20–21 Dec (in Japanese)
Takagi K, Fujimoto K, Watanabe T, Kaeriyama H, Shigenobu Y, Miki S, Ono T, Morinaga K,
Nakata K, Morita T (2014) Radiocesium concentration of small epipelagic fishes (sardine and
Japanese anchovy) off Kashima–Boso area. Nippon Suisan Gakkaishi 80:786–791 (in Japanese)
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released into the atmosphere and the ocean accompanying the FNPP accident due to the impact
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Uchiyama M (1998) Immature fish during the wintering season. In: Watanabe Y, Wada T (eds)
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Chapter 10

Why Do the Radionuclide Concentrations
of Pacific Cod Depend on the Body Size?
Yoji Narimatsu, Tadahiro Sohtome, Manabu Yamada, Yuya Shigenobu,
Yutaka Kurita, Tsutomu Hattori, and Ryo Inagawa

Abstract We examined year-class-related differences in radiocesium concentrations in Pacific cod (Gadus macrocephalus) and evaluated the potential factors
affecting the differences after the release of large amounts of radionuclides from
Fukushima Dai-ichi Nuclear Power Plant (FNPP) in March 2011. The concentration
of radiocesium was highest in the 2009 and earlier year-classes (yc) (≤2009 yc),
followed by the 2010 yc, and was rarely detected in the 2011 yc. Trawl surveys
throughout the year revealed that a proportion of Pacific cod born in or before 2009
and 2010 were distributed in the coastal area from winter to early summer, whereas
all individuals were on the upper continental slope from early summer to winter.
The concentration of radiocesium decreased more rapidly in the 2010 yc than in the
≤2009 yc. The diet of cod changed ontogenetically and spatiotemporally. The
organisms preyed upon on the upper continental slope by cod of all year-classes and
in the coastal area by the 2010 yc contained very low concentrations of radiocesium.
However, some food items ingested in the coastal area by the ≤2009 yc had relatively

Y. Narimatsu (*) • T. Hattori
Hachinohe Laboratory, Tohoku National Fisheries Research Institute, Fisheries Research
Agency, 25-259, Shimomekurakubo, Samemachi, Hachinohe, Aomori 031-0841, Japan
e-mail: nary@affrc.go.jp
T. Sohtome • M. Yamada
Fukushima Prefectural Fisheries Experimental Station,
13-2, Matsushita, Onahamashimokajiro, Iwaki, Fukushima 970-0316, Japan
Y. Shigenobu
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
Y. Kurita
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama-cho, Shiogama-city, Miyagi, 985-0001, Japan
R. Inagawa
Hachinohe Laboratory, Tohoku National Fisheries Research Institute, Fisheries Research
Agency, 25-259, Shimomekurakubo, Samemachi, Hachinohe, Aomori 031-0841, Japan
Kushiro Laboratory, Hokkaido National Fisheries Research Institute, Fisheries Research
Agency, 116 Katsurakoi, Kushiro, Hokkaido 085-0802, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_10

123

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Y. Narimatsu et al.

high radiocesium levels. These results suggest that Pacific cod primarily accumulated
radiocesium during the first few months after the FNPP accident. Age- and body
size-dependent differences in growth, metabolic rate, and diet, as well as seasonal
migration patterns, also affected the rate of decrease in radiocesium levels, which
likely led to the differences we observed between year-classes.
Keywords Pacific cod • Nuclear Power Plant accident • Radiocesium • Year-class
• Seasonal migration • Ontogenetic shift of diet

10.1

Introduction

Huge amounts of radionuclides were released from the devastated Fukushima Daiichi Nuclear Power Plant following the Great East Japan Earthquake on 11 March
2011. The radionuclides contaminated the air, land, and ocean both directly and
indirectly. Model estimates suggest that 3.5 ± 0.7 PBq radiocesium 137 was emitted
directly to the ocean (Tsumune et al. 2012). A number of marine organisms ingested
radionuclides into their body via the water and their diet. As a result, high concentrations of radiocesium were detected in almost all fish that inhabit the coast of
Fukushima Prefecture within a year after the tsunami (Buesseler 2012). The level of
contamination has decreased over time, and has now stabilized at a low level in
pelagic fish species and invertebrates (Wada et al. 2013; Sohtome et al. 2014). In
contrast, the decline in radionuclide levels has occurred more slowly in demersal
fishes, resulting in food safety problems.
Pacific cod (Gadus macrocephalus) are one of the most important species in the
upper continental slope ecosystem for commercial fishermen in the North Pacific
off northern Japan (Tohoku area). The concentration of radiocesium in demersal
fishes such as bighand thornyhead (Sebastolobus macrochir) and threadfin hakeling
(Laemonema longipes) that inhabit the upper continental slope was low and stable
even soon after the Fukushima Daiichi Power Plant (FNPP) accident (MAFF 2014).
Despite occupying a similar spatial niche as these species, the radiocesium levels in
some Pacific cod individuals were higher than allowable values in Japan (134Cs + 137Cs,
100 Bq/kg-wet). Additionally, the majority of demersal fishes that had radiocesium
levels exceeding this standard were clustered in Fukushima and neighboring prefectures. In contrast, unsafe levels of radiocesium were measured in Pacific cod over a
much wider area in 2011 and 2012, including five prefectures in the Tohoku
district.
Commercial fishing or landing of cod was prohibited for 8 months after the
shipment of cod was regulated in May 2012 in Miyagi Prefecture. The cod fishery
was partially restarted in September 2012 when small cod (<1 kg) were approved
for harvest, because high levels of radiocesium were only detected in large fish
(≥1 kg). Therefore, the concentration of radiocesium in Pacific cod appears to be a

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Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

125

function of age and body length. Our objective was to evaluate the relationship
between age, body size, and radiocesium concentrations in Pacific cod following the
FNPP accident. We documented the seasonal change in the distribution of fish of
two age classes. Additionally, we evaluated the feeding ecology of Pacific cod in
two regions to document ontogenetic shifts in diet. We measured radiocesium concentrations in the primary diet items of Pacific cod. Based on these data, we estimated when and how radiocesium was taken up by Pacific cod and the rate of
decrease. We then used these results to predict conditions in the near future.

10.2

Radiocesium Concentration of Pacific Cod

We recorded the standard length and body weight of Pacific cod that were captured
from April 2011 to March 2014 off Fukushima Prefecture and then removed the
sagittal otoliths. One of the sagittal otoliths was cut into slices with hard resin and
used for age determination following the method of Hattori et al. (1992). We determined the birth year-class of all specimens. Muscle tissue samples were removed
from the vertebrae and skin to measure radiocesium concentrations. We examined
the temporal changes in radiocesium concentration following the nuclear accident
and compared the levels among year-classes (ycs).
The radiocesium concentration of Pacific cod was always higher in the year
classes of 2009 and earlier (≤2009 yc) than in the 2010 yc (Fig. 10.1). The radiocesium concentrations measured from April 2012 to March 2013 ranged from

500

Radiocesium concentration
(Cs134+137, Bq/kg-wet)

2011 yc
2010 yc

400

2009≥ yc
300

200

100

0

NN
DD

r. Ap

ne
Ju

2011

NN
DD

N
D

N
D

N
D

N
D

NN
DD

NN
DD

.
t.
.
t.
c.
c.
ne
ne
ar
ar
ep
ep
De
Ju
De
Ju
-S
-S
.-M
.-M
t .r. r. lyy
y
l
n
l
n
c
p
u
p
J
A
O
A
Ju
Ja
Ju
Ja

2012

2013

Fig. 10.1 Temporal changes in radiocesium (134Cs + 137Cs) concentration in the 2011, 2010, and
≤2009 year-classes of Pacific cod. Boxes and bars represent the average and maximum values,
respectively. ND no data

Y. Narimatsu et al.

Radiocesium concentration (Cs134+137, Bq/kg-wet)

126
500
450
400
350
300
250
200
150
100
50
0
200
180
160
140
120
100
80
60
40
20
0

0

0

200

400

600

800

1000

200

400

600

800

1000

Days after the Great East Japan Earthquake

Fig. 10.2 Decay process of radiocesium in ≤2009 (upper) and 2010 (lower) year-classes of
Pacific cod. The relationships were fitted for exponential function, expressed by the curved lines

0.37 to 0.75 times (average ± SD = 0.57 ± 0.16) lower in the 2010 yc than in the
year-classes from 2009 and earlier. The concentration of radiocesium has
decreased temporally since the nuclear plant accidents in both year-classes
(Fig. 10.1). Interestingly, radiocesium was rarely detected, or detected at very low
levels, in the 2011 yc.
The ecological half-life (Morita and Yoshida 2005; Iwata et al. 2013) was calculated using the exponential regression for surveyed concentrations of radiocesium
and used to estimate the half-lives of radiocesium. This value can be used to predict
future radiocesium concentrations. The regressions suggest that the ecological halftime of radiocesium was 309 and 258 days in the ≤2009 and 2010 year classes,
respectively (Fig. 10.2). These results suggest that older and larger individuals concentrated higher levels of radiocesium and/or excreted radiocesium at a slower rate
than younger and smaller Pacific cod individuals. The factors affecting age-related
difference are examined in the subsequent sections.

10

Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

10.3

127

Seasonal Change in Distribution

We conducted benthic trawl surveys from 2004 to 2013 in the northern Pacific off
Honshu Island, Japan (Tohoku area) and in Sendai Bay using two research vessels
(Table 10.1). Surveys off Tohoku area were conducted in April and in October–
November at depths between 150 and 900 m (Fig. 10.3, Table 10.1). Surveys in
Sendai Bay were conducted in January, February, April, June, July, and November
at depths between 30 and 122 m. The details of the benthic trawl survey

Table 10.1 List of trawl survey cruises conducted in the present study by the research vessels
Dai-nana Kaiyo-maru (D), or Wakataka-maru (W) in Sendai Bay (S) or offshore of Tohoku (T)
giving the duration of the survey and number of benthic trawl tows (N)
Cruise
200407
201006
201202
201204
201210
201304
201310

Vessel
W
W
D
W
W
W
W

Fig. 10.3 Location of the
study site and the epicenter
of the Great East Japan
Earthquake. Surveys were
conducted at depths of
38–650 m in Sendai Bay and
offshore of Tohoku

Area
S
S
S
S&T
S&T
S&T
S&T

Duration
28 Jun–2 Jul 2004
20–23 Jun 2010
2–6 Feb 2012
17–25 Feb 2012
20 Oct–21 Nov 2012
16–23 Apr 2013
15 Oct–25 Nov 2013

N
12
12
6
19
31
20
38

Y. Narimatsu et al.

128
fish density
(n/km2)
30,000
3,000

Feb.

fish density
(n/km2)
30,000
3,000

300

Apr.

fish density
(n/km2)
30,000
3,000

300

June

300

38 20N

40m

80m

40m

120m

80m

120m
160m

160m

38 00N

fish density
(n/km2)
30,000
3,000
300

July

140 00N

fish density
(n/km2)
30,000
3,000
300

140 20N

140 40N

Nov.

38 20N

40m

80m

40m

120m

80m

120m
160m

160m

38 00N

140 00N

140 20N

800

140 00N

140 40N

fish density
(n/km2)
8,000

Feb.

140 20N

140 40N

fish density
(n/km2)
8,000
800

80

Apr.

fish density
(n/km2)
8,000
800

80

June

80

38 20N

40m

80m

120m

40m

80m

fish density
(n/km2)
8,000
800

July

80m

140 00N

fish density
(n/km2)
8,000

120m
160m

160m

800
80

40m

120m

160m

38 00N

140 20N

140 40N

Nov.

80

38 20N

40m

80m

120m

40m

80m

140 00N

140 20N

140 40N

120m
160m

160m

38 00N

140 00N

140 20N

140 40N

Fig. 10.4 Seasonal changes in the distribution of age 1+ (upper) and age ≥2+ (lower) Pacific cod
in and off Sendai Bay. The timing of the surveys is described in Table 10.1

methodology are described by Hattori et al. (2008). We counted the number of age
1+ and 2+ Pacific cod caught in the net and estimated fish density (numbers/km2) by
dividing the number of fish captured by the trawl area.
Pacific cod aged 1+ year old were captured in shallow areas in Sendai Bay from
February to June, but not in July and November (Fig. 10.4). In February and June,
the majority of age 1+ cod were captured at depths >80 m, whereas in April they

10

Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

129

were captured in shallower waters. Pacific cod of age ≥2+ were also captured in
Sendai Bay from February to June, with peak catches occurring in February and
April. Only a few individuals remained in the Bay in June, and none was captured
in the area shallower than 120 m in July and November.
Based on the results of this long-term trawl survey, Pacific cod appear to be
widely distributed offshore of Tohoku in the spring and autumn (Fig. 10.5). In April,
1+-year-old Pacific cod tend to occupy the 100 to 400 m depth zone off Tohoku,
but the density is highest at 100–200 m and very low at ≥300 m. In October–
November, age 1+ cod occupied the depth zone from 200 to 500 m, with density
peaking at 200–400 m. Cod were not captured in areas shallower than 200 m during
these months. Age ≥2+ cod were captured at depths of 100–600 m and 200–600 m
in April and October, respectively. The distribution of Pacific cod differed between
months. The cod occupied depths that are about 100 m shallower in April (300–
400 m) than in October.
The density of fish was compared between Sendai Bay and Tohoku for samples
collected in April and in October–November. The density of 1+-year-old individuals
was high at depths of 50–200 m, and particularly at 80–150 m (Fig. 10.5). Fish were
seldom captured deeper than 300 m. The density of age 1+ Pacific cod was about
four times higher at the 38–100 m depth than at 120–450 m in April. The age ≥2+
individuals were widely distributed, from 50 to 500 m. In contrast, in autumn,
Pacific cod of both age classes were distributed from 200 to 600 m, but were most
39 00N

39 00N

density (n/km2)

density (n/km2)

density (n/km2)
20000

20000

20000

2000
20

2000
20

2000
20

Apr. 2012
Age 1+

Apr. 2013
Age 1+

Oct.-Nov. 2012
Age 1+

38 30N

38 30N

38 00N

38 00N

50m
100m

37 30N

39 00N

200m

50m
100m
500m

density (n/km2)

200m

500m

37 30N

39 00N

density (n/km2)

5000
500
50

Apr. 2012
Age 2+

38 30N

38 00N

38 00N

141 00E

200m

141 30E

50m
100m
500m

142 00E

50m
100m

200m

50m
100m
500m

141 00E

200m

141 30E

500m

142 00E

37 30N

500m

5000
500
50

Oct. –Nov. 2013
Age 2+

50m
100m

141 00E

200m

density (n/km2)

density (n/km2)

Oct. –Nov. 2012
Age 2+

Apr. 2013
Age 2+

50m
100m

Oct.-Nov. 2013
Age 1+

5000
500
50

5000
500
50

38 30N

37 30N

density (n/km2)

20000
2000
20

200m

141 30E

50m
100m

200m

500m

142 00E

141 00E

141 30E

500m

142 00E

Fig. 10.5 Comparison of the distribution of age 1+ (upper) and age ≥2+ (lower) Pacific cod
between spring and autumn. The timing of the surveys is described in Table 10.1

130

Y. Narimatsu et al.

abundant at 200 to 500 m. The density of age ≥2+ Pacific cod was about two times
higher at 38–100 m than at 120–450 m in April. These observations suggest that
Pacific cod could inhabit the area near the FNPP at high density in April, during the
time when cold water flows into Sendai Bay and offshore areas (Ito et al. 2004), but
these fish migrate to the continental slope in July and remain there for several
months.
Trawl surveys conducted off Tohoku throughout the year revealed that age 1+
and older Pacific cod were distributed at depths of 200–600 m in autumn, consistent
with a previous report (Kitagawa et al. 2002), indicating that Pacific cod only inhabit
the upper-continental slope during the autumn. In contrast, Pacific cod were distributed over both the upper continental slope and the continental shelf from winter to
early summer. In Sendai Bay, age 1+ and ≥2+ individuals were represented in the
catch from February to June. The older cod migrated into Sendai Bay and moved
offshore slightly earlier than the younger individuals. In April, Pacific cod aged 1+
and ≥2+ years old were distributed throughout Sendai Bay, and their density was
highest at the bay mouth (80–200 m deep). A large amount of radiocesium was
released into the ocean after the FNPP accident in mid-March 2011, at a time when
Pacific cod had likely moved into the shallower area. After occupying this area for
a maximum of 3 or 4 months, the cod migrated off the continental shelf in July and
did not return to the bay until February of the next year. Cod were distributed at
depths similar to those of bighand thornyhead, Sebastolobus macrochir (Hattori
et al. 2008), and threadfin hakeling, Laemonema longipes (Narimatsu et al. 2014),
in offshore areas. The concentration of radiocesium in these two species remained
very low or was nondetectable (Wada et al. 2013; MAFF 2014). Taking into consideration the pattern of seasonal migration, the rate of decline of radiocesium levels in
Pacific cod, and the concentration of radiocesium in other species that occupy the
upper continental slope, we conclude that contamination of Pacific cod with radiocesium occurred soon after the nuclear plant accident, from March to June in 2011.

10.4

Ontogenetic and Seasonal Diet Shift of Pacific Cod

Age 1+ and 2+ Pacific cod caught in Sendai Bay and off the Tohoku area, which is
located off FNPP with a depth of 250 m, were used to evaluate their diet. Samples
of fish were collected in April, June, and November in Sendai Bay, and in April and
November off Tohoku. Fish were frozen soon after capture, their standard length
and body weight were recorded, and they were dissected in the laboratory. The
stomach was cut open and food items were sorted to the lowest possible taxon. Prey
items were weighed to nearest 1 mg (wet weight). The percent contribution of each
prey item to the diet of each age class was calculated. We compared the seasonal
and spatial variation and ontogenetic shifts in the diet of Pacific cod.
A total of 247 fish stomachs were examined yielding 36 taxon or species of prey
items. The primary prey items (>1 % of the total wet weight) differed among seasons, habitat types, and the body size of cod. In Sendai Bay, age 1+ Pacific cod

10

Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

131

Wet weight % in stomach contents

100

80

60

40

20

0

2+≤
1+
Age class
Fig. 10.6 Ontogenetic shift in diet for Pacific cod in Sendai Bay from April to June in 2012 and
2013

preyed primarily on Crangon spp. (Crustacea) such as Crangon affinis and C. dalli,
followed by white croaker (Pennahia argentata, Pisces; Fig. 10.6). These two prey
items accounted for 84 % of the total diet. Unidentified Pisces (6.9 %) and Betaeus
granulimanus (Decapoda) were the next most common prey items. Age ≥2+ Pacific
cod consumed a wider range of organisms compared with younger fish. In Sendai
Bay, the older cod most commonly preyed on sand lance (Ammodytes personatus),
followed by Paroctopus spp. (P. dofleini and P. conispadiceus), Pleuronectes spp.
(P. herzensteini and P. yokohamae), and Crangon spp. A number of other fish and
invertebrates were observed in the stomachs of age 2+ Pacific cod captured from
April to June in Sendai Bay.
Age 1+ Pacific cod fed on the small pelagic invertebrates Euphausia pacifica,
Watasenia scintillans, and Themisto japonica in April and June on the upper continental slope off Tohoku (Fig. 10.7). Age ≥2+ Pacific cod preyed primarily on flathead flounder Hippoglossoids dubius, followed by Euphausia pacifica. In October
and November, benthic shrimp Pandalus eous were the most abundant (wet-weight)
prey item of 1-year-old Pacific cod, followed by myctophid fish Diaphus watasei
and unidentified fishes (Fig. 10.7). Older cod frequently fed on unidentifiable fishes,
as well as Diaphus watasei and horsehair crab Erimacrus isenbeckii. These observations suggest that Pacific cod shift food items not only ontogenetically but also
spatiotemporally.
Age 1+ cod fed on benthic Natantia euphausiids, small decapod cephalopods,
small fishes, and cephalopod octopi whereas age ≥2+ individuals fed on Cephalopoda

132

Y. Narimatsu et al.

Wet weight % in stomach contents

100

80

60

40

20

0

1+

2+≤ 1+

2+≤

Apr. - June Oct. – Nov.
Fig. 10.7 Ontogenetic and temporal changes in diet for Pacific cod off Tohoku from October to
November in 2012 and 2013

(octopods), benthic Natantia, Brachyura, and fish, including flatfish. Prior studies
have documented a diet shift in Pacific cod distributed in areas deeper than 100 m
(Hashimoto 1974; Yamamura 1994; Fujita et al. 1995). Cod smaller than 30 cm SL
(corresponding to 1+-year-old individuals) primarily consume planktonic organisms. Cod in the range 30–40 cm SL (1+ to 2+ years old) also depend on Euphausiids,
but the contribution to their diet is lower than for 30 cm fish, and they also feed on
demersal organisms. Fish larger than 40 cm SL (≥2+ years old) primarily prey on
fish and macrobenthos and rarely on planktonic invertebrates. Seasonal changes in
diet were also observed in this population. Pelagic organisms such as euphasiids and
mesopelagic fishes were the main prey items in the spring, whereas benthic species
were the dominant prey item in autumn. Such variability in the type of prey items
consumed by Pacific cod may reflect the general feeding characteristics of this species and seasonal changes in the biotic environment. Our observations suggest that
large Pacific cod (age ≥2+) also consume mesopelagic invertebrates and that small
individuals (age 1+) feed on similar items. However, Pacific cod basically shift their
feeding habit from small plankton to macrobenthos with growth, and macrobenthic
organisms such as large octopi and flatfishes can be prey items only for large cod
because of the gape limitation of Pacific cod. The demersal fish such as sand lance
and flatfish tended to accumulate radiocesium in their body and are only preyed on
by large Pacific cod. The ontogenetic niche shift and species-specific difference in

10

Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

133

radiocesium concentration may result in the size-dependent difference in radiocesium concentrations observed in Pacific cod.

10.5

Radiocesium Concentration of Prey Items

A part of the species that occurred in the stomachs of Pacific cod were caught in the
trawl surveys. The radiocesium concentrations of them and a part of prey items were
measured by same method as the fish samples. The concentrations of the rest organisms were referred from the previous reports, respectively (MAFF 2014; Sohtome
et al. 2014).
The radiocesium concentrations were analyzed for 17 species or taxon, which
are the main prey items of Pacific cod in Sendai Bay and Tohoku (Fig. 10.8). The
1300

1300
range

average

Radiocesium concentration (Cs134+137, Bq/kg-wet)

1000

400

400
150
100
50
0

Pa

Cgs

Ap*1

Pls

Pos

Ap*2

Pgs

90
75
60
45
30
15
0
Hd

Dw

Ej

Pe

Ep

Tj

Gs

Ws

Bs

Ei

Pos

Primary prey items of Pacific cod in Sendai Bay

Fig. 10.8 Radiocesium concentrations in the primary prey items of Pacific cod in Sendai Bay
(upper) and off Tohoku (lower). Species or taxon are shown by abbreviations: Cgs Crangon spp.,
Pa Pennahia argentata, Ap Ammodytes personatus, Pos Paroctopus spp., Pls Pleuronectes spp.,
Pgs Pagurus spp., Hd Hippoglossoides dubius, Dw Diaphus watasei, Ej Engraulis japonicus, Pe
Pandalus eous, Ep Euphausia pacifica, Tj Themisto japonica, Gs Gammaridea spp., Ws Watasenia
scintillans, Bs Brachyura spp., Ei Erimacrus isenbeckii. The indicators *1 and *2 indicate specimens caught from April 2011 to March 2012 and from April 2012 to December 2012,
respectively

134

Y. Narimatsu et al.

concentration of radiocesium in Crangon spp. and white croaker (Pennahia argentata,
Pisces) ranged from below the detection limit (DL) to 126.3 Bq/kg-wet weight
(mean ± SD =19.5 ± 24.3) and below the DL to 41.0 Bq/kg-wet (12.5 ± 16.3), respectively. The concentration of radiocesium was higher within 1 year after the accident
(134.5 ± 102.7) than 1 year after the accident (29.0 ± 21.8) in the sand lance
Ammodytes personatus, the dominant prey item of age ≥2+ cod. Although the radiocesium concentrations in all Paraoctopus spp. and hermit crab Pagurus spp.
(Anomura) were below the DL or relatively low (24.4 ± 24.3), high levels were
detected in some Pleuronectes spp. specimens (102.5 ± 169.2). Almost all the prey
items consumed on the upper continental slope had levels below the DL, except for
the flathead flounder Hippoglossoids dubius (7.7 ± 14.7) and crabs (Tymolus japonicus, Carcinoplax vestiva: 2.8 ± 4.9). These results suggest that the concentrations of
radiocesium were very low in the prey of Pacific cod (all age groups) off the FNPP
at a depth of 250 m. In Sendai Bay, organisms consumed by age 1+ Pacific cod had
relatively low radiocesium levels. However, some prey items observed in the stomach of age ≥2+ cod had relatively high radiocesium levels.
As described here, the timing of the migration from offshore to inshore and vice
versa was similar between age classes, suggesting that the exposure to radiocesium
was similar regardless of age and body size. However, the concentration of radiocesium was always higher in older and larger fish than in younger and smaller fish.
A number of marine organisms, including seaweeds, invertebrates, and fish, were
contaminated by the radiocesium released from FNPP. The concentration and rate
of decrease varied among species, likely because of differences in their biological
characteristics (Wada et al. 2013). The levels of radiocesium were highest soon after
the FNNP accident in all taxon (Wada et al. 2013). This pattern suggests that radiocesium contamination of all organisms primarily occurred in the first few months
after the accident. Organisms that were distributed near the FNPP accumulated
radiocesium from the seawater and prey items. The concentration of radiocesium in
Pacific cod was variable, likely dependent on the initial intake of radiocesium, rate
of decrease speed of radiocesium, the amount of additional intake of radiocesium
from seawater, and the rate of growth (BW) during the first few months. However,
additional intake of radiocesium only occurred via prey because radiocesium concentration in seawater was rapidly diluted/transported out of the area within a year,
except for that in the port of FNPP (Buesseler et al. 2011; Aoyama et al. 2013;
Kaeriyama et al. 2013, 2014); those levels in pelagic fish rapidly decreased (Iwata
et al. 2013; Wada et al. 2013), and Pacific cod seldom inhabit and stay in the
intertidal zone.
Pacific cod grow very rapidly (Hattori et al. 1992), resulting in dilution of the
radiocesium in their body (dilution effect). Age 1+ cod are about 0.5 kg BW but
grow to 1.5 kg BW in 1 year. Similarly, cod that are 1.0 kg BW (age 2+) grow to
2.3 kg BW in a year. A 0.5-kg BW individual has a 1.30 times higher dilution effect
for radiocesium than does a 1.0-kg BW cod. The ecological half-time of radiocesium was estimated to be 258 and 309 days in the 2010 and the ≤2009 year-classes,
respectively. Taking into consideration both the dilution effect and the age-specific
decrease in concentrations, the level of radiocesium in the 2010 year-class is

10

Why Do the Radionuclide Concentrations of Pacific Cod Depend on the Body Size?

135

expected to decrease 1.56 times earlier than in the ≤2009 year-classes. The mean
concentration of radiocesium in the ≤2009 year-classes was 1.75 times higher than
in the 2010 year-class during the period January 2012 to March 2013. Assuming the
initial concentrations were similar between year-classes, the difference between
observed values and estimated values (based on dilution and age-specific effects)
may be explained by the ontogenetic differences in prey items and their radiocesium
concentration.

10.6

Conclusion

Large numbers of marine organisms were contaminated by radiocesium following
the FNPP accident in March 2011. In some demersal fishes that inhabit the coastal
regions, the rate of decrease in tissue radiocesium levels was lower than for other
pelagic fishes and invertebrates, suggesting that additional radiocesium was taken
up from the benthic ecosystem. This finding delayed the reopening of fisheries in
the region. The estimated ecological half-life of radiocesium in Pacific cod was
from 258 to 309 days; this value is consistent with values in other demersal fishes
caught off Fukushima Prefecture (Wada et al. 2013). The half-life was longer in old
and larger individuals than in young and small individuals, probably a result of differences in metabolic rate and growth rates between age and body size classes (Doi
et al. 2012). Radiocesium concentrations decreased to low levels soon after the accident in seawater and prey items (Buesseler et al. 2011; Aoyama et al. 2013) and
have continued to decease in the period up to 2014 (Sohtome et al. 2014). Thus, the
potential for intake of radiocesium from the benthic ecosystem is very low in and
after 2014. Additionally, radiocesium was rarely detected in the 2011 year-class.
Pacific cod hatch during January to February in Sendai Bay (Narimatsu et al.,
unpublished data) and live a pelagic life for 3–4 months in the coastal zone. Some
individuals of the 2011 year-class took in radiocesium via seawater and diet.
However, the concentration of radiocesium in their body was diluted by growth, and
the fish were only exposed to very low levels of radiocesium after settlement to
benthic life. The Pacific cod of the following year-classes had already recruited into
the ecosystem of the upper continental slope and were commercially caught in the
Tohoku region. This population is primarily composed of young fish, and the generation cycle alters quickly (Narimatsu et al. 2010). We observed a decrease in
radiocesium concentrations in the 2010 and ≥2009 year classes and an increase in
the proportion of individuals born after the accident at the Nuclear Power Plant.
Both these factors reduce the radiocesium concentrations at the population level and
suggest the risk of restarting fisheries is minimal.
Acknowledgments We are grateful to the crews of R/Vs Wakataka maru and Dai-nana Kaiyo
maru for assistance in obtaining samples. We also thank Drs. T. Wada and M. Ito for comments on
the manuscript, and the staff of Hachinohe Laboratory, Tohoku National Fisheries Research
Institute, for help in preparing samples. This work was financially supported by the Fisheries
Agency, Japan.

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Y. Narimatsu et al.

Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
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of TEPCO Fukushima NPP1 released 134Cs and 137Cs. Biogeosci Discuss 10:265–285
Buesseler KO, Aoyama M, Fukasawa M (2011) Impacts of the Fukushima nuclear power plants on
marine radioactivity. Environ Sci Technol 45:9931–9935
Buesseler KO (2012) Fishing for answers off Fukushima. Science 388:480–482
Doi H, Takahara T, Tanaka K (2012) Trophic position and metabolic rate predict the long-term
decay process of radiocesium in fish: a meta-analysis. PLoS ONE 7:e29295. doi:10. 1371/
journal.pone.0029295
Fujita T, Kitagawa D, Okuyama Y, Ishito Y, Inada T, Jin Y (1995) Diets of the demersal fishes on
the shelf off Iwate, northern Japan. Mar Biol 123:219–233
Hashimoto R (1974) Investigation of feeding habits and variation of inhabiting depths with cod
(Gadus macrocephalus) distributed on the northeastern fishing ground in Japan. Bull Tohoku
Reg Fish Res Lab 33:51–67
Hattori T, Narimatsu Y, Ito M, Ueda Y, Kitagawa D (2008) Annual changes in distribution depths
of bighand thornyhead Sebastolobus macrochir off the Pacific coast of northern Honshu Japan.
Fish Sci 74:594–602
Hattori T, Sakurai Y, Shimazaki K (1992) Age determination by sectioning of otoliths and growth
pattern of Pacific cod. Nippon Suisan Gakkaishi 58:1203–1210 (In Japanese with English
abstract)
Ito S, Uehara K, Miyao T, Miyake H, Yasuda I, Watanabe T, Shimizu Y (2004) Characteristics of
SSH anomaly based on TOPEX/POSEIDON altimetry and in situ measured velocity and transport of Oyashio on OICE. J Oceanogr 60:425–438
Iwata K, Tagami K, Uchida S (2013) Ecological half-lives of radiocesium in 16 species in marine
biota after the TEPCO’s Fukushima Daiichi Nuclear Power Plant accident. Environ Sci Technol
47:7696–7703
Kaeriyama H, Ambe D, Shimizu Y, Fujimoto K, Ono T, Yonezaki S, Kato Y, Matsunaga H,
Minami H, Nakatsuka S, Watanabe T (2013) Direct observation of 134Cs and 137Cs in the
western and central North Pacific after the Fukushima Dai-ichi Nuclear Power Plant accident.
Biogeosciences 10:4287–7295
Kaeriyama H, Shimizu Y, Ambe D, Masujima M, Shigenobu Y, Fujimoto K, Ono T, Nishiuchi K,
Taneda T, Kurogi H, Setou T, Sugisaki H, Ichikawa T, Hidaka K, Hiroe Y, Kusaka A, Kodama
T, Kuriyama M, Morita H, Nakata K, Morinaga K, Morita T, Watanabe T (2014) Southwest
intrusion of 134Cs and 137Cs derived from the Fukushima Dai-ichi Nuclear Power Plant accident
in the western North Pacific. Environ Sci Technol 48:3120–3127
Kitagawa D, Hattori T, Narimatsu Y (2002) Monitoring on the demersal fish resources in the
Tohoku area. Kaiyo Mon 34:793–798 (in Japanese)
MAFF (Japan Ministry of Agriculture, Forestry and Fisheries) (2014) Results of the inspection on
radioactivity materials in fisheries products. http://www.jfa.maff.go.jp/e/inspection/index.
html. Accesssed 31 July 2014
Morita T, Yoshida K (2005) Effective ecological half-lives of Cs-137 for fishes controlled by their
surrounding sea-waters. Radioprotection 40(Suppl, 1):S635–S640
Narimatsu Y, Ito M, Hattori T, Inagawa R (2014) Stock assessment and evaluation for the threadfin
hakeling stock of the north Pacific, Japan (fiscal year 2013). In: Marine fisheries stock assessment and evaluation for Japanese waters (fiscal year 2013/2014), Fishries Agency and Fisheries
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in life-history traits on reproductive potential in an exploited population of Pacific cod, Gadus
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Fukushima dai-ichi Nuclear Power Plant simulated numerically by a regional ocean model. J
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with special reference to niche dynamics among dominant fishes. Doctoral dissertation,
Hokkaido University

Chapter 11

Radiocesium Contamination Histories
of Japanese Flounder (Paralichthys olivaceus)
After the 2011 Fukushima Nuclear Power
Plant Accident
Yutaka Kurita, Yuya Shigenobu, Toru Sakuma, and Shin-ichi Ito
Abstract Radiocesium (Cs) contamination histories of the Japanese flounder,
Paralichthys olivaceus, after the 2011 Fukushima Nuclear Power Plant (FNPP)
accident were examined by analysis of the spatiotemporal changes in observed Cs
concentrations, by comparison of the dynamics of the Cs concentrations in several
year-classes of fish, and by simulation studies. Two contamination histories were
revealed: (1) severe contamination by water that was directly released from the
FNPP with extremely high Cs concentrations for a few months after the accident,
which had a highly variable spatial distribution; and (2) long-duration contamination at relatively low concentrations resulting from consumption of contaminated
food. These two histories were supported by three observations. First, high Cs concentrations with high variability were observed in the first year after the accident.
Second, the highest values of the minimum Cs concentrations were observed in the
autumn of 2011. Third, Cs concentrations were lower with smaller variation for fish
from the 2011 year-­class and younger, which were not exposed to the highly contaminated directly released water, than for fish from the 2010 year-class and older.
Simulation studies also indicated that the Cs concentrations in some individuals that
were exposed to the directly released water might not be in an equilibrium state
even at 3 years after the accident. On the basis of these contamination histories, it
can be expected that the Cs concentrations in most Japanese flounder will continue
to decrease.

Y. Kurita (*) • S.-i. Ito
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama-cho, Shiogama, Miyagi 985-0001, Japan
e-mail: kurita@affrc.go.jp
Y. Shigenobu
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
T. Sakuma
Fukushima Prefectural Fisheries Experimental Station,
13-2, Matsushita, Onahamashimokajiro, Iwaki, Fukushima 970-0316, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_11

139

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Y. Kurita et al.

Keywords Radiocesium • Contamination history • Paralichthys olivaceus
• Simulation • Fukushima Nuclear Power Plant • Directly released water • Food
• Year-class • Equilibrium

11.1  Introduction
The marine environment and animals living in it have been severely contaminated by radionuclides, including radiocesium (Cs; 134Cs + 137Cs), released from
the Fukushima Nuclear Power Plant (FNPP) after the accident on 11 March
2011. The Japanese provisional regulatory limit for Cs in fish products was set at
500 Bq/kg-­wet starting immediately after the accident and was enforced until
March 2012; a limit of 100 Bq/kg-wet has been enforced since April 2012. After
the accident, the landing of many commercially important fish species in
Fukushima and neighboring prefectures was legally banned or voluntarily suspended, and the landing of many species in Fukushima Prefecture is still banned
(Wada et al. 2013).
Marine fish take up Cs from seawater and food. The rate of intake is related to
the Cs concentrations in seawater and food sources. Excretion from the body is
related to the Cs concentration in the fish body. It has been suggested that the
impact of contamination resulting from the FNPP accident has been temporally
and spatially heterogeneous (Tateda et al. 2013; Wada et al. 2013). Marine animals are likely to have been severely contaminated for a few months after the
accident, as a consequence of the direct release from the FNPP of massive amounts
of water with extremely high Cs concentrations between 26 March and the end of
April 2011 and the subsequent consumption of contaminated food (Tsumune
et al. 2012; Tateda et al. 2013). The Cs concentrations were higher in the coastal
waters south of the FNPP (Wada et al. 2013). An understanding of the contamination histories that produced the observed temporal changes and spatial variation in
the intensity of contamination will facilitate prediction of the dynamics of Cs
concentrations in fish and will guide decisions regarding the appropriate time to
restart fishing operations.
The Japanese flounder Paralichthys olivaceus, the studied fish species in this
chapter, is a bottom fish inhabiting coastal waters at depths of 150 m or less. They
are given birth in summer (June–August). These fish reach 250–300 mm in total
length (TL) during their first year, during which time most of them inhabit sandy
coasts at depths of less than 20 m and feed on mysids and larval fish. After their first
year, they move to deeper waters and feed exclusively on two bait fish, the Japanese
anchovy Engraulis japonicus and the Japanese sand lance Ammodytes personatus
(Tomiyama and Kurita 2011). The Japanese flounder is an end-member of the
pelagic food chain (from phytoplankton through zooplankton and bait fish to fish
feeder). They reach TLs of approximately 400 mm at 2 years and 500 mm at 3 years

141

Miyagi
Sendai
Bay
FNPP
Fukushima
Ibaraki
Chiba

I
II
III
IV
V
VI
VII

100 km
140° E

100

b

Area I

c

Area II

500

e

Area IV

f

Area V

g

Area VI

0
100

0
1000

0

d

400

Area III

137

Iwate

Cs concentration (134Cs +

40°N

a

Cs) in muscle (Bq/kg-wet)

11  Radiocesium Contamination Histories of Japanese Flounder…

500

200
0
200
0

0

1200 100

800

400

Days after the accident
0
Jul
2011

Jan
2012

Jul

Jan

Jul

2013

Calendar date

Jan
2014

h

50
0

0

Area VII
400

800

1200

Fig. 11.1 (a) Locations of areas I–VII and the Fukushima Nuclear Power Plant (FNPP, star) and
(b–h) temporal changes in the concentrations of Cs (134Cs + 137Cs; Bq/kg-wet) in the muscle of the
Japanese flounder Paralichthys olivaceus collected in the seven areas. Cs concentrations (circles)
were measured by local governments and published by the Fisheries Agency of the Ministry of
Agriculture, Forestry and Fisheries of Japan. Open circles indicate Cs concentrations that were less
than the detection limit; in these cases, the plotted values correspond to the detection limit. In (e–
g), arrows show the peaks in the lowest observed concentration in areas IV–VI, respectively. Cs
concentrations of 1,610 Bq/kg-wet at 187 days after the FNPP accident (14 September 2011) in
area IV (e) and 4,500 Bq/kg-wet at 250 days (16 November 2011) in area V (f) were omitted. Note
that the y-axis scales in e and f differ from those of the other parts

(Yoneda et al. 2007). The flounder inhabiting the waters off Miyagi, Fukushima,
and Ibaraki Prefectures (an area that extends 110 km to the north and 200 km to the
south of the FNPP; Fig. 11.1) are considered to be a subpopulation (Kurita et al.
2014), although movement within this area is somewhat limited (Kurita et al.,
unpublished data).
In this chapter, we examine the temporal changes and spatial variation of Cs
concentrations in Japanese flounder in detail and suggest contamination histories
that would produce the observed variation. First, we analyzed Cs concentration data
collected by local governments and published by the Fisheries Agency of the
Ministry of Agriculture, Forestry and Fisheries (2014) to gain a rough understanding of the temporal changes and spatial variation of Cs concentrations (Sect. 11.2).
We then investigated temporal changes in Cs concentrations among different year-­
classes of the flounder, specifically year-classes born before and after the accident,
to understand temporal changes in the intensity of contamination (Sect. 11.3).
Finally, we simulated the temporal changes in Cs concentration in an effort to
understand how the observed Cs contamination distribution was produced
(Sect. 11.4).

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11.2  S
 patiotemporal Distribution of Cs Concentrations
in Japanese Flounder
For our analysis, we used Cs concentrations in the flounder monitored by local governments (Fisheries Agency 2014) in the region from 35°45′N to 40°25′N, which
was subdivided into seven areas (Fig. 11.1). The sizes and ages of the flounder were
not recorded, but almost all the data are expected to be from fish with a TL greater
than 300 mm (corresponding to a minimum age of 1–1.5 years; Yoneda et al. 2007),
which is the landing size limit for this flounder. The sample sizes for the data points
in the figure are not known for certain, but most of the data points represent concentrations from more than three individuals, except in the areas immediately to the
north and south of Fukushima Prefecture (areas IV and V; Fig. 11.1e, f); in these
areas, most of the data points collected after October 2011 are for individuals.
Examination of the observed concentration data revealed the following
features:
• The Cs concentrations clearly differed among the areas (Fig. 11.1). In the far
north (areas I and II) and the far south (area VII) from FNPP, the concentrations were low; only 1.1 % of the data exceeded 50 Bq/kg-wet. In contrast,
41.0 % of the data in the area around the FNPP (areas IV and V) exceeded
50 Bq/kg-wet. The average Cs concentrations in the seven areas during the
period between 200 and 600 days after the accident decreased in the order
V > IV > III = VI > I = II = VII.
• The Cs concentrations were highly variable among individuals (or individual
data points) within each area (Fig. 11.1). Some extremely high concentrations
were observed, especially during the first year after the accident; for example,
concentrations of 1,610 and 4,500 Bq/kg-wet, respectively, were observed on 14
September 2011 (187 days after the accident) in area IV and on 16 November
2011 (250 days) in area V (these two values were omitted in Fig. 11.1). The
maximum:minimum ratio during October 2011 and March 2012 in area V was
375 (=4,500/12).
• The dynamic patterns of the higher and lower concentrations differed from each
other, especially in area VI (Fig. 11.2). Specifically, examination of the temporal
changes in the concentration percentiles in area VI for six consecutive 6-month
periods starting in April 2011 revealed that the upper concentration percentiles
(75 %, 90 %, and 95 %) decreased steadily during the observed periods, and the
lower percentiles (5 %, 10 %, 25 %, and 50 %) increased from April–September
2011 to October 2011–March 2012 and then decreased steadily.
• The lowest observed concentrations increased slightly in areas IV, V, and VI
(Fig.  11.1); specifically, the lowest observed concentrations peaked at around
200 days after the accident (September–October 2011; arrows in Fig. 11.1e–g)
and then decreased. The peak values of the lowest observed concentrations were
approximately 80, 80, and 30 Bq/kg-wet in areas IV, V, and VI, respectively.
Although these peak values were clearly lower than the values of the higher per-

11  Radiocesium Contamination Histories of Japanese Flounder…

143

Apr – Sep 2011 Oct ’11 – Mar ’12

2.4

Apr – Sep ’12 Oct ’12 – Mar ’13

N = 102

N = 37

N = 116

Apr – Sep ’13

N = 176

Oct ’13 – Mar ’14

N = 157

N = 115

1.6

0.8

0.0
0

20

0

20

0

20

0

20

0

20

0

20

Frequency (%)

2.0

1.0

Oct ’13
– Mar ’14

Apr
– Sep ’13

Oct ’12
– Mar ’13

Apr
– Sep ’12

Oct ’11
– Mar ’ 12

0.0
Apr
– Sep ’11

b

Cs concentration (134Cs + 137Cs;
log transformed; Bq/kg-wet)

Cs concentration (134Cs + 137Cs;
log transformed; Bq/kg-wet)

a

Fig. 11.2  Temporal changes in the (a) frequency distribution and (b) percentiles of the concentrations of Cs (134Cs + 137Cs; Bq/kg-wet) in Japanese flounder Paralichthys olivaceus from area VI,
April 2011–March 2014. Open bars in a indicate individuals with concentrations below the detection limit; the value of detection limit was used as the Cs concentration for these individuals. The
concentrations of detection limits differ among monitored data. N number of samples for each period

centiles, they were still higher than the concentrations before the accident (137Cs,
0.11–0.50 Bq/kg-wet during the period from 1984 to 1995; Kasamatsu and
Ishikawa 1997).
These features, along with the results of previous studies of Cs contamination in
the environment and in animals (Tsumune et al. 2012; Tateda et al. 2013; Wada
et al. 2013), suggest two contamination histories for Japanese flounder. In the first,
water released directly from the FNPP, which had extremely high Cs concentrations, contaminated the fish during a short period, probably from March to April
2011 (Tsumune et al. 2012). The spatial variation of the contamination intensity
was high; some fish were severely contaminated, whereas others were only slightly
contaminated. Second, consumption of bait fish contaminated with relatively low
concentrations of Cs led to longer-duration contamination compared to that caused
by the directly released water. All flounder can be expected to take up Cs from their
food, which indicates that the variation in Cs concentration among individual flounders resulting from Cs in food was smaller than the variation from the Cs in the
directly released water.

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Y. Kurita et al.

The first contamination history is supported by the large variation in Cs concentrations, even in the same area, and the occurrence of individuals with extremely
high Cs concentrations in 2011 (Figs. 11.1 and 11.2). These individuals apparently
were contaminated shortly after the accident, and the amount of additional contamination after that seems to have been relatively low. This history is also supported by
the coincidence of the spatial variation of the Cs concentrations in fish bodies and
the path of the extremely contaminated water released from the FNPP between 26
March and the end of April 2011; the high Cs concentrations in fish (Wada et al.
2013) and the path of the directly released water (Tsumune et al. 2012) were distributed along the coast to the south of the FNPP.
The second history is supported by the dynamics of the lower Cs concentrations, specifically the temporary increase in the lower percentiles in area VI and
the peaking of the lowest concentrations at around 200 days after the accident in
areas IV, V, and VI. These features indicate that all the fish were contaminated
through the food web because the highly contaminated water was present in the
study areas much earlier than the 200th day after the accident (Tsumune et al.
2012) and the contaminated water cannot explain the delayed peak (see also
Sect. 11.4).
We validated these histories by comparison of the Cs concentrations in fish from
different year-classes, that is, fish born before and after the accident (Sect. 11.3),
and by conducting model simulations (Sect. 11.4).

11.3  D
 ifference in Cs Concentrations Among Year-Classes
Born Before and After the Accident
On the basis of the contamination histories described in the preceding section, we
hypothesized that some of the individuals in the 2010 year-class and older would be
heavily contaminated by the directly released water and that, in contrast, all the
members of the 2011 year-class and younger would be less contaminated because
the latter group of fish has not been exposed to the directly released water, and their
main source of Cs contamination would have been their food, which contained Cs
at much lower concentrations than the directly released water.
To validate this hypothesis, we compared the Cs concentrations among year-­
classes during the period from 250 to 950 days after the accident. Fish were collected
in Sendai Bay (area III). Total length was measured, age was validated by otolith
analysis (Yoneda et al. 2007), and Cs concentrations in the muscle of individual fish
were measured individually. The muscle tissue specimens were packed tightly into
plastic cylindrical containers, and specific gamma rays emitted from 134Cs (605 and
796 keV) and 137Cs (662 keV) were measured with a high-purity germanium semiconductor detector (ORTEC; GEM30-70-LB-C, 1.85 KeV/1.33 MeV resolution)
with a multichannel analyzer. The concentrations of 134Cs and 137Cs were corrected
back to the date of sampling for physical decay.

145

Cs concentration (134Cs + 137Cs)
in muscle (Bq/kg-wet)

11  Radiocesium Contamination Histories of Japanese Flounder…

10 2

10

1

0

500
Days after the accident

1000

Fig. 11.3  Temporal changes in the concentrations of Cs (134Cs + 137Cs; Bq/kg-wet) in four year-­
classes of individual Japanese flounder Paralichthys olivaceus collected in area III (Sendai Bay).
Regression lines for each year-class (yc) excluding outliers (see text) are shown; p < 0.01 for solid
lines [2009 yc (thin line) and 2010 yc (bold line)] and p > 0.05 for broken lines [2011 yc (thin line)
and 2012 yc (bold line)]

As expected, the Cs concentrations in the fish from the 2009 and 2010 yearclasses varied widely, from 4.8 to 100.2 (0.68–2.00, log transformed) and from 1.3
to 118.8 (0.11–2.07, log transformed) Bq/kg-wet, respectively (Fig. 11.3). There
were some sporadic outliers (that is, fish with Cs concentrations outside the values
predicted by linear regression ± 2 SD). Except for these outliers, the Cs concentrations of each 2009 and 2010 year-class showed a decreasing tendency. In contrast,
the Cs concentrations in the fish from the 2011 and 2012 year-classes were less than
10 (1.0 log transformed) Bq/kg-wet, and there were no outliers (that is, concentrations more than 2 SD from the mean). The Cs concentrations in fish from these
year-classes between 644 and 841 days after the accident decreased in the order
2009 > 2010 > 2011 = 2012 year-class (Steel–Dwass test; p < 0.05).
Differences in Cs concentrations among the year-classes were likely the result of
differing exposures to the highly contaminated environment during the first few
months after the accident at the different ages (Fig. 11.4a). Japanese flounder switch
from eating mysids during the first year of life to eating bait fish as they age.
Therefore, fish from the 2009 year-class experienced the accident when they were
1 year and 9 months old, at which point they were feeding on bait fish. Fish in the
2010 year-class were only 9 months old at the time of the accident, and most of
them were inhabiting shallow areas (<20 m deep) and feeding on mysids until summer 2011, at which point they shifted to feeding on bait fish. Fish in the 2011 year-­
class were not born until 4 months after the accident.
The Cs concentrations in fish caught during the period from December 2012 to
June 2013 (644–841 days after the accident) from different year-classes are plotted
against TL in Fig. 11.4b; the plot shows clear differences between the 2010 and
2011 year-classes, even in the same size range (344–420 mm TL; U test, p < 0.01).
The major difference was that fish in the 2011 year-class were not exposed to the

146

Y. Kurita et al.

a

2009

2010

2011

2012

2013

2009 yc
2010 yc
2011 yc
accident

Cs concentration (134Cs +
(Bq/kg-wet)

137Cs)

b
100
2009 yc
2010 yc
2011 yc

50

0
300

400

500

600

Total length (mm)
Fig. 11.4  Comparison of the concentrations of Cs (134Cs + 137Cs; Bq/kg-wet) in three year-classes
of individual Japanese flounder Paralichthys olivaceus. (a) Scheme showing the birth time of
each year class (yc), the date of the FNPP accident, and the period during which the fish were collected (644–841 days after the accident; black bars). Japanese flounder feed on mysids during their
first year (gray bars) and then on bait fish (open and black bars). (b) Relationship between Cs
concentration and total length of individual Japanese flounder by year-class

directly released water during March–April 2011 and thus were not heavily contaminated. Differences between the 2010 and 2009 year-classes were also observed
within the overlapping size range (420–628 mm TL; U test, p < 0.01). Differences in
habitat and growth rate after the accident are the likely causes of these differences.

11.4  Simulation
In the preceding sections, we described two possible contamination histories: shortduration extremely severe contamination caused by directly released water containing
extremely high Cs concentrations, and long-duration relatively low-level contamination via the food chain. In this section, these two histories are tested by simulations.
Marine fish take up Cs both from seawater and from food in amounts that are
proportional to the Cs concentrations in the seawater and food, respectively. In addition, the amount of Cs excreted from the body of a fish is proportional to the Cs
concentration in the body. Therefore, the change in the Cs concentration in the body
of a fish can be described by the following equation:

147

11  Radiocesium Contamination Histories of Japanese Flounder…

dCb / dt = aCw + bCf − cCb



where Cb, Cw, and Cf indicate the Cs concentrations (Bq/kg-wet) in fish muscle (as
a proxy for the whole-body concentration), seawater, and food, respectively. The
coefficients a, b, and c designate the constant rates (day−1) of intake and excretion.
For simplicity’s sake, we ignored the effects of fish growth (Ugedal et al. 1995,
1997) and water temperature (Rowan and Rasmussen 1995), as well as the effect of
physical radioactive decay. Coefficients b and c are given by the following
equations:
b = DR × AR



c = ( ln 2 ) / BHL

where DR, AR, and BHL are daily food ration (kg food/kg body), the proportion of
Cs in food absorbed by the gastrointestinal tract, and the biological half-life of the
flounder (days), respectively.
In the simulation, we used the following seawater Cs concentrations (Fig. 11.5a):
high Cs concentration (seawater A), moderate Cs concentration (seawater B), and

102

10-2

b
102

Food

10

1

0

400

800

1200

Days after the accident

1

d

0
1

e

2009 yc (A+F)
3

10

137

1

c
Source ratio (food / total)

Cs; Bq/kg-wet)

104

Cs concentration (134Cs +

Cs concentration (134Cs +

137

Cs; Bq/kg-wet)

4

10

a

2

10

2009 yc (B+F)
0
1

f
2010 yc

0
1

g

10

2011 yc

0
1

h
2012 yc

1

0

400

800

Days after the accident

1200

0

0

400

800

1200

Days after the accident

Fig. 11.5  Simulation of the temporal changes in the concentrations of Cs (134Cs + 137Cs; Bq/kg-­
wet) in Japanese flounder Paralichthys olivaceus with different contamination histories and from
different year-classes. Temporal changes in Cs concentrations in seawater A and B (a) and in food
(bait fish and mysids) (b). (c) Temporal changes in simulated Cs concentrations for fish in the
2009, 2010, 2011, and 2012 year-classes. Also shown are Cs concentrations in fish in the 2009
year-class (yc) that took up Cs from seawater A and food (A + F), seawater B and food (B + F), and
seawater C and food (C + F). Ratios of Cs sources (food/total) are shown for the 2009 yc that took
up Cs from seawater A and food (A + F) (d) and from seawater B and food (B + F) (e), and for the
2010 (f), 2011 (g), and 2012 (h) year-classes

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Y. Kurita et al.

Cs concentration of zero (seawater C) during the first 100 days after the accident
and a moderate Cs concentration after the first 100 days that is common to all seawaters. The high Cs concentration for the initial 100 days was taken from the
coastal monitoring data off Iwasawa, which is 16 km south of the FNPP (Tsumune
et al. 2012; TEPCO 2014). As a proxy for moderately contaminated water, we used
a value that was 1/10 of the high concentration (see Fig. 3 in Tateda et al. 2013).
For the Cs concentrations in food consumed by fish ≥1 year old for six 6-month
periods from March 2011 to February 2014, we used values of 80, 40, 10, 5, 2, and
1 Bq/kg-wet, which were based on monitoring data for Japanese sand lance and
Japanese anchovy (bait fish) in the coastal waters off northern Fukushima Prefecture
(northern half of area IV) (Fisheries Agency 2014) (Fig. 11.5b). For fish younger
than 1 year old, we used food concentrations of 40, 20, 10, 5, 2, and 1 Bq/kg-wet
for the same 6-month periods; these values were based on data for mysids in the
same area (Sohtome et al. 2014). Fish in the 2009 year-class fed on bait fish
throughout the simulation period; the fish in the 2010 year-class fed on mysids
from March to August 2011 and then shifted to bait fish; and fish in the 2011 and
2012 year-classes fed on mysids during their first 12 months (Fig. 11.4). The coefficient for Cs intake from seawater (a) was set at 0.1 (approximately equal to the
value of 0.11 reported by Tateda et al. 2013). DR and AR were set at 0.02 (Kurita
et al., unpublished data) and 0.6 (between the value of 0.5 reported by Tateda et al.
2013 and the value of 0.78 reported by Kasamatsu et al. 2001), respectively. BHL
was set at 104 days so that the saturated Cs concentration in the fish body was
twice the Cs concentration in the food, which was the observed relationship
between the concentrations in fish body and food in the equilibrium state before
the accident (Kasamatsu and Ishikawa 1997).
In the simulations, we focused on three issues: variation of the Cs concentrations
among individuals, the influence of the contamination history during the initial
100 days, and differences in Cs concentrations among the year-classes.
First, the effect of Cs concentration in the seawater was evaluated (Fig. 11.5c–e).
The Cs concentrations in the fish body were simulated for fish in the 2009 year-­
class, which fed on bait fish and were exposed to seawater categories A, B, or
C. Differences in the Cs intake levels from seawater during the initial 100 days after
the accident produced large variations in the maximum Cs concentrations
(Fig.  11.5c): 109 Bq/kg-wet (2.04 log transformed; sources of Cs were seawater
C + food), 286 Bq/kg-wet (2.46 log transformed; seawater B + food), and 2,504 Bq/
kg-wet (3.40 log transformed; seawater A + food). For fish that were exposed to
directly released water (seawater A or B), the body Cs concentration peaked shortly
after the accident, at 43 days (23 April 2011) and at 50 days (30 April 2011) for
seawaters A and B, respectively, and then decreased rapidly. Even if fish did not take
up Cs from seawater during the initial 100 days (seawater C), the body Cs concentration increased to 109 Bq/kg-wet at 184 days (11 September 2011), which corresponds to the peak period of the lowest observed concentrations (as described in
Sect. 11.2). High individual variation and a gradual increase in the lowest concentrations until September were observed in the monitored data (Figs. 11.1 and 11.2).
Contamination from seawater A was greater than contamination from food during

11  Radiocesium Contamination Histories of Japanese Flounder…

149

the first 100 days after the accident and from seawater B during the first 50 days
after the accident (Fig. 11.5d, e). The actual observed maximum value, 4,500 Bq/
kg-wet, was comparable to the value obtained from the simulation.
Second, different exposures to contaminated seawater during the initial 100 days
after the accident influenced the Cs concentration in the fish body for a long time after
the accident. Specifically, the Cs concentrations in the bodies of fish that were exposed
to seawaters A, B, and C for the initial 100 days (until the middle of June 2011) were
47.6, 21.5, and 18.6 Bq/kg-wet, respectively, at 2 years after the accident and 6.5, 4.2,
and 4.0, respectively, at 3 years after the accident (Fig. 11.5c). These results indicate
that the Cs concentrations in fish exposed to the directly released seawater, especially
seawater A, have not been in the equilibrium state for more than 3 years.
Third, differences between year-classes were evaluated (Fig. 11.5c, f–h). Cs concentrations in fish bodies were simulated for the 2010, 2011, and 2012 year-classes
on the assumption that the fish fed on prey and were exposed to seawater B. Fish in
the 2010 year-class (purple line), which fed on mysids for the first 4 months after
the accident and then shifted to bait fish, showed a temporal variation in Cs concentration that was similar to that for the 2009 year-class (dark blue line). In contrast,
the Cs concentrations in the 2011 year-class (yellow line) and 2012 year-class (light
blue line) were clearly lower than those in the older fish. The maximum values were
32 (1.51 log transformed) and 8 (0.90 log transformed) Bq/kg-wet for the 2011 and
2012 year-class, respectively, and peak concentrations occurred at 254 days old for
both year-classes. Food was the greatest source of Cs for the 2011 and 2012 year-­
classes throughout their lives (Fig. 11.5g, h), which indicates less individual variation than in the older fish that were exposed to directly released water. The observed
data for the year-classes (Fig. 11.3) were in agreement with the simulated results;
that is, lower concentrations and less variability were observed for the 2011 and
2012 year-classes than for the older year-classes.
The observed features were reproduced by the simulations under the condition of
the two possible contamination histories: fish were contaminated both by exposure
to directly released seawater containing extremely high Cs concentrations, that
showed high spatial variability and drastically decreased after May 2011, and by
exposure via food, in which the Cs concentration was much lower than that in seawater and decreased slowly. The values of additional parameters should be evaluated in future quantitative studies. In particular, the effects of fish size and water
temperature, as well as the effects of growth on the accumulation or dilution of Cs
(growth accumulation/dilution), are critical because Japanese flounder grow fast
and inhabit water with a wide range of temperatures.

11.5  Conclusions
Observed Cs concentration data showed high variation among individual fish, peaks
in the lowest concentrations in autumn 2011 for the 2010 year-class and older fish,
and lower concentrations with less variation for the 2011 year-class and younger

150

Y. Kurita et al.

fish. We suggest two major Cs contamination histories. The first involved contamination by directly released highly contaminated water during March and April in
2011. The Cs concentrations in this water showed high spatial variability, and the
effects of seawater decreased drastically after the first few months following the
FNPP accident. The other history involved contamination from food: mysids for
fish younger than 1 year and bait fish for older fish. The maximum Cs concentrations in food were very low compared to those in the directly released water and
decreased slowly. The existence of these two contamination histories was supported
by simulation studies. These histories seem to be common to many other fish species (Tateda et al. 2013; Wada et al. 2013; Narimatsu et al. 2014).
The observation of major effects resulting from directly released seawater during
the initial few months after the accident is characteristic of the FNPP accident. Most
fish that showed high Cs concentrations in 2012 and later were likely to have taken
up Cs in the initial few months after the accident but are currently taking up little Cs
from food and are excreting Cs continuously. Therefore, it is important to recognize
that the observed high Cs concentrations in some individuals may not have reached
an equilibrium state, and the Cs concentrations in these individuals do not necessarily indicate the current intensity of contamination from the environment, but rather
reflect contamination during the first few months after the accident.
On the basis of the proposed histories of contamination, the intensity of contamination should be low after the first few months following the accident. Even old fish
that were exposed to the directly released water currently show low Cs concentrations, below the regulatory value for fish products, 100 Bq/kg-wet. In addition, the
abundance of fish in the 2010 year-class and older is decreasing as these fish age and
die. Therefore, the Cs concentrations in most fish will continue to decrease to less
than 20 Bq/kg-wet, which is the present concentration (as of March 2014) in most
of the 2010 year-class and older fish and all of the 2012 year-class and younger fish.
The only potential problem is that individuals inhabiting the port in front of the
FNPP still show higher Cs concentrations than those of fish inhabiting outside the
port (Shigenobu et al. 2014; TEPCO 2014), which indicates that intense contamination is still occurring in the port, although the number of these fish is negligible relative to the overall stock in this area.
Acknowledgments We are grateful to Kaoru Nakata and Adriaan Rijnsdorp for their valuable
comments on an earlier version of this manuscript. We also thank Takami Morita, Yoji Narimatsu,
Takuji Mizuno, and Tadahiro Sohtome for discussions and useful information. Thanks are also due
to Hiroyuki Togashi, Yukinori Nakane, Yosuke Amano, and Tsuyoshi Tamate for their assistance in
sampling fish and discussions. The crew of the R/V Wakataka-maru and the fishing vessels Seikomaru and Daiei-maru are appreciated for assistance with fish sampling.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

11  Radiocesium Contamination Histories of Japanese Flounder…

151

References
Fisheries Agency, Ministry of Agriculture, Forestry and Fisheries (2014) Results of the inspection
on radioactivity materials in fisheries products. http://www.jfa.maff.go.jp/e/inspection/index.
html. Accessed on 31 May 2014
Kasamatsu F, Ishikawa Y (1997) Natural variation of radionuclide 137Cs concentration in marine
organisms with special reference to the effect of food habits and trophic level. Mar Ecol Prog
Ser 160:109–120
Kasamatsu F, Nakamura M, Nakamura R, Suzuki Y, Kitagawa D (2001) Estimation of daily feeding rate of Japanese flounder Paralichthys olivaceus taken off Pacific coast of Aomori
Prefecture by a radioisotope method. Nippon Suisan Gakkaishi 67:500–502
Kurita Y, Tamate T, Ito M (2014) Stock assessment and evaluation for Japanese flounder, north
Pacific stock (fiscal year 2013). In: Marine fisheries stock assessment and evaluation for
Japanese waters (fiscal year 2013/2014). Fisheries Agency and Fisheries Research Agency of
Japan, Tokyo, pp 1373–1398 (in Japanese)
Narimatsu Y, Sohtome T, Yamada M, Shigenobu Y, Kurita Y, Hattori T, Inagawa R (2014) Why do
the radionuclide concentrations of Pacific cod depend on the body size? In: Nakata K, Sugisaki
H (eds) Impact of the Fukushima nuclear accident on fish and fishing grounds. Springer, Berlin
(chapter 10 in this volume)
Rowan DJ, Rasmussen JB (1995) Bioaccumulation of radiocesium by fish: the influence of physicochemical factors and trophic structure. Can J Fish Aquat Sci 51:2388–2410
Shigenobu Y, Fujimoto K, Ambe D, Kaeriyama H, Ono T, Morinaga K, Nakata K, Morita T,
Watanabe T (2014) Radiocesium contamination of greenlings (Hexagrammos otakii) off the
coast of Fukushima. Sci Rep 4:6851
Sohtome T, Wada T, Mizuno T, Nemoto Y, Igarashi S, Nishimune A, Aono T, Ito Y, Kanda J,
Ishimaru T (2014) Radiological impact of TEPCO’s Fukushima Dai-ichi Nuclear Power Plant
accident on invertebrates in the coastal benthic food web. J Environ Radioact 138:106–115
Tateda Y, Tsumune D, Tsubono T (2013) Simulation of radioactive cesium transfer in the southern
Fukushima coastal biota using a dynamic food chain transfer model. J Environ Radioact
124:1–12
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index-e.html. Accessed on 30 May 2014
Tomiyama T, Kurita Y (2011) Seasonal and spatial variations in prey utilization and condition of a
piscivorous flatfish Paralichthys olivaceus. Aquat Biol 11:279–288
Tsumune D, Tsubono T, Aoyama M, Hirose K (2012) Distribution of oceanic 137Cs from the
Fukushima Dai-ichi Nuclear Power Plant simulated numerically by a regional ocean model. J
Environ Radioact 111:100–108
Ugedal O, Forseth T, Jonsson B, Njåstad O (1995) Sources of variation in radiocaesium levels
between individual fish from a Chernobyl contaminated Norwegian lake. J Appl Ecol
32:352–361
Ugedal O, Forseth T, Jonsson B (1997) A functional model of radiocesium turnover in brown trout.
Ecol Appl 7:1002–1016
Wada T, Nemoto Y, Shimamura S, Fujita T, Mizuno T, Sohtaome T, Kamiayama K, Morita T,
Igarashi S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ
Radioact 124:246–254
Yoneda M, Kurita Y, Kitagawa D, Ito M, Tomiyama T, Goto T, Takahashi K (2007) Age validation
and growth variability of Japanese flounder Paralichthys olivaceus off the Pacific coast of
northern Japan. Fish Sci 73:585–592

Part IV

Mechanisms of Severe Contamination
in Fish

Chapter 12

Evaluating the Probability of Catching Fat
Greenlings (Hexagrammos otakii) Highly
Contaminated with Radiocesium off the Coast
of Fukushima
Yuya Shigenobu, Ken Fujimoto, Daisuke Ambe, Hideki Kaeriyama,
Tsuneo Ono, Takami Morita, and Tomowo Watanabe

Abstract On 1 August 2012, a total of 25,800 Bq/kg-wet of radiocesium
(134Cs = 9,800 Bq/kg-wet, 137Cs = 16,000 Bq/kg-wet) was detected in the muscle tissue of two fat greenlings (Hexagrammos otakii) caught approximately 20 km north
of the Fukushima Dai-ichi Nuclear Power Plant (FNPP). To estimate the contamination level of this fish species off the coast of Fukushima, we measured the radiocesium concentration in the muscle tissue of individual fat greenlings in 2012 and
2013. Radiocesium concentration of fat greenlings caught in southern coastal waters
from the FNPP was significantly higher than that of fat greenlings collected in other
waters off the coast of Fukushima. However, fat greenlings with a radiocesium concentration greater than 10,000 Bq/kg-wet were not detected, not even from highly
contaminated areas. In addition, data obtained from specimens collected off the
coast of Fukushima from April to December 2012 suggested that the probability of
catching fat greenlings with a concentration greater than 16,000 Bq/kg-wet of 137Cs
was exceedingly low (less than 2.794 × 10−6). In contrast, highly contaminated fat
greenlings were frequently caught within the FNPP port. The geometric mean of
137
Cs was 55,400 Bq/kg-wet, as calculated from specimens obtained during
December 2012 to May 2013. Our investigation suggests that fat greenlings with an
extremely high concentration of radiocesium were contaminated within the FNPP
port and then migrated offshore.
Keywords Fat greenling • Marine products • High contamination • Radiocesium
• Probability
Y. Shigenobu (*) • K. Fujimoto • D. Ambe • H. Kaeriyama • T. Ono • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: yshig@affrc.go.jp
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_12

155

156

12.1

Y. Shigenobu et al.

Introduction

Immediately after the Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident in
March 2011, high concentrations of radiocesium (134Cs and 137Cs) were detected in
several specimens of marine products off the coast of Fukushima (Ministry of
Agriculture, Forestry and Fisheries 2014). In April 2011, a concentration of
12,500 Bq/kg-wet and 14,400 Bq/kg-wet of radiocesium was detected in whole-fish
specimens of Japanese sand lance (Ammodytes personatus) collected approximately
30 km south of the FNPP. These extremely high concentrations in coastal pelagic
fish species were caused from their direct exposure to highly contaminated seawater
(Bailly et al. 2012; Oikawa et al. 2013). It is known that cesium absorbed by marine
organisms is excreted by their potassium ion transport system during osmoregulation (Furukawa et al. 2012; Kaneko et al. 2013). Therefore, a rapid decrease in the
radiocesium concentration of seawater would reduce contamination of marine
organisms, especially for pelagic fish species (Buesseler 2012; Wada et al. 2013).
Temporal trends in radiocesium concentration of marine organisms off the coast of
Fukushima gradually declined after the summer of 2011 (Wada et al. 2013). Marine
organisms with a radiocesium concentration greater than 10,000 Bq/kg-wet were
not reported until 1.5 years after April 2011. On 1 August 2012, however, a total of
25,800 Bq/kg-wet of radiocesium (134Cs = 9,800 Bq/kg-wet; 137Cs = 16,000 Bq/kgwet) was detected in the muscle tissue of two fat greenlings (Hexagrammos otakii)
caught approximately 20 km north of the FNPP (Tokyo Electric Power Corporation
2012a). Although Tokyo Electric Power Corporation (2012b) had carried out an
intensive investigation within the 20-km radius from the FNPP port, such a highly
contaminated fish had not been caught until that point, and the reason for this
extremely high level of contamination remains unclear.
Fat greenling is a coastal demersal fish species that lives by preying on benthic
organisms. A previous tagging study suggested that the migration distance of fat
greenling was restricted within an area of approximately 30-km radius (Fukushima
Prefectural Fisheries Experimental Station FPFES 1974). It is assumed that in
highly contaminated areas, as is the zone within and around the FNPP port, sedentary demersal fish species continuously receive radiocesium through the benthic
food web more constantly than migratory demersal fish species such as Japanese
flounder (see Chap. 11) and Pacific cod (see Chap. 10). In this section, we measured
radiocesium concentration in the muscle tissue of individual fat greenlings caught
off the coast of Fukushima to estimate the contamination level in this fish species.
In addition, we attempted to calculate the probability that 137Cs concentration
exceeds 16,000 Bq/kg-wet in fat greenlings collected off the coast of Fukushima
from April 2012 to March 2013, using our original data in combination with datasets published by the Ministry of Agriculture, Forestry and Fisheries (MAFF) and
TEPCO (2014).

12

Evaluating the Probability of Catching Fat Greenlings (Hexagrammos otakii)…

12.2

157

Radiocesium Contamination of Fat Greenlings off
the Coast of Fukushima

From May 2012 to March 2013, we collected 236 fat greenlings in northern (approximately 50 km north of the FNPP) and southern (approximately 40 km south of the
FNPP) waters (Fig. 12.1). Radiocesium concentration was measured as described
by Shigenobu et al. (2014). Fat greenlings caught from the northern waters had a
relatively lower radiocesium concentration than those collected from the southern
waters (Table. 12.1). In the southern waters, the level of contamination was significantly higher (p < 0.001) in coastal waters, at depth less than 30 m (geometric mean,
128 Bq/kg-wet) than in offshore waters, at depth greater than 50 m (geometric
mean, 28.4 Bq/kg-wet). The highest radiocesium concentration detected was
1,070 Bq/kg-wet in a fat greenling collected from the southern coastal waters on 20
May 2012. In this study, none of the fish specimens had a radiocesium concentration
higher than 10,000 Bq/kg-wet weight.
Figure 12.2 shows the time-series trend of radiocesium concentration of fat
greenlings caught within the FNPP port and off the coast of Fukushima from May

Fig. 12.1 Fat greenlings were collected from several sampling locations. The gray circle indicates
a sampling area of approximately 20-km radius around the Fukushima Dai-ichi Nuclear Power
Plant (FNPP), and the black spot indicates the sampling point, where fat greenlings with a
25,800 Bq/kg-wet radiocesium concentration were caught on 1 August 2012

158

Y. Shigenobu et al.

Table 12.1 Radiocesium concentrations in individual fat greenlings off the coast of Fukushima

Sampling area
Northern coastal waters (at depth less
than 30 m)
Northern offshore waters (at depth
more than 50 m)
Southern coastal waters (at depth less
than 30 m)
Southern offshore waters (at depth
more than 50 m)

Number of
individuals
30
54
68
84

134
Cs + 137Cs concentration
(Bq/kg-wet)
Range
Geometric
Min.
Max.
meana
4.46
39.2
13.1

n.d.
(<4.24)
n.d.
(<5.31)
n.d.
(<3.28)

193
1,070
987

21.9
128
28.4

a

Detection limit was used for the calculation of geometric mean in samples in which radiocesium
was not detected (n.d.)

Fig. 12.2 Temporal trend of radiocesium concentration (134Cs + 137Cs) in fat greenlings caught
within and outside an area of approximately 20-km radius around the Fukushima Dai-ichi Nuclear
Power Plant (FNPP). Tokyo Electric Power Corporation (2012b) has been monitoring marine
organisms within an area of 20-km radius around FNPP since April 2012

12

Evaluating the Probability of Catching Fat Greenlings (Hexagrammos otakii)…

159

2011 to May 2013, using our original data and datasets published from MAFF and
TEPCO. Radiocesium concentration of fat greenlings caught off the coast of
Fukushima gradually declined over time. Except for the datasets of fat greenlings
collected within the FNPP port, radiocesium concentration exceeded the Japanese
threshold (100 Bq/kg-wet) in 76.3 % and 41.2 % of specimens caught off the coast
of Fukushima in 2011 and 2012, respectively. In particular, geometric means were
209 Bq/kg-wet in specimens collected from April to December 2011 and 77.2 Bq/
kg-wet in those collected from April to December 2012.
Previous studies have reported that radiocesium concentration in marine organisms (Wada et al. 2013) and sediments (Ambe et al. 2014) within the southern
coastal area of FNPP was comparatively higher than those in other areas. However,
according to our data and published datasets from MAFF and TEPCO, fat greenlings with a radiocesium concentration greater than 10,000 Bq/kg-wet were not
identified, not even in specimens collected from highly contaminated areas. This
circumstantial evidence suggests a low probability of catching extremely highly
contaminated fat greenling off the coast of Fukushima. Our field investigation and
laboratory-rearing experiments of a benthic polychaete in highly contaminated sediment suggests that radiocesium intake from contaminated sediments is limited for
benthic organisms and demersal fish species (see Chap. 7). Progressive simulation
analysis of the contamination mechanism in fat greenling off the coast of Fukushima
is presented in Chap. 13.

12.3

Site of Contamination of the Highly Contaminated Fat
Greenling

Data of 137Cs concentration in fat greenling specimens collected off the coast of
Fukushima from April to December 2012 were log-transformed. A normal distribution curve of log-transformed values was used to calculate the probability of catching fat greenlings with a137Cs concentration greater than 16,000 Bq/kg-wet
(log-transformed value of 4.204) as shown in Fig. 12.3. Values below the detection
limit of 137Cs were excluded from this analysis to obtain a more conservative estimate. Normality of the log-transformed values from the combined datasets was confirmed. Arithmetic mean ± standard deviation of log-transformed 137Cs concentration
was 1.676 ± 0.5567. The calculated probability of catching fat greenlings with a
concentration greater than 16,000 Bq/kg-wet of 137Cs was below 2.794 × 10−6. This
very low value strongly suggests that fat greenlings off the coast of Fukushima from
April to December 2012 did not include any highly contaminated individuals.
In contrast, the level of radiocesium contamination in fat greenlings caught in the
FNPP port from December 2012 to May 2013 was extremely high. The geometric
mean was 55,400 Bq/kg-wet and ranged from 1,030 to 740,000 Bq/kg-wet. Kanda
(2013) reported that the average values of 137Cs concentration in seawater samples
collected from the intake canal area of Units 1–4 of the FNPP from June to August
2011 ranged between 305 and 1,650 Bq/l. Concentration ratio (CR) of the 25,800 Bq/

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Y. Shigenobu et al.

Fig. 12.3 Probability of catching contaminated fat greenlings off the coast of Fukushima. The
normal distribution curve was constructed using log-transformed 137Cs concentration in specimens
collected from April to December 2012. Black spot indicates the 16,000 Bq/kg-wet 137Cs concentration. The probability of catching fat greenlings with a 137Cs concentration greater than 16,000 Bq/
kg-wet was less than approximately 2.794 × 10−6

kg-wet (137Cs of 16,000 Bq/kg-wet) fish specimens to the seawater from the intake
canal area of Units 1–4 was between 9.70 and 52.5 for the period of June to August
2011. These results were consistent with previous findings that CR of 137Cs between
demersal fish species and seawater around Japan ranged from 15 to 54 (Tagami and
Uchida 2013). The results also indicated that the contamination level within the
FNPP was much higher immediately after the FNPP accident. Accordingly, for a
period of several months after the FNPP accident, the radiocesium contamination
level of fat greenlings within the FNPP port was never less than 25,800 Bq/kg-wet.
Although the site where the extremely contaminated fat greenlings were caught was
20-km away from FNPP, this distance is within the possible migration distance for
this species (FPFES 1974). Therefore, it is assumed that the extremely contaminated fat greenlings had been exposed to highly contaminated seawater over a certain period of time after the accident within or near the FNPP port before they
migrated offshore.
Acknowledgments This section is based on the article entitled “Radiocesium contamination of
greenlings (Hexagrammos otakii) off the coast of Fukushima” published in the open access journal
of Scientific Reports (doi: 10.1038/srep06851). The authors wish to thank all the fishery workers in

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161

Fukushima Prefecture who collected the greenlings for this study. We also thank all the members
of our research group for their assistance with specimen preparation. This study was supported by
the Fisheries Agency, the Ministry of Agriculture, and the Forestry and Fisheries of Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
Ambe D, Kaeriyama H, Shigenobu Y, Fujimoto K, Ono T, Sawada H, Saito H, Miki S, Setou T,
Morita T, Watanabe T (2014) Five-minute resolved spatial distribution of radiocesium in sea
sediment derived from the Fukushima Dai-ichi Nuclear Power Plant. J Environ Radioact
138:264–275
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source-term following Fukushima Daiichi accident. J Environ Radioact 114:2–9
Buesseler KO (2012) Fishing for answers off Fukushima. Science 338:480–482
Fukushima Prefectural Fisheries Experimental Station (FPFES) (1974) Research report of resource
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potassium-transporting pathway in Mozambique tilapia. Fish Sci 78:597–602
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Watanabe T (2014) Radiocesium contamination of greenlings (Hexagrammos otakii) off the
coast of Fukushima. Sci Rep 4. doi:10.1038/srep06851
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S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ Radioact
124:246–254

Chapter 13

Analysis of the Contamination Process
of the Extremely Contaminated Fat Greenling
by Fukushima-Derived Radioactive Material
Tomowo Watanabe, Ken Fujimoto, Yuya Shigenobu, Hideki Kaeriyama,
and Takami Morita
Abstract  We analyzed the contamination process by which the fat greenling,
which was caught in the area off the mouth of the Ota River of Fukushima prefecture on August 1, 2012, concentrated radiocesium (134Cs + 137Cs) to the level of
25,800 Bq/kg-wet. The radioactivity environment of the area was insufficient to
maintain or increase the radiocesium concentration in the fish at the time. Distribution
of the radioactive materials in the otolith of the fat greenling estimated by beta-ray
emissions suggested that the fat greenling was in a highly contaminated environment during the period immediately following the Fukushima Dai-ichi Nuclear
Power Plant (FNPP) accident. We used a biokinetic simulation of the 137Cs concentration to demonstrate that the fat greenling had to have been exposed to radioactivity
from the FNPP to achieve such a high radiocesium concentration. Thus, the extremely
contaminated fat greenling originated in the heavily contaminated environment of
the FNPP port or the adjoining area in the period just after the accident.
Keywords Fat greenling • Contamination • Radiocesium • Autoradiography

13.1  Introduction
Radioactive nuclides leaked from the Fukushima Dai-ichi Nuclear Power Plant
(FNPP), operated by Tokyo Electric Power Company (TEPCO), when it was
damaged by the tsunami following the Tohoku Earthquake on March 11, 2011.
The United Nations Scientific Committee on the Effects of Atomic Radiation
T. Watanabe (*)
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
K. Fujimoto • Y. Shigenobu • H. Kaeriyama • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_13

163

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(UNSCEAR 2013) estimated the scale of the release of several radioactive nuclides:
the range for radioactive iodine (131I) was from 100 to 500 petabecquerel (PBq) and
the range for radiocesium (137Cs) was from 6 to 20 PBq. The committee noted that
the amounts of released radioactive nuclides were much lower than that which
occurred after the Chernobyl accident (the FNPP accident released 20 % of the 137Cs
levels released after Chernobyl). The remarkable feature of the FNPP accident was
the swift and direct release of highly polluted water to the ocean. Coastal area of
Fukushima and adjacent prefectures were covered with seawater bearing high concentrations of 131I and radiocesium (134Cs and 137Cs) after the accident. The direct
leakage of 137Cs was estimated as 3.5 PBq and the highest seawater concentration
(>6 × 104 Bq/l) was observed at the coast near the FNPP (Tsumune et al. 2012). This
value was seven orders of magnitude higher than the pre-accident levels.
The Ministry of Agriculture, Forestry and Fisheries (MAFF) and local government initiated emergency monitoring of radioactivity in marine products immediately after the accident to ensure food safety. Their findings were published on the
websites of MAFF (2014) and of the Ministry of Health, Labor and Welfare (MHLW
2014). The Fisheries Research Agency (FRA) supported the measurement of radioactivity in marine products. In April 2011, extremely high levels of 131I and radiocesium (134Cs + 137Cs; >1.0 × 104 Bq/kg-wet) were reported in sand lance larvae. Such
high contamination levels were confined to larvae of pelagic fish in the area south of
the FNPP and were thought to result from the spread of contaminated water after the
accident (Tateda et al. 2013). After that, 131I contamination levels decreased rapidly,
consistent with its short half-life (about 8.02 days), and returned to the levels below the
limit of detection (hereinafter referred to as ND) after August 2011 (Wada et al. 2013).
The relatively longer half-life of 134Cs (about 2.07 years) and 137C (about 30.1 years)
caused them to remain in the marine environment for much longer; monitoring of
radiocesium in the marine environment and marine products has continued.
Cesium is an alkali metal that is metabolized by the same pathway that metabolizes potassium, which is an essential mineral (Kaneko et al. 2013). As are other
alkali metals, radiocesium is exchanged between the environment and body of
marine teleost fish by their osmoregulatory systems, which maintain electrolyte balance (Evans 2010). Thus, radiocesium concentrations in the fish depend on the concentrations in the surrounding seawater. Wada et al. (2013) showed continuous
reduction in radiocesium concentrations in marine products obtained off the coast
of Fukushima Prefecture; the ecological half-life of radiocesium is much shorter
than the physical half-lives of 134Cs and 137Cs.
TEPCO began to monitor radioactivity in marine fishes within a 20-km radius of
FNPP (hereinafter referred to as the 20-km area) in March 2012. Against the
decreasing trend of radiocesium in marine products, extremely high radiocesium
concentrations were detected in Hexagrammos otakii (fat greenling) in the summer
of 2012. The fat greenlings were caught about 1 km offshore near the mouth of the
Ota River on August 1, 2012 (Chap. 12). The reported radiocesium (134Cs + 137Cs)
level was 25,800 Bq/kg-wet (TEPCO 2012a), the highest radiocesium concentration found in marine fishes at the time. An additional survey of fat greenlings in the
area was conducted by TEPCO from September to October 2012, during which
time 57 samples were examined (TEPCO 2012b). Most of the surveyed greenlings

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showed radiocesium concentrations two orders of magnitude lower than that of the
fat greenling caught in the area off the mouth of the Ota River on August 1, 2012.
Radiocesium concentrations ranged from ND to 1,350 Bq/kg-wet (median, 77 Bq/
kg-wet), equivalent to the levels found in samples taken outside the 20-km area.
TEPCO’s research on marine fish in the port of FNPP beginning in October 2012
showed highly contaminated fish species, including fat greenlings, with radiocesium concentrations exceeding 10,000 Bq/kg-wet (TEPCO 2014a). Statistical analysis of the data from fat greenlings showed that the probability of finding fat
greenlings with 137Cs concentrations exceeding 16,000 Bq/kg-wet was below
3.0 × 10−6, suggesting their radioactive exposure history was similar to that of the
population in the port of FNPP (Shigenobu et al. 2014, Chap. 12).
The purpose of this study was to determine the contamination process of fat
greenling by performing a quantitative analysis. We evaluated the radioactivity of the
marine environment and the potential for generating highly contaminated fat greenlings. Analysis of fat greenling otoliths revealed the radioactive exposure history of
the fish, the progress of which was examined by biokinetic model simulations.

13.2  137
 Cs Concentrations in Coastal Seawater and Marine
Fish off the Coast of Fukushima Prefecture
Daily observed 137Cs concentrations in seawater sampled at TEPCO’s monitoring
stations around FNPP and the Fukushima Dai-ni Nuclear Power Plant (TEPCO
2014b) were used to evaluate radioactivity in the coastal areas of Fukushima
Prefecture. Station locations are indicated in Fig. 13.1. The station at the shallow
draft quay in the port of FNPP (hereinafter referred to as site-FP) was selected for
the FNPP port; the northern side of the discharge channel for units 5–6 of FNPP
(T-1) and the south discharge channel of FNPP, including stations T-2 and T-2-1,
were selected to represent areas outside the FNPP port. The station at the north
discharge channel of the Fukushima Dai-ni Nuclear Power Plant (T-3) and stations
south thereof, around the Iwasawa shore (T-4), the north side of the Asami River
(T-4-1), and the south side of the Kitasako River (T-4-2), were also chosen. To represent the average 137Cs concentration in the area outside the FNPP port (site-F1),
data were averaged from T-1, T-2, and T-2-1. Averages were also generated for T-3,
T-4, T-4-1, and T-4-2 to represent seawater around the Fukushima Dai-ni Nuclear
Power Plant (site-F2). Thus, three daily time-series of 137Cs concentrations were
generated for the period from March 21, 2011 to August 31, 2014. These values
were used for the simulation of 137Cs concentrations in fat greenling.
Data points of ND were interpolated to produce continuous daily data. ND data
during several days at site-FP were interpolated by using the minimum values obtained
in the 15 days around the target day; longer consecutive ND periods were filled with
values calculated from data obtained at other station in the port by ­regression analysis.
ND data in the site-F1 and site-F2 time-series were filled in the same way.
Figure  13.2 shows the variations in seawater 137Cs concentration at the three
sites. High 137Cs concentrations were simultaneously detected at all three stations

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Fig. 13.1 Locations of radiocesium monitoring stations along the coast of Fukushima prefecture.
Site-FP represents the station at the shallow draft quay in the Fukushima Dai-ichi Nuclear Power
Plant (FNPP) port. Stations T-1, T-2, and T-2-1 are adjacent to the FNPP port and are referred to as
site-F1. Stations T-3, T-4, T-4-1, and T-4-2 are located around the Fukushima Dai-ichi Nuclear
Power Plant and southward, referred to as site-F2. Station T-S1 is the collection point for the
extremely contaminated fat greenling exhibiting 25,800 Bq/kg-wet radiocesium (134Cs + 137Cs)

Fig. 13.2  Combined time-series of observed and interpolated daily 137Cs concentration data at
site-FP, site-F1, and site-F2 from March 21, 2011, to August 31, 2014

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from late March to the beginning of April 2011. Peak values were 6.6 × 105 Bq/l at
site-FP, 2.4 × 104 Bq/l at site-F1, and 1.4 × 103 Bq/l at site-F2; values this high have
never before been observed in the marine environment (Tsumune et al. 2012; Baxter
and Camplin 1993; IAEA 2005; HELCOM 2009). Accumulated values for the
period from March 21, 2011 to July 31, 2012, when the fat greenling was thought to
be affected by contamination off the coast of Fukushima Prefecture, were as high as
5.4 × 106 Bq/l at site-FP, 2.2 × 105 Bq/l at site-F1, and 1.8 × 104 Bq/l at site-F2. These
accumulated values were indicative of the direct load of radioactivity in the ecosystem at each site. In addition, accumulation curves of 137Cs concentrations of each
sites indicated sharp increase during the early days and reached 90 % of accumulated values of July 31, 2012 in first 20 (site-FP), 21 (site-F1), and 45 (site-F2) days.
137
Cs concentration data for fat greenlings in the coastal waters of Fukushima
Prefecture were extracted from the dataset published by MHLW (2014) and from
TEPCO data reports for the 20-km area and the FNPP port (TEPCO 2014a). Time-­
series for fat greenlings in the coastal waters of Fukushima and for the 20-km area
indicate similar decreasing trends beginning in the spring of 2012 (Fig. 13.3). The
median and the 95th percentile values were calculated from the combined data set
of both for each 6-month period beginning March 1, 2011. Ecological half-lives
calculated from these values for the period from March 2012 to August 2014 were
175 days for 95th percentile and 194 days for median. The values were slightly
lower than the results for fat greenlings (217 days) collected from the southern area
off the coast of Fukushima Prefecture between August 2011 and September 2012
(Tateda et al. 2013). The difference reflected the variation in analytical period.

Fig. 13.3  Temporal trends of observed 137Cs concentrations in fat greenlings caught in the coastal
waters of Fukushima Prefecture, except the 20-km area and in the 20-km area with median values
and 95th percentile values calculated from combined data of both for each 6-month period. The
first term includes data from March 1, 2011 to August 31, 2011

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13.3  T
 he Marine Environment as a Source of Radioactive
Contamination of the Fat Greenling
We sought to determine whether the observed radioactivity in the environment in
the summer of 2012 could maintain radiocesium (134Cs + 137Cs) concentrations of
25,800 Bq/kg-wet in the fat greenling. Marine fish obtain radiocesium from the
environment via uptake of food and water. 137Cs concentrations in marine fish
directly correlate with the concentrations in seawater under stable conditions
(Kasamatsu 1999; IAEA 2004), expressed as the concentration factor (CF).
Kasamatsu (1999) summarized the CFs of 137Cs for 27 species of marine teleost fish
around Japan. The CFs were calculated from data obtained between 1984 and 1996;
the average CF value for each fish species ranged from 22 to 122. The IAEA-­
recommended CF value of 100 for marine fish lies within this range (IAEA 2004).
We estimated the CF for fat greenling off the coast of Fukushima prefecture from 29
measures obtained in 1982–2010, archived, and published by the NRA (Nuclear
Regulation Authority 2014). The average CF was 67 ± 29, also within the range
described by Kasamatsu (1999).
The CF value for fat greenling off the coast of Fukushima suggested that the surrounding seawater should contain 137Cs concentrations of 240 Bq/l to maintain a
137
Cs concentration of 16,000 Bq/kg-wet (25,800 Bq/kg-wet for 134Cs + 137Cs) in the
fish. In August 2012, the 137Cs concentration of seawater was less than 0.1 Bq/l off
the coast of Fukushima Prefecture; the highest values observed in the FNPP port
were also less than 100 Bq/l (TEPCO 2014b). TEPCO (2012b) also reported values
much lower than 0.1 Bq/l in samples obtained around the Ota River.
We also considered the possibility that excretion of 137Cs from the fish was compensated for by ingestion of prey. Assuming a biological half-life of 100 days
(World Health Organization and Food and Agriculture Organization of the United
Nations 2011), the daily excretion rate was calculated as 0.0069 day−1 and the daily
amount of 137Cs excreted from the fat greenling was 110 Bq/kg-wet. Assuming an
ingestion rate of 0.03 day−1 and assimilation rate of 0.5 (Tateda 1997), the fat greenling would have to consume more than 7,300 Bq/kg-wet 137Cs daily to compensate
for excretion. The 137Cs concentrations in the marine biota within the 20-km area
were ND to 1,000 Bq/kg-wet (TEPCO 2014a), far below the required level.
Thus, the status of environmental 137Cs contamination in the area off the Ota
River and in the 20-km area were insufficient to maintain the 16,000 Bq/kg-wet
137
Cs concentration observed in the fat greenling, which were then assumed to be
excreting excess radiocesium.

13.4  R
 adioactivity in the Otolith of Contaminated Fat
Greenling
The fish otolith is a hard tissue that retains information on the age of the fish and the
history of its environment, including temperature, salinity, and chemical composition (Campana 1999). The fish otolith consists mostly of calcium carbonate and

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169

other elements that indicate environmental exposure. For example, strontium is
often used as an indicator of environmental salinity (Tsukamoto et al. 1998).
Radioactive materials absorbed in the otolith are also used as indicators of environmental conditions. Baker and Wilson (2001) showed that the otolith core of red
snapper from the Gulf of Mexico contains 14C produced by nuclear testing. We
analyzed the radioactive nuclides contained in the otolith of the fat greenling to
characterize its history of radioactive exposure.
Contaminated fat greenling with radiocesium (134Cs + 137Cs) concentrations of
25,800 Bq/kg-wet were caught from the area off the mouth of the Ota River and
inspected for radioactivity by TEPCO, which provided the fish remnants from
which the otoliths were extracted (Fig. 13.4). Radiation emitted from the otolith was
measured with a germanium semiconductor detector for gamma-emitting nuclides
and with a gas flow radiation counter for beta-emitting nuclides. Significant beta-­
ray emission was detected and gamma-ray emission was not detected (Fujimoto
et al. 2013). Autoradiography was performed with imaging plates (IP) to visualize
the distribution of radiation scatter from the sample materials.
We mounted a thin slice of the otolith on a glass slide and placed it on an IP
(BAS-MS 2025; Fuji Film) for 13 days. The reaction strength to beta-ray emission

Fig. 13.4  Otolith of the fat greenling (a) and its slice (b). The otolith in this figure was extracted
from the right side of the fat greenling’s head. The slice was cut from the left-hand otolith

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Fig. 13.5  Image of the otolith slice and distribution of cumulative strength of incident radiation
on an imaging plate (IP). Dense (light) shading areas of the otolith slice correspond to the transparent (opaque) zone. Colors indicate the cumulative strength normalized to the highest value. The
rectangle encloses the area of detailed analysis where the zonal patterns of the annulus were obvious and the one-dimensional analysis along the vertical direction could be applied

was recorded on the IP and retrieved by an image analyzer (Typhoon 9400; GE
Healthcare) with 25-μm resolution. Beta rays were randomly emitted from the otolith and absorbed by the stimulatable phosphor layer of the IP. The reaction strength
reflects the accumulated number or energy of the beta rays. The distribution of the
reaction strength on the IP was compared to digital images of the slice obtained by
microscopy after careful justification of the pixel positions of both data. Figure 13.5
shows the distribution of reaction strength relative to the highest value on the image
of the otolith slice. Higher reactions of the IP were observed around the area corresponding to the outer peripheral region of the slice. The relationship between the
two images was quantified in the area indicated by the rectangle in Fig. 13.5, where
the annulus had a clear zonal pattern and allowed one-dimensional analysis in the
vertical direction. Thirty vertical rows of IP pixel data were included in the area.
Relative reaction strength data in each vertical row were reconstructed by using the
peak position of the second transparent zone as the origin. We compared the distribution of reaction strength detected by the IP with the vertical pattern consisting of
opaque zones and transparent zones of the slice. The higher reaction of the IP corresponded to the area around the second transparent-opaque zone from outer edge
of the slice (Fig. 13.6). We fitted a curve that had a form proportional to 1/(h2 + r2)
to the vertical distribution of the reaction strength. h is the distance from the otolith
slice to the stimulatable phosphor layer of the IP and r is the distance on the IP surface from the peak of the second transparent zone of the slice to each pixel position
along the vertical axis. The formula approximated the distribution of incident radiation on a flat plane from a point source. The proportional coefficient and parameter
h were estimated by the least-squares method using Solver in Excel. The statistical
significance of the fitted curve in Fig. 13.6 was checked in a form of single regression analysis obtained by variable conversion. The fitted curve indirectly indicated
that the position of the source of the radiation was located around the peak of the
second transparent zone of the otolith slice. Considering an assumed error of

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171

Fig. 13.6  Comparison between the grey level of the otolith slice and the relative reaction strength
of the IP for the enclosed area in Fig. 13.5. Thirty vertical rows of IP pixel data were included.
Relative reaction strength data for each vertical row were reconstructed by using the peak position
of the second transparent zone as the origin. The vertical distribution of the zonally averaged grey
level of the otolith slice is shown by a solid thin line. Lower (higher) grey levels in the otolith slice
correspond to the opaque (transparent) zone. The relative reaction strength of each pixel of the IP
is shown with a full circle. The fitted curve for the IP pixel data in the area around the peak of the
second transparent zone is shown by a sequence of large full circles. Upward arrow indicates the
center of the second transparent zone

±1 pixel (0.025 μm) in justifying the slice and IP images, the probability of
­containing more radioactive materials was high in the area from the second to the
third opaque zones of the otolith slice.
The opaque zone of the otolith was formed in the summer season (Sekigawa
et al. 2002); the first transparent-opaque zone on the slice from the fat greenling
caught in the summer of 2012 was thought to correspond to the period from autumn
2011 to summer 2012. Thus, the second zone containing the most beta ray-emitting
radionuclides corresponded to the period from autumn 2010 to summer 2011. These
results strongly suggested that the fat greenling was in an environment rich in beta
ray-emitting nuclides between the spring and summer of 2011.
A possible candidate of beta ray-emitting radionuclide contained in the otolith
was 90Sr. The beta-ray emissions from the otolith of several fish species collected in
the FNPP port were associated with 90Sr concentration in the body, excluding the
viscera, and were associated with 137Cs in the muscle tissue (Fujimoto et al. 2013).
The amount of 90Sr leakage was estimated at about 3 % of 137Cs (Casacuberta et al.
2012), but it was thought that the 90Sr concentration in seawater rapidly increased,
similar to 137Cs from late March to the beginning of April 2011. From these relationships, we hypothesized that the fat greenling absorbed a large amount of radioactive
nuclides in the period just after the FNPP accident when contaminated seawater
covered the coastal area of Fukushima Prefecture.

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13.5  S
 imulation of  137Cs Concentrations in Fat Greenlings
Using a Biokinetic Model
To test our hypothesis, we simulated the contamination of fat greenling in a biokinetic model of 137Cs exchange between environment and biota. Many types of biokinetic model have been used to simulate the concentration of radioactive nuclides
in fish (Brown et al. 2006; Kanish and Aust 2013; Tateda et al. 2013). We constructed a simple model of two compartments as shown by Brown et al. (2006). The
equation for 137Cs concentration in a fat greenling is expressed as Eq. (13.1). The
137
Cs concentrations in marine fish are mediated by uptake through drinking seawater (first term), ingestion of prey (second term), and excretion by the osmoregulation
system (last term). Explanations for each variable and parameter are given in
Table 13.1. Most values were set according to Tateda (1997). As the fat greenling is
thought to be omnivorous (Kasamatsu 1999), we set the 137Cs concentration of prey
as a mixture of two groups of marine biota: one group was fish and the other was
invertebrates. The 137Cs concentration in prey fish was determined by Eq. (13.1).
The 137Cs concentrations in invertebrates were calculated by Eq. (13.2), in which
uptake of 137Cs is directly related to the seawater concentration of 137Cs. The parameters of kpi and CFpi empirically determined that the predicted 137Cs values by Eq.
(13.2) followed the observed 137Cs values for invertebrates off Fukushima Prefecture.
After determining the parameters in Eq. 13.2, we tuned the mixture rate of the prey
groups to obtain a simulated CF of fat greenling in the range of 60–70 by using the
constant 137Cs concentration value. In addition, the effect of physical disintegration
of 137Cs was discarded because it has a 100-fold-longer half-life (about 30.1 years)
in comparison to the biological half-life (about 100 days):

Table 13.1  Variables and parameters in the biokinetic equation for a fat greenling
Variable
Cf
Cpf
Cw
Cpi
kw
IRf
AEf
kf
CFpi
kpi
a

Value

0.10a
0.030a
0.50a
0.0088a
10b
0.0087b
0.36b

Unit
Bq/kg-wet
Bq/kg-wet
Bq/l
Bq/kg-wet
(kg/l) day−1
day−1
No dimension
day−1
No dimension
day−1
No dimension

Explanation
137
Cs concentration in fish body
137
Cs concentration in prey fish body
137
Cs concentration of surrounding seawater
137
Cs concentration of prey invertebrate
Uptake rate of 137Cs activity from seawater
Ingestion rate per unit mass of fish
Assimilation efficiency for fish
Excretion rate of 137Cs for fish
Concentration factor for prey invertebrate
Excretion rate of 137Cs for prey invertebrate
Mixing ratio of prey fish

Values were adopted from Tateda (1997)
Values were experimentally determined in this study

a

b

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13  Analysis of the Contamination Process of the Extremely Contaminated…

dC f ( t )
dt


= kw ⋅ Cw ( t ) + IR f ⋅ AE f ⋅  a ⋅ C pf ( t ) + (1 − a ) ⋅ C pi ( t )
− k f ⋅ C f (t )
dC pi ( t )



dt

= CFpi × k pi × C w ( t ) - k pi × C pi ( t )





(13.1)

(13.2)

The time course of 137Cs accumulation in the fat greenlings was simulated by
using the 137Cs concentration data from seawater at site-FP, site-F1, and site-F2
(shown in Fig. 13.7 with observed data). The derivation curve of 137Cs concentrations for site-F2 (thick solid line) was a good approximation of the envelope curve
of observation data. The 137Cs concentration of fat greenling at site-F2 reached maximum in mid-July 2011, then decreased. The simulated ecological half-life for the
period after March 2012 is about 208 days, similar to the values calculated from
observed data (13.2). An evaluation of the contribution of each term in Eq. (13.1)
showed that uptake of 137Cs from the seawater was largely responsible for the
increasing 137Cs concentration in the first month, during which time the concentration increased to 80 % of the maximum value. After this point, low but steady uptake
via prey contributed to a slow increase toward the maximum 137Cs concentration in
mid-July and the slow decrease thereafter. These features are identical to the simulation results for coastal fish indicated by Tateda et al. (2013). We conclude that the
simplified model is appropriate for simulating 137Cs concentrations in fat greenling
off the coast of Fukushima.

Fig. 13.7 Simulated 137Cs concentration of fat greenlings for site-FP, site-F1, and site-F2 with
observed 137Cs concentrations in fat greenling caught in the coastal waters of Fukushima Prefecture,
except the 20-km area, in the 20-km area, and in the FNPP port

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Simulation results for site-F1 (dashed line) and site-FP (thin solid line) are also
shown in Fig. 13.7. The same curve shape was observed, although at a different
level. Maximum 137Cs concentration were observed in mid-July and correlated with
the integrated values in seawater. The observed 137Cs concentration in fat greenling
from the FNPP port was moderately simulated by the model. The 137Cs concentration in the highly contaminated fat greenling was in the range between simulations
for site-FP in the FNPP port and site-F1. These model simulations support the
hypothesis that the fat greenling collected in the summer of 2012 off the mouth of
the Ota River had been exposed to the highly contaminated environment in the
FNPP port or adjoining areas.
The range of 137Cs concentrations formed by the large difference between simulations for site-FP and site-F1 bracketed the majority of the distribution of 137Cs
concentrations in fat greenlings in the FNPP port. The 137Cs concentration data at
site-FP were within the intermediate range compared with other observation points
at the initial stage of the radiation leak. Available seawater 137Cs concentration data
from April 2011 showed that the averaged value for the observation point in the
intake canal south of site-FP was several times higher than the value at site-FP. The
minimum values of 137Cs concentrations in the port, where the concentrations were
probably no lower than the level found outside the port (site-F1), where the concentration was about one order of magnitude lower than at site-FP. The large variability
of observed 137Cs concentrations in fat greenling was partly attributed to the local
spatial and temporal distribution of 137Cs in the FNPP port. In additional simulations
of a fat greenling entering the FNPP port after the peak period of environmental
contamination, highly contaminated fat greenlings were also generated, mainly by
prey uptake. This process might also maintain the wider range in the group of highly
contaminated fat greenlings in the FNPP port.
As for the extremely contaminated fat greenling caught in the area off the mouth
of the Ota River, radioactivity in the otolith and the simulation suggested a generation scenario. The fat greenling were living in the FNPP port or in the adjoining area
when contaminated water leaked to the sea and highly contaminated seawater covered the area. The 137Cs concentration of the fat greenling may have reached about
100,000 Bq/kg-wet. The relatively lower concentration compared with other fat
greenlings in the FNPP port suggest the habitat was apart from the intake canal of
the FNPP port and the fat greenling was able to avoid a direct encounter with the
more highly contaminated seawater. After the direct leakage of highly contaminated
water to the sea, the fat greenling eventually left the port.
Acknowledgments  The authors appreciate the members of the Research Center for Fisheries
Oceanography and Marine Ecosystem of the National Research Institute of Fisheries Science for
their support. The sliced sample of the otolith was processed by Japan NUS, and the ­autoradiographic
measurement of the otolith slice was performed by BayBioImaging. This study was financially
supported by the Fisheries Agency.
Open Access  This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Brown J, Dowdall M, Gwynn JP, Børretzen P, Selnæs ØG, Kovacs KM, Lydersen C (2006)
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in seawater off Japan as a consequence of the Fukushima Dai-ichi nuclear accident.
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Evans DH (2010) A brief history of the study of fish osmoregulation: the central role of the Mt.
Desert Island Biological Laboratory. Front Physiol 1:13
Fujimoto K, Miki S, Kaeriyama H, Shigenobu Y, Takagi K, Ambe D, Ono T, Watanabe T, Morinaga
K, Nakata K, and Morita T (2013) Levels of radioactive cesium contamination in three fish
species caught in the main harbor of Fukushima Dai-ichi Nuclear Power Plant, and a trial to
estimate strontium-90 from fish otoliths. (submitted to Environ Sci Technol)
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Baltic Sea environment proceedings no. 117. HELCOM, Helsinki
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environment. Technical reports series no. 422. IAEA, Vienna
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and seas. IAEA-TECDOC-1429. IAEA, Vienna
Kaneko T, Furukawa F, Watanabe S (2013) Excretion of cesium through potassium transport pathway in the gills of a marine teleost. In: Nakanishi TM, Tanoi K (eds) Agricultural implications
of the Fukushima nuclear accident. Springer Japan, Tokyo
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maff.go.jp/e/inspection/index.html. Date of access: 11 Nov 2014
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www.mhlw.go.jp/english/topics/2011eq/index_food_radioactive.html. Date of access: 11 Nov
2014
NRA (2014) Environmental radioactivity and radiation in Japan (in Japanese). http://www.kankyohoshano.go.jp/. Date of access: 11 Nov 2014
Sekigawa T, Takahashi T, Takatsu T (2002) Age and growth of fat greenling Hexagrammos otakii
in Kikonai Bay, Hokkaido. Aquat Sci 50:395–400 (in Japanese)
Shigenobu Y, Fujimoto K, Ambe D, Kaeriyama H, Ono T, Morinaga K, Nakata K, Morita T,
Watanabe T (2014) Radiocesium contamination of greenlings (Hexagrammos otakii) off the
coast of Fukushima. Sci Rep 4:6851
Tateda Y (1997) Basic model for the prediction of 137Cs concentration in the organisms of detritus
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Tateda Y, Tsumune D, Tsubono T (2013) Simulation of radioactive cesium transfer in the southern
Fukushima coastal biota using a dynamic food chain transfer model. J Environ Radioact
124:1–12
TEPCO (2012a) High cesium density detected in greenling. http://www.tepco.co.jp/en/nu/fukushima-­np/images/handouts_120828_02-e.pdf. Date of access: 11 Nov 2014

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TEPCO (2012b) Additional survey on high-cesium-level greenling and future countermeasures.
http://www.tepco.co.jp/en/nu/fukushima-np/images/handouts_121126_03-e.pdf. Date of
access: 11 Nov 2014
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Fukushima Daiichi NPS). http://www.tepco.co.jp/en/nu/fukushima-np/f1/smp/index-e.html.
Date of access: 21 Nov 2014
TEPCO (2014b) Result of radioactive nuclide analysis for the seawater sampled onshore and offshore of the power station. http://www.tepco.co.jp/en/nu/fukushima-np/f1/smp/2014/images/
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Wada T, Nemoto Y, Shimamura S, Fujita T, Mizuno T, Sohtaome T, Kamiyama K, Morita T,
Igarashi S (2013) Effects of the nuclear disaster on marine products in Fukushima. J Environ
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World Health Organization and Food and Agriculture Organization of the United Nations (2011)
Impact on seafood safety of the nuclear accident in Japan. ­http://www.iaea.org/newscenter/
focus/fukushima/seafoodsafety0511.pdf

Chapter 14

Contamination Levels of Radioactive Cesium
in Fat Greenling Caught at the Main Port
of the Fukushima Dai-ichi Nuclear
Power Plant
Ken Fujimoto, Shizuho Miki, and Tamaki Morita

Abstract Levels of radioactive cesium (radiocesium, 134Cs + 137Cs) detected in fish
caught at the Fukushima Dai-ichi Nuclear Power Plant (FNPP) Port are summarized. The mean concentration of radiocesium in three fish species (fat greenling,
Japanese rockfish, and spotbelly rockfish) was significantly different from that in
other fish species studied (brown hakeling, black rockfish, Japanese black porgy,
olive flounder, marbled flounder). The levels of radiocesium in fat greenling
decreased gradually from 100 kBq/kg-wet in 2013 to several kBq/kg-wet in 2014.
A migration of fat greenling into the FNPP Port was assumed to explain the fact that
fish containing low radiocesium levels were caught at the port. A low but significant
correlation between the total length of the fish and the radiocesium concentration in
the muscles was observed in fat greenling caught at the FNPP Port.
Keywords Radiocesium • Fat greenling • Japanese rockfish • Spotbelly rockfish •
FNPP Port

14.1

Introduction

The Ministry of Agriculture, Forestry and Fisheries (MAFF), Fukushima Prefecture,
and the Fisheries Research Agency (FRA) have been monitoring marine organisms
to ensure the safety of fish and fishery products since 2011, immediately after the
Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident (MAFF 2013). Although
about 40 % of marine organisms collected from the area off the coast of Fukushima
Prefecture within a year after the accident contained radiocesium (134Cs + 137Cs) at
levels exceeding the Japanese safety limit (100 Bq/kg-wet) (Buesseler 2012), the

K. Fujimoto (*) • S. Miki • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
e-mail: fujiken@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_14

177

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K. Fujimoto et al.

percentage of samples containing radiocesium levels exceeding the allowable limit
decreased to 1.9 % by the end of 2013 (MAFF 2013). The contamination levels of
radiocesium were gradually decreased even in fish caught in Fukushima Prefecture
coastal waters (MAFF 2013). However, an extremely high concentration of radiocesium (25,800 Bq/kg-wet) was detected in fat greenlings caught in the Ota River
(20 km north of the FNPP) on August 1, 2012, as reported by the Tokyo Electric
Power Company (TEPCO 2014).
In contrast to intensive monitoring of fishery products caught in offshore waters,
data for the radionuclide contamination of fish at the FNPP Port were limited
because sample collection from this area was difficult. Highly contaminated water
was directly discharged from the reactors into the port of FNPP during the early
period after the FNPP accident. TEPCO has been monitoring water quality at several stations at the FNPP Port daily, and the results are available on http://www.
tepco.co.jp/en/nu/fukushima-np/f1/smp/index-e.html. TEPCO also conducted a
Fish Contaminant Monitoring Program at the FNPP Port, and the results were published in 2014. However, the data were focused only on the levels of radiocesium in
fish, whereas other related information (e.g., size of the fish) was not made available
to the public.
In this section, we summarize the data released from TEPCO relating to radiocesium levels in eight fish species (fat greenling, Japanese rockfish, spotbelly rockfish,
brown hakeling, black rockfish, Japanese black porgy, olive flounder, marbled
flounder) caught at the FNPP Port, focused on the radiocesium concentration in the
muscle tissues of fat greenling (Hexagrammos otakii).
In this study, the data of 137Cs concentration in seawater and the concentration of
radiocesium in the muscles of fish species caught at the FNPP Port were obtained
from the TEPCO website (http://www.tepco.co.jp/en/nu/fukushima-np/f1/smp/
index-e.html). Fat greenling samples were collected using small cages and gill nets
in a period from February 25, 2013 to May 16, 2014 by TEPCO (Fig. 14.1). After
analyzing the data, TEPCO provided the samples to the National Research Institute
of Fisheries Science (NRIFS) of FRA. The samples were stored at −20 °C at the
TEPCO laboratory near the Hirono Thermal Power Plant (21 km south of the FNPP)
before shipment.

14.2

Concentrations of Radiocesium in Seawater and Fish
Caught at the Port of FNPP

The concentration of 137Cs in seawater at the unloading deck (station ULD in
Fig. 14.1) steeply increased shortly after the beginning of discharge from the reactors. The maximum level of 137Cs (660 kBq/l) was detected on April 6, 2011. The
level of 137Cs rapidly decreased to 1 kBq/l at the end of April 2011 and to 100 Bq/l
in mid-June 2011 (Fig. 14.2). The concentration factor of 137Cs in fish ranged
between 5 and 100 (IAEA 2004). Considering the concentration factor, 137Cs levels

14 Contamination Levels of Radioactive Cesium in Fat Greenling Caught…

179

Fig. 14.1 Map of the monitoring sites at the Fukushima Dai-ichi Nuclear Power Plant (FNPP) and
Port. 1–4 reactor units 1–4, ULD point of cage sampling at the unloading deck, SJ point of cage
sampling at the north jetty, NJ point of cage sampling at the south jetty, JN point of gill net sampling at the port entrance

in fish at the FNPP Port could have reached 1,000 kBq/kg-wet between early and
mid-April 2011 and 10 kBq/kg-wet in mid-June 2011.
Box plots shown in Fig. 14.3 illustrate the levels of radiocesium in the muscles
of eight fish species caught at the FNPP Port. The average radiocesium concentrations of three species (fat greenling, Japanese rockfish, and spotbelly rockfish) were
significantly different from those in the other five species (Fig. 14.3; p < 0.05,
Scheffe’s test). The inter-quartile range of spotbelly rockfish and Japanese rockfish
was narrower than that of fat greenling. Although the 75th quartiles of spotbelly

K. Fujimoto et al.

180
1000000

The concentration of 137Cs
in seawater (Bq/L)

100000

10000

1000

100

10

1
3/28/11

4/7/11

4/17/11

4/27/11

5/7/11

5/17/11

5/27/11

6/6/11

6/16/11

Sampling of date

Fig. 14.2 Temporal changes in 137Cs concentration in seawater samples collected at the unloading
deck at the FNPP Port. Data were obtained from http://www.tepco.co.jp/en/nu/fukushima-np/f1/
smp/index-e.html

The concentration of radiocesium
in muscle (Bq/kg-wet)

1000000
100000
10000
1000
100
10
1
A

B

C

D

E

F

G

H

Fish species

Fig. 14.3 Boxplots of radiocesium concentration in the muscles of fish caught at the FNPP Port
from December 20, 2012 to November 19, 2013. Each box indicates the inter-quartile range. The
line inside the box shows the median. The lines extending vertically from the boxes (whiskers)
show the variability outside the quartiles. Fish species: A fat greenling (Hexagrammos otakii), B
brown hakeling (Physiculus maximowiczi), C black rockfish (Sebastes schlegeli), D Japanese black
porgy (Acanthopagrus schlegelii), E Japanese rockfish (Sebastes cheni), F olive flounder
(Paralichthys olivaceus), G marbled flounder (Pleuronectes yokohamae), H spotbelly rockfish
(Sebastes pachycephalus)

14 Contamination Levels of Radioactive Cesium in Fat Greenling Caught…

181

rockfish and Japanese rockfish were higher than 100 kBq/kg-wet, the median of
radiocesium concentration in black rockfish was less than 10 kBq/kg-wet.
Furthermore, the inter-quartile range of black rockfish was wider than that of the
other two rockfish species, indicating that fluctuations in radiocesium levels in the
black rockfish sample population were more intense than those observed in other
rockfish. Interestingly, within the flatfish group, the mean radiocesium concentration in marbled flounder was significantly higher than that in olive flounder
(p < 0.001; Wilcoxon–Mann–Whitney test).
Differences in concentrations of radiocesium among the studied fish species
could not be explained only by the changes in radiocesium concentration in seawater. In addition to the direct intake of contaminated water by osmosis via the gills,
incorporation of radiocesium through the consumption of prey via the food web
might cause variations in radiocesium levels in fish. For example, although the
Japanese flounder and marbled flounder live in the same environment, the mean
concentrations of radiocesium differ between these two species, probably because
their feeding habits are quite different. Japanese flounder prefer fish, whereas marbled flounder prefer worms living on the seabed. Similar to fish, prey organisms
(e.g., crustaceans and worms) were labeled with radiocesium at various concentrations. Hence, the kind and amount of prey consumed were key factors influencing
the levels of radiocesium within and between fish species living in waters at the
FNPP Port.

14.3

Temporal Changes in Radiocesium Levels
in Fat Greenling Caught at the FNPP Port

Figure 14.4 shows the temporal changes in radiocesium levels in the muscle tissues
of fat greenling caught at the FNPP Port in a period from February 25, 2013 to
May 16, 2014. The decreasing trend of radiocesium concentrations confirmed that
the fluctuations among individual fish were intense in 2014. The levels of radiocesium were 100 kBq/kg-wet and several kBq/kg-wet at the beginning of 2013 and
2014, respectively. The radiocesium levels in a fish sample collected between June
12 and August 2, 2013 ranged between 0.48 and 0.92 kBq/kg-wet, and the mean
value was significantly lower than that of other samples collected within the same
period (p < 0.005; Student’s t test). Additionally, a fat greenling captured on February
3, 2014 had a radiocesium concentration of 0.13 Bq/kg-wet, which was the lowest
concentration compared to that in other fat greenling caught at the FNPP Port.
Although an explanation of these low radiocesium levels could be that some fat
greenling either escaped from contaminated seawater or did not consume organisms
containing high concentrations of radiocesium, it is more likely that these fish
migrated to the FNPP Port long after the accident. TEPCO constructed barriers
made of gill nets at the entrance of the FNPP Port to prevent the escape of fish.
However, these barriers were temporarily removed to allow ships to enter and exit

K. Fujimoto et al.

182

The concentration of radiocesium
in muscle (kBq/kg-wet)

1000

100

10

1

0.1

Sampling of date
Fig. 14.4 Temporal changes in radiocesium concentration in fat greenling caught at the FNPP
Port. Fish samples were collected from February 25, 2013 to May 16, 2014

the port. Therefore, the possibility of fat greenling migrating into the FNPP Port
cannot be excluded. The concentration of 137Cs in seawater sampled at the unloading
deck (Fig. 14.1, ULD) was below 10 Bq/l in 2014 (TEPCO 2014). Taking into
account the concentration factor, which ranged between 5 and 100 (IAEA 2004),
137
Cs levels in fat greenling that migrated into the FNPP Port would currently attain
a maximum radiocesium concentration of 1 kBq/kg-wet.

14.4

Relationship Between Total Length and Radiocesium
Level in the Muscles of Fat Greenling Caught
at the FNPP Port

A low but significant correlation (r = 0.395, p < 0.005) between the total length and
radiocesium concentration in the muscles was observed in fat greenling caught at
the FNPP Port (Fig. 14.5). Because individuals caught within the experimental
period were more than 3 years of age, as deduced from their total length (Fukushima
Prefecture Fisheries Experimental Station 1974), all sampled fat greenling would
have experienced an extremely high concentration of radiocesium in the seawater
shortly after the accident (Fig. 14.2). The “size effect” reported for top fish species
(Koulikov and Ryabov 1992) was also observed in fat greenling to some extent.
Large-sized fat greenling (e.g., total length >400 mm) contained more radiocesium
than did smaller ones because the former were 2 or more years of age and were able

14 Contamination Levels of Radioactive Cesium in Fat Greenling Caught…

183

The concentration of radiocesium
in muscle (kBq/ kg-wet)

1000

100

10

1

0.1
200

250

300

350

400

450

500

550

Total length of fish (mm)
Fig. 14.5 Relationship between the total length of the fish and the concentration of radiocesium
in muscles in fat greenling caught at the FNPP Port from February 25, 2013 to May 16, 2014

to catch prey at the time when extremely contaminated water was discharged into
the FNPP Port. The amount of radiocesium that was once incorporated into the adult
fish has been metabolized and excreted from the body; hence, the levels of radiocesium gradually decreased. In contrast, the concentration of radiocesium in young
fish decreased more rapidly as the fish grew and the body mass increased. If the
amount of radiocesium remains constant in the fish body, the concentration is
reduced by half the initial value when the body mass of the fish doubles. The
“growth effect” explains the low levels of radiocesium in small fat greenling (less
than 300 mm during the sampling period) because they were very young in March
2011.
Acknowledgments We thank the staff of Tokyo Power Technology Co., Inc. for transporting the
samples. This study was supported by the Fisheries Research Agency, Ministry of Agriculture,
Forestry and Fisheries of Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
Buesseler KO (2012) Fishing for answers off Fukushima. Science 338:480–482
Fukushima Prefecture Fisheries Experimental Station (1974) Reports of stocks and habitat for
selective fish living in fishing ground around northern part of the Pacific. No. 127 (in Japanese)

184

K. Fujimoto et al.

International Atomic Energy Agency (IAEA) (2004) Sediment distribution coefficients and concentration factors for biota in the marine environment. Technical report series no. 422.
International Atomic Energy Agency, Vienna, p 95
Koulikov AO, Ryabov IN (1992) Specific cesium activity in freshwater fish and the size effect. Sci
Total Environ 112:125–142
Ministry of Agriculture, Forestry and Fisheries (MAFF) (2013) Results of the inspection on radioactivity level in fisheries products. http://www.jfa.maff.go.jp/e/inspection/. Accessed 15 Sept
2014
Tokyo Electric Power Company (TEPCO) (2014) Results of radioactive analysis around Fukushima
Daiichi Nuclear Power Station. http://www.tepco.co.jp/en/nu/fukushima-np/f1/smp/index-e.
html. Accessed 15 Sept 2014

Part V

Freshwater Systems

Chapter 15

Comparison of the Radioactive Cesium
Contamination Level of Fish and their Habitat
Among Three Lakes in Fukushima Prefecture,
Japan, After the Fukushima Fallout
Keishi Matsuda, Kaori Takagi, Atsushi Tomiya, Masahiro Enomoto,
Jun-ichi Tsuboi, Hideki Kaeriyama, Daisuke Ambe, Ken Fujimoto,
Tsuneo Ono, Kazuo Uchida, and Shoichiro Yamamoto

Abstract Levels of radiocesium (134Cs + 137Cs) contamination in lake water, bottom
sediment, plankton, and fish were investigated in three geographically separated
lakes in Fukushima Prefecture (Lake Hayama, Lake Akimoto, and Lake Tagokura)
between June 2012 and November 2013. Levels of contamination differed among
the three lakes, with the highest levels in each measured component found in Lake
Hayama, followed by Lake Akimoto, and the least contamination in Lake Tagokura.
Among the lakes, the magnitude of contamination decreased with distance from the
Fukushima Dai-ichi Nuclear Power Plant. Mean radiocesium concentrations were
higher in piscivorous fish than in other fish, possibly reflecting differences in trophic
levels. Radiocesium concentrations of the lake water, bottom sediment, plankton,
and fish were significantly correlated with surface soil radiocesium content near
lake sites.

K. Matsuda (*) • J. Tsuboi • S. Yamamoto
National Research Institute of Aquaculture, Fisheries Research Agency,
2482-3 Chugushi, Nikko, Tochigi 321-1661, Japan
e-mail: matsukei@affrc.go.jp
K. Takagi
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
A. Tomiya • M. Enomoto
Fukushima Prefectural Inland Water Fisheries Experimental Station,
3447-1, Inawashiro, Maya, Fukushima 969-3283, Japan
H. Kaeriyama • D. Ambe • K. Fujimoto • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
K. Uchida
Fisheries Research Agency, Yokohama, Kanagawa 220-6115, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_15

187

188

K. Matsuda et al.

Keywords Lake Hayama • Lake Akimoto • Lake Tagokura • Piscivorous fish •
Radiocesium contamination • Trophic level

15.1

Introduction

Radiocesium is one of the major radioactive components of the fallout from the
Fukushima Dai-ichi Nuclear Power Plant (FNPP). The total amount of 137Cs discharged into the atmosphere between 12 March and 6 April 2011 was estimated as
approximately 1.3 × 1016 Bq (Chino et al. 2011). Before 20 April 2011, 18 % of the
total fallout settled on Japanese land (Stohl et al. 2012). Radiocesium monitoring
of freshwater organisms (Fisheries Agency 2012) showed that trophic level is an
important ecological factor affecting bioaccumulation of 137Cs in fish (Mizuno
and Kubo 2013). For example, in the Agano River basin in Fukushima, 137Cs contamination of carnivorous salmonids was roughly twice that of the herbivore ayu
Plecoglossus altivelis (Mizuno and Kubo 2013). However, levels of radiocesium
contamination among individuals within conspecifics have also been found to differ among habitats (Iguchi et al. 2013; Mizuno and Kubo 2013; Yamamoto et al.
2014a), and the causes of these differences are uncertain.
The objective of this study was to investigate factors affecting the differences in
concentrations of radiocesium (134Cs + 137Cs) in fish of three geographically separate
lakes in Fukushima Prefecture (Fig. 15.1, Table 15.1). These three lakes are located
at differing distances from the FNPP and have different air dose rates and radiocesium concentrations in the adjacent surface soil, but have roughly similar retention
times (Table 15.1). Sampling of lake water, bottom sediment, plankton, and fish was
conducted up to three times per year in spring, summer, and autumn from June 2012
to November 2013.

15.2

Contamination Levels of Lake Water, Bottom Sediment,
and Plankton

In each lake, lake water was sampled from one site (n = 1), and plankton was sampled one time along a constant distance of the lake surface (n = 1) (Fig. 15.1). Bottom
sediment samples were collected from one point in each lake during one sampling
event (n = 1) (Fig. 15.1). Temporal changes in radiocesium concentrations of the
lake water, bottom sediment, and plankton are shown in Fig. 15.2. In Lake Tagokura,
radiocesium concentrations were not detected in the lake water from November
2012 to October 2013 (detection limits, <2.1 mBq l−1), as was plankton in October
2013 (detection limit, 1,413 Bq kg−1 dry mass).
Among these ecosystem components, only the bottom sediment showed significant temporal changes, with a significant decreasing trend in Lake Hayama (Table 15.2;
t test, P < 0.05) and a significant increasing trend in Lake Tagokura (Table 15.2;
t test, P < 0.05). Continuing investigation is necessary to determine the patterns and
temporal changes of radiocesium contamination in lake water and plankton.

15

Comparison of the Radioactive Cesium Contamination Level of Fish…
130°0’0”E

189

140°0’0”E

45°0’0”N

2
40°0’0”N

3

1

FNPP

35°0’0”N

f

f

w

1. Lake Hayama
f
f

f

f

f

f

1 km
f
2. Lake Akimoto
f

f

f
fw

1 km

ff

f

f
w

3. Lake Tagokura

3 km

Bottom sediment sampling area
Plankton sampling area

Fig. 15.1 Upper figure shows the locations of the study lakes and the Fukushima Dai-ichi Nuclear
Power Plant (FNPP) in Fukushima Prefecture. Lower figure show the sampling sites in each of
the lakes (w lake water sampling point, f fish sampling point). Arrows point to bottom sediment
sampling points (Modified from Matsuda et al. 2015)

K. Matsuda et al.

190
Table 15.1 Characteristics of the study lakes
Lake area
Volume
Max depth
Altitude
Linear distance from FNPPa
Retention timeb
Lake type
Air dose rates at lakesidec
Radiocesium contents
of surface soil at lakesidec

Unit
(km2)
(103 × m3)
(m)
(m)
(km)
(years)

(μSv h−1)
(Bq m−2)

Hayama
1.75
36,200
70
175
39
0.48
Artificial dam
reservoir
2.88
637,663

Akimoto
3.6
32,800
40
736
85
0.26
Natural
0.57
80,018

Tagokura
9.95
494,000
80
515
157
0.31
Artificial dam
reservoir
0.12
16,232

a

Fukushima Dai-ichi Nuclear Power Plant
Citation from Fukushima and Arai (2014)
c
Air dose rates at 1-m height from the ground and radiocesium (134Cs + 137Cs) concentrations of
surface soil (depth, 0–50 mm) on 6 June 2011 to 8 July 2011 (MEXT 2011) (Cited from Matsuda
et al. 2015)
b

The order of contamination levels of lake water, bottom sediment, and plankton
for the study period (2012–2013) in three lakes was Lake Hayama > Lake
Akimoto > Lake Tagokura (Table 15.2).

15.3

Radiocesium Concentrations in Fish

Fish from Lake Hayama were analyzed individually, except for Japanese smelt
(Hypomesus nipponensis); all other fish samples were analyzed from 2 to 103
pooled individuals. Temporal changes in radiocesium concentrations in several fish
species in each lake are shown in Fig. 15.3. Significant decreasing trends of radiocesium concentrations in fish from 2012 to 2013 were observed for white-spotted
char in Lake Tagokura; smallmouth bass in both Lake Hayama and Lake Akimoto;
bluegill, Japanese dace, and crucian carp in Lake Hayama; and Japanese barbell in
Lake Akimoto (Table 15.3; t tests for parametric groups or Mann–Whitney tests for
nonparametric groups, P < 0.05). Radiocesium concentrations significantly
decreased by 33 % to 65 % between 2012 and 2013 in these fish species (Table 15.3).
Considering only physical decay of radiocesium, the loss of radiocesium concentration in the fish on 20 June 2013 (the first sampling day on 2013) would have been
expected to decrease by 9 % of that on 29 November 2012 (the last sampling day on
2012). Therefore, the radiocesium concentrations of crucian carp in Lake Tagokura
might increase during the period between 2012 and 2013 without physical decay
(Table 15.3). Fukushima and Arai (2014) also found that radiocesium concentrations in channel catfish (Ictalurus punctatus) and kokanee (Oncorhynchus nerka)
increased between 2011 and 2013 in some lakes in northeastern Japan. The order of
the contamination level in each fish species for the study period (2012–2013) among
the three lakes was also Lake Hayama > Lake Akimoto > Lake Tagokura (Table 15.3).

191

Comparison of the Radioactive Cesium Contamination Level of Fish…

Dissolved

134Cs+137Cs

concentration
(mBq L-1)

a

Lake water
100

10

1
400

134Cs+137Cs

concentration
(Bq kg-1 dry mass)

b

100,000

600

800

1,000

Bottom sediment

10,000
1,000
100
10
1
400

c
concentration
(Bq kg-1 dry mass)

Fig. 15.2 Time-course of
radiocesium (134Cs + 137Cs)
concentrations in samples
from each lake: lake water
(a); bottom sediment (b);
plankton (c). Vertical bars
indicate 1 SD derived from
counting statistics. Samples
below detection limits are
indicated by closed squares
on the x-axis

134Cs+137Cs

15

10,000

600

800

1,000

Plankton

1,000

100

Lake Hayama
Lake Akimoto

10
Lake Tagokura
1
400

600
800
1,000
Days after the nuclear accident

192

K. Matsuda et al.

Table 15.2 Mean radiocesium (134Cs + 137Cs) concentrations of the water, bottom sediment, and
plankton in each lake

Sample
Lake water
(mBq l−1)

Lakea
H
A
T
H

Bottom
sediment
(Bq kg−1 dry A
mass)
T
Plankton
H
(Bq kg−1 dry A
mass)
T

Mean
radiocesium
concentration
± SDb in
2012–2013
66.2 ± 27.4a
24.5 ± 13.9b
1.6 ± 0.4
17,340 ±
8,519a
2,357 ± 2,091
301 ± 138b
4,295 ± 2,495
1,383 ± 1,004
25

nc
5
5
1
6
6
6
4
3
2

(x) Mean
radiocesium
concentration
± SDb in
2012
89
29
1.6 ± 0.4
24,189 ±
5,636
2,841 ± 3,140
191 ± 85
4,852 ± 78

nc
2
2
1
3
3
3
1

(y) Mean
radiocesium
concentration
± SDb in
2013
51 ± 25
22 ± 8.3
ND
10,491 ±
2,987
1,874 ± 607
410 ± 66
4,109 ± 3,021
1,383 ± 1,004
25

nc
3
3

Loss of
radiocesium
concentration
in 2012–2013:
(1−y/x) × 100
(%)
43
25

3

57*

3
3
3
3
2

34
−114*
15

Significant difference between the 2012 period and 2013 period was examined by a t test. Asterisk
of [Loss of the radiocesium concentration from 2012 to 2013] indicates significant difference
between the x and the y (P < 0.05). These tests were conducted if there were more than two samples
in both or all groups
a
Lake: H = Hayama, A = Akimoto, T = Tagokura
b
SD: If n = 1, SD is counting error (1 sigma)
c
n: ND data were excluded. Significant differences among the lakes were examined by a t test
(lake water) and by a Kruskal–Wallis test (bottom sediment and plankton). Different small letters
following an entry indicates significant difference among the lakes (P < 0.05) (Modified from
Matsuda et al. 2015)

15.4

Relationship Between Trophic Level and Radiocesium
Concentration

Freshwater fish primarily accumulate radiocesium through the food chain rather
than directly from the water (Williams and Pickering 1961; Hewett and Jefferies
1976; Yamamoto et al. 2014b). Species-specific food intake and food availability
can cause differences in radiocesium concentrations among fish species. Because
metals are concentrated in organisms as they are transferred up trophic levels by
consumption, the trophic level of a fish is an important ecological factor affecting its
concentration of radiocesium (Rowan and Rasmussen 1994). For example, after the
Chernobyl accident in 1987, a higher annual mean concentration of 137Cs has been
detected in fish from higher trophic levels in some lakes of Finland, including perch
(Perca fluviatilis) and pike (Esox lucius) (Rask et al. 2012).
Okino (2002) showed that fishes classified as piscivorous, including salmonid
fishes, the Japanese catfish Silurus asotus, and the largemouth bass Micropterus
salmoides, occupy the top of the food chain in temperate lakes in Japan. We also
categorized fish into two groups: (1) piscivorous fish (the white-spotted char
Salvelinus leucomaenis pluvius, Japanese catfish, the smallmouth bass Micropterus

15

Comparison of the Radioactive Cesium Contamination Level of Fish…
Salvelinus leucomaenis pluvius
(White-spotted char)
10,000

Silurus asotus
(Japanese catfish)

a

193

Micropterus dolomieu
(Smallmouth bass)

b

c

1,000
100

Lake Hayama
Lake Akimoto

10

Lake Tagokura

1

Micropterus salmoides
(Largemouth bass)

134Cs+137 Cs

concentration (Bq kg-1 wet mass)

10,000

Oncorhynchus masou masou
(Masu salmon)

d

Lepomis macrochirus
(Bluegill)

e

f

1,000
100
10
1

Carassius spp.
(Crucian carp)

Cyprinus carpio
(Common carp)

g

h

i

Hemibarbus barbus
(Japanese barbel)

Hypomesus nipponensis
(Japanese smelt)

j

k

Tribolodon hakonensis
(Japanese dace)

10,000
1,000
100
10
1
10,000
1,000

0

200

400

600

800 1,000

100
10
1
0

200

400

600

800 1,000

0

200

400

600

800 1,000

Days after the nuclear accident
Fig. 15.3 Time-course of radiocesium (134Cs + 137Cs) concentrations in fish from each lake.
Concentrations in Lake Hayama are for individual samples except for Hypomesus nipponensis; all
other values were measured from pooled samples. Vertical bars indicate 1 SD. Samples below
detection limits are indicated by closed squares on the x-axis

Lakea
H
A
T

H
A
T
H
Micropterus
dolomieu (Bq kg−1 A
wet mass)
T
H
Micropterus
salmoides (Bq kg−1 A
wet mass)
T
H
Oncorhynchus
masou masou
A
(Bq kg−1 wet mass) T
H
Lepomis
macrochirus
A
(Bq kg−1 wet mass) T

Species
(scientific name)
Salvelinus
leucomaenis
pluvius (Bq kg−1
wet mass)
Silurus asotus
(Bq kg−1 wet mass)
174
6
16
1
2
4
4
2
29
6
3

2,534 ± 1,881a
370 ± 223b
2,708 ± 1,882a
212 ± 4.2
23b
746 ± 80a
118 ± 66b
3.5b
399 ± 236a
145 ± 125b
14 ± 13b

375 ± 145
278 ± 18
266 ± 65
323 ± 62
275 ± 31
348 ± 86
123 ± 26
143 ± 36
113 ± 45

8

4
5
6

339 ± 77
298 ± 39

nc

2,745 ± 893

Mean radiocesium
concentration ± SDb
in 2012–2013
4,445 ± 704a
176 ± 83
8.5 ± 6.0b

491 ± 56

Mean total
length ± SDb
(mm)
440 ± 48
283 ± 55
328 ± 100
7

4
2
3

16
1
1
1
1
22
3
2

471 ± 227
219 ± 146
18

124
3

nc

2,708 ± 1,882
212 ± 4.2
29 ± 6.3
862 ± 10
217 ± 7.8

3,111 ± 1,885
519 ± 228

2,911 ± 820

(x) Mean
radiocesium
concentration ± SDb
in 2012
4,445 ± 704
266
12 ± 7.2

Table 15.3 Mean radiocesium (134Cs + 137Cs) concentrations of fish in each lake

14 ± 1.0
707 ± 27
86 ± 6.6
3.5
172 ± 46
70 ± 36
6.5 ± 1.1

1,104 ± 799
220 ± 71

1,582 ± 18

116 ± 16
5.0 ± 1.0

(y) Mean
radiocesium
concentration ± SDb
in 2013

1
3
3
2
7
3
1

50
3

1

3
3

nc

63*
68
64

53
18
60

65*
58*

46

56
59*

Loss of the
radiocesium
concentration
in 2012–2013:
(1−y/x) × 100 (%)

194
K. Matsuda et al.

1,338 ± 828a
196 ± 58b
7.5 ± 2.7b
1,216 ± 556a
158 ± 106b
5.7 ± 1.1b
753 ± 100a
100 ± 33b
8.4b
150 ± 38
263 ± 31
62 ± 21
ND

258 ± 64
235 ± 49
181 ± 68
367 ± 62
161 ± 99
224 ± 57
704 ± 52
433 ± 230
658 ± 139

426 ± 73

92 ± 1
98 ± 12
74 ± 10

1
3

4

56
6
6
78
5
5
4
4
2

72
ND

180

1,960 ± 632
232 ± 61
8.7 ± 3.1
1,255 ± 564
194 ± 110
5.8
753 ± 100
111 ± 29
8.9 ± 1.2

2

2

28
3
3
71
3
2
4
3
1

263 ± 31
41 ± 5.0
ND

1
1

2

1
1

66 ± 3.6
7.9 ± 0.9
121

28
3
3
7
2
3

716 ± 440
159 ± 29
6.4 ± 2.1
817 ± 230
104
5.6 ± 1.5

44

33*

41
11

63*
31
26
35*
46
3

Significant difference between the 2012 period and 2013 period was examined by a t test or a Mann–Whitney test. Asterisk of [Loss of the radiocesium concentration from 2012 to 2013] indicates significant difference between the x and the y (P < 0.05). These tests were conducted if there were more than two
samples in both or all groups
a
Lake: H Hayama, A Akimoto, T Tagokura
b
SD: In n = 1, SD is counting error (1 sigma)
c
n ND data were excluded. Significant differences among the lakes were examined by a Mann–Whitney test (smallmouth bass and largemouth bass), by a oneway ANOVA, or by a Kruskal–Wallis test (white-spotted char, masu salmon, bluegill, Japanese dace, crucian carp, and common carp). Different small letters
following numbers indicates significant difference among the lakes (P < 0.05) (Cited from Matsuda et al. 2015)

Tribolodon
H
hakonensis
A
(Bq kg−1 wet mass) T
H
Carassius spp.
(Bq kg−1 wet mass) A
T
H
Cyprinus carpio
(Bq kg−1 wet mass) A
T
Hemibarbus
H
barbus (Bq kg−1
A
wet mass)
T
H
Hypomesus
nipponensis
A
(Bq kg−1 wet mass) T

15
Comparison of the Radioactive Cesium Contamination Level of Fish…
195

K. Matsuda et al.

196
Table 15.4 Mean radiocesium (134Cs +
during the study period (2012–2013)

Lake Hayama
Lake Akimoto
Lake Tagokura

137

Cs) concentrations of each fish group in each lake

Bq kg−1 wet mass ± SD
Piscivorous fish
2,636 ± 1,311a
219 ± 108
12 ± 10

na
5
4
3

Other fish
794 ± 478b
135 ± 47
9.0 ± 3.7

na
5
6
4

a

n: ND data were excluded. Significant differences between piscivorous fish and others were examined by a t test. Different small letters after number entries indicates significant difference (P < 0.05)
(Cited from Matsuda et al. 2015)

dolomieu, largemouth bass, and masu salmon Oncorhynchus masou); (2) other fish
(the bluegill Lepomis macrochirus, the Japanese dace Tribolodon hakonensis, the
crucian carp Carassius spp., the common carp Cyprinus carpio, the Japanese barbel
Hemibarbus barbus, and Japanese smelt). We found that the mean radiocesium concentration in piscivorous fish was significantly higher than in other types of fish only
in Lake Hayama during the study period (2012–2013) (Table 15.4; t test, P < 0.01).

15.5

Geographic Differences in Levels of Radiocesium
Contamination

The FNPP fallout was the source of radiocesium in freshwater fish and in lake water,
bottom sediment, and plankton. Therefore, correlations between radiocesium concentrations in each of these lake ecosystem components and concentrations in lakeside surface soil were analyzed. Soil samples were taken at a 0- to 50-mm depth on
the lakeside of each lake between 6 June and 8 July 2011 (MEXT 2011). The radiocesium concentrations of surface soil on each lakeside (MEXT 2011) are shown in
Table 15.1. Significant correlations were found between surface soil radiocesium
content and that of lake water (R2 = 0.590, P < 0.01), bottom sediment (R2 = 0.729,
P < 0.001), plankton (R2 = 0.555, P < 0.01), and all fish (R2 = 0.273–0.971, P < 0.01)
(Fig. 15.4).
Thus, the differences in radiocesium concentrations in the lake samples likely
reflect the quantity of radiocesium from the FNPP that was deposited at each lake.
A previous report found a strong relationship between the distance from the FNPP
and the radiocesium concentrations in freshwater fish (Mizuno and Kubo 2013). A
similar relationship was observed in the present study, where the quantity of radiocesium deposited in lakeside soil decreased with distance from the FNPP. However,
this relationship has not been found in all of northeastern Japan because the pollution did not spread concentrically from the FNPP. For example, Lake Chuzenji
(located southwest of the FNPP) and Lake Tagokura are both located roughly
160 km from the FNPP in linear distance, but radiocesium concentrations in the

Comparison of the Radioactive Cesium Contamination Level of Fish…
Bottom sediment

100,000

Y=0.027x + 11.157
2
R =0.729
P<0.001

100
10

a

100
10

b

d

1
100,000

-1

100
10

g

1

e
Tribolodon hakonensis
(Japanese dace)
Y=0.002x – 0.91
2
R =0.287
P<0.001

10,000
1,000
100
10

-1

c
Oncorhynchus masou masou
(Masu salmon)

10,000

Y=0.001x + 11.32
2
R =0.969
P<0.001

1,000
100
10

f

100,000

h
1

Bq kg wet mass

10

1

1

100,000

100

1

100,000

Y=0.001x + 68.47
2
R =0.273
P<0.001

1,000

10
1

Lepomis macrochirus
(Bluegill)

10,000

100

-1

10

1,000

1,000

100,000

-1

100

Micropterus salmoides
(Largemouth bass)
Y=0.004x – 74.25
2
R =0.296
P<0.01

10,000

Y=0.006x + 485.64
R2=0.558
P<0.05

10,000

1

Bq kg wet mass

-1

Bq kg wet mass

1,000

100,000

Bq kg wet mass

-1

Bq kg wet mass

Salvelinus leucomaenis pluvius
(White-spotted char)
Y=0.007x – 237.86
2
R =0.969
P<0.001

10,000

-1

Cs+137Cs concentration

100,000

134

1,000

1

1

Bq kg wet mass

10,000

100

10,000 1,000,000

197

Plankton

100,000

-1

1,000

-1

mBq L

-1

10,000

Bq kg dry mass

-2

Y=0.008 10 x + 14.80
2
R =0.590
P<0.01

Bq kg dry mass

Lake water

100,000

Bq kg wet mass

15

10,000
1,000

100

10,000 1,000,000

Carassius spp.
(Crucian carp)
Y=0.002x – 11.54
2
R =0.325
P<0.001

100
10
1
1

i
100

10,000 1,000,000

Cyprinus carpio
(Common carp)
Y=0.001x + 7.21
2
R =0.970
P<0.001

10,000
1,000
100
10

j

1
1

100

10,000 1,000,000

134

Cs+137Cs contents of surface soil (Bq/m2)

Fig. 15.4 Correlations between the mean radiocesium concentrations (134Cs + 137Cs) in each lake
sample taken during the study period (2012–2013) and those of the surface soil taken at a 0- to
50-mm depth on each lakeshore between 6 June and 8 July 2011 (MEXT 2011). Vertical bars
indicate 1 SD. Solid lines show significant fitted regression lines (Cited from Matsuda et al. 2015)

muscle of salmonids in 2012 were 142.9–249.2 Bq kg−1 wet mass in Lake Chuzenji
and only 12 Bq kg−1 wet mass in Lake Tagokura (Yamamoto et al. 2014a).
In addition, there is some evidence that different levels of radiocesium contamination of fish among lakes can also be caused by variation in retention time
(Fukushima and Arai 2014), depth (Broberg et al. 1995), lake water hardness and
conductivity (Hakanson et al. 1992; Särkkä et al. 1995), suspended sediment concentration, and temperature (Rowan and Rasmussen 1994).
In addition to continuing to measure levels of radiocesium contamination in
these lakes, future studies are needed to determine the factors underlying continued
contamination and the retention of radiocesium in these lakes.

198

K. Matsuda et al.

Acknowledgments This chapter was adapted from a paper published by Matsuda et al. (2015).
The authors are grateful to Masato Murakami, Tomoko Okazaki, and Maki Yoshida for their assistance with the sample assays and data analyses. They also thank Kaoru Nakata for critical review
of the manuscript. This study was supported by the Fisheries Agency, Ministry of Agriculture,
Forestry and Fisheries, Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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the soil. http://www.mext.go.jp/b_menu/shingi/chousa/gijyutu/017/shiryo/icsFiles/afieldfile/2011/09/02/1310688_1.pdf. Accessed 3 June 2014 (in Japanese)
Mizuno T, Kubo H (2013) Overview of active cesium contamination of freshwater fish in
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Okino T (2002) Ecosystem of lake. Kyoritsu Shuppan, Tokyo (in Japanese)
Rask M, Saxen R, Ruuhijarvi J, Arvola L, Jarvinen M, Koskelainen U, Outola I, Vuorinen PJ
(2012) Short- and long-term patterns of Cs-137 in fish and other aquatic organisms of small
forest lakes in southern Finland since the Chernobyl accident. J Environ Radioact 103:41–47
Rowan DJ, Rasmussen JB (1994) Bioaccumulation of radiocesium by fish: the influence of physicochemical factors and trophic structure. Can J Fish Aquat Sci 51:2388–2410
Särkkä J, Jämsä A, Luukko A (1995) Chernobyl-derived radiocaesium in fish as dependent on
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Stohl A, Seibert P, Wotawa G, Arnold D, Burkhart JF, Eckhardt S, Tapia C, Vargas A, Yasunari TJ
(2012) Xenon-133 and caesium-137 releases into the atmosphere from the Fukushima Dai-ichi
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Chapter 16

Radiocesium Concentrations and Body Size
of Freshwater Fish in Lake Hayama 1 Year
After the Fukushima Dai-Ichi Nuclear Power
Plant Accident
Kaori Takagi, Shoichiro Yamamoto, Keishi Matsuda, Atsushi Tomiya,
Masahiro Enomoto, Yuya Shigenobu, Ken Fujimoto, Tsuneo Ono,
Takami Morita, Kazuo Uchida, and Tomowo Watanabe

Abstract We measured radiocesium (134Cs + 137Cs) concentrations in five freshwater
fish species in Lake Hayama, Fukushima Prefecture, 1 year after the Fukushima Daiichi Nuclear Power Plant (FNPP) accident in March 2011. The five species included
bluegill (Lepomis macrochirus), Carassius spp. (Carassius auratus langsdorfii and
Carassius cuvieri), Japanese dace (Tribolodon hakonensis), largemouth bass
(Micropterus salmoides), and smallmouth bass (Micropterus dolomieu). We observed
a “positive size effect” for radiocesium concentrations in fish muscle, but the coefficient of determination was low for bluegill, Carassius spp., and Japanese dace. In
contrast, the coefficient of determination was high for the exponential relationship
between body size and radiocesium concentrations in largemouth and smallmouth
K. Takagi (*)
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
S. Yamamoto • K. Matsuda
National Research Institute of Aquaculture, Fisheries Research Agency,
2482-3 Chugushi, Nikko, Tochigi 321-1661, Japan
e-mail: ysho@affrc.go.jp
A. Tomiya • M. Enomoto
Fukushima Prefectural Inland Water Fisheries Experimental Station,
3447-1, Inawashiro, Maya, Fukushima 969-3283, Japan
Y. Shigenobu • K. Fujimoto • T. Ono • T. Morita
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
K. Uchida
Fisheries Research Agency, 2-3-3, Minatomirai, Nishi, Yokohama, Kanagawa 220-6115,
Japan
T. Watanabe
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi 985-0001, Japan
e-mail: wattom@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_16

201

202

K. Takagi et al.

bass. The geometric mean radiocesium concentration in each body size class was
generally higher for carnivorous fish than for omnivorous and herbivorous fish.
Keywords Bluegill • Carassius spp. • Japanese dace • Largemouth bass • Nuclear
accident • Positive size effect • Radiocesium concentration • Smallmouth bass

16.1

Introduction

The Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident released a large concentration of nuclides, including 131I, 134Cs, and 137Cs, into the atmosphere (Butler 2011;
Chino et al. 2011). The Tokyo Electric Power Co. (2012) estimated the total amount of
131 134
I, Cs, and 137Cs released during March 2011 to be approximately 500 PBq, approximately 10 PBq, and approximately 10 PBq, respectively. Because the half-life of 137Cs
is relatively long (30.2 years), contamination of the ecosystem is expected to be long
lasting. Following the Chernobyl nuclear power plant accident, research showed that
the chemical composition of the water (e.g., potassium levels) and the rate of circulation or turnover of water in freshwater systems affects the bioaccumulation of radiocesium in fish (Elliot et al. 1992; Saxén and Koskelainen 1992; Rask et al. 2012). In
addition to these environmental factors, fish body size is often correlated with radiocesium concentrations in fish (Elliot et al. 1992; Koulikov and Ryabov 1992; Smith et al.
2002). Fish body size may be a proxy for age and life stage, with the latter being associated with differences in traits such as feeding ecology and metabolism. The excretion
rates for radiocesium are higher in younger age groups than in older age classes.
Furthermore, the decrease in radiocesium concentrations in water over time also results
in lower radiocesium levels in younger fish (Kryshev and Ryabov 2000). Under these
conditions, it is likely that radiocesium levels in fish will be a positive function of size.
As described in Chapter 15, the Fisheries Research Agency has conducted radiocesium monitoring of freshwater fish, lake water, sediment, and plankton in three
lakes (Lake Akimoto, Lake Tagokura, and Lake Hayama) in Fukushima Prefecture
since 2012. Lake Hayama (Fig. 16.1), the lake nearest to the FNPP among the three
lakes, is a small artificially dammed lake (~60 m maximum depth, 36.2 × 106 m3
gross capacity of reservoir) in the Mano River system. This lake is located within a
30–50 km radius of the FNPP. The lake is also located in the area that was subject
to high levels of radiocesium deposition (~300–600 kBq/m2) in the period to 28
June 2012 (Ministry of Environment 2012a) as it was in the pathway of the radioactive plume from the FNPP. Indeed, Lake Hayama received the highest deposition of
radiocesium among the lakes that are locally important for recreational fishing.
The concentration of radiocesium decreased in the water of Lake Hayama
between the accident and 2012 (Chap. 15). Thus, we hypothesized that there would
be a positive relationship between radiocesium concentrations in fish and fish body
size in Lake Hayama. To test this, we measured radiocesium concentrations in individuals from the five dominant species in Lake Hayama in 2012, including bluegill
(Lepomis macrochirus), Carassius spp. (Carassius auratus langsdorfii and
Carassius cuvieri), Japanese dace (Tribolodon hakonensis), largemouth bass
(Micropterus salmoides), and smallmouth bass (Micropterus dolomieu).

16 Radiocesium Concentrations and Body Size of Freshwater Fish…
Fig. 16.1 Location of
collection sites in Lake
Hayama

140°
49′58 E

203

Miyagi
Pref.

37°
43′06 N

Sampling site

Lake
Hayama
FNPP

Lake Inawashiro

Fukushima
Pref.

30 km

50 km

Tochigi
Pref.

0

16.2

20 km

Ibaragi
Pref.

Pacific
Ocean

Fish Species and Lake Water

The five dominant fish species in Lake Hayama (bluegill, Carassius spp., Japanese
dace, largemouth bass, and smallmouth bass) were collected by gillnet during 2012
(see Chapter 15). Bluegill, largemouth bass, and smallmouth bass are invasive species. These three species have been observed in lakes and rivers in Fukushima
Prefecture since the 1990s. Smallmouth bass were the most dominant species in our
surveys in 2012. Largemouth bass and smallmouth bass are carnivorous whereas
bluegill, Carassius spp., and Japanese dace are omnivorous, and Carassius spp. is
also herbivorous. Although there are few biological data for Lake Hayama, the five
species we collected typically live for several years, so it is likely that some of the
fish we collected were exposed to the fallout at the time of the accident in 2011.
The environmental characteristics of Lake Hayama are described in Chapter 15.
The concentration of radiocesium in the surface water of Lake Hayama was 89
mBq/l from September to November 2012 (Table 15.2). According to the Ministry
of Environment (2011), 134Cs and 137Cs levels had declined to less than 1 Bq/l by
September 2011 in the surface water of Lake Hayama whereas levels at the bottom
of the lake were 10 and 12 Bq/l, respectively, at this time. From August to November
2012, levels of 134Cs and 137Cs decreased to less than 2 Bq/l and less than 3 Bq/l,
respectively, in the water immediately above the lake bed (Ministry of Environment
2012b, 2013a). Thus, radiocesium concentrations decreased rapidly in the water of
Lake Hayama during the first year after the fallout.

204

16.3

K. Takagi et al.

“Positive Size Effect” on Radiocesium Concentrations
in Five Freshwater Fish Species

The total length (TL) distribution for the five fish species is shown in Fig. 16.2. The
TL of bluegill, Carassius spp., and Japanese dace ranged from 86 to 163 mm, 217
to 461 mm, and 220 to 374 mm, respectively (Fig. 16.2). Both largemouth and
smallmouth bass had a wider range of TL, 80–545 mm and 79–457 mm, respectively (Fig. 16.2). Because we used gill nets to capture fish, it is likely that small
Carassius spp. and Japanese dace (TL < 200 mm) were not captured. Conversely,
small bluegill, smallmouth bass, and largemouth bass have a high body height so are

Fig. 16.2 Total length
(TL, mm) distribution for
bluegill (a), Carassius spp.
(b), Japanese dace (c),
largemouth bass (d), and
smallmouth bass (e)

8

n = 22

a

n = 71

b

n = 28

c

n = 36

d

n = 124

e

6
4
2
0
15
10
5

Number of fish

0
8
6
4
2
0
10
8
6
4
2
0
15
10
5
0

100

200

300

400

500

Total length (mm)

600

16 Radiocesium Concentrations and Body Size of Freshwater Fish…

205

more susceptible to capture in our gill nets. The small-sized Carassius spp. and
Japanese dace represent younger fish including age 0 and 1 (Suzuki and Kimura
1977; Liu et al. 1986; Ishizaki et al. 2009).
Judging from our data and the information of age and growth for largemouth and
smallmouth bass (Yodo and Kimura 1996; Nakamura et al. 2004), we assume that
the samples of these two species included age 0 and older fish. The bluegill we captured were likely older than age 0, although their growth varies considerably with
population size structure (Drake et al. 1997; Belk 1995). Taken together, these
observations suggest that we obtained both age 0 and older fish only for largemouth
and smallmouth bass.
The radiocesium (134Cs + 137Cs) concentrations were generally lower in smaller
fish than in larger fish (Fig. 16.3). The natural log of radiocesium concentrations
Fig. 16.3 Relationship
between total length (TL)
of fish and radiocesium
(134Cs + 137Cs) concentrations
for bluegill (open triangles),
Carassius spp. (crosses), and
Japanese dace (open circles)
(a), largemouth bass (b), and
smallmouth bass (c). There
was an exponential
relationship between
radiocesium concentrations
and TL in largemouth bass
(b) and smallmouth bass (c)

206

K. Takagi et al.

were positively but poorly correlated with TL for bluegill (R2 = 0.30, p < 0.01),
Carassius spp. (R2 = 0.23, p < 0.01), and Japanese dace (R2 = 0.30, p < 0.01), species
for which we were unable to collect younger fish. Conversely, we observed a strong
positive exponential correlation between TL and radiocesium concentrations in
largemouth bass (R2 = 0.96, p < 0.01) and smallmouth bass (R2 = 0.77, p < 0.01)
(Fig. 16.3).

16.4

Influence of Diet on Radiocesium Concentrations
in Freshwater Fish

Both younger and older fish are needed to detect the positive size effect described
by Kryshev and Ryabov (2000). We found evidence for a positive size effect in
carnivorous bass, the only species for which we were able to obtain both young and
old individuals. We compared the radiocesium levels in fish from different trophic
positions, although we only collected older individuals from omnivorous and herbivorous species.
The geometric mean radiocesium concentrations by body size class (interval of
100 mm TL) for each species are given in Table 16.1. The geometric mean radiocesium concentration in each size class (n > 2) was higher for carnivorous fish than for
omnivorous or herbivorous fish, suggesting that trophic position is an important
determinant of species-specific concentrations. Only two exceptions to this pattern
were observed, in bluegill in the 100 mm < TL ≤ 200 mm size class, and in Japanese
dace in the 200 mm < TL ≤ 300 mm size class. Such exceptions may be a function of
different life stages; adult (older) omnivorous and herbivorous fish have higher levels than younger carnivorous fish.
We speculate that the larger largemouth and smallmouth bass individuals, which
had relatively high radiocesium concentrations, were adults at the time the FNPP
accident occurred. These individuals have likely preyed continuously upon
radiocesium-contaminated insects and fishes since the time of the accident. Because
of their low rate of metabolism, much of the radiocesium was retained within their
body during the year following the fallout. In contrast, smaller bass (≤200 mm TL)
were likely juveniles (1 year old or younger), larvae, eggs, or did not exist at the
time of the FNPP accident. Even if these younger individuals consumed highly
contaminated prey items after the fallout from the FNPP, they would still likely have
lower radiocesium concentrations than older fish because of their high metabolic
rate and dilution resulting from tissue growth.
The radiocesium concentrations in fish were variable, but generally high in the
diet items of omnivorous and herbivorous fish, such as bluegill, Carassius spp., and
Japanese dace in 2012. Radiocesium concentrations in Spirogyra and aquatic insects
fluctuated from 94 to 1,870 Bq/kg wet weight and from 92 to 1,100 Bq/kg wet
weight, respectively (Ministry of Environment 2012c, 2013b, c, d). Thus, the
concentration of radiocesium in Spirogyra was as high as in small fish (≤200 mm
TL) in our study (Table 16.1). Given this, even herbivorous Carassius spp. are susceptible to radiocesium.

Total length (TL, mm)
0 < TL ≤ 100
100 < TL ≤ 200
200 < TL ≤ 300
300 < TL ≤ 400
400 < TL ≤ 500
500 < TL ≤ 600
Total

Carassius spp.
Geometric mean Cs
(Bq/kg-wet) ± δ (n)
–(0)
–(0)
730 ± 1.5 (15)
1,250 ± 1.4 (30)
1,360 ± 1.4 (26)
–(0)
1,150 ± 1.5 (71)

Japanese dace
Geometric mean Cs
(Bq/kg-wet) ± δ (n)
–(0)
–(0)
1,670 ± 1.5 (16)
2,110 ± 1.3 (12)
–(0)
–(0)
1,850 ± 1.5 (28)

Largemouth bass
Geometric mean Cs
(Bq/kg-wet) ± δ (n)
340 ± 1.2 (14)
470 ± 1.2 (9)
849 ± 1.1 (2)
826 (1)
3,440 ± 1.3 (8)
5,450 ± 1.0 (2)
776 ± 2.8 (36)

Smallmouth bass
Geometric mean Cs
(Bq/kg-wet) ± δ (n)
404 ± 1.2 (7)
639 ± 1.3 (2)
1,220 ± 1.5 (10)
2,510 ± 1.8 (69)
1,360 ± 1.4 (36)
–(0)
1,150 ± 1.5 (124)

Cs + 137Cs) concentration (Bq/kg-wet) ± geometric standard deviation (δ) for each fish species by fish body

134

Bluegill
Geometric mean Cs
(Bq/kg-wet) ± δ (n)
188 ± 1.1 (5)
537 ± 1.5 (17)
–(0)
–(0)
–(0)
–(0)
423 ± 1.8 (22)

Table 16.1 Geometric mean radiocesium (Cs:
size class

16 Radiocesium Concentrations and Body Size of Freshwater Fish…
207

208

K. Takagi et al.

Lake Hayama was located in the zone of high radiocesium deposition, so fish are
likely exposed to radiocesium from the surrounding forest ecosystem. Compared
with European forests, the forests in Japan experience a warmer climate with higher
mean annual precipitation. These differences make it likely that Japanese forests
will circulate radiocesium deposited by the FNPP accident more rapidly than did
the European forests following the Chernobyl accident (Hashimoto et al. 2013).
Indeed, the levels of radiocesium in trees dropped rapidly during the first 2 years
after the fallout, but radiocesium in the soil surface organic layer and soil surface
layer (0–5 cm) components kept the same level during 2012–2013 (Forestry Agency
2014). During this period, fish in Lake Hayama were likely exposed to radiocesium
from the organic components of the surrounding forest through the food web.
Further monitoring of radiocesium concentrations in fish (including information on
body size and age) is needed to predict the long-term dynamics of radiocesium
concentrations in fish.
Acknowledgments This chapter was written based on Takagi et al. (accepted).
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Chapter 17

Spatiotemporal Monitoring of 134Cs and 137Cs
in Ayu, Plecoglossus altivelis, a MicroalgaeGrazing Fish, and in Their Freshwater
Habitats in Fukushima
Jun-ichi Tsuboi, Shin-ichiro Abe, Ken Fujimoto, Hideki Kaeriyama,
Daisuke Ambe, Keishi Matsuda, Masahiro Enomoto, Atsushi Tomiya,
Takami Morita, Tsuneo Ono, Shoichiro Yamamoto, and Kei’ichiro Iguchi

Abstract Ayu, Plecoglossus altivelis, is a herbivorous fish that is an important fishery resource and a key component of the food web in many Japanese streams. After
the Fukushima Daiichi Nuclear Power Plant (FNPP) accident in March 2011, ayu
were exposed to highly contaminated silt while feeding on benthic microalgae
attached to riverbed stones. To understand the effects of radioactive contamination
on ayu, radiocesium (134Cs + 137Cs) concentrations were analyzed in riverbed samples (microalgae and silt) and in the internal organs and muscle of ayu in five river
systems in the Fukushima Prefecture between summer 2011 and autumn 2013. The
concentrations of radiocesium in both the internal organs and the muscles of ayu
declined over time. The radiocesium concentrations in the muscle were correlated
with, but much lower than, those in the internal organs. The concentrations in the
internal organs were correlated with those in the riverbed samples. The concentrations in the muscle were further correlated with ayu body size. Our results suggest
J. Tsuboi (*) • K. Matsuda • S. Yamamoto
National Research Institute of Aquaculture, Fisheries Research Agency,
2482-3 Chugushi, Nikko, Tochigi 321-1661, Japan
e-mail: tsuboi118@affrc.go.jp
S. Abe
Japan Sea National Fisheries Research Institute, Fisheries Research Agency,
5939-22, 1, Suido-cho, Chuo-ku, Niigata Niigata 951-8121, Japan
K. Fujimoto • H. Kaeriyama • D. Ambe • T. Morita • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
M. Enomoto • A. Tomiya
Fukushima Prefectural Inland Water Fisheries Experimental Station,
3447-1, Inawashiro, Maya, Fukushima 969-3283, Japan
K. Iguchi
Faculty of Environmental Studies, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki,
Nagasaki 852-8521, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_17

211

212

J. Tsuboi et al.

that ayu ingest radiocesium while consuming silt and microalgae from the riverbed,
and that a small proportion (about 15 %) is assimilated into the muscle of the fish.
Keywords Bioaccumulation • Soil contamination • Nuclear accident • Radioactive
cesium • Ayu

17.1

Introduction

Ayu (Plecoglossus altivelis) is a herbivorous fish that is distributed throughout the
Japanese Archipelago (Iguchi et al. 1999) (Fig. 17.1). The species exhibits an amphidromous and annual life cycle. After the winter juvenile stage in the sea, young
ayu migrate into rivers and graze on benthic microalgae attached to the riverbed
(Iguchi and Hino 1996). Ayu are also an important resource for humans and for
avian species, such as the great cormorant Phalacrocorax carbo (Takahashi et al.
2006); therefore, the radionuclide contamination of ayu may have a significant
effect on both humans and aquatic and terrestrial ecosystems. In Fukushima
Prefecture, Iguchi et al. (2013) reported high levels of radionuclide contamination
in the riverbed sediments. Ayu ingest silt while grazing on benthic microalgae,
exposing themselves to the radiation from the contaminated sediments, including
the silt component.

Fig. 17.1 Ayu feed on benthic microalgae attached to the riverbed, grazing it off the rocks with
their teeth

17 Spatiotemporal Monitoring of 134Cs and 137Cs in Ayu, Plecoglossus altivelis…

213

The aerosol-bound Cs was deposited on land and became integrated into the
surface soil within 2 months after the Fukushima Daiichi Nuclear Power Plant
(FNPP) disaster (Masson et al. 2011; Hirose 2012; Yasunari et al. 2011).
Radionuclides subsequently spread over central and northern Honshu, Japan. The
rivers in Honshu typically have steep gradients and are subject to erosion during
snowmelt and typhoons (Yoshimura et al. 2005). As a result, contaminated soils
were transported by the rivers from the mountains to the plains in Fukushima
Prefecture (Evrard et al. 2013). To understand the route by which herbivorous fish
are exposed to radiocesium, we measured radiocesium concentrations in riverbed
samples (microalgae and silt) and in the internal organs and muscle of ayu in
Fukushima Prefecture.

17.2

Relationship Between the Radiocesium Concentrations
in Ayu Internal Organs and Muscle

Ayu (n = 166; fork length, 68–206 mm) were collected from five rivers in the
Fukushima Prefecture by casting nets (periphery, 16 m; mesh size, 9 mm) between
9 July 2011 and 14 October 2013 (Fig. 17.2). The Niida and Kido Rivers were not

38ºN

N

AK

E

W
S

NI
FNPP

KD

OK

SM

37ºN

20Km
140ºE

141ºE

Fig. 17.2 Location of collection sites for ayu and riverbed samples (NI Niida River, KD Kido
River, AK Abukuma River, SM Same River, OK Okawa River). The symbol for each site corresponds to those in Figs. 17.4 and 17.5

214

J. Tsuboi et al.

Fig. 17.3 1 River water, 2 muddy sediment, 3 riverbed samples, and 4 ayu were sampled in five
rivers between 2011 and 2013

sampled before May 2012 because of concerns about radiation safety in those areas.
Collections of water, sediment, and riverbed samples, consisting primarily of benthic microalgae and silt, were made simultaneously at each site (Fig. 17.3) [see
Tsuboi et al. (2015) for more details]. Radiocesium was detected in all 36 water and
muddy sediment samples, 34 of 36 riverbed samples, and 119 internal organs and
98 muscle samples from 166 fish.
In 2013 the median 134Cs/137Cs ratio was 0.46 in all analyzed samples, which is
identical to the value 2 years after the fallout from the FNPP. Radiocesium was
detected in both the internal organs and the muscle of 84 individuals. Although there
was a positive correlation between the concentrations of radiocesium in the internal
organs and the muscle of ayu (r = 0.746, p = 0.006), the median concentration in the
muscle was 14.5 % that of the median concentration in the internal organs (n = 84,
p < 0.001). Thus, a small proportion (about 15 %) of the radiocesium ingested from
the riverbed appears to be transferred to the muscle. Cesium strongly interacts with
clay minerals, especially vermiculite and illite minerals (Comans
and Hockley 1992). Furthermore, leaching experiments have demonstrated that
radiocesium is relatively insoluble in the river suspended sediment in Fukushima,
and that the adsorption of radiocesium to the suspended sediment was irreversible
(Tanaka et al. 2013). Therefore, most of the radiocesium in the silt ingested by ayu
is unlikely to be absorbed but will instead be excreted.

17 Spatiotemporal Monitoring of 134Cs and 137Cs in Ayu, Plecoglossus altivelis…

17.3

215

Biological and Environmental Factors Involved
in the Temporal Pattern of Radiocesium Contamination

To evaluate temporal changes in 134Cs and 137Cs concentrations in water, muddy
sediment, and ayu, we fitted a generalized linear mixed model (GLMM) with a
Gaussian distribution of errors. The GLMM results suggest that the radiocesium
concentrations in the muddy sediment but not river water have declined through
time (river water: t = −1.016, p = 0.318; muddy sediment: t = −3.131, p = 0.004)
(Figs. 17.4 and 17.5). The radiocesium concentrations have declined through time

134Cs

+ 137Cs (mBq/L)

1000

NI
KD
AK
SM
OK

100

10

1
2011/03/11

2012/03/11

2013/03/11

Sampling date

Fig. 17.4 Time-series of radiocesium concentrations in the river water. Symbols correspond to the
collection sites in Fig. 17.2 (NI Niida River, KD Kido River, AK Abukuma River, SM Same River,
OK Okawa River)

134

Cs + 137Cs (Bq/kg-dry)

10000

NI
KD
AK
SM
OK

1000

100

10

1
2011/03/11

2012/03/11

2013/03/11

Sampling date
Fig. 17.5 Time-series of radiocesium concentrations in muddy sediment. Symbols correspond to
the collection sites in Fig. 17.2 (NI Niida River, KD Kido River, AK Abukuma River, SM Same
River, OK Okawa River)

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J. Tsuboi et al.

in both the internal organs and muscle of ayu (internal organs: t = −3.855, p < 0.001;
muscle: t = −2.809, p = 0.006) (Fig. 17.6). The concentrations in the internal organs
of ayu were positively correlated with those in the riverbed samples (i.e., fish prey)
that were collected simultaneously with the ayu (t = 8.197, p < 0.001). In contrast,
there was no correlation between the concentrations in the ayu muscle and the riverbed samples (t = −1.202, p = 0.261; Fig. 17.6). Thus, we conclude that herbivorous
fish assimilate radiocesium from the microalgae and silt on the riverbed stones as
they forage. Between 2011 and 2013, the activity concentration of radiocesium in
the internal organs and the muscle of ayu declined, mainly because of the half-life
of 134Cs (2.07 years), which is considerably shorter than the 30.1 years for 137Cs.
However, the concentration of 137Cs in the whole ayu body tended to decrease during 2011 (Iguchi et al. 2013). Therefore, the decrease in the concentration of 137Cs
in ayu cannot be explained only by the half-life of 134Cs. The activity concentration
of 137Cs in the internal organs, which represented the majority of the 137Cs in ayu,
was correlated with that in the riverbed samples. Therefore, the decrease of 137Cs in
the riverbed, which may have been caused by flushing out of the contaminated soil
from the mountains, would explain the decrease of 137Cs in ayu. In European lakes,
137
Cs concentrations in fish muscle peaked a few years after the Chernobyl disaster
(Jonsson et al. 1999; Smith et al. 2000). Then, the rate of decrease in muscle 137Cs
concentrations was initially rapid, but later slowed. Conversely, in the rivers of
Fukushima, the radiocesium contamination levels in ayu peaked immediately after
the FNPP accident. The concentrations then decreased slowly, fluctuating with the
transport of fresh polluted sediment from the mountains following snowmelt and
typhoon events (Figs. 17.5 and 17.6).
Ayu fork length was correlated not with concentrations of radiocesium in the
internal organs but with that in the muscle (internal organs: t = −1.168, p = 0.246;
muscle: t = 4.329, p < 0.001). The concentration of 137Cs in fish increases with fish
size according to a power law relationship because of changes in prey items (Smith
et al. 2002). For instance, the concentration in northern pike (Esox lucius) increased
as the trophic level of prey increased from plankton to invertebrates and then to
small fish. Indeed, the level of radiocesium contamination in fish at Fukushima
increased according to the order herbivores (i.e., ayu) < omnivores < piscivores at
Fukushima (Mizuno and Kubo 2013). A positive correlation was also observed for
ayu body size relative to the muscle concentration of radiocesium. Thus, in this
case, the positive correlation between ayu body size and radiocesium concentrations
in their muscle could not be explained by a change in feeding patterns because the
prey size and the prey items do not change as the ayu grows. Also, the time (season)
of collection had no effect on the activity concentrations of radiocesium in ayu
muscle. The activity concentration of radiocesium in fish is a function of uptake and
elimination rates. In hatchery-reared ayu, assimilation efficiency decreases as the
fish grow (Akutsu et al. 2001). Larger ayu therefore need much more food per unit
weight gain than smaller individuals. Thus, at our study site, larger ayu have greater
potential to accumulate radiocesium from microalgae on the riverbed stones than
smaller ayu.

17 Spatiotemporal Monitoring of 134Cs and 137Cs in Ayu, Plecoglossus altivelis…
Fig. 17.6 Time-series of
radiocesium concentrations in
the riverbed samples (i.e., fish
dietary items; cross symbols)
and the internal organs (i.e.,
stomach contents, stomach,
gut contents, gut, liver,
spleen, gonad; solid symbols)
and the muscle (open
symbols) samples from ayu
collected in the five rivers (NI
Niida River, KD Kido River,
AK Abukuma River, SM
Same River, OK Okawa
River)

10000 NI
1000
100
10
1
10000 KD
1000
100
10

134

Cs +137Cs (Bq/kg-wet)

1
10000 AK
1000
100
10
1
10000 SM
1000
100
10
1
10000 OK
1000
100
10
1
2011/03/11

2012/03/11

2013/03/11

Sampling date

217

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J. Tsuboi et al.

The overall radiocesium concentrations have declined with time in both the internal organs and muscle of ayu (Fig. 17.6). However, in some rivers surveyed, the
radiocesium concentrations in the whole ayu body (i.e., internal organ and muscle)
exceeded the Japanese standard limit for radiocesium in foods (100 Bq/kg-wet).
Thus, fishing activities were banned in three of the five rivers during the sampling
periods of this study (Niida, Kido, and Abukuma Rivers). Spatiotemporal monitoring of the levels of radiocesium in freshwater ecosystems, in areas close to human
centers, should continue to increase our understanding of the long-term dynamics of
radionuclide contamination and to reveal the effects on the biological and environmental characteristics of each ecosystem.
Acknowledgements This chapter was revised from a paper published by Tsuboi et al. (2015).
The authors are grateful to Masato Murakami and Tomoko Okazaki for their assistance with the
sample assays and data analyses. They also thank Kaoru Nakata and Kazuo Uchida for critical
review of the manuscript. This study was supported by the Fisheries Agency, Ministry of
Agriculture, Forestry and Fisheries, Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

References
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Tochigi Pref Fish Exp Stat 44:3–4 (in Japanese)
Comans RNJ, Hockley DE (1992) Kinetics of cesium sorption on illite. Geochim Cosmochim
Acta 56:1157–1164
Evrard O, Chartin C, Onda Y, Patin J, Lepage H, Lefèvre I, Ayrault S, Ottlé C, Bonté P (2013)
Evolution of radioactive dose rates in fresh sediment deposits along coastal rivers draining
Fukushima contamination plume. Sci Rep 3:3079
Hirose K (2012) Fukushima Dai-ichi nuclear power plant accident: summary of regional radioactive deposition monitoring results. J Environ Radioact 111:13–17
Iguchi K, Hino T (1996) Effect of competitor abundance on feeding territoriality in a grazing fish,
the ayu Plecoglossus altivelis. Ecol Res 11:165–173
Iguchi K, Tanimura Y, Takeshima H, Nishida M (1999) Genetic variation and geographic population structure of amphidromous ayu Plecoglossus altivelis as examined by mitochondrial DNA
sequencing. Fish Sci 65:63–67
Iguchi K, Fujimoto K, Kaeriyama H, Tomiya A, Enomoto M, Abe S, Ishida T (2013) Cesium-137
discharge into the freshwater fishery ground of grazing fish, ayu Plecoglossus altivelis, after
the March 2011 Fukushima nuclear accident. Fish Sci 79:983–988
Jonsson B, Forseth T, Ugedal O (1999) Chernobyl radioactivity persists in fish. Nature (Lond)
400:417
Masson O, Baeza A, Bieringer J, Brudecki K, Bucci S, Cappai M, Carvalho FP, Connan O, Cosma
C, Dalheimer A, Didier D, Depuydt G, De Geer LE, Vismes AD, Gini L, Groppi F, Gudnason
K, Gurriaran R, Hainz D, Haldórsson O, Hammond D, Hanley O, Holeý K, Zs H, Ioannidou A,
Isajenko K, Jankovic M, Katzlberger C, Kettunen M, Kierepko R, Kontro R, Kwakman PJM,
Lecomte M, Leon Vintro L, Leppänen AP, Lind B, Lujaniene G, Ginnity PM, Mahon CM,
Malá H, Manenti S, Manolopoulou M, Mattila A, Mauring A, Mietelski JW, Møller B, Nielsen

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SP, Nikolic J, Overwater RMW, Pálsson SE, Papastefanou C, Penev I, Pham MK, Povinec PP,
Ramebäck H, Reis MC, Ringer W, Rodriguez A, Rulík P, Saey PRJ, Samsonov V, Schlosser C,
Sgorbati G, Silobritiene BV, Söderström C, Sogni R, Solier L, Sonck M, Steinhauser G,
Steinkopff T, Steinmann P, Stoulos S, Sýkora I, Todorovic D, Tooloutalaie N, Tositti L,
Tschiersch J, Ugron A, Vagena E, Vargas A, Wershofen H, Zhukova O (2011) Tracking of
airborne radionuclides from the damaged Fukushima Dai-ichi nuclear reactors by European
networks. Environ Sci Technol 45:7670–7677
Mizuno T, Kubo H (2013) Overview of active cesium contamination of freshwater fish in
Fukushima and eastern Japan. Sci Rep 3:1742
Smith JT, Comans RNJ, Beresford NA, Wright SM, Howard BJ, Camplin WC (2000) Chernobyl’s
legacy in food and water. Nature (Lond) 405:141
Smith JT, Kudelsky AV, Ryabov IN, Daire SE, Boyer L, Blust RJ, Fernandez JA, Hadderingh RH,
Voitsekhovitch OV (2002) Uptake and elimination of radiocaesium in fish and the “size effect”.
J Environ Radioact 62:145–164
Takahashi T, Kameda K, Kawamura M, Nakajima T (2006) Food habits of great cormorant
Phalacrocorax carbo hanedae at Lake Biwa, Japan, with special reference to ayu Plecoglossus
altivelis. Fish Sci 72:477–484
Tanaka K, Sakaguchi A, Kanai Y, Tsuruta H, Shinohara A, Takahashi Y (2013) Heterogeneous
distribution of radiocesium in aerosols, soil and particulate matters emitted by the Fukushima
Daiichi Nuclear Power Plant accident: retention of micro-scale heterogeneity during the migration of radiocesium from the air into ground and river systems. J Radioanal Nucl Chem
295:1927–1937
Tsuboi J, Abe S, Fujimoto K, Kaeriyama H, Ambe D, Matsuda K, Enomoto M, Tomiya A,
Morita T, Ono T, Yamamoto S, Iguchi K (2015) Exposure of a herbivorous fish to 134Cs and
137
Cs from the riverbed following the Fukushima disaster. J Environ Radioact 141:32–37
Yasunari TJ, Stohl A, Hayano RS, Burkhart JF, Eckhardt S, Yasunari T (2011) Cesium-137 deposition and contamination of Japanese soils due to the Fukushima nuclear accident. Proc Natl
Acad Sci U S A 108:19530–19534
Yoshimura C, Omura T, Furumai H, Tockner K (2005) Present state of rivers and streams in Japan.
River Res Appl 21:93–112

Chapter 18

Radiocesium Concentrations in the Muscle
and Eggs of Salmonids from Lake Chuzenji,
Japan, After the Fukushima Fallout
Shoichiro Yamamoto, Tetsuya Yokoduka, Ken Fujimoto, Kaori Takagi,
and Tsuneo Ono

Abstract Approximately 18 months (September–December 2012) after the
Fukushima Dai-ichi Nuclear Power Plant accident, elevated radiocesium concentrations were detected in muscle and egg samples from masu salmon (Oncorhynchus
masou), kokanee (Oncorhynchus nerka), brown trout (Salmo trutta), and lake trout
(Salvelinus namaycush) from the Lake Chuzenji system, central Honshu Island,
Japan (160 km from the station). Mean muscle concentrations were 142.9–249.2 Bq/
kg-wet, and mean egg concentrations were 38.7–79.0 Bq/kg-wet. No relationship
between fork length and muscle radiocesium concentration was observed in any of
the species, but significant relationships were found between individual muscle and
egg radiocesium concentrations from masu salmon, brown trout, and lake trout.
Keywords Brown trout • Kokanee • Lake trout • Masu salmon • Nuclear accident

S. Yamamoto (*)
National Research Institute of Aquaculture, Fisheries Research Agency,
2482-3 Chugushi, Nikko, Tochigi 321-1661, Japan
e-mail: ysho@affrc.go.jp
T. Yokoduka
Tochigi Prefectural Fisheries Experimental Station,
Sarado, Ohtawara, Tochigi 324-0404, Japan
K. Fujimoto • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
K. Takagi
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
e-mail: takagik@affrc.go.jp
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_18

221

222

18.1

S. Yamamoto et al.

Introduction

A Japanese governmental agency (Fisheries Agency) and local governments initiated monitoring programs soon after the Fukushima fallout to monitor radioactivity
contamination in freshwater and marine fish and invertebrates in the affected areas.
The results revealed that radiocesium contamination was transferred quickly to
freshwater and marine ecosystems, and elevated radiocesium concentrations were
detected in many fish and invertebrates (Fisheries Agency 2012). These concentrations decreased over time in most of the epipelagic fish and neustonic organisms
(Buesseler 2012). However, some demersal fish off the coast of Fukushima and
some freshwater fish in central and northern Honshu Island continue to exhibit
higher radiocesium concentrations (Tateda et al. 2013). Freshwater masu salmon
(Oncorhynchus masou) from the Niida River in Fukushima Prefecture contained the
highest measured radiocesium concentrations in March 2012 (18,700 Bq/kg-wet
weight; Fisheries Agency 2012). Restrictions have been placed on shipping and
consumption of 19 commercially important freshwater fish and invertebrate species
as of October 2013 in the extensive deposition area of central and northern Honshu
Island.
Because of differences in osmoregulatory physiology, radionuclides usually bioaccumulate at higher concentrations in freshwater compared with marine fish. After
the Chernobyl nuclear accident (Ukraine), higher radiocesium concentrations persisted in freshwater fish from several European lakes for 10 years and more (Jonsson
et al. 1999; Brittain and Gjerseth 2010; Rask et al. 2012). Lake-dwelling freshwater
fish in high deposition areas may also sustain long-standing radionuclide contamination, which results from radionuclide recycling within the aquatic environment
(Smith and Comans 1996). In this chapter, we describe radiocesium concentrations
in muscle and eggs of masu salmon, kokanee, O. nerka; brown trout, Salmo trutta;
and lake trout, Salvelinus namaycush, from the Lake Chuzenji system, central
Honshu Island, Japan (Fig. 18.1) to understand the effects of radionuclide
contamination on salmonid fish. Although Lake Chuzenji is approximately 160 km
from the Fukushima Dai-ichi Nuclear Power Plant (FNPP) in linear distance, the
lake watershed area received radiocesium deposits of 8–36 kBq/m2 after the
Fukushima accident (Fisheries Research Agency 2012). Salmonid fish support
important recreational and commercial fisheries throughout the Japanese
Archipelago. Salmonid eggs (usually raw eggs) are also an important food resource
for the Japanese.

18

Radiocesium Concentrations in the Muscle and Eggs of Salmonids…

223

Fig. 18.1 A photograph of Lake Chuzenji

18.2

Study Area (Lake Chuzenji)

Lake Chuzenji (36°44′ latitude, 139°27′ longitude) is an oligotrophic, cold-water
lake system located in Nikko, Kanto District, Japan (mean surface water quality:
pH, 8.2; chemical oxygen demand, 1.4 mg/l; total phosphorus, 0.004 mg/l; total
nitrogen, 0.26 μg/l; chlorophyll a, 2.4 μg/l) (Tochigi Prefecture Japan 2012). At
1,269 m above sea level, it is the highest major natural lake in Japan. It is approximately 11.5 km2 in surface area and 163 m in maximum depth (Yokoyama and
Yamamoto 2012). The water turnover rate is about 6 years. No fish originally inhabited Lake Chuzenji. However, many freshwater fish, mostly salmonids, have been
introduced repeatedly since 1873. The lake system is currently inhabited by four
exotic salmonids, namely brook trout, Salvelinus fontinalis; lake trout, brown trout,
rainbow trout, O. mykiss; and three native Japanese salmonids, white-spotted charr,
Salvelinus leucomaenis; masu salmon, and kokanee. Different masu salmon subspecies (O. masou masou and O. masou subsp.) were introduced in the 1880s. The
current thinking is that the masu salmon in Lake Chuzenji are an admixture of two
subspecies or a hybrid between two subspecies and are often referred to as
“Honmasu” (Munakata et al. 1999). Detailed descriptions of Lake Chuzenji and its
fish fauna are provided in Yamamoto et al. (2010) and Yokoyama and Yamamoto
(2012).

224

18.3

S. Yamamoto et al.

Muscle Radiocesium Concentrations in Salmonid Fish

Mature female masu salmon, kokanee, brown trout, and lake trout were collected
from Lake Chuzenji using angling gear and gill nets from October to December
2012. Masu salmon and kokanee that were migrating upstream for spawning during
September–October 2012 were collected from a weir located in a Lake Chuzenji
inlet stream that passes through Fisheries Research Agency (FRA) property. Streamdwelling S. trutta were also collected using electrofishing equipment from the
Toyama Stream, a main Lake Chuzenji inlet stream (Fig. 18.2).
Mean radiocesium concentrations (134Cs + 137Cs) in muscle of masu salmon,
kokanee, brown trout, and lake trout collected from the lake were 236.5 ± 57.2 [Bq/
kg-wet ± standard deviation (SD), n = 13], 149.9 ± 19.6 (n = 13), 249.2 ± 39.6 (n = 10),
and 146.9 ± 52.2 (n = 7), respectively (Fig. 18.3). The relationship between fork
length and radiocesium concentration was not statistically significant for any of the
four species (r = 0.24–0.59, P < 0.05). Mean muscle radiocesium concentration (±
SD) in brown trout samples collected from the inlet stream was 36.7 ± 15.6 Bq/kgwet (n = 10). The difference in radiocesium concentration between lake- and streamdwelling brown trout was statistically significant (F = 248.93, d.f. = 1,18, P < 0.001).
A significant difference in muscle radiocesium concentration was observed among
the four species collected from the lake (F = 16.38, d.f. = 3,38, P < 0.01). Masu
salmon and brown trout had higher radiocesium concentrations than those of
kokanee and lake trout (Bonferroni multiple comparisons).
Mean muscle radiocesium concentrations in the four species measured during
the study period were 142.9–249.2 Bq/kg. Muscle radiocesium concentrations were
also greater than 100 Bq/kg in co-distributed species [rainbow trout, freshwater
goby, Rhinogobius sp., and smelt (whole body) Hypomesus nipponensis; Fisheries
Agency 2012; Fisheries Research Agency 2012]. The Ministry of Health, Labor,
and Welfare, Japan placed restrictions on shipping fish with more than 100 Bq/kg
radiocesium. All salmonid fishing activities, except for catch-and-release, were prohibited in Lake Chuzenji as of June 2014.
Muscle radiocesium concentrations differed among species and between habitats
within species. Lake Chuzenji masu salmon and brown trout had higher radiocesium concentrations than those of kokanee and lake trout. Lake-dwelling brown
trout had much higher concentrations than those of inlet stream-dwelling brown
trout. These differences may be related to differences in species-specific food intake
or food availability or both. Radiocesium accumulation in freshwater fish organs
results mainly from food intake (Hewett and Jefferies 1976; Forseth et al. 1991;
Ugedal et al. 1995; Yamamoto et al. 2014a). Lake Chuzenji kokanee consume
mostly zooplankton or chironomid larvae, whereas masu salmon, brown trout, and
lake trout are omnivorous (Japan Fisheries Resource Conservation Association
2003, 2008). Higher radiocesium concentrations were found in benthic fish from
Lake Chuzenji during September–November 2012 compared with zooplankton
species (Fisheries Research Agency 2012). A case study of a Norwegian lake
conducted after the Chernobyl reactor accident showed that brown trout feeding
mostly on zoobenthos had higher radiocesium concentrations compared with those

18

225

Radiocesium Concentrations in the Muscle and Eggs of Salmonids…

37° N

Yukawa Stream
36° N
Tone R.

35° N
Pacific Ocean

Toyama Stream

139° E

FRA

141° E

140° E

Lake Chuzenji

Yanagi Stream

Kegon Fall

Radiocesium concentrations in muscle (Bq/kg-wet)

Fig. 18.2 Location of the Lake Chuzenji system, where the study was conducted

400

400

a

300

300

200

200

100

100

0
300
180

c

0
350

400

450

500

0
250

b

200

160

200

400

600

d

150
140
100
120
100
200

50
250

300

350

400

0
400

500

600

700

800

Fork Length (mm)
Fig. 18.3 Relationships between fork length and radiocesium concentrations in muscle of masu
salmon (a), kokanee (b), brown trout (c), and lake trout (d) collected in Lake Chuzenji, Japan, from
September to November 2012. Solid triangles indicate brown trout collected from the Lake
Chuzenji inlet stream

226

S. Yamamoto et al.

of sympatric Arctic charr (Salvelinus alpinus), which are planktonic feeders (Forseth
et al. 1991). Segregated habitats with different dominant prey species could also
cause differences in radiocesium accumulation in freshwater fish; Lake Chuzenji
brown trout mainly prey on benthic gobies and smelt (Japan Fisheries Resource
Conservation Association 2003), whereas inlet stream-dwelling brown trout feed on
aquatic and terrestrial insects.
Radiocesium concentrations varied individually in the four salmonid species,
regardless of body size. The variation was more pronounced in omnivorous masu
salmon, brown trout, and lake trout than that in the planktonic kokanee. Radiocesium
concentrations also varied within salmonid food items. For example, in October–
November 2012, Lake Chuzenji Ephyra sp. shrimp contained 128–132 Bq/kg
(134Cs + 137Cs), Palaemon sp. shrimp contained 47–94 Bq/kg, the freshwater sculpin
Cottus reinii contained 166–211 Bq/kg, and freshwater goby contained 86–145 Bq/kg
(Yamamoto and Yokoduka, unpublished data). These species are major food sources
for masu salmon, brown trout, and lake trout. Size-independent individual variations in diet composition may be one of the most important factors affecting variations in radiocesium accumulation, as suggested by Ugedal et al. (1995), who
examined Arctic charr and brown trout in a Norwegian lake.
Mean radiocesium concentration in lake trout, which prey mainly on small fish and
aquatic insects, was lower than that in masu salmon and lake-dwelling brown trout.
Therefore, diet composition does not completely explain the observed radiocesium
accumulation patterns. Differences in metabolic rates could also partially explain differences between fish species. Metabolic rate, which is dependent on water temperature, could affect radionuclide intake, retention, and excretion rates (Elliott et al. 1992;
Ugedal et al. 1992) and thus predicts ecological half-life (Doi et al. 2012). We did not
collect data on the metabolic rates of lake trout or the other co-distributed salmonids
in Lake Chuzenji. However, lake trout are larger at maturity than other species, which
would affect metabolic rate, food intake, and radiocesium excretion rates.

18.4

Radiocesium Concentrations in Salmonid Eggs

Mean radiocesium concentrations (134Cs + 137Cs) in masu salmon, kokanee, brown
trout, and lake trout eggs were 79.0 ± 19.1 (Bq/kg-wet ± SD, n = 13), 53.8 ± 6.9
(n = 13), 38.7 ± 30.7 (n = 20), and 54.5 ± 22.5 (n = 7), respectively (Fig. 18.4). The
difference was statistically significant among the four species (F = 8.07, d.f. = 3, 49,
P < 0.001). In brown trout, mean radiocesium concentration (±SD) in eggs collected
from Lake Chuzenji fish was 65.6 ± 17.5 Bq/kg (n = 10). Mean radiocesium concentration in eggs collected from fish inhabiting the inlet stream was 11.9 ± 9.2 Bq/kg
(n = 10). This difference was statistically significant (F = 73.86, d.f. = 1, 18,
P < 0.001). There were significant relationships in radiocesium concentration
between individual muscle and egg samples from masu salmon (r = 0.80, P < 0.01),
brown trout (r = 0.96, P < 0.0001), and lake trout (r = 0.90, P < 0.01). Analysis of
covariance, in which egg radiocesium concentration was the dependent variable and

Radiocesium concentrations in eggs (Bq/kg-wet)

18

227

Radiocesium Concentrations in the Muscle and Eggs of Salmonids…
150

100

a

c

80

100

60
40

50

20
0

0
0

80

100

200

300

0

400
100

b

200

300

400

d

80

60

100

60
40

40

20
20
100

0
120

140

160

180

200

0

50

100

150

200

250

Radiocesium concentrations in muscle (Bq/kg-wet)
Fig. 18.4 Relationships between radiocesium concentrations in muscle and eggs of masu salmon
(a), kokanee (b), brown trout (c), and lake trout (d) collected from Lake Chuzenji, Japan, from
September to November 2012. Solid triangles indicate brown trout collected from the Lake
Chuzenji inlet stream

muscle radiocesium concentration was the covariate, revealed that the cesium concentrations between individual muscle and egg was significantly different among
the four species (F = 8.94, d.f. = 3, 48, P < 0.001). For brown trout, egg radiocesium
concentrations were significantly lower than the concentrations in the other three
salmonid fishes (Bonferroni multiple comparisons).
The mean radiocesium concentration ratio in eggs compared with that in muscle
were 0.34 for masu salmon, 0.36 for kokanee, 0.28 for brown trout, and 0.37 for
lake trout. These ratios were similar to the ratios in co-distributed wild white-spotted
charr (0.31) and rainbow trout (0.34; Yamamoto et al., unpublished data). Our analyses also revealed that radiocesium concentrations in masu salmon, brown trout,
and lake trout eggs increased proportionally with muscle concentrations. This relationship has not been reported previously and suggests that radiocesium levels in
salmonid muscle constitute a convenient surrogate for radiocesium concentrations
in eggs. Salmonid eggs are important for hatchery production programs and as food.
Release of hatchery-reared fish into many Japanese lakes and rivers, including the
Lake Chuzenji system, contribute to immediate resource enhancement and supplement wild fisheries, which are essential components of successful freshwater fisheries management programs (Kitada 2001). Although current radiocesium levels in
individual eggs were low, radiocesium turnover studies for each fish species, including elimination rate estimates, and biological and ecological half-lives at each life
history stage would be indispensable to further investigate this issue.

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Acknowledgments This chapter was revised from a paper published by Yamamoto et al. (2014b).
The authors are grateful to Kouji Mutou and the Lake Chuzenji Fishermen’s Cooperative for collecting the fish samples and to Masato Murakami, Tomoko Okazaki, Yumiko Watanuki, and Maki
Yoshida for their assistance with the sample assays and data analyses. We also thank Hiroyasu
Hasegawa, Takami Morita, Kaoru Nakata, Kazuo Uchida, and Hitoshi Kubota for their critical
reviews of the manuscript. This study was supported by the Fisheries Agency, Ministry of
Agriculture, Forestry, and Fisheries, Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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Rask M, Saxén R, Ruuhijärvi J, Arvola L, Järvinen M, Koskelainen U, Outola I, Vuorinen PJ
(2012) Short- and long-term patterns of 137Cs in fish and other aquatic organisms of small forest
lakes in southern Finland since the Chernobyl accident. J Environ Radioact 103:41–47
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Lake Biwa. Ichthyol Res 59:389–393

Chapter 19

Assessment of Radiocesium Accumulation
by Hatchery-Reared Salmonids After
the Fukushima Nuclear Accident
Shoichiro Yamamoto, Kouji Mutou, Hidefumi Nakamura, Kouta Miyamoto,
Kazuo Uchida, Kaori Takagi, Ken Fujimoto, Hideki Kaeriyama,
and Tsuneo Ono

Abstract To understand the process of radiocesium uptake in salmonids after the
Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident, a lake caging experiment and two captive-rearing experiments with controlled radiocesium concentrations of water and feed were conducted in and around Lake Chuzenji, central
Honshu Island, Japan (160 km from the station). Substantial accumulations of
radiocesium were confirmed in muscle of hatchery-reared kokanee (Oncorhynchus
nerka) and masu salmon (Oncorhynchus masou) after release into the cages, indicating that radionuclide contamination of fish is an ongoing process, 1.5 years after
the nuclear accident. Two captive experiments, controlling water and feed radiocesium levels, showed that direct radiocesium transfer from water (43 mBq/l) in Lake
Chuzenji to muscle tissue was undetected, at least during the approximately 90-day
experimental period, whereas a rapid increase in radiocesium levels was observed
when fish were cultured using radiocesium-contaminated pellets. The results
revealed that radiocesium contamination in salmonids is mainly via the food chain,
and that direct intake from water via the skin, gut, or gills has no major direct impact
on muscle tissue concentrations.
Keywords Bioaccumulation • Caging experiments • Captive-rearing experiments •
Kokanee • Lake Chuzenji • Masu salmon • Radiocesium

S. Yamamoto (*) • K. Mutou • H. Nakamura • K. Miyamoto • K. Uchida
National Research Institute of Aquaculture, Fisheries Research Agency,
2482-3, Chugushi, Nikko, Tochigi 321-1661, Japan
e-mail: ysho@affrc.go.jp
K. Takagi
Marine Biological Research Institute of Japan Co., LTD,
4-3-16, Yutaka, Shinagawa, Tokyo 142-0042, Japan
e-mail: takagik@affrc.go.jp
K. Fujimoto • H. Kaeriyama • T. Ono
National Research Institute of Fisheries Sciences, Fisheries Research Agency,
2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
© The Author(s) 2015
K. Nakata, H. Sugisaki (eds.), Impacts of the Fukushima Nuclear Accident
on Fish and Fishing Grounds, DOI 10.1007/978-4-431-55537-7_19

231

232

19.1

S. Yamamoto et al.

Introduction

In the preceding chapters, we documented individual radiocesium concentrations in
fish from a variety of locations, including in muscle and eggs of several salmonid
fishes from the Lake Chuzenji system in central Honshu Island (Chap. 18), in muscle and internal organs of a herbivorous fish, the ayu Plecoglossus altivelis, from
several rivers in Fukushima Prefecture (Chap. 17), and in muscle of lake-dwelling
freshwater fishes from Lake Hayama in Fukushima Prefecture (Chap. 16). There is
also a sizeable dataset of radiocesium concentrations in freshwater fishes from
northern and central Honshu Island, Japan, an area that was affected by the
Fukushima Dai-ichi Nuclear Power Plant (FNPP) accident (Mizuno and Kubo
2013; Arai 2014; Murakami et al. 2014).
Several preceding studies have demonstrated that radionuclide accumulation in
freshwater fish results mainly from food intake (Forseth et al. 1991; Ugedal et al.
1995). Experimental studies under controlled laboratory conditions, conversely,
have shown that high radiocesium concentrations in water can be transferred into
the organs of freshwater fish (Hewett and Jefferies 1976; Man and Kwok 2000). In
the recently affected areas of Japan, however, the nature of the processes underlying
radionuclide intake by freshwater fish has not yet been explored in detail, despite
the economic and biological importance of understanding radionuclide contamination of aquatic biota.
As an urgent investigation into the effects of the FNPP accident on salmonids by
the Fisheries Agency of Japan, a caging experiment in Lake Chuzenji (central
Honshu Island), and two captive-rearing experiments were conducted using controlled concentrations of radiocesium in water and food to understand radiocesium
bioconcentration and bioaccumulation in salmonids. At present (Oct. 2013), most
salmonid fishes in Lake Chuzenji still have radiocesium concentrations greater than
100 Bq/kg-wet, which is the Japanese standard limit for radiocesium in foods.

19.2

A Caging Experiment in Lake Chuzenji

To establish the radiocesium uptake rate of hatchery-reared fish released into Lake
Chuzenji, two cages about 180 m3 (6 × 6 × 5 m in height) were placed about 50 m
from the shore (Fig. 19.1). Each cage was covered on all sides in 4-mm plastic
mesh. Five hundred juvenile kokanee (Oncorhynchus nerka) and masu salmon
(Oncorhynchus masou), which were chosen from captive-bred fish in the Fisheries
Research Agency (FRA), were selected randomly and released into the respective
cages on 22 November 2012. Initial mean fork length and body weight (±SD) of
kokanee and masu salmon were 150 ± 13 (mm) and 30.5 ± 8.4 (g), and 93 ± 13 (mm)
and 7.2 ± 2.5 (g), respectively. During the experimental period, fish were not given
any artificial food. Up until 10 April 2013, 20 fish from each cage were collected
randomly at intervals of about 14 days. Sampled fish were frozen immediately, the

19

Assessment of Radiocesium Accumulation by Hatchery-Reared Salmonids…

233

Fig. 19.1 Cages set in Lake Chuzenji

fork length and body weight of each fish recorded, and a sample of muscle tissue
removed for measurement of radiocesium concentrations. During the experimental
period, water temperature in the cages (1-m depth) had a range of 1.4 °C (27
February 2013) to 10.2 °C (29 March 2013).
The kokanee in cages showed little or no growth during the experimental period.
Mean fork length and body weight (±SD) at the termination of the experiment
(139 days after the start of the experiment) were 149 ± 8 (mm) and 30.0 ± 5.8 (g),
respectively. There were no significant differences between initial and final fork
lengths and body weights of kokanee (t tests; P > 0.05). Mean fork length and body
weight (±SD) at the termination of the experiment (139 days after the start of the
experiment) of masu salmon were 97 ± 11 (mm) and 9.0 ± 3.2 (g), respectively.
Mean fork length and body weight of masu salmon at the termination of the experiment were significantly greater than those at the start of the experiment (t tests;
P < 0.05). Substantial radiocesium concentrations (134Cs + 137Cs) in both kokanee
and masu salmon muscle tissue from the cages were detected at first sampling
(14 days after the start of the experiment), with 2.2 Bq/kg-wet for kokanee and
3.9 Bq/kg-wet for masu salmon (Fig. 19.2). Thereafter, radiocesium levels increased
approximately linearly with the duration of the experiment (kokanee: R2 = 0.97,
P < 0.001; masu salmon: R2 = 0.89, P < 0.001). The final radiocesium concentrations
in kokanee and masu salmon were 19.2 Bq/kg-wet (ratio of 134Cs/137Cs, 0.55) and

S. Yamamoto et al.
Radiocesium concentration in muscle (Bq/kg-wet)

234
35
30
25
20
15
10
5
0
0

50

100

150

Days (initial 22 November 2012)

Fig. 19.2 Changes in radiocesium concentrations in kokanee (●) and masu salmon (○) in cages
set up in Lake Chuzenji between 22 November 2012 and 10 April 2013

30.9 Bq/kg (134Cs/137Cs, 0.47), respectively. Daily radiocesium accumulation rates
were estimated at 0.14 Bq/kg/day in kokanee and 0.22 Bq/kg/day in masu salmon,
assuming linear relationships between radiocesium concentrations and experiment
duration. During the experimental period, masu salmon had higher radiocesium
concentrations than kokanee (F = 11.3, d.f. = 1,21, P = 0.007).
In Lake Chuzenji, mean muscle radiocesium concentrations of wild salmonid
fishes [kokanee, masu salmon, brown trout (Salmo trutta), and lake trout (Salvelinus
namaycush)] collected during September to December, 2012, were in the range of
142.9 to 249.2 Bq/kg-wet (Chap. 18). Substantial accumulation of radiocesium was
also confirmed in muscle tissue of hatchery-reared salmonids after release into
cages set in Lake Chuzenji, indicating that radionuclide contamination of fish was
an ongoing process, 1.5 years after the FNPP accident. Both kokanee and masu
salmon juveniles in the cages were assumed to have fed mainly on zooplankton
entering through the mesh. Radiocesium concentrations in plankton sampled over
the same period in Lake Chuzenji (12.6 Bq/kg-dry; Fisheries Research Agency
2015) were much lower than the levels recorded in kokanee and masu salmon muscle tissue within the cages. The result provides strong evidence of in situ radiocesium bioaccumulation from food to fish muscle tissue in a natural lake in Japan.
After the Chernobyl nuclear accident, radiocesium concentrations in crustacean
zooplankton in Finnish lakes were significantly correlated with those in the water
(Rask et al. 2012). During the experimental period of our study, planktivorous
kokanee and masu salmon juveniles, with a short food chain, would closely track
the environmental contamination of water and zooplankton in Lake Chuzenji.

19

Assessment of Radiocesium Accumulation by Hatchery-Reared Salmonids…

19.3

235

Captive-Rearing Experiments with Controlled
Radiocesium Concentrations of Water and Feed

To understand the process of radiocesium uptake in freshwater fish, two experiments were conducted on fish in captivity using known concentrations of radiocesium in water and feed. Two fiberglass circular tanks of 0.5 m3 (1,170 mm in
diameter, 770 mm in depth) were set up in the FRA facility at Nikko. Throughout
the experimental period, rearing water for this tank was drawn from Lake Chuzenji
via an electronic pump. Before influx into the tank, the water was filtered through a
60-μm mesh to remove any particles, including plankton. The discharge rate of filtered water into the tanks was controlled at about 1.24 × 10−4 m3/s. Into this tank,
200 juvenile kokanee, selected randomly from captive-bred fish in FRA, were
released on 7 January 2013, and fed commercial food pellets of approximately 2 %
body weight per day. Initial mean fork length and body weight (±SD) were 147 ± 10
(mm) and 27.9 ± 6.3 (g), respectively. Up until 10 April 2013, 20 fish from the tank
were collected randomly at intervals of about 14 days. Collected fish were frozen
immediately, the fork length and body weight of each fish recorded, and a sample of
muscle tissue removed for measurement of radiocesium concentrations. During the
experimental period, water temperature in the tank was in the range of 2.0 °C (26
February) to 12.5 °C (5 April). Dissolved radiocesium concentration of the surface
water in Lake Chuzenji, collected on 28 November, 2012, was 43 mBq/l (Fisheries
Research Agency 2015).
The other tank was filled with spring-fed water upwelling in the FRA facility
(Fig. 19.3). Radiocesium concentrations of this water were below the limits of
detection. The discharge rate of the spring-fed water into the tank was controlled at
about 5.57 × 10−4 m3/s. Two hundred juveniles of kokanee, selected randomly from
captive-bred fish in FRA, were released into the tank on 7 January 2013. Initial
mean fork length and body weight (±SD) were 157 ± 10 (mm) and 37.0 ± 7.1 (g),
respectively. Fifteen smallmouth bass (Micropterus salmoides), collected in Lake
Hayama in Fukushima Prefecture (linear distance from the FNPP, ~17 km) in June
2012, were used to prepare food pellets for the experimental fish. Radiocesium concentrations in the muscle of smallmouth bass individuals had a range of 4,213 to
7,188 Bq/kg-wet (mean ± SD, 5,777 ± 891 Bq/kg; median, 5,829 Bq/kg) (Chap. 16).
The muscle tissue was carefully homogenized with commercial food pellets, the
food pellets having been adjusted to contain an average radiocesium level of 445 Bq/
kg-dry. Experimental fish were fed these commercial food pellets with radiocesium
material of approximately 2 % body weight per day. Until 10 April 2013, 20 fish
from the tank were sampled randomly at intervals of about 14 days. Collected fish
were frozen immediately, the fork length and body weight of each fish recorded, and
a sample of muscle tissue removed for measurement of radiocesium concentrations.
During the experimental period, water temperature in the tank was in the range
8.8 °C (31 January) to 10.1 °C (5 April). All experimental fish used in this study
were fed food pellets once or twice a day until used in the experiments but were not
acclimated to the experimental tanks before the start of the experiments.

236

S. Yamamoto et al.

Fig. 19.3 An experimental facility in the Fisheries Research Agency for examining the process of
radiocesium intake in salmonid fish

When fish were reared in water from Lake Chuzenji and a diet of commercial
pellets, no radiocesium was detected in muscle tissue at any sampling period (detection limits, <1.74 Bq/kg) (Fig. 19.4). Final mean fork length and body weight (±SD)
of kokanee in this experiment were 162 ± 12 (mm) and 49.5 ± 11.4 (g), respectively.
When fish were reared using spring-fed water and pellets containing radiocesium,
radiocesium concentrations in muscle tissue increased rapidly during the experiment. At 93 days after the start of the experiment, the radiocesium concentration
increased to 126.2 Bq/kg-wet (134Cs/137Cs, 0.51). Final mean fork length (±SD) of
kokanee in this experiment were 183 ± 68 (mm) and 67.8 ± 16.6 (g), respectively.
Two captive experiments with controlled water and feed radiocesium concentrations demonstrated that direct radiocesium transfer from water (43 mBq/l) in Lake
Chuzenji to fish muscle tissue was undetected, at least during the approximately
90-day experimental period, whereas a rapid increase in radiocesium concentration
was observed when fish were cultured using pellets contaminated with high concentrations of radiocesium. The results reinforce the evidence that radiocesium contamination of freshwater fish is mainly via the food chain, and that direct intake
from the water via the skin, gut, or gills has little or no effect on muscle tissue levels.
Previous experimental studies, however, showed that freshwater fish exposed to
water with extremely high concentrations of radionuclides can accumulate the
nuclides into their organs (Hewett and Jefferies 1976; Man and Kwok 2000). After
the FNPP accident, Japanese governmental agencies initiated detailed sampling

237

Assessment of Radiocesium Accumulation by Hatchery-Reared Salmonids…
Radiocesium concentration in muscle (Bq/kg-wet)

19

150

100

50

0
0

20

40

60

80

100

Days (initial 7 January 2013)

Fig. 19.4 Changes in radiocesium concentrations in kokanee in captivity between 7 January and
10 April 2013. Circles and triangles indicate the radiocesium concentrations in kokanee reared
using spring-fed water with commercial pellets containing radiocesium material and in kokanee
reared using water from Lake Chuzenji and fed with commercial pellets without any radionuclides,
respectively

programs to establish the contamination levels of water in the affected area.
Monitoring programs did not detect water with radiocesium concentrations greater
than 1 Bq/l in any natural rivers or lakes during 2012–2013, with very few exceptions (Ministry of Environment 2015). Water itself, if it should contain radionuclides, is unlikely to have a significant direct impact on levels of radiocesium in fish
muscle tissues, at least within current Japanese freshwater systems.

19.4

For Further Study

A meta-analysis of the relevant literature revealed that radiocesium concentrations
in fish were a positive function of contamination concentrations in the water, particularly for nonpiscivorous fish species (Rowan and Rasmussen 1994). Although
direct radiocesium transfer from water to fish muscle tissue seems to be negligible,
water may act as a radiocesium source to planktivorous fish via the food chain
(Elliott et al. 1992; Rask et al. 2012; Tuovinen et al. 2013). In many Japanese lakes
and rivers, including the Lake Chuzenji system, the release of hatchery-reared fish
enhances resources and supplements wild fish stocks, which are essential components of successful freshwater fisheries management programs (Kitada 2001;
Yamamoto et al. 2011). Continued monitoring of radiocesium concentrations in
water and zooplankton, as well as in fish, is crucial for estimating bioconcentration
and bioaccumulation and, thus, for predicting contamination concentrations in
released hatchery-reared fish within the affected area.

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Acknowledgments This chapter was revised from a paper published by Yamamoto et al (2014).
We thank Masato Murakami, Tomoko Okazaki, Yumiko Watanuki, and Maki Yoshida for their
assistance with sample assays and data analyses, and the staff of FRA for collecting fish samples.
We are grateful to Kaoru Nakata for a critical review of the manuscript, and Hiroyasu Hasegawa
and Takami Morita for operational management of the study. This study was supported by the
Fisheries Agency, Ministry of Agriculture, Forestry and Fisheries, Japan.
Open Access This chapter is distributed under the terms of the Creative Commons Attribution
Noncommercial License, which permits any noncommercial use, distribution, and reproduction in
any medium, provided the original author(s) and source are credited.

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