Contents lists available at ScienceDirect

Journal of Environmental Radioactivity

journal homepage: www.elsevier.com/locate/jenvrad

Evaluation of body size and temperature on 137Cs uptake in marine animals

Derin M. Thomas, Nicholas S. Fisher∗
School of Marine and Atmospheric Sciences, Stony Brook University, Stony Brook, NY, 11794-5000, USA

A R T I C LE I N FO A B S T R A C T

137
Keywords: Cs bioaccumulation and retention in seven different marine animal species, including crustaceans, mollusc
Radiocesium larvae, and fish larvae were compared under different temperature conditions (10 °C, 18 °C and 25 °C). Replicate
Bioaccumulation animals were experimentally exposed to 0.5 nM 137Cs dissolved in filtered seawater for 3 days, and their 137Cs
Bioconcentration factor contents were periodically measured using gamma spectrometry. Among the seven species, 137Cs bioconcen-
Depuration
tration factors ranged from 14 to 239 at the end of the exposure periods. Following uptake, the137Cs loss rate
Marine prey species
Cesium
constants from the animals ranged from 5 to 50% d−1 and were unaffected by temperature or animal size. The
137
Cs bioconcentration factors were directly related to animal size and hence their surface: volume ratios,
consistent with the conclusion that Cs sorption from the aqueous phase is the principal uptake mechanism in
these animals. With the exception of gastropods, temperature had no major influence on Cs uptake and efflux in
the experimental species.

1. Introduction shown significantly different uptake rates of 137Cs in different sized

The damaged Fukushima Dai-ichi Nuclear Power Plant (FDNPP)
released massive amounts of radionuclides in March and April, 2011,
resulting in the largest accidental release of radioactive materials into
the oceans (Buesseler et al., 2012, 2017; Du Bois et al., 2012; Strand
et al., 2017). Among many radionuclides discharged into marine en-
vironments, radiocesium 134Cs and 137Cs are of specific interest because
of their sheer abundance, relatively long half-lives, and residence times
in the water. The field data collected from coastal waters off Fukushima
revealed great variations of 137Cs concentrations in different marine
species, and these varied with animal size and ecological habitat
(Buesseler et al., 2012; Iwata et al., 2013; Wada et al., 2013; Wang
et al., 2018).
Despite the long-recognized importance of cesium waste products,
our understanding of the uptake of Cs from contaminated seawater in
marine organism is still somewhat limited. 137Cs accumulated by higher
organisms, e.g. fish, originates from ingestion of 137Cs-contaminated
prey organisms rather than from direct sorption of the radionuclide
from water (Guimarães, 1992; Komarov and Bennett, 1983; Mathews
and Fisher, 2009). The uptake of dissolved Cs is thought to be an im-
portant route of 137Cs bioconcentration among small diverse marine
invertebrates such as zooplankton, shrimp, and some molluscs as well
as fish larvae, but the influence of body size and environmental tem-
perature on 137Cs uptake by marine animals has been shown to be
variable and sometimes contradictory. Some experimental studies have
molluscs from the dissolved phase (Kuranchie-Mensah et al., 2018;
Nolan and Dahlgaard, 1991), while other studies have shown no sig-
nificant effects on mussel body size on 137Cs uptake (Güngör et al.,
2001). Because our understanding of the influence of body size and
environmental temperature on 137Cs uptake by marine organisms is
limited, we conducted a study to investigate their effects on the uptake
radiocesium in seven marine animal species. These organisms are
common prey species for fish higher in the food chain and are com-
monly found in coastal waters everywhere, including near Fukushima,
Japan. The effect of temperature on 137Cs uptake and depuration from
the organisms was examined to assess how metabolic rates may influ-
ence 137Cs bioaccumulation in these animals.
These evaluations are important because it may identify the role of
prey organisms in the trophic transfer of radiocesium in marine food
chains. Most other metals enter food chains primarily via primary
producers that greatly concentrate metals out of ambient water and
serve as highly enriched sources of these metals to herbivores (Fisher,
1986; Fisher and Reinfelder, 1995). However, Cs is little concentrated
out of seawater by marine phytoplankton (Heldal et al., 2001) as well as
sea grasses and macroalgae (Warnau et al., 1996), hence these plants
are not significant sources of Cs for marine animals (Mathews and
Fisher, 2009; Thomas et al., 2018). The absorption efficiency of Cs from
the aqueous phase is analogous to its assimilation efficiency from an
ingested food source, which has been extensively studied in marine
organisms (Ke et al., 2000; Sezer et al., 2014; Thomas et al., 2018;

∗
Corresponding author. School of Marine and Atmospheric Sciences (SoMAS), Stony Brook University, Stony Brook, NY, 11794-5000, USA.
E-mail address: nicholas.fisher@stonybrook.edu (N.S. Fisher).

https://doi.org/10.1016/j.jenvrad.2019.02.005
Received 30 August 2018; Received in revised form 28 November 2018; Accepted 7 February 2019
D.M. Thomas and N.S. Fisher

Table 1
Geometric shape, body length and weight, and surface: volume ratio of marine prey species Acartia tonsa Leptocheirus plumulosus, Americamysis bahia and Palaemonetes
vulgaris representing crustaceans, Crepidula fornicata larvae representing molluscs, and Fundulus heteroclitus and Cyprinodon variegatus larvae representing chordates.
Number of organisms indicates number of experimental organisms evaluated experimentally.
Species No. of organisms Mean length (cm) Mean dry wt. (mg) Surface:Volume (μm2: μm3) Geometry

Acartia tonsa 50 0.05 0.01 470 Ellipsoid

Leptocheirus plumulosus 40 0.4 0.07 45 Box + Elliptic prism
Americamysis bahia 7 0.4 0.13 21 Sickle shaped prism
Palaemonetes vulgaris 3 2.5 30 5.7 Box + Elliptic prism
Crepidula fornicata 16 0.1 0.06 12 Cylinder
Fundulus heteroclitus 20 0.5 0.37 9 Box + Elliptic prism
Cyprinodon variegatus 20 0.5 0.21 10 Box + Elliptic prism

Fig. 1. Mean 137Cs Concentration factors of marine prey species from radiolabeled seawater at 10 °C, 18 °C and 25 °C. Concentration factors (mL g−1 dw) represent
137
Cs activity in animals (Bq g−1 dw) divided by 137Cs activity in ambient water (Bq mL−1) for each treatment. (A) calanoid copepod Acartia tonsa; (B) mysid shrimp
Americamysis bahia; (C) amphipod Leptocheirus plumulosus; (D) grass shrimp Palaemonetes vulgaris; (E) mollusc larvae Crepidula fornicata; (F) fish larvae Fundulus
heteroclitus; (G) fish larvae Cyprinodon variegatus at 24 h (open symbols) and 48 h (shaded symbols). Data points are means of three replicates ± 1 SD.

Wang et al., 2016; Zhao et al., 2001). Thomas et al. (2018) presented quantitative parameters assessing Cs bioavailability from the dissolved
experimental results indicating that, for crustacean zooplankton, at phase. The uptake rate constant is a function of the animal's filtration
least, the predominant source of 137Cs is the dissolved phase. Bio- rate and the absorption efficiency of metals from the dissolved phase
concentration factors (BCF) and uptake rate constants (ku) are key (Wang et al., 1996).
D.M. Thomas and N.S. Fisher

Table 2 2. Materials and methods

Uptake and depuration rate constants of 137Cs in the marine prey species at
10 °C, 18 °C, and 25 °C. Acartia tonsa Leptocheirus plumulosus, Americamysis bahia Uptake of dissolved 137Cs in seven marine prey species was de-
and Palaemonetes vulgaris representing crustaceans, Crepidula fornicata larvae termined experimentally by radiotracer techniques. The species from
representing molluscs, and Fundulus heteroclitus and Cyprinodon variegatus
various taxonomic groups were chosen for the experiment based on
larvae representing chordates.
their body size including four crustaceans, one mollusc larvae and two
Species Temperature (° C) Uptake rate Loss rate fish larvae. The body length of the organisms ranged from 0.05 cm to
constant (ku) constant(ke) 2.5 cm; dimensions, the approximate geometrical shape, and weights of
(L g−1 d−1) (d−1)
the experimental animals are given in Table 1. We estimated the sur-
Acartia tonsa 10 0.1 0.5 face: volume ratios (μm2: μm3) by measuring the body dimensions of
18 0.1 0.5 the organism based on their geometrical shapes.
25 0.1 0.4

Americamysis bahia 10 0.06 0.2 2.1. Experimental organisms

18 0.06 0.4
25 0.07 0.3 The crustacean models examined in this study included calanoid
copepods (Acartia tonsa) collected from Stony Brook Harbor, New York,
Leptocheirus 10 0.04 0.1
mysid shrimp (Americamysis bahia) and amphipods (Leptocheirus plu-
plumulosus 18 0.04 0.1
25 0.04 0.1 mulosus) obtained from Aquatic Research Organisms, Inc., and grass
shrimp (Palaemonetes vulgaris) collected from Flax Pond in Setauket,
Palaemonetes vulgaris 10 0.01 0.1 New York. All species were maintained in 1-μm filtered Stony Brook
18 0.01 0.2
Harbor water, 30 psu and held under a 14:10 h light: dark cycle at
25 0.01 0.2
25 ± 1 °C). For all experimentation, light intensity was 210 μEin m−2
Crepidula fornicata 10 0.001 0.2 sec−1 provided by cool white fluorescent lamps. During the acclimation
larvae 18 0.003 0.4 period marine phytoplankton (the diatom Thalassiosra pseudonana,
25 0.002 0.3 CCMP 1335) and Artemia salina nauplii were fed to the organisms on a
Fundulus heteroclitus 12 0.03 0.1
daily basis.
larvae 18 0.03 0.1 Adult molluscs (the slipper snail Crepidula fornicata) were collected
25 0.02 0.1 from West Meadow beach, Stony Brook, New York, and maintained in
the laboratory at 25 °C on a mixed diet of the marine phytoplankton
Cyprinodon variegatus 12 0.02 0.07
Isochrysis galbana (CCMP 1324) and Emiliania huxleyi (CCMP 2090).
larvae 18 0.01 0.05
25 0.01 0.05 Following release, larvae were collected and reared at 25 °C with the
marine phytoplankton diet. The growth of C. fornicata was sustained
with low mortality under these conditions (Pechenik, 1987); larvae

Table 3
137
Cs uptake rate constants (ku), loss rate constants (ke) and bioconcentration factors determined in (a) laboratory experiments representing organisms from each
taxonomic group; and (b)137Cs concentration factors in field-collected animals from the Fukushima coast, Japan. nd: not determined.
Species Size range (cm) ku (L g−1 d−1) ke (d−1) CF Range (mL g−1 dw) Reference

a) Lab Studies

Crustaceans
Acartia tonsa 0.05 0.1 0.5 200–239 Present study
A. tonsa 0.08 0.07 nd 30 Thomas et al. (2018)
Americamysis bahia 0.4 0.06 0.02 139–157 Present study
Leptocheirus plumulosus 0.4 0.04 0.1 77–81 Present study
Palaemonetes vulgaris 2.5 0.01 0.2 32–34 Present study
Palaemon adspersus 5 0.3 15 Sezer et al., 2014
Molluscs
Crepidula fornicata 0.1 0.003 0.2 14–69 Present study
Perna virdis 3 to 4 0.26 0.02 145 Ke et al. (2000)
Septifer virgatus 3 to 4 2.7 0.03-0.2 13 Pan et al., 2016
Chordates
F. heteroclitus larvae 0.5 0.03 0.1 43–58 Present Study
F. heteroclitus 2 0.003 0.2 10 Thomas et al. (2018)
Cyprinodon variegatus 0.5 0.02 0.05 41–49 Present Study
Psetta maxima 5 0.0002 0.027 10 Jeffree et al. (2006),
Mathews and Fisher (2009)
Scyliorhinus canicula 8.5 to 16 0.0001 0.014 2.4 Jeffree et al. (2006),
Mathews and Fisher (2009)

b) Field data: Fukushima coast, Japan

Sample composition Sampling net size (cm) CF Range (mL g−1 d. w.) Reference

Crustaceans Buesseler et al. (2012);

Copepods 0.03 10–285 Kaeriyama et al., 2008
Zooplankton 0.03 10–78 Baumann et al. (2015)
Euphausiids, shrimps and fishes 0.4 4–39 Buesseler et al. (2012)
Chordates
Fish 0.4 4–20 Buesseler et al. (2012)
D.M. Thomas and N.S. Fisher

Fig. 2. Retention of 137Cs in marine prey species A) Acartia tonsa, (B) Americamysis bahia, (C) Leptocheirus plumulosus, (D) Palaemonetes vulgaris, (E) Crepidula fornicata
(F) Fundulus heteroclitus, (G) Cyprinodon variegatus following uptake from the aqueous phase. Time 0 represents the radioactivity measured immediately after
exposure, which is assigned as 100%; other data points represent fractions of 137Cs remaining in animals. Each data point represents the average of three replicate
cultures with 1 SD error bars.

were maintained in flow-through aerated Stony Brook Harbor seawater
(under a 14:10 h light: dark cycle, 25 ± 1 °C) prior to experiments.
Two-day old fish larvae of killifish (Fundulus heteroclitus) and
sheepshead minnow (Cyprinodon variegatus) were obtained from
Aquatic Research Organisms, Inc. The fish larvae were gently trans-
ferred into 0.2–μm filtered Stony Brook Harbor water and maintained
under a 14:10 h light: dark cycle, 25 ± 1 °C, allowing them to accli-
mate to laboratory conditions for 2 d. A. salina nauplii were fed to the
fish larvae at a daily ration of about 5% of their body weights during
the acclimation period. Prior to the experiments, the animals were
gradually acclimated to the targeted temperature over a period of 3 d.
137
2.2. Experimental exposures to Cs at different temperatures
Uptake of 137Cs in the marine prey species from the dissolved phase
was assessed at 10 °C, 18 °C and 25 °C, representative of coastal surface
water variations at different seasons. All the experimental organisms
were acclimated in the laboratory at respective temperatures for 2 days
in 0.2–μm filtered Stony Brook Harbor seawater prior to the 137Cs ex-
posure. Temperatures were monitored every 4 h with a digital ther-
mometer. The animals were transferred to filtered water in aquaria
without food for 24 h to allow them to evacuate their guts of ingested
material prior to exposure. Each animal species (adults for all species
except for larvae for C. fornicata) was held in three replicate aquaria at
each experimental temperature. In each experimental vessel, the
number of animals were as follows: A. tonsa (n = 50), L. plumulosus
(n = 40), A. bahia (n = 6), P. vulgaris (n = 3), C. fornicata larvae
(n = 16), F. heteroclitus larvae (n = 20) and C. variegatus larvae
(n = 20).
To study the uptake of 137Cs, the experimental organisms were
D.M. Thomas and N.S. Fisher
Fig. 3. Relationship between the 137Cs concentration factor and body size
(Surface: Volume) in 7 marine animals.
placed in 100 ml of 0.2–μm filtered Stony Brook Harbor seawater (pH
8.05) containing 8 kBq of the gamma-emitting radioisotope 137Cs (t1/
137
2 = 30 y) (corresponding to 0.5 nM), as CsCl; the Cs (obtained from
Amersham) was dissolved in 0.1 N HCl. This addition of Cs was about
25% of the background molar Cs concentration in seawater (Donat and
Bruland, 1995). The low volume (3.75 μl) of dilute acid added had no
effect on the pH of the experimental water. Aliquots of seawater (1 mL)
were sampled to measure the radioactivity in the water periodically; no
significant decrease of the radioactivity in the seawater over time was
observed. The exposures lasted for 48 h for crustaceans (preliminary
experiments indicated that many copepods died after 48 h without
food) and 72 h for molluscs and fishes.
Animals were incubated at the selected temperatures under 14:10
light:dark cycles. During the exposure periods, the organisms were
periodically sampled from each of the three replicates, rinsed 3 times
with filtered unlabeled seawater (maintained at 10 °C, 18 °C and 25 °C)
to remove loosely bound 137Cs, and then placed in 20 mL of unlabeled
seawater in a radioactivity counting container. Their radioactivity was
then immediately counted non-destructively for 5 min in a Canberra
NaI (Tl) well-type gamma detector. Radioactivity of 137Cs-labeled sea-
water was measured using an LKB Wallac 1282 Compugamma NaI (Tl)
well-type gamma detector. The activity of 137Cs in all samples was as-
sessed at 661 keV; the counting efficiency was 66%. Intercalibration
between the two gamma counters was performed and all samples were
counted with standards of appropriate geometry and decay-corrected.
To minimize counting geometry problems, movement of the organisms
within counting chambers was limited by placing a minimal amount of
water in the counting chambers. Propagated counting errors were <
5%.
Following the radioactivity measurements, the organisms were re-
turned to the radioactive seawater. After 48 h–72 h uptake, the animals
were placed in 100 ml of unlabeled seawater where they were allowed
to depurate their 137Cs for 72 h, undergoing daily water changes and
feeding every 12 h. All experiments included control treatments with
unlabeled seawater which were used to correct the total background
137
Cs concentrations in all the species and were always found to be
undetectable. After depuration, the experimental organisms were dried
at 80 °C to obtain the body dry weights.
The weight-normalized 137Cs uptake (ku) and depuration (ke) rate
constants were calculated from the regression slopes of uptake and loss,
respectively, against the time of exposure at each temperature (Wang
et al., 1996). Bioconcentration factors were calculated as the 137Cs
activity g−1 dw of animal divided by 137Cs activity ml−1 of ambient
water (Fisher et al., 1996; Ke et al., 2000; Wang et al., 2000).
3. Results and discussion
137
Cs uptake from the dissolved phase over time was observed for
all 7 marine prey species at all experimental temperatures. In all cases,
the animals acquired < 3% of the total 137Cs under the experimental
conditions within 3 d. The concentration factors (CFs) of 137Cs did not
change appreciably after 1 day of exposure at all temperatures in all
species but A. tonsa and A. bahia, where the CFs increased over time at
all temperatures (Fig. 1). Overall, analysis of the uptake and retention
data by one-way ANOVA indicated that temperature did not sig-
nificantly (p > 0.1) affect the biological uptake of 137Cs in crustaceans
and fish larvae (Fig. 1, Table 2), but in mollusc larvae the 137Cs uptake
was significantly higher (p < 0.0001) at 25 °C than at 18 °C and 10 °C
(Fig. 1). Nolan and Dahlgaard (1991) also concluded from an experi-
mental study that the uptake rate of 137Cs by adult mussels, Mytilus
edulis, was consistent with a metabolic-type behavior, as seen in the
mollusc larvae in this study.
A comparison of BCF, uptake rate constant and loss rate constant
values of 137Cs among the various taxa and as compared with other
experimental studies is shown in Table 3. The bioconcentration factors
of 137Cs were highest in the smallest animal (A. tonsa), where they
ranged from 47 to 239 at 25 °C after a 2-d exposure (Table 1, Fig. 1).
The mean BCF in A. tonsa was close to the value (CF = 40) suggested
for marine zooplankton by the IAEA (IAEA, 2004) and directly com-
parable to reported CF values ranging from 10 to 278 for 137Cs in si-
milar size marine zooplankton collected in the field off Fukushima or
studied in laboratory experiments (Table 3) (Baumann et al., 2015;
Buesseler et al., 2012; Thomas et al., 2018). The 137Cs ku, calculated as
the slope of the uptake of 137Cs normalized to the experimental 137Cs
concentration and dry weight of each species, were largely unaffected
by temperature and highest for A. tonsa (0.1 L g−1 d−1) and lowest for
C. fornicata (0.001 L g−1 d−1 at 12 °C) (Table 2).
The estimated 137Cs ku in A. tonsa was close to the ku (0.07 L g−1
−1
d ) reported in the same species (Thomas et al., 2018), but up to 3
orders of magnitude lower than that reported for other trace metals
such as methylmercury (35 L g−1 d−1), silver (10.42 L g−1 d−1), zinc
(3.29 L g−1 d−1), cadmium (0.694 L g−1 d−1) and cobalt (0.606 L g−1
d−1) (Lee and Fisher, 2017; Wang and Fisher, 1998). The BCF in shrimp
species A. bahia (157) was higher than L. plumulosus (77) and P. vulgaris
(34) after 2 d exposure. These results were comparable with the BCF of
137
Cs in large shrimp species Palaemon adspersus (15) (Sezer et al.,
2014). The ku in A. bahia (0.07 L g−1 d−1), L. plumulosus (0.04 L g−1
d−1), and P. vulgaris (0.01 L g−1 d−1) were lower than reported pre-
viously for laboratory experiments with the marine shrimp P. adspersus
(0.3 L g−1 d−1) (Sezer et al., 2014). The greater ku in P. adspersus may
have been due to the low salinity (26.6 psu) in the ambient water since
Cs uptake rate is inversely related to concentrations of potentially
competing potassium ions (K+) in seawater (Bryan, 1963; Ke et al.,
2000; Wang and Dei, 1999; Wolfe and Coburn, 1970). Cs bioconcen-
tration factors in freshwater crustacean zooplankton have been shown
to be significantly greater than in comparably sized marine copepods
(Thomas et al., 2018), consistent with the inverse relationship of K+ ion
concentrations and Cs BCFs.
The 137Cs BCF in mollusc larvae C. fornicata was 5 times higher at
25 °C than at 10 °C. The ku in C. fornicata varied from 0.001 to
0.003 L g−1 d−1 with a change in temperature. The ku of radiocesium in
marine bivalves Perna virdis (0.026 L g−1 d−1), Septifer virgatus
(2.7 L g−1 d−1) and Babylonia formosae habei (1.4–1.6 L g−1 d−1) were
higher than C. fornicata larvae (Ke et al., 2000; Pan et al., 2016; Wang
et al., 2000). This could be primarily due to the body size and allometry
of the gill surface area in marine bivalves (Wang and Dei, 1999). Si-
milarly, initial 134Cs uptake rates in brittle stars from water were sig-
nificantly greater at 12 °C than at 2 °C, resulting in a Q10 value of 4.1,
but after 14 d exposure the Q10 of the Cs BCF was 1.3 (Hutchins et al.,
1996).
The BCFs of 137Cs in fish larvae were inversely related to
D.M. Thomas and N.S. Fisher
temperature and higher than in fish samples collected from Fukushima,
Japan (Buesseler et al., 2012) and previous laboratory studies (Jeffree
et al., 2006; Mathews and Fisher, 2009; Thomas et al., 2018) (Table 3).
Much of these BCF differences are presumably due to differences in
137
Cs accumulation between adult and larval stages of the fish. The ku
in F. heteroclitus larvae (0.03 L g−1 d−1) and C. variegatus reported in
this study (0.02 L g−1 d−1) was comparable with a previous report for
similar species reported by Thomas et al. (2018) but was at least twice
as high as previous reports in the adult F. heteroclitus
(0.0006 L g−1 d−1) (Wang et al., 2016), in mangrove snapper Lutjanus
argentimaculatus (0.001 L g−1 d−1) (Zhao et al., 2001), in dogfish Scy-
liorhinus canicula (0.0001 L g−1 d−1), and in turbot Psetta maxima
(0.0002 L g−1 d−1) (Jeffree et al., 2006; Mathews and Fisher, 2009).
The higher ku values in fish larvae than in the adult fish previously
studied might be due to the very small size of the larvae, hence higher
surface area-to-volume ratios.
Once accumulated, the 137Cs was not irreversibly bound in the an-
imals, as all animals depurated their 137Cs after being transferred to
unlabeled seawater (Fig. 2). Efflux rate constants (ke), estimated as the
slopes of the regression lines of 137Cs loss over time for the slowly ex-
changing pools (Wang and Fisher, 1999), were greatest in A. tonsa
(approx, 0.5 d−1) and lowest in A. bahia (approx. 0.02 d−1) (Fig. 2,
Table 2). Temperature and body size generally had little to no effect on
depuration rates (Table 2), in contrast to findings with adult brittle stars
where loss rates were 0 at 2 °C but 0.02 d−1 at 12 °C (Hutchins et al.,
1996) and in adult Salmo trutta where the loss rates where high at 15 °C
(Ugedal et al., 1992). The ke in C. variegatus larvae was close to those in
Psetta maxima (0.02 d−1), Scyliorhinus canicula (0.01 d−1) and Lutjanus
argentimaculatus (0.02 d−1) (Jeffree et al., 2006; Mathews and Fisher,
2009; Zhao et al., 2001). The ke in F. heteroclitus larvae (0.1 d−1) was
comparable to the previous report by Thomas et al. (2018) in the same
species but higher than in adult F. heteroclitus (0.06 d−1) (Wang et al.,
2016) (Table 3). The interspecies differences in ke in the organisms
were presumably due to the difference in clearance or desorption rate
between adult and larval stages.
Perhaps most strikingly, the 137Cs concentration factors among the 7
species were inversely related to animal size and positively related to
the surface: volume ratios of the animal bodies (Fig. 3). The linear re-
lationship among the species demonstrates that body dimensions of the
animals are correlated with Cs uptake from the aqueous phase among
these marine prey species, suggesting that Cs sorption to reactive sites
on the animal surfaces determines the uptake. Because Cs uptake by
marine phytoplankton is so low (Heldal et al., 2001), these cells do not
represent a significantly enriched source of Cs for herbivorous marine
zooplankton. Instead, Thomas et al. (2018) experimentally demon-
strated that Cs in marine zooplankton is primarily acquired from the
dissolved phase rather than diet, and the strong correlation of Cs uptake
with surface:volume ratios in the current study indicate that sorption of
Cs to zooplankton surfaces accounts for this uptake.
Other biological factors such as gill surface area (which regulates
solute uptake and clearance rate) and membrane permeability may also
account for interspecies differences in Cs uptake. Previous investiga-
tions in marine bivalves also reported body size as a controlling factor
in the accumulation of other metals (Chong and Wang, 2001; Ke et al.,
2000; Lee et al., 1998; Nolan and Dahlgaard, 1991; Wang and Dei,
1999; Wang and Fisher, 1997).
Acknowledgments
The authors thank S. Zegers for technical assistance, Z. Baumann for
valuable discussions and two anonymous reviewers for constructive
comments. This research was supported by Science and Engineering
Research Board and Indo-US Science and Technology Forum,
(Government of India) (No. SERB Indo-US Postdoctoral Fellowship
2016/ 147-Derin Mary Thomas).
References
Baumann, Z., Fisher, N.S., Gobler, C.J., Buesseler, K.O., George, J., Breier, C.F.,
Nishikawa, J., 2015. Fukushima 137Cs at the base of planktonic food webs off Japan.
Deep Sea Res. Part I 106, 9–16.
Bryan, G., 1963. The accumulation of radioactive caesium by marine invertebrates. J.
Mar. Biol. Assoc. U. K. 43, 519–539.
Buesseler, K.O., Dai, M., Aoyama, M., Benitez-Nelson, C., Charmasson, S., Higley, K.,
Maderich, V., Masqué, P., Morris, P.J., Oughton, D., Smith, J.N., 2017. Fukushima
Daiichi–derived radionuclides in the ocean: transport, fate, and impacts. Ann. Rev.
Mar. Sci. 9, 173–203.
Buesseler, K.O., Jayne, S.R., Fisher, N.S., Rypina, I.I., Baumann, H., Baumann, Z., Breier,
C.F., Douglass, E.M., George, J., Macdonald, A.M., 2012. Fukushima-derived radio-
nuclides in the ocean and biota off Japan. Proc. Natl. Acad. Sci. Unit. States Am. 109,
5984–5988.
Chong, K., Wang, W.-X., 2001. Comparative studies on the biokinetics of Cd, Cr, and Zn in
the green mussel Perna viridis and the manila clam Ruditapes philippinarum. Environ.
Pollut. 115, 107–121.
Donat, J.R., Bruland, K.W., 1995. Trace elements in the ocean. In: Salbu, B., Steinnes, E.
(Eds.), Trace Elements in Natural Waters. CRC Press, Florida, pp. 247–281.
Du Bois, P.B., Laguionie, P., Boust, D., Korsakissok, I., Didier, D., Fiévet, B., 2012.
Estimation of marine source-term following Fukushima Dai-ichi accident. J. Environ.
Radioact. 114, 2–9.
Fisher, N.S., 1986. On the reactivity of metals for marine phytoplankton. Limnol.
Oceanogr. 31, 443–449.
Fisher, N.S., Reinfelder, J.R., 1995. The trophic transfer of metals in marine systems. In:
Tessier, A., Turner, D.R. (Eds.), Metal Speciation and Bioavailability in Aquatic
Systems. John Wiley & Sons, Chichester, pp. 363–406.
Fisher, N.S., Teyssié, J.-L., Fowler, S.W., Wang, W.-X., 1996. Accumulation and retention
of metals in mussels from food and water: a comparison under field and laboratory
conditions. Environ. Sci. Technol. 30, 3232–3242.
Guimarães, J.R.D., 1992. Bioaccumulation of 137Cs and 60Co by a tropical marine teleost
Epinephelus sp. Sci. Total Environ. 120, 205–212.
Güngör, N., Tugrul, B., Topcuoǧlu, S., Güngör, E., 2001. Experimental studies on the
biokinetics of 134Cs and 241Am in mussels (Mytilus galloprovincialis). Environ. Int. 27,
259–264.
Heldal, H.E., Stupakoff, I., Fisher, N.S., 2001. Bioaccumulation of 137Cs and 57Co by five
marine phytoplankton species. J. Environ. Radioact. 57, 231–236.
Hutchins, D.A., Teyssié, J.-L., Boisson, F., Fowler, S.W., Fisher, N.S., 1996. Temperature
effeccts on uptake and retention of contaminant radionuclides and trace metals by the
brittle star Ophiothrix fragilis. Mar. Environ. Res. 41, 363–378.
IAEA, 2004. Sediment Distribution Coefficients and Concentration Factors for Biota in the
Marine Environment. Tech. Rept. Ser.. vol. 422 International Atomic Energy
Agency, Vienna.
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.
Jeffree, R.A., Warnau, M., Teyssié, J.-L., Markich, S.J., 2006. Comparison of the bioac-
cumulation from seawater and depuration of heavy metals and radionuclides in the
spotted dogfish Scyliorhinus canicula (Chondrichthys) and the turbot Psetta maxima
(Actinopterygii: teleostei). Sci. Total Environ. 368, 839–852.
Kaeriyama, H., Watabe, T., Kusakabe, M., 2008. 137Cs concentration in zooplankton and
its relation to taxonomic composition in the western North Pacific Ocean. J. Environ.
Radioact 99, 1838–1845.
Ke, C., Yu, K., Lam, P.K., Wang, W.-X., 2000. Uptake and depuration of cesium in the
green mussel Perna viridis. Mar. Biol. 137, 567–575.
Komarov, E., Bennett, B., 1983. Selected Radionuclides. World Health Organization,
Geneva, pp. 491.
Kuranchie-Mensah, H., Pouil, S., Teyssié, J.-L., Oberhänsli, F., Warnau, M., Metian, M.,
2018. Allometric relationship in the bioaccumulation of radionuclides (134Cs &
241
Am) and delineation of contamination pathways (food and seawater) in bloody
cockle Anadara senilis using radiotracer techniques. J. Environ. Radioact. 192,
448–453.
Lee, B.-G., Wallace, W.G., Luoma, S.N., 1998. Uptake and loss kinetics of Cd, Cr and Zn in
the bivalves Potamocorbula amurensis and Macoma balthica: effects of size and salinity.
Mar. Ecol. Prog. Ser. 175, 177–189.
Lee, C.-S., Fisher, N.S., 2017. Bioaccumulation of methylmercury in a marine copepod.
Environ. Toxicol. Chem. 36, 1287–1293.
Mathews, T., Fisher, N.S., 2009. Dominance of dietary intake of metals in marine elas-
mobranch and teleost fish. Sci. Total Environ. 407, 5156–5161.
Nolan, C., Dahlgaard, H., 1991. Accumulation of metal radiotracers by Mytilus edulis. Mar.
Ecol.: Prog. Ser. 70, 165–174.
Pan, K., Tan, Q.-G., Wang, W.-X., 2016. Two-compartment kinetic modeling of radio-
cesium accumulation in marine bivalves under hypothetical exposure regimes.
Environ. Sci. Technol. 50, 2677–2684.
Pechenik, J.A., 1987. Environmental influences on larval survival and development. In:
Giese, A.C., Pearse, J.S., Pearse, V.B. (Eds.), Reproduction of Marine Invertebrates.
Blackwell Sci. Publ., Palo Alto, pp. 551–608.
Sezer, N., Belivermiş, M., Kılıç, Ö., Topcuoğlu, S., Çotuk, Y., 2014. Biokinetics of radio-
cesium in shrimp (Palaemon adspersus): seawater and food exposures. J. Environ.
Radioact. 132, 15–20.
Strand, P., Sundell-Bergman, S., Brown, J., Dowdall, M., 2017. On the divergences in
assessment of environmental impacts from ionising radiation following the
Fukushima accident. J. Environ. Radioact. 169, 159–173.
Thomas, D.M., Lee, C.-S., Fisher, N.S., 2018. Bioaccumulation and trophic transfer of
D.M. Thomas and N.S. Fisher
137
Cs in marine and freshwater plankton. Chemosphere 209, 599–607.
Ugedal, O., Jonsson, B., Njåstad, O., Næumann, R., 1992. Effects of temperature and body
size on radiocaesium retention in brown trout, Salmo trutta. Freshw. Biol. 28,
165–171.
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.
Wang, C., Baumann, Z., Madigan, D.J., Fisher, N.S., 2016. Contaminated marine sedi-
ments as a source of cesium radioisotopes for benthic fauna near Fukushima. Environ.
Sci. Technol. 50, 10448–10455.
Wang, C., Cerrato, R.M., Fisher, N.S., 2018. Temporal changes in 137Cs concentrations in
fish, sediments, and seawater off Fukushima Japan. Environ. Sci. Technol. 52,
13119–13126.
Wang, W.-X., Dei, R.C., 1999. Factors affecting trace element uptake in the black mussel
Septifer virgatus. Mar. Ecol. Prog. Ser. 186, 161–172.
Wang, W.-X., Fisher, N.S., 1997. Modeling metal bioavailability for marine mussels. Rev.
Environ. Contam. Toxicol. 151, 39–65.
Wang, W.-X., Fisher, N.S., 1998. Accumulation of trace elements in a marine copepod.
Limnol. Oceanogr. 43, 273–283.
Wang, W.-X., Fisher, N.S., 1999. Assimilation efficiencies of chemical contaminants in
aquatic invertebrates: a synthesis. Environ. Toxicol. Chem. 18, 2034–2045.
Wang, W.-X., Fisher, N.S., Luoma, S.N., 1996. Kinetic determinations of trace element
bioaccumulation in the mussel Mytilus edulis. Mar. Ecol. Prog. Ser. 140, 91–113.
Wang, W.-X., Ke, C., Yu, K., Lam, P.K., 2000. Modeling radiocesium bioaccumulation in a
marine food chain. Mar. Ecol. Prog. Ser. 208, 41–50.
Warnau, M., Fowler, S.W., Teyssié, J.-L., 1996. Biokinetics of selected heavy metals and
radionuclides in two marine macrophytes: the seagrass Posidonia oceanica and the
alga Caulerpa taxifolia. Mar. Environ. Res. 41, 343–362.
Wolfe, D.A., Coburn Jr., C., 1970. Influence of salinity and temperature on the accumu-
lation of cesium-137 by an estuarine clam under laboratory conditions. Health Phys.
18, 499–505.
Zhao, X., Wang, W.-X., Yu, K.N., Lam, P.K.S., 2001. Biomagnification of radiocesium in a
marine piscivorous fish. Mar. Ecol. Prog. Ser. 222, 227–237.