Article
pubs.acs.org/est
Comparison of Bioavailability and Biotransformation of Inorganic
and Organic Arsenic to Two Marine Fish
Wei Zhang,† Wen-Xiong Wang,‡ and Li Zhang*,†
†
Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology,
South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
‡
Division of Life Science, State Key Laboratory of Marine Pollution, Hong Kong University of Science and Technology (HKUST),
Clearwater Bay, Kowloon, Hong Kong China
S Supporting Information
*
ABSTRACT: Dietary uptake could be the primary route of
arsenic (As) bioaccumulation in marine fish, but the bioavailability of inorganic and organic As remains elusive. In this study,
we investigated the trophic transfer and bioavailability of As in
herbivorous rabbitfish Siganus f uscescens and carnivorous seabass
Lateolabrax japonicus. Rabbitfish were fed with one artificial diet
or three macroalgae, whereas seabass were fed with one artificial
diet, one polychaete, or two bivalves for 28 days. The six spiked
fresh prey diets contained different proportions of inorganic As
[As(III) and As(V)] and organic As compounds [methylarsenate
(MMA), dimethylarsenate (DMA), and arsenobetaine (AsB)],
and the spiked artificial diet mainly contained As(III) or As(V).
We demonstrated that the trophic transfer factors (TTF) of As in
both fish were negatively correlated with the concentrations of
inorganic As in the diets, while there was no relationship between TTF and the AsB concentrations in the diets. Positive
correlation was observed between the accumulated As concentrations and the AsB concentrations in both fish, suggesting that
organic As compounds (AsB) were more trophically available than inorganic As. Furthermore, the biotransformation ability of
seabass was higher than that in rabbitfish, which resulted in higher As accumulation in seabass than in rabbitfish. Our study
demonstrated that different prey with different inorganic/organic As proportions resulted in diverse bioaccumulation of total As
in different marine fish.
■
inorganic As species,17−19 and little is known about the
bioavailability of organic As. Earlier, we employed a radiotracer
technique to quantify the dissolved uptake, dietary assimilation
and subsequent efflux of As(V) in a marine predatory fish,
Terapon jarbua. We found that As(V) had a low bioavailability to
T. jarbua.18 Thus, far, no study has compared the bioavailability
of inorganic and organic As in marine fish.
The purpose of this study was therefore to differentiate
between the bioavailability of inorganic and organic As from
different prey species and examine how As species may control
bioaccumulation in marine fish. We investigated the trophic
transfer and bioavailability of As in two marine fish, namely,
herbivorous rabbitfish (Siganus f uscescens) and carnivorous
seabass (Lateolabrax japonicus), following a series of artificial
and fresh dietary (three macroalgae, one polychaete, and two
bivalves) exposures. We chose artificial and different fresh diets
to elucidate the effects of prey types containing different As
INTRODUCTION
Arsenic (As) is a pervasive environmental toxin with worldwide
human health implications and its contamination in the environment has been widely reported.1,2 Arsenic is widely distributed in
all organisms,3 and total As concentrations in marine fish are
higher (1−10 μg/g) than those in freshwater fish (<1 μg/g).4−6
Much higher concentrations of As in marine fish has been
documented in the coastal waters of China, e.g., 4.81 to 134 μg/g dw
in seven marine fish collected from Zhanjiang, Guangdong.7
Variation of As concentrations among fish species can be significant,8−10 but little is known about the mechanism underlying
such interspecies difference.
Arsenic has a very complex chemistry, and its speciation
influences its bioavailability and bioaccumulation in marine
organisms.11−14 Therefore, the relative proportions of inorganic
and organic As are potentially important in affecting their
bioavailability and may explain the differences in bioaccumulation of marine fish. However, much uncertainty still exists on the
bioavailability of the various forms of As in marine fish. Several
studies have addressed the bioavailability of As from water or
sediment, but few on the trophic transfer along a food chain.15,16
Most of these earlier bioavailability studies merely focused on
© 2016 American Chemical Society
Received:
Revised:
Accepted:
Published:
2413
December 25, 2015
January 26, 2016
February 2, 2016
February 2, 2016
DOI: 10.1021/acs.est.5b06307
Environ. Sci. Technol. 2016, 50, 2413−2423
Article
Environmental Science & Technology
seabass are important commercial and cage-cultured marine fish,
and are also commonly consumed. The two fish have different
feeding habits. The rabbitfish is considered herbivorous, feeding
primarily on macroalgae, and the seabass is considered
carnivorous, feeding on polychaetes, oysters, and clams. They
were acclimated under the test conditions for 2 weeks prior to the
beginning of exposure experiment. Rabbitfish and seabass were
then exposed to dietborne As for 28 d. In the control treatment,
the fish were fed with the unspiked artificial diet. There were thus
a total of 16 treatment tanks [four dietborne exposures for both
As(III) and As(V) for each fish species] with a sample number of
17−24 fish per tank for rabbitfish, and 21−26 fish per tank for
seabass. The rabbitfish in As(III) exposed artificial diets
treatment were all dead. The tanks were under a light/dark
cycle of 12:12 h. Fish were fed twice per day (1 h for each feeding
regime) and any uneaten food was removed to prevent negligible
waterborne As exposure. Feeding amounts were about 3 ± 0.2%,
and there was no significant difference among different
treatments. At the end of 28 d exposure, they were starved for
approximately 24 h to allow the depuration of gut contents. The
fish were then collected and placed in a sealed polyethylene bag.
After the seawater on the surface of whole fish body was blotted
dry, they were immediately measured for standard length and wet
weight, and then frozen at −80 °C for further analysis.
Chemicals, Reagents, Total Arsenic, and Arsenic
Species Analysis. The frozen fish for each treatment were
thawed on ice and the intestine, liver, and dorsal muscle tissues of
the fish were carefully dissected. Then, they were freeze-dried
until constant weight. The dried samples were homogenized and
stored in small polyethylene plastic vials for later total As and As
speciation analysis.
Total As analysis was described in our previous study.32 The
accuracy of our digestion method was testified by analysis of
standard reference material (SRM) of tuna fish (BCR-627,
Institute for Reference Materials and Measurements, Geel,
Belgium). The detected total As concentration in tuna fish was
4.81 ± 0.12 μg/g, as compared to the certified value of 4.8 ±
0.3 μg/g. The As concentrations in the tuna fish were expressed
as μg/g dry weight. As speciation analysis was also described in
our previous study.32 The extraction efficiencies and analysis
methods were evaluated by the analysis of SRM tuna fish.
BCR-627 tuna fish tissue (0.05 g) was used for AsB and
dimethylarsinic acid (DMA) analysis. They contained AsB 3.80 ±
0.35 μg/g (97% recovery, n = 6) and DMA 1.24 ± 0.26 μg/g
(83% recovery, n = 6). Spikes were used to confirm the recovery
of other As species detected during speciation analysis. In our
study, the recovery rates of As(III), As(V) and monomethylarsonic acid (MMA) were 76−94%, 78−99%, and 80−91%,
respectively. Additionally, we used arsenocholine (AsC) to
quantify the unidentified As. If a compound was detected with a
retention time that did not correspond to those of available
standard materials, then it was recorded as an unidentified
compound.
Statistical Analysis. Statistical analysis was performed using
SPSS version 16.0. The differences of the corresponding values
among different treated groups were tested by one-way analysis
of variance (ANOVA) followed by a least significant difference
(LSD) test. A probability level (p-value) of less than 0.05 was
regarded as statistically significant.
species on bioaccumulation and bioavailability of As. Among
these prey, As(V) was the most abundant species in marine
macroalgae, especially in contaminated environment, and
arsenosugars (AsS) were also the common As species.20−24
The polychaete Arenicola marina contained mainly inorganic As
with a ratio of inorganic As to total As of 74%,25 60.9%,26
respectively. In contrast, the oyster Saccostrea cucullata contained
mainly organic As, with arsenobetaine (AsB) constituting about
83.0−95.1% of total As.27−29 In an earlier study, the amount of
assimilated As in the crab Carcinus maenas was dependent on the
chemical form of As present in the food.30 Biotransformation of
inorganic As to organic As can determine its bioavailability in
organisms ingesting food containing these compounds.31
Therefore, we hypothesized that species differences in prey
selection may be responsible for the differences in bioaccumulation and bioavailability of As for marine fish.
■
MATERIALS AND METHODS
Exposure Diets. The red algae Gracilaria lemaneiformis and
Gracilaria gigas were collected from Shantou, the polychaete
Nereis succinea was collected from Zhanjiang, and the green algae
Ulva lactuca, the oyster Saccostrea cucullata and the clam Asaphis
violascens were collected from Shenzhen, China, in March 2014.
For artificial diets (purchased from a feed company in
Shenzhen, China), As(III) or As(V) was added to the diet as
an aqueous solution of arsenite and arsenate (NaAsO2 and
Na2HAsO4·7H2O, Sigma, U.S.A.), respectively, to achieve a
nominal concentration of 20 μg As/g diet. After the diet pellets
were completely soaked with the As solution, they were dried at
60 °C to constant weight. The diets were only spiked with
As(III) or As(V) for 2 h to minimize the possible transformation
of As in the diets. The diets were then stored at −20 °C in sealed
polyethylene bags until they were used. The spiked artificial diets
were fed to both fish (rabbitfish and seabass).
The red algae G. lemaneiformis, G. gigas, green alga U. lactuca as
the food of rabbitfish were directly exposed to waterborne
As(III) and As(V) (1 mg/L) for 4−7 d. After the exposure, they
were minced on a chopping board using a knife, and after
weighing, they were mixed with pure gelatin powder at a ratio
of 5 (ww prey):1 (dw gelation) with addition of a ratio of 3
(ww prey): 1 (Milli-Q water). The polychaete, oyster, and clam
as the food of seabass were also directly exposed to waterborne
As(III) and As(V) (1 mg/L) for 4−7 d. After the exposure,
oysters and clams were dissected to obtain their soft tissues. They
were then minced on a chopping board using a knife, and after
weighing, they were mixed with pure gelatin powder at a ratio of
31 (ww prey):1(dw gelation) without addition of Milli-Q water.
The mixture was heated in a 40 °C water bath for several
minutes and frozen at −80 °C. The homogenization ensured
replicability of uniform meals, mainly because different
constituent organs (especially digestive glands of the molluscs)
had different accumulated metal compositions. The frozen
macroalgae, polychaete, oyster, and clam homogenates in gelatin
were then cut into small pieces (about 5 × 5 mm2), partially
thawed at room temperature and fed to the marine fish.
Experimental Design. Rabbitfish S. f uscescens (8.6−9.8 cm
in length) and seabass L. japonicus (7.6−15.9 cm in length) were
obtained from a fish farm at Shenzhen, China, maintained
in natural sand-filtered seawater (24−26 °C, 33‰) and fed with
unspiked artificial and fresh diets twice a day at about 3% of their
body weight. The control treatments were fed with unspiked
artificial diets, and the exposed treatments were fed with unspiked
fresh diets in order to acclimate to the food. The rabbitfish and
■
RESULTS
Arsenic Speciation in Exposed Food. Different fish diets
contained different proportions of inorganic As [As(III) and
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DOI: 10.1021/acs.est.5b06307
Environ. Sci. Technol. 2016, 50, 2413−2423
Values are means ± SD (n = 3). The foods consist of artificial diets, red algae G. lemaneiformis, G.gigas, green algae U. lactuca, polychaete N. succinea, oyster S. cucullata, and clam A. violascens. As(III),
arsenite; As(V), arsenate; MMA, monomethylarsonate; DMA, dimethylarsinate; AsB, arsenobetaine. BDL (below detection limit).
BDL
19.0 ± 0.47 (79.7 ± 1.33%)
3.67 ± 0.39 (15.4 ± 1.02%)
0.48 ± 0.03 (2.01 ± 0.20%)
0.43 ± 0.08 (1.81 ± 0.26%)
As(V) clam
0.25 ± 0.07 (1.06 ± 0.25%)
3.85 ± 0.58 (16.8 ± 3.54%)
1.02 ± 0.08 (4.45 ± 0.61%)
As(V) oyster
a
28.2 ± 4.50
25.6 ± 2.46
BDL
5.07 ± 1.02 (22.0 ± 3.06%)
12.6 ± 1.10 (54.6 ± 0.41%)
15.2 ± 3.46
5.05 ± 0.18 (23.6 ± 1.82%)
2.69 ± 0.01 (12.5 ± 0.49%)
As(V) polychaete
0.50 ± 0.04 (2.16 ± 0.32%)
BDL
11.2 ± 1.09 (52.2 ± 2.84%)
1.87 ± 0.02 (8.70 ± 0.28%)
24.7 ± 0.40
0.31 ± 0.01 (2.07 ± 0.01%)
0.20 ± 0.00 (1.32 ± 0.09%)
As(III) clam
0.66 ± 0.02 (3.09 ± 0.24%)
BDL
10.6 ± 0.73 (70.2 ± 1.34%)
3.73 ± 0.04 (24.6 ± 0.96%)
20.4 ± 4.46
2.72 ± 0.10 (11.3 ± 0.77%)
1.81 ± 0.35 (7.53 ± 1.68%)
As(III) oyster
0.27 ± 0.03 (1.79 ± 0.28%)
BDL
BDL
7.35 ± 0.21 (36.4 ± 0.01%)
12.0 ± 0.73 (49.7 ± 1.51%)
7.03 ± 0.50 (29.1 ± 1.20%)
1.01 ± 0.01 (4.99 ± 0.19%)
5.71 ± 0.17 (28.3 ± 0.03%)
5.77 ± 0.12 (28.6 ± 0.20%)
As(III) polychaete
0.59 ± 0.04 (2.45 ± 0.26%)
6.71 ± 0.25 (66.6 ± 1.58%)
0.08 ± 0.00 (0.80 ± 0.01%)
As(V) U. lactuca
0.35 ± 0.08 (1.71 ± 0.34%)
16.8 ± 1.32
13.0 ± 2.58
2.09 ± 0.10 (20.7 ± 1.29%)
0.26 ± 0.05 (2.61 ± 0.43%)
0.83 ± 0.03 (8.24 ± 0.40%)
5.59 ± 1.40
8.44 ± 0.37 (54.8 ± 1.04%)
0.11 ± 0.01 (0.70 ± 0.12%)
As(V) G.gigas
0.11 ± 0.03 (1.04 ± 0.30%)
4.51 ± 0.11 (29.2 ± 1.11%)
0.75 ± 0.13 (19.0 ± 2.21%)
0.74 ± 0.03 (19.1 ± 2.06%)
0.01 ± 0.00 (0.03 ± 0.01%)
2.06 ± 0.46 (13.3 ± 2.16%)
0.57 ± 0.07 (14.5 ± 0.76%)
1.73 ± 0.07 (44.3 ± 0.96%)
0.07 ± 0.01 (1.66 ± 0.04%)
As(V) G. lemaneiformis
0.31 ± 0.04 (2.00 ± 0.12%)
15.8 ± 1.48 (67.5 ± 5.98%)
0.48 ± 0.02 (2.06 ± 0.07%)
As(III) U. lactuca
0.05 ± 0.00 (1.34 ± 0.01%)
74.9 ± 3.64
26.5 ± 4.01
3.50 ± 1.71 (15.0 ± 7.39%)
0.80 ± 0.06 (3.42 ± 0.23%)
2.65 ± 0.22 (11.3 ± 0.88%)
34.5 ± 1.05
76.9 ± 1.97 (83.2 ± 0.18%)
5.06 ± 0.67 (5.46 ± 0.58%)
0.17 ± 0.05 (0.72 ± 0.23%)
7.21 ± 0.27 (7.79 ± 0.08%)
BDL
2.86 ± 0.35 (3.10 ± 0.46%)
34.2 ± 4.46
As(III) G.gigas
0.43 ± 0.00 (0.46 ± 0.01%)
3.19 ± 2.90 (12.9 ± 2.51%)
BDL
0.18 ± 0.01 (0.54 ± 0.01%)
0.11 ± 0.04 (0.30 ± 0.10%)
1.44 ± 0.04 (3.97 ± 0.23%)
0.07 ± 0.02 (0.21 ± 0.05%)
28.3 ± 1.69 (78.0 ± 2.41%)
1.13 ± 0.07 (3.11 ± 0.10%)
As(III) G. lemaneiformis
BDL
30.1 ± 0.94 (94.1 ± 1.88%)
1.66 ± 0.67 (5.15 ± 1.83%)
As(V) artificial diets
0.62 ± 0.06 (1.69 ± 0.12%)
total As
DMA
8.57 ± 0.14 (28.5 ± 0.78%)
MMA
BDL
5.35 ± 0.13 (17.8 ± 0.62%)
16.0 ± 0.53 (53.1 ± 1.18%)
As species concentrations (μg/g) and distribution (%)
AsB
2415
As(III) artificial diets
We chose the muscle tissue mainly because it was the major
storage compartment of As. TTF can better illustrate the
bioavailability of As in two marine fish within a relatively short
exposure period. Accordingly, the calculated TTF was 0.002−
0.078 and 0.021−0.244 in muscle of rabbitfish and seabass,
respectively (Table 2). These calculated values were much
lower than 1, suggesting that As did not biomagnify in the marine
fish during the trophic transfer process. However, there was
clear difference among the different diets, e.g., TTF (0.244)
in the As(III) exposed clam treatment was 120 times higher than
that in the As(III) exposed U. lactuca treatment. In rabbitfish,
the TTF (0.078) in the As(V) exposed G. lemaneiformis
treatment was about 40 times higher than that in the As(III)
As(V)
/metal concentration in food type
As(III)
Table 1. Total As, As Species Concentrations and Distribution (%) in Spiked/Exposed Fooda
TTF = newly accumulated concentration in muscle
0.15 ± 0.075 (0.49 ± 0.23%)
BDL
unidentified As
21.6 ± 1.70
As(V)] and organic As compounds (MMA, DMA, unidentified
As, and AsB) (Table 1). The background concentrations and
distribution of unspiked diets are shown in the Supporting
Information, SI, Table S1. For artificial diets, As(III) and As(V)
exposed artificial diets exhibited a predominance of As(III)
(53.1%) and As(V) (91.4%), respectively, while the percentages
of AsB (0.49−0.54%) were very low. For macroalgal diets, As(V)
(44.3−83.2%) was the predominant form of As in As(III) and
As(V) exposed G. lemaneiformis, G. gigas, U. lactuca, followed by
unidentified As, DMA, AsB, As(III), and MMA. Distributions of
AsB (19.1%), unidentified As (19.0%), and DMA (14.5%) were
comparable in the As(V) exposed G. lemaneiformis. The
unidentified As was presumably AsS.
For polychaete diets, inorganic As (56.9%) was the
predominant As compound in the As(III) exposed polychaetes,
followed by AsB (36.4%). For bivalve diets, AsB (49.7%) was the
predominant As compound in the As(III) exposed oysters,
followed by DMA, whereas DMA was the major As compound
(54.6%) followed by AsB in the As(V) exposed oysters.
Moreover, AsB (70.2−79.7%) was the predominant As
compound in the exposed clams, followed by DMA. Therefore,
different prey had different As species distributions.
Bioaccumulation and Trophic Transfer Factor (TTF) in
Fish. The ranges of total As concentrations were 0.65−1.43 μg/g,
0.78−1.78 μg/g, and 1.04−1.86 μg/g in intestine, liver, and
muscle tissues of rabbitfish, and were 2.37−6.49 μg/g, 1.83−
9.83 μg/g, and 2.59−7.85 μg/g in intestine, liver, and muscle
tissues of seabass, respectively (Table 2). After exposure to
As(V) exposed artificial diets for 28 d, the As concentrations in
intestine (2.91 μg/g), liver (3.09 μg/g), and muscle (4.64 μg/g)
of seabass were significantly higher than the background
concentrations, whereas no significant change was found for
rabbitfish (Figure 1A, B). These suggested that the bioaccumulation ability of seabass was much higher than that in rabbitfish.
We further calculated the newly accumulated As concentrations
as the total As minus the background concentrations in fish.
The newly accumulated As concentrations were 0.43−0.82 μg/g
and 0.43−5.26 μg/g in the muscle of rabbitfish and seabass,
respectively. Differences in the newly As accumulation in the
muscle were 3.6 and 12.2-fold in rabbitfish and seabass
respectively, suggesting that different diets and As concentrations
had significant effects on As bioaccumulation.
Since there were large differences in As concentrations in
different prey, the TTF of As from each food type to the fish in
muscle tissue after 28 d of exposure was calculated using the
following equation:
27.3 ± 0.19
Article
Environmental Science & Technology
DOI: 10.1021/acs.est.5b06307
Environ. Sci. Technol. 2016, 50, 2413−2423
Article
Environmental Science & Technology
Table 2. Total As Concentrations in Intestine, Liver, And Muscle Tissues of Marine Rabbitfish and Seabass after 28 d Different
Dietborne Exposurea,b
As concentrations (μg/g)
number
intestine
liver
muscle
TTF
0.78 ± 0.23
1.46 ± 0.58c
1.20 ± 0.16
1.76 ± 0.37c
1.19 ± 0.18
1.78 ± 0.37c
1.30 ± 0.27
1.62 ± 0.39c
1.04 ± 0.09
1.86 ± 0.33d
1.65 ± 0.09d
1.71 ± 0.34d
1.15 ± 0.12
1.48 ± 0.13c
1.54 ± 0.12c
1.66 ± 0.11d
0.024 ± 0.010b
0.008 ± 0.001a
0.002 ± 0.001a
0.004 ± 0.001a
0.078 ± 0.023d
0.030 ± 0.007b
0.048 ± 0.009c
1.83 ± 0.67
3.38 ± 0.84c
3.47 ± 0.36c
6.77 ± 1.48d
8.69 ± 1.00d
3.09 ± 0.81
2.78 ± 0.62
5.85 ± 1.10d
9.83 ± 1.42d
2.59 ± 0.67
4.36 ± 0.88c
3.68 ± 0.65c
4.03 ± 0.64c
6.29 ± 1.26d
4.64 ± 1.76d
4.08 ± 0.86c
3.02 ± 0.36
7.85 ± 0.86d
0.082 ± 0.041b
0.054 ± 0.032ab
0.058 ± 0.026ab
0.244 ± 0.083c
0.060 ± 0.052ab
0.053 ± 0.031ab
0.021 ± 0.011a
0.193 ± 0.032c
Rabbitfish
control
As(III) G. lemaneiformis
As(III) G.gigas
As(III) U. lactuca
As(V) artificial diets
As(V) G. lemaneiformis
As(V) G.gigas
As(V) U. lactuca
12
14
20
20
14
24
24
12
0.65 ± 0.04
1.27 ± 0.30d
1.14 ± 0.28c
1.08 ± 0.23c
0.86 ± 0.26
1.39 ± 0.35d
1.43 ± 0.27d
1.07 ± 0.12c
control
As(III) artificial diets
As(III) polychaete
As(III) oyster
As(III) clam
As(V) artificial diets
As(V) polychaete
As(V) oyster
As(V) clam
20
24
22
22
20
12
22
14
14
2.37 ± 0.25
3.09 ± 0.85
3.09 ± 0.44
4.94 ± 0.70d
6.49 ± 0.60d
2.91 ± 0.04
2.98 ± 0.51
3.54 ± 0.34c
5.94 ± 0.77d
Seabass
a
Values are means ± SD (n = 12−24). The foods consist of artificial diets, red algae G. lemaneiformis, G.gigas, green algae U. lactuca, polychaete,
oyster, and clam. bDifferent letters indicate statistically significant differences among different treatments (p < 0.05). cIndicate significant difference
(p < 0.05). dIndicate significant difference (p < 0.01).
Figure 1. Comparison of the As concentrations (μg/g) in rabbitfish (A) and seabass (B) after As(V) exposed artificial diet exposure. Data are means ±
SD (n = 18−20). The ratio of organic As and inorganic As in intestine, liver, and muscle tissues of rabbitfish (C) and seabass (D) after different dietborne
exposure for 28 d. The foods contain artificial diets, red algae G. lemaneiformis, G.gigas, green algae U. lactuca, polychaete N. succinea, oyster S. cucullata,
and clam A. violascens. Data are means ± SD (n = 3). *represent significant differences between control and treatment (p < 0.05).
exposed U. lactuca treatment. Thus, different diets affected the As
trophic transfer potential in marine fish.
In this study, the bioavailability of As can be quantified by TTF
and accumulated As concentration. We first analyzed the
relationships between As species concentration in fish and
in diets. Three tissues of both fish displayed no significant
correlation between inorganic As concentrations in fish and
those in diets, except inorganic As in intestine of rabbitfish.
In contrast, three tissues of seabass displayed significant correlations between their AsB concentrations and those in diets
(Figure 2; Figure 3). Clearly, the trophic transfer of As in seabass
was dependent on its existing form in the prey.
We further analyzed the relationships between TTF and As
species concentrations in different diets, and between the newly
accumulated As concentrations and As species (both inorganic
and organic As species) concentrations in both fish. An inverse
relationship between TTF and inorganic As concentrations in
diets was observed, while there was no relationship between TTF
and AsB concentrations in diets (Figure 4). In muscle tissues of
rabbitfish and seabass, a positive correlation was observed
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DOI: 10.1021/acs.est.5b06307
Environ. Sci. Technol. 2016, 50, 2413−2423
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Environmental Science & Technology
Figure 2. Correlation between As species concentrations in rabbitfish and in diets after dietborne exposure for 28 d.
between the newly accumulated As concentrations and AsB
concentrations (subtracting the background concentrations),
while there was no correlation between the newly accumulated
As concentrations and inorganic As concentrations (Figure 5).
These results strongly indicated that AsB was easier transferred
and assimilated than inorganic As in the fish, therefore, the
bioavailability of organic compounds (mainly AsB) was higher
than inorganic As.
Arsenic Biotransformation in Fish. The speciation of As in
different fish tissues by the end of 28 d of exposure was further
analyzed (Table 3; Table 4). In three tissues of rabbitfish, with a
few exceptions, AsB was the predominant As species (54.8−
82.0%, 53.3−88.2%, 88.4−93.8% in intestine, liver, and muscle,
respectively). Inorganic As was 12.9−50.3%, 10.0−59.0%, and
5.2−10.2% in intestine, liver, and muscle, respectively. Similarly,
AsB was also the predominant As species in different tissues of
seabass, and DMA and inorganic As were only minor components. DMA (4.4−34.7%) and inorganic As (1.22−36.8%)
were comparable in livers. In both fish, AsB was enriched in the
intestine (30−80%) from the diet, and became the predominant
As component in the liver and muscle (>90%), independent of
the As speciation in the diet. Moreover, the AsB proportion of
total As in diets and different tissues followed the order of diets<
intestine ≤ liver < muscle (Figure S1). In addition, in all exposed
treatments of rabbitfish except As(V) exposed artificial diets
treatments and artificial diets exposed treatments of seabass, the
accumulated concentrations of AsB in the tissues followed the
pattern of diets < intestine < liver < muscle (Table 1; Table S2;
Table S3). For instance, in the As(III) exposed G. lemaneiformis
treatment for rabbitfish, through calculation, ingestion rate was
maintained constant at about 3% of fish body weight. The total
input of AsB through feed was 16.04 g (wet weight) × 3% ×
28 d × 0.11 μg/g (AsB concentration in food) = 1.48 μg. If we
assumed that the assimilation efficiency was 100% at the end
of 28 d exposure, then the accumulated AsB concentration was
1.48 μg/17.9 g (wet weight by the end of 28 d) = 0.083 μg/g,
but the detected AsB concentration in muscle of rabbitfish was
1.97 μg/g. Therefore, these results strongly suggested that
biotransformation of As occurred in marine fish. For simplicity,
we compared the ratio of organic As to inorganic As in different
tissues to contrast the differences in biotransformation. Such
ratios in different tissues of seabass were relatively higher than
those in rabbitfish, suggesting that the conversion ability in
seabass was higher than that in rabbitfish (Figure 1C and D).
For example, in the As(V) exposed artificial diet in which
the predominant form of As was As(V), while the ratios of
organic As to inorganic As were 0.72, 3.18, 8.84 in intestine,
liver, and muscle tissues of rabbitfish, and those were 11.75,
14.35, 14.75 in intestine, liver, and muscle tissues of seabass,
respectively.
■
DISCUSSION
Bioavailability of Inorganic and Organic Arsenic in
Fish. In our study, three tissues of rabbitfish and seabass
displayed no significant correlation between inorganic As
concentrations in fish and those in diets, except inorganic As in
the intestine of rabbitfish. One possibility was that inorganic As
was transformed to organic As in the fish. In contrast, AsB in
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Figure 3. Correlation between As species concentrations in seabass and in diets after dietborne exposure for 28 d.
Figure 4. Correlation between trophic transfer factors (TTF) and As species concentrations in diets after 28 d exposure.
compared the bioavailability of inorganic vs organic As. Kirby and
Maher33 investigated the accumulation and distribution of As
compound in marine fish species in relation to their trophic
position. They speculated that As compounds present in fish
tissues may be different depending on trophic position (diet)
carnivorous seabass was strongly correlated with those in diets
(containing major AsB), indicating that AsB was more
trophically available (bioavailable) than inorganic As. One likely
explanation for such a correlation was that AsB was the final
storage form of As in the fish tissues. Very few earlier studies have
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Figure 5. Correlation between newly accumulated As concentrations and As species concentrations in muscle of rabbitfish and seabass in different
exposure treatments for 28 d. (AsB subtracted the background concentrations).
Table 3. As Species Distribution (%) in Intestine, Liver, And Muscle Tissues of Marine Rabbitfish after Different Dietborne
Exposure for 28 da
As species distribution (%)
As(III)
a
control
As(III) G. lemaneiformis
As(III) G.gigas
As(III) U. lactuca
As(V) artificial diets
As(V) G. lemaneiformis
As(V) G.gigas
As(V) U. lactuca
4.81 ± 2.02
23.2 ± 5.87
10.6 ± 2.23
9.92 ± 3.98
11.9 ± 1.57
3.39 ± 1.70
2.62 ± 1.37
7.15 ± 1.58
control
As(III) G. lemaneiformis
As(III) G.gigas
As(III) U. lactuca
As(V) artificial diets
As(V) G. lemaneiformis
As(V) G.gigas
As(V) U. lactuca
26.0 ± 4.17
33.5 ± 4.58
20.2 ± 0.18
21.0 ± 8.96
14.3 ± 3.26
13.6 ± 0.18
7.64 ± 0.47
4.76 ± 0.70
control
As(III) G. lemaneiformis
As(III) G.gigas
As(III) U. lactuca
As(V) artificial diets
As(V) G. lemaneiformis
As(V) G.gigas
As(V) U. lactuca
3.04 ± 1.09
2.74 ± 0.92
4.80 ± 1.99
3.76 ± 1.15
4.21 ± 1.44
2.32 ± 0.47
3.71 ± 2.04
2.65 ± 0.30
As(V)
Intestine
8.09 ± 1.38
27.1 ± 8.56
18.0 ± 0.99
9.92 ± 3.98
46.2 ± 5.40
13.0 ± 0.40
14.4 ± 1.32
18.9 ± 0.56
Liver
20.6 ± 4.25
25.5 ± 1.26
15.9 ± 6.20
12.3 ± 0.26
9.63 ± 0.07
12.9 ± 1.68
9.18 ± 4.07
5.27 ± 0.08
Muscle
2.48 ± 0.86
2.50 ± 1.40
2.80 ± 1.09
4.58 ± 3.88
5.95 ± 1.03
1.86 ± 0.08
3.56 ± 1.02
3.05 ± 0.11
MMA
DMA
AsB
2.01 ± 0.02
3.03 ± 2.25
3.21 ± 1.49
1.97 ± 0.04
3.16 ± 0.57
2.18 ± 0.38
2.02 ± 0.70
1.70 ± 0.28
3.07 ± 0.44
20.2 ± 7.31
13.4 ± 4.22
22.9 ± 1.87
12.2 ± 6.20
15.4 ± 12.2
12.8 ± 7.77
7.19 ± 0.04
82.0 ± 0.23
26.5 ± 9.37
54.8 ± 3.98
55.3 ± 6.04
26.6 ± 0.20
66.1 ± 14.7
68.2 ± 4.39
65.0 ± 1.35
BDL
2.45 ± 0.02
BDL
BDL
BDL
BDL
BDL
BDL
10.2 ± 0.12
16.2 ± 1.30
10.6 ± 4.76
3.98 ± 2.04
4.66 ± 1.80
4.49 ± 1.35
3.33 ± 1.51
1.73 ± 0.19
43.3 ± 8.54
22.4 ± 7.12
53.3 ± 10.8
62.8 ± 6.66
71.4 ± 5.12
69.0 ± 0.51
79.9 ± 3.02
88.2 ± 0.43
0.87 ± 0.00
0.50 ± 0.22
0.80 ± 0.29
BDL
0.76 ± 0.34
BDL
BDL
BDL
1.05 ± 0.25
0.61 ± 0.25
1.07 ± 0.08
0.35 ± 0.03
0.72 ± 0.08
1.31 ± 0.30
0.98 ± 0.25
0.53 ± 0.32
92.6 ± 0.03
93.7 ± 2.79
90.5 ± 3.45
91.3 ± 5.05
88.4 ± 0.83
94.5 ± 0.10
91.7 ± 3.31
93.8 ± 0.51
Values are means ± SD (n = 3). The foods consist of artificial diets, G. lemaneiformis, G.gigas, and U. lactuca. BDL (below detection limit).
between inorganic As concentrations in fish and those in diets,
mainly because intestine was the extrinsic digestive part,
which was likely influenced by the surrounding environment
(or biotransformation was low).
and/or their association with marine sediments. Pelagic
carnivorous fish species exposed mainly to AsB through their
diet accumulated this compound in their tissues.14,34 However,
the intestine of rabbitfish displayed significant correlation
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Table 4. As Species Distribution (%) in Intestine, Liver, And Muscle Tissues of Marine Seabass after Different Dietborne Exposure
for 28 da
As species distribution (%)
As(III)
a
control
As(III) artificial diets
As(III) polychaete
As(III) oyster
As(III) clam
As(V) artificial diets
As(V) polychaete
As(V) oyster
As(V) clam
0.60 ± 0.30
0.85 ± 0.67
1.76 ± 0.25
2.65 ± 0.72
1.19 ± 0.24
3.22 ± 0.58
2.88 ± 0.85
2.75 ± 0.87
2.45 ± 0.71
control
As(III) artificial diets
As(III) polychaete
As(III) oyster
As(III) clam
As(V) artificial diets
As(V) polychaete
As(V) oyster
As(V) clam
4.46 ± 1.26
2.82 ± 0.43
3.27 ± 0.31
0.42 ± 0.03
0.23 ± 0.04
3.06 ± 0.76
1.68 ± 0.04
2.66 ± 0.40
0.27 ± 0.01
control
As(III) artificial diets
As(III) polychaete
As(III) oyster
As(III) clam
As(V) artificial diets
As(V) polychaete
As(V) oyster
As(V) clam
3.14 ± 0.34
1.75 ± 0.33
3.41 ± 0.35
2.56 ± 0.59
1.57 ± 0.30
3.24 ± 0.39
2.49 ± 0.01
3.60 ± 0.85
1.84 ± 0.04
As(V)
Intestine
5.31 ± 1.47
3.33 ± 0.07
2.26 ± 0.24
7.15 ± 1.91
1.42 ± 0.33
4.62 ± 0.7
1.49 ± 0.16
3.28 ± 1.46
3.68 ± 0.71
Liver
15.0 ± 7.27
7.38 ± 0.35
33.6 ± 10.7
2.10 ± 1.18
1.61 ± 0.68
3.46 ± 0.48
5.20 ± 1.51
2.32 ± 0.83
0.95 ± 0.15
Muscle
3.62 ± 0.30
1.38 ± 0.30
3.20 ± 0.93
1.37 ± 0.29
1.02 ± 0.11
3.11 ± 0.52
2.21 ± 064
3.34 ± 1.28
1.11 ± 0.05
MMA
DMA
AsB
BDL
4.06 ± 1.10
3.00 ± 1.53
BDL
1.97 ± 0.77
2.19 ± 0.86
0.73 ± 0.33
1.52 ± 0.06
BDL
18.2 ± 9.12
1.80 ± 0.54
0.95 ± 0.17
6.81 ± 0.07
12.0 ± 1.18
7.48 ± 0.04
1.89 ± 0.28
15.4 ± 6.72
6.94 ± 0.95
75.9 ± 10.9
90.0 ± 2.39
92.0 ± 1.70
83.4 ± 2.56
83.4 ± 2.03
82.5 ± 0.70
93.0 ± 0.74
77.0 ± 7.37
86.9 ± 2.37
21.3 ± 1.29
8.16 ± 1.92
8.45 ± 0.61
BDL
BDL
5.01 ± 0.66
5.58 ± 1.54
2.91 ± 0.35
1.30 ± 0.60
22.2 ± 2.93
13.6 ± 2.59
5.31 ± 3.14
34.7 ± 8.77
9.00 ± 2.27
4.42 ± 1.74
8.22 ± 1.27
9.07 ± 3.00
11.4 ± 0.19
37.2 ± 12.8
68.1 ± 0.74
49.4 ± 6.61
62.8 ± 9.91
89.2 ± 1.63
84.1 ± 0.80
79.3 ± 4.27
83.0 ± 2.92
86.1 ± 0.55
BDL
0.07 ± 0.03
0.39 ± 0.03
0.63 ± 0.18
0.25 ± 0.12
0.69 ± 0.48
0.86 ± 0.17
BDL
BDL
0.77 ± 0.08
0.62 ± 0.23
0.64 ± 0.34
0.94 ± 0.16
0.63 ± 0.05
1.37 ± 0.09
0.47 ± 0.05
0.62 ± 0.17
0.62 ± 0.10
92.5 ± 0.72
96.2 ± 0.29
92.4 ± 0.91
94.5 ± 0.54
96.5 ± 0.23
91.6 ± 0.52
94.0 ± 0.52
92.4 ± 0.60
96.4 ± 0.18
Values are means ± SD (n = 3). The foods consist of artificial diets, polychaete, oyster, and clam. BDL (below detection limit).
Earlier studies reported that once inorganic As was inside the
cells, As(V) was removed by several reactions and transformations, including competition with phosphate, binding to
polyphosphates (i.e., adenosine diphosphate, ADP), hydrolysis,
and enzymatic reduction.38,39 Thus, reduction in TTF with
increasing exposure concentration appeared to be driven mostly
by changes in As AE or biotransformation instead of elimination.
There was no relationship between TTF and AsB concentrations in diets, suggesting that TTF was not influenced by the
AsB burden. Presumably, these compounds passed more easily
through the apical membranes of the epithelial cells of the
digestive organs than inorganic As. It is possible that AsB is taken
up via the glycine betaine transport system of marine fish, and
does not participate in metabolism processes. In other words, the
marine fish receiving AsB in their diets accumulated As in this
form without further metabolizing it. Thus, our present study
demonstrated that As transfer along the food chain was
influenced by prey types containing different As species, in
which AsB was assimilated more easily than inorganic As along
the food chain. Very few studies have quantified the
bioavailability of inorganic As and organic As in marine fish.
Earlier studies have simply reported the As bioaccumulation in
organisms following dietborne As exposure. For instance,
yelloweye mullet Aldrichetta forsteri fed upon a range of As
compounds had low retention of As(V) in their muscle tissues,
We observed an inverse relationship between the TTF and
inorganic As concentrations in diets. Inverse correlations
between the TTF and metal (such as Cd, Pb and Zn) concentrations in prey were previously found in juvenile fish T. jarbua
and rainbow trout Oncorhynchus mykiss,35,36 but such correlation
had not been tested for inorganic As. The potential for metal
trophic transfer can be described by the equation: TTF =
(AE × IR)/ke, where AE represents the assimilation efficiency
from ingested prey, IR is the ingestion rate of the predator, and ke is
the efflux rate constant. This equation expressed theoretically the
positive relationship between TTF and AE or IR but a negative
relationship with ke. In this study, IR was maintained constant at
about 3% of the body weight. Therefore, any change in TTF was
likely due to changes of AE and ke. A lower TTF at a higher
inorganic As burden suggested a somewhat less complete digestion and assimilation in the fish or more efficient elimination of
As. One possible mechanism was that inorganic As was less
efficiently assimilated by the limited number of transporters on
the intestine epithelium. Alternatively, the biotransformation
process may influence the assimilation of inorganic As. At high
external inorganic As concentrations, biotransformation may be
facilitated when inorganic As uptake became saturated. WhaleyMartin et al.37 found that high proportions of inorganic As might
result from saturation of biochemical pathways responsible for the
transformation of inorganic arsenicals (from food, water, and/or
sediment) into AsB and other complex organoaresenicals.
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whereas fish that received either AsB or AsC had elevated levels
of As in their muscles.40
In our study, As did not biomagnify in the marine fish,
consistent with earlier studies in aquatic food chain.14,15,18,41,42
Maher et al.14 found no evidence of biomagnification of As in two
Zostera capricorni seagrass ecosystems. Zhang et al.18 suggested
that As did not biomagnify in a marine juvenile fish T. jarbua due
to the very low AE and the relatively high ke. However, feeding on
different diets might affect As biomagnification potential in
marine fish. Biomagnification can occur in some ecosystems as
evidenced by gastropods in rocky intertidal systems.43
After dietary exposure, the bioavailability of AsB was higher
than inorganic As, and AsB contributed to the accumulation of
total As in marine fish. Hong et al.44 investigated the in situ
bioaccumulation of As in various aquatic organisms in a highly
industrialized area of Pohang City, Korea. AsB was the most
dominant form of As in fish, bivalves, crabs, and shrimp and was
directly proportional to the total concentration of As in their
tissues. In our study, positive correlation was observed between
the newly accumulated As concentration and the ratio of organic
As (subtracting the background concentrations)/inorganic As in
seabass (Figure S2). Thus, following the absorption in the
intestine, the bioaccumulation of As compounds may be altered
by biotransformation, leading to dramatic changes in the
bioaccumulation. Therefore, As biotransformation could influence the bioaccumulation of As in marine fish.
Arsenic Bioaccumulation and Biotransformation in
Fish. Our study demonstrated that the potential of As bioaccumulation in seabass was higher than that in rabbitfish. Such
high bioaccumulation in carnivorous seabass may be attributed to
its prey types. Different prey contained different proportions of
inorganic As and organic As compounds, and the diets of seabass
contained more AsB than rabbitfish. AsB could be more
efficiently transmitted than inorganic As along the food chain.
Therefore, our findings again confirmed the relative significance
of prey type in regard to As bioaccumulation in marine fish. The
observed interspecific differences in wild-caught fish found in
previous studies may be explained by differences in diet among
species.45 The herbivorous cyprinids and carnivore fish species
exhibited significantly different abilities to accumulate As in their
body organs, with the maximum As concentration of 4.01 μg/g
recorded in a carnivorous fish Wallago attu, and the minimum
one (2.12 μg/g) in a herbivorous fish Catla catla.46 Therefore,
variation of As concentration among fish species could be
attributed to prey type including different As species.
Alternatively, such high bioaccumulation may be explained by
the higher biotransformation ability in seabass than that in
rabbitfish. When both fish feeding on artificial diets containing
mainly As(V), for example, more As(V) was biotransformed into
organic As by seabass, leading to more As accumulated in seabass
compared with rabbitfish. The fish may adapt and regulate when
different As species pass through the body. One possibility is that
they biotransform As to less toxic forms or reduce the toxic As
accumulation, which may be responsible for the higher
bioaccumulation in seabass than that in rabbitfish. Cockell47
reported that with continued exposure to dietborne As, epithelial
cells in the hepatobiliary system must undergo an adaptation in
order to allow them to regenerate. Such adaptation may occur by
the increase of metabolic transformation of As to a less toxic
form, or the reduction of net accumulation by decreasing uptake
or increasing excretion of As. Until now, limited data have been
available for the comparison of bioaccumulation with some
information on biotransformation. Therefore, it would be
interesting to use radiotracer studies to quantify the relationship
between As bioaccumulation and As speciation in a future study.
This study examined the trophic transfer and bioavailability of
As in two typical marine fish, herbivorous rabbitfish and
carnivorous seabass feeding on different prey types with different
proportions of inorganic As and organic As compounds.
We demonstrated that different diets had significant effects on
As bioavailability and bioaccumulation in marine fish. The
bioavailability of AsB was higher than that of inorganic As.
Inorganic As in both fish was difficult to be transmitted along the
food chain, due to their biotransformation in the fish tissue rather
than direct accumulation. While AsB was more assimilated than
inorganic As, possibly because AsB passed more easily through
the apical membranes of the cells of the digestive organs, and was
the final storage form of As in the fish tissues. Therefore,
differential bioavailability of inorganic and organic As contributed to their different bioaccumulation in marine fish.
■
ASSOCIATED CONTENT
S Supporting Information
*
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.est.5b06307.
The AsB distribution (%) in exposed diets and different
tissues of rabbitfish and seabass after different exposed
treatments for 28 d, the correlation between newly
accumulated As concentrations and the ratio of organic
As/inorganic As in seabass, total As, As species
concentrations and distribution (%) in unspiked food,
As species concentrations in intestine, liver, and muscle
tissues of marine rabbitfish and seabass (PDF)
■
AUTHOR INFORMATION
Corresponding Author
*Tel: +86-20-89221322; fax: +86-20-84452611; e-mail: zhangli@
scsio.ac.cn (L.Z.).
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS
This work was supported by National Natural Science
Foundation of China (21407156, 41376161), The State Key
Development Program for Basic Research of China
(2015CB452904), the 100 Talents Project of Chinese Academy
of Sciences, Science and Technology Planning Project of
Guangdong Province, China (2014B030301064).
■
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