Comparison of Bioavailability and ... - ACS Publications

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 (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 2417

DOI: 10.1021/acs.est.5b06307 Environ. Sci. Technol. 2016, 50, 2413−2423

Article

Environmental Science & Technology

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 2418


Article


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


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


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 2419


Article


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


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


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. 2420


Article

Environmental Science & Technology 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).

■

REFERENCES

(1) Sohel, N.; Persson, L. A.; Rahman, M.; Streatfield, P. K.; Yunus, M.; Ekstrom, E. C.; Vahter, M. Arsenic in drinking water and adult mortality: a population-based cohort study in rural Bangladesh. Epidemiology 2009, 20 (6), 824−830. (2) Li, G.; Sun, G. X.; Williams, P. N.; Nunes, L.; Zhu, Y. G. Inorganic arsenic in Chinese food and its cancer risk. Environ. Int. 2011, 37 (7), 1219−1225. (3) Craig, P. J. Organometallic Compounds in the Environment; John Wiley and Sons: New York, 2003. (4) Ciardullo, S.; Aureli, F.; Raggi, A.; Cubadda, F. Arsenic speciation in freshwater fish: Focus on extraction and mass balance. Talanta 2010, 81 (1−2), 213−221. (5) Schaeffer, R.; Francesconi, K. A.; Kienzl, N.; Soeroes, C.; Fodor, P.; Varadi, L.; Raml, R.; Goessler, W.; Kuehnelt, D. Arsenic speciation in freshwater organisms from the river Danube in Hungary. Talanta 2006, 69 (4), 856−865.

2421


Article


polychaetes Nereis diversicolor and Nereis virens. Environ. Sci. Technol. 2002, 36 (13), 2905−2910. (26) Casado-Martinez, M. C.; Duncan, E.; Smith, B. D.; Maher, W. A.; Rainbow, P. S. Arsenic toxicity in a sediment-dwelling polychaete: detoxification and arsenic metabolism. Ecotoxicology 2012, 21 (2), 576− 590. (27) Vilano, M.; Rubio, R. Determination of arsenic species in oyster tissue by microwave-assisted extraction and liquid chromatographyatomic fluorescence detection. Appl. Organomet. Chem. 2001, 15 (8), 658−666. (28) Zhang, W.; Wang, W. X.; Zhang, L. Arsenic speciation and spatial and interspecies differences of metal concentrations in mollusks and crustaceans from a South China estuary. Ecotoxicology 2013, 22 (4), 671−682. (29) Berges-Tiznado, M. E.; Paez-Osuna, F.; Notti, A.; Regoli, F. Arsenic and arsenic species in cultured oyster (Crassostrea gigas and C. corteziensis) from coastal lagoons of the SE Gulf of California, Mexico. Biol. Trace Elem. Res. 2013, 151 (1), 43−49. (30) Unlu, M. Y. Chemical transformation and flux of different forms of arsenic in the crab. Chemosphere 1979, 8 (5), 269−275. (31) Edmonds, J. S.; Shibata, Y.; Francesconi, K. A.; Rippingale, R. J.; Morita, M. Arsenic transformations in short marine food chains studied by HPLC-ICP MS. Appl. Organomet. Chem. 1997, 11 (4), 281−287. (32) Zhang, W.; Guo, Z. Q.; Zhou, Y. Y.; Liu, H. X.; Zhang, L. Biotransformation and detoxification of inorganic arsenic in Bombay oyster Saccostrea cucullata. Aquat. Toxicol. 2015, 158, 33−40. (33) Kirby, J.; Maher, W. Tissue accumulation and distribution of arsenic compounds in three marine fish species: relationship to trophic position. Appl. Organomet. Chem. 2002, 16 (2), 108−115. (34) Price, A.; Maher, W.; Kirby, J.; Krikowa, F.; Duncan, E.; Taylor, A.; Potts, J. Distribution of arsenic species in an open seagrass ecosystem: relationship to trophic groups, habitats and feeding zones. Environ. Chem. 2012, 9 (1), 77−88. (35) Hansen, J. A.; Lipton, J.; Welsh, P. G.; Cacela, D.; MacConnell, B. Reduced growth of rainbow trout (Oncorhynchus mykiss) fed a live invertebrate diet pre-exposed to metal-contaminated sediments. Environ. Toxicol. Chem. 2004, 23 (8), 1902−1911. (36) Guo, F.; Yao, J.; Wang, W. X. Bioavailability of purified subcellular metals to a marine fish. Environ. Toxicol. Chem. 2013, 32 (9), 2109− 2116. (37) Whaley-Martin, K. J.; Koch, I.; Moriarty, M.; Reimer, K. J. Arsenic speciation in blue mussels (Mytilus edulis) along a highly contaminated arsenic gradient. Environ. Sci. Technol. 2012, 46 (6), 3110−3118. (38) Radabaugh, T. R.; Aposhian, H. V. Enzymatic reduction of arsenic compounds in mammalian systems: reduction of arsenate to arsenite by human liver arsenate reductase. Chem. Res. Toxicol. 2000, 13 (1), 26−30. (39) Radabaugh, T. R.; Sampayo-Reyes, A.; Zakharyan, R. A.; Aposhian, H. V. Arsenate reductase II. Purine nucleoside phosphorylase in the presence of dihydrolipoic acid is a route for reduction of arsenate to arsenite in mammalian systems. Chem. Res. Toxicol. 2002, 15 (5), 692−698. (40) Francesconi, K. A.; Edmonds, J. S.; Stick, R. V. Accumulation of arsenic in yelloweye mullet (Aldrichetta Forsteri) following oral administration of organoarsenic compounds and arsenate. Sci. Total Environ. 1989, 79 (1), 59−67. (41) Barwick, M.; Maher, W. Biotransference and biomagnification of selenium copper, cadmium, zinc, arsenic and lead in a temperate seagrass ecosystem from Lake Macquarie Estuary, NSW, Australia. Mar. Environ. Res. 2003, 56 (4), 471−502. (42) Liu, C. W.; Lin, K. H.; Jang, C. S. Tissue accumulation of arsenic compounds in aquacultural and wild mullet (Mugil cephalus). Bull. Environ. Contam. Toxicol. 2006, 77 (1), 36−42. (43) Foster, S.; Maher, W.; Schmeisser, E.; Taylor, A.; Krikowa, F.; Apte, S. Arsenic species in a rocky intertidal marine food chain in NSW, Australia, revisited. Environ. Chem. 2006, 3 (4), 304−315. (44) Hong, S.; Khim, J. S.; Park, J.; Son, H. S.; Choi, S. D.; Choi, K.; Ryu, J.; Kim, C. Y.; Chang, G. S.; Giesy, J. P. Species- and tissue-specific bioaccumulation of arsenicals in various aquatic organisms from a highly

(6) Amlund, H.; Berntssen, M. H. G. Arsenobetaine in Atlantic salmon (Salmo salar L.): influence of seawater adaptation. Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol. 2004, 138 (4), 507−514. (7) Zhang, W.; Wang, W. X. Large-scale spatial and interspecies differences in trace elements and stable isotopes in marine wild fish from Chinese waters. J. Hazard. Mater. 2012, 215, 65−74. (8) Phillips, D. J. H. Arsenic in aquatic organisms: a review, emphasizing chemical speciation. Aquat. Toxicol. 1990, 16 (3), 151− 186. (9) Castro-Gonzalez, M. I.; Mendez-Armenta, M. Heavy metals: Implications associated to fish consumption. Environ. Toxicol. Pharmacol. 2008, 26 (3), 263−271. (10) Maher, W.; Butler, E. Arsenic in the marine environment. Appl. Organomet. Chem. 1988, 2, 191−214. (11) Price, R. E.; Pichler, T. Distribution, speciation and bioavailability of arsenic in a shallow-water submarine hydrothermal system, Tutum Bay, Ambitle Island, PNG. Chem. Geol. 2005, 224 (1−3), 122−135. (12) Casado-Martinez, M. C.; Smith, B. D.; Luoma, S. N.; Rainbow, P. S. Bioaccumulation of arsenic from water and sediment by a depositfeeding polychaete (Arenicola marina): A biodynamic modelling approach. Aquat. Toxicol. 2010, 98 (1), 34−43. (13) Agusa, T.; Takagi, K.; Kubota, R.; Anan, Y.; Iwata, H.; Tanabe, S. Specific accumulation of arsenic compounds in green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) from Ishigaki Island, Japan. Environ. Pollut. 2008, 153 (1), 127−136. (14) Maher, W. A.; Foster, S. D.; Taylor, A. M.; Krikowa, F.; Duncan, E. G.; Chariton, A. A. Arsenic distribution and species in two Zostera capricorni seagrass ecosystems, New South Wales, Australia. Environ. Chem. 2011, 8 (1), 9−18. (15) Kuroiwa, T.; Ohki, A.; Naka, K.; Maeda, S. Biomethylation and biotransformation of arsenic in a freshwater food chain: Green alga (Chlorella vulgaris)→Shrimp (Neocaridina denticulata)→killifish (Oryzias latipes). Appl. Organomet. Chem. 1994, 8 (4), 325−333. (16) Bryan, G. W.; Langston, W. J. Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ. Pollut. 1992, 76 (2), 89−131. (17) Laparra, J. M.; Velez, D.; Barbera, R.; Farre, R.; Montoro, R. Bioavailability of inorganic arsenic in cooked rice: Practical aspects for human health risk assessments. J. Agric. Food Chem. 2005, 53 (22), 8829−8833. (18) Zhang, W.; Huang, L. M.; Wang, W. X. Arsenic bioaccumulation in a marine juvenile fish Terapon jarbua. Aquat. Toxicol. 2011, 105 (3− 4), 582−588. (19) Mamindy-Pajany, Y.; Hurel, C.; Geret, F.; Galgani, F.; BattagliaBrunet, F.; Marmier, N.; Romeo, M. Arsenic in marine sediments from French Mediterranean ports: geochemical partitioning, bioavailability and ecotoxicology. Chemosphere 2013, 90 (11), 2730−2736. (20) Kirby, J.; Maher, W.; Spooner, D. Arsenic occurrence and species in near-shore macroalgae-feeding marine animals. Environ. Sci. Technol. 2005, 39 (16), 5999−6005. (21) Koch, I.; McPherson, K.; Smith, P.; Easton, L.; Doe, K. G.; Reimer, K. J. Arsenic bioaccessibility and speciation in clams and seaweed from a contaminated marine environment. Mar. Pollut. Bull. 2007, 54 (5), 586−594. (22) Pell, A.; Kokkinis, G.; Malea, P.; Pergantis, S. A.; Rubio, R.; LopezSanchez, J. F. LC-ICP-MS analysis of arsenic compounds in dominant seaweeds from the Thermaikos Gulf (Northern Aegean Sea, Greece). Chemosphere 2013, 93 (9), 2187−2194. (23) Tukai, R.; Maher, W. A.; McNaught, I. J.; Ellwood, M. J. Measurement of arsenic species in marine macroalgae by microwaveassisted extraction and high performance liquid chromatographyinductively coupled plasma mass spectrometry. Anal. Chim. Acta 2002, 457 (2), 173−185. (24) Tukai, R.; Maher, W. A.; McNaught, I. J.; Ellwood, M. J.; Coleman, M. Occurrence and chemical form of arsenic in marine macroalgae from the east coast of Australia. Mar. Freshwater Res. 2002, 53 (6), 971−980. (25) Geiszinger, A. E.; Goessler, W.; Francesconi, K. A. Biotransformation of arsenate to the tetramethylarsonium ion in the marine 2422


Article

Environmental Science & Technology industrialized area in the Pohang City, Korea. Environ. Pollut. 2014, 192, 27−35. (45) Amlund, H.; Francesconi, K. A.; Bethune, C.; Lundebye, A. K.; Berntssen, M. H. G. Accumulation and elimination of dietary arsenobetaine in two species of fish, Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Environ. Toxicol. Chem. 2006, 25 (7), 1787−1794. (46) Jabeen, G.; Javed, M. Evaluation of arsenic toxicity to biota in river Ravi (Pakistan) aquatic ecosystem. Int. J. Agric. Biol. 2011, 13 (6), 929− 934. (47) Cockell, K. A. Chronic toxicity of dietborne arsenic to rainbow trout, Oncorhynchus mykiss. Ph.D., University of Guelph: Guelph, Ontario, 1990.

2423
