The degradation of arsenoribosides from Ecklonia radiata tissues decomposed in natural and microbially manipulated microcosms
Elliott G. Duncan A C D , William A. Maher A , Simon D. Foster A , Frank Krikowa A and Katarina M. Mikac B
+ Author Affiliations
- Author Affiliations
A Ecochemistry Laboratory, Institute for Applied Ecology, University of Canberra, University Drive, Bruce, ACT 2601, Australia.
B Institute for Conservation Biology and Environmental Management, University of Wollongong, Northfields Avenue, Wollongong, NSW 2522, Australia.
C Present address, CSIRO Plant Industry, Centre for Environment and Life Sciences, Underwood Avenue, Floreat, WA 6014, Australia.
D Corresponding author. Email: elliott.duncan@csiro.au.
Environmental Chemistry 11(3) 289-300 https://doi.org/10.1071/EN13155
Submitted: 19 August 2013 Accepted: 30 January 2014 Published: 5 June 2014
Environmental context. Arsenoribosides are the major arsenic species in marine macro-algae, yet inorganic arsenic is the major arsenic species found in seawater. We investigated the degradation of arsenoribosides associated with Ecklonia radiata by the use of microcosms containing both natural and autoclaved seawater and sand. The decomposition and persistence of arsenic species was linked to the use of autoclaved seawater and sand, which suggests that arsenoriboside degradation is governed by the microbial composition of microenvironments within marine systems.
Abstract. We investigated the influence of microbial communities on the degradation of arsenoribosides from E. radiata tissues decomposing in sand and seawater-based microcosms. During the first 30 days, arsenic was released from decomposing E. radiata tissues into seawater and sand porewaters in all microcosms. In microcosms containing autoclaved seawater and autoclaved sand, arsenic was shown to persist in soluble forms at concentrations (9–18 µg per microcosm) far higher than those present initially (~3 µg per microcosm). Arsenoribosides were lost from decomposing E. radiata tissues in all microcosms with previously established arsenoriboside degradation products, such as thio-arsenic species, dimethylarsinoylethanol (DMAE), dimethylarsenate (DMA) and arsenate (AsV) observed in all microcosms. DMAE and DMA persisted in the seawater and sand porewaters of microcosms containing autoclaved seawater and autoclaved sand. This suggests that the degradation step from arsenoribosides → DMAE occurs on algal surfaces, whereas the step from DMAE → AsV occurs predominantly in the water-column or sand–sediments. This study also demonstrates that disruptions to microbial connectivity (defined as the ability of microbes to recolonise vacant habitats) result in alterations to arsenic cycling. Thus, the re-cycling of arsenoribosides released from marine macro-algae is driven by microbial complexity plus microbial connectivity rather than species diversity as such, as previously assumed.
Additional keywords: algal decomposition, arsenic cycling, macro-algae, microbial ecology.
References
[1] R. Tukai, W. A. Maher, I. J. McNaught, M. J. Ellwood, M. Coleman, Occurrence and chemical form of arsenic in marine macroalgae from the east coast of Australia Mar. Freshwater Res. 2002, 53, 971.| Occurrence and chemical form of arsenic in marine macroalgae from the east coast of AustraliaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlvFamtQ%3D%3D&md5=866ec2a2f8543328ffbb93c5a51817abCAS |
[2] S. Foster, W. Maher, F. Krikowa, Changes in proportions of arsenic species within an Ecklonia radiata food chain Environ. Chem. 2008, 5, 176.
| Changes in proportions of arsenic species within an Ecklonia radiata food chainCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntlCrtrk%3D&md5=936d1ee95a95bd5eaada1dd341560636CAS |
[3] D. Thomson, W. Maher, S. Foster, Arsenic and selected elements in inter-tidal and estuarine marine algae, south-east coast, NSW, Australia Appl. Organomet. Chem. 2007, 21, 396.
| Arsenic and selected elements in inter-tidal and estuarine marine algae, south-east coast, NSW, AustraliaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1yit7s%3D&md5=71e7b70107e310574ae0c95fa0523870CAS |
[4] M. Morita, Y. Shibata, Chemical form of arsenic in marine macroalgae Appl. Organomet. Chem. 1990, 4, 181.
| Chemical form of arsenic in marine macroalgaeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmvVGlsQ%3D%3D&md5=8062f1af6d48f5cfd6e7fce5ab2ef375CAS |
[5] J. S. Edmonds, K. A. Francesconi, Arseno-sugars from brown kelp (Ecklonia radiata) as intermediates in cycling of arsenic in a marine ecosystem Nature 1981, 289, 602.
| Arseno-sugars from brown kelp (Ecklonia radiata) as intermediates in cycling of arsenic in a marine ecosystemCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVegt70%3D&md5=122ccd5d6fc3349be3a12ee5a677126eCAS |
[6] S. Foster, W. Maher, Degradation of arsenoribosides from marine macroalgae in simulated rock pools, in Arsenic in geosphere and human diseases (Eds J. S. Jean, J. Bundschuh, P. Battacharya) 2010, pp. 230–232 (CRC Press: London).
[7] P. Pengprecha, M. Wilson, A. Raab, J. Feldmann, Biodegradation of arsenosugars in marine sediment Appl. Organomet. Chem. 2005, 19, 819.
| Biodegradation of arsenosugars in marine sedimentCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFKku70%3D&md5=d7ba23d5387d718b1cc5410e11df7589CAS |
[8] J. Navratilova, G. Raber, S. J. Fisher, K. A. Francesconi, Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenic Environ. Chem. 2011, 8, 44.
| Arsenic cycling in marine systems: degradation of arsenosugars to arsenate in decomposing algae, and preliminary evidence for the formation of recalcitrant arsenicCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1GlsLc%3D&md5=fc9c0433f676675f071cfc450fa09bebCAS |
[9] J. S. Edmonds, K. A. Francesconi, J. A. Hansen, Dimethyloxarsylethanol from anaerobic decomposition of brown kelp (Ecklonia radiata): a likely precursor of arsenobetaine in marine fauna Experientia 1982, 38, 643.
| Dimethyloxarsylethanol from anaerobic decomposition of brown kelp (Ecklonia radiata): a likely precursor of arsenobetaine in marine faunaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xks12js7s%3D&md5=808a98cceec15594630522cc0516f90cCAS |
[10] K. A. Smart, H. L. Smart, C. R. Jackson, The effects of fine scale environmental variation on microbial community structure and functioning in aquatic environments, in Environmental Microbiology Research Trends (Ed. G. V. Kurladze) 2008, pp. 167–190 (Nova Science Publishers: New York).
[11] J. C. Sanderson, Subtidal macroalgal assemblages in temperate Australian coastal waters, Australia. State of the Environment Technical Paper Series (Estuaries and the Sea) 1997 (Department of the Environment: Canberra).
[12] S. Foster, D. Thomson, W. Maher, Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutum Mar. Chem. 2008, 108, 172.
| Uptake and metabolism of arsenate by anexic cultures of the microalgae Dunaliella tertiolecta and Phaeodactylum tricornutumCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVyrtQ%3D%3D&md5=07a9f29543ef9407437f7acc20dd2f39CAS |
[13] J. Cannon, J. Edmonds, K. Francesconi, C. Raston, J. Saunders, B. Skelton, A. H. White, Isolation, crystal structure and synthesis of arsenobetaine, a constituent of the western rock lobster, the dusky shark, and some samples of human urine Aust. J. Chem. 1981, 34, 787.
| Isolation, crystal structure and synthesis of arsenobetaine, a constituent of the western rock lobster, the dusky shark, and some samples of human urineCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltFemt7k%3D&md5=5a0a0e96ea021adf42d99c0cda9d0cdaCAS |
[14] R. Minhas, D. S. Forsyth, B. Dawson, Synthesis and characterization of arsenobetaine and arsenocholine derivatives Appl. Organomet. Chem. 1998, 12, 635.
| Synthesis and characterization of arsenobetaine and arsenocholine derivativesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFOnu78%3D&md5=d9dfdc7ffcef58c23a3e98c2ab1aea84CAS |
[15] A. Merijanian, R. A. Zingaro, Arsine oxides Inorg. Chem. 1966, 5, 187.
| Arsine oxidesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28Xktl2lsQ%3D%3D&md5=9be729a3a996a5a5ab269dcee8b1463aCAS |
[16] G. M. Momplaisir, J. S. Blais, M. Quinteiro, W. D. Marshall, Determination of arsenobetaine, arsenocholine, and tetramethylarsonium cations in seafoods and human urine by high-performance liquid chromatography-thermochemical hydride generation-atomic absorption spectrometry J. Agric. Food Chem. 1991, 39, 1448.
| Determination of arsenobetaine, arsenocholine, and tetramethylarsonium cations in seafoods and human urine by high-performance liquid chromatography-thermochemical hydride generation-atomic absorption spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkvFSktLw%3D&md5=e52d95e82825e907b6dbe456d4a0d2b2CAS |
[17] K. A. Francesconi, J. S. Edmonds, R. V. Stick, Accumulation of arsenic in yelloweye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenate Sci. Total Environ. 1989, 79, 59.
| Accumulation of arsenic in yelloweye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenateCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhsV2gs70%3D&md5=8d0cc99948a98490c4dde343a8e5119cCAS | 2928771PubMed |
[18] A. D. Madsen, W. Goessler, S. N. Pedersen, K. A. Francesconi, Characterization of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studies J. Anal. At. Spectrom. 2000, 15, 657.
| Characterization of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studiesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjslWksLY%3D&md5=a08a15985d64a6286e04d5dac6926e72CAS |
[19] R. Raml, W. Goessler, K. A. Francesconi, Improved chromatographic separation of thio-arsenic compounds by reversed-phase high performance liquid chromatography-inductively coupled plasma mass spectrometry J. Chromatogr. A 2006, 1128, 164.
| Improved chromatographic separation of thio-arsenic compounds by reversed-phase high performance liquid chromatography-inductively coupled plasma mass spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFSrsr0%3D&md5=9b841870c0ada40257efbcef5505b96eCAS | 16854422PubMed |
[20] S. Baldwin, M. Deaker, W. Maher, Low volume microwave digestion of marine biological tissues for the measurement of trace elements Analyst 1994, 119, 1701.
| Low volume microwave digestion of marine biological tissues for the measurement of trace elementsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmtVSgtLo%3D&md5=8d057aac52e04fda24593f1e2042dfb4CAS | 7978323PubMed |
[21] W. Maher, F. Krikowa, J. Kirby, A. Townsend, P. Snitch, Measurement of trace elements in marine environmental samples using solution ICPMS. Current and future applications Aust. J. Chem. 2003, 56, 103.
| Measurement of trace elements in marine environmental samples using solution ICPMS. Current and future applicationsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjslGnsLk%3D&md5=4971859f9f7b98405da7912cfe99a329CAS |
[22] W. Maher, S. Foster, F. Krikowa, P. Snitch, G. Chapple, P. Craig, Measurement of trace metals and phosphorus in marine animal and plant tissues by low volume microwave digestion and ICPMS J. Anal. At. Spectrom. 2001, 22, 361.
| 1:CAS:528:DC%2BD3MXovVOisbs%3D&md5=f55b9a4f1c125a0e56b834e63d8c7fa7CAS |
[23] J. Kirby, W. Maher, Measurement of water-soluble arsenic species in freeze-dried marine animal tissues by microwave-assisted extraction and HPLC-ICP-MS J. Anal. At. Spectrom. 2002, 17, 838.
| Measurement of water-soluble arsenic species in freeze-dried marine animal tissues by microwave-assisted extraction and HPLC-ICP-MSCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVKhsbs%3D&md5=b8dd1f69b3893d516db496d1cbbf4674CAS |
[24] M. J. Ellwood, W. A. Maher, Measurement of arsenic species in marine sediments by high-performance liquid chromatography–inductively coupled plasma mass spectrometry Anal. Chim. Acta 2003, 477, 279.
| Measurement of arsenic species in marine sediments by high-performance liquid chromatography–inductively coupled plasma mass spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpvVWku78%3D&md5=d96cb3acbd708ebaa6499fbfe805e5deCAS |
[25] S. Foster, W. Maher, F. Krikowa, S. Apte, A microwave assisted sequential extraction of water and dilute acid soluble arsenic species from marine plant and animal tissues Talanta 2007, 71, 537.
| A microwave assisted sequential extraction of water and dilute acid soluble arsenic species from marine plant and animal tissuesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotFSltA%3D%3D&md5=a1020889f64757b5876b3cabc25648c2CAS | 19071338PubMed |
[26] J. Kirby, W. Maher, M. Ellwood, F. Krikowa, Arsenic species determination in biological tissues by HPLC-ICP-MS and HPLC-HG-ICP-MS Aust. J. Chem. 2004, 57, 957.
| Arsenic species determination in biological tissues by HPLC-ICP-MS and HPLC-HG-ICP-MSCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXps1SjsrY%3D&md5=b727b765c05fd4fb02e7669ceea283d7CAS |
[27] W. A. Maher, S. Foster, F. Krikowa, E. Duncan, A. St John, K. Hug, J. W. Moreau, Thio arsenic species measurements in marine organisms and geothermal waters Microchem. J. 2013, 111, 82.
| Thio arsenic species measurements in marine organisms and geothermal watersCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivFylt7k%3D&md5=9743dba6fef1b29b3536642be768ff87CAS |
[28] S. Foster, W. Maher, E. Schmeisser, A. Taylor, F. Krikowa, S. Apte, Arsenic speciation in a rocky intertidal marine food chain in NSW, Australia, revisited Environ. Chem. 2006, 3, 304.
| Arsenic speciation in a rocky intertidal marine food chain in NSW, Australia, revisitedCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVaksr4%3D&md5=e0cf36f25f038b024d2f7718ca43d945CAS |
[29] E. Duncan, S. Foster, W. Maher, Uptake and metabolism of arsenate, methylarsonate and arsenobetaine by axenic cultures of the phytoplankton Dunaliella tertiolecta Bot. Mar. 2010, 53, 377.
| Uptake and metabolism of arsenate, methylarsonate and arsenobetaine by axenic cultures of the phytoplankton Dunaliella tertiolectaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKis7bI&md5=1129c410a05c925e04fe9ad65daf7197CAS |
[30] E. G. Duncan, W. A. Maher, S. D. Foster, F. Krikowa, Influence of culture regime on arsenic cycling by the marine phytoplankton Dunaliella tertiolecta and Thalassiosira pseudonana Environ. Chem. 2013, 10, 91.
| Influence of culture regime on arsenic cycling by the marine phytoplankton Dunaliella tertiolecta and Thalassiosira pseudonanaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosVCkt7Y%3D&md5=1f9df0b815e62c3a075893cfbec69da3CAS |
[31] K. J. Reimer, The methylation of arsenic in marine sediments Appl. Organomet. Chem. 1989, 3, 475.
| The methylation of arsenic in marine sedimentsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhsVGitro%3D&md5=8a2e4c3c5940111861f6699ccb175f24CAS |
[32] D. Páez-Espino, J. Tamames, V. de Lorenzo, D. Canovas, Microbial responses to environmental arsenic Biometals 2009, 22, 117.
| Microbial responses to environmental arsenicCrossref | GoogleScholarGoogle Scholar | 19130261PubMed |
[33] R. Bentley, T. G. Chasteen, Microbial methylation of metalloids: arsenic, antimony, and bismuth Microbiol. Mol. Biol. Rev. 2002, 66, 250.
| Microbial methylation of metalloids: arsenic, antimony, and bismuthCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFSltrs%3D&md5=48186e246fd2c12054bdda68c760d523CAS | 12040126PubMed |
[34] F. Azam, T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil, F. Thingstad, The ecological role of water-column microbes in the sea Mar. Ecol. Prog. Ser. 1983, 10, 257.
| The ecological role of water-column microbes in the seaCrossref | GoogleScholarGoogle Scholar |
[35] S. Kjelleberg, M. Hermansson, P. Marden, The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environment Annu. Rev. Microbiol. 1987, 41, 25.
| The transient phase between growth and nongrowth of heterotrophic bacteria, with emphasis on the marine environmentCrossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1c%2FnsFynsQ%3D%3D&md5=dd80d636a03db1d065bcf0ba51b06bbdCAS | 3318670PubMed |
[36] E. F. Delong, D. G. Franks, A. L. Alldredge, Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblages Limnol. Oceanogr. 1993, 38, 924.
| Phylogenetic diversity of aggregate-attached vs. free-living marine bacterial assemblagesCrossref | GoogleScholarGoogle Scholar |
[37] L. Gram, J. Melchiorsen, J. B. Bruhn, Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organisms Mar. Biotechnol. (NY) 2010, 12, 439.
| Antibacterial activity of marine culturable bacteria collected from a global sampling of ocean surface waters and surface swabs of marine organismsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1OjsLk%3D&md5=0b8d954b6f359b0cb265e85d19173be8CAS | 19823914PubMed |
[38] K. G. Boyd, D. R. Adams, J. G. Burgess, Antibacterial and repellent activities of marine bacteria associated with algal surfaces Biofouling 1999, 14, 227.
| Antibacterial and repellent activities of marine bacteria associated with algal surfacesCrossref | GoogleScholarGoogle Scholar |
[39] H. Kirkman, G. Kendrick, Ecological significance and commercial harvesting of drifting and beach-cast macro-algae and seagrasses in Australia: a review J. Appl. Phycol. 1997, 9, 311.
| Ecological significance and commercial harvesting of drifting and beach-cast macro-algae and seagrasses in Australia: a reviewCrossref | GoogleScholarGoogle Scholar |
[40] E. Armstrong, L. Yan, K. G. Boyd, P. C. Wright, J. G. Burgess, The symbiotic role of marine microbes on living surfaces Hydrobiologia 2001, 461, 37.
| The symbiotic role of marine microbes on living surfacesCrossref | GoogleScholarGoogle Scholar |
[41] M. Rieper-Kirchner, Microbial degradation of North Sea macroalgae: field and laboratory studies Bot. Mar. 1989, 32, 241.
| Microbial degradation of North Sea macroalgae: field and laboratory studiesCrossref | GoogleScholarGoogle Scholar |
[42] G. C. Pellikaan, Laboratory experiments on eelgrass (Zostera marina L.) decomposition Neth. J. Sea Res. 1984, 18, 360.
| Laboratory experiments on eelgrass (Zostera marina L.) decompositionCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXlslGmsb8%3D&md5=30a7f48d1a4f4053fc3dd1e4961cabaeCAS |
[43] J. M. Hill, C. D. McQuaid, Variability in the fractionation of stable isotopes during degradation of two intertidal red algae Estuar. Coast. Shelf Sci. 2009, 82, 397.
| Variability in the fractionation of stable isotopes during degradation of two intertidal red algaeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjvVWhs7w%3D&md5=71c3fdc726d511ae3c819e395ff9e76eCAS |
[44] H. Higgins, D. Mackey, Role of Ecklonia radiata (C.Ag.) J.Agardh in determining trace metal availability in coastal waters. II. Trace metal speciation Mar. Freshwater Res. 1987, 38, 317.
| Role of Ecklonia radiata (C.Ag.) J.Agardh in determining trace metal availability in coastal waters. II. Trace metal speciationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXlvVaqu7o%3D&md5=8e1f186eb05ba89a0a92772e8de3ca78CAS |
[45] H. Urakawa, K. Kita-Tsukamoto, K. Ohwada, Microbial diversity in marine sediments from Sagami Bay and Tokyo Bay, Japan, as determined by 16S rRNA gene analysis Microbiology 1999, 145, 3305.
| 1:CAS:528:DyaK1MXnsVGns7s%3D&md5=d00f5f535c72d275743f6c4d61f3c517CAS | 10589740PubMed |
[46] N. Velmurugan, D. Kalpana, J.-Y. Cho, G.-H. Lee, S.-H. Park, Y.-S. Lee, Phylogenetic analysis of culturable marine bacteria in sediments from South Korean Yellow Sea Microbiology 2011, 80, 261.
| Phylogenetic analysis of culturable marine bacteria in sediments from South Korean Yellow SeaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVyisL8%3D&md5=74df16b76cf28320148d92ecef633dd0CAS |
[47] S. A. Gerlach, Food-chain relationships in subtidal silty sand marine sediments and the role of meiofauna in stimulating bacterial productivity Oecologia 1978, 33, 55.
| Food-chain relationships in subtidal silty sand marine sediments and the role of meiofauna in stimulating bacterial productivityCrossref | GoogleScholarGoogle Scholar |
[48] A. Bellgrove, M. N. Clayton, G. P. Quinn, An integrated study of the temporal and spatial variation in the supply of propagules, recruitment and assemblages of intertidal macroalgae on a wave-exposed rocky coast, Victoria, Australia J. Exp. Mar. Biol. Ecol. 2004, 310, 207.
| An integrated study of the temporal and spatial variation in the supply of propagules, recruitment and assemblages of intertidal macroalgae on a wave-exposed rocky coast, Victoria, AustraliaCrossref | GoogleScholarGoogle Scholar |
[49] M. O. Andreae, Distribution and speciation of arsenic in natural waters and some marine algae Deep-Sea Res. 1978, 25, 391.
| Distribution and speciation of arsenic in natural waters and some marine algaeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXks1Cqsb4%3D&md5=1d4f356c4b1a7717e90f56e4886440fcCAS |
[50] G. E. Millward, L. Ebdon, A. P. Walton, Seasonality in estuarine sources of methylated arsenic Appl. Organomet. Chem. 1993, 7, 499.
| Seasonality in estuarine sources of methylated arsenicCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXosF2ntw%3D%3D&md5=6354f4520cca53096fc897cbe40dd3d7CAS |
[51] G. E. Millward, H. J. Kitts, S. D. W. Comber, L. Ebdon, A. G. Howard, Methylated arsenic in the southern North Sea Estuar. Coast. Shelf Sci. 1996, 43, 1.
| Methylated arsenic in the southern North SeaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFeqtLY%3D&md5=498c6f2764a1b98c08242e20abf441b4CAS |
