Ecological factors affecting the accumulation and speciation of arsenic in twelve Australian coastal bivalve molluscs
William Maher A C , Joel Waring A , Frank Krikowa A , Elliott Duncan A B and Simon Foster A
+ Author Affiliations
- Author Affiliations
A Ecochemistry Laboratory, Institute for Applied Ecology, University of Canberra, Bruce, ACT 2601, Australia.
B Present address: Environmental Contaminants Group, Future Industries Institute, University of South Australia, Mawson Lakes, SA 5095, Australia.
C Corresponding author. Email: bill.maher@canberra.edu.au
Environmental Chemistry 15(2) 46-57 https://doi.org/10.1071/EN17106
Submitted: 7 June 2017 Accepted: 30 October 2017 Published: 9 May 2018
Environmental context. Knowledge of the pathways by which arsenic is accumulated and transferred in marine ecosystems is scarce. Molluscs are important keystone organisms providing a link between primary producers (micro and macroalgae) and higher trophic levels such as fish. The present study examines the accumulation and species of arsenic in common bivalve molluscs from south-east Australia to understand the cycling of arsenic in marine food webs.
Abstract. The present paper reports the whole-tissue total arsenic concentrations and water-soluble arsenic species in 12 common coastal Australian bivalve mollusc species. Mean arsenic concentrations ranged from 18 to 57 µg g−1 dry mass. Planktivores had significantly less arsenic (20–40 µg g−1; 22 ± 3 µg g−1) than did suspension and deposit feeders (36–57 µg g−1; 43 ± 7 µg g−1), with those associated with fine clay–silt sediments (49 ± 7 µg g−1) having significantly more arsenic than those associated with sand substrates (31 ± 11 µg g−1 ). Most planktivores and suspension feeders had similar arsenic species, with high proportions of arsenobetaine (AB) (64–92 %) and relatively low proportions of other arsenic species (0.55–15.8 %). Lower proportions of AB (13–57 %) and larger proportions of inorganic arsenic (6–7 %) were found in deposit feeders, reflecting increased exposure to inorganic arsenic in sediments. The study indicated that at lower trophic levels, organisms feed on algae and suspended matter containing a range of arsenic species including arsenosugars and AB. The implications for arsenic cycling are that as all bivalve molluscs accumulate AB and are a source of AB in benthic food webs. Because all bivalve molluscs also contained appreciable concentrations of arsenoriboses, precursors are present for the de novo synthesis of AB. As well, deposit feeders have higher proportions of inorganic arsenic that can be metabolised to different end products when ingested by higher trophic organisms
References
[1] A. J. Jones, The arsenic content of some of the marine algae Pharm. J. 1922, 109, 86.| 1:CAS:528:DyaB38Xit12mtg%3D%3D&md5=63b5f8ce96b6fdf86c1b9110b2223234CAS |
[2] G. Lunde, Water soluble arseno-organic compounds in marine fishes Nature 1969, 224, 186.
| Water soluble arseno-organic compounds in marine fishesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXhtVaqtw%3D%3D&md5=cd9c59718fa6807a87f1e7481693e2e6CAS |
[3] G. Lunde, Analysis of arsenic and bromine in marine and terrestrial oils J. Am. Oil Chem. Soc. 1972, 49, 44.
| Analysis of arsenic and bromine in marine and terrestrial oilsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XpvVWjtQ%3D%3D&md5=5c330dc07a7de616ec957061af765887CAS |
[4] J. S. Edmonds, K. A. Francesconi, J. R. Cannon, C. L. Raston, B. W. Skelton, A. H. White, Isolation, crystal structure and synthesis of arsenobetaine, the arsenical constituent of the western rock lobster Panulirus longipes cygnus George Tetrahedron Lett. 1977, 18, 1543.
| Isolation, crystal structure and synthesis of arsenobetaine, the arsenical constituent of the western rock lobster Panulirus longipes cygnus GeorgeCrossref | GoogleScholarGoogle Scholar |
[5] J. S. Edmonds, K. A. Francesconi, Arseno-sugars from brown kelp (Ecklonia radiata) as intermediates in cycling of arsenic in marine ecosystems Nature 1981, 289, 602.
| Arseno-sugars from brown kelp (Ecklonia radiata) as intermediates in cycling of arsenic in marine ecosystemsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVegt70%3D&md5=53157c4b5ef0d3778df5c682ffe1cbdfCAS |
[6] 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=db9d9b4e29fb82b6d07fa104eb487656CAS |
[7] V. Nischwitz, K. Kanaki, S. A. Pergantis, Mass spectrometric identification of novel arsinothioylsugars in marine bivalves and algae J. Anal. At. Spectrom. 2006, 21, 33.
| Mass spectrometric identification of novel arsinothioylsugars in marine bivalves and algaeCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCiurvM&md5=c8b9cfa7bc447e691c39d7021febb234CAS |
[8] K. J. Reimer, I. Koch, W. R. Cullen, Organoarsenicals. Distribution and transformation in the environment Metal Ions in Life Sciences 2010, 7, 165.
| Organoarsenicals. Distribution and transformation in the environmentCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvVehu7c%3D&md5=26202f1b0df991353ba11381179da542CAS |
[9] V. Sele, J. J. Sloth, A.-K. Lundebye, E. H. Larsen, M. H. G. Berntssen, H. Amlund, Arsenolipids in marine oils and fats: a review of occurrence, chemistry and future research needs Food Chem. 2012, 133, 618.
| Arsenolipids in marine oils and fats: a review of occurrence, chemistry and future research needsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivV2msb0%3D&md5=96982bd00e6350f516244609153e30dbCAS |
[10] E. G. Duncan, W. A. Maher, S. D. Foster, Contribution of arsenic species in unicellular algae to the cycling of arsenic in marine ecosystems Environ. Sci. Technol. 2015, 49, 33.
| Contribution of arsenic species in unicellular algae to the cycling of arsenic in marine ecosystemsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVSgsLfN&md5=64ffa1e7ba965bbabe198cd561989d75CAS |
[11] W. Maher, S. Foster, F. Krikowa, Arsenic species in Australian temperate marine food chains Mar. Freshwater Res. 2009, 60, 885.
| Arsenic species in Australian temperate marine food chainsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGhs77F&md5=0e5cfde5e9073201e97033c668cda73cCAS |
[12] B. Morton, M. B. Prezant, B. Wilson, Class Bivalvia, in Mollusca: The Southern Synthesis. Fauna of Australia (Eds P. L. Beesley, G. J. B. Ross, A. Wells) 1998, p. 563 (CSIRO Publishing: Melbourne, Vic., Australia).
[13] J. S. Edmonds, K. A. Francesconi, Organoarsenic compounds in the marine environment, in Organometallic Compounds in the Environment. (Ed. P. J. Craig) 2003, pp. 196–222 (John Wiley and Sons: New York).
[14] D. J. H. Phillips, Arsenic in aquatic organisms: a review, emphasizing chemical speciation Aquat. Toxicol. 1990, 16, 151.
| Arsenic in aquatic organisms: a review, emphasizing chemical speciationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXktF2jsrw%3D&md5=c6b62b1ba925f28e9c402bd0adbd8714CAS |
[15] S. Hirata, H. Toshimitsu, M. Aihara, Determination of arsenic species in marine samples by HPLC–ICP–MS Anal. Sci. 2006, 22, 39.
| Determination of arsenic species in marine samples by HPLC–ICP–MSCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVyisw%3D%3D&md5=335217e615fb533ddbbe5e2d1b537c9dCAS |
[16] W. A. Maher, S. D. Foster, A. M. Taylor, F. Krikowa, E. G. Duncan, A. A. Chariton, Arsenic distribution and species in two Zostera capricorni seagrass ecosystems, New South Wales, Australia Environ. Chem. 2011, 8, 9.
| Arsenic distribution and species in two Zostera capricorni seagrass ecosystems, New South Wales, AustraliaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs1GlsLg%3D&md5=5038d9317ec2c3e88da2494d14363bf5CAS |
[17] A. Price, W. Maher, J. Kirby, F. Krikowa, E. Duncan, A. Taylor, J. Potts, Distribution of arsenic species in an open seagrass ecosystem: relationship to trophic groups, habitats and feeding zones Environ. Chem. 2012, 9, 77.
| Distribution of arsenic species in an open seagrass ecosystem: relationship to trophic groups, habitats and feeding zonesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xis1amtb0%3D&md5=39dc4841edc4f729f92b8a616c9f2f4bCAS |
[18] Y. Shibata, M. Morita, Characterization of organic arsenic compounds in bivalves Appl. Organomet. Chem. 1992, 6, 343.
| Characterization of organic arsenic compounds in bivalvesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVynur4%3D&md5=7795aff1a3fafde9825934b811527b9eCAS |
[19] J. Waring, W. Maher, S. Foster, F. Krikowa, Occurrence and speciation of arsenic in common Australian coastal polychaete species Environ. Chem. 2005, 2, 108.
| Occurrence and speciation of arsenic in common Australian coastal polychaete speciesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvVChs70%3D&md5=3989f9b6d21218bce97c7ca9e293e9a7CAS |
[20] J. Waring, W. Maher, Arsenic bioaccumulation and species in marine polychaeta Appl. Organomet. Chem. 2005, 19, 917.
| Arsenic bioaccumulation and species in marine polychaetaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXntFCjur8%3D&md5=cdeb054ed4150eaacc026b57a017a24eCAS |
[21] H. Amlund, K. Ingebrigtsen, K. Hylland, A. Ruus, D. Ø. Eriksen, M. H. Berntssen, Disposition of arsenobetaine in two marine fish species following administration of a single oral dose of [14C] arsenobetaine Comp. Biochem. Physiol. Part C: Toxicol. Pharmacol. 2006, 143, 171.
[22] 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=3c0eed37af1655bd04bcff5e3706709aCAS |
[23] W. A. Maher, E. Duncan, G. Dilly, S. Foster, F. Krikowa, E. Lombi, K. Scheckel, P. Girguis, Arsenic concentrations and species in three hydrothermal vent worms, Ridgeia piscesae, Paralvinella sulficola and Paralvinella palmiformis Deep Sea Res. Part I Oceanogr. Res. Pap. 2016, 116, 41.
| Arsenic concentrations and species in three hydrothermal vent worms, Ridgeia piscesae, Paralvinella sulficola and Paralvinella palmiformisCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtlyjs77L&md5=5f960ee18ed585a16d713e2b71032438CAS |
[24] J. S. Waring, W. A. Maher, F. Krikowa, Trace metal bioaccumulation in eight common coastal Australian polychaeta J. Environ. Monit. 2006, 8, 1149.
| Trace metal bioaccumulation in eight common coastal Australian polychaetaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFeru7jP&md5=b1fef4e9011867ab44374dd53e649dd9CAS |
[25] S. Foster, Arsenic Cycling in Marine Ecosystems: Investigating the Link Between Primary Production and Secondary Consumption 2008 (Institute of Applied Ecology, University of Canberra: Canberra, ACT).
[26] J. Kirby, W. Maher, D. Spooner, Arsenic occurrence and species in near-shore macroalgae-feeding marine animals Environ. Sci. Technol. 2005, 39, 5999.
| Arsenic occurrence and species in near-shore macroalgae-feeding marine animalsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVWit7g%3D&md5=b42dbcb645bd7af2e1a70e856fbc5fdfCAS |
[27] W. Maher, F. Krikowa, J. Kirby, A. T. 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=a318bd98e879d309d71e222f542e91b4CAS |
[28] 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=c21d797c63e8a0729165be2f96f244afCAS |
[29] J. Kirby, W. Maher, M. J. 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=aac72c5bcd52aef1073eaebc8c4ba457CAS |
[30] M. Deaker, W. Maher, Determination of arsenic in arsenic compounds and marine biological tissues using low-volume microwave digestion and electrothermal atomic absorption spectrometry J. Anal. At. Spectrom. 1999, 14, 1193.
| Determination of arsenic in arsenic compounds and marine biological tissues using low-volume microwave digestion and electrothermal atomic absorption spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltFWgt7k%3D&md5=a40540d2efa44545678d53e65657d05dCAS |
[31] 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.
| 1:CAS:528:DC%2BD38XlvVKhsbs%3D&md5=90867d45276d36c837ab12e224092c66CAS |
[32] K. R. Clarke, R. M. Warwick, Changes in Marine Communities: An Approach to Statistical Analysis and Interpretation 1994 (Plymouth Marine Laboratory: Plymouth, UK).
[33] A. Benson, R. Summons, Arsenic accumulation in Great Barrier Reef invertebrates Science 1981, 211, 482.
| Arsenic accumulation in Great Barrier Reef invertebratesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXpslCjug%3D%3D&md5=5c07453d226873a13fdeeea61b024d35CAS |
[34] M. Gibbs, J. M. Earl, J. L. Ritchie, Metabolism of ribose-1-C14 by cell-free extracts of yeast J. Biol. Chem. 1955, 217, 161.
| 1:CAS:528:DyaG28Xhs1KhsQ%3D%3D&md5=e09ca91e5cfbead5ad92e9dacafcb957CAS |
[35] D. Fattorini, A. Notti, F. Regoli, Characterisation of arsenic content in marine organisms from temperate, tropical and polar environments Chem. Ecol. 2006, 22, 405.
| 1:CAS:528:DC%2BD28XhtlCisrbO&md5=0fc9ac93dfaac95d1758336b19ca3a1aCAS |
[36] J. P. Meador, D. W. Ernest, A. Kagley, Bioaccumulation of arsenic in marine fish and invertebrates from Alaska and California Arch. Environ. Contam. Toxicol. 2004, 47, 223.
| Bioaccumulation of arsenic in marine fish and invertebrates from Alaska and CaliforniaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmsVCls70%3D&md5=ba2ccb44804c7ef21a2ce387482acd58CAS |
[37] P. Peshut, R. Morrison, B. Brooks, Arsenic speciation in marine fish and shellfish from American Samoa Chemosphere 2008, 71, 484.
| Arsenic speciation in marine fish and shellfish from American SamoaCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVWjsLs%3D&md5=ba3f8a2458f44af094369ec9ab3c6fb1CAS |
[38] C. M. Santos, M. A. Nunes, I. S. Barbosa, G. L. Santos, M. C. Peso-Aguiar, M. G. Korn, E. M. Flores, V. L. Dressler, Evaluation of microwave and ultrasound extraction procedures for arsenic speciation in bivalve mollusks by liquid chromatography–inductively coupled plasma mass spectrometry Spectrochim. Acta B At. Spectrosc. 2013, 86, 108.
| Evaluation of microwave and ultrasound extraction procedures for arsenic speciation in bivalve mollusks by liquid chromatography–inductively coupled plasma mass spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpslCrtLk%3D&md5=1a43927897101a01ab70fa6a79967890CAS |
[39] 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=632adada1ef39e96a0183097b706d67eCAS |
[40] W. Langston, Availability of arsenic to estuarine and marine organisms: a field and laboratory evaluation Mar. Biol. 1984, 80, 143.
| Availability of arsenic to estuarine and marine organisms: a field and laboratory evaluationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhs1Wksrw%3D&md5=8e30bc06c3aa05f11c33843148417b81CAS |
[41] K. i. Hanaoka, S. Tagawa, T. Kaise, The degradation of arsenobetaine to inorganic arsenic by sedimentary microorganisms Hydrobiologia 1992, 235, 623.
| The degradation of arsenobetaine to inorganic arsenic by sedimentary microorganismsCrossref | GoogleScholarGoogle Scholar |
[42] S. Foster, W. Maher, E. Schmeisser, A. Taylor, F. Krikowa, S. Apte, Arsenic species in a rocky intertidal marine food chain in NSW, Australia, revisited Environ. Chem. 2006, 3, 304.
| Arsenic species in a rocky intertidal marine food chain in NSW, Australia, revisitedCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptVaksr4%3D&md5=aa89f1b59dd4ecd317fa83ecb5461185CAS |
[43] J. Kirby, W. Maher, Tissue accumulation and distribution of arsenic compounds in three marine fish species: relationship to trophic position Appl. Organomet. Chem. 2002, 16, 108.
| 1:CAS:528:DC%2BD38Xht1Sku70%3D&md5=0c1cac37bf98fb75d5da0b9f3b284d98CAS |
[44] S. McSheehy, J. Szpunar, R. Lobinski, V. Haldys, J. Tortajada, J. Edmonds, Characterization of arsenic species in kidney of the clam Tridacna derasa by multidimensional liquid chromatography–ICPMS and electrospray time-of-flight tandem mass spectrometry Anal. Chem. 2002, 74, 2370.
| Characterization of arsenic species in kidney of the clam Tridacna derasa by multidimensional liquid chromatography–ICPMS and electrospray time-of-flight tandem mass spectrometryCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis12gtrw%3D&md5=9dc8af1fbf9e7935c8a6237f427a2d4aCAS |
[45] 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=6a7b5d9848203f08d6f0e495e4769806CAS |
