Arsenic compounds in tropical marine ecosystems: similarities between mangrove forest and coral reef
Somkiat Khokiattiwong A , Narumol Kornkanitnan A , Walter Goessler B , Sabine Kokarnig B and Kevin A. Francesconi B CA Phuket Marine Biological Center, PO Box 60, Phuket 83000, Thailand.
B Institute of Chemistry-Analytical Chemistry, Karl-Franzens University Graz, A-8010 Graz, Austria.
C Corresponding author. Email: kevin.francesconi@uni-graz.at
Environmental Chemistry 6(3) 226-234 https://doi.org/10.1071/EN09009
Submitted: 17 January 2009 Accepted: 24 April 2009 Published: 18 June 2009
Environmental context. Despite the widespread occurrence of arsenobetaine in marine animals the origin of this arsenic compound remains unknown. A current hypothesis is that arsenobetaine is formed from more complex arsenic compounds found in marine algae. To test this hypothesis, we examined the arsenic compounds in a mangrove ecosystem where algae play a limited role in primary productivity.
Abstract. Marine algae are known to bioaccumulate arsenic and transform it into arsenosugars, which are thought to be precursors of the major arsenic compound, arsenobetaine, found in marine animals. Marine ecosystems based on mangrove forests have high nutrient input from mangrove leaves, and thus provide a unique opportunity to study the cycling of arsenic in a marine system where algae are not the dominant food source. Two mangrove forests in Phuket, Thailand were selected as sampling sites for this study. For comparison, samples were also collected from two coral reef sites at and near Phuket. The samples collected included mangrove leaves, corals, algae, molluscs, fish and crustaceans. Arsenic contents in the samples and in aqueous extracts of the samples were determined by hydride generation atomic absorption spectrometry following a dry-ashing mineralisation procedure, and arsenic species were determined in the aqueous extracts by HPLC-MS (mainly ICPMS). Mangrove leaves contained only low concentrations of total arsenic (0.10–0.73 mg kg–1 dry mass) and the aqueous extracts thereof contained inorganic arsenic species, methylarsonate and dimethylarsinate, but arsenosugars were not detected. The total mean arsenic contents (3.2–86 mg kg–1 dry mass) of the animals from the mangrove ecosystem, however, were typical of those found in animal samples from other marine ecosystems. Similarly the arsenic compounds present were typical of those in animals from other marine ecosystems comprising mainly arsenobetaine with smaller quantities of other common arsenicals including arsenosugars, arsenocholine, tetramethylarsonium ion, trimethylarsine oxide and dimethylarsinate. A trimethylated arsenosugar, which is not commonly reported in marine organisms, was a significant arsenical (6–8% of total As) in some gastropod species from the mangrove ecosystem. The coral samples contained mainly arsenosugars and arsenobetaine, and the other animals collected from the coral ecosystem contained essentially the same pattern of arsenicals found for the mangrove animals. The data suggest that food chains based on algae are not necessary for animals to accumulate large concentrations of arsenobetaine.
Acknowledgements
We thank DANIDA for financial support.
[1]
K. A. Francesconi ,
J. S. Edmonds ,
Arsenic and marine organisms.
Adv. Inorg. Chem. 1996
, 44, 147.
| Crossref | GoogleScholarGoogle Scholar |
[2]
M. O. Andreae ,
Determination of arsenic species in natural waters.
Anal. Chem. 1977
, 49, 820.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[3]
S. J. Santosa ,
S. Wada ,
S. Tanaka ,
Distribution and cycle of arsenic compounds in the ocean.
Appl. Organomet. Chem. 1994
, 8, 273.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[4]
W. K. Gong ,
J. E. Ong ,
Plant biomass and nutrient flux in a managed mangrove forest in Malaysia.
Estuar. Coast. Shelf Sci. 1990
, 31, 519.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[5]
E. Kristensen ,
M. Holmer ,
G. T. Banta ,
M. H. Jensen ,
K. Hansen ,
Carbon, nitrogen and sulfur cycling in sediments of the Ao Nam Bor mangrove forest, Phuket, Thailand: a review.
Phuket Mar. Biol. Cent. Res. Bull. 1995
, 60, 37.
[6]
J. Kirby ,
W. Maher ,
F. Chariton ,
Krikowa, Arsenic concentrations and speciation in a temperate mangrove ecosystem, NSW, Australia.
Appl. Organomet. Chem. 2002
, 16, 192.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[7]
D. Thomson ,
W. Maher ,
S. Foster ,
Arsenic and selected elements in marine angiosperms, south-east coast, NSW, Australia.
Appl. Organomet. Chem. 2007
, 21, 381.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[8]
B. Bachmann ,
D. A. Hunter ,
K. A. Francesconi ,
Accumulation and fate of ingested tetramethylarsonium ion in the shrimp Crangon crangon.
Appl. Organomet. Chem. 1999
, 13, 771.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[9]
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[10]
[11]
K. A. Francesconi ,
J. Gailer ,
J. S. Edmonds ,
W. Goessler ,
K. J. Irgolic ,
Uptake of arsenic-betaines by the mussel Mytilus edulis.
Comp. Biochem. Physiol. C 1999
, 122, 131.
|
CAS |
[12]
K. A. Francesconi ,
J. S. Edmonds ,
R. V. Stick ,
Synthesis, NMR spectra and chromatographic properties of five trimethylarsonioribosides.
Appl. Organomet. Chem. 1994
, 8, 517.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[13]
K. A. Francesconi ,
J. S. Edmonds ,
R. V. Stick ,
Arsenic compounds from the kidney of the giant clam Tridacna maxima: isolation and identification of an arsenic-containing nucleoside.
J. Chem. Soc., Perkin Trans. 1 1992
, 1, 1349.
| Crossref | GoogleScholarGoogle Scholar |
[14]
K. A. Francesconi ,
J. S. Edmonds ,
R. V. Stick ,
Accumulation of arsenic in yellow-eye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenate.
Sci. Total Environ. 1989
, 79, 59.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[15]
D. A. Hunter ,
W. Goessler ,
K. A. Francesconi ,
Uptake of arsenate, trimethylarsine oxide, and arsenobetaine from seawater and food by the shrimp Crangon crangon (L.).
Mar. Biol. 1998
, 131, 543.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[16]
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[17]
Y. Bohari ,
G. Lobos ,
H. Pinochet ,
F. Pannier ,
A. Astruc ,
M. Potin-Gautier ,
Speciation of arsenic in plants by HPLC-HG-AFS: extraction optimization on CRM materials and application to cultivated samples.
J. Environ. Monit. 2002
, 4, 596.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[18]
V. W. M. Lai ,
W. R. Cullen ,
S. Ray ,
Arsenic speciation in scallops.
Mar. Chem. 1999
, 66, 81.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[19]
K. A. Francesconi ,
W. Goessler ,
S. Panutrakul ,
K. J. Irgolic ,
A novel arsenic containing riboside (arsenosugar) in three species of gastropod.
Sci. Total Environ. 1998
, 221, 139.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[20]
S. Foster ,
W. Maher ,
A. Taylor ,
F. Krikowa ,
K. Telford ,
Distribution and speciation of arsenic in temperate marine saltmarsh ecosystems.
Environ. Chem. 2005
, 2, 177.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[21]
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[22]
S. Foster ,
W. Maher ,
F. Krikowa ,
Changes in proportions of arsenic species within an Ecklonia radiata food chain.
Environ. Chem. 2008
, 5, 176.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[23]
A. Rumpler ,
J. S. Edmonds ,
M. Katsu ,
K. G. Jensen ,
W. Goessler ,
G. Raber ,
H. Gunnlaugsdottir ,
K. A. Francesconi ,
Arsenic-containing long-chain fatty acids in cod liver oil: a result of biosynthetic infidelity?
Angew. Chem. Int. Ed. 2008
, 47, 2665.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[24]
M. S. Taleshi ,
K. B. Jensen ,
G. Raber ,
J. S. Edmonds ,
H. Gunnlaugsdottir ,
K. A. Francesconi ,
Arsenic-containing hydrocarbons: Natural compounds in oil from the fish capelin, Mallotus villosus.
Chem. Commun. 2008
, 39, 4706.
| Crossref | GoogleScholarGoogle Scholar |
[25]
K. A. Francesconi ,
S. Khokiattiwong ,
W. Goessler ,
S. N. Pedersen ,
M. Pavkov ,
A new arsenobetaine from marine organisms identified by liquid chromatography-mass spectrometry.
Chem. Commun. 2000
, 12, 1083.
| Crossref | GoogleScholarGoogle Scholar |
[26]
J. S. Edmonds ,
K. A. Francesconi ,
P. C. Healy ,
A. H. White ,
Isolation and crystal structure of an arsenic-containing sugar sulphate from the kidney of the giant clam, Tridacna maxima. X-ray crystal structure of (2S)-3-[5-deoxy-5-(dimethylarsinoyl)-B-D-ribofuranosyloxy]-2-hydroxypropyl hydrogen sulphate.
J. Chem. Soc., Perkin Trans. 1 1982
, 2989.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[27]
B. E. Brown ,
R. P. Dunne ,
I. Ambarsari ,
M. D. A. Le Tissier ,
U. Satapoomin ,
Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species.
Mar. Ecol. Prog. 1999
, 191, 53.
| Crossref | GoogleScholarGoogle Scholar |
[28]
B. E. Brown ,
Coral bleaching: causes and consequences.
Coral Reefs 1997
, 16, S129.
| Crossref | GoogleScholarGoogle Scholar |
[29]
T. P. Scoffin ,
B. E. Brown ,
R. P. Dunne ,
M. D. A. Le Tissier ,
The controls on growth from of intertidal massive corals, Phuket, South Thailand.
Palaios 1997
, 12, 237.
| Crossref | GoogleScholarGoogle Scholar |
[30]
R. Rowan ,
N. Knowlton ,
A. Baker ,
J. Jara ,
Landscape ecology of algal symbionts creates variation in episodes of coral bleaching.
Nature 1997
, 388, 265.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[31]
W. Goessler ,
W. Maher ,
K. J. Irgolic ,
D. Kuehnelt ,
C. Schlagenhaufen ,
T. Kaise ,
Arsenic compounds in a marine food chain.
Fresenius J. Anal. Chem. 1997
, 359, 434.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[32]
V. Nischwitz ,
S. A. Pergantis ,
First report on the detection and quantification of arsenobetaine in extracts of marine algae using HPLC-ES-MS/MS.
Analyst 2005
, 130, 1348.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
[33]
M. Grotti ,
F. Soggia ,
C. Lagomarsino ,
W. Goessler ,
K. A. Francesconi ,
Arsenobetaine is a significant arsenical constituent of the red Antarctic alga Phyllophora antarctica.
Environ. Chem. 2008
, 5, 171.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
[34]
E. H. Larsen ,
C. R. Quetel ,
R. Munoz ,
A. Fiala-Medioni ,
O. F. X. Donard ,
Arsenic speciation in shrimp and mussel from the Mid-Atlantic hydrothermal vents.
Mar. Chem. 1997
, 57, 341.
| Crossref | GoogleScholarGoogle Scholar |
CAS |