Advertisement

Environmental Geochemistry and Health

, Volume 35, Issue 1, pp 13–25 | Cite as

Arsenic speciation in polychaetes (Annelida) and sediments from the intertidal mudflat of Sundarban mangrove wetland, India

  • M. J. WattsEmail author
  • T. S. Barlow
  • M. Button
  • S. K. Sarkar
  • B. D. Bhattacharya
  • Md. Aftab Alam
  • A. Gomes
Original Paper

Abstract

This paper documents the concentration of total arsenic and individual arsenic species in four soft-bottom benthic polychaetes (Perenereis cultifera, Ganganereis sootai, Lumbrinereis notocirrata and Dendronereis arborifera) along with host sediments from Sundarban mangrove wetland, India. An additional six sites were considered exclusively for surface sediments for this purpose. Polychaetes were collected along with the host sediments and measured for their total arsenic content using inductively coupled plasma mass spectrometry. Arsenic concentrations in polychaete body tissues varied greatly, suggesting species-specific characteristics and inherent peculiarities in arsenic metabolism. Arsenic was generally present in polychaetes as arsenate (AsV ranges from 0.16 to 0.50 mg kg−1) or arsenite (AsIII ranges from 0.10 to 0.41 mg kg−1) (30–53 % as inorganic As) and dimethylarsinic acid (DMAV <1–25 %). Arsenobetaine (AB < 16 %), and PO4-arsenoriboside (8–48 %) were also detected as minor constituents, whilst monomethylarsonic acid (MAV) was not detected in any of the polychaetes. The highest total As (14.7 mg kg−1 dry wt) was observed in the polychaete D. arborifera collected from the vicinity of a sewage outfall in which the majority of As was present as an uncharacterised compound (10.3 mg kg−1 dry wt) eluted prior to AB. Host sediments ranged from 2.5 to 10.4 mg kg−1 of total As. This work supports the importance of speciation analysis of As, because of the ubiquitous occurrence of this metalloid in the environment, and its variable toxicity depending on chemical form. It is also the first work to report the composition of As species in polychaetes from the Indian Sundarban wetlands.

Keywords

Arsenic Sundarban Polychaetes Arsenic speciation Sediment 

Notes

Acknowledgments

The research work was financially supported by the University Grants Commission (UGC), New Delhi, India (Sanction No UGC/199/UPE/07) under the scheme ‘University with Potential for Excellence’ (Modern Biology Group). One of the authors (Md. A. Alam) is greatly indebted to UGC for awarding him project fellowship. The collaboration was facilitated through funding from the Royal Society. This work is published with the permission of the Executive Director of the British Geological Survey.

References

  1. Bhattacharya, A., & Sarkar, S. K. (2003). Impact of over exploitation of shellfish: Northeastern coast of India. Ambio, 32(1), 70–75.Google Scholar
  2. Boyle, E. A., Edmond, J. M., & Sholkovitz, E. R. (1977). Mechanism of iron removal in estuaries. Geochimica et Cosmochimica Acta, 41(9), 1313–1324.CrossRefGoogle Scholar
  3. Button, M., Jenkins, G. T., Harrington, C. F., & Watts, M. J. (2009). Biotransformation of As in earthworms from a contaminated mine site. Journal of Environmental Monitoring, 11, 1484–1491.CrossRefGoogle Scholar
  4. Canuel, E. A., & Martens, C. S. (1993). Seasonal variations in the sources and alteration of organic matter associated with recently-deposited sediments. Organic Geochemistry, 20, 563–577.CrossRefGoogle Scholar
  5. Casado-Martinez, M. C., Duncan, E. G., Smith, B. D., Maher, W. A., & Rainbow, P. S. (2012). Arsenic toxicity in a sediment-dwelling polychaete: Detoxification and arsenic metabolism. Toxicology, 21, 576–590.Google Scholar
  6. Casado-Martinez, M. C., Smith, B. D., Luoma, S. N., & Rainbow, P. S. (2010). Bioaccumulation of arsenic from water and sediment by a deposit-feeding polychaete (Arenicola marina): A biodynamic modeling approach. Aquatic Toxicology, 98, 34–43.CrossRefGoogle Scholar
  7. Chatterjee, M., Canario, J., Sarkar, S. K., Brancho, V., Bhattacharya, A. K., & Saha, S. (2009a). Mercury enrichments in core sediments in Sundarban mangroves, northeastern part of Bay of Bengal and their ecotoxicological significance. Environmental Geology, 57(5), 1125–1134.CrossRefGoogle Scholar
  8. Chatterjee, M., Massolo, S., Sarkar, S. K., Bhattacharya, A. K., Bhattacharya, B. D., Satpathy, K. K., et al. (2009b). An assessment of trace element contamination in intertidal sediment cores of Sundarban mangrove wetland, India for evaluating sediment quality guidelines. Environmental Monitoring and Assessment, 150, 307–322.CrossRefGoogle Scholar
  9. Chatterjee, M., Silva Filho, E. V., Sarkar, S. K., Sella, S. M., Bhattacharya, A., Satpathy, K. K., et al. (2007). Distribution and possible source of trace elements in the sediment cores of a tropical macrotidal estuary and their ecotoxicological significance. Environment International, 33, 346–356.CrossRefGoogle Scholar
  10. Cullen, W. R., & Reimer, K. J. (1989). Arsenic speciation in the environment. Chemistry Reviews, 89, 713–764.CrossRefGoogle Scholar
  11. Depledge, M. H., & Rainbow, P. S. (1990). Models of regulation and accumulation of trace metals in marine invertebrates. Comparative Biochemistry and Physiology, C: Comparative Pharmacology and Toxicology, 97, 1–7.CrossRefGoogle Scholar
  12. Domínguez, C., Sarkar, S. K., Bhattacharya, A., Chatterjee, M., Bhattacharya, B. D., Jover, E., et al. (2010). Quantification and source identification of polycyclic aromatic hydrocarbons in core sediments from Sundarban Mangrove Wetland, India. Archives of Environmental Contamination and Toxicology, 59, 49–61.CrossRefGoogle Scholar
  13. Edmonds, J. S., & Francesconi, K. A. (1987). Transformations of arsenic in the marine environment. Experientia, 43, 553–557.CrossRefGoogle Scholar
  14. Ellwood, M. J., & Maher, W. A. (2003). Measurement of arsenic species in marine sediments by high performance liquid chromatography inductively coupled plasma mass spectrometry. Analytica Chimica Acta, 477, 279–291.CrossRefGoogle Scholar
  15. Fattorini, D., Alonso-Hernandez, C. M., Diaz-Asencio, M., Munoz-Caravaca, A., Panacciulli, F. G., Tangherlini, M., et al. (2004). Chemical speciation of arsenic in different marine organisms: Importance in monitoring study. Marine Environmental Research, 58, 845–850.CrossRefGoogle Scholar
  16. Fattorini, D., Notti, A., Di Mento, R., Cicero, A. M., Gabellini, M., Russo, A., et al. (2008). Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: A regional gradient for arsenic and implications for monitoring the impact of offshore activities. Chemosphere, 72, 1524–1533.CrossRefGoogle Scholar
  17. Fattorini, D., Notti, A., Halt, M. N., Gambi, M. C., & Regoli, F. (2005). Levels and chemical speciation of arsenic in polychaetes: A review. Marine Ecology, 26, 255–264.CrossRefGoogle Scholar
  18. Francesconi, K. A., & Edmonds, J. S. (1994). Biotransformation of arsenic in the marine environment. In J. O. Niagu (Ed.), Arsenic in the environment, part I: Cycling and characterization (p. 221). New York: Wiley.Google Scholar
  19. Francesconi, K. A., & Edmonds, J. S. (1997). Arsenic and marine organisms. Advances in Inorganic Chemistry, 44, 147–189.CrossRefGoogle Scholar
  20. Francesconi, K. A., Goessler, W., Panutrakul, S., & Irgolic, K. J. (1998). A novel arsenic containing riboside arsenosugar in three species of gastropod. The Science of Total Environment, 221, 139–148.CrossRefGoogle Scholar
  21. Gallardo, M. V., Bohari, Y., Astruc, A., Potin-Gautier, M., & Astruc, M. (2001). Speciation analysis of arsenic in environmental solids reference materials by high performance liquid chromatography hydride generation atomic fluorescence spectrometry following orthophosphoric acid extraction. Analytica Chimica Acta, 441, 257–268.CrossRefGoogle Scholar
  22. Garcia-Manyes, S., Jiminez, G., Padro, A., Rubio, R., & Rauret, G. (2002). Arsenic speciation in contaminated soils. Talanta, 58, 97–109.CrossRefGoogle Scholar
  23. Gebel, T. W. (2001). Genotoxicity of arsenical compounds. International Journal of Hygiene and Environmental Health, 203, 249–262.CrossRefGoogle Scholar
  24. Geiszinger, A. E., Goessler, W., & Francesconi, K. A. (2002a). The marine polychaete Arenicola marina: Its unusual arsenic compound pattern and its uptake of arsenate from seawater. Marine Environmental Research, 53, 37–50.CrossRefGoogle Scholar
  25. Geiszinger, A. E., Goessler, W., & Francesconi, K. A. (2002b). Biotransformation of arsenate to the tetramethylarsonium ion in the marine polychaetes Nereis diversicolor and Nereis virens. Environmental Science and Technology, 36, 2905–2910.CrossRefGoogle Scholar
  26. Geiszinger, A., Goessler, W., Kuehnelt, D., Francesconi, K., & Kosmus, W. (1998). Determination of arsenic compounds in earthworms. Environmental Science and Technology, 32, 2238–2243.CrossRefGoogle Scholar
  27. Gibbs, P. E., Langston, W. J., Burt, G. R., & Pascoe, P. L. (1983). Tharyx marioni (Polychaeta): A remarkable accumulator of arsenic. Journal of Marine Biological Association of UK, 63, 313–325.CrossRefGoogle Scholar
  28. Gomez-Ariza, J. L., Sanchez-Rodas, D., Giraldez, I., & Morales, E. (2000). Comparison of biota sample pretreatments for arsenic speciation with coupled HPLC-HG-ICP-MS. Analyst, 125, 401–407.CrossRefGoogle Scholar
  29. Hanaoka, K., Koga, H., Tagawa, S., & Kaise, T. (1992a). Degradation of arsenobetaine to inorganic arsenic by the microorganisms occurring in the suspended substances. Comparative Biochemistry and Physiology, 101B, 595–599.Google Scholar
  30. Hanaoka, K., Koga, H., Tagawa, S., & Kaise, T. (1992b). The degradation of arsenobetaine to inorganic arsenic by sedimentary microorganisms. Hydrobiologia, 235/236 (Dev. Hydrobiol. 75), 623–628.Google Scholar
  31. Hanaoka, K., Tagawa, S., & Kaise, T. (1996). The fate of organoarsenic compounds in marine ecosystems. Applied Organometallic Chemistry, 6, 139–146.CrossRefGoogle Scholar
  32. Hatje, V., Macedo, S. M., de Jesus, R. M., Cotrim, G., Garcia, K. S., de Queiroz, A. F., et al. (2010). Inorganic As speciation and bioavailability in estuarine sediments of Todos os Santosh Bay, BA, Brazil. Marine Pollution Bulletin, 60, 2225–2232.CrossRefGoogle Scholar
  33. Hutchings, P. A. (1984). A preliminary report on the spatial and temporal patterns of polychaete recruitment on the Great Barrier Reef. In Hutchings PA (Ed.), Proceedings of 1st international polychaete conference Sydney. Limnological Society NSW (pp. 227–237).Google Scholar
  34. Islama, S. M. N., Rahmana, S. H., Chowdhury, D. A., Rahmana, M. M., & Tareq, S. M. (2012). Seasonal variations of arsenic in the Ganges and Brahmaputra River, Bangladesh. Journal of Scientific Research, 4(1), 65–75.Google Scholar
  35. Jankong, P., Chalhoub, C., Kienzl, N., Goessler, W., Fransesconi, K., & Visoottiviseth, P. (2007). Arsenic accumulation and speciation in freshwater fish living in arsenic contaminated waters. Environmental Chemistry, 4, 11–17.CrossRefGoogle Scholar
  36. Kuehl, S. A., Hariu, T. M., & Moore, W. S. (1989). Shelf sedimentation off the Ganges–Brahmaputra river system: Evidence for sediment bypassing to the Bengal fan. Journal of Geology, 17, 1132–1135.CrossRefGoogle Scholar
  37. Kuehnelt, D., Goessler, W., & Irgolic, K. J. (1997). Arsenic compounds in terrestrial organisms III: Arsenic compounds in Formica sp. from an old arsenic smelter site. Applied Organometallic Chemistry, 11, 289–296.CrossRefGoogle Scholar
  38. Lee, J. S., & Lee, B. G. (2005). Effects of salinity, temperature and food type on the uptake and elimination rates of Cd, Cr and Xn in the Asiatic Clam Corbicula fluminea. Ocean Science Journal, 40, 79–89.CrossRefGoogle Scholar
  39. Luoma, S. N., & Cloern, J. E. (1982). The impacts of waste-water discharge on biological communities in San Francisco Bay. In H. J. Kockelman, T. J. Conomos, & A. E. Leviton (Eds.), San Francisco Bay, use and protection (pp. 137–160). San Francisco: Pacific Division, AAAS.Google Scholar
  40. Madsen, A. D., Goessler, W., Pedersen, S. N., & Francesconi, K. A. (2000). Characterisation of an algal extract by HPLC-ICP-MS and LC-electrospray MS for use in arsenosugar speciation studies. Journal of Analytical Atomic Spectrometry, 15, 657–662.CrossRefGoogle Scholar
  41. Maher, W. A., Foster, S. D., Taylor, A. M., Krikowa, F., Duncan, E. G., & Chariton, A. A. (2011). Arsenic distribution and species in two Zostera capricorni seagrass ecosystems, New South Wales. Environmental Chemistry, 8, 9–18.CrossRefGoogle Scholar
  42. Meador, J. P., Ernest, D. W., & Kagley, A. (2004). Bioaccumulation of arsenic in marine fish and invertebrates from Alaska and California. Archives of Environmental Contamination and Toxicology, 47, 223–233.CrossRefGoogle Scholar
  43. Moore, J. W., & Ramamoorthy, S. (1984). Heavy metals in natural waters. Applied monitoring and impact assessment. New York: Springer.CrossRefGoogle Scholar
  44. Nam, S.-H., Oh, H.-J., Min, H.-S., & Lee, J.-H. (2010). A study on the extraction and quantization of total arsenic and arsenic species in seafood by HPLC-ICP-MS. Microchemical Journal, 95, 20–24.CrossRefGoogle Scholar
  45. Neff, J. M. (1997). Ecotoxicology of arsenic in the marine environment: A review. Environmental Toxicology and Chemistry, 16, 917–927.Google Scholar
  46. Nischwitz, V., & Pergantis, S. A. (2006). Optimization of an HPLC selected reaction monitoring electrospray tandem mass spectrometry method for the detection of 50 arsenic species. Journal of Analytical Atomic Spectrometry, 21, 1277–1286.CrossRefGoogle Scholar
  47. Notti, A., Fattorini, D., Razzetti, E. M., & Regoli, F. (2007). Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii: Experimental observations. Environmental Toxicology and Chemistry, 26, 1186–1191.CrossRefGoogle Scholar
  48. O’Reilly, J., Watts, M. J., Shaw, R. A., Marcilla, A. L., & Ward, N. I. (2010). Arsenic contamination of natural waters in San Juan and La Pampa, Argentina. Environmental Geochemistry and Health, 32, 491–515.CrossRefGoogle Scholar
  49. Pérez-López, R., Nieto, J. M., López-Cascajosa, M. J., Díaz-Blanco, M. J., Sarmiento, A. M., Oliveira, V., et al. (2011). Evaluation of heavy metals and arsenic speciation discharged by the industrial activity on the Tinto-Odiel estuary, SW Spain. Marine Pollution Bulletin, 62, 405–411.CrossRefGoogle Scholar
  50. Phillips, D. J. H. (1990). Arsenic in aquatic organisms: A review, emphasizing chemical speciation. Aquatic Toxicology, 16, 151–186.CrossRefGoogle Scholar
  51. Pierce, M. L., & Moore, C. B. (1982). Adsorption of arsenite and arsenate on amorphous iron hydroxide. Water Research, 16, 1247–1253.CrossRefGoogle Scholar
  52. Rattanachongkiat, S., Millward, G. E., & Foulkes, M. E. (2004). Determination of arsenic species in fish, crustacean and sediment samples from Thailand using high performance liquid chromatography (HPLC) coupled with inductively coupled plasma mass spectrometry (ICP-MS). Journal of Environmental Monitoring, 6, 254–261.CrossRefGoogle Scholar
  53. Reimer, K. J., & Thompson, A. J. (1988). Arsenic speciation in marine interstitial water. The occurrence of organoarsenicals. Biogeochemistry, 6, 211–237.CrossRefGoogle Scholar
  54. Sarkar, S. K., & Bhattacharya, A. K. (2003). Conservation of biodiversity of the coastal resources of Sundarbans, northeast India: An integrated approach through environmental education. Marine Pollution Bulletin, 47, 260–264.CrossRefGoogle Scholar
  55. Sarkar, S. K., Bhattacharya, B. D., & Saha, S. (2007a). Spatial variations of zooplankton in Sundarban mangrove wetland, northeastern part of the Bay of Bengal. The ICFAI Journal of life Sciences, 1, 7–21.Google Scholar
  56. Sarkar, S. K., Franciscovic-Bilinski, S., Bhattacharya, A., Saha, M., & Bilinski, H. (2004). Levels of elements in the surficial estuarine sediments of the Hugli River, northeast India and their environmental implications. Environment International, 30, 1089–1098.CrossRefGoogle Scholar
  57. Sarkar, S. K., Saha, M., Takada, H., Bhattacharya, A., Mishra, P., & Bhattacharya, B. (2007b). Water quality management in the lower stretch of the river Ganges, east coast of India: An approach through environmental education. Journal of Cleaner Production, 15(16), 1459–1467.CrossRefGoogle Scholar
  58. Shiomi, K., Shiagawa, A., Azuma, A., Yamanaka, H., & Kikuchi, T. (1983). Purification of water-soluble arsenic compounds in a flatfish Limanda herzensteini, sea squirt Halocynthia roretzi, and sea cucumber Stichopus japanicus. Comparative Biochemistry and Physiology, 74, 393–396.Google Scholar
  59. Shumilin, E., Meyer-Willerer, A., Marmolejo-Rodriguez, A. J., Morton-Bermea, O., Galicia-Perez, M. A., Hernandez, E., et al. (2005). Iron, cadmium, chromium, copper, cobalt, lead, and zinc distribution in the suspended particulate matter of the tropical Marabasco River and its estuary, Colima, Mexico. Bulletin of Environmental Contamination and Toxicology, 74, 518–525.CrossRefGoogle Scholar
  60. Swaine, D. J. (2000). Why trace elements are important. Fuel Processing Technology, 65–66, 21–33.CrossRefGoogle Scholar
  61. Waldichuk, M. (1985). Biological availability of metals to marine organisms. Marine Pollution Bulletin, 16, 7–11.CrossRefGoogle Scholar
  62. Wang, Y.-C., Chaung, R.-H., & Tung, L.-C. (2004). Comparison of the cytotoxicity induced by different exposure to sodium arsenite in two fish cell lines. Aquatic Toxicology, 69, 67–79.CrossRefGoogle Scholar
  63. Wang, W. X., & Fisher, N. S. (1999). Assimilation efficiencies of chemical contaminants in aquatic invertebrates: A synthesis. Environmental Toxicology and Chemistry, 18, 2023–2045.CrossRefGoogle Scholar
  64. Wang, W.-X., Qiu, J.-W., & Qian, P.-Y. (1999). Significance of trophic transfer in predicting the high concentration of zinc in barnacles. Environmental Science and Technology, 33, 2906–2909.Google Scholar
  65. Waring, J. S., & Maher, W. (2005). Arsenic bioaccumulation and species in marine Polychaeta. Applied Organometallic Chemistry, 19, 917–929.CrossRefGoogle Scholar
  66. Waring, J., Maher, W., Foster, S., & Krilkowa, F. (2005). Occurrence and speciation of arsenic in common Australian coastal polychaetes species. Environmental Chemistry, 2, 108–118.CrossRefGoogle Scholar
  67. Waring, J., Maher, W. A., Foster, S., & Krilkowa, F. (2006). Trace metal bioaccumulation in eight common coastal Australian polychaeta. Journal of Environmental Monitoring, 8, 1149–1157.CrossRefGoogle Scholar
  68. Watts, M. J., Button, M., Brewer, T., & Harrington, C. F. (2008). Quantitative arsenic speciation in two species of earthworms from a former mine site. Journal of Environmental Monitoring, 10, 753–759.CrossRefGoogle Scholar
  69. Whalley, C., Rowlatt, S., Bennett, M., & Lovell, D. (1999). Total arsenic in sediments from the Western North Sea and the Humber Estuary. Marine Pollution Bulletin, 38, 394–400.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • M. J. Watts
    • 1
    Email author
  • T. S. Barlow
    • 1
  • M. Button
    • 2
  • S. K. Sarkar
    • 3
  • B. D. Bhattacharya
    • 3
  • Md. Aftab Alam
    • 3
  • A. Gomes
    • 4
  1. 1.British Geological SurveyNottinghamUK
  2. 2.Environmental Science GroupRoyal Military College of CanadaKingstonCanada
  3. 3.Department of Marine ScienceUniversity of CalcuttaCalcuttaIndia
  4. 4.Department of PhysiologyUniversity of CalcuttaCalcuttaIndia

Personalised recommendations