Phytoremediation of heavy metals by the dominant mangrove associate species of Indian Sundarbans
Abstract
The present study aims to investigate the phytoremediation potential of zinc (Zn), copper (Cu), and lead (Pb) by two dominant mangrove associate species, Suaeda maritima, and Salicornia brachiata, found in the high saline supralittoral zone of Indian Sundarbans in four stations of the Hooghly-Matla estuarine complex during the premonsoon season (May 2019). We found that concentrations of biologically available heavy metals (HMs) in the ambient soil and bioaccumulated HMs within the vegetative plant parts occurred as per the order: Sagar South > Bakkhali > Jharkhali > Bali Island. The order of biologically available and bioaccumulated HMs was Zn > Cu > Pb. Interestingly, the selected HMs display high organ-specificity for both species with the highest enrichment in roots, followed by stems and leaves. We propose that these halophytes could be used as agents of phytoremediation and their farming would be effective in the ecorestoration of this deltaic complex in context to conservative pollutants.
Keyword : Indian Sundarbans, heavy metals, bioaccumulation, mangrove associate species, phytoremediation
How to Cite
Mukherjee, P., Pramanick, P., Zaman, S., & Mitra, A. (2021). Phytoremediation of heavy metals by the dominant mangrove associate species of Indian Sundarbans. Journal of Environmental Engineering and Landscape Management, 29(4), 391–402. https://doi.org/10.3846/jeelm.2021.15773
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Banerjee, K., Chakraborty, S., Paul, R., & Mitra, A. (2018). Accumulation of metals by mangrove species and potential for bioremediation. In N. Nagabhatla & Ch. D. Metcalfe (Eds.), Multifunctional wetlands (pp. 275–300). Springer. https://doi.org/10.1007/978-3-319-67416-2
Banerjee, K., Roy Chowdhury, M., Sengupta, K., Sett, S., & Mitra, A. (2012). Influence of anthropogenic and natural factors on the mangrove soil of Indian Sundarbans wetland. Archives of Environmental Science, 6, 80–91.
Bighiu, M. A., Eriksson-Wiklund, A. K., & Eklund, B. (2017). Biofouling of leisure boats as a source of metal pollution. Environmental Science and Pollution Research International, 24, 997–1006. https://doi.org/10.1007/s11356-016-7883-7
Blute, N. K., Brabander, D. J., Hemond, H. F., Sutton, S. R., Newville, M. G., & Rivers, M. L. (2004). Arsenic sequestration by ferric iron plaque on cattail roots. Environmental Science & Technology, 38, 6074–6077. https://doi.org/10.1021/es049448g
Caçador, I., Caetano, M., Duarte, B., & Vale, C. (2009). Stock and losses of trace metals from salt marsh plants. Marine Environmental Research, 67(2), 75–82. https://doi.org/10.1016/j.marenvres.2008.11.004
Chakraborty, S., Rudra, T., Guha, A., Ray, A., Pal, N., & Mitra, A. (2016). Spatial variation of heavy metals in Tenualosa ilisha muscle: A case study from the lower Gangetic delta and coastal West Bengal. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 1–14.
Chakraborty, S., Trivedi, S., Fazli, P., Zaman, S., & Mitra, A. (2014a). Avicennia alba: An indicator of heavy metal pollution in Indian Sundarban estuaries. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 1796–1807.
Chakraborty, S., Zaman, S., Fazli, P., & Mitra, A. (2014b). Spatial variations of dissolved zinc, copper and lead as influenced by anthropogenic factors in estuaries of Indian Sundarbans. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 182–189.
Chaudhuri, A. B., & Choudhury, A. (1994). Mangroves of the Sundarbans. Vol. 1: India. International Union for Conservation of Nature and Natural Resources (IUCN). https://portals.iucn.org/library/node/6855
Chowdhury, A., & Maiti, S. K. (2016). Identification of metal tolerant plant species in mangrove ecosystem by using community study and multivariate analysis: A case study from Indian Sunderban. Environmental Earth Sciences, 75, 744. https://doi.org/10.1007/s12665-016-5391-1
Essaidi, I., Brahmi, Z., Snoussi, A., Koubaier, H. B. H., Casabianca, H., Abe, N., Omri, A. E., Chaabouni, M. M., & Bouzouita, N. (2013). Phytochemical investigation of Tunisian Salicornia herbacea L., antioxidant, antimicrobial and cytochrome P450 (CYPs) inhibitory activities of its methanol extract. Food Control, 32(1), 125–133. https://doi.org/10.1016/j.foodcont.2012.11.006
Facciola, S. (1990). Cornucopia – A source book of edible plants. Kampong Publications.
Gopal, B., & Chauhan, M. (2006). Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquatic Sciences, 68(3), 338–354. https://doi.org/10.1007/s00027-006-0868-8
Hansel, C., Fendorf, S., Sutton, S., & Newville, M. (2001). Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science & Technology, 35(19), 3863–3868. https://doi.org/10.1021/es0105459
Hedrick, U. P. (Ed.). (1972). Sturtevant’s edible plants of the world. Dover Publications.
Kathiresan, K., Moorthy, P., & Rajendran, N. (1994). Seedling performance of mangrove Rhizophora apiculata (Rhizophorales: Rhizophoraceae) in different environs. Indian Journal of Marine Sciences, 23(3), 168–169. http://nopr.niscair.res.in/handle/123456789/37638
Krishnamurty, K. V., Shpirt, E., & Reddy, M. (1976). Trace metal extraction of soils and sediments by nitric acid and hydrogen peroxide. Atomic Absorption Newsletter, 15, 68–71.
Kunkel, G. (1984). Plants for human consumption. Koeltz Scientific Books.
MacFarlane, G. R. (2002). Leaf biochemical parameters in Avicennia marina (Forsk.) Vierh as potential biomarkers of heavy metal stress in estuarine ecosystems. Marine Pollution Bulletin, 44(3), 244–256. https://doi.org/10.1016/S0025-326X(01)00255-7
Malo, B. A. (1977). Partial extraction of metals from aquatic sediments. Environmental Science & Technology, 11(3), 277–282. https://doi.org/10.1021/es60126a007
Mitra, A. (1998). Status of coastal pollution in West Bengal with special reference to heavy metals. Journal of Indian Ocean Studies, 5, 135–138.
Mitra, A. (2013a). Blue carbon: A hidden treasure in the climate change science. Journal of Marine Science: Research & Development, 3(2), 1–14. https://doi.org/10.4172/2155-9910.1000e116
Mitra, A. (2013b). Sensitivity of mangrove ecosystem to changing climate. Springer. https://doi.org/10.1007/978-81-322-1509-7
Mitra, A. (2019). Estuarine pollution in the lower Gangetic Delta. Springer International Publishing. https://doi.org/10.1007/978-3-319-93305-4
Mitra, A. (2000). The northeast coast of the Bay of Bengal and Deltaic Sundarbans. In C. Sheppard (Ed.), Seas at the Millennium – An environmental evaluation (p. 62). Elsevier Science.
Mitra, A. (2020). Mangrove forests in India. Springer International Publishing. https://doi.org/10.1007/978-3-030-20595-9
Mitra, A., & Choudhury, A. (1992). Trace metals in macrobenthic molluscs of the Hooghly estuary, India. Marine Pollution Bulletin, 26(9), 521–522. https://doi.org/10.1016/0025-326X(93)90471-U
Mitra, A., & Choudhury, A. (1993). Heavy metal concentrations in oysters Crassostrea cucullata of sagar Island, India. Indian Journal of Environmental Health, 35, 139–141.
Mitra, A., & Ghosh, R. (2014). Bioaccumulation pattern of heavy metals in commercially important fishes in and around Indian Sundarbans. Global Journal of Animal Scientific Research, 2(1), 33–44.
Mitra, A., & Zaman, S. (2014). Carbon sequestration by coastal floral community. TERI Press.
Mitra, A., & Zaman, S. (2015). Blue carbon reservoir of the blue planet. Springer. https://doi.org/10.1007/978-81-322-2107-4
Mitra, A., & Zaman, S. (2016). Threats to marine and estuarine ecosystems. In Basics of marine and estuarine ecology (pp. 365–417). Springer. https://doi.org/10.1007/978-81-322-2707-6
Mitra, A., & Zaman, S. (2020). Environmental Science – A ground zero observation on the Indian subcontinent. Springer International Publishing. https://doi.org/10.1007/978-3-030-49131-4
Mitra, A., Chakraborty, R., Sengupta, K., & Banerjee, K. (2011). Effects of various cooking processes on the concentrations of heavy metals in common finfish and shrimps of the River Ganga. National Academy of Science Letters, 34(3), 161–168.
Mitra, A., Nayak, B., Pramanick, P., Roy, M., Chakraborty, S., Banerjee, K., Amin, G., & Zaman, S. (2014). Heavy metal accumulation in a mangrove associate species Ipomoea pes-caprae in and around the World Heritage Site of Indian Sundarbans. Journal of Environmental Science, Computer Science and Engineering & Technology, 4, 1–7.
Mitra, A., Trivedi, S., & Choudhury, A. (1994). Inter-relationship between trace metal pollution and physico-chemical variables in the frame work of Hooghly estuary. Indian Ports, 2, 27–35.
Mukherjee, P., Mitra, A., & Roy, M. (2019). Halomonas rhizobacteria of Avicennia marina of Indian Sundarbans promote rice growth under saline and heavy metal stresses through exopolysaccharide production. Frontiers in Microbiology, 10, 1–18. https://doi.org/10.3389/fmicb.2019.01207
Nascimento, C. W. A. D., & Xing, B. (2006). Phytoextraction: A review on enhanced metal availability and plant accumulation. Scientia Agricola, 63(3), 299–311. https://doi.org/10.1590/S0103-90162006000300014
Naskar, K., & Mandal, R. (1999). Ecology and biodiversity of Indian mangroves. Daya Publishing House.
Nath, D., Misra, R. N., & Karmakar, H. C. (2004). The Hooghly estuarine system – Ecological flux, fishery resources and production potential (Bulletin No. 130). Central Inland Fisheries Research Institute. http://www.cifri.res.in/Bulletins/Bulletin%20No.130.pdf
Singh, D., Buhmann, A. K., Flowers, T. J., Seal, C. E., & Papenbrock, J. (2014). Salicornia as a crop plant in temperate regions: Selection of genetically characterized ecotypes and optimization of their cultivation conditions. AoB Plants, 6, plu071. https://doi.org/10.1093/aobpla/plu071
Smillie, C. (2015). Salicornia spp. as a biomonitor of Cu and Zn in salt marsh sediments. Ecological Indicators, 56, 70–78. https://doi.org/10.1016/j.ecolind.2015.03.010
Tanaka, T., & Nakao, S. (1976). Tanaka’s cyclopaedia of edible plants of the world. Keigaku Publishing Co.
Tripathi, R. D., Tripathi, P., Dwivedi, S., Kumar, A., Mishra, A., Chauhan, P. S., Norton, G. J., & Nautiyal, C. S. (2014). Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics, 6(10), 1789–1800. https://doi.org/10.1039/C4MT00111G
Trivedi, S., Mitra, A., Bag, M., Ghosh, I., & Choudhury, A. (1995). Heavy metal concentrations in mud skipper Boleophthalmus boddaerti of Nayachar Island, India. Indian Journal of Environmental Health, 37(1), 42–45.
Trivedi, S., Zaman, S., Chaudhuri, T. R., Pramanick, P., Fazli, P., Amin, G., & Mitra, A. (2016). Inter-annual variation of salinity in Indian Sundarbans. Indian Journal of Geo-Marine Sciences, 45(3), 410–415.
Wetson, A. M., Zorb, C., John, E. A., & Flowers, T. J. (2012). High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis. Annals of Botany, 109(5), 1027–1036. https://doi.org/10.1093/aob/mcs014
Yamamoto, K., Oguri, S., Chiba, S., & Momonoki, Y. S. (2009). Molecular cloning of acetylcholinesterase gene from Salicornia europaea L. Plant Signaling and Behaviour, 4(5), 361–366. https://doi.org/10.4161/psb.4.5.8360
Zhao, G., Cheng, J., Sun, N., Ma, C., & Dai, M. (2019). Two endophytic bacterial strains modulate Mn oxidation and accumulation in the wetland plant Suaeda salsa pall. Plant and Soil, 438(1–2), 223–237. https://doi.org/10.1007/s11104-019-04019-8
Banerjee, K., Roy Chowdhury, M., Sengupta, K., Sett, S., & Mitra, A. (2012). Influence of anthropogenic and natural factors on the mangrove soil of Indian Sundarbans wetland. Archives of Environmental Science, 6, 80–91.
Bighiu, M. A., Eriksson-Wiklund, A. K., & Eklund, B. (2017). Biofouling of leisure boats as a source of metal pollution. Environmental Science and Pollution Research International, 24, 997–1006. https://doi.org/10.1007/s11356-016-7883-7
Blute, N. K., Brabander, D. J., Hemond, H. F., Sutton, S. R., Newville, M. G., & Rivers, M. L. (2004). Arsenic sequestration by ferric iron plaque on cattail roots. Environmental Science & Technology, 38, 6074–6077. https://doi.org/10.1021/es049448g
Caçador, I., Caetano, M., Duarte, B., & Vale, C. (2009). Stock and losses of trace metals from salt marsh plants. Marine Environmental Research, 67(2), 75–82. https://doi.org/10.1016/j.marenvres.2008.11.004
Chakraborty, S., Rudra, T., Guha, A., Ray, A., Pal, N., & Mitra, A. (2016). Spatial variation of heavy metals in Tenualosa ilisha muscle: A case study from the lower Gangetic delta and coastal West Bengal. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 1–14.
Chakraborty, S., Trivedi, S., Fazli, P., Zaman, S., & Mitra, A. (2014a). Avicennia alba: An indicator of heavy metal pollution in Indian Sundarban estuaries. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 1796–1807.
Chakraborty, S., Zaman, S., Fazli, P., & Mitra, A. (2014b). Spatial variations of dissolved zinc, copper and lead as influenced by anthropogenic factors in estuaries of Indian Sundarbans. Journal of Environmental Science, Computer Science and Engineering & Technology, 3(4), 182–189.
Chaudhuri, A. B., & Choudhury, A. (1994). Mangroves of the Sundarbans. Vol. 1: India. International Union for Conservation of Nature and Natural Resources (IUCN). https://portals.iucn.org/library/node/6855
Chowdhury, A., & Maiti, S. K. (2016). Identification of metal tolerant plant species in mangrove ecosystem by using community study and multivariate analysis: A case study from Indian Sunderban. Environmental Earth Sciences, 75, 744. https://doi.org/10.1007/s12665-016-5391-1
Essaidi, I., Brahmi, Z., Snoussi, A., Koubaier, H. B. H., Casabianca, H., Abe, N., Omri, A. E., Chaabouni, M. M., & Bouzouita, N. (2013). Phytochemical investigation of Tunisian Salicornia herbacea L., antioxidant, antimicrobial and cytochrome P450 (CYPs) inhibitory activities of its methanol extract. Food Control, 32(1), 125–133. https://doi.org/10.1016/j.foodcont.2012.11.006
Facciola, S. (1990). Cornucopia – A source book of edible plants. Kampong Publications.
Gopal, B., & Chauhan, M. (2006). Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquatic Sciences, 68(3), 338–354. https://doi.org/10.1007/s00027-006-0868-8
Hansel, C., Fendorf, S., Sutton, S., & Newville, M. (2001). Characterization of Fe plaque and associated metals on the roots of mine-waste impacted aquatic plants. Environmental Science & Technology, 35(19), 3863–3868. https://doi.org/10.1021/es0105459
Hedrick, U. P. (Ed.). (1972). Sturtevant’s edible plants of the world. Dover Publications.
Kathiresan, K., Moorthy, P., & Rajendran, N. (1994). Seedling performance of mangrove Rhizophora apiculata (Rhizophorales: Rhizophoraceae) in different environs. Indian Journal of Marine Sciences, 23(3), 168–169. http://nopr.niscair.res.in/handle/123456789/37638
Krishnamurty, K. V., Shpirt, E., & Reddy, M. (1976). Trace metal extraction of soils and sediments by nitric acid and hydrogen peroxide. Atomic Absorption Newsletter, 15, 68–71.
Kunkel, G. (1984). Plants for human consumption. Koeltz Scientific Books.
MacFarlane, G. R. (2002). Leaf biochemical parameters in Avicennia marina (Forsk.) Vierh as potential biomarkers of heavy metal stress in estuarine ecosystems. Marine Pollution Bulletin, 44(3), 244–256. https://doi.org/10.1016/S0025-326X(01)00255-7
Malo, B. A. (1977). Partial extraction of metals from aquatic sediments. Environmental Science & Technology, 11(3), 277–282. https://doi.org/10.1021/es60126a007
Mitra, A. (1998). Status of coastal pollution in West Bengal with special reference to heavy metals. Journal of Indian Ocean Studies, 5, 135–138.
Mitra, A. (2013a). Blue carbon: A hidden treasure in the climate change science. Journal of Marine Science: Research & Development, 3(2), 1–14. https://doi.org/10.4172/2155-9910.1000e116
Mitra, A. (2013b). Sensitivity of mangrove ecosystem to changing climate. Springer. https://doi.org/10.1007/978-81-322-1509-7
Mitra, A. (2019). Estuarine pollution in the lower Gangetic Delta. Springer International Publishing. https://doi.org/10.1007/978-3-319-93305-4
Mitra, A. (2000). The northeast coast of the Bay of Bengal and Deltaic Sundarbans. In C. Sheppard (Ed.), Seas at the Millennium – An environmental evaluation (p. 62). Elsevier Science.
Mitra, A. (2020). Mangrove forests in India. Springer International Publishing. https://doi.org/10.1007/978-3-030-20595-9
Mitra, A., & Choudhury, A. (1992). Trace metals in macrobenthic molluscs of the Hooghly estuary, India. Marine Pollution Bulletin, 26(9), 521–522. https://doi.org/10.1016/0025-326X(93)90471-U
Mitra, A., & Choudhury, A. (1993). Heavy metal concentrations in oysters Crassostrea cucullata of sagar Island, India. Indian Journal of Environmental Health, 35, 139–141.
Mitra, A., & Ghosh, R. (2014). Bioaccumulation pattern of heavy metals in commercially important fishes in and around Indian Sundarbans. Global Journal of Animal Scientific Research, 2(1), 33–44.
Mitra, A., & Zaman, S. (2014). Carbon sequestration by coastal floral community. TERI Press.
Mitra, A., & Zaman, S. (2015). Blue carbon reservoir of the blue planet. Springer. https://doi.org/10.1007/978-81-322-2107-4
Mitra, A., & Zaman, S. (2016). Threats to marine and estuarine ecosystems. In Basics of marine and estuarine ecology (pp. 365–417). Springer. https://doi.org/10.1007/978-81-322-2707-6
Mitra, A., & Zaman, S. (2020). Environmental Science – A ground zero observation on the Indian subcontinent. Springer International Publishing. https://doi.org/10.1007/978-3-030-49131-4
Mitra, A., Chakraborty, R., Sengupta, K., & Banerjee, K. (2011). Effects of various cooking processes on the concentrations of heavy metals in common finfish and shrimps of the River Ganga. National Academy of Science Letters, 34(3), 161–168.
Mitra, A., Nayak, B., Pramanick, P., Roy, M., Chakraborty, S., Banerjee, K., Amin, G., & Zaman, S. (2014). Heavy metal accumulation in a mangrove associate species Ipomoea pes-caprae in and around the World Heritage Site of Indian Sundarbans. Journal of Environmental Science, Computer Science and Engineering & Technology, 4, 1–7.
Mitra, A., Trivedi, S., & Choudhury, A. (1994). Inter-relationship between trace metal pollution and physico-chemical variables in the frame work of Hooghly estuary. Indian Ports, 2, 27–35.
Mukherjee, P., Mitra, A., & Roy, M. (2019). Halomonas rhizobacteria of Avicennia marina of Indian Sundarbans promote rice growth under saline and heavy metal stresses through exopolysaccharide production. Frontiers in Microbiology, 10, 1–18. https://doi.org/10.3389/fmicb.2019.01207
Nascimento, C. W. A. D., & Xing, B. (2006). Phytoextraction: A review on enhanced metal availability and plant accumulation. Scientia Agricola, 63(3), 299–311. https://doi.org/10.1590/S0103-90162006000300014
Naskar, K., & Mandal, R. (1999). Ecology and biodiversity of Indian mangroves. Daya Publishing House.
Nath, D., Misra, R. N., & Karmakar, H. C. (2004). The Hooghly estuarine system – Ecological flux, fishery resources and production potential (Bulletin No. 130). Central Inland Fisheries Research Institute. http://www.cifri.res.in/Bulletins/Bulletin%20No.130.pdf
Singh, D., Buhmann, A. K., Flowers, T. J., Seal, C. E., & Papenbrock, J. (2014). Salicornia as a crop plant in temperate regions: Selection of genetically characterized ecotypes and optimization of their cultivation conditions. AoB Plants, 6, plu071. https://doi.org/10.1093/aobpla/plu071
Smillie, C. (2015). Salicornia spp. as a biomonitor of Cu and Zn in salt marsh sediments. Ecological Indicators, 56, 70–78. https://doi.org/10.1016/j.ecolind.2015.03.010
Tanaka, T., & Nakao, S. (1976). Tanaka’s cyclopaedia of edible plants of the world. Keigaku Publishing Co.
Tripathi, R. D., Tripathi, P., Dwivedi, S., Kumar, A., Mishra, A., Chauhan, P. S., Norton, G. J., & Nautiyal, C. S. (2014). Roles for root iron plaque in sequestration and uptake of heavy metals and metalloids in aquatic and wetland plants. Metallomics, 6(10), 1789–1800. https://doi.org/10.1039/C4MT00111G
Trivedi, S., Mitra, A., Bag, M., Ghosh, I., & Choudhury, A. (1995). Heavy metal concentrations in mud skipper Boleophthalmus boddaerti of Nayachar Island, India. Indian Journal of Environmental Health, 37(1), 42–45.
Trivedi, S., Zaman, S., Chaudhuri, T. R., Pramanick, P., Fazli, P., Amin, G., & Mitra, A. (2016). Inter-annual variation of salinity in Indian Sundarbans. Indian Journal of Geo-Marine Sciences, 45(3), 410–415.
Wetson, A. M., Zorb, C., John, E. A., & Flowers, T. J. (2012). High phenotypic plasticity of Suaeda maritima observed under hypoxic conditions in relation to its physiological basis. Annals of Botany, 109(5), 1027–1036. https://doi.org/10.1093/aob/mcs014
Yamamoto, K., Oguri, S., Chiba, S., & Momonoki, Y. S. (2009). Molecular cloning of acetylcholinesterase gene from Salicornia europaea L. Plant Signaling and Behaviour, 4(5), 361–366. https://doi.org/10.4161/psb.4.5.8360
Zhao, G., Cheng, J., Sun, N., Ma, C., & Dai, M. (2019). Two endophytic bacterial strains modulate Mn oxidation and accumulation in the wetland plant Suaeda salsa pall. Plant and Soil, 438(1–2), 223–237. https://doi.org/10.1007/s11104-019-04019-8