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Accumulation and Tolerance of Mangroves to Heavy Metals: a Review

  • Sediment Pollution (P Zhang, Section Editor)
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Abstract

Purpose of review

Mangroves are under increasing heavy metal (HM) pollution pressure from human activities because of the rapid industrialization and urbanization in coastal areas. Field and laboratory experiments showed that the tolerance of mangrove plants to HM stress is normally a mixture of metal avoidance and scavenging of reactive oxygen species (ROS). In this review, related studies during the past few decades on the accumulation and tolerance of mangrove to HMs have been synthesized.

Recent findings

In mangroves, metal accumulation mainly occurred at the root level with restricted transport to the aerial portions of the plant. The common founded HMs, such as copper, zinc, cadmium, chromium, and mercury, generally showed high bioconcentration factor in roots, while the concentration factors for these metals in leaves were usually much lower than one. The limited translocation of the toxic metals to the aerial parts renders the mangrove plants a high endurance ability to high levels of HM stress. To protect the cellular components from oxidative damage by HMs, mangroves have developed both enzymatic and nonenzymatic antioxidant mechanisms to scavenge the ROS. In some circumstances, the changes of antioxidative enzyme activity were usually in accordance with the changes of toxic metal concentrations in plant tissues. However, the responses of antioxidative enzymes in mangroves to HM stress varied with plant species, metal type, and concentration, as well as the duration of the treatment time.

Summary

More toxicity tests are needed with early life stages of mangroves to determine threshold effect concentrations under more realistic conditions.

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References

  1. Caregnato FF, Koller CE, MacFarlane GR, Moreira JC. The glutathione antioxidant system as a biomarker suite for the assessment of heavy metal exposure and effect in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull. 2008;56(6):1119–27.

    Article  CAS  Google Scholar 

  2. Sun Z, Chen J, Wang X, Lv C. Heavy metal accumulation in native plants at a metallurgy waste site in rural areas of Northern China. Ecol Eng. 2016;86:60–8.

    Article  Google Scholar 

  3. Zhang Q, Yan C, Liu J, Lu H, Duan H, Du J, et al. Silicon alleviation of cadmium toxicity in mangrove (Avicennia marina) in relation to cadmium compartmentation. J Plant Growth Regul. 2014b;33(2):233–42.

    Article  CAS  Google Scholar 

  4. Zhang ZW, Xu XR, Sun YX, Yu S, Chen YS, Peng JX. Heavy metal and organic contaminants in mangrove ecosystems of China: a review. Environ Sci Pollut Res. 2014a;21(20):11938–50.

    Article  CAS  Google Scholar 

  5. Harbison PA. Mangrove muds—a sink and a source for trace metals. Mar Pollut Bull. 1986;17(6):246–50.

    Article  CAS  Google Scholar 

  6. Tomlinson PB. The botany of mangroves: Cambridge University Press; 1986.

  7. Tam NF. Pollution studies on mangroves in Hong Kong and mainland China. In: The environment in Asia Pacific harbours. Netherlands: Springer; 2006. p. 147–63.

    Chapter  Google Scholar 

  8. Tam NF, Wong YS. Mangrove soils as sinks for wastewater-borne pollutants. In: Asia-Pacific symposium on mangrove ecosystems. Netherlands: Springer; 1995a. p. 231–41.

    Chapter  Google Scholar 

  9. Tam NF, Wong YS. Spatial and temporal variations of heavy metal contamination in sediments of a mangrove swamp in Hong Kong. Mar Pollut Bull. 1995b;31(4–12):254–61.

    Article  CAS  Google Scholar 

  10. Wu Q, Zhou H, Tam NF, Tian Y, Tan Y, Zhou S, et al. Contamination, toxicity and speciation of heavy metals in an industrialized urban river: implications for the dispersal of heavy metals. Mar Pollut Bull. 2016;104(1):153–61.

    Article  CAS  Google Scholar 

  11. Tam NF, Wong YS. Retention of nutrients and heavy metals in mangrove sediment receiving wastewater of different strengths. Environ Technol. 1993;14(8):719–29.

    Article  CAS  Google Scholar 

  12. Lacerda LD, Carvalho CE, Tanizaki KF, Ovalle AR, Rezende CE. The biogeochemistry and trace metals distribution of mangrove rhizospheres. Biotropica. 1993:252–7.

  13. Silva CA, Lacerda LD, Rezende CE. Metals reservoir in a red mangrove forest. Biotropica. 1990;22(4):339–45.

    Article  Google Scholar 

  14. Stigliani WM. Global perspectives and risk assessment. In: Salomons W, Stigliani WM (Eds), Biogeodynamics of Pollutants in Soil and Sediments. Berlin: Springer Verlag; 1995. pp. 331–343.

  15. Clark MW, McConchie D, Saenger P, Pillsworth M. Hydrological controls on copper, cadmium, lead and zinc concentrations in an anthropogenically polluted mangrove ecosystem, Wynnum, Brisbane, Australia. J Coastal Res. 1997;13:1150–1158.

  16. Spratt HG Jr, Hodson RE. The effect of changing water chemistry on rates of manganese oxidation in surface sediments of a temperate salt marsh and a tropical mangrove estuary. Estuar Coast Shelf S. 1994;38:119–135.

  17. Peters EC, Gassman NJ, Firman JC, Richmond RH, Power EA. Ecotoxicology of tropical marine ecosystems. Environ Toxicol Chem. 1997;16(1):12–40.

    Article  CAS  Google Scholar 

  18. Sruthi P, Shackira AM, Puthur JT. Heavy metal detoxification mechanisms in halophytes: an overview. Wetl Ecol Manag. 2017;25:1–20.

    Article  CAS  Google Scholar 

  19. MacFarlane GR. Leaf biochemical parameters in Avicennia marina (Forsk.) Vierh as potential biomarkers of heavy metal stress in estuarine ecosystems. Mar Pollut Bull. 2002;44(3):244–56.

    Article  CAS  Google Scholar 

  20. Zhang FQ, Wang YS, Lou ZP, Dong JD. Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere. 2007;67(1):44–50.

    Article  CAS  Google Scholar 

  21. MacFarlane GR, Koller CE, Blomberg SP. Accumulation and partitioning of heavy metals in mangroves: a synthesis of field-based studies. Chemosphere. 2007;69(9):1454–64.

    Article  CAS  Google Scholar 

  22. Wang WQ, Ke L, Tam N, Wong YS. Changes in the main osmotica during the development of Kandelia candel hypocotyls and after mature hypocotyls were transplanted in solutions with different salinities. Mar Biol. 2002;141(6):1029–34.

    Article  CAS  Google Scholar 

  23. Yan Z, Wang W, Tang D. Effect of different time of salt stress on growth and some physiological processes of Avicennia marina seedlings. Mar Biol. 2007;152(3):581–7.

    Article  CAS  Google Scholar 

  24. Prasad MBK, Ramanathan AL, Shrivastav SK, Anshumali RS. Metal fractionation studies in surfacial and core sediments in the Achankovil river basin in India. Environ Monitor Assess. 2006;21:77–102.

    Article  CAS  Google Scholar 

  25. Schützendübel A, Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot. 2002;53(372):1351–65.

    Google Scholar 

  26. Vangronsveld J, Clijsters H. Toxic effects of metals. In: Farago ME, editor. Plants and the chemical elements. Weinheim: VCH Verlagsgesellschaft; 1994.

    Google Scholar 

  27. Lu H, Liu B, Zhang Y, Ye J, Yan C. Comparing analysis of elements sub-cellular distribution in Kandelia obovata between SEM-EDX and chemical extraction. Aquat Bot. 2014;112:10–5.

    Article  CAS  Google Scholar 

  28. Naidoo G, Hiralal T, Naidoo Y. Ecophysiological responses of the mangrove Avicennia marina to trace metal contamination. Flora. 2014;209(1):63–72.

    Article  Google Scholar 

  29. Thomas C, Eong OJ. Effects of the heavy metals Zn and Pb on R. mucronata and A. alba seedlings. In: Soepadmo E, Rao AM, MacIntosh MD, editors. Proceedings of the Asian symposium on mangroves and environment: research and management. ISME, Malaysia. 1984.

  30. Chiu CY, Hsiu FS, Chen SS, Chou CH. Reduced toxicity of Cu and Zn to mangrove seedlings (Kandelia candel (L.) Druce.) in saline environments. Bot Bull Acad Sinica. 1995;36(1):19–24.

    CAS  Google Scholar 

  31. Nguyen KL, Nguyen HA, Richter O, Pham MT, Nguyen VP. Ecophysiological responses of young mangrove species Rhizophora apiculata (Blume) to different chromium contaminated environments. Sci Total Environ. 2017;574:369–80.

    Article  CAS  Google Scholar 

  32. MacFarlane GR, Burchett MD. Toxicity, growth and accumulation relationships of copper, lead and zinc in the grey mangrove Avicennia marina (Forsk.) Vierh. Mar Environ Res. 2002;54(1):65–84.

    Article  CAS  Google Scholar 

  33. Yan ZZ, Ke L, Tam NF. Lead stress in seedlings of Avicennia marina, a common mangrove species in South China, with and without cotyledons. Aquat Bot. 2010;92(2):112–28.

    Article  CAS  Google Scholar 

  34. Cheng H, Tam NF, Wang Y, Li S, Chen G, Ye Z. Effects of copper on growth, radial oxygen loss and root permeability of seedlings of the mangroves Bruguiera gymnorrhiza and Rhizophora stylosa. Plant Soil. 2012;359(1–2):255–66.

    Article  CAS  Google Scholar 

  35. Macfarlane GR, Burchett MD. Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the grey mangrove, Avicennia marina (Forsk.) Vierh. Mar Pollut Bull. 2001;42(3):233–40.

    Article  CAS  Google Scholar 

  36. Yan Z, Li X, Chen J, Tam NF. Combined toxicity of cadmium and copper in Avicennia marina seedlings and the regulation of exogenous jasmonic acid. Ecotoxicol Environ Safe. 2015;113:124–32.

    Article  CAS  Google Scholar 

  37. Huang GY, Wang YS. Physiological and biochemical responses in the leaves of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza) exposed to multiple heavy metals. J Hazard Mater. 2010;182(1):848–54.

    Article  CAS  Google Scholar 

  38. Yadav A, Ram A, Majithiya D, Salvi S, Sonavane S, Kamble A, et al. Effect of heavy metals on the carbon and nitrogen ratio in Avicennia marina from polluted and unpolluted regions. Mar Pollut Bull. 2015;101(1):359–65.

    Article  CAS  Google Scholar 

  39. Rovai AS, Barufi JB, Pagliosa PR, Scherner F, Torres MA, Horta PA, et al. Photosynthetic performance of restored and natural mangroves under different environmental constraints. Environ Pollut. 2013;181:233–41.

    Article  CAS  Google Scholar 

  40. Kozlowski TT, Pallardy SG. Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev. 2002;68:270–334.

  41. Shu X, Yin L, Zhang Q, Wang W. Effect of Pb toxicity on leaf growth, antioxidant enzyme activities, and photosynthesis in cuttings and seedlings of Jatropha curcas L. Environ Sci Pollut Res Inter. 2012;19:893–902.

    Article  CAS  Google Scholar 

  42. Yan Z, Tam NF. Effects of lead stress on anti-oxidative enzymes and stress-related hormones in seedlings of Excoecaria agallocha Linn. Plant Soil. 2013a;367(1–2):327–238.

    Article  CAS  Google Scholar 

  43. Yan Z, Tam NF. Differences in lead tolerance between Kandelia obovata and Acanthus ilicifolius seedlings under varying treatment times. Aquat Toxicol. 2013b;126:154–62.

    Article  CAS  Google Scholar 

  44. Rahman MM, Chongling Y, Rahman MM, Islam KS. Accumulation, distribution and toxicological effects induced by chromium on the development of mangrove plant Kandelia candel (L.) Druce. Ambiente e Agua-An Interdiscipl J Appl Sci. 2009 Apr 23;4(1):6–19.

    Article  Google Scholar 

  45. Cheng H, Liu Y, Tam NF, Wang X, Li SY, Chen GZ, et al. The role of radial oxygen loss and root anatomy on zinc uptake and tolerance in mangrove seedlings. Environ Pollut. 2010;158(5):1189–96.

    Article  CAS  Google Scholar 

  46. Walsh GE, Ainsworth KA, Rigby R. Resistance of red mangrove (Rhizophora mangle L.) seedlings to lead, cadmium, and mercury. Biotropica. 1979;1:22–7.

    Article  Google Scholar 

  47. Tao Y, Chen Y, Liang S, Liang Y. Physiological and biochemical properties of Bruguiera Gymnorrhiza seedlings under cadmium stress. Chinese J Ecol. 2008;27:762–6.

    CAS  Google Scholar 

  48. Yang S, Wu Q. Effect of cd on growth and physiological characteristics of Aegiceras conrniculatum seedlings. Mar Environ Sci. 2002;22(1):38–42.

    CAS  Google Scholar 

  49. Chen RH, Lin P. Influence of mercury and salinity on the growth of seedlings of three mangrove species. Universit Amoi Acta Scienti Natural. 1988;27:110–5.

    CAS  Google Scholar 

  50. Rocha AC, Canal EC, Campostrini E, Reis FO, Cuzzuol GR. Influence of chromium in Laguncularia racemosa (L). Gaertn f. physiology. Brazil J Plant Physiol. 2009;21(2):87–94.

    Article  Google Scholar 

  51. Lacerda LD. Trace metals biogeochemistry and diffuse pollution in mangrove ecosystems. ISME Mangrov Ecosys Occasional Papers. 1998;2:1–61.

    Google Scholar 

  52. Chiu CY, Chou CH. The distribution and influence of heavy metals in mangrove forests of the Tamshui estuary in Taiwan. Soil Sci Plant Nut. 1991;37(4):659–69.

    Article  CAS  Google Scholar 

  53. Baker AJ, Walker PL. Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ, editor. Heavy metal tolerance in plants: evolutionary aspects. Boca Raton: CRC Press; 1989. p. 155–76.

    Google Scholar 

  54. Tam NF, Li SH, Lan CY, Chen GZ, Li MS, Wong YS. Nutrients and heavy metal contamination of plants and sediments in Futian mangrove forest. Hydrobiologia. 1995;295(1):149–58.

    Article  CAS  Google Scholar 

  55. Zheng WJ, Lin P. Accumulation and distribution of cu, Pb, Zn and cd in Avicennia marina mangrove community of Futian in Shenzhen. Oceanol Limnol Sin. 1996;27:386–93.

    CAS  Google Scholar 

  56. Ding ZH, Liu JL, Li LQ, Lin HN, Wu H, Hu ZZ. Distribution of Hg in mangrove plants and correlation with Hg speciation in sediments. Environ Sci. 2010;31:2234–9. (in Chinese)

    Google Scholar 

  57. Wang Y, Qiu Q, Xin G, Yang Z, Zheng J, Ye Z, et al. Heavy metal contamination in a vulnerable mangrove swamp in South China. Environ Monitor Assess. 2013;185(7):5775–87.

    Article  CAS  Google Scholar 

  58. Zheng WJ, Chen XY, Lin P. Accumulation and biological cycling of heavy metal elements in Rhizophora stylosa mangroves in Yingluo Bay. China Mar Ecol Prog Ser. 1997;159:293–30.

    Article  CAS  Google Scholar 

  59. Nath B, Chaudhuri P, Birch GF. Assessment of biotic response to heavy metal contamination in Avicennia marina mangrove ecosystems in Sydney Estuary. Australia Ecotoxicol Environ Safe. 2014;107:284–90.

    Article  CAS  Google Scholar 

  60. Ong Che RG. Concentration of 7 heavy metals in sediments and mangrove root samples from Mai Po. Hong Kong Mar Pollut Bull. 1999;39:269–79.

    Article  Google Scholar 

  61. Sarangi RK, Kathiresan K, Subramanian AN. Metal concentrations in five mangrove species of the Bhitarkanika, Orissa, east coast of India. Indian J Mar Sci. 2002;31:251–3.

    CAS  Google Scholar 

  62. Sadiq M, Zaidi TH. Sediment composition and metal concentrations in mangrove leaves from the Saudi coast of the Arabian Gulf. Sci Total Environ. 1994;155(1):1–8.

    Article  CAS  Google Scholar 

  63. Harish SR, Murugan K. Oxidative stress indices in natural populations of Avicennia alba Blume. as biomarker of environmental pollution. Environ Res. 2011;111(8):1070–3.

    Article  CAS  Google Scholar 

  64. Weng B, Xie X, Weiss DJ, Liu J, Lu H, Yan C. Kandelia obovata (S., L.) Yong tolerance mechanisms to cadmium: subcellular distribution, chemical forms and thiol pools. Mar Pollut Bull. 2012;64(11):2453–60.

    Article  CAS  Google Scholar 

  65. MacFarlane GR, Burchett MD. Cellular distribution of copper, lead and zinc in the grey mangrove, Avicennia marina (Forsk.) Vierh. Aquat Bot. 2000;68(1):45–59.

    Article  CAS  Google Scholar 

  66. Zan Q, Wang Y, Wang B. Accumulation and cycle of heavy metals in Sonneratia apetala and S. caseolaris mangrove community at Futian of Shenzhen, China. Environ Sci. 2002;23:81–8. (in Chinese)

    CAS  Google Scholar 

  67. Chaudhuri P, Nath B, Birch G. Accumulation of trace metals in grey mangrove Avicennia marina fine nutritive roots: the role of rhizosphere processes. Mar Pollut Bull. 2014;79(1):284–92.

    Article  CAS  Google Scholar 

  68. Saenger P, McConchie D, Clark M. Mangrove forests as a buffer zone between anthropogenically polluted areas and the sea. In: Saenger P, editors, Proceedings 1990 CZM Workshop. Yeppoon.

  69. Harmens H, Den Hartog PR, Bookum WM, Verkleij JA. Increased zinc tolerance in Silene vulgaris (Moench) Garcke is not due to increased production of phytochelatins. Plant Physiol. 1993;103(4):1305–9.

    Article  CAS  Google Scholar 

  70. Marchand C, Fernandez JM, Moreton B. Trace metal geochemistry in mangrove sediments and their transfer to mangrove plants (New Caledonia). Sci Total Environ. 2016;562:216–27.

    Article  CAS  Google Scholar 

  71. Han W, Zhao Y, Lu C, Lin P. Seven metal elements’ biological accumulation and circulation of Sonneratia apetala plantation in Leizhou. Guangdong Chin J Appl Environ Biol. 2004;10:27–34. (in Chinese)

    Google Scholar 

  72. Liang Y, Liu X, Yuan D, Gong Z. Characteristics of total mercury in different Kandelia candel tissues of Fugong mangrove forest reserve at estuary of Jiulongjiang. Trans Oceanol Limnol. 2011;3:83–8. (in Chinese)

    Google Scholar 

  73. Zhou YW, Peng YS, Li XL, Chen GZ. Accumulation and partitioning of heavy metals in mangrove rhizosphere sediments. Environ Earth Sci. 2011;64(3):799–807.

    Article  CAS  Google Scholar 

  74. Ding Z, Wu H, Feng X, Liu J, Liu Y, Yuan Y, et al. Distribution of Hg in mangrove trees and its implication for Hg enrichment in the mangrove ecosystem. Appl Geochem. 2011;26:205–12.

    Article  CAS  Google Scholar 

  75. Du J, Yan C, Li Z. Formation of iron plaque on mangrove Kandelia obovata (SL) root surfaces and its role in cadmium uptake and translocation. Mar Pollut Bull. 2013;74(1):105–9.

    Article  CAS  Google Scholar 

  76. Smolders AJP, Roelofs JGM. The roles of internal iron hydroxide precipitation, sulphide toxicity and oxidizing ability in the survival of Stratiotes aloides roots at different iron concentrations in sediment pore water. New Phytol. 1996;133(2):253–60.

    Article  CAS  Google Scholar 

  77. Pi N, Tam NF, Wong MH. Formation of iron plaque on mangrove roots receiving wastewater and its role in immobilization of wastewater-borne pollutants. Mar Pollut Bull. 2011;63(5):402–11.

    Article  CAS  Google Scholar 

  78. Machado W, Gueiros BB, Lisboa-Filho SD, Lacerda LD. Trace metals in mangrove seedlings: role of iron plaque formation. Wetl Ecol Manag. 2005;13(2):199–206.

    Article  CAS  Google Scholar 

  79. Chiu CY, Chou CH. Oxidation in the rhizosphere of mangrove Kandelia candel seedlings, Soil Sci Plant Nutr. 1993;39(4):725–731.

  80. Armstrong J, Armstrong W, Beckett PM. Phragmites australis: ventuir-and hunmidity-induced pressure flows enhance rhizome aeration and rhizosphere oxidation. New Phytol. 1992;120;197–207.

  81. Otte ML, Dekkers IM, Rozema J, Broekman RA. Uptake of arsenic by Aster tripolium in relation to rhizosphere oxidation. Can J Bot. 1991;69(12):2670–7.

  82. Moller CL, Sandjensen K. Iron plaques improve the oxygen supply to root meristems of the freshwater plant, Lobelia dortmanna. New Phytol. 2008;179(3):848–56.

    Article  CAS  Google Scholar 

  83. Pi N, Tam NF, Wong MH. Effects of wastewater discharge on formation of Fe plaque on root surface and radial oxygen loss of mangrove roots. Environ Pollut. 2010;158(2):381–7.

    Article  CAS  Google Scholar 

  84. Pi N, Tam NF, Wu Y, Wong MH. Root anatomy and spatial pattern of radial oxygen loss of eight true mangrove species. Aquat Bot. 2009;90(3):222–30.

    Article  Google Scholar 

  85. Liu Y, Tam NF, Yang JX, Pi N, Wong MH, Ye ZH. Mixed heavy metals tolerance and radial oxygen loss in mangrove seedlings. Mar Pollut Bull. 2009;58(12):1843–9.

    Article  CAS  Google Scholar 

  86. Cobbett CS. Phytochelatins and their roles in heavy metal detoxification. Plant Physiol. 2000;123(3):825–832.

  87. Cobbett C, Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol. 2003;53(1):159–82.

    Article  CAS  Google Scholar 

  88. Mejare M, Bulow L. Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals. Trends Biotechnol. 2001;19(2):67–73.

    Article  CAS  Google Scholar 

  89. Chen J, Yan Z, Li X. Effect of methyl jasmonate on cadmium uptake and antioxidative capacity in Kandelia obovata seedlings under cadmium stress. Ecotoxicol Environ Saf. 2014 Jun 30;104:349–56.

    Article  CAS  Google Scholar 

  90. Gonzalez-Mendoza D, Moreno AQ, Zapata-Perez O. Coordinated responses of phytochelatin synthase and metallothionein genes in black mangrove, Avicennia germinans, exposed to cadmium and copper. Aquat Toxicol. 2007;83(4):306–14.

    Article  CAS  Google Scholar 

  91. Huang GY, Wang YS. Expression analysis of type 2 metallothionein gene in mangrove species (Bruguiera gymnorrhiza) under heavy metal stress. Chemosphere. 2009;77(7):1026–9.

    Article  CAS  Google Scholar 

  92. Huang GY, Wang YS, Ying GG, Dang AC. Analysis of type 2 metallothionein gene from mangrove species (Kandelia candel). Trees. 2012;26(5):1537–44.

    Article  CAS  Google Scholar 

  93. Xiang C, Oliver DJ. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell. 1998;10(9):1539–50.

    Article  CAS  Google Scholar 

  94. Maksymiec W, Wojcik M, Krupa Z. Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to cadmium and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere. 2007;66(3):421–7.

    Article  CAS  Google Scholar 

  95. Theil EC. Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu Rev Biochem. 1987;56(1):289–315.

    Article  CAS  Google Scholar 

  96. Jithesh MN, Prashanth SR, Sivaprakash KR, Parida A. Monitoring expression profiles of antioxidant genes to salinity, iron, oxidative, light and hyperosmotic stresses in the highly salt tolerant grey mangrove, Avicennia marina (Forsk.) Vierh. by mRNA analysis. Plant Cell Rep. 2006;25(8):865–76.

    Article  CAS  Google Scholar 

  97. Lavid N, Schwartz A, Yarden O, Tel-Or E. The involvement of polyphenols and peroxidase activities in heavy-metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta. 2001;212(3):323–31.

    Article  CAS  Google Scholar 

  98. Guangqiu Q, Chongling Y, Haoliang L. Influence of heavy metals on the carbohydrate and phenolics in mangrove, Aegiceras corniculatum L., seedlings. Bull Environ Contam Toxicol. 2007;78(6):440–4.

    Article  CAS  Google Scholar 

  99. Yan ZZ, Tam NF. Temporal changes of polyphenols and enzyme activities in seedlings of Kandelia obovata under lead and manganese stresses. Mar Pollut Bull. 2011;63(5):438–44.

    Article  CAS  Google Scholar 

  100. Manousaki E, Kadukova J, Kalogerakis N. Excretion of metals by the leaves of plants: a new approach to the phytoremediation of sites contaminated with heavy metals. In: Proceedings of the 10th International Conference on Environmental Science and Technology Kos island, Greece, 5–7 September 2007.

  101. Weis JS, Weis P. Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environ Inter. 2004;30(5):685–700.

    Article  CAS  Google Scholar 

  102. Drennan P, Pammenter NW. Physiology of salt excretion in the mangrove Avicennia marina (Forsk.) Vierh. New Phytol. 1982;91(4):597–606.

    Article  CAS  Google Scholar 

  103. Thompson WW. The structure and function of salt glands. In: Poljakoff-Mayber A, Gale J, editors. Plants in saline environments. New York: Springer; 1975. p. 118–46.

    Chapter  Google Scholar 

  104. MacFarlane GR, Burchett MD. Zinc distribution and excretion in the leaves of the grey mangrove, Avicennia marina (Forsk.) Vierh. Environ Exp Bot. 1999;41(2):167–75.

    Article  CAS  Google Scholar 

  105. Waisel Y, Ethel A, Sagami M. Salt balance of leaves of the mangrove Avicennia marina. Physiol Plant. 1986;67:67–72.

    Article  CAS  Google Scholar 

  106. Chowdhury R, Favas PJ, Pratas J, Jonathan MP, Ganesh PS, Sarkar SK. Accumulation of trace metals by mangrove plants in Indian Sundarban Wetland: prospects for phytoremediation. Int J Phytoremediat. 2015;17(9):885–94.

    Article  CAS  Google Scholar 

  107. Clough B. Continuing the journey amongst mangroves. ISME Mangrove Educational Book Series. 2013, pp.86

  108. Arrivabene HP, Campos CQ, da Costa SI, Wunderlin DA, Milanez CR, Machado SR. Differential bioaccumulation and translocation patterns in three mangrove plants experimentally exposed to iron. Consequences for environmental sensing. Environ Pollut. 2016;215:302–13.

    Article  CAS  Google Scholar 

  109. Thatoi HN, Patra JK, Das SK. Free radical scavenging and antioxidant potential of mangrove plants: a review. Acta Physiol Plant. 2014;36(3):561–79.

    Article  CAS  Google Scholar 

  110. Tao YM, Chen YZ, Tan T, Liu XC, Yang DL, Liang SC. Comparison of antioxidant responses to cadmium and lead in Bruguiera gymnorrhiza seedlings. Biol Plant. 2012;56(1):149–52.

    Article  CAS  Google Scholar 

  111. Sticher L, Mauch-Mani B, Métraux AJ. Systemic acquired resistance. Annu Rev Phytopathol. 1997;35(1):235–70.

    Article  CAS  Google Scholar 

  112. Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, et al. Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot. 2012;75:307–24.

    CAS  Google Scholar 

  113. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48(12):909–30.

    Article  CAS  Google Scholar 

  114. Huang GY, Wang YS, Sun CC, Dong JD, Sun ZX. The effect of multiple heavy metals on ascorbate, glutathione and related enzymes in two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Oceanol Hydrobiol St. 2010;39(1):11–25.

    Article  CAS  Google Scholar 

  115. Banerjee D, Chakrabarti S, Hazra AK, Banerjee S, Ray J, Mukherjee B. Antioxidant activity and total phenolics of some mangroves in Sundarbans. Afr J Biotechnol. 2008;7(6):805–10.

    Google Scholar 

  116. Kraus TE, Dahlgren RA, Zasoski RJ. Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil. 2003;256(1):41–66.

    Article  CAS  Google Scholar 

  117. Sakihama Y, Cohen MF, Grace SC, Yamasaki H. Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology. 2002;177(1):67–80.

    Article  CAS  Google Scholar 

  118. Shi C, Xu MJ, Bayer M, Deng ZW, Kubbutat MH, Waejen W, et al. Phenolic compounds and their anti-oxidative properties and protein kinase inhibition from the Chinese mangrove plant Laguncularia racemosa. Phytochemistry. 2010;71(4):435–42.

    Article  CAS  Google Scholar 

  119. Thakur S, Singh L, Ab Wahid Z, Siddiqui MF, Atnaw SM, Din MFM. Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess. 2016;188(4):206.

    Article  Google Scholar 

  120. Wang W. Factors affecting metal toxicity to (and accumulation by) aquatic organisms—overview. Environ Int. 1987;13:437–57.

    Article  CAS  Google Scholar 

  121. Lutts S, Lefèvre I. How can we take advantage of halophyte properties to cope with heavy metal toxicity in salt-affected areas? Ann Bot. 2015;115(3):509–28.

    Article  Google Scholar 

  122. Zhu X, Yang F, Wei C. Factors influencing the heavy metal bioaccessibility in soils were site dependent from different geographical locations. Environ Sci Pollut Res. 2015;22:13939–49.

    Article  CAS  Google Scholar 

  123. Chakraborty P, Ramteke D, Chakraborty S. Geochemical partitioning of cu and Ni in mangrove sediments: relationships with their bioavailability. Mar Pollut Bull. 2015;93(1):194–201.

    Article  CAS  Google Scholar 

  124. Greger M, Brammer E, Lindeberg S, Lisson G, Idestam-Almquist J. Uptake and physiological effects of cadmium in sugar beet (Beta vulgaris) related to mineral provision. J Exper Bot. 1991;42:729–37.

    Article  CAS  Google Scholar 

  125. Ekvall L, Greger M. Effects of environmental biomass-producing factors on Cd uptake in two Swedish ecotypes of Pinus sylvestris. Environ Pollut. 2003;121:401–11.

    Article  CAS  Google Scholar 

  126. Marschner H. Mineral nutrition of higher plants. London: Academic Press; 1995.

    Google Scholar 

  127. Tőzsér D, Magura T, Simon E. Heavy metal uptake by plant parts of willow species: a meta-analysis. J Hazard Mater. 2017;336:101–9.

    Article  CAS  Google Scholar 

  128. Acosta JA, Jansen B, Kalbitz K, Faz A, Martínez-Martínez S. Salinity increases mobility of heavy metals in soils. Chemosphere. 2011;85:1318–24.

    Article  CAS  Google Scholar 

  129. Greger M, Kautsky L, Sandberg T. A tentative model of Cd uptake in Potamogeton pectinatus in relation to salinity. Environ Exper Bot. 1995;35:215–25.

    Article  CAS  Google Scholar 

  130. Fritioff Å, Kautsky L, Greger M. Influence of temperature and salinity on heavy metal uptake by submersed plants. Environ Pollut. 2005;133(2):265–74.

    Article  CAS  Google Scholar 

  131. Pan Y, Koopmans GF, Bonten LT, Song J, Luo Y, Temminghoff EJ, et al. Temporal variability in trace metal solubility in a paddy soil not reflected in uptake by rice (Oryza sativa L.). Environ Geochem Health. 2016;38(6):1355–72.

    Article  CAS  Google Scholar 

  132. Moreno-Jiménez E, Sepúlveda R, Esteban E, Beesley L. Efficiency of organic and mineral based amendments to reduce metal [loid] mobility and uptake (Lolium perenne) from a pyrite-waste contaminated soil. J Geochem Explor. 2017;174:46–52.

    Article  CAS  Google Scholar 

  133. Santner A, Estelle M. Recent advances and emerging trends in plant hormone signalling. Nature. 2009;459(7250):1071–8.

    Article  CAS  Google Scholar 

  134. Sharma SS, Dietz K, Mimura T. Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant Cell Environ. 2016;39(5):1112–26.

    Article  CAS  Google Scholar 

  135. Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016;16(1):86.

    Article  CAS  Google Scholar 

  136. Wasternack C. Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot. 2007;100(4):681–97.

    Article  CAS  Google Scholar 

  137. Salt DE, Prince RC, Pickering IJ, Raskin I. Mechanisms of cadmium mobility and accumulation in Indian mustard. Plant Physiol. 1995;109(4):1427–33.

    Article  CAS  Google Scholar 

  138. Kanwar MK, Bhardwaj R, Arora P, Chowdhary SP, Sharma P, Kumar S. Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica Juncea L. Chemosphere. 2012;86(1):41–9.

    Article  CAS  Google Scholar 

  139. Dong Y, Wang X, Cui X. Exogenous nitric oxide involved in subcellular distribution and chemical forms of Cu2+under copper stress in tomato seedlings. J Integrat Agricul. 2013;12(10):1783–90.

    Article  Google Scholar 

  140. Liang Y, Sun W, Zhu YG, Christie P. Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollut. 2007;147(2):422–8.

    Article  CAS  Google Scholar 

  141. Ye J, Yan C, Liu J, Lu H, Liu T, Song Z. Effects of silicon on the distribution of cadmium compartmentation in root tips of Kandelia obovata (S., L.) Yong. Environ Pollut. 2012;162:369–73.

    Article  CAS  Google Scholar 

  142. Zhang Q, Liu J, Lu H, Zhao S, Wang W, Du J, et al. Effects of silicon on growth, root anatomy, radial oxygen loss (ROL) and Fe/Mn plaque of Aegiceras corniculatum (L.) Blanco seedlings exposed to cadmium. Environ Nanotechnol Monitor Manag. 2015;4:6–11.

    Article  Google Scholar 

  143. Dai M, Lu H, Liu W, Jia H, Hong H, Liu J, et al. Phosphorus mediation of cadmium stress in two mangrove seedlings Avicennia marina and Kandelia obovata differing in cadmium accumulation. Ecotoxicol Environ Saf. 2017;139:272–9.

    Article  CAS  Google Scholar 

  144. Kathiresan K, Bingham BL. Biology of mangroves and mangrove ecosystems. Adv Mar Biol. 2001;40:81–251.

    Article  Google Scholar 

  145. Rabinowitz D. Mortality and initial propagule size in mangrove seedlings in Panama. J Ecol. 1978;66(1):45–51.

    Article  Google Scholar 

  146. Lewis M, Pryor R, Wilking L. Fate and effects of anthropogenic chemicals in mangrove ecosystems: a review. Environ Pollut. 2011;159(10):2328–46.

    Article  CAS  Google Scholar 

  147. Chen XY. Heavy metals contents in sediments, mangroves and bivalves from ting Kok, Hong Kong. China Environ Sci (Chinese edition). 2003;23(5):480–4.

    CAS  Google Scholar 

  148. Clouse SD, Sasse JM. Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Biol. 1998;49(1):427–51.

    Article  CAS  Google Scholar 

  149. Kraus ML. Accumulation and excretion of five heavy metals by the salt marsh grass Spartina alterniflora. Bull-N J Acad Sci. 1988;33:39–43.

    Google Scholar 

  150. Lin G, Sternberg LD. Variation in propagule mass and its effect on carbon assimilation and seedling growth of red mangrove (Rhizophora mangle) in Florida. USA J Trop Ecol. 1995;11(01):109–19.

    Article  Google Scholar 

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Acknowledgments

The work described in this paper was supported by Natural Science Foundation of Shanghai (16ZR1410300), independent project of the State Key Laboratory of Estuarine and Coastal Researches (2016RCPY01) and National Nature Science Foundation of China (41201525).

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Yan, Z., Sun, X., Xu, Y. et al. Accumulation and Tolerance of Mangroves to Heavy Metals: a Review. Curr Pollution Rep 3, 302–317 (2017). https://doi.org/10.1007/s40726-017-0066-4

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