Global Distribution and Ecology of Hyperaccumulator Plants

  • Roger D. ReevesEmail author
  • Antony van der Ent
  • Alan J. M. Baker
Part of the Mineral Resource Reviews book series (MIRERE)


A large body of analytical data is available on the inorganic composition of many thousands of plant species, for which typical concentration ranges have been tabulated for major, minor, and trace elements. These elements include those that have been shown essential for plant growth, as well as others that lack this status, at least universally. Metalliferous soils, having abnormally high concentrations of some of the elements that are generally present only at minor (e.g. 200–2000 μg g−1) or trace (e.g. 0.1–200 μg g−1) levels, vary widely in their effects on plants and have attracted increasing attention during the last 50 years. The effects depend on the species, the relevant elements, and soil characteristics that influence the availability of metals to plants. Some of these soils are toxic to all or most higher plants. Others have hosted the development of specialized plant communities consisting of a restricted and locally characteristic range of metal-tolerant species. These plants often show a slightly elevated concentration of the elements with which the soil is enriched, but in places a species exhibits extreme accumulation of one or more of these elements, to a concentration level that may be hundreds or even thousands of times greater than that usually found in plants on the most common soils. These plants, now widely referred to as hyperaccumulators, are a remarkable resource for many types of fundamental scientific investigation (plant systematics, ecophysiology, biochemistry, genetics, and molecular biology) and for applications such as phytoremediation and agromining, and are discussed in detail below.


  1. Aggett J, Aspell AC (1980) Arsenic from geothermal sources in the Waikato catchment. NZ J Sci 23:77–82Google Scholar
  2. Al-Shehbaz IA (2014) A synopsis of the genus Noccaea (Coluteocarpeae, Brassicaceae). Harv Pap Bot 19:25–51CrossRefGoogle Scholar
  3. Anderson C, Brooks R, Chiarucci A, LaCoste C, Leblanc M, Robinson B, Simcock R, Stewart R (1999) Phytomining for nickel, thallium and gold. J Geochem Explor 67:407–415CrossRefGoogle Scholar
  4. Antonovics J, Bradshaw AD, Turner AG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRefGoogle Scholar
  5. Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654CrossRefGoogle Scholar
  6. Baker AJM (1987) Metal tolerance. New Phytol 106:93–111CrossRefGoogle Scholar
  7. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126Google Scholar
  8. Baker AJM, Whiting SN (2002) In search of the Holy Grail—a further step in understanding metal hyperaccumulation? New Phytol 155:1–4CrossRefGoogle Scholar
  9. Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the ultramafic flora of Palawan, Republic of the Philippines. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 291–304Google Scholar
  10. Baker AJM, Reeves RD, Hajar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl (Brassicaceae). New Phytol 127:61–68CrossRefGoogle Scholar
  11. Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biological resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos GS (eds) Phytoremediation of contaminated soil and water. CRC, Boca Raton, FL, pp 85–107Google Scholar
  12. Baker AJM, Ernst WHO, van der Ent A, Malaisse F, Ginocchio R (2010) Metallophytes: the unique biological resource, its ecology and conservational status in Europe, central Africa and Latin America. In: Batty LC, Hallberg KB (eds) Ecology of industrial pollution. Cambridge University Press, Cambridge, pp 7–40CrossRefGoogle Scholar
  13. Bani A, Echevarria G, Sulce S, Morel JL (2015a) Improving the agronomy of Alyssum murale for extensive phytomining: a five-year field study. Int J Phytoremediation 17:117–127CrossRefGoogle Scholar
  14. Bani A, Echevarria G, Zhang X, Benizri A, Laubie E, Morel JL, Simonnot M-O (2015b) The effect of plant density in nickel-phytomining field experiments with Alyssum murale in Albania. Aust J Bot 63:72–77Google Scholar
  15. Bañuelos GS, Mayland HF (2000) Absorption and distribution of selenium in animals consuming canola grown for selenium phytoremediation. Ecotoxicol Environ Safety 46:322–328CrossRefGoogle Scholar
  16. Bañuelos GS, Lin Z-Q, Yin X (2014) Selenium in the environment and human health. CRC, Boca Raton, FLGoogle Scholar
  17. Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentinite-endemic species of central Queensland. Aust J Bot 38:121–130CrossRefGoogle Scholar
  18. Beeson KC, Lazar VA, Boyce SG (1955) Some plant accumulators of the micronutrient elements. Ecology 36:155–156CrossRefGoogle Scholar
  19. Berazaín IR (1981) Sobre el endemismo de la florula serpentinicola de Lomas de Galindo, Canasi, Habana. Rev Jard Bot Nacional (Cuba) 2:29–59Google Scholar
  20. Bert V, Bonnin I, Saumitou-Laprade P, De Laguérie P, Petit D (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57CrossRefGoogle Scholar
  21. Bidwell SD, Woodrow IE, Batianoff GN, Sommer-Knudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905. doi: 10.1071/pp 01192 CrossRefGoogle Scholar
  22. Blissett AH (1966) Copper tolerant plants from the Ukaparinga copper mine, Williamstown. Quart Geol Notes Geol Surv S Aust 18:1–3Google Scholar
  23. Broadley MR, White PJ, Hammond JP, Zelko I, Lux A (2007) Zinc in plants. New Phytol 173(4):677–702CrossRefGoogle Scholar
  24. Brooks RR (1977) Copper and cobalt uptake by Haumaniastrum species. Plant Soil 48(2):541–544CrossRefGoogle Scholar
  25. Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland, ORGoogle Scholar
  26. Brooks RR (1998) Geobotany and hyperaccumulators. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford pp 55–94Google Scholar
  27. Brooks RR, Malaisse F (1985) The heavy metal-tolerant flora of southcentral Africa. Balkema, RotterdamGoogle Scholar
  28. Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc R Soc Lond B 200:217–224CrossRefGoogle Scholar
  29. Brooks RR, Robinson BH (1998) The potential use of hyperaccumulators and other plants for phytomining. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, pp 327–356Google Scholar
  30. Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea bengalensis (Wall.) O.K. J Geochem Explor 7:295–300CrossRefGoogle Scholar
  31. Brooks RR, Yang XH (1984) Elemental levels and relationships in the endemic serpentine flora of the Great Dyke, Zimbabwe, and their significance as controlling factors for the flora. Taxon 33:392–399CrossRefGoogle Scholar
  32. Brooks RR, Lee J, Jaffré T (1974) Some New Zealand and New Caledonian plant accumulators of nickel. J Ecol 62:493–499CrossRefGoogle Scholar
  33. Brooks RR, Lee J, Reeves RD, Jaffré T (1977a) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57CrossRefGoogle Scholar
  34. Brooks RR, Wither ED, Zepernick B (1977b) Cobalt and nickel in Rinorea species. Plant Soil 47:707–712CrossRefGoogle Scholar
  35. Brooks RR, McCleave JA, Schofield EK (1977c) Cobalt and nickel uptake by the Nyssaceae. Taxon 26:197–201CrossRefGoogle Scholar
  36. Brooks RR, Morrison RS, Reeves RD, Malaisse F (1978) Copper and cobalt in African species of Aeolanthus Mart. (Plectranthinae, Labiatae). Plant Soil 50:503–507CrossRefGoogle Scholar
  37. Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc R Soc Lond B203:387–403CrossRefGoogle Scholar
  38. Brooks RR, Reeves RD, Morrison RS, Malaisse F (1980) Hyperaccumulation of copper and cobalt—a review. Bull Soc R Bot Belg 113:166–172Google Scholar
  39. Brooks RR, Naidu SD, Malaisse F, Lee J (1987) The elemental content of metallophytes from the copper/cobalt deposits of central Africa. Bull Soc R Bot Belg 119:179–191Google Scholar
  40. Brooks RR, Dunn CE, Hall GEM (1995) Biological systems in mineral exploration and processing. Ellis Horwood, Hemel Hempstead, 80 pGoogle Scholar
  41. Byers HG, Miller JT, Williams KT, Lakin HW (1938) Selenium occurrence in certain soils in the United States, with a discussion of related topics. III. US Dept Agric Tech Bull 601:1–74Google Scholar
  42. Campbell LR, Stone CO, Shamsedin NM, Kolterman DA, Pollard AJ (2013) Facultative hyperaccumulation of nickel in Psychotria grandis (Rubiaceae). Carib Nat 1:1–8Google Scholar
  43. Chaney RL, Angle JS, McIntosh MS, Reeves RD, Li Y-M, Brewer EP, Chen K-Y, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang A, Baker AJM (2005) Using hyperaccumulator plants to phytoextract soil Ni and Cd. Z Naturforsch C 60c:190–198Google Scholar
  44. Chardot V, Massoura S, Echevarria G, Reeves RD, Morel JL (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediation 7:323–335CrossRefGoogle Scholar
  45. Cole MM (1973) Geobotanical and biogeochemical investigations in the sclerophyllous woodland and scrub associations of the eastern goldfields area of Western Australia, with particular reference to the role of Hybanthus floribundus (Lindl.) F. Muell. as nickel indicator and accumulator plant. J Appl Ecol 10:269–320CrossRefGoogle Scholar
  46. Deng D-M, Deng J-C, Li J-T, Zhang J, Hu M, Lin Z, Liao B (2008) Accumulation of zinc, cadmium, and lead in four populations of Sedum alfredii growing on lead/zinc mine spoils. J Integr Plant Biol 50:691–698CrossRefGoogle Scholar
  47. Deng H, Li MS, Chen YX, Luo YP, FM Y (2010) A new discovered manganese hyperaccumulator—Polygonum pubescens Blume. Fresenius Environ Bull 19:94–99Google Scholar
  48. Doksopulo EP (1961) Nickel in rocks, soils, water and plants adjacent to the talc deposits of the Chorchanskaya group. Izdat Tbilisk University, TbilisiGoogle Scholar
  49. Dykeman WR, De Sousa AS (1966) Natural mechanisms of copper tolerance in a copper swamp. Can J Bot 44:871–878CrossRefGoogle Scholar
  50. Ernst WHO (1966) Ökologisch-soziologische Untersuchungen an Schwermetallpflanzengesellschaften Südfrankreichs und des östlichen Harzvorlandes. Flora (Jena) B156:301–318Google Scholar
  51. Ernst WHO (1968) Das Violetum calaminariae westfalicum, eine Schwermetallpflanzengesellschaften Südfrankreichs und des östlichen Harzvorlandes. Mitteil. Floristisch. Arbeit 13:263–268Google Scholar
  52. Escarré J, Lefèbvre C, Gruber W, Leblanc M, Lepart J, Rivière Y, Delay B (2000) Zinc and cadmium accumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437CrossRefGoogle Scholar
  53. Faucon M-P, Shutcha MN, Meerts P (2007) Revisiting copper and cobalt concentrations in supposed hyperaccumulators from SC Africa: influence of washing and metal concentrations in soil. Plant Soil 301:29–36CrossRefGoogle Scholar
  54. Fernando DR, Woodrow IE, Jaffré T, Dumontet V, Marshall AT, Baker AJM (2008) Foliar manganese accumulation by Maytenus fournieri (Celastraceae) in its native New Caledonian habitats: populational variation and localization by X-ray microanalysis. New Phytol 177:178–185Google Scholar
  55. Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for ‘new’ Mn hyperaccumulators and potential applications in taxonomy. Ann Bot 103:931–939CrossRefGoogle Scholar
  56. Fernando ES, Quimado MO, Trinidad LC, Doronila AL (2013) The potential use of indigenous nickel hyperaccumulators for small-scale mining in The Philippines. J Degrad Mining Lands Manag 1:21–26Google Scholar
  57. Howes A (1991) Investigations into nickel hyperaccumulation by the plant Berkheya coddii. MSc Thesis, University of Natal, PietermaritzburgGoogle Scholar
  58. Jaffré T (1977) Accumulation du manganèse par les espèces associées aux terrains ultrabasiques de Nouvelle Calédonie. Compt Rend Acad Sci Paris Sér D 284:1573–1575Google Scholar
  59. Jaffré T (1979) Accumulation du manganèse par les Proteacées de Nouvelle Calédonie. Compt Rend Acad Sci Paris Sér D 289:425–428Google Scholar
  60. Jaffré T (1980) Etude écologique du peuplement végétal des sols dérivés de roches ultrabasiques en Nouvelle Calédonie. Trav et Documents de l’ORSTOM 124, ParisGoogle Scholar
  61. Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle Calédonie, Psychotria douarrei (G. Beauvisage) Däniker. Compt Rend Acad Sci Paris Sér D 278:1727–1730Google Scholar
  62. Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193:579–580CrossRefGoogle Scholar
  63. Jaffré T, Brooks RR, Trow JM (1979a) Hyperaccumulation of nickel by Geissois species. Plant Soil 51:157–162CrossRefGoogle Scholar
  64. Jaffré T, Kersten WJ, Brooks RR, Reeves RD (1979b) Nickel uptake by the Flacourtiaceae of New Caledonia. Proc R Soc Lond B205:385–394CrossRefGoogle Scholar
  65. Jaffré T, Pillon Y, Thomine S, Merlot S (2013) The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci 4:279. doi: 10.3389/fpls.2013.00279 CrossRefGoogle Scholar
  66. Koch M, Mummenhoff K (2001) Thlaspi s.str. (Brassicaceae) versus Thlaspi s.l. morphological and anatomical characters in the light of ITS and nrDNA sequence data. Plant Syst Evol 227:209–225CrossRefGoogle Scholar
  67. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61(1):517–534CrossRefGoogle Scholar
  68. Kruckeberg AR (1954) The ecology of serpentine soils. III. Plant species in relation to serpentine soils. Ecology 35:267–274Google Scholar
  69. Kubota J, Lazar VA, Beeson KC (1960) The study of cobalt status of soils in Arkansas and Louisiana using the black gum as the indicator plant. Soil Sci Proc 24:527–528CrossRefGoogle Scholar
  70. LaCoste C, Robinson BH, Brooks RR, Anderson CWN, Chiarucci A, Leblanc M (1999) The phytoremediation potential of thallium-contaminated soils using Iberis and Biscutella species. Int J Phytoremediation 1:327–338CrossRefGoogle Scholar
  71. Lancaster RJ, Coup MR, Hughes JW (1971) Toxicity of arsenic present in lakeweed. NZ Vet J 19:141–145Google Scholar
  72. Lange B, van der Ent A, Baker AJM, Echevarria G, Mahy G, Malaisse F, Meerts P, Pourret O, Verbruggen N, Faucon M-P (2017) Copper and cobalt accumulation in plants: a critical assessment of the current state of knowledge. New Phytol 213(2):537–551CrossRefGoogle Scholar
  73. Leblanc M, Petit D, Deram A, Robinson BH, Brooks RR (1999) The phytomining and environmental significance of hyperaccumulation of thallium by Iberis intermedia from southern France. Econ Geol 94:109–113CrossRefGoogle Scholar
  74. Lee J, Reeves RD, Brooks RR, Jaffré T (1977) Isolation and identification of a citrato-complex of nickel from nickel-accumulating plants. Phytochemistry 16:1503–1505CrossRefGoogle Scholar
  75. Li Y-M, Chaney RL, Brewer E, Roseberg R, Angle JS, Baker AJM, Reeves RD, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant Soil 249:107–115CrossRefGoogle Scholar
  76. Liddle JR (1982) Arsenic and other elements of geothermal origin in the Taupo volcanic zone. PhD Thesis, Massey University, Palmerston North, New ZealandGoogle Scholar
  77. Liu W, Shu W, Lan C (2004) Viola baoshanensis, a plant that hyperaccumulates cadmium. Chin Sci Bull 49:29–32CrossRefGoogle Scholar
  78. Liu K, Yu F, Chen M, Zhou Z, Chen C, Li MS, Zhu J (2016) A newly found manganese hyperaccumulator-Polygonum lapathifolium Linn. Int J Phytoremediation 18:348–353CrossRefGoogle Scholar
  79. Lombi E, Zhao FJ, Dunham SJ, McGrath SP (2000) Cadmium accumulation in populations of Thlaspi caerulescens and Thlaspi goesingense. New Phytol 145:11–20CrossRefGoogle Scholar
  80. Losfeld G, L’Huillier L, Fogliani B, McCoy S, Grison C, Jaffré T (2015) Leaf-age and soil-plant relationships: key factors for reporting trace-elements hyperaccumulation by plants and design applications. Environ Sci Pollut Res 22:5620–5632CrossRefGoogle Scholar
  81. Ma LQ, Komar KM, Tu C, Zhang WH, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579. doi: 10.1038/35054664 CrossRefGoogle Scholar
  82. Malaisse F, Grégoire J, Brooks RR, Morrison RS, Reeves RD (1978) Aeolanthus biformifolius: a hyperaccumulator of copper from Zaïre. Science 199:887–888CrossRefGoogle Scholar
  83. Malaisse F, Grégoire J, Brooks RR, Morrison RS, Reeves RD (1979) Copper and cobalt in vegetation of Fungurume, Shaba Province, Zaïre. Oikos 33:472–478CrossRefGoogle Scholar
  84. Malaisse F, Brooks RR, Baker AJM (1994) Diversity of vegetation communities in relation to soil heavy metal content at the Shinkolobwe copper/cobalt/uranium mineralization, Upper Shaba, Zaïre. Belg J Bot 127:3–16Google Scholar
  85. McAlister RL, Kolterman DA, Pollard AJ (2015) Nickel hyperaccumulation in populations of Psychotria grandis (Rubiaceae) from serpentine and non-serpentine soils of Puerto Rico. Aust J Bot 63:85–91Google Scholar
  86. Meharg A (2002) Arsenic and old plants. New Phytol 156:1–4CrossRefGoogle Scholar
  87. Menezes de Sequeira E (1969) Toxicity and movement of heavy metals in serpentinitic rocks (north-eastern Portugal). Agron Lusit 30:115–154Google Scholar
  88. Meyer FK (1973) Conspectus der “Thlaspi”-Arten Europas, Afrikas und Vorderasiens. Feddes Rep 84:449–470CrossRefGoogle Scholar
  89. Minguzzi C, Vergnano O (1948) Il contenuto di nichel nelle ceneri di Alyssum bertolonii Desv. Atti Soc Tosc Sci Natur Mem Ser A 55:49–77Google Scholar
  90. Mizuno T, Asahina R, Hosono A, Tanaka A, Senoo K, Obata H (2008) Age-dependent manganese hyperaccumulation in Chengiopanax sciadophylloides (Araliaceae). J Plant Nutr 31:1811–1819. doi: 10.1080/01904160802325396 CrossRefGoogle Scholar
  91. Morrey DR, Balkwill K, Balkwill M-J (1989) Studies on serpentine flora: preliminary analyses of soils and vegetation associated with serpentine rock formations in the southeastern Transvaal. S Afr J Bot 55:171–177CrossRefGoogle Scholar
  92. Morrey DR, Balkwill K, Balkwill M-J, Williamson S (1992) A review of some studies of the serpentine flora of southern Africa. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 147–157Google Scholar
  93. Nicks LJ, Chambers MF (1995) Farming for metals. Mining Environ Manage 3:15–18Google Scholar
  94. Nicks LJ, Chambers MF (1998) A pioneering study of the potential of phytomining for nickel. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, pp 313–325Google Scholar
  95. Nkrumah PN, Baker AJM, Chaney RL, Erskine PD, Echevarria G, Morel JL, van der Ent A (2016) Current status and challenges in developing nickel phytomining: an agronomic perspective. Plant Soil 406(1-2):55–69CrossRefGoogle Scholar
  96. Parker DR, Feist LJ, Varvel TW, Thomason DN, Zhang Y (2003) Selenium phytoremediation potential of Stanleya pinnata. Plant Soil 249:157–165CrossRefGoogle Scholar
  97. Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of metals and metalloids. Plant Sci 217-218:8–17CrossRefGoogle Scholar
  98. Proctor J, van Balgooy MMJ, Fairweather GM, Nagy L, Reeves RD (1994) A preliminary re-investigation of a plant geographical “El Dorado”. Trop Biodiversity 2:303–316Google Scholar
  99. Rascio N (1977) Metal accumulation by some plants growing on zinc-mine deposits. Oikos 29:250–253CrossRefGoogle Scholar
  100. Raskin I, Ensley BD (eds) (2000) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New YorkGoogle Scholar
  101. Reeves RD (1988) Nickel and zinc accumulation by species of Thlaspi L., Cochlearia L., and other genera of the Brassicaceae. Taxon 37:309–318CrossRefGoogle Scholar
  102. Reeves RD (1992) Hyperaccumulation of nickel by serpentine plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 253–277Google Scholar
  103. Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249:57–65CrossRefGoogle Scholar
  104. Reeves RD (2005) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) NATO science series: IV: Earth and environmental sciences, vol 68, 360 p. Springer, Berlin, pp 25–52; online as pp 1–25 in Phytoremediation of metal-contaminated soils. NATO Advanced Study Institute, Třešť Castle, 18–30 Aug 2002 at
  105. Reeves RD, Adıgüzel N (2004) Rare plants and nickel accumulators from Turkish serpentine soils, with special reference to Centaurea species. Turk J Bot 28:147–153Google Scholar
  106. Reeves RD, Adıgüzel N (2008) The nickel hyperaccumulating plants of Turkey and adjacent areas: a review with new data. Turk J Biol 32:143–153Google Scholar
  107. Reeves RD, Baker AJM (1984) Studies on metal uptake by plants from serpentine and non-serpentine populations of Thlaspi goesingense Halácsy (Cruciferae). New Phytol 98:191–204CrossRefGoogle Scholar
  108. Reeves RD, Baker AJM (2000) Metal accumulating plants. In: Raskin I, Ensley B (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
  109. Reeves RD, Brooks RR (1983a) European species of Thlaspi L. (Cruciferae) as indicators of nickel and zinc. J Geochem Explor 18:275–283CrossRefGoogle Scholar
  110. Reeves RD, Brooks RR (1983b) Hyperaccumulation of lead and zinc by two metallophytes from a mining area in central Europe. Environ Pollut 31:277–287CrossRefGoogle Scholar
  111. Reeves RD, Liddle JR (1986) Dispersal of arsenic from geothermal sources of the central North Island. In: Baker MJ (ed) Trace elements in the eighties. NZ Trace Element Group, Palmerston North, pp 31–34Google Scholar
  112. Reeves RD, Brooks RR, Press JR (1980) Nickel accumulation by species of Peltaria Jacq. (Cruciferae). Taxon 29:629–633CrossRefGoogle Scholar
  113. Reeves RD, Brooks RR, Macfarlane RM (1981) Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae). Am J Bot 68:708–712CrossRefGoogle Scholar
  114. Reeves RD, Brooks RR, Dudley TR (1983a) Uptake of nickel by species of Alyssum, Bornmuellera and other genera of old world tribus Alysseae. Taxon 32:184–192CrossRefGoogle Scholar
  115. Reeves RD, Macfarlane RM, Brooks RR (1983b) Accumulation of nickel by western North American genera containing serpentine-tolerant species. Am J Bot 70:1297–1303CrossRefGoogle Scholar
  116. Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytol 133:217–224CrossRefGoogle Scholar
  117. Reeves RD, Baker AJM, Borhidi A, Berazaín R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38CrossRefGoogle Scholar
  118. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behaviour of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172Google Scholar
  119. Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás State, Brazil. Plant Soil 293:107–119CrossRefGoogle Scholar
  120. Reeves RD, Laidlaw WS, Doronila A, Baker AJM, Batianoff GN (2015) Erratic hyperaccumulation of nickel, with particular reference to the Queensland serpentine endemic Pimelea leptospermoides F. Mueller. Aust J Bot 63:119–127Google Scholar
  121. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997a) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126CrossRefGoogle Scholar
  122. Robinson BH, Chiarucci A, Brooks RR, Petit D, Kirkman JH, Gregg PEH, De Dominicis V (1997b) The nickel hyperaccumulator plant Alyssum bertolonii as a potential agent for phytoremediation and phytomining of nickel. J Geochem Explor 59:75–86CrossRefGoogle Scholar
  123. Robinson BH, Leblanc M, Petit D, Brooks RR, Kirkman JH, Gregg PEH (1998) The potential of Thlaspi caerulescens for phytoremediation of contaminated soils. Plant Soil 203:47–56CrossRefGoogle Scholar
  124. Rosenfeld I, Beath OA (1964) Selenium—geobotany, biochemistry, toxicity and nutrition. Academic Press, New YorkGoogle Scholar
  125. Sachs J (1865) In: Hofmeister W (ed.) Handbuch der Experimental-Physiologie der Pflanzen. Handbuch der Physiologischen Botanik, vol IV. Engelmann, Leipzig, pp 153–154Google Scholar
  126. Schwartz C, Sirguey C, Peronny S, Reeves RD, Bourgaud F, Morel JL (2006) Testing of outstanding individuals of Thlaspi caerulescens for cadmium phytoextraction. Int J Phytoremediation 8:339–357CrossRefGoogle Scholar
  127. Severne BC, Brooks RR (1972) A nickel accumulating plant from Western Australia. Planta 103:91–94CrossRefGoogle Scholar
  128. Stebbins GL (1942) The genetic approach to rare and endemic species. Madroño 6:241–272Google Scholar
  129. Strawn KE (2013) Unearthing the habitat of a hyperaccumulator: case study of the invasive plant yellowtuft (Alyssum; Brassicaceae) in southwest Oregon, USA. Manage Biol Invasions 4:249–259CrossRefGoogle Scholar
  130. van der Ent A, Reeves RD (2015) Foliar metal accumulation in plants from copper-rich ultramafic outcrops: case studies from Malaysia and Brazil. Plant Soil 389:401–418CrossRefGoogle Scholar
  131. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334CrossRefGoogle Scholar
  132. van der Ent A, Erskine P, Sunmail S (2015) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25:243–259CrossRefGoogle Scholar
  133. Vittoottiviseth P, Francesconi K, Sridokchan W (2002) The potential of Thai indigenous plant species for the phytoremediation of arsenic contaminated land. Environ Pollut 118:453–461CrossRefGoogle Scholar
  134. Warren HV, Delavault RE, Barakso J (1964) The role of arsenic as a pathfinder in biogeochemical prospecting. Econ Geol 59:1381–1389CrossRefGoogle Scholar
  135. Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R, Jaffré T, Johns R, McIntyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophytes and their potential for restoration and site remediation. Restor Ecol 12:106–116CrossRefGoogle Scholar
  136. Wild H. (1970) The vegetation of nickel-bearing soils. Kirkia 7 (suppl):1–62Google Scholar
  137. Wither ED, Brooks RR (1977) Hyperaccumulation of nickel by some plants of South-East Asia. J Geochem Explor 8:579–583CrossRefGoogle Scholar
  138. Wulff A, Hollingsworth PM, Ahrends A, Jaffré T, Veillon JM, L’Huillier L, Fogliani B (2013) Conservation priorities in a biodiversity hotspot; analysis of narrow endemic plant species in New Caledonia. PLoS One 8(9):e73371CrossRefGoogle Scholar
  139. Xue SG, Chen YX, Reeves RD, Baker AJM, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Roger D. Reeves
    • 1
    Email author
  • Antony van der Ent
    • 2
    • 3
  • Alan J. M. Baker
    • 2
    • 3
    • 4
  1. 1.Palmerston NorthNew Zealand
  2. 2.Centre for Mined Land Rehabilitation, Sustainable Minerals InstituteThe University of QueenslandBrisbaneAustralia
  3. 3.Laboratoire Sols et EnvironnementUMR 1120, Université de Lorraine-INRAVandoeuvre-lès-NancyFrance
  4. 4.School of BioSciencesThe University of MelbourneMelbourneAustralia

Personalised recommendations