Abstract
Nickel hyperaccumulator plants have been the focus of considerable research because of their unique ecophysiological characteristics that can be exploited in phytomining technology. Comparatively little research has focussed on the soil chemistry of tropical nickel hyperaccumulator plants to date. This study aimed to elucidate whether the soil chemistry associated with nickel hyperaccumulator plants has distinctive characteristics that could be indicative of specific edaphic requirements. The soil chemistry associated with 18 different nickel hyperaccumulator plant species occurring in Sabah (Malaysia) was compared with local ultramafic soils where nickel hyperaccumulator plants were absent. The results showed that nickel hyperaccumulators in the study area were restricted to circum-neutral soils with relatively high phytoavailable calcium, magnesium and nickel concentrations. There appeared to be a ‘threshold response’ for the presence of nickel hyperaccumulator plants at >20 μg g−1 carboxylic-extractable nickel or >630 μg g−1 total nickel, and >pH 6.3 thereby delimiting their edaphic range. Two (not mutually exclusive) hypotheses were proposed to explain nickel hyperaccumulation on these soils: (1) hyperaccumulators excrete large amounts of root exudates thereby increasing nickel phytoavailability through intense rhizosphere mineral weathering; and (2) hyperaccumulators have extremely high nickel uptake efficiency thereby severely depleting nickel and stimulating re-supply of Ni from diffusion from labile Ni pools. It was concluded that since there was an association with soils with highly labile nickel pools, the available evidence primarily supports hypothesis (2).
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References
Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, Van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158(1):219–224. doi:10.1046/j.1469-8137.2003.00721.x
Alves S, Trancoso MA, de Lurdes Simões Gonçalves M, dos Santos MMC (2011) A nickel availability study in serpentinised areas of Portugal. Geoderma 164(3–4):155–163. doi:10.1016/j.geoderma.2011.05.019
Anderson PR, Christensen TH (1988) Distribution coefficients of Cd Co, Ni, and Zn in soils. J Soil Sci 39(1):15–22. doi:10.1111/j.1365-2389.1988.tb01190.x
Baker AJM (1981) Accumulators and excluders—strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654. doi:10.1080/01904168109362867
Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements. A review of their distribution, ecology and phytochemistry. Biorecovery 1(2):81–126
Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept, Andover, pp 291–304
Bani A, Echevarria G, Montargès-Pelletier E, Gjoka F, Sulçe S, Morel JL (2014) Pedogenesis and nickel biogeochemistry in a typical Albanian ultramafic toposequence. Environ Monit Assess 186(7):4431–4442. doi:10.1007/s10661-014-3709-6
Barbaroux R, Plasari E, Mercier G, Simonnot MO, Morel J-L, Blais JF (2012) A new process for nickel ammonium disulfate production from ash of the hyperaccumulating plant Alyssum murale. Sci Total Environ 423:111–119. doi:10.1016/j.scitotenv.2012.01.063
Basta NT, Ryan JA, Chaney RL (2005) Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. J Environ Qual 34(1):49–63. doi:10.2134/jeq2005.0049dup
Becquer T, Bourdon E, Pétard J (1995) Disponibilité du nickel le long d’une toposéquence de sols développés sur roches ultramafiques de Nouvelle-Calédonie. C R Acad Sci II 321(7):585–592
Becquer T, Pétard J, Duwig C, Bourdon E, Moreau R, Herbillon AJ (2001) Mineralogical, chemical and charge properties of Geric Ferralsols from New Caledonia. Geoderma 103(34):291–306. doi:10.1016/S0016-7061(01)00045-3
Becquer T, Rigault F, Jaffré T (2002) Nickel bioavailability assessed by ion exchange resin in the field. Commun Soil Sci Plant Anal 33(3–4):439–450. doi:10.1081/CSS-120002755
Becquer T, Quantin C, Boudot JP (2010) Toxic levels of metals in Ferralsols under natural vegetation and crops in New Caledonia. Eur J Soil Sci 61(6):994–1004. doi:10.1111/j.1365-2389.2010.01294.x
Bernal MP, McGrath SP (1994) Effects of pH and heavy metal concentrations in solution culture on the proton release, growth and elemental composition of Alyssum murale and Raphanus sativus L. Plant Soil 166(1):83–92. doi:10.1007/BF02185484
Bernal MP, McGrath SP, Miller AJ, Baker AJM (1994) Comparison of the chemical changes in the rhizosphere of the nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus. Plant Soil 164(2):251–259. doi:10.1007/BF00010077
Bisessar SS (1989) Effects of lime on nickel uptake and toxicity in celery grown on muck soil contaminated by a nickel refinery. Sci Total Environ 84:82–90. doi:10.1016/0048-9697(89)90372-0
Brooks RR, Robinson BH (1998) The potential use of hyperaccumulators and other plants for phytomining. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals: their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining. CAB International, Wallingford, pp 327–356
Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11(1):2–12. doi:10.1007/s00775-005-0056-7
Callahan DL, Roessner U, Dumontet V, Perrier N, Wedd AG, O’Hair RAJ et al (2008) LC-MS and GC-MS metabolite profiling of nickel (II) complexes in the latex of the nickel-hyperaccumulating tree Sebertia acuminata and identification of methylated aldaric acid as a new nickel (II) ligand. Phytochemistry 69(1):240–251. doi:10.1016/j.phytochem.2007.07.001
Callahan DL, Roessner U, Dumontet V, De Livera AM, Doronila A, Baker AJM, Kolev SD (2012) Elemental and metabolite profiling of nickel hyperaccumulators from New Caledonia. Phytochemistry 81:80–89. doi:10.1016/j.phytochem.2012.06.010
Centofanti T, Siebecker MG, Chaney RL, Davis AP, Sparks DL (2012) Hyperaccumulation of nickel by Alyssum corsicum is related to solubility of Ni mineral species. Plant Soil 359(1–2):71–83. doi:10.1007/s11104-012-1176-9
Chaney RL, Angle JS, Baker AJM, Li Y-M (1998) Method for phytomining of nickel, cobalt, and other metals from soil. U.S. Patent, 5, pp 711–784
Chaney RL, Chen K-Y, Li Y-M, Angle JS, Baker AJM (2008) Effects of calcium on nickel tolerance and accumulation in Alyssum species and cabbage grown in nutrient solution. Plant Soil 311(1–2):131–140. doi:10.1007/s11104-008-9664-7
Chardot V, Massoura ST, Echevarria G, Reeves RD, Morel JL (2005) Phytoextraction potential of the nickel hyperaccumulators Leptoplax emarginata and Bornmuellera tymphaea. Int J Phytoremediation 7(4):323–335. doi:10.1080/16226510500327186
Chardot V, Echevarria G, Gury M, Massoura S, Morel JL (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges Mountains (France). Plant Soil 293(1–2):7–21. doi:10.1007/s11104-007-9261-1
Chardot-Jacques V, Calvaruso C, Simon B, Turpault M-P, Echevarria G, Morel J-L (2013) Chrysotile dissolution in the rhizosphere of the nickel Hyperaccumulator Leptoplax emarginata. Environ Sci Technol 47(6):2612–2620. doi:10.1021/es301229m
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth 192 pp
Coinchelin D, Bartoli F, Robin C, Echevarria G (2012) Ecophysiology of nickel phytoaccumulation: a simplified biophysical approach. J Exp Bot 63(16):5815–5827. doi:10.1093/jxb/ers230
Cornu S, Deschatrettes V, Salvador-Blanes S, Clozel B, Hardy M, Branchut S, Le Forestier L (2005) Trace element accumulation in Mn–Fe-oxide nodules of a planosolic horizon. Geoderma 125(1–2):11–24. doi:10.1016/j.geoderma.2004.06.009
Crooke WM (1956) Effect of soil reaction on uptake of nickel from a serpentine soil. Soil Sci 81(4):269–276
Dohrmann R (2006) Cation exchange capacity methodology II: a modified silver–thiourea method. Appl Clay Sci 34(1–4):38–46. doi:10.1016/j.clay.2006.02.009
Dublet G, Juillot F, Morin G, Fritsch E, Fandeur D, Ona-Nguema G, Brown Jr, GE (2012) Ni speciation in a New Caledonian lateritic regolith: A quantitative X-ray absorption spectroscopy investigation. Geochim et Cosmochim Acta 95:119–133. doi:10.1016/j.gca.2012.07.030
Echevarria G, Morel J-L, Fardeau J, Leclerc-Cessac E (1998) Assessment of phytoavailability of nickel in soils. J Environ Qual 27(5):1–7. doi:10.2134/jeq1998.00472425002700050011x
Echevarria G, Massoura S, Sterckeman T, Becquer T, Schwartz C, Morel J-L (2006) Assessment and control of the bioavailability of nickel in soils. Environ Toxicol Chem 25(3):643–651. doi:10.1897/05-051R.1
Elzinga EJ, Sparks DL (2001) Reaction condition effects on nickel sorption mechanisms in illite–water suspensions. Soil Sci Soc Am J 65(1):94–101. doi:10.2136/sssaj2001.65194x
Estrade N, Cloquet C, Echevarria G, Sterckeman T, Deng THB, Tang YT, Morel JL (2015) Weathering and vegetation controls on nickel isotope fractionation in surface ultramafic environments (Albania). Earth Planet Sci Lett 423(1):24–25. doi:10.1016/j.epsl.2015.04.018
Everhart JL, McNear D Jr, Peltier E, Van der Lelie D, Chaney RL, Sparks DL (2006) Assessing nickel bioavailability in smelter-contaminated soils. Sci Total Environ 367(2–3):732–744. doi:10.1016/j.scitotenv.2005.12.029
Fan R, Gerson AR (2011) Nickel geochemistry of a Philippine laterite examined by bulk and microprobe synchrotron analyses. Geochim Cosmochim Acta 75(21):6400–6415. doi:10.1016/j.gca.2011.08.003
Feng M, Shan X, Zhang S, Wen B (2005) A comparison of the rhizosphere-based method with DTPA, EDTA, CaCl2, and NaNO3 extraction methods for prediction of bioavailability of metals in soil to barley. Environ Pollut 137(2):231–240. doi:10.1016/j.envpol.2005.02.003
Gabbrielli R, Pandolfini T (1984) Effect of Mg2+ and Ca2+ on the response to Ni toxicity in a serpentine endemic and Ni- accumulating species. Physiol Plant 62(4):540–544. doi:10.1111/j.1399-3054.1984.tb02796.x
Harper M, Davison W, Zhang H, Tych W (1998) Kinetics of metal exchange between solids and solutions in sediments and soils interpreted from DGT measure fluxes. Geochim Cosmochim Acta 62(16):2757–2770. doi:10.1016/S0016-7037(98)00186-0
Heikal MMD, Berry WL, Wallace A, Herman D (1989) Alleviation of nickel toxicity by calcium salinity. Soil Sci 147:413–415
Jaffré T, Brooks RR, Lee J, Reeves RD (1976) Sebertia acuminata: a hyperaccumulator of nickel from New Caledonia. Science 193(4253):579–580. doi:10.1126/science.193.4253.579
Krämer U, Smith RD, Wenzel WW, Raskin I, Salt DE (1997) The role of metal transport and tolerance in nickel Hyperaccumulation by Thlaspi goesingense Halacsy. Plant Physiol 115(4):1641–1650. doi:10.1104/pp.115.4.1641
Kukier U, Chaney RL (2001) Amelioration of nickel phytotoxicity in muck and mineral soils. J Environ Qual 30(6):1949–1960. doi:10.2134/jeq2001.1949
Kukier U, Chaney RL (2004) In situ remediation of nickel phytotoxicity for different plant species. J Plant Nutr 27(3):465–495. doi:10.1081/PLN-120028874
Kukier U, Peters CAC, Chaney RL, Angle JS, Roseberg RJR (2004) The effect of pH on metal accumulation in two Alyssum species. J Environ Qual 33(6):2090–2102. doi:10.2134/jeq2004.2090
L’Huillier L, Edighoffer S (1996) Extractability of nickel and its concentration in cultivated plants in Ni-rich ultramafic soils of New Caledonia. Plant Soil 186(2):255–264. doi:10.1007/BF02415521
Leleyter L, Probst JL (1999) A new sequential extraction procedure for the speciation of particulate trace elements in river sediments. Int J Environ Anal Chem 73(2):109–128. doi:10.1080/03067319908032656
Li Y-M, Chaney RL, Brewer EP, Angle JS, Nelkin J (2003) Phytoextraction of nickel and cobalt by hyperaccumulator Alyssum species grown on nickel-contaminated soils. Environ Sci Technol 37(7):1463–1468. doi:10.1021/es0208963
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42(3):421–428. doi:10.2136/sssaj1978.03615995004200030009x
Losfeld G, Escande V, Jaffré T, L’Huillier L, Grison C (2012) The chemical exploitation of nickel phytoextraction: an environmental, ecologic and economic opportunity for New Caledonia. Chemosphere 89(7):907–910. doi:10.1016/j.chemosphere.2012.05.004
Ma Y, Lombi E, McLaughlin MJ, Oliver IW, Nolan AL, Oorts K, Smolders E (2013) Aging of nickel added to soils as predicted by soil pH and time. Chemosphere 92(8):962–968. doi:10.1016/j.chemosphere.2013.03.013
Marcussen H, Holm PE, Strobel BW, Hansen HCB (2009) Nickel sorption to goethite and montmorillonite in presence of citrate. Environ Sci Technol 43(4):1122–1127. doi:10.1021/es801970z
Massoura ST, Echevarria G, Leclerc-Cessac E, Morel J-L (2004) Response of excluder, indicator, and hyperaccumulator plants to nickel availability in soils. Aust J Soil Res 42(8):933–938. doi:10.1071/SR03157
Massoura ST, Echevarria G, Becquer T, Ghanbaja J, Leclerc-Cessac E, Morel J-L (2006) Control of nickel availability by nickel bearing minerals in natural and anthropogenic soils. Geoderma 136(1–2):28–37. doi:10.1016/j.geoderma.2006.01.008
McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188:153–159. doi:10.1023/A:1004248123948
McNear DH Jr, Chaney RL, Sparks DL (2007) The effects of soil type and chemical treatment on nickel speciation in refinery enriched soils: a multi-technique investigation. Geochim Cosmochim Acta 71(9):2190–2208. doi:10.1016/j.gca.2007.02.006
McNear DH, Chaney RL, Sparks DL (2010) The hyperaccumulator Alyssum murale uses complexation with nitrogen and oxygen donor ligands for Ni transport and storage. Phytochemistry 71:188–200. doi:10.1016/j.phytochem.2009.10.023
Mesjasz-Przybyłowicz J, Barnabas A, Przybyłowicz W (2007) Comparison of cytology and distribution of nickel in roots of Ni-hyperaccumulating and non-hyperaccumulating genotypes of Senecio coronatus. Plant Soil 293(1):61–78. doi:10.1007/s11104-007-9237-1
Montargès-Pelletier E, Chardot V, Echevarria G, Michot LJ, Bauer A, Morel J-L (2008) Identification of nickel chelators in three hyperaccumulating plants: an X-ray spectroscopic study. Phytochemistry 69(8):1695–1709. doi:10.1016/j.phytochem.2008.02.009
Nachtegaal M, Sparks DL (2003) Nickel sequestration in a kaolinite–humic acid complex. Environ Sci Technol 37:529–534. doi:10.1021/es025803w
Poulsen IF, Hansen HCB (2000) Soil sorption of nickel in presence of citrate or arginine. Water Air Soil Pollut 120(3):249–259. doi:10.1023/A:1005201925212
Proctor J (2003) Vegetation and soil and plant chemistry on ultramafic rocks in the tropical Far East. Perspect Plant Ecol Evol Syst 6(1–2):105–124. doi:10.1078/1433-8319-00045
Puschenreiter M, Schnepf A, Millán IM, Fitz WJ, Horak O, Klepp J, Schrefl T, Lombi E, Wenzel WW (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 271(1–2):205–218. doi:10.1007/s11104-004-2387-5
Quantin C, Becquer T, Rouiller JH, Berthelin J (2001) Oxide weathering and trace metal release by bacterial reduction in a New Caledonia Ferralsol. Biogeochemistry 53(3):323–340. doi:10.1023/A:1010680531328
Quantin C, Becquer T, Rouiller JH, Berthelin J (2002) Redistribution of metals in a New Caledonia Ferralsol after microbial weathering. Soil Sci Soc Am J 66(6):1797–1804. doi:10.2136/sssaj2002.1797
Quantin C, Ettler V, Garnier J, Šebek O (2008) Sources and extractibility of chromium and nickel in soil profiles developed on Czech serpentinites. C R Geosci 340(12):872–882. doi:10.1016/j.crte.2008.07.013
Raous S, Echevarria G, Sterckeman T, Hanna K, Thomas F, Martins ES, Becquer T (2013) Potentially toxic metals in ultramafic mining materials: identification of the main bearing and reactive phases. Geoderma 192(1):111–119. doi:10.1016/j.geoderma.2012.08.017
Rayment GE, Higginson FR (1992) Australian laboratory handbook of soil and water chemical methods. Inkata Press, Melbourne
Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant Soil 249(1):57–65. doi:10.1023/A:1022572517197
Reeves RD, Baker AJM, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83(1):1–10. doi:10.1006/anbo.1998.0786
Robertson AI (1985) The poisoning of roots of Zea mays by nickel ions, and the protection afforded by magnesium and calcium. New Phytol 100:173–189. doi:10.1111/j.1469-8137.1985.tb02769.x
Robinson BH, Brooks RR, Kirkman JH, Gregg PEH, Gremigni P (1996) Plant-available elements in soils and their influence on the vegetation over ultramafic (“serpentine”) rocks in New Zealand. J R Soc N Z 26(4):457–468. doi:10.1080/03014223.1996.9517520
Robinson BH, Brooks RR, Clothier B (1999) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot 84(6):689–694. doi:10.1006/anbo.1999.0970
Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158(2):279–285. doi:10.1046/j.1469-8137.2003.00743.x
Salt DE, Kato N, Kramer U, Smith RD, Raskin I (2000) The role of root exudates in nickel hyperaccumulation and tolerance in accumulator and nonaccumulator species of Thlaspi. In: Terry N, Bañuelos GS (eds) Phytoremediation of contaminated soil and water. Lewis Publishers, Boca Raton, pp 189–200
Scheckel KG, Sparks DL (2001) Dissolution kinetics of nickel surface precipitates on clay mineral and oxide surfaces. Soil Sci Soc Am J 65(3):685–694. doi:10.2136/sssaj2001.653685x
Shallari S, Echevarria G, Schwartz C, Morel J-L (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale (Waldst. and Kit.). S Afr J Sci 97:568–570
Shi Z, Peltier E, Sparks DL (2012) Kinetics of Ni sorption in soils: roles of soil organic matter and Ni precipitation. Environ Sci Technol 46(4):2212–2219. doi:10.1021/es202376c
Siebecker M, Sparks DL (2010) Nickel speciation in serpentine soils using synchrotron radiation techniques. In: 2010 19th World congress of soil science, soil solutions for a changing world, 1–6 Aug 2010, Brisbane, Australia
Siebielec G, Chaney RL, Kukier U (2007) Liming to remediate Ni contaminated soils with diverse properties and a wide range of Ni concentration. Plant Soil 299(1–2):117–130. doi:10.1007/s11104-007-9369-3
Sochaczewski L, Tych Wlodek Davison B, Zhang H (2007) 2D DGT induced fluxes in sediments and soils (2D DIFS). Environ Model Softw 22:14–23. doi:10.1016/j.envsoft.2005.09.008
Tappero R, Peltier E, Gräfe M, et al (2006) Hyperaccumulator Alyssum murale relies on a different metal storage mechanism for cobalt than for nickel. New Phytol 175:641–654. doi:10.1111/j.1469-8137.2007.02134.x
Van der Ent A, Mulligan D (2015) Multi-element concentrations in plant parts and fluids of Malaysian nickel hyperaccumulator plants and some economic and ecological considerations. J Chem Ecol 41(4):396–408. doi:10.1007/s10886-015-0573-y
Van der Ent A, Reeves RD, Baker AJM, Pollard J, Schat H (2013a) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362(1–2):319–334. doi:10.1007/s11104-012-1287-3
Van der Ent A, Baker AJM, Van Balgooy MMJ, Tjoa A (2013b) Ultramafic nickel laterites in Indonesia: mining, plant diversity, conservation and nickel phytomining. J Geochem Explor 128:72–79. doi:10.1016/j.gexplo.2013.01.009
Van der Ent A, Mulligan D, Erskine PD (2013c) Discovery of nickel hyperaccumulators from Kinabalu Park, Sabah (Malaysia) for potential utilization in phytomining. In: Enviromine 2013, Santiago, Chile, 4–6 Dec 2013, pp 213–221
Van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson C, Meech J, Erskine PD, Simonnot M-O, Vaughan J, Morel J-L, Echevarria G, Fogliani B, Mulligan D (2015a) ‘Agromining’: Farming for metals in the future? Environ Sci Technol 49(8):4773–4780. doi:10.1021/es506031u
Van der Ent A, Wong KM, Sugau J, Repin R (2015b) Plant diversity of ultramafic outcrops in Sabah (Malaysia). Aust J Bot 63:204–215. doi:10.1071/BT14214
Van der Ent A, Erskine PD, Sumail S (2015c) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25(5):243–259. doi:10.1007/s00049-015-0192-7
Van der Ent A, Erskine PD, Mulligan DR, Repin R, Karim R (2016) Vegetation on ultramafic edaphic islands in Kinabalu Park (Sabah, Malaysia) in relation to soil chemistry and altitude. Plant Soil (in press)
Wenzel WW, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environ Pollut 123(1):131–138. doi:10.1016/S0269-7491(02)00341-X
Yamaguchi NU, Scheinost AC, Sparks DL (2002) Influence of gibbsite surface area and citrate on Ni sorption mechanisms at pH 7.5. Clay Clay Miner 50(6):784–790
Zhao F, Hamon R, McLaughlin M (2001) Root exudates of the hyperaccumulator Thlaspi caerulescens do not enhance metal mobilization. New Phytol 151(3):613–620. doi:10.1046/j.0028-646x.2001.00213.x
Acknowledgments
We wish to thank Sabah Parks for their support and the SaBC for granting permission for conducting research in Sabah, and to extend our gratitude to Sukaibin Sumail and Rositti Karim (Sabah Parks) for help in Kinabalu Park. We like to thank Rufus Chaney (USDA) and three anonymous reviewers for helpful and constructive comments on an earlier version of the manuscript. Trang Huynh (University of Queensland) is thanked for her help with the DGT deployment and modelling. The University of Queensland is gratefully acknowledged for financial support that made this project possible. Antony van der Ent was the recipient of an IPRS scholarship in Australia and a post-doctoral scholarship from the French National Research Agency through the national “Investissements d’avenir” program (ANR-10-LABX-21 - LABEX RESSOURCES21).
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AVDE and MT conceived and designed the field study and analytical procedures. AVDE conducted the experiments. AVDE and GE analysed the data. AVDE, MT and GE wrote the manuscript. All authors read and approved the manuscript.
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van der Ent, A., Echevarria, G. & Tibbett, M. Delimiting soil chemistry thresholds for nickel hyperaccumulator plants in Sabah (Malaysia). Chemoecology 26, 67–82 (2016). https://doi.org/10.1007/s00049-016-0209-x
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DOI: https://doi.org/10.1007/s00049-016-0209-x