Erratic hyperaccumulation of nickel, with particular reference to the Queensland serpentine endemic Pimelea leptospermoides
Roger D. Reeves A D , W. Scott Laidlaw A , Augustine Doronila B , Alan J. M. Baker A and (the late) George N. Batianoff CA School of Botany, The University of Melbourne, Vic. 3010, Australia.
B School of Chemistry, The University of Melbourne, Vic. 3010, Australia.
C Queensland Herbarium, Toowong, Qld 4066, Australia.
D Corresponding author. Email: rdjmreeves@xtra.co.nz
Australian Journal of Botany 63(2) 119-127 https://doi.org/10.1071/BT14195
Submitted: 13 August 2014 Accepted: 17 October 2014 Published: 7 April 2015
Abstract
Many hyperaccumulators of nickel (Ni) are endemic to ultramafic soils and always show very high Ni concentrations. Others occur on a variety of substrates but accumulate high Ni from the ultramafic ones. Pimelea leptospermoides is unusual in being an ultramafic endemic that shows a very wide range of Ni concentrations. The present work sought to establish the factors governing the wide variation in Ni uptake by P. leptospermoides, and aimed to investigate the likelihood of this variation originating from plant differences or soil differences. Multiple paired plant and soil samples were taken over the geographic range of occurrence of P. leptospermoides. Plant and soil metal concentrations and soil pH were measured. No evidence was found to suggest that the plants belong to populations with inherent ‘high-Ni’ and ‘low-Ni’ accumulation capability. Instead, the soil pH (covering a range from 6.0 to 8.3) and the total soil Ni concentrations of the ultramafic soils were found to be the major influences on the level of Ni accumulation. The wide variation observed in Ni accumulation by P. leptospermoides from ultramafic soils can be explained by a combination of variations in soil pH and total soil Ni concentrations.
Additional keywords: hyperaccumulator categories, soil pH, ultramafic soils.
References
Alford ER, Pilon-Smits EAH, Paschke MW (2010) Metallophytes: a view from the rhizosphere. Plant and Soil 337, 33–50.| Metallophytes: a view from the rhizosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVWmtbrJ&md5=589a8f069f118086e67098bf21704ac4CAS |
Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the ultramafic flora of Palawan, Republic of the Philippines. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds J Proctor, AJM Baker, RD Reeves) pp. 291–304. (Intercept Ltd: Andover, UK)
Batianoff GN, Specht RL (1992) Queensland (Australia) serpentinite vegetation. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds J Proctor, AJM Baker, RD Reeves) pp. 109–128. (Intercept Ltd: Andover, UK)
Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentinite-endemic species of central Queensland. Australian Journal of Botany 38, 121–130.
| Stackhousia tryonii Bailey: a nickel-accumulating serpentinite-endemic species of central Queensland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXpslKr&md5=8d269244e7ee1612e002dc17232f8797CAS |
Batianoff GN, Specht RL, Reeves RD (1991) The serpentinite flora of the humid subtropics of eastern Australia. Proceedings of the Royal Society of Queensland 101, 137–157.
Batianoff GN, Reeves RD, Specht RL (1997) The effect of serpentine on vegetation structure, species diversity and endemism in central Queensland. In ‘Écologie des milieux sur roches ultramafiques et sur sols metallifères. Documents scientifiques et techniques no. III/2’. (Eds T Jaffré, RD Reeves, T Becquer) pp. 147–153. (ORSTOM: Nouméa)
Batianoff GN, Neldner VJ, Singh S (2000) Vascular plant census and floristic analysis of serpentine landscapes in central Queensland. Proceedings of the Royal Society of Queensland 109, 1–30.
Bidwell SD (2000) Hyperaccumulation of metals in Australian native plants. PhD Thesis, University of Melbourne, Australia.
Brooks RR (1987) ‘Serpentine and its vegetation: a multidisciplinary approach.’ (Dioscorides Press: Portland, OR)
Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proceedings of the Royal Society of London. Series B. Biological Sciences 200, 217–224.
| Nickel accumulation by European species of the genus Alyssum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtFOrs7w%3D&md5=19ab16d38a3f9b9cfd5ecb266e041c8dCAS |
Brooks RR, Wither ED (1977) Nickel accumulation by Rinorea bengalensis (Wall.) O.K. Journal of Geochemical Exploration 7, 295–300.
| Nickel accumulation by Rinorea bengalensis (Wall.) O.K.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXltVCltr8%3D&md5=c3add0fa505cdfdfd7ae9d0eed3223f3CAS |
Brooks RR, Lee J, Jaffré T (1974) Some New Zealand and New Caledonian plant accumulators of nickel. Journal of Ecology 62, 493–499.
| Some New Zealand and New Caledonian plant accumulators of nickel.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhtVOjurc%3D&md5=be6c974fd0312a38e480250d2ce20270CAS |
Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proceedings of the Royal Society of London. Series B. Biological Sciences 203, 387–403.
| Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtVSisbk%3D&md5=51becf4f80bf7377ad95517abb738e52CAS |
Brooks RR, Reeves RD, Baker AJM, Rizzo JA, Ferreira HD (1990) The Brazilian serpentine plant expedition (BRASPEX), 1988. National Geographic Research 6, 205–219.
Brooks RR, Reeves RD, Baker AJM (1992) The serpentine vegetation of Goiás State, Brazil. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds J Proctor, AJM Baker, RD Reeves) pp. 67–81. (Intercept Ltd: Andover, UK)
Burrows CJ (1960) Studies in Pimelea. I. The breeding system. Transactions of the Royal Society of New Zealand 88, 29–45.
Campbell LR, Stone CO, Shamsedin NM, Kolterman DA, Pollard AJ (2013) Facultative hyperaccumulation of nickel in Psychotria grandis (Rubiaceae). Caribbean Naturalist 1, 1–8.
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. Journal of Applied Ecology 10, 269–320.
| 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.Crossref | GoogleScholarGoogle Scholar |
Echevarria G, Massoura ST, Sterckman T, Becquer T, Schwartz C, Morel JL (2006) Assessment and control of the bioavailabilty of nickel in soils. Environmental Toxicology and Chemistry 25, 643–651.
| Assessment and control of the bioavailabilty of nickel in soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVajurY%3D&md5=ca5664826c209d62a8e37b6500c07238CAS | 16566147PubMed |
Forster BA, Baker DE (1997) Characterisation of the serpentinite soils of central Queensland, Australia. In ‘Écologie des milieux sur roches ultramafiques et sur sols métallifères. Documents scientifiques et techniques no. III/2’. (Eds T Jaffré T, RD Reeves, T Becquer) pp. 27–37. (ORSTOM: Nouméa)
Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In ‘Characterization, functional genomics and health benefits’. Brassicaceae. (Ed. Minglin Lang) pp. 121–148. (Nova Science Publishers: New York)
Ghaderian SM, Mohtadi R, Rahiminejad R, Baker AJM (2007a) Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran. Environmental Pollution 145, 293–298.
| Nickel and other metal uptake and accumulation by species of Alyssum (Brassicaceae) from the ultramafics of Iran.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFWhsr3M&md5=dc2641578d4fd0741c19c861c37825d4CAS | 16781032PubMed |
Ghaderian SM, Mohtadi R, Rahiminejad R, Reeves RD, Baker AJM (2007b) Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran. Plant and Soil 293, 91–97.
| Hyperaccumulation of nickel by two Alyssum species from the serpentine soils of Iran.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaktLc%3D&md5=ab01d72cba5dc26134c142ec15156622CAS |
Jaffré T, Schmid M (1974) Accumulation du nickel par une Rubiacée de Nouvelle Calédonie, Psychotria douarrei (G. Beauvisage) Däniker. Comptes Rendus de l’Academie des Sciences, Séries D 278, 1727–1730.
Kabata-Pendias A, Mukherjee AB (2007) ‘Trace elements from soil to human.’ (Springer-Verlag: Berlin)
Kukier U, Peters CA, Chaney RL, Angle JS, Roseberg RJ (2004) The effect of pH on metal accumulation in two Alyssum species. Journal of Environmental Quality 33, 2090–2102.
| The effect of pH on metal accumulation in two Alyssum species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVegs7vE&md5=de3115e8f7d536f4c60b6110798dc2d7CAS | 15537931PubMed |
Li Y-M, Chaney R, Brewer E, Roseberg R, Angle JS, Baker A, Reeves R, Nelkin J (2003) Development of a technology for commercial phytoextraction of nickel: economic and technical considerations. Plant and Soil 249, 107–115.
| Development of a technology for commercial phytoextraction of nickel: economic and technical considerations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVyrs74%3D&md5=0708e75b82b0162996210868f5a224c2CAS |
Lyon GL, Brooks RR, Peterson PJ, Butler GW (1968) Trace elements in a New Zealand serpentine flora. Plant and Soil 29, 225–240.
| Trace elements in a New Zealand serpentine flora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXkvFGmsrg%3D&md5=2f4f9e8da173891d842d7eb2d16f2a16CAS |
McGrath SP (1995) Nickel. In ‘Heavy metals in soils’. 2nd edn. (Ed. BJ Alloway) (Blackie Academic and Professional: London)
Minguzzi C, Vergnano O (1948) Il contenuto di nichel nelle ceneri di Alyssum bertolonii Desv. Atti della Societa Toscana di Scienze Naturali. Memorie Serie A 55, 49–77.
Murray CG (1969) ‘The petrology of the ultramafic rocks of the Rockhampton district, Queensland.’ Geological Survey of Queensland Publication No. 343. (Queensland Department of Mines: Brisbane)
Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Science 217–218, 8–17.
| Facultative hyperaccumulation of heavy metals and metalloids.Crossref | GoogleScholarGoogle Scholar | 24467891PubMed |
Pope N, Fong M, Boyd R, Rajakaruna N (2014) The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator. Plant Ecology and Diversity 7, 421–432.
| The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator.Crossref | GoogleScholarGoogle Scholar |
Rajakaruna N, Bohm BA (2002) Serpentine and its vegetation: a preliminary study from Sri Lanka. Journal of Applied Botany 76, 20–28.
Reeves RD (1992) Hyperaccumulation of nickel by serpentine plants. In ‘The vegetation of ultramafic (serpentine) soils’. (Eds J Proctor, AJM Baker, RD Reeves) pp. 253–277. (Intercept Ltd: Andover, UK)
Reeves RD (2003) Tropical hyperaccumulators of metals and their potential for phytoextraction. Plant and Soil 249, 57–65.
| Tropical hyperaccumulators of metals and their potential for phytoextraction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsVyrs78%3D&md5=3aa4a3b1fccc31b40f8804ddaf3af344CAS |
Reeves RD (2005) Metal uptake by the serpentine plants of Queensland. In ‘Marlborough serpentine, landscape management and conservation’. (Eds A Exelby, K Wormington, A Melzer) pp. 23–40. (Central Queensland University: Gladstone, Qld)
Reeves RD, Adıgüzel N (2004) Rare plants and nickel accumulators from Turkish serpentine soils, with special reference to Centaurea species. Turkish Journal of Botany 28, 147–153.
Reeves RD, Adıgüzel N (2008) The nickel hyperaccumulating plants of Turkey and adjacent areas: a review with new data. Turkish Journal of Biology 32, 143–153.
Reeves RD, Baker AJM (2000) Metal accumulating plants. In ‘Phytoremediation of toxic metals: using plants to clean up the environment’. (Eds I Raskin, B Ensley) pp. 193–229. (Wiley and Sons: New York)
Reeves RD, Brooks RR, Macfarlane RM (1981) Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae). American Journal of Botany 68, 708–712.
| Nickel uptake by Californian Streptanthus and Caulanthus with particular reference to the hyperaccumulator S. polygaloides Gray (Brassicaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktl2is7w%3D&md5=1dd2b3ae3c737faf60b4150f0abf3d79CAS |
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1996) Nickel-accumulating plants from the ancient serpentine soils of Cuba. New Phytologist 133, 217–224.
| Nickel-accumulating plants from the ancient serpentine soils of Cuba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFKlsLc%3D&md5=fd3caffb6a094cdb888125308d3bafd7CAS |
Reeves RD, Baker AJM, Kelepertsis A (1997) The distribution and biogeochemistry of some serpentine plants of Greece. In ‘Écologie des milieux sur roches ultramafiques et sur sols métallifères. Documents scientifiques et techniques no. III/2’. (Eds T Jaffré, RD Reeves, T Becquer) pp. 205–207. (ORSTOM: Nouméa)
Reeves RD, Baker AJM, Borhidi A, Berazaín R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Annals of Botany 83, 29–38.
| Nickel hyperaccumulation in the serpentine flora of Cuba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1ajsL4%3D&md5=6f1477942217c49230dce50fdbfcb529CAS |
Reeves RD, Baker AJM, Becquer T, Echevarria G, Miranda ZJG (2007) The flora and biogeochemistry of the ultramafic soils of Goiás State, Brazil. Plant and Soil 293, 107–119.
| The flora and biogeochemistry of the ultramafic soils of Goiás State, Brazil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltlaktbo%3D&md5=e7ecd2abfbd315d8454398d56ba800f5CAS |
Reeves RD, Adıgüzel N, Baker AJM (2009) Nickel hyperaccumulation in Bornmuellera kiyakii Aytaç & Aksoy and associated plants of the Brassicaceae from Kızıldağ (Derebucak, Konya – Turkey). Turkish Journal of Botany 33, 33–40.
Severne BC, Brooks RR (1972) A nickel accumulating plant from Western Australia. Planta 103, 91–94.
| A nickel accumulating plant from Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38Xht1Gkurk%3D&md5=907a2b76d2d2ba825f1a799ffe12a364CAS | 24481475PubMed |
Shepherd PR (1983) Biogeochemical and geobotanical studies of the ultramafic areas of North Cape. BSc(Hons) Report, Massey University, Palmerston North, New Zealand.
Tye AM, Young S, Crout NMJ, Zhang H, Preston S, Zhao FJ, McGrath SP (2004) Speciation and solubility of copper, nickel and lead in contaminated soils. European Journal of Soil Science 55, 579–590.
| Speciation and solubility of copper, nickel and lead in contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXotVCntL8%3D&md5=28b29b326af2cd9e72dc84ce81752f74CAS |
van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant and Soil 362, 319–334.
| Hyperaccumulators of metal and metalloid trace elements: facts and fiction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ks7bF&md5=bee356700f51fe2ae7218429ac2a5674CAS |
Willmott WF, O’Flynn ML, Trezise DL (1986) ‘Rockhampton region, Queensland. 1 : 100 000 Geological Map Commentary.’ (Department of Mines, Geological Survey of Queensland)
Wither ED (1977) Biogeochemical studies in South-east Asia by use of herbarium material. MSc Thesis, Massey University, Palmerston North, New Zealand.