Ecological Research

, Volume 33, Issue 3, pp 651–658 | Cite as

Senecio conrathii N.E.Br. (Asteraceae), a new hyperaccumulator of nickel from serpentinite outcrops of the Barberton Greenstone Belt, South Africa

  • Stefan John SiebertEmail author
  • Nadine Carol Schutte
  • Stoffel Pieter Bester
  • Dennis Mmakgabo Komape
  • Nishanta Rajakaruna
Special Feature Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology


Five nickel hyperaccumulators belonging to the Asteraceae are known from ultramafic outcrops in South Africa. Phytoremediation applications of the known hyperaccumulators in the Asteraceae, such as the indigenous Berkheya coddii Roessler, are well reported and necessitate further exploration to find additional species with such traits. This study targeted the most frequently occurring species of the Asteraceae on eight randomly selected serpentinite outcrops of the Barberton Greenstone Belt. Twenty species were sampled, including 12 that were tested for nickel accumulation for the first time. Although the majority of the species were excluders, the known hyperaccumulators Berkheya nivea N.E.Br. and B. zeyheri (Sond. & Harv.) Oliv. & Hiern subsp. rehmannii (Thell.) Roessler var. rogersiana (Thell.) Roessler hyperaccumulated nickel in the leaves at expected levels. A new hyperaccumulator of nickel was discovered, Senecio conrathii N.E.Br., which accumulated the element in its leaves at 1695 ± 637 µg g−1 on soil with a total and exchangeable nickel content of 503 mg kg−1 and 0.095 µg g−1, respectively. This makes it the third known species in the Senecioneae of South Africa to hyperaccumulate nickel after Senecio anomalochrous Hilliard and Senecio coronatus (Thunb.) Harv., albeit it being a weak accumulator compared with the latter. Seven tribes in the Asteraceae have now been screened for hyperaccumulation in South Africa, with hyperaccumulators only recorded for the Arctoteae and Senecioneae. This suggests that further exploration for hyperaccumulators should focus on these tribes as they comprise all six species (of 68 Asteraceae taxa screened thus far) to hyperaccumulate nickel.


Asteraceae Hyperaccumulation Nickel Senecio Ultramafic 



Mr Arnold Frisby from the University of Pretoria is thanked for assistance with fieldwork. Dr Marinda Koekemoer from the Pretoria National Herbarium confirmed the identity of the hyperaccumulator. Prof Marthie Coetzee from the North-West University confirmed the rock samples as serpentinite. National Geographic Society funded the fieldwork and the Botanical Education Trust funded the plant and soil analyses conducted at the labs of EcoAnalytica at the North-West University. We thank two anonymous reviewers for their constructive comments which helped in improving the manuscript. Opinions expressed and conclusions arrived at, are those of the authors and are not necessarily to be attributed to the funders. The authors declare that they have no conflict of interest.


  1. Borhidi A (2001) Phylogenetic trends in Ni-accumulating plants. S Afr J Sci 97:544–547Google Scholar
  2. Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567CrossRefGoogle Scholar
  3. Boyd RS, Davis MA, Balkwill K (2008) Elemental patterns in Ni hyperaccumulating and non-hyperaccumulating ultramafic soil populations of Senecio coronatus. S Afr J Bot 74:158–162CrossRefGoogle Scholar
  4. Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc R Soc B-Biol Sci 200:217–224CrossRefGoogle Scholar
  5. Burge DO, Barker WR (2010) Evolution of nickel hyperaccumulation by Stackhousia tryonii (Celastraceae), a serpentinite-endemic plant from Queensland, Australia. Aust Syst Bot 23:415–430CrossRefGoogle Scholar
  6. Cecchi L, Gabbrielli R, Arnetoli M, Gonnelli C, Hasko A, Selvi F (2010) Evolutionary lineages of nickel hyperaccumulation and systematics in European Alysseae (Brassicaceae): evidence from nrDNA sequence data. Ann Bot 106:751–767CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chaney RL, Reeves RD, Baklanov IA, Centofanti T, Broadhurst CL, Baker AJM, Van der Ent A, Roseberg RJ (2014) Phytoremediation and phytomining: using plants to remediate contaminated or mineralized environments. In: Rajakaruna N, Boyd RS, Harris TB (eds) Plant ecology and evolution in harsh environments. Nova Science Publishers, New York, pp 365–392Google Scholar
  8. Ellery KS, Walker BH (1986) Growth characteristics of selected plant species on asbestos tailings from Msauli Mine, Eastern Transvaal. S Afr J Bot 52:201–206CrossRefGoogle Scholar
  9. Ernst WH (2006) Evolution of metal tolerance in higher plants. For Snow Landsc Res 80:251–274Google Scholar
  10. Gabbrielli R, Pandolfini T (1984) Effect of Mg2+ and Ca2+ on the response to nickel toxicity in a serpentine endemic and nickel-accumulating species. Physiol Plant 62:540–544CrossRefGoogle Scholar
  11. Galey ML, Van der Ent A, Iqbal MCM, Rajakaruna N (2017) Serpentine geoecology of South and Southeast Asia. Bot Stud 58:18CrossRefPubMedPubMedCentralGoogle Scholar
  12. Gall JE, Rajakaruna N (2013) The physiology, functional genomics, and applied ecology of heavy metal-tolerant Brassicaceae. In: Lang M (ed) Brassicaceae: characterisation, functional genomics and health benefits. Nova Sciences Publishers, New York, pp 121–148Google Scholar
  13. Hughes JC, Noble AD (1991) Extraction of chromium, nickel and iron and the availability of chromium and nickel to plants from serpentine derived soils from the Eastern Transvaal as revealed by various single and sequential extraction techniques. Commun Soil Sci Plan 22:1753–1766CrossRefGoogle Scholar
  14. 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 4:279CrossRefPubMedPubMedCentralGoogle Scholar
  15. Koekemoer M (1996) An overview of the Asteraceae of southern Africa. In: Hind DJN, Beentje HJ, Smith SAL (eds) Compositae: systematics. Proceedings of the international compositae conference, vol 1. Royal Botanic Gardens, Kew, pp 95–110Google Scholar
  16. Kruckeberg AR, Kruckeberg AL (1990) Endemic metallophytes: their taxonomic, genetic, and evolutionary attributes. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca-Raton, pp 301–312Google Scholar
  17. Mengoni A, Baker AJM, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbrielli R, Gonnelli C (2003) Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by ITS nrDNA analysis. New Phytol 159:691–699CrossRefGoogle Scholar
  18. Mesjasz-Przybylowicz J, Przybylowicz WJ, Rama DBK, Pineda CA (2001) Elemental distribution in Senecio anomalochrous, a Ni hyperaccumulator from South Africa. S Afr J Sci 97:593–595Google Scholar
  19. 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 293:61–78CrossRefGoogle Scholar
  20. Morgenthal T, Maboeta M, Van Rensburg L (2004) Revegetation of heavy metal contaminated mine dumps using locally serpentine-adapted grassland species. S Afr J Bot 70:784–789CrossRefGoogle Scholar
  21. Morrey DR, Balkwill K, Balkwill M-J (1989) Studies on serpentine flora: preliminary analyses of soils and vegetation associated with serpentinite rock formations in the south-eastern Transvaal. S Afr J Bot 55:171–177CrossRefGoogle Scholar
  22. Nishida S, Tsuzuki C, Kato A, Aisu A, Yoshida J, Mizuno T (2011) AtIRT1, the primary iron uptake transporter in the root, mediates excess nickel accumulation in Arabidopsis thaliana. Plant Cell Physiol 52:1433–1442CrossRefPubMedGoogle Scholar
  23. Proctor J (1971) The plant ecology of serpentine: III. The influence of a high magnesium/calcium ratio and high nickel and chromium levels in some British and Swedish serpentine soils. J Ecol 59:827–842CrossRefGoogle Scholar
  24. Rajakaruna NB, Harris TB, Alexander EB (2009) Serpentine geoecology of eastern North America: a review. Rhodora 111:21–108CrossRefGoogle Scholar
  25. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181CrossRefPubMedGoogle Scholar
  26. Reeves RD, Adigüzel N (2004) Rare plants and nickel accumulators from Turkish serpentine soils, with special reference to Centaurea species. Turk J Bot 28:147–153Google Scholar
  27. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
  28. Reeves RD, Baker AJM, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38CrossRefGoogle Scholar
  29. Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126CrossRefGoogle Scholar
  30. Robinson BH, Brooks RR, Clothier BE (1999) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot 84:689–694CrossRefGoogle Scholar
  31. Sabienë N, Brazauskienë DM, Rimmer D (2004) Determination of heavy metal mobile forms by different extraction methods. Ekologija 1:36–41Google Scholar
  32. Schöning A, Brümmer GW (2008) Extraction of mobile element fractions in forest soils using ammonium nitrate and ammonium chloride. J Plant Nutr Soil Sci 171:392–398CrossRefGoogle Scholar
  33. Severne BC (1974) Nickel accumulation by Hybanthus floribundus. Nature 248:807–808CrossRefPubMedGoogle Scholar
  34. Shallari S, Schwartz C, Hasko A, Morel JL (1998) Heavy metals in soils and plants of serpentine and industrial sites of Albania. Sci Total Environ 209:133–142CrossRefPubMedGoogle Scholar
  35. Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726CrossRefPubMedGoogle Scholar
  36. Siebert SJ, Van Wyk AE, Bredenkamp GJ (2002) The physical environment and major vegetation types of Sekhukhuneland, South Africa. S Afr J Bot 68:127–142CrossRefGoogle Scholar
  37. Smith S, Balkwill K, Williamson S (2001) Compositae on serpentine in the Barberton Greenstone Belt, South Africa. S Afr J Sci 97:518–520Google Scholar
  38. 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
  39. Van der Ent A, Erskine P, Sumail S (2015) Ecology of nickel hyperaccumulator plants from ultramafic soils in Sabah (Malaysia). Chemoecology 25:243–259CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2017

Authors and Affiliations

  • Stefan John Siebert
    • 1
    Email author
  • Nadine Carol Schutte
    • 1
  • Stoffel Pieter Bester
    • 1
    • 2
  • Dennis Mmakgabo Komape
    • 1
  • Nishanta Rajakaruna
    • 1
    • 3
  1. 1.Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa
  2. 2.National Herbarium, South African National Biodiversity InstitutePretoriaSouth Africa
  3. 3.Biological Sciences DepartmentCalifornia Polytechnic State UniversitySan Luis ObispoUSA

Personalised recommendations