Plant and Soil

, Volume 430, Issue 1–2, pp 245–262 | Cite as

Soil trace metal content does not affect the distribution of the hyperaccumulator Noccaea caerulescens in the Vosges Mountains (France)

  • C. Sirguey
  • G. Seznec
  • T. Mahevas
  • G. Echevarria
  • C. Gonneau
  • T. Sterckeman
Regular Article



Noccaea caerulescens is a pseudo-metallophyte known to hyperaccumulate Zn, Cd and Ni, and a model species for the study of the hyperaccumulation of trace metals. However, information about its ecology is rather scarce. The aim of this work was thus to determine if soil metal content was the main factor responsible for the distribution of N. caerulescens.


During 4 years, the Vosges Mountains (north eastern France) were explored during the flowering season. Plants and their rooting soil were analyzed for their trace element content (Cd, Mn, Ni and Zn). The ecological amplitude of N. caerulescens was analyzed using Maximum Entropy Modelling (MaxEnt).


Only five populations of the 67 recorded were found on metalliferous soils. All the recorded populations presented a Zn-hyperaccumulator phenotype, whereas only two presented a Cd and/or Ni-hyperaccumulator phenotype. The spatial distribution of mineralized areas did not explain the spatial distribution of the species. The MaxEnt distribution model suggested that the principle explanatory factors were the annual precipitation, soil use and underlying geology.


Trace metal concentrations in soils are not the main drivers of N. caerulescens distribution in the Vosges Mountains. Instead, pedological and climatic factors along with recent human activity are the main factors of the colonization of the massif.


Ecological niche Human activity Hyperaccumulation MaxEnt modelling Trace elements 



The authors are grateful to Jean-Louis Morel and to Alan J. M. Baker for carefully pre-reviewing the manuscript.

Supplementary material

11104_2018_3731_MOESM1_ESM.xlsx (12.3 mb)
ESM 1 (XLSX 12641 kb)


  1. Antonovics J, Bradshaw AD, Turner R (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRefGoogle Scholar
  2. Assunção AGL, Bookum WM, Nelissen HJM et al (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytol 159:411–419. CrossRefGoogle Scholar
  3. Assunção AGL, Bleeker P, ten Bookum WM et al (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299. CrossRefGoogle Scholar
  4. Baker AJM (1994) Thlaspi caerulescens. In: Stewart A, Pearman DA, Preston CD (eds) Scarce plants in Britain, pp 407–409Google Scholar
  5. 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
  6. Banásová V, Horak O, Čiamporová M et al (2006) The vegetation of metalliferous and non-metalliferous grasslands in two former mine regions in Central Slovakia. Biologia (Bratisl) 61.
  7. Basic N, Salamin N, Keller C et al (2006) Cadmium hyperaccumulation and genetic differentiation of Thlaspi caerulescens populations. Biochem Syst Ecol 34:667–677. CrossRefGoogle Scholar
  8. Berher DE (1887) La flore des Vosges. Phanérogames, muscinées, lichens..Google Scholar
  9. Boudot J-P, Bruckert S, Souchier B (1981) Végétation et sols climax Sur les grauwackes de la série du Markstein (Hautes-Vosges). Ann Sci For 38:87–106CrossRefGoogle Scholar
  10. Brady KU, Kruckeberg AR, Bradshaw HD Jr (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  11. BRGM (1998) Cartographie des concentrations et des fonds géochimiques métalliques connus du massif des VosgesGoogle Scholar
  12. BRGM (2008) Carte géologique interactive de la France à 1/1 000 000 (6ème édition révisée)Google Scholar
  13. Chardot V, Echevarria G, Gury M et al (2007) Nickel bioavailability in an ultramafic toposequence in the Vosges Mountains (France). Plant Soil 293:7–21. CrossRefGoogle Scholar
  14. Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:92–99. CrossRefPubMedGoogle Scholar
  15. Dechamps C, Elvinger N, Meerts P et al (2011) Life history traits of the pseudometallophyte Thlaspi caerulescens in natural populations from northern Europe. Plant Biol 13:125–135. CrossRefPubMedGoogle Scholar
  16. Denayer-De Smet S, Duvigneaud P (1974) Accumulation de métaux lourds toxiques dans divers écosystèmes terrestres pollués par des retombées d’origine industrielle. Bull Société R Bot Belg Van K Belg Bot Ver:147–156Google Scholar
  17. Deng T-H-B, Cloquet C, Tang Y-T et al (2014) Nickel and zinc isotope fractionation in hyperaccumulating and nonaccumulating plants. Environ Sci Technol 48:11926–11933CrossRefPubMedGoogle Scholar
  18. Dubois S (2005) Etude d’un réseau de populations métallicoles et non-métallicoles de Thlaspi caerulescens (Brassicaceae): Structure génétique, démographie et pressions de sélection. PhD Thesis, Montpellier 2Google Scholar
  19. Duchaufour PH, Souchier B (1978) Roles of iron and clay in genesis of acid soils under a humid, temperate climate. Geoderma 20:15–26CrossRefGoogle Scholar
  20. Dvořáková M (1968) Zur Nomenklatur einiger Taxa aus dem Formenkreis von Thlaspi alpestre (L.) L. Folia Geobot Phytotaxon 3:341–343CrossRefGoogle Scholar
  21. Elith J, Phillips SJ, Hastie T et al (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57. CrossRefGoogle Scholar
  22. Escarré J, Lefèbvre C, Gruber W et al (2000) Zinc and cadmium hyperaccumulation by Thlaspi caerulescens from metalliferous and nonmetalliferous sites in the Mediterranean area: implications for phytoremediation. New Phytol 145:429–437CrossRefGoogle Scholar
  23. European Environment Agency (2007) CLC2006 technical guidelines. Publications Office, LuxembourgGoogle Scholar
  24. Flageollet J-C (2008) Morpho-structures vosgiennes. Géomorphologie Relief Process Environ 2:75–86CrossRefGoogle Scholar
  25. Fluck P, Ancel B (1989) Le paysage minier des sites métalliques des Vosges et de la Forêt-noire. Ann Bretagne Pays Ouest 96:183–201CrossRefGoogle Scholar
  26. Godron D (1883) Flore de Lorraine. 2ème éd, N. Grosjean Libraire éditeur. Tome premierGoogle Scholar
  27. Goepp S (2007) Origine, histoire et dynamique des Hautes-Chaumes du massif vosgien. Déterminismes environnementaux et actions de l’Homme. PhD Thesis, Université Louis PasteurGoogle Scholar
  28. Gonneau C, Genevois N, Frérot H et al (2014) Variation of trace metal accumulation, major nutrient uptake and growth parameters and their correlations in 22 populations of Noccaea caerulescens. Plant Soil 384:271–287. CrossRefGoogle Scholar
  29. Gonneau C, Noret N, Godé C et al (2017) Demographic history of the trace metal hyperaccumulator Noccaea caerulescens (J. Presl and C. Presl) F. K. Mey. In Western Europe. Mol Ecol 26:904–922. CrossRefPubMedGoogle Scholar
  30. Hanikenne M, Nouet C (2011) Metal hyperaccumulation and hypertolerance: a model for plant evolutionary genomics. Curr Opin Plant Biol 14:252–259. CrossRefPubMedGoogle Scholar
  31. Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS version 7.5 manualGoogle Scholar
  32. Hohl J-L (1994) Minéraux et mines du massif vosgien. Editions du RhinGoogle Scholar
  33. Ingrouille MJ, Smirnoff N (1986) Thlaspi caerulescens J. & C. Presl. (T. alpestre L.) in Britain. New phytol 219–233Google Scholar
  34. ISO 10390 (2005) Soil quality - Determination of pHGoogle Scholar
  35. ISO 23470 (1999) Soil quality - Chemical methods - Determination of cationic exchange capacity (CEC) and extractible cationsGoogle Scholar
  36. Julve P (2015) Baseveg. Répertoire synonymique des groupements végétaux de France. Version : 16 février 2015.
  37. Kazakou E, Dimitrakopoulos PG, Baker AJM et al (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508PubMedGoogle Scholar
  38. Koch MA, German DA (2013) Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. Front Plant Sci 4.
  39. Koopmans GF, Römkens PFAM, Fokkema MJ et al (2008) Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils. Environ Pollut 156:905–914. CrossRefPubMedGoogle Scholar
  40. Krämer U (2005) Phytoremediation: novel approaches to cleaning up polluted soils. Curr Opin Biotechnol 16:133–141. CrossRefPubMedGoogle Scholar
  41. Lloyd-Thomas DH (1995) Heavy metal hyperaccumulation by Thlaspi caerulescens J. & C. Presl. PhD Thesis, University of SheffieldGoogle Scholar
  42. Marand C, Zumstein J-F (1990) La modélisation des précipitations moyennes annuelles appliquée au Massif vosgien. Hydrol Cont 5:29–39Google Scholar
  43. Maxted AP, Black CR, West HM et al (2007) Phytoextraction of cadmium and zinc from arable soils amended with sewage sludge using Thlaspi caerulescens: development of a predictive model. Environ Pollut 150:363–372. CrossRefPubMedGoogle Scholar
  44. McGrath SP, Lombi E, Gray CW et al (2006) Field evaluation of cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ Pollut 141:115–125. CrossRefPubMedGoogle Scholar
  45. Meerts P, Van Isacker N (1997) Heavy metal tolerance and accumulation in metallicolous and non-metallicolous populations of Thlaspi caerulescens from continental Europe. Plant Ecol 133:221–231CrossRefGoogle Scholar
  46. Méloux J, Bureau de recherches géologiques et minières (France). Service géologique national, Commission géotechnique suisse (1982) Carte des gîtes minéraux de la France à 1/500 000 StrasbourgGoogle Scholar
  47. Meyer FK (2006) Kritische revision der Thlaspi-Arten Europas, Afrikas und Vorderasiens. Spezieller Teil. IX, NoccaeaGoogle Scholar
  48. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102:3–13. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Molitor M, Dechamps C, Gruber W, Meerts P (2005) Thlaspi caerulescens on nonmetalliferous soil in Luxembourg: ecological niche and genetic variation in mineral element composition. New Phytol 165:503–512. CrossRefPubMedGoogle Scholar
  50. Mougeot J (1845) Considérations générales Sur la végétation spontanée (phanérogames et cryptogames) du département des Vosges. Stat Dép Vosges 1:163–516Google Scholar
  51. Parent GH (1997) Atlas des Ptéridophytes des régions lorraines et vosgiennes, avec les territoires adjacents. Musée National d’Histoire Naturelle, LuxembourgGoogle Scholar
  52. Parent GH (2011) La flore calcicole et basophile du massif vosgien. Musée National d’Histoire Naturelle, LuxembourgGoogle Scholar
  53. Pearson RG, Raxworthy CJ, Nakamura M, Townsend Peterson A (2007) Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J Biogeogr 34:102–117. CrossRefGoogle Scholar
  54. Peer WA, Mahmoudian M, Freeman JL et al (2006) Assessment of plants from the Brassicaceae family as genetic models for the study of nickel and zinc hyperaccumulation. New Phytol 172:248–260. CrossRefPubMedGoogle Scholar
  55. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. CrossRefGoogle Scholar
  56. Reeves R, Brooks R (1983) Hyperaccumulation of lead and zinc by two metallophytes from mining areas of Central Europe. Environ Pollut Ser Ecol Biol 31:277–285CrossRefGoogle Scholar
  57. Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediation 3:145–172. CrossRefGoogle Scholar
  58. Schwartz C, Echevarria G, Morel JL (2003) Phytoextraction of cadmium with Thlaspi caerulescens. Plant Soil 249:27–35CrossRefGoogle Scholar
  59. Schwartz D, Thinon M, Goepp S et al (2005) Premières datations directes de défrichements protohistoriques Sur les chaumes secondaires des Vosges (Rossberg, haut-Rhin). Approche pédoanthracologique. Comptes Rendus Geosci 337:1250–1256. CrossRefGoogle Scholar
  60. Sterckeman T, Cazes Y, Gonneau C, Sirguey C (2017) Phenotyping 60 populations of Noccaea caerulescens provides a broader knowledge of variation in traits of interest for phytoextraction. Plant Soil 418:523–540. CrossRefGoogle Scholar
  61. Théobald N, Thiébaut J, Bernatzky M, Bureau de recherches géologiques et minières. Service géologique national (1974) Carte géologique de la France à 1/50 000. 411, Giromagny [Notice explicative]Google Scholar
  62. van der Ent A, Baker AJM, Reeves RD et al (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334. CrossRefGoogle Scholar
  63. Verbruggen N, Hermans C, Schat H (2009) Molecular mechanisms of metal hyperaccumulation in plants. New Phytol 181:759–776. CrossRefPubMedGoogle Scholar
  64. Verbruggen N, Hanikenne M, Clemens S (2013) A more complete picture of metal hyperaccumulation through next-generation sequencing technologies. Front Plant Sci 4.
  65. Visioli G, Vincenzi S, Marmiroli M, Marmiroli N (2012) Correlation between phenotype and proteome in the Ni hyperaccumulator Noccaea caerulescens subsp. caerulescens. Environ Exp Bot 77:156–164. CrossRefGoogle Scholar
  66. Visioli G, Gullì M, Marmiroli N (2014) Noccaea caerulescens populations adapted to grow in metalliferous and non-metalliferous soils: Ni tolerance, accumulation and expression analysis of genes involved in metal homeostasis. Environ Exp Bot 105:10–17. CrossRefGoogle Scholar
  67. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets – iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182:49–84. CrossRefPubMedGoogle Scholar
  68. Wu Z, Bañuelos GS, Lin Z-Q et al (2015) Biofortification and phytoremediation of selenium in China. Front Plant Sci 6.
  69. Zhao FJ, Lombi E, McGrath SP (2003) Assessing the potential for zinc and cadmium phytoremediation with the hyperaccumulator Thlaspi caerulescens. Plant Soil 249:37–43CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • C. Sirguey
    • 1
  • G. Seznec
    • 2
  • T. Mahevas
    • 2
  • G. Echevarria
    • 1
  • C. Gonneau
    • 1
  • T. Sterckeman
    • 1
  1. 1.Université de Lorraine, Inra, Laboratoire Sols et EnvironnementNancyFrance
  2. 2.Conservatoire & Jardins Botaniques de NancyVillers-lès-NancyFrance

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