Abstract
Background and aims
Metallophytes are plants that can tolerate extreme metal concentrations in the soil in which they grow. The Dugald River zinc (Zn)-lead (Pb) gossan in Queensland (Australia) is one of the largest metal deposits in the world with a surface gossan formed after weathering over millions of years. It hosts a range of metallophytes which may have potential to be used in mine site rehabilitation. This study aimed to investigate the soil-plant relationships of metallophytes on the Dugald River gossan.
Methods
Plant samples and associated rooting soil samples were collected across the gossan and then analysed for metal concentrations. Soil-plant metal relationships were subsequently explored to characterise the species in relation to metal uptake behaviour.
Results
The metallophyte grass, Eriachne mucronata, dominated the gossan, yet there appeared to be no direct relationship between the occurrence of metallophytes and prevailing soil metal concentrations. Using transformation-based redundancy analysis (tb-RDA), two groups of metals, copper (Cu) and Zn-Cadmium (Cd), have been identified to be the primary metals driving species distribution. Crotalaria novae-hollandiae, was able to accumulate high concentrations of each of these metals in its leaves, with up to 16,200 mg Zn kg−1, 545 mg Cu kg−1 and 170 mg Cd kg−1.
Conclusions
Soil metal concentrations alone are not suitable indications for metallophyte distribution or composition in a polymetallic environment. Crotalaria novae-hollandiae can tolerate high concentrations of metals and accumulate Zn-Cu-Cd above the respective hyperaccumulation thresholds; the species can be described for the first time as a strong polymetallic indicator-type metallophyte.
Similar content being viewed by others
Data availability
The data underlying this article will be shared on reasonable request to the corresponding author.
Code availability
Not applicable.
References
Abubakari F, Nkrumah PN, Fernando DR, Brown GK, Erskine PD, Echevarria G, van der Ent A (2021) Incidence of hyperaccumulation and tissue-level distribution of manganese, cobalt, and zinc in the genus Gossia (Myrtaceae). Metallomics 13. https://doi.org/10.1093/mtomcs/mfab008
Baker AJM (1981) Accumulators and excluders -strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654. https://doi.org/10.1080/01904168109362867
Baker AJM (2009) Darwinian Approach to Mine Closure and Restoration. Proc Int Con Mine Clos 4:21–24
Baker AJ, Ernst WH, 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
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 155:47–57
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 29:899–890
Bivand RS, Pebesma E, Gomez-Rubio V (2013) Applied spatial data analysis with R, 2nd edn. Springer, New York
Bivand R, Keitt T, Rowlingson B (2020) rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. R package version 1.5–18. https://CRAN.R-project.org/package=rgdal. Accessed 1 Sep 2020
Bizoux JP, Daïnou K, Raspé O, Lutts S, Mahy G (2008) Fitness and genetic variation of Viola calaminaria, an endemic metallophyte: implications of population structure and history. Plant Biol 10:684–693
Blake D (1987) Geology of the Mt Isa Inlier and environs. Bur Min Res Bull 225
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632
Blissett AH (1966) Copper tolerant plants from the Ukaparinga copper mine, Williamstown. Quart Geol Notes Geol Surv S Aust 18:1–3
BOM (2021) Cloncurry Airport, station number 02141, Daily temperature and rainfall. http://www.bom.gov.au/climate/data/index.shtml. Accessed 23 May 2021
Bradshaw AD (2000) The use of natural processes in reclamation–advantages and difficulties. Landsc. Urban Plan 51:89–100
Brooks RR (1979) Indicator plants for mineral prospecting—A critique. J Geochem Explor 12:67–78
Brooks RR, McCleave JA, Malaisse F (1977) Copper and cobalt in African species of Crotalaria. L Proc R Soc Lond 197(1127):231–236
Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3(9):359–362
Brown SL, Chaney RL, Angle JS, Baker AJM (1995) Zinc and cadmium uptake by hyperaccumulator Thlaspi caerulescens grown in nutrient solution. Soil Sci Soc Am J 59(1):125–133
Chaney RL (1993) Zinc phytotoxicity. In: Robson AD (ed) Zinc in soils and plants. Springer, Dordrecht
Chaney RL, Malik M, Li YM, Brown SL, Brewer EP, Angle JS, Baker AJ (1997) Phytoremediation of soil metals. COBIOT 8(3):279–284
Cole MM (1973) Geobotanical and Biogeochemical Investigations in the Sclerophyllous Woodland and Shrub Associations of the Eastern Goldfield Area of Western Australia, with Particular Reference to the Role of Hybanthus floribundus (Lindl.) F. Muell. as a Nickel Indicator and Accumulator. Plant J Appl Ecol 1:269–320
Cole MM, Smith RF (1984) Vegetation as Indicator of Environmental Pollution. Trans Inst Br Geogr 9:477–493. https://doi.org/10.2307/621782
Cole MM, Provan DMJ, Tooms JS (1968) Geobotany, biogeochemistry and geochemistry in the Bulman-Waimuna Springs area, Northern Territory, Australia. Trans Inst Min Met Sec B 77:81–104
Craw D, Rufaut C, Haffert L, Paterson L (2007) Plant colonization and arsenic uptake on high arsenic mine wastes, New Zealand. Water Air Soil Pollut 179:351–364. https://doi.org/10.1007/s11270-006-9238-3
Ernst WH (2006) Evolution of metal tolerance in higher plants. Snow Landsc Res 80(3):251–274
Erskine P, van der Ent A, Fletcher A (2012) Sustaining metal-loving plants in mining regions. Science 337(6099):1172–1173
Esfeld K, Hensen I, Wesche K, Jakob SS, Tischew S, Blattner FR (2008) Molecular data indicate multiple independent colonizations of former lignite mining areas in Eastern Germany by Epipactis palustris (Orchidaceae). Biodiv Cons 17:2441–2453
Farago ME, Clark AJ, Pitt MJ (1977) Plants which accumulate metals. Part I. The metal content of three Australian plants growing over mineralised sites. Inorganica Chim Acta 24:53–56
Foy CD, Chaney RT, White MC (1978) The physiology of metal toxicity in plants. Ann Rev Plant Physio 29(1):511–566
Gerhardt KE, Gerwing PD, Greenberg BM (2017) Opinion: Taking phytoremediation from proven technology to accepted practice. Plant Sci 256:170–185
Ginocchio R, Toro I, Schnepf D, Macnair MR (2002) Copper tolerance in populations of Mimulus luteus var. variegatus exposed and non exposed to copper pollution. Geochem Explor Env Analy 2:151–156
Grooves RW, Stevenson BG, Stevenson EA, Taylor RG (1972) Geochemical and geobotanical studies in the Emuford district of the Herberton tin field, North Queensland, Australia. Trans Inst Min Metall (Sec B: Applied Earth Sci) 81:127–137
Hijmans RJ (2020) raster: Geographic Data Analysis and Modeling. R package version 3.3-13. https://CRAN.Rproject.org/package=raster. Accessed 1 Sep 2020
Holland AE (2002) A review of Crotalaria L. (Fabaceae: Crotalarieae) in Australia. Austrobaileya 6(2):293–324
Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 5(1):46–51
Jhee EM, Boyd RS, Eubanks MD (2006) Effectiveness of metal–metal and metal–organic compound combinations against Plutella xylostella: implications for plant elemental defense. J Chem Ecol 32(2):239–259
Krämer U (2010) Metal hyperaccumulation in plants. Ann. Rev. Plant Biol. 61:517–534
Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge
Lindsay WL, Norvell W (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper 1. Soil Sci Soc Am J 42(3):421–428
Lombi E, Zhao F, McGrath S, Young S, Sacchi G (2001) Physiological evidence for a high-affinity cadmium transporter highly expressed in a Thlaspi caerulescens ecotype. New Phytol 149:53–60
Lottermoser BG, Ashley PM, Munksgaard NC (2008) Biogeochemistry of Pb–Zn gossans, northwest Queensland, Australia: implications for mineral exploration and mine site rehabilitation. Appl Geochem 23(4):723–742
Malaisse F, Gregoire J, Brooks RR, Morrison RS, Reeves RD (1978) Aeolanthus biformifolius De Wild.: a hyperaccumulator of copper from Zaire. Science 199(4331):887–888
McGrath SP, Zhao FJ, Lombi E (2001) Plant and rhizosphere processes involved in phytoremediation of metal-contaminated soils. Plant Soil 232(1):207–214
Malaisse F, Schaijes M,D’Outreligne C (2016) Copper-cobalt Flora of Upper Katanga and Copperbelt: Field Guide. Gembloux, Les Presses Agronomiques de Gembloux (Belgium), 422 pp
Microsoft Corporation (2021) Microsoft 365 Excel Enterprise. https://www.microsoft.com/en-au/microsoft-365?rtc=1
Mogopodi D, Mosetlha K, Torto N, Wibetoe G (2008) Accumulation patterns of Cu and Ni for Indigofera melanadenia and Tephrosia longipes plant species growing in Cu–Ni mining area in Botswana. J Geochem Explor 97(1):21–28
Nicolls OW, Provan DMJ, Cole MM, Tooms JS (1965) Geobotany and geochemistry in mineral exploration in the Dugald River Area, Cloncurry District, Australia. Trans Inst Min Metall 74:695–799
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.Rproject.org/package=vegan. Accessed 1 Sep 2020
Paul AL, Erskine PD, van der Ent A (2018) Metallophytes on Zn-Pb mineralised soils and mining wastes in Broken Hill, NSW, Australia. Aust J Bot 66(2):124–133
Pebesma EJ (2004) Multivariable geostatistics in S: the gstat package. Comp Geosci 30:683–691
Pebesma E (2018) Simple Features for R: Standardized Support for Spatial Vector Data. R J 10(1):439–446. https://doi.org/10.32614/RJ-2018-009
Pebesma EJ, Bivand RS (2005) Classes and methods for spatial data in R. R News 5(2):9–13
Pollard AJ, Reeves RD, Baker AJ (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217:8–17
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/. Accessed 1 Sep 2020
Rajakaruna N, Bohm BA (2002) Serpentine and its vegetation: a preliminary study from Sri Lanka. J Appl Bot 76:20–28
Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel JL, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Dordrecht
Reeves RD, Kruckeberg AR (2018) Re-examination of the elemental composition of some Caryophyllaceae on North American ultramafic soils. Ecol Res 33(4):715–722
Reeves RD, Schwartz C, Morel JL, Edmondson J (2001) Distribution and metal-accumulating behavior of Thlaspi caerulescens and associated metallophytes in France. Int J Phytoremediat 3(2):145–172
Reeves RD, van der Ent A, Baker AJ (2018a) Global distribution and ecology of hyperaccumulator plants. In: van der Ent A, Echevarria G, Baker AJM, Morel JL (eds) Agromining: farming for metals. Springer, Cham
Reeves RD, Baker AJ, Jaffré T, Erskine PD, Echevarria G, van der Ent A (2018b) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218(2):407–411
Reisch C (2007) Genetic structure of Saxifraga tridactylites (Saxifragaceae) from natural and man-made habitats. Conserv Genet 8:893–902
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 203:47–56
Severne BC, Brooks RR (1972) A nickel accumulating plant from Western Australia. Planta 103:91–94
Smith RAH, Bradshaw AD (1972) Stabilization of toxic mine wastes by the use of tolerant plant populations. Instit. Ming Metall Bull Trans 81(791):230–237
Tang RH, Erskine PD, Lilly R, van der Ent A (2020) The biogeochemistry of copper metallophytes in the Roseby Corridor (North-West Queensland, Australia). Chemoecology 31(1):1–12
Taylor GF, Appleyard EC (1983) Weathering of the zinc-lead lode, Dugald River, northwest Queensland: I. The gossan profile. J Geochem Explor 18(2):87–110
Tennekes M (2018) tmap: Thematic Maps in R. J Stat Softw 84(6):1–39. https://doi.org/10.18637/jss.v084.i06
Tibbett M (2015) Mining in ecologically sensitive landscapes. CSIRO Publishing, Melbourne
Tordoff GM, Baker AJM, Willis AJ (2000) Current approaches to the revegetation and reclamation of metalliferous mine wastes. Chemosphere 41:219–228
van der Ent A, Baker AJ, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant soil 362(1):319–334
van der Ent A, Baker AJM, Reeves RD, Chaney RL, Anderson CWN, Meech JA, Erskine PD, Simonnot M-O, Vaughan J, Morel JL, Echevarria G, Fogliani B, Rongliang Q, Mulligan DR (2015) Agromining: Farming for metals in the future? Environ Sci Technol 49:4773–4780
Wang Y, Kanipayor R, Brindle ID (2014) Rapid high-performance sample digestion for ICP determination by ColdBlock™ digestion: part 1 environmental samples. J Anal At Spectrom 29(1):162–168
Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Paton A, Smith JAC, Angle JS, Chaney RL, Ginocchio R (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12(1):106–116
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. https://cran.rproject.org/doc/Rnews/. Accessed 1 Sep 2020
Wu C, Liao B, Wang S-L, Zhang J, Li J-T (2010) Pb and Zn accumulation in a Cd-hyperaccumulator (Viola baoshanensis). Int J Phytoremediat 12:574–585
Xu G (1996) Structural geology of the Dugald River Zn-Pb-Ag deposit, Mount Isa Inlier, Australia. Ore Geo Rev 11(6):339–361
Yang XE, Long XX, Ye HB, He ZL, Calvert DV, Stoffella PJ (2004) Cadmium tolerance and hyperaccumulation in a new Zn-hyperaccumulating plant species (Sedum alfredii Hance). Plant Soil 259(1):181–189
Funding
Roger Tang is the recipient of a UQ Graduate School Scholarship (UQGSS) from The University of Queensland. MMG Limited provided funding and operational support during the fieldwork.
Author information
Authors and Affiliations
Contributions
RHT, PDE, PNN, GE and AVDE conducted the fieldwork. RHT performed the chemical analysis of the samples and undertook the statistical analysis. All authors contributed to interpretation of data, writing of the article and final approval of the version submitted.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Conflict of interest
The authors declare no conflict of interest.
Additional information
Responsible Editor: Fangjie Zhao.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 6155 kb)
Rights and permissions
About this article
Cite this article
Tang, R.H., Erskine, P.D., Nkrumah, P.N. et al. Soil-plant relationships of metallophytes of the zinc-lead-copper Dugald River gossan, Queensland, Australia. Plant Soil 471, 227–245 (2022). https://doi.org/10.1007/s11104-021-05209-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05209-z