Skip to main content
SpringerLink
Log in

Strategies of heavy metal uptake by three Armeria species growing on different geological substrates in Serbia

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

This study surveyed three species of the genus Armeria Willd. from five ultramafic outcrops, two non-ultramafic (schist) soils, and one tailing heap of an abandoned iron-copper mine from Serbia. Similarities and differences among the three Armeria species growing on different geological substrates in the ability to control uptake and translocate nine metals were examined. Chemical characteristics of the soil and plant samples (concentrations of P2O5, K2O, Ca, Fe, Mn, Ni, Zn, Cu, Cr, Co, Cd, and Pb) are presented. In order to assess accumulative potential of these three Armeria species, biological concentration, accumulation, as well as translocation factors were used. Three investigated Armeria species growing on eight different localities showed large differences in heavy metal uptake, translocation, and accumulation. The differences were present among the plant samples of the same species and even more among three different Armeria species and were primarily the result of the different contents of available heavy metals in the investigated soils. Additionally, differences might be the consequence of diverse responses and possible presence of supplementary resistance mechanisms in the plants from the ultramafic soils. None of the three Armeria species showed shoot hyperaccumulative potential for any of the investigated heavy metals and they could be considered as root accumulators, considering their potential to accumulate medium to large amounts of Zn (BCF up to 134), Cr (BCF up to 148), and Cd (BCF up to 9) in their roots.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Alexeeva-Popova NV, Drozdova IV (2013) Micronutrient composition of plants in the Polar Urals under contrasting geochemical conditions. Russ J Ecol 44(2):100–107

    Article  CAS  Google Scholar 

  • Ančev M (1982) Armeria Willd. In: Velčev V, Kožuharov S (eds) Flora na Narodna Republika Bălgaria 8. Bălgarskata Akademija na naukite, Sofija, pp 345–349 [In Bulgarian]

    Google Scholar 

  • Anonymous (2009) Prostorni plan područja posebne namene Nacionalnog parka Kopaonik. ‘Službeni glasnik RS’ 72/09, Beograd

  • Babalonas D, Karataglis S, Kabassakalis V (1984) The ecology of plant populations growing on serpentine soils. Phyton (Austria) 24(2):225–238

    Google Scholar 

  • Babović M, Cvetković D (1976) Osnovna geološka karta SFRJ 1:100000, List Trgovište. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3(1–4):643–654

    Article  CAS  Google Scholar 

  • Baker AJM, Walker PL (1990) Ecophysiology of metal uptake by tolerant plants. In: Shaw AJ (ed) Heavy metal tolerance in plants. CRC Press, Boca Raton, pp 155–177

    Google Scholar 

  • Baker AJM, Whiting SN (2002) In search of the Holy Grail—a further step in understanding metal hyperaccumulation? New Phytol 155(1):1–4

    Article  Google Scholar 

  • Baker AJM, Ernst WHO, van der Ent A, Malaisse F, Ginocchio R (2010) Metallophytes: the unique biological resource, its ecology and conservation status in Europe, Central Africa, and Latin America. In: Batty LC, Hallberg KB (eds) Ecology of industrial pollution. Cambridge University Press, New York, pp 7–40

    Chapter  Google Scholar 

  • Bani A, Pavlova D, Echevarria G, Mullaj A, Reeves RD, Morel JL, Sulçe S (2010) Nickel hyperaccumulation by the species of Alyssum and Thlaspi (Brassicaceae) from the ultramafic soils of the Balkans. Bot Serb 34(1):3–14

    Google Scholar 

  • Baycu G, Tolunay D, Özden H, Günebakan S (2006) Ecophysiological and seasonal variations in Cd, Pb, Zn, and Ni concentrations in the leaves of urban deciduous trees in Istanbul. Environ Pollut 143(3):545–554

    Article  CAS  Google Scholar 

  • Bokhari MH, Edmondson JR (1982) Goniolimon Boiss. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands 7. Edinburgh University Press, Edinburgh, p 477

    Google Scholar 

  • Brej T, Fabiszewski J (2006) Plants accumulating heavy metals in the Sudety Mts. Acta Soc Bot Pol 75(1):61–68

    Article  CAS  Google Scholar 

  • Brewin LE, Mehra A, Lynch PT, Farago ME (2003) Mechanisms of copper tolerance by Armeria maritima in Dolfrwynog bog, North Wales—initial studies. Environ Geochem Health 25:147–156

    Article  CAS  Google Scholar 

  • Brooks RR (1987) Serpentine and its vegetation: a multidisciplinary approach. Dioscorides Press, Portland

    Google Scholar 

  • Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc R Soc London Ser B Biol Sci 200(1139):217–224

    Article  CAS  Google Scholar 

  • Buzurović U, Jakovljević K, Niketić M, Senić T, Tomović G (2015) Genus Armeria Willd. (Plumbaginaceae) in Serbia based on two herbarium collections in Belgrade. Bull Nat Hist Mus Belgrade 8:75–86

    Google Scholar 

  • Chen PS Jr, Toribara TT, Warner H (1956) Microdetermination of phosphorus. Anal Chem 28(11):1756–1758

    Article  CAS  Google Scholar 

  • Colzi I, Arnetoli M, Gallo A, Doumett S, Del Bubba M, Pignattelli S, Gonnelli C (2012) Copper tolerance strategies involving the root cell wall pectins in Silene paradoxa L. Environ Exp Bot 78:91–98

    Article  CAS  Google Scholar 

  • Colzi I, Rocchi S, Rangoni M, Del Bubba M, Gonnelli C (2014) Specificity of metal tolerance and use of excluder metallophytes for the phytostabilization of metal polluted soils: the case of Silene paradoxa L. Environ Sci Pollut Res 21(18):10960–10969

    Article  CAS  Google Scholar 

  • Dahmani-Muller H, van Oort F, Gélie B, Balabane B (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238

    Article  CAS  Google Scholar 

  • Davies BE (1995) Lead. In: Alloway BJ (ed) Heavy metals in soils. Blackie Academic, London, pp 206–223

    Chapter  Google Scholar 

  • Ducić V, Milovanović M (2005) Klima Srbije. Zavod za udžbenike i nastavna sredstva, Beograd [In Serbian]

    Google Scholar 

  • Đurović S, Jakovljević K, Buzurović U, Niketić M, Mihailović N, Tomović G (2016) Differences in trace element profiles of three subspecies of Silene parnassica (Caryophyllaceae) growing on ophiolitic substrate. Aust J Bot 64(3):235–245

    Google Scholar 

  • Egnér H, Riehm H, Domingo WR (1960) Untersuchungen über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nährstoffzustandes der Böden. II. Chemische Extraktionsmethoden zur Phosphor-und Kaliumbestimmung. Kungl Lantbrukshögskolans Ann 26:199–215

    Google Scholar 

  • van der Ent A (2007) Possibilities for restoration of the zinc flora in the upper Geul valley (in Dutch). De Levende Natuur 108:14–19

    Google Scholar 

  • 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 362:319–334

    Article  CAS  Google Scholar 

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Ernst WHO (1974) Schwermetallvegetation der Erde. Gustav Fisher Verlag, Stuttgart

    Google Scholar 

  • Ernst WHO (1982) Schwermetallpflanzen. In: Kinzel H (ed) Pflanzenökologie und Mineralstoffwechsel. Ulmer, Stuttgart, pp 472–506

    Google Scholar 

  • Ernst WHO (1998) Effects of heavy metals in plants at the cellular and organismic level. In: Schuurmann G (ed) Ecotoxicology: ecological fundamentals, chemical exposure and biological effects. Wiley, Heidelberg, pp 587–620

    Google Scholar 

  • FAO (1974) The Euphrates pilot irrigation project. Methods of soil analysis. Gadeb soil laboratory (a laboratory manual). Food and Agriculture Organization

  • Farago ME, Mullen WA, Cole MM, Smith RF (1980) A study of Armeria maritima (Mill.) Willdenow growing in a copper-impregnated bog. Environ Pollut 21(3):225–244

    Article  CAS  Google Scholar 

  • Filipović I, Pavlović Z, Marković B, Radin V, Marković O, Gagić N, Atin B, Milićević M (1967) Osnovna geološka karta SFRJ 1:100000, List Gornji Milanovac. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Freitas H, Prasad MNV, Pratas J (2004) Analysis of serpentinophytes from north-east of Portugal for trace metal accumulation—relevance to the management of mine environment. Chemosphere 54:1625–1642

    Article  CAS  Google Scholar 

  • Gajić M (1972) Plumbaginaceae Lindl. In: Josifović M (ed) Flora SR Srbije 3. Srpska Akademija nauka i umetnosti, Beograd, pp 90–98 [In Serbian]

    Google Scholar 

  • Greger M (1999) Metal availability and bioconcentration in plants. In: Prasad MNV, Hagemeyer J (eds) Heavy metal stress in plants. Springer, Berlin, pp 1–27

    Google Scholar 

  • Group of authors (1970) Osnovna geološka karta SFRJ 1:100000, List Novi Pazar. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Group of authors (1973) Osnovna geološka karta SFRJ 1:100000, List Kumanovo. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Henriques FS (2002) Heavy metal content of spoil heaps from an abandoned iron- and copper-mine and metal accumulation in Armeria linkiana Nieto Feliner. Bull Environ Contam Toxicol 68:555–560

    Article  CAS  Google Scholar 

  • Hijmans RJ, Guarino L, Mathur P (2012) DIVA-GIS version 7.5. http://www.diva-gis.org/. Accessed 22 Aug 2017

  • Hobbs RJ, Streit B (1986) Heavy metal concentrations in plants growing on a copper mine spoil in the Grand Canyon, Arizona. Am Midl Nat 115:277–281

    Article  CAS  Google Scholar 

  • ISO 11047 (1998) Soil quality—determination of cadmium, chromium, cobalt, copper, lead, manganese, nickel and zinc—flame and electrothermal atomic absorption spectrometric methods. International Standard Organization, Geneva

    Google Scholar 

  • ISO 11466 (1995) International standard. Soil quality—extraction of trace elements soluble in aqua regia, 03–01

  • ISO 3166/2 (1998) Codes for the representation of names of countries and their subdivisions—part 2: country subdivision code. International Standard Organization, Geneva

    Google Scholar 

  • ISO 6636/2 (1981) International Standard. Fruits, vegetables and derived products—determination of zinc content—part 2: atomic absorption spectrometric method

  • Jakovljević K, Buzurović U, Andrejić G, Đurović S, Niketić M, Mihailović N, Tomović G (2015) Trace elements contents and accumulation in soils and plant species Goniolimon tataricum (L.) Boiss. (Plumbaginaceae) from the ultramafic and dolomitic substrates of the central Balkans. Carpathian J Earth Environ Sci 10(1):147–160

    Google Scholar 

  • Johnston WR, Proctor J (1977) Metal concentrations in plants and soils from two British serpentine sites. Plant Soil 46:275–278

    Article  CAS  Google Scholar 

  • Kabata-Pendias A (2011) Trace elements in soils and plants, 4th edn. CRC Press, Taylor & Francis Group, Boca Raton, London, New York

    Google Scholar 

  • Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    CAS  Google Scholar 

  • Kazakou E, Adamidis GC, Baker AJ, Reeves RD, Godino M, Dimitrakopoulos PG (2010) Species adaptation in serpentine soils in Lesbos Island (Greece): metal hyperaccumulation and tolerance. Plant Soil 332(1–2):369–385

    Article  CAS  Google Scholar 

  • Kruckeberg AR (2002) Geology and plant life: the effects of landforms and rock type on plants. University Washington Press, Seattle/London

    Google Scholar 

  • Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105

    Article  CAS  Google Scholar 

  • Malik RN, Husain SZ, Nazir I (2010) Heavy metal contamination and accumulation in soil and wild plant species from industrial area of Islamabad, Pakistan. Pak J Bot 42(1):291–301

    CAS  Google Scholar 

  • Markert B (1995) Sample preparation (cleaning, drying, homogenization) for trace element analysis in plant matrices. Sci Total Environ 176:45–61

    Article  CAS  Google Scholar 

  • Martin MH, Coughtrey PJ (1982) Biological indicators of natural ore-bodies: geobotanical and biogeochemical prospecting for heavy metal deposits. In: Martin MH, Coughtrey PJ (eds) Biological monitoring of heavy metal pollution. Land and air. Applied Science Publishers Ltd, London, New York, pp 34–59

    Chapter  Google Scholar 

  • Matko Stamenković U, Andrejić G, Mihailović N, Šinžar-Sekulić J (2017) Hyperaccumulation of Ni by Alyssum murale Waldst. & Kit. from ultramafics in Bosnia and Herzegovina. Appl Ecol Environ Res 15(3):359–372

    Article  Google Scholar 

  • McGrath D (1996) Application of single and sequential extraction procedures to polluted and unpolluted soils. Sci Total Environ 178(1):37–44

    Article  CAS  Google Scholar 

  • McKeague JA (1978) Manual on soil sampling and methods of analysis. Canadian Society of Soil Science

  • Merhaut DJ (2007) Magnesium. pp. 145–181. In: Barker AV, Pilbeam DJ (eds.) Handbook of plant nutrition, CRC Press, Taylor & Francis Group, Boca Raton, London New York

  • Mertz W, Angino EE, Cannon HL, Hambidge KM, Voors AW (1974) Chromium. In: Mertz W (ed) US National Committee for Geochemistry. Subcommittee on the Geochemical Environment. Geochemistry and the Environment. Volume I. The Relation of Selected Trace Elements to Health and Disease. National Academy of Sciences. pp. 29–35

  • Micevski K, Matevski V (1995) Armeria Willd. In: Micevski K (ed) Flora na Republika Makedonija 1(3): 474–479. Makedonska Akademija na naukite i umetnostite, Skopje. [In Macedonian]

  • Mojsilović S, Baklajić D, Đoković I (1977) Osnovna geološka karta SFRJ 1:100000, List Titovo Užice. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Mojsilović S, Baklajić D, Đoković I (1978) Osnovna geološka karta SFRJ 1:100000, List Sjenica. Savezni geološki zavod, Beograd [In Serbian]

    Google Scholar 

  • Neumann D, Nieden UZ, Lichtenberger O, Leopold I (1995) How does Armeria maritima tolerate high heavy metal concentrations? J Plant Physiol 146(5):704–717

    Article  CAS  Google Scholar 

  • Panda SK, Choudhury S (2005) Chromium stress in plants. Braz J Plant Physiol 17(1):95–102

    Article  CAS  Google Scholar 

  • Pollard AJ, Reeves RD, Baker AJM (2014) Facultative hyperaccumulation of heavy metals and metalloids. Plant Sci 217–218:8–17

    Article  CAS  Google Scholar 

  • Pourret O, Lange B, Bonhoure J, Colinet G, Decrée S, Mahy G, Séleck M, Shutcha M, Faucon M-P (2016) Assessment of soil metal distribution and environmental impact of mining in Katanga (Democratic Republic of Congo). Appl Geochem 64:43–55

    Article  CAS  Google Scholar 

  • Proctor J (1999) Toxins, nutrient shortages and droughts: the serpentine challenge. Trends Ecol Evol 14(9):334–335

    Article  Google Scholar 

  • van Reeuwijk LP (2002) Procedures for soil analysis. 6th ed. Technical Paper 9. International Soil Reference and Information Centre, Wageningen. Available at http://www.isric.org/Isric/Webdocs/Docs/ISRIC_TechPap09_2002.pdf

  • Reeves R (1992) Hyperaccumulation of nickel by serpentine plants. In: Proctor J, Baker A, Reeves R (eds) The vegetation of ultramafic (serpentine) soils. Intercept Ltd., Andover, pp 253–277

    Google Scholar 

  • Reeves RD (2006) Hyperaccumulation of trace elements by plants. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Dordrecht, pp 25–52

    Chapter  Google Scholar 

  • 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. John Wiley & Sons, Inc., New York, pp 193–229

    Google Scholar 

  • Reeves RD, Baker AJM, Borhidi A, Berazain R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83(1):29–38

    Article  CAS  Google Scholar 

  • StatSoft, Inc. (2004) STATISTICA (Data Analysis Software System), Version 7.0. www.statsoft.com. Tulsa, USA

  • Stevanović V, Tan K, Iatrou G (2003) Distribution of the endemic Balkan flora on serpentine I.—obligate serpentine endemics. Plant Syst Evol 242(1–4):149–170

    Article  Google Scholar 

  • Stoltz E, Greger M (2002) Accumulation properties of As, Cd, Cu, Pb and Zn by four wetland plant species growing on submerged mine tailings. Environ Exp Bot 47(3):271–280

    Article  CAS  Google Scholar 

  • Szarek-Łukaszewska G, Słysz A, Wierzbicka M (2004) Response of Armeria maritima (Mill.) Willd. to Cd, Zn and Pb. Acta Biol Cracoviensia Ser Bot 46:19–24

    Google Scholar 

  • Talukder G, Sharma A (2007) Cobalt. In: Barker AV, Pilbeam DJ (eds) Handbook of plant nutrition. CRC Press, Taylor & Francis Group, Boca Raton, London New York, pp 499–514

    Google Scholar 

  • Thiers B (2017) Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available at http://sweetgum.nybg.org/ih (continuously updated)

  • Tomović GM, Mihailović NL, Tumi AF, Gajić BA, Mišljenović TD, Niketić MS (2013) Trace metals in soils and several Brassicaceae plant species from serpentine sites of Serbia. Arch Environ Prot 39(4):29–49

    Article  Google Scholar 

  • Tumi AF, Mihailović N, Gajić BA, Niketić M, Tomović G (2012) Comparative study of hyperaccumulation of nickel by Alyssum murale s.l. populations from the ultramafics of Serbia. Pol J Environ Stud 21(6):1855–1866

    CAS  Google Scholar 

  • Wójcik M, Gonnelli C, Selvi F, Dresler S, Rostański A, Vangronsveld J (2017) Metallophytes of serpentine and calamine soils—their unique ecophysiology and potential for phytoremediation. Adv Bot Res 83:1–42

    Article  Google Scholar 

  • Zayed A, Lytle CM, Qian JH, Terry N (1998) Chromium accumulation, translocation and chemical speciation in vegetable crops. Planta 206(2):293–299

    Article  CAS  Google Scholar 

  • Zhao FJ, Hamon RE, Lombi E, McLaughlin MJ, McGrath SP (2002) Characteristics of cadmium uptake in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 53:535–543

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank two anonymous reviewers for their comments and suggestions on an earlier draft of this paper.

Funding

The Ministry of Education, Science and Technological Development of the Republic of Serbia supported this research through Grant 173030 “Plant biodiversity of Serbia and the Balkans—assessment, sustainable use and protection.”

Author information

Authors and Affiliations

  1. Faculty of Biology, Institute of Botany and Botanical Garden, University of Belgrade, Takovska 43, Belgrade, 11000, Serbia

    Gordana Tomović, Uroš Buzurović, Sanja Đurović & Ksenija Jakovljević

  2. Institute for the Application of Nuclear Energy—INEP, University of Belgrade, Banatska 31b, Belgrade, 11080, Serbia

    Dražen Vicić & Nevena Mihailović

Authors
  1. Gordana Tomović
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uroš Buzurović
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sanja Đurović
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dražen Vicić
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nevena Mihailović
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ksenija Jakovljević
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gordana Tomović.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomović, G., Buzurović, U., Đurović, S. et al. Strategies of heavy metal uptake by three Armeria species growing on different geological substrates in Serbia. Environ Sci Pollut Res 25, 507–522 (2018). https://doi.org/10.1007/s11356-017-0445-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-0445-9

Keywords

Search

Navigation