Skip to main content
Log in

Using phytostabilisation to conserve threatened endemic species in southeastern Democratic Republic of the Congo

  • Special Feature
  • Ultramafic Ecosystems: Proceedings of the 9th International Conference on Serpentine Ecology
  • Published:
Ecological Research

Abstract

Outcrops in the southeastern Democratic Republic of the Congo (DRC) are recognized as some of the largest copper–cobalt orebodies in the world. They support a unique vegetation with nearly 600 metallophytes that include rare and endemic species. Mineral exploitation has increased considerably in the region since the 1900s, affecting both environmental and public health. Phytostabilisation of polluted areas represents an opportunity to decrease the bioavailability of heavy metals in the highly polluted soils that result from ore extraction. Such a technique has been successfully implemented near Lubumbashi with the grass Microchloa altera. However, long-term maintenance requires a good understanding of interspecific relationships, such as competition and facilitation. This study tested the establishment success of four herbaceous species from the Katangan Copperbelt by assessing the potential role of Microchloa altera as a nurse species. Two annual and two perennial species were sown in an experiment designed to study the influence of soil amendment and vegetation cover on seedling emergence, growth, and survival. These variables were monitored during the vegetation growing season as well as resprouting success for perennials. Microchloa altera showed a distinct effect on the emergence and survival of annual and perennial species and negatively affected the growth of individuals belonging to both groups of species.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Bader MY, Van Geloof I, Rietkerk M (2007) High solar radiation hinders tree regeneration above the alpine treeline in northern Ecuador. Plant Ecol 191:33–45. https://doi.org/10.1007/s11258-006-9212-6

    Article  Google Scholar 

  • Baker AJM, Ernst WHO, 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 L, Hallberg K (eds) Ecology of industrial pollution. Cambridge University Press, Cambridge, pp 7–40

    Chapter  Google Scholar 

  • Banza CLN, Nawrot TS, Haufroid V, Decrée S, De Putter T, Smolders E, Kabyla BI, Luboya ON, Ilunga AN, Mutombo AM, Nemery B (2009) High human exposure to cobalt and other metals in Katanga, a mining area of the Democratic Republic of Congo. Environ Res 109:745–752. https://doi.org/10.1016/j.envres.2009.04.012

    Article  PubMed  CAS  Google Scholar 

  • Battogtokh B, Lee JM, Woo N (2013) Contamination of water and soil by the Erdenet copper–molybdenum mine in Mongolia. Environ Earth Sci 71:3363–3374. https://doi.org/10.1007/s12665-013-2727-y

    Article  CAS  Google Scholar 

  • Beltrán E, Valiente-Banuet A, Verdú M (2012) Trait divergence and indirect interactions allow facilitation of congeneric species. Ann Bot 110:1369–1376. https://doi.org/10.1093/aob/mcs089

    Article  PubMed  PubMed Central  Google Scholar 

  • Berti WR, Cunningham SD (2000) Phytostabilization of metals. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean-up the environment. Wiley, New York, pp 71–88

    Google Scholar 

  • Blacksmith Institute (2007) The World’s Worst Polluted Places: The Top Ten of The Dirty Thirty. Blacksmith Institute, New York

    Google Scholar 

  • Boisson S, Le Stradic S, Collignon J, Séleck M, Malaisse F, Shutcha MN, Faucon MP, Mahy G (2016a) Potential of copper-tolerant grasses to implement phytostabilisation strategies on polluted soils in South DR Congo: Poaceae candidates for phytostabilisation. Environ Sci Pollut Res 23:13693–13705. https://doi.org/10.1007/s11356-015-5442-2

    Article  CAS  Google Scholar 

  • Boisson S, Le Stradic S, Commans M, Dumont A, Leclerc N, Thomas C, Mahy G (2016b) Copper tolerance of three Crotalaria species from southeastern DR Congo at the early development stage. Biotechnol Agron Soc Environ 20:151–160

    CAS  Google Scholar 

  • Boisson S, Faucon M-P, Le Stradic S, Lange B, Verbruggen N, Garin O, Wetshy AT, Séleck M, Kalenga WM, Shutcha MN, Mahy G (2017) Specialized edaphic niches of threatened copper endemic plant species in the DR Congo: implications for ex situ conservation. Plant Soil 413:261–273. https://doi.org/10.1007/s11104-016-3095-7

    Article  CAS  Google Scholar 

  • Bonanomi G, Incerti G, Mazzoleni S (2011) Assessing occurrence, specificity, and mechanisms of plant facilitation in terrestrial ecosystems. Plant Ecol 212:1777–1790. https://doi.org/10.1007/s11258-011-9948-5

    Article  Google Scholar 

  • Bradshaw A, Chadwick M (1980) The restoration of land: the ecology and reclamation of derelict and degraded land. University of California Press, Berkeley and Los Angeles

    Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F, Armas C, Coll L, Corcket E, Delzon S, Forey E, Kikvidze Z, Olofsson J, Pugnaire F, Quiroz CL, Saccone P, Schiffers K, Seifan M, Touzard B, Michalet R (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34. https://doi.org/10.1111/j.1365-2745.2007.01295.x

    Article  Google Scholar 

  • Cailteux JLH, Kampunzu AB, Lerouge C, Kaputo AK, Milesi JP (2005) Genesis of sediment-hosted stratiform copper–cobalt deposits, central African Copperbelt. J Afr Earth Sci 42:134–158. https://doi.org/10.1016/j.jafrearsci.2005.08.001

    Article  CAS  Google Scholar 

  • Callaway RM (2007) Positive interactions and interdependence in plant communities. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6224-7

    Book  Google Scholar 

  • Callaway RM, Lawrence WR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Cheyns K, Nkulu CBL, Ngombe LK, Asosa JN, Haufroid V, De Putter T, Nawrot T, Kimpanga CM, Numbi OL, Ilunga BK, Nemery B, Smolders E (2014) Pathways of human exposure to cobalt in Katanga, a mining area of the DR Congo. Sci Total Environ 490:313–321. https://doi.org/10.1016/j.scitotenv.2014.05.014

    Article  PubMed  CAS  Google Scholar 

  • Córdova S, Neaman A, González I, Ginocchio R, Fine P (2011) The effect of lime and compost amendments on the potential for the revegetation of metal-polluted, acidic soils. Geoderma 166:135–144. https://doi.org/10.1016/j.geoderma.2011.07.022

    Article  CAS  Google Scholar 

  • Donath TW, Bissels S, Hölzel N, Otte A (2007) Large scale application of diaspore transfer with plant material in restoration practice—impact of seed and microsite limitation. Biol Conserv 138:224–234. https://doi.org/10.1016/j.biocon.2007.04.020

    Article  Google Scholar 

  • Duvigneaud P, Denaeyer-De Smet S (1963) Etudes sur la végétation du Katanga et de ses sols métallifères. Communication n°7 Cuivre et végétation au Katanga. Bull la Société R Bot Belgique 96:93–231

    Google Scholar 

  • Duvigneaud P, Timperman J (1959) Etudes sur la végétation du Katanga et de ses sols métallifères. Communication n°3 Etudes sur le genre Crotalaria. Bull la Société R Bot Belgique 91:135–176

    Google Scholar 

  • Faucon M-P, Colinet G, Mahy G, Luhembwe MN, Verbruggen N, Meerts P (2009) Soil influence on Cu and Co uptake and plant size in the cuprophytes Crepidorhopalon perennis and C. tenuis (Scrophulariaceae) in SC Africa. Plant Soil 317:201–212. https://doi.org/10.1007/s11104-008-9801-3

    Article  CAS  Google Scholar 

  • Faucon M-P, Meersseman A, Shutcha MN, Mahy G, Luhembwe MN, Malaisse F, Meerts P (2010) Copper endemism in the Congolese flora: a database of copper affinity and conservational value of cuprophytes. Plant Ecol Evol 143:5–18. https://doi.org/10.5091/plecevo.2010.411

    Article  Google Scholar 

  • Faucon M-P, Parmentier I, Colinet G, Mahy G, Luhembwe MN, Meerts P (2011) May rare metallophytes benefit from disturbed soils following mining activity? The case of the Crepidorhopalon tenuis in Katanga (DR Congo). Restor Ecol 19:333–343. https://doi.org/10.1111/j.1526-100X.2009.00585.x

    Article  Google Scholar 

  • Faucon M-P, Chipeng F, Verbruggen N, Mahy G, Colinet G, Shutcha M, Pourret O, Meerts P (2012) Copper tolerance and accumulation in two cuprophytes of South Central Africa: Crepidorhopalon perennis and C. tenuis (Linderniaceae). Environ Exp Bot 84:11–16. https://doi.org/10.1016/j.envexpbot.2012.04.012

    Article  CAS  Google Scholar 

  • François A (1973) L’extrémité occidentale de l’Arc Cuprifère Shabien. Etude géologique-Département de géologie de la Gécamines, Likasi (République du Zaire)

    Google Scholar 

  • Frérot H, Lefèbvre C, Gruber W, Collin C, Santos Dos A, Escarré J (2006) Specific interactions between local metallicolous plants improve the phytostabilization of mine soils. Plant Soil 282:53–65. https://doi.org/10.1007/s11104-005-5315-4

    Article  CAS  Google Scholar 

  • Furini A (2012) Plants and heavy metals. Springer, Dordrecht

    Book  Google Scholar 

  • Gan J, Xiong Z-T, Li J-P, Chen D-Q (2013) Differential response to copper stress in the reproductive resources and allocation of metallophyte Kummerowia stipulacea. Ecotoxicol Environ Saf 89:204–211. https://doi.org/10.1016/j.ecoenv.2012.11.033

    Article  PubMed  CAS  Google Scholar 

  • Garnier E (1992) Growth analysis of congeneric annual and perennial grass species. J Ecol 80:665–675. https://doi.org/10.2307/2260858

    Article  Google Scholar 

  • Gonnelli C, Galardi F, Gabbrielli R (2001) Nickel and copper tolerance and toxicity in three Tuscan populations of Silene paradoxa. Physiol Plant 113:507–514. https://doi.org/10.1034/j.1399-3054.2001.1130409.x

    Article  CAS  Google Scholar 

  • Ilunga wa Ilunga E, Mahy G, Piqueray J, Séleck M, Shutcha MN, Meerts P, Faucon M-P (2015) Plant functional traits as a promising tool for the ecological restoration of degraded tropical metal-rich habitats and revegetation of metal-rich bare soils: a case study in copper vegetation of Katanga, DRC. Ecol Eng 82:214–221. https://doi.org/10.1016/j.ecoleng.2015.04.084

    Article  Google Scholar 

  • International Council on Mining and Minerals (ICMM) (2006) Good practice guidance for mining and biodiversity. ICMM, London

    Google Scholar 

  • Järup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. https://doi.org/10.1093/bmb/ldg032

    Article  PubMed  Google Scholar 

  • Kacprzak M, Grobelak A, Grosser A, Prasad MNV (2014) Efficacy of biosolids in assisted phytostabilization of metalliferous acidic sandy soils with five grass species. Int J Phytoremediation 16:593–608. https://doi.org/10.1080/15226514.2013.798625

    Article  PubMed  CAS  Google Scholar 

  • Ke W, Xiong Z, Chen S, Chen J (2007) Effects of copper and mineral nutrition on growth, copper accumulation and mineral element uptake in two Rumex japonicus populations from a copper mine and an uncontaminated field sites. Environ Exp Bot 59:59–67. https://doi.org/10.1016/j.envexpbot.2005.10.007

    Article  CAS  Google Scholar 

  • Kucak A, Blanuša M (1998) Comparison of two extraction procedures for determination of trace metals in soil by atomic absorption spectrometry. Arh Hig Rada Toksikol 49:327–334

    PubMed  CAS  Google Scholar 

  • Lakanen E, Erviö R (1971) A comparison of eight extractants for the determination of plant available micronutrients in soil. Acta Agral Fenn 123:223–232

    Google Scholar 

  • Le Stradic S, Séleck M, Lebrun J, Boisson S, Handjila G, Faucon MP, Enk T, Mahy G (2016) Comparison of translocation methods to conserve metallophyte communities in the Southeastern DR Congo. Environ Sci Pollut Res 23:13681–13692. https://doi.org/10.1007/s11356-015-5548-6

    Article  CAS  Google Scholar 

  • Leteinturier B (2002) Evaluation du potential phytocénotique des gisements cupriferes d’Afrique centro-australe en vue de la phytoremédiation de sites pollués par l’activité minière. Faculté des Sciences Agronomiques de Gembloux, Belgium

  • Levine JM (2013) Complex interactions in a streamside plant community. Ecology 81:3431–3444

    Article  Google Scholar 

  • Li X, Poon CS, Liu PS (2001) Heavy metal contamination of urban soils and street dusts in Hong Kong. Appl Geochem 16:1361–1368. https://doi.org/10.1016/S0883-2927(01)00045-2

    Article  CAS  Google Scholar 

  • Lorestani B, Cheraghi M, Yousefi N (2011) Phytoremediation potential of native plants growing on a heavy metals contaminated soil of copper mine in Iran. World Acad Sci Eng Technol 5:341–346

    Google Scholar 

  • Malaisse F, Schaijes M, D’Outreligne C (2016) Copper–cobalt flora of upper Katanga and Copperbelt: Field Guide. Les Presses agronomiques de Gembloux

  • Manda B, Colinet G, André L (2010) Evaluation de la contamination de la chaîne trophique par les éléments traces (Cu, Co, Zn, Pb, Cd, U, V et As) dans le bassin de la Lufira supérieure (Katanga/. Tropicultura 246–252

  • Margesin R, Schinner F (2005) Manual for soil analysis—monitoring and assessing soil bioremediation. Soil Biology, vol 5. Springer Verlag, Berlin, p 359

  • Mench M, Vangronsveld J, Lepp N, Bleeker P, Ruttens A, Geebelen W (2006) Phytostabilisation of metal-contaminated sites. In: Morel J-L, Echevarria G, Goncharova N (eds) Phytoremediation of metal-contaminated soils. Springer, Trest, pp 109–190

    Chapter  Google Scholar 

  • Mench M, Lepp N, Bert V, Schwitzguébel JP, Gawronski SW, Schröder P, Vangronsveld J (2010) Successes and limitations of phytotechnologies at field scale: outcomes, assessment and outlook from COST Action 859. J Soils Sediments 10:1039–1070. https://doi.org/10.1007/s11368-010-0190-x

    Article  CAS  Google Scholar 

  • Mendez MO, Maier RM (2008) Phytostabilization of mine tailings in arid and semiarid environments—an emerging remediation technology. Environ Health Perspect 116:278–283. https://doi.org/10.1289/ehp.10608

    Article  PubMed  CAS  Google Scholar 

  • Narendrula R, Nkongolo K, Beckett P (2012) Comparative soil metal analyses in sudbury (Ontario, Canada) and Lubumbashi (Katanga, DR-Congo). Bull Environ Contam Toxicol 88:187–192

    Article  PubMed  CAS  Google Scholar 

  • O’Dell RE, Claassen VP (2006) Relative performance of native and exotic grass species in response to amendment of drastically disturbed serpentine substrates. J Appl Ecol 43:898–908. https://doi.org/10.1111/j.1365-2664.2006.01193.x

    Article  CAS  Google Scholar 

  • Padilla FM, Pugnaire FI (2006) The role of nurse plants in the restoration of degraded environments. Front Ecol Environ 4:196–202

    Article  Google Scholar 

  • Parra A, Zornoza R, Conesa E, Gómez-López MD, Faz A (2014) Seedling emergence, growth and trace elements tolerance and accumulation by Lamiaceae species in a mine soil. Chemosphere 113:132–140. https://doi.org/10.1016/j.chemosphere.2014.04.090

    Article  PubMed  CAS  Google Scholar 

  • Parraga-Aguado I, Gonzalez-Alcaraz MN, Alvarez-Rogel J, Jimenez-Carceles FJ, Conesa HM (2013) The importance of edaphic niches and pioneer plant species succession for the phytomanagement of mine tailings. Environ Pollut 176:134–143. https://doi.org/10.1016/j.envpol.2013.01.023

    Article  PubMed  CAS  Google Scholar 

  • Prasad MS (1989) Production of copper and cobalt at Gecamines, Zaire. Miner Eng 2:521–541. https://doi.org/10.1016/0892-6875(89)90087-3

    Article  CAS  Google Scholar 

  • R Development Core Team (2010) A language and environment for statistical computing. Vienna (Austria)

  • Remon E, Bouchardon JL, Cornier B, Guy B, Leclerc JC, Faure O (2005) Soil characteristics, heavy metal availability and vegetation recovery at a former metallurgical landfill: implications in risk assessment and site restoration. Environ Pollut 137:316–323. https://doi.org/10.1016/j.envpol.2005.01.012

    Article  PubMed  CAS  Google Scholar 

  • Rengel Z (1992) Role of calcium in aluminium toxicity. New Phytol 121:499–513. https://doi.org/10.1111/j.1469-8137.1992.tb01120.x

    Article  CAS  Google Scholar 

  • Rizzi L, Petruzzelli G, Poggio G, Guidi GV (2004) Soil physical changes and plant availability of Zn and Pb in a treatability test of phytostabilization. Chemosphere 57:1039–1046. https://doi.org/10.1016/j.chemosphere.2004.08.048

    Article  PubMed  CAS  Google Scholar 

  • Saad L, Parmentier I, Colinet G, Malaisse F, Faucon M-P, Meerts P, Mahy G (2012) Investigating the vegetation-soil relationships on the copper–cobalt rock outcrops of Katanga (DR Congo), an essential step in a biodiversity conservation plan. Restor Ecol 20:405–415. https://doi.org/10.1111/j.1526-100X.2011.00786.x

    Article  Google Scholar 

  • Secretariat of the Convention on Biological Diversity (2014) Global Biodiversity Outlook 4. Montréal

  • Séleck M, Bizoux J-P, Colinet G, Faucon M-P, Guillaume A, Meerts P, Piqueray J, Mahy G (2013) Chemical soil factors influencing plant assemblages along copper–cobalt gradients: implications for conservation and restoration. Plant Soil 373:455–469. https://doi.org/10.1007/s11104-013-1819-5

    Article  CAS  Google Scholar 

  • Semereab E, Rensonnet A, Lebrun J, Handjila G, Saad L, Parmentier I, Senterre B, Guillaume A, Weiskopf T, Malaisse F, Mahy G (2009) Biodiversity Action Plan Tenke Fungurume Mining 2007–2009. Gembloux

  • 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 209:133–142

    Article  PubMed  CAS  Google Scholar 

  • Sharma K, Basta NT, Grewal PS (2014) Soil heavy metal contamination in residential neighborhoods in post-industrial cities and its potential human exposure risk. Urban Ecosyst 18:115–132. https://doi.org/10.1007/s11252-014-0395-7

    Article  Google Scholar 

  • Sherameti I, Varma A (2015) Heavy metal contamination of soils: monitoring and remediation. Soil Biology. Springer International Publishing, Switzerland. https://doi.org/10.1007/978-3-319-14526-6

  • Shutcha MN, Mubemba MM, Faucon M-P, Luhembwe MN, Visser M, Colinet G, Meerts P (2010) Phytostabilisation of copper-contaminated soil in Katanga: an experiment with three native grasses and two amendments. Int J Phytoremediation 12:616–632. https://doi.org/10.1080/15226510903390411

    Article  PubMed  CAS  Google Scholar 

  • Shutcha MN, Faucon M-P, Kissi CK, Colinet G, Mahy G, Luhembwe MN, Visser M, Meerts P (2015) Three years of phytostabilisation experiment of bare acidic soil extremely contaminated by copper smelting using plant biodiversity of metal-rich soils in tropical Africa (Katanga, DR Congo). Ecol Eng 82:81–90. https://doi.org/10.1016/j.ecoleng.2015.04.062

    Article  Google Scholar 

  • Soliveres S, DeSoto L, Maestre FT, Olano JM (2010) Spatio-temporal heterogeneity in abiotic factors modulate multiple ontogenetic shifts between competition and facilitation. Perspect Plant Ecol Evol Syst 12:227–234. https://doi.org/10.1016/j.ppees.2010.02.003

    Article  Google Scholar 

  • Tembo BD, Sichilongo K, Cernak J (2006) Distribution of copper, lead, cadmium and zinc concentrations in soils around Kabwe town in Zambia. Chemosphere 63:497–501. https://doi.org/10.1016/j.chemosphere.2005.08.002 (Elsevier)

    Article  PubMed  CAS  Google Scholar 

  • Van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, Van de Voorde TFJ, Wardle DA (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054

    Article  Google Scholar 

  • Wang J, Ge Y, Chen T, Bai Y, Qian BY, Zhang CB (2014) Facilitation drives the positive effects of plant richness on trace metal removal in a biodiversity experiment. PLoS One 9:e93733. https://doi.org/10.1371/journal.pone.0093733

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whiting SN, Reeves RD, Richards D, Johnson MS, Cooke JA, Malaisse F, Johns R, Mcintyre T, Purvis OW, Salt DE, Schat H, Zhao FJ, Baker AJM (2004) Research priorities for conservation of metallophyte biodiversity and their potential for restoration and site remediation. Restor Ecol 12:106–116

    Article  Google Scholar 

  • Wyn Jones RG, Lunt OR (1967) The function of calcium in plants. Bot Rev 33:407–426

    Article  Google Scholar 

  • Zhang X, Xia H, Li Z, Zhuang P, Gao B (2010) Potential of four forage grasses in remediation of Cd and Zn contaminated soils. Bioresour Technol 101:2063–2066. https://doi.org/10.1016/j.biortech.2009.11.065

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The research was made possible thanks to the financial input of the Fonds de la Recherche dans l’Industrie et dans l’Agriculture (FRIA) of the FNRS (Fonds National de la Recherche Scientifique), Belgium. Sylvain Boisson was an FNRS PhD student. The authors also thank Tenke Fungurume Mining SARL (TFM, Freeport McMoran Copper & Gold) for the seeds of endemic species. The Coopération Universitaire au Développement (CUD) is acknowledged for the funding support of the seedbank of the Faculty of Agronomy in the University of Lubumbashi (PIC REMEDLU) and the fellowship of Julien Collignon and Olivier Garin who performed their Master theses in the DRC. The authors also gratefully acknowledge Benjamin Delory, from the Leuphana University, Lüneburg for the scientific and English formulation advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sylvain Boisson.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boisson, S., Séleck, M., Le Stradic, S. et al. Using phytostabilisation to conserve threatened endemic species in southeastern Democratic Republic of the Congo. Ecol Res 33, 789–798 (2018). https://doi.org/10.1007/s11284-018-1604-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-018-1604-2

Keywords

Navigation