Plant and Soil

, Volume 413, Issue 1–2, pp 261–273 | Cite as

Specialized edaphic niches of threatened copper endemic plant species in the D.R. Congo: implications for ex situ conservation

  • Sylvain Boisson
  • Michel-Pierre Faucon
  • Soizig Le Stradic
  • Bastien Lange
  • Nathalie Verbruggen
  • Olivier Garin
  • Axel Tshomba Wetshy
  • Maxime Séleck
  • Wilfried Masengo Kalengo
  • Mylor Ngoy Shutcha
  • Grégory Mahy
Regular Article

Abstract

Background and aims

Copper (Cu) rich soils derived from rocks of the Katangan Copperbelt in the south-eastern Democratic Republic of Congo (DRC) support a rich diversity of metallophytes including 550 heavy metal tolerant; 24 broad Cu soil endemic; and 33 strict Cu soil endemic plant species. The majority of the plant species occur on prominent Cu hills scattered along the copperbelt. Heavy metal mining on the Katangan Copperbelt has resulted in extensive degradation and destruction of the Cu hill ecosystems. As a result, approximately 80 % of the strict Cu endemic plant species are classified as threatened according to IUCN criteria and represent a conservation priority. Little is known about the soil Cu tolerance optimum of the Cu endemic plant species. The purpose of this study was to quantify the soil Cu concentration (Cu edaphic niche) of four Cu endemic plant species to inform soil propagation conditions and microhabitat site selection for planting of the species in Cu hill ecosystem restoration.

Methods

The soil Cu concentration tolerance of Cu endemic plant species was studied including Crotalaria cobalticola (CRCO); Gladiolus ledoctei (GLLE); Diplolophium marthozianum (DIMA); and Triumfetta welwitschii var. rogersii (TRWE-RO). The in situ natural habitat distributions of the Cu endemic plant species with respect to soil Cu concentration (Cu edaphic niche) was calculated by means of a generalised additive model. Additionally, the seedling emergence and growth of the four Cu endemic plant species in three soil Cu concentrations was tested ex situ and the results were compared to that of the natural habitat soil Cu concentration optimum (Cu edaphic niche).

Results

CRCO exhibited greater performance on the highest soil Cu concentration, consistent with its calculated Cu edaphic niche occurring at the highest soil Cu concentrations. In contrast, both DIMA and TRWE-RO exhibited greatest performance at the lowest soil Cu concentration, despite the calculated Cu edaphic niche occurring at moderate soil Cu concentrations. GLLE exhibited equal performances in the entire range of soil Cu concentrations.

Conclusions

These results suggest that CRCO evolved via the edaphic specialization model where it is most competitive in Cu hill habitat with the highest soil Cu concentration. In comparison, DIMA and TRWE-RO appear to have evolved via the endemism refuge model, which indicates that the species were excluded into (i.e., took refuge in) the lower plant competition Cu hill habitat due to their inability to effectively compete with higher plant competition on normal soils. The soil Cu edaphic niche determined for the four species will be useful in conservation activities including informing soil propagation conditions and microhabitat site selection for planting of the species in Cu hill ecosystem restoration.

Keywords

Copper soil Heavy metal tolerance Edaphic Endemic Niche Generalised additive model Endangered plant 

References

  1. Aikaike H (1987) Factor analysis and AIC. Psychopharmacology 52:317–332Google Scholar
  2. Anacker BL (2014) The nature of serpentine endemism. Am J Bot 101:219–224. doi:10.3732/ajb.1300349 CrossRefPubMedGoogle Scholar
  3. Antonovics J, Bradshaw AD, Turner RG (1971) Heavy metal tolerance in plants. Adv Ecol Res 7:1–85CrossRefGoogle Scholar
  4. Baker AJM (1987) Metal Tolerance. New Phytol 106:93–111. doi:10.1111/j.1469-8137.1987.tb04685.x CrossRefGoogle Scholar
  5. 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. doi:10.1111/j.1438-8677.2008.00077.x CrossRefPubMedGoogle Scholar
  6. Boisson S, Collignon J, Langunu S, Lebrun J, Shutcha MN, Mahy G (2015) Concilier la phytostabilisation des sols pollués avec la conservation de la flore cupro-cobalticole dans la région de Lubumbashi (R.D. Congo) : une stratégie nouvelle pour valoriser les écosystèmes extrêmes. In: Bogart J, Halleux J-M (eds) Territoires périurbains: Développement, enjeux et perspectives dans les pays du Sud. Presses Agronomiques de Gembloux, Gembloux, pp. 127–138Google Scholar
  7. Boisson S, Ortmans W, Maréchal J, Majerus M, Mahy G, Arnaud M (2016a) No copper required for germination of an endangered endemic species from the Katangan Copperbelt (Katanga, DR Congo): Diplolophium marthozianumGoogle Scholar
  8. Boisson S, Le Stradic S, Collignon J, Séleck M, Malaisse F, Ngoy Shutcha M, Faucon MP, Mahy G (2016b) Potential of copper-tolerant grasses to implement phytostabilisation strategies on polluted soils in south D. R. Congo: Poaceae candidates for phytostabilisation. Environ Sci Pollut Res 23:13693–13705. doi:10.1007/s11356-015-5442-2 CrossRefGoogle Scholar
  9. Boisson S, Le Stradic S, Commans M, Dumont A, Leclerc N, Thomas C, Mahy G (2016c) Copper tolerance of three crotalaria species from southeastern D. R. Congo at the early development stage. Biotechnol Agron Soc Environ 20:151–160Google Scholar
  10. Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. doi:10.1007/s11104-007-9240-6 CrossRefGoogle Scholar
  11. Boyd R, Rajakaruna N (2013) Heavy metal tolerance. In: Gibson D (ed) Oxford bibliographies in ecology. Oxford University Press, New York, pp. 1–24Google Scholar
  12. Brooks R (1998) Plants that hyperaccumulate heavy metals. CAB International, Wallingford, UKGoogle Scholar
  13. Brooks RR, Malaisse F (1990) Metal-enriched sites in south central africa. In: Shaw J (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Inc, New York, pp. 53–71Google Scholar
  14. Cailteux JLH, Kampunzu AB, Lerouge C, Kaputo AK, Milesi JP (2005) Genesis of sediment-hosted stratiform copper–cobalt deposits, central African Copperbelt. J African Earth Sci 42:134–158. doi:10.1016/j.jafrearsci.2005.08.001 CrossRefGoogle Scholar
  15. Chipeng FK, Hermans C, Colinet G, Faucon M-P, Ngongo M, Meerts P, Verbruggen N (2010) Copper tolerance in the cuprophyte Haumaniastrum katangense (S. Moore) P.A. Duvign. & Plancke. Plant Soil 328:235–244. doi:10.1007/s11104-009-0105-z CrossRefGoogle Scholar
  16. Di Salvatore M, Carafa AM, Carratù G (2008) Assessment of heavy metals phytotoxicity using seed germination and root elongation tests: A comparison of two growth substrates. Chemosphere 73(9):1461–1464Google Scholar
  17. 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 96:93–231Google Scholar
  18. Eriksson O (2002) Ontogenetic niche shifts and their implications for recruitment in three clonal Vaccinium shrubs: Vaccinium myrtillus, Vaccinium vitis-idaea, and Vaccinium oxycoccos. Can J Bot 80:635–641. doi:10.1139/B02-044 CrossRefGoogle Scholar
  19. Escarré J, Lefèbvre C, Frérot H, Mahieu S, Noret N (2013) Metal concentration and metal mass of metallicolous, non metallicolous and serpentine Noccaea Caerulescens populations, cultivated in different growth media. Plant Soil 370:197–221. doi:10.1007/s11104-013-1618-z CrossRefGoogle Scholar
  20. 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. doi:10.5091/plecevo.2010.411 CrossRefGoogle Scholar
  21. Faucon M-P, Parmentier I, Colinet G, Mahy G, Ngongo Luhembwe M, Meerts P (2011) May rare metallophytes benefit from disturbed soils following mining activity? The case of the Crepidorhopalon tenuis in Katanga (D. R. Congo). Restor Ecol 19:333–343. doi:10.1111/j.1526-100X.2009.00585.x CrossRefGoogle Scholar
  22. Faucon M-P, Chipeng F, Verbruggen N, Mahy G, Colinet G, Shutcha M, Pourret O, Meerts P (2012a) Copper tolerance and accumulation in two cuprophytes of south Central Africa: Crepidorhopalon perennis and C. tenuis (Linderniaceae). Environ Exp Bot 84:11–16. doi:10.1016/j.envexpbot.2012.04.012 CrossRefGoogle Scholar
  23. Faucon M-P, Tshilong BM, Van RF, Meerts P, Decocq G, Mahy G (2012b) Ecology and hybridization potential of two sympatric metallophytes, the narrow endemic Crepidorhopalon perennis ( Linderniaceae ) and its more widespread congener. Biotropica 44:454–462CrossRefGoogle Scholar
  24. Faucon MP, Le Stradic S, Boisson S, EI w I, Séleck M, Lange B, Guillaume D, MN S, Pourret O, Meerts P, Mahy G (2016) Implication of plant-soil relationships for conservation and restoration of copper-cobalt ecosystems. Plant Soil 403:153–165. doi:10.1007/s11104-015-2745-5 CrossRefGoogle Scholar
  25. Fones H, Davis C a R, Rico A, Fang F, Smith JAC, Preston GM (2010) Metal hyperaccumulation armors plants against disease. PLoS Pathog 6:1–13. doi:10.1371/journal.ppat.1001093 CrossRefGoogle Scholar
  26. 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
  27. Furini A (ed) (2012) Plants and heavy metals. Springer Netherlands, DordrechtGoogle Scholar
  28. Gankin R, Major J (1964) Arctostaphylos myrtifolia, its biology and relationship to the problem of endemism. Ecotoxicology 45:792–808Google Scholar
  29. Gégout J-C, Pierrat J-C (1998) L’autécologie des espèces végétales : Une approche par régression non paramétrique. Ecotoxicology 29:473–482Google Scholar
  30. Ghasemi R, Chavoshi ZZ, Boyd RS, Rajakaruna N (2014) A preliminary study of the role of nickel in enhancing fl owering of the nickel hyperaccumulating plant Alyssum inflatum Nyár. (Brassicaceae). South African J Bot 92:47–52. doi:10.1016/j.sajb.2014.01.015 CrossRefGoogle Scholar
  31. Godefroid S, Van de VA, Massengo Kalenga W, Handjila Minengo G, Rose C, Ngongo Luhembwe M, Vanderborght T, Mahy G (2013) Germination capacity and seed storage behaviour of threatened metallophytes from the Katanga copper belt (DR Congo): implications for ex situ conservation. Plant Ecol Evol 146:183–192. doi:10.5091/plecevo.2013.745 CrossRefGoogle Scholar
  32. Harrison SP, Rajakaruna N (2011) Serpentine: the evolution and ecology of a model system. University of California Press, BerkeleyGoogle Scholar
  33. Hastie T, Tibshirani R (1986) Generalized additive models. Stat Sci 1:297–318CrossRefGoogle Scholar
  34. Hörger AC, Fones HN, Preston GM (2013) The current status of the elemental defense hypothesis in relation to pathogens. Front Plant Sci 4:395. doi:10.3389/fpls.2013.00395 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ilunga wa Ilunga E, Séleck M, Colinet G, Meerts P, Mahy G (2013) Small-scale diversity of plant communities and distribution of species niches on a copper rock outcrop in upper Katanga, DR Congo. Plant Ecol Evol 146:173–182. doi:10.5091/plecevo.2013.816 CrossRefGoogle Scholar
  36. Khan AG (2005) Role of soil microbes in the rhizospheres of plants growing on trace metal contaminated soils in phytoremediation. J Trace Elem Med Biol 18:355–364. doi:10.1016/j.jtemb.2005.02.006 CrossRefPubMedGoogle Scholar
  37. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534. doi:10.1146/annurev-arplant-042809-112156 CrossRefPubMedGoogle Scholar
  38. Kruckeberg AR (1986) An essay: the stimulus of unusual geologies for plant speciation. Syst Bot 11:455. doi:10.2307/2419082 CrossRefGoogle Scholar
  39. Kruckeberg AR, Kruckeberg A (1990) Endemic metallophytes: their taxonomic, genetic and evolutionary attributes. In: Shaw J (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press Inc, New York, pp. 301–312Google Scholar
  40. Kruckeberg AR, Rabinowitz D (1985) Biological aspects of endemism in higher plants. Annu Rev Ecol Syst 16:447–479. doi:10.1146/annurev.es.16.110185.002311 CrossRefGoogle Scholar
  41. Lakanen E, Erviö R (1971) A comparison of eight extractants for the determination of plant available micronutrients in soil. Acta Agral Fenn 123:223–232Google Scholar
  42. 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. PHD Thesis. p 358Google Scholar
  43. Leteinturier B, Baker AJM, Malaisse F (1999) Early stages of natural revegetation of metalliferous mine workings in south Central Africa: a preliminary survey. Biotechnol Agron Soc Environ 3:28–41Google Scholar
  44. Macnair MR (1993) The genetics of metal tolerance in vascular plants. New Phytol 124:541–559. doi:10.1111/j.1469-8137.1993.tb03846.x CrossRefGoogle Scholar
  45. Macnair M, Gardner M (1998) The evolution of edaphic endemics. In: Howard D, Berlocher S (eds) Endless Forms. Species and Speciation. Oxford University Press, New York, pp. 157–171Google Scholar
  46. Macnair M, Tilstone G, Smith S (2000) The genetics of metal tolerance and accumulation in higher plants. In: Terry N (ed) phytoremediation of contaminated soil and water. CRC Press Inc, p. 408Google Scholar
  47. Malaisse F, Baker AJM, Ruelle S (1999) Diversity of plant communities and leaf heavy metal content at Luiswishi copper/cobalt mineralization, upper Katanga, Dem. Rep. Congo. Biotechnol Agron Soc Environ 3:104–114Google Scholar
  48. Margesin R, Schinner F (2005) Manual for soil analysis - monitoring and assessing soil bioremediation: monitoring and assessing soil bioremediation. SpringerGoogle Scholar
  49. Mateos-Naranjo E, Andrades-Moreno L, Redondo-Gómez S (2011) Comparison of germination, growth, photosynthetic responses and metal uptake between three populations of Spartina densiflora under different soil pollution conditions. Ecotoxicol Environ Saf 74:2040–2049. doi:10.1016/j.ecoenv.2011.06.019 CrossRefPubMedGoogle Scholar
  50. Mengoni A, Gonnelli C, Galardi F, Gabbrielli R, Bazzicalupo M (2000) Genetic diversity and heavy metal tolerance in populations of Silene paradoxa L. (Caryophyllaceae): a random amplified polymorphic DNA analysis. Mol Ecol 9:1319–1324CrossRefPubMedGoogle Scholar
  51. Meyer S (1986) The ecology of gypsophile endemism in the eastern Mojave Desert. Ecotoxicology 67:1303–1313Google Scholar
  52. Millie Burrell A, Hawkins AK, Pepper AE (2012) Genetic analyses of nickel tolerance in a north American serpentine endemic plant, Caulanthus amplexicaulis var. barbarae (Brassicaceae). Am J Bot 99:1875–1883. doi:10.3732/ajb.1200382 CrossRefPubMedGoogle Scholar
  53. Miriti MN (2006) Ontogenetic shift from facilitation to competition in a desert shrub. J Ecol 94:973–979. doi:10.1111/j.1365-2745.2006.01138.x CrossRefGoogle Scholar
  54. Mukalay MJ, Shutcha NM, Tshomba KJ, Mulowayi KA, Kamb CF, Ngongo Luhembwe M (2008) Causes d’une forte hétérogénéité des plants dans un champ de maïs dans les conditions pédoclimatique de Lubumbashi. Ann la Fac des Sci Agron 1:4–11Google Scholar
  55. Noret N, Meerts P, Tolrà R, Poschenrieder C, Barceló J, Escarre J (2005) Palatability of Thlaspi Caerulescens for snails: influence of zinc and glucosinolates. New Phytol 165:763–771. doi:10.1111/j.1469-8137.2004.01286.x CrossRefPubMedGoogle Scholar
  56. Parish J, Bazzaz F (1985) Ontogenetic niche shifts in old-field annuals. Ecotoxicology 66:1296–1302Google Scholar
  57. Peng H, Wang-Müller Q, Witt T, Malaisse F, Küpper H (2012) Differences in copper accumulation and copper stress between eight populations of Haumaniastrum katangense. Environ Exp Bot 79:58–65. doi:10.1016/j.envexpbot.2011.12.015 CrossRefGoogle Scholar
  58. Pereira SIA, Barbosa L, Castro PML (2015) Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil. Int J Environ Sci Technol 12:2127–2142. doi:10.1007/s13762-014-0614-z CrossRefGoogle Scholar
  59. R Development Core Team (2010) A language and environment for statistical computing. Vienna (Austria)Google Scholar
  60. Rajakaruna N (2004) The edaphic factor in the origin of species. Int Geol Rev 46:471–478CrossRefGoogle Scholar
  61. Rajakaruna N, Boyd RS (2008) The edaphic factor. In: Jorgensen SE, Fath B (eds) The encyclopedia of ecology, Elsevier, vol 2. Oxford, United Kingdom, pp. 1201–1207CrossRefGoogle Scholar
  62. Roosens N, Verbruggen N, Meerts P, Ximénez-Embun P, Smith JAC (2003) Natural variation in cadmium tolerance and its relationship to metal hyperaccumulation for seven populations of Thlaspi caerulescens from western Europe. Plant, Cell Environ 26:1657–1672CrossRefGoogle Scholar
  63. 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 (D. R. Congo), an essential step in a biodiversity conservation plan. Restor Ecol 20:405–415. doi:10.1111/j.1526-100X.2011.00786.x CrossRefGoogle Scholar
  64. Sambatti JBM, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution (N Y) 60:696–710. doi:10.1111/j.0014-3820.2006.tb01149.x Google Scholar
  65. 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. doi:10.1007/s11104-013-1819-5 CrossRefGoogle Scholar
  66. Shaw J (1990) Heavy metal tolerance in plants: evolutionary aspects. CRC Press Inc, New YorkGoogle Scholar
  67. Shutcha MN, Faucon M-P, Kamengwa Kissi C, Colinet G, Mahy G, Ngongo Luhembwe M, 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. doi:10.1016/j.ecoleng.2015.04.062 CrossRefGoogle Scholar
  68. Springer YP (2009) Do extreme environments provide a refuge from pathogens? A phylogenetic test using serpentine flax. Am J Bot 96:2010–2021. doi:10.3732/ajb.0900047 CrossRefPubMedGoogle Scholar
  69. Strauss SY, Boyd RS (2011) Herbivory and other cross-kingdom interactions on harsh soils. In: Rajakaruna N (ed) Harrison SP. University of California Press, SerpentineThe Evolution and Ecology of a Model System, pp. 180–199Google Scholar
  70. Van Rossum F, Bonnin I, Fenart S, Pauwels M, Petit D, Saumitou-Laprade P (2004) Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species. Mol Ecol 13:2959–2967. doi:10.1111/j.1365-294X.2004.02314.x CrossRefPubMedGoogle Scholar
  71. Whiting SN, Neumann PM, Baker AJM (2003) Nickel and zinc hyperaccumulation by Alyssum murale and Thlaspi Caerulescens (Brassicaceae) do not enhance survival and whole-plant growth under drought stress. Plant, Cell Environ 26:351–360. doi:10.1046/j.1365-3040.2003.00959.x CrossRefGoogle Scholar
  72. Wright JW, Stanton ML, Scherson R (2006) Local adaptation to serpentine and non-serpentine soils in Collinsia sparsiflora. Evol Ecol Res 8:1–21Google Scholar
  73. Yang XE, Jin XF, Feng Y, Islam E (2005) Molecular mechanisms and genetic basis of heavy metal tolerance/hyperaccumulation in plants. J Integr Plant Biol 47:1025–1035. doi:10.1111/j.1744-7909.2005.00144.x CrossRefGoogle Scholar
  74. Yruela I (2005) Copper in plants. Brazilian J Plant Physiol 17:145–156CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Sylvain Boisson
    • 1
  • Michel-Pierre Faucon
    • 2
  • Soizig Le Stradic
    • 1
  • Bastien Lange
    • 3
    • 2
  • Nathalie Verbruggen
    • 4
  • Olivier Garin
    • 1
  • Axel Tshomba Wetshy
    • 5
  • Maxime Séleck
    • 1
  • Wilfried Masengo Kalengo
    • 5
  • Mylor Ngoy Shutcha
    • 5
  • Grégory Mahy
    • 1
  1. 1.Biodiversity and Landscape Unit, BIOSE - Biosystem Engineering Department, Gembloux Agro-Bio TechUniversity of LiegeGemblouxBelgium
  2. 2.Hydrogeochimical Interactions Soil-Environment (HydrISE) UnitPolytechnic Institute LaSalle Beauvais (ISAB-IGAL)BeauvaisFrance
  3. 3.Laboratory of Plant Ecology and BiogeochemistryUniversité Libre BruxellesBruxellesBelgium
  4. 4.Laboratory of Plant Physiology and Molecular GeneticsUniversité Libre de BruxellesBruxellesBelgium
  5. 5.Ecology, Restoration Ecology and Landscape Research Unit, Faculty of AgronomyUniversity of LubumbashiLubumbashiDemocratic Republic of Congo

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