Abstract
The present paper aims to study the phytoremediation of a polymetallic abandoned mine site in the northwest of Marrakesh, Morocco, by exploring the potential of the symbiotic relationship between Pinus halepensis and the ectomycorrhizal fungi belonging to the Scleroderma genus. This process was combined with the use of sand to neutralize the acidic mine tailings (pH < 3) and to stabilize the heavy metals. Inoculated and non-inoculated plants were grown under greenhouse conditions in a substrate containing different proportions of mine tailings: 0%, 10%, 25%, 50%, 75% and 100% mixed with sand as an amendment. After a growth period of six months, the results showed a significant increase (p \(\le\) 0.05) of the pH (11%) and the electrical conductivity of the substrate (29%). Moreover, these treatments significantly increased (p \(\le\) 0.05) the amounts of metallic trace elements, lead (39%), cadmium (22%) and zinc (28%) in the roots of inoculated seedlings compared to non-inoculated ones. The bioaccumulation factor reached a value higher than 1, and the translocation factor recorded a value below 1 particularly for zinc in all treatments and for copper and lead in the 25%, 50% and 75% treatments, indicating that Pinus halepensis has the ability to accumulate significant concentrations of these metals in its roots, thus making a suitable plant for phytoremediation or phytostabilization programs. The results of this study also revealed that the mine tailing amendment had a significant impact on the efficiency of the phytoremediation process toward the metals detected in these polluted soils.
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References
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals — Concepts and applications. Chemosphere 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Amir H, Jourand P, Cavaloc Y, Ducousso M (2014) Role of mycorrhizal fungi in the alleviation of heavy metal toxicity in plants. In: Soil Biology. pp 241–258
Aubert G (1978) Methods of soil analysis. In: G.R.D.P, Marseille. p 191
Bâ A, Duponnois R, Diabaté M, Dreyfus B (2011) Les champignons ectomycorhiziens des arbres forestiers en Afrique de l’Ouest: Méthodes d’étude, diversité, écologie, utilisation en foresterie et comestibilité. In: IRD Editions, IRD. p 252
Bano SA, Ashfaq D (2013) Role of mycorrhiza to reduce heavy metal stress. Nat Sci 5:16–20
Barbafieri M, Dadea C, Tassi E et al (2011) Uptake of heavy metals by native species growing in a mining area in Sardinia, Italy: Discovering native flora for phytoremediation. Int J Phytoremed 13:985–997. https://doi.org/10.1080/15226514.2010.549858
Becerra A, Pritsch K, Arrigo N et al (2005) Ectomycorrhizal colonization of Alnus acuminata Kunth in northwestern Argentina in relation to season and soil parameters. Ann for Sci 62:325–332. https://doi.org/10.1051/forest
Boulli A, Baaziz M, Hirit OM (2001) Polymorphism of natural populations of Pinus halepensis Mill. In: Morocco as revealed by morphological characters. euphytica 119: 309–316
Bremner JM (1996) Nitrogen-total. In:Sparks DL (ed). Methods of soil analysis, Part 3, chemical methods-SSSA Book Series no. 5. In: Soil Science Society of America. pp 1085–1121
Caravaca F, Barea JM, Palenzuela J et al (2003) Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111
Colpaert JV, Van AJA (1992) Zinc toxicity in ectomycorrhizal Pinus sylvestris. Plant Soil 143:201–211
Council Directive of the European Communities (86/278/EEC) (1986) on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture (86 / 278 /EEC). Off J Eur Communities L181(6):6–12
El Amari K, Valera P, Hibti M et al (2014) Impact of mine tailings on surrounding soils and ground water : case of Kettara old mine, Morocco. J African Earth Sci 100:437–449. https://doi.org/10.1016/j.jafrearsci.2014.07.017
Essaifi A (2011) L ’ ancienne mine de pyrrhotite de Kettara (Jebilet centrales). In: les mines de la meseta méridionale et du haut atlas occidental. pp 205–209
Essalmani and Lahlou (2003) Bioprotection mechanisms of the lentil plant by Rhizobium leguminosarum against Fusarium oxysporum f. sp. lentis. Comptes Rendus Biologies 326(12):1163–1173. https://doi.org/10.1016/j.crvi.2003.10.003
Feng S, Yang H, Wang W (2015) Improved chalcopyrite bioleaching by Acidithiobacillus sp. via direct step-wise regulation of microbial community structure. Biores Technol 192:75–82. https://doi.org/10.1016/j.biortech.2015.05.055
Fuentes D, Disante KB, Valdecantos A et al (2007) Response of Pinus halepensis Mill. seedlings to biosolids enriched with Cu, Ni and Zn in three Mediterranean forest soils. Environ Pollut 145:316–323. https://doi.org/10.1016/j.envpol.2006.03.005
Gaba-chahboub H, Lamhamedi MS, Abrous-Belbachir O (2016) Effet de l ’ inoculation ectomycorhizienne en pépinière sur la croissance et la nutrition des plants du cèdre de l ’ Atlas en Algérie. Bois Forêt Des Trop 330:57–68
Gagnon J, Lamhamedi MS (2011) L’inoculation des plants résineux en récipients par des spores de champignons ectomycorhiziens à l’automne pourrait-elle contribuer à réduire les problèmes d’insuffisance racinaire dans les pépinières forestières du Québec ? In: Carrefour Forêt Innovations. pp 27–32
Gan Y, Siddique KHM, Turner NC, et al (2013) Ridge-furrow mulching systems-an innovative technique for boosting crop productivity in semiarid rain-fed environments. In: Advances in Agronomy. Elsevier, pp 429–476
Garbaye J (1991) Biological interactions in the myeorrhizosphere. Experientia 47:370–375
Gaye O, Thiam NM, Bellamine Y et al (2021) Initial results of laser ureteroscopy treatment for lithiasis of the upper urinary tract at aristide le Dantec hospital in Dakar Senegal. J Endoluminal Endourol 4:13–19
González V, García I, Del MF, Simón M (2012) Effectiveness of amendments on the spread and phytotoxicity of contaminants in metal – arsenic polluted soil. J Hazard Mater 206:72–80. https://doi.org/10.1016/j.jhazmat.2011.12.011
Goyal T, Mitra P, Singh P et al (2021) Assessment of blood lead and cadmium levels in occupationally exposed workers of Jodhpur, Rajasthan. Indian J Clin Biochem 36:100–107. https://doi.org/10.1007/s12291-020-00878-6
Grzegórska A, Rybarczyk P, Rogala A, Zabrocki D (2020) Phytoremediation — from environment cleaning to energy generation — current status and future perspectives. Energies 13:43
Guo M, Ding G, Gao G et al (2020) Community composition of ectomycorrhizal fungi associated with Pinus sylvestris var. mongolica plantations of various ages in the Horqin Sandy Land. Ecol Indic 110:1058
Gupta DK, Chatterjee S, Walther C (2020) Lead in Plants and the Environment
Hakkou R, Benzaazoua M, Bussière B (2016) Valorization of phosphate waste rocks and sludge from the Moroccan phosphate mines : challenges and perspectives. Procedia Eng 138:110–118. https://doi.org/10.1016/j.proeng.2016.02.068
Hulseman J (1966) An inventory of marine carbonate materials. J Sediment Petrol ASCE 36(2):622–625
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–585
Lghoul M (2014) Apport de la Géophysique, de l’hydrogéochimie et de la modélisation du transfert en DMA: projet de réhabilitation de la mine abandonnée de Kettara (région de Marrakech, Maroc). Dissertation, University of Cadi Ayyad
Li Y, Chen Z, He JZ et al (2019) Ectomycorrhizal fungi inoculation alleviates simulated acid rain effects on soil ammonia oxidizers and denitrifiers in Masson pine forest. Environ Microbiol 21:299–313. https://doi.org/10.1111/1462-2920.14457
Lindahl BD, Tunlid A (2015) Ectomycorrhizal fungi - potential organic matter decomposers, yet not saprotrophs. New Phytol 205:1443–1447. https://doi.org/10.1111/nph.13201
Liu B, Wang S, Wang J et al (2020) The great potential for phytoremediation of abandoned tailings pond using ectomycorrhizal Pinus sylvestris. Sci Total Environ 719:137475. https://doi.org/10.1016/j.scitotenv.2020.137475
Juste C, Tauzin J (1986) Effect of a 56 year-period of various fertilizer application on the total heavy metal content of a loamy fallow soil. Comptes Rendus des Séances de l'Académie d'Agriculture de France Académie d'agriculture de France 72(9):739–746
Maestre F, Cortina J (2004) Are Pinus halepensis plantations useful as a restoration tool in semiarid Mediterranean areas ? For Ecol Manage 198:303–317. https://doi.org/10.1016/j.foreco.2004.05.040
Maiti SK, Jaiswal S (2008) Bioaccumulation and translocation of metals in the natural vegetation growing on fly ash lagoons : a field study from Santaldih thermal power plant, West Bengal, India. Environ Monit Assess 136:355–370. https://doi.org/10.1007/s10661-007-9691-5
Manaut N, Sanguin H, Ouahmane L, Bressan M, Thioulouse J, Baudoin E, Galiana A, Hafidi M, Prin Y, Duponnois R (2015) Potentialities of ecological engineering strategy based on native arbuscular mycorrhizal community for improving afforestation programs with carob trees in degraded environments. Ecol Eng 79:113–119. https://doi.org/10.1016/j.ecoleng.2015.03.007
Meeinkuirt W, Kruatrachue M, Pichtel J et al (2016) Influence of organic amendments on phytostabilization of Cd-contaminated soil by Eucalyptus camaldulensis. Sci Asia 42:83–91. https://doi.org/10.2306/scienceasia1513-1874.2016.42.083
Midhat L, Ouazzani N, Esshaimi M et al (2017) Assessment of heavy metals accumulation by spontaneous vegetation : screening for new accumulator plant species grown in Kettara mine-Marrakech, Southern Morocco. Int J Phytoremed 19:191–198
Midhat L, Ouazzani N, Hejjaj A et al (2018) Phytostabilization of polymetallic contaminated soil using Medicago Sativa L. in combination with powdered marble : sustainable rehabilitation. Int J Phytoremed 20:764–772
Midhat L, Ouazzani N, Hejjaj A et al (2019) Accumulation of heavy metals in metallophytes from three mining sites (Southern Centre Morocco) and evaluation of their phytoremediation potential. Ecotoxicol Environ Saf 169:150–160
Mleczek M, Goliński P, Waliszewska B et al (2018) The importance of substrate compaction and chemical composition in the phytoextraction of elements by Pinus sylvestris L. J Environ Sci Heal Part A. https://doi.org/10.1080/10934529.2018.1471116
Mukhopadhyay S, Maiti SK (2011) Trace metal accumulation and natural mycorrhizal colonisation in an afforested coalmine overburden dump: a case study from India. Int J Mining, Reclam Environ 25:187–207. https://doi.org/10.1080/17480930.2010.548663
Nedjimi B, Difi M, Haddioui A (2014) Effets des différents prétraitements sur la germination des semences de pin d’Alep (Pinus halepensis Mill.). Rev Des BioRessources 4:40–45
Nounsi A, Outcoumit A, Selmaoui K et al (2014) Inventaire des champignons ectomycorhiziens du Maroc. J Appl Biosci 79:6826–6854
Olchowik J, Suchocka M, Malewski T, Baczewska-Dąbrowska A, Studnicki M, Hilszczańska D (2020) The ectomycorrhizal community of crimean linden trees in Warsaw. Poland. Forests 11:926. https://doi.org/10.3390/f11090926
Orwin KH, Kirschbaum MUF, St John MG, Dickie IA (2011) Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecol Lett 14:493–502. https://doi.org/10.1111/j.1461-0248.2011.01611.x
Pandey J, Chand S, Pandey S et al (2015) Palmarosa [Cymbopogon martinii (Roxb.) Wats.] as a putative crop for phytoremediation, in tannery sludge polluted soil. Ecotoxicol Environ Saf 122:296–302. https://doi.org/10.1016/j.ecoenv.2015.08.005
Pandey VC, Bajpai O (2019) Phytoremediation : from theory toward practice. In: Phytomanagement of Polluted Sites. Elsevier Inc., pp 1–49
Párraga-aguado I, Álvarez-rogel J, González-alcaraz MN et al (2013) Assessment of metal (loid) s availability and their uptake by Pinus halepensis in a Mediterranean forest impacted by abandoned tailings. Ecol Eng 58:84–90. https://doi.org/10.1016/j.ecoleng.2013.06.013
Parraga-Aguado I, González-Alcaraz MN, Álvarez-Rogel J, Conesa HM (2014) Assessment of the employment of halophyte plant species for the phytomanagement of mine tailings in semiarid areas. Ecol Eng 71:598–604. https://doi.org/10.1016/j.ecoleng.2014.07.061
Pasqualini V, Robles C, Garzino S et al (2003) Phenolic compounds content in Pinus halepensis Mill. needles: a bioindicator of air pollution. Chemosphere 52:239–248. https://doi.org/10.1016/S0045-6535(03)00268-6
Pérez-Moreno J, Guerin-Laguette A, Arzú RF, Yu F-Q (2020) Mushrooms, humans and nature in a changing world perspectives from ecological, agricultural and social sciences
Prance M, Fechner N (2017) Collecting and preserving fungi specimens, a manual version 2.1. Dep. Sci. Inf. Technol. Innov. Brisbane
Rai M (2006) Handbook of microbial biofertilizers
Raj D, Maiti SK (2020) Sources, bioaccumulation, health risks and remediation of potentially toxic metal(loid)s (As, Cd, Cr, Pb and Hg): an epitomised review. Environ Monit Assess 192:1–20. https://doi.org/10.1007/s10661-019-8060-5
Raj D, Kumar A, Maiti SK (2019) Evaluation of toxic metal(loid)s concentration in soils around an open-cast coal mine (Eastern India). Environ Earth Sci 78:1–19. https://doi.org/10.1007/s12665-019-8657-6
Raj D, Kumar A, Maiti SK (2020) Brassica juncea (L.) Czern. (Indian mustard): a putative plant species to facilitate the phytoremediation of mercury contaminated soils. Int J Phytoremed 22:733–744. https://doi.org/10.1080/15226514.2019.1708861
Remon E, Bouchardon J, Cornier B et al (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
Repáč I (2011) Ectomycorrhizal Inoculum and Inoculation Techniques. In: Rai M, Varma A (eds) Diversity and biotechnology of ectomycorrhizae, Soil Biology, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-15196-5_3
Robinson GW (1922) A new method for the mechanical analysis of soils and other dispersions. Agric Sci 12:306–321
Rodriguez JH, Wannaz ED, Salazar MJ et al (2012) Accumulation of polycyclic aromatic hydrocarbons and heavy metals in the tree foliage of Eucalyptus rostrata, Pinus radiata and Populus hybridus in the vicinity of a large aluminium smelter in Argentina. Atmos Environ 55:35–42. https://doi.org/10.1016/j.atmosenv.2012.03.026
Sanon K, Dianda M, Guissou T, Ba A (2009) Description des champignons ectomycorhiziens du genre scleroderma de quelques formations forestieres du Burkina Faso. Cameroon J Exp Biol 5:69–78. https://doi.org/10.4314/cajeb.v5i2.51942
Seb J, Ajungla T (2018) Role of ectomycorrhza in forest ecosystems. Int J Adv Res 6:866–873
Sharma S, Singh B, Manchanda VK (2014) Phytoremediation : role of terrestrial plants and aquatic macrophytes in the remediation of radionuclides and heavy metal contaminated soil and water. Environ Sci Pollut Res 22:946–962. https://doi.org/10.1007/s11356-014-3635-8
Smith SE, Read DJ (1997) Mycorrhizal Symbiosis
Stomp A, Han K, Wilbert S et al (1994) Genetic strategies for enhancing phytoremediation. Ann N Y Acad Sci 721:481–491. https://doi.org/10.1111/j.1749-6632.1994.tb47418.x
Tang Y, Shi L, Zhong K et al (2019) Ectomycorrhizal fungi may not act as a barrier inhibiting host plant absorption of heavy metals. Chemosphere 215:115–123. https://doi.org/10.1016/j.chemosphere.2018.09.143
Torkshavand Z, Gholami M, Farzadkia M, Esrafili A (2014) Adsorption of Cu2+ from aqueous solution onto modified glass beads with 3-aminopropyltriethoxysilane. Iran J Heal Saf Environ 1:101–110
Toussaint A, Bueno G, Davison J et al (2020) Asymmetric patterns of global diversity among plants and mycorrhizal fungi. J Veg Sci 31:355–366. https://doi.org/10.1111/jvs.12837
Tozsin G, Oztas T, Arol AI et al (2014) The effects of marble wastes on soil properties and hazelnut yield. J Clean Prod 81:146–149. https://doi.org/10.1016/j.jclepro.2014.06.009
Wahid N, Jouidre H, Lamhamedi MS et al (2010) Acta Botanica Gallica Évaluation de la structure et de la variabilité génétiques des populations naturelles du pin d ’ Alep (Pinus halepensis Mill.) au Maroc à l ’ aide de marqueurs isoenzymatiques. Acta Bot Gall 157:419–431. https://doi.org/10.1080/12538078.2010.10516219
Wamberga C, Christensen S, Jakobsen I et al (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35:1349–1357. https://doi.org/10.1016/S0038-0717(03)00214-1
Xu Z, Zhang T, Wang S, Wang Z (2020) Soil pH and C/N ratio determines spatial variations in soil microbial communities and enzymatic activities of the agricultural ecosystems in Northeast China: Jilin Province case. Appl Soil Ecol 155:103629. https://doi.org/10.1016/j.apsoil.2020.103629
Yang S, Liang S, Yi L et al (2014) Heavy metal accumulation and phytostabilization potential of dominant plant species growing on manganese mine tailings. Front Environ Sci Eng 8:394–404. https://doi.org/10.1007/s11783-013-0602-4
Yanqun Z, Yuan L, Schvartz C et al (2004) Accumulation of Pb, Cd, Cu and Zn in plants and hyperaccumulator choice in Lanping lead – zinc mine area. China 30:567–576. https://doi.org/10.1016/j.envint.2003.10.012
Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464. https://doi.org/10.1016/j.scitotenv.2006.01.016
Yu P, Sun Y, Huang Z et al (2020) The effects of ectomycorrhizal fungi on heavy metals ’ transport in Pinus massoniana and bacteria community in rhizosphere soil in mine tailing area. J Hazard Mater 381:121203. https://doi.org/10.1016/j.jhazmat.2019.121203
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The authors are thankful to the operating staff of the Laboratories (BioMAgE) and (CNEREE). We thank all reviewers and the coordinating editor for their comments and suggestions that helped to improve the manuscript. The authors thank Dr. Issam jadrane for the language revision of the manuscript.
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This study focuses on the combination of a native plant species Pinus halepensis and the ectomycorrhizal fungus belonging to the Scleroderma genus in a phytoremediation strategy of a polymetallic abandoned mine site. The originality of this work lies in the choice of the plant species and the symbiotic fungus and their combination in a mine tailing amended with sand.
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Ouatiki, E., Midhat, L., Tounsi, A. et al. The association between Pinus halepensis and the Ectomycorrhizal fungus Scleroderma enhanced the phytoremediation of a polymetal-contaminated soil. Int. J. Environ. Sci. Technol. 19, 12537–12550 (2022). https://doi.org/10.1007/s13762-022-03993-4
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DOI: https://doi.org/10.1007/s13762-022-03993-4