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Phytoremediation of heavy metals by four aquatic macrophytes and their potential use as contamination indicators: a comparative assessment

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Abstract

The present study estimated the ability of four aquatic macrophytes (Eichhornia crassipes (Mart.) Solms, Ludwigia stolonifera (Guill. & Perr.) P.H. Raven, Echinochloa stagnina (Retz.) P. Beauv. and Phragmites australis (Cav.) Trin. ex Steud.) to accumulate Cd, Ni and Pb and their use for indicating and phytoremediating these metals in contaminated wetlands. Three sites at five locations in the Kitchener Drain in Gharbia and Kafr El-Sheikh Governorates (Egypt) were selected for plant, water and sediment sampling. The water in the Kitchener Drain was polluted with Cd, while Pb and Ni were far below the maximum level of Pb and Ni in the irrigation water. In comparison to the other species, P. australis accumulated the highest concentrations of Cd and Ni, while E. crassipes accumulated the highest concentration of Pb in its tissues. The four species had bioaccumulation factors (BAFs) greater than one, while their translocation factors (TFs) were less than 1 for most heavy metals, except Cd in the leaf and stem of E. stagnina and L. stolonifera, respectively, and Ni in the stem and leaf of E. stagnina. The BAF and TF results indicated that the studied species are suitable for phytostabilizing the studied heavy metals, except Ni in E. stagnina and Cd in L. stolonifera, which are suitable for phytoextracting these metals. Significant positive correlations were found between the investigated heavy metals in the water or sediment and the plant tissues. Their high BAFs, with significant proportional correlations, supported the potential of these species to serve as bioindicators and biomonitors of heavy metals in general and in the investigated metals specifically.

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References

  • Abdel-Shafy H, Hegemann W, Teiner A (1994) Accumulation of metals by vascular plants. Environ Manag Health 5:21–24

    Google Scholar 

  • Abubakar MM, Ahmad MM, Getso BU (2014) Rhizofiltration of heavy metals from eutrophic water using Pistia stratiotes in a controlled environment. J Environ Sci Toxicol Food Technol 8:1–3

    Google Scholar 

  • Abu-Ziada ME (2007) Ecological studies on the aquatic macrophytes II: Ludwigia stolinefera (Guill. & Perr.) P.H. Raven. Pak J Biol Sci 10:2025–2038

    CAS  Google Scholar 

  • Agunbiade FO, Olu-Owolabi BI, Adebowale KO (2009) Phytoremediation potential of Eichornia crassipes in metal-contaminated coastal water. Bioresour Technol 100:4521–4526

    CAS  Google Scholar 

  • Ahmad SS, Reshi ZA, Shah MA, Rashid I, Ara R, Andrabi SMA (2014) Phytoremediation potential of Phragmites australis in Hokersar wetland: a Ramsar site of Kashmir Himalaya. Int J Phytoremediat 16:1183–1191

    CAS  Google Scholar 

  • Aitta A, El-Ramady H, Alshaal T, El-Henawy A, Shams M, Talha N, Elbehiry F, Brevik EC (2019) Seasonal and spatial distribution of soil trace elements around Kitchener Drain in the Northern Nile Delta, Egypt. Agriculture 9:1–25

    Google Scholar 

  • Allen SE (1989) Chemical analysis of ecological materials. Blackwell Scientific Publications, London

    Google Scholar 

  • APHA (American Public Health Association) (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

    Google Scholar 

  • Ashraf S, Ali Q, Ahmad Z, Ashraf S, Naeem H (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727

    CAS  Google Scholar 

  • Baker AJM, McGrath SP, Reeves RD, Smith JAC (2000) Metal hyperaccumulator plants: a review of the ecology and physiology of a biochemical resource for phytoremediation of metal-polluted soils. In: Terry N, Bañuelos G (eds) Phytoremediation of contaminated soil and water. Lewis, Boca Raton, pp 85–107

    Google Scholar 

  • Baldantoni D, Ligrone R, Alfani A (2009) Macro- and trace-element concentrations in leaves and roots of Phragmites australis in a volcanic lake in Southern Italy. J Geochem Explor 101:166–174

    CAS  Google Scholar 

  • Bello AO, Tawabini BS, Khalil AB, Boland CR, Saleh TA (2018) Phytoremediation of cadmium-, lead- and nickel-contaminated water by Phragmites australis in hydroponic systems. Ecol Eng 120:126–133

    Google Scholar 

  • Bonanno G (2013) Comparative performance of trace element bioaccumulation and bio- monitoring in the plant species Typha domingensis, Phragmites australis and Arundo donax. Ecotoxicol Environ Saf 97:124–130

    CAS  Google Scholar 

  • Bonanno G, Lo GR (2010) Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecol Indic 10:639–645

    CAS  Google Scholar 

  • Bonanno G, Borg JA, Di Martino V (2017) Levels of heavy metals in wetland and marine vascular plants and their biomonitoring potential: a comparative assessment. Sci Total Environ 576:796–806

    CAS  Google Scholar 

  • Boulos L (2000) Flora of Egypt, volume two. Geraniaceae-Boraginaceae. Al Hadara Publish, Cairo

    Google Scholar 

  • Boulos L (2005) Flora of Egypt, volume four. Monocotyledons (Alismataceae-Orchidaceae). Al Hadara Publish, Cairo

    Google Scholar 

  • Bragato C, Brix H, Malagoli M (2006) Accumulation of nutrients and heavy metals in Phragmites australis (Cav.) Trin. ex Steudel and Bolboschoenus maritimus (L.) Palla in a constructed wetland of the Venice lagoon watershed. Environ Pollut 144:967–975

    CAS  Google Scholar 

  • Brix H, Schierup HH (1989) The use of aquatic macrophytes in water pollution control. Ambio 18:101–107

    Google Scholar 

  • Carrión C, Ponce-de León C, Cram S, Sommer I, Hernández M, Vanegas C (2012) Potential use of water hyacinth (Eichhornia crassipes) in Xochimilco for metal phytoremediation. Agrociencia 46:609–620

    Google Scholar 

  • Caselles-Osorio A, Vegab H, Lancherosa JC, Casierra-Martíneza HA, Mosquera JE (2017) Horizontal subsurface-flow constructed wetland removal efficiency using Cyperus articulatus L. Ecol Eng 99:479–485

    Google Scholar 

  • Cicero-Fernández D, Peña-fernández M, Expósito-camargo JA, Antizar-ladislao B, Peña-fernández M, Expósito-camargo JA, Cicero-fern D (2016) Role of Phragmites australis (common reed) for heavy metals phytoremediation of estuarine sediments. Int J Phytoremediat 18:575–582

    Google Scholar 

  • Du Laing G, Tack FMG, Verloo MG (2003) Performance of selected destruction methods for the determination of heavy metals in reed plants (Phragmites australis). Anal Chim Acta 497:191–198

    Google Scholar 

  • Du Laing G, Van de Moortel AMK, Moors W, De Grauwe P, Meers E, Tack FMG, Verloo MG (2009) Factors affecting metal concentrations in reed plants (Phragmites australis) of intertidal marshes in the Scheldt estuary. Ecol Eng 35:310–318

    Google Scholar 

  • Duman F, Cicek M, Sezen G (2007) Seasonal changes of metal accumulation and distribution in common club rush (Schoenoplectus lacustris) and common reed (Phragmites australis). Ecotoxicology 16:457–463

    CAS  Google Scholar 

  • Dummee V, Kruatrachue M, Trinachartvanit W, Tanhan P, Pokethitiyook P, Damrongphol P (2012) Bioaccumulation of heavy metals in water, sediments, aquatic plant and histopathological effects on the golden apple snail in Beung Boraphet reservoir, Thailand. Ecotoxicol Environ Saf 86:204–212

    CAS  Google Scholar 

  • Eid EM, Shaltout KH (2014) Monthly variations of trace elements accumulation and distribution in above- and below-ground biomass of Phragmites australis (Cav.) Trin. ex Steudel in Lake Burullus (Egypt): a biomonitoring application. Ecol Eng 73:17–25

    Google Scholar 

  • Eid EM, Shaltout KH, El-Sheikh MA, Asaeda T (2012) Seasonal courses of nutrients and heavy metals in water, sediment and above- and below-ground Typha domingensis biomass in Lake Burullus (Egypt): perspective for phytoremediation. Flora 207:783–794

    Google Scholar 

  • Eid EM, Shaltout KH, Moghanm FS, Youssef MS, El-Mohsnawy E, Haroun SA (2019) Bioaccumulation and translocation of nine heavy metals by Eichhornia crassipes in Nile Delta, Egypt: perspectives for phytoremediation. Int J Phytoremediat 21:821–830

    CAS  Google Scholar 

  • El-Amier YA, Zahran MA, Gebreil AS, Abd El-Salam EH (2017) Anthropogenic activities and their impact on the environmental status of Kitchener drain, Nile Delta, Egypt. J Environ Sci 46:251–262

    Google Scholar 

  • Fawzy MA, Badr NE, El-Khatib A, Abo-El-Kassem A (2012) Heavy metal biomonitoring and phytoremediation potentialities of aquatic macrophytes in River Nile. Environ Monit Assess 184:1753–1771

    CAS  Google Scholar 

  • Galal TM, Shehata HS (2014) Evaluation of the invasive macrophyte Myriophyllum spicatum L. as a bioaccumulator for heavy metals in some watercourses of Egypt. Ecol Indic 41:209–214

    CAS  Google Scholar 

  • Galal TM, Eid EM, Dakhil MA, Hassan LM (2018) Bioaccumulation and rhizofiltration potential of Pistia stratiotes L. for mitigating water pollution in the Egyptian wetlands. Int J Phytoremediat 20:440–447

    CAS  Google Scholar 

  • Galal TM, Al-Sodany YM, Al-Yasi HM (2019) Phytostabilization as a phytoremediation strategy for mitigating water pollutants by the floating macrophyte Ludwigia stolonifera (Guill. & Perr.) P.H. Raven. Int J Phytoremediat 25:1–10. https://doi.org/10.1080/15226514.2019.1663487

    Article  CAS  Google Scholar 

  • Garbisu C, Alkorta I (2003) Basic concepts on heavy metal soil bioremediation. Eur J Min Proc Environ Protect 13:58–66

    Google Scholar 

  • Ghazi SM, Galal TM, Husein KH (2019) Monitoring water pollution in the Egyptian watercourses: a phytoremediation approach. LAP LAMBERT Academic Publishing, Saarbrücken

    Google Scholar 

  • Gupta S, Satpati S, Nayek S, Garai D (2010) Effect of wastewater irrigation on vegetables in relation to bioaccumulation of heavy metals and biochemical changes. Environ Monit Assess 165:169–177

    CAS  Google Scholar 

  • Harun NH, Tuah PM, Markom NZ, Yusof MY 2008 Distribution of heavy metals in Monochoria hastata and Eichornia crassipes in natural habitats. Int Conf Environ Res Technol 550–553

  • Kabata-Pendias A (2011) Trace elements in soils and plants, Fourth edn. Taylor & Francis Group, Boca Raton

    Google Scholar 

  • Kamari A, Yusof N, Abdullah H, Haraguchi A, Abas MF (2017) Assessment of heavy metals in water, sediment, Anabas testudineus and Eichhornia crassipes in a former mining pond in Perak, Malaysia. Chem Ecol 33:637–651

    CAS  Google Scholar 

  • Kassaye YA, Skipperud L, Einset J, Salbu B (2016) Aquatic macrophytes in Ethiopian Rift Valley lakes: their trace elements concentration and use as pollution indicators. Aquat Bot 134:18–25

    CAS  Google Scholar 

  • Lu RK (2000) Methods of inorganic pollutants analysis. In: Soil and agro-chemical analysis methods. Agricultural Science and Technology Press, Beijing

    Google Scholar 

  • Mganga N, Manoko M, Rulangaranga Z (2011) Classification of plants according to their heavy metal content around North Mara Gold Mine, Tanzania: implication for phytoremediation. Tanz J Sci 37:109–119

    Google Scholar 

  • Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216

    CAS  Google Scholar 

  • Olivares-Rieumont S, Lima L, De la Rosa D, Graham DW, Columbie I, Santana JL, Sánchez MJ (2007) Water hyacinths (Eichhornia crassipes) as indicators of heavy metal impact of a large landfill on the Almendares River near Havana, Cuba. Bull Environ Contam Toxicol 79:583–587

    CAS  Google Scholar 

  • Pandey VC (2016) Phytoremediation efficiency of Eichhornia crassipes in fly ash pond. Int J Phytoremediat 18:450–452

    CAS  Google Scholar 

  • Qian JH, Zayed A, Zhu YL, Yu M, Terry N (1999) Phytoaccumulation of trace elements by wetland plants: III. Uptake and accumulation of ten trace elements by twelve plant species. J Environ Qual 28:1448–1455

    CAS  Google Scholar 

  • Rezania S, Park J, Rupani PF, Darajeh N, Xu X (2019) Phytoremediation potential and control of Phragmites australis as a green phytomass: an overview. Environ Sci Pollut Res 26:7428–7441

    CAS  Google Scholar 

  • Rezaniaa S, Taib SM, Md Din MH, Dahalan FA, Kamyab H (2016) Comprehensive review on phytotechnology: heavy metals removal by diverse aquatic plants species from wastewater. J Hazard Mater 318:587–599

    Google Scholar 

  • Rowe DR, Abdel-Magid IM (1995) Handbook of wastewater reclamation and reuse. CRC Press, Boca Raton

    Google Scholar 

  • Saha P, Shinde O, Sarkar S (2017) Phytoremediation of industrial mines wastewater using water hyacinth. Int J Phytoremediat 19:87–96

    CAS  Google Scholar 

  • Salawu MO, Sunday ET, Oyelola H, Oloyede B (2018) Bioaccumulative activity of Ludwigia peploides on heavy metals-contaminated water. Environ Technol Innov 10:324–334

    Google Scholar 

  • Saleh HM, Aglan RF, Mahmoud HH (2019) Ludwigia stolonifera for remediation of toxic metals from simulated wastewater. Chem Ecol 35:164–178

    CAS  Google Scholar 

  • Samecka-Cymerman A, Kempers AJ (2001) Concentrations of heavy metals and plants nutrients in water, sediments and aquatic macrophytes of anthropogenic lakes (former open cut brown coal mines) differing in stage of acidification. Sci Total Environ 281:87–98

    CAS  Google Scholar 

  • Sarwar N, Imran M, Shaheen MR, Ishaq W, Kamran A, Matloob A, Rehim A, Hussain S (2017) Phytoremediation strategies for soils contaminated with heavy metals: modifications and future perspectives. Chemosphere 171:710–721

    CAS  Google Scholar 

  • Shaltout KH, Galal TM, El-Komy TM (2009) Evaluation of the nutrient status of some hydrophytes in the water courses of Nile Delta, Egypt. Aust J Bot 2009:862565

    Google Scholar 

  • Statsoft (2007) Statistica version 7.1. Statsoft Inc, Tulsa

    Google Scholar 

  • Szyczewski P, Siepak J, Niedzielski P, Sobczyński T (2009) Research on heavy metals in Poland. Pol J Environ Stud 5:755–768

    Google Scholar 

  • Valipour A, Ahn YH (2016) Constructed wetlands as sustainable ecotechnologies in decentralization practices: a review. Environ Sci Pollut Res 23:180–197

    CAS  Google Scholar 

  • Vodyanitskii YN, Shoba SA (2015) Biogeochemistry of carbon, iron, and heavy metals in wetlands (analytical review). Moscow Univ Soil Sci Bull 70:89–97

    Google Scholar 

  • Weis JS, Weis P (2004) Metal uptake, transport and release by wetland plants: implications for phytoremediation and restoration. Environ Int 30:685–700

    CAS  Google Scholar 

  • Yan P, Xia JS, Chena YP, Liu ZP, Guoa JS, Shen Y, Zhangc CC, Wang J (2017) Thermodynamics of binding interactions between extracellular polymeric substances and heavy metals by isothermal titration microcalorimetry. Bioresour Technol 232:354–363

    CAS  Google Scholar 

  • Zhang WH, Tong LZ, Yuan Y, Huang H, Qiu RL (2011) Metal mobility and fraction distribution in a multi-metal contaminated soil chemically stabilized with different agents. J Hazard Toxic Radioact Waste 15:1–11

    Google Scholar 

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Funding

This work was supported by the Deanship of Scientific Research at King Khalid University under grant number R.G.P. 1/94/40.

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Author notes

  1. Ebrahem M. Eid

    Present address: Botany Department, Faculty of Science, Kafr El-Sheikh University, Kafr El-Sheikh, 33516, Egypt

  2. Tarek M. Galal

    Present address: Botany and Microbiology Department, Faculty of Science, Helwan University, Cairo, Egypt

Authors and Affiliations

  1. Biology Department, College of Science, King Khalid University, P.O. Box 9004, Abha, 61321, Saudi Arabia

    Ebrahem M. Eid & Samy M. Abdallah

  2. Biology Department, Faculty of Science, Taif University, Taif, Saudi Arabia

    Tarek M. Galal

  3. Botany Department, Faculty of Science, Tanta University, Tanta, 31527, Egypt

    Nasser A. Sewelam

  4. Soil, Water and Environment Research Institute, Agriculture Research Center, Sakha, Kafr El-Sheikh, Egypt

    Nasser I. Talha

  5. Prince Sultan Bin Abdul-Aziz Center for Environment and Tourism Research and Studies, King Khalid University, P.O. Box 960, Abha, 61421, Saudi Arabia

    Samy M. Abdallah

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  1. Ebrahem M. Eid
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Correspondence to Ebrahem M. Eid.

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Eid, E.M., Galal, T.M., Sewelam, N.A. et al. Phytoremediation of heavy metals by four aquatic macrophytes and their potential use as contamination indicators: a comparative assessment. Environ Sci Pollut Res 27, 12138–12151 (2020). https://doi.org/10.1007/s11356-020-07839-9

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