SEEFOR 15(1): early view
Article ID: 2409
DOI: https://doi.org/10.15177/seefor.24-09
REVIEW PAPER
Practices for Phytoremediation of Soil in Serbia
Filip Vasić1,*, Snežana Belanović Simić1, Dragana Čavlović1, Predrag Miljković1, Milica Caković1, Nikola Jovanović1, Aleksandar Marković1, Tara Grujić2, Sara Lukić1
(1) University of Belgrade, Faculty of Forestry, Kneza Višeslava 1, RS-11000 Belgrade, Serbia;
(2) Institute of Soil Science, Teodora Drajzera 7, RS-11000 Belgrade, Serbia
Citation: Vasić F, Belanović-Simić S, Čavlović D, Miljković P, Caković M, Jovanović N, Marković A, Grujić T, Lukić S, 2024. Practices for Phytoremediation of Soil in Serbia. South-east Eur for 15(1): early view. https://doi.org/10.15177/seefor.24-09.
Received: 30 Dec 2023; Revised: 5 Apr 2024; Accepted: 12 Apr 2024; Published online: 9 May 2024
Cited by: Google Scholar
Abstract
Phytoremediation stands as a crucial tool for addressing pollution, yet its application in Europe remains inadequately explored. Taking Serbia as a test case, this literature review delves into the state of knowledge regarding phytoremediation, exploring the regional distribution of contaminated sites, the prevalence of analysed contaminants, and the diversity of plant species employed for phytoremediation. Analysis revealed 24 distinct locations, 11 sampling parts, scrutiny of 24 potential toxic elements (PTEs) and nutrients, and the involvement of 65 plant species. Predominantly, research sites were associated with industrial areas, particularly mining sites. The efficacy of various plants varied across multiple factors, with soil, roots, and leaves emerging as the most frequently sampled components in reviewed manuscripts. Notably, the scientific literature emphasized Cu, Zn, Cd, and Pb as the most frequently studied PTEs in the context of phytoremediation. This review underscores the need for increased attention to phytoremediation research in Serbia, advocating a more widespread and intensive exploration, both geographically and in research efforts. The compilation of plant species employed for phytoremediation offers valuable insights into the effectiveness of particular species in distinct phytoremediation practices.
Keywords: potential toxic elements (PTEs); soil pollution; plant uptake; soil reclamation; phytostabilisation; biomonitoring
INTRODUCTION
Phytoremediation is an environmentally friendly technology that uses plants to clean up various contaminated sites (Pilon-Smits 2005, Jiang et al. 2024). It is a sustainable, eco-friendly treatment method for contaminated soil, water, and air that entails procedures including removing, transferring, stabilising, or degrading pollutants from these ecosystems (Haynes 2009, Wei et al. 2021). Despite its promising aspects, phytoremediation also has certain limits (Drzewiecka et al. 2024). The effectiveness of phytoremediation techniques depends on various factors, such as plant species, field conditions, desired cleanup goals, and the nature of contaminants present. These techniques include phytostabilization/phytoimmobilization for lowering the mobility of contaminants and phytovolatization/phytoextraction for the removal of pollutants (Bortoloti and Baron 2022). Furthermore, the justification for implementing phytoremediation is also the opportunity for cost-effective remediation (Ghosh and Singh 2005).
Phytoremediation is one of the most effective solutions for solving environmental pollution, with a specific focus on the challenges posed by heavy metals. Within the domain of literature, particularly in the context of environmental pollution, the term "heavy metals" refers to a set of elements that are classified based on their density or molar mass (Zhang et al. 2019). This category encompasses not only metals but also metalloids and nonmetals, without a precise definition. The phrase in question is deemed ambiguous by the International Union of Pure and Applied Chemistry due to the lack of a recognized definition. Consequently, a comprehensive category of elements investigated in the environment has been referred to as "potentially toxic elements (PTEs)" (Pourret and Hursthouse 2019). PTEs primarily consist of trace elements that are essential for the growth and development of plants (e.g., Zn, Cu), but can become toxic at higher concentrations, as well as of other elements (e.g., As, Cd, Hg, Ni, and Pb), which have a harmful effect on the living world even in small quantities (Belanović Simić 2017). PTEs cannot be degraded by biological or chemical processes, and therefore they are accumulated in various environments such as soil, sediments, water, as well as in living organisms (Sun et al. 2013). Pollution by PTEs can occur as a result of both natural (rock weathering, volcanic eruptions) and human activities (industry, urbanisation, intensive agriculture, etc.) (Ali et al. 2013). PTEs derived from natural sources are less harmful to the environment in general, while metals derived from anthropogenic sources represent a hazard to the environment as well as to human health (Jaishankar et al. 2014, Muthusaravanan et al. 2018).
Mining represents one of the most significant drivers of soil and water pollution, and it is well-known for its negative effects on the ecosystem (Jakovljević et al. 2019). Even when mining operations in a particular location are over, waste material dumps continue to harm the environment for an extended period of time (Fernández-Caliani et al. 2009). The disposal of fly ash can pose a hazard since the leaching of PTEs may further have a negative impact on the ecosystem (Pandey and Singh 2010). To reduce environmental pollution, plant species that are resistant to the particular mixture of abiotic stress factors occurring in the contaminated environment, and which can develop self-sustaining vegetation cover, would be beneficial (Pietrzykowski et al. 2018). Growing in highly polluted environments, some plant species can be severely harmed, while others can endure with no noticeable alterations (Marić et al. 2013). PTEs can be taken up by plants via roots from the soil and then transported to the leaves, or by leaves straight from the air (Alagić et al. 2013).
PTEs contamination of soil presents a huge risk to the environment and humans (Shah and Daverey 2020). Various regions worldwide, such as the USA, China, Central-Eastern Europe, and others, grapple with finding solutions to PTE’s contamination, although the nature of the problem varies across regions (Yao et al. 2012, Sharma and Pandey 2014). Serbia, too, faces similar challenges, necessitating new knowledge, solutions, and achievements. In relation to this, our research contributes to filling this gap through the following goals:
- Assess the state of knowledge regarding phytore-mediation practices in Serbia by reviewing scientific literature;
- Assess the performance of plant species used for phytoremediation and the frequency of various contaminants (PTEs and nutrients).
MATERIALS AND METHODS
We reviewed scientific publications pertaining to the application of techniques for phytoremediation of soil related to the territory of Serbia. A literature review was performed using data from the Web of Science multidisciplinary research engine, which has been recognised as a trusted source of high-quality peer-reviewed papers. A keyword-based search on Web of Science was conducted between April and September 2023. To categorise and manage all the papers, this research built a database based on the following combination of keywords: "phytoremediation OR phytostabilization OR phytoextraction OR phytovolatilization AND “Serbia". These terms were used to search in all fields. Papers in English and Serbian language were considered, while publication date was not used as a selection criterion. For performing this review, we used the Rayyan (http://rayyan.qcri.org) online application for systematic reviews by Ouzzani et al. (2016). All identified papers’ abstracts were reviewed. Intensive manual interpretation was performed in order to obtain a set of papers related to phytoremediation experience in Serbia. Articles were considered relevant if they were related to some phytoremediation practices within the territory of Serbia. In cases where the article was related to Serbia and other countries, only results related to Serbia were considered relevant and analyzed. A full text analysis was conducted for the selected number of publications. Additionally, the review was supplemented with a backward snowball search, which included a review of selected references cited in the reviewed articles.
RESULTS AND DISCUSSION
In total, 155 papers were obtained. Finally, 31 papers were selected as suitable for an overview. The analysis of the papers included 24 different locations in Serbia, while 65 different plant species were detected as the ones used for phytoremediation practice. Furthermore, we established that the analysed studies contained 11 different sampling parts (soil and specific plant parts). The identified studies were related to 24 detected PTEs in total.
Analysed Locations
Papers covered various locations in Serbia (Figure 1). The majority of them were related to the vicinity of mining sites, as these may be the most hazardous ones. Other sites were related to the landfill, some specific source of pollution, municipalities, or experimental study sites. Most of the reviewed studies were performed in the area or vicinity of Bor municipality (eastern Serbia). The reason for this could be found in the copper mining and smelting complex RTB Bor, whose surrounding area acts as a phytoremediation laboratory. Similar to this, other two locations—the vicinity of thermal power plant TENT and Rudnik mine—were also recognised as common locations for phytoremediation practices.
Analysed Species Used for Phytoremediation Practices
Various plant species (65) were applied in the analysed papers for phytoremediation practice. These species have been divided into the following five groups: 1) shrubs or small trees; 2) trees; 3) annual or biennial plants; 4) perennial plants; and 5) crops.
Shrubs or Small Trees
In this category, eight species were identified and analysed in the reviewed papers (Table 1). The detected species showed various results depending on multiple factors. For example, in terms of phytostabilization, three species were marked as potentially suitable. Among them, Tamarix tetrandra Pall. Ex M. Bieb. was recognised as the one with the highest potential in terms of phytostabilization of PTEs such as As, Cr, and Ni (Kostić et al. 2021). Nevertheless, this species showed that it is not suitable for phytostabilization on fly ash sites (Kostić et al. 2022). Salix viminalis L. clone ‘SV068’ showed the ability to phytostabilize Cr, Ni, Pb, and Cu, mostly in the root zone (Pilipović et al. 2019). Rubus fruticosus L. was also marked as a species with potential for phytostabilisation practice (Alagić et al. 2016, Alagić et al. 2017). In terms of phytoextraction, T. tetrandra (Kostić et al. 2021, 2022), Salix viminalis L. clone ‘SV068’ (Pilipović et al. 2019) and Rubus fruticosus L. (Alagić et al. 2017, Alagić et al. 2016) were recognised as suitable species. Vaccinium uliginosum L. showed the greatest tendency to mobilise Cd and Cu compared to Vaccinium myrtillus L. and Vaccinium vitis-idaea L., while both of these species could be used on soils with elevated Cd levels (Belanović et al. 2013). The rest of the analyzed species from this group showed a tendancy towards other phytoremediation practices, respectively Amorpha fruticosa L. - sustainable phytomanagement (Kostić et al. 2021) and Salix caprea L. - bioaccumulator (Brković et al. 2021).
Table 1. Shrubs or small tree species analysed in the reviewed papers.
Tree Species
Seventeen tree species were detected among the reviewed papers shown in Table 2. Among them, Aesculus hippocastanum L., Betula pendula Roth, Acer platanoides L. (Gorelova et al. 2011), Betula sp. (Alagić et al. 2013, 2014) and Tilia sp. (Gorelova et al. 2011, Alagić et al. 2013, 2014) were detected as potentially suitable candidates for biomonitoring practices. Fraxinus ornus L. (Brković et al. 2021) and Populus deltoides Bartr. ex Marsh.‘Bora’ (Pilipović et al. 2019, 2020) both showed the ability for phytoextraction, while Tilia sp. and Betula sp. were not suitable for phytoextraction practices (Alagić et al. 2013, 2014). Nevertheless, these two species showed to be of interest as phytostabilization species (Alagić et al. 2013, 2014), while Robinia pseudoacacia L. and Populus alba L. were recognised as not suitable for phytostabilization on fly ash (Kostić et al. 2021). Populus deltoides Bartr. ex Marsh.‘Bora’, Populus deltoides ‘PE 19/66’ and Populus x euramericana (Dode) Guinier ‘Pannonia’ have shown similar reactions to PTEs, diesel, and herbicide treatments, where PTEs had a more significant effect on growth and physiology as the trees matured, while diesel and herbicide treatments were most pronounced during the first growing season, with diminishing effects over time (Trudić et al. 2013, Pilipović et al. 2020). Furthermore, in research by Trudić et al. (2013), two poplar clones, Populus euramericana-M1 and Populus deltoides B 229, were recognised as primary and secondary clones, respectively, in terms of potential application for phytoremediation in soil ecosystems that are polluted by PTEs. Populus nigra L. was efficient for the accumulation of Mn and Cd, while Salix alba L. was recognised as a useful bioaccumulator of Mn, Fe, Cr, Pb, Zn, and Ca (Brković et al. 2021). Quercus petraea (Matt.) Liebl. and Quercus robur L. both showed significantly high concentration of Mn and Fe within foliage, while concentrations of Zn and Cu were slightly higher in branch material (Stojnić et al. 2019).
Table 2. Tree species analyzed in the reviewed papers.
Annual and Biennial Plant Species
Eight annual or biennial plant species have been identified and are presented in Table 3. Tripleurospermum inodorum (L.) Sch.Bip. (syn. Matricaria inodora L.), Crepis setosa Haller fill. (Glisic et al. 2021) and Erigeron canadensis L. (syn. Conyza canadensis L.) (Krgović et al. 2015, Vukojević et al. 2016) showed to be efficient for phytoextraction and phytostabilization purposes. Vicia sativa L., Ranunculus arvensis L., Amaranthus retroflexus L., and Galium aparine L. all showed a high accumulation of Cu, while the accumulation of Pb was slight (Marić et al. 2013). Euphorbia helioscopia L. proved to be valuable for biomonitoring purposes (Petrović et al. 2021).
Table 3. Annual and biennial plant species analysed in the reviewed papers.
Perennial Plant Species
The majority of the analysed plants were perennial, comprising twenty-eight species, as summarised in Table 4. Achillea millefolium L. and Saponaria officinalis L. demonstrated potential suitability for phytoextraction practices ( Nujkić et al. 2020, Glisić et al. 2021), while Tussilago farfara L. was recognised as not suitable for phytoextraction management (Jakovljević et al. 2020). A. millefolium (Nujkić et al. 2020, Glisić et al. 2021), Dactylis glomerata L. (Marić et al. 2013, Gajić et al. 2020), Vitis vinifera L. (Alagić et al. 2018), Epilobium dodonaei Vill. (Randjelović et al. 2016), and Festuca rubra L. (Gajić et al. 2016) manifested potential abilities for phytostabilization, while Calamagrostis epigejos (L.) had only certain potential for phytostabilization, but it was not recommended to be used as a single remediation choice (Randjelović et al. 2018). Urtica dioica L. (Petrović et al. 2021), V. vinifera (Alagić et al. 2018) and Phragmites australis (Cav.) Trin. ex Steud (Nikolić et al. 2014, Prica et al. 2019) were recognised as useful in biomonitoring practices. Odontarrhena chalcidica (Janka) Španiel, Al-Shehbaz, D.A.German & Marhold (syn. Alyssum markgrafii O.E. Schulz.) and Odontarrhena muralis (Waldst. & Kit.) Endl. (syn. Alyssum murale Waldst. & Kit.) both showed abilities to accumulate several elements and especially to act as hyperaccumulators for Ni, while Alyssum montanum L. showed higher concentrations of Mn in tissues than the two previously mentioned species (Branković et al. 2013). Certain species showed the tendency to accumulate Cu, such as D. glomerata (Marić et al. 2013, Gajić et al. 2020), P. australis (Nikolić et al. 2014, Prica et al. 2019), Epilobium dodonaei Vill. (Randjelović et al. 2016), F. rubra (Gajić et al. 2016), Eryngium serbicum Pančić, Sanguisorba minor Scop. (Branković et al. 2015) Euphorbia cyparissias L., Cynodon dactylon L., Anthoxanthum odoratum L., Lollium perenne L., Agrostis gigantea L., Trifolium pratense L., Medicago falcata L., Lotus corniculatus L., Helleborus odorus L., Equisetum arvense L., and Taraxacum sect. Taraxacum F.H.Wigg. (Marić et al. 2013). Furthermore, Miscanthus × longiberbis (Hack.) Nakai (syn. Miscanthus × giganteus) was able to manage extremely harsh conditions in the flotation tailings while retaining the accumulated metals (Zn, Pb, and Cu) within the root zone, being recognised as an excluder of Cu, Zn, and especially Pb (Andrejić et al. 2019).
Table 4. Perennial plant species analysed in the reviewed papers.
Crops
Three crop species were determined, each with four different inbred lines or sorts (Table 5). On average, soybean demonstrated the highest efficiency in uranium accumulation (root and shoot) when cultivated in both regular soil and tailing soil conditions (Stojanović et al. 2016). However, due to some results that varied among different cultivars, uranium uptake was not only based on substrate types but also on specific cultivars (Stojanović et al. 2016).
Table 5. Crops analyzed in the reviewed papers.
Native, Non-native, Hybrids, Clones, and Crops
Previously described species were further divided into native and non-native species, while hybrid, clone, and crop species were categorised separately (Figure 2). The native species had the highest proportion, while non-native species, hybrids, clones, and crops species were utilised less frequently. Even though sites for phytoremediation practices may be very challenging for plant species and likely more suitable for invasive plant species, the high share of native plant species used is an encouraging practice. Invasive plants are recognised as a serious threat to the environment, even to the biosphere itself, but despite that, they are valued in phytoremediation practice for their high tolerance, wide distribution, and rapid growth (Khan et al. 2023). It cannot be disregarded that invasive plants are opportunists, and once established in a naturalised environment, it is almost impossible to eradicate them completely (Prabakaran et al. 2019). The spread of exotic and invasive species poses a serious threat, especially for vulnerable habitats such as wetlands. It may lead to the disruption of natural balance, displacement or extinction of the characteristic species, or even native biota loss (Yang et al. 2005, Leguizamo et al. 2017). Therefore, it is necessary to weigh the risk of the use of exotic and invasive species and their ability to offer substantial ecologically viable services for the sake of achieving holistic management of the entire environmental setting (Prabakaran et al. 2019).
Most Used Species
Out of the 65 previously mentioned plant species, certain ones have been featured in multiple research papers. Tilia sp. (Gorelova et al. 2011, Alagić et al. 2013, 2014, ) and Betula sp. (Gorelova et al. 2011, Alagić et al. 2013, 2014, ) have been identified in three different studies and are, as such, the most commonly used species according to reviewed scientific literature. In addition, the following species have been identified in two different studies: Tamarix tetrandra Pall. Ex M. Bieb. (Kostić et al. 2021, 2022); Achillea millefolium L. (Nujkić et al. 2020, Glisić et al. 2021,); Rubus fruticosus L. (Alagić et al. 2016, 2017); Erigeron canadensis L. (Conyza canadensis L.) (Krgović et al. 2015, Vukojević et al. 2016); Euphorbia cyparissias L. (Branković et al. 2015, Marić et al. 2013); Dactylis glomerata L. (Marić et al. 2013, Gajić et al. 2020).
Analysed Samples
The analysed studies were conducted on various samples such as soil, roots, leaves, shoots, stem/stalk, fly ash, rhizomes, whole plants, litterfall, branches, and inflo-rescences. The majority of studies included samples of soil, roots, and leaves, while the minority related to litterfall, branches, and inflorescences (Figure 3).
Figure 3. Different types of samples per publication number.
The observed results may indicate that most phytoremediation techniques incorporate considerations of the soil's condition. Moreover, given that the examination of roots has been widely acknowledged, it may be concluded that the practice of phytostabilization is the most employed. Other frequently examined parts, including leaves, shoots, and stems, may provide indications of phytoextraction techniques. Furthermore, given the existence of multiple studies focusing on fly ash areas, it can be assumed that there is a demand for the implementation of phytoremediation techniques in such sites. Our literature review did not identify any existing research that has investigated the implementation of phytovolatilization practices.
Analysed PTEs and Nutrients
Multiple studies have been conducted to investigate the occurrence of different elements in soil ecosystems. The PTEs identified in these studies include Cu, Zn, Cd, Pb, Ni, Mn, Fe, As, Cr, Ca, Mg, Co, B, Al, Ag, Se, S, Ti, Ba, Sb, and U. Additionally, nutrients N, P, and K were identified. Most of the publications evaluated in this study focused on the investigation of Cu, Zn, Cd, Pb, Ni, Mn, Fe, As, and Cr, while other PTEs were less included (Figure 4).
Figure 4. Analysed PTEs per publication number.
The obtained findings may provide insight into the state of pollution sources and, subsequently, the most frequently encountered pollutants. Most of the analysed papers are related to the mining sites (especially RTB Bor), which reveals the predominant site distribution for phytoremediation practice so far. This further implies that specific site characteristics may also have a significant influence on the appearance of contaminants. However, it is important to consider that the obtained results could potentially be influenced to some degree by limited funding resources. For instance, sampling and analysis of some elements might be complex, expensive, and unfamiliar, thus hindering researchers from conducting such analyses.
CONCLUSIONS
The examined body of scientific literature highlights the need for increased attention to phytoremediation research in Serbia, both in terms of its geographical distribution and research intensity. The summarised overview of plant species used for phytoremediation offers valuable insights into the potential efficiency of specific phytoremediation practices. However, it is crucial to acknowledge that the performance of various species may vary based on different factors. Additionally, combining multiple plant species may yield superior results compared to the application of a single species in phytoremediation practices. Whenever possible and feasible, native species should be prioritised, considering other relevant factors. Beyond the 65 species analysed, we recommend further research to explore the capabilities of additional native plants in the context of phytoremediation.
Author Contributions
FV, SBS, and SL developed the original idea and conceptualised the manuscript. FV conducted a review of the scientific literature and drafted the manuscript. SBS, DČ, MC, PM, NJ, AM, TG, and SL reviewed the drafted manuscript, performed editing, and critically revised the work. All authors have read and agreed to the final version of the manuscript.
Funding
This research received no external funding.
Acknowledgments
We would like to thank Jelena Beloica for helpful comments and suggestions, as well as Nemanja Nišavić for proofreading.
Conflicts of Interest
The authors declare no conflict of interest.
REFERENCES
Alagić SČ, Šerbula SS, Tošić SB, Pavlović AN, Petrović JV, 2013. Bioaccumulation of Arsenic and Cadmium in Birch and Lime from the Bor Region. Arch Environ Contam Toxicol 65(4):671–682. https://doi.org/10.1007/s00244-013-9948-7.
Alagić SČ, Tošić SB, Pavlović AN, 2014. Nickel content in deciduous trees near copper mining and smelting complex Bor (East Serbia). Carpathian J Earth Environ Sci 9: 191–199.
Alagić SČ, Jovanović VPS, Mitić VD, Cvetković JS, Petrović GM, Stojanović GS, 2016. Bioaccumulation of HMW PAHs in the roots of wild blackberry from the Bor region (Serbia): Phytoremediation and biomonitoring aspects. Sci Total Environ 562: 561–570. https://doi.org/10.1016/j.scitotenv.2016.04.063.
Alagić SČ, Stankov Jovanović VP, Mitić VD, Nikolić JS, Petrović GM, Tošić SB, Stojanović GS, 2017. The effect of multiple contamination of soil on LMW and MMW PAHs accumulation in the roots of Rubus fruticosus L. naturally growing near The Copper Mining and Smelting Complex Bor (East Serbia). Environ Sci Pollut Res 24(18): 15609–15621. https://doi.org/10.1007/s11356-017-9181-4.
Alagić SČ, Tošić SB, Dimitrijević MD, Nujkić MM, Papludis AD, Fogl VZ, 2018. The content of the potentially toxic elements, iron and manganese, in the grapevine cv Tamjanika growing near the biggest copper mining/metallurgical complex on the Balkan peninsula: phytoremediation, biomonitoring, and some toxicological aspects. Environ Sci Pollut Res 25(34): 34139–34154. https://doi.org/10.1007/s11356-018-3362-7.
Ali H, Khan E, Sajad MA, 2013. Phytoremediation of heavy metals—Concepts and applications. Chemosphere 91(7): 869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075.
Andrejić G, Šinžar-Sekulić J, Prica M, Dželetović Ž, Rakić T, 2019. Phytoremediation potential and physiological response of Miscanthus × giganteus cultivated on fertilized and non-fertilized flotation tailings. Environ Sci Pollut Res 26(33): 34658–34669. https://doi.org/10.1007/s11356-019-06543-7.
Belanović-Simić S, Bjedov I, Čakmak D, Obratov-Petković D, Kadović R, Beloica J, 2013. Influence of Zn on the availability of Cd and Cu to vaccinium Species in unpolluted areas - a case study of Stara Planina Mt. (Serbia). Carpathian J Earth Environ Sci 8(3): 5–14.
Belanović-Simić S, Čakmak D, Beloica J, Obratov-Petkovic D, Kadović R, Miljković P, Lukić S, Marković Đ, 2017. Bioaccumulation of Pb and Cd in soils of meadow associations Agrostietum capillaris (Z. Pavlović 1955): On Zlatar and Stara planina. Zemljište i biljka 66(2): 1–14.
Bortoloti GA, Baron D, 2022. Phytoremediation of toxic heavy metals by Brassica plants: A biochemical and physiological approach. Environmental Advances 8: 100204. https://doi.org/10.1016/j.envadv.2022.100204.
Branković S, Glisić R, Djekić V, Marin М, 2015. Metal accumulation and tolerance of selected plants of asbestos tailings (Stragari). Hem Ind 69(3): 313–321. https://doi.org/10.2298/HEMIND131017045B.
Branković S, Glisić R, Pavlović-Muratspahić D, Topuzović M, Đekić V, 2013. Phytoaccumulation of some metals by three species of genus Alyssum on one serpentine locality (Serbia). Fresenius Environ Bull 22(11): 3146–3154.
Brković DL, Bošković Rakočević LS, Mladenović JD, Simić ZB, Glišić RM, Grbović FJ, Branković SR, 2021. Metal bioaccumulation, translocation and phytoremediation potential of some woody species at mine tailings. Not Bot Horti Agrobo 49(4): 12487. https://doi.org/10.15835/nbha49412487.
Drzewiecka K, Gąsecka M, Magdziak Z, Rybak M, Budzyńska S, Rutkowski P, Niedzielski P, Mleczek M, 2024. Drought Differently Modifies Tolerance and Metal Uptake in Zn- or Cu-Treated Male and Female Salix × fragilis L. Forests 15(3): 562. https://doi.org/10.3390/f15030562.
Fernández-Caliani JC, Barba-Brioso C, González I, Galán E, 2009. Heavy Metal Pollution in Soils Around the Abandoned Mine Sites of the Iberian Pyrite Belt (Southwest Spain). Water Air Soil Pollut200(1–4): 211–26. https://doi.org/10.1007/s11270-008-9905-7.
Gajić G, Djurdjević L, Kostić O, Jarić S, Stevanović B, Mitrović M, Pavlović P, 2020. Phytoremediation Potential, Photosynthetic and Antioxidant Response to Arsenic-Induced Stress of Dactylis glomerata L. Sown on Fly Ash Deposits. Plants 9(5): 657. https://doi.org/10.3390/plants9050657.
Ghosh M, 2005. A review on phytoremediation of heavy metals and utilization of it’s by products. Appl Ecol Env Res 3(1): 1–18. https://doi.org/10.15666/aeer/0301_001018.
Glišić RM, Simić ZB, Grbović FJ, Rajičić VR, Branković SR, 2021. Phytoaccumulation of metals in three plants species of the Asteraceae family sampled along a highway. Not Bot Horti Agrobo 49(2): 12180. https://doi.org/10.15835/nbha49212180.
Gorelova SV, Frontasyeva MV, Yurukova L, Coskun M, Pantelica A, Saitanis CJ, Tomasević M, Aničić M, 2011. Revitalization of urban ecosystems through vascular plants: preliminary results from the BSEC-PDF project. Agrochimica 8(3): 5–14.
Haynes RJ, 2009. Reclamation and revegetation of fly ash disposal sites – Challenges and research needs. J Environ Manage 90(1): 43–53. https://doi.org/10.1016/j.jenvman.2008.07.003.
Jakovljević K, Mišljenović T, Savović J, Ranković D, Ranđelović D, Mihailović N, Jovanović S, 2020. Accumulation of trace elements in Tussilago farfara colonizing post-flotation tailing sites in Serbia. Environ Sci Pollut Res 27(4): 4089–4103. https://doi.org/10.1007/s11356-019-07010-z.
Jiang C, Wang Y, Chen Y, Wang S, Mu C, Shi X, 2024. The Phytoremediation Potential of 14 Salix Clones Grown in Pb/Zn and Cu Mine Tailings. Forests 15(2): 257. https://doi.org/10.3390/f15020257.
Khan IU, Qi S-S, Gul F, Manan S, Rono JK, Naz M, Shi XN, Zhang H, Dai ZC, Du DL, 2023. A Green Approach Used for Heavy Metals ‘Phytoremediation’ Via Invasive Plant Species to Mitigate Environmental Pollution: A Review. Plants 12(4): 725. https://doi.org/10.3390/plants12040725.
Kostić O, Gajić G, Jarić S, Vukov T, Matić M, Mitrović M, Pavlović P, 2021. An Assessment of the Phytoremediation Potential of Planted and Spontaneously Colonized Woody Plant Species on Chronosequence Fly Ash Disposal Sites in Serbia—Case Study. Plants 11(1): 110. https://doi.org/10.3390/plants11010110.
Kostić O, Jarić S, Gajić G, Pavlović D, Mataruga Z, Radulović N, Mitrović M, Pavlović P, 2022. The Phytoremediation Potential and Physiological Adaptive Response of Tamarix tetrandra Pall. Ex M. Bieb. during the Restoration of Chronosequence Fly Ash Deposits. Plants 11(7): 855. https://doi.org/10.3390/plants11070855.
Krgović R, Trifković J, Milojković-Opsenica D, Manojlović D, Marković M, Mutić J, 2015. Phytoextraction of metals by Erigeron canadensis L. from fly ash landfill of power plant “Kolubara.” Environ Sci Pollut Res 22(14): 10506–10515. https://doi.org/10.1007/s11356-015-4192-5.
Marić M, Antonijević M, Alagić S, 2013. The investigation of the possibility for using some wild and cultivated plants as hyperaccumulators of heavy metals from contaminated soil. Environ Sci Pollut Res 20(2): 1181–1188. https://doi.org/10.1007/s11356-012-1007-9.
Muthusaravanan S, Sivarajasekar N, Vivek JS, Paramasivan T, Naushad Mu, Prakashmaran J, Gayathri V, Al-Duaij OK, 2018. Phytoremediation of heavy metals: mechanisms, methods and enhancements. Environ Chem Lett 16(4): 1339–1359. https://doi.org/10.1007/s10311-018-0762-3.
Nikolić L, Džigurski D, Ljevnaić-Mašić B, 2014. Nutrient removal by Phragmites australis (Cav.) Trin. ex Steud. In the constructed wetland system. Contemp Probl Ecol 7(4): 449–454. https://doi.org/10.1134/S1995425514040106.
Nujkić M, Milić S, Spalović B, Dardas A, Alagić S, Ljubić D, Papludis A, 2020. Saponaria officinalis L. and Achillea millefolium L. as possible indicators of trace elements pollution caused by mining and metallurgical activities in Bor, Serbia. Environ Sci Pollut Res 27(36): 44969–44982. https://doi.org/10.1007/s11356-020-10371-5.
Oyuela Leguizamo MA, Fernández Gómez WD, Sarmiento MCG, 2017. Native herbaceous plant species with potential use in phytoremediation of heavy metals, spotlight on wetlands — A review. Chemosphere 168: 1230–1247. https://doi.org/10.1016/j.chemosphere.2016.10.075.
Pandey VC, Singh N, 2010. Impact of fly ash incorporation in soil systems. Agric Ecosyst Environ 136(1–2): 16–27. https://doi.org/10.1016/j.agee.2009.11.013.
Petrović JV, Alagić SČ, Milić SM, Tošić SB, Bugarin MM, 2021. Chemometric characterization of heavy metals in soils and shoots of the two pioneer species sampled near the polluted water bodies in the close vicinity of the copper mining and metallurgical complex in Bor (Serbia): Phytoextraction and biomonitoring contexts. Chemosphere 262: 127808. https://doi.org/10.1016/j.chemosphere.2020.127808.
Pietrzykowski M, Antonkiewicz J, Gruba P, Pająk M, 2018. Content of Zn, Cd and Pb in purple moor-grass in soils heavily contaminated with heavy metals around a zinc and lead ore tailing landfill. Open Chem 16(1): 1143–1152. https://doi.org/10.1515/chem-2018-0129.
Pilipović A, Zalesny RS, Orlović S, Drekić M, Pekeč S, Katanić M, Poljaković-Pajnik L, 2020. Growth and physiological responses of three poplar clones grown on soils artificially contaminated with heavy metals, diesel fuel, and herbicides. Int J Phytoremediation 22(4): 436–450. https://doi.org/10.1080/15226514.2019.1670616.
Pilipović A, Zalesny RS, Rončević S, Nikolić N, Orlović S, Beljin J, Katanić M, 2019. Growth, physiology, and phytoextraction potential of poplar and willow established in soils amended with heavy-metal contaminated, dredged river sediments. J Environ Manage 239: 352–365. https://doi.org/10.1016/j.jenvman.2019.03.072.
Pilon-Smits E. 2005. Phytoremediation. Annu Rev Plant Biol 56(1): 15–39. https://doi.org/10.1146/annurev.arplant.56.032604.144214.
Pourret O, Hursthouse A, 2019. It’s Time to Replace the Term “Heavy Metals” with “Potentially Toxic Elements” When Reporting Environmental Research. Int J Eniron Res Pub Health 16(22): 4446. https://doi.org/10.3390/ijerph16224446.
Prabakaran K, Li J, Anandkumar A, Leng Z, Zou CB, Du D, 2019. Managing environmental contamination through phytoremediation by invasive plants: A review. Ecol Eng 138: 28–37. https://doi.org/10.1016/j.ecoleng.2019.07.002.
Prica M, Andrejić G, Šinžar-Sekulić J, Rakić T, Dželetović Ž, 2019. Bioaccumulation of heavy metals in common reed (Phragmites australis) growing spontaneously on highly contaminated mine tailing ponds in Serbia and potential use of this species in phytoremediation. Bot Serb 43(1): 85–95. https://doi.org/10.2298/BOTSERB1901085P.
Ranđelović D, Gajić G, Mutić J, Pavlović P, Mihailović N, Jovanović S, 2016. Ecological potential of Epilobium dodonaei Vill. for restoration of metalliferous mine wastes. Ecol Eng 95: 800–810. https://doi.org/10.1016/j.ecoleng.2016.07.015.
Ranđelović D, Jakovljević K, Mihailović N, Jovanović S, 2018. Metal accumulation in populations of Calamagrostis epigejos (L.) Roth from diverse anthropogenically degraded sites (SE Europe, Serbia). Environ Monit Assess 190(4): 183. https://doi.org/10.1007/s10661-018-6514-9.
Shah V, Daverey A, 2020. Phytoremediation: A multidisciplinary approach to clean up heavy metal contaminated soil. Environ. Technol Innov 18: 100774. https://doi.org/10.1016/j.eti.2020.100774.
Sharma P, Pandey S, 2014. Status of Phytoremediation in World Scenario. Int J Environ Bioremediat Biodegrad 2(4): 178–191.
Stojanović M, Pezo L, Lačnjevac Č, Mihajlović M, Petrović J, Milojković J, Stanojević M, 2016. Biometric approach in selecting plants for phytoaccumulation of uranium. Int J Phytoremediation 18(5): 527–533. https://doi.org/10.1080/15226514.2015.1115966.
Stojnić S, Orlović S, Tepavac A, Kesić L, Galić Z, Drekić M, Kebert M, 2019. Heavy Metals Content in Foliar Litter and Branches of Quercus petraea (Matt.) Liebl. and Quercus robur L. Observed at Two ICP Forests Monitoring Plots. South-east Eur for 10(2): 151–157. https://doi.org/10.15177/seefor.19-11.
Sun H, Wang Z, Gao P, Liu P, 2013. Selection of aquatic plants for phytoremediation of heavy metal in electroplate wastewater. Acta Physiol Plant 35(2): 355–364. https://doi.org/10.1007/s11738-012-1078-8.
Trudić B, Kebert M, Popović MB, Stajner D, Orlović S, Galović V, Pilipović A, 2013. The effect of heavy metal pollution in soil on serbian poplar clones. Sumar List 137(5–6): 287–296.
Vukojević V, Trifković J, Krgović R, Milojković-Opsenica D, Marković M, Amaizah N, Mutić J, 2016. Uptake of metals and metalloids by Conyza canadensis L. from a thermoelectric power plant landfill. Arch biol sci (Beogr) 68(4): 829–835. https://doi.org/10.2298/ABS151011071V.
Wei Z, Van Le Q, Peng W, Yang Y, Yang H, Gu H, Lam SS, Sonne C, 2021. A review on phytoremediation of contaminants in air, water and soil. J Hazard Mater 403: 123658. https://doi.org/10.1016/j.jhazmat.2020.123658.
Yang X, Feng Y, He Z, Stoffella PJ, 2005. Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J TraceElem Med Biol 18(4): 339–353. https://doi.org/10.1016/j.jtemb.2005.02.007.
Yao Z, Li J, Xie H, Yu C, 2012. Review on Remediation Technologies of Soil Contaminated by Heavy Metals. Procedia Environ Sci 16: 722–729. https://doi.org/10.1016/j.proenv.2012.10.099.
Zhang X, Yan L, Liu J, Zhang Z, Tan C, 2019. Removal of Different Kinds of Heavy Metals by Novel PPG-nZVI Beads and Their Application in Simulated Stormwater Infiltration Facility. Appl Sci-Basel 9(20): 4213. https://doi.org/10.3390/app9204213.
© 2024 by the Croatian Forest Research Institute. This is an Open Access paper distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0).