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Potential of Selected Canadian Plant Species for Phytoextraction of Trace Elements From Selenium-Rich Soil Contaminated by Industrial Activity a

a

a

Werther Guidi Nissim , Séverine Hasbroucq, Hafssa Kadri , Frederic E. Pitre & Michel a

Labrecque a

Institut de recherche en biologie végétale, Montreal Botanical Garden, Montréal, Québec, Canada Published online: 01 Jun 2015.

Click for updates To cite this article: Werther Guidi Nissim, Séverine Hasbroucq, Hafssa Kadri, Frederic E. Pitre & Michel Labrecque (2015) Potential of Selected Canadian Plant Species for Phytoextraction of Trace Elements From Selenium-Rich Soil Contaminated by Industrial Activity, International Journal of Phytoremediation, 17:8, 745-752, DOI: 10.1080/15226514.2014.987370 To link to this article: http://dx.doi.org/10.1080/15226514.2014.987370

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International Journal of Phytoremediation, 17: 745–752, 2015 C Taylor & Francis Group, LLC Copyright  ISSN: 1522-6514 print / 1549-7879 online DOI: 10.1080/15226514.2014.987370

Potential of Selected Canadian Plant Species for Phytoextraction of Trace Elements From Selenium-Rich Soil Contaminated by Industrial Activity ´ WERTHER GUIDI NISSIM , SEVERINE HASBROUCQ, HAFSSA KADRI, FREDERIC E. PITRE, and MICHEL LABRECQUE

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Institut de recherche en biologie v´eg´etale, Montreal Botanical Garden, Montr´eal, Qu´ebec, Canada

In this preliminary screening study, we tested the phytoextraction potential of nine Canadian native/well-adapted plant species on a soil highly polluted by trace elements (TE) from a copper refinery. Plant physiological parameters and soil cover index were monitored for a 12-week period. At the end of the trial, biomass yield, bioconcentration (BFC) and translocation (TF) factors for the main TE as well as phytoextraction potential were determined. Most plants were severely injured by the high pollution levels, showing symptoms of toxicity including chlorosis, mortality and very low biomass yield. However, Indian mustard showed the highest selenium extraction potential (65 mg m−2), even under harsh growing conditions. Based on our results, tall fescue and ryegrass, which mainly stored As, Cu, Pb and Zn within roots, could be used effectively for phytostabilization. Keywords: Se, heavy metals, As, phytoremediation, salix, indian mustard

Introduction Despite increasing sensitivity to environmental issues worldwide, some industrial activities continue to generate pollutants. Even in countries where industrial processes are strictly regulated, environmental contamination may be found on sites that have been exploited over an extended period of time. This is the case for many pre-World War II industrial sites, on which environmental impacts were scarcely controlled. Today, many remain heavily contaminated by organic or inorganic (mostly trace elements) compounds and require clean-up. Copper refining is one example of an industrial process that can generate environmental pollution. Copper is mostly refined by electrolysis, which converts copper anodes into pure copper cathodes (Cooper 1990). This process also generates other valuable metals (e.g., gold and silver) that can be sold, as well as trace elements (TE) (e.g., selenium, arsenic, nickel, lead) that are concentrated in the slimes, and, if not properly managed, can be disseminated in the environment. Relatively few conventional remediation techniques for organic contamination are applicable to soils polluted by inorganics (McEldowney et al. 1993). The remediation of harmful environmental contaminants using living organisms such as plants and soil microorganisms (known as phytoremediation)

Address correspondence to Michel Labrecque, Institut de recherche en biologie v´eg´etale, Universit´e de Montr´eal and Montreal Botanical Garden, 4101 Sherbrooke East, Montreal, QC H1X 2B2, Canada. E-mail: [email protected]

is becoming very popular, mainly because of its low environmental impact and low cost, compared with most conventional decontamination techniques (Vangronsveld et al. 2009). The term “phytoremediation” includes a wide range of techniques that exploit the ability of plants and their microbial rhizospheres to uptake, degrade and sequester organic and inorganic pollutants from soil and water (Pilon-Smits 2005). In the case of inorganic contaminants such as TE, two main phytoremediation strategies can be proposed. In phytoextraction, plants are used to uptake pollutants from soils and accumulate them in their tissues, with or without the assistance of microbial rhizospheres. This technique may eventually achieve an acceptable level of decontamination once the plant biomass is harvested and removed from the site. Another approach is to reduce bioavailable TE in the environment through stabilization techniques. Vegetative covers reduce the leaching of contaminants into groundwater and prevent the dispersal of polluted dusts through wind and water erosion of bare sites. Most current phytoremediation approaches use highmaintenance, short-term agricultural techniques, including the planting of selected species that are often not represented among spontaneous vegetation on the site. However, there is growing interest in a more ecological approach, relying on indigenous or well-adapted species to maintain higher local biodiversity more appropriate to the specificity of the site. It has been suggested that any ecologically-conscious and sitespecific rehabilitation approach should be based on observations of spontaneous revegetation patterns and should use species that are most effective at phytoremediation as well as

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746 able to adapt readily to local environmental conditions (Danh et al. 2009). This should eventually lead to a greater diversity of associated soil microorganisms (Eisenhauer et al. 2010), potentially increasing the effectiveness of the remediation process. Plants used in phytoextraction fall into two groups: some demonstrate tolerance and very high accumulation levels of the TE targeted; others have lower TE accumulation levels but a profuse root system, rapid growth rate and high biomass production (Marques et al. 2009). Plants in the first group are referred to as “hyperaccumulators,” having the potential to accumulate very high amounts of one or more TE in their biomass. They show TE concentrations in their dry biomass that may be 100 times higher than non-hyperaccumulators growing on the same site. Most hyperaccumulator plants are able to concentrate TE over a threshold of 100 mg g−1 (0.01% dry weight) for Cd, As, 1,000 mg g−1 (0.1% dry weight) for Co, Cu, Cr, Ni, and Pb and 10,000 mg g−1 (1% dry weight) Mn and Ni (Baker and Brooks 1989). Unfortunately, hyperaccumulators do not produce very high biomass rates. The second group of plant species commonly used for phytoextraction (e.g., willows and poplars) do not take-up TE in excessive amounts compared to their weight, but their high biomass yield makes them particularly efficient (Rockwood et al. 2004). Therefore, the choice of species is vast and may represent a complex issue. The aim of the current study was to test the performance of several indigenous and/or well-adapted plant species from Canada on polluted soil from a copper refinery with very high concentrations of Se as well as other trace elements (i.e., As, Cd, Cu, Pb, and Zn).

Materials and Methods In the spring of 2013, we set up a greenhouse pot trial to test the ability of nine indigenous (or adapted) Canadian species to accumulate TE. The species tested were: two willow cultivars (S05 Salix nigra Marsh. and S25 S. eriocephala Michx.), balsam poplar (Populus balsamifera L.), alfalfa (Medicago sativa L.), tall fescue (Festuca arundinacea Schreb.), wild carrot (Daucus carota L.), Indian mustard (Brassica juncea (L.) Czern.), switchgrass (Panicum virgatum L.), and ryegrass (Lolium perenne L.). The polluted soil to be used for planting was obtained from the site of a copper refinery in Montreal, Quebec that processes copper anodes, converting them into 99.9% copper cathodes for sale on world markets. This refinery has been in operation since 1931. In total, ten 1 L pots per species were prepared, randomly arranged into five blocks, each containing two replicates per species. Total-recoverable trace elements in the soil were measured by ICP-MS after nitric acid digestion (Wilson et al. 2005). Available trace element concentrations were also determined by ICP-MS on soil water extraction samples (1:10 soil-water ratio). The main pollutants in the excavated soil were selenium (Se), arsenic (As) and copper (Cu), (Table 1). The selected herbaceous plants were sown from seed at a 20 kg ha−1 equivalent dose whereas for willows and poplars,

W. G. Nissim et al. Table 1. Properties and contamination of the excavated soil used in this study Parameters CEC pH Ca OM Clay Silt Sand As Cd Cu Pb Se Zn

Units

meq/100g — kgha−1 % % % % Main pollutants mg kg−1

Values 30.1 8.0 12574 1.4 18.7 25.2 56.1 Total 48.6 1.0 1760 204 536 270

Available 0.459 0.0004 1.382 0.084 18.964 0.212

one-year-old 20 cm long cuttings were used as planting material (1 cutting per pot). Plants were left to grow under the following environmental conditions: Tday 22◦ C, Tnight 18◦ C, RH 70%, light intensity 300 μE m−2s−1, natural lighting augmented with full-spectrum fluorescent lighting to provide a 16h-photoperiod; plants were watered regularly to maintain soil moisture around field capacity. The experiment was conducted for a period of 12 weeks (90 days). After two weeks of growth (W2), plants were fertilized with 100 ml of a NH4 NO3 solution (1.25 mM) every three/four days. After three weeks (W3), the height of the twig/canopy and the cover-abundance scale (Braun-Blanquet 1951) were measured weekly. After seven weeks of growth (W7), several physiological parameters were also documented. Stomatal conductance was measured on the abaxial leaf surface of plants with a SC-1 Leaf Porometer (Decagon Devices, Inc.). Total leaf chlorophyll content was estimated by means of a handheld chlorophyll meter LEAF+ (FT Green LLC). These parameters were not noted for tall fescue, ryegrass or switchgrass, because leaves were too small to manipulate. At the end of the trial (W12), all plants were harvested, and the dry matter of aboveground parts (leaves + newly formed twigs) and roots was determined. The roots were then rinsed several times in a 0.05 M CaCl2 solution. The concentrations of TE in the biomass of leaves and roots were determined through ICP-MS after nitric acid digestion. The bioconcentration factor for roots (BCFr ) and aerial organs (BCFs ) was calculated as the ratio between element concentration in the plant and in the soil (i.e., BCFr = Croot /Csoil BCFs = Caerial /Csoil ). The translocation factor TF = [(C aerial /C root )×100] was calculated as the ratio between metal concentration in the shoots and the roots, and reported as a percentage (Mattina et al. 2003; Marchiol et al. 2004). Finally, the element uptake per square meter was calculated for each species by multiplying element concentrations and biomass (root and leaf) where available. The data collected were subjected to statistical analysis using SAS software with one-way ANOVA with post hoc separation of

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the means by Tukey’s method to identify significant (p < 0.05) differences among species.

Results and Discussion

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Plant Growth and Physiology Most species planted in this study were negatively affected by the contaminated soil and showed symptoms of toxicity (chlorosis) as soon as a few weeks after sowing/planting. The soil cover index for some species (i.e. wild carrot and switchgrass) was very low from the beginning of the trial, attesting to their low adaptability to this type of growing medium (Fig. 1A). Other species (i.e., Indian mustard, alfalfa) experienced an initial period of relatively constant values, then showed a decrease beginning in W7. Others (i.e., ryegrass and tall fescue) showed a constant increase of soil cover index throughout the duration of the study. Overall, the highest Braun-Blanquet cover-abundance index was registered for Indian mustard. For woody species, we observed a generally constant decrease in the number of twigs per cutting that was less abrupt in willow S05, suggesting that this species had a higher tolerance toward this type of soil. The most productive species in terms of aboveground biomass was Indian mustard (50 g m−2), followed by ryegrass (40 g m−2) and tall fescue (30 g m−2) (Fig. 1B). The less productive species were switchgrass and wild carrot. With regard to root biomass production, the highest values were found in ryegrass (23 g m−2) and tall fescue (22 g m−2), whereas Indian mustard performed less well (10 g m−2). A recent review (Schippers and Mnzava 2007) reported that equivalent leaf yield of Indian mustard at the farm level ranges from 800–3500 g m−2 (i.e., 8 – 35 Mg ha−1). The same holds for ryegrass, which under normal conditions shows aerial biomass yield of about 1000–1300 g m−2 (10–13 Mg ha−1)(Elsaesser 2004). These figures illustrate the extent to which even the more tolerant species in this trial were severely affected by the high contamination levels of the soil. Leaf chlorophyll content is a valuable index to estimate plant health (Liu et al. 1997) and nutritional status (Cooke et al. 2005). In our study, most species had a rather low average leaf chlorophyll content compared to most data in the literature (Fig. 2A). Herbaceous species had an even lower chlorophyll content than woody species. However, this cannot necessarily be attributed to differing tolerance to contaminants and may be mainly a reflection of the different resource availability experienced by these species during the establishment period. In particular, woody species in this trial were planted as cuttings, which have a relatively high amount of stored nonstructural carbohydrate reserves available to permit plant functionality even under harsh environmental conditions (Carpenter et al. 2008). Stomatal conductance values, which did not differ statistically among species, were in general very low throughout the trial (Fig. 2B). For example, available data for willows grown under unpolluted conditions show values ranging from 400 mmol m−2 s−1 to 800 mmol m−2 s−1, far above the 40–80 mmol m−2 s−1 measured in this trial. This is likely

Fig. 1. Cover abundance index during the trial (A), and biomass yield (B) of the plants at harvest time. Different letters indicate significant differences according to Tukey test (p < 0.05).

because high soil metal content affected the functionality of the root system. A recent study has highlighted the similarity between plant response to metals and to drought, likely due to the reduced water uptake ability of roots exposed to metals (de Silva et al. 2012). The reduction we found in plant functionality affected both above and belowground biomass yields, which in general were very low, although with some differences among species. Surprisingly, all woody species showed very low root and leaf biomass values. Bioaccumulation and Translocation Factors Both bioconcentration factors (BCF) and translocation factors (TF) can be used to assess the potential of a species for phytoremediation purpose. BCF is suited to evaluate the ability of plants to accumulate TE from the soil (i.e., the ratio between TE concentration in the roots and in the soil) whereas TF is useful to estimate the plant’s ability to translocate TEs from the roots to the shoots. The process of phytoextraction generally requires the translocation of TE to the easily harvestable plant parts. By comparing BCF and TF, we can compare the ability of different plants in taking up TE from soils and translocating them to the shoots. Tolerant plants show low accumulation in their biomass, whereas hyperaccumulators actively take up and translocate metals into their

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Fig. 2. Physiological parameters of the plants tested in the experiment. (A) Chlorophyll content and (B) Stomatal conductance. Different letters indicate significant differences according to Tukey test (p < 0.05).

aboveground biomass. Plants exhibiting BCF values less than 1 are considered unsuitable for phytoextraction (Fitz and Wenzel 2002). At the end of the current trial, several species were severely injured (or had died). This did not allow us to collect enough biomass to perform chemical analysis, specifically in the case of poplar. Other species, such as wild carrot and willows, produced insufficient root biomass for chemical analysis. Data concerning the BCF of and TF are shown in Figure 3. Highest BCFs for Se were found for wild carrot (2.83), Indian mustard (2.40), and tall fescue (2.34) whereas BCFr for Se were highest in Indian mustard (2.26) and alfalfa (1.98). BCFs for As was highest in wild carrot (0.12) whereas BCFr was highest for Indian mustard (0.12). Wild carrot also showed the highest BCFs for Cu (0.21) and Pb (0.19). The BCFs for Cd was particularly remarkable, very high in both willow species, ranging from 8.9 in willow S25 and 4.2 in willow S05 respectively. These two species also showed the highest BCFs for Zn. Some of these data are relatively lower than findings in other studies. For instance, values of BCFs and BCFr of Indian mustard have been reported to be 1.40 and 0.45 for Cd, 1.17 and 0.18 for Cu, 0.55 and 0.08 for Pb, and 1.01 and 0.34 for Zn (Marchiol et al. 2004). These discrepancies could be attributed

W. G. Nissim et al. to differences in the composition of the growing medium. In addition, it should be noted that BCF coefficients under field conditions are known to be lower than those observed in the laboratory, where the concentration of available elements is generally higher than in the field (Kumar et al. 1995). On the other hand, data concerning Se concur with other comparable ˜ studies showing high Se affinity in Indian mustard (Banuelos ˜ et al. 2000) and tall fescue (Wu et al. 1988; Banuelos and Lin 2005). Our data on Cu accumulation within plant tissues are also in line with findings in other studies that reported Festuca spp. has a high affinity with this element (Padmavathiamma and Li 2009). The highest translocation factors (TF) for Se, Zn, As, Pb, and Cu were found in Indian mustard (84%, 67%, 57%, 54%, 49% respectively) and alfalfa (75%, 67%, 59%, 57%, 50% respectively). The high capacity of Indian mustard to translocate Se to aboveground organs has been demonstrated ˜ in other studies (Banuelos et al. 1996), and alfalfa has been reported to be able to translocate Se to its leaves, although the extent depends on certain soil properties (i.e., sulphate content) (Bell et al. 1992). Plant metal uptake depends on many parameters such as soil properties, contamination levels, and plant species, also varies according to seasons (Bidar et al. 2009). A recent research showed that the TE uptake process is species- and/or element-dependent and cannot be generalised (Djingova and Kuleff 2007). However, it has been found that plant exposure to TE induces stress in many species by overproducing reactive oxygen species (ROS) which can generate oxidative damage to various biomolecules, and possibly engender cell death (Mittler 2002). Thus one of the main plant characteristic influencing TE uptake is the ability to withstand this stress. Plants have different enzymes like catalases (CAT), peroxidases, superoxide dismutases (SOD), and nonenzymatic constituents which remove, neutralize ROS (Munn´e-Bosch 2005) This can explain the high variability in plant response to the same polluted environment.

Phytoextraction Potential Once the element concentrations and the plant biomass yield over a unit surface are considered, the actual phytoextraction potential is shown for each species (Fig. 4). In the current trial, Indian mustard showed the highest Se extraction potential (65 mg m−2) by aerial parts, followed by ryegrass (42 mg m−2) and tall fescue (21 mg m−2), both with values well above those for other herbaceous and woody species (about 4-5 mg m−2). Tall fescue and ryegrass had a high affinity towards As (0.27 mg m−2 and 0.24 mg m−2), Cu (20.6 mg m−2 and 18.7 mg m−2), Pb (1.58 mg m−2 and 1.39 mg m−2), and Zn (3.72 mg m−2 and 5.30 mg m−2), storing it mainly in their roots. Willows showed the highest Cd uptake per square meter (0.8 mg), but these values are not very high. However, there are several ways to improve the phytoextraction potential of certain plants. For example, it has been shown that in some species that uptake Pb at a low rate (i.e. Indian mustard), using multiple (i.e., three) crops in one growing season may lead to a drop in soil concentrations of Pb to acceptable levels (Blaylock et al. 1999). We attempted to apply this

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Selected Plant Species for Phytoextraction of Selenium

Fig. 3. Translocation and Bioconcentration Factors for the 8 species evaluated in this study.

strategy by re-sowing the same species after harvesting, but the results were not satisfactory, since we still observed the same symptoms of toxicity (e.g., chlorosis, very low growth rates, etc.) as soon as a few weeks after sowing (data not shown). Phytoextraction potential can also be improved by inoculating plants with specific microorganism strains that have been shown to improve plant response to such extreme growing conditions by either enhancing plant growth (Belimov

et al. 2005) or protecting the plant from metal toxicity (Wu et al. 2006). However, in the current screening trial we believe that phytoextraction was limited by high contaminant concentrations, which likely restricted plant growth and thereby decreased pollutant uptake and translocation. Moreover, the phytoextraction capacity of most plants in the current trial could have been hindered by the fact the substrate contained a

W. G. Nissim et al.

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Fig. 4. Trace element accumulation in the leaves and roots over a unit surface. Different letters indicate significant differences according to Tukey test (p < 0.05).

mixture of contaminants. Several studies have reported that the phytoremediation capacity of a plant (i.e., uptake of metal/metalloid) may be very different for mixtures of metals than for one metal/metalloid alone (Ebbs et al. 1997). Therefore, for effective phytoextraction of mixed metals/metalloids from soil, other technologies may be required. Phytoremediation might be used on the less contaminated areas of the site or, as suggested by some authors, in a final phase of clean-up, when conventional land treatment has been completed without achieving the desired drop in contaminant concentration (Pivetz 2001). Implementation at Field-Scale To date, phytoremediation has mostly been restricted to bench and greenhouse scale trails, particularly in the case of phytoextraction. This makes it difficult to extrapolate reliable information for large-scale application. Several studies have

shown that results obtained under controlled environmental conditions (i.e., greenhouse) may differ largely when plants are grown in the field. For instance, a recent trial on TE accumulation in Brassica napus showed that this species was able to accumulate high amount of metals in greenhouse conditions, whereas it grew with difficulty or not at all in the open field, and metal accumulation in plant fractions was relatively low (Brunetti et al. 2011). These differences in metal uptake between field and controlled pot conditions were attributed to the different physiological state of the plant and to some modification of soil properties and climate parameters in pot conditions (Conesa et al. 2007). This can also be explained by the restricted volume of soil prospected by the roots in potted plants and thus their better efficiency in TE uptake (Rosselli et al. 2003). Besides, it is now well established that the plant modifies TE bioavailability in the rhizosphere, either enhancing or reducing their availability, by directly affecting acidification, chelation, precipitation and redox reactions, or

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Selected Plant Species for Phytoextraction of Selenium indirectly, through their effects on microbial activity, physical and chemical properties of the rhizosphere and root growth pattern (Kidd et al. 2009). Therefore, the phytoremediation potential of a plant species at field scale is not always easy to predict. We believe that most results in the current trial likely reflect the field-scale conditions since the soil used was homogeneous and representative of the site. This applies also for some unsuccessful results concerning woody species. In the current trial poplar and willow unexpectedly failed in establishing on this highly polluted substrate. However, there exist different technologies that can be used to assist plant establishment in field. For instance, planting cuttings in tranches backfilled with clean, uncontaminated topsoil has been shown to allow for greater tree cutting growth and survival in the long term (Cook et al. 2010). It has been shown, that the supply of appropriate amounts of common soil amendments (biosolids), which contain a variety of nutrients, as well as a large proportion of organic matter may enhance plant establishment on poor sites (Kim and Owens 2010). This would eventually allow these plants to establish good fibrous root systems whose long-term impact on phytoextraction (both through enhanced plant uptake and activity of the rhizopshere microorganisms) could be comparable (or greater) to grasses.

Preliminary Conclusions We conducted a preliminary pot trial to evaluate which plant species may be most suitable for use in phytoextraction of trace metals from heavily polluted soil from a copper refinery. Establishment and growth of most plant species tested was affected negatively. Herbaceous species showed high affinity to Se. Due to the combination of high BCF and TF, as well as biomass yield, Indian mustard showed the highest Se extraction potential (65 mg m−2), even under challenging environmental conditions. Tall fescue, ryegrass, which mainly stores As, Cu, Pb and Zn in its roots, could be used for phytostablization. Willows (in particular the indigenous Salix eriocephala S25 cultivar) should be further investigated to screen their potential for Cd phytoextraction.

Acknowledgments The authors wish to thank St´ephane Daigle for assistance with statistical analysis and interpretation of the results; and Karen Grislis for review of the English style of the manuscript.

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Potential of selected Canadian plant species for phytoextraction of trace elements from selenium-rich soil contaminated by industrial activity.

In this preliminary screening study, we tested the phytoextraction potential of nine Canadian native/well-adapted plant species on a soil highly pollu...
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