Advertisement

Metal Tolerance Capability of Helichrysum microphyllum Cambess. subsp. tyrrhenicum Bacch., Brullo & Giusso: A Candidate for Phytostabilization in Abandoned Mine Sites

  • G. Bacchetta
  • M. E. Boi
  • G. Cappai
  • G. De Giudici
  • M. Piredda
  • M. Porceddu
Article

Abstract

Sardinia was known as an important mine pole in Europe during his history. Still after decades from mine closure, 75.000.000 m3 of mine waste, rich in heavy metals, were left abandoned causing a huge environmental legacy on the mine district area. Consequently, cost effective remediation is required. In this frame, phytoremediation is considered a feasible candidate. This research was focused on Helichrysum microphyllum subsp. tyrrhenicum, which is pioneer in xeric soils with low-functions, like mine tailings. The aim of this study was to evaluate its ability to extract heavy metals from mine soils and accumulate them in plant tissues and its suitability for phytostabilization. Sundry samples of soil, roots and epigean organ were collected through field sampling and analysed in order to obtain metals concentration and mineralogical characteristics. Our results indicate that this species tolerates high concentration of zinc, lead and cadmium, behaving as a species suitable for phytostabilization.

Keywords

Heavy metals Mine tailings Mediterranean flora Phytostabilization Vascular plant 

Sardinia was one of the most important mining poles in Europe until the fifties of twentieth century when it reached the most productive period of its history (Bacchetta et al. 2012; Jimènez et al. 2014). However, after the mines closure, only few remediation actions have been done. As a result, high quantities of polluted materials are left abandoned and exposed to weathering (Jimènez et al. 2011). This process combined to the low presence or the absence of plant canopy affect mobilization of pollutants like soluble salts of heavy metals, which were recognized in high concentration in fresh waters, soils and plants (Bacchetta et al. 2015; Concas et al. 2015; De Giudici et al. 2017). Phytoremediation can be applied in these areas by using vascular plant species and their associated microbiota in combination with amendments and different kind of agronomic strategies in order to remove, limit or make contamination as harmless as possible (Raskin and Ensley 2000). Moreover, it can provide a cost efficient, long-lasting and visual impact solution for contaminated sites (Mulligan et al. 2001). In order to preserve local plant diversity, it is important to use autochthonous species because they do not interfere with floristic and vegetation dynamics (Cao et al. 2009; Sprocati et al. 2014; Concas et al. 2015; Lai et al. 2015), and are adapted to local climatic conditions. Lately, several studies on Sardinia mining sites have suggested different autochthonous plant species which present these properties, like Dittrichia viscosa L. (Greuter), Cistus salviifolius L. (Jimènez et al. 2005, 2014), Pistacia lentiscus L. and Scrophularia canina L. subsp. bicolor (Sibth.) Greuter (Jimènez et al. 2005, 2014; Bacchetta et al. 2012, 2015; De Giudici et al. 2015; Tamburini et al. 2016), Euphorbia cupanii Bertol ex Moris (Jimènez et al. 2005; Medas et al. 2015), Phragmites australis (Cav.) Trin. ex Steud and Juncus acutus L. (De Giudici et al. 2017; Medas et al. 2017). It has been shown that in E. cupanii, P. lentiscus and P. australis, there are bio-minerals of Zn, Si and/or Pb on roots epidermis different from soil’s minerals (De Giudici et al. 2015, 2017; Medas et al. 2015), indicating that roots build bio-minerals as a survival strategy of the species (Caldelas et al. 2017).

Helichrysum microphyllum Cambess. subsp. tyrrhenicum Bacch., Brullo & Giusso (hereafter H. tyrrhenicum), is an endemic shrub of Sardinia and Corse. It is well adapted to the Mediterranean climatic conditions and grows on different kind of substrates, especially on sandy and muddy soils, and arid substrates with low organic matter content (Angiolini et al. 2005; Bacchetta et al. 2009). In Sardinia, it can grow from sea level up to 1500 m a.s.l. and it can be recognized as part of different vegetation assemblages of mine environment (Angiolini et al. 2005; Bacchetta et al. 2003, 2007). Specific studies involving the metal tolerance and the accumulation strategies of H. tyrrhenicum are at present fairly scarce (Cao et al. 2004). In this study, we collected specimens of H. tyrrhenicum spontaneously grown in heavy metals contaminated areas and their related soils and we evaluated the content of cadmium, zinc and lead in soil samples and their distribution in the plant’s tissues, with the aim to perform a preliminary evaluation of the plant’s metal tolerance and accumulation mechanisms, in the perspective of using it within phytoremediation applications.

Materials and Methods

The studied area was the mine dump of Campo Pisano (Iglesias, South-West Sardinia) which is hosted in the Paleozoic carbonate platform, in particular on the Gonnesa’s Formation and the Metalliferous belt (Bechstädt and Boni 1994). The metalliferous bodies are hosted in Cambrian limestones and dolomites (Bechstädt and Boni 1994). The activity at Campo Pisano ceased in 1997 after centuries of mine exploitation. The exploited ore minerals were mainly sphalerite and galena, plus some Zn calamina minerals like smithsonite, hydrozincite (and hemimorphite). The dump is made of fine material (< 100 µm), residue of flotation treatment for metal extraction, characterized by high levels of metal contamination. It is noteworthy that soils of this area are naturally enriched with heavy metals due to the geochemical background, and Zn, Pb and Cd being the main pollutants (Bacchetta et al. 2012, 2015; Concas et al. 2015). The whole area is characterized by a Mediterranean pluviseasonal bioclimate, with thermotypes ranging between the upper thermo-Mediterranean and the lower meso-Mediterranean and ombrotypes between the upper dry and the lower sub-humid (Bacchetta et al. 2009).

For the aim of this study, samples of spontaneously growing plants of H. tyrrhenicum and related soils were collected in 2016 in four sampling sites: two inside the mining area (CP and PLOT), one outside the mine and with a similar mineralogical background (OCP), and one far away from the mine site and without mine impact (SS, Capoterra, South-West Sardinia) (see Table 1 for details about codes, and Fig. 1 for details about localisation). The PLOT sampling site was chosen within an area where a field phytoremediation experiment using native plants such as Pistacia lentiscus L. and Scrophularia canina L. subsp. bicolor (Sibth et Sm.) Greuter has been previously carried out (Bacchetta et al. 2012).

Table 1

Sampling sites and codes, geographical coordinates and number of collected samples

Sampling sites

Code

Coordinates (WGS 84)

Campo Pisano mine dump

CP

39°17′45.2″N, 8°32′15.1″E

5

Phytoremediaton plot in Campo Pisano mine dump

PLOT

39°17′47.9″N, 8°31′53.9″E

3

Out of Campo Pisano mine dump

OCP

39°17′32.3″N, 8°32′34.9″E

5

Su Spantu

SS

39°06′17.4″N, 8°56′09.3″E

3

Fig. 1

Sketch of the sampling points. Upper part: localisation of Campo pisano area (red spot) and su Spantu area (yellow spot) and related sampling points (a, b, c, d); Lower part: detail on the Campo Pisano area sampling points. a CP (Campo Pisano); b PLOT (Area of a field phytoremediation experiment); c OCP (Out of Campo Pisano); d SS (Su Spantu)

The number of specimens collected at each site was chosen according to the plant’s availability at the different selected locations. In similar works the number of collected samples varied between 3 and 5 (Li et al. 2011; Jimènez et al. 2014; Concas et al. 2015; Erdemir et al. 2017) and these numbers were considered statistically adequate for inter- and intra-population variations (Concas et al. 2015).

Plants and soils were jointly sampled and immediately processed after harvesting. Plants of similar dimensions were collected, in order to have homogenous samples. The roots were shaken to remove the bulk soil (S), i.e. all the particles that were not tightly adherent, while the rizosphere soil (RZ), i.e. the particles more closely associated, was collected by putting the roots into a bag and shaking them vigorously. S and RZ samples were air dried for a week.

Zn, Pb and Cd content in S (D < 2 mm) and RZ were determined by a microwave assisted acid digestion (Start D, Milestone), adding to 0.50 g of matrix (dried at 40°C), 9 mL HNO3 65% and 4 mL HF (EPA method 3052). A reference material (GSS-4, limy-yellow soil) and blank solutions were used during analysis in order to guarantee trustworthy results. The bioavailable metal concentrations (BF) were determined by a single extraction suitable for not-acidic soils as proposed by Italian official analytical methods for soils (D.M. 13/09/1999). This method is based on the study of Linsday and Norvell (1978) and Barbafieri et al. (1996) and it has been used in other similar phytoremediation studies (Gupta and Sinha 2007; Zhu et al. 2012; Li and Zhjang 2013). In this method, a solution of 0.5 M DTPA (Diethylene Triamine Penta acetic Acid), 0.01 M CaCl2 (Calcium Chloride) and 0.1 M TEA (Tri Ethanol Ammine) buffered at the pH 7.3, is put in contact with soil (solid liquid ratio 1:2) for 2 hours. After the supernatant was filtered and finally analysed. DTPA extraction procedure was described by Lindsay and Norvell (1978) as the most thermodynamically efficient and is able to prevent the carbonates dissolution and the consequent release of bounded metals (Feng et al. 2005). The total and bioavailable metal concentrations in filtered extracts were analysed through Inductively Coupled Plasma Spectrometry (ICP-OES, Perkin Elmer Optima DV 7000). The operative wavelengths (nm) and detection limits (mg/L) were: Zn 213.857 (0.005), Pb 220.353 (0.02) and Cd 228.802 (0.02). The pH of soils was determined using the potentiometric method proposed by GURI (1999) using a solution of CaCl2 as eluent. This method gives realistic values of the reaction potential of field sample (Conyers and Davey 1988); total carbon (TC) and nitrogen (TN) were obtained by CHN analyzer (LECO, CHN 1000). A reference material (Ore Tailings) was used to calibrate CHN analyzer.

Plants were divided in roots (R) and epigean organs (EO), washed in deionized water, dried at 40°C for a week and finely ground through electric mill. Zn, Pb and Cd contents in plant samples were determined by a microwave assisted acid digestion using 0.50 g of the matrix and a 9 mL HNO3 and 0.5 mL HF solution (EPA method 3052) as described above for soil matrices. The metal concentrations in filtered extract were determined by ICP-OES. The operative wavelengths and detection limits were the same of S, RZ and BF. Two reference materials were used in order to guarantee trustworthy result’s method (GSV-2 bush twigs and leaves and INCT-PVLT-6 Polish Virginia Tobacco leaves) and blank solutions were prepared and analysed.

Two biological indexes, namely the Biological Concentration Factor (BCF) and the Translocation Factor (TF) were calculated in order to evaluate the capability of H. tyrrhenicum to uptake Zn, Pb and Cd in roots and eventually translocate them to the epigean organs. The BCF gives information about the uptake from soil to roots and it is defined as the ratio between the metal content in roots and soil (Fellet et al. 2007). In this work, this parameter was calculated with reference to both the total content (BCF) and the bioavailable fraction (BCF bf) in soils. The TF indicates the rate of heavy metals translocated from roots into epigean organ (Brooks 1998).

S, RZ and roots samples were finely ground in an agate mortar and investigated by XRD analyzer in order to obtain mineralogical composition. XRD analysis were performed by a θ-2θ conventional diffractometer (PANalytical X’PERT MPD) with Cu Kα radiation (1.5418 Å). Samples were lightly ground in agate mortar and packed into the sample holder for X-ray diffraction analysis. Peaks for the mineral were attributed according to the Powder Diffraction Cards by using X’Pert Highscore plus software. Roots surface and chemical composition were investigated using a SEM coupled with an EDAX analyzer.

Generalized Linear Models (GLMs) were used to evaluate the differences in concentration of Zn, Pb and Cd in bulk soil (Tot S), rizosphere (Tot RZ) and in bioavailable fraction (BF S) of bulk soil (mg/kg), as well as in the plant tissues (e.g., R and EO). GLMs were used also for the biological indexes (BCF, BCF bf and TF) calculated for the three metals. Significant differences highlighted by GLM (with a log link function and quasi poisson error structure) were then analysed by a post hoc pairwise comparisons t-test (with Bonferroni adjustment). Quasi poisson error structure and F test with an empirical scale parameter instead of chi-squared on the subsequent ANOVA were used in order to overcome residual overdispersion (Crawley 2007). Statistical analyses were carried out using R version v. 3.0.3 (R Development Core Team 2014).

Results and Discussion

The main chemical characteristics of bulk soils were reported in Table 2. The pH of both Campo Pisano’s waste surface samples (CP, PLOT) and those outside the mine area (OCP) was classified as neutral or slightly alkaline on the basis of the USDA classification (1998), while SS ones showed an acidic pH which is ascribable to granitic lithology. The content of TC was similar for all the sites influenced by mine activity, and low content of TN was measured in all sites inside and outside the mine district. The pH values and TC of the mine district are consistent with the dominant carbonate lithology as reported by Bacchetta et al. (2015), where carbon was present mainly in an inorganic form such as calcite (48.0 ± 4.4 g/kg) and dolomite (430.0 ± 10.1 g/kg). These data are also consistent with XRD analysis conducted in this study on bulk soils and rizosphere (see in the Results chapter, Mineralogical analysis paragraph). Moreover, the poor agronomic properties are typical for soils of mining areas and this has been recognized as one of the critical issues in applying phytoremediation actions (Nicoara et al. 2014; Sprocati et al. 2014).

Table 2

pH, TC (g/kg) and TN (g/kg) in the bulk soils of sampling sites (mean values ± SD)

 

pH

TC

TN

CP

7.2 ± 0.2

45 ± 22

0.3 ± 0.2

PLOT

7.2 ± 0.1

69 ± 8

0.7 ± 0.2

OCP

7.3 ± 0.3

74 ± 6

0.2 ± 0.1

SS

6.3 ± 0.3

11 ± 5

0.2 ± 0

Table 3 reports the total metal concentrations in S and RZ and the BF in bulk soils. Metal concentrations in S and RZ appeared very similar: Zn was always the most concentrated element, followed by Pb and Cd. As reported in other similar studies (Bacchetta et al. 2012, 2015; Concas et al. 2015), samples at the mine dump (CP and PLOT) contained very high quantities of metals, well above the threshold contamination levels established by the Italian law (Dlgs 152/2006) for an industrial use of soil (1500, 1000, 15 mg/kg for Zn, Pb and Cd, respectively). The high variation in total concentrations measured in CP and PLOT samples can be explained by the heterogeneity of mine waste deposited in the Campo Pisano dump. Metal concentration values assessed in PLOT soils are consistent with the study of Bacchetta et al. (2012). It is noteworthy that also the OCP soils samples were highly contaminated, confirming a very high contaminant dispersion in the areas surrounding the mine site due to the wind dispersion of fine soil particles. The differences between metals content measured at OCP, nearby the mine area, and those inside the mine area (CP / PLOT) were in fact, in most cases, not statistically significant (p < 0.05). In the case of Zn measured in rhizosphere soils, concentration in OCP was found to be even higher that that measured in PLOT.

Table 3

Zn, Cd and Pb total content (Tot S) and bioavailable fraction in bulk soil (BF S) and rizosphere (Tot RZ) (mg/kg); mean ± SD (n = 5 for CP and OCP; n = 3 for PLOT and SS); n.d.: not detected; Different letters indicate significant differences between sampling sites at p < 0.05

 

CP

PLOT

OCP

SS

Zn

 Tot S

24,823 ± 6713a

14,251 ± 4064ab

25,043 ± 13702a

40 ± 14b

 BF S

124 ± 9a

93 ± 26a

135 ± 34a

0.8 ± 0.7b

 Tot RZ

25,218 ± 5366a

8296 ± 2819b

23,209 ± 9180a

46 ± 14b

Pb

 Tot S

5082 ± 183.55a

1659 ± 202.59b

1380 ± 562b

29 ± 2b

 BF S

21 ± 7a

5 ± 1b

13 ± 5ab

0.31 ± 0.27b

 Tot RZ

4540 ± 1189a

1316 ± 583b

1499 ± 513b

21 ± 0b

Cd

 Tot S

95 ± 19a

51 ± 5a

253 ± 219a

n.d

 BF S

2.1 ± 0.3a

1.6 ± 0.6a

8 ± 6a

n.d

 Tot RZ

158 ± 29ab

68 ± 20ab

222 ± 112a

4.14 ± 0.20b

As expected, SS did not exceed the above mentioned threshold levels, and this indicates the absence of either an anthropogenic impact or an anomalous geochemical background. The BF S values were a minimal percentage of the total content (Zn and Pb values < 1% and Cd around 3%) and this indicates that only a small quantity of metals is linked to the soluble fraction and to mineral and organic phases and thus available for plant species. The differences between metals content measured at the sampling sites inside and nearby the mine area and those measured in the site not influenced by the mining activity were statistically significant (p < 0.05). In some cases, significant differences were found also among the sampling site of the mine district CP and PLOT.

The plant samples of H. tyrrhenicum collected at the different sites exhibited different metal concentrations and metal distributions in the plant tissues. As shown in Table 4, Zn was the most abundant heavy metal in roots and epigean tissues, followed by Pb and Cd, consistently with the abundance order observed in bulk soils and rizosphere. The highest concentrations of metals in R were recognized in CP samples followed by PLOT and OCP ones, and as expected much lower values were found in SS, coherently with the lower metal content measured in the bulk and rizosphere soils at SS site. The amount of these metals in EO decreased in the order CP > PLOT > OCP >> SS and generally the concentrations measured in roots were comparable with that assessed in epigean organs for every metal tested. Studies carried out for other pioneer plants investigated in this area, for instance P. lentiscus, C. salviifolius, S. canina subsp. bicolor (Cao et al. 2009; Bacchetta et al. 2015; Concas et al. 2015) report concentrations of Zn, Cd and Pb in roots and aerial organs lower in comparison to the results found in this study (around 500 and 200 mg/kg of Pb and around 3500 and 1000 mg/kg of Zn in C. salviifolius and S. canina subsp. bicolor, respectively).

Table 4

Concentration (mg/kg) of Zn, Pb, Cd in plant tissue (mean ± SD; n = 5 CP; n = 3 PLOT; n = 5 OCP; n = 3 SS); R and EO correspond to roots and epigean organ respectively; n.d.: not detected; different letters indicate significant difference between sampling sites at p < 0.05

 

CP

PLOT

OCP

SS

Zn R

2634 ± 1091a

2200 ± 1785ab

1700 ± 839ab

33 ± 12b

Zn EO

3466 ± 620a

1679 ± 1229b

718 ± 413c

44 ± 2c

Pb R

541 ± 224a

243 ± 203ab

140 ± 113ab

2.37 ± 0.60b

Pb EO

1035 ± 28a

353 ± 313b

46 ± 34b

2.08 ± 0.32b

Cd R

20 ± 8a

13 ± 5a

33 ± 21a

n.d

Cd EO

19 ± 6a

11 ± 8a

9.73 ± 8.22a

n.d

Statistical analysis on Zn and Pb content measured in R and EO (Table 4) highlighted statistically significant differences among sampling sites (p < 0.05), while no statistical differences were observed for Cd (p > 0.05). In details, Zn and Pb content in R measured at CP site were significantly higher than those measured in SS (p < 0.05), while metal uptake in roots assessed at PLOT and OCP did not show significant differences (p > 0.05) with respect to CP and SS. As far as Zn content in EO was considered, significant differences were found among the different sampling sites (p < 0.05) with the exception of OCP and SS, which showed similar values to each other. Pb content in EO measured in CP site was significantly higher than the other sites (p < 0.05).

Table 5 shows the values of BCF, BCF bf and TF. Bioaccumulation and translocation data assessed at each sampling site reflect the variability already found for the concentration of metals in soil and plant tissues. Despite this considerable variability, one can generally find the same accumulation pattern irrespectively of both sampling site and metal. The BCF values were always lower than 1, but as far as BCF bf values are considered, a significant attitude to accumulate metals in roots tissue can be revealed. As far as metals distribution among plant tissues is concerned, H. tyrrhenicum showed the capability to transfer the metals from roots to leaves. The BCF bf and TF values measured for the different sites and the different metals indicate the attitude to behave as a species suitable for phytostabilization (Baker et al. 1994). Moreover, the root’s concentrations of every metal tested were above the reported phytotoxic levels (Kabata-Pendias and Pendias 1992), indicating the high metal tolerance of the species. In the study of Cao et al. (2004), H. tyrrhenicum showed a high tolerance to high concentration of both Zn and Pb, behaving as accumulator for Zn and as excluder for Pb. Taking into account the values measured on other pioneering species, H. tyrrhenicum has BCF and TF higher than P. lentiscus (Bacchetta et al. 2015; Concas et al. 2015), and lower than C. salviifolius (TF values 2.2 and 2 for Zn and Pb respectively), whilst S. canina subsp. bicolor presented a lower TF for Pb and a TF similar to our results for Zn (Lai et al. 2015). The statistical analysis showed no significant differences among the different sampling sites (p < 0.05) in BCF, BCF bf and TF (Table 5) with the exception of the BCF for Zn measured far away to the mine district (SS), that was significantly higher if compared to sampling sites inside the mine district (CP, PLOT and OCP).

Table 5

BCF, BCF bf and TF mean values; / = undeterminable value; different letters indicate significant differences between sampling sites at p < 0.05

 

CP

PLOT

OCP

SS

Zn

 BCF

0.1 ± 0.1a

0.2 ± 0.2a

0.1 ± 0.1a

0.9 ± 0.3b

 BCF bf

21 ± 9a

28 ± 29a

15 ± 6a

53 ± 29a

 TF

1.7 ± 1.4a

0.8 ± 0.1a

0.5 ± 0.4a

1.5 ± 0.7a

Pb

 BCF

0.11 ± 0.05a

0.2 ± 0.1a

0.07 ± 0.13a

0.10 ± 0.01a

 BCF bf

29 ± 19a

42 ± 30a

18 ± 14a

13 ± 8a

 TF

2.45 ± 2.05a

1.7 ± 0.6a

0.5 ± 0.3a

0.9 ± 0.1a

Cd

 BCF

0.2 ± 0.1a

0.3 ± 0.1a

0.2 ± 0.1a

/

 BCF bf

9.6 ± 4 a

11 ± 10a

6.6 ± 4.2a

/

 TF

1.1 ± 0.7a

0.8 ± 0.3a

0.4 ± 0.3a

/

The assessed biological indexes and the ability of this native species to withstand high concentrations of Zn, Pb and Cd in the soils of mining site indicate that H. tyrrhenicum can be potentially suitable for phytostabilization projects.

Table 6 shows the mineralogical composition of S, RZ and root’s powder obtained through XRD. CP soil samples were mainly made of quartz, dolomite, pyrite and blende according to previous mineralogical studies of this area (De Giudici et al. 2015). PLOT samples were similar to CP, but they contained also clay minerals such as alloysite. Rizosphere of CP, PLOT and OCP had a similar composition to bulk soil with the addition of ankerite, jarosite, goethite. Root’s powders showed the presence of amorphous cellulose and quartz in all samples collected, also observed by Medas (2015). SEM investigation on CP root samples showed biomineral layers and isolated grains coating the surface of the roots. These layers were rich in Fe oxide, whereas the grains are constituted of barite, Fe and Ti oxides and Al silicate. On the uncoated root’s surface traces of Si, Cl, Zn and Pb were observed. Furthermore, trace of Si and Cl were recognized on all the samples, also out of the mine area. On the surface of PLOT and OUT roots, there were grains and coats, with Zn, Fe and Ti traces.

Table 6

Mineralogical composition of bulk soil, rizosphere and root powder in the different sampling sites

 

Bulk Soil

Rizosphere

Root’s powder

CP

Quartz, dolomite, pyrite, jarosite, gypsum, blende

Quartz, dolomite, ankerite, jarosite, gypsum, pyrite, goethite

Amorphous cellulose; quartz

PLOT

Quartz, dolomite, pyrite, gypsum, goethite, alloysite

Quartz, dolomite, ankerite, gypsum, pyrite, goethite, cerussite, alloysite

Amorphous cellulose, quartz

OCP

Quartz, dolomite, pyrite, goethite, phyllosilicate

Quartz, dolomite, muscovite, smithsonite, kaolinite, anglesite

Amorphous cellulose, quartz

SS

Quartz, muscovite, albite, microcline

Quartz, muscovite, albite, microcline, illite, rutilo

Amorphous cellulose, quartz

Mineral coating of Zn and Si were observed also in other studies carried on E. cupanii and J. acutus (Medas et al. 2015, 2017), P. lentiscus and P. australis (De Giudici et al. 2015, 2017) grown on Campo Pisano’s area. They were interpreted as a result of a survival strategy. Particularly, their physiological purpose is limiting the bioavailability of Zn and other ions (Caldelas and Weiss, 2017). Similarly to other biomineralization occurring in the area, amorphous Zn biomineralization could be present in H. tyrrhenicum roots, but they cannot be detected by XRD (Medas et al. 2014; Podda et al. 2014).

The aim of this study was evaluating the suitability of H. tyrrhenicum for remediation of contaminated sites. Samples of the plant grown on mine waste rich in Zn, Pb and Cd were studied. Different plant compartments and soil samples were analysed for their content in heavy metals. It was found that high content of pollutants in H. tyrrhenicum roots with respect to the bioavailable metals in the soils. Moreover, the calculated translocation factor indicated fair translocation to aerial organs, thus, H. tyrrhenicum can be considered as a tolerant plant. H. tyrrhenicum has also been found able to influence the minerals in the rizosphere and this could be part of its pioneering strategy. These reasons, along with the capability to spontaneously colonize mining sites, allowed us to consider this plant species for revegetating the mine areas and developing phytostabilization technology. Phytoremediation laboratory experiment and seed germination tests on H. tyrrhenicum under heavy metals stress are taking place with the aim of defining the best condition for future phytostabilization actions to be applied in this area and similar ones in other Mediterranean mine contexts.

Notes

Acknowledgements

This work is part of the research project RE-MINE -REstoration and remediation of abandoned MINE sites, funded by the Fondazione di Sardegna and Regional Sardinian Government (Grant CUP F72F16003160002). We gratefully acknowledge the University of Cagliari for the financial support of the Ph.D scholarship of Maria Enrica Boi (years 2015–2018).

References

  1. Angiolini C, Bacchetta G, Brullo S, Casti M, Giusso del Galdo G, Guarino R (2005) The vegetation of mining dumps in SW-Sardinia. Feddes Repert 116:243–276CrossRefGoogle Scholar
  2. Bacchetta G, Brullo S, Mossa L (2003) Note tassonomiche sul genere Helichrysum Miller (Asteraceae) in Sardegna. Inf Bot Ital 35:217–225Google Scholar
  3. Bacchetta G, Casti M, Mossa L, Piras ML (2007) La flora del distretto minerario di Montevecchio (Sardegna sud-occidentale). Webbia 62:27–52CrossRefGoogle Scholar
  4. Bacchetta G, Bagella S, Biondi E, Farris E, Filigheddu R, Mossa L (2009) Vegetazione forestale e serie di vegetazione della Sardegna (con rappresentazione cartografica alla scala 1:350.000). Fitosociologia 46:3–82Google Scholar
  5. Bacchetta G, Cao A, Cappai G, Carucci A, Casti M, Fercia ML, Lonis R, Mola F (2012) A field experiment on the use of Pistacia lentiscus L. and Scrophularia canina L. subsp. bicolor (Sibth. et Sm.) Greuter for the phytoremediation of abandoned mining areas. Plant Biosyst 146:1054–1063CrossRefGoogle Scholar
  6. Bacchetta G, Cappai G, Carucci A, Tamburini E (2015) Use of native plants for the remediation of abandoned mine sites in Mediterranean semiarid environments. Bull Environ Contam Toxicol 94:326–333CrossRefGoogle Scholar
  7. Baker AJM, Reeves RD, Haiar ASM (1994) Heavy metal accumulation and tolerance in British populations of the metallophyte Thlaspi caerulescens J. & C. Presl. (Brassicaceae). New Phytol 127:61–68CrossRefGoogle Scholar
  8. Barbafieri M, Lubrano L, Petruzzelli G (1996) Characterization of pollution in sites contaminated by heavy metals: a proposal. Ann Chim 86:585–594Google Scholar
  9. Bechstädt T, Boni M (1994) Sedimentological, stratigraphical and ore deposits field guide of the autochthonous Cambro–Ordovician of Southwestern Sardinia, Italy. Servizio Geologico d’Italia. 434 ppGoogle Scholar
  10. Brooks GG (1998) Plants that hyperaccumulate heavy metals. CAB International, WallingfordGoogle Scholar
  11. Caldelas C, Weiss DJ, Cao A, Cappai G, Carucci A, Muntoni A (2017) Zinc homeostasis and isotopic fractionation in plants: a review. Plant Soil 411:17–46CrossRefGoogle Scholar
  12. Cao A, Cappai G, Carucci A, Muntoni A (2004) Selection of plants for zinc and lead phytoremediation. J Environ Sci Health 39:1011–1024.CrossRefGoogle Scholar
  13. Cao A, Carucci A, Lai T, Bacchetta G, Casti M (2009) Use of native species and biodegradable chelating agent in phytoremediation of abandoned mining area. J Chem Technol Biotechno 84:884–889CrossRefGoogle Scholar
  14. Concas S, Lattanzi P, Bacchetta G, Barbafieri M, Vacca A (2015) Zn, Pb and Hg contents of Pistacia lentiscus L. grown on heavy metal-rich soils: implications for phytostabilization. Water Air Soil Pollut 226:340–355CrossRefGoogle Scholar
  15. Conyers MK, Davey BG (1988) Observation of same routine methods for soil pH determination. Soil Sci 145:29–36CrossRefGoogle Scholar
  16. Crawley MJ (2007) The R Book. Wiley, ChichesterCrossRefGoogle Scholar
  17. De Giudici G, Medas D, Meneghini C, Casu MA, Giannoncelli A, Iadecola A, Podda S, Lattanzi P (2015) Microscopic bio mineralization processes and Zn bioavailability: a synchrotron-based investigation of Pistacia lentiscus L. root. Environ Sci Pollut Res 22:19352–19361CrossRefGoogle Scholar
  18. De Giudici G, Pusceddu C, Medas D, Meneghini C, Giannoncelli A, Rimondi V, Podda F, Cidu R, Lattanzi P, Wanty RB, Kimball BA (2017) The role of natural biogeochemical barriers in limiting metal loading to a stream affected by mine drainage. Appl Geochem 76:124–135CrossRefGoogle Scholar
  19. Erdemir Ü, Arslan H, Güleryüz G, Gücer (2017) Elemental composition of plant species from an abandoned tungsten mining area: Are they useful for biogeochemical exploration and/or phytoremediation purposes? Bull Environ Contam Toxicol 98:299–303CrossRefGoogle Scholar
  20. Fellet G, Marchiol L, Perosa D, Zerbia G (2007) The application of phytoremediation technology in a soil contaminated by pyrite cinders. Ecol Eng 31:207–214CrossRefGoogle Scholar
  21. Feng MH, Shan XQ, Zhang S, Wen B (2005) Comparison of rhizosphere-based method with other one-step extraction methods for assessing the bioavailability of soil metals to wheat. Chemosphere 59:939–949CrossRefGoogle Scholar
  22. Gupta AK, Sinha S (2007) Assessment of single extraction methods for the prediction of bioavailability of metals to Brassica juncea L. Czern (var Vaibhav) grown on tannery wate contaminated soil. J Hazard Mater 149:144–150CrossRefGoogle Scholar
  23. GURI (1999) Metodi ufficiali di analisi chimica del suolo. Supplemento ordinario alla Gazzetta Ufficiale n p. 248Google Scholar
  24. Jimènez MN, Fernandez E, Navarro EB, Contini E, Casti M, Bacchetta G (2005) Livelli di metalli pesanti in Dittrichia viscosa (L.) Greuter, Cistus salviifolius L. e Euphorbia cupanii Bertol. ex Moris su suoli contaminati e non contaminati dalle attività estrattive nell’Iglesiente (Sardegna sudoccidentale). Inf Bot Ital 37:794–795Google Scholar
  25. Jimènez MN, Bacchetta G, Casti M, Navarro FB, Lallena AM, Fernandèz-Ondono E (2011) Potential use in phytoremediation of three plant species growing on contaminated mine-tailing soils in Sardinia. Ecol Eng 37:392–398CrossRefGoogle Scholar
  26. Jimènez MN, Bacchetta G, Casti M, Navarro FB, Lallena AM, Fernandèz-Ondono E (2014) Study of Zn, Cu and Pb content in plants and contaminated soils in Sardinia. Plant Biosyst 148:419–428CrossRefGoogle Scholar
  27. Kabata-Pendias A, Pendias H (1992) Trace elements in soils and plants, 2nd edt. CRC Press, Boca RatonGoogle Scholar
  28. Lai T, Cappai G, Carucci A, Bacchetta G (2015) Phytoremediation of abandoned mining areas using native plant species: a Sardinian case study. Environ Sci Eng 11:256–277Google Scholar
  29. Li Y, Zhjang MK (2013) A comparison of physiologically based extraction test (PBET) and single-extraction methods for release of Cu, Zn, and Pb from mildy acidic and alkali soils. Environ Sci Pollut Res 20:3140–3148CrossRefGoogle Scholar
  30. Li G, Hu N, Ding D, Zheng J, Liu Y, Wang Y, Nie X (2011) Screening of plant species for phytoremediation of uranium,. thorium, barium, nickel, strontium and lead contaminated soils from a uranium mill tailings repository in south china. Bull Environ Contam Toxicol 86:646–652CrossRefGoogle Scholar
  31. Linsday WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428CrossRefGoogle Scholar
  32. Medas D, Lattanzi P, Casu MA, Musu E, De Giudici G (2014) The amorphous Zn biomineralization at Naracauli stream, Sardinia: Electron microscopy and X-ray absorption spectroscopy. Environ Sci Pollut Res 21:6775–6782CrossRefGoogle Scholar
  33. Medas D, De Giudici G, Casu MA, Musu E, Giannoncelli A, Iadecola A, Meneghini C, Tamburini E, Sprocati AR, Turnau K, Lattanzi P (2015) Microscopic processes ruling the bioavailability of Zn to roots of Euphorbia pithyusa L. pioneer plant. Environ Sci Technol 49:1400–1408CrossRefGoogle Scholar
  34. Medas D, De Giudici G, Pusceddu C, Casu MA, Birarda G, Vaccari L, Giannoncelli A, Meneghini C (2017) Impact of Zn excess on biomineralization processes in Juncus acutus grown in mine polluted sites. J Hazard Mater.  https://doi.org/10.1016/j.jhazmat.2017.08.031 CrossRefGoogle Scholar
  35. Mulligan CN, Yong RN, Gibbs BF (2001) Remediation technologies for metal-contaminated soils and groundwater, an evaluation. Eng Geol 60:193–207CrossRefGoogle Scholar
  36. Nicoară A, Neagoe A, Stancu P, De Giudici G, Langella F, Sprocati AR (2014) Coupled pot and lysimeter experiments assessing plant performance in microbially assisted phytoremediation. Environ Sci Pollut Res 21:6905–6920CrossRefGoogle Scholar
  37. Podda F, Medas D, De Giudici G, Ryszka P, Wolowski K, Turnau K (2014) Zn biomineralization processes and microbial biofilm in a metal-rich stream (Naracauli, Sardinia). Environ Sci Pollut Res 21:6793–6808CrossRefGoogle Scholar
  38. R Development Core Team (2014) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org
  39. Raskin I, Ensley B (2000) Phytoremediation of toxic metals using plants to clean the environment. Wiley, New YorkGoogle Scholar
  40. Sprocati AR, Alisi C, Pinto V, Montereali MR, Marconi P, Tasso F, Turnau K, De Giudici G, Goralska K, Bevilacqua M, Marini F, Cremisini C (2014) Assessment of the applicability of a “toolbox” designed for microbially assisted phytoremediation: the case study at Ingurtosu mining site (Italy). Environ Sci Pollut Res 21:6939–6951CrossRefGoogle Scholar
  41. Tamburini E, Sergi S, Serreli L, Bacchetta G, Milia S, Cappai G, Carucci A (2016) Bioaugmentation-assisted phytostabilisation of abandoned mine sites in south west Sardinia. Bull Environ Contam Toxicol 98:310–316CrossRefGoogle Scholar
  42. Zhu QH, Huang DY, Liu SL, Luo ZC, Zhu HH, Zhou B, Lei M, Rao ZX, Cao XL (2012) Assessment of single extraction methods for evaluatingthe immobilization effect of amendments on cadmiumin contaminated acidic paddy soil. Plant Soil Environ 58:98–103CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.DISVA - Department of Life and Environmental Sciences, Centre for the Conservation of Biodiversity (CCB)University of CagliariCagliariItaly
  2. 2.BG-SAR - Sardinian Germplasm Bank, HBK - Hortus Botanicus KaralitanusUniversity of CagliariCagliariItaly
  3. 3.DICAAR - Department of Civil and Environmental Engineering and ArchitectureUniversity of CagliariCagliariItaly
  4. 4.DSCG - Department of Chemical and Geological ScienceUniversity of CagliariCagliariItaly

Personalised recommendations