Printer Friendly

Evaluation of two Brazilian indigenous plants for phytostabilization and phytoremediation of copper-contaminated soils/Avaliacao de duas plantas nativas brasileiras para fitoestabilizacao e fitorremediacao de solos contaminados com cobre.

1. Introduction

Copper contamination is an eminent problem often found in a wide range of soils, sediments and water courses (Lacerda et al., 2009; Andrade et al., 2010). Furthermore, in some cases as vineyards, copper is a fundamental agent used to control leave diseases, which it is commonly and constantly used to produce grapes and wines (Komarek et al., 2010). Also, copper mining waste sites are enormous areas with notable problems such as low nutrient content and high copper concentrations (Laybauer, 1998). However, polluted environments with heavy metals change the plants community during the time (Dazy et al., 2009). Indigenous or wild plants are located in heavy metal contaminated areas and their contribution to environment should be evaluated, once, these plants can uptake the heavy metals and then, mitigate the negative impact of the contamination of adjacent soils and water courses.

Moffat (1995) notified that researchers discovered natural and ornamental plants grown vigorously in metal contaminated areas; and they reported that phytoremediation would be much better and cost-effective using these plants than the use of conventional cleanup strategies. Native plants have been studied by their capacity to accumulate heavy metals in the shoots and roots by uptake from contaminated sites (Yoon et al., 2006) using their characteristics such as rusticity and adaptability.

Phytoremediation is the use of plants to reduce the concentrations or toxic effects of contaminants in the environments (Ali et al., 2013). Furthermore it has been used for cleaning up the environment with high success (Babu et al., 2013; Pandey, 2013). Lonicerajaponica, an Asian native plant showed high accumulation and tolerance characteristics for cadmium (Cd), being a useful plant with potential in hyperaccumulating cadmium (Liu et al., 2009). The wild plant Bidens tripartita, other species of B. pilosa was found grown in a super-large antimony (Sb) deposit area with high concentrations of Sb in the roots (Qi et al., 2011). Also, B. tripartite has been studied to phytoremediation of Cd contaminated soils (Wei et al., 2010). Other wild plant, Arthrocnemum macrostachyum showed characteristics of Cd-hyperaccumulator (Redondo-Gomez et al., 2010); and Spartina argentinensis, an Argentine native plant showed high accumulation and tolerance characteristics for chromium (Redondo-Gomez et al., 2011). However, native plants with copper hyperaccumulation abilities are incipient and there is a gap of information that must be filled requiring more studies.

Many indigenous plants grown surrounding mining wastes showed high BCF with high heavy metal hyperaccumulation characteristics (Gonzalez and Gonzalez-Chavez, 2006), but B. pilosa and P. lanceolata plants were not found in these areas. In other study, B. pilosa was characterized as a potential Cd-hyperaccumulator plant with high potential for resistance, growth, BCF and TF for Cd (Sun et al., 2009). However, there is a paucity of studies with B. pilosa and P. lanceolata plants in copper contaminated sites, where both were found abundantly in vineyard soils and P. lanceolata was also found in copper mining waste area, both sites in Southern Brazil. Thus, it was evaluated the growth ability, macro and micronutrients uptake and different phytoremediation capability of B. pilosa and P. lanceolata plants in vineyard soils contaminated with copper and copper mining waste as a bioremediation tool to improve the soil quality.

2. Material and Methods

2.1. Soil and experiment characterization

A greenhouse experiment was carried out with topsoil samples (0-20 cm) taken from two 40 year old vineyard soils (Inceptisol and Mollisol) at Brazilian Agriculture Research Corporation research (EMBRAPA) farm located in Bento Goncalves, RS, Southern Brazil. A native soil was sampled from a native forestry area located nearby the vineyards. The copper mining waste was sampled from a copper mine in Cacapava do Sul, RS, Southern Brazil. Copper mining waste, native soil, and the two types of copper contaminated soils were characterized to physical-chemical analysis (Table 1). All soil samples were air dried, ground and sieved (3 mm). It was not added any nutrient to treatments because of these indigenous plants are considering weeds to agricultural crops and consequently no nutrient recommendations is required.

Five replicates of 1 kg subsamples were placed in pots of 700 [dm.sup.3]. Deionized water was then added to bring the soil moisture up to 80% field capacity water content and was maintained during the 64 and 85 days of plant growth for B. pilosa and P. lanceolata respectively. Four soil treatments were tested: Native soil (Control); Inceptisol; Mollisol; and copper mining waste (40% of Native soil and 60% of copper mining waste).

2.2. Plant growth for copper phytoremediation, harvest and analysis

Ten seeds of each species were seeded per pot. After 10 days of incubation, it was kept until the end of the study in each pot 4 and 3 plants of B. pilosa and P. lanceolata respectively. The pots were watered during the growth period to maintain soil water content near to 80% of field capacity. After the growth period, shoots were harvested and immediately measured for height and green mass. The height of B. pilosa plants was determined with respect to the main stem from the base to the tip of each plant and calculated the average. Shoots of both species were then oven-dried for 72 h at 60[degrees]C and the shoot dry weight was recorded. Green and dry roots biomass were also measured to compose the soil-root system. After green mass measured, each plant root was separated by washing with deionized water, oven-dried for 72 h at 60[degrees]C, and weighed for further analysis.

Nutrient concentration in the roots and shoots dry matters were determined. Nitrogen was determined after digestion with concentrated sulfuric-peroxide by steam distillation, and quantification by titration. The macronutrients (P, K, Ca, Mg and S), copper and micronutrients (Zn, Mn, Na and Fe) were determined following digestion in concentrated nitric-perchloric acid by Inductively Coupled Plasma--Optical Emission Spectrometry.

2.3. Characterization of potential phytoremediation

The tolerance index (TI) was expressed on the basis of plant growth parameters including height, green and dry biomass of the roots and shoots (Wilkins, 1978). The translocation factor (TF) of the Cu, Zn, Na, Mn and Fe from the roots to shoots, and the bioconcentration factor (BCF) were calculated (Yoon et al., 2006; Shi and Cai, 2009). Also, the metal extraction ratio (MER) is defined as the ratio of metal accumulation in the shoots to that in soil (Mertens et al., 2005). The plant effective number of the shoots (PENs) and the plant effective number of the total plant (PENt) have been applied to evaluate the ability of remedying contaminated soil by a hyperaccumulator according with Sun et al. (2008).

2.4. Statistical analysis

The statistical design used was randomized complete block with five replicates. Statistical analysis was performed using ANOVA. When the significance difference was observed between treatments (P [less than or equal to] 0.05), multiple comparisons were carried out using Tukey test.

3. Results and Discussion

3.1. Plant growth

Both B. pilosa and P lanceolata grown vigorously in the both vineyard soils contaminated with copper; however, they poorly grown in the copper mining waste (Figures 1 and 2). B. pilosa plants showed high height after 64 days of growth in the both vineyard soils with height of 17 cm (Mollisol) and 10.4 cm (Inceptisol) (Figure 1). On the other hand, B. pilosa plants showed low growth in the copper mining waste with height of 4 cm (Figure 1).

B. pilosa plants cultivated in the Mollisol and Inceptisol showed the highest green mass production of the shoots (8.4 and 8.1 g [pot.sup.-1], respectively) and roots (14.6 and 9.3 g [pot.sup.-1], respectively) (Figure 2A), and dry mass of the shoots (1.6 and 1.3 g [pot.sup.-1], respectively) and roots (1.2 and 0.77 g [pot.sup.-1], respectively) (Figure 2B). Copper mining waste drastically affected both indigenous plants with green and dry mass production around 0.1 g [pot.sup.-1]. P. lanceolata showed significantly high green and dry biomass production in the Mollisol followed by the Inceptisol treatment (Figure 2C, D). However, P lanceolata showed high green mass production in both Mollisol and Inceptisol in the shoots (9.4 and 3.1 g [pot.sup.-1], respectively) and roots (9.3 and 1.3 g [pot.sup.-1], respectively) (Figure 2C), and also to dry mass of the shoots (1.3 and 0.27 g [pot.sup.-1], respectively) and roots (0.31 and 0.05 g [pot.sup.-1], respectively) (Figure 2D).

Heavy metals in toxic concentrations can interfere in the plant growth (Ke et al., 2007). Some indigenous plants (Populus deltoids and P. nigra) were negatively affected after exposure to toxic concentrations of cadmium (Wu et al., 2010). In other study, the B. pilosa dry weight was drastically reduced when Cd concentration was increased (Sun et al., 2009). Some authors proved that indigenous plants (P. lanceolata and P. media) with high nutrient demands showed high fitness as seeders respectable of nutrient availability after growth in negatively impacted areas (Latzel and Klimesova, 2009). However, the results in this study demonstrated a high potential of growth of both indigenous species (B. pilosa and P. lanceolata) in the both vineyard soils contaminated with copper, and low potential to growth in the copper mining waste.

Both B. pilosa and P lanceolata showed high tolerance index (TI) values in the vineyard soils contaminated with copper; and copper mining waste showed high visual toxicity effects and promoted a very low tolerance by the both indigenous plants (Table 2). B. pilosa showed TI values between 2 to 4-folds higher than the control among the variables analyzed in the Mollisol and Inceptisol soils, showing that both vineyards in study can promote B. pilosa growth. Surprisingly, P. lanceolata plants showed the highest adaptability in both vineyard soils, especially in the Mollisol soil with TI values ranged from 839 to 23285% among the growth evaluations. It shows a high potential of both indigenous plants to growth in both vineyard soils contaminated with high copper concentrations.

In an ecological study, B. pilosa was classified as a copper tolerant plant with substantial growth in a high copper contaminated site (He et al., 2010). Other study with eight high potential bioenergy crops presented tolerance indexes in a range of TI of 13 and 111% (Shi and Cai, 2009). Compiling with the results obtained in this study, B. pilosa and P. lanceolata showed high tolerance to copper contaminated soils. It explains the potential to growth in the vineyard soils.

3.2. Macro and micronutrient uptake

Macro and micronutrient uptake and concentration in the shoots were affected in the both B. pilosa and P lanceolata after growth for 64 and 85 days respectively in the copper contaminated soils (Table 3). B. pilosa plants cultivated in the Inceptisol did not show any significant depletion on all macro and micronutrient uptake in the shoots. On the other hand, B. pilosa cultivated in the other vineyard soil (Mollisol) showed significant low concentrations in the shoots for N (0.85 g [kg.sup.-1]), K (1.6 g [kg.sup.-1]), Ca (1.38 g [kg.sup.-1]), Mg (0.57 g [kg.sup.-1]), Zn (136 mg [kg.sup.-1]) and Mn (85 mg [kg.sup.-1]). B. pilosa cultivated in the copper mining waste treatment showed high depletion on K (1.45 g [kg.sup.-1]), Ca (1.3 g [kg.sup.-1]), Mg (0.47 g [kg.sup.-1]), Zn (119 mg [kg.sup.-1]), Fe (174 mg [kg.sup.-1]) and Mn (61 mg [kg.sup.-1]) uptake and concentration in the shoots.

P lanceolata cultivated in the vineyard soils contaminated with copper showed no depletion in all macronutrients concentration in the shoots, on the contrary, some macronutrients showed the highest concentrations (Table 3). Due the low biomass production by P lanceolata, it was not able to determine N and Na in all treatments; also, the amounts of macro and micronutrients in P lanceolata grown in copper mining waste. Only micronutrients were affected after P. lanceolata cultivated in the Inceptisol and Mollisol for Fe (956 and 620 mg [kg.sup.-1], respectively) and Mn (197 and 106 mg [kg.sup.-1], respectively); and Zn (98 mg [kg.sup.-1]) in the Mollisol treatment.

Macro and micronutrients accumulation in the roots were affected after both B. pilosa and P lanceolata plants cultivated in the copper contaminated soils (Table 4). B. pilosa plants showed high nutrient accumulation when plants were cultivated in the Inceptisol such as P (0.15 g [kg.sup.-1]), K (1.99 g [kg.sup.-1]), Ca (0.51 g [kg.sup.-1]), S (0.32 g [kg.sup.-1]), Zn (381 mg [kg.sup.-1]) and Na (2696 mg [kg.sup.-1]). B. pilosa cultivated in the Mollisol showed low concentration of the most nutrients in the roots such as N (0.81 g [kg.sup.-1]), K (1.54 g [kg.sup.-1]), Ca (0.44 g [kg.sup.-1]), S (0.2 g [kg.sup.-1]), Zn (80 mg [kg.sup.-1]) and Mn (44 mg [kg.sup.-1]). B. pilosa did not show significant difference in P and Fe concentration in the roots after grown in copper contaminated soils. Macro and micronutrients uptake in the roots of B. pilosa and P lanceolata cultivated in the copper mining waste also were not able to be determined due the insufficient biomass production to perform the analysis. P. lanceolata cultivated in the Inceptisol and Mollisol showed the same level of the macronutrients concentration in the roots for P (0.37 and 0.34 g [kg.sup.-1], respectively), K (2.60 and 2.27 g [kg.sup.-1], respectively), Ca (1.10 and 0.89 g [kg.sup.-1], respectively) and Mg (0.62 and 0.54 g [kg.sup.-1], respectively). Micronutrients evaluation in the roots of P lanceolata cultivated in vineyard soils showed different trends and showed higher concentrations in the Inceptisol than the Mollisol for Zn (381 and 81 mg [kg.sup.-1], respectively) and Mn (257 and 91 mg [kg.sup.-1], respectively).

Generally, macro and micronutrients uptake and concentrations in the shoots and roots can be affected by heavy metal contamination in different soils (Ke et al., 2007). There is a paucity of information in the evaluation of the different effects on nutrient uptakes by indigenous plants, furthermore, it is incipient and requires more studies. However, it is notorious that both indigenous plants (B. pilosa and P lanceolata) have high relationship in the nutrient cycling in the environment with high nutrient concentrations in the biomass; and these results can help in further studies and provide more substantial scientific information.

3.3. Copper phytoremediation

Copper concentration in the roots and total biomass were high when both B. pilosa and P. lanceolata were cultivated in the vineyard soils contaminated with copper (Figure 3). B. pilosa cultivated in the Inceptisol showed the highest copper concentration in the shoots, roots and entire plant with 36, 844, 880 mg [kg.sup.-1] of copper, respectively; followed by plants cultivated in the Mollisol soil with 15, 395 and 410 mg [kg.sup.-1] of copper in the shoots, roots and entire plant, respectively (Figure 3A). P. lanceolata showed the same behavior with higher levels of copper phytoaccumulation than B. pilosa plants, even in the native soil (Figure 3B). P. lanceolata plants cultivated in the Inceptisol and Mollisol showed high copper concentrations in the shoots (142 and 68 mg [kg.sup.-1], respectively), roots (964 and 452 mg [kg.sup.-1], respectively) and entire plant (1106 and 520 mg [kg.sup.-1], respectively) (Figure 3B).

The maximum copper concentration in the biomass of the indigenous plants grown in surrounding mining wastes was 110 mg [kg.sup.-1] by Stachys coccinea, in the same study, other indigenous plants showed copper concentrations in a range between 10 and 35 mg [kg.sup.-1] (Gonzalez and Gonzalez-Chavez, 2006). Other study with medicinal plants (B. tripartita, Leonurus cardiaca, Marrubium vulgare, Melissa officinalis and Origanum heracleoticum) showed copper concentration in plant parts in the following order: higher in the roots, than leaves, than flowers, than stems (Zheljazkov et al., 2008). Furthermore, B. tripartite another specie of Bidens showed the lower copper concentrations in the roots, however, wild plants demonstrated copper concentrations ranging from 20 to 40 mg [kg.sup.-1] of dry mass of the roots, in the shoots showed a ranging between 40 and 60 mg [kg.sup.-1] of dry mass, and in the whole plants showed a ranging between 60 and 110 mg [kg.sup.-1] of dry mass. However, Plantago sp. grown such as wild vegetation in a pyrite mine located in the village of Aznalcollar, Sevilla (Southern Spain) showed 22 mg [kg.sup.-1] of copper in the phytomass (Del Rio et al., 2002). This information demonstrates the high potential of both B. pilosa and P. lanceolata plants in copper phytoaccumulation, and the potential use of indigenous plants for phytoremediation.

Average values of phytomass production of the B. pilosa plants are between 3,000 and 6,000 kg [ha.sup.-1] (Fleck et al., 2003). P. major can produce levels of 2,000 kg [ha.sup.-1] of phytomass (Nascimento et al., 2007), once P. lanceolata can produce higher levels of phytomass than P. major.

Based on these references values, it was calculated the potential copper extraction by the indigenous plants assuming the phytomass production of 4,000 (B. pilosa) and 2,000 (P lanceolata) g [ha.sup.-1]. Both indigenous species showed high potential for copper phytoextraction in both vineyard soils contaminated with copper (Figure 4). High levels of copper can be phytoextracted by both B. pilosa and P lanceolata in the Inceptisol with levels of more than 3,500 and 2,200 g [ha.sup.-1] of copper phytoextracted respectively. Both plants cultivated in the Mollisol also showed high levels of copper phytoextraction, but significantly lower than the plants cultivated in the Inceptisol, with values of 1,600 and 1,000 g [ha.sup.-1] for both B. pilosa and P lanceolata respectively in the Mollisol. The estimated values of potential copper phytoextraction by indigenous plants show the importance of these plants mainly in copper phytostabilization of these areas. However, B. tripartite also showed potential for phytoremediation of Cd contaminated soils (Wei et al., 2010).

Both indigenous plants B. pilosa and P lanceolata cultivated in copper contaminated soils showed low translocation factor (TF) with values of 0.04 and 0.15, respectively (Table 5). B. pilosa showed high bioaccumulation factor (BCF) grown in the Inceptisol and Mollisol with values of 4.08 and 2.77, respectively. Also, P lanceolata plants showed high BCF for both vineyard soils with BCF values of 4.68 (Inceptisol) and 3.20 (Mollisol).

In one study with P. major and B. alba, it was demonstrated low TF values for copper with values of 0.43 and 0.8, respectively (Yoon et al., 2006). In other study, B. pilosa showed high TF with values higher than 2.4, when it was increased Cd concentration the TF values were decreased (Sun et al., 2009). Different plant stages also can interfere in the metal uptakes and transportation into the plants. It was demonstrated by Sun et al. (2009) which TF values for cadmium of B. pilosa at the flowering and mature stages were between 1.3-7.4 and 1.9-14.4, respectively.

Both P major and B. alba plants cultivated in copper contaminated sites showed BCF values of 1.2 and 0.48, respectively (Yoon et al., 2006). B. pilosa plants showed high BCF to Cd with values between 1.2 and 5.6, depending of the physiologic stage of the plant and Cd concentration in the soil (Sun et al., 2009). BCF of wild plants growing on soil-slag mixtures surrounding slag heaps in Mexico showed different values in many species such as Solanum elaeagnifolium (4.6), B. odorata (1.6), Asphodelusfistulosus (0.2), Schinus molle (0.9), Reseda luteola (0.4) (Gonzalez and Gonzalez-Chavez, 2006). Other indigenous species such as Acia raddiena and Avera javanica, the BCFs were almost 0.2 and 0.23 respectively in plants grown in mine tailings (Rashed, 2010). However, it is notorious that the copper concentrations in these soils are lower than concentrations obtained in the vineyard soils studied, which increases the BCF values. However, the results of B. pilosa and P. lanceolata showed higher BCF to both B. pilosa and P. lanceolata in the vineyard soils compared with the most BCF values reported in the literature.

B. pilosa plants cultivated in the Inceptisol showed high metal extraction ratio (MER) with value of 14.40%, and it is compared to the native soil with MER of 14.82%. B. pilosa cultivated in the Mollisol also showed high MER index of 4.38%. Surprisingly the expectations, P. lanceolata cultivated in both vineyard soils showed the highest values of MER of 65.74% (Inceptisol) and 21.70% (Mollisol). MER index is related with the percentage of the copper that can be accumulated in the shoots to that in the soil (Mertens et al., 2005). It shows a high potential to extract the metals from soil, and it indicates these both indigenous species (B. pilosa and P lanceolata) as copper hyperaccumulator plants.

The plant effective number of the shoots (PENs) necessary to extract 1 g of copper were high to B. pilosa cultivated in the Inceptisol (83,001 plants) and to P lanceolata cultivated in the Mollisol (43,814 plants) (Table 4). Plant effective number of the total plant (PENt) showed the same behavior; however, the number of the plants was highly reduced to both B. pilosa and P. lanceolata. B. pilosa showed the PENt to Inceptisol and Mollisol soils of the 2,109 and 3,536 plants, and the P lanceolata grown in the Inceptisol and Mollisol showed PENt of 7,844 and 2,985 plants, respectively. These PEN numbers were much higher than other plant such as Piptatherum miliaceum (Smilo grass) in edaphic Pb and Zn contaminated sites in short periods (Garcia et al., 2004). However, the B. pilosa and P. lanceolata species in this study were naturally found in the vineyard soils in high plant densities.

Indigenous plants with high hyperaccumulation capacity are especially common in the tropics and subtropics, apparently because the metal accumulation is a defense against plant-eating insects and microbial pathogens (Moffat, 1995). However, the results found in this study showed high capacity in growth, macro and micronutrient uptake, and copper phytoaccumulation in the biomass. Compiling all these characteristics of the both indigenous plants B. pilosa and P. lanceolata, it culminates in a high potential of these plants in copper phytoremediation and phytostabilization from copper contaminated soils.

4. Conclusions

The results presented in this study demonstrate that both indigenous plants B. pilosa and P. lanceolata are efficient tools for bioremediation of copper-contaminated sites such as vineyard soils. These plants demonstrate high growth potential with high tolerance to copper contaminated areas, acting as cover crops against the direct impact of the rainfall in the soil surface, reducing soil and water losses by surface runoff with consequently contamination of the adjacent environments. Furthermore, high macro and micronutrients were accumulated in the biomass, showing an important role in the nutrient cycling. However, high copper concentrations were extracted from soils and phytoaccumulated. Even these plants are considered weeds to agriculture, they are easily controlled and managed to do not affect negatively the vineyard production. Furthermore, both indigenous plants B. pilosa and P lanceolata showed high potential to growth, phytostabilize and phytoremediate copper from both vineyard soils, being important candidates to phytoremediation of copper contaminated vineyards and to allow further alternative crops.

http://dx.doi.org/10.1590/1519-6984.01914

Acknowledgements

This Project was supported by CAPES (Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior) and CNPq (Conselho Nacional de Desenvolvimento Cientifico e Tecnologico), Brazil. Thanks to Marcelo Gioacometti, Guilherme Siviero and Dione Dinael Rohers for technical assistance.

References

ALI, H., KHAN, E. and SAJAD, M.A., 2013. Phytoremediation of heavy metals--concepts and applications. Chemosphere, vol. 91, no. 7, pp. 869-881. http://dx.doi.org/10.1016/j. chemosphere.2013.01.075. PMid:23466085.

ANDRADE, S.A.L., GRATAO, P.L., AZEVEDO, R.A., SILVEIRA, A.P.D., SCHIAVINATO, M.A. and MAZZAFERA, P, 2010. Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. EnvironmentExpimental Botany, vol. 68, no. 2, pp. 198-207. http://dx.doi.org/10.1016/j.envexpbot.2009.11.009.

BABU, A.G., KIM, J.D. and OH, B.T., 2013. Enhancement of heavy metal phytoremediation by Alnus firma with endophytic Bacillus thuringiensis GDB-1. Journal of Hazardous Materials, vol. 250-251, pp. 477-483. http://dx.doi.org/10.1016/jjhazmat.2013.02.014. PMid:23500429.

DAZY, M., BERAUD, E., COTELLE, S., GREVILLIOT, F., FERARD, J. and MASFARAUD, J., 2009. Changes in plant communities along soil pollution gradients: Responses of leaf antioxidant enzyme activities and phytochelatin contents. Chemosphere, vol. 77, no. 3, pp. 376-383. http://dx.doi.org/10.1016j. chemosphere.2009.07.021. PMid:19692108.

DEL RIO, M., FONT, R., ALMELA, C., VELEZ, D., MONTORO, R. and BAILON, A.D.H., 2002. Heavy metals and arsenic uptake by wild vegetation in the Guadiamar river area after the toxic spill of the Aznalcollar mine. Journal of Biotechnology, vol. 98, no. 1, pp. 125-137. http://dx.doi.org/10.1016/S0168-1656(02)00091-3. PMid:12126811.

FLECK, N.G., RIZZARDI, M.A., AGOSTINETTO, D. and VIDAL, R.A., 2003. Producao de sementes por picao-preto e guanxuma em funcao de densidades das plantas daninhas e da epoca de semeadura da soja. Planta Daninha, vol. 21, no. 2, pp. 191-202. http://dx.doi.org/10.1590/S0100-83582003000200004.

GARCIA, G., FAZ, A. and CUNHA, M., 2004. Performance of Piptatherum miliaceum (Smilo grass) in edaphic Pb and Zn phytoemediation over a short growth period. International Biodeterioration & Biodegradation, vol. 54, no. 2-3, pp. 245-250. http://dx.doi.org/10.1016/j.ibiod.2004.06.004.

GONZALEZ, R.C. and GONZALEZ-CHAVEZ, M.C.A., 2006. Metal accumulation in wild plants surrounding mining wastes. Environmental Pollution, vol. 144, no. 1, pp. 84-92. http://dx.doi. org/10.1016/j.envpol.2006.01.006. PMid:16631286.

KE, W., XIONG, Z.T., CHEN, S. and CHEN, J., 2007. Effects of copper and mineral nutrition on growth, copper accumulation and mineral element uptake in two Rumex japonicus populations from a copper mine and an uncontaminated field sites. Environmental and Experimental Botany, vol. 59, no. 1, pp. 59-67. http://dx.doi. org/10.1016/j.envexpbot.2005.10.007.

HE, L.Y., ZHANG, Y.F., MA, H.Y., SU, L.N., CHEN, Z.J., WANG, Q.Y., QIAN, M. and SHENG, X.F., 2010. Characterization of copper-resistant bacteria and assessment of bacterial communities in rhizosphere soils of copper-tolerant plants. Applied Soil Ecology, vol. 44, no. 1, pp. 49-55. http://dx.doi.org/10.1016/). apsoil.2009.09.004.

KOMAREK, M., CADKOVA, E., CHRASTNY, V., BORDAS, F. and BOLLINGER, J., 2010. Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environment International, vol. 36, no. 1, pp. 138-151. http://dx.doi.org/10.1016/j.envint.2009.10.005. PMid:19913914.

LACERDA, L.D., SANTOS, J.A. and LOPES, D.V., 2009. Fate of copper in intensive shrimp farms: bioaccumulation and deposition in pond sediments. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 69, no. 3, pp. 851-858. http://dx.doi.org/10.1590/S1519- 69842009000400012. PMid:19802444.

LATZEL, V. and KLIMESOVA, J., 2009. Fitness of resprouters versus seeders in relation to nutrient availability in two Plantago species. Acta Oecologica, vol. 35, no. 4, pp. 541-547. http:// dx.doi.org/10.1016/j.actao.2009.04.003.

LAYBAUER, L., 1998. Incremento de metais pesados na drenagem receptora de efluentes de mineracao--Minas do Camaqua, Sul do Brasil. Revista Brasileira de Recursos Hidricos, vol. 3, pp. 29-36.

LIU, Z., HE, Z., CHEN, W., YUAN, F., YAN, K. and TAO, D., 2009. Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator--Lonicera japonica Thunb. Journal of Hazardous Materials, vol. 169, no. 1-3, pp. 170-175. http://dx.doi.org/10.1016/jjhazmat.2009.03.090. PMid:19380199.

MERTENS, J., LUYSSAERT, S. and VERHEYEN, K., 2005. Use and abuse of trace metal concentrations in plants tissue for biomonitoring and phytoextraction. Environmental Pollution, vol. 138, no. 1, pp. 1-4. http://dx.doi.org/10.1016Zj.envpol.2005.01.002. PMid:16023913.

MOFFAT, A.S., 1995. Plants proving their worth in toxic metal cleanup. Science, vol. 269, no. 5222, pp. 302-303. http://dx.doi. org/10.1126/science.269.5222.302. PMid:17841233.

NASCIMENTO, E.X., MOTA, J.H., VIEIRA, M.C. and ZARATE, N.A.H., 2007. Producao de biomassa de Pfaffia glomerata (Spreng.) Pedersen e Plantago major L. em cultivo solteiro e consorciado. Ciencia e Agrotecnologia, vol. 31, no. 3, pp. 724-730. http:// dx.doi.org/10.1590/S1413-70542007000300019.

PANDEY, V.C., 2013. Suitability of Ricinus communis L. cultivation for phytoremediation of fly ash disposal sites. Ecological Engineering, vol. 57, pp. 336-341. http://dx.doi.org/10.1016/j. ecoleng.2013.04.054.

QI, C., WU, F., DENG, Q., LIU, G., MO, C., LIU, B. and ZHU, J., 2011. Distribution and accumulation of antimony in plants in the super-large Sb deposit areas, China. Microchemistry Journal, vol. 99, no. 1, pp. 44-51. http://dx.doi.org/10.1016/j. microc.2010.05.016.

RASHED, M.N., 2010. Monitoring of contaminated toxic and heavy metals, from mine tailings through age accumulation, in soil and some wild plants at Southeast Egypt. Journal of Hazardous Materials, vol. 178, no. 1-3, pp. 739-746. http://dx.doi. org/10.1016/j.jhazmat.2010.01.147. PMid:20188467.

REDONDO-GOMEZ, S., MATEOS-NARANJO, E. and ANDRADES-MORENO, L., 2010. Accumulation and tolerance characteristics of cadmium in a halophytic Cd-hyperaccumulator, Arthrocnemum macrostachyum. Journal of Hazardous Materials, vol. 184, no. 1-3, pp. 299-307. http://dx.doi.org/10.1016/j. jhazmat.2010.08.036. PMid:20832167.

REDONDO-GOMEZ, S., MATEOS-NARANJO, E., VECINOBUENO, I. and FELDMAN, S.R., 2011. Accumulation and tolerance characteristics of chromium in a cordgrass Cr-hyperaccumulator, Spartina argentinensis. Journal of Hazardous Materials, vol. 185, no. 2-3, pp. 862-869. http://dx.doi.org/10.1016/j.jhazmat.2010.09.101. PMid:20970921.

SHI, G. and CAI, Q., 2009. Cadmium tolerance and accumulation in eight potential energy crops. Biotechnology Advances, vol. 27, no. 5, pp. 555-561. http://dx.doi.org/10.1016/j.biotechadv.2009.04.006. PMid:19393309.

SUN, Y., ZHOU, Q. and DIAO, C., 2008. Effects of cadmium and arsenic on growth and metal accumulation of Cd-hyperaccumulator Solanum nigrum L. Bioresource Technology, vol. 99, no. 5, pp. 1103-1110. http://dx.doi.org/10.1016/j.biortech.2007.02.035. PMid:17719774.

SUN, Y., ZHOU, Q., WANG, L. and LIU, W., 2009. Cadmium tolerance and accumulation characteristics of Bidens pilosa L. as a potential Cd-hyperaccumulator. Journal of Hazardous Materials, vol. 161, no. 2-3, pp. 808-814. http://dx.doi.org/10.1016/j. jhazmat.2008.04.030. PMid:18513866.

WEI, S., ZHOU, Q., ZHAN, J., WU, Z., SUN, T., LYUBU, Y. and PRASAD, M.N.V., 2010. Poultry manured Bidens tripartite L. extracting Cd from soil--potential for phytoremediating Cd contaminated soil. Bioresource Technology, vol. 101, no. 22, pp. 8907-8910. http://dx.doi.org/10.1016/j.biortech.2010.06.090. PMid:20624678.

WILKINS, D.A., 1978. The measurement of tolerance to edaphic factors by means of root growth. The New Phytologist, vol. 80, no. 3, pp. 623-633. http://dx.doi.org/10.1111/j.1469-8137.1978. tb01595.x.

WU, F., YANG, W., ZHANG, J. and ZHOU, L., 2010. Cadmium accumulation and growth responses of a poplar (Populus deltoids x Populus nigra) in cadmium contaminated purple soil and alluvial soil. Journal of Hazardous Materials, vol. 177, no. 1-3, pp. 268-273. http://dx.doi.org/10.1016/j.jhazmat.2009.12.028. PMid:20042282.

YOON, J., CAO, X., ZHOU, Q. and MA, L.Q., 2006. Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. The Science of the Total Environment, vol. 368, no. 2-3, pp. 456-464. http://dx.doi.org/10.1016/j.scitotenv.2006.01.016. PMid:16600337.

ZHELJAZKOV, V.D., JELIAZKOVA, E.A., KOVACHEVA, N. and DZHURMANSKI, A., 2008. Metal uptake by medicinal plant species grown in soils contaminated by a smelter. Environmental and Experimental Botany, vol. 64, no. 3, pp. 207-216. http:// dx.doi.org/10.1016/j.envexpbot.2008.07.003.

R. Andreazza (a) *, L. Bortolon (b), S. Pieniz (c), F M. Bento (d) and F.A.O. Camargo (e)

(a) Laboratorio de Quimica Ambiental, Centro de Engenharia, Universidade Federal de Pelotas--UFPel, Av. Almirante Barroso, 1734, CEP 96010-208, Pelotas, RS, Brazil

(b) Centro Nacional de Investigacao Pesqueira, Aquicultura e Sistemas Agricolas, Empresa Brasileira de Pesquisa Agropecuaria--Embrapa, Quadra 104 Sul, 34, Av. LO 1, CEP 77020-020, Palmas, TO, Brazil

(c) Laboratorio de Quimica Ambiental, Faculdade de Nutricao, Universidade Federal de Pelotas--UFPel, Av. Almirante Barroso, 1734, CEP 96010-208, Pelotas, RS, Brazil

(d) Laboratorio de Microbiologia, Departamento de Microbiologia, Universidade Federal do Rio Grande do Sul--UFRGS, Rua Sarmento Leite, 500, CEP 90050-170, Porto Alegre, RS, Brazil

(e) Laboratorio de Biorremediacao, Departamento de Ciencia do Solo, Universidade Federal do Rio Grande do Sul--UFRGS, Av. Bento Goncalves, 7712, CEP 91541-000, Porto Alegre, RS, Brazil

* e-mail: robsonandreazza@yahoo.com.br

Received: February 19, 2014--Accepted: May 28, 2014--Distributed: November 30, 2015

(With 4 figures)

Table 1. Chemical-physical * characteristics of soils: Native
soil, Inceptisol and Mollisol, and copper mining waste.

Solo                 pH         Carbon        Clay

                    1:1                  %

Native soil         5.8          2.4           25
Inceptisol          6.3          1.5           19
Mollisol            6.0          1.4           29
Waste               7.9          0.5           02

               Cu Extrac
Solo          ([dagger])    Cu Total    Ca    Mg    Mn    S     Zn

                                       mg [kg.sup.-1]

Native soil   3.8 (1.0)        35      1860   150   59   6.3   8.1
Inceptisol    207 (171)       507      2180   388   55   6.1   19.0
Mollisol      142 (104)       281      1560   263   35   5.9   18.0
Waste         576 (479)       852      4840   213   2    0.1   0.8

Solo         P (Extrac)  P (Total)              N (Extrac)

                                mg [kg.sup.-1]

                                    N[H.sub.4.sup.+]   N[O.sub.3.sup.-]

Native soil      14         600            277               216
Inceptisol       28         700            12                 11
Mollisol         27         900            13                 10
Waste            32         700             1                 2

Solo                     N (Total)          K

                             %        mg [kg.sup.-1]

Native soil                0.31            217
Inceptisol                 0.20            142
Mollisol                   0.18            167
Waste                      0.01             32

Table 2. Tolerance index (TI) of the height, green mass of the
shoots and roots, and dry mass of the shoots and roots of
Bidenspilosa and Plantago lanceolata plants after 64 and 85 days
of growth respectively in three copper contaminated soils:
Inceptisol, Mollisol and copper mining waste (waste).

                                   Bidens pilosa

Soils                     Green mass                       Dry mass

             Height     Shoots         Roots         Shoots     Roots

                                         %

Inceptisol   119.14     208.46         273.33        216.97     302.56
Mollisol     194.37     201.24         328.00        337.33     432.69
Waste        45.71       3.16           2.00          2.88       3.85

                                Plantago lanceolata

Soils                            Green mass               Dry mass

             Height     Shoots         Roots         Shoots    Roots

                                         %

Inceptisol    ND *      279.02         411.11        153.42   3476.19
Mollisol       ND       839.73        1992.59       1065.68   23285.71
Waste          ND        3.57           1.48          4.33     19.05

* ND not determined.

Table 3. Macro and micronutrients in dry mass of the shoots of
the Bidens pilosa and Plantago lanceolata plants, after 64 and 85
days of growth respectively in different copper contaminated
soils: Native soil (Control, no contaminated); Inceptisol;
Mollisol and copper mining waste (waste).

                                Bidens pilosa

                        N                       P

                               g [kg.sup.-1]

Native Soil   3.30 [+ or -] 0.14a *   0.10 [+ or -] 0.01a
Inceptisol    1.25 [+ or -] 0.08c     0.15 [+ or -] 0.01a
Mollisol      0.85 [+ or -] 0.02c     0.22 [+ or -] 0.02a
Waste         2.48 [+ or -] 0.01b     0.27 [+ or -] 0.01a
CV (%) **             19.76                   34.76

                                Bidens pilosa

                        K                      Ca

                               g [kg.sup.-1]

Native Soil   2.88 [+ or -] 0.14a     1.57 [+ or -] 0.02ab
Inceptisol    2.27 [+ or -] 0.05a     1.76 [+ or -] 0.09a
Mollisol      1.60 [+ or -] 0.05b     1.38 [+ or -] 0.03b
Waste         1.45 [+ or -] 0.09b     1.30 [+ or -] 0.05b
CV (%) **             15.24                   13.06

                      Bidens pilosa

                           Mg

                  g [kg.sup.-1]

Native Soil       0.38 [+ or -] 0.05b
Inceptisol        0.79 [+ or -] 0.04a
Mollisol          0.57 [+ or -] 0.00b
Waste             0.47 [+ or -] 0.01b
CV (%) **                 25.16

Soils                       S

                      g [kg.sup.-1]

Native Soil       0.17 [+ or -] 0.01a
Inceptisol        0.26 [+ or -] 0.04a
Mollisol          0.09 [+ or -] 0.00a
Waste             0.09 [+ or -] 0.00a
CV (%)                    58.45

Soils                  Zn                      Fe

                              mg [kg.sup.-1]

Native Soil    80.05 [+ or -] 1.36b   323.50 [+ or -] 25.07a
Inceptisol    385.10 [+ or -] 23.7a   290.60 [+ or -] 11.07a
Mollisol      136.78 [+ or -] 2.05b   226.45 [+ or -] 17.19a
Waste         119.40 [+ or -] 5.09b   174.70 [+ or -] 10.59b
CV (%)                48.73                   35.65

Soils                  Mn                      Na

                              mg [kg.sup.-1]

Native Soil   303.73 [+ or -] 5.54a   258.50 [+ or -] 10.0a
Inceptisol    307.83 [+ or -] 8.62a   220.57 [+ or -] 11.8a
Mollisol      85.47 [+ or -] 2.28b    161.70 [+ or -] 8.79a
Waste         61.17 [+ or -] 3.75b    133.40 [+ or -] 9.75a
CV (%)                36.40                   30.74

                              Plantago lanceolata

Soils             N                P                       K

                              g [kg.sup.-1]

Native Soil    ND ***    0.29 [+ or -] 0.02b     5.45 [+ or -] 0.18a
Inceptisol       ND      0.41 [+ or -] 0.02a     4.61 [+ or -] 0.14a
Mollisol         ND      0.37 [+ or -] 0.01a     5.47 [+ or -] 0.10a
Waste            ND               ND                       ND
CV (%)           --              22.43                   13.47

                          Plantago lanceolata

Soils                  Ca                      Mg

                            g [kg.sup.-1]

Native Soil   7.74 [+ or -] 0.16a     0.42 [+ or -] 0.01b
Inceptisol    8.79 [+ or -] 0.06a     0.99 [+ or -] 0.04a
Mollisol      7.12 [+ or -] 0.19a     0.90 [+ or -] 0.02a
Waste                  ND                      ND
CV (%)                11.13                   13.55

Soils                   S                      Zn

                              g [kg.sup.-1]

Native Soil   1.97 [+ or -] 0.07a     232.2 [+ or -] 4.70a
Inceptisol    1.49 [+ or -] 0.07a     185.5 [+ or -] 5.44a
Mollisol      1.14 [+ or -] 0.03a      99.8 [+ or -] 1.14b
Waste                  ND                      ND
CV (%)                25.70                   20.55

Soils                  Fe                      Mn              Na

                 mg [kg.sup.-1]

Native Soil   1473.0 [+ or -] 67.8a   405.4 [+ or -] 50.9a     ND
Inceptisol     959.3 [+ or -] 16.6b   197.3 [+ or -] 3.62b     ND
Mollisol       620.5 [+ or -] 3.23b   106.8 [+ or -] 1.82b     ND
Waste                  ND                      ND              ND
CV (%)                20.33                   73.27            --

* Values are means [+ or -] standard error of the mean. Different
letters in the column represent significant differences (P<0.05).
** CV is the coefficient of variation of the means. *** ND means
not determined by low biomass production, being not enough to
evaluations.

Table 4. Macro and micronutrients in dry mass of the roots of the
Bidens pilosa and Plantago lanceolata plants, after 64 and 85
days of growth respectively in different copper contaminated
soils: Native soil (Control, no contaminated); Inceptisol;
Mollisol and copper mining waste (waste).

                               Bidens pilosa

Soils                    N                        P

                                g [kg.sup.-1]

Native Soil    2.52 [+ or -] 0.07a *     0.09 [+ or -] 0.00a
Inceptisol      1.22 [+ or -] 0.01b      0.15 [+ or -] 0.01a
Mollisol        0.81 [+ or -] 0.01c      0.13 [+ or -] 0.01a
Waste                  ND **                     ND
CV (%) ***             12.00                    25.74

                                Bidens pilosa

Soils                    K                       Ca

                                g [kg.sup.-1]

Native Soil     2.78 [+ or -] 0.05a      0.67 [+ or -] 0.04a
Inceptisol      1.99 [+ or -] 0.11b     0.51 [+ or -] 0.02ab
Mollisol        1.54 [+ or -] 0.03c      0.44 [+ or -] 0.01b
Waste                   ND                       ND
CV (%) ***             14.86                    19.87

                         Bidens pilosa

Soils                          Mg

Native Soil            0.15 [+ or -] 0.01c
Inceptisol             0.31 [+ or -] 0.02b
Mollisol               0.45 [+ or -] 0.01a
Waste                          ND
CV (%) ***                    18.28

Soils                           S

                          g [kg.sup.-1]

Native Soil           0.25 [+ or -] 0.02ab
Inceptisol             0.32 [+ or -] 0.02a
Mollisol               0.20 [+ or -] 0.01b
Waste                          ND
CV (%)                        25.02

Soils                   Zn                       Fe

                                           mg [kg.sup.-1]

Native Soil    147.0 [+ or -] 8.36b     1472.7 [+ or -] 52.8a
Inceptisol     381.9 [+ or -] 35.6a     1104.3 [+ or -] 88.5a
Mollisol        80.5 [+ or -] 2.36b     1037.7 [+ or -] 45.6a
Waste                   ND                       ND
CV (%)                 43.27                    27.72

Soils                   Mn                       Na

                  mg [kg.sup.-1]

Native Soil    256.8 [+ or -] 17.6a     1631.0 [+ or -] 126.2b
Inceptisol     150.3 [+ or -] 7.14b     2696.2 [+ or -] 146.0a
Mollisol        44.8 [+ or -] 1.43b     1423.7 [+ or -] 15.71b
Waste                   ND                       ND
CV (%)                 61.70                    24.24

                             Plantago lanceolata

Soils                    N                        P

                                g [kg.sup.-1]

Native Soil             ND               0.34 [+ or -] 0.01a
Inceptisol              ND               0.37 [+ or -] 0.01a
Mollisol                ND               0.34 [+ or -] 0.02a
Waste                   ND                       ND
CV (%)                  --                      20.82

                            Plantago lanceolata

                         K                       Ca

                                g [kg.sup.-1]

                6.52 [+ or -] 0.18a      2.29 [+ or -] 0.14a
                2.60 [+ or -] 0.16b      1.10 [+ or -] 0.03b
                2.27 [+ or -] 0.10b      0.89 [+ or -] 0.04b
                        ND                       ND
                       18.67                    24.44

                      Plantago lanceolata

Soils                         Mg

                         g [kg.sup.-1]

Native Soil           0.47 [+ or -] 0.01a
Inceptisol            0.62 [+ or -] 0.03a
Mollisol              0.54 [+ or -] 0.01a
Waste                         ND
CV (%)                       17.45

                               S

                         g [kg.sup.-1]

Native Soil           0.72 [+ or -] 0.02a
Inceptisol            0.51 [+ or -] 0.01b
Mollisol              0.24 [+ or -] 0.01c
Waste                         ND
CV (%)                       22.27

                        Zn                       Fe

                              mg [kg.sup.-1]

Native Soil    408.3 [+ or -] 20.5b     5896.0 [+ or -] 166.9a
Inceptisol     1321.0 [+ or -] 91.7a    3410.0 [+ or -] 171.3a
Mollisol       464.7 [+ or -] 6.88b     1678.6 [+ or -] 67.22b
Waste                   ND                       ND
CV (%)                 31.78                    36.38

                        Mn                       Na

                              mg [kg.sup.-1]

Native Soil    607.7 [+ or -] 29.3a              ND
Inceptisol     257.3 [+ or -] 14.8a              ND
Mollisol        91.4 [+ or -] 1.80b              ND
Waste                   ND                       ND
CV (%)                 61.34                     --

* Values are means [+ or -] standard error of the mean. Different
letters in the column represent significant differences
(P < 0.05). ** CV is the coefficient of variation of the means.
*** ND means not determined by low biomass production, being not
enough to evaluations.

Table 5. Translocation factor (TF) and bioaccumulation factor
(BCF) for copper, copper extraction ratio (MER), plant effective
number of shoots (PENs) and plant effective number of total plant
(PENt) of Bidens pilosa and Plantago lanceolata, after 64 and 85
days of growth respectively in different copper contaminated
soils: Native soil (Control); Inceptisol and Mollisol.

                                Bidens pilosa

Soils            TF      BCF      MER         PENs        PENt

                                   %       plants (a)

Native Soil     0.57    8.27     14.82       446594      106642
Inceptisol      0.04    4.08     14.40       83001        2109
Mollisol        0.04    2.77      4.38       154344       3536
Waste           ND *     ND        ND          ND          ND

                               Plantago lanceolata

Soils            TF      BCF      MER         PENs        PENt

                                   %       plants (b)

Native Soil     0.99    38.28    549.33      412957      190274
Inceptisol      0.15    4.68     65.74       102539       7844
Mollisol        0.15    3.20     21.70       43814        2985
Waste            ND      ND        ND          ND          ND

* ND means not determined by low biomass production, being not
enough to evaluations. (a) Values are the average number of
Bidens pilosa plants capable to remove 1 g of copper after 64
days of growth. (b) Values are the average number of Plantago
lanceolata plants capable to remove 1 g of copper after 85 days
of growth.
COPYRIGHT 2015 Association of the Brazilian Journal of Biology
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2015 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Original Article
Author:Andreazza, R.; Bortolon, L.; Pieniz, S.; Bento, F.M.; Camargo, F.A.O.
Publication:Brazilian Journal of Biology
Date:Nov 1, 2015
Words:7233
Previous Article:Microhabitats occupied by Myxomycetes in the Brazilian Atlantic Forest: Heliconiaceae inflorescences/Microhabitats ocupados por Myxomycetes na...
Next Article:Population genetics of Chrysoperla externa (Neuroptera: Chrysopidae) and implications for biological control/Genetica de populacoes de Chrysoperla...
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters