Ecotoxicology and emediation of agricultural soils
polluted with lead in Argentina
By: 1Rodriguez, J.H.,
1Salazar, M.J., 1Vergara Cid, C., 1Blanco, A., *1Pignata, M.L.
Heavy metal pollution of soils is a problem of considerable concern worldwide due to the potential toxicological risk to the environment and food safety. In many developing countries, agricultural areas are frequently affected by industrial emissions since they are often located in peripheral areas to urban agglomerations. These sites experience progressive environmental degradation as a consequence of their rapid development, when it is not accompanied by effective environmental and land use regulations. Consequently, large areas of farmland have been contaminated by metals owing to anthropogenic input from mining, smelting, fossil fuel burning, phosphate fertilizers and sewage sludge.
Heavy metal pollution has a harmful effect on biological systems and does not undergo biodegradation, as heavy metals which lie in soils have residence time of thousands of years and during which it accumulates in living organisms. Thus, once soil has become polluted, it remains a long-term source of metal exposure, affecting crop growth and the quality of agricultural products, as well as a serious threat to human health through contamination of the food chain, due to the potential toxicological risk from the consumption of crops that are grown under these conditions.
Many studies, have been carried out worldwide in industrial areas near agricultural soils, and have reported toxic metal concentrations in crops above permitted levels. Regarding lead (Pb), it has been shown that this metal is a highly toxic element, even at low concentrations, leading to serious consequences in human health and ecosystems. The harmful effects on human health include neurological damage, neurotoxic diseases and anemia. For this reason, remediation of soils polluted with this toxic metal is necessary in order to reduce the associated risks, make land safe for agricultural production and enhance food security.
Toxicological risk of crops growing in contaminated soils
Studies about the potential enrichment of heavy metals in soils as a result of antropogenic activities and their subsequent transfer to crops have been performed in the main crop production area of Argentina (Córdoba and Buenos Aires), with results indicating that Pb concentrations in some agricultural soils of Córdoba have exceeded the permitted maximum levels according to national and international laws. Moreover, in these sites, an effective translocation and bioaccumulation of Pb in the principal crop soybean was observed, and it is important to note that accumulation of Pb above the permissible levels was also reported in soybean and wheat growing in soils which did not reach high levels of pollution. In fact, the uptake of heavy metal by plants, with soil–plant transfer of metals, is a very complex process governed by several factors (both natural and anthropogenic) such as environmental conditions, soil heavy metal content, and the sorptive capacity of soil, redox conditions, organic matter and pH.
These parameters are known to control the processes of mobility and availability of metals in soils. Moreover, in sites highly polluted with Pb in Córdoba, there is evidence that an enrichment of soil by Pb can modify the bioavailability of other toxic elements, such as Cd, which although only present at low concentrations in soil, was observed at higher concentrations in soybean seeds, a process known as “concomitant bioaccumulation” of contaminants in the plants.
To assess the toxicological risk of consuming crops exposed to heavy metals, an index named “target hazard quotient” has been developed, which considers the concentration of contaminants in food and some consumer characteristics (age, origin and weight). Another index called “hazard index” summarizes the effects of different pollutants. Both the indices are considered as lifetime risk.
In a study performed in Pb polluted soils in Córdoba, by applying this above mentioned indices we reported an effective toxicological risk for potential Chinese consumers, due to the high consumption of soybean in comparison with Argentina or Europe (taking into account that they are the main recipients of this export product). In addition, regarding the quality of crops, it is expected that the accumulation of toxic elements causes physiological damage affecting their productivity and quality. However, an optimal quality of soybean crops has been reported, which presented toxic levels of metals in their seeds. Thus, these results suggest the importance of monitoring agricultural soils and metal transfer to crops.
Remediation of heavy metal contaminated soils
As mentioned above, taking into account the residence times and poor degradation of heavy metals in soil, with consequent damage to the environment and human health, it is necessary to develop environmental friendly remediation methodologies.
Traditional remediation methodologies, which are based on engineering processes, generally involve the removal of the contaminated soil and its physico-chemical treatment. However, traditional remediation involves the loss of fertile soil as an agricultural resource. Thus, taking into account that the loss of fertile soil in the world is about 24 billion tons per year, and it requires 500 years for the natural formation of 2 cm of fertile soil (a process which can not be artificially reproduced), it is pertinent to replace this remediation methodology by a more environmental friendly techniques. Therefore, in this context, phytoremediation is an attractive alternative as it is a biotechnological process that involves the use of plants and associated microorganisms to remedy the contamination of the environment (soils, sediments, and water). This harnesses the physiological or mechanical processes of plants to alleviate pollution, through degradation, extraction and stabilization. Regarding heavy metal contaminated soils phytoremediation is limited to the immobilization of metals in roots and the rhizosphere (phytostabilization) or metal accumulation in aerial parts (phytoextraction).
Focussing on the potential use of phytoremediation, we performed a screening study of native plants, growing in Pb-polluted soils in the province of Córdoba, Argentina and identified two species (Bidens pilosa and Tagetes minuta) with a high capability of extracting Pb and accumulating it in their aerial tissues. In addition, a useful phytostabilizator species (Sorghum halepense) has been reported. It is noteworthy that the ability of these phytoextractor species depends on many factors that interact in complex ways, thus making it difficult to standardize this method for different cases. For this reason, we carried out studies about the influence of factors such as the content of other elements in soil and their interaction with Pb, the presence of natural rhizosphere microorganisms and agricultural implications, and the application of phytohormones plant growth promoters. As the results indicated a strong intraspecific variability, we are currently performing investigations about acclimation and adaptation of different populations of these species, in order to isolate and select individuals with higher phytoextractor efficiencies for reproduction and employment. Once these individuals are identified, the study of their genetic profile will allow general parameters applicable to different phytoremediation projects to be established.
Remediation of lead and economic profit.
In emerging economies the implementation of remediation programs in contaminated agricultural soils has encountered opposition when addressing the interests of the different social sectors involved. For example, the control authorities do not have sufficient influence on producers and landowners, who often perceive remediation as a negative concept since the entails a loss of productivity during the period required to attain permitted metal concentrations. However, the latest advances in science in this context can offer alternatives which include the possibility of obtaining financial gains during the remediation process.
Below, we relate three different remediation studies in which our research group works:
1- Phytoremediation: a case study of Tagetes minuta.
The aim of combining phytoextraction of metals with the ability to provide a return in investment was attained through the use of aromatic crops associated with essential oil production, Tagetes minuta was one of the species identified in the screening study for its ability to accumulate Pb. This is an annual aromatic plant that belongs to the Asteraceae family, originally from the temperate regions of South America, it has been recently introduced in several regions of the world for medicinal purposes. The plant has a rich chemistry for obtaining natural products and also yields volatile essential oils, which can be extracted by hydrodistillation, and are widely used in cosmetics, perfumery (with its aroma being classified as sweet and similar to citrus fruits), as a food flavoring and in beverages and medicine. It has antioxidant and anti-inflammatory effects, antibacterial and nematicidal properties, and it can be used in repellents for mosquitoes, ticks and mites, as well as in insecticides against the family Psychodidae and vectors of diseases such as leishmaniasis. This extensive potential usage makes T. minuta an optimal candidate for Pb phytorremediation with a view towards obtaining economic profit, thus we decided to concentrate our investigation on this species in Córdoba, Argentina. We found that when this species accumulated Pb in its harvestable organs, this metal was not present in its essential oil, which was therefore a safe product of good quality. It was also observed that the Pb concentration in leaves affected the production of some minor oil components, which are involved in the plant response against stress. These components may explain the high Pb tolerance of T. minuta, and further study might reveal important clues for the enhancement of Pb uptake by other accumulator species.
2- Phytoremediation: a case study of co-cropping.
As mentioned above, phytoremediation is a favorable alternative from the environmental perspective in agricultural soils polluted with toxic metals. However, this methodology is generally time-consuming and requires the cessation of agriculture for a number of years, which represents a non-economical alternative for agricultural producers. To circumvent this problem, co-cropping systems have been recently applied that involve the growth of a metal hyperaccumulator plant associated with a low metal accumulating crop, in order to improve the remediation of heavy metals. In contrast to mono-cropping, co-cropping can enhance the growth and metal uptake of the hyper-accumulating plant. This is done by producing a synergistic effect between the species through the sharing of their rhizospheres,. Furthermore, it may be possible to use hyperaccumulators to alleviate the metal uptake of conventional plants by depletion of the potentially toxic metals within shared rhizospheres, which has been given the name ‘phytoprotection’. However, a better understanding of the rhizosphere interactions of co-cropped species is still required in order to be able to optimize phytoremediation technologies. Thus, the purpose of our study was to evaluate two potential phytoextractor plants (the native species Bidens pilosa and Tagetes minuta) co-cropped with agricultural species growing on lead-polluted soils in Córdoba, Argentina. The concentrations of Pb, as well as those of other heavy metals, were investigated in the phytoextractors, crop species and soils, with the potential risk to the health of consumers also being estimated. The soil parameters pH, EC, OM% and bioavailable lead showed a direct relationship with the accumulation of Pb in roots. In addition, the concentration of Pb in roots of native species was closely related to Fe, Cu, Mn and Zn. Our results indicate that the interaction between rhizospheres increased the phytoextraction of lead, which was accompanied by an increase in the biomass of the phytoextractor species.
3- Organic amendments: a case study of biochar.
Phytoremediation is not effective where heavy metal contamination in soils is very high. Thus, in these cases, in situ remediation in order to reduce the availability of metals is the most appropriate alternative. Heavy metal immobilization technology often uses organic and inorganic amendments to accelerate the attenuation of metal mobility and toxicity in soils. Among those used to treat heavy metal contaminated soils are municipal solid waste, compost, cattle manure, sewage sludge, red mud, lime and beringite, zeolites, charcoal coal, and biochar. However, it is important to consider the effects of these amendments on the environment, such as the incorporation of new pollutants by the use of municipal waste. Moreover, currently there is a lack of information on emissions of greenhouse gases (GHG) that these amendments may generate, which is very important to consider when evaluating the cost benefits of applying a soil amendment. Thus, in recent years some studies have been performed in relation to the use of an effective amendment such as biochar, which is the incomplete pyrolysis of the biomass, with the characteristics of biochar depending on other factors such as the biomass used and the physicochemical characteristics of the production process. The original aim of the use of biochar was to obtain C sequestration in soils, due to its recalcitrant characteristics. However, numerous other potential applications have been recently reported as a result of its effects on soils, such as liming of acidic soils (increase pH) and increasing the cation exchange capacity. Moreover, these features can decrease the heavy metal availability of soils.
Other studies have evaluated the potential effects of the amendment of biochar to soils and GHG emissions, and have reported a net decrease of these emissions by reducing the availability of N for nitrification and denitrification through adsorption (microbial or physical). However, few studies have been performed about the evolution of metal bioavailability with the aging of biochar.
Considering the above mentioned findings, we conducted preliminary studies with the purpose of assessing different biochar (BiC) amendments in Pb polluted soils with respect to the bioavailability of the metal and food security, and evaluating the effects on the N cycle and potential GHG emissions. Our first study was performed using various contaminated Pb soils from Córdoba according to a pollution gradient, which were amended with two different quality biochars using various woods as the biomass and in the pyrolysis process, with the effect of the biochar amendment in polluted soils being evaluated on the amonification and nitrification rates. These results indicated a direct relationship between the amendment contents in soils and the water retention capacity (WHC), which was dependent on hydrophobicity, surface area and improvement of the soil structure. Furthermore, for the purpose of assessing the ammonification and nitrification gross rate, we analyzed the content of NH4+, NO3-, TNb and TOC extractables of amendment soils. Our partial results reveal a direct relationship between Pb content in soils and extractable nitrogen, especially nitrates, as well as a direct relation with the content of soil organic matter. Thus, in soils contaminated with metals where phytoremediation has been applied, some studies have employed nitrogen fertilizers such as urea and ammonium nitrate in order to provide nutrients to the hyperaccumulator plants in addition to the fact that they can accumulate heavy metals through soil acidification and a greater bioavailability of metals.
As mentioned above, the incorporation of BiC in Pb contaminated soils reduces the bioavailability of this metal, which is reflected in the amount of total extractable nitrate. Consequently, in the second phase of these studies, we evaluated the effect of an amendment of organic carbon (charcoal) on the bioavailability of Pb in soils and assessed bioaccumulation in soybean, as well as GHG emissions. Especially in the case of N2O, we observed an increase of its emissions in soils with a natural content of Pb without amendment and cultivated with soybean at the maturity growth stage, which was the result of the senescence process that increased the organic matter on decomposition. Furthermore, our results indicated that the application of this charcoal to the soil was particularly toxic for the plant at a 10% W/W amendment concentration. Finally, the soils amended with 5% charcoal reduced N2O emissions in comparison with soils without an amendment for both lead polluted (700 ppm) and natural soils.
Therefore, we conclude that the N cycle in soils with an agricultural history is modified in the presence of elevated levels of Pb, and that the immobilization efficiency of Pb after an amendment depends on characteristics such as biomass and the pyrolysis process, as well as on soil processes such as ammonification and net nitrification, and ultimately, the potential N2O emissions.
1Pollution and Bioindicator Section, Multidisciplinary Institute of Plant Biology,
National University of Córdoba, Córdoba,