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Fate of Persistent Organic Pollutants (Pops) in Soils and Their Effect on Food Safety
Rai S Kookana
CSIRO Land and Water, PMB 2, Glen Osmond, 5064, Australia
E-mail: Rai.Kookana@csiro.au, 2011-07-13

Abstract

Partitioning of POPs into different compartments of environment (soil, air, water, sediment) determine their environmental fate, transport, accumulation and impact on biota and food quality. Physico-chemical properties of soil and sediments, especially the content and the chemistry of organic carbon, have a major bearing on not only the sorption and accumulation of POPs but also their degradation and plant uptake. It is now well known that "black carbon (BC)" (partially combusted material such as soot and charcoal) which has a strong affinity for POPs is ubiquitous in soils and sediments. However, the role of soil and sediment organic carbon, especially of BC, has not been fully appreciated or accounted for in assessment of distribution and impact of POPs on food safety. This paper demonstrates the importance of the chemistry of organic carbon as a strong moderating factors for several processes governing the accumulation, distribution and plant uptake of POPs, namely, sorption-desorption, degradation and bioavailability to plants/microorganisms. Recognizing that, as a response to climate change, biochar amendments of soils is attracting increasing interest globally and "black is seen as a new green", the paper highlights the need for better understanding of the long term implications of BC in determining the fate and behaviour of POPs in soils and their potential impact on food safety. Key words: Soil organic matter, black carbon, partitioning, plant uptake, food safety, bioavailability, POPs.

Key words: Soil organic matter, black carbon, partitioning, plant uptake, food safety, bioavailability, POPs

Abbreviations: BC, black carbon; HCB, hexachlorobenzene; HCH, hexachlorocyclo- hexane; Koc, organic carbon normalised sorption coefficient; MIR, midinfrared spectroscopy; NMR, nuclear magnetic resonance spectro- scopy; OCDD, octachlorodibenzodioxin; PAH, polynuclear aromatic hydrocarbon, PCDD/Fs, dibenzo-p-dioxins and dibenzofurans; POPs, persistent organic pollutants; PCBs, polychlorinated biphenyls; SOC, soil/sediment organic carbon

Introduction

Persistent organic pollutants (POPs) produced and used in industrialized nations are a cause of great concern globally due to their persistent, bioaccumulative and toxic nature and their propensity to travel long distances to affect even remote, uninhabited parts of the globe. POPs have diverse physical-chemical properties and are released in the environment from varied sources. Based on their partitioning properties in different environmental compartments (e.g. air, water, soil) POPs have been classified by Wania (2006) as "swimmers" (e.g. HCHs), "single to multiple hoppers" (e.g. PCBs, organochlorine pesticides, chlorobenzenes) and "flyers" (emerging polar POPs such as perfluorinated octyl sulfonamides, Lohmann et al. 2007). Therefore, their partitioning properties play a crucial role in determining their environmental fate, transport, accumulation, impact on biota and food safety.

Soil has been identified as a one of the most important repositories for fluxes of POPs between soil and air and soil processes can have a large bearing on their future distribution patterns (Meijer et al. 2003, Sweetman et al. 2005, Lohmann et al. 2007). While the importance of soil biogeochemistry and the role of soil or sediment organic carbon (SOC) was recognized some thirty years ago (Kirckhoff et al. 1979), it is only in the last decade, SOC has been recognized as the key parameter governing spatial variability of POPs in soils (Cousins et al. 1999) and partitioning in the marine environment (Lohmann et al. 2005). However, most POP studies so far have not incorporated the complex biogeochemistry of SOC in terrestrial and aquatic ecosystems (Lohmann et al. 2007).

Lohmann et al. (2007) compared the predicted potential reservoirs of POPs with the measured data on soils. The predicted soil maximum reservoir capacities for POPs ranged from 60 ?N to 80?N, and were mainly a function of SOC content and temperature ( Fig. 1(1188)). However, the actual measurements by Meijer et al. (2003) showed the maximum soil concentrations at 60 ?N, but ranging from 50 ?N to 70 ?N, suggesting that other processes such as differences in sources and other biogeochemical and global dynamics were playing a role. Meijer et al., (2003) also highlighted the likelihood of a much retarded transport (grass-hopping of POPs) due to strong sorption to SOC than what has been taken into account in such predictions. Studies have shown that temperature and SOC are the drivers of the observed variability in the distribution of POPs.

Relationship of Fate and Distribution of Pops with Soil Organic Carbon

Due to their hydrophobic nature, most POPs have a strong affinity for SOC. Therefore, global surface soils have been recognized to serve as an important reservoir for POPs, representing an integration of several processes over a time scale of years to decades (Sweetman et al. 2005). A strong relationship between soil concentration and SOC is to be expected depending on the partitioning and degradation processes and the inherent properties of POPs. Meijer et al. (2002) using soils from a transect from the UK and Norway showed that PCB concentrations varied up to 4 orders of magnitude and SOC played an important role in their spatial distribution. Sweetman et al. (2005) further examined the data and found the strongest correlation between HCB concentrations in soil and the SOC, followed by PCB-52 ( Fig. 2(1271)). However, the correlation between OCDD with SOC was the weakest. HCB being the most volatile of the three, a near steady-state condition between air and SOC via recurring soil-air exchange was suggested as the mechanism. However, for octachlorodibenzodioxin (OCDD) the opposite was the likely scenario. Heywood et al 2006 also reported no correlation between SOC content and the sum of total or heavy PAH concentrations. A weak, but nonetheless significant (P < 0.05), positive correlation was found with the total light PAHs congeners. Wilcke and Amelung (2000) found a strong positive correlation between total PAH concentration and SOC content in soil from remote sites in North America. Notably the PAH profiles at these sites were dominated by lighter compounds. In all of the above studies, the partition coefficient determined the strength of the relationship.

Ren et al. (2007) assessed the distribution of PCBs load in 52 Chinese surface soils (0-20cm) collected from different regions and found a statistically significant but weaker (p <0.005) correlation with SOC ( Fig. 3(1228)). However, the correlation improved significantly (p <0.001) when the longitude was considered. They also noted a longitudinal fractionation of PCBs in Chinese background/ rural soil from east to west ( Fig. 3(1228)). Clearly, both the proximity of the source region and SOC determined the distribution of PCBs in this study. Recently Koblickova et al. 2008 reported a similar relation between spatial distribution of PCBs and SOC in soils from the Czech Republic.

Considering the importance of SOC in dynamics, distributions and long range transport of POPs, in recent years several workers have called for a greater understanding and accounting of role of SOC in fluxes, distributions and long range transport of organic contaminants (Lohmann et al. 2007, Scheringer, 2009, Koblickova et al. 2008).

The Role of Soil Organic Carbon Chemistry in Determining the Fate and Effects of Pops

Not only the content of SOC but its chemistry has a strong influence on the environmental fate and behaviour of POPs in soils and sediments. Soil organic matter consists of heterogeneous mix of organic materials often classified as an amorphous, gel-like "soft carbon" matrix or domain and a condensed, glasslike "hard carbon" matrix or domain (Weber et al. 1992), including altered and relatively unaltered aliphatic polymers, polysaccharides (e.g., cellulose), lignin and lignin degradation products, fats, proteins, pectines (Schumann 2006). Highly carbonaceous organic matter from partial combustion processes represents another important constituent of organic matter in soils and sediments. This includes chars, soots, and other highly carbonaceous material commonly termed as "black carbon" (Accardi-Dey and Gschwend, 2003). Black carbon (BC) fraction in soils and sediments can be as high as 45-50% of total organic carbon (Allen-King et al. 2002; Schmidt et al. 2002).

Highly carbonaceous BC acts like activated carbon and shows very high affinities for organic compounds including POPs (e.g. Ahmad et al 2001; Allen-King et al. 2002; Jonker and Koelmans, 2002). Studies on sorption of pesticides in soils have established a direct correlation between aromaticity of SOC and sorption coefficients of pesticides (Ahmad et al 2001, Ablemann et al. 2005). The relationship between partition coefficient of a pesticide and the aromaticity of SOC, as determined by a solid state C13 nuclear magnetic resonance (NMR), has been shown in Fig. 4(1161). Sorption of other organic compounds such as PAHs, chlorobenzenes and mono-ortho-polychlorinated biphenyls (PCBs) in soils and sediment has been reported to be up to 4 orders of magnitude higher than could be anticipated based on the compounds' hydrophobicities (Ahmad et al. 2001, Allen-King et al. 2002; Jonker and Koelman, 2002).

In recent years, it is increasingly being recognized that BC is a key vector for transport and partitioning of POPs in marine environment (Lohmann et al. 2005). In sediments also, BC has been found to be the major sorbent for hydrophobic and planar POPs (Gustafson et al.1997; Cornelissen et al. 2005). Armitage et al. 2008 assessed the aquatic fate of dibenzo-p-dioxins and dibenzofurans (PCDD/Fs) and made a comparison of model predictions with observed organic carbon normalized sediment-water partition coefficients (Koc) and dissolved water concentrations. They found that for estimation of Koc or dissolved water concentrations, the sorption models inclusive of black carbon provided greatly improved estimates compared to the amorphous carbon only model. In Fig. 5(1154), the typical log Koc values observed for different chemistries of organic carbon found in soils and sediments have been shown, highlighting that Koc values can vary by several orders of magnitude between humic acids and charcoal or BC in soils and sediments (Kleineidam et al. 1999). Furthermore, sorption on BC is generally highly non-linear (indicated by decreasing Freundlich exponent (n) with increase in aromaticity of SOC in Fig. 5(1154)) and has been found to be highly irreversible leading to strong sorption-desorption hysteresis and reduced bioavailability (e.g. Braida et al. 2002; Yu et al. 2006). Yu et al. (2006) assessed the sorption and desorption behaviour of a pesticide in soils that were amended with different types of biochars at different amounts. They observed that as the content of biochar (especially the one produced at higher temperature and with higher aromaticity) increased in the soil, the sorbed pesticide in soil became resistant to desorption, indicating effective sequestration of the sorbed residue by BC in soil ( Fig. 6(1149)). The implications of BC on persistence of organic compounds in soils and food safety are discussed in the following section.

Implications for Food Safety

Food safety of POPs is directly linked to the environmental fate and behaviour of POPs in soil which is strongly influenced by the content and chemistry of SOC. In addition to the effect on partitioning and accumulation of POPs, soil organic matter provides the substrate to support microbial activity and thereby plays a direct role in their persistence and degradation. However, for a contaminant to be degraded by microorganisms or to be taken up by plant, it needed to be released into soil solution or sediment pore waters, in other words, it needs to be "bioavailable". The organic matter in soil can influence the food safety of POPs through several direct and indirect ways, as described in the following:

  • 1. SOC content and chemistry determines the partition and extent of accumulation of POPs in soil, as described in the sections above;
  • 2. The release behaviour of POPs is related to SOC and its chemistry which determines its bioavailability in the environment;
  • 3. The flux or air-soil exchange of POPs depends on the strength of partitioning and accumulation of POPs in soils, which in turn depends on SOC, as discussed above. Furthermore, both the content as well as the chemistry of SOC can potentially affect direct deposition of the airborne POPs - an important pathway impacting food quality;
  • 4. Microbial population density or soil's ability to degrade an organic compound is often linked to SOC and thereby persistence of POPs depends on SOC. Also, the content and chemistry of SOC can determine the enantio-selective degradation of chiral POPs. Enantiomers are often used as tracers for sources in atmosphere of several POPs that are chiral in nature (Kurt-Karakus et al. 2005);
  • 5. For plant uptake, the residues of POPs bound to SOC need to be first mobilised into soil solution for it to be phytoavailable. Phytoavailability of POPs has been shown to be related to SOC, as discussed below.

Both extractability and bioavailability of POPs in soils depend on soil organic matter content and its chemistry. Tao et al. (2006) tested the hypotheses by assessing the extractability of polycyclic aromatic hydrocarbons (PAHs) by wheat roots (Triticum aestivum L.) from artificially contaminated soils in pot experiments. They added four PAHs (naphthalene, acenaphthylene, fluorene, and phenanthrene) to 20 Chinese surface soils containing varying amounts of SOCs. The apparent accumulation of PAHs by wheat roots was found to be positively and negatively correlated with dissolved organic matter and total organic matter, respectively. These results were explained on the basis that while total SOC reduced the extractability through sorption, the dissolved organic matter mobilised the sorbed PAHs and facilitated their availability to wheat roots, thus showing the contrasting role of the soil organic matter based on its chemistry.

The role of SOC chemistry on persistence and plant uptake of pesticide residue from contaminated soils was further demonstrated recently through a study by Yu et al. (2009). They amended soils with different amounts of two types of biochars (produced at different temperatures and representing different physico-chemical properties) and assessed the plant uptake of two pesticides (of differing hydrophobicities) in both above and below ground plant parts of spring onions (Allium cepa). They observed that the bioavailability of the two pesticides to microorganisms for degradation as well as for plant uptake decreased as the content of the BC in soil increased. Figure 7 shows that the persistence of carbofuran insecticide increased with increased BC content in soil (indicating reduced bioavailability to soil microorganisms), whereas the decreased plant uptake of two insecticides with increased BC contents by spring onions is shown in Fig. 8(1171).

The above studies highlight the importance of understanding the role of SOC and BC content and chemistry in the plant uptake and food safety of POPs in soil. In this era of climate change, this is becoming increasingly important for the prediction and management of POPs residues in contaminated soils. Let us explore this aspect further in the following section.

Management of Residues of Pops in Soils and Food Safety: A Climate Change Link

The foregoing discussion clearly demonstrates the importance of BC in sequestration of the organic contaminants in terrestrial and aquatic ecosystems and how this could have bearing on the accumulation of POPs in soils and their potential uptake by plants. The importance of biochar or BC in sequestration of carbon, reducing the emission of greenhouse gases and improving the soil fertility has led to International Biochar Initiative (www.biochar-international.org) promoting the biochar as a soil amendment which is increasingly attracting the attentions of policy makers in USA (Bracmort, 2009), Australia and elsewhere.

The presence of legacy POPs in agricultural soils and potential implications for food safety, especially plants belonging to the Cucurbita genera (Otani et al. 2007) has highlighted the need to manage agricultural soils as source of POPs and predict the extractability of residues by plants based on soil physico-chemical properties such as SOC (Tao et al. 2006). The link between food safety and physico-chemical properties of soils as demonstrated by several workers (Tao et al. 2006, Yu et al. 2009) means that alteration of the nature of the SOC pool would have implication for the strength of binding and potential extractability of the residues by plant roots. Therefore, predictive tools incorporating the role of SOC and BC need to be developed which could be used as a screening tools to identify soils with potential concern for food safety.

To study soil organic matter chemistry, solid state NMR has historically been employed as a gold-standard. However, the technique involves labour-intensive sample preparation steps limiting its broad scale applicability as a rapid screening tool. Recently, however, studies have shown that MIR spectroscopy can better predict sorption of organic contaminants in soils, by incorporating a range of soil physico-chemical properties such as SOC content, its chemistry, soil mineralogy and texture (Kookana, et al. 2008, Forouzangohar et al. 2008). MIR spectroscopy is a rapid assessment tool requiring less sample preparation and high throughput making it a cost-effective screening tool to incorporate soil physico-chemical properties in assessment of contaminant behaviour.

Assuming that the fraction of bound organic pollutants inaccessible to plant root may not be recovered from soil by certain mild chemical extraction, Tao et al. (2006) also explored the approach of using mild solvent extraction as a predictive or management tool for assessment of plant extractable pool of POPs in soil. They found that the water or n-hexane-extractable PAHs were positively correlated to dissolved organic matter fraction and negatively correlated to total organic matter, indicating mobilization and immobilization effects of the two different types of organic matter on soil PAHs, respectively. This, together with other approaches, such as a rapid assessment of soil organic carbon content and chemistry through MIR spectroscopy, may potentially provide a relatively rapid screening tool for identifying the problem soils and predicting the potential uptake of contaminants by plants.

In recent years substantial investment is being directed to conduct research on biochars in soils in USA, Australia and several other countries. "Black is now seen as a new green" as one of the articles in Nature (Marris, 2006) put it. Based on limited research cited in the above sections, biochar amendment can conceivably reduce the bioavailability of POPs on one hand but can potential serve as a source as well as a phase of accumulation of POPs and other organic contaminants on the other. The implication of biochar amendment to soil and potential implications for the environmental accumulation, distribution and food safety of POPs needs to be understood. The long term effect of biochar on the fate and behaviour of POPs deserves urgent attention both as a potential management tool as well as a factor affecting the distribution and global transport of POPs.

Conclusions

Physico-chemical properties of soil and sediments, especially the content and nature of BC, have a major bearing on not only the sorption and accumulation of POPs but also their degradation and plant uptake. BC is ubiquitous in soils and sediments and can make upto half of the total content of soil or sediment organic carbon mass. BC has a strong affinity for POPs and can accumulate and render the compound unavailable. However, the role of soil and sediment organic carbon, especially of BC, has not been fully appreciated in assessment of distribution and impact of POPs on food safety. As shown above, the chemistry of SOC as a strong moderating influence on a range of processes, namely, sorption-desorption, degradation, bioavailability to plants and soil microorganisms governing the accumulation, distribution and plant uptake of POPs. Since biochar amendments of soils is attracting increasing interest globally, in response to climate change, and "black is seen as a new green", there is an urgent need for better understanding of the long term implications of BC in determining the fate and behaviour of POPs in soils and their potential impact on food safety. Combination of rapid assessment tools such as MIR spectroscopy and mild solvent extractants for identifying problem soils for food safety can potentially be a useful management tool for food safety of plant products.

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Index of Images

Figure 1 Predicted Maximum Soil Reservoir Capacity of Pops in Top Soils and Surface Mixed Layer of Ocean in Comparison to That in the Atmosphere. Source Lohmann Et Al. 2007 Based on Dalla Valle Et Al. 2005.

Figure 1 Predicted Maximum Soil Reservoir Capacity of Pops in Top Soils and Surface Mixed Layer of Ocean in Comparison to That in the Atmosphere. Source Lohmann Et Al. 2007 Based on Dalla Valle Et Al. 2005.

Figure 2 Correlation between Soil Concentrations of Pops (HCB and PCB-52) and Soil Organic Carbon Contents. Source: Sweetman Et Al. 2005.

Figure 2 Correlation between Soil Concentrations of Pops (HCB and PCB-52) and Soil Organic Carbon Contents. Source: Sweetman Et Al. 2005.

Figure 3 Correlation of Total PCB Load in 52 Chinese Soils with Soil Organic Carbon (Upper) and with Organic Carbon and Location (Lower Panel). Source: Ren Et Al. 2007

Figure 3 Correlation of Total PCB Load in 52 Chinese Soils with Soil Organic Carbon (Upper) and with Organic Carbon and Location (Lower Panel). Source: Ren Et Al. 2007

Figure 4 Correlation between Chemistry of Soil Organic Carbon (Aromaticity Measured through Solid State NMR Spectroscopy) and Partition Coefficient of a Pesticide. Source: Ahmad Et Al. 2001.

Figure 4 Correlation between Chemistry of Soil Organic Carbon (Aromaticity Measured through Solid State NMR Spectroscopy) and Partition Coefficient of a Pesticide. Source: Ahmad Et Al. 2001.

Figure 5 Log Sorption Coefficients (Log Koc) for Different Chemistries of Organic Carbon Found in Terrestrial and Aquatic Ecosystems. Adapted from K Leineidam Et Al. 1999.

Figure 5 Log Sorption Coefficients (Log Koc) for Different Chemistries of Organic Carbon Found in Terrestrial and Aquatic Ecosystems. Adapted from K Leineidam Et Al. 1999.

Figure 6 Sorption Desorption Isotherms Demonstrating the Increased Sorption (and Its Non-Linearity) and Sorption-Desorption Hysteresis with Increase in Black Carbon Content of Soil (BC 850 Is Black Carbon Produced at 850oc). Source: Yu Et Al. 2006.

Figure 6 Sorption Desorption Isotherms Demonstrating the Increased Sorption (and Its Non-Linearity) and Sorption-Desorption Hysteresis with Increase in Black Carbon Content of Soil (BC 850 Is Black Carbon Produced at 850oc). Source: Yu Et Al. 2006.

Figure 7 Demonstration of Increased Persistence of Carbofuran Insecticide in Soil with Increase in Contents of Two Types of Black Carbon Content of Soil (BC450 and BC850 Are Two Wood Biochars Produced at 450o C and 8500C, Respectively). Source: Yu Et Al. 2009.

Figure 7 Demonstration of Increased Persistence of Carbofuran Insecticide in Soil with Increase in Contents of Two Types of Black Carbon Content of Soil (BC450 and BC850 Are Two Wood Biochars Produced at 450o C and 8500C, Respectively). Source: Yu Et Al. 2009.

Figure 8 Demonstration of Decreased Plant Uptake of Two Insecticides (Carbofuran _ Solid Bars and Chlorpyrifos _ Empty Bars) in Above- and under-Ground Plant Parts of Spring Onion with Increase in Contents of Two Types of Black Carbon Content of Soil (BC450 and BC850 Are Two Wood Biochars Produced at 4500C and 8500C, Respectively). Source: Yu Et Al. 2009.

Figure 8 Demonstration of Decreased Plant Uptake of Two Insecticides (Carbofuran _ Solid Bars and Chlorpyrifos _ Empty Bars) in Above- and under-Ground Plant Parts of Spring Onion with Increase in Contents of Two Types of Black Carbon Content of Soil (BC450 and BC850 Are Two Wood Biochars Produced at 4500C and 8500C, Respectively). Source: Yu Et Al. 2009.

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