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## Introduction

The term “heavy metals” has been used to describe a group of metals which have been linked to contamination and toxicity (Duffus 2002). Chemically, heavy metals are defined as metallic elements with a density of ≥ 5 g/ cm3 (Schulze et al. 2005). Elements which fall into this category include Ag, Ar, Au, Bi, Cd, Co, Cr, Cu, Fe, Hg, Mn, Mo, Ni, No, Pb, Pt, Sb, Ti, Tl, U, V, Zn and Zr (Schulze et al. 2005). Some heavy metals are essential in plant nutrition as micronutrients (Helal et al. 1990) but plants growing in a polluted environment can accumulate heavy metals at high concentrations (Voutsa et al. 1996, Schulze et al. 2005). Accumulation of heavy metals in agricultural soils has become a major concern for food crop production (Cieslinski et al. 1996) as they may cause a serious health hazard as they travel through the food chain unaltered (Bharti et al. 2001) as they are not biodegradable and have long biological half- lives (Jarup 2003).

## Heavy metals

### Sources of heavy metals

Soil, air and both organic and inorganic fertilizers are the main sources of heavy metals to plants (Martensson 1992) from which heavy metals are taken up by the root or leaves (Voutsa et al. 1996). Uptake of heavy metals by roots depends on soil and plant factors such as soil pH, organic matter, plant species, plant age (Voutsa et al. 1996). The concentration ranges of deficiency, optimal supply and toxicity for essential heavy metals as Zn and Cu are very close together (Schulze et al. 2005). Soil metal contamination has increased significantly in the previous century due to rapid industrialization including mining (Dudka et al. 1997). The surplus of heavy metals in soils is caused by the use of fertilizers, pesticides and sewage sludges, or by industrial activities (Gimeno-Gracia et al.1996). Elevated levels of metals in soil may lead to increased uptake by plants (Voutsa et al. 1996). The heavy metal distribution in soils and sediments can indicate the potential harm to the environment through the chemical associations (Mulligan et al. 2001) as a build up of heavy metals at high concentrations can cause serious risk to human health when food plants are consumed (Voutsa et al. 1996).

### Toxicology of heavy metals

Heavy metals are of great environmental concern due to their toxicity and cumulative behaviour (Yusuf et al. 2002). Heavy metals such as copper and zinc are necessary for plant and human nutrition, and small amounts are required whereas other metals such as cadmium and lead are not

needed. However, excessive amounts of any of the heavy metals can generate toxic effects (Voutsa et al. 1996).

Lead and cadmium are among the most abundant heavy metals and are particularly toxic (Yusuf et al. 2002). The extreme content of these metals in food is associated with aetiology of a range of diseases, especially with cardiovascular, kidney, nervous and bone diseases (Jarup 2003).

Heavy metals are also implicated in causing carcinogenesis, mutagenesis and teratogenesis (Yusuf et al. 2002).

### Effects of heavy metals on plants

Most heavy metals are not necessary for plant growth and metabolism, yet they are often readily taken up and accumulated by plants (Bharti et al. 2001). Heavy metals have shown to reduce the “qualitative and quantitative productivity” of plants (Bharti et al. 2001). These metals have been reported to affect seed germination (Mukherji and Maitra 1976), seedling growth (Kumar et al. 1992), photosynthesis (Muthuchelian et al. 1988), nitrate assimilation (Chugh et al. 1992) and other metabolic processes (Stiborova et al. 1988) of plants. Other effects include chlorosis of leaves of plants and restricted yields of dry matter (Xian 1989). Roots proved more sensitive than the aerial parts, because of direct exposure to metals while translocation to the aerial parts is steady (Bharti et al. 2001). Cadmium, lead and copper have been thought to inhibit growth by affecting uptake of water, activity of hydrolytic enzymes and hydrolysis of storage macromolecules in endosperms or cotyledons, transfer of hydrolytic products to the embryonic axis, root and shoot, and resynthesis of essential macromolecules such as nucleic acids and

proteins (Bharti et al. 2001). The occurrence of heavy metals in certain chemical forms may have more effect on plant growth, than their concentration in soil (Xian 1989) yet too high metal concentrations in contaminated soils can end in less soil microbial activity and soil fertility and yield losses (McGrath 1998).

## Agriculture and Heavy Metals

Metals pose a problem in agricultural soils and crops as metals are elements and as such they do not breakdown but rather persist in the environment essentially forever (McGrath 1998, Jarup 2003). Even if only a small amount of a metal is added each year to a soil, its concentration will slowly increase over time. The only natural way that the total concentrations of a metal can decrease over time is physical removal from a site by processes such as erosion and leaching (Anderson 1993). Plants accumulate many metals and nutrients from the soil (Kachenko and Singh 2006). As concentrations of metals in soils increases, the uptake of metals into plants also increases (Muchuweti et al. 2006).

Although metals naturally occur in soils, heavy metals found in agricultural soils and crops are introduced from a number of different sources, some natural and some man-made (Kachenko and Singh 2006). Natural concentrations of metals in soils depend on the parent rock from which the soil originated and these are highly variable. In terms of metals in rain and irrigation water, very low concentrations are found in this medium. However, if sources are from sewage treatment plants, irrigation water should be monitored as it may be contaminated with metals (Moeletsi et al. 2004). Fertilizers are generally deliberately added in order to improve plant growth and yields, and these may contain high concentrations of cadmium and other non-essential metals (Martensson 1992). Cadmium occurs naturally with deposits of zinc and also phosphorus depending on the source of rock phosphate used in producing fertilizer.

## Heavy metals in vegetables

Commercial and residential vegetable growing areas are usually located in urban areas, and are subject to man-made contamination (Kachenko and Singh 2006). Both commercial and residential growing areas are subject to atmospheric pollution, in the form of metal containing aerosols (Kachenko and Singh 2006). These aerosols can enter the soil and be absorbed by vegetables, or otherwise be deposited on leaves and adsorbed (Kachenko and Singh 2006).

Excessive accumulation of heavy metals in agricultural soils may not only result in environmental contamination, but lead to elevated heavy metal uptake by crops, which may affect food quality safety (Muchuweti et al. 2006, Sharma and Chettri 2005, Sharma et al. 2007). Studies of vegetables grown in locations in close proximity to industrial areas have reported high levels of heavy metals (Kachenko and Singh 2006). Most plant species have a tendency to sequester metals in their roots, with only small amounts of metals being translocated to the aboveground parts (Yang et al. 2009). Fruit and root vegetables appear to be low accumulators of cadmium in their edible parts, whereas leafy vegetables tend to accumulate more cadmium in leaves (Yang et al. 2009). A number of factors influence the concentration of heavy metals on and within plants (Muchuweti et al. 2006). These factors include climate, atmospheric deposition, the nature of the soil on which the plant is grown and the degree of maturity of the plant at the time of harvesting (Scott et al. 1996; Voutsa et al. 1996; Lake 1984). The soil is one of the most important factors in determining the heavy metal content of food plants (Itanna 2002, Madyiwa et al. 2002). Heavy metal contamination of agricultural soils can pose long-term environmental problems and is not without health implications (Sauve et al. 1996; Ferguson 1990; Chumbley 1982).

## Tolerance to heavy metals

There are two basic strategies by which plants react to high concentrations of heavy metals in the environment: exclusion mechanisms, whereby plants avoid too much uptake and transport of metals and the other – accumulation and sequestration mechanisms, whereby large amounts of metals are taken up and transported to the plant shoots (Baker 1981). There are two groups of plants evolved to tolerate heavy metals, namely chemoecotypes and metallophytes. These plants may serve as indicator plants for heavy metals (Larcher 2001) as concentrations of heavy metals in plants have been used to measure pollution (Leavitt et al. 1979). Chemoecotypes display characteristic patterns of isoenzymes (Larcher 2001). These plants show element-specific increases in the ability of the protoplasm to resist the high concentrations of heavy metals in tissues when growing on soils rich in these elements (Larcher 2001). The greater the exposure to a certain element, the more tolerance is adopted toward the element (Larcher 2001). These are taxa with a high degree of genetic plasticity from which a number of specialized ecotypes evolved that are resistant to a number of heavy metals (Larcher 2001). Metallophytes take up large amounts of heavy ions and store them (Larcher 2001). Non-resistant plants may also collect certain elements (Larcher 2001). There are also hyperaccumulators i.e. plants that have very high concentrations of heavy metals (Larcher 2001). These plants are capable of accumulating more than 100 times greater concentrations of metals than normal plants (Brooks et al. 1997). Heavy metal ions can be extracted from the harvested biomass of these plants (Larcher 2001). In some species this tolerance is limited to a particular heavy metal, in other species co-tolerance to numerous heavy metals exists (Cox and Hutchinson 1979). These plants have also developed a

range of avoidance mechanisms by which the surplus of heavy metals can be rendered harmless, these mechanisms include:

1)       immobilization of toxic ions in the cell walls

2)       slowing down of permeation across boundary layers of the protoplasm

3)       chelation in the cytoplasm

4)       compartmentalization and complex formation with organic and inorganic acids, phenol derivatives and glycosides in the vacuole (Marschner 1986) Plants may also produce peptides called phytochelatins which attach naturally and detoxify toxic metals such as lead, mercury and cadmium (Spiro 2003).

## Monitoring of Heavy Metals

Heavy metals are naturally present at low concentrations in agricultural soils (Korkmaz et al. 2010). A number of factors contribute to heavy metal contamination of agricultural soils including industrial and traffic emission, atmospheric deposition from town wastes, using metal- containing agricultural expedients and metal production (Alloway and Jackson 1991, Korkmaz et al. 2010). Heavy metal ions in contaminated soils may easily enter the human food chain through crop plants (Korkmaz et al. 2010).

Once heavy metals are accumulated as contaminants, they can neither be destroyed nor can they be altered by chemically or physically, and are spread in the ecosystems (Sharma and Chettri 2005). Plants tolerate heavy metals either by detoxification mechanism or accumulation in different plant parts or cell organelles (Sharma and Chettri 2005). Some plants have the ability to absorb and accumulate heavy metals, which makes them valuable as indicators of environmental pollution (Buszewski et al. 2000) and therefore provide an understanding of the bioavailability and mobilization of heavy metals (Murphy et al. 2000). However, few studies have been done to investigate plants and their role as biomarkers to identify metal mobility for continuous monitoring purposes (Murphy et al. 2000).

Most common methods of assessing metal toxicity to plants from soil:

(1)   monitoring the presence or absence of specific plant ecotypes and/or plant species (indicator plants)

(2)   measurements of metal concentration in tissues of selected species (accumulative bioindicators)

(3)   recording of physiological and biochemical responses (biomarkers) in sensitive bioindicators (Buszewski et al. 2000).

Cadmium is one of the most toxic pollutants found in air, water and soil (Dixit et al. 2000) and is not essential for humans, animals and plants. It enters the environment mainly from industrial processes and phosphate fertilizers and then is transferred to the food chain (Sandalio et al. 2001). It is known to be easily taken up by plants and translocated within the plant (John et al. 1972). Once entered, cadmium accumulates immediately in roots, later in the stem and leaves (Dixit et al. 2000). About 75 % of cadmium entering the plant is in one way or another bound in the root system (Jastrow and Koeppe 1980, Krupa 1999). Up to 11 % of the total cadmium content in plants can be founding stems and about 15 %, depending on plant species and the ability to detoxicate this heavy metal, enters the leaves (Jastrow and Koeppe 1980). In terms of cadmium accumulation within mesophyll cells, 48 % is in the cell wall, 39 % in the cytoplasm and vacuole and 13 % in chloroplasts and mitochondria (Ernst 1980). Cadmium produces alterations in the functionality of membranes by inducing changes in lipid composition and by affecting the enzymatic activities associated with membranes (Sandalio et al. 2001).

Cadmium toxicity is also correlated with disturbances in the uptake and distribution of macro and micronutrients in plants (Sandalio et al. 2001). It interacts with the uptake of essential nutritional elements for example, iron, calcium, potassium, magnesium and manganese (Krupa 1999). Cadmium is strongly phytotoxic and causes growth inhibition and even plant death (Sandalio et al. 2001). Cadmium also initiates senescence in plants (Krupa 1999). Leaf chlorosis is the most visible symptom of cadmium toxicity, as cadmium inhibits chlorophyll synthesis and interacts with iron (Krupa 1999). Photosynthesis is also sensitive to cadmium (Sandalio et al.

2001). Cadmium interacts with photosynthetic, respiratory and nitrogen metabolism in plants and

produces oxidative stress by producing free radicals and active oxygen species, resulting in poor growth and low biomass accumulation (Dixit et al. 2000). Increasing the concentration of cadmium produced a significant growth inhibition of pea plants which was accompanied by a significant decrease in the photosynthesis rate (Sandalio et al. 2001) and causes a decrease in biomass (Dixit et al. 2000). Once plants are exposed to cadmium, a variety of detoxification processes are triggered in the cells, including complexing of the metal by phytochelatins, compartmentalization in vacuoles, immobilization at the level of cell wall, exclusion through the action of plasma membrane, and production of stress proteins play very major roles (Dixit et al. 2000).

2005). When lead enters the plant root, it encounters the neutral pH, high phosphate and high carbonate environment of the intercellular spaces (Li Li et al. 2008) which would result in it being immobilized.

## Heavy Metal Pollution in South Africa

South Africa has a high concentration of industrial and mining activity. Studies of vegetables grown in locations close to industrial and mining industries have reported elevated levels of heavy metals (Kachenko and Singh 2006). Poor monitoring and control of safe disposal of waste means that industrial waste is illegally dumped in urban areas, causing health risks to communities and environments (Whyte 1995). The deposition of processed and unprocessed waste materials has led to continuous, persistent leaching of dissolved metals into soil and water systems (Naicker et al. 2003; Roychoudury and Starke 2006). Numerous reports have indicated heavy metal contamination of South African rivers and soils (Abbu et al. 2000; Binning and Baird 2001; Okonkwo and Mothiba 2005). There is also clear evidence of heavy metal contamination in some vegetable farming areas (Meerkotter 2003, 2012; Sogayiso 2003).

## Aims and Objectives

The aim of this study is to investigate the heavy metals namely cadmium and lead which have shown to have a negative effect on vegetable farming in Cape Town (Meerkotter 2003, 2012; Sogayiso 2003).

### Research Objectives

The main objective of the study is to examine the effect these metals have on the growth and chemical composition of Bahama and St.Augustine grass.

### Research Questions

1. Do heavy metals accumulate in Bahama and St.Augustine grass ?
2. Can phosphate and EDTA mitigate the effects of Pb and Cd on the growth and nutrient content of Bahama and St.Augustine grass?
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