Essential metal and metalloid elements in the Philippi Horticultural area, and their uptake into selected vegetable crops.

This study evaluated Co, Cr, Mn, Ni, Se, Sn and V status in the soils of the PHA, as well as the vegetables produced on these soils. We also determined the agronomic sources of these elements to the soils in the PHA. Farmyard manures applied as fertilizer amendments to the soils in the PHA were found to be the major agronomic sources of the metal and metalloid elements. These elements were however, retained in significantly higher concentrations in the soils compared to the concentrations found in the edible portions of the vegetable crops collected. This, in turn, resulted in these vegetables being poor sources of several of the essential mineral nutrients. It is therefore suggested that: (1) a wider variety of crops are assessed for their mineral nutrient status, (2) to find ways to increase the availability of these mineral nutrients and (3), that the possibilities of micronutrient and trace element deficiencies be assessed in the communities surrounding the PHA.

heavy metals; hidden hunger; nutrient deficiencies; selenium; trace elements

Mineral nutrient deficiencies are a global problem, but it is usually more prevalent in low-income areas in developing countries where human diets are usually highly monotonous and primarily cereal and/or tuber based (White and Broadley [38] , White and Brown [39] ; Zhao and Shewry [41] ; Bouis and Islam [3] ; Labadarios et al. [19] ; [19] ; FAO, WTP, IFAD [11] ; FAO, WTP, IFAD [12] ). Within these areas, plant based foods contribute significantly to the nutritional food security of the surrounding communities (Faber and Wenhold [13] ; Steyn et al. [32] ; Temple and Steyn [33] ; Temple and Steyn [34] ; Temple et al. [35] ; Wolfhard [40] ; Malan et al. [23] ; Faber et al. [14] ). Human beings however, generally require more than 25 mineral nutrients, while only 17 have been shown to be metabolically essential to the growth and development of the plant foods that we consume (White and Broadley [38] , White and Brown [39] ; Hopkins and Hüner [16] ). Several, but not all, of the mineral nutrients lacking from human diets are therefore, those mineral nutrients that are not deemed metabolically essential to plant growth and development. This is because these mineral nutrients are only exceptionally added to commercial fertilizers (Eurola et al. [10] ; Hartikainen [15] ; Johnsson [17] ; Legard [20] ; Broadley et al. [5] ), and therefore, through continual cropping, could easily become depleted from agricultural soils, and the crops grown on these soils. These elements include chromium (Cr), cobalt (Co), fluoride (F), iodine (I), selenium (Se), silicon (Si), tin (Sn) and vanadium (V) (White and Broadley [38] , White and Brown [39] ).

The Philippi horticultural area (PHA) in the Western Cape Province of South Africa (Figure 1) is one of the major fresh produce suppliers in the Cape Town area of South Africa (Battersby-Lennard and Haysom [2] ). The all year round continuous vegetable production taking place in the PHA makes it a major source of fresh produce to the surrounding communities which are often faced with moderate to high levels of food insecurity (Temple and Steyn [33] ; Battersby-Lennard and Haysom [2] ). Within the PHA, mineral nutrients that have been mined from the agricultural soils due to continuous cropping are usually replaced by the addition of farmyard manures as fertilizer amendments to the soil or, in certain areas, with the aid of chemical fertilizer applications (Malan et al. [22] ). These farmyard manures used in the PHA however, have been shown to result in high concentrations of potentially toxic heavy metals in the soils and sometimes also in the fresh produce grown on those soils (Malan et al. [22] ; Malan et al. [23] ). No information is however, currently available regarding the contribution that these soil amendments make to the concentrations of metal and metalloid elements, deemed essential to humans, in the fresh produce grown in the PHA. This work therefore, assesses the concentrations of chromium (Cr), selenium (Se), vanadium (V), manganese (Mn), nickel (Ni) and tin (Sn), elements generally deemed essential to humans, but not to the plant foods that we eat, in the soils, irrigation water, fertilizer amendments (chemical and organic) and fresh produce in the PHA.

Soil, water, agro-chemicals and vegetable samples were collected from 34 sampling locations from farms in the PHA. Water samples were collected from the irrigation ponds, and soil and vegetable samples were collected from the cropping sites adjacent to the irrigation ponds. The soil samples were only collected to a depth of 15 cm and herbicides, pesticides, fungicides, and nutrient solutions (grouped as crop sprays), as well as the manure samples, were collected based on their availability at each of the locations. After collection, all vegetable samples were oven dried at 80°C until a constant mass was achieved. Soil and manure samples were air dried at room temperature, after which the soils were sieved through a 2 mm mesh size sieve. After drying, all vegetable and manure samples were milled and ashed at 450°C. Heavy metals were leached from 5 g of the soil samples using 20 ml of 0.1 M HCl solution, and the leachate filtered. Water and crop spray samples were filtered and acidified (pH ± 2) using approximately 1-2 ml of 32% hydrochloric acid (HCl). Thereafter, all samples were analysed for Co, Cr, Mn, Ni, Se, Sn and V using a Varian Vista Mega Pixel Detector Inductively Coupled Plasma Optical Emission Spectrophotometer (MPXICP-OES), and tested against certified standards. The statistical package for the social sciences version 22 (SPSS Inc., Chicago IL) was then used to test the data for normality using a Shapiro-Wilk test, after which a Kruskal-Wallis analyses was performed to determine whether there were statistically significant differences (p ≥ 0.05) between the mineral nutrient concentrations between the fertilizer amendments, irrigation water, soils and vegetables. After nutrient determination, the amount of each of the mineral nutrients was calculated for one portion of 40 g fresh mass for each crop species collected. This was used to determine the percentage contribution that one portion of the crops would make to the dietary reference intake or upper tolerable limits of each of the mineral nutrients (National Academic Pres: Daily Recommended Intakes (DRIs)).

The major agronomic source of the target mineral nutrients to the agricultural soils in the PHA was found to be the farmyard manures used as fertilizer amendments (Table 1). The use of organic amendments such as farmyard manures have been well documented as sources of heavy metals to agricultural soils (Malan et al. [22] ; Verkleji [36] ; Nicholson et al. [26] ). Of the two types of manures used in the PHA, ‘kraal manure’, a combination of pig and cattle manure, was found to contain higher concentrations of Cr (56.01 ± 0.14), V (2.98 ± 0.79) and Ni (44.30 ± 13.02) than the poultry manure (Cr (10.73 ± 2.42), V (1.18 ± 0.08) and Ni (12.20 ± 1.68) (Table 1). Animal manure fertilizers are known to be significant sources of certain trace elements and micronutrients. This is because these mineral nutrients are essential to the farm animals and therefore, are usually added to animal feeds to reduce the occurrence of mineral deficiencies in the livestock (Sager [31] ; Luo et al. [21] ; Sahin et al. [30] ). The metal and metalloid contents of manures therefore, are largely a reflection of the concentrations of these elements found in the feeds that are consumed by the livestock, and subsequently, the excess amounts excreted by the livestock (Nicholson et al. [27] ).

Concentrations of essential mineral nutrients in manure, crop spray and irrigation water collected from the Philippi Horticultural area. Concentrations with the same letters are not statistically different from one another (p ≥ 0.05).

Although relatively high concentrations of these mineral nutrients were supplied to the agricultural soils by the addition of the farmyard manures, the majority of these mineral nutrients were found to be retained in the soil, and were not taken up and incorporated into the plant tissues. This resulted in the target mineral nutrient concentrations in the soils to be significantly higher than the concentrations thereof found in the edible portions of the crops grown on the soils (Table 2). The bioavailability of metal and metalloid elements are usually affected by several soil characteristics such as soil pH, cation exchange capacity, redox potential, texture, clay content and the amount of organic matter in the soil (Hopkins and Hüner [16] ; Prasad [29] ; Dhillon et al. [8] ; Ajwa et al. [1] ). Due to the addition of the farmyard manures to the agricultural soils in the PHA, a significant amount of organic matter is added to the soils with each manure application. This, in turn, could lead to these mineral nutrients binding to the increased organic acids in the soils, which subsequently, renders them immobilized. High concentrations of metals in soils is toxic to soil microbes that are generally tasked with improving the bioavailability of mineral nutrients in the soil (Bruins et al. [6] ). Consequently, without or, with reduced microbial activity, the residence time of the elements in the soil increases, but their bioavailability to the plants grown on these soils decreases (Prasad [29] ). Similar results were observed by other researchers. Ajwa et al. ([1] ) for instance, showed that the addition of farmyard manures to selenite treated soils resulted in reduced selenium accumulation in the leaves of canola plants grown on these soils. Øgaard et al. ([28] ) showed that the addition of cattle manure in combination with selenite reduced the absorption of the selenite from the soil by plants by increasing the retention thereof by the soils. Malan et al. ([22] ) found that the heavy metals assessed in their study, were also retained in significantly higher concentrations in the soil, than what was being taken up by the crops grown on the soils.

Mineral nutrient concentrations in the soil and vegetables collected from the Philippi Horticultural area. Concentrations with the same letters are not statistically significantly different from one another (p ≥ 0.05).

Percentage contribution that the fresh produce grown in the PHA makes to the daily-recommended intakes (DRIs) or tolerable upper limits (TULs) of several mineral nutrients.

nd = not determined.

The mineral nutrient concentrations of the vegetables collected from the PHA were assessed against the dietary reference intakes (DRI) or tolerable upper limits (TUL) of the mineral nutrients (National Academic Pres: Daily Recommended Intakes (DRIs)). From this work, it was found that the concentrations of certain of the mineral nutrients studied in the edible portions of the vegetable crops, contributed less than 1% of the DRI, while it contributed up to 28% of certain other mineral nutrients (Table 3). Of particular concern are the low concentrations of Se in the vegetable crops. It is estimated that more than 15% of the worlds' population is selenium deficient (White and Broadley [38] ), where deficiencies have been found to result in increased susceptibility to infectious diseases due to its role in enhancing immunocompetence (Hartikainen [15] ; Brown and Arthur [4] ; Combs [7] ; Ellis and Salt [9] ; Navarro-Alarcon and Cabrera-Vique [25] ). From the findings of the current study (Table 3), it is clear that pregnant and lactating females would be affected more severely by the low contributions that the fresh produce make to the DRI of each of the mineral nutrients. In this category, the fresh produce contributed less 10% of all mineral elements assessed of the DRI for lactating and pregnant females, and less than 1% of the DRI of Se. This result is worrying when one takes into consideration the important role that the PHA plays in providing food security to the communities surrounding it (Battersby-Lennard and Haysom [2] ).

It is suggested that further research is conducted in the PHA. Firstly, it is important to assess the mineral nutrient quality of a wider variety of crops grown in the PHA. Secondly, ways in which to increase the bio-availability of the essential mineral nutrients to the crops needs to be evaluated. Careful consideration is however needed when attempting this point. This is because Malan et al. (Malan et al. [22] ; Malan et al. [23] ) have shown that high concentrations of potentially toxic heavy metals are also found in the soils of the PHA. These heavy metals, just like the essential mineral nutrients assessed in this study, are mostly contained in forms that are not freely available to be taken up by the crops. Therefore, increasing the bioavailability of these essential mineral nutrients could also result in the heavy metals becoming more available which, in turn, could result in excessive uptake of these toxic elements by the vegetable crops. Also, the essential mineral nutrients assessed in this study, are only needed in trace amounts by humans. Excessive uptake and accumulation of these elements in the vegetables could potentially lead to toxicities. Lastly, it is important to assess the possibility of mineral nutrient deficiencies in the communities surrounding the PHA.

The manuscript entitled: Essential metal and metalloid elements in the Philippi Horticultural area, and their uptake into selected vegetable crops authored by Marÿke Malan, Francuois Müller, Lincoln Raitt, Lilburne Cyster and Luc Brendonck contains original research and has not been submitted or published earlier in any journal and is not being considered for publication elsewhere. All authors have seen and approved the manuscript and have contributed significantly to the preparation of the paper. The research conducted in this study meets all applicable standards with regard to the ethics of experimentation and research integrity. No competing interests are at stake, and there is no conflict of interest with other people or organizations that could inappropriately influence or bias the content of the paper.

The authors would like to thank the farmers of the Philippi horticultural area for their support and co-operation as well as the VLIR-UOS programme “Dynamics of building a better society” for providing funding to conduct the research. The opinions expressed and conclusions arrived at, are however, those of the authors.

PHOTO (COLOR): Figure 1. Location of the Philippi study site in the Western Cape Province of South Africa.