Urban farming as a possible source of trace metals in human diets

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DOI: 10.17159/sajs.2016/20140444
Rapid industrialisation and urbanisation have greatly increased the concentrations of trace metals as pollutants in the urban environment. These pollutants (trace metals) are more likely to have an adverse effect on peri-urban agriculture which is now becoming a permanent feature of the landscape of many urban cities in the world. This review reports on the concentrations of trace metals in crops, including leafy vegetables harvested from different urban areas, thus highlighting the presence of trace metals in leafy vegetables. Various pathways of uptake of trace metals by leafy vegetables, such as the foliar and roots, and possible health risks associated with urban faming are discussed and various morphological and physiological impacts of trace metals in leafy vegetables are described. Defensive mechanisms and positive aspects of trace metals in plants are also highlighted. © 2016. The Author(s). Published under a Creative Commons Attribution Licence.
South African Journal of Science
Volume 112 | Number 1/2
January/February 2016
Review Article Pollution and farming
Page 1 of 6
© 2016. The Author(s).
Published under a Creative
Commons Attribution Licence.
Urban farming as a possible source of trace metals
in human diets
Joshua O. Olowoyo1
Gladness N. Lion1
1Department of Biology, Sefako
Makgatho Health Sciences
University, Pretoria, South Africa
Joshua Olowoyo
Department of Biology,
Sefako Makgatho Health
Sciences University, PO Box 60,
Medunsa 0204, South Africa
Received: 08 Dec. 2014
Revised: 08 Apr. 2015
Accepted: 16 June 2015
pollution; vegetables; soil;
human health
Olowoyo JO, Lion GN. Urban
farming as a possible source
of trace metals in human diets.
S Afr J Sci. 2016;112(1/2),
Art. #2014-0444, 6 pages.
Rapid industrialisation and urbanisation have greatly increased the concentrations of trace metals as
pollutants in the urban environment. These pollutants (trace metals) are more likely to have an adverse effect
on peri-urban agriculture which is now becoming a permanent feature of the landscape of many urban cities
in the world. This review reports on the concentrations of trace metals in crops, including leafy vegetables
harvested from different urban areas, thus highlighting the presence of trace metals in leafy vegetables.
Various pathways of uptake of trace metals by leafy vegetables, such as the foliar and roots, and possible
health risks associated with urban faming are discussed and various morphological and physiological
impacts of trace metals in leafy vegetables are described. Defensive mechanisms and positive aspects of
trace metals in plants are also highlighted.
Urban farming can be defined as the act of cultivating food crops, mostly vegetables, wherever land is available
around or in the immediate vicinity of a major city.1,2 Farming activities around urban areas have become a
prominent feature of some urban city landscapes, especially in developing countries.3 There are several reasons for
farming activities around peri-urban areas and these include easy access to markets and transportation of goods.
In some countries, poor urban households use urban farming to increase their household income by selling the
yield or surplus to reduce part of daily expenses.4 The other probable reason for the increase in urban farming is the
shortage of land. This involves farming areas previously used for either household or industrial waste,5 supported
by the notion that the soil will be very fertile. Urban farming also supports the campaign for organic farming.
Consumers, in most cases, evaluate quality of leafy vegetables on their dark green colour and on size of the leaves
as opposed to where farming activities have taken place.6 However, in urban city centres where farming activities
are carried out around industrial areas, safety around the consumption of these vegetables cannot be guaranteed
because various disposal practices often cause the accumulation of potentially toxic trace elements in the soil.7,8
Anthropogenic activities such as mining, emissions from vehicles, wrong agricultural practices and improper waste
disposal are major sources of trace metal pollution in the urban environment.5,9 It was recently discovered that a
large percentage of toxic trace metals find their way into the human diet through consumption of vegetables and
agricultural products.5-14
In acceptable limits, trace metals play an important role in the health and physiological activities of plants, animals
and humans.15 They are required in minute quantities as natural components of the environment. For example, zinc
is an essential element required in minute quantities in living organisms, but when supplied in high quantities, it
can be toxic to plants, producing purplish-red coloured leaves which is a symptom associated with phosphorus
deficiency. Zinc may also cause chlorosis in younger leaves which may extend to older leaves.16 In humans, excess
zinc may lead to metal poisoning and growth retardation. Excess nickel and lead may result in increased production
of reactive oxygen species and membrane permeability disruption in plants. In all, concentrations of heavy metals
above the required limits in plants are known to cause various deleterious effects on several plants systems such
as the photosynthetic ability of the plants, mineral uptake and interactions with the water regime from the soil. In
humans, excess lead may affect the functions of the liver and kidneys.10,17,18
The present review will establish, amongst others, the various pathways by which trace metals may be taken
up by plants, the effects of trace metals on the morphology and physiology of the plants, the positive aspects of
trace metals in plants and also the possible health risk for humans and livestock if trace metals are ingested in
high concentrations.
Evidence of trace metals in plants
High deposition and accumulation of trace metals in the edible part of root and leafy crops has been reported
in the literature.19,20 Vegetables are capable of accumulating trace metals from polluted soil and also from
surface deposition onto their shoots in polluted atmospheric environments.14 Trace metals in the air have been
reported to significantly influence total metal concentration of vegetable plants, especially when washing is not
thoroughly done.18
Atmospheric fallout is one of the chief contributors to heavy metal uptake by plants through the stomata. The
stomata openings are located on the surface of the plant leaves and perform multiple functions that include water
regulation in the plant. Particulate matter from atmospheric fallout may be found deposited on the leaf surface and
find a way into the leaves through the stomata. Smaller particles from atmospheric fallout may be incorporated into
the leaves, whereas large agglomerates are trapped on the surface wax.21,22 The extent of uptake and the pathways
involved may depend on the plant species and on the metal involved.23 The opening and closing of stomata may
provide entrance for trace metals, blocking the stomata in some cases and may ultimately lead to the death of
the plant.23 Entrance of metals via the foliage parts of plants was noted to be one of the major pathways by which
metals enter leaves in a polluted area.24 Figures 1 and 2 indicate the presence of trace metals around the stomata.
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In a separate study on lead uptake by lettuce leaves, it was discovered
that particulate matter deposited on plant leaves may be retained by
cuticular waxes and trichomes, while some of the metals contained
in particulate matter can penetrate inside plant tissues.26 Micro-X-
ray fluorescence, scanning electron microscopy coupled with energy
dispersive X-ray microanalysis, and time-of-flight secondary ion mass
spectrometry were used to investigate the localisation and the speciation
of lead in the leaves of different plants around a copper smelter
company and it was found out that lead-enriched particulate matter was
present on the surface of plant leaves.24 The study fur ther reported on
biogeochemical transformations on the leaf surfaces with the formation
of lead secondary species (PbCO3 and organic lead).
Toxicity of trace metals in plants
The effect of trace metals on the epidermis was demonstrated on the
young leaves of soyabean.26,27 The young leaves did not show visual
symptoms when exposed to cadmium ions and the authors observed
that cadmium ions did not have any effect on the closing and opening
of the stomata. However, findings have revealed that interactions
of cadmium ions with K+, Ca2+ and abscisic acid showed strong
interference with the guard cells.28,29 The application of cadmium on the
leaf surfaces influenced the number of stomata, decreasing the number
of stomata and stomatal openings on the leaf surface of the young
leaves of soybeans.27
Several authors have also reported on the adverse effect of lead in plants.
Lead toxicity is said to have a negative effect on biomass production
in plants as it affects chlorophyll biosynthesis and photosynthesis.30,31
Increased concentrations of lead may also inhibit or delay enzyme
activity changes in membrane permeability and water disturbance in
plants, which may affect the growth of the plant negatively.32
Cadmium may penetrate the root via cortical tissue and reach the xylem
through either the apoplastic or symplastic pathways possibly resulting
in cadmium toxicity in plants.33,34 Soil pH is known to influence cadmium
uptake and transportation. Uptake of cadmium by corn was lower in
acid soils with high organic matter content. Cadmium has also been
found co-accumulated with zinc in the aerial parts of Arabidopsis
halleri.35 Toxicity of nickel affected the seedlings of Pisum sativum by
changing the potassium uptake and water content,36 showing that higher
concentrations of nickel may lead to a reduction in plant growth, leading
to oxidative stress.
When leafy vegetables are properly washed, the concentrations
of chromium and lead may be reduced. However, the exogenous
contamination of leaves may not be reduced in some instances owing
to the nature of the vegetables, as was in the case with Gynandropsis
gynandra L. that showed a marked tendency to accumulate lead and
chromium.5 A similar observation was noted in a study by Gabrielli and
Sanità di Toppi37 where the dominant pathway for most trace elements
Figure 1: Presence of pollutants around the stomata of leaves collected for a study conducted in Pretoria, South Africa at (a) 2000X magnification and
(b) 3000X magnification.9 The stomata are the bean-shaped structures and the arrow is pointing to the pollutants around them.
Figure 2: Presence of pollutants around the stomata of leaves collected for a study conducted in Belgrade, Serbia.25 at (a) 648X magnification and (b) at
2400X magnification. The stomata are the bean-shaped structures and the arrow is pointing to pollutants around them.
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to vegetable roots was from the soil, while trace elements in vegetable
leaves appeared to originate mostly from the atmosphere. The result
further indicated that high accumulation of trace metals such as lead,
cadmium and chromium were the result of atmospheric deposition.
In all, it was evident that trace metals could reach the edible parts of
vegetables, especially the leafy parts, through atmospheric deposition
and could also be translocated to various parts of the plants via the
root system.
Trace metals uptake mechanism by plants
The process of uptake, translocation and bioaccumulation of trace
metals in plants could be influenced by a number of factors such as
climate, atmospheric deposition, the concentration of trace metals in
soil, the nature of the soil in which plants are grown (soil pH, soil organic
matter content and soil texture), the degree of maturity of the plants at
the time of harvest and the type of trace metals.15,37-39 Among crop types,
leafy vegetables such as lettuce and cabbage have the greatest ability
to take up trace elements from the soil.40 The mobility of trace metals in
soil is favoured mostly under acidic conditions. Treating soil with lime in
order to reduce soil acidity reduces the bioavailability of trace metals.41,42
Therefore, low pH levels are effective in the remediation of polluted soil,
while the soil organic matter ensures the availability of trace metals to
the plant.42 On the other hand, at high levels of soil pH, the formation
of soluble organometallic complexes may increase metal solubility
although this is not true for calcareous soil.43
An increase in the amount of soil organic matter helps plants minimise
trace metal absorption.44 The introduction of organic matter amendments
in conjunction with lime had been used to assist in immobilising trace
metals.45 However, the effects of organic matter on the bioavailability of
trace metals in soil depend on the nature of the organic matter, microbial
degradability, salt content, soil type and the particular heavy metal.46 In
most cases, metallic elements are actively retained by lands that are
rich in organic matter. The retention of trace metals in the soil affects the
mobility of these elements and interferes with the uptake process. The
bioavailability of trace metals is much lower in the presence of manure
when compared to humified compost, suggesting that different types
of organic matter may affect mobility of trace metals differently.47 This
may be as a result of the ability of the matter used to redistribute trace
metals from soluble and exchangeable forms to fractions associated
with organic matter or carbonates and the residual fraction.48
In the root area where the plant interacts with the soil, metal ions cannot
move freely across the cellular membranes. The membrane structure
of the plant root is lipophilic, which requires that the transport be
facilitated by proteins with transport functions.49,50 In the rhizosphere,
metal transport is carried out by two processes known as bulk flow
and diffusion.51,52 This process of uptake by plants is soon followed
by a process controlled by root pressure and leaf evaporation, called
transpiration. Through transpiration, the plant is able to absorb the trace
metals through the roots via the xylem to the shoot of the plant. The
process is dependent on water demand by the leaves in the aerial part
of the plant.49
Uptake of trace metals by higher or vascular plants is often through the
root system, but can also occur through the leaves. It may therefore
be difficult to distinguish whether the metals found in the plant tissues
were originally from the air or soil.53 Plants that are tolerant to high levels
of trace metals (also called hyperaccumulators) have the capacity to
remove contaminants from the soil. One example of such a plant is
Thlaspi caerulescens that has been used for phytoremediation of
soils, especially in areas previously polluted by mining activities.41 The
mechanism for hyperaccumulation remains unclear though it is generally
believed to invlove three major phases involving rapid uptake of metals
by the roots, high rate of translocation from roots to shoots and high
storage capacity by vascular compartmentalisation.41
Metal uptake by plants is affected by metal solubility and availability in
the soil. In a situation where the level of trace metals in soil is very high,
the release of root exudates and acidification are common mechanisms
that are used by plants to modify the root area to acquire nutrients from
the soil.41,49 In the case of nutrient movement across the biological
membrane, plants have developed a specific mechanism meditated
by proteins, for uptake, translocation and storage of the nutrients.42,49
Membrane transporters are equipped with a structure that binds ions
before transportation. This structure is receptive only to certain ions
and as such is specific in their mode of action49,54 The transmembrane
structure then facilitates the transfer of bound ions from extracellular
space through the hydrophobic environment of the membrane into the
cell. Despite the presence of this structure, only a fraction of the total
amount of ions associated with the roots are finally absorbed into plant
cells.54 The other form of metal uptake in plants, apart from binding to
the cell wall, is sequestration in cellular structures such as the vacuole,
though this may make the heavy metals unavailable for translocation to
the shoot.55
The evaporation of water from the leaves may also affect plant uptake
and accumulation of trace metals. The evaporation process serves as
a pump for more nutrients and other substances to be absorbed into
plant roots. This process, called evapotranspiration, moves water and
contaminants into the plants.42 The accumulation of metal contaminants
is mostly assisted by microorganisms, fungi and bacteria that live in
the root area. These microorganisms in the rhizosphere and closely
associated plants may contribute to the mobility of metal ions. At the
same time, plant roots release nutrients that sustain a rich microbial
community in the root area, thus establishing an important symbiotic
relationship between soil microorganisms and plants.42,49 In order
to facilitate the transport process, several families of proteins are
involved namely (1) influx transporter families such as zinc, a regulated
transporter, iron, a regulated transporter protein, yellow-stripe and
natural resistance associated macrophage protein and (2) efflux protein
families such as cation exchanger, ATB-binding cassette and cation
diffusion facilitator.42,56 Because these proteins are substrate specific, the
comparison between influx and efflux transporters revealed that efflux
proteins export metals from the cytoplasm while influx proteins take up
proteins from the soil or medium.56
Depending on their ability to adapt and reproduce in soils heavily
contaminated with trace metals, higher plant species can be divided into
two main groups. The two groups are the pseudometallophytes (plants
that grow on both contaminated and non-contaminated soil) and absolute
metallophytes (plants that grow only on metal contaminated and naturally
metal-rich soils).57 The use of Raphanus sativus (a pseudometallophyte)
for example, demonstrated the potential for root uptake in lead
contaminated soil.58 Baker58 showed that radish is a hyperaccumulator
plant that can concentrate trace metals in different plant parts. It was
also demonstrated that radishes are effective for remediation of polluted
soil through their potential to extract metals from soil up to a certain level
of concentration.58 The ability of plants to accumulate metals, thereby
remediating metals, is directly proportional to the presence or availability
of microorganisms in that plant’s rhizosphere.59 In the study it was
explained that microbial communities such as fungi, bacteria and other
microbes are capable of altering the soil environment and as a result will
translocate, absorb or sequester contaminants such as trace metals.59,60
Over the years, more than 400 plant species with the ability to take up
high levels of heavy metals in soil and water have been identified. Thlapsi
spp., Brassica spp., Sedum affredii and Arabidopsis spp., among
others, were studied.61,62 The use of vegetable plants has also been
demonstrated by some researchers.63 For example, Amaranthus dubius,
also known as morogo or wild spinach in South Africa, was found to have
the ability to take up and translocate metals such as chromium, mercury,
arsenic, lead, copper and nickel to the aerial parts of the plant.64 Some
medicinal plants such as Datura stramonium and Amaranthus spinosus
are capable of accumulating some trace metals in their tissues.60
It is believed that trace metals can help plants protect themselves from
diseases and biological stress.65,66 If a metal becomes more toxic to a
pathogen than to the plant, the metal can hamper the virulence of the
pathogen and can increase the resistance of the plant to the biotic
stress65 by suffocating the pathogen in the plant. The excess trace
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metals found in the plant after the pathogen has been suffocated will
then be redirected to normal growth.
The production of high levels of reactive oxygen species can adversely
affect the plant. Therefore, plants have developed a defensive mechanism
that involves glutathione in the detoxification of reactive oxygen species
through the ascorbate–glutathione cycle.67 During exposure to high levels
of trace metals, accumulated metal ions are detoxified by phytochelatins
that are produced from glutathione in the plant. These metal ions are then
bound to phytochelatins to form complex structures that are sequestered
or compartmentalised in the vacuole.,49,67
Exposure to trace elements such as mercury, cadmium, lead and nickel
in the soil, encourages the plants to formulate steps to counteract the
effects of these toxins. Defensive mechanisms largely prevent the metals
from getting inside the cells, but for metals that find a way into plants
cells, they are neutralised and sequestered.68
Quantifying human risk associated with trace
metals in plants
In a bid to quantify the likely health hazard associated with vegetables
that are high in concentrations of trace metals, the target hazard
quotient method (THQ) was developed and has been used by several
authors.69,70-72 Human health risks associated with these metals can
be assessed based on the THQ method,41 which takes into account
the concentration of trace metals in food, the frequency of exposure,
and the individual’s age, body weight and frequency of consumption
of the contaminated food. Should the THQ calculated for both adults
and children exceed 1 (THQ>1) then a potential risk to the consumer
will be suspected.5,14,41 Mercury was recorded as the major health
risk contributor in children and chromium as the least contributor. The
method for calculating the THQ is:
HQM = ADDM / RfDM, Equation 1
where ADDM = (DI x MFveg) / WB.14
ADDM is the average daily dose (mg.kg/day) of the metal and RfDM
is the reference dose (mg.kg/day). RfDM is defined as the maximum
tolerable daily intake of a specific metal that has no adverse effect.73 DI
is the daily intake of leafy vegetables (kg/day), MFveg denotes the trace
metal concentration in the vegetable tissues (mg/kg) and WB represents
the body weight of investigated individuals. The DI is usually calculated
at 0.182 kg/day for adults and 0.118 kg/day for children.14,74 The body
weight of investigated adults is assumed to be 55.7 kg and for children
14.2 kg.3,14 If the value of HQM calculated should exceed 1 (HQM>1),
then there may be potential risk to the consumer.
Trace metals are known for high mobility and bioavailability in consumed food
products such as vegetables. Studies have shown that trace metals may find
their way into the human system via the consumption of contaminated food
crops harvested from polluted soil. The urban environment is constantly
witnessing an increase in various developmental projects, with special
reference to developing countries. If not properly managed, these projects
may introduce contaminants, with special reference to trace metals, into the
environment. However, farming activities are continuously been practised
both on a small scale and a large scale around major cities and hence
may be affected negatively by these contaminants.71,75 Reports from the
literature have suggested that leafy vegetables are capable of accumulating
and storing these trace metals in their edible parts. There may be a serious
problem associated with urban agriculture relating to balancing demands
associated with increasing populations against potential hazards arising
from the use of contaminated urban sites for food production. It is necessary
to investigate and document the ability and uptake mechanism of most
vegetables in order to identify and document those that can grow without
accumulating trace metals in order to reduce the danger trace metals might
pose to consumers. It is also important to develop new farming practices
around urban city centres that will reduce or elucidate the availability and
uptake of trace metals by plants.
We thank the National Research Foundation (South Africa) for financial support.
Authors’ contributions
G.N.L. was responsible for the study under the supervision of J.O.O.
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