Journal of Environmental Biology J. Environ. BioI.

ISSN : 0254-8704 26 (2 suppl), 301-313 (2005)

http://www.geocities.com/Lenviron_biol/ Lenviron_biol @yahoo.com

Biological effects of heavy metals: An overview

Rajesh Kumar Sharma and Madhoolika Agrawal
Ecology Research Laboratory, Department of Botany
Banaras Hindu University, Varanasi - 221 005, India
(Received: 20 December, 2003 ; Accepted: 01 April, 2004)

Abstract: Heavy metals constitute a very heterogeneous group of elements widely varied in their chemical properties and biological functions.
Heavy metals are kept under environmental pollutant category due to their toxic effeqJ$" on plants, animals and human being. Heavy metal
contamination of soil results from anthropogenic as well as natural activitiei~'Anthropogenic activities such as mining, smelting operation and
agriculture have locally increased the levels of heavy metals such as Cd, Co, Cr, Pb, As and Ni in soil up to dangerous levels. Heavy metals
are persistent in nature, therefore get accumulated in soils and plants. Heavy metals interfere with physiological activities of plants such as
photosynthesis, gaseous exchange and nutrient absorption, and cause reductions in plant growth, dry matter accumulation and yield. Heavy
metals also interfere with the levels of antioxidants in plants, and reduce the nutritive value of the produce. Dietary intake of many heavy
metals through consumption of plants has long term detrimental effects on human health

Key words: Heavy metals, Sources, Effects, Plants, Human health

Introduction
The term 'heavy metal' although often not rigidly
defined is commonly held for those metals, which have
specific weights more than 5 g cm-3 (Holleman and Wiberg,
1985). There are about 40 elements that fall into this
category. Heavy metals are largely found in disperse form in
rock formations. Industrialization and urbanization have
increased the anthropogenic contribution of heavy metals in
biosphere. Heavy metals have largest availability in soil and
aquatic ecosystems and to a relatively smaller proportion in
atmosphere as particulate or vapours. Heavy metal toxicity 'to
plants vary with plant species, specific metal, concentra~ion,
chemical form, and soil composition and pH, as many heavy
metals are considered to be essential for plant growth.
Similarly many heavy metals are essential trace nutrients of
animals and human body (Wintz et al., 2002). Some of these
heavy metals like Cu and Zn serve either as cofactor and
activators of enzyme reactions e.g. informing
enzymes/substrate metal complex (Mildvan, 1970) or exert a
catalytic property such as prosthetic group in metalloproteins.
These essential trace metal nutrients take part in redox
reactions, electron transfer and structural functions in nucleic
acid metabolism. Some of heavy metal such as Cd, Hg and
As, etc are strongly poisonous to metal sensitive enzymes,
resulting in growth inhibition and death of organisms.
An alternative classification of metals based on their
coordination chemistry, categorizes heavy metals as class B
metals that come under non-essential trace
elements, which are highly toxic elements such as Hg, Ag,
Pb, Ni (Nieboer and Richardson, 1980). These heavy metals
are persistent and bioaccumulative, and do not readily break
down in the environment or not easily metabolized. Such
metals accumulate in ecological food chain through uptake at
primary producer level and then through consumption at
consumer levels. Plants are stationary and roots of a plant are
the primary contact site for heavy metal ions. In aquatic
systems, whole plant body is exposed to these ions. Heavy
metals are also adsorbed directly to the leaves due to
particles deposited on the foliar surfaces. Heavy metals enter
the human body either through inhalation or ingestion, which
is the main route of entry for general population. However,
urbanization and traffic, industrial and agricultural activities,
waste incineration and mining have significantly contributed to
\"the entry of heavy metals through inhalation in human body.
Heavy metals such as Cd, Ni, As and Cr pose a number of
hazards to humans. Heavy metals are also potent
carcinogens. Cadmium intake leads to itai- itai disease and
mercury intake leads to minimata disease. Other heavy
metals such as As causes poisoning due to drinking water
contamination.
This paper presents an overview of the research
information on sources and effects of heavy metals on plants.
Impact of heavy metals on human being is also s,ummarized.
Essentiality of heavy metals: Some of heavy metals (Fe, Cu
and Zn) are essential for plants and animals (Wintz et al.,
2002). The availability of heavy metals in
302
medium varies. The range of concentrations of different heavy
metals in soil and crops is given in Table 1. Some of these
heavy metals such as Cu, In, Fe, Mn, Mo, Ni and Co are
called micronutrients (Reeves and Baker, 2000), and are only
toxic when taken in excess of requirement (Monni et al.,
I2000;
I' Blaylock and Huang, 2000). The toxic limit and
recommended cor safe intake of heavy metals for human
health are given in Table 2. Heavy metals are also called as
trace elements due to their presence in trace (10 mg kg-1 or
1'1) or in ultra trace (1 ~ g kg-1 or 1-1) quantities in the
environmental matrices. The essential heavy metals (Cu, In,
Fe, Mn and Mo) play biochemical and physiological functions
in plants and animals. Two major functions of essential heavy
metals are: (a) Participation in redox reaction, and (b) Direct
participation, being an integral part of several enzymes.
Copper is an essential heavy metal for higher plants
and algae, particularly for photosynthesis (Ouzounidou et al.,
1992). Cu is a constituent of primary electron donor in
photosystem I, the copper protein plastocyanin. Because Cu
can readily gain and lose an electron, it is a cofactor of
oxidases, mono- and di oxygenase (e.g. amine oxidase,
ammonia monoxidase, ceruloplasmin, Iysyl oxidase) and of
enzymes involved in he elimination of superoxide radicals
(e.g. Superoxide dismutase and ascorbate oxidase). Several
enzymes contain In, such as carbonic anhydrase, alcohol
dehydrogenase, superoxide dismutase and RNA polymerase.
line is required to maintain the integrity of ribosome. It takes
part in the formation of carbohydrates, and catalyzes the
oxidation processes in plants. line also provides a structural
role in many transcription factors, and is a cofactor of RNA
polymerase.
Nickel is also recognized as an essential
micronutrient for living organisms. Nickel is a component of
the enzyme urease, and essential for its functioning and good
health in animals. Other heavy metals such as Molybdenum
are present in nitrate reductase. Mangnese plays an
important role in reactions of enzymes like malic
dehydrogenase and oxalosuccinic decarboxylase. It is also
needed for water splitting at photosystem II, and for
superoxide dismutase. In plants, Co complex is found in the
form of vitamin B12. Iron is an essential element in many
metabolic processes and is indispensable for all organisms. It
is a component of haem-containing protein such as
haemoglobin, myoglobin and cytochrome, and innumerable
non haem-iron containing proteins with vital functions in many
metabolic processes. Iron and Cu are
/
Rajesh Kumar Sharma and Madhoolika Agrawal
found as components of protein, and catalyses redox
reactions.
Sources of heavy metals: Heavy metal pollution can originate
from both natural and anthropogenic sources. Activities such
as mining and smelting operations and agriculture have
contaminated extensive areas of world such as Japan,
Indonesia and China mostly by heavy metals such as Cd, Cu
and In (Herawati et al., 2000), Cu, Cd and Pb in North Greece
(lantopoulos et al., 1999), in Albania (Shallari et al., 1998) and
Cr, Pb, Cu, Ni, In and Cd in Australia (Smith et al., 1996).
Heavy metals originate within the Earth's crust, hence their
natural occurrence in soil is simply a product of weathering
process.
(a) Natural sources of heavy metals: The most important
natural source of heavy metals is geologic parent material or
rock outcroppings. The composition and concentration of
heavy metals depend on the rock type and environmental
conditions, activating the weathering process. The geologic
plant materials generally have high concentrations of Cr, Mn,
Co, Ni, Cu, In, Cd, Sn, Hg and Pb. However, class wise the
heavy metal concentrations vary within the rocks (Table 3).
Soil formation takes place mostly from sedimentary rock, but
is only a small source of heavy metals, since it is not generally
or easily weathered. However, many igneous rocks such as
olivine, augite and hornblende contribute considerable
amounts of Mn, Co, Ni, Cu and In to the soils. Within the class
of sedimentary rocks, shale has highest concentrations of Cr,
Mn, Co, Ni, Cu, In, Cd, Sn, Hg and Pb followed by limestone
and than sandstone.
Volcanoes have been reported to emit high levels of
AI, In, Mn, Pb, Ni, Cu and Hg along with toxic and harmful
gases (Seaward and Richardson, 1990). Airborne emissions
of heavy metals originate from forest and prairie fires (Ross,
1994). Volatile heavy metals such Hg and Se are part of
carbonaceous matter produced during the fire. Wind dust,
which arises from desert region such as Sahara, has high
levels of Fe and lesser amounts of Mn, In, Cr, Ni and Pb
(Ross, 1994). Natural vegetation emits heavy metals into the
soil and atmosphere through leaching from leaves and stems,
decomposition and volatilization. Many heavy metals have
been detected in inland coastal areas due to seasprays and
aerosols produced in oceanic activities.
(b) Agricultural sources of heavy metals: The
inorganic and organic fertilizers are the most important
sources of heavy metals to agricultural soil include liming,
Biological effects of heavy metals: an overview 303

Table -1 : Heavy metal composition of typical uncontaminated soils and agricultural crops (Modified from Allaway, 1968).
Heavy metals Range in soil (ppm d. wt) Range in agricultural crops (ppm d. wt)
Cd 0.01-0.7 0.2-0.8
Co 1-40 0.05-0.5
Cr 5-3000 0.2-1.0
Cu 2-100 4-15
Fe 7000-550000
Mn 100-4000 15-100
Mo 0.2-5 1-100
Ni 10-1000 1.0
Pb 2-200 0.1-10
Zn 10-300 15-200

Table - 2: Toxic limits and recommendedl safe intake of selected heavy metals for human health (Modified from Oliver, 1997).

Heavy metal Toxic limits Recommended/ safe intake

As 3 mg/day for 2-3 weeks 200 15-25 ~g/day (adults)
Cd ~ g/kg of fresh weight Max. tolerable intake: 70 ~ g/day
2-25 ~ g/day (children)
15-50 ~g/day (adults)
Cr 50-200 ~ g/day
Cu 12 mg/day (adults) 150 2 mg/day (adults)
~g/day (children) 80 ~ g/day (infants)
40 ~ g/day (children)
Pb ? 500 ~ g/I toxic concentration in blood. 20-282 ~ g/day (adults)
250-550 ~ g/I (children) 9-278 ~ g/day (children)
Zn 150 ~ g/day Safe intake: 15 ~ g/day
Recommended upper limit: 45 ~ g/day

Table - 3 : Range of heavy metal concentrations (ppm) in igneous and sedimentary rocks (Cannon et al., 1978).
Metals Basaltic Granitie Shales Black Sand
igneous igneous and clays shales stone
As 0.2-10 0.2-13.8 --- _n 0.6-9.7
Cd 0.006-0.6 0.003-0.18 0.0-11 <0.3-8.4
Cr 40-600 2-90 30-590 26-1000
Co 24-90 1-15 5-25 7-100
Cu 30-160 4-30 18-120 20-200
Pb 2-18 6-30 16-50 7-150 <1-31
Mo 0.9-7 1-6 --- 1-300
Ni 45-410 2-20 20-250 10-500 -

Zn 48-240 5-140 18-180 34-1500 2-41

Table - 4 : Heavy metal concentrations (g g-1) in agricultural amendments (Modified from Ross, 1994).

Metals Agricultural amendments

Sewage Compost Farmyard Phosphate Nitrate Lime Pesticides
sludge refuse manure fertilizers fertilizers
Cr 8-40,600 1.8-410 1.1-55 66-245 3.2-19 10-15
Ni 6-5300 0.9-279 2.1-30 7-38 7-34 10-20
Cu 50-8000 13-3580 2-172 1-300 --- 2-125
Zn 91-49000 82-5894 15-566 50-1450 1-42 1 0-450
Cd <1-3410 0.01-100 0.1-0.8 0.1-190 0.05-8.5 0.04-0.1
Pb 2-7000 1.3-2240 0.4-27 4-1000 2-120 20-1250 11-26
304 Rajesh Kumar Sharma and Madhoolika Agrawal

Table - 5: Sources of heavy metal contamination in the environment (Modified from Verkleji, 1993).
Sources of heavy metals Cd Cu Pb Zn Ni Mn Fe Hg Se As
Industry
Ore outcrops + + + + +
Metal smelters + + + + +
Blast furnaces + + +
Electrolysis +
Traffic density
Leaded gasoline +
Metal emission from tires + +
House hold
Waste + + + + +
Sewage sludge + + + + +
Energy supply
Coal burning + +
Petroleum combustion +
High tension lines + +
Agriculture
Food additives + +
Phosphate fertilizers +
Pesticides + + +

Table - 6 : Indian standards for heavy metals in soil, food and drinking water (Awashthi, 2000).
Heavy metal Soil (mg/kg) Food (mglkg) Water (mgll)
Cd 3-6 1.5 0.01
Cr - 20 0.05
Cu 135.270 30 0.05
Fe . - 0.3
Ni 75-150 1.5 -
Pb 250-500 2.5 0.1
Zn 300-600 50 5.0
As - 1.1 0.05
Mn - - 0.1

sewage sludge, irrigation waters and pesticides, sources of

contamination of agricultural soil depends on the rate of
heavy metals in the agricultural soils. Other particularly
application of the contributors with its elemental
fungicides. Inorganic fertilizers, particularly phosphate
concentration, and soil characteristics to which it is applied
fertilizers have variable levels of Cd, Cr, Ni, Pb and In
(Table 4). Heavy metal accumulation in soil is also due to
depending on their sources. Cadmium is of particular concern
application of soil amendments such as compost refusing and
in plants since it accumulates in leaves at very high levels,
nitrate fertilizers (Ross, 1994). Liming increases the heavy
which may be consumed by animals or human being.
metal levels in the soil more than the nitrate fertilizers and
Cadmium enrichment also occurs due to sewage sludge,
compost refuse. Sewage sludge is one of the most important
manures and limes (Nriagu and Pacnya, 1988). Although the
sources of heavy metal contamination to the soil (Ross,
levels of heavy metals in agricultural soil is very small, but
1994). Several heavy metal based pesticides are used to
repeated use of phosphate fertilizer and the long residence
control the diseases of grain and fruit crops and vegetables,
time for metals, there may be dangerously high accumulation
and are sources of heavy metal pollution to the soil (Verkleji
of some metals (Verkleji, 1993).
1993; Ross 1994). The orchards where these compounds
Ar,imal manure enriches the soil by Mn, In, Cu and
have been used frequently resulted into contamination of
Co, and sewage sludge by In, Cr, Pb, Ni, Cd, and Cu
orchard soil with high levels of heavy metals such as Cu, As,
(Verkleji, 1993). The increase in heavy metal
Pb, In, Fe, Mn and Hg (Ross, 1994). Pesticides such
Biological effects of heavy metals: an overview
as lead arsenate were used in Canadian orchards for more
than six decades and were found to be enriched with Pb, As
and In, having greater consequences for food contamination.
Continued irrigation of agricultural soil can lead to
accumulation of heavy metals such as Pb and Cd. The
contamination of soil by heavy metals may also be from
irrigation water sources such as deep wells, rivers, lakes or
irrigation canals (Ross, 1994).
(c) Industrial sources of heavy metals: Industrial sources of
heavy metals include mining, refinement (spoil heaps and
tailings, transport of ores, smelting and metal finishing and
recycling of metals). Mining operation emits different heavy
metals depending on the type of mining. For example
coalmines are sources of As, Cd, Fe, etc, which enrich the
soil around the coalfield directly or indirectly. High
temperature processing of metals such as smelting and
castings emit metals in particulate and vapor forms. Vapor
form of heavy metals such as As, Cd, Cu, Pb, Sn and In
combine with water in the atmosphere to form aerosols.
These may be either dispersed by wind (dry deposition) or
precipitated in rainfall (wet deposition) causing contamination
of soil or water bodies. Contamination of soil and water
bodies can also occur through runoff from erosion of mine
wastes, dusts produced during the transport of crude ores,
corrosion of metals, and leaching of heavy metals to soil and
ground water. Soil contamination of heavy metals occurs due
to different types of processing in refineries. Energy supplying
power stations such as coal burning power plants, petroleum
combustion, nuclear power stations and high tension lines
contribute many heavy metals such as Se, B, Cd, Cu, In, Cs
and Ni to the environment (Verkleji, 1993; Table 5). Other
industrial sources include processing of plastics, textiles,
microelectronics, wood preseNation and paper processing.
Contamination of plants growing beneath the power line with
high concentration of Cu is reported to be toxic to the grazing
animals (Kraal and Ernst, 1976).
Other sources of heavy metals include refuse
incineration, landfills and transportation (automobiles, diesel-
powered vehicles and aircraft). Two main anthropogenic
sources that contaminate the soil are fly ash produced due to
coal burning and the corrosion of commercial waste products,
which add Cr, Cu, Pb and galvanized metals (primarily In) (AI-
Hiyaly et al., 1988). Coal burning adds heavy metals such as
Cd, Hg, Mn, Ni, AI, Fe and Ti into the soils (Verkleji, 1993).
Oil burning contributes V, Fe, Pb and Ni to the environment.
Metal
305
emission during the transportation of vehicles includes Ni and
In from tires, AI from catalyst, Cd and Cu primarily from diesel
engines and Ni and In from aerosol emissions. Lubricants,
which are antiwear protectants for vehicles emit Cd, Cr, Hg,
Ni, Pb and In, particularly in case of inefficient engines. The
burning of leaded gasoline has been an important source of
Pb in the environment. Incinerations of municipal wastes
generate significant concentrations of In, Pb, AI, Sn, Fe and
Cu.
Effects of heavy metals on plants: Like all organisms, plants
are often in a state of dilemma that some heavy metal ions
are essential micronutrient, while the same at higher
concentrations and even more ions such as Cd, Hg, As, etc
are strongly poisonous to the metabolic activities. Researches
have been conducted throughout the world to determine the
effects of toxic heavy metals on plants (Reeves and Baker,
2000; Fernandez and Henariques, 1991).
(a) Effects,on membrane: Several heavy metal ions are
reported to cause preoccupation of membrane lipids (plasma
and chloroplast membrane). For example Cd modified the
lipid composition of root plasma membrane of Pisum sativum
(Hernandez and Cooke, 1997). Among metals, increased
level of lipid peroxidation has been reported under Cd stress
in Oryza sativa (Ros et al., 1990; Shah et al., 2000), Holcus
lanatus (Hendry et al., 1992) and Phaseolus vulgaris
(Somasekharaiah et al., 1992; Chaoui et al., 1997). Increased
lipid peroxidation is also reported under Ni stress in Oryza
sativa (Ros et al., 1990), AI stress in Glycine max (Cakmak
and Horst, 1991) and tobacco (Yamamoto et al., 1997), In
stress in Phaseolus vulgaris (Chaoui et al., 1997; Weckex
and Clijsters, 1997) and rice (Panda and Khan, 2003), Cu
stress in Silene cucubalus (DeVos et al., 1991, 1993), Avena
sativa (Luna et al., 1994) and Lycopersicum esculentum
(Mazhoudi et al., 1997), Pb stress in Oryza sativa (Verma and
Dubey, 2003), and Cr stress in rice and wheat (Panda and
Khan, 2003). These heavy metals have greater potential to
catalyze the formation of hydroxy free radicals, which are
capable of starting the peroxidative process by primary
initiation and Haberweiss and Fenton reactions.
The increased lipid peroxidation is considered to be
an initiation of increased oxidative stress caused by heavy
metals in variety of plants such as rice (Ros et al., 1990), oat
(Luna et al., 1994) and mung bean (Weckex and Clijsters,
1997). Inceased level of lipid peroxidation is also known to
modify membrane properties such as
306
fluidity and permeability and modulate the activities of
membrane bound ATPase. Damage to ATPase activity in
cellular membrane of cotton has been reported by Tu and
Brouillette (1987). Lipid peroxidation severely affects the
functioning of membranes, including the plasma membrane
as reported in Silene cucubalus (DeVos et al., 1993). Lipid
peroxidation, however, is suggested to be a secondary target
for metal ions (DeVos et al., 1993).
(b) Effects on physiological processes: Heavy metals such
as Cd, Ni, and Cu are reported to affect the photosynthetic
functions of higher plants (Baszynski, 1986) either directly or
indirectly. Sheoran et al. (1990) reported that Cd and Ni affect
the enzymes of the photosynthetic carbon reduction cycle in
Cajanus cajan. Similar results are also reported for Beta
vulgaris (Greger and Orgen, 1991), radish (Krupa et al.,
1987), and Silene and Thalaspi (Ouzounidou, 1993). Cu
stress is reported to inhibit chlorophyll biosynthesis in
Thalaspi ochrolucum (Ouzounidou, 1993) and Phaseolus
vulgaris (Gadallah, 1995). Heavy metal induced reduction in
total chlorophyll has been reported in pigeon pea due to Cd
and Ni stress (Sheoran et al., 1990), and in Brassica juncea
due to Cd stress (Singh and Tewari, 2003). Chlorophyll aIb
ratio
was found to decrease in pigeon pea (Sheoran et al
1990) or increase in Brassica juncea (Singh and Tewari,
2003). In general carotenoids were less affected by heavy
metals, resulting in lower chlorophyll and carotenoid ratio in
plants. Reduction in chlorophyll content due to its degradation
and unfavorable effect on photosynthetic electron transport
have been reported due to Cu toxicity
in sensitive species of Silene compecta and Thalpsi
ochrolucum (Ouzounidou, 1993). Nickel also reduced the total
chlorophyll content the leaves of plants that grow in presence
of its inorganic forms in Phaseolus vulgaris (Krupa et al.,
1993) and organic form in cabbage leaves (Molas, 2002).
Nickel reduces photosynthetic activity of plants
(Mohanty et al., 1989; Sheoran et al., 1990; Krupa et al.,
1993). Reduction of photosynthetic activity may result both
from the disturbance of photochemical and biochemical
photosynthetic reduction, and the damage of photosynthetic
apparatus at all levels of organization (Mohanty et al., 1989)
as reported in Cajanus cajan (Sheoran et al., 1990), P.
vulgaris (Krupa et al., 1993) and Brassica olaracea (Molas,
2002). The contents of plastoglobuli increase due to heavy
metal stress such as due to Ni in cabbage (Molas, 2002) and
in pine and birch needles exposed to elevated levels of Cu
and Ni (Kukkola
Rajesh Kumar Sharma and Madhoolika Agrawal
and Huttunen, 1998). Disturbance and inhibition of
carbohydrate transport from the place of photosynthesis
result into the accumulation of starch under the influence of
Ni in pine and birch (Kukkola and Huttunen, 1998) and rice
(Moya and Ros, 1993).
Net photosynthesis rate reduced significantly in
mature leaves of Spinacea olaracea (Barua and Jana, 1986)
and mung bean (Gadallah, 1995) due to heavy metal
accumulation. Cadmium reduced leaf area, net photosynthesis
rate and transpiration rate in corn and sunflower (Bazzaz et
al., 1974 b) and pea and sugar beet (Greger and Johansson.,
1992). Zn and Cd both inhibited photosynthetic CO2 fixation
and Hill reaction activity of isolated spinach chloroplasts
(Barua and Jana, 1986) and photosynthetic electron transport
in isolated barley chloroplasts (Tripathi and Mohanty, 1980).
Copper is known to interfere with oxidative enzymes in Avena
sativa leaves (Luna et al., 1994). In Zea mays, Cd
altered the photosynthesis and enzymes of photosynthetic
sulphate and nitrate assimilation pathways (Ferretti et al.,
1993). In Phaseolus vulgaris, Zn affected RUBP carboxylase
without affecting oxygenase activity (Van Assche and Clijsters,
1986). Inhibition of photosynthetic CO2 fixation rate and
decrease of CO2 compensation point in intact leaf of
Phaseolus vulgaris after Zn treatment has also been reported
(Van Assche et al., 1988).
Heavy metal toxicity is reported to increase the
activity of enzymes such as, glucose-6- phosphate
dehydogenase and peroxidases in the leaf of plants grown in
polluted soil (Van Assche and Clijsters, 1987). Mercury, Cu
and Zn ions have changed the hydrolytic activity of
chlorophyllase in rice leaves, with Hg increasing the activity
maximally out of the three metals (Drazkiewicz, 1994). Zinc
increased chlorophyllase activity moderately, whereas Cu
affected it least. Plants exposed to excess heavy metals have
been reported to increase stomatal resistance, decrease
transpiration rate and alter the water relation in sunflower and
corn (Bazzaz et al., 1974a, b). Cd inhibits net photosynthesis
by increasing both stomatal and mesophyll resistance to CO2
uptake in silver maple leaves (Lanoreaux and Chaney, 1978).
Interference with
stomatal function is considered to be a preparing mode of
action of Cd as well as other heavy metals. Physiological
responses such as net CO2 assimilation, water use efficiency
and stomatal conductance were depressed under Cd stress in
wheat plants (Abo-Kassem et al., 1995). Both permanent
stomatal closure and increased ethylene production may be
responsible for senescence
Biological effects of heavy metals: an overview
induction in leaf tissue of beans under Cd toxicity (Fuhrer,
1988). Heavy metal accumulation in leaves enhanced the
production of ethylene a promoter of senescence.
Toxic heavy metals like Cd, Ni, Co, Cr, Zn and Pb
are reported to cause Fe deficiency either by decreased
uptake or by causing immobilization in roots. Mineral uptake
is also inhibited in presence of heavy metals as reported in
Beta vulgaris (Greger and Lindberg, 1987). Heavy metals
also lead to water stress in sunflower (Kastori et al., 1992)
and Brassica juncea (Singh and Tewari, 2003).
Contaminated soils have phytotoxic levels of heavy metals
including Pb, Cd, Zn, Cr, and Ni. Chromium in nature exists
in the form of Cr (VI) and Cr (III) of which earlier one is more
toxic. Chromium toxicity is known to affect seed germination,
seedling growth, senescence, pigment status, and nutrient
contents of crop plants (Bishnoi et al., 1993).
Zinc is an essential micronutrient that affects several
metabolic processes of plants (Cakmak and Marschner, 1993)
and has a long biological half-life. The phytotoxicity of Zn and
Cd are indicated by decrease in growth and development,
metabolism and an induction of oxidative damage in various
plant species such as Phaseolus vulgaris (Cakmak and
Marschner, 1993) and Brassica juncea (Prasad et al., 1999).
Cd and Zn have reported to cause alteration in catalytic
efficiency of enzymes in Phaseolus vulgaris (Van Assche and
Clijsters, 1988; Somashekaraiah et al., 1992), and pea plants
(Romero-Puertas et al., 1999).
(c) Effects on antioxidant activity: Metal ions play an important
role in the antioxidant network, as these are essential
cofactors of most antioxidant enzymes. For example all
isoforms of super oxide dismutase (SOD) contain bound
heavy metal ions. Cu and Zn constitute the cofactor of the
Cu/Zn- SOD associated with chloroplast, glyoxisomes and
cytosol. Mitochondria, peroxisomes and glyoxisomes contain
Mn-SOD. Fe-SOD has been found in the chloroplast of some
plants. Metals are involved in the direct or indirect generation
of free radicals (FR) and reactive oxygen species (ROS) in the
following ways: (1) direct transfer of electron in single electron
reduction; (2) disturbance of metabolic pathways resulting in
an increase in the rate of FR and ROS formation; (3)
inactivation and down regulation of the enzymes of the
antioxidative defense system; and (4) depletion of low
molecular weight antioxidants (Aust et al., 1985). The ROS
produced in leaf cells are removed by complex non-enzymes
(ascorbate, glutathione, and alpha- tocoferol) and enzymes
(catalase
307
(CAT), ascorbate peroxidases (APX), glutathione
peroxidases (GPx), superoxide dismutase (SOD), and
glutathione reductases (GR)) of antioxidant systems. Heavy
metals induced oxidative damage in senescing oat leaf cells
(Luna et al., 1994), primary leaves of mung bean (Weckex
and Clijsters, 1997), and in wheat leaves (Panda and Patra,
2000). Proline is known to playa role in the detoxification of
active oxygen in Brassica juncea and Cajanus cajan under
heavy metal stress (Alia et al., 1995). Accumulation of proline
has been observed in various
plants species subjected to heavy metal stress (Bohnert et al.,
1995; Shah and Dubey, 1998). It is reported that antioxidant
enzyme activities increase under Zn.stress in Brassica juncea
(Prasad et al., 1999). Verma and Dubey (2003) have reported
that with increase in the level of Pb treatment, antioxidant
enzymes such as guaiacol peroxidase, SOD, APX, and GR
activities increased compared to control in rice plants. It has
been further suggested that SOD and GR playa pivotal role in
combating oxidative stress in rice plants and Pb toxicity.
(d) Effects on heavy metals accumulation: Plants exhibit
variations in heavy metal accumulation in different plant parts
in response to contamination. The levels of heavy metal
detected in leaves of metal tolerant plants were often not
exceeding than 10% of the total plant accumulation (Ernst et
al., 1992). The level of heavy metal translocated to chloroplast
is estimated to be only about 1 %, however, it varies from
species to 9pecies. The oldest leaves of plants have capacity
to accumulate the highest concentration of heavy metal
(Prasad, 1995). The presence of Pb in senesced leaves
remains constant throughout the year. However,
bioaccumulation of Zn
gradually increases as senescence progresses (Ernst et al.,
1992).
Absorption, accumulation and distribution of heavy
metals in different food crops such as rice, wheat, barley,
maize and potato, oil seed crops and forage crops have been
documented (Devkota and Schmidt, 2000; Jeng and Singh,
1995; Grant and Bailey, 1996). Cadmium accumulation in
different parts of cucumber (MorenoCase lies et al., 2000) and
barley (Aery and Rana, 2003) are reported. Cadmium
accumulation in different plant parts increases with increasing
concentration of Cd and the exposure time. The gradient of
accumulation of heavy
metals was found highest in root followed by stem, branch,
leaf and then in fruit «Aery and Rana, 2003; Moreno-Caselles
et al., 2000; Kim et al., 1988). The uptake of heavy metals
increases with age (Prasad,
 308
1995). Heavy metals accumulate more in reproductive than
vegetative stage. It has been reported that the translocation of
heavy metals from root to top increases with an increase in
substrate metal concentration. Metals are transported from
root to shoots as organic metal complexes with citric acid or
some other organic acids in xylem. Translocation of metals is
a metabolic process controlled by physico-chemical condition.
Application of excessive amounts of metal reduces the
translocation ratio due to reduced metabolic activities of roots
(Aery and Rana, 2003). The concentration of different heavy
metals in different plant parts differ, for example Pb is
accumulated more in leaves of Silene vulgaris, while in
Thalaspi alpestre and Armeria maritima, it is found mainly in
root (Baker, 1981). Cd concentration in root of cucumber was
found higher (Moreno-Caselles et al., 2000) than for other
heavy metals such as Ni and Cr (Moral et aI, 1994). Specificity
of accumulation is also reflected by different plant families
(Baker, 1987). Low Cd accumulations have been observed in
,.ijFabaceae, moderate in Poaceae, Cucurbitaceae and
Apiaceae while high in Chenopodiaceae, Brassicaceae,
Solanaceae and Asteraceae. Dicots have found to absorb
more heavy metals than monocots.
(e) Effects on growth, biomass and yield: Studies on
. heavy metal tolerance in plants indicate that root growth is
particularly sensitive to heavy metals (Punz and Sieghardt,
1993). Copper toxicity affected the growth of Alyssum
montanum (Ouzounidou, 1994) and Cd of cucumber
(Moreno-Case lies et al., 2000) and Brassica juncea (Singh
and Tewari, 2003). Copper and Cd in combination have
affected adversely the germination, seedling length, and
number of lateral roots in Solanum melongena (Neelima and
Reddy, 2002). Reduction in root growth due to heavy metals
has also been reported in wheat seedlings (Oncel et al.,
2000). The number of leaves and branches, root and shoot
length and biomass decreased as concentration of Cr
increased in egg plant and tomato (Purohit et al., 2003) and
in barley (Aery and Rana, 2003). Cd concentration (1-5 IJ M)
decreased leaf area and biomass, whereas at 11J M
concentration the same increased in barley (Wu et al., 2003).
The dry matter and yield of many higher plants such as pea,
wheat, fodder veteh, rapeseed and maize have been
reported to decrease under multiple heavy metal stress.
Presence of Zn at higher concentrations retarded the growth
and development of plants by interfering with certain
important metabolic processes (Alia et al., 1995).
Rajesh Kumar Sharma and Madhoolika Agrawal
Fresh and dry weights of root, stem, branch and leaves of
cucumber were found to decrease at 10 to 20 mg/l Cd
concentration (Moreno-Caselles et al., 2000). A significant
decrease in clover biomass production has been reported in
Cd polluted soil (McGrath et al., 1995). The length of root and
shoot were smaller for plants growing in Cd polluted soil.
Significant reductions in length of Solanum melongena
(Mehindirata et al., 1999) and plant height and fresh and dry
matter in Brassica juncea (Singh and Tewari, 2003) at higher
Cd concentration have also been reported. Higher
concentrations of Cd (500 ppm) decreased secondary growth
(Costa and Spitz, 1997).
Effects on human health: Mostly edible parts of plants are
the major source of heavy metal intake for human through
consumption, which have long-term detrimental
. effects on human health. Several heavy metals are
considered toxic metals due to adverse human health effects,
when taken in excess. Heavy metals pose hazards to human
health because these are persistent in nature and have
accumulation tendency in biological systems. Indian
standards for heavy metal concentrations in soil, food and
drinking water are given in Table 6. Heavy metals can b-e
divided into four major groups based on their health
importance (1) Essential metals such as Cu, Zn, Co, Cr, Mn
and Fe, (2) Non-essential metals such as Ba, AI, Li and Zr,
(3) less toxic metals such as Sn and As, and (4) highly toxic
metals such as Hg, Cd and Pb. Heavy metals have potential
to affect the organs of human body and some of them are
carcinogenic to man. Unfavorable effects of selected heavy
metals on human health are discussed below:
(a) Zinc: The recommended Daily Dietary Allowance of Zn is
15 mg for adults and 20 to 25 mg for pregnant and lactating
women (NRC-NAS, 1980). Acute Zn toxicity in human
includes vomiting, dehydration, drowsiness, lethargy,
electrolytic imbalance, abdominal pain, nausea, lack of
muscular coordination, and renal failure (Prasad and
Oberleas, 1976). Chronic dose of Zn increases the risk of
developing anemia, damage to the pancreas, lowers down
HDL cholesterol levels and raises LDL cholesterol levels and
possibly enhances the symptoms of the Alzheimer's disease
(Athar and Vohora, 1995). Workers exposed to Zn fumes from
smelting or welding have suffered from a short-term illness
called mental fume fever.
(b) Lead: The general population is exposed to Pb from air
and food. Children are particularly susceptible to Pb
Biological effects of heavy metals: an overview 309

exposure due to high gastrointestinal uptake, and the industrial workers and people exposed to Cd in general
permeable blood brain barrier leading to neurotoxic effects environment(Jarup et al., 1998).
even at low level of exposure (Jarup, 2003). The toxicity of (e) Nickel: Daily intake of nickel through food is approximately
Pb is caused by its direct interference with activity of different 300 ~ g (WHO, 1987). Nickel induces embryo toxic and
enzymes or displacing essential metal ions from nephrotoxic effects, allergic reactions and contact dermatitis
metalloenzymes. The major exposure pathway of inorganic (EPA, 2002). Nickel sensitization also occurs in general
Pb is via ingestion and adsorption through the gastrointestinal population from exposure to coins, jwellery, watchcases,
tract, respiratory tract and inhalation. Kidney and liver are clothing and fasteners. It causes conjunctivitis, eocinophilic
considered potential targets of Pb toxicity before storage in pheumonites, asthma and local or system reaction to Ni
bones (Athar and Vohora, 1995). Depending on the level of containing prostheses such as joint replacGments, pins,
exposure, Pb has potential to cause a variety of biological cardiac valve replacements, cardiac pacemaker wires and
effects such as decreased hemoglobin synthesis, impairment dental inlays (Athar and Vohora, 1995). Nickel is a potential
of neurobehavioral and psychological functions, peripheral carcinogen for lung and may cause skin allergies, lung fibrosis
neuropathy, indirect effect on heart, renal tubular damage and cancer of respiratory tract in occupationally exposed
and reproductive problems (Brown and Kodama, 1986). populations (Kasprazak et al., 2003).
(c) Copper: Copper is essential for the formation of enzyme (1) Arsenic: Intake of 70 to 80 mg of trivalent arsenic (III)
inhuman beings. Intake of excessively large doses of Cu oxide has been reported to be fatal for man (WHO, 1987).
leads to severe mucosal irritation and corrosion, wide spread Inorganic arsenic produces acute, subacute and chronic toxic
capillary damage, hepatic and renal damage and central effects, which may be either local or system. Acute toxic
nervous system irritation followed by depression (Athar and effects include abdominal cramping, hypersthesia in
Vohora, 1995). Copper toxicity includes blue green diarrhoea extremities, abdominal patellar reflexes and abdominal
stool and saliva and acute haemolysis and abnormalities of electrocardiograms (Franzblau and Lilis, 1989). Such effects
kidney functions. Wilson's disease is an inborn error of generally occur at the levels of exposure equal to 50 ~ glkg
metabolism where the inherited defect lies in the weight/day. However, chronic poisoning of As includes
incorporation of Cu2+ into apocerplasmin to form anemia, liver - and kidney damage,
ceruloplasmin and also impaired ability of the liver to excrete hyperpigmentation and keratosis Le. skin damage (Wu et al.,
Cu into the bile which leads to Cu accumulation in tissues of 1989; ATSDR, 2000) Other effects of arsenic include
liver, brain, kidney and cornea resulting in organ damage peripheral vascular disturbances resulting in gangrene and a
(Krishnamurti and Viswanathan, 1991). The safe and disease termed Black foots disease (Tseng, 1977).
adequate daily dietary allowance for Cu is 2 to 3 mg for (g) Chromium: Average daily intake of chromium ranges
adults and 1 to 3 mg the children (Table 2). between 100 and 300 ~g/day (WHO, 1984). The harmful
(d) Cadmium: Food and cigarette smoking are the most effects of Cr to human are mostly associated with
important sources of Cd apart from water. Daily dietry intake its hexavalent form. Chromium toxicity includes liver nercosis,
of Cd ranges from 40 to 50 ~gl day (WHO, 1987). Cd nephrites and gastrointestinal irritation (Athar and Vohora,
accumulates within the kidney and liver over long time 1995). Cr+6 can also produce cuetaneous, nasal and mucous
(McLaughlin et al., 1999). Long-term low-level exposure membrane ulcers and cause dermatitis by skin contact.
leads to r.ardiovascular disease and cancer. It is known to Differentiation between the biological effects caused by Cr+6
primarily affect renal tubular function of reabsorbing protein, and Cr+3 is difficult because after penetration through
sugar and amino acids (McLaughlin et al., 1999). Cadmium membrane the Cr+6 gets reduced into Cr+3 form. A similar
exposure in conjunction with Ca, Fe, Zn, protein, fat and response is also brought by the activity of gastric juice for
vitamin D deficiencies, led to ostomalacia and bone fractures chromium (VI) that ingested through oral route. Chromium has
in postmenopausal women in polluted Jintsu valley, Japan potent carcinogenic
commonly referred to as Itai-Itai effects on human beings and other animals (O'Brien et al.,
disease (Noda and Kitagawa., 1990). Cadmium can affect 2003).
calcium, phosphorus and bone metabolisms in both . (h) Manganese: Mn is an essential nutrient and its daily
requirement is estimated to be between 2.5 to 5.0 mg for
 310
adults (NRC-NAS, 1980). It is a metal having relatively low
toxicity to human being, and causes acute poisoning effect at
higher concentrations. The neurological disorder known as
manganism results from exposure of Mn dust fume to
occupational workers (Brown and Kodama, 1986). Effects of
Mn are decrease in systolic blood pressure, disturbed
excretion of 17-ketosteroids, change in erythropoesis and
granulocyte formation (Athar and Vohora, 1995).
(i) Mercury: The safe daily intake of mercury as suggested
by WHO is 43 ~ g (KrishnaMurti, 1987) Mercury has no
physiological function in human, and hence exerts many toxic
effects. The effect of Hg poisoning depends on its different
forms. Maximum toxicity results due to methyl mercury or
mercury vapor. Mercury toxicity includes neurological and
renal disturbances (Diuresis and saluresis) (Athar and
Vohora, 1995). Mercury intake led to minimata disease,
where liver accumulated substantial amounts of Hg. Fishes
containg more than 0.4 ppm Hg (0.3 ppm methyl mercury)
are unfit for human consumption. The critical urinary
cOflcentration of Hg has been suggested as 1 to 2 ~ g/ml.
Minimata disease is characterized by symptoms of fatigue,
loss of memory and concentration, tremours constriction of
visual field, cortical blindness, etc (Jarup, 2003). Mercury
passes through placental barrier and may cause intra-uterine
death, foetal resorption and stillbirth. The alkyl derivatives are
particularly foetotoxic (Brown and Kodama, 1986).
Anthropogenic activities greatly influence the
:>< availability of heavy metals in the environment. Since heavy
metals are not naturally degraded, they are progressively
accumulated in plants and soil. Copper, Fe, Mn and Zn cause
growth reductions at high concentrations, whereas Cd, Ni, Pb
and Cr cause growth reductions at lower levels of
accumulation. Heavy metals interfere with physiological
processes such as gaseous exchange, CO2 fixation,
respiration, and nutrient absorption and photosynthate
translocation. Heavy metal uptake is not linear in response to
the increasing concentrations. Wide species variations are
recorded for the accumulative efficiency for different heavy
metals. The difference in metal accumulation is not correlated
with tolerance to the heavy metal. Heavy metals pose a
number of hazards to human health. Therefore their
concentration in the environment and their effects on human
health must be regularly monitored. More researches are
required to understand the mechanisms
Rajesh Kumar Sharma and Madhoolika Agrawal
involved in heavy metal tolerance in plants. Metal induced
defense response at molecular level need to be worked out
for understanding the cascade of chemical mechanisms of
heavy metal tolerance.
Acknowledgments
The authors are thankful to Department for International
Development, U.K. for providing the financial support.
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Correspondence to :
Professor Madhoolika Agrawal,
Ecology Research Laboratory, Department of Botany, Banaras Hindu University, Varanasi - 221 005 (U.P.), India. E-
mail: madhoo@bhu.ac.in
Tel. : +91-542-2368156
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