You are on page 1of 11

Sengupta, M. and Dalwani, R. (Editors).

2008
Proceedings of Taal2007: The 12th World Lake Conference: 1028-1038

Heavy Metal Accumulation by Certain Aquatic Macrophytes from Lake


Sevan (Armenia)
L. Vardanyan1, K. Schmieder2, H. Sayadyan3, T. Heege4, J. Heblinski2,4, T. Agyemang2 and J. De5, J.
Breuer6
1

Dept. of Biology, University of Vanevan, #19, Gulbenkyan 29A, Yerevan, Armenia.


University of Hohenheim, Institute of Landscape and Plant Ecology (320), D - 70593 Stuttgart, Germany,
3
State Agrarian University, Dep. of Forestry and Agro-ecology, 74 Teryan, 375079 Yerevan, Armenia,
4
EOMAP GmbH & Co KG, Sonderflughafen Oberpfaffenhofen, Geb.319 D - 82205 Gilching, Germany,
5
Graduate School of Kuroshio Science, Kochi University, Nankoku, Kochi- 783 8502, Japan,
6
State Institute of Agricultural Chemistry, Department of Soil and Fertilizer Analysis, D-70593 Stuttgart,
Germany.
Email:
livag777@yahoo.com,
schmied@uni-hohenheim.de,
hovik_s@yahoo.com,
heege@eomap.de,
jaysankarde@yahoo.com, breuerj@uni-hohenheim.de
2

ABSTRACT
General contamination of heavy metals in the environment is a major global concern, which has provoked
the emergence of phytoremediation technologies for cleaning aquatic environment. Heavy metals are
released into the environment from a wide range of natural and anthropogenic sources. Macrophytes are
known as good indicators of heavy metal contamination in aquatic ecosystems and they act as biological
filters by accumulating heavy metals from the surrounding environments. Concentrations of heavy metals
such as Hg, Cd, Co, Cu, Mo, Ni, Pb, Tl and Zn were measured in macrophytes and water samples from
the mouth of five rivers namely; Gavaraget, Argichi, Makenis, Masrik each of them meeting the Lake
Sevan, Armenia. The collected plants were Batrachium rionii, Myosotis palustris, Lythrum salicaria,
Scrophularia alata, Calamagrostis epigeios, Lepidium latifolium, Glyceria plicata, Veronica anagallisaquatica, Butomus umbellatus, Sparganium erectum. The highest concentration of Ni (5.5 mg/kg) was
observed in Glyceria plicata whereas concentrations (mg/kg) of all other metals were highest (Hg, 0.02;
Cd, 0.46; Co, 3; Cu, 18.9; Pb, 6.9; Tl, 0.13 and Zn, 113) in Batrachium rionii. Range and trend in
concentrations of Co (<0.5g/l), Cd (<0.5g/l), Tl (<0.1g/l) and Hg (<0.3g/l) in water samples were
similar at all the sites. Occurrence of heavy metals was much higher in macrophytes and water from
Gavaraget and Masrik than that of the Argichi and Makenis due to the discharge of sewage into the river
Gavaraget and industrial wastewaters into the river Masrik. The fact that the concentrations of different
heavy metals in these macrophytes were far higher than in their respective water column indicates to their
role in the biogeochemical cycles of heavy metals. This study aimed at understanding the importance of
macrophytes in accumulation of heavy metals and suggesting remedial measures for the preservation and
restoration of the lake ecosystem.
Keywords: phytoremediation, bioaccumulation, pollution, rivers, freshwater.

INTRUDUCTION
Contamination of soils, groundwater, sediments,
surface water and air with trace metals is one of the
major environmental problems. Aquatic systems
often act as final receptacles to these metals whose
concentration in interstitial waters might increase
several thousand folds by effluents from wastes
(Bastian and Hammer 1993). Heavy metals are the
stable metals or metalloids whose density is greater
than 5 g/cm3; namely, mercury, cadmium, cobalt,
lead, molybdenum, nickel, copper, zinc etc. (Nies
1999). Heavy metals are natural constituents of the
Earth's crust. They are stable and cannot be degraded
or destroyed, and therefore they tend to accumulate in
soils, water and sediments. However, human
activities have drastically altered the biochemical and
geochemical cycles and balance of some heavy

metals. The principal man-made sources of heavy


metals are industrial point sources (mines, foundries
and smelters etc.) and diffuse sources (combustion
by-products, traffic etc.).
Pollutants enter aquatic systems via numerous
pathways, including effluent discharge, industrial,
urban and agricultural run-off, as well as airborne
deposition. Heavy metals are especially toxic due to
their ability to bind with proteins and prevent DNA
replication (Kar and Sahoo 1992). Many technologies
have been used to reduce aquatic pollution, but they
are generally costly, labour-intensive and generate
secondary waste. An interesting alternative approach
is phytoremediation (rhizofiltration) (Flathman and
Lanza 1998; EPA 2000).
Removal of metals from these soils and waters
using
natural
or
induced
metal
tolerance/accumulation capacities of some plant

species or populations originating from contaminated


areas is the goal of phytoremediation (Baker and
Brooks 1989; Salt et al. 1998; McCutcheon and
Schnoor 2003). In 1991, Baker et al. concluded that
phytoremediation by using certain species could offer
a low cost and low technology alternative to current
clean up technologies. Best plant candidates for
phytoremediation must show accumulating capacities
and tolerance to elevated contaminant concentrations
to be able to survive and produce biomass. Some
trace metals (e.g. Cu, Fe Zn, Mn, Ni, Mo, Se etc.) are
essential for normal plant growth although both
essential and non-essential metals (e.g. Hg, Cd, Pb,
As) can result in growth inhibition and toxicity
symptoms (Poschenrieder et al. 2006). Deleterious
effects of trace metal pollution on plant at cellular
levels might result from binding to proteins
sulphydryl groups and thereby ending in the
inhibition of enzyme activity and protein function
and/or from disruption of cell transport processes.
Also, most of the metals induce production of free
radicals and active oxygen species (ROS) leading to
an oxidative stress (Van Assche et al. 1990; Meharg
1994; Grato et al. 2005). Phytoremediation is a
biological process in which living plants are used to
remove,
accumulate,
degrade,
or
contain
environmental
contaminants.
This
passive
remediation technique is based on the natural ability
of vegetation to utilize nutrients, which are
transported by capillary action from the soil and
groundwater through a plants root system. The use
of a plants own biological mechanisms to contain
and reduce concentrations of inorganic and organic
contaminants in soils, sediments, and groundwater is
a slow process relying on a plants growth rate.
However, with advances in biological, chemical, and
engineering technologies, phytoremediation has the
potential to serve as a sustained, ecologically sound
method to remediate contaminated soil and
groundwater (Brown et al. 1990). There are few
mechanisms helping this process:
Phytoextraction - uptake and concentration of
substances from the environment into the plant
biomass.
Phytostabilization - reducing the mobility of
substances in the environment, for example by
limiting the leaching of substances from the soil.
Phytotransformation - chemical modification of
environmental substances as a direct result of plant
metabolism, often resulting in their inactivation,
detoxification (phytodegradation) or immobilization
(phytostabilization).
Phytostimulation - enhancement of soil microbial
activity for the detoxification of contaminants,
typically by organisms that associate with roots. This
process is also known as rhizosphere detoxification

Phytovolatilization - removal of substances from soil


or water with release into the air, sometimes as a
result of phytotransformation to more volatile and /
or less polluting substances.
Rhizofiltration - filtering water through a mass of
roots to remove toxic substances or excess nutrients.
The pollutants remain absorbed in or adsorbed by the
roots.
Aquatic macrophytes have been used for years
for this phytoremediation purpose due to their
characteristics to accumulate metals and metalloids
(Welsh and Denny 1980; Say et al.1981; Heisey and
Damman, 1982; Bishop and DeWaters 1986; Brix
and Schierup 1989; Gardea-Torresday et al. 2005).
Several works have demonstrated that aquatic
macrophytes can perform as biological filters and
they carry out a purifying function by accumulating
dissolved metals and toxins in their tissue (Mejare
and Bulow 2001; Prasad et al. 2005; Vardanyan and
Ingole 2006). Macrophytes are an important
component of aquatic communities due to their roles
in oxygen production, nutrient cycling, controlling
water quality, sediment stabilization and providing
habitat and shelter for aquatic life (Gibbons et al.
1994; Ravera 2001). Hence changes in community
dynamics can affect not only other biota but also
other uses such as recreational and navigational use
of the water body (Lewis 1996). Macrophytes
actively take up metals from the sediments through
their roots and translocate them to the shoots, which
are available for grazing by fish. These may also be
available for epiphytic phytoplankton and
herbivorous and detritivorous invertebrates (Cardwell
et al. 2002), representing a major route of
bioaccumulation of heavy metals in the aquatic food
chain. It is therefore of interest to assess the levels of
heavy metals in macrophytes due to their importance
in ecological processes. The immobile nature of
macrophytes makes them a particularly effective
bioindicator of heavy metal pollution as they
represent/reflect
the
actual
environmental
contamination prevailing at that site. From an
ecological perspective, the apparent lack of
translocation of metals from roots to shoots means
that the likelihood of bioaccumulation along trophic
levels is reduced (Matagi 1998). This is because the
higher concentrations of heavy metals are found in
plant roots, organs that are unavailable for ingestion
and heavy metals are thus tied up, or stored, in areas
that are unlikely to be transferred into other areas of
the ecosystem and its biota. Studies on the total
ecosystem effects involving not only macrophytes
but also sediment and other biota are necessary to
provide a complete picture of the effects of heavy
metals on aquatic ecosystems. Significant differences
obtained for the heavy metal concentrations between
macrophyte species suggest that the interactions and
behaviours of heavy metals with macrophytes are
different for each species (Prasad and Frietas 2003).

1029

Even after years of research on heavy metal


accumulation in aquatic plants and water, and its
hazardous impacts on environment, major questions
still need to be answered. The factors affecting
distribution and abundance of submerged aquatic
vegetation and the effect of submerged aquatic
vegetation on water quality are poorly understood.
Also the problem with the selectivity of accumulation
of elements by the macrophytes is yet to be studied
properly (Monni et al. 2000). The present situation in
many coastal waters does not provide an optimistic
view (Samecka et al. 2001).
Lake Sevan was once a reservoir of water fit for
drinking, according to the physical, chemical, and
biological indices. But today, as a result of the
intensive exploitation of the lake over the years, its
ecological system has been disturbed, with falling
water level and resultant swamping bringing about
qualitative changes, and the state of its native fish life,
the most sensitive index of the health of the lake, has
changed.
The Sevan basin has a unique and relatively
abundant flora and fauna. The flora of the lake basin
is typical to the highlands of the Transcaucasus
Region. Here seems to be the greatest diversity in
plants (Vardanyan 2002). Along the shoreline of the
lake, the greatest artificial woodland of the country is
situated which gives a number of interesting
examples of natural and human affected successions.
Aquatic associations (plankton, benthos and
ichthyofauna) are qualitatively poor with only a few
dominant species, which simplified studies on
ecological relationships (food web etc.).
About 1,600 species of vascular plants (50% of
Armenias flora) have been registered in the lake
basin. Of them, 48 species are in the Red Data Book
of Armenia. The dominant communities of the Sevan
basin are mountain steppe, sub-alpine and alpine
vegetation (Barseghyan 1990).
Surface water in Armenia, and especially in
Sevan Basin, generally seems to be of remarkably
high quality, as compared to international standards.
Groundwater resources are very well protected from
pollution. Spring water usually is of good quality and
can be used for drinking without further treatment.
However, without proper attention the situation could
change easily. The discharge of industrial pollutants,
domestic sewerage and agricultural run-off into the
lake increases the organic loading. Decomposition of
organic matter decreases the oxygen concentrations
of the water body. In Lake Sevan in the 1970s
oxygen saturation in the bottom water of the
profundal during the stratification period were close
to analytical zero (Babayan et al. 2003). Worsening
of oxygen conditions may seriously contaminate the
water, endangering the plant and animals living
therein. Dumping of garbage is a big problem for
urban areas, especially for Sevan, Gavar, and Martuni.
Taking in consideration the role of macrophyte
in Sevan basin and the fact that mentioned issues

1030

have not been elucidated in the region, we proceeded


to study the heavy metal accumulation peculiarities in
macrophyte elucidation. Such discussions and
investigations have become especially urgent over
last few years keeping metal pollution of the
environment (especially aquatic media) in view.
Macrophytes are at the priority level in the list of
cleaning and detoxification methods. Important
functions of the lake ecosystem include the direct
retention of nutrients and toxic substances during the
growth period as well as by forming biotic structures
for biofilms degrading organic and toxic substances;
for epiyphytic algae and macroinvertebrates; and for
providing measures for protection and redevelopment
of juvenile fishes.
The aim of the present work was to investigate
total concentrations of metals in ten of the most
abundant aquatic macrophytes existing in the littoral
zone of the Lake Sevan. Due to the high sensitivity of
the used analytical method (inductively coupled
plasma mass spectrometry; ICP-MS) elements not yet
determined before in these plants species could be
assayed. This study is done under the Sevan
Management Information System (SEMIS) project.
The project focuses on the fact that shore macrophyte
vegetation has decreased immensely due to the direct
loss of littoral area by lowering the lake level, the
consequential increase of shore erosion and the
unstable growing conditions due to the water level
fluctuations.
MATERIALS AND METHODS
Sampling site
The present study reports on the uptake of heavy
metals, by aquatic macrophytes in Lake Sevan area.
Lake Sevan is situated in the north-eastern part of
Armenia. It is the greatest lake of the Caucasus
Region and one of the greatest freshwater high
mountain lakes of Eurasia (Fig.1). Before the
increased artificial outflow which began in 1933, the
surface of Lake Sevan was at an altitude of 1916.20
m above mean sea level with a surface area of 1,416
km2 and volume of 58.5km3 (Babayan et al. 2003).
The decrease in water-level (about 20m) influenced
an array of hydrological and ecological conditions.
The Lake Sevan watershed is located at the
intersection of the Caucasian, Iranian and
Mediterranean flora regions, each of which has its
own distinctive plant assemblies. The range in
altitude, sharp fluctuations in relief and soil
variability create numerous landscape types that
promote diversity in flora and plant associations. The
watershed is known to contain over 1,500 species of
flower and seed-producing and more than 250 species
of spore-producing plants such as mosses and lichens.
In addition, a large number of endemic (local
varieties specific to the Sevan Basin) and relict
(representatives of old disappearing flora) species can

be found in the watershed (Barseghyan 1990). Many


of these endemic and endangered plants have highly
restricted areas of coverage and are sensitive to
changes in environmental conditions.
Concentrations of heavy metals such as Hg, Cd,
Co, Cu, Ni, Pb, Tl and Zn were measured in
macrophytes and water samples from the mouth of
four rivers namely, Gavaraget (sampling site No A),
Argichi (site No B), Makenis (site No C), Masrik
(site No D), each of them meeting the Lake Sevan
(Fig.2).
Water and plant samples
Water samples were collected from four sites (Fig. 2)
along the Lake shore: site A (Gavaraget), site B
(Argichi), and site C (Makenis) and site D (Masrik)
during our field trip on July 15, 2006. All samples
were stored in clean polyethylene bottles under
freezing temperature until analysis. Measurements of
temperature, dissolved oxygen (DO), and pH were
performed in the field.

Ten plant samples with similar sizes from each


species (table 1) were collected at sites. The plants
were thoroughly washed at the sampling site with a
jet stream of tap water until the surfaces appeared to
be clean. The bulk water was removed by vigorous
shaking of the plants and then by air-drying for 3 h.
Plants were packed into paper bags and transported to
the laboratory. There, the samples were washed
several times with deionized water, air-dried and then
placed in a drying oven at 700C for 6 h. Microscopic
inspection of plant surfaces did not show any visible
deposits of solid matter on it.
A composite sample from each group of ten
plants was prepared by mechanically grinding all of
them, using a stainless steel grinder, and then by
careful homogenization of the powder. Before
analysis, aliquots of this powder were again dried
overnight at 700C.

Figure 1: Location of the Lake Sevan (Armenia).

1031

Figure 2: Sampling locations in the Lake Sevan Basin.

Table 1: Macrophyte samples from Sevan Lake


(Armenia)
No

Name

Family

Batrachium rionii
(Lagger.) Nym.
Myosotis palustris
Lam.
Lythrum salicaria
L.
Scrophularia alata
Gilib.
Calamagrostis
epigeios (L.) Roth.
Lepidium
latifolium L.
Glyceria plicata
Fries.
Veronica
anagallis-aquatica
L.
Sparganium
erectum L.
Butomus
umbellatus L.

Ranunculaceae

Sampling
site
C

Boraginaceae

Lythraceae

Scrophulariaceae

Poaceae

Brassicaceae

Gramineae

Scrophulariaceae

Sparganiaceae

Butomaceae

2
3
4
5
6
7
8

9
10

Digestion of the samples:


The acidified and filtered water samples were
analyzed directly, whereas plant materials were

1032

submitted to an acid mineralization procedure prior to


ICP-MS (Elan 6000, Perkin Elmer-Sciex, Canada)
measurements. Glass and plastic ware were
decontaminated by immersing them for 2 days in
10% (v/v) Extran R_ solution (MERCK), followed
by immersion for 3 days in diluted HNO3 (10% v/v)
and finally rinsing with Milli-Q water. All chemical
reagents used in this process were of at least
analytical grade.
The samples were milled in a metal-free ball
mill (ZrO2). An amount of 500 mg sample was
weight into PTFE-vessels and 5 ml HNO3 and 1 ml
H202 (high analytical grade) were added. The samples
in closed vessels were left at room temperature over
night, and then the vessels were put into a
microwave-heated pressure digestion system (MLS
1200, MLS GmbH, Germany). They were digested
for 20 minutes at 800 W and left to cool down to
room temperature. After that the digests were
transferred to 25-ml volumetric flasks and filled up to
the mark with ultra pure water.
Measurement of the elements:
The elements Cd, Co, Cu, Ni, Pb, Tl and Zn were
measured by ICP-MS. The instrument was equipped
with a Scott type Rhyton spray chamber and a
quadrupole mass filter. Rh (10g/l) served as an

internal standard. The samples were diluted as


appropriate by 2% HNO3-solution and measured
against external calibration curves.
Hg was measured by flow-injection hydride
generation Atomic Absorption Spectrometry (AAS).
The samples were mixed with a sodium-borohydride
solution in an automated system. Elementary Hg
formed due to the reduction was removed from the
solution by a stream of Ar and transferred to a quartzcell.
We determined the concentration of metals in
water, plant, and sediment samples by Inductive1y
Coup1ed Plasma- Optica1 Emission Spectrometry
(ICP- OES; EN ISO 11885; for Ni, Zn), ICP-MS
(DIN 38406-29; for Cd, Co and Cu) and by Cold
Vapour Atomic Emission Spectrometry (CV-AAS;
DIN EN 1483; for Hg).
The study on the uptake of heavy metals by
plant from contaminated soils is based on the analysis
of plant samples after pressure digestion for 20
minutes with 5 ml HNO3- and 1 ml H2O2. Soils were
digested with aqua regia (DIN ISO 11466; 1997).
RESULTS
Water samples
General water parameters showed little differences
between the four selected sites. The temperature was
15 0.70C and the pH was 7.25-7.95). Details of
other parameters are shown in table 2.
Water samples for heavy metal analyses were
collected from four rivers namely; Masrik, Argichi,
Makenis, and Gavaraget. Concentrations of heavy
metals such as Cd, Co, Cu, Ni, Pl, Tl, Zn and Hg
were estimated. Concentrations of Co (<0.5g/l), Cd
(<0.5g/l), Tl (<0.1g/l) and Hg (<0.3g/l) in water
were in the same range for the all sites. For Cu, the
highest concentration (2.4g/l) was recorded in
Gavaraget and the lowest (1.3g/l) was in Makenis
(Fig. 3). For Ni, the highest concentration was in
Masrik (3.5g/l) and the lowest in Gavaraget
(1.4g/l). For Pb the highest (1.3g/l) concentration
was in Gavaraget and at the rest of the sites the value
was always <0.5g/l. Zn was the highest (34.6g/l)
in Gavaraget and the lowest (<0.5g/l) in Masrik and
Makenis. It was quite obvious that the water in the
Gavaraget was most polluted in terms of load of
different heavy metals (Fig. 3 and table 3) which
might be attributed to the discharge of untreated
sewage from the city of Gavaraget into the river.

as the water from this habitat is being used for


drinking and irrigation.
Table 2. Water parameters in the rives
Index/river
pH
HCO-3
(g/m3)
Cl(g/m3)
Ca2+
(g/m3)
Mg2+
(g/m3)
SO42(g/m3)
Total Ions
(g/m3)
NH4+
(g/m3)
NO2(g/m3)
NO3(g/m3)
Nmin
(g/m3)
PO43(g/m3)
BOD5
(gO2/m3)

Gavaraget
7.25

Argichi
7.6

Makenis
7.8

Masrik
7.95

158.5

98.6

92

171.3

26.4

12.5

13.3

17.4

23.7

20.8

18.6

30.4

18.4

9.6

9.3

18.4

28.2

21.5

22.3

26.3

259

165

157

267

0.29

0.15

0.05

0.14

0.008

0.005

0.002

0.009

2.86

1.86

1.12

2.63

3.16

2.02

1.18

2.8

0.26

0.11

0.08

0.14

3.83

3.51

2.2

3.65

Table 3: Occurrence of heavy metals in the river


Rivers

Masrik

Argichi

Makenis

Gavaraget

Heavy
metals*
Cd
Co
Pb
Tl
Zn
Hg

<0.5
<0.5
<0.5
<0.1
<5
<0.3

<0.5
<0.5
<0.5
<0.1
5
<0.3

<0.5
<0.5
<0.5
<0.1
<5
<0.3

<0.5
<0.5
1.3
<0.1
34.6
<0.3

*Concentration in g/l

Plants
Analyses of metal accumulation in plants have
practical values in outlining ore deposits of variety of
metals and also in making of new discovery. The
concentration of heavy metals in 10 aquatic
macrophytes from Lake Sevan is shown in Fig.s 3-5.
The present study has greater significance; especially

Figure 3: Concentrations of Ni and Cu in four rivers.


In general, Hg (0.02mg/kg), Co (3.00mg/kg),
Cd (0.46mg/kg) Pb (6.90mg/kg), Cu (18.90mg/kg),
Tl (1.13kg/kg) and Zn (113.00mg/kg) were the
1033

maximum in Batrachium rionii. Only Ni (5.50mg/kg)


was the maximum in Glyceria plicata (Fig. 4-5). The
minimum accumulation of Cd (0.03mg/kg), Co
(0.11mg/kg), Ni (0.94mg/kg), Pb (0.22mg/kg) and Tl
(0.01mg/kg) were observed in Butomus umbellatus
whereas, Cu (3.1mg/kg) and Zn (14 mg/kg) were in
its minimum in Lepidium latifolium.
It is quite interesting to note that the
macrophytes accumulated toxic heavy metals like Hg,
Cd or Tl several hundred folds than that of the water
bodies where these metals were always below
detection limit. This shows the unique properties of
these plants in purifying the water by means of
entrapment of the heavy metals in their tissues.
DISCUSSION
Factors such as light intensity, oxygen tension and
temperature are known to affect the uptake of
minerals (Devlin 1967). Moreover, the energy
derived from photosynthesis and the oxygen released
can improve conditions for the active absorption of
elements. However, interactions between metals are
often complex, and they are dependent on the metal
concentration and pH of the growth medium
(Balsberg-Pohlsson 1989).

Figure 5: Concentrations of Cd (upper panel), Cu and


Pb (middle panel) and Zn (lower panel) in ten plants
collected from the Lake Sevan Basin Rivers.

Figure 4: Concentrations of Hg (upper panel), Co and


Ni (middle panel) and Tl (lower panel). in ten plants
collected from the Lake Sevan Basin Rivers.

1034

The effects of trace elements in an aquatic


ecosystem can be assessed by changes in the
community structure, physiological activity and
ultrastructural components of macrophytes (Chester
and Stoner 1974; Bohn 1975; Gunterspergen et al.
1989; Blaylock and Huang 2000). However,
comparison of metal content in macrophytes is often
difficult because of differences in sampling time (age
of plants) and presence of pollution sources.
Moreover, the metal data cannot be extrapolated from
one species to another or even within the same
species, largely due to different accumulation rates.
Nevertheless, copper (Cu) is known to reduce
photosynthesis rates and respiration of aquatic moss,
Fontinalis antipyretica (Vazguez et al. 2000). In
eutrophic lakes, such as the Sevan Lake, very high
local concentrations of metals often occur as a result
of the strong reducing environment coupled with
industrial and municipal discharges (Vardanyan
2002). Sevan Basin rivers have in and out flow of
freshwater that may reduce the rate of metal
accumulation in aquatic macrophytes.
Driel and Groot (1974) have studied the metal
uptake, translocation and effects in plants growing on

naturally polluted and unpolluted sediments. Their


results suggest that aquatic plants may facilitate the
transportation of metals from sediments up into
shoots. The metals are thereby made available to
grazing mollusks and, thus, reintroduced into the
food web via fish to birds and humans (Brown and
Chow 1977). In addition, macrophytes in shallow
coastal zones function as living filters for nutrients
and metals that become bound to living plant material
and remain in the inner archipelago areas (Sawidis et
al. 1995).
The problem of environment protection and
rational utilization is extremely urgent today and its
solution requires availability of great amount of
ecological
information.
Hydrochemical
and
hydrobiological investigations provide the main part
of such information. The increasing interest to the
lake basin study with respect to the earlier mentioned
information is related to eutrophication of the Lake
Sevan due anthropogenic activities. Besides
hydrological
factors
anthropogenic
impact,
recreational load, settlements growth, industry and
agricultural development affected the lake water
quality and hydrobiont quantitative and qualitative
development.
However, one should recall that an increase in
the concentration of these microelements in water is
toxic for hydrobionts. Many of them produce toxic
salts that occur in very low concentrations and
therefore for their determination special methods
with high determination accuracy, i.e. where
determination error ratio is minimal, are required.
One of the major properties of heavy metals is their
ability to interact with a number of organic
compounds that produce relatively strong complex
ionic compounds such as cyanide, radonide and
thiosulfates by combining with ions (Babayan 1988).
The microelements such as Cu, Zn, by
combining with proteins of special type, produce
compounds that form bases of several enzyme
systems. A decrease in the concentration of Cu or Zn
in a nutrient medium may cause different functional
disorders, such as choroids. Availability of copper in
sufficient levels in plants is essential to provide effect
of Zn and Mn in plants (Heisey and Damman 1982).
Deficiency of Zn causes a reduction in leaf size effect,
yellow pigmentation of leaves, a reduction of fruit
size effect, inhibition of young shoot growth (Bryan
1976). Zn is a component of several enzymes. Iron
is a part of a number of oxidizing emzyms, plays a
leading part in respiration function, and participates
in photosynthesis and oxide reducing reactions in
cells as a mediator of electrodes (Kamal et al. 2004).
Compared with other heavy metals, copper has
the most toxic effects upon the growth and
development of plants. A 1 mg/l concentration of
copper may cause a withering of a plant (BalsbergPohlsson 1989). Copper affects the oxidizing system
of a cell and is a compound of several enzyme
systems.

It has been revealed that though the


microelements Zn, Mo and Cu play a leading part in
photosynthesis activity of plants and contribute in
transfer of assimilators from leaves to generative
organs and roots in plants, even a slight increase in
the concentration of these elements in nutrient
medium may inhibit mainly the growth and
development of plants (Balsberg-Pohlsson 1989;
Guilizzoni 1991). The microelements Co, Zn and Cu
increase the drought-resistance of plants. Several
microelements directly participate in the build-up of
enzymes that act as catalysts in protein, carbohydrate
and other cellular compounds exchange processes
(Vangronsveld and Clijsters 1994).
Heavy metals generally penetrate from aquatic
medium into human through waterplanthuman or
waterplantanimalhuman
biological
chains
(Smirnova 1984). Therefore finding solution to the
problem of toxin tolerance in an aquatic medium is
essential for an ecosystem and its components. There
are reports with a variety of data detailing the effects
of heavy metals on water and water plant structure
and their properties, their enzymatic activity and
nutrition pattern (Wittman 1979). A negative
correlation was revealed between heavy metal
content in growth medium and plants submerged
organs and green biomass (Zayed et al. 1998).
However these peculiarities are not always welldefined and greatly depend on the plant spices and
compound forms of certain metals (Clemens et al.
2002.).
The effect of microelements on metabolism
process is closely realated with composition of
nutrient medium where the plants develop. For
instance, our experiments indicate that plants of one
species taken from different riverbank sites show
different rates of heavy metal content (Vardanyan
and Ingole 2006).
High concentration of heavy metal salts in
storage reservoirs may depend on both geochemical
peculiarities of the area and water inflow. If in the
former case, aquatic organisms have developed some
properties that are helpful in adaptation to the
medium during long evolutionary process, then in the
latter case aquatic organisms are exposed to injurious
effects because of water pollution by heavy metals
from industrial waste.
Water plants, by accumulating heavy metals in
their tissues, play an important role in heavy metal
transport mechanism. Experiments showed that
plants accumulate 2.5 kg zinc from 1 hectare water
surface (Fritioff and Greger 2001). Submerged
vegetation accumulates heavy metals (Cu and Cr) 4-9
times more than riverside vegetation do. The
accumulation ratio of magnesium and copper in
respect to/against their content in the medium is the
highest about 10 times in moss (Fontinalis).
Submerged water plants, particularly hornwort
(Ceratophyllum) accumulate mercury, particularly its
inorganic compounds and they are so rapid in so

1035

doing that a balance with the solution is established


in after two hours (Vardanyan and Ingole 2006).
Riverside vegetation also take up and
accumulate mercury very rapidly, especially by
underwater part/segment of the stem. Reed leaves
can even evaporate mercury vapour into atmosphere,
by taking it up from soil and bottom deposits,
especially under optimum lighting and high
transpiration factors (James et al. 1980). The
accumulation of heavy metals in plants greatly
depends on the concentration of these microelements
in the medium. Experiments studying microelement
accumulating properties of water plants revealed that
they 'prefer' Mn, Ni, Cu, Mo, V, Sr, Ba, Fe, Al
(Greger 1999). Chemical analysis of higher plants
taken from industrial sewage polluted storage
reservoirs indicate that accumulation of heavy metals
by aquatic plants reduces concentration of these
microelements in the water (Samecka et al. 2001).
This study was targeted to gain a better
understanding of the importance of aquatic plants in
heavy metal accumulation and detoxification
mechanisms that may lead to elaboration of new
pollution control and prevention facilities aimed to
reserve the lakes ecosystem. Many of plant species
investigated in the study were recognized as
medicinal and edible ones.
CONCLUSION
From the present observations, it is concluded that
there is a uniform pattern of heavy metal variation in
the macrophytes of Lake Sevan Basin. In general,
values of some metals like zinc and lead were high in
almost all the specimens. Since the investigations on
the heavy metals accumulation in macrophytes of
Sevan Lake were carried out after a long time, hence
the results presented here could be very useful for
environmental monitoring and checking the health of
the water body. The data presented here is
indispensable information for studies of related
nature. The aquatic macrophytes were found to be the
potential source for accumulation of heavy metals
from water and wetlands. Therefore, such studies
should become an integral part of the sustainable
development of the ecosystems and pollution
assessment program.
Among various future tasks related to habitat
technology, priority should be given to the restoration
and creation of coastal nurseries such as macrophyte
beds. There is an urgent need to study more of those
specific macrophytes which are responsible for
cleaning the water body from toxic heavy metals. It
would be advantageous to understand the similarities
and differences between accumulation pathways
across different macrophyte for effective deployment
in phytoremediation, as well as to identify new
macrophytes capable of such activities.

1036

ACKNOWLEDGEMENTS
This study was carried out as a part of the SEMIS
international project, funded by the Volkswagen
Foundation.
REFERENCES
Babayan, A., Hakobyan, S., Jenderedjian, K., Muradyan, S.,
Voskanov, M. 2003. Lake Sevan, Lake Basin
Management Initiative Experience and Lessons
Learned Brief. Lake Basin Management Initiative
Regional Workshop for Europe, Central Asia and the
Americas held at Saint Michaels College in Vermont,
USA, 18-21 June.
Babayan, G.G. 1988. Dynamics of some heavy metals and
types of their migration in Lake Sevan, Candidate of
Geology dissertation, 115.
Baker, A.J.M. and Brooks, R.R. 1989. Terrestrial higher
plants which accumulate metallic elements - a review
of their distribution, ecology and phytochemistry.
Biorecovery 1: 81-126.
Baker, A.J.M., Reeves, R.D. and McGrath, S.P. 1991. In
situ decontamination of heavy metal polluted soils
using crops of metal-accumulating plants - A
feasibility study. pp. 600-605. In Hinchee, R.E. and
Oflenbuttel, R.F. (eds.), In Situ Bioreclamation:
Applications and Investigations for Hydrocarbon and
Contaminated Site Remediation. Battelle Memorial
Institute, Columbus, OH. Butterworth-Heinemann,
Boston, MA.
Balsberg-Phlsson, A.M., 1989. Toxicity of heavy metals
(Zn, Cu, cd, Pb) to vascular plants. A literature
review. Water Air and Soil pollution. 47: 287-319.
Barseghyan, A.M. 1990. Marsh aquatic vegetation of
Armenian SSR. Publ. of NAS RA, pp.353.
Bastian, R.K., Hammer D. 1993. The Use of Constructed
Wetlands for Wastewater Treatment and Recycling. p.
59. In Moshiri, G.A. (ed.). Constructed Wetlands for
Water Quality Improvement, Lewis Publishers, CRC
Press: Boca Raton, Fl.
Bishop, P., and DeWaters, J. 1986. Heavy metal removal
by aquatic macrophytes in a temperate climate
aquatic treatment system. Proceedings: International
Conference on Innovative Biological Treatment of
Toxic Wastewaters, Arlington, VA, 100-117.
Blaylock, M.J, Huang, J.W. 2000. Phytoextraction of
metals.
In:
Raskin
I,
Ensley
BD,Eds.
Phytoremediation of Toxic Metals Using Plants to
Clean Up the Environment, John Wiley and Sons,
New York.
Bohn, A. 1975. Arsenic in marine organisms from west
Greenland. Mar. Pollut. Bull. 6: 87-89.
Brix, H., and Schierup, H.H. 1989. The use of aquatic
macrophytes in water pollution control. Ambio
18:101107.
Brown, J.R. and Chow, L.Y. 1977. Heavy metal
concentrations in Ontario fish. Bull. Environ. Cont.
Toxicol. 17:190-195.
Brown, M.T., and Hall, I.R. 1990. Ecophysiology of metal
uptake by tolerant plants. Pp 95104 in Shaw AJ (ed.)
Heavy Metal Tolerance in Plants: Evolutionary
Aspects. Boca Raton: FL: CRC Press.
Bryan, G. W. 1976. Heavy metal contamination in the sea.
In: Marine Pollution. Johnston, R. (ed.). London:
Academic Press, pp. 185-302.

Cardwell, A.J., Hawker, D.W. and Greenway, M. 2002.


Metal accumulation in aquatic macrophytes from
southeast Queensland, Australia. Chemosphere. 48:
653-663.
Chester, R. and Stoner, J.H. 1974. The distribution of Zinc,
nickel, manganese, cadmium, copper and iron in
some surface waters from the world ocean. Mar.
Chem. 2:17-32.
Clemens, S., Palmgren, M.G., Kramer, U. 2002. A long
way ahead: understanding and engineering plant
metal accumulation. TRENDS in Plant Science.
7:309315.
Devlin, R. M., 1967. Plant Physiology. Reinhold, New
York, 564.
Driel, W. van and de Groot, A.J. 1974. Heavy metals in
river sediments. Geol. Mijnbouw 53:201-203.
EN ISO 11885. 1997. Detennination of 33 elements by
inductive1y coup1ed plasma atomic emisiion
spectroscopy.
EPA. 2000. US Environmental Agency Report EPA/600/R99/107, Introduction to phytoremediation. 72.
Flathman, P.E., and Lanza, G.R. 1998. Phytoremediation:
current views on emergent green technology. Journal
of Soil Contamation. 7: 415432.
Fritioff, A, Greger, M. 2001. Submersed plant species for
removal of copper, zinc and lead from stormwater.
Abstract, ICOBTE, 6th Internatioal Congress on
Biogeochemistry of Trace Elements, Guelph, August
2001.
Gardea-Torresday, J.L., Peralta-Videa, J.R., De La Rosa,
G., and Parsons, J.G. 2005. Phytoremadiation of
heavy metals and study of the metal coordination by
X-ray
absorption
spectroscopy.
Coordnation
Chemistry Reviews. 249: 17971810.
Gibbons, M.V., Gibbons, H.L., Sytsma, M.D. 1994. A
Citizen's Manual for Developing Integrated Aquatic
Vegetation Management Plans. 50
Grato, P.L, Prasad, M.N.V., Cardoso, P.F., Lea, P.J.,
Azevedo, R.A. 2005. Phytoremediation: green
technology for the clean up of toxic metals in the
environment. Brazilian Journal of Plant Physiology.
17:53-64.
Greger, M. 1999. Metal availability and bioconcentration in
plants. In: Prasad MNV, Hagemeyer J, Ed. Heavy
Metal Stress in Plants From Molecules to
Ecosystems, Berlin Heidelberg, Germany, Springer
Verlag, 127.
Guilizzoni, P. 1991. The role of heavy metals and toxic
materials in the physiological ecology of submerged
macrophytes. : Aquatic Botany, 41: 87-109.
Gunterspergen, G.R, Stearns, F., Kadlec, J.A. 1989.
Wetland vegetation. In: Hammer DA, Ed.
Constructed wetlands for wastewater treatment:
Municipal industrial and agricultural. Lewis
Publishers, Chelsea, Michigan, 7388.
Heisey, R.M., Damman, A.W.H. 1982. Copper and lead
uptake by aquatic macrophytes in eastern
Connecticut, U.S.A. Aquatic Botany. 14:213229.
Heisey, R.M., Damman, A.W.H. 1982. Copper and lead
uptake by aquatic macrophytes in eastern
Connecticut, U.S.A. Aquatic Botany. 14:213229.
James, R., Wells, P., Kaufman, B., and Jones, J.D. 1980.
Heavy metal contents in some macrophytes from
Saginaw Bay (Lake Huron, U.S.A). : Aquatic Botany.
9:185-193.

Kamal, M., Ghaly, A.E., Mahmoud, C.R. 2004.


Phytoaccumualtion of metals by aquatic plants.
Environmental pollution. 29:10291039.
Kar, R.N., Sahoo, B.N., and Sukla, L.B. 1992. Removal of
heavy metal from mine water using sulphate reducing
Bacteria. Pollution Research. 11: 113.
Lewis, W.M. 1996. Defining the riparian zone: lessons
from the regulation of wetlands. In: At the waters
edge: the science of riparian forestry. Conference
Proceedings June 19-20, 1995. Minnesota Extension
Service. BU-6637-S.
Matagi, S.V., Swai, D. and Mugabe, R. 1998. A review of
heavy metal removal mechanisms in wetlands,
African Journal of Tropical Hydrobiology and
Fisheries, 8: 23-35.
McCutcheon, S.C. and Schnoor, L.L. (Eds). 2003.
Phytoremediation: Transformation and control of
contaminants. Wiley-Interscience, Inc. Hoboken,
New Jersey.
Meharg, A.A. 1994. Integrated tolerance mechanisms constitutive and adaptive plant - responses to
elevated metal concentrations in the environment.
Plant Cell Environment 17: 989-993.
Mejare, M. and Bulow, L. 2001. Metal-binding proteins
and peptides in bioremediation and phytoremediation
of heavy metals. Trends Biotechnology, 19: 6773.
Monni, S., Salemaa, M. and Millar, N. 2000. The tolerance
of Empetrum nigrum to copper and nickel.
Environmental Pollution, 109:221-229.
Nies, D.H. 1999 Microbial heavy-metal resistance. Appl
Microbiol Biotechnol 51:730 50.
Poschenrieder, C., Tolr, R. y Barcel, J. 2006. Can metals
defend plants against biotic stress? Trends in Plant
Science 11: 288-295.
Prasad, M.N.V. and Freitas, H. 2003. Metal
hyperaccumulation in plants - Biodiversity
prospecting for phytoremediation technology.
(Review article). Electronic Journal of Biotechnology.
Prasad, M.N.V., Freitas, H., Pratas, J. 2005. Metal tolerant
plants and biodiversity prospecting to promote
phytotechnologies for cleanup of metals in the
environment. Chap. 25 In: Trace elements in the
environment: Biogeochemistry, Biotechnology and
Bioremediation. M.N.V. Prasad, K.S.Sajwan, and
Ravi Naidu (Eds). (eds) CRCPress, USA. 483-506pp.
Ravera, O. 2001. Ecological monitoring for water body
management. In: Timmerman J.G. (Ed.), Proceedings
of the International Workshop on information for
sustainable water management. (25-28 Sept. 2000)
Nunspeet, NL: 157-167.
Salt, D.E., Smith, R.D. and Raskin, I. 1998.
Phytoremediation. Annual Rev. Plant Phys. Plant
Mol. Bio. 49: 643-668.
Samecka, A., Cymerman, A., and Kempers J., 2001.
Contentracions of heavy metals and plant nutrients in
water, sediments and aquatic macrophytes of
anthropogenic lakes (former open cut brown coal
minces) differing in stage of acidification. The
Science of the Total Environment 281:87-98.
Sawidis, T., Chettri, M.K., Zachariadis, G.A. and Siratis,
J.A. 1995. Heavy metals in aquatic plants and
sediments from water systems in Macedonia, Greece.
Ecotoxicol Environ Safety, 32:73-80.
Say, P.J., Harding J.P.C., and Whitton, B.A. 1981. Aquatic
mosses as monitors of heavy metal contamination in
the River Etherow, Great Britian. Environ. Pollut.
(Series B) 2:295-307.

1037

Smirnova, N. N. 1984. The role of higher aquatic plants in


heavy metal migration in water reservoirs.
Limnology of mountainous water reservoirs. Yerevan,
288-289.
Van Assche, F., Vangronsveld, J. and Clijsters, H. 1990.
Physiological aspects of metal toxicity in plants.
Environmental Contamination (ed. J. Barcelo), 246250. CEP Consultants, Edinburgh.
Vangronsveld, J., Clijsters, H. 1994. Toxic effects of
metals. In: Farago ME. Eds. Plants and the chemical
elements: Biochemistry, uptake, tolerance and
toxicity, VCH, New FL. 149177.
Vardanyan L.G., Ingole, B. 2006. Studies on heavy metal
accumulation in aquatic macrophytes from Sevan
(Armenia) and Carambolim (India) lake systems.
Environment International, Elsevier. 32: 208-218.
Vardanyan, L.G. 2002. Heavy metals concentration in
some dominant aquatic macrophytes from Lake

1038

Sevan. XXI century: Ecological science in Armenia.


Materials of the III Republican Youth Scientific
Conference, Yerevan. 117- 121.
Vazguez, M.D., Fernandes, J.A., Lopez, J., and Carballeira,
A. 2000. Effects of water acidity and metals
concentration on accumulation and within plant
distribution of metals in the aquatic bryophyte
Fontinalis antipyretica. Water Air Soil Poll. 120: 1-19.
Welsh, R.P.H., and Denny, P. 1980. The uptake of lead and
copper by submerged aquatic macrophytes in two
English Lakes. Journal of Ecology, 68, 443-455.
Wittman, G. 1979. Toxic metals. In: Forstner U, Wittman
GTW, Eds. Metal Pollution in the Aquatic
Environment. Springer-Verlag, Berlin, 370.
Zayed, A., Gowthaman, S., Terry, N. 1998.
Phytoaccumulation of trace elements by wetland
plants: I. Duckweed. Journal of Environmental
Quality. 27:715721.