Determination of Heavy Metal Accumulation in Plant Samples by Spectrometric Techniques in Turkey

Applied Spectroscopy Reviews
ISSN: 0570-4928 (Print) 1520-569X (Online) Journal homepage: http://www.tandfonline.com/loi/laps20
Determination of Heavy Metal Accumulation in

Plant Samples by Spectrometric Techniques in
Turkey
Ilker Ugulu
To cite this article: Ilker Ugulu (2015) Determination of Heavy Metal Accumulation in Plant
Samples by Spectrometric Techniques in Turkey, Applied Spectroscopy Reviews, 50:2, 113-151,
DOI: 10.1080/05704928.2014.935981
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Applied Spectroscopy Reviews, 50:113–151, 2015
Copyright © Taylor & Francis Group, LLC
ISSN: 0570-4928 print / 1520-569X online
DOI: 10.1080/05704928.2014.935981
Determination of Heavy Metal Accumulation

in Plant Samples by Spectrometric Techniques
in Turkey
ILKER UGULU
Buca Faculty of Education, Dokuz Eylul University, Izmir, Turkey
Abstract: Heavy metals are significant and extremely persistent environmental pollu-
tants and their toxicity is a problem of increasing significance for ecological, nutritional,
and environmental reasons. Biomonitoring methods are gaining more importance be-
cause they allow for prediction, detection, and control of potential environmental haz-
ards caused by heavy metal pollution. The objective of the present study was to collect
and analyze research on heavy metal accumulation in plant samples using spectrometric
detection techniques in Turkey published between 2003 and 2013. Five main criteria
were predetermined to limit the study and better portray the studies on heavy metal
accumulation using plant samples in Turkey. These criteria were as follows: studies
aiming to determine heavy metal accumulation levels, studies sampling plant species
growing at various localities in Turkey, studies using spectrometric detection techniques,
studies published as journal articles, and studies undertaken between 2003 and 2013.
Consequently, 47 studies that satisfied all criteria were considered and selected for this
investigation. A content analysis method was used for the review and analysis of the
selected studies. The results of the review analysis were grouped under three categories
and the findings obtained in this scope were presented.
Keywords: Biomonitoring, heavy metal pollution, spectrometric techniques, plants
Introduction
Environmental toxicology deals with toxic substances, their negative effects on living
organisms, and environmental pollution assessment (1, 2). The interactions between the
xenobiotics, environment, and organisms may, under certain conditions, result in the degra-
dation of toxic compounds through their modification, inducing changes in the environment
and causing a negative effect on living organisms (3). All constituents of the biosphere are
polluted by a variety of inorganic and organic xenobiotics as a result of anthropogenic activ-
ities and change the normal biogeochemical cycling (1). Among these xenobiotics, heavy
metals and their mobilization in the biosphere, since the beginning of the 20th century, have
become an important issue (4), and during the last 20 years, environmental problems have
become a part of daily life in several countries (5, 6).
Heavy metals are significant and extremely persistent environmental pollutants and
their toxicity is a problem of increasing significance for ecological, nutritional, and
Address correspondence to Ilker Ugulu, Buca Faculty of Education, Dokuz Eylul University,
Izmir 35100, Turkey. E-mail: ilker.ugulu@deu.edu.tr
113
114 I. Ugulu
environmental reasons (7). The term “heavy metals” refers to any metallic element that
has a relatively high density and is toxic or poisonous even at low concentration (8). Heavy
metals as a general collective term are a group of elements with atomic density greater
than 4 g/cm3 or five times or more greater than water (9), which tend to release electrons
in chemical reactions and form simple cations. In the solid and liquid states, they are
characterized by good heat and electrical conductivity and are glossy and opaque. The
metals serving as microelements in living organisms usually occur in trace amounts that are
precisely defined for each species. Both their deficiency and excess negatively affect living
organisms. The strongest toxic properties are characteristic of inorganic metal compounds,
which dissociate well and are easily soluble because they can easily penetrate through cell
membranes and thereby enter internal organs (10).
The circulation and migration of metals in the natural environment are mainly related
to processes such as rock decay, volcano eruptions, evaporation of oceans, forest fires, and
soil formation processes (10). The sources of anthropogenic contamination or pollution of
the environment by heavy metals include industrial exhalations and wastes, agricultural
applications, municipal waste management, metalliferous mining and smelting, energy and
fuel production, and vehicle emissions (10–18). The heavy metals from these sources are
dispersed in the environment and they contaminate soil, water, and air. They also (directly
or indirectly through plants) enter human and animal bodies (10).
Biological monitoring within a quality control program involves the systematic use of
living beings for obtaining valuable information about the quantity and quality of pollutants
in the environment, often due to anthropogenic activities (19). Biological responses can
be considered more representative than data supplied by chemical or physical detectors,
because they are spatially and temporally extensive; moreover, they allow for estimating
both the levels of pollutants and the impact on biological receptors (20). For this reason,
in order to evaluate, reduce, and avoid damaging effects of toxic metals, there has been
an emphasis in the use of natural bioindicators to monitor quality in both urban and rural
environments (21, 22). However, selection of an organism for biomonitoring is an important
criterion for successful scientific study of heavy metal pollution in any environment (23,
24). A suitable biomonitor will indicate the presence of the pollutant and attempt to provide
additional information about the amount and intensity of the exposure (25). With appropriate
selection of organisms, the general advantage of the biomonitoring approach is related
primarily to the permanent and common occurrence of the organism in the field, even in
remote areas; the facility of sampling; and the absence of any necessary expensive technical
equipment (23, 25, 26).
Since the advent of biological materials for monitoring, numerous biomonitors have
been used to observe heavy metal pollution (27). These include mollusks, fish, birds,
cyanobacteria, lichens, mosses, and many parts of plants (tree barks, tree rings, pine needles,
grasses and leaves) (23, 27–32). The responses of plants to high heavy metal content of
soil, sediment, and water vary with species. For instance, some plant species can be injured
by the increased heavy metal content in their environment. On the other hand, some plant
species called “indicators” can tolerate heavy metals, reflecting the external heavy metal
(33), and they can be used as bio-indicators or biomonitors for quality assessment in
aquatic and terrestrial ecosystems (34). In addition, some plants have the capability to
safely accumulate of heavy metals in different ways (12, 33–36).
Effects of Heavy Metals on Plants

Plant samples are more frequently used for ecosystem quality estimation due to their
sensitivity to chemical changes in environmental composition and the fact they accumulate
Heavy Metal Accumulation in Plant Samples 115
pollutants. The use of plants as bioindicators has many advantages, including low costs,
the possibility of long-term sampling, and high availability (1, 2). Nevertheless, like all
living organisms, plants are frequently sensitive both to the deficiency and to the excess
availability of some heavy metal ions as essential micronutrient, while the same at higher
concentrations and even more ions such as As, Cd, Hg are strongly poisonous to the
metabolic activities (8).
The phytoavailability of heavy metals is influenced by a number of factors, such as
climate, atmospheric deposition, the concentration of heavy metals in the soil, the nature of
the soil, and the maturity of the plants at the time of harvesting (37). Plant species behave
differently regarding heavy metal uptake: some of them have high metal contents in their
tissues compared to a very low soil metal concentration, other species have a low uptake of
the metal at quite high soil concentrations, and others have metal concentration reflecting
soil metal contents (38, 39). In addition, the effects of various heavy metals on plants are
indicated in various forms.
Zinc (Zn) is an essential element in all organisms and plays an important role in
the biosynthesis of enzymes, auxins, and some proteins (40). The phytotoxicity of Zn
is indicated by decrease in growth and development, metabolism, and an induction of
oxidative damage in various plant species. Zinc toxicity in plants limited the growth of both
root and shoot (41–43). Zinc toxicity also causes chlorosis in the younger leaves, which
can extend to older leaves after prolonged exposure to high soil Zn levels (42).
Cadmium (Cd), in general, has been shown to interfere with the uptake, transport,
and use of several elements (Ca, Mg, P, and K) and water by plants (44). Plants grown in
soil containing high levels of Cd show visible symptoms of injury reflected in terms of
chlorosis, growth inhibition, browning of root tips, and finally death (45–48).
Copper (Cu) is a minor trace metal, with 70% copper in leaves contained in the
chloroplast of land plants (49, 50). Copper plays an important role in CO2 assimilation and
adenosine triphosphate synthesis. Cu is also an essential component of various proteins
like plastocyanin of the photosynthetic system and cytochrome oxidase of the respiratory
electron transport chain (51). Excess of Cu in soil plays a cytotoxic role, induces stress,
and causes injury to plants. This leads to plant growth retardation and leaf chlorosis (52).
Mercury (Hg) is a unique metal due to its existence in different forms; for example, HgS,
Hg2+, and methyl-Hg. However, in agricultural soil, the ionic form (Hg2+) is predominant
(53). A high level of Hg2+ is strongly phytotoxic to plant cells. A toxic level of Hg2+
can induce visible injuries and physiological disorders in plants (54). A high level of
Hg2+ interferes with mitochondrial activity and induces oxidative stress. This leads to the
disruption of biomembrane lipids and cellular metabolism in plants (55, 56).
Chromium (Cr) is widely distributed in the Earth’s crust, though usually at very low
levels of concentration. Cr compounds are highly toxic to plants and are detrimental to
their growth and development. Chromium stress is one of the important factors that affect
photosynthesis in terms of CO2 fixation, electron transport, photophosphorylation, and
enzyme activities (57).
Lead (Pb) is one of the ubiquitously distributed most abundant toxic elements in the
soil. It exerts adverse effect on morphology, growth, and photosynthetic processes of plants.
A high lead level in soil induces abnormal morphology in many plant species. Lead also
induces proliferation effects on the repair process of vascular plants (58). A high level of
Pb also causes inhibition of enzyme activities (59, 60), water imbalance, and alterations in
membrane permeability and disturbs mineral nutrition (61).
Cobalt (Co) naturally occurs in the Earth’s crust as cobaltite, erythrite, and smaltite.
Plants can accumulate a small amount of Co from the soil. Very little information is
available regarding the phytotoxic effect of excess Co. A phytotoxicity study of Co in
116 I. Ugulu
barley (Hordeum vulgare L.), oilseed rape (Brassica napus L.), and tomato (Lycopersicon
esculentum L.) has recently shown the adverse effect on shoot growth and biomass (62).
Nickel (Ni) is an abundant element naturally found in soil, water, and food (4). An
excess of Ni2+ in soil causes various physiological alterations and diverse toxicity symptoms
such as chlorosis and necrosis in different plant species (63–65). Other symptoms observed
in Ni2+-treated plants were related with changes in water balance (64, 66).
Manganese (Mn) is an essential element for plant growth, though it is required in small
quantities. It is also an important element from the point of view of biochemical activity,
because it associates with an antioxidant enzyme superoxide dismutase. Mn accumulation
in leaves causes a reduction in the photosynthetic rate (67). Another common symptom is
known as “crinkle-leaf,” and it occurs in the youngest leaf, stem, and petiole tissue. It is
also associated with chlorosis and browning of these tissues (68, 69).
Iron (Fe), an essential element for all plants, has many important biological roles in
processes as diverse as photosynthesis, chloroplast development, and chlorophyll biosyn-
thesis. The appearance of iron toxicity in plants is related to high Fe2+ uptake by roots and
its transportation to leaves and via transpiration stream. Excess Fe2+ causes free radical
production that impairs cellular structure irreversibly and damages membranes, DNA, and
proteins (70, 71).
Spectrometric Heavy Metal Detection Techniques

The adequate monitoring and control of heavy metals in the environment and particu-
larly in soil, sediments, and biological samples requires processing a large amount of
samples to characterize the presence and abundance of heavy metals and to reach sig-
nificant conclusions (72). The main methods for the determination of these metals are
inductively coupled plasma–optical emission spectrometry (ICP-OES), inductively cou-
pled plasma–atomic emission spectrometry (ICP-AES), inductively coupled plasma–mass
spectrometry (ICP-MS), flame atomic absorption spectrometry (FAAS), and electrother-
mal atomic absorption spectrometry (ETAAS), mainly using a graphite furnace (GF) as the
atomizer (72–76).
FAAS is the spectrometric method most frequently used due to its simplicity, effective-
ness, and relatively low cost. This method is very suitable for routine measurements. FAAS
has been applied for the determination of heavy metals in biological samples (77). However,
the sensitivity of this technique is usually insufficient for many samples, and the interfering
effect of the matrix components is often a serious problem in FAAS determinations. In most
cases, FAAS requires a digestion and/or preconcentration step prior to detection (76–80).
ETAAS is a powerful tool with sufficiently high detection power and is a widely used
technique to determine the total heavy metal concentration in biological samples (76). The
disadvantage of FAAS is the low transport efficiency of the analyte atoms to the flame due to
nebulization efficiency of the pneumatic nebulizers. To overcome this problem, ETAAS was
proposed. In this method, instead of aspirating the sample to a flame, the sample solution
is put into a holder, usually graphite, on the optical path of the instrument and heated (81).
The direct determination of heavy metals by ETAAS is of great interest because it offers an
easy and rapid analysis. However, the determination of heavy metals in biological samples
by ETAAS is very susceptible to interference (76).
The main drawback of the other spectrometric techniques is the single analyte de-
termination. It is time consuming to complete analysis in the case of multiple analyte
determination (81). Inductively coupled plasma–based techniques (ICP-AES, ICP-OES,
and ICP-MS) have been applied as multi-elemental techniques for the determination of
heavy metals in several biological samples. ICP-OES and ICP-AES can be used as optical
techniques in plasma. The reference to atoms is misleading in a way because most of the
particles are ions in plasma. In addition, the abbreviation AES stands for auger electron
spectroscopy, which is a entirely different method. Therefore, it is better not to use ICP-AES
for emission spectrometry in plasma. ICP-OES is the best abbreviation for this technique
(81, 82). ICP-OES is attractive for trace analysis due to the satisfactory sensitivity coupled
with the advantage of simultaneous determinations of metals with different spectral lines.
Additionally, this technique presents other advantages, such as the increased power of de-
tection and excellent precision and accuracy attainable with modern instruments of high
resolution. ICP-MS has been developed for the determination of trace elements in several
matrices because of its high sensitivity and wide dynamic range. Although there are many
advantages to ICP techniques, they suffer from both spectroscopic and nonspectroscopic
interference. The direct analysis of samples with high organic matrix contents by these
techniques usually causes the plasma to be extinguished. Another negative effect is injector
blocking due to carbon deposition from incomplete oxidation of the organic matrix (76,
83–87).
Rationale and Objective

A close look at the literature on ecology and environmental pollution in Turkey failed
to reveal systematic and careful review of research on heavy metal accumulation. The
absence of this kind of review study encouraged the collection and systematic analyis of
biomonitoring research using plant samples to observe the trends and present common
results. The objective of the present study was to collect and analyze research on heavy
metal accumulation in plant samples using spectrometric detection techniques in Turkey
published between 2003 and 2013.
Method
Research Design
Content analysis was used for the review and analysis of the selected studies. Content
analysis allows scrutinizing what is and what is not within written, verbal, and visual
communications (88). Content analysis can be used in two traditions; for example, as a
method for research design and as amethod for analyzing the data (89). In the present study,
both traditions were employed to design the study and analyze the selected studies.
Criteria for Selecting the Research Studies

Five main criteria were predetermined to limit the study and better portray the studies on
heavy metal accumulation using plant samples in Turkey. These criteria were as follows:
(1) studies aiming to determine heavy metal accumulation levels, (2) studies sampling plant
species growing at various localities in Turkey, (3) studies using spectrometric detection
techniques, (4) studies published as journal articles, and (5) studies undertaken between
2003 and 2013.
Sources of Research Studies

In order to access potentially relevant studies, several sources were consulted. Databases
covering national and international refereed journals were initially listed. Of the databases,
118 I. Ugulu
ULAKBIM, Google Scholar, and EBSCOHOST were preferred for close examination of
the relevant studies.
Analysis
Analysis of the selected studies was undertaken in five steps. These steps were (1) con-
ducting a search of determined key words in the selected sources and gathering the studies,
(2) developing a coding form, (3) excerpting the relevant information from the studies, (4)
constructing a table by considering this information, and (5) analyzing, interpreting, and
summarizing the results.
Search for Studies

Initially, key words determined earlier were investigated within the databases (ULAKBIM,
Google Scholar, and EBSCOHOST). Within these databases, the key words most related
to heavy metal accumulation such as “biomonitoring,” “bioindicator,” “heavy metal accu-
mulation,” “heavy metal pollution,” and “trace element accumulation” were then searched.
Substantial efforts and careful search for the studies within these sources resulted in more
than 60 research papers. These studies were analyzed with regard to five criteria and some
of them were found to be irrelevant, provide insufficient information, or did not meet the
predetermined criteria. Consequently, 47 studies that satisfied all criteria were considered
and selected for this investigation.
Developing Coding Form

Secondly, a coding form was established for extracting the method, sample characteris-
tics, and outcomes in the selected studies in the first step. The dimensions of the coding
form utilized for analyzing the selected studies consisted of six dimensions; for example,
plant species, plant parts used, heavy metals assessed, detection techniques, study area,
and results. This coding form was also discussed with three researchers on ecology and
environmental pollution.
Analyzing and Charting the Selected Studies

In the third step, each selected study was coded using the coding form. Downloaded studies
were read carefully and then a separate coding form was filled out for each study. In the
fourth step, a table (see Table 1) was created to better describe and compare the information
extracted from the studies. This table summarizes the sample characteristics, research
method, and outcomes of the research.
Results and Discussion

The results of the review analysis were grouped into three categories: (1) sample character-
istics, (2) research method (detection technique, assessed heavy metals, study areas), and
(3) outcomes of research. The findings obtained in this scope are presented in Table 1.
Sample Characteristics of the Studies

In 47 studies analyzed within the scope of the literature review, it was found that various
plants were used as biomonitors. Whereas some studies evaluated the average accumulation
Table 1
Methodological description of the selected studies
Studies
Plant parts Heavy Lowest Highest
Year Reference Plant samples used metals levels levels Method Localities
2003 Simsek et al. (120) Corylus avellana L. (Betulaceae) Seed B 13.80 mg/kg 22.20 mg/kg ICP-OES Ordu, Giresun, Trabzon
2003 Baslar et al. (113) Pinus brutia TEN. (Pinaceae) Leaf Cd 0.37 µg g−1 0.54 µg g−1 FAAS Aydin, Balikesir,
Cr 0.83 µg g−1 12.12 µg g−1 Canakkale, Denizli,
Cu 3.10 µg g−1 10.10 µg g−1 Izmir, Kutahya,
Fe 93.13 µg g−1 595.50 µg g−1 Manisa, Mugla
Ni 4.10 µg g−1 10.40 µg g−1
Pb 2.80 µg g−1 12.10 µg g−1
2004 Demirezen and Typha angustifolia L. (Typhaceae) Leaf, root, stem Cd ICP-AES Kayseri
Aksoy (107) Potamogeton pectinatus L. Cr Accumulation values are
(Potamogetonaceae) Cu showed as graphics
Ni
Pb
Zn
2004 Cicek and Koparal Salix alba L. (Salicaceae) Leaf Cd 0.10 mg/kg 7.23 mg/kg FAAS Kutahya
(141) Populus tremula L. (Salicaceae) Cr 0.60 mg/kg 110.00 mg/kg
Robinia pseudo-acacia L. (Fabaceae) Cu 2.10 mg/kg 59.00 mg/kg
Quercus infectoria Oliver (Fagaceae) Fe 86.30 mg/kg 845.80 mg/kg
Pinus nigra Arn. ssp. pallasiana (Lamb) Ni 1.90 mg/kg 81.70 mg/kg
Holmboe (Pinaceae) Pb 0.10 mg/kg 55.00 mg/kg
Zn 1.70 mg/kg 222.40 mg/kg
2004 Yilmaz and Zengin Pinus sylvestris L. (Pinaceae) Leaf Cu 1.52 ppm 24.96 ppm FAAS Erzurum
(114) Pb 13.50 ppm 40.30 ppm
Zn 20.78 ppm 115.01 ppm
(Continued on next page)
119
Table 1
120
Methodological description of the selected studies (Continued)
Studies
2005 Tokalioglu and Allium sativum L. (Liliaceae) Leaf, root, stem Cd 0.20 µg g−1 2.99 µg g−1 FAAS Kayseri
Kartal (109) Allium cepa L. (Liliaceae) Co 0.80 µg g−1 4.49 µg g−1
Raphanus sativus L. (Brassicaceae) Cr 0.16 µg g−1 2.77 µg g−1
Petroselinum crispum (Miller) A.W. Hill. Cu 5.00 µg g−1 16.40 µg g−1
(Apiaceae) Fe 13.10 µg g−1 450.00 µg g−1
Solanum tuberosum L. (Solanaceae) Mn 6.10 µg g−1 67.80 µg g−1
Cucumis sativus L. (Cucurbitaceae) Ni 1.50 µg g−1 8.17 µg g−1
Lycopersicum esculentum L. Pb 1.77 µg g−1 6.49 µg g−1
(Solanaceae) Zn 9.26 µg g−1 45.80 µg g−1
Daucus carota L. (Apiaceae)
Capsicum annuum L. (Solanaceae)
2005 Ozcan (142)a Salvia aucheri var. canescens Aboveground part Al 97.64 ppm ICP-AES Icel
(Lamiaceae) B 37.82 ppm
Cd 1.67 ppm
Co 2.52 ppm
Cr 2.28 ppm
Cu 82.40 ppm
Fe 108.48 ppm
Mn 12.36 ppm
Ni 2.99 ppm
Pb 29.50 ppm
Zn 33.27 ppm
2005 Celik et al. (116) Robinia pseudo-acacia L. (Fabaceae) Leaf Cd 0.36 µg g−1 3.70 µg g−1 FAAS Denizli
−1
Cu 5.64 µg g 20.81 µg g−1
Fe 100.20 µg g−1 3,087.00 µg g−1
Mn 53.60 µg g−1 349.20 µg g−1
Pb 15.11 µg g−1 206.20 µg g−1
Zn 13.02 µg g−1 139.00 µg g−1
2005 Baslar et al. (115) Populus nigra L. (Salicaceae) Leaf Cd 2.10 µg g−1 42.90 µg g−1 FAAS Aydin, Balikesir,
Cu 21.30 µg g−1 169.30 µg g−1 Canakkale, Denizli,
Fe 258.40 µg g−1 3,325.70 µg g−1 Izmir, Kutahya,
Pb 12.10 µg g−1 253.40 µg g−1 Manisa, Mugla
Zn 68.30 µg g−1 143.10 µg g−1
2006 Aksoy and Fraxinus excelsior L. (Oleaceae) Leaf Cd 2.02 µg g−1 3.43 µg g−1 ICP-OES Kayseri
Demirezen (117) Cr 1.01 µg g−1 1.70 µg g−1
Cu 6.62 µg g−1 16.21 µg g−1
Ni 13.42 µg g−1 27.04 µg g−1
Pb 8.02 µg g−1 18.41 µg g−1
Zn 13.22 µg g−1 29.41 µg g−1
2006 Demirezen and Petroselinum crispum (Miller) A.W.Hill. Fruit, leaf, seed Cd 0.24 µg g−1 0.97 µg g−1 ICP-OES Kayseri
Aksoy (110) (Apiaceae) Cu 22.19 µg g−1 76.50 µg g−1
Lactuca sativa L. (Asteraceae) Ni 0.44 µg g−1 13.45 µg g−1
Allium cepa L. (Liliaceae) Pb 3.00 µg g−1 10.70 µg g−1
Solanum melongena L. (Solanaceae) Zn 3.56 µg g−1 259.20 µg g−1
Capsicum annuum L. (Solanaceae)
Lycopersicum esculantum L.
(Solanaceae)
Mentha × piperita L. (Lamiaceae)
Cucumis sativus L. (Cucurbitaceae)
Cucurbita pepo L. (Cucurbitaceae)
Hibiscus esculentus L. (Malvaceae)
Phaseolus vulgaris L. (Fabaceae)
2006 Coskun (112) Pinus nigra Arn. ssp. pallasiana (Lamb) Bark As 0.13 mg/kg 1.91 mg/kg GFAAS Istanbul, Tekirdag
Holmboe (Pinaceae) Cd 0.04 mg/kg 0.68 mg/kg
Cu 1.54 mg/kg 46.70 mg/kg
Pb 0.60 mg/kg 82.20 mg/kg
Zn 6.36 mg/kg 57.70 mg/kg
121
Table 1
122
Studies
2006 Divrikli et al. (108) Rosmarinus officinalis L. (Lamiaceae) Flower, leaf, root Cd 0.20 mg/kg 2.70 mg/kg FAAS Western Anatolia
Ocimum basilicum L. (Lamiaceae) Cr 0.10 mg/kg 9.70 mg/kg
Laurus nobilis L. (Lauraceae) Cu 3.80 mg/kg 35.40 mg/kg
Beta vulgaris L. var. cicla (L) Moq. Fe 30.00 mg/kg 945.30 mg/kg
(Chenopodiaceae) Ni 1.40 mg/kg 11.30 mg/kg
Origanum majorana L. (Lamiaceae) Mn 7.90 mg/kg 152.50 mg/kg
Rumex acetosella L. (Polygonaceae) Pb 0.10 mg/kg 2.80 mg/kg
Centaurium erythraea Rafn Zn 5.20 mg/kg 83.70 mg/kg
(Gentianaceae)
Achillea millefolium L. (Asteraceae)
Allthae officinalis L. (Malvaceae)
Lavandula angustifolia Miller
(Lamiaceae)
Verbascum sp. (Scrophulariaceae)
2006 Yilmaz et al. (111) Aesculus hippocastanum L. Bark, leaf Cd 0.05 µg g−1 0.06 µg g−1 FAAS Edirne, Tekirdag
(Hippocastanaceae) Cu 0.34 µg g−1 1.02 µg g−1
Pb 0.06 µg g−1 0.62 µg g−1
Zn 0.40 µg g−1 0.66 µg g−1
2007 Onder et al. (143) Lolium perenne L. (Poaceae) Aboveground part Cd 0.09 ppm 0.16 ppm ICP-AES Konya
Co — —
Cr 9.72 ppm 23.02 ppm
Cu 5.02 ppm 10.45 ppm
Ni 5.25 ppm 15.59 ppm
Pb 1.39 ppm 2.14 ppm
V 0.67 ppm 5.66 ppm
Zn 36.43 ppm 64.67 ppm
2007 Dogan et al. (118) Pinus brutia TEN. (Pinaceae) Bark Cd 0.60 µg g−1 0.71 µg g−1 FAAS Aydin, Balikesir,
−1 Canakkale, Denizli,
Cr 0.44 µg g 3.17 µg g−1
Fe 486.35 µg g−1 1,274.04 µg g−1 Manisa, Mugla
Ni 3.56 µg g−1 18.87 µg g−1
Pb 4.59 µg g−1 20.03 µg g−1
2008 Yakupoglu et al. Cichorium intybus L. (Asteraceae) Leaf Pb 3.88 mg/L 19.19 mg/L FAAS Ankara
(119)
2008 Bakirdere and Malus sylvestris Miller (Rosaceae) Fruit, leaf Cd 0.80 ng g−1 98.00 ng g−1 STAT-FAAS FAAS Elazig
Yaman (96) Vitis vinifera L. (Vitaceae) Cr 0.80 ng g−1 5.60 ng g−1
Capsicum annuum L. (Solanaceae) Pb 120.00 ng g−1 866.00 ng g−1
Petroselinum crispum (Miller) A.W. Hill.
(Apiaceae)
2008 Guleryuz et al. (36) Rumex obtusifolius L. (Polygonaceae) Leaf, root, stem Cr 5.00 mg/kg 160.00 mg/kg ICP-MS Bursa
Polygonum lapathifolium L. Cu 8.00 mg/kg 286.00 mg/kg
(Polygonaceae) Mn 7.00 mg/kg 163.00 mg/kg
Urtica dioica L. (Urticaceae) Ni 6.00 mg/kg 152.00 mg/kg
Xanthium strumarium L. (Asteraceae) Zn 15.00 mg/kg 317.00 mg/kg
2008 Akguc et al. (23) Pyracantha coccinea Roem. (Rosaceae) Leaf, stem Cd 0.16 µg g−1 0.36 µg g−1 ICP-OES Mugla
Pb 5.60 µg g−1 14.93 µg g−1
Zn 8.99 µg g−1 15.57 µg g−1
−1
2008 Kaya and Yaman Cupressus sempervirens (Cupressaceae) Leaf Cd 17.00 ng g 180.00 ng g−1 FAAS Gaziantep
(97) Cupressus arizonica (Cupressaceae) Cu 1.60 mg/kg 7.20 mg/kg
Biota thuja (Cupressaceae) Pb 1.00 mg/kg 5,768.00 mg/kg
2009 Baslar et al. (104) Pinus brutia TEN. (Pinaceae) Bark Mn 19.10 µg g−1 24.00 µg g−1 FAAS Western Anatolia
Zn 8.40 µg g−1 14.10 µg g−1
123
124
Table 1
Studies
−1 −1
2009 Saracoglu Armeniaca vulgaris Lam. (Rosaceae) Fruit Al 0.08 µg g 0.22 µg g FAAS GFAAS Kayseri
et al. (121) Cd 0.02 µg g−1 0.72 µg g−1
Cr 4.76 µg g−1 28.90 µg g−1
Cu 0.92 µg g−1 6.49 µg g−1
Fe 10.40 µg g−1 80.10 µg g−1
Mn 0.97 µg g−1 8.27 µg g−1
Ni 2.30 µg g−1 5.83 µg g−1
Pb 0.72 µg g−1 3.77 µg g−1
Se 0.32 µg g−1 0.64 µg g−1
Zn 2.96 µg g−1 12.00 µg g−1
2009 Yaylali-Abanuz and Camelia sinensis (L.) O. Kuntze Leaf Al 0.12 mg/kg 0.61 mg/kg ICP-MS Artvin, Rize, Trabzon
Tuysuz (122) (Theaceae) Cd 0.02 mg/kg 0.12 mg/kg
Cu 2.48 mg/kg 20.50 mg/kg
Fe 0.01 mg/kg 0.05 mg/kg
2009 Baslar et al. Picnomon acarna (L.) Cass. Aboveground Cd — — FAAS Denizli
(144) (Asteraceae) Papaver rhoeas L. part (bushy Fe 0.86 µg g−1 3.84 µg g−1
(Papaveraceae) species), Mn 0.02 µg g−1 0.98 µg g−1
Melissa officinalis L. (Lamiaceae) leaf Ni 0.09 µg g−1 0.84 µg g−1
Viscum album L. (Loranthaceae) Pb 0.22 µg g−1 0.48 µg g−1
Populus nigra L. (Salicaceae) Zn 0.23 µg g−1 0.90 µg g−1
Pyrus communis L. (Rosaceae)
Salix alba L. (Salicaceae)
Juncus acutus L. (Juncaceae)
Quercus coccifera L. (Fagaceae)
Quercus ithaburensis Decne. ssp.
macrolepis (Kotschy) Hedge et Yalt.
(Fagaceae)
Vitis sylvestris Gmelin (Vitaceae)
Ficus caprificus L. (Moraceae)
Rubus sanctus Schreber (Rosaceae)
Ulmus glabra Hudson (Ulmaceae)
Onobrychis sp. (Fabaceae)
Alyssum corsicum Duby (Brassicaceae)
Euphorbia macroclada Boiss.
(Euphorbiaceae)
Coronilla emerus L. ssp. emeroides
(Boiss & Spnun) Uhrova (Fabaceae)
Juniperus oxycedrus L. ssp. oxycedrus L.
(Cupressaceae)
Pinus nigra Arn. ssp. pallasiana (Lamb)
Holmboe. (Pinaceae)
Juniperus foetidissima Wild
(Cupressaceae)
Rosa canina L. (Rosaceae)
Anthemis tinctoria L. (Asteraceae)
Populus tremula L. (Salicaceae)
Hordeum bulbosum L. (Poaceae)
Aegilops umbellulata Zhuk. (Poaceae)
Crataegus monogyna Jacq. ssp. azorella
(Gris.) Franco (Rosaceae)
Pyrus amygdaliformis Vill. var.
lanceolata Drop. (Rosaceae)
Berberis crataegina DC. (Berberidaceae)
2009 Huseyinova et al. Corylus avellana L. (Betulaceae) Leaf Cu 1.80 ppm 33.80 ppm FAAS Ordu
(98) Alopecurus myosuroides Hudson Fe 13.50 ppm 519.90 ppm
(Poaceae) Zn 15.60 ppm 703.60 ppm
Helleborus orientalis Lam. (Continued on next page)
(Ranunculaceae)
125
126
Table 1
Studies
Glechoma hederacea L. (Lamiaceae)
Calamintha nepeta (L.) Savi
(Lamiaceae)
Urtica dioica L. (Urticaceae)
2009 Sasmaz (99) Astragalus gummifer Lab. (Fabaceae) Root, shoot Se 0.22 mg/kg 2.66 mg/kg ICP-MS Elazig
Euphorbia macroclada L.
(Euphorbiaceae)
Verbascum cheiranthifolium L.
(Scrophulariaceae)
2010 Celik et al. (91) Populus × canadensis Moench Bark, leaf Cd 0.50 ppm 2.00 ppm FAAS Tokat
(Salicaceae) Cu 5.00 ppm 14.00 ppm
Fe 39.00 ppm 575.00 ppm
Pb 14.50 ppm 40.00 ppm
Zn 40.00 ppm 1,468.00 ppm
2010 Yildiz et al. (105) Juniperus oxycedrus L. ssp. oxycedrus Aboveground Cd — — FAAS Izmir
(Cupressaceae) part (bushy Fe 0.57 µg g−1 5.98 µg g−1
Phillyrea latifolia L. (Oleaceae) species), Mn 0.17 µg g−1 3.35 µg g−1
Sambucus nigra L. (Caprifoliaceae) leaf Ni 0.02 µg g−1 1.60 µg g−1
Pistacia terebinthus L. (Anacardiaceae) Pb 0.28 µg g−1 1.34 µg g−1
−1
Pinus brutia L. (Pinaceae) Zn 0.23 µg g 1.25 µg g−1
Castanea sativa Miller. (Fagaceae)
Cercis siliquastrum L. (Caesalpiniaceae)
Ruscus aculeatus L. (Liliaceae)
Lapsana communis L. (Asteraceae)
Urtica dioica L. (Urticaceae)
Dryopteris filix-max (L.) Schott
(Aspidiaceae)
Rubus idaeus L. (Rosaceae)
Spartium junceum L. (Fabaceae)
Stachys cretica ssp. smyrnaea Rech. Fil.
(Lamiaceae)
Pyrus amigdaliformis L. (Rosaceae)
Salix sp. L. (Salicaceae)
Juniperus foetidissima Willd.
(Cupressaceae)
Quercus cerris L. subsp. cerris
(Fagaceae)
Vincetoxicum tmolea (Willd.)
(Asclepiadaceae)
Rosa canina L. (Rosaceae)
Euphorbia sp. (Euphorbiaceae)
Genista lydia L. ssp. lydia (Fabaceae)
Lamium pisidicum L. (Lamiaceae)
Tripleurospermum sp. (Asteraceae)
Plantago maritima L. (Plantaginaceae)
Delphinium peregrinum L.
(Ranunculaceae)
Erysimum caricum L. (Brassicaceae)
2010 Kaya et al. (146) Pinus nigra L. (Pinaceae) Leaf Cd 32.00 ng g−1 283.00 ng g−1 FAAS Gaziantep
Eriobotrya japonica (Thunb.) Lindl. Cu 1.60 mg/kg 8.00 mg/kg
(Rosaceae) Pb 0.70 mg/kg 3,056.00 mg/kg
Armeniaca sp. (Rosaceae)
2010 Yasar et al. (5) Cercis siliquastrum L. subsp. Bark, leaf Cr 1.63 µg g−1 6.12 µg g−1 ICP-OES Istanbul
siliquastrum (Caesalpiniaceae) Fe 44.97 µg g−1 134.74 µg g−1
Ni 2.19 µg g−1 4.47 µg g−1
2010 Kaya et al. (145) Nerium oleander L. (Apocynaceae) Leaf Cd 40.00 ng g−1 172.00 ng g−1 FAAS Gaziantep
Robinia pseudoacacia L. (Fabaceae) Cu 4.30 mg/kg 14.00 mg/kg
Pb 1.00 mg/kg 2,820.00 mg/kg
127
128
Table 1
Studies
2010 Hamurcu et al. (100) Malus communis L. (Rosaceae) Fruit B 4.79 mg/kg 10.60 mg/kg ICP-AES Konya
Cornus mass L. (Cornaceae) Cd 0.06 mg/kg 0.16 mg/kg
Prunus sp. (Rosaceae) Cr 0.18 mg/kg 0.32 mg/kg
Rosa canina L. (Rosaceae) Cu 0.05 mg/kg 0.27 mg/kg
Ni 0.26 mg/kg 0.68 mg/kg
Se 5.42 mg/kg 12.96 mg/kg
2010 Akguc et al. (90) Pyracantha coccinea Roem. (Rosaceae) Leaf, stem Cu 5.20 µg g−1 5.89 µg g−1 ICP-OES Mugla
Fe 1.73 µg g−1 9.53 µg g−1
−1
Mn 0.40 µg g 1.00 µg g−1
Ni 4.05 µg g−1 14.34 µg g−1
2010 Arslan et al. (18) Verbascum bombyciferum Boiss. Flower, leaf, Cd 0.01 mg/kg 1.89 mg/kg ICP-OES Bursa
(Scrophulariaceae) root, stem, Cr 0.02 mg/kg 130.86 mg/kg
above- Cu 0.27 mg/kg 23.21 mg/kg
ground, Fe 4.44 mg/kg 46.75 mg/kg
whole plant Ni 0.41 mg/kg 34.82 mg/kg
2010 Dogan et al. (92) Pinus brutia TEN. (Pinaceae) Bark, leaf Cd 0.37 µg g−1 0.71 µg g−1 FAAS Aydin, Balikesir,
−1 Canakkale, Denizli,
Cr 0.44 µg g 12.12 µg g−1
Fe 57.28 µg g−1 1,274.04 µg g−1 Manisa, Mugla
Ni 0.88 µg g−1 18.87 µg g−1
Pb 1.40 µg g−1 20.03 µg g−1
2011 Demirayak et al. Laurocerasus officinalis Roenier Leaf, twig Cd 0.10 ppm 0.15 ppm FAAS Samsun
(40) (Rosaceae) Cu 5.00 ppm 45.00 ppm
Eucalyptus camaldulensis Dehnhardt Pb 1.20 ppm 12.00 ppm
(Myrtaceae) Zn 10.00 ppm 70.00 ppm
Picea abies (L.) Karst (Pinaceae)
Acacia cyanophylla L. (Mimosaceae)
Clematis vitalba L. (Ranunculaceae)
Olea europaea L.var.europaea
(Oleaceae)
Platanus orientalis L. (Platanaceae)
Ligustrum vulgare L. (Oleaceae)
Magnolia grandifora L. (Magnoliaceae)
Phoenix dactylifera L. (Arecacea)
2011 Turan et al. (93) Olea europaea L. (Oleaceae) Leaf Al 3,060.00 µg/kg 37,300.00 µg/kg ICP-MS Aydin
As 2.60 µg/kg 33.00 µg/kg
B 228.00 µg/kg 1, 680.00 µg/kg
Co 2.20 µg/kg 19.00 µg/kg
Cr — 91.00 µg/kg
Cu 33.00 µg/kg 3,850.00 µg/kg
Fe 2,770.00 µg/kg 35,800.00 µg/kg
Li — 400.00 µg/kg
Mn 353.00 µg/kg 4,491.00 µg/kg
Ni 18.00 µg/kg 383.00 µg/kg
Pb — 87.00 µg/kg
Sr 175.00 µg/kg 16,750.00 µg/kg
2012 Ugulu et al. (2) Alyssum fulvescens Sibth. & Sm. ssp. Aboveground Cd — — FAAS Kutahya, Usak
fulvescens (Brassicaceae) part (bushy Fe 0.35 µg g−1 8.89 µg g−1
Cistus creticus L. (Cistaceae) species), Mn 0.07 µg g−1 3.50 µg g−1
Verbascum sp. (Scrophulariaceae) leaf Ni 0.19 µg g−1 6.24 µg g−1
Quercus cerris L. subsp. cerris Pb 0.34 µg g−1 0.72 µg g−1
(Fagaceae) Zn 0.22 µg g−1 1.00 µg g−1
Bupleurum trichopodum Boiss. et (Continued on next page)
Spruner (Apiaceae)
129
Table 1
130
Studies
Stachys cretica ssp. smyrnaea Rech. fil.
(Lamiaceae)
Muscari sp. (Liliaceae)
Vicia cracca L. (Fabaceae)
Pimpinella anisum L. (Apiaceae)
Polygala pruinosa L. (Polygalaceae)
Achillea nobilis L. ssp. sipylea
(Asteraceae)
Cedrus sp. (Pinaceae)
Rhus coriaria L. (Anacardiaceae)
Lolium temulentum L. (Poaceae)
Celtis australis L. (Ulmaceae)
Buglossoides arvensis (L.) Johnston
(Boraginaceae)
Salvia sp. (Lamiaceae)
Orobanche sp. (Orobanchaceae)
Geranium pyrenaicum L. (Geraniaceae)
Euphorbia rigida L. (Euphorbiaceae)
Myosotis alpestris F.W. Schmidt ssp.
alpestris (Boraginaceae)
Alyssum fulvescens Sibth. & Sm
(Brassicaceae)
Euphorbia anacompseros Boiss. ssp.
anacompseros (Euphorbiaceae)
Inula orientalis L. (Asteraceae)
Platanus orientalis L. (Platanaceae)
Pinus nigra Arn. subsp. pallasiana
(Lamb) Holmboe (Pinaceae)
2012 Ozmen and Aksu Vitis vinifera L. (Vitaceae) Fruit, seed Cd — — FAAS Elazig
(94) Co — —
Cu 2.97 mg/L 14.78 mg/L
Fe 10.45 mg/L 33.94 mg/L
Ni — —
Pb — —
Zn 3.95 mg/L 18.83 mg/L
2012 Kaya and Yaman Platanus sp. (Platanaceae) Leaf Cd 7.00 ng g−1 102.00 ng g−1 STAT-FAAS Gaziantep
(101) Olea europaea L. (Oleaceae) Cu 2.70 mg/kg 21.00 mg/kg
Vitis vinifera L. (Vitaceae) Pb 1.40 mg/kg 3,850.00 mg/kg
Armeniaca sp. (Rosaceae)
2012 Avci (106) Capsicum annuum L. (Solanaceae) Fruit Cd 0.01 mg/kg 0.52 mg/kg ICP-MS Gaziantep
Solanum lycopersicum L. (Solanaceae) Cr 1.40 mg/kg 4.80 mg/kg
Solanum melongena L. (Solanaceae) Cu 7.41 mg/kg 60.54 mg/kg
Ni 0.60 mg/kg 6.10 mg/kg
2012 Osma et al. (6) Petroselinum crispum (Miller) A.W.Hill. Leaf Cd 0.24 µg g−1 0.89 µg g−1 ICP-OES Istanbul
(Apiaceae) −1 −1
Cr 3.73 µg g 14.04 µg g
Brassica oleraceae L. var. acephala DC. Cu 1.47 µg g−1 5.19 µg g−1
(Brassicaceae) Ni 3.13 µg g−1 13.65 µg g−1
Beta vulgaris L. var. cicla (L) Moq. Pb 29.28 µg g−1 87.00 µg g−1
(Chenopodiaceae) Zn 3.48 µg g−1 5.74 µg g−1
2012 Ozmen and Aksu Vitis vinifera L. (Vitaceae) Seed, stem Fe 2.31 mg/kg 116.85 mg/kg FAAS Elazig
(95) Zn 1.15 mg/kg 16.17 mg/kg
2013 Karaaslan and Pinus nigra L. (Pinaceae) Leaf Cr 0.16 mg/kg 0.83 mg/kg FAAS Elazig
Yaman (102) Cedrus libani A. Richard (Pinaceae) Ni 0.41 mg/kg 2.06 mg/kg
Cupressus arizonica (Cupressaceae)
131
132
Table 1
Studies
a
2013 Saglam (39) Brassica oleracea var. capitata Fruit, leaf, Cd 0.11 mg/kg ICP-AES Isparta
(Brassicaceae) root Co 0.10 mg/kg
Portulaca oleracea L. (Portulacaceae) Cr 1.09 mg/kg
Vitis vinifera L. (Vitaceae) Cu 12.11 mg/kg
Raphanus sativus L. (Brassicaceae) Fe 68.09 mg/kg
Phaseolus vulgaris L. (Fabaceae) Mn 59.86 mg/kg
Vigna unguiculata (L.) Walp. subsp. Mo 9.56 mg/kg
unguiculata (Fabaceae) Ni 1.57 mg/kg
Pb 0.27 mg/kg
Zn 32.58 mg/kg
2013 Osma et al. (103) Capsicum annuum L. (Solanaceae) Fruit Cd 0.28 µg g−1 0.89 µg g−1 ICP-OES Istanbul
Phaseolus vulgaris L. (Fabaceae) −1
Cr 5.33 µg g 14.04 µg g−1
Solanum melongena L. (Solanaceae) Cu 1.47 µg g−1 5.19 µg g−1
−1
Ni 3.06 µg g 13.65 µg g−1
Pb 29.28 µg g−1 86.20 µg g−1
Zn 3.70 µg g−1 5.74 µg g−1
a
Average accumulation values.
Taxon Number
60
50
Study Number/Percent
40
30
20
10
0
1 2 3 4 4+
f 24 2 7 4 10
% 51 4 15 9 21
Figure 1. Study numbers and percentages according to the plant taxa used.
values of a plant species selected from various localities of the field of study intended for
the determination process of heavy metal accumulation levels by means of biomonitoring
(5, 18, 90–95), studies evaluated accumulation values of various plant species (36, 40,
96–103), and some other studies evaluated the average accumulation values of various
plant species (2, 39, 104–106).
The majority of the studies analyzed (n = 24, 51%) used a sample of a specific plant
species as a data collection tool (Figure 1). It was found that 10 studies (21%) used five or
more plant species as biomonitors, 4 studies (9%) used four plant species as biomonitors,
7 studies (15%) used three plant species as biomonitors, and 2 studies (4%) used two plant
species sample as biomonitors.
When the studies intended for the determination of heavy metal accumulation values
were analyzed based on the systematic properties of the plant samples used as biomonitor,
it was found that 155 taxa from 55 families of plants were used as data collection tools
(Table 1). Further analysis on the families of plants that are used as biomonitors has shown
that the family Rosaceae is represented by the highest number of taxa (19 taxa). Pinaceae is
represented by 15 taxa and Fabaceae and Lamiaceae are represented by 13 taxa. These are
followed by Solanaceae (12 taxa) and Asteraceae (10 taxa). Other families of plants vary
between 1 and 8 taxa based on the species they contain (Figure 2). The genera represented
by the highest number of taxa in the study are as follows: Pinus is represented by 12 taxa,
Verbascum and Vitis by 6 taxa, and Capsicum, Euphorbia, Populus, Quercus, and Solanum
by 5 taxa (Figure 3). In the scope of Pinus, the studies analyzed indicate that the plant
species most extensively used in these studies are Pinus nigra (n = 6) and Pinus brutia
(n = 5).
In the process of preparation of the plant samples for spectroscopic analysis techniques,
it was seen that either various parts of the plants were used or the plant was used whole
(Figure 4). On the other hand, leaves were the most often used plant parts, indicated by
a significant percentage (44%) followed by fruits (n = 8, 11%), bark (n = 7, 9%), roots
(n = 7, 9%), and stems (n = 7, 9%). A comparison of accumulation values based on seasons
134 I. Ugulu
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20
Rosaceae
Pinaceae
Fabaceae
Lamiaceae
Solanaceae
Asteraceae
Brassicaceae
Cupressaceae
Salicaceae
Apiaceae
Fagaceae
Oleaceae
Scrophulariaceae
Vitaceae
Euphorbiaceae
Liliaceae
Poaceae
Cucurbitaceae
Platanaceae
Polygonaceae
Ranunculaceae
Urcaceae
Anacardiaceae
Betulaceae
Boraginaceae
Caesalpiniaceae
Chenopodiaceae
Malvaceae
Ulmaceae
Apocynaceae
Arecaceae
Asclepiadaceae
Aspidiaceae
Berberidaceae
Caprifoliaceae
Cistaceae
Cornaceae
Genanaceae
Geraniaceae
Hippocastanaceae
Juncaceae
Lauraceae
Loranthaceae
Magnoliaceae
Mimosaceae
Moraceae
Myrtaceae
Orobanchaceae
Papaveraceae
Plantaginaceae
Polygalaceae
Portulacaceae
Potamogetonaceae
Theaceae
Typhaceae
Figure 2. Most used families in the selected studies.
and years is one of the most common factors to determine the parts of the plants to be used.
Comparisons of the heavy metal accumulation values were carried out by using several
parts of the plants specified in the aforementioned studies (5, 18, 23, 36, 40, 92, 107, 108).
Measurement of the accumulation on the edible parts of the plants is another efficient factor
to determine the parts of the plants to be used. In particular, this factor is significant in
Genus
13
12
11
10
9
8
Number
7
6
5
4
3
2
1
0
Verbascum Capsicum Euphorbia Quercus Solanum
Pinus sp. Vis sp. Populus sp.
sp. sp. sp. sp. sp.
Genus 12 6 6 5 5 5 5 5
Figure 3. Most used genus in the selected studies.
terms of the studies intended for the determination of heavy metal accumulation values on
vegetables (39, 103, 106, 109, 110).
Various reasons were identified in the determination of the plant species to be used
in the studies. Some studies used plant species such as Aesculus hippocastanum (111),
Pinus brutia (92, 104), and Pinus nigra (112) for data collection tools because they have
been proven to have efficient biomonitoring characteristics; other studies have intended
to analyze the biomonitoring characteristics of the plant species used in addition to the
determination of heavy metal accumulation within the scope of the study (5, 18, 23, 90,
93, 113–118). In various other studies, the samples were chosen based on the plant species
consumed as vegetables in the region and emphasis was put on the effects of heavy metal
pollution on human health (96, 103, 106, 109, 110, 119). In addition, such plants as Corylus
Plant Parts Used

50
45
Number/Percent
40
35
30
25
20
15
10
5
0
Above
Whole
ground Bark Flower Fruit Leaf Root Seed Stem Twig
plant
Part
f 6 7 2 8 34 7 4 7 1 1
% 8 9 3 11 44 9 5 9 1 1
Figure 4. Study numbers and percentages according to the plant parts used.
136 I. Ugulu
avellana (120), Armeniaca vulgaris (121), and Camelia sinensis (122) were selected within
the context of the studies based on the fact that these plants are cultivated in large numbers
and consumed in Turkey and throughout the world.
Methods of the Studies

Study Areas. Turkey, located on the Anatolian peninsula and Thrace region and consisting
of 81 provinces, is a country that has a wide variety of topographical and climatic conditions,
which form the basis of seven different regions: Marmara, Aegean, Mediterranean, Central
Anatolian, Black Sea, Eastern Anatolian, and Southern Anatolian. These regions show
significant varieties compared to each other based on geographical conditions, climate,
transportation, and flora as well as industrialization and population levels. These varieties
also had an effect on the ecological characteristics of the regions and led to different results
among the regions in terms of pollution. The studies conducted in Turkey based on the
pollution results distributed to the provinces and regions provide significant indications
about such results (Figure 5).
An analysis of the studies based on the areas of study indicates that these studies
were conducted based on the determination of heavy metal accumulation in plants in 28
(34.5%) of the 81 provinces in Turkey. Izmir, Denizli, Kutahya, and Mugla provinces were
included in six different studies, more than any other provinces in Turkey (Figure 5). The
distribution of the studies based on the provinces indicates that the studies focus on the
western parts of Turkey. The distribution of the studies based on the regions also supports
this claim. Based on these results, the regions mostly preferred as the areas of study are
Aegean and Marmara regions. On the other hand, the eastern parts of the Black Sea region
stand out compared to other regions. Among the regions specified, Aegean and Marmara
are more densely populated. In addition, these regions are significant for their industrial
and commercial development compared to other regions in Turkey. It can be concluded that
the number of studies conducted in these regions by means of biomonitoring is high due to
the correlation between industrialization and heavy metal pollution.
Assessed Heavy Metals. In the studies conducted in various regions of Turkey with an aim to
determine heavy metal pollution levels in those regions, the biological accumulation values
of 17 metals considered as heavy metals were analyzed (Figure 6). Although accumulation
values have been analyzed for various kinds of heavy metals, the number of studies on each
heavy metal does not indicate a balanced distribution. Lead was the most analyzed heavy
metal in terms of accumulation values (38 studies, 15%), followed by cadmium and copper
(35 studies, 14%), zinc (31 studies, 13%), nickel (27 studies, 11%), iron (23 studies, 9%),
chromium (22 studies, 9%), and manganese (13 studies, 5%). The order of heavy metals
based on the number of studies conducted is as follows: Pb > Cd > Cu > Zn > Ni > Fe >
Cr > Mn. Lithium, molybdenum, strontium, and vanadium were the least analyzed heavy
metals (one study each; Figure 6).
Detection Techniques. An analysis of international studies shows that spectrometric tech-

niques are often used for quantitative detection of heavy metals and metalloids (10). Studies
conducted in Turkey also make use of this technique. Spectrometric techniques are based on
the interaction of electromagnetic radiation with matter in all of its macroscopic and micro-
scopic forms. The most common technique in this group is atomic absorption spectrometry
(AAS) (Figure 7).
Figure 5. Study numbers according to the provinces: (1) Istanbul, (2) Tekirdag, (3) Edirne, (4)
Canakkale, (5) Bursa, (6) Balikesir, (7) Kutahya, (8) Manisa, (9) Izmir, (10) Usak, (11) Denizli, (12)
Aydin, (13) Isparta, (14) Mugla, (15) Konya, (16) Ankara, (17) Mersin, (18) Kayseri, (19) Gaziantep,
(20) Elazig, (21) Samsun, (22) Tokat, (23) Ordu, (24) Giresun, (25) Trabzon, (26) Rize, (27) Artvin,
(28) Erzurum.
The popularity of AAS in quantitative analysis of elements is not surprising due to the
high sensitivity and selectivity of the technique. Moreover, the technique is characterized by
low detectability limits and high precision (10). The basis for more detailed classification of
atomic absorption spectrometry is the type of atomizer used. The most common atomization
138 I. Ugulu
Heavy Metals Assessed

40
35
30
Number/Percent
25
20
15
10
0
Al As B Cd Co Cr Cu Fe Li Mn Mo Ni Pb Se Sr V Zn
f 4 2 4 35 6 22 35 23 1 13 1 27 38 3 1 1 31
% 2 1 2 14 2 9 14 9 0 5 0 11 15 1 0 0 13
Figure 6. Heavy metals according to number/percentage of assessment.
technique was flame atomization (FAAS). The application of FAAS was significantly more
common (53%, n = 26) compared to other techniques (Figure 7). Within the scope of two
studies (96, 101), a slotted tube atom trap (STAT) was used to increase the sensitivity of some
heavy metals like lead and cadmium in FAAS. Another type of atomizer is electrothermal
(ETAAS), also used in determinations of metals. Electrothermal atomization most often
occurs in so-called graphite furnaces (GFAAS). A review of the literature shows that two
studies were carried out using this method (112, 121).
60
50
40
Frequency/Percent
30
20
10
0
FAAS GFAAS STAT-FAAS ICP-AES ICP-MS ICP-OES
f 26 2 2 5 5 9
% 53 4 4 10 10 19
Figure 7. Usage numbers and percentages of heavy metal detection techniques in selected studies.
4
Number
0
2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013
AAS 1 2 3 3 1 3 4 5 1 4 1
ICP 1 1 1 2 1 2 2 4 1 2 2
Figure 8. Usage numbers of heavy metal detection techniques according to the years.
An analysis of the studies showed that classic AES was not used in these studies. How-
ever, combined with a plasma spectrochemical source using inductively coupled plasma
(ICP-OES and ICP-AES) was a development of this method. As a result, a very sensitive
and selective technique was created and used for the quantitative determination of metals in
a variety of environmental samples (10). The findings on the use of this technique indicate
that these developments have also been applied in the studies carried out in Turkey (Fig-
ure 7). In other words, the number of studies using ICP-OES or ICP-AES constitutes 29%
(n = 14) of the total number of studies analyzed. ICP-MS is another convenient tool for the
analysis of trace quantities of metallic elements. It is characterized by a low detectability
limit and good selectivity (10). This system was used in 5 of 47 studies analyzed within the
scope of this study.
When AAS and ICP were compared to each other in terms of their use for the detection
of heavy metal accumulation in plant species, it was found that the use of AAS was more
common except in 2013 (Figure 8). This is most likely due to the fact that AAS is a lower
cost technique. Moreover, it was found that AAS was more often used compared to other
techniques in the studies carried out by Szyczewski et al. (10) and Lemos and Carvalho
(76) to analyze heavy metal accumulation in biological materials.
Outcomes of the Studies

The ecological and human health impacts of elevated environmental metal concentrations
have been known for several decades, and focused research on adverse effects and mitiga-
tion strategies has grown over the past 30–40 years (106). The use of biological materials
and especially plants in the detection of heavy metal accumulation levels plays a signif-
icant role among these strategies. However, the extent to which plants take up elements
depends on several factors, both internal and external. Plants have developed several mech-
anisms that enhance their ability to adapt to environmental conditions and tolerate new
or chemically imbalanced environments. The degree to which any particular species can
140 I. Ugulu
Table 2
Critical toxicity level of a few environmentally important heavy metals in plants (123–127)
Elements Land plants (µg g−1 dry wt)

As < 2–80
Cd 5–30
Co 0.4–several
Cr 5–30
Cu 20–100
Fe 50–200
Mn 200–3, 500
Ni 10–50
Pb 30–300
Se 3–100
Sr 0.3–several
Zn 80–200
tolerate environmental perturbations is variable. Therefore, plant responses to environmen-

tal concentrations of potential stress agents should always be investigated for each particular
system. Nevertheless, some generalizations can be made (Table 2) regarding heavy metal
tolerance and contents in plants and the physiological aspects of plant response (123–127).
Based on these generalizations about heavy metal tolerance and content values in
plants, the results of the studies within the scope of this review were analyzed and a heavy
metal pollution map of Turkey was created (Figure 9). The values of heavy metals illustrated
on the map and determined to be higher than normal accumulation levels provide insight
Figure 9. Heavy metals identified as toxic levels according to provinces.

Heavy metals
20
19
18
17
16
15
14
13
12
Frequency
11
10
9
8
7
6
5
4
3
2
1
0
d (Cd) e (Co) f (Cr) g (Cu) h (Fe) j (Mn) l (Ni) m (Pb) n (Se) o (Sr) q (Zn)
f 11 2 12 19 15 1 10 15 1 1 13
Figure 10. Frequencies of heavy metals identified as being at toxic levels.
with regard to the levels of heavy metal pollution based on the provinces and regions
of Turkey and possible causes of such pollution. Based on the analysis of the pollution
map, the primary observation indicates that heavy metal pollution in the western regions
of Turkey is higher than those of other regions. As previously mentioned, overpopulation,
industrialization, and traffic density in these regions, including Aegean and Marmara, are
the causes of this expected heavy metal pollution. A similar generalization with regard to
regional pollution can be applicable to the eastern parts of the Black Sea region. However,
local copper pollution can be observed in this region instead of other heavy metals.
Based on the analysis of the heavy metal pollution map of Turkey (Figure 9), Cu has
been found among other heavy metals to cause pollution in more localities than other heavy
metals (n = 19; Figure 10), followed by Fe and Pb in 15 localities each. These heavy metals
are followed by Zn in terms of high pollution levels observed in 13 localities. An analysis
of the origins of these heavy metals, considered to be significantly more responsible for
heavy metal pollution in Turkey, shows that the metal industry is a major factor in this
pollution. The heavy metals identified to have high pollution levels based on the number of
localities reported are as follows: Cu > Fe = Pb > Zn > Cr > Cd > Ni > Co > Mn > Se
> Sr (Figure 10).
Among heavy metals, cadmium (Cd) is one of the elements of greatest environmental
concern (118). This concern has been indicated in the studies conducted in Turkey and Cd
has become one of the most prominent heavy metals whose accumulation and pollution
levels have been analyzed in various studies (see Figure 6). Industrial activities such as
mining, ore dressing, and smelting of nonferrous metals, Cd compound production, battery
manufacturing and electroplating, combustion of fossil fuels, iron and steel production,
nonferrous metals production, and municipal solid waste combustion are the main sources
of Cd emissions to air (6, 128, 129). In parallel with these resource data, an analysis of
the provinces and regions where Cd is at toxicity levels shows that Cd pollution is more
common in Western Anatolia where industrial activities are more intensive (Figure 9). The
142 I. Ugulu
provinces where Cd pollution has been detected in Western Anatolia are Aydin, Balikesir,
Canakkale, Denizli, Izmir, Kutahya, Manisa, and Mugla. Based on the Industrial Status
Report of the Provinces of Turkey, issued by the General Directorate of Industry—The
Republic of Turkey, The Ministry of Science, Industry and Technology (130), activities
such as mining and quarrying, machine and equipment manufacturing, and fabricated metal
products manufacturing that cause Cd pollution have an important place in the industrial
activities of these provinces. With regard to other regions, pollution was detected in Elazig,
Gaziantep, and Kayseri provinces. The Industrial Status Report (130) indicates that mining
and quarrying manufacturing came in the first place among the industrial activities in Elazig
and fabricated metal products manufacturing came in second place among the industrial
activities in Kayseri. Cd pollution in these two provinces can be accounted for by these
industrial activities and collateral factors with regard to advanced textile and leather trade
activities are considered as the factors of pollution in Gaziantep.
Chromium (Cr) has many industrial uses, both in its metallic form and in various
compounds (131). The main sources of exposition to toxic forms of Cr are dyes and leather
tanning, when wastes are discharged directly into waste streams, either as liquids or as
solids (132–134). An analysis of the aforementioned heavy metal pollution map shows that
Cr pollution has been observed especially in the western parts of Turkey. The provinces
where pollution has been detected are Aydin, Balikesir, Bursa, Canakkale, Denizli, Istanbul,
Izmir, Kutahya, Manisa, and Mugla (Figure 9). The fact that Bursa and Denizli are the textile
leaders among these provinces accounts for the Cr pollution in the region. Based on the
Industrial Status Report (130), the textile activities in Bursa, Denizli, and Istanbul are in first
place among the industrial activities in these provinces and such textile activities are also
carried out to an extent in the other provinces. Furthermore, an analysis of the distribution
of leather trade activities considered to be another cause of Cr pollution shows that 5 out
of 9 leather trade organized industrial zones are located in Bursa, Denizli, Istanbul, Izmir,
and Manisa. This accounts for another cause of Cr pollution in the region.
In nature, copper (Cu) occurs in rocks, water, and air and is present naturally in the
environment in elemental form, but most commercial production comes from sulfides and
oxide minerals (135, 136). Cu is widely used for electrical equipment; construction, such
as roofing and plumbing; and industrial machinery, such as heat exchangers and alloys.
Cu also has a wide range of other applications in agriculture (nutrients, pesticides, and
fungicides), wood preservation, and medical applications (6, 135). The extensive use of Cu
specified within the context of this study has been indicated in Cu pollution and Cu has
been reported to cause pollution in more localities than any other heavy metals (n = 19;
Figure 10). In addition to Western Anatolia and Marmara, where industrial activities such
as machine and equipment manufacturing and fabricated metal products manufacturing are
carried on a large scale (130), Cu pollution, especially along the coast of the Eastern Black
Sea, is quite significant (Figure 9). Cu has been found to have at toxicity levels in each
province (Artvin, Ordu, Rize, Samsun, Trabzon) located in this region and was included
within the scope of previous studies. Among the most significant causes of Cu pollution in
the region, rich copper deposits in Lahanos-Espiye, Çayeli, Kutlular, Murgul, and Cerattepe
counties and copper processing facilities located in Borçka, Çayeli, and Küre counties can
be considered to be the most significant causes of Cu pollution.
Iron (Fe) is a principle element in the Earth’s crust (115). The main emission sources
of this element are the steel industry, coal burning, and intensive traffic; there may also be
an influence from soil dust, especially in agricultural regions (137). Reported as being the
source of heavy metal pollution in most localities together with Pb subsequent to Cu, Fe
(n = 15; Figure 10) shows a broader distribution throughout Turkey in terms of pollution
compared to other heavy metals. On the other hand, Fe pollution is observed more often in
Western Anatolia (Aydin, Balikesir, Bursa, Canakkale, Denizli, Istanbul, Izmir, Kutahya,
Manisa, and Mugla) due to intensive industrial activities (Figure 9). In addition to Western
Anatolia, Fe accumulation in plant samples obtained from Elazig, Isparta, Kayseri, Mersin,
Ordu, and Tokat provinces has been determined to be above normal limits. Based on the
Industrial Status Report (130), the industrial enterprises related to mining and quarrying as
well as machine and equipment manufacturing remain in the forefront in terms of industrial
activities in these provinces. These industrial activities can be considered to cause high Fe
accumulation values observed in the said provinces.
Nickel (Ni) is a common element naturally found in soil, water, and food (4). Natural
sources of atmospheric nickel are dusts from volcanic emissions and the weathering of
rocks and soils (134, 138). Nickel mainly originates from oil and coal burning, the steel
industry, and smelters (139). This metal is absorbed easily and rapidly by plants (140).
Activities such as oil and coal burning, often observed in heavily populated regions, and the
intensity of industrial activities such as the steel industry and smelters can be considered to
be the causes of Ni pollution in Western Anatolia (i.e., Aydin, Balikesir, Bursa, Canakkale,
Denizli, Izmir, Kutahya, Manisa, and Mugla; Figure 9). In addition, the intensity of activities
such as machine and equipment manufacturing, fabricated metal products manufacturing,
and mining in Konya and Kayseri can be listed among the causes of pollution in these
provinces.
Lead (Pb) has been mined since ancient times and has been known to be toxic since
then (133). World production amounts to millions of tons and it is used in the manufacture
of accumulators, batteries, solders, pigments, cables, ceramics, soldering and building
materials, anti-rust agents, and leaded petrol (6). In addition, some fertilizers, which are
used in many countries, also contain lead (132). Pb has become one of the most significant
causes of environmental problems due to its extensive area of use and a failure to carry
out local control procedures for wastes containing lead. This concern has been indicated
in the studies carried out in Turkey. As a matter of fact, Pb is one of the heavy metals
whose pollution levels have been analyzed more than other heavy metals in a large number
of studies (n = 15; Figure 10). Results of such studies indicate that Pb pollution has been
detected in various localities, especially in Western Anatolia (Figure 9). The availability
of manufacturing facilities for materials such as accumulators, batteries, pigments, cables,
ceramics, and anti-rust agents accounts for the Pb pollution in the region. In addition,
Pb accumulation in plant samples obtained from Elazig, Gaziantep, Kayseri, and Tokat
provinces has been determined to be at high pollution levels. Industrial activities causing
lead (Pb) emissions are extensively carried out in these regions (130).
Zinc (Zn) is a heavy metal that is present in all living structures, plant and animal
(138). Zn is used in various industries, mainly as corrosion protection for steel components
and other metals. It is an important component of various alloys and is widely used as a
catalyst in chemical production (e.g., rubber, pigments, plastic, lubricants, and pesticides).
Zn has been determined as a heavy metals with high accumulation levels based on the
studies carried out in Western Anatolia (Figure 9). In addition, the results of the studies
carried out in Kayseri, Ordu, and Tokat indicate that Zn is at high pollution levels.
Conclusion
One of the most important environmental problems caused by dispersal of industrial and
urban wastes generated by human activities is the heavy metal contamination of soil,
water, and plants. Heavy metals are resistant to degradation and represent an ongoing
144 I. Ugulu
toxicological threat to both wildlife and human beings. Biomonitoring methods are gaining
more importance because they allow for prediction, detection, and control of potential
environmental hazards caused by heavy metal pollution. This has been indicated in the
studies carried out in Turkey, and hundreds of studies have been carried out using these
methods during the last decade. Using plant samples as biomonitors has made a significant
contribution to these studies.
This study has some limitations with regard to its methodology. As a result of careful
analysis of biological monitoring using plant samples within the context of Turkey, 63
studies were accessed or found to be related to predetermined criteria. Although some
of these studies met predetermined criteria, they were not included in the review due to
their methodological characteristics. Plant samples such as tea, olives, and herbs used as
biomonitors in certain studies were purchased from grocery stores, markets, and herbalists
or collected from various herbariums after they were processed. Such studies were not
included in this study due to some concerns that heavy metal accumulation values may
undergo significant changes during processing, shipment, and storage of such plant samples.
Furthermore, due to the fact that the origins of the plants and their Latin names were not
mentioned in some studies where such plant samples were purchased from various vendors,
such studies were not included in the scope of this study. On the other hand, such studies
intended for the determination of inorganic and organic components in various plant samples
were not included within the scope of the review because this study analyzed studies that
focused on the determination of heavy metal pollution by biomonitoring methods. Lastly,
the studies that analyzed heavy metal accumulation in plant samples using spectrometric
methods were reviewed in this study and other studies that make use of various techniques
such as BCR (Community Bureau of Reference of the European Commission) extraction
procedure were not included in the scope of this study.
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Determination of Heavy Metal Accumulation in Plant Samples by Spectrometric Techniques in Turkey

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Applied Spectroscopy Reviews

ISSN: 0570-4928 (Print) 1520-569X (Online) Journal homepage: http://www.tandfonline.com/loi/laps20

Determination of Heavy Metal Accumulation in

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Determination of Heavy Metal Accumulation

Keywords: Biomonitoring, heavy metal pollution, spectrometric techniques, plants

Effects of Heavy Metals on Plants

Spectrometric Heavy Metal Detection Techniques

Rationale and Objective

Criteria for Selecting the Research Studies

Sources of Research Studies

Search for Studies

Developing Coding Form

Analyzing and Charting the Selected Studies

Results and Discussion

Sample Characteristics of the Studies

Figure 2. Most used families in the selected studies.

Figure 3. Most used genus in the selected studies.

Plant Parts Used

Methods of the Studies

Detection Techniques. An analysis of international studies shows that spectrometric tech-

Heavy Metals Assessed

Figure 6. Heavy metals according to number/percentage of assessment.

Outcomes of the Studies

Elements Land plants (µg g−1 dry wt)

tolerate environmental perturbations is variable. Therefore, plant responses to environmen-

Figure 9. Heavy metals identified as toxic levels according to provinces.

Figure 10. Frequencies of heavy metals identified as being at toxic levels.

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