Atmospheric Environment 42 (2008) 8273–8277
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Atmospheric Environment
journal homepage: www.elsevier.com/locate/atmosenv
Long-term monitoring of metal pollution by urban trees
Loretta Gratani*, Maria Fiore Crescente, Laura Varone
Department of Plant Biology, Sapienza Univerity of Rome, P.le A. Moro, 5 00185 Rome, Italy
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 25 February 2008
Received in revised form 14 July 2008
Accepted 21 July 2008
The atmospheric pollution level in Rome was monitored in the year 2006. Five sites in the
historical centre were considered. The concentration of Al, Fe, Cu, Zn, and Pb was analysed in
washed and unwashed Quercus ilex leaf samples. Moreover, in order to verify the changes in
atmospheric pollution in the historical centre of the city after the introduction of the limited
traffic zone (LTZ), previous data collected in the years 1979 and 1996 were also considered.
The leaf’s internal concentration of Al, Fe, Cu, Zn, and Pb was 28, 22, 40, 77 and 37%,
respectively, of the total concentration, and it was in the same range monitored in the years
1979 and 1996. The results underlined a significant (p < 0.05) decreasing of metal concentration on unwashed leaves with on an average 92%, compared to ones monitored in the year
1979. The mean value of the total traffic flow during the limitated period (Monday to Friday,
from 6:30 a.m. to 6:00 p.m, and Saturday from 2:00 to 6:00 p.m.) was 75.000 vehicles,
compared to 90.000 ones before the electronic gates were activated; moreover, a 15%
decrease in the daily traffic peak (8:30–9:30 a.m) was monitored. The metal concentration in
Q. ilex leaves was be related to motor vehicle emissions, confirmed also by PCA. The data
obtained on the leaf metal concentration trend in Rome, over a period of 27 years, underlined
the importance of the City Council provisions. These results confirmed the use of Q. ilex for
long-term monitoring of metal concentration in those urban areas where the species was
naturally present, and widely distributed in the landscape.
Ó 2008 Published by Elsevier Ltd.
Keywords:
Bio-monitor
Metal pollution
Quercus ilex
Rome
Vehicular traffic
1. Introduction
Vehicular traffic is one of the major sources of heavy
metal contamination, either in soils or roadside dusts in
urban areas, and it has increased in the last years (Colvile
et al., 2001; Çelik et al., 2005; Ahmed and Ishiga, 2006;
Ovadnevaitë et al., 2006). The spatial and temporal distribution of air pollutants within urban areas is crucial to
human health (Urbat et al., 2004), since they are readily
inhaled by humans (Rossini Oliva and Espinosa, 2007).
Nevertheless, many factors influence pollutant concentration in urban areas, including climate, urbanistic
characteristics, and both volume and type of the ‘‘green’’.
Plants not only have an ornamental function in urban
areas, but they may also improve the quality of urban life
* Corresponding author. Tel./fax: þ39 06 49912358
E-mail address: loretta.gratani@uniroma1.it (L. Gratani).
1352-2310/$ – see front matter Ó 2008 Published by Elsevier Ltd.
doi:10.1016/j.atmosenv.2008.07.032
(Akbari, 2002; Brack, 2002), having a role in carbon dioxide
sequestration and oxygen releasing through photosynthesis, contributing to air temperature mitigation by
shading and transpiration (Akbari, 2002; Gratani and Varone, 2006). Moreover, plants can uptake and accumulate
pollutants through their roots and leaf surfaces (Sawdis
et al., 2001); in particular, leaves can act as biological
absorbers of pollutants (Gratani et al., 2000; Pal et al., 2002).
Particles can be dry deposited on plant surfaces and accumulated through sedimentation under the influence of
gravity through impaction resulting from wind (Nowak,
2004). They can also be kept with internal leaf accumulation
and/or retention on the leaf surface (Gratani et al., 2000).
Atmospheric metal concentration monitoring can be
carried out by different types of biological monitors,
including plants, fungi, lichens, and tree bark (Capannesi
et al., 1981; Gratani and Crescente, 1999; Gratani et al., 2000;
Monaci et al., 2000; Pyatt, 2001; Del Rio et al., 2002; Yilmaz
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L. Gratani et al. / Atmospheric Environment 42 (2008) 8273–8277
and Zengin, 2004; Madejon et al., 2006; Al – Alawi and
Mandiwana, 2007; Rossini Oliva and Espinosa, 2007). Biological monitors are organisms that provide quantitative
information on some aspects of their environment, such as
how much of a pollutant is present (Martin and Coughtrey,
1982). Moreover, in urban area higher plants are mostly
suitable for monitoring metal pollution since as lichens and
mosses are often missing (Al – Alawi and Mandiwana, 2007).
Alfani et al. (1996), Pyatt (2001), Avila et al. (2003), Urbat
et al. (2004), Maisto et al. (2004), Sardans and Peñuelas
(2005) underline the use of tree leaves for pollution biomonitoring. The main advantage of the plants use as
bio-monitor is that plants are wide-spread providing a high
density of sampling points (Moreno et al., 2003). Moreover,
the most economical and reasonable method for biomonitoring heavy metal levels in the atmosphere is using
plants (Çelik et al., 2005). Among trees, evergreen species
are better traps for particles than deciduous ones because of
their longer leaf longevity, which can accumulate pollutants
throughout the year (Gratani and Varone, 2006, 2007). Thus,
information on atmospheric pollution may be deduced from
the concentration of specific substances in plant tissues
(Wolterbeek and Peters, 2000; Kapusta et al., 2006), offering
low-cost information about environmental quality (Çelik
et al., 2005; Rossini Oliva and Espinosa, 2007).
The main objective of this research was to monitor the
atmospheric pollution level in Rome, after the introduction
of the limitation traffic zone (LTZ) in the centre of the city,
by the City Council. We considered Quercus ilex L., which is
naturally present in the Rome landscape; moreover, it is
widely distributed since it is furnished for ‘‘green’’ streets in
the city.
To evaluate the efficacy of this provision we compared
the data collected in the year 2006 with those by Capannesi
et al. (1981), and Gratani et al. (2000), for the same sites, in
the years 1978 and 1996, respectively. Moreover, we would
identify the main trend of the data along with the variables,
throughout the years, by factorial analysis.
value S.E.), were selected in each of the considered sites.
These trees were the same plants investigated in the years
1979 and 1996. Three leaf samples (per tree), of 250 g each,
were collected from the south-eastern side of the lower
crown portion (according to Capannesi et al., 1981; Gratani
et al., 2000), in July 2006, a week after the last rainfall.
Leaf samples were stored in polyethylene bags and
transferred immediately to the laboratory. Chemical
analysis were carried out following the same analytical
procedure used by Capannesi et al. (1981), and Gratani et al.
(2000), in order to compare the results of 2006 with those
monitored in the years 1978 and 1996.
Two leaf sub-samples, without petioles, were selected
and one of them was washed with deionised water and
an aqueous solution of 5% Triton-x100 (Ratcliffe and
Beeby, 1980) to remove superficial leaf deposit. Both
washed and unwashed leaf samples were oven dried at
90 C to constant mass, and pulverised by a Retsch PMA
pulveriser, then Al, Fe, Cu, Zn and Pb concentration was
analysed.
The concentration of Al, Fe, Cu, Zn, and Pb was analysed
in triplicate by flame atomic absorption spectrometry (AAS;
maximum versatility 82547), after hashing them in
a muffle furnace (Haeraeus). The hashed samples were
digested by a hotplate at 80–90 C for 3 h in 20 ml of 1:1
(w/w) (constant boiling) HCl pure water solution, according
to Wheeler and Rolfe (1979).
The leaf’s internal metal concentration was calculated
as the difference between unwashed and washed leaf
samples.
In order to verify the atmospheric pollution change in
the historical centre in response to LTZ, the results were
compared with the data previous collected at the same five
sites, in the year 1979, before the green fuel and catalytic
exhaust introduction (Capannesi et al., 1981), and in the
year 1996 (Gratani et al., 2000), when LTZ was active but
without electronic gates.
2. Materials and methods
2.3. Statistic analysis
2.1. Study site
Statistical significance of the mean values of the metal
concentration with respect to the considered years (1978,
1996 and 2006) were analyzed by a one-way analysis of
variance (ANOVA), followed by the Tukey test for multiple
comparisons.
Two Principal Component Analysis (PCA) were used to
get associations of metal factors in order to identify their
trend in 1979 and 2006. PCA was carried out on the basis of
a matrix of the normalised data using unwashed leaf
samples.
All statistical tests were performed using a statistical
software package (Statistica, Statsoft, USA).
The study was carried out in the city of Rome, in July
2006. We considered five sites (Popolo Square, Pincio Slope,
Cairoli Square, Fori Imperiali Street, Venezia Square) in the
historical centre of the city, which have been transformed
into a limited traffic zone (LTZ), by the City Council
provision since 1989, in order to limit vehicle traffic. This
limitation was implemented in the year 2001 by the
introduction of electronic gates to control the access. In the
LTZ, the traffic limitation during the week was active
Monday to Friday, from 6:30 a.m. to 6:00 p.m and Saturday
from 2:00 to 6:00 p.m. The five sites had been chosen
among those monitored by Capannesi et al. (1981), and
Gratani et al. (2000).
3. Results
3.1. Leaf metal concentration
2.2. Chemical analysis
Three Q. ilex trees, of comparable size (plant height was
16 1 m and diameter at breast height 50 4 cm, mean
The metal concentration of unwashed and washed leaf
samples monitored in the years 1979, 1996, and 2006 are
shown in Fig. 1A and B.
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L. Gratani et al. / Atmospheric Environment 42 (2008) 8273–8277
Ln of metal concentration
A
10
Unwashed
a
a
b
8
b
c
b
b
a b
a
4
c
c
c
2
0
Ln of metal concentration
B
10
Washed
8
1979
1996
2006
a
a
b
b
6
a
c
c
b
b
a b
4
a
c
c
2
c
0
Al
Fe
Pb
Cu
Zn
Fig. 1. Ln of metals concentration in unwashed (A) and washed (B) Q. ilex
leaf samples collected in different years (1979, 1996 and 2006) at the same
sites. The annual differences in mean values of the metal concentration with
different letters are significantly different (ANOVA, p < 0.005 and the Tukey
Test for multiple comparisons).
Significant differences (p < 0.05) in the metal concentration among the unwashed leaf samples collected in
1979, 1996 and 2006 were found (Table 1).
Comparing unwashed and washed leaf samples
collected in the year 2006, the leaf’s internal concentration
of Al, Fe, Cu, Zn, and Pb was 28, 22, 40, 77 and 37%,
respectively, of the total concentration, and it was in the
same range monitored in the years 1979 and 1996. On an
average, the total leaf concentration monitored in the year
2006 was 92% lower than that monitored in the year 1979.
3.2. Statistic analysis
The results of PCA, carried out using data monitored in
1979 and 2006, showed two factors explaining the variation of the metal concentration for the considered years
(Table 2). Factor 1 accounted for 49% of the total variance in
1979, and it was significantly correlated to Pb and Zn, while
Table 1
Results of ANOVA
Metals
Al
Fe
Table 2
Factors loadings for PCA of metal content in Q. ilex unwashed leaf samples
carried out using data collected in the years 1979 and 2006
Metal
a
c
6
1979
1996
2006
Cu
Zn
Pb
Degrees of freedom 2
2
2
2
2
F values
5.3
10.9
7.0
4.8
16.4
Observed p values
0.0084* 0.00015* 0.0023* 0.013* 0.000005*
*Significant difference among the samples collected at the same sites in
1979, 1996 and 2006 (at p values < 0.05).
Al
Pb
Fe
Cu
Zn
Eigen values
% Of explained
variance
1979
2006
Factor 1
Factor 2
Factor 1
Factor 2
0.213
0.915*
0.269
0.490
0.895*
2.4
49
0.811*
0.165
0.850*
0.463
0.263
1.3
25
0.963*
0.179
0.935*
0.076
0.082
2.0
41
0.135
0.731*
0.253
0.752*
0.756*
1.6
31
*Statistically significant (p > 0.7).
In the year 1979 Factor 1 accounting for the most of the total variance
(49%) was significantly correlated to Pb and Zn. In the year 2006 Factor 1,
explaining the most of the total variance (41%) was significantly correlated
to Al and Fe.
Factor 2, accounted for 25% of the total variance, and it was
significantly correlated to Al and Fe. On the contrary,
Factor 1, explained 41% of the total variance in the year
2006, and it was significantly correlated to Al and Fe, while
Factor 2 accounted for 31% of the total variance and it was
significantly correlated to Pb, Cu, and Zn.
4. Discussion
Rome represents an example of a mega city where air
pollution has been increasing over time, causing risks to the
health of the population. The urbanisation process in Rome
has been increased during the last few years, and many
new suburban areas have been built by scaling down free
areas surrounding the city (129.000 ha of urbanised area,
2.810.931 inhabitants, with 32.569 in the historical centre).
Moreover, a strong increasing of the private means of
transportation (56% increase of the vehicular park in Rome
from 1985 to 2006, data from ACI, 2006) has been monitored. Air pollution in Rome is most likely due to emissions
from motor vehicles (Moreno et al., 2003). Consequently, in
these last years the City Council has promulgated some
provisions to limit pollution levels, such as the LTZ introduction in the historical centre of the city.
The mean value of the total traffic flow, during the
limited period, was 75.000 vehicles, compared to 90.000
ones before the electronic gates where activated; moreover,
a 15% decrease in the daily traffic peak (8:30–9:30 a.m) was
monitored (data from ATAC Mobilty Agency, 2006).
Although metals are naturally present in soils,
contamination comes from local sources, mostly industry,
agriculture, sewage sludge, waste incineration, and road
traffic (Çelik et al., 2005). Zn, Fe and Cu are microelements essential for plants (Shuman, 1994), and they are
natural constituents of the soil (Larcher, 2003); nevertheless the source of Zn and Cu in the street dust has
been ascribed to corrosion of the metallic parts of cars
like engine wear, thrust bearing and brush wear (Divrikli
et al., 2003; Al – Khashman and Shwabkeh, 2006). Pb is
directly related to the emissions from motor vehicles
(Koeppe, 1981; Al – Khlaifat and Khashman, 2007).
On the whole, our results underline the effects of the
Council provision throughout the use of Q. ilex leaves. The
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L. Gratani et al. / Atmospheric Environment 42 (2008) 8273–8277
metal concentration in Q. ilex leaves seems to be related to
motor vehicle emissions; Çelik et al. (2005), Al – Alawi and
Mandiwana (2007), and Urbat et al. (2004) underline the
relationship between motor vehicle emissions and metal
concentration in leaves of Robinia pseudo – acacia L. Pinus
halepensis L., and Pinus nigra L., respectively.
On an average, Q. ilex leaves accumulated more metals in
1979, when there were a greater number of motor vehicles
in the historical centre than in 2006, according to the results
of Kapusta et al. (2006) for Moehringia trinervia Clairv.
The PCA underlines that in 1979, when LTZ had not been
established yet, and there was a higher Pb concentration in
gasoline, Factor 1 (describing most of the total variance) is
dominated by Pb and Zn, which are directly correlated to
motor vehicles (Al – Khlaifat and Khashman, 2007). In the
years following 1979, a significant increase of the traffic
density has been observed (1.582.754 vehicles registered in
1985 to 2.476.179, in 2006). Starting from 1990, further
measures have been taken in Italy to limit pollution levels
increasing; since 1989 ‘‘green’’ fuel and catalytic exhausts
have become compulsory, and in 1989, the Rome City
Council have introduced the traffic limitation zones (LTZ) in
the centre of the city. The effects of these provisions
resulted in a significant traffic density lowering, that is
underlined by PCA; in fact, the Factor 1, explaining most of
the total variance in the data monitored in 2006, is dominated by Fe and Al, which are typical soil constituents
(Rossini Oliva and Mingorance, 2006); on the contrary, the
concentration of Zn, Cu and Pb, which are directly related to
the traffic density (Çelik et al., 2005; Al – Khlaifat and
Khashman, 2007) are correlated to Factor 2, accounting for
a lower variance.
Total element contents in the aboveground parts of
plants depend on the root uptake and elements re-translocation from the assimilation organs (Garland et al., 1981;
Zimcka and Stackurski,1994). It has also been suggested that
direct uptake through bark or foliage may be a major
pathway by which metals enter trees, particularly in heavily
polluted areas (Baes and McLaughlin, 1987). The wood
accumulates elements mainly from the soil, and its metal
concentration does not reflect the atmospheric pollution
making this plant portion unsuitable for bio-monitoring
(Rossini Oliva and Mingorance, 2006). It is possible to
measure differences between aerial deposition and root
uptake through washing leaves (Matarrese Palmieri et al.,
2005). Plant bark and leaves accumulate pollutants straight
from the atmosphere and they are deposited mainly on the
surface (Rossini Oliva and Mingorance, 2006): our results
underline that the mean metal concentration of Q. ilex leaf
surface is 74% of the total concentration.
The obtained data of the leaf metal concentration trend
in Rome over a period of 27 years, and in relationship with
the traffic density, underlines the importance of the City
Council provisions. These results may be used to carry out
a data-bank improving the City Council management.
Understanding the relationship among urban trees,
people, and the environment can facilitate future urban
designs, that might enhance environmental and social
benefits (Dwyer et al., 1992). According to Market (1993)
and Al-Alawi and Mandlwana (2007), the basic criteria for
the selection of a plant to bio-monitor are that it should be
represented in large numbers all over the monitoring area,
be easy and inexpensive to sample, and determine a 50%
saving over the use of pollution monitors. Moreover, the
main advantage is that plants are wide-spread, providing
a high density of sampling points, so there is the possibility of building high-resolution maps of air pollution in
urban areas (Moreno et al., 2003). Our results suggest the
use of Q. ilex for long-term monitoring of metal concentration in those urban areas where the species is naturally
present and widely distributed, according to the results of
Alfani et al. (1996), Maisto et al. (2004), Sardans and
Peñuelas (2005) for the same species in other geographical
areas.
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