Environ Monit Assess
DOI 10.1007/s10661-009-0796-x
Comparison of the suitability of two lichen species and one
higher plant for monitoring airborne heavy metals
Giuseppa Grazia Aprile Mina Di Salvatore
Giovanna Carrat Antonio Mingo
Anna Maria Carafa
Received: 23 January 2008 / Accepted: 27 January 2009
Springer Science + Business Media B.V. 2009
Abstract We compared the capacity to accu-
mulate airborne heavy metals of two lichens
(Flavoparmelia caperata and Parmotrema chi-
nense) and one higher plant (Nerium oleander) at
a very densely populated urban site near Naples.
After 15, 45, 75, and 120 days of exposure at four
sites with different levels of air pollution, equal
portions of thalli and 20 leaves were collected,
and four environmentally significant elements, Fe,
Cu, Zn, and Pb, were measured by inductively
coupled plasma analysis. To compare the accumu-
lation rates of lichens and the vascular plant, we
determined an index of relative accumulation rate
of pollutants during time and the ratio between
the concentrations of each element in exposed
samples to that of control samples (exposed-to-
control ratio). Our data indicate F. caperata as
being the most suitable bioaccumulator, followed
by P. chinense. N. oleander was also found to be a
useful heavy metal biomonitor though not suitable
as a bioaccumulator.
G. G. Aprile (B) M. Di Salvatore G. Carrat
A. Mingo A. M. Carafa
Dipartimento di Arboricoltura, Botanica,
Patologia Vegetale-Sez. di Botanica,
Federico II Facolt di Agraria,
Universit degli Studi di Napoli, via Universit,
100-80055 Portici, Naples, Italy
e-mail: gaprile@unina.it
Keywords Air pollution Biomonitoring
Flavoparmelia caperata Lichen transplants
Nerium oleander Parmotrema chinense
Introduction
Since the beginning of the twentieth century,
air pollution has worsened as a consequence of
urbanization and industrialization, together with
the rapid growth of motorized transportation and
population. Of the main components of air pollu-
tants, an important group to be considered is that
of heavy metals, mostly associated with airborne
particulate matter. This is particularly true in city
centers, where vehicle engines, as well as the heat-
ing systems inside buildings, represent the most
important sources of air pollution (Sawidis et al.
1995; Monaci et al. 2000).
Environmental monitoring methods are based
on expensive and sophisticated measuring sys-
tems. Since the element composition of vascular
plants, bryophytes and lichens can change as a
consequence of pollution, a complementary use of
their parts as biomonitors may be an appropriate
alternative (Bargagli 1998; Bari et al. 2001). The
organisms most frequently used for monitoring
metal pollutants are lower plants, such as mosses,
and lichens (Conti and Cecchetti 2001; Adamo
et al. 2003; Figueira et al. 2002) due to their con-
siderable ability to accumulate metals. However,

since these organisms are rare in urban areas with
high degrees of pollution, in recent years, the use
of vascular plants has been introduced to monitor
heavy metal pollution (Sawidis et al. 1995).
The aim of this work is to test the different
heavy metal accumulation capabilities in a sper-
matophyte and two lichens transplanted to an
urban area in order to quantify the suitability
of different taxa for monitoring airborne heavy
metals.
Materials and methods
The tested species
Two epiphytic foliose lichens and one spermato-
phyte were selected for this experiment. The
lichen species were Flavoparmelia caperata (L.)
Hale (hereafter Flavoparmelia) and Parmotrema
chinense (Osbeck) Hale & Ahti (hereafter Par-
motrema), two species widespread in Europe and
naturally present near the examined area. The
spermatophyte was Nerium oleander L. (hereafter
oleander), an urban ornamental shrub widely used
in parks, gardens, and along roadsides, growing
in nutrient-poor soils and in drought conditions.
Flavoparmelia had already been used in other
bioaccumulation studies (Bargagli et al. 2002;
Godinho et al. 2004; Loppi et al. 1994; Loppi and
Corsini 2003; Minganti et al. 2003). The use of
oleander as a biomonitor was reported elsewhere
(Sawidis et al. 1995; Aksoy and ztrk 1997;
de Jesus et al. 2000; Rossini Oliva and Mingorance
2004); Espinosa and Rossini Oliva (2006) used
oleander as a passive biomonitor along a pollution
gradient to study the spatial distribution of pollu-
tants and found a positive and significant correla-
tion between trace element contents in PM10 and
in oleander leaves. In our study, all biomonitors
were transplanted. Hence, oleander was an ac-
tive biomonitor, just like lichens.
The lichen samples with their substrate bark
were gathered in the forest reserve of the
Vesuvius National Park (an unpolluted site;
Fig. 1); the potted oleander came from the Botani-
cal gardens at the Faculty of Agriculture in Portici
(Naples).
Environ Monit Assess
Fig. 1 Location of the study area in Campanian region,
Italy
Experimental design
After collection, both lichen samples and oleander
leaves were analyzed to obtain the initial element
contents. Three samples of potted oleander were
exposed at each of the four sites selected in the
urban area of Portici, a densely populated town
near Naples (density/km2 , 13,322.6) with heavy
road traffic. Sites 1 and 2 were located along
the sparsely vegetated urban roadside, with heavy
traffic flow and tall buildings limiting the circula-
tion of air, site 3 was near the trees of the small
urban park, and site 4 was in the park facing the
sea. Vehicle density in the four sites was found
to reflect a decreasing gradient from sites 1 to 4
as for cars, whereas bus traffic was found to be
considerably higher at site 2 relative to the other
three locations (Fig. 2).
The exposure period of lichen transplants and
potted oleander was relatively short (from March
to July) so as not to alter their morphologi-
cal, anatomical, or physiological characteristics, as
suggested by Mikhailova (2002, p. 302). Lichen
samples (ten thalli of each species) were collected
together with bark substrate and put in nylon
mesh bags (10- 10-cm wide, with 1-mm2 mesh)
closed with a nylon wire. This exposure method
Environ Monit Assess
25.000 450
Cars
400
20.000
350
300
-1
Vehicles h
15.000
250
200
10.000
150
5.000 100
50
0 0
1 2 3 4 1 2
Fig. 2 Vehicle density (cars and bus) in the four exposition
sites
was chosen because, as demonstrated by Bari et al.
(2001, p. 217), it was the most efficient with the
highest heavy metal accumulation rates and to
detect correlations with environmental levels of
these elements in air and in atmospheric partic-
ulates. Eight bags were exposed on the branch
of each potted oleander, far removed from rain
pipes. The first sampling (both lichen thalli and
oleander leaves) was carried out after 15 days,
while the subsequent three were performed after
45, 75, and 120 days, respectively. The lichen sam-
ples, in triplicate, were taken to the laboratory
and cleaned to remove dead or senescent tissue
and extraneous material, such as adhering bark,
mosses, other lichen species, and soil particles,
following the methods proposed by Nimis and
Bargagli (1999). For the oleander, 20 fully ex-
panded leaves were picked up, and half of the
samples were washed with deionized water and
cleaned with blotting paper to remove the pol-
lutants still present on the leaf surface. The dif-
ferences between the total concentrations of the
heavy metals measured in the uncleaned and
cleaned samples were calculated in order to quan-
tify only the metals deposited on the leaves with
particulate (Aksoy and ztrk 1997).
This double measurement was necessary be-
cause the period of time in which the study was
carried out (from March to July) is a period of in-
tense growth for oleander; the plant absorbs large
Bus
amounts of water and solutes from the ground and
supplies nutrients to its leaves through the xylem.
Consequently, the increase in metals found in the
leaves was not due exclusively to metals from the
atmosphere but also to those from the ground.
In lichens, whose growth is extremely slow, the
increase in metals found during the study was due
exclusively to airborne pollution.
Both the oleander and lichen samples were
oven-dried at 70 C until constant weight and then
ground to a fine powder. Five hundred milligrams
of powder was weighed in a Teflon container and
mineralized in a mixed acid solution [HNO3 /H2 O2
3 4
(6:1, v/v)] using a High Performance Microware
Digest Unit (Mega FKV). The digested samples
were brought to 50 ml with deionized water and
analyzed by inductively coupled argon plasma
emission spectrometry (ICP emission spectrome-
ter, Liberty 150 Varian) for the determination of
the total concentration of Zn, Cu, Pb, and Fe. The
latter element was known to be an element with a
mixed natural and urban origin (de Minguel
et al. 1997), whereas the others were considered
as urban elements, derived from traffic and cor-
rosion of building materials.
In order to ascertain the accuracy and preci-
sion of the digestion and ICP analysis procedure,
two blanks and a Standard Reference Material
(Community Bureau of Reference BCR 62), olive
leaves were analyzed using the same procedure.
Statistical analysis
The time course of metal accumulation was an-
alyzed for each species and each metal both in
absolute (metal concentration) and relative terms.
An index of relative accumulation rate (RAR)
was used to estimate the daily rate of metal ac-
cumulation per gram of accumulated metal:
 
RAR = ln (Cn ) ln (Cn1 ) (tn tn1 ) (1)
where Cn and Cn1 are the metal concentration
at two sequential times (tn and tn1 , respectively)
with n ranging between 0 (non-exposed control
samples) and 4 (120 days exposed samples).
The concentrations of each element in the ex-
posed samples at the end of the experiment were

normalized to control values (unexposed samples
at time 0) in order to compare on the same scale
the responses of the three biomonitors in the four
exposure site. To this aim, the index of exposed-
to-control ratio was used (Frati et al. 2005):
 
E C ratio=CE CC
where CE is the metal concentration of samples
subjected to 120 days exposition to pollutants and
CC is the metal concentration measured on bio-
monitors before the exposure time. E/C values
were log transformed before analysis of data in
order to achieve a non-skewed distribution.
Final metal concentrations and log transformed
E/C ratio were analyzed with a general linear
model, with metal, site, and species as main fac-
tors. The relationship between final metal accu-
mulation and vehicle density was tested by using
the Pearson coefficient. Statistical analysis was
carried out by using Sigma Stat and SPSS 13.0
packages.
Fig. 3 Concentrations of
four heavy metals
(Cu, Fe, Zn, and Pb)
in three biomonitor
species as a function of
the time of exposition to
Metal concentration (mg Kg -1 d.w.)
pollutants. Points
represent means and
standard errors of 12
replicated stratified for
four exposition sites
Environ Monit Assess
Results
Time course of metal accumulation by species
In the first step of the analysis, metal concen-
tration during time was monitored on the three
species independently of site effects. Metal accu-
(2) mulation of the two lichens species was gener-
ally higher relative to that of oleander (Fig. 3).
In absolute terms, Parmotrema tended to cap-
ture the largest amount of Fe and Pb, whereas
Flavoparmelia showed a relatively higher Cu ac-
cumulation. Zn was accumulated with a very close
pattern by both Flavoparmelia and Parmotrema,
whereas oleander showed a relatively lower
capture.
The pattern of metal accumulation by species,
however, appeared quite different if analyzed in
terms of RAR. Oleander tended to show a con-
siderably higher RAR relative to the other species
(Fig. 4). RAR was generally greater at the begin-
ning of the exposure time, declining later. RAR
of oleander was particularly high for Fe and Pb,
during the first time interval (015 days). Among
Time (days)
Environ Monit Assess

Fig. 4 Relative
accumulation rate
(RARsee text for the
definition of the index)
of four heavy metals
(Cu, Fe, Zn, and Pb) as a

Relative Accumulation Rate (day-1)

function of the time of
exposition to pollutants.
Points represent means
and standard errors of 12
replicated stratified for
four exposition sites

Time (days)

the lichens, Flavoparmelia tended to show a rela- No correlations were found for Zn accumulation
tive higher accumulation rate, particularly for Zn by oleander.
during the first time interval; Parmotrema, on the
contrary, showed a negative RAR for Zn at the
beginning of exposure time, increasing later.
Discussion

Final values by species and sites
The general linear model revealed highly signif-
icant effects of all main factors and interactions,
both in terms of final concentrations and exposed-
to-control ratio (Table 1). Oleander showed the
highest E/C ratio values (Fig. 5), particularly for
Fe and Pb. Among lichens, Flavoparmelia tended
to accumulate more than Parmotrema, the latter
showing some negative E/C value for Fe and Zn
in the less-polluted sites.
Correlation analysis revealed interesting rela-
tionship between metal accumulation and vehicle
density (Table 2). Cu accumulation was strongly
correlated with bus density for all three species,
whereas lichen Fe and Pb accumulation were sig-
nificantly correlated with car density. Zn accumu-
lation was correlated with bus density in the case
of Flavoparmelia and with cars for Parmotrema.
The high quantity of heavy metals found both in
the lichen and oleander samples along the urban
roadside (sites 1 and 2) was probably due to the
particularly high traffic flow, which is considered
the major source of heavy metal pollution in this
area, although in Italy, since 1992, the gradual
shift from leaded to unleaded petrol and catalytic
mufflers in vehicles should have reduced Pb emis-
sions. This agrees with the results found by other
authors, namely, de Minguel et al. (1997, p. 2737),
Frati et al. (2005, p. 227), and Monaci et al. (2000,
p. 323), suggesting that Pb contamination is found
on roads with heavy traffic due to street dust re-
suspension, where this element can also be associ-
ated with coarse particles.
On the contrary, the higher values of Cu and
Zn measured in lichen samples at site 2 were
probably not only due to common sources such
as the traffic flows but also to abrasion processes
 Environ Monit Assess

Table 1 Results of the general linear model applied to metal accumulation in three biomonitor species, with metal, site, and
species as main factors
General linear model Final metal concentration E/C ratio
Source df F F
Corrected model 47 343.4a 46.7a
Intercept 1 2,529.1a 4,594.6a
Metal 3 2,239.9a 100.2a
Site 3 112.9a 43.1a
Species 2 712.8a 520.4a
Metal site 9 106.7a 6.7a
Metal species 6 672.5a 88.6a
Site species 6 110.5a 4.5a
Metal site species 18 111.0a 5.9a
Error 96
Total 144
Corrected total 143 R2 = 0.99 R2 = 0.96
The tested variables are the final concentration of heavy metals in bio-tissues and the ratio between metal concentration in
exposed to non-exposed control samples (E/C ratiolog transformed values)
a All factors and interactions were significant at 0.001 level

due to tyres and trolley bus lines (Giordano et al.
2005). Among the sampling sites, the amounts of
Fe accumulated by lichens showed considerable
heterogeneity. Finally, all the heavy metals an-
alyzed increasingly declined in concentration, as
the sites become less urbanized (sites 3 and 4).
When measured in relative terms, oleander
demonstrated a greater capacity to accumulate
heavy metals throughout the experiment and at
all sites with respect to the two lichen species,
so that it would seem, at first glance, to be more
useful as a biomonitor. However, as the metal

Fig. 5 Values of the

ratios between the
concentrations of four
heavy metals in exposed
and non-exposed control
samples(E/C ratio, log
E/C ratio (log transformed values)

transformed values
see text for the definition
of the index), among
three biomonitors species
and four sites of
exposition. Bars
represent means and
standard errors of three
replicate measures

Bioindicator species
Environ Monit Assess

Table 2 Pearson correlation values and significance level (P) between the E/C ratios of four heavy metals (Cu, Fe, Pb, and
Zn) in three bioindicator species and vehicle density (car and bus) in the exposition sites
Flavoparmelia Parmotrema Oleander
Pearson P Pearson P Pearson P
Cu Car 0.45 0.144 0.51 0.092 0.02 0.960
Bus 0.86 0.000 0.88 0.000 0.89 0.000
Fe Car 0.81 0.002 0.69 0.014 0.55 0.062
Bus 0.34 0.276 0.77 0.004 0.08 0.794
Pb Car 0.92 0.000 0.94 0.000 0.21 0.517
Bus 0.29 0.356 0.29 0.369 0.79 0.002
Zn Car 0.51 0.087 0.71 0.010 0.47 0.121
Bus 0.79 0.002 0.47 0.121 0.16 0.613
N = 12

accumulation is very low if considered in ab-
solute values, it may not be considered a good
bioaccumulator.
Comparative evaluation of the accumulation
capacity of both kinds of samples (lichens and
leaves) was performed by calculating the E/C ra-
tio. The choice of this index was justified by the
fact that in the three plant samples and for all
the elements in question, the background concen-
tration differed greatly. Hence, the calculation of
relative change (EC), compared with the absolute
change is the best way to compare the bioaccumu-
lation capacity of the various biomonitor species,
as suggested by Bergamaschi et al. (2007). For
lichens, the measured EC values are conspicuous
and are indicative of the kind of pollution. Indeed,
for Cu and Zn, the highest values were found
at site 2, which is justified by the presence of a
trolleybus line being an additional source of these
metals, while as far as Pb is concerned, the highest
values were found at site 1 where the traffic flow
is very heavy and vehicles are often blocked in
long queues. On the basis of the scale of accu-
mulation/loss suggested by Frati et al. (2005), the
E/C ratios investigated in all sites show severe
accumulation for F. caperata and often for N.
oleander, while for P. chinense for Zn at all sites,
Pb at site 3, and for all elements at site 4, they
indicate accumulation.
Our data confirm the particular ability of both
lichens and oleander to accumulate pollutants due
to their morphological and physiological charac-
teristics, as reported elsewhere (Bargagli 1998;
Nimis et al. 2002; Aksoy and ztrk 1997). In both
lichens and leaves, there was a direct relationship
between the traffic conditions at the different sites
and the concentration of heavy metals. However,
as regards oleander, the high variations in concen-
trations of the same heavy metal, for example, Fe
and Cu, which had a mixed (anthropogenic and
natural) origin (de Minguel et al. 1997), suggest
that there is not only a direct relationship between
the traffic flow and these concentrations, but there
are also other factors that may interfere with the
deposit of the elements on the leaves, such as wind
and soil characteristics, as also found by de Jesus
et al. (2000, p. 1186). Oleander leaves exhibit a
waxy adaxial epidermis and a rough abaxial epi-
dermis due to the tangled hairs protecting sunken
stomata. For this reason, airborne metals and soil
particles are easily and strongly fixed to these
structures on the epidermis.
With regard to the two lichen species tested,
F. caperata and P. chinense, the former is more
suitable for transplanting. These results are con-
sistent with those found by other authors (i.e.,
Garty 2001), who observes that lichen species with
finely divided or densely sorediate thalli show a
greater affinity for collecting particulate matter.
Finally, our results suggest that oleander could
be suitably used for biomonitoring, as reported
by other authors (Rossini Oliva and Mingorance
2004; Aksoy and ztrk 1997; Sawidis et al. 1995),
as well as the lichen species.
The first results obtained from our data indi-
cate that, although oleander can be used as a
qualitative biomonitor, correct determination of
the variation in metal content on the leaf surface

should include soil analysis in order to ascertain
whether the same differences are also due to soil
composition.
Acknowledgements We are grateful to Prof. Stefano
Loppi (University of Siena, Italy) for his critical review
of the manuscript and his helpful suggestions and Mark
Walters for his critical revision of the language.
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