Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769

https://doi.org/10.1007/s00128-019-02595-0

Biomonitoring of Air Pollution in Bosnia and Herzegovina Using

Epiphytic Lichen Hypogymnia physodes
Emina Ramić1,2 · Jasna Huremović1   · Tidža Muhić‑Šarac1 · Samir Đug3 · Sabina Žero1 · Almir Olovčić1

Received: 29 January 2019 / Accepted: 16 March 2019 / Published online: 27 March 2019
© Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract
The aim of the study was to assess heavy metals (Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn) air pollution in Bosnia and Herzegovina
by using a lichen, Hypogymnia physodes. Metal content was determined by flame atomic absorption spectrometry (FAAS)
and was between very high naturality or alteration to middle naturality or alteration. Strong correlations between Cr and
Ni confirmed mainly anthropogenic sources. The scanning electron microscopy and energy dispersive X-ray spectroscopy
(SEM/EDS) analysis of C, O, Na, Mg, Al, Si, P, S, Cl, K, Ca, V, Co, As, Sn, Sb, Hg and Bi were performed on the lichen
surface and hyphae of the transplanted samples. Despite significant damage to tissue and cell integrity, the recurrent pres-
ence of particulate matter in lichen indicates the considerable presence of dust in the urban atmosphere which, according to
chemical composition, may be due to anthropogenic and natural sources such as soil.

Keywords  Biomonitoring · Air pollution · Hypogymnia physodes · Heavy metals · FAAS · SEM/EDS

In 2013, air pollution induced around 93% of all death cases
in countries where its population was exposed to danger-
ous levels of air pollution (European Environment Agency
2015; Kodros et al. 2018). Although air quality monitoring
using lichens and mosses as bioindicators is very popular
in Europe and worldwide (Jeran et al. 2007; Harmens et al.
2008; Godinho et al. 2009; Kularatne and De Freitas 2013;
Klimek et al. 2015; McMullin et al. 2017) this method is still
not much represented in Bosnia and Herzegovina (B&H).
Epiphytic plants are efficient air pollution biomonitors
because they obtain their nutrients, water and pollutants
from the atmosphere and have no contact with the soil
(Chaparro et al. 2013). They are longevous organisms (lifes-
pan is 30–80 years) and they do not discard old and less
* Jasna Huremović
jasnahuremovic@yahoo.com
1
Department of Chemistry, Faculty of Science, University
of Sarajevo, Zmaja od Bosne 33‑35, 71000 Sarajevo,
Bosnia and Herzegovina
2
Department of Natural Sciences in Pharmacy, Faculty
of Pharmacy, University of Sarajevo, Zmaja od Bosne 8,
71000 Sarajevo, Bosnia and Herzegovina
3
Department of Biology, Faculty of Science, University
of Sarajevo, Zmaja od Bosne 33‑35, 71000 Sarajevo,
Bosnia and Herzegovina
functional parts of talus. So, they can accumulate harmful
substances during long term periods. Hypogymnia physodes
is a foliose species and used to monitor trace element deposi-
tion. H. physodes is very common epiphytic lichen on trees
with a slightly acidic or neutral bark, e.g. conifers, oaks,
­ O2 but very sensitive
birches, etc. It is rather resistant to S
to ­NH3 pollution (Jeran et al. 2007; Huremović et al. 2017).
World Health Organization (WHO) (2017) reported that the
number of death cases caused by air pollution in B&H for
2012 was 230.6 deaths/100 000 people, which places B&H
at the top of the list for Europe.
The objectives of this study were: (1) to determine heavy
metals content (Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn) in epi-
phytic lichens H. physodes collected in urban and rural sites
in B&H (44 locations) by flame atomic absorption spectrom-
etry (FAAS); (2) to analyse transplanted lichens after 3, 6,
9 and 12 months of exposure in the urban area of Sarajevo
by FAAS and scanning electron microscopy and energy dis-
persive X-ray spectroscopy (SEM/EDS); (3) to obtain poten-
tial emission sources by SEM/EDS and correlation analysis
among the metals.

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Materials and Methods
The lichen samples were collected from July–October 2017,
at 44 locations: 21 urban and 23 rural sites in B&H. The
sampling locations are shown in Fig.  1. Healthy lichen
thalli were sampled from the trunks of 3–5 neighbouring
trees, belonging to the same tree species group at each site.
Samples were carefully collected using plastic knife and
plastic gloves to avoid contamination. Samples were placed
in paper bags and transported to the laboratory and were
carefully removed from the branches using plastic tweezers.
The lichen samples were not washed. The air dried samples
were homogenized by grinding in agate mortars and stored
in paper bags prior to elemental analysis.
The transplanted lichen species H. physodes, originating
in a relatively unpolluted site in village Vukasovići located
in municipality Ilijaš, were placed in Pofalići site (urban part
of the city Sarajevo). Lichens were treated for a period of 3
months (September–December 2017), 6 months (September
2017–March 2018), 9 months (September 2017–June 2018)
and 12 months (September 2017–September 2018). Samples
were analyzed immediately after the end of the sampling
period. A total of about 1 g (± 0.1 mg) of dry lichens was
weighted directly in polytetrafluoroethylene (PTFE) diges-
tion vessels. Following the addition of 25 mL concentrated
­HNO3, after the evaporation of nitrogen oxides, the ves-
sel was sealed and allowed to react at 60°C for 12 h. The
digest was transferred to 50 mL with Milli-Q water. For the
FAAS method, an atomic absorption spectrometer, model
AA240FS, Varian was used.
Fig. 1  Sampling locations in Bosnia and Herzegovina
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Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769
To control the accuracy of heavy metals determination in
lichens, certified reference material (CRM–IAEA–336-Li-
chen) was analyzed. All samples, blanks and CRMs were
prepared in triplicate and every measurement for each rep-
licate was repeated three times. Comparison of the results
shows excellent agreement, confirming the quality of the
data. The value of the detection limit (LOD) (calculated
as three times the standard deviation of the blank signal)
were: Cd (0.002 mg/L), Cr (0.006 mg/L), Cu (0.27 mg/L),
Fe (6.24  mg/L), Mn (0.20  mg/L), Ni (0.01  mg/L), Pb
(1.00 mg/L) and Zn (0.74 mg/L).
Selected lichen samples of the background and trans-
planted lichens were examined by SEM, using a SEM model
JEOL JSM-6610LV microscope. Before SEM observation,
powdered lichen samples were prepared with a thin coating
of Au on the device for coating (model LEICA SCD005).
The composition was analysed by x–ray EDS. EDS analy-
sis was performed on the same instrument equipped with
detector, model X-Max large area analytical silicon drift,
connected with INCA Energy 350 microanalysis system. It
was possible to quantify elements with the Z ≥ 5, limit detec-
tion ~ 0.1 mass%, resolution 126 eV.
Results and Discussion
The content of eight metals: Cd, Cr, Cu, Fe, Mn, Ni, Pb
and Zn in lichen H. physodes was determined by FAAS.
The descriptive statistic parameters (mean, median, min,
max, no. of plots, range) for the determined elements in
Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769 765

H. physodes in urban (Table 1) and rural areas (Table 2)
of B&H are presented in Tables 1 and 2.
According to the scale of environmental naturality/
alteration proposed by Nimis et al. (2000), the content
of the determined elements in urban and rural areas was
between very high naturality and very high alteration (Cr,
Mn and Ni), very high naturality and high alteration (Cu),
middle naturality and middle alteration (Fe) and between
very high naturality and middle alteration for Zn. The only
difference in heavy metals content in lichens from urban
and rural area was for Cd and Pb. The content of the deter-
mined elements in urban areas was very high naturality to
middle alteration for Cd and for Pb from very high natural-
ity to low naturality/alteration. In rural areas the content of
Cd was very high naturality to high alteration and for Pb
from very high naturality to middle naturality.
Generally, there were no significant deviations in the con-
tent of metals in the lichens from urban and rural areas. A
slightly higher mean concentration value was obtained in the
urban area for Cr, Cu, Fe, Ni and Pb compared to the rural
area and slightly higher mean concentration in rural sam-
ples for Cd, Mn and Zn. By concentrations in lichens metals
were arranged as the following diminishing series: Fe > Z
n > Mn > Cu > Pb > Ni > Cr > Cd, which is similar with the
results of Balabanova et al. (2012), Ng et al. (2006), Di Lella
et al. (2004) and Nimis et al. (2000). Eight elements (Cr,
Cu, Mn, Fe, Ni, Cd, Pb and Zn) were compared in all lichen
samples by correlation analysis using the statistical tools
within Microsoft excel. The element correlations (Pearson)
in lichen H. physodes from various sampling sites in the
studied urban and rural areas are reported in Tables 3 and 4.
A very strong positive correlation between Cr–Ni in
lichen H. physodes from various sampling sites in urban

Table 1  Descriptive statistics for metals (mean, median, min, max, no. of plots, range) determined in Hypogymnia physodes in urban areas in
B&H
Metals (mg/kg) Cd Cr Cu Fe Mn Ni Pb Zn

Mean 0.14 6.33 15.89 986 37.95 7.99 9.55 55.60

Median 0.12 4.26 10.40 956 27.19 5.01 8.00 50.16
Min 0.022 0.022 4.85 637 9.85 0.58 2.13 18.19
Max 0.648 17.54 41.68 1346 173 22.31 27.68 103
No. of plots 21 21 21 21 21 21 21 21
Range 0.022–0.648 0.022–17.54 4.85–41.68 637–1346 9.85–173 0.58–22.13 2.13–27.68 11.19–103

Table 2  Descriptive statistics for metals (mean, median, min, max, no. of plots, range) determined in Hypogymnia physodes in rural areas in
B&H
Metals (mg/kg) Cd Cr Cu Fe Mn Ni Pb Zn

Mean 0.355 4.86 15.11 945 46.13 6.26 7.81 64.73

Median 0.182 2.17 9.80 1001 31.04 4.40 6.57 58.11
Min 0.015 0.158 5.16 523 11.97 0.193 2.53 28.69
Max 2.33 24.17 47.39 1260 152 18.31 20.93 107
No. of plots 23 23 23 23 23 23 23 23
Range 0.015–2.33 0.158–24.17 5.16–47.39 523–1260 11.97–152 0.719–18.31 2.53–20.93 28.69–107

Table 3  Significant element Metals Cr Cu Mn Fe Ni Cd Pb Zn

correlations (Pearson) in lichen
Hypogymnia physodes from Cr 1.00 0.11 −0.06 −0.54 0.81 −0.02 0.19 −0.14
urban areas
Cu 1.00 0.01 0.27 0.33 0.25 0.42 0.58
Mn 1.00 0.11 0.03 0.57 0.23 −0.04
Fe 1.00 −0.22 −0.07 0.18 0.10
Ni 1.00 0.07 0.26 −0.07
Cd 1.00 0.35 0.38
Pb 1.00 0.37
Zn 1.00

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766 Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769

Table 4  Significant element Metals Cr Cu Mn Fe Ni Cd Pb Zn

correlations (Pearson) in lichen
Hypogymnia physodes from Cr 1.00 −0.11 −0.16 −0.39 0.83 0.16 0.28 −0.49
rural areas
Cu 1.00 −0.01 0.38 0.06 −0.22 0.28 0.48
Mn 1.00 −0.02 −0.21 0.28 −0.10 0.00
Fe 1.00 −0.23 −0.40 0.39 0.38
Ni 1.00 0.22 0.23 −0.35
Cd 1.00 −0.27 −0.22
Pb 1.00 0.24
Zn 1.00

and rural areas is suggesting that probably Cr and Ni are
coming from the same pollution source. According to Ite
et al. (2014), these elements are considered as indicators
of anthropogenic emissions such as vehicular traffic, power
generation plants, fossil fuel combustion and incineration of
municipal wastes, metal works and application of anti–cor-
rosion paints. Apart from significant element correlations in
lichen from urban and rural areas with Ni and moderate neg-
ative correlation with Fe in the lichens from the urban areas
the concentrations of Cr were not significantly correlated
with concentrations of other metals. A moderate positive
correlation was found between Mn–Cd and Cu–Zn in the
lichens from the urban areas. A correlation between Cu–Zn
is rather common in lichens, and according to Ormrod
(1984) it may be due to anthropogenic sources or metabolic
interactions, since these two elements are essential for lichen
metabolism. A weak negative correlation between metals in
the lichens meaning that they are probably competing for
the same cell wall exchange sites (Stamenković et al. 2013).
The content of heavy metals in H. physodes transplants
after 3, 6, 9 and 12 months of exposition was shown in
Table 5.
The results showed that increasing the time of exposure
of lichens also increases the content of accumulated met-
als: Cu and Fe (3 and 6 months), Pb and Zn (3, 6 and 9
months), but Cr, Cd and Ni decreased after 3 months of
lichen exposure. Content of Pb and Zn in lichen after 9
months of exposure was 80% and 65% higher, respectively,
compared to the control sample. After 6 months Fe was 42%
and Cu 33% higher. Content of Ni in the lichen after 12
months was decreased for 80%. The reason for that trend in
metals content may be due to the season (abundant rains)
since the lichens have been transplanted in autumn. Accord-
ing to Godinho et al. (2008) and Kularatne and de Freitas
(2013) weather conditions and the hydration of the thallus
may influence on metal uptake and/or release mechanisms.
Bojko et al. (2004) showed metal loads up to about 90 mg/kg
(Mn, Zn), 700 mg/kg (Fe), 20 mg/kg (Pb) and 14 mg/kg (Cu)
in lichen that had a crucial impact on the processes of deg-
radation, particularly on the decomposition of chlorophyll.
A scanning electron microscope characterizes physico-
chemical composition of the airborne particulate on biologi-
cal material from multiple pollution sources. In addition to
the analyzed metals (Cd, Cr, Cu, Fe, Mn, Ni, Pb and Zn), the
analysis was further performed for C, O, Na, Mg, Al, Si, P,
S, Cl, K, Ca, V, Co, As, Sn, Sb, Hg and Bi. The SEM/EDS
analysis was performed on the lichen surface and hyphae
of the transplanted samples. The SEM microscopic images
of the H. physodes are given in Fig. 2. Observing the SEM
microscopic images of the control sample of the lichens par-
ticles with irregular morphology, with well-defined edges,
agglomerates of different sizes and shapes can be noticed.
After 3 months of exposure, it was noticed that the sur-
face of the lichen was significantly lighter than the surface
of the control sample, which is one of the signs that a slight
destruction of the lichen occurred. After 3, 6, 9 and 12

Table 5  Mean (± standard Metals (mg/kg) Background 3 months 6 months 9 months 12 months

deviation) element
concentrations (mg/kg d.w.) Cd 0.233±0.040 < LOD 0.213 ± 0.04 0.381±0.096 0.203±0.02
in Hypogymnia physodes
Cr 16.99±1.59 2.90 ± 0.52 < LOD 1.23±0.35 1.55±0.37
transplants before and after 3, 6,
9 and 12 months of exposure Cu 5.17±0.69 7.84 ± 0.10 7.83 ± 0.74 7.13±0.19 9.32±1.17
Fe 553±1.87 815 ± 0.40 951 ± 8 709±7 952±5.32
Mn 18.23±0.72 19.31 ± 1.42 14.51 ± 0.29 19.82±0.90 20.96±0.05
Ni 12.39±0.65 2.53 ± 1.25 2.27 ± 0.18 4.79±0.78 2.31±0.86
Pb 2.53±0.79 6.04 ± 0.65 10.05 ± 0.32 12.48±2.17 7.41±0.32
Zn 28.69±2.82 40.55 ± 2.02 47.29 ± 0.74 81.70±1.42 47.77±4.40
*
 <LOD below the limit of detection

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Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769 767

Fig. 2  Scanning electron micrographs of lichen Hypogymnia physodes. Surface of the lichen: A (×1000) and B (×5000), surface of the hyphae:
C (×1000) and D (×5000); 0 – control sample, 3 and 6 month exposed samples (left) and 9 and 12 month exposed samples (right)

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768 Bulletin of Environmental Contamination and Toxicology (2019) 102:763–769

months of exposure to the lichen, SEM images show that Table 7  Results of EDS analysis of the background and transplanted
on the surface of the lichen and hyphae are still deposited lichen after 3, 6, 9 and 12 months of exposure – hyphae surface
particles that are flat, irregular, smooth, oval or agglomer- Elements Back- 3 months 6 months 9 months 12 months
ates of different sizes, the edges of the particles are generally (%) ground
smooth and rounded indicating that the particles deposited
Al 0.32 0.24 0.29 0.25 0.25
on the surface of the lichens are atmospheric dust. Accord-
As < LOD 0.23 < LOD < LOD < LOD
ing to Chaparro et al. (2013) particles from 2 µm up to 5 µm
Bi 1.17 0.86 0.98 < LOD < LOD
and finer ones, as well as smaller irregular particles prob-
C 36.36 38.43 37.55 38.06 37.26
ably originate from vehicles (wear particles). In addition,
Ca 4.02 0.53 1.96 1.58 0.72
the spherules are different from the other ones, showing an
Cd 0.62 0.34 0.12 0.18 < LOD
irregular surface with aggregates of submicron-sized parti-
Cl 0.52 0.15 0.19 0.18 0.16
cles. Characterization of the particles deposited on the sur-
Cr 0.12 < LOD < LOD < LOD < LOD
face of the lichen was done by EDS analysis. The results are
Cu 1.48 0.79 0.63 0.69 0.75
presented in Table 6.
Fe 0.27 < LOD 0.18 < LOD < LOD
Results of EDS analysis for the hyphae surface are pre-
K 0.93 0.47 0.29 0.36 0.25
sented in Table 7.
Mg < LOD 0.11 < LOD 0.19 < LOD
Based on the results presented in Tables 6 and 7, the C
Mn 0.17 < LOD 0.11 < LOD < LOD
and O are present in the largest percentage by weight on the
Na 0.18 < LOD < LOD < LOD < LOD
lichen and hyphae surface. The percentage by weight of Al
O 50.53 56.79 56.23 56.96 59.71
and Si indicates that the particles deposited on the lichen and
P < LOD < LOD 0.15 < LOD < LOD
hyphae surface are in the form of silicates or alumosilicates.
Pb 0.57 0.24 0.27 < LOD < LOD
Also, the mass fraction of Ca, C and O could indicate that
S 0.41 0.36 0.4 0.35 < LOD
particles deposited on the surface of the lichen could be in
Si 1.46 0.3 0.64 1.18 0.15
the form of oxalate (Williamson et al. 2004). The elemental
Zn < LOD 0.16 < LOD < LOD < LOD
analysis of the lichen surface of the control sample shows the
*
dominance of Si, Al, Cl and Bi and on the surface of hyphae  <LOD below the limit of detection

Ca, Si, Cu, Bi and K. The content of Cl on the surface of the

Table 6  Results of EDS analysis of the background and transplanted lichens was almost the same during the time of exposure.
lichen after 3, 6, 9 and 12 months of exposure – lichen surface In conclusion, research of air pollution in urban and rural
Elements Back- 3 months 6 months 9 months 12 months areas by heavy metals using lichen H. physodes as the bioin-
(%) ground dicator revealed that there were no significant deviations in
the content of metals in the lichens from urban and rural
Al 1.84 1.91 0.53 1.03 1.43
areas. SEM and EDS analysis showed that despite significant
Bi 1.47 1.53 1.65 0.96 < LOD
damage to tissue and cell integrity, the recurrent presence of
C 32.69 32.55 38.47 35.04 36.11
particulate matter in lichen, indicates the considerable pres-
Ca 0.69 0.54 2.52 1.31 0.58
ence of dust in the urban atmosphere which, according to
Cd 0.41 0.55 0.20 < LOD 0.44
chemical composition, may be due to the anthropogenic and
Cl 1.62 0.62 0.52 0.46 0.24
natural sources such as soil. Eventually, the study implicates
Cu 0.77 0.65 0.71 0.97 0.63
that lichens H. physodes are good and appropriate biomoni-
Fe 0.59 1.23 0.28 0.48 0.51
tors of air pollutants.
K 0.86 1.4 0.4 0.40 0.79
Mg 0.19 0.43 0.17 0.29 0.22
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