Environmental Pollution 161 (2012) 70e75

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Long-term biological monitoring of environmental quality around a solid waste

landfill assessed with lichens
L. Paoli a, c, A. Corsini b, V. Bigagli b, J. Vannini b, C. Bruscoli b, S. Loppi a, *
a
Department of Environmental Science, University of Siena, Italy
b
ARPAT, Department of Pistoia, Italy
c
Institute of Botany, Slovak Academy of Sciences, Slovakia

a r t i c l e i n f o a b s t r a c t

Article history: The diversity of epiphytic lichens and the accumulation of selected trace elements in the lichen Fla-
Received 24 June 2011 voparmelia caperata L. (Hale) were used as indicators of pollution around a landfill in central Italy along
Received in revised form 14 years of waste management. Lichens revealed an increased deposition for some elements (i.e., Cd, Cr,
20 September 2011
Fe and Ni) and a decrease of the lichen diversity at sites facing the landfill after an enlargement of the
Accepted 27 September 2011
dumping area. However, the results allowed to exclude a significant increase in heavy metal depositions
in the surrounding area and suggested that successful waste management may be associated with
Keywords:
environmental quality. It is concluded that lichen monitoring might provide essential information to
Air pollution
Biomonitoring
enhance the implementation of ecological impact assessment, supporting industrial regulatory proce-
Heavy metals dures, also when waste management is concerned.
Landfill Ó 2011 Elsevier Ltd. All rights reserved.
Lichens

1. Introduction Particulate matter emissions from landfills reflect the chemical

Landfilling is still the main waste disposal method in Europe
(Giusti, 2009) and recent EU legislation prescribes strict rules for
waste disposal in landfills (European Union, Directive, 2008/98/EC
of the European Parliament and of the Council of 19 November
2008).
The public acceptance of waste disposal sites is very low owing
to concern for adverse affects on the environment and human
health, and landfills are often causes of concern for the population
living nearby. Besides potential health hazards, concern on the
environmental impact of solid waste landfilling relies on vegetation
damage, unpleasant odours, fires and explosions, landfill settle-
ment, groundwater and air pollution and global warming (El-Fadel
et al., 1997).
Consequence of the practice of waste disposal in landfills is the
emission of pollutants via the leachate and gas generation (El-Fadel
et al., 1997). Operating solid waste landfills emit a variety of air
pollutants and among them landfill gas and particulate matter (PM)
are particularly important (Bogner and Matthews, 2003; Koshy
et al., 2009). Landfill gas emissions contain methane, carbon
dioxide and a mixture of contaminants of environmental concern,
including volatile organic compounds (Schuetz et al., 2003).
* Corresponding author.
E-mail addresses: loppi@unisi.it, stefano.loppi@unisi.it (S. Loppi).
composition of the disposed waste and may include elements of
toxicological concern (Koshy et al., 2009). These emissions are the
result of decomposition processes, re-suspension from the
disposed waste and other waste management operations, such as
mechanical recycling and composting, waste unloading and sort-
ing, the process of coating residues and waste transport by trucks
(Fitz and Bumiller, 2000). Furthermore, emissions are strongly
influenced by local microclimatic conditions. In general, despite
a large amount of data on landfill leachate and gas characterization
is available (El-Fadel et al., 1997), more information is needed on
airborne particles from landfills and their biological effects on the
surrounding environment (Koshy et al., 2009).
Reliable and regular environmental monitoring should be
included in any process of ecological impact assessment of waste
management, evaluating the ecological impacts of specific activities
in support of regulatory procedures and providing consistent data
for environmental management (Treweek, 1999). In this scenario,
biomonitoring of air pollution is considered a valuable tool for the
implementation of environmental policy on air quality and atmo-
spheric pollution control (Pirintsos and Loppi, 2008) and lichens
offer a unique opportunity to investigate the biological effects of air
pollution, providing reliable information on the quality and char-
acteristics of the environment (Nimis et al., 2002).
Lichens are perennial, slow-growing organisms that maintain
a fairly uniform morphology in time, are highly dependent on the

0269-7491/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2011.09.028
 L. Paoli et al. / Environmental Pollution 161 (2012) 70e75
atmosphere for nutrients, and do not shed plant parts as readily as
vascular plants. The lack of a waxy cuticle and stomata allows many
contaminants to be absorbed over the whole lichen surface (Hale,
1983). These symbiotic organisms have been widely used in bio-
monitoring of air pollution since they can be used both to estimate
the biological effects of pollutants by measuring changes at
community or population level, and as accumulative monitors of
persistent pollutants, by assaying their trace element content (Ferry
et al., 1973). The mapping of lichen diversity is becoming routine in
several countries (see e.g., Kricke and Loppi, 2002) since it gives an
indication of the biological impact of air pollution. It is also quick
and inexpensive, and provides results on which predictions for
human health can be based (Cislaghi and Nimis, 1997). There is also
evidence that lichens can be used to monitor air quality changes in
urban areas over intervals of a few years (Loppi et al., 1997). Lichens
are also very effective in trapping trace elements from the
surrounding environment and it has been demonstrated that the
concentrations of trace elements in lichen thalli are directly
correlated with environmental levels of these elements (Bari et al.,
2001; Sloof, 1995). In addition to floristic changes, variations in
lichen trace element contents in time can provide useful evidence
for trends in ambient pollution burdens. Therefore, lichens are very
useful for monitoring not only spatial patterns but also temporal
trends of trace element deposition (Bennett and Wetmore, 1999,
2000).
In the present paper, the results of a long-term study using
lichens for monitoring the environmental effects of a solid waste
landfill in central Italy are presented. The diversity of epiphytic
lichens and the accumulation of selected elements in the lichen
Flavoparmelia caperata L. (Hale) were used to give an indication of
the biological effects of the atmospheric emissions around a landfill
in central Italy along 14 years of waste management. The envi-
ronmental performance of the landfill was evaluated using
a before-after control-impact approach to ensure environmental
protection of the surroundings. To the best of our knowledge, this is
the first study using lichens for monitoring the environmental
impact of landfilling.
2. Materials and methods
2.1. Study area
The investigated landfill (Discarica del Cassero, 43
520 5200 N, 10
530 2100 E, ca.
60 m asl) is located in Tuscany, Central Italy, 5 km SW of the town of Pistoia.
It started operating during 1996 with an authorized volume of 1,510,000 cubic
meters. In 2007, an extension of the landfill capacity was authorized. Actually, it
extends over an area of 160,000 m2 and it is foreseen to operate until 2025, when the
overall volume will be 3,010,000 cubic meters.
Every day, up to 420 tonnes of waste is authorized for landfilling after careful
analysis: the disposed waste includes municipal solid, hazardous and non hazardous
wastes and the material for landfill cover. Wastes may include scraps of paper,
plastics and metals, packing, spent tires, textile products, building materials, ashes
from municipal solid waste incinerators, polluted terrain from environment recla-
mation, etc.
The landfill site is located over an impermeable natural clay layer; bottom and
side boundaries may vary according to the period of cultivation, however they
generally include several protective layers, such as a compact clay layer (100 cm),
geotextile membranes, gravel (50 cm), geomembranes (2.5 mm) non-woven fabric
(1200 g/m2), pulper products (50 cm).
Landfill covers (top and side) are formed by a waste layer (terrain) to stabilize
the surface, drainage systems, compact clay (20 cm), soil bentonite and a vegetative
soil layer (up to 100 cm). A grassy mantle and/or forestation with local vegetation
will complete the recovery of the environment after closing of each parcel. Systems
for leachate treatment, and gas recovery, collection and treatment are in operation;
in addition, landfill gas is used to support energy needs of the facility.
The landfill is surrounded to the N, W and S by a vegetation belt dominated by
Quercus cerris and Q. pubescens. The hilly landscape in the western part of the study
area is characterized by vineyards, olive plantations and woodlands, while to the E
lowland, in direction of the main town (Pistoia), several plant nurseries and
inhabited areas prevail.
71
The climate of the area is intermediate between sub-oceanic and sub-
Mediterranean, with mean annual rainfall over 1300 mm and mean annual
temperature of 14.1
C.
2.2. Lichen sampling
The diversity of epiphytic lichens and the accumulation of selected elements
were investigated before (1996) and after (2000) the opening of the site and before
(2008) and after (2010) its enlargement as part of the Ecological Impact Assessment
characterization involving water, soil and air quality. The assessment of environ-
mental quality with epiphytic lichens is part of prescriptions implemented to
improve the environmental performance and enhance health protection (Eco-
Management and Audit Scheme, EMAS).
2.3. Sampling design and sampling strategy
During the first lichen survey (1996), a tree-based random approach was used to
select 36 sampling units in the area surrounding the forthcoming landfill. In 2000
the study area was centred on the landfill and divided into 36 sampling units of
500  500 m, following a systematic sampling design. At each sampling unit, 3
standard trees were randomly selected, georeferenced and lichen sampling was
carried out. In 2008, prior to the enlargement of the landfill, other 14 sampling plots
(60 m diameter) were randomly selected around the landfill following a double-ring
scheme. The inner ring consisted of 8 plots directly facing the landfill and the outer
ring consisted of 6 plots at distances <500 m from the landfill, roughly corre-
sponding to the outer margin of the vegetation belt directly surrounding the landfill.
Trees for epiphytic lichen sampling (deciduous Quercus or, alternatively, Tilia,
which proved valid alternative trees; Loppi and Putortì, 1995) were deemed suitable
if well lit, with girth >60 cm, trunk near straight, not damaged and without parts
with >25% cover of bryophytes.
2.4. Diversity of epiphytic lichens
At each sampling unit an Index of Lichen Diversity (ILD) was calculated as the
sum of frequencies of epiphytic lichens in a sampling grid of 30  50 cm (consisting
of 10 units, each 15  10 cm) positioned on the bole of standard trees at 1 m from
ground, on the side where lichen abundance was the greatest. This sampling
methodology was adopted before the opening of the landfill (1996) and after four
years of operation (2000).
In 2001, a new standardized protocol for lichen monitoring was developed in
Italy (ANPA, 2001) and contributed to the European guidelines (Asta et al., 2002).
Consequently, in 2008 and 2010 the ILD was computed with a new standard
sampling grid (ANPA, 2001) consisting of four 50  10 cm ladders, each divided into
five 10  10 cm units. The grid was positioned systematically on the N, E, S and W
cardinal sides of the bole of each tree, at a height of 1 m above ground.
The ILD of the tree corresponded to the sum of frequencies of epiphytic lichens
in the grid and the ILD of each monitoring site was the arithmetic mean of the ILD
measured for each sampled tree. Lichen diversity values recorded in 1996 and 2000
were converted to the new sampling protocol (ANPA, 2001) following Frati and
Brunialti (2006), to allow direct comparison with the data measured in 2008 and
2010.
In case of identification problems during field sampling, specimens were
collected and identified later in the laboratory. Nomenclature follows the online
database italic (Nimis and Martellos, 2008). Species belonging to the genus Lepraria
have been determined up to the genus level, Punctelia borreri (Sm.) Krog. may include
the similar P. subrudecta (Nyl). Krog and Cladonia coniocraea (Flörke) Spreng. may
include undeveloped thalli of other Cladonia species (such as C. fimbriata (L.) Fr.).
2.5. Bioaccumulation of trace elements
Thalli of the foliose lichen Flavoparmelia caperata were collected for element
analysis at 36 sampling units in 1996 and 2000, whereas in 2008 and 2010 samples
have been collected at 25 selected sampling units, most of them (14) within 500 m of
the landfill area. Sampling units investigated for element depositions are the same
investigated for lichen biodiversity.
The species F. caperata was chosen because of its wide distribution in the study
area and because it had been already used in bioaccumulation studies in neigh-
bouring areas (e.g., Loppi et al., 1994, 1995). At each sampling unit, 10e30 thalli
growing on the bole of 3e10 trees (chiefly Quercus) were harvested from all cardinal
exposures, between 100 and 200 cm from ground. Tree boles were deemed suitable
for lichen harvesting if almost straight, not damaged and without parts with >25%
cover of bryophytes.
Samples were carefully cleaned under a binocular microscope to remove
extraneous material deposited onto the surface, such as moss samples, bark pieces
and soil particles.
Only the peripheral part of the thalli (up to 5 mm from lobe tips) was selected for
the analysis; in F. caperata this part roughly corresponds to 1 year age and can be
easily separated from the bark, being distinguishable by a paler colour and absence
of rhizinae.
72 L. Paoli et al. / Environmental Pollution 161 (2012) 70e75

Samples were not washed, since the washing procedure may unpredictably alter Table 2
their chemical composition (Bettinelli et al., 1996). Lichen samples were air-dried to Lichen species found before (1996) and after (2000) the opening of the landfill and
constant weight and then immersed in liquid nitrogen, pulverized and homogenized before (2008) and after (2010) the enlargement of the landfill. P ¼ percentage
with a ceramic mortar and pestle. About 200 mg of powdered lichen material was occurrence (sites where the species was found expressed as percentage);
mineralized with a mixture of 6 mL of 70% HNO3, 0.2 mL of 60% HF and 1 mL of 30% F ¼ frequency expressed as percentage. * ¼ nitrophilous species. Nomenclature
H2O2 in a microwave digestion system (Milestone Ethos 900) at 280
C and 55 bars. follows Nimis and Martellos (2008).
Concentrations of selected elements of toxicological concern (As, Cd, Cr, Ni, Pb, V, Zn)
and Fe (being associated to soil contamination of the samples) were determined by Lichen species 1996 2000 2008 2010
ICP-MS (Perkin Elmer e Sciex, Elan 6100) and expressed on a dry weight basis (mg/g P F P F P F P F
dw). Analytical quality was checked by analyzing the Standard Reference Material
Flavoparmelia caperata 97 87.1 100 74.7 97 53.8 97 54.8
IAEA-336 ‘lichen’. Precision of analysis was estimated by the coefficient of variation
Lepraria spp. 92 61.8 94 78.4 95 52.5 97 46.1
of 4 replicates and was found to be within 10% for all elements. Three replicates were
Candelariella reflexa* 19 78.6 56 45.7 90 40.9 95 37.1
measured at every monitoring site.
Parmelia sulcata 81 59.3 84 45.4 85 21.5 89 21.8
Physcia adscendens* 17 46.8 72 49.1 92 41.2 87 43.6
2.6. Data interpretation and statistical analysis Hyperphyscia adglutinata* e e 34 32.7 90 40.4 87 34.7
Punctelia borreri 44 28.8 88 24.4 74 18.6 87 19.7
To assess possible biological effects caused by the presence of the landfill, Leprocaulon microscopicum 17 63.3 66 39 69 28.6 87 28
sampling units were classified into 3 groups at increasing distance from the landfill: Normandina pulchella e e 53 37.1 67 27.8 76 27.8
1) sampling units directly facing the landfill (8 plots, data available since 2008); 2) Lecidella elaeochroma* 42 35.3 59 33.2 74 28.7 71 24.9
sampling units within 500 m of the landfill (13 plots); 3) sites located at more than Melanelixia fuliginosa e e 56 41.1 74 36 71 32.5
500 m from the landfill (29 plots). Parmotrema perlatum 17 36.7 91 22.3 64 9.8 66 7.4
Significance of differences (P < 0.05) was checked by ANOVA, using the Bon- Lecanora strobilina e e e e 56 18.8 66 27.3
ferroni test for post-hoc comparisons. Prior to analysis data not matching a normal Cladonia coniocraea 11 72.5 75 30.7 59 11.5 58 10.8
distribution (KolmogoroveSmirnov test at the 95% confidence interval) were treated Candelaria concolor* 31 42.7 22 29 59 17.3 58 19.7
with Box-Cox transformation. Evernia prunastri 25 24.4 53 18.6 49 4 53 4.3
The ILD values were interpreted in terms of air pollution according to the Lecanora chlarotera* e e 50 19.2 49 8.9 42 7.4
following scale valid for Tyrrhenian Italy (Loppi et al., 2006; Paoli and Loppi, 2008): Amandinea punctata* e e 3 83.3 33 17.7 39 11.4
0 ¼ very high (lichen desert), 1e40 ¼ high, 41e80 ¼ moderate, 81e120 ¼ low, Parmelina tiliacea 61 25.9 34 10 38 4.9 34 3.5
>120 ¼ negligible. Physcia tenella* 44 46.8 34 38.2 18 35.5 29 25
Metal concentrations were interpreted in terms of air pollution based on a scale Lecanora symmicta e e 13 5 13 10.7 29 5.5
(Table 1) desumed from Bargagli and Nimis (2002). Phlyctis argena e e 25 10.8 18 4.8 26 5.3
Pertusaria albescens e e 22 4.8 33 3.4 24 3.7
Flavoparmelia soredians e e 44 32.1 23 16.9 24 13.1
3. Results Hypogymnia physodes e e 22 12.9 18 5.5 24 4.4
Ramalina farinacea e e 53 13.3 15 2.5 24 2.4
3.1. Diversity of epiphytic lichens Physconia grisea ssp. grisea* 3 70 9 3.3 21 5.2 21 5.2
Lecanora carpinea* 17 31.7 25 5.8 21 2.3 13 2
Xanthoria parietina* e e 16 4.7 21 4.8 13 9.3
The whole lichen flora recorded during all years consists of 70 Aplotomma turgida e e e e 15 7 13 4.3
taxa (Table 2). Twenty species were always found throughout the Tephromela atra v. torulosa e e e e 10 2.1 13 1.7
14 years of the study. In particular, considering all data since 2000  Candelariella xanthostigma 6 50 6 66.7 13 15.7 11 17.5
Physconia servitii 3 20 3 10 13 6.7 11 9.2
when the systematic sampling grid of 9 km2 still in use was
Catillaria nigroclavata e e e e 13 8.4 11 6.7
installed, the following species have been always observed in more Melanelixia subaurifera 56 70 22 53.3 10 15.9 11 12.5
than 70% of the sites: F. caperata, Parmelia sulcata, Physcia adscen- Lecanora expallens e e e e 8 14.5 11 6.3
dens, P. borreri and Lepraria spp. In addition, F. caperata and Lepraria Physcia clementei e e 9 27.8 5 15 11 9.2
spp. are the most abundant throughout the study area. Apart from Phaeophyscia chloantha* e e e e 5 20.9 11 18.8
Phaeophyscia hirsuta e e e e 5 1.7 11 4.6
Candelariella reflexa, P. adscendens, H. adglutinata and few other
Heterodermia obscurata e e 16 11.3 13 4.4 8 16.1
nitrophilous and pollution-tolerant lichens common in all the Dimerella pineti e e e e 3 11.7 8 10
environments, ca. 70% of total recorded frequencies was deter- Lecanora argentata e e e e 8 3.9 5 1.7
mined by mesophilous and acidophilous or subneutrophilous Chrysothrix candelaris e e 44 42.4 5 6.7 5 13.3
species. Overall the epiphytic lichen flora was characterized by Caloplaca ferruginea 3 10 6 10 5 1.7 5 1.7
Rinodina pyrina e e 6 11.7 5 5 5 5
rather hygrophytic and low nitrophytic species throughout the 14 Collema subflaccidum e e e e 5 5 5 5
years of the study. Lecania cyrtella e e e e 5 3.4 5 3.3
The results of lichen diversity measurements are summarized in Melanohalea elegantula e e 9 15.6 3 5 5 10.8
Table 3. Within each group of sampling units, differences between Phaeophyscia orbicularis* e e 9 20 18 5.3 3 8.3
Parmelina pastillifera e e 6 8.3 3 3.4 3 3.3
years were statistically (P < 0.05) not significant. Different groups
Physconia perisidiosa e e 6 16.7 3 3.4 3 1.7
of sites showed statistically (P < 0.05) different ILD values as Caloplaca flavorubescens e e e e 3 1.7 3 5
a function of distance from the landfill, and indicated some wors- Caloplaca obscurella* e e e e 3 15 3 20
ening of the air quality status at the landfill passing from low air Pertusaria flavida e e e e 3 25 3 23.3
pollution at sites located at a certain distance (irrespective Mycomicrothelia confusa e e e e 3 50 3 28.3
Physcia aipolia* e e 9 4.4 e e 3 1.7
if < 500 m or > 500 m) from the landfill, to moderate air pollution Ramalina fraxinea e e 3 3.3 3 1.7 e e
at sites directly facing the landfill. Pertusaria amara 6 15 e e 3 1.7 e e
Schismatomma decolorans e e e e e e 3 1.7
Candelariella vitellina e e e e 3 1.7 e e
Table 1 Parmelia saxatilis e e e e 3 6.7 e e
Scale for the interpretation of trace element concentrations in lichens (mg/g dw). Pertusaria hymenea e e e e 3 1.7 e e
Physcia leptalea e e 13 7.5 e e e e
air pollution Pb Cu Cr Zn Fe Ni Cd As Physconia venusta e e 9 12.2 e e e e
very low <10 <9 <2 <35 <400 <1.5 <0.3 <0.4 Haematomma ochroleucum e e 6 15 e e e e
low 25 15 4 65 800 3.0 0.6 1.2 Parmotrema stuppeum e e 6 6.7 e e e e
moderate 55 25 6 95 1200 5.0 1.2 1.9 Usnea sp. e e 6 3.3 e e e e
high 95 40 13 135 1600 7.0 2.1 2.5 Collema subnigrescens e e 3 30 e e e e
very high >95 >40 >13 >135 >1600 >7 >2.1 >2.5 Parmelina quercina e e 3 3.3 e e e e
Physcia biziana v. biziana* e e 3 6.7 e e e e
 L. Paoli et al. / Environmental Pollution 161 (2012) 70e75 73

Table 3 Table 4
Values of the Index of Lichen Diversity (ILD) and air pollution status as a function of Concentrations of trace elements (mg/g dw  standard deviations) in the lichen
distance from the landfill. 1996 ¼ before the opening of the landfill, 2000 ¼ after the F. caperata as a function of distance from the landfill. 1996 ¼ before the opening of
opening of the landfill, 2008 ¼ before the enlargement of the landfill, 2010 ¼ after the landfill, 2000 ¼ after the opening of the landfill, 2008 ¼ before the enlargement
the enlargement of the landfill. Differences between years are statistically (P < 0.05) of the landfill, 2010 ¼ after the enlargement of the landfill. Statistically significant
not significant; differences between sites (P < 0.05) are indicated by different letters. (P < 0.05) temporal differences (vertical) are indicated by different capital letters;
statistically significant (P < 0.05) spatial differences (horizontal) are indicated by
Year Landfill <500 m >500 m different small letters.
1996 e 82  11a 85  18a
low low Element Year Landfill <500 m >500 m
2000 e 828a 85  18a Pb 1996 e 12.4  10.2Aa 13.2  10.4Aa
low low low low
2008 69  13a 82  13b 88  18b 2000 e 6.7  3.2Ba 6.0  3.6Ba
moderate low low very low very low
2010 68  18a 81  18b 85  16b 2008 5.2  2.5Aa 4.7  2.4Ba 4.1  1.1Ba
moderate low low very low very low very low
2010 10.1  2.4Ba 5.3  1.6Bb 7.3  3.3Bb
low very low very low
Cu 1996 e 10.2  1.5Aa 9.9  4.5Aa
low low
Locally, symptoms of injury to lichen thalli i.e. discoloration and 2000 e 6.9  1.1Ba 5.9  1.2Ba
necrosis, were observed in 2010 at a few sites directly facing the very low very low
southern boundary of the landfill, close to the new parcel under 2008 12.2  1.6Aa 9.6  0.9Ab 9.1  1.1Ab
low low low
cultivation, and in 1 unit the ILD shifted from 75  15 in 2008 to 2010 11.0  2.1Aa 8.4  1.3Bb 6.7  1.1Bc
45  20 in 2010. low very low very low
Cr 1996 e 1.43  0.40Aa 1.44  1.26Aa
very low very low
3.2. Bioaccumulation of trace elements 2000 e 1.36  0.37Aa 1.36  0.65Aa
very low very low
2008 2.19  0.88Aa 1.53  0.31Ab 1.22  0.25Ab
The results of analytical determination of heavy metals in low very low very low
F. caperata are summarized in Table 4. 2010 4.81  1.71Ba 2.99  1.55Ab 1.52  0.35Ac
Statistically significant (P < 0.05) spatial patterns were found moderate low very low
for all elements except As and Zn, with concentrations always Zn 1996 e 49.2  5.3Aa 42.6  8.7Aa
low low
higher at the landfill and in some cases (Ni; Cd and Fe in 2010) 2000 e 39.9  9.1Aa 35.8  12.1Aa
also at sites <500 m from the landfill. At sites located at low low
distances >500 m from the landfill all elements were found at 2008 89.4  31.5Aa 81.2  29.9Ba 80.7  13.0Ba
concentrations indicating low or very low air pollution. The moderate moderate moderate
2010 52.2  8.0Ba 48.6  8.2Aa 41.2  6.0Aa
same situation was found also for sites located at distances
low low low
<500 m from the landfill, with the sole exception of Ni, which Fe 1996 e e e
showed moderate air pollution. At the landfill, Pb in 2008 was 2000 e e e
the only element indicating very low air pollution, Cd and Fe 2008 506  273Aa 320  76Ab 277  92Ab
indicated moderate air pollution in 2010, and Ni indicated low very low very low
2010 1072  604Ba 442  114Bb 294  66Ac
moderate pollution in 2008 and high pollution in 2010; the moderate low very low
remaining elements throughout the years of sampling indicated Ni 1996 e e e
low air pollution. Zn in 2008 constantly showed moderate air 2000 e e e
pollution. 2008 4.6  1.0Aa 3.6  0.8Aa 2.4  0.3Ab
moderate moderate low
Statistically significant (P < 0.05) temporal patterns emerged for
2010 5.5  1.1Ba 3.6  0.6Ab 2.9  0.7Ac
several elements. Concentrations of Pb showed a reduction from high moderate low
1996 (low air pollution) compared with the following years (2000, Cd 1996 e e e
2008, 2010 e very low air pollution); at the landfill an increase in 2000 e e e
the concentrations (from very low to low air pollution) was noted in 2008 0.41  0.08Aa 0.24  0.04Ab 0.25  0.07Ab
low very low very low
2010 after the enlargement. Cu remained stable (low air pollution)
2010 0.60  0.14Ba 0.37  0.08Bb 0.29  0.06Ac
at the landfill and showed some fluctuation (low or very low air moderate low very low
pollution) at the other sites. Cr showed an increase at the landfill As 1996 e e e
(from low to moderate air pollution) and at sites <500 m in 2010 2000 e e e
2008 0.49  0.12Aa 0.40  0.05Aa 0.42  0.09Aa
(from very low to low air pollution), while remained stable at sites
low low low
>500 m from the landfill. Concentrations of Zn indicated always 2010 0.46  0.18Aa 0.40  0.06Bb 0.40  0.04Bb
low air pollution with the exception of the year 2008 at all sites, low low low
where moderate air pollution was found. Fe showed an increase at
the landfill (from low to moderate air pollution) and at sites
<500 m (from very low to low air pollution), while remained stable 4. Discussion
at sites >500 m from the landfill. Concentrations of Ni increased
only at the landfill (from moderate to high), whereas were constant There is enough scientific evidence that lichen species occurring
both at sites <500 m (moderate air pollution) and > 500 m (low air naturally within an area of interest show measurable responses to
pollution) from the landfill. Cadmium showed an increase at the environmental changes and that lichen diversity counts can be
landfill (from low to moderate air pollution) and at sites <500 m taken as reliable estimates of environmental quality, with high
(from very low to low air pollution), while remained stable at sites values corresponding to unpolluted environments and low values
>500 m from the landfill. Arsenic did not show any temporal to polluted ones (Nimis et al., 2002). The results of the present
variation. study indicated moderate air pollution at the landfill, suggesting
74 L. Paoli et al. / Environmental Pollution 161 (2012) 70e75
that dumping activities are the cause of such moderate worsening
compared with the surrounding area. This negative effect is
however very local and modest since sites surrounding but not
directly facing the landfill were not influenced and the situation did
not change in time. Moreover, based on field observations, we
suggest that adverse effects on lichens observed in 2010 at a few
sites directly facing the new parcel under cultivation are mainly
caused by airborne dust originating from digging operations to
enlarge the landfill.
According to Loppi and Pirintsos (2000) all lichens, except for
a few resistant species, are injured and may die when subjected to
high airborne dust concentrations, irrespective of dust chemistry.
When damage is not so intense, the general picture of the epiphytic
lichen vegetation influenced by sources of dust such as quarries,
cement plants or dirty roads consists in a shift from lichen
communities dominated by Flavoparmelia caperata and Parmo-
trema perlatum towards communities dominated by Xanthoria
parietina and Physcia adscendens (Del Guasta, 1994; Gilbert, 1976;
Jürging, 1975; Loppi, 1996). The effect of dust on lichen communi-
ties is similar to that of ammonia emissions, promoting nitrophytic
lichen vegetation (Loppi and De Dominicis, 1996).
The present results clearly outlined that throughout the period
of the study, the area remained characterized by a low degree of
eutrophication, both in the surroundings of the landfill as well
as in rural sites, and these conditions did not change. Usually, in
rural areas, pollution-tolerant and nitrophilous species dominate
lichen communities as a consequence of increasing eutrophication
and this process is generally enhanced in semi-arid environments
(Paoli et al., 2006). The lichen vegetation of the study area,
dominated by mesophilous and acidophilous or subneutrophilous
species, seems to be primarily driven by climatic parameters (sub-
oceanic and sub-Mediterranean) and to a lower extent by other
stress factors. Furthermore, part of the differences concerning the
presence of new species reflects natural heterogeneity of the area
and may be due to differences in the sampling protocols during
the study.
It is well known that the chemical composition of lichens
reflects the availability of trace elements in the environment
(Backor and Loppi, 2009). In general, high concentrations of litho-
genic elements (e.g., Al and Fe) measured in lichens and mosses are
associated with high levels of deposition from airborne soil dust
(Bargagli, 1998). The increase in Fe levels observed in F. caperata
thalli at the landfill in 2010 is likely due to soil dust containing Fe,
recently resuspended during excavation works and waste stabili-
zation related to the enlargement of the dumping area. Vega et al.
(2001) found that resuspended surface dust from the Mexico City
landfill, characterized by high levels of Si and Al, influenced the
composition of particulate matter around the landfill.
A comparison between PM10 in a landfill in Crete (Greece) and
the nearby background area indicated the influence of dumping
activities and dust re-suspension on local concentrations at the
landfill (Chalvatzaki et al., 2010). The analysis of airborne emissions
from a landfill in the UK, compared with a neighbouring urban area,
revealed Fe, Cr, Ni, Pb and Zn as the main components of the
particulate matter around the landfill (Koshy et al., 2009). Similarly,
in our study we observed higher Cr, Fe and Ni depositions in front of
the landfill in 2010. However, low levels of heavy metals were
found in the area surrounding the landfill, within 500 m of distance,
allowing to exclude a significant increase in element depositions in
the surrounding area due to dumping activities.
For Pb, a progressive decrease in time was observed. Pollution
by Pb is traditionally linked to motor combustion processes and
ambient levels of this element have dramatically fallen owing to the
ban of leaded gasoline (Loppi et al., 2004). The low concentrations
found suggest the lack of other potential sources in our study area.
Moderately high values of Zn in 2008, spread all over the area,
are probably related with seasonal spraying of Zn-containing
fertilizers and pesticides, heavy use of which is made in the
numerous plant nurseries in the study area. Previous bio-
monitoring studies (Loppi et al., 1992, 1994) showed that in the
Pistoia area overall air quality was quite good and that the atmo-
spheric concentrations of Cd, Cr, Ni and Pb were comparable with
those found in areas not subject to atmospheric pollution, while Cu
and especially Zn were found in rather high concentrations. Both
studies concluded that the main sources of air pollution were from
fertilizers and pesticides used in plant nurseries.
Symptoms of injury to lichen thalli (discolouration and
necrosis), lower ILD and higher element concentrations (Cd, Cr, Fe
and Ni) were found only in the sampling sites directly facing the
southern part of the landfill, corresponding to the parcel under
cultivation. In this context, it is noteworthy the buffering role on
particulate matter diffusion of the vegetation belt dominated by
oak trees that surrounds the landfill site.
The deposition of heavy metals may be detrimental to human
health and knowledge of element concentrations in atmospheric
deposits is fundamental to understand which elements promote
the occurrence of specific diseases (Ghio, 2004). To estimate
element deposition rates from element concentrations in lichens,
a knowledge of the biomass of F. caperata is required. For this
purpose, several thallus pieces were cut, measured for their surface
area and weighed (dry weight), allowing to calculate a weight/area
ratio of w100 g/m2. Based on the fact that the analyzed material
roughly corresponded to the biomass formed during the last year
(Showman, 1976; Fisher and Proctor, 1978), and assuming 100%
retention in the lichen, it was possible to convert metal concen-
trations into estimates of average metal deposition rates (in g/ha/
y): Pb ¼ 10.1; Cu ¼ 5.5; Cr ¼ 2.4; Zn ¼ 26.1; Fe ¼ 536; Ni ¼ 2.8;
Cd ¼ 0.6; As ¼ 0.23. As a confirmation of the validity of this
calculation approach, our estimates of Cd and Pb fluxes are
perfectly in line with those of 0.25e0.75 and 10e20 respectively
reported for these elements for the study area (www.msceast.org/
countries/Italy). Moreover, data estimated for the study area are
consistent with those measured at several localities of the Medi-
terranean basin (Gieu et al., 2010).
An investigation of trace elements accumulated in mosses
transplanted around solid waste landfills in northern Italy allowed
to exclude a significant increase in heavy metal deposition in the
surrounding area along two years of monitoring (Cenci et al., 2005).
Researches carried out in Germany (Ilgen et al., 2008) showed a low
risk of organometallic compounds release to the adjacent air due to
flaring of landfill gases around 12 landfill sites. These evidences
suggest that when the waste disposal option of landfilling is
correctly managed, there is a relatively low risk of environmental
contamination.
On the contrary, incorrect waste management practises clearly
determine air pollution by toxic elements and compounds, as
shown for the area of Acerra, near Naples (south Italy), concerned
by years of illegal waste dumping and management of hazardous
waste (Senior and Mazza, 2004). In that area, Basile et al. (2009)
demonstrated by means of moss biomonitoring a diffuse environ-
mental contamination by heavy metals, a large proportion of which
was likely present in the atmosphere in particulate form.
5. Conclusions
The diversity of epiphytic lichens and the accumulation of trace
elements in F. caperata thalli along a period of 14 years revealed an
increased deposition for some elements (i.e., Cd, Cr, Fe and Ni) and
a decrease of the lichen diversity limited to sites facing the landfill
after the enlargement of the dumping area. However, data allowed
 L. Paoli et al. / Environmental Pollution 161 (2012) 70e75
to exclude a significant increase in heavy metal depositions in the
surrounding area and suggested that successful waste management
may be associated with environmental quality.
This study showed that lichen monitoring might provide
essential information to enhance the implementation of ecological
impact assessment, supporting industrial regulatory procedures,
also when waste management is concerned.
Acknowledgments
We are grateful to Pistoiambiente for supporting this research.
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