Ecological Indicators 95 (2018) 831–840

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Original Articles

Atmospheric pollution assessed by in situ measurement of magnetic T

susceptibility on lichens
⁎
Débora C. Mariéa, Marcos A.E. Chaparroa, , Juan M. Lavorniab,c, Ana M. Sinitoa,
Ana G. Castañeda Mirandaa, José D. Gargiuloa, Mauro A.E. Chaparrod, Harald N. Böhnele
a
Centro de Investigaciones en Física e Ingeniería del Centro de la Provincia de Buenos Aires (CIFICEN, CONICET-UNCPBA), Pinto 399, 7000 Tandil, Argentina
b
Instituto de Ciencias Polares, Ambiente y Recursos Naturales (ICPA), Universidad Nacional de Tierra del Fuego (UNTDF), Fuegia Basket 251, 9410 Ushuaia, Argentina
c
Centro de Investigaciones y Estudios Ambientales (CINEA-UNCPBA), Pinto 399, 7000 Tandil, Argentina
d
Centro Marplatense de Investigaciones Matemáticas (CEMIM-UNMDP, CONICET), Mar del Plata, Argentina
e
Centro de Geociencias – UNAM, Boulevard Juriquilla No. 3001, 76230 Querétaro, Mexico

A R T I C LE I N FO A B S T R A C T

Keywords: The use of environmental magnetism methods and biomonitors allows us the development of a low-cost tool for
Fe-rich particles assessing atmospheric pollution through trapped magnetic particulate matter. Such particles concentration was
In situ biomonitoring monitored in situ, on the lichen’s thallus, using magnetic susceptibility as a pollution proxy. We studied the
Magnetic susceptibility magnetic particle distribution on the thallus surface from weekly measurements of in situ magnetic susceptibility
Parmotrema pilosum
κis during 16 months for seven sites. A total of ∼8300 measurements was carried out; and mean overall κis values
PM2.5
for each lichen varied between 4.1 and 23.9 × 10−5SI revealing the influence of different atmospheric pollution
sources on Parmotrema pilosum, such as metallurgical factories and vehicular emissions. Weekly measurements of
κis show areas of magnetic accumulation on the thallus over a period of 60 measurement campaigns. Iron rich
spherules and irregular particulate matter between PM2.5 and PM1.0 were observed by SEM-EDS. A joint analysis
of meteorological variables and magnetic susceptibility shows an inverse relation between this magnetic para-
meter and temperature, i.e., a trend of decreasing κis values during seasons of higher temperatures which tend
toward higher values of atmospheric mixing height. Precipitation also affects the magnetic signal over time,
producing decreases in mean values of κis after rainy periods.

1. Introduction 2003; Lodenius, 2013). Lichens accumulate metals and others pollu-
tants (NO2, SO2, HF, ozone compounds and particulate matter) from the
The terms bioindicator and biomonitor have different meanings, the atmosphere by dry and wet deposition (Sett and Kundu, 2016,
first one refers to the use of organisms through which any current (or Boamponsem and de Freitas, 2017). Particulate matter (PM) and po-
past) phenomenon or event related to the study of the environment can tentially toxic elements (PTE) can be incorporated by these natural
be decoded. The second term is the quantitative measurement of par- collectors in different ways and times.
ticulate matter, elements and compounds (e.g., polycyclic aromatic According to Chaparro de Valencia and Aguirre Ceballos (2002), the
hydrocarbons PAHs, polychlorinated biphenyls PCBs, etc.) deposited accumulation of contaminants in the lichen’s thallus over time may be
and/or accumulated in organisms or their parts. Among epiphytic determined because of their longevity. The growth of lichens depends
species, lichens, Tillandsia spp. and mosses in their natural state have on the presence of PM and/or PTE and may even stop in highly con-
been used as bioindicators and/or biomonitors (Shacklette, 1973; taminated environments (Bardelás, 2012); since the lichen’s sensitivity
Grodzinska, 1978; Schrimpff, 1984; Rhoades, 1999; Ares et al., 2012; is greater (and resistance is lesser) when the stems are young. In par-
Chaparro et al., 2013; Kováčik et al., 2014). Lichens are recognized as ticular, the growth can be interrupted by high values of SO2; although
air pollution bioindicators and biomonitors, as due to the absence of a some species such as Lecanora conizaeoides have shown in experiments
root system, a protective cuticle, and of stomata, their exchange of to be resistant to this compound. Kováčik et al. (2011) studied the
nutrients with the atmosphere occurs over the entire surface of their physiological responses of lichens Hypogymnia physodes and Xanthoria
thalli; moreover, they grow slowly and are long-lived (Zschau et al., parietina, as well as the Bromeliaceae Tillandsia albida, exposed to

⁎
Corresponding author at: CIFICEN (UNCPBA), Pinto 399, B7000GHG Tandil, Argentina.
E-mail address: [email protected] (M.A.E. Chaparro).

https://doi.org/10.1016/j.ecolind.2018.08.029
Received 2 May 2018; Received in revised form 7 August 2018; Accepted 13 August 2018
Available online 23 August 2018
1470-160X/ © 2018 Elsevier Ltd. All rights reserved.
D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 1. Study area in Tandil city (Buenos Aires Province, Argentina). Measurement sites (and lichen individuals L0–L6) and metallurgical factories location (plus
signed).

simulated acid rain. Pigments were depressed in all species, with Til- during 60 measurement campaigns; b) to determine the distribution of
landsia sp. being the most affected. Macronutrients (K, Ca, and Mg) magnetic particulate matter on thalli surface for lichens exposed to
decreased more pronouncedly in comparison with micronutrients in all different pollution sources; c) to evaluate temporal changes of such PM
species. The comparison between lichen species showed that X. par- distribution and the influence of meteorological conditions during
ietina has the highest tolerance, suggesting its use as a long-term bio- about one year; d) last but most important, to validate the use of in situ
monitor. Recently, studies carried out by Kováčik et al. (2018a,b) measurements of magnetic susceptibility (κis) on lichen’s thallus as a
showed changes in metabolism and oxidative stress symptoms for two novel methodology for magnetic assessment of the atmospheric pollu-
lichen species Cladonia arbuscula subsp. mitis and Cladonia furcata ex- tion over periods from days to years, which is non-destructive and thus
posed to Ni, Cu, and Cr excess. preserves the species.
Sett and Kundu (2016) found that the lichen’s size is a good in-
dicator of air quality. However, the lichen growth rate is species de- 2. Methods
pendent and is influenced by their habitat, that is, specific geographical
conditions for each zone, such as height above the sea level, length of 2.1. Study area, measurement sites and lichens
sun exposure, etc. Dumont et al. (2013) obtained a growth rate for li-
chen Caloplaca cinericola of 0.2 mm/year that is comparable to those This study was carried out in Tandil city (37° 19.5′ S; 59° 08.3′ W),
obtained by Lindsay et al. (1973) for the species Rhizocarpon geo- which is located in the SE part of Buenos Aires Province, Argentina. The
graphicum (0.13 mm/year), where their studies were carried out in the city has a population of 125,000 inhabitants (Censo, 2010) and a
Antarctic Peninsula. number of 60,000 vehicles (Sosa, 2015), including cars, trucks and
The use of biological material for atmospheric pollution monitoring heavy transport. The study area has a sub-humid to humid climate and
is an alternative method to assess the air quality in urban areas and is characterized by strongly differing summer and winter seasons that is
other sites of interest such as industrial settings (e.g., Salo et al., 2014; a distinctive characteristic at this Pampean region. As general char-
Abril et al., 2014; Castañeda Miranda et al., 2016; Gargiulo, 2018). acteristics, summer seasons are hot and rainy, and the winters are cold
Magnetic biomonitoring combines environmental magnetism techni- and dry. Meteorological analysis realized in 2001–2010 (Picone et al.,
ques and the use of biological collectors (e.g., epiphytic species) for 2012) indicates an annual mean temperature of 13.4 °C and annual
assessing industrial and urban pollution. This kind of magnetic bio- precipitation of 845.2 mm (Picone, 2014; Sosa, 2015). Meteorological
monitoring studies has become a methodology of growing interest since variables for the study period (March 2016–July 2017) indicate an
last decades. Jordanova et al. (2010), Chaparro et al. (2013), Marié annual precipitation of 1237.6 mm, and maximum and minimum mean
et al. (2016), and Kodnik et al. (2017) have conducted magnetic temperatures of 19.6 °C and 6.7 °C, respectively (CIM, 2017).
monitoring studies using different lichen species as biomonitors of at- Seven lichen individuals labelled as L0 to L6 were selected in lo-
mospheric pollution. Chaparro et al. (2014), Castañeda Miranda et al. cations with variable pollution sources and intensities within this urban
(2016) and Mejia-Echeverry et al. (2018) proved the inexpensive use of area (Fig. 1- Table 1). The species Parmotrema pilosum living on tree
Tillandsia spp. as efficient collectors and sensors of airborne pollutants, bark was studied for these seven sites.
which allowed identifying adversely impacted areas in Argentina, The longest measurement period was carried out on a lichen located
México and Colombia. Fabian et al. (2011), Salo et al. (2012), and close to a car parking at the University Campus (L0, Fig. 1) where the
Vuković et al. (2015) used in situ and transplanted mosses for mon- only pollution source is vehicular emission of busses and cars. An in-
itoring air pollution in Norway, Finland and Republic of Serbia. dividual thallus of about 70 mm of diameter located at 98 cm above the
Marié et al. (2016) determined that among 20 species of corticolous ground was selected. In addition, other six lichens of the same species
foliose and microfoliose lichens, Parmotrema pilosum was the most exposed to other pollution sources were selected (L1–L6, Fig. 1). Lichen
abundant species living in tree bark and having a good distribution over L1 is located in the vicinity of two metallurgical factories and on an
the urban area of Tandil city (Argentina). The aims of the present work avenue with high vehicular traffic, being one of the main accesses to the
are: a) to study the P. pilosum morphological change and its growth rate city. L4 is pinpointed in front of an important metallurgical factory and

832
D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Lichen samples inside of urban area with influence from different pollution sources. The distance from base (h) and the tree diameter at 150 cm from the tree base (DBH) are detailed, as well as, measurements of lichen
on an avenue. The remaining lichens are influenced by vehicular
emissions as the main source of pollution. Lichen L2 is located behind
Annual
growth

[mm2/

953.2

583.9

258.8
687.5
608.3

218.2
359.2
rate

yr.]
the bus terminal; L3 in a square on an avenue and L5 at downtown. A
control site (L6) located in a green area (park) at high elevation and
with minimal pollution influence was also studied. The lichen locations,
Summer-
Feb–Jun
height above the ground, and the trunk diameter at 150 cm height from
Jan/

21.4

30.4
Fall
the ground are detailed in Table 1. Lichen contours were recorded on

–
–
tracing paper with a grid and scanned in the laboratory.
Nov–Jan
Summer

21.4

2.2. Magnetic measurements

–

–
–
–

–
–
Measurements were done in situ using the susceptibility meter MS3
Oct–Nov
spring

(Bartington Instruments Ltd.) connected to an MS2E sensor, which is

58.7

designed for doing high resolution measurements of magnetic sus-

–

–
–
–

–
–
ceptibility (κ) along surfaces. Measurements were done using the re-
solution range (0.1 × 10−5SI), and κ values were corrected for drift
Aug–Oct
spring

22.3

11.2

through a 3 measurement protocol (two air and one sample readings).

–
–
–

–
–

Accuracy value for this measurement is 2% of the measured value; the

Growth rate [mm2/week]

fall-winter

sensor has a response area of 4 mm × 10 mm, and 50% of the magnetic

Mar–Aug

signal is integrated from 1 mm depth. A measurement grid of 10 mm

14.4

spacing was used for mapping the thallus surface. Measurements were
–

–
–
–

–
–

made over a period of 60 measurement campaigns for L0, and 44

Feb spring-

measurement campaigns for Lichens L1–L6.

Aug–Jan/

summer

A tracing paper with a grid of 10 mm × 10 mm was used for each

26.9

13.2
11.7
5.0

4.2
6.9

lichen, with the center matched to the lichen’s growing center. The li-
–

chen’s contour was recorded and measurement points inside the thallus
winter

surface were marked for centering the susceptibility sensor. This was
2017

5581

3344
Jun.

oriented with the long response axis horizontally. Susceptibility contour

–

–
–

maps were constructed using each weekly dataset of κis (about 50 va-
summer

lues for each lichen) in order to study the concentration and distribu-
2017

2718
2918
2675

3446
2429
Feb.

tion of magnetic PM accumulated on the thallus of each P. pilosum.

–

The magnetic PM density and distribution on the thallus surface was

summer

determined from weekly measurements of κis during 60 measurement

2017

5175
Jan.

campaigns for L0, accounting for a total of ∼3200 measurements. The

–

–
–
–

–
–

other lichens (L1–L6) were measured during a shorter period of about

spring

44 campaigns and involved ∼1000 measurements for each lichen. A

2016

4982
Nov.

total of ∼8300 measurements of κis was carried out during this study.
–

–
–
–

–
–
spring
2016

4806

7697
Oct.

2.3. Scanning electron microscopy

Lichen thallus area [mm2]

–
–
–

–
–
thallus surface between March 2016 and June 2017 and its corresponding growth rate.

In order to characterize the PM morphology and quantify its ele-

Aug.2016

mental composition, two small thallus portions (about 3 mm × 3 mm)

winter

4583

7585

2584
2562
2360

3333
2243

from L0 were cut after 27 weeks, identified as C1 and C2 (Fig. 2), and
stored in the laboratory for additional microscopy studies. Such small
2016

4338

samples that include the deposited particles on its surface were

Mar.

fall

mounted on an Aluminum plate and carbon coated, which was designed

–

–
–
–

–
–

to avoid altering particle morphology. Particles were identified by a

[cm]
DBH

133
139
159

210
75

97

63

Phillips model XL30 scanning electron microscopy (SEM). This micro-

scope also allowed to analyze the elemental composition of each spe-
h [cm]

cimen by X-ray energy dispersive spectroscopy (EDS) with an EDAX

186

193
117
147

182
153
98

model DX4 (detection limit 0.5%).

[UTM m N]

5867486.0

5867186.3

5867480.3
5867248.5
5868405.5

5866606.2
5865210.8
Longitude

3. Results and discussion

3.1. Growth rate of Parmotrema pilosum

315656.0

313048.5

312405.4
311117.6
310312.7

310639.3
310679.6
[UTM m
Latitude

The thallus area of L0 was determined by scanning its surface six

times during 60 measurement campaigns, from March 2016
E]

(4338 mm2) to June 2017 (5581 mm2) (Table 1, Fig. 2). The polygonal
maps were created from each lichen scan and its corresponding thallus
Green area –
Bus terminal
Metallugical

Metallugical
observation

City centre
Parking at
University

area was calculated by using open source software (QGIS software).

Campus

Control
factory

factory
Square

Surface growth rate between measurement periods is expressed as area

Site

increase per week (mm2/week). Growth rates varied between 14.4 and
58.7 mm2/week and was in average 18.3 mm2/week (0.4% of its sur-
Table 1

Lichen

face per week) over the period of 16 months (68 weeks). The lowest
L0

L1

L2
L3
L4

L5
L6

growth rate was recorded during autumn/winter, and the highest

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D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 2. Size measurements of lichen’s thallus surface for L0 (a); L3 (b); L4 (c); and L6 (d). Measurement periods are: March 2016 (forest green), August 2016 (olive
green), October 2016 (pale green), November 2016 (lime green), January 2017 (yellow green) and June 2017 (lawn green). The growing center (white cross) and
extracted thallus portions (3 mm × 3 mm) C1 and C2 for SEM-EDS analysis (orange diamond) are indicated. (For interpretation of the references to colour in this
figure legend, the reader is referred to the web version of this article.)

during winter/spring when this lichen seems to be more active as evi- the area (Marié et al. 2016) indicates that it is a wide-ranging species,
denced by its growth rate (Table 1). Nash et al. (1995) and Bačkor and another common characteristic in pollution-tolerant species.
Loppi (2009), also reported a greater metabolic activity during wet
periods, which favors mineral absorption and growth.
The thallus areas of lichens L1, L2, L3, L4, L5, and L6 were only 3.2. Fe-rich particles on thallus and in situ magnetic assessment
determined twice during measurement campaigns 10 and 27, from
August to October 2016 and to February 2017 (Table 1). The growth Magnetic properties of trapped PM were determined from the
rates for these lichens varied between 4.2 and 13.2 mm2/week, being magnetic susceptibility, which is a concentration dependent parameter
lower than the growth rate of 26.9 mm2/week of L0 for a comparable used as a proxy for atmospheric pollution (Petrovský and Elwood,
period of 22 weeks. 1999). This parameter allows assessing the magnetic concentration of
Growth rates were variable between individuals (percent annual iron rich particles trapped in biomonitors like corticolous foliose and
growth = 6.5–26.8%) and therefore growing conditions seem to be a microfoliose lichens as reported by Chaparro et al. (2013). Magnetic
site-specific characteristic. Because lichens usually live in habitats enhancement on lichen’s thallus is based on two contrasting magnetic
where nutrients are scarce (Johanson et al., 2012), their exposition to minerals: ferrimagnetic (magnetite) and ferromagnetic (iron) materials
atmospheric deposition can show different responses, ranging from (with specific magnetic susceptibility χ = 0.4–1.1 × 10−3 m3 kg−1,
increased growth (McCune and Caldwell 2009) to becoming unhealthy and χ = 2.8 × 10−1 m3 kg−1, respectively), which are much different
or even die (Bando and Sugino, 1995). Sometimes the same lichen from the diamagnetic matrix of the organic thallus
species can show a first phase in which its growth rate is accelerated (χ = −0.9 × 10−8 m3 kg−1; Dearing, 1999). Natural particles may be
followed by a deceleration before dying (Johanson et al., 2012). This differentiated from the anthropogenic ones because they are generally
could explain why P. pilosum reacted in some contaminated sites with a irregular in shape and their composition contains lithic material, with
high growth rate (L3 and L4), while in others the growth rate decreased the exception of those containing iron and titanium oxides, which can
(L1 and L2) as the species were in the final phase of accumulation. In be both of anthropogenic or natural origin.
addition, since there are no native trees in the study area, P. pilosum is SEM observations on the thallus portions with slightly different
an exotic species. This species characteristic and its wide distribution in magnetic susceptibility values (κis = 18.0 × 10−5SI for C1; and
κis = 14.5 × 10−5SI for C2) that were extracted at the 27th campaign,

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D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 3. SEM observations on two small thallus portions from L0 extracted after 27 measurement campaigns; C1 (high values of κis) and C2 (average/low values of κis).
Irregular particles rich in Fe (≤1 μm), spherules (1–2 μm) and aggregates with different shapes and grain sizes are observed. Compositional analysis by EDS indicates
the presence of Fe, Al, Si, K, Ca, Ti and Ba.

revealed the presence of iron rich particles with different morphologies campaigns) show differences in concentration of magnetic PM and re-
and grain sizes (L0; Fig. 3a and b). The elemental analysis by EDS in- vealed the impact of atmospheric pollution on lichens in this order: L1
dicates also the presence of trace elements such as Al, Si, K, Ca, Ti, and (Factory) > L3 (Square) > L2 (Bus terminal) > L4 (Factory) > L5
Ba. Particles are of irregular shape, spherules or form aggregates with (Downtown) > L0 (Campus) > L6 (Green area).
different sizes, and 13 out of 22 are Fe-rich (Fe content = 13–88%wt)
spherules of 1–2 μm in size, that is PM2.5 (Fig. 3c and d). In addition,
irregular shaped particles seem to be common components of trapped 3.3. Spatio-temporal magnetic biomonitoring
PM as well, being smaller PM1.0 (≤1 μm) with Fe content between 35
and 92%wt (Fig. 3e and f). Such particles are thought to come from Sixty magnetic susceptibility contour maps for L0 are represented in
emissions produced by cars and buses circulating at the University Fig. 5 for the whole period of 60 campaigns, showing in general a wide
Campus. Similar Fe-rich particles (irregular shape, spherules and ag- variability of κis reflecting the evolution of magnetic PM concentration
gregates with different sizes) have been observed from vehicle-derived (deposition and partial loss) on this lichen’s thallus. These graphics
emissions, produced by wear particles of the brake system, engine, tires show how Fe-rich PM accumulation changed over time in different
and pavement, and diesel/gas soot as reported by Lu et al. (2005) and areas of the thallus, which seems to be related to the capability of this
Chaparro et al. (2010). species to adsorb and store natural/anthropogenic airborne PM. Pre-
Descriptive statistics of magnetic data (measurements of κis) for ferential accumulation areas could be related with morphological
each lichen are shown in Fig. 4. Overall mean values of κis (i.e.: values characteristics of this lichen, such as topography, micro-scale roughness
calculated for each dataset and recorded over all measurement of the thallus surface, deformation and its retention capacity. The
variation of magnetic susceptibility within this lichen shows magnetic

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D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 4. Descriptive statistics of in situ magnetic sus-

ceptibility (κis) data for each lichen. Each dataset has
a number of data of 3194 (L0); 638 (L1); 956 (L2);
1033 (L3); 738 (L4); 1,202 (L5); and 508 (L6). The
box delineates interquartile range 25–75%, and the
horizontal line in box indicates the median.
Minimum and maximum values are shown using
whiskers, as well as the mean value is shown with an
open square.

enhancement around the growth center (Fig. 5) which was stronger in Mean values of κis present increasing trends during autumn
the upper and right part (39 out of 60 measurement campaigns) and (March–July 2016) and winter (July–September 2016) reaching
less in the lower and left-lower part (9–17 out of 60 measurement maxima during early spring (September 2016, Fig. 6). Afterwards, κis
campaigns). Moreover, magnetic PM was preferentially absorbed in the decreased during spring (September–December 2016) and summer
rougher areas of the thallus surface (Fig. 3a and b). Over time, no re- (December 2016–March 2017), followed by minor increments for au-
petitive patterns were observed, suggesting that PM mobility, accu- tumn and winter (March–July 2017). Similar seasonal trends of PM2.5
mulation, and partial loss occurred within the thallus. concentration (averaged hourly data of concentrations measured using
Using the κis data obtained from the weekly measurements (n ≈ 50), a micro oscillating balance method) were reported in five cities from
an average was calculated for each lichen and defined as the re- China (Wang et al., 2018), reaching the highest concentrations in
presentative value of PM pollution load. Fig. 6 shows the weekly mean winter (126–203 µg m−3), followed by autumn (79–118 µg m−3),
values of κis, temperature, and rainfall during 16 months. In situ mean spring (82–98 µg m−3), and summer (67–82 µg m−3), successively.
magnetic susceptibility shows increments during winter and spring sea- Higher temperatures and consequently, higher mean values of atmo-
sons, reaching high susceptibility values between 16.0 and spheric mixing height (Singh and Pandya, 2013; Myrick et al., 1994;
23.4 × 10−5SI for the spring season. On the other hand, the highest Wark and Warner, 1998) during the summer season allow for a greater
initial values (19.5 × 10−5SI for L1, and 10.2 × 10−5SI for L4) are ob- dispersion of pollutants in these cities. According to Wang et al. (2018),
served for locations affected by industrial and vehicular emissions. L1 stagnant meteorological conditions in Southern North China often oc-
reaches the highest mean value of κis = 43.2 × 10−5SI in September curred in winter and autumn with less precipitation, moderate hu-
2016. In a supposedly clean site, i.e. L6, with an initial mean value of midity, and lower planetary boundary layer heights, which together
2.6 × 10−5SI recorded in August 2016, the highest mean value of suppressed pollution diffusion and facilitated particle production and
7.2 × 10−5SI was obtained during the summer season (January 2017) hygroscopic growth. Although the warm temperature and high hu-
which coincides with an increase of vehicular traffic in this area due to midity during summer promoted the photochemical formation of par-
the holiday period. ticles, the lower emissions and higher precipitation resulted in the
There is a general trend of magnetic susceptibility increase with lowest PM2.5 concentrations. In the present study, such meteorological
reducing mean temperatures and vice versa. On the other hand, rapid factors seem to be responsible for variations of mean values of para-
changes in mean values of κis are often observed after moderate to in- meter κis (Fig. 6a), that is, precipitation periods correspond to relative
tense rainy periods (i.e. measurement campaign 9, 12, 16, 23, 26, 28, lows of κis, and lower mean temperatures (Fig. 6b) correspond to higher
30, 37, 38, 42, 43, 46, 47, 48, 52, 56, 59, and 60, see Fig. 6b), which is mean values of κis, and vice versa.
indicative of two possibly inter-related pollutant dependent processes
taking place in 1) the lichen’s thallus, and 2) the atmosphere. The first
4. Conclusion
one is related to a superficial “washing” of trapped particles on the
thallus and hence the storage capacity of P. pilosum and the second to a
A new methodology of magnetic biomonitoring of the pollution
reduction of dispersed airborne PM by wet deposition or “pollution
tolerant species lichen Parmotrema pilosum, living on urban trees of
cleaning” by rain (Fig. 6). Contaminants previously accumulated on the
Tandil city in Argentina is proposed. In situ measurements of magnetic
thallus may be eliminated by the rainwater, reducing the magnetic PM
susceptibility distribution of the thallus suggests a highly variable
content as was observed during the raining periods, while this increased
particle accumulation over time, comprising up to 16 months. Growth
during dry periods. Matzka and Maher (1999) have shown that rainfall
rates of seven lichen individuals selected from areas with different
reduces the concentration of magnetic particles on tree leaf surfaces.
pollution degree were variables (from 218.2 to 953.2 mm2/yr.) and
Similar results were reported by Aničić et al. (2009) using non-mag-
growing conditions seemed to be site-specific for this exotic lichen.
netic techniques for wet and dry bags mosses, with a linear increment of
Preferential accumulation areas (of the thallus) of magnetic PM
trace element concentration with time. Lichens are most active during
were determined through spatio-temporal distribution of in situ mag-
the wet seasons, which provoke growth and consumption of minerals
netic susceptibility κis measured on the surface of seven lichen in-
(Bačkor and Loppi, 2009; Hofman et al., 2017).
dividuals. Scanning electron microscope observations indicate the

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D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

presence of 1–2 μm Fe-rich spherules and irregular particles of ≤1 μm, Low temperatures reduce the mobility of contaminant particles in the
corresponding to particles of the PM2.5 and PM1.0 categories. atmosphere, which is evidenced by the increase of mean values of κis
Thus, magnetic biomonitoring is a suitable methodology to assess during autumn and winter. The highest mean values of κis were reached
air pollution because it measures trapped magnetic particles on the during late winter and early spring, followed by a decrease of κis values
thallus and it is independent of species’ growth rates. indicative of dispersion and pollution reduction. Precipitation records

Fig. 5. Weekly contour maps of κis for the species P. pilosum from L0, based on 45–54 measurements of κis. Lower values of κis (< 0.3 × 10−5SI) are represented with
light green, higher values of κis (> 18.0 × 10−5SI) with dark red. The growth center is marked (cross). Map #1 corresponds to measurements done in March 2016,
and map #60 to measurements in July 2017. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this
article.)

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D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 5. (continued)

show that rain influenced the magnetic signal measured on thalli, as rapid the collection of measurement data in any chosen time period, from
changes of mean values of κis were observed after moderate to intense days to years. Performing in situ magnetic measurements not only
rainy periods. Such changes are related to a partial washing of trapped contributes to preserve biomonitors such as Parmotrema pilosum, but
particles from the thallus, and a reduction of PM in air by wet deposition. also provides a useful low-cost tool that allows assessing atmospheric
The main advantage of the new methodology used in this work is pollution over short to long periods.

838
D.C. Marié et al. Ecological Indicators 95 (2018) 831–840

Fig. 6. Weekly average measurements for all studied

lichens of (a) mean κis values were normalized using
the corresponding overall mean κis for each lichen,
that is, 8.3 × 10−5SI (L0); 23.9 × 10−5SI (L1);
12.8 × 10−5SI (L2); 16.5 × 10−5SI (L3);
12.8 × 10−5SI (L4); 8.5 × 10−5SI (L5);
4.1 × 10−5SI (L6); and (b) rainfall and temperature
per week in Tandil city.

Conflict of interest 1016/j.ecolind.2015.06.025.

Censo, 2010. http://www.censo2010.indec.gov.ar/ (24/06/15).
Centro de Información Meteorológica (CIM), 2017. Servicio Meteorológico Nacional.
There is no conflict of interest. Datos climatológicos del periodo Febrero 2016 – Julio 2017. Consultas: 02/11/2017
and 01/12/2017. https://www.smn.gob.ar/.
Acknowledgements Chaparro, M.A.E., Marié, D.C., Gogorza, C.S.G., Navas, A., Sinito, A.M., 2010. Magnetic
studies and scanning electron microscopy X-ray energy dispersive spectroscopy
analyses of road sediments, soils, and vehicle-derived emissions. Stud. Geophys.
The authors would like to thanks UNCPBA, CONICET and UNAM for Geod. 54 (4), 633–650. https://doi.org/10.1007/s11200-010-0038-2.
their financial support. This contribution was supported by the Agencia Chaparro, Marcos A.E., Lavornia, Juan M., Chaparro, Mauro A.E., Sinito, Ana M., 2013.
Biomonitors of urban air pollution: magnetic studies and SEM observations of cor-
Nacional de Promoción Científica y Tecnológica (Argentina), grant ticolous foliose and microfoliose lichens and their suitability for magnetic mon-
number: PICT-2013-1274. The authors thank to two anonymous re- itoring. Environ. Pollut. 172, 61–69. https://doi.org/10.1016/j.envpol.2012.08.006.
viewers whose comments improved the manuscript. The authors also Chaparro, M.A.E., Castañeda Miranda, A.G., Gargiulo, J.D., Wannaz, E.D., Böhnel, H.N.,
2014. Estudios magnéticos en colectores naturales (Tillandsia capillaris) de con-
thank to Mr. Pablo Zubeldía (CICPBA) for his help in the field and to Dr.
taminantes en Córdoba, Argentina [Magnetic studies of pollutants in Tillandsia ca-
Marina Vega González (Centro de Geociencias, UNAM) for their help pillaris from Córdoba, Argentina]. Geos 34 (1), 70–71.
performing SEM-EDS studies. Chaparro de Valencia, M., Aguirre Ceballos, J., 2002. Hongos Liquenizados [Lichenized
fungi]. Ed. Elmalpensante, Universidad Nacional de Colombia. Bogotá 220 pp. ISBN:
958-701-241-0.
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