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We evaluated heavy metal deposition in Parmotrema arnoldii and Tillandsia usneoides in response to air pollution in Loja city, Ecuador. We assessed heavy metal (cadmium, copper, manganese, lead and zinc) content in these organisms at nine study sites inside Loja city and three control sites in nearby forests. Concentrations of all studied heavy metals (i.e., cadmium (Cd), copper (Cu), lead (Pb), manganese (Mn) and zinc (Zn)) were highest in downtown Loja. Our study confirms that passive monitoring using lichens and/or bromeliads can be an efficient tool to evaluate heavy metal deposition related to urbanization (e.g., vehicle emissions). We recommend these organisms to be used in cost-effective monitoring of air pollution in tropical countries.
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Lichens and Bromeliads as Bioindicators of Heavy
Metal Deposition in Ecuador
Ángel Benítez 1, 2, *, Jefferson Medina 2, Cristina Vásquez 1, Talía Loaiza 1, Yesenia Luzuriaga 1
and James Calva 3
Sección de Ecología y Sistemática, Departamento de Ciencias Biológicas, Universidad Técnica Particular de
Loja, San Cayetano s/n, Loja 1101608, Ecuador; (C.V.); (T.L.); (Y.L.)
2Maestría en Biología de la Conservación y Ecología Tropical, Universidad Técnica Particular de Loja,
San Cayetano s/n, Loja 1101608, Ecuador;
Departamento de Química y Ciencias Exactas, Universidad Técnica Particular de Loja (UTPL), San Cayetano
s/n, Loja 1101608, Ecuador;
*Correspondence:; Tel.: +593-072-370-1444 (ext. 3034)
Received: 19 December 2018; Accepted: 21 February 2019; Published: 25 February 2019
We evaluated heavy metal deposition in Parmotrema arnoldii and Tillandsia usneoides
in response to air pollution in Loja city, Ecuador. We assessed heavy metal (cadmium, copper,
manganese, lead and zinc) content in these organisms at nine study sites inside Loja city and three
control sites in nearby forests. Concentrations of all studied heavy metals (i.e., cadmium (Cd), copper
(Cu), lead (Pb), manganese (Mn) and zinc (Zn)) were highest in downtown Loja. Our study confirms
that passive monitoring using lichens and/or bromeliads can be an efficient tool to evaluate heavy
metal deposition related to urbanization (e.g., vehicle emissions). We recommend these organisms to
be used in cost-effective monitoring of air pollution in tropical countries.
Keywords: air pollution; epiphytes; passive monitoring; vehicle emissions
1. Introduction
Air pollution is considered one of the biggest environmental problems in many cities around
the world [
], due to increased urbanization, industrial production, rising emissions from traffic and
the lack of urban planning [
]. Automobiles are one of the major factors, as they emit exhaust
and non-exhaust contaminants [
]. Heavy metal deposition is one of the most serious aspects of
air pollution. Due to the high toxicity and persistence in the environment, heavy metals have a
direct and serious impact on human health [
]. In this context, several studies documented that
heavy metals, for example, cadmium (Cd), copper (Cu), lead (Pb) and zinc (Zn) are among the most
toxic air pollutants. Furthermore, in urban zones additional anthropogenic sources of heavy metals
may include industrial activities, fuel combustion and the production of batteries [
]. For these
reasons, implementing accurate and cost-effective air-monitoring strategies is critical to understand
how emissions from different sources affect air quality.
Ecuador is among the many countries that suffer from severe air pollution. Recently, substantial
population growth in Ecuador has generated increased emissions from industry, increased traffic,
and rise in the use of low quality fuels [
]. In Loja city, air pollution is currently considered
one of the main environmental problems [
]. Nevertheless, to date, only the largest Ecuadorian
cities (i.e., Quito, Guayaquil and Cuenca) have established permanent air quality monitoring stations.
This follows a general trend throughout Ecuador, where only few studies have reported any effects of
fine particulate matter or low air quality [1315].
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Contrary to expectations, air pollution monitoring programs using low-cost biological indicators
as an alternative to expensive measuring stations have not been carried out anywhere in the country.
This is surprising, as many organisms are cost-effective and efficient indicators of air quality. Among the
organisms best suited to this task are bromeliads and lichens, as they obtain all their nutrients directly
from the air. Thus, heavy metal content of their biological tissues directly reflects air quality [
Both types of organisms have been widely used in monitoring schemes in several cities around the
globe [
]. Lichens, particularly in the family Parmeliaceae (e.g., Evernia prunastri (L.) Ach. [
Flavoparmelia caperata (L.) Hale [
], and Hypogymnia physodes (L.) Nyl. [
]), and species in the genus
Parmotrema A. Massal. [
]), are effective indicators of heavy metal deposition. Moreover, epiphytic
vascular plants, particularly bromeliads in the genus Tillandsia L., are efficient bioaccumulators of heavy
metal deposition [
]. Heavy metal concentrations in the tissues of both Tillandsia usneoides and
Parmotrema ssp. presented a strong correlation with heavy metal deposition from either automobile
emissions or industrial sources [9,20,3943].
Previously, we have used lichens as indicators of air pollution in Ecuador [
]. However, our study
evaluated lichen species diversity throughout Loja city as a proxy of air pollution and did not measure
heavy metal concentrations [
]. Here, we fill this gap and measure heavy metal concentrations
directly in the biological tissues. We show that our technique represents an efficient and cost-effective
alternative compared to using expensive measuring devices [
]. We hypothesized that increased
urbanization towards the geographic center of the city will result in increased bioaccumulation of
heavy metals in Parmotrema arnoldii (Du Rietz) Hale and Tillandsia usneoides (L.) L.
2. Materials and Methods
2.1. Study Area
Our study area is located in both the urban parts of the city of Loja and the surrounding forests
(Figure 1). The mean annual temperature in this region is 20
C, with annual average rainfalls of
ca. 1900 mm, and throughout the year it is characterized by an average relative humidity of ca. 80%
(Instituto Nacional de Meteorología e Hidrología, INAMI). Altitude above sea level in the area ranges
from 2000 to 2300 m. Three study sites were selected within three zones (South, Center and North) of
the city and a control zone (Forests) outside the city, for a total of twelve sites. The three city zones have
been shown previously to have high levels of fine particulate matter (PM 2.5), for example, 0.025, 0.05,
and 0.038
for South, Centre and North zones, respectively [
]. In addition, these city zones are
localized in critical points of traffic congestion (738–2791 vehicles) where the concentration of PM 2.5
exceeds the norm (0,015 µg/m3) [12]. Additional information on study sites is as follows [12,44,46]:
Forested Zone (F): Our control zone is characterized by fragments of evergreen tropical forest
close to the Podocarpus National Park. The area is generally densely vegetated with a low human
population and very little rural traffic. This zone presumably acts as an air pollution buffer for
the larger area surrounding the city of Loja.
Southern Zone (S): This district is characterized by extensive green areas and recreational parks
(1,053,000 m
), and a low quantity of green area per inhabitant (15.38 m
/inhabitant), but is
nevertheless subject to relatively high traffic due to the transit between this area and the city.
Central Zone (C): The downtown district is a mostly urban area, with a low quantity of green
area per inhabitant (11.58 m
/inhabitant) and very little vegetation (green areas cover only
635,000 m2); and is subject to high volumes of traffic.
(4) Northern Zone (N): With a relatively large quantity of green space (1,060,000 m
), this city district
has a high amount of green space per inhabitant (38.95 m
/inhabitant); it is subject to moderate
traffic only.
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Figure 1. Study area in Loja Province (city of Loja), Southern Ecuador, showing the location of study
sites for different levels of air pollution: Forests (F); South (S); Center (C) and North (N).
Figure 1.
Study area in Loja Province (city of Loja), Southern Ecuador, showing the location of study
sites for different levels of air pollution: Forests (F); South (S); Center (C) and North (N).
2.2. Heavy Metal Measures
Within each locality, we collected five samples on different trees (Salix humboldtiana Willd.
and Alnus acuminata Kunth). Each sample consisted of 0.5–1 g of both Parmotrema arnoldii and
Tillandsia usneoides. To assess content of cadmium (Cd), copper (Cu), manganese (Mn), lead (Pb)
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and zinc (Zn) in these samples, we measured the absorption spectra of five replicas of each sample.
Each sample was weighed and digested with 8 ml HNO
(70%) and 2 ml H
(30%), using a high
performance microware system (Milestone SRL., Sorisole (BG), Italy), following the US EPA 3502
method. After digestion, the volume of each sample was adjusted to 100 ml using double deionised
water. The content of heavy metal in these samples was then analyzed using inductively coupled
plasma optical emission spectroscopy (ICP-OES, Optima 8000; Perkin Elmer). The argon flow rate was
adjusted to 12 L/min and air flow rate to 1.2 L/min. Certificated standards (Merk KGaA, Germany)
were used for the calibration curves.
Tillandsia usneoides and Parmotrema arnoldii were identified using published keys [
Furthermore, we tested for specific secondary compounds of Parmotrema arnoldii using spot tests based
on thallus fluorescence under ultraviolet light, with K (10% water solution of potassium hydroxide) and
Cl (bleach). The specimens were stored in the Herbarium HUTPL of Universidad Técnica Particular
de Loja under AB 232 museum codes.
2.3. Data Analysis
The effect of zone and species on heavy metal accumulation in Parmotrema arnoldii and Tillandsia
usneoides was modelled by linear mixed models (LMMs). For several heavy metals (zinc), log (x+2)
transformations were applied to meet model assumptions. Models were finally checked for residual
normality with the Shapiro–Wilk test (p-value > 0.05). The minimal adequate model was selected
based on Akaike’s Information Criterion (AIC). We used the package ‘nlme’ [
]. Data were analyzed
from a multi-level approach, considering locality as a random factor and introducing the explanatory
variables as fixed factors (Zone and species). In the selected model, we evaluated heavy metals
accumulation between zone, species, and the interaction between the two using F tests. To identify
significant differences in heavy metals accumulation between zones, post-hoc Tukey HSD multiple
comparison tests were implemented in the package ‘lsmeans’. All analyses were performed using R
statistical software version 3.1.13 (R Foundation for Statistical Computing, Vienna, Austria) [50].
3. Results
In Parmotrema arnoldii, Cd levels ranged from 0.6 mg/g (Forests) to 34.7 mg/g (Center). Cu levels
ranged from 10.41 mg/g (Forests) to 31.02 mg/g (North). Mn levels ranged from 12.30 mg/g (Forests)
to 56.81 mg/g (North). Pb levels ranged from 7.14 mg/g (Forests) to 42.95 mg/g (North). Finally,
Zn levels ranged from 16.19 mg/g (Forests) to 100.54 mg/g (Center). On the other hand, in T. usneoides,
Cd levels ranged from 1.1 mg/g (Forests) to 49.2 mg/g (South). Cu levels ranged from 9.08 mg/g
(Forests) to 28.44 mg/g (North). Mn levels ranged from 15.60 mg/g (Forests) to 96.12 mg/g (North).
Pb levels ranged from 12.29 mg/g (Forests) to 49.93 mg/g (North). Finally, Zn levels ranged from
54.65 mg/g (Forests) to 89.54 mg/g (Center).
At all sites within the Control zone (Forests), Parmotrema arnoldii and Tillandsia usneoides exhibited
a low concentration for all heavy metals examined (Cd, Cu, Mn, Pb) in comparison with the South,
Center and North zones (Figure 2a,b; Table A1). However, T. usneoides showed a low concentration
of Zn in the North compared with the Control zone (Figure 2b). The maximum accumulation of Cd
and Zn for the two species was found at the Central zone, followed by the Southern and Northern
(Table A1). In the case of zinc, for both P. arnoldii and T. usneoides the highest concentration was found
in the Center zone (100.54 and 89.54 mg/g, respectively), followed by South (91.37 and 70.97 mg/g,
respectively) and North (44.46 and 30.11 mg/g, respectively). The level of lead (Pb) was also highest
in urban areas for P. arnoldii and T. usneoides, with the highest levels in the North Zone (42.95 and
49.93 mg/g respectively), followed by South (39.48 and 35.53 mg/g, respectively) and Center (25.29 and
27.74 mg/g, respectively). The highest concentrations of Cu for the two species were recorded in the
urban zones (South, Center and North), while the lowest concentration was found at the control site
(Forests) (Figure 2a,b; Table A1).
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the two species were recorded in the urban zones (South, Center and North), while the lowest
concentration was found at the control site (Forests) (Figure 2a,b; Table A).
Figure 2. Boxplots depicting heavy metal (Cd, Pb, Mn, Cu and Zn) concentrations in (a) Parmotrema
arnoldii, and (b) Tillandsia usneoides in Loja. Colours correspond to zones: Yellow = South, orange =
North, red = Center, green = Forest.
Results of LMM showed that the concentrations of heavy metals Cd, Cu, Mn, Pb, Zn in
Parmotrema arnoldii and Tillandsia usneoides were significantly different in the four zones. The
concentration of these metals in both Parmotrema arnoldii and Tillandsia usneoides significantly
decreased in control zones where air pollution and, thus, heavy metal deposition was lower (Figure
2a,b; Table 1).
Table 1. Linear mixed model (LMM) and a post-hoc Tukey test of heavy metal accumulation in
Parmotrema arnoldii and Tillandsia usneoides according to the different study sites. F-value = statistical;
p < 0.05 is considered significant.
LMM Cd Pb Mn Cu Zinc
Factor F p-value F p-value F
-value F
-value F
Zone 51.84 <0.001 26.37 <0.001 33.48 <0.001 28.12 <0.001 53.35 <0.001
Specie 3.80 0.054 0.005 0.944 22.17 <0.001 0.03 0.863 0.051 0.822
Zone x Specie 6.27 <0.001 1.061 0.37 2.32 0.08 2.457 0.067 15.67 <0.001
Tukey's HSD Test Cd Pb Mn Cu Zinc
Zone Est
-value Est
-value Est
-value Est
-value Est
F - S -38.79 <0.001 -0.865 <0.001 16.58 0.419 -14.68 <0.001 -0.73 <0.001
F - C 30.54 <0.001 -0.583 <0.001 -61.38 0.001 -14.14 <0.001 -0.92 <0.001
F - N -26.99 <0.001 -0.891 <0.001 -47.00 0.004 -19.98 <0.001 -0.08 0.823
S - C -8.25 0.185 0.282 0.039 -30.41 0.042 0.53 0.993 -0.19 0.132
S - N -11.79 0.043 -0.026 0.994 14.38 0.457 -5.30 0.045 0.652 <0.001
C - N 3.54 0.798 -0.309 0.028 -44.79 0.006 -5.84 0.033 0.841 <0.001
The interaction between zone and species was only significant for Cd and Zn, and species
showed an effect on concentration of Cd and Mn (Table 1). The Tukey HSD test showed significant
differences according to zone between the heavy metal accumulation of forests (control zone) and the
three urbanized zones (South, Center and North; Table 1).
4. Discussion
Our results demonstrate that heavy metal concentrations in Parmotrema arnoldii (a lichen) and
Tillandsia usneoides (a bromeliad) closely reflected heavy metal deposition in Loja city. We
hypothesized that heavy metal accumulation in P. arnoldii and T. usneoides may be responding to
Figure 2.
Boxplots depicting heavy metal (Cd, Pb, Mn, Cu and Zn) concentrations in (
arnoldii, and (
)Tillandsia usneoides in Loja. Colours correspond to zones: Yellow = South, orange =
North, red = Center, green = Forest.
Results of LMM showed that the concentrations of heavy metals Cd, Cu, Mn, Pb, Zn in Parmotrema
arnoldii and Tillandsia usneoides were significantly different in the four zones. The concentration of
these metals in both Parmotrema arnoldii and Tillandsia usneoides significantly decreased in control zones
where air pollution and, thus, heavy metal deposition was lower (Figure 2a,b; Table 1).
Table 1.
Linear mixed model (LMM) and a post-hoc Tukey test of heavy metal accumulation in
Parmotrema arnoldii and Tillandsia usneoides according to the different study sites. F-value = statistical;
p< 0.05 is considered significant.
LMM Cd Pb Mn Cu Zinc
Factor F p-Value F p-Value F p-Value F p-Value F p-Value
Zone 51.84 <0.001 26.37 <0.001 33.48 <0.001 28.12 <0.001 53.35 <0.001
Specie 3.80 0.054 0.005 0.944 22.17 <0.001 0.03 0.863 0.051 0.822
Zone x Specie 6.27 <0.001 1.061 0.37 2.32 0.08 2.457 0.067 15.67 <0.001
Tukey’s HSD Test Cd Pb Mn Cu Zinc
Zone Est p-Value Est p-Value Est p-Value Est p-Value Est p-Value
F-S 38.79 <0.001 0.865 <0.001 16.58 0.419 14.68 <0.001 0.73 <0.001
F - C 30.54 <0.001 0.583 <0.001 61.38 0.001 14.14 <0.001 0.92 <0.001
F-N 26.99 <0.001 0.891 <0.001 47.00 0.004 19.98 <0.001 0.08 0.823
S-C 8.25 0.185 0.282 0.039 30.41 0.042 0.53 0.993 0.19 0.132
S-N 11.79 0.043 0.026 0.994 14.38 0.457 5.30 0.045 0.652 <0.001
C - N 3.54 0.798 0.309 0.028 44.79 0.006 5.84 0.033 0.841 <0.001
The interaction between zone and species was only significant for Cd and Zn, and species showed
an effect on concentration of Cd and Mn (Table 1). The Tukey HSD test showed significant differences
according to zone between the heavy metal accumulation of forests (control zone) and the three
urbanized zones (South, Center and North; Table 1).
4. Discussion
Our results demonstrate that heavy metal concentrations in Parmotrema arnoldii (a lichen) and
Tillandsia usneoides (a bromeliad) closely reflected heavy metal deposition in Loja city. We hypothesized
that heavy metal accumulation in P. arnoldii and T. usneoides may be responding to automobile traffic
contamination. Previous research has found a high correlation between heavy metals in air and
automobile traffic in the urban parts of Loja [
]. A similar pattern has been found in many other
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areas of the world, that is, that air pollution caused by heavy metal deposition generally tends to be
higher in urban zones with more traffic, than in rural areas with less traffic [1,16,26,33,51]
The accumulation of Cd, Cu, Pb and Mn in Parmotrema arnoldii and Tillandsia usneoides tissues
showed a similar pattern, with more heavy metals in urban areas than in nearby forest controls.
The strong enrichment of heavy metals at the urban sites of Loja is not unexpected, particularly
enrichment of lead from particle deposition as a result of an increased volume of traffic [
Our findings are consistent with Monna et al. [
], who found high enrichment of Cd, Cu, Mn and
Pb in urban areas for Parmotrema crinitum and Tillandsia usneoides. Following a similar pattern,
Figueiredo et al. [20]
also reported high concentrations of heavy metal in urban zones for Tillandsia
usneoides. In addition, Sánchez-Chardi [
] demonstrated that five different species of Tillandsia
accumulated Pb and Cd according to traffic intensity in Asunción, Paraguay, reporting particularly
high levels for Pb from all five species obtained from the most polluted areas. Several studies showed
that these pollutants (e.g., cadmium, copper, lead and manganese), are related not only directly with
exhausts emissions from road traffic caused by fuel and lubricant combustion, but also indirectly
from catalytic converters, particulate filters, resuspension, lubricating oils, engine corrosion and wear
and tear of tyres [
]. Other potential sources of heavy metals can generally be related to metal
extraction, industrial uses, waste incineration and oil combustion [
]. However, Loja does not have
big industries, which could otherwise contribute to higher levels of background pollution. This might
be different for much larger cities of Ecuador, such as Guayaquil, Quito or even Cuenca, where heavy
metal emissions from traffic may not be the only pollution source.
Our results agree well with previous studies that used other species of Parmotrema (e.g., Parmotrema
chinense,Parmotrema crinitum, Parmotrema reticulatum and Parmotrema tinctorum), and with several
studies that used bromeliads like Tillandsia usneoides to indirectly measure heavy metal deposition.
All these studies showed similar patterns, where urban zones have high concentrations of Cd, Cu,
Pb and Mn [
]. However, the concentrations of these heavy metals in our control site
(Forest) were relatively low [
]. This would suggest that the overall background contamination
by heavy metals in Ecuador might generally be quite low; thus, the air in rural areas goes largely
unaffected and an increased concentration is present only in the city itself [46].
We found that heavy metal deposition in Parmotrema arnoldii and Tillandsia usneoides varied
within the city, as compared to control sites (Forest). Relatively high values of zinc (Zn) were
detected in specimens of Parmotrema arnoldii in somewhat more urbanized zones (Center and South).
This is possibly a result of collecting the specimens along bus lines. Similarly, Giordano et al. [
Aprile et al. [33]
, and Rhzaoui et al. [
] also found zinc deposition in lichens typically related to
increases of traffic along traffic routes serving inner city urban areas. In addition, several studies found
higher concentrations of zinc in specimens of genus Parmotrema at urban zones with high levels of
vehicular traffic [
]. Air pollution from Zn can typically be ascribed to tyre wear, and this
metal is also a common component of antioxidants used as dispersants to improve lubricating oils [
Thus, the main sources of Zn are indirect emissions oftraffic, not only directly from the exhaust, but also
from industrial sources [
]. A comparatively low accumulation of Zn was found in specimens of
Tillandsia usneoides, particularly in the North and Forest control site, especially in comparison with the
other, more urban sites. This was probably due to a buffering effect present in the North, where some
of the collection sites are characterized by stands of mixed forests. Ochoa-Jimenez et al. [
] also found
less air pollution in similar areas characterized by small mixed forest fragments within urban areas
but away from the city center. The sites that they studied resemble some of our sample sites in the
Northern zone.
In conclusion, lichens and bromeliads closely correspond with heavy metal deposition likely
related to increased traffic emissions in the urban parts of Loja. Our study demonstrates that
Parmotrema arnoldii and Tillandsia usneoides are both suitable and cost-effective indicators of heavy
metal deposition in Loja. Thus, we recommend using these lichens and bromeliads to monitor
air pollution. We acknowledge that heavy metal measurements from specimens only represent an
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indirect approximation to the accumulation of heavy metals on a daily basis. Lichens and bromeliads
cannot necessarily replace more sophisticated technologies to measure heavy metal deposition directly.
Nevertheless, in a relatively small city like Loja, which lacks expensive equipment to measure air
pollutants directly, assessing overall contamination using bromeliads and lichens as bioindicators
may be an attractive and cheap alternative. In our opinion, it is imperative to establish a more robust,
long-term monitoring scheme using both lichens and bromeliads as bioindicators.
Author Contributions:
Conceptualization, Á.B. and J.C.; methodology, A.B., J.M., C.V., T.L., Y.L. and J.C.; formal
analysis, A.B. and J.C.; investigation, A.B.; resources, A.B. and J.C.; data curation, A.B.; writing—original draft
preparation, A.B.; writing—review and editing, A.B. and J.C.; project administration, A.B.; funding acquisition,
A.B. and J.C.
This research was funded by the “Universidad Técnica Particular de Loja” (PROJECT_CCNN_941) and
the “Secretaría Nacional de Educación Superior, Ciencia, Tecnología e Innovación” of Ecuador.
We thank the Ministerio del Ambiente del Ecuador for granting access to the field sites and
the necessary collection permits. We also thank Frank Bungartz and David A. Donoso for the English review,
and for comments and suggestions to improve the manuscript. We thank the editor and two anonymous reviewers
for their constructive comments, which helped us to improve the manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
Appendix A
Table A1.
Mean concentration and standard error of Cd, Cu, Mn, Pb and Zn in Parmotrema arnoldii (PA)
and Tillandsia usneoides (TU) from the Loja city (mg/g).
Species Heavy Metal Forest South Center North
Parmotrema arnoldii
Cd 0.60 ±0.81 30.83 ±19.12 34.66 ±9.22 27.99 ±9.06
Cu 10.41 ±7.37 21.27 ±3.93 25.41 ±4.44 31.02 ±4.13
Mn 12.30 ±3.43 53.49 ±18.97 20.03 ±8.42 56.81 ±25.59
Pb 7.14 ±3.05 39.48 ±14.66 25.29 ±9.46 42.95 ±18.03
Zn 16.19 ±3.69 91.37 ±35.78 100.54 ±23.92 44.46 ±26.49
Tillandsia usneoides
Cd 1.10 ±1.27 49.16 ±6.93 28.93 ±12.16 28.11 ±8.17
Cu 9.08 ±5.98 27.57 ±11.55 22.36 ±9.69 28.44 ±5.97
Mn 15.60 ±2.52 71.43 ±34.94 43.27 ±22.31 96.12 ±29.60
Pb 12.29 ±3.68 35.53 ±10.75 27.74 ±14.53 49.93 ±10.81
Zn 54.65 ±13.00 70.97 ±33.70 89.54 ±24.09 30.11 ±8.49
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... Some of the most used are based on passive monitoring and focused on using native species of the different areas; for instance, several studies have focused on lichens [23,28,37,38], bryophytes [25,32,39,40] and vascular plants for determining air quality [30,[41][42][43][44]. Aquatic bryophytes are also used to assess water quality [13,21,[45][46][47]. However, few studies have incorporated different taxonomic groups for air and water quality monitoring; for instance, previous studies used a combination of lichens and bryophytes [25,28,48,49], lichens with vascular plants [50,51] and bryophytes with vascular plants for monitoring air pollution [40,42,52,53]. In terms of water pollution, studies of macroinvertebrates and bryophytes can be found [21,54,55]. ...
... As a precedent, most studies have focused on using a single species for air quality monitoring [34,57] and water pollution [24,47]. Only one study has used lichens and bromeliads to determine air quality [50]; however, this study did not determine the accumulation effectiveness of the species. ...
... The average annual temperature in the region is 20 • C, and it is characterized by an average relative humidity of about 80% [1]. For further information, see previous studies by Benítez et al. [50] related to air quality, and by Vásquez et al. [47] and Benítez et al. [24] focused on water quality in the city of Loja, Ecuador. ...
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Air and water pollution are global environmental problems; thus, bioindicators have become important tools for monitoring various pollutants, including metals and metalloids. Parmotrema arnoldii (Du Rietz) Hale and Tillandsia usneoides L. were evaluated as indicators of heavy metals in the air and Platyhypnidium aquaticum A. Jaeger and Marchantia polymorpha L. as indicators of heavy metals and a metalloid in water. The concentrations of cadmium (Cd), lead (Pb), copper (Cu), manganese (Mn) and zinc (Zn) as air pollutants and aluminum (Al), cadmium (Cd), iron (Fe), manganese (Mn), lead (Pb), zinc (Zn) and arsenic (As) as water pollutants were analyzed within four different zones (control, northern, central and southern) in an Andean city of Ecuador. The level of metal concentrations in the air for P. arnoldii and T. usneoides had the following order of concentration: Zn > Mn > Pb > Cd > Cu. In the case of water, P. aquaticum pointed out a concentration of Al > Mn > Fe > Zn > As > Pb > Cd and proved to be more effective in detecting water pollution than the species M. polymorpha, which had a concentration of Al >Zn > Fe > Cd >As > Mn > Pb. P. aquaticum showed a higher capacity to accumulate heavy metals than M. polymorpha; therefore, it can be used as a model species for passive water quality monitoring. However, P. arnoldii and T. usneoides showed similar heavy metal accumulation related to air quality. The passive monitoring of air quality using bromeliads and lichens as well as bryophytes for water quality proved their effectiveness and applicability in tropical regions such as Ecuador.
... In Ecuador, only one active biomonitoring study has been conducted using mosses as indicators of air pollution in the city of Quito [35], where the authors found the presence of lead and cadmium related to vehicular traffic, but the identification of the species used was not realized. On the other hand, air quality monitoring studies have been carried out in the city of Loja using lichens and bromeliads [36,37]. These studies have shown that urban areas have lower species diversity and a higher accumulation of metals compared to control zones. ...
... However, this is the first study to analyze air quality by transplanting bryophytes, which allows the use of low-cost air pollution monitoring systems [15,38]. The present study aims to determine the air quality of the city of Loja by transplanting three species of mosses (Rhacocarpus purpurascens, Sphagnum sp. and Thuidium delicatulum) due to the fact that urban areas of the city of Loja, Ecuador have high levels of air pollution (e.g., metals) related to vehicular traffic [36,37]. We hypothesized that increased urbanization and vehicular traffic towards the center of the city will result in increased bioaccumulation of heavy metals in transplanted mosses. ...
... For monitoring purposes, the city of Loja was divided into three zones (North, Central and South), with three locations in the North and South zones and four locations in the Central zone ( Figure 1). The design has been structured based on previous environmental monitoring studies [37,39,40]. The study was conducted between March and May 2019. ...
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Air pollution is one of the main global environmental problems, where bryophytes, due to their high capacity to retain metals and other pollutants, have been widely used in active air quality monitoring studies in temperate and tropical zones. Thus, in this study, we analyzed for the first time the concentrations of eight metals (cadmium, copper, nickel, aluminum, iron, manganese, lead and zinc) in three species of transplanted mosses (Rhacocarpus purpurascens (Brid.) Paris, Sphagnum sp. and Thuidium delicatulum (Hedw.) Schimp.) from Ecuador. Significant differences were found for the three species in the concentrations of Al, Mn, Fe and Zn between urban and control areas, pointing to the Central zone as the main source of contamination with the highest concentrations of Al, Fe, Mn and Zn, related to vehicular traffic. Lead did not differ between zones for Rhacocarpus purpurascens and Sphagnum sp.; however, Thuidium delicatulum accumulated different concentrations between urban areas and the control areas. The three species of mosses provided valuable information on the contamination of Al, Fe, Mn, Pb and Zn in the urban area of the city of Loja, and therefore can be used in future air quality monitoring programs over time in tropical cities.
... Previous studies found that higher IAP values had shown better air quality [28][29][30][31][32]. Conversely, low IAP values are related with reduction of the most sensitive species, indicating higher degrees of air pollution [14,16,32]. Thus, studies in tropical areas have documented that urban areas have high levels of air pollutant related with vehicular traffic and industrial activities than areas far from the city [11,14,16,30,[33][34][35][36][37]. ...
... Studies in Ecuador using bioindicators to detect air pollution are scarce [3,32,37]. Thus, for the first time, epiphytic cryptogams (lichens and bryophytes) were used as biomonitors to assess the air pollution in the city of Ambato. Specifically, we addressed the following questions: (1) Are the richness, IAP and composition of cryptogams (lichens and bryophytes) influenced by land use changes? ...
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Air pollution is one of the main environmental problems in developed and developing countries. Epiphytic cryptogams (bryophytes and lichens) are proposed as a reliable indicator to detect environmental changes, given to their sensitivity to pollutants. In this study we evaluated air quality in the city of Ambato using bryophytes and epiphytic lichens on three land uses (urban, peri-urban and control). In each zone we selected ten trees (a total of 90 trees) for each station (a total of nine stations), where we recorded the frequency and cover of epiphytic cryptogams in a quadrat of 10 × 50 cm that was divided into 5 × 5 cm squares. Differences in richness, index of atmospheric purity (IAP) and diversity were analyzed using a generalized linear model (GLM) and changes in species composition using multivariate analysis. We recorded 39 species of cryptogams (25 lichens and 14 bryophytes). Richness, diversity and index of atmospheric purity were higher in the control zone compared to the urbanized zones. Community composition changed between the different zones, with increasing differences between the control and urban zones. The urban areas of the city of Ambato were identified with high levels of air pollution due to their lower diversity related to higher vehicular traffic and industrial activities (e.g., footwear and textile factories, tanneries). Thus, epiphytic cryptogams are a fast and low-cost method for air quality assessment in tropical areas.
... Wolterbeek [84], Augusto et al. [85], Van der Wat and Forbes [86], Bargagli [87] Year Carrillo et al. [104] With regard to biomonitor species, epiphytic foliose and/or fruticose lichens are usually sampled. Among the foliose species, the most widely adopted in forest monitoring belong to the family Parmeliaceae, such as Flavoparmelia caperata, Parmotrema arnoldii, and Hypogymnia physodes (e.g., [77,88,89,98,99,101,103,104]), while Letharia vulpina, Pseudevernia furfuracea, and Usnea are the most widely used fruticose species (e.g., [69,91,92,94,96,100]). ...
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Currently, forest ecosystems are often located in remote areas, far from direct sources of air pollution. Nonetheless, they may be affected by different types of atmospheric deposition, which can compromise their health and inner balance. Epiphytic lichens respond to air pollution and climate change, and they have been widely adopted as ecological indicators, mainly in urban and industrial areas, while forest ecosystems are still underrepresented. However, in recent years, their use has become increasingly widespread, especially in the context of long-term monitoring programs for air pollution in forests. In this review, we provide a critical analysis of the topic from the point of view of the different methodological approaches based on lichen responses adopted in forest ecosystems. Further, we discuss the main challenges posed by the current global change scenario.
... The current urbanisation gradient has restricted native forests to the high elevations, agriculture to the mid-elevations, and dense urban settlement to the lower elevations (Iñiguez-Armijos et al., 2016). In addition, population growth has exerted several environmental pressures, affecting streams and rivers with sewage, agricultural and urban runoff, and metal pollution (Benítez et al., 2019;Zúñiga-Sarango et al., 2020), as well as changing the perception of people about water quality along the urbanisation gradient (Hormel et al., 2021). ...
However, knowledge about multiple-stressors effects on urbanised Andean streams is lacking. In southern Ecuador, we assessed how multiple stressors determine the structural (aquatic invertebrate metrics) and functional (organic matter breakdown and delta N of primary consumers) attributes of streams in a densely populated watershed without wastewater treatment and with contrasting land uses. We found that urbanised streams exhibited individual-stressor effects and that stressor interactions were rare. While structural and function attributes responded negatively to urbanisation, ecosystem functioning metrics were influenced most. Stream ecosystem functions were influenced by water-chemistry stressors, whereas aquatic invertebrate metrics were influenced by physical-habitat stressors. We suggest that managers of urbanised streams in the Andes immediately focus on the most important stressors by reducing inputs of inorganic N and P, re-establishing stream flow and substrate heterogeneity, and restoring riparian vegetation instead of attempting to elucidate intricate interactions among stressors. Our result also demonstrate that stream biomonitoring programs would benefit from a combination of structural and functional indicators to assess anthropogenic effects in a multiple-stressors scenario.
... These metals are usually found in relatively high or medium concentrations in phosphate or micronutrient fertilizers (Guilherme and Marchi 2007). Parmotrema species are highly sensitive to these metals (Benítez et al. 2019;Zulaini et al. 2019;Port et al. 2018;Boamponsem and Freitas 2017). In the present study, chemical pollutants were dispersed from agricultural matrices, confirming our hypothesis that P. tinctorum may serve as a bioindicator for monitoring pollutant dispersal. ...
Full-text available
Pollutants inhibit thallus growth and development or alter the metabolism and associated anatomical and morphophysiological characteristics of lichens. Since agricultural matrices can act as sources of pollution by dispersing agrochemicals to vegetation fragments, this study tested the hypothesis that Parmotrema tinctorum can serve as the indicator of edge effect in such fragments. In other words, we assumed the impact of pollutant accumulation to be greater at the vegetation edges and explored the utility of this lichen as a bioindicator of pollutants dispersed from agricultural matrices. Differences in the anatomical layers of P. tinctorum thalli sampled from the edge and center of four vegetation fragments (CER, SSF, SSC, and ENP) were evaluated, and the effects of agricultural matrices on macro- and micronutrient levels, heavy metal levels, and photosynthetic pigment content were analyzed. Anatomical layers were thicker in P. tinctorum thalli from the edges of SSC and ENP, indicating the need for photobiont protection at these sites. Edge effect was observed on Al accumulation in the thallus, indicating dispersion of this metal from agricultural matrices and its greater impact in the edge populations. Edge effect was also evident on photosynthetic pigment content, macro- and micronutrient levels, and heavy metal concentration in the thallus, and the values reflected high ecological imbalance currently verified at the edge of ENP, an area of permanent protection. In areas within ENP, chlorophyll a/b ratio reflected stress factors acting on the thallus, indicating that even legally protected areas are not free from the impact of atmospheric pollutants. P. tinctorum may serve as an effective indicator of edge effects and may be used for biomonitoring pollutant dispersion from agricultural matrices. Graphical abstract
... Based on previous studies in the urban area of Malaysia, there was a high correlation between heavy metals' accumulation in lichen and automobile traffic (Abas and Awang 2017;Abas et al. 2018a). A similar pattern has been found in many other areas of the world, that is, that air pollution caused by heavy metal deposition generally tends to be higher in urban zones with more traffic, than in rural areas with less traffic (Benitez et al. 2019). All those heavy metals usually come from anthropogenic activities such as industrial activity and motor vehicles emission. ...
Full-text available
Background Indoor air quality (IAQ) is a concern in kindergartens as children spend much of their time there. Yet, there is a shortage of biological indicators needed for assessing IAQ. Thus, this study evaluated IAQ using transplanted lichen Usnea misaminensis as a biological indicator. Methods Lichen samples, collected from Bukit Larut, Perak, Malaysia, were exposed to indoor and outdoor environments in an urban area (Ummi Aiman Kindergarten) and a rural area (Ummi Qaseh Pelangi Kindergarten) for 2 months during August 15 to October 14, 2019. The concentrations of 12 selected elements and the vitality of the lichens were then evaluated. Results Increased concentrations of eleven of the twelve elements deposited in the lichen samples in both urban and rural areas were observed. For both areas, the element concentrations in the samples from the indoor environment was lower than those from the outdoor environment, and those in the rural area were lower than those from in the urban area, suggesting the impacts of traffic emissions. The vitality of the lichens showed no significant change in indoor environment, compared to that in outdoor environment, indicating that even exposed to indoor environment, the lichens remained effective biological indicators as same as they were in the outdoor environment. Conclusions Lichens are effective biological indicators for both outdoor and indoor environments. Furthermore, outdoor emissions could influence IAQ, which could be problematic in densely populated areas such as kindergartens. Mitigation measures should be taken.
... Monitoring Manual carries all the necessary information for the utility of mosses for biomonitoring (Benitez et al., 2019). ...
Environmental contamination by heavy metals is an extremely important issue, which can affect water, air, and soil, creating a variable and irreversible cycle of toxicity. The increasing use of chemical products, including heavy metals, by many industries, including agriculture, results in a corresponding increase in the risk of contamination. Soil contamination is a widespread and important pathway for pollution, with microorganisms, plants, and their functions and interactions being greatly affected. In this chapter we describe the backgrounds to toxic compounds and heavy metals, and their interactions with their surroundings including the sources and origins of different types of contamination and the principal consequences on the different functions of soil and microorganisms, and also the impact on human health.
The biomarker response of Spanish moss was investigated along the Savannah River basin including inland villages, low traffic, and high traffic areas using instrumental neutron activation analysis. When comparing the high-traffic areas of Savannah to the low-traffic areas, a considerable increase in heavy metal concentration, of the order of 6–8-fold, was noticed. However, low- traffic regions of urban cities showed a little enhancement in heavy metal concentration as compared to rural areas. The most significant heavy metal pollutants in the air caused by vehicle traffic were identified (Cr, Zn, Ba, Sb, and Cd) using principal component analysis.
Lichen is a composite organism lives in symbiotic relationship between algae and cyanobacteria. Lichens are plant-like, can be found living on plant, rocks and buildings. On plants, lichens can be found on barks, leaves and roots. This study aimed to create a checklist of lichen species found on trees at Bidong Island, Terengganu and to determine the relationship between lichens species with its host tree species. Observation of lichens’ characteristics was done using stereomicroscope and identification of lichens was done based on their morphological characters by referring to the key lichen genera. All the data obtained were sorted in family composition in order to build a checklist. Results showed that 76 lichens species was found but only 55 were positively identified based on their morphological features. A total of 55 lichens specimen were collected from eight host plants were classified into 21 families.KeywordsBioindicatorTree hostMicrolichensSouth China seaMalaysia
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In this study, we investigated the bioaccumulation, tissue distribution and physiological responses to different metal concentration (0.2 and 2 mM) and time of exposure of 1, 2 and 3 weeks with cadmium (Cd), copper (Cu), lead (Pb) and zinc (Zn) using the model liverwort Marchantia polymorpha. Our data showed, on one hand, a significant enrichment and tissue translocation of Cu, Zn, and specially Cd, reaching concentrations of 1800 µg g− 1 in 3 weeks. On the other hand, Pb exhibited the lowest concentration values (50 µg g− 1), and 90% of the total concentration in the rhizoids. We could observe a positive correlation between tissue concentration, metal translocation and an enhanced toxic response. The results obtained in this study might contribute not only in the application of this species in environmental studies with heavy metals but also as a starting point to study the evolution of metal tolerance in land plants.
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Samples of one lichen species, Parmotrema crinitum, and one bromeliad species, Tillandsia usneoides, were collected in the state of Rio de Janeiro, Brazil, at four sites differently affected by anthropogenic pollution. The concentrations of aluminum, cadmium, copper, iron, lanthanum, lead, sulfur, titanium, zinc, and zirconiumwere determined by inductively coupled plasma– atomic emission spectroscopy. The environmental diagnosis was established by examining compositional changes via perturbation vectors, an underused family of methods designed to circumvent the problem of closure in any compositional dataset. The perturbation vectors between the reference site and the other three sites were similar for both species, although body concentration levels were different. At each site, perturbation vectors between lichens and bromeliads were approximately the same, whatever the local pollution level. It should thus be possible to combine these organisms, though physiologically different, for air quality surveys, after making all results comparable with appropriate correction. The use of perturbation vectors seems particularly suitable for assessing pollution level by biomonitoring, and for many frequently met situations in environmental geochemistry, where elemental ratios are more relevant than absolute concentrations.
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Elemental characterization of fine particulate matter was undertaken at schools and residences in three low income neighborhoods in Quito, Ecuador. The three zones were located in the northern (Cotocollao), south central (El Camal), and south east (Los Chillos) neighborhoods and were classified as zones 1–3, respectively. Forty elements were quantified via ICP-MS analysis. Amongst the geogenic elements, the concentration of Si was the most abundant followed by S, Al, and Ca. Elements with predominantly anthropogenic sources such as Zn, V, and Ni were higher in zone 3 school followed by zone 2 and zone 1 schools. Enrichment factors were calculated to study the role of crustal sources in the elemental concentrations. Geogenic elements, except K, all had values <10 and anthropogenic elements such as Ni, V, Zn, Pb, As, Cr had >10. Principal Component Analysis suggested that Ni and V concentrations were strongly attributable to pet coke and heavy oil combustion. Strong associations between As and Pb could be attributed to traffic and other industrial emissions. Resuspended dust, soil erosion, vehicular emissions (tailpipe, brake and tire wear, and engine abrasion), pet coke, heavy oil combustion, and heavy industrial operations were major contributors to air pollution.
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Due to considerable progress in exhaust control emission technology and extensive regulatory work regarding this issue, non-exhaust sources of air pollution have become a growing concern. This research involved studying three types of road environment samples such as road dust, sludge from storm drains and roadside soil collected from heavily congested and polluted cities in Poland (Krakow, Warszawa, Opole and Wroclaw). Particles below 20 µm were examined since it was previously estimated that this fine fraction of road dust is polluted mostly by metals derived from non-exhaust sources of pollution such as brake linings wear. Chemical analysis of all samples was combined with a fractionation study using BCR protocol. It was concluded that the finest fractions of road environment samples were significantly contaminated with all of the investigated metals, in particular with Zn, Cu, both well-known key tracers of brake and tire wear. In Warszawa, the pollution index for Zn was on average 15-18 times the background value, in Krakow 12 times, in Wroclaw 8-12 times and in Opole 6-9 times the background value. The pollution index for Cu was on average 6-14 times the background in Warszawa, 7-8 times in Krakow, 4-6 times in Wroclaw and in Opole 5 times the background value. Fractionation study revealed that mobility of examined metals decreases in that order: Zn (43-62%) > Cd (25-42%) > Ni (6-16%) > Cu (3-14%) > Pb (1-8%). It should, however, be noted that metals even when not mobile in the environment can become a serious health concern when ingested or inhaled.
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Automobile traffic, industrial processes and natural phenomena cause notable air pollution, including gaseous and particulate contaminants, in urban centers. Exposure to particulate matter (PM) air pollution affects human health, and has been linked to respiratory, cardiovascular and neurological diseases. The mechanisms underlying inflammation in these diverse diseases, and to what extent health effects are different for PM obtained from different sources or locations, are still unclear. This study investigated the in vitro toxicity of ambient course (PM10) and fine (PM2.5) particulate matter collected at seven sites in the urban and periurban zones of Quito, Ecuador. Material from all sites was capable of activating TLR2 and TLR4 signaling pathways, with differences in the activation related to particle size. Additionally, airborne particulate matter from Quito is an effective activator of the NLRP3 inflammasome.
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In this study, Evernia prunastri, a lichen growing in its natural habitat in Morocco was analysed for the concentration of five heavy metals (Fe, Pb, Zn, Cu and Cr) from eleven sites between Kenitra and Mohammedia cities. The control site was Dar Essalam, an isolated area with low traffic density and dense vegetation. In the investigated areas, the concentration of heavy metals was correlated with vehicular traffic, industrial activity and urbanization. The total metal concentration was highest in Sidi Yahya, followed by Mohammedia and Bouznika. The coefficient of variation was higher for Pb and lower for Cu, Zn and Fe. The concentrations of most heavy metals in the thalli differed significantly between sites (p<0.01). Principal component analysis (PCA) revealed a significant correlation between heavy metal accumulation and atmospheric purity index. This study demonstrated also that the factors most strongly affecting the lichen flora were traffic density, the petroleum industry and paper factories in these areas. Overall, these results suggest that the index of atmospheric purity and assessment of heavy metals in lichen thalli are good indicators of the air quality at the studied sites.
Particle matter (PM) and its associated compounds are a serious problem for urban air quality and a threat to human health. In the present study, we assessed the intraurban variation of PM, and characterized the human health risk associated to the inhalation of particles measured on PM filters, considering different land use areas in the urban area of Cordoba city (Argentina) and different age groups. To assess the intraurban variation of PM, a biomonitoring network of T. capillaris was established in 15 sampling sites with different land use and the bioaccumulation of Co, Cu, Fe, Mn, Ni, Pb and Zn was quantified. After that, particles were collected by instrumental monitors placed at the most representative sampling sites of each land use category and an inhalation risk was calculated. A remarkable intraurban difference in the heavy metals content measured in the biomonitors was observed, in relation with the sampling site land use. The higher content was detected at industrial areas as well as in sites with intense vehicular traffic. Mean PM10 levels exceeded the standard suggested by the U.S. EPA in all land use areas, except for the downtown. Hazard Index values were below EPA's safe limit in all land use areas and in the different age groups. In contrast, the carcinogenic risk analysis showed that all urban areas exceeded the acceptable limit (1 × 10−6), while the industrial sampling sites and the elder group presented a carcinogenic risk higher that the unacceptable limit. These findings validate the use of T. capillaris to assess intraurban air quality and also show there is an important intraurban variation in human health risk associated to different land use.
The present study quantifies non essential heavy metals highly toxic for biological systems (Pb, Hg and Cd) in five autochthonous epiphytic plants from Tillandsia genus (T. recurvata, T. meridionalis, T. duratii, T. tricholepis, T. loliacea) according to different traffic levels (reference, low, medium and high polluted sites) in Asunción (Paraguay). The three metals increased in polluted sites following Pb (till 62.99 ppm in T. tricholepis) > Cd (till 1.35 ppm in T. recurvata) > Hg (till 0.36 ppm in T. recurvata) and Pb and Cd levels were directly related to traffic flow. Although the species showed similar bioaccumulation pattern (namely, higher levels of metals in polluted sites), enrichment factors (maximum EF values 37.00, 18.16, and 11.90 for Pb, Hg, and Cd, respectively) reported T. tricholepis as the most relevant bioindicator due to its wide distribution and abundance in study sites, low metal content in control site and high metal contents in polluted sites, and significant correlations with traffic density of Pb and Cd. This study emphasizes the necessity of biomonitoring air pollution in areas out of air monitoring control such as Asunción, where the high levels of metal pollution especially Pb, may represent an increment of risk for the human population inhabiting this urban area.