Open Access This article is
- freely available
Diversity 2019, 11(2), 28; https://doi.org/10.3390/d11020028
Lichens and Bromeliads as Bioindicators of Heavy Metal Deposition in Ecuador
Sección de Ecología y Sistemática, Departamento de Ciencias Biológicas, Universidad Técnica Particular de Loja, San Cayetano s/n, Loja 1101608, Ecuador
Maestría 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
Author to whom correspondence should be addressed.
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
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 [2,3,4]. 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 [6,7,8]. 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 [10,11]. 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 [13,14,15].
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 [16,17]. Both types of organisms have been widely used in monitoring schemes in several cities around the globe [18,19,20,21,22]. Lichens, particularly in the family Parmeliaceae (e.g., Evernia prunastri (L.) Ach. [23,24,25,26], Flavoparmelia caperata (L.) Hale [27,28], and Hypogymnia physodes (L.) Nyl. ), and species in the genus Parmotrema A. Massal. [30,31,32,33,34,35]), 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 [16,36,37,38]. 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 [9,20,39,40,41,42,43].
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 µg/m3 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) . 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 m2), and a low quantity of green area per inhabitant (15.38 m2/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 m2/inhabitant) and very little vegetation (green areas cover only 635,000 m2); and is subject to high volumes of traffic.
- Northern Zone (N): With a relatively large quantity of green space (1,060,000 m2), this city district has a high amount of green space per inhabitant (38.95 m2/inhabitant); it is subject to moderate traffic only.
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) 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 HNO3 (70%) and 2 ml H2O2 (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 [47,48]. 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) .
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).
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).
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).
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 [12,46]. 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 [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 [12,46]. 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.  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 [53,54,55,56,57,58]. 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 [20,21,33,35,52]. However, the concentrations of these heavy metals in our control site (Forest) were relatively low [9,41,42,60]. 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 .
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. , 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 [21,33,35,50]. 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 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.
Conceptualization, ÁB. 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.
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).
|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|
- Mateos, A.C.; Amarillo, A.C.; Carreras, H.A.; González, C.M. Land use and air quality in urban environments: Human health risk assessment due to inhalation of airborne particles. Environ. Res. 2018, 161, 370–380. [Google Scholar] [CrossRef] [PubMed]
- Mayer, H. Air pollution in cities. Atmos. Environ. 1999, 33, 4029–4037. [Google Scholar] [CrossRef]
- Han, X.; Naeher, L.P. A review of traffic-related air pollution exposure assessment studies in the developing world. Environ. Int. 2006, 32, 106–120. [Google Scholar] [CrossRef] [PubMed]
- Hassanien, M.A.; El Shahawy, A.M. Environmental heavy metals and mental disorders of children in developing countries. In Environmental Heavy Metal Pollution and Effects on Child Mental Development: Risk Assessment and Prevention Strategies; Simeonov, L.I., Kochubovski, M.V., Simeonova, B.G., Eds.; Springer: Dordrecht, The Netherlands, 2011; pp. 1–25. [Google Scholar]
- Adamiec, E. Chemical fractionation and mobility of traffic-related elements in road environments. Environ. Geochem. Health 2017, 39, 1457–1468. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Ares, Á.; Itouga, M.; Kato, Y.; Sakakibara, H. Differential Metal Tolerance and Accumulation Patterns of Cd, Cu, Pb and Zn in the Liverwort Marchantia polymorpha L. Bull. Environ. Contam. Toxicol. 2017, 100, 444–450. [Google Scholar] [CrossRef] [PubMed]
- Hill, M.K. Understanding Environmental Pollution; Cambridge University Press: New York, NY, USA, 2010. [Google Scholar]
- Pescott, O.L.; Simkin, J.M.; August, T.A.; Randle, Z.; Dore, A.J.; Botham, M.S. Air pollution and its effects on lichens, bryophytes, and lichen-feeding Lepidoptera: Review and evidence from biological records. Biol. J. Linn. Soc. 2015, 115, 611–635. [Google Scholar] [CrossRef]
- Sánchez-Chardi, A. Biomonitoring potential of five sympatric Tillandsia species for evaluating urban metal pollution (Cd, Hg and Pb). Atmos. Environ. 2016, 131, 352–359. [Google Scholar] [CrossRef]
- Jurado, J.; Southgate, D. Dealing with air pollution in Latin America: The case of Quito, Ecuador. Environ. Dev. Econ. 1999, 4, 375–388. [Google Scholar] [CrossRef]
- Ministerio del Ambiente. Plan Nacional de Calidad del Aire; Agencia Suiza para el Desarrollo y la Cooperación, COSUDE y del Ministerio del Ambiente: Quito, Ecuador, 2010. [Google Scholar]
- Programa de las. Naciones Unidas para el Medio Ambiente, Municipalidad de Loja & Naturaleza y Cultura Internacional; Geo-Loja: Loja, Ecuador, 2007. [Google Scholar]
- Espinoza, E.P.; Molina, C.E. Contaminación del aire exterior Cuenca-Ecuador, 2009–2013. Posibles efectos en la salud. Revista de la Facultad de Ciencias Médicas 2014, 32, 6–17. [Google Scholar]
- Cevallos, V.M.; Díaz, V.; Sirois, C.M. Particulate matter air pollution from the city of Quito, Ecuador, activates inflammatory signaling pathways in vitro. Innate Immun. 2017, 23, 392–400. [Google Scholar] [CrossRef] [PubMed]
- Raysoni, A.U.; Armijos, R.X.; Weigel, M.M.; Echanique, P.; Racines, M.; Pingitore, N.E.; Li, W.W. Evaluation of sources and patterns of elemental composition of PM2.5 at three low-income neighborhood schools and residences in Quito, Ecuador. Int. J. Environ. Res. Public Health 2017, 14, 674. [Google Scholar] [CrossRef] [PubMed]
- Bermudez, G.M.A.; Rodriguez, J.H.; Pignata, M.L. Comparison of the air pollution biomonitoring ability of three Tillandsia species and the lichen Ramalina celastri in Argentina. Environ. Res. 2009, 109, 6–14. [Google Scholar] [CrossRef] [PubMed]
- Demiray, A.D.; Yolcubal, I.; Akyol, N.H.; Çobanoğlu, G. Biomonitoring of airborne metals using the Lichen Xanthoria parietina in Kocaeli Province, Turkey. Ecol. Ind. 2012, 18, 632–643. [Google Scholar] [CrossRef]
- Garty, J. Biomonitoring atmospheric heavy metals with lichens: Theory and application. Crit. Rev. Plant Sci. 2001, 20, 309–371. [Google Scholar] [CrossRef]
- Adamo, P.; Giordano, S.; Vingiani, S.; Cobianchi, R.C.; Violante, P. Trace element accumulation by moss and lichen exposed in bags in the city of Naples (Italy). Environ. Pollut. 2003, 122, 91–103. [Google Scholar] [CrossRef]
- Figueiredo, A.M.G.; Alcalá, A.L.; Ticianelli, R.B.; Domingos, M.; Saiki, M. The use of Tillandsia usneoides L. as bioindicator of air pollution in São Paulo, Brazil. J. Radioanal. Nucl. Chem. 2004, 259, 59–63. [Google Scholar] [CrossRef]
- Käffer, M.I.; Lemos, A.T.; Apel, M.A.; Rocha, J.V.; de Azevedo Martins, S.M.; Vargas, V.M.F. Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environ. Pollut. 2012, 163, 24–31. [Google Scholar] [CrossRef] [PubMed]
- Llop, E.; Pinho, P.; Matos, P.; Pereira, M.J.; Branquinho, C. The use of lichen functional groups as indicators of air quality in a Mediterranean urban environment. Ecol. Ind. 2012, 13, 215–221. [Google Scholar] [CrossRef]
- Conti, M.E.; Tudino, M.; Stripeikis, J.; Cecchetti, G. Heavy metal accumulation in the lichen Evernia prunastri transplanted at urban, rural and industrial sites in Central Italy. J. Atmos. Chem. 2004, 49, 83–94. [Google Scholar] [CrossRef]
- Balabanova, B.; Stafilov, T.; Sajn, R.; Baèeva, K. Characterization of heavy metals in lichen species Hypogymnia physodes and Evernia prunastri due to biomonitoring of air pollution in the vicinity of copper mine. Int. J. Environ. Res. Public Health 2012, 6, 779–792. [Google Scholar]
- Lackovičová, A.; Guttova, A.; Bačkor, M.; Pišút, P.; Pišút, I. Response of Evernia prunastri to urban environmental conditions in Central Europe after the decrease of air pollution. Lichenologist 2013, 45, 89–100. [Google Scholar] [CrossRef]
- Rhzaoui, G.; Divakar, P.K.; Crespo, A.; Tahiri, H. Biomonitoring of air pollutants by using lichens (Evernia prunastri) in areas between Kenitra and Mohammedia cities in Morocco. Lazaroa 2015, 36, 21–30. [Google Scholar] [CrossRef]
- Loppi, S.; Frati, L.; Paoli, L.; Bigagli, V.; Rossetti, C.; Bruscoli, C.; Corsini, A. Biodiversity of epiphytic lichens and heavy metal contents of Flavoparmelia caperata thalli as indicators of temporal variations of air pollution in the town of Montecatini Terme (central Italy). Sci. Total Environ. 2004, 326, 113–122. [Google Scholar] [CrossRef] [PubMed]
- Godinho, R.M.; Wolterbeek, H.T.; Verburg, T.; Freitas, M.C. Bioaccumulation behaviour of transplants of the lichen Flavoparmelia caperata in relation to total deposition at a polluted location in Portugal. Environ. Pollut. 2008, 151, 318–325. [Google Scholar] [CrossRef] [PubMed]
- Jeran, Z.; Jaćimović, R.; Batič, F.; Mavsar, R. Lichens as integrating air pollution monitors. Environ. Pollut. 2002, 120, 107–113. [Google Scholar] [CrossRef]
- Cañas, M.S.; Orellana, L.; Pignata, M.L. Chemical response of the lichens Parmotrema austrosinense and P. conferendum transplanted to urban and non-polluted environments. Ann. Bot. Fenn. 1997, 34, 27–34. [Google Scholar]
- Pyatt, F.B.; Grattan, J.P.; Lacy, D.; Pyatt, A.J.; Seaward, M.R.D. Comparative effectiveness of Tillandsia usneoides L. and Parmotrema praesorediosum (Nyl.) Hale as bio-indicators of atmospheric pollution in Louisiana (USA). Water Air Soil Pollut. 1999, 111, 317–326. [Google Scholar] [CrossRef]
- Zhang, Z.H.; Chai, Z.F.; Mao, X.Y.; Chen, J.B. Biomonitoring trace element atmospheric deposition using lichens in China. Environ. Pollut. 2002, 120, 157–161. [Google Scholar] [CrossRef]
- Aprile, G.G.; Di Salvatore, M.; Carratù, G.; Mingo, A.; Carafa, A.M. Comparison of the suitability of two lichen species and one higher plant for monitoring airborne heavy metals. Environ. Monit. Assess. 2010, 162, 291–299. [Google Scholar] [CrossRef] [PubMed]
- Chaparro, M.A.; Lavornia, J.M.; Chaparro, M.A.; Sinito, A.M. Biomonitors of urban air pollution: Magnetic studies and SEM observations of corticolous foliose and microfoliose lichens and their suitability for magnetic monitoring. Environ. Pollut. 2013, 172, 61–69. [Google Scholar] [CrossRef] [PubMed]
- Kularatne, K.I.A.; De Freitas, C.R. Epiphytic lichens as biomonitors of airborne heavy metal pollution. Environ. Exp. Bot. 2013, 88, 24–32. [Google Scholar] [CrossRef]
- Calasans, C.F.; Malm, O. Elemental mercury contamination survey in a chlor-alkali plant by the use of transplanted Spanish moss, Tillandsia usneoides (L.). Sci. Total Environ. 1997, 208, 165–177. [Google Scholar] [CrossRef]
- Pignata, M.L.; Plá, R.R.; Jasan, R.C.; Martinez, M.S.; Rodriguez, J.H.; Wannaz, E.D.; Gudino, G.L.; Carreras, H.A.; Gonzalez, C.M. Distribution of atmospheric trace elements and assesment of air quality in Argentina employing the lichen, Ramalina celastri, as a passive biomonitor: Detection of air pollution emission sources. Int. J. Environ. Health 2007, 1, 29–46. [Google Scholar] [CrossRef]
- Rodriguez, J.H.; Weller, S.B.; Wannaz, E.D.; Klumpp, A.; Pignata, M.L. Air quality biomonitoring in agricultural areas nearby to urban and industrial emission sources in Córdoba province, Argentina, employing the bioindicator Tillandsia capillaris. Ecol. Indic. 2011, 6, 1673–1680. [Google Scholar] [CrossRef]
- Amado-Filho, G.M.; Andrade, L.R.; Farina, M.; Malm, O. Hg localization in Tillandsia usneoides L. (Bromeliaceae), an atmospheric biomonitor. Atmos. Environ. 2002, 5, 881–887. [Google Scholar] [CrossRef]
- Alves, E.S.; Moura, B.B.; Domingos, M. Structural analysis of Tillandsia usneoides L. exposed to air pollutants in São Paulo City–Brazil. Water Air Soil Pollut. 2008, 189, 61–68. [Google Scholar] [CrossRef]
- Vianna, N.A.; Gonçalves, D.; Brandão, F.; de Barros, R.P.; Amado Filho, G.M.; Meire, R.O.; Andrade, L.R. Assessment of heavy metals in the particulate matter of two Brazilian metropolitan areas by using Tillandsia usneoides as atmospheric biomonitor. Environ. Sci. Pollut. Res. 2011, 18, 416–427. [Google Scholar] [CrossRef] [PubMed]
- Sutton, K.T.; Cohen, R.A.; Vives, S.P. Evaluating relationships between mercury concentrations in air and in Spanish moss (Tillandsia usneoides L.). Ecol. Indic. 2014, 36, 392–399. [Google Scholar] [CrossRef]
- Giampaoli, P.; Wannaz, E.D.; Tavares, A.R.; Domingos, M. Suitability of Tillandsia usneoides and Aechmea fasciata for biomonitoring toxic elements under tropical seasonal climate. Chemosphere 2016, 149, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Ochoa-Jimenez, D.A.; Cueva-Agila, A.; Prieto, M.; Aragon, G.; Benitez, A. Changes in the epiphytic lichen composition related with air quality in the city of Loja (Ecuador). Caldasia 2015, 37, 333–343. [Google Scholar]
- Wolterbeek, B. Biomonitoring of trace element air pollution: Principles, possibilities and perspectives. Environ. Pollut. 2002, 120, 11–21. [Google Scholar] [CrossRef]
- Hérnandez, O.H.Á.; Montaño, T.; Maldonado, J.; Caraballo, M.A.; Ojeda, C.G.S.; Granda, J.C.; Castillo, B.S. Método de selección para la ubicación de puntos de monitoreo de gases de combustión provenientes de fuentes fijas puntuales en la ciudad de Loja, Ecuador. Rev. Tecnol. ESPOL 2016, 29, 38–52. [Google Scholar]
- Smith, L.B.; Downs, R.J. Tillandsioideae (Bromeliaceae). Flora Neotrop. Monogr. 1997, 14, 663–1492. [Google Scholar]
- Sipman, H.J.M. Mason Hale’s Key to Parmotrema, Revised Edition: Key to Wide-Lobed Parmelioid Species Occurring in Tropical America (Genera Canomaculina, Parmotrema, Rimelia, Rimeliella). 2005. Available online: http://www.bgbm.org/sipman/keys/Neoparmo.htm (accessed on 2 February 2019).
- Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; R Core Team. Nlme: Linear and Nonlinear Mixed Effects Models; R Package: Vienna, Austria, 2018. [Google Scholar]
- R Team Development Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2015. [Google Scholar]
- Fuga, A.; Saiki, M.; Marcelli, M.P.; Saldiva, P.H. Atmospheric pollutants monitoring by analysis of epiphytic lichens. Environ. Pollut. 2008, 151, 334–340. [Google Scholar] [CrossRef] [PubMed]
- Monna, F.; Marques, A.N.; Guillon, R.; Losno, R.; Couette, S.; Navarro, N.; Dongarra, G.; Tamburo, E.; Varrica, D.; Chateau, C.; et al. Perturbation vectors to evaluate air quality using lichens and bromeliads: A Brazilian case study. Environ. Monit. Assess. 2017, 189, 566. [Google Scholar] [CrossRef] [PubMed]
- Thorpe, A.; Harrison, R.M. Sources and properties of non-exhaust particulate matter from road traffic: A review. Sci. Total Environ. 2008, 400, 270–282. [Google Scholar] [CrossRef] [PubMed]
- Block, M.L.; Calderón-Garcidueñas, L. Air pollution: Mechanisms of neuroinflammation and CNS disease. Trends Neurosci. 2009, 32, 506–516. [Google Scholar] [CrossRef] [PubMed]
- Mielke, H.W.; Laidlaw, M.A.; Gonzales, C. Lead (Pb) legacy from vehicle traffic in eight California urbanized areas: Continuing influence of lead dust on children’s health. Sci. Total Environ. 2010, 408, 3965–3975. [Google Scholar] [CrossRef] [PubMed]
- Pulles, T.; Van der Gon, H.D.; Appelman, W.; Verheul, M. Emission factors for heavy metals from diesel and petrol used in European vehicles. Atmos. Environ. 2012, 61, 641–651. [Google Scholar] [CrossRef]
- Sysalová, J.; Sýkorová, I.; Havelcová, M.; Száková, J.; Trejtnarová, H.; Kotlík, B. Toxicologically important trace elements and organic compounds investigated in size-fractionated urban particulate matter collected near the Prague highway. Sci. Total Environ. 2012, 437, 127–136. [Google Scholar] [CrossRef] [PubMed]
- Pant, P.; Harrison, R.M. Estimation of the contribution of road traffic emissions to particulate matter concentrations from field measurements: A review. Atmos. Environ. 2013, 77, 78–97. [Google Scholar] [CrossRef]
- Singh, R.; Gautam, N.; Mishra, A.; Gupta, R. Heavy metals and living systems: An overview. Indian J. Pharmacol. 2011, 43, 246–253. [Google Scholar] [CrossRef] [PubMed]
- Abril, G.A.; Wannaz, E.D.; Mateos, A.C.; Invernizzi, R.; Plá, R.R.; Pignata, M.L. Characterization of atmospheric emission sources of heavy metals and trace elements through a local-scale monitoring network using T. capillaris. Ecol. Indic. 2014, 40, 153–161. [Google Scholar] [CrossRef]
- Giordano, S.; Adamo, P.; Sorbo, S.; Vingiani, S. Atmospheric trace metal pollution in the Naples urban area based on results from moss and lichen bags. Environ. Pollut. 2005, 136, 431–442. [Google Scholar] [CrossRef] [PubMed]
- Gope, M.; Masto, R.E.; George, J.; Hoque, R.R.; Balachandran, S. Bioavailability and health risk of some potentially toxic elements (Cd, Cu, Pb and Zn) in street dust of Asansol, India. Ecotoxicol. Environ. Saf. 2017, 138, 231–241. [Google Scholar] [CrossRef] [PubMed]
- Minganti, V.; Capelli, R.; Drava, G.; De Pellegrini, R.; Brunialti, G.; Giordani, P.; Modenes, I.P. Biomonitoring of trace metals by different species of lichens (Parmelia) in North-West Italy. J. Atmos. Chem. 2003, 45, 219–229. [Google Scholar] [CrossRef]
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 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.
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.
|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|
|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|
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).