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The use of Parmotrema tinctorum (Parmeliaceae) as a bioindicator of air pollution

Abstract

Air quality monitoring by automatic stations, although efficient, does not allow evaluating the effects of pollution on living organisms and communities. Thus, the aim of the present study was to use lichens of the Parmotrema tinctorum species in active air quality biomonitoring. We used a new methodology of chlorosis area analyses in QGis software, as low-cost and complementary tool to physicochemical methods. Samples of the aforementioned species were exposed to atmospheric pollution for 30 consecutive days in the dry and rainy seasons, in urban and industrial regions. The chlorosis rate (34% of the lichen thalli, on average) and the accumulation of sulfur (1.1 g.kg-1, on average) were higher in the samples of lichens exposed in the industrial region, in the dry season. There was a moderate-to-high positive correlation between chlorosis rate and lichen content of nitrogen, sulfur, iron and zinc, in the dry season, mainly with sulfur (r = 0.71). The results confirmed the sensitive of P. tinctorum to atmospheric pollution, even after a short exposure time. Such new active biomonitoring methodology (chlorosis analysis in the QGis) can be used in future studies of air quality assessment by environmental and health surveillance managers.

Key words
active biomonitoring; air quality; lichen

Resumo

O monitoramento da qualidade do ar por estações automáticas, apesar de eficiente, não permite avaliar os efeitos da poluição sobre organismos e comunidades. Assim, o objetivo do presente estudo foi usar liquens da espécie Parmotrema tinctorum em biomonitoramento ativo da qualidade do ar, baseado em uma nova metolologia de análise de clorose por meio do software Qgis, como uma ferramenta de baixo custo e complementar aos métodos físico-químicos. Amostras dessa espécie foram expostas à poluentes do ar por 30 dias consecutivos, nas estações seca e chuvosa, em regiões urbanas e industriais. A taxa de clorose (34% do talo dos liquens, em média) e o acúmulo de enxofre (1,1 g.kg-1, em média) foram maiores em amostras expostas na região industrial, na estação seca. Houve correlação positiva moderada a alta entre a taxa de clorose e o acúmulo de nitrogênio, enxofre, ferro e zinco, no período seco, principalmente com exnofre (r = 0,71). Os resultados confirmaram a sensibilidade de P. tinctorum à poluição atmosférica, mesmo após um curto período de exposição. Essa nova metodologia de biomonitoramento ativo (análise de clorose por meio do QGis) pode ser usada em estudos futuros sobre avaliação da qualidade do ar por gestores de vigilância ambiental e de saúde.

Palavras-chave
biomonitoramento ativo; qualidade do ar; líquen

Air quality is often assessed through physicochemical means in automatic monitoring stations, which measure pollutants at local scale. These methods are efficient, but do not allow evaluating the systemic effects of pollution on living organisms and communities. Biological indicators can show these impacts with results in the short-, mid- and long-term, not necessarily using high-cost equipments. Although biomonitoring should not replace physicochemical methods, it can provide complementary information about biological damages caused by pollutants, mainly about the cumulative ones (Ellenberg et al. 1991Ellenberg H, Arndt U, Bretthauer R, Ruthsatz B & Steubing L (1991) Biological monitoring: signals from the environment. Ed. Vieweg, Berlin. Available at <http://www.nzdl.org/cgi-bin/library.cgi?e=d-00000-00---off-0envl--00-0----0-10-0---0---0direct-10---4-------0-1l--11-en-50---20-about---00-0-1-00-0-0-11-1-0utfZz-8-10&a=d&c=envl&cl=CL1.1&d=HASH76bee393577eaa81eb621c.9.pr>. Access on 14 April 2020.
http://www.nzdl.org/cgi-bin/library.cgi?...
; Klumpp 2001Klumpp A (2001) Utilização de bioindicadores de poluição em condições temperadas e tropicais. In: Maia NB, Martos HL & Barrella W (eds.) Indicadores ambientais: conceitos e aplicações. Ed. EDUC, São Paulo. Pp. 77-94.; Saiki et al. 2014Saiki M, Santos JO, Alves ER, Genezini FA, Marcelli MP & Saldiva PHN (2014) Correlation study of air pollution and cardio-respiratory diseases through NAA of an atmospheric pollutant biomonitor. Journal of Radioanalytical and Nuclear Chemistry 299: 773-779.; Lucheta et al. 2019).

Lichens stand out as one of the most efficient living organisms used as bioindicators of air pollution (Nimis et al. 1990Nimis PL, Castello M & Perotti M (1990) Lichens as biomonitors of sulphur dioxide pollution in La Spezia (Northern Italy). The Lichenologist 22: 333-344.). This happens due several characteristics such as: a) lack of protective layers such as cuticle or serous layers, as seen in phanerogams; b) wide geographical distribution; c) lack of excretion structure, which allows compounds absorbed throughout lichens’ life to be retained in their thallus (Raven et al. 2014Raven PH, Eichhorn SE & Evert RF (2014) Biologia vegetal. Guanabara Koogan, Rio de Janeiro. 876p.).

Certain elements that are incorporated in the lichens can be found in different parts of the thallus, from its surface, linked to cell membranes or in connections with intracellular substances, such as proteins. The accumulation process of these elements in the lichen thalli occurs in different ways, which can be due to simple deposition on the surface of the cortex, by accumulation between the fungi hyphae, by passive transport in response to differences in osmotic and electrical potential, or also by active transport, when membrane connections occur (Bargagli & Mikhailova 2002Bargagli R & Mikhailova I (2002) Accumulation of inorganic contaminants. In: Nimis PL, Scheidegger C & Wolseley PA (eds.) Monitoring with lichens. Ed. Kluwer Academic Publishers, Berlim. Pp. 65-84.; Mazitelli et al. 2006Mazitelli SMM, Mota Filho FO, Pereira ECG & Figueira R (2006) Utilização de liquens no biomonitoramento da qualidade do ar. In: Xavier Filho L, Legaz ME, Vicente C & Pereira EC (eds.) Biologia de líquens. Ed. Âmbito Cultural, Rio de Janeiro. Pp. 100-143.).

Passive biomonitoring uses organisms that already exist in a given area, while active biomonitoring is done with the exposure of organisms in the area to be evaluated for a defined time and under controlled conditions (Klumpp 2001Klumpp A (2001) Utilização de bioindicadores de poluição em condições temperadas e tropicais. In: Maia NB, Martos HL & Barrella W (eds.) Indicadores ambientais: conceitos e aplicações. Ed. EDUC, São Paulo. Pp. 77-94.). Most studies passively assess lichen diversity based on the association between low species richness and increased pollution rates in the investigated. These studies are of paramount importance because they help better understand lichen communities’ response to prolonged exposure to air pollutants. However, adequate sampling efforts and prior knowledge about the subject are required to enable lichen species identification environments (Raimundo-Costa & Mineo 2013Raimundo-Costa W & Mineo MF (2013) Os líquens como bioindicadores de poluição atmosférica no município de Uberaba, Minas Gerais. Revista Eletrônica em Gestão, Educação e Tecnologia Ambiental 13: 2690-2700.; Luchetta et al. 2018Luchetta F, Koch NM, Martins SMDA & Schmitt JL (2018) Corticolous lichen community in an urbanization gradient in the Rio dos Sinos Hydrographic Basin, southern Brazil. Rodriguésia 69: 323-334.; Luchetta et al. 2019Luchetta F, Koch NM, Käffer MI, Riegel RP, Martins SMA & Schmitta JL (2019) Lichens as indicators of environmental quality in southern Brazil: an integrative approach based on community composition and functional parameters. Ecological Indicators 107: 105587.; Loppi 2019Loppi S (2019). May the diversity of epiphytic lichens be used in environmental forensics? Diversity 11: 36.). On the other hand, active biomonitoring has been mainly based on the analysis of potentially toxic metal accumulations in lichen thalli and morphophysiological damages (Käffer et al. 2012Käffer MI, Lemos AT, Apel MA, Rocha JV, Martins SMA & Vargas VMF (2012) Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environmental Pollution 163: 24-31.; Saiki et al. 2014Saiki M, Santos JO, Alves ER, Genezini FA, Marcelli MP & Saldiva PHN (2014) Correlation study of air pollution and cardio-respiratory diseases through NAA of an atmospheric pollutant biomonitor. Journal of Radioanalytical and Nuclear Chemistry 299: 773-779.; Koch et al. 2018Koch NM, Lucheta F, Käffer MI, Martins SA & Vargas VMF (2018) Air quality assessment in different urban areas from Rio Grande do Sul state, Brazil, using lichen transplants. Anais da Academia Brasileira de Ciências 90: 2233-2248.; Port et al. 2018Port RK, Käffer MI & Schmitt JL (2018) Morphophysiological variation and metal concentration in the thallus of Parmotrema tinctorum (Despr. ex Nyl.) Hale between urban and forest areas in the subtropical region of Brazil. Environmental Science and Pollution Research 25: 33667-33670.).

In this context, this study aimed to use Parmotrema tinctorum (Despr. ex Nyl.) Hale (Parmeliacea) in active air quality biomonitoring, based on a new methodology of chlorosis area analyses in QGis software, comparing to metals content in lichen thalli.

This species was selected because it has wide geographical distribution, it is easily recognizable in the field and because it is sensitive to atmospheric pollution (Benatti & Marcelli 2009Benatti MN & Marcelli MP (2009) Espécies de Parmotrema (Parmeliaceae, Ascomycota) do litoral centro-sul do estado de São Paulo, Brasil. I. Grupos químicos girofórico e lecanórico. Acta Botanica Brasilica 23: 1013-1026.; Käffer et al. 2012Käffer MI, Lemos AT, Apel MA, Rocha JV, Martins SMA & Vargas VMF (2012) Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environmental Pollution 163: 24-31.; Koch et al. 2018Koch NM, Lucheta F, Käffer MI, Martins SA & Vargas VMF (2018) Air quality assessment in different urban areas from Rio Grande do Sul state, Brazil, using lichen transplants. Anais da Academia Brasileira de Ciências 90: 2233-2248.; Port et al. 2018Port RK, Käffer MI & Schmitt JL (2018) Morphophysiological variation and metal concentration in the thallus of Parmotrema tinctorum (Despr. ex Nyl.) Hale between urban and forest areas in the subtropical region of Brazil. Environmental Science and Pollution Research 25: 33667-33670.). Its foliose thallus ranges from silver to greenish gray, or to olive green when it is wet; it presents full or sub-crenated margins, as well as smooth upper cortex, which may be rough or cracked and present ridges on the ridges or simple/granular fissures (Benatti & Marcelli 2009Benatti MN & Marcelli MP (2009) Espécies de Parmotrema (Parmeliaceae, Ascomycota) do litoral centro-sul do estado de São Paulo, Brasil. I. Grupos químicos girofórico e lecanórico. Acta Botanica Brasilica 23: 1013-1026.). In addition, P. tinctorum positively responds to the “C” test (contact with sodium hypochlorite), since it shows orange color in contact with the reagent; as well as to the “K” test, since it shows reddish color in contact with potassium hydroxide (Fleig & Grüninger 2008Fleig M & Grüninger W (2008) Liquens da floresta com Araucária no Rio Grande do Sul, Pró-mata. Ed. PUCRS, Porto Alegre. 217p.; Benatti & Marcelli 2009Benatti MN & Marcelli MP (2009) Espécies de Parmotrema (Parmeliaceae, Ascomycota) do litoral centro-sul do estado de São Paulo, Brasil. I. Grupos químicos girofórico e lecanórico. Acta Botanica Brasilica 23: 1013-1026.).

The study was conducted in Uberaba Municipality, Triângulo Mineiro region, Minas Gerais state, Brazil, whose estimated population comprises 334 thousand inhabitants (IBGE 2020IBGE - Brazilian Institute of Geography and Statistics (2020) Censo demográfico. Available at <http://cidades.ibge.gov.br/xtras/perfil.php?lang=&codmun=317010> . Access on 19 April 2020.
http://cidades.ibge.gov.br/xtras/perfil....
). Uberaba has the 4th largest vehicle fleet in Minas Gerais state (Denatran 2020Denatran - National traffic department (2020) Estatística: frota veicular. Available at <http://www.denatran.gov.br/index.php/estatistica>. Access on 14 April 2020.
http://www.denatran.gov.br/index.php/est...
); it is crossed by two important highways and has four industrial districts. However, the region lacks air quality monitoring and control program, which is only available at the state’s capital.

Parmotrematinctorum samples were collected in a Conservation Unit located in a rural area (30 km North of the urban center; 19°32’34.10”S, 47°53’38.22”W) which is less exposed to atmospheric pollution. They were collected with part of the substrate (tree bark) and remained in the laboratory for one week for acclimation and physiological homogenization purposes (Martins-Mazzitelli et al. 2006Martins-Mazzitelli SMA, Mota Filho FO, Pereira EC & Figueira R (2006) Utilização de liquens no biomonitoramento da qualidade do ar. In: Xavier Filho L, Legaz ME, Córdoba CV & Pereira EC (eds.) Biologia de Líquens. Vol 3. Ed. Âmbito Cultural, Rio de Janeiro. Pp. 100-133.). During this period, lichen samples were drawn and measured in the QGis software version 2.18, in order to be compared to macroscopically changed areas of each lichen thallus, after the exposure period. Thus, it was possible calculating the total lichen thallus area and the affected area rate (chlorosis and/or necrosis).

This software, usually used for geographical analyses and making maps, was quite efficient since it has efficient tools for checking previously inserted areas using raster or vector files (produced manually). In the present study, scale measures in meters were established in the program environment, thus being able to calculate the area values for each lichen thalli, which were inserted as vector-type files, drawn from photographs in scale 1 to 1 of the lichen stalks themselves. No plug-ins were used, only layers of polygons and the area function in QGis’ own calculator.

Lichen samples were exposed to atmospheric pollution for 30 consecutive days in the dry (August to September) and rainy (December to January) seasons. Lichen thalli were transplanted from the laboratory (after the period for acclimation) to each exposure points, which comprised three samples per point, set in trees at 2 m above the ground. About four thalli was exposed in each sample, with 12–15 cm in diameter each thallus, approximately. The samples were transported in sterile vials in order to avoid contamination and loss of material that could compromise the results.

Lichen exposure points (in supplementary data <https://doi.org/10.6084/m9.figshare.12797468.v1>) were distributed as follows: three points in urban areas (A, B and C), with air pollution specially by vehicle emissions, and one point in industrial area (D) presenting chemical, fertilizer and fuel distribution industries (19°58’9.25”S, 47°53’22.46”W). Points A (19°44’3.68”S, 47°59’13.45”W) and B (19°46’39.33”S, 47°56’1.09”W) were in residential areas, while point C was downtown (19°45’5.83”S, 47°55’55.74”W), 40 meters away from an important avenue that presented intense traffic on a daily basis. This point was a typical commercial area, which hosted a few homes and many vertical condominiums that hindered airborne pollutant spreading.

Control group samples were kept in sterile vials in the laboratory during the exposure period.

The thalli from the exposure points and from the control group were homogenized to obtain 2 g per sample for acid digestion and further analysis of some chemical element concentration related to air pollution (nitrogen (N), sulfur (S), copper (Cu), iron (Fe) and zinc (Zn)). The analyzes were performed in a private laboratory, by atomic emission spectrometer (Agilent MP AES 4100), in order to validate the chlorosis analysis.

Chlorosis rate and pollutant concentration data were compared between exposure points based on analysis of variance (one-way ANOVA) and Tukey’s test for parametric data, or on Kruskal-Wallis and Dunn tests for non-parametric (p < 0.05). The data were also compared between the dry and rainy seasons by T test or Mann-Whitney (p < 0.05), in the BioEstat 5.3 software.

Lichen thalli at all exposure points showed pink shade chlorosis, which is characteristic of exposure to S (Ellenberg et al. 1991Ellenberg H, Arndt U, Bretthauer R, Ruthsatz B & Steubing L (1991) Biological monitoring: signals from the environment. Ed. Vieweg, Berlin. Available at <http://www.nzdl.org/cgi-bin/library.cgi?e=d-00000-00---off-0envl--00-0----0-10-0---0---0direct-10---4-------0-1l--11-en-50---20-about---00-0-1-00-0-0-11-1-0utfZz-8-10&a=d&c=envl&cl=CL1.1&d=HASH76bee393577eaa81eb621c.9.pr>. Access on 14 April 2020.
http://www.nzdl.org/cgi-bin/library.cgi?...
). Some toxic air elements have affinity to chloroplasts, where the chlorophyll can be degraded to pheophytin, leading to the emergence of chlorosis and, later, of necrosis areas (Ellenberg et al. 1991Ellenberg H, Arndt U, Bretthauer R, Ruthsatz B & Steubing L (1991) Biological monitoring: signals from the environment. Ed. Vieweg, Berlin. Available at <http://www.nzdl.org/cgi-bin/library.cgi?e=d-00000-00---off-0envl--00-0----0-10-0---0---0direct-10---4-------0-1l--11-en-50---20-about---00-0-1-00-0-0-11-1-0utfZz-8-10&a=d&c=envl&cl=CL1.1&d=HASH76bee393577eaa81eb621c.9.pr>. Access on 14 April 2020.
http://www.nzdl.org/cgi-bin/library.cgi?...
; Bargagli & Mikhailova 2002Bargagli R & Mikhailova I (2002) Accumulation of inorganic contaminants. In: Nimis PL, Scheidegger C & Wolseley PA (eds.) Monitoring with lichens. Ed. Kluwer Academic Publishers, Berlim. Pp. 65-84.). Photobiont vitality in samples of P. tinctorum has decreased in urban and industrial areas; this morphological damage is a sensitive variable in active biomonitoring, considered as an initial response to the air pollutants exposure (Port et al. 2018Port RK, Käffer MI & Schmitt JL (2018) Morphophysiological variation and metal concentration in the thallus of Parmotrema tinctorum (Despr. ex Nyl.) Hale between urban and forest areas in the subtropical region of Brazil. Environmental Science and Pollution Research 25: 33667-33670.).

Lichens recorded higher chlorosis rates during the dry season, as seen in the dark areas of Figure 1 (supplementary data <https://doi.org/10.6084/m9.figshare.12797468.v1>). Significant difference in chlorosis rates was observed between exposure points, in the dry season; the highest value was recorded for the industrial region (34% of lichen thalli, on average) (Tab. 1). Although no significant differences were observed between exposure points in the rainy season, the chlorosis rate tended to present higher values in the industrial (D) and central (C) regions.

Figure 1
a-h. Chlorosis area verified in lichen thalli – a-d. samples exposed in the dry season at sampling points A, B, C and D, respectively; e-h. samples exposed during the rainy season at sampling points A, B, C and D, respectively (in supplementary data).
Table 1
Mean of chlorosis (%) and concentration of polluting elements in samples of lichens from different points, in the dry and rainy season.

Pearson’s coefficient showed moderate-to-high positive correlation between chlorosis rate in the lichen thalli and N, S, Fe and Zn concentrations (Tab. 2). The highest correlation was recorded between chlorosis rate and S concentration (r = 0.71).

Table 2
Pearson correlation matrix between variables collected in the dry period, in the studied points.

Based on results of chemical element accumulation in lichen thalli, spatial variation was observed only for the concentrations of S, during the dry season; it was higher in the industrial region (D), with 1.1 g.kg-1 on average (Tab. 1). The concentrations of N, Fe and Zn tended to be higher in the industrial region (D), and Cu higher in the central region (C), although there was no significant difference.

Some averages showed a very high standard deviation; so it is suggested to increase the number of samples and, if possible, to leave them exposed for a longer time, for future studies, in order to increase the accumulation of chemical elements related to air pollution. Studies carried out with P. tinctorum in active biomonitoring adopted a longer exposure time (7 months) and recorded higher concentrations of S and metals, as well as more significant morphophysiological damages (Käffer et al. 2012Käffer MI, Lemos AT, Apel MA, Rocha JV, Martins SMA & Vargas VMF (2012) Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environmental Pollution 163: 24-31.; Koch et al. 2018Koch NM, Lucheta F, Käffer MI, Martins SA & Vargas VMF (2018) Air quality assessment in different urban areas from Rio Grande do Sul state, Brazil, using lichen transplants. Anais da Academia Brasileira de Ciências 90: 2233-2248.).

The industrial region comprised chemical and fertilizer industries that use S and N in their production processes, stood out. The intense traffic in the central and industrial regions is also responsible for releasing air pollutants deriving from fuel combustion (Braun et al. 2004Braun S, Appel LG & Schmal M (2004) A poluição gerada por máquinas de combustão interna movidas a diesel - a questão dos particulados. Estratégias atuais para a redução e controle das emissões e tendências futuras. Química Nova 27: 472-482.; Lopes et al. 2018Lopes TFA, Policarpo NA, Vasconcelos VMR & Oliveira MLMD (2018) Vehicular emissions estimate in the Fortaleza, Ceará, Brazil, metropolitan region in 2010. Engenharia Sanitária e Ambiental 23: 1013-1025.). Cu, Fe and Zn found in the atmosphere may be of vehicular origin, since one of the emission sources of these elements refers to the wearing of automotive parts, tires and brakes, whose particulate matter deposited on different surfaces is continuously resuspended in the environment (Qi et al. 2016Qi L, Zhang Y, Ma Y, Chen M, Ge X, Ma Y, Zheng J, Wang Z & Li S (2016) Source identification of trace elements in the atmosphere during the second Asian Youth Games in Nanjing, China: influence of control measures on air quality. Atmospheric Pollution Research 7: 547-556.). These elements are also found in the composition of motor oils, which have potential to increase their concentration in the environment (Silveira et al. 2010Silveira ELC, Coelho RC, Moita Neto JM, Moura CVR & Moura EM (2010) Determinação de metais em óleos lubrificantes, provenientes de motores de ônibus urbano, utilizando a FAAS. Química Nova 33: 1863-1867.).

The concentrations of S, Cu and Fe were higher in the dry season, regardless of the region (Tab. 1). The seasonal difference may be associated with lower temperature and rainfall records in the region, which are common in winter and, consequently, with lower pollutant dispersion. On the other hand, the concentration of chemical elements in the atmosphere tends to be lower in the rainy season, since they are removed from the air and incorporated in water particles (Baird & Cann 2011Baird C & Cann M (2011) Química ambiental. Ed. Bookman, Porto Alegre. 844p.; Ouyang et al. 2015Ouyang W, Guo B, Cai G, Li Q, Han S, Liu B & Liu X (2015) The washing effect of precipitation on particulate matter and the pollution dynamics of rainwater in downtown Beijing. Science of The Total Environment 505: 306-314.).

The results confirmed the sensitive of P. tinctorum to atmospheric pollution, even after a short exposure time. It could increase the accumulation of chemical elements related to such pollution and find significant differences between the points studied, with a longer time of exposure. On the other hand, as the morphological effects, with the gradual loss of the photobiont component, are the first responses to air polluted, the analysis of chlorosis using the QGis software proposed here proved to be effective in providing fast results.

As a low-cost tool, complementary to the physical-chemical methods of monitoring air pollutants, this new methodology can be used to improve researches on active biomonitoring and air quality assessment by environmental and health surveillance managers.

Supplementary data: <https://doi.org/10.6084/m9.figshare.12797468.v1>.

Acknowledgements

The authors are grateful for the financial support provided by Minas Gerais Research Funding Foundation - Fapemig (APQ-00317-14), and National Council for Scientific and Technological Development - CNPq (443850/2014-3).

References

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  • Bargagli R & Mikhailova I (2002) Accumulation of inorganic contaminants. In: Nimis PL, Scheidegger C & Wolseley PA (eds.) Monitoring with lichens. Ed. Kluwer Academic Publishers, Berlim. Pp. 65-84.
  • Benatti MN & Marcelli MP (2009) Espécies de Parmotrema (Parmeliaceae, Ascomycota) do litoral centro-sul do estado de São Paulo, Brasil. I. Grupos químicos girofórico e lecanórico. Acta Botanica Brasilica 23: 1013-1026.
  • Braun S, Appel LG & Schmal M (2004) A poluição gerada por máquinas de combustão interna movidas a diesel - a questão dos particulados. Estratégias atuais para a redução e controle das emissões e tendências futuras. Química Nova 27: 472-482.
  • Denatran - National traffic department (2020) Estatística: frota veicular. Available at <http://www.denatran.gov.br/index.php/estatistica>. Access on 14 April 2020.
    » http://www.denatran.gov.br/index.php/estatistica
  • Ellenberg H, Arndt U, Bretthauer R, Ruthsatz B & Steubing L (1991) Biological monitoring: signals from the environment. Ed. Vieweg, Berlin. Available at <http://www.nzdl.org/cgi-bin/library.cgi?e=d-00000-00---off-0envl--00-0----0-10-0---0---0direct-10---4-------0-1l--11-en-50---20-about---00-0-1-00-0-0-11-1-0utfZz-8-10&a=d&c=envl&cl=CL1.1&d=HASH76bee393577eaa81eb621c.9.pr>. Access on 14 April 2020.
    » http://www.nzdl.org/cgi-bin/library.cgi?e=d-00000-00---off-0envl--00-0----0-10-0---0---0direct-10---4-------0-1l--11-en-50---20-about---00-0-1-00-0-0-11-1-0utfZz-8-10&a=d&c=envl&cl=CL1.1&d=HASH76bee393577eaa81eb621c.9.pr
  • Fleig M & Grüninger W (2008) Liquens da floresta com Araucária no Rio Grande do Sul, Pró-mata. Ed. PUCRS, Porto Alegre. 217p.
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    » http://cidades.ibge.gov.br/xtras/perfil.php?lang=&codmun=317010
  • Käffer MI, Lemos AT, Apel MA, Rocha JV, Martins SMA & Vargas VMF (2012) Use of bioindicators to evaluate air quality and genotoxic compounds in an urban environment in Southern Brazil. Environmental Pollution 163: 24-31.
  • Klumpp A (2001) Utilização de bioindicadores de poluição em condições temperadas e tropicais. In: Maia NB, Martos HL & Barrella W (eds.) Indicadores ambientais: conceitos e aplicações. Ed. EDUC, São Paulo. Pp. 77-94.
  • Koch NM, Lucheta F, Käffer MI, Martins SA & Vargas VMF (2018) Air quality assessment in different urban areas from Rio Grande do Sul state, Brazil, using lichen transplants. Anais da Academia Brasileira de Ciências 90: 2233-2248.
  • Lopes TFA, Policarpo NA, Vasconcelos VMR & Oliveira MLMD (2018) Vehicular emissions estimate in the Fortaleza, Ceará, Brazil, metropolitan region in 2010. Engenharia Sanitária e Ambiental 23: 1013-1025.
  • Loppi S (2019). May the diversity of epiphytic lichens be used in environmental forensics? Diversity 11: 36.
  • Luchetta F, Koch NM, Käffer MI, Riegel RP, Martins SMA & Schmitta JL (2019) Lichens as indicators of environmental quality in southern Brazil: an integrative approach based on community composition and functional parameters. Ecological Indicators 107: 105587.
  • Luchetta F, Koch NM, Martins SMDA & Schmitt JL (2018) Corticolous lichen community in an urbanization gradient in the Rio dos Sinos Hydrographic Basin, southern Brazil. Rodriguésia 69: 323-334.
  • Martins-Mazzitelli SMA, Mota Filho FO, Pereira EC & Figueira R (2006) Utilização de liquens no biomonitoramento da qualidade do ar. In: Xavier Filho L, Legaz ME, Córdoba CV & Pereira EC (eds.) Biologia de Líquens. Vol 3. Ed. Âmbito Cultural, Rio de Janeiro. Pp. 100-133.
  • Mazitelli SMM, Mota Filho FO, Pereira ECG & Figueira R (2006) Utilização de liquens no biomonitoramento da qualidade do ar. In: Xavier Filho L, Legaz ME, Vicente C & Pereira EC (eds.) Biologia de líquens. Ed. Âmbito Cultural, Rio de Janeiro. Pp. 100-143.
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Supplementary Material

See supplementary material at <https://doi.org/10.6084/m9.figshare.12797468.v1 >

Edited by

Area Editor: Dr. Marcelo Moro

Publication Dates

  • Publication in this collection
    22 Oct 2021
  • Date of issue
    2021

History

  • Received
    11 Oct 2019
  • Accepted
    03 Sept 2020
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