The use of plants in the assessment of air pollution has been used for many years. The pioneers were the Scandinavian researchers Rühling and Tyler [1968]. The scientific literature is dominated by the classic definition of terms related to environmental bioindication proposed by Markert et al. [2003]: ‘A bioindicator is an organism (or part of an organism or a community of organisms) that contains information on the quality of the environment (or a part of the environment). A biomonitor, on the other hand, is an organism (or a part of an organism or a community of organisms) that contains information on the quantitative aspects of the quality of the environment’. Wolterbeek et al. [2010] proposed a much shorter definition ‘Biomonitoring, in a general sense, may be defined as the use of bio-organisms/materials to obtain (quantitative) information on certain characteristics of the biosphere’. Bioindication methods are used especially when we are dealing with many contaminants occurring simultaneously. They are also helpful in learning about the history of changes in the degree of pollution over hundreds of years. The final effect of properly used bioindication is a more complete picture of the state of the environment than assessed only by physico-chemical methods [Gorovtsov et al. 2017; Chaudhuri, Roy 2023]. Presentations of the benefits and falsification of bioindication methods are presented in Table 1.
Comparing the advantages and disadvantages of biological monitoring (compiled by authors)
| Benefits | Disadvantages |
|---|---|
| Plants have a great ability to absorb and store pollutants | Plants absorb pollutants from the air and soil, which makes it difficult to interpret the results |
| Contaminants accumulated in plants or on their surface can be analysed by physical or chemical methods | The results of determining the content of pollutants in plants are not as precise as their measurements directly in the air |
| Plant research enables comprehensive and long-term measurements | Short-term fluctuations in the level of contamination distort the results |
| Plants can be used to identify sources of pollutant emissions, their dispersion and deposition | The need to use specific plant taxa |
| Relatively low cost | |
| Possibility to select a large number of measuring points over a large area | Difficulties in finding a suitable taxon in the entire study area |
| The use of plants enables a real assessment of the state of pollution and threat | It is not possible to compare the results with legal environmental pollution standards |
| Independence from the source of energy in the field. No risk of equipment damage | The condition and condition of the indicator plant depends on many factors such as climate change, pathogens, etc. |
Indicator plants can be divided into two basic groups [Birungi et al. 2007]:
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Passive bioindicators are living organisms that naturally occur in the study area. The disadvantage of their use is often the difficulty of finding them throughout the area, and the advantages of the lack of maintenance and lower research costs. In return, the interpretation of results must take into account an important number of criteria related to the heterogeneity of the living conditions: soil quality, climatic conditions and season, genetic variability and metabolic state, heterogeneity of the spatial distribution of selected species.
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Active bioindicators are plants imported on the study site. The exposure of biological material in specific greenhouses generally makes it possible to be freed from the preceding.
Bioindication methods make it possible to supplement physical and chemical tests, which usually show individual data of specific pollutants, not taking into account other pollutants and not taking into account the changing environmental conditions [Wolterbeek 2002]. Mosses, thanks to their properties discussed in further chapters, are very often used in the assessment of air pollution [e.g. Dołęgowska et al. 2021; Godzik 2020; Kapusta et al. 2020; Chaudhuri, Roy 2023].
The disadvantage of bioindication methods is the inability to obtain results with legal norms of pollutants determined by instrumental methods restrictions. In practice, it is often used to combine physicochemical measurements with bioindication observations. Zechmeister et al. [2003] showed that in the moss-bag method, the metal content in the exposed moss was correlated with the concentration in the air, which proves the effectiveness of this method. The effectiveness of moss testing methods in assessing air pollution is evidenced by the large number of international, national and local programs using these methods.
The aim of our publication was to assess the possibility of using mosses in biomonitoring of air pollution in the terrestrial environment. The effectiveness of various methods and their practical applications are discussed. The main international programs using mosses are presented. The analysis partly used the literature review method proposed by Snyder [2019] for environmental analyses. The literature search method PRISMA (Preferred Reporting Items for Systematic Review and Meta-analyses) was also used [Diener, Mudu 2021; Sarkis-Onofre et al. 2021; Chaudhuri, Roy 2023]. As a result of this procedure, 95 publications were selected for our review. Database searches of SCOPUS, Science Direct, Web of Science and Google Scholar were performed using the following search terms: biomonitoring, pollution, moss, moss-bac, metals, nitrogen, PAHs, persistent organic pollutants (POPs), urban, agriculture, country side, industrial, radionuclides, metals smelter.
Critical discussion of all basic bioindication methods based on the latest literature are elements of novelty. Thus, 50% of the publications used were from the last four years, and ‘historical’ publications from the previous century were also cited.
The selection of organisms bioindicators must be particularly careful and must meet many characteristics. The classic publications of Füreder and Reynolds [2003] and Gorovtsov et al. [2017] give a list of traits that must be met good bioindicators, most of which relate to the use of mosses:
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Taxonomic stability, easily recognised in the field by anyone;
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Relatively low sensitivity to pollution allowing to survive in conditions of moderate stress;
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Well-recognised conditions for growth and development;
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Numerous in various locations; and
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High capacity for quantification and standardisation, should show a consistent, increasing response.
Mosses are used in air pollution biomonitoring in three basic methods:
- (1)
Native mosses;
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Naturally growing mosses;
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Live mosses transplanted into the study area;
- (2)
Display of prepared dead dried moss.
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Rühling and Tyler [1968] pioneered the study of heavy metal accumulation in naturally growing mosses as indicators of air pollution. The earliest studies were conducted in Sweden [Rühling, Tyler 1968], Denmark [Pakarinen, Tolonen 1976], Finland [Makinen 1977], Norway [Steinnes 1977] and Poland [Grodzińska 1978]. Mosses are mainly used in the monitoring of air pollution with metals, but they can also be effective in assessing nitrogen deposition [Díaz-Álvarez et al. 2018].
The properties of mosses have made them dominant for many years in biomonitoring in basic academic and practical research [Markert et al. 2020]. Advantages of using native mosses in bioindication of air pollution:
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Mosses are used as bioindicators of complex contamination: wet and dry deposition, which facilitates the assessment of total contamination [Markert et al. 2003; Aničić et al. 2009];
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Mosses take up water and minerals but also air pollutants almost exclusively from the air. Only minimal amounts of these components are taken up by some species from the soil [Ruchling, Tyler 1970; Jiang et al. 2018];
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Metals are practically not translocated inside the plant due to the lack of conductive tissues. transport of minerals between segments is limited [Schillin, Lehman 2002; Dragovič, Mihailovič 2009];
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strong correlation between pollutant deposition and accumulation in mosses [Macedo-Miranda et al. 2016; Oishi 2018];
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Very thin or even no cuticula, which results in easy transport of ions through the cell walls [Roberts et al. 2012];
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Extremely large surface area in relation to volume many times larger than in vascular plants [Adamo et al. 2007; Jiang et al. 2018];
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A relatively high tolerance of mosses to contamination [Itouga et al. 2017];
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Rapid development through repeated reproductive cycles through spores and vegetative fragments [Martin, Mallik 2017].
When using methods with mosses as bioindicators, one must remember that the measurements are not always precise. According to Bargagli [2016], the determination of Hg content in mosses cannot, however, be used to accurately determine atmospheric deposition, but only allows to locate Hg hot spots and changes in spatial distribution. An important issue is the methodological correctness of biomonitoring studies. Fernandez et al. [2015] evaluated 362 scientific publications discussing methodological and application studies of biomonitoring of metal deposition by mosses. The conclusions of these reviews indicated that most studies did not fully meet the criteria for valid scientific research. This fact does not undermine the desirability of conducting biomonitoring studies with mosses, but requires caution when formulating final conclusions.
Live mosses in biomonitoring are used as two methods (i) native growing mosses and (ii) transplanted from a slightly polluted site to a heavily polluted one. Table 2 presents examples of the use of native mosses in pollution biomonitoring in different regions of the world. In 1985 Rühling et al launched the international research project Survey of atmospheric heavy metal deposition in the Nordic countries in 1985 - monitored by moss analyses (1987), initially covering eight locations in seven countries (Denmark, Finland, Norway, Sweden, Greenland, Svalbard, Iceland and northern part of West Germany), with Iceland using mosses Hylocomium splendens and Pleurozium schreberi. The studies covered nine metals: As, Cd, Cr, Cu, Fe, Pb, Ni, V, Zn. In 2005/6, 27 European countries already participated in this programme and the research was extended by Al, Sb and N [Harmens et al. 2010]. After pilot studies in 2010, POP (PAHs, PCBs, PBDEs, PFOS and dioxins) studies were included in the program in 2015, in which 36 countries, including non-European countries, have already participated (Armenia, Azerbaijan, Canada, Georgia, Mongolia, Tajikistan, Vietnam) [Harmens et al. 2015; Frontasyeva et al. 2020].
Examples of the use of live mosses in biomonitoring of air pollution
| Air pollutant/deposition | Moss | Environment | Country | References |
|---|---|---|---|---|
| Native moss | ||||
| 8 elements | Hypnum cupressiforme | countryside | Albania | Qarri et al. 2019 |
| Fe, Cd, Cu, Pb, Zn | Hypnum cupressiforme | countryside | Albania | Lazo et al. 2022 |
| 37 elements | Multiple moss species | Pb-Zn smelter | Bułgaria | Hristozova et al. 2020 |
| 11 metals, N | Hylocomium splendens, Hypnum cupressiforme, Pseudoscleropodium purum | countryside | Europe, 15 countries | Harmens et al. 2015 |
| 12 metals | Grimmia pulvinata | cemeteries | France | Lequy et al. 2022 |
| 9 elements | Pseudocleropodium purum Hypnum cupressiforme | countryside | Kosowo | Maxhuni et al. 2016 |
| 6 elements | Pleurozium schreberi | countryside | Latvia | Tabors et al. 2023 |
| 35 elements | Hypnum cupressiforme | countryside | Moldova | Zinicovscaia et al. 2021 |
| Cr, Cu, Fe, Ni, Pb, V, Zn | Pleurozium schreberi, Scleropodium purum, Hypnum cupressiforme, Hylocomium splendens | countryside | Netherlands, Germany, Poland | Herpin et al. 1996 |
| 27 elements | Hypnum cupressiforme, Homalothecium lutescens, Homalothecium sericeum | countryside | North Macedonia | Barandovski et al. 2020 |
| Cd, Pb | Pleurozium schreberi | industrial | Poland | Dmuchowski et al. 2011a |
| S, δ34 S | Pleurozium schreberi | industrial | Poland | Kosior et al. 2015 |
| PAHs | Pleurozium schreberi | Industrial, | Poland | Godzik et al. 2014 |
| PBDEs, PCBs | Pleurozium schreberi | industrial | Poland | Kosior et al. 2017 |
| 17 elements | Pleurozium schreberi | countryside | Poland | Godzik 2020 |
| Cd, Cr, Cu, Fe, Ni, Pb | Pleurozium schreberi | urban | Russia | Yushin et al. 2020 |
| 34 elements | Pleurozium schreberi | urban | Russia | Vergel et al. 2022 |
| Pb isotopes, 7 metals | Hylocomium microphyllum | countryside | China | Zhou et al. 2021 |
| Radionuclides: 210Po,210Pb, 226Ra,7Be,40K,226Ra,238U,232T h,137Cs | Leptobryum pyriforme, Ditrichum pallidum, Hypnodendron reinwardtii | highway, urban, industrial | China | Zhong et al. 2019 |
| NO3− | Leskeella nervosa | urban | Japan | Liu et al. 2012 |
| Brachytheciun plumosum | mountain | |||
| Pb isotope ratios: 207Pb/206Pb,208Pb/206Pb | Calohypnum plumiforme | countryside | Japan | Oishi 2022 |
| Fe, Al | Calymperes afzelli, Acanthorrhynchium papillatum. | tropical forest | Malaysia | Baharuddin, Zuhairi 2021 |
| 30 elements | Barbula indica | urban | Vietnam | Doan Phan et al. 2018 |
| Cr, Zn, Cd, Pb | Fabriona ciliaris, Leskea angustata | countryside, urban parks | Mexico | Macedo-Miranda et al. 2016 |
| N compounds | Biaraun sp. | urban, oak forest | Mexico | Díaz-Álvarez et al. 2016 |
| 21 elements | Orthotrichum lyellii | industrial | USA | Jovan et al. 2021 |
| 22 elements | Orthotrichum lyellii | urban | USA | Comess et al. 2021 |
| PAHs | Orthotrichum lyellii | urban | USA | Jovan et al. 2022 |
| Live transplanted | ||||
| S, δ34 S | Pleurozium schreberi | industrial | Poland | Kosior, et al. 2015 |
| PBDEs, PCBs | Pleurozium schreberi | industrial | Poland | Kosior, et al. 2017 |
| 7 elements | Pleurozium schreberi | zinc smelter | Poland | Kaczmarek et al. 2017 |
| 17 elements | Sphagnum palustre | urban | Poland | Astel, et al. 2008 |
| survivability | Leucobryum glaucum | urban, forest | Malaysia | Yatim, Azman 2021 |
| 8 elements | Taxiphyllum giraldii, Thuidium sparsifolium | traffic | Nepal | Shakya et al., 2012 |
| 18 elements | moss | still mill | Nigeria | Olise et al. 2019 |
| Al, Fe, Mn, Pb, Zn | Rhacocarpus purpurascens, Sphagnum sp., Thuidium delicatulum | urban | Equator | Benítez et al. 2021 |
| As, Cd, Hg, Pb | Callicostella pallida, Versicularia versicularis, Isopterygium tenerum | traffic | Paraguay | Coronel-Teixeira et al. 2022 |
PAHs - Polycyclic aromatic hydrocarbons
PCBs - polychlorinated biphenyls
PBDEs - Polybrominated diphenyl ethers
Table 3 shows changes (in %) in the median value of elements contained in European mosses in the years 1990–2015 (100% content was assumed for 1990), developed on the basis of Frontasyev et al. [2020]. The largest changes were found in the Pb content in mosses in the years 1990–2015, a decrease of as much as 87%, which is related to the cessation of the use of leaded gasoline to drive cars. The smallest decrease was determined for N by only 1.5% and Hg by 2%. The reason for this reduction was: elimination of large industrial emission sources the change in technology to less emitting ones; the use of filters; the abandonment of leaded gasoline; the replacement of coal with other raw materials, such as gas; and the increasing dissemination of green energy [EEA 2019; Schröder et al. 2023]. The EMEP report draws attention to the decrease in emissions from European sources is accompanied by an increase in the share of non-European emissions and ground emissions from historical sources [Ilyin et al. 2016].
Changes in (in %) the value of the median of elements contained in European mosses in the years 1990–2015 (100% content in 1995) (based on Frontasyeva et al. 2020)
| Element | Median changes |
|---|---|
| Al | − 24* |
| An | − 38* |
| As | −13 |
| Cd | − 63 |
| Cr | − 24 |
| Cu | − 30 |
| Fe | − 22 |
| Pb | − 82 |
| Hg | − 2** |
| Ni | − 25 |
| V | − 57 |
| Zn | − 23 |
| N | − 1.5* |
− 2005–2015
− 1995–2015
Chaudhuri and Roy [2023] presented the contribution of individual species of mosses in the European Moss Survey Program in the study of metals: Pleurozium schreberi −39.6%, Hypnum cupressiforme −23.1%, Hylocomium splendens − 19.9%, Pseudoscleropodium purum 6.3%, and others − 11.2%. Mosses were used in the N studies: Pleurozium schreberi − 33.4%, Hypnum cupressiforme − 29.8%, Pseudoscleropodium purum −18%, Hylocomium splendens −13.1%, and other 5.6%.
Lee and Tallis [1973] determined the Pb content in mosses Hypnum cupressiforme from the botanical collection (herbarium) of the Manchester Museum in the years 1850–1900 and present (1972–1973) from an industrial region of Britain. They showed the highest values (> 200 ppm Pb) from the years 1850–1870 when there was a peak of metallurgical production. Roblin and Aherne [2020] proposed using mosses to assess microplastic air pollution. Research in Ireland has shown that determining the content of microplastics in moss is an effective method of assessing the risk of this dangerous and so far little recognised pollution.
Samecka-Cymerman et al. [2005] compared the content of elements in a heavily polluted area: in the moss Plagiothecium denticulatum transplanted from uncontaminated areas for 60 days with naturally growing moss. They found higher contents of N, P, K and Ca in the native moss than in the transplanted moss, which they explained by the possibility of increasing the loss of these elements in the transplanted moss. Kosior et al. [2015] compared the S content in Pleurozium schreberi mosses from heavily polluted rural, urban and industrial areas’ native moss with the transplanted from a relatively low-polluted control site. Native moss contained more S in rural and urban areas and less in industrial than the transplanted one. The conclusion of the study is that native moss is a more effective bioindicator in less polluted environments and worse in heavily polluted environments than transplanted.
The use of native mosses as biomonitors is a convenient way to determine the level of deposition of elements and other pollutants in the air. However, where samples of epiphytic mosses have been difficult to find at locations of interest, such as in urban and industrial areas, moss-bag methods has been employed as an option [Aničić et al. 2009; De Agostini et al. 2020]. Goodman and Roberts [1971] used the transplant method to assess air pollution in a heavily polluted area of Wales. The method involved moving moss (Hypnum cupressiforme) from a relatively unpolluted area to an industrial region. The method consisted in exposing a bag with moss coming from a ‘clean’ and a heavily polluted area for a certain period of time. After exposure, moss metal content was determined in the laboratory using standard physico-chemical methods. The moss-bag method uses the following features [Zechmeister et al. 2003; Aničić et al. 2009]:
The moss-bag method is based on the following properties of moss:
- -
Dry moss can absorb metals without significant limitations [Tavares, Vasconcelos 1996].
- -
The metal content in the moss exposed in the bag is proportional to its concentration in the air [Zechmeister et al. 2003; Aničić et al. 2009; Sang et al. 2021].
Sphagnum are characterised by the ability to efficiently absorb metals in tissues and therefore have found widespread use in moss-bag methods [Ares 2012; Shvetsova et al. 2019]. Figure 1 shows a moss bag prepared for exposure. The method of moss exposure in the form of moss bags is by far the most commonly used. However, other forms of exposure were used, such as moss mats [Ares 2012].
Figure 1.
Sang et al. [2021] compared two methods of using mosses Barbula indica in the assessment of air pollution with elements: moss bag and native moss. The results obtained by both methods gave a similar view of contamination. Native mosses accumulated more pollutants, but the moss-bag method enabled measurements in urban environments where native mosses did not occur or died during the summer drought. Świsłowski et al. [2022] assessed urban air pollution with seven metals (Cu, Zn, Cd, Pb, Mn, Fe, Hg), comparing three moss species: Dicranum polysetum, Pleurozium schreberi and Sphagnum fallax, as a moss bag and native moss transplants in boxes. Pleurozium schreberi was recommended as the best bioindicator accumulating the most and tested metals, and the moss-bag method was recommended for biomonitoring due to the much higher content of metals than native moss.
Figure 2 shows an exemplary application of the moss-bag method in the assessment of air pollution with chromium in the area of heavy pollution from the steel mill source. The use of this method made it possible to show changes in air pollution over a long period (15 years) based on a large number of measurement points and the same research material [Dmuchowski et al. 2011b]. Table 4 presents examples of the use of moss-bag methods in pollution biomonitoring in different regions of the world.
Figure 2.
Examples of application of the moss-bag method in biomonitoring of air pollution
| Air pollutant/deposition | Moss | Environment | Country | References |
|---|---|---|---|---|
| Pb | Hypnum cupressiforme | industrial | England | Goodman ans Roberts 1971 |
| Cd, Pb, Zn | Sphagnum fallax | urban | Poland | Dmuchowski and Bytnerowicz 2009 |
| 18 elements | Hypnum cupressiforme | industrial | Italy | Tretiach et al. 2011 |
| Cd, Pb | Sphagnum fallax | industrial | Poland | Dmuchowski et al. 2001a |
| Cd, Cr, Pb | Sphagnum fallax | still mill | Poland | Dmuchowski et al. 2011b |
| 19 elements | Hypnum cupressiforme | urban | Italy | Giordano et al. 2013 |
| Particulate matter | Sphagnum papillosum | industrial | Finland | Salo and Mäkinen 2014 |
| PAHs*, 39 elements | Hypnum cupressiforme | urban | Italy | Capozzi et al. 2016a |
| 10 elements | Pseudoscleropodium purum | agricultural, urban, industrial | Austria, Italy, Spain | Capozzi et al. 2016b |
| Sb, Cu, Cr | Sphagnum girgensohnii, Hypnum cupressiforme | urban | Serbia | Vuković et al. 2016 |
| 7 elements | Pleurozium ssp, Polytrichum ssp, Rhytidiadelphus ssp. | mining | Slovakia | Demková et al. 2017 |
| Particulate matter, 23 elements | Pseudoscleropodium purum | agricultural, urban, industrial | Austria, Italy, Spain | Di Palma et al. 2017 |
| 9 elements | Sphagnum fallax, Dicranum polysetum | urban | Poland | Świsłowski et al. 2022 |
| 134Cs, 137Cs | Hypnum cupressiforme, Hypnum plumaeforme | Fukushima breakdown | Japan | Di Palma et al. 2022 |
| 12 elements | Taxiphyllum taxirameum | agricultural, urban, traffic, industrial | China | Mao et el. 2022 |
| Microplastic | Pleurozium schreberi | urban, traffic. rural | Canada | Bertrim and Aherne 2023 |
| PAHs* | Hypnum plumaeforme | urban | Malysia | Hanifah and Sani 2023 |
| 35 elements | Hypnum cupressiforme, Sphagnum girgensohnii | urban, rural | Southeastern Europe, 10 countries | Urošević et al. 2023 |
PAHs - Polycyclic aromatic hydrocarbons
Bioindication methods can be an important element in environmental monitoring. The relatively low cost and the possibility of using a large number of measurement points make them a perfect complement to the instrumental methods. Methods using mosses as effective bioindicators are particularly recommended. It can be said that in recent years, moss research has dominated biomonitoring around the world. The advantage of mosses over other bioindicators is that they collect pollutants only from the air. These methods have been used in international research programmes. Other methods that have also found wide application is the method with prepared moss – ‘moss bag’. The moss exposed in the bags can be displayed in places where moss does not occur naturally, such as urban and industrial environments. Features of biomonitoring, such as the relative simplicity of all elements: collecting moss samples, simple and cheap technical equipment, no need to employ super specialists, easy interpretation of the results obtained. All these properties cause that the biomonitoring of elements will develop and increase the scale and geographical scope of research The significant value of information from biomonitoring can only be discussed when it is linked to databases on the environment, pollutant emissions, changes in ecosystems, living standards and health of the population. The development of analytical physicochemical methods and computer science will not eliminate bioindication methods, which will remain as a supplement to more advanced methods. A threat to the use of bioindication with mosses is not following strict methodologies. Over interpretation of results and drawing unauthorised conclusions may discourage the use of mosses in biomonitoring.