Environment International 66 (2014) 28–37

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Environment International journal homepage: www.elsevier.com/locate/envint

Review

Biomonitoring persistent organic pollutants in the atmosphere with mosses: Performance and application Qimei Wu, Xin Wang, Qixing Zhou ⁎ Key Laboratory of Pollution Processes and Environmental Criteria (Ministry of Education), College of Environmental Science and Engineering, Nankai University, Tianjin 300071, PR China

a r t i c l e

i n f o

Article history: Received 31 October 2013 Accepted 31 December 2013 Available online 8 February 2014 Keywords: Moss Biomonitoring Persistent organic pollutant (POP) Atmosphere

a b s t r a c t Persistent organic pollutants (POPs) have aroused environmentalists and public concerns due to their toxicity, bioaccumulation and persistency in the environment. However, monitoring atmospheric POPs using conventional instrumental methods is difficult and expensive, and POP levels in air samples represent an instantaneous value at a sampling time. Biomonitoring methods can overcome this limitation, because biomonitors can accumulate POPs, serve as long-term integrators of POPs and provide reliable information to assess the impact of pollutants on the biota and various ecosystems. Recently, mosses are increasingly employed to monitor atmospheric POPs. Mosses have been applied to indicate POP pollution levels in the remote continent of Antarctica, trace distribution of POPs in the vicinity of pollution sources, describe the spatial patterns at the regional scale, and monitor the changes in the pollution intensity along time. In the future, many aspects need to be improved and strengthened: (i) the relationship between the concentrations of POPs in mosses and in the atmosphere (different size particulates and vapor phases); and (ii) the application of biomonitoring with mosses in human health studies. © 2014 Elsevier Ltd. All rights reserved.

Contents 1. 2. 3. 4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . Atmospheric sources and fate of POPs in mosses . . . . . . . Moss species used as bioindicators of POPs . . . . . . . . . Application of mosses as biomonitors of atmospheric POPs . . 4.1. Biomonitoring of POP levels in remote areas . . . . . 4.2. Biomonitoring of the vicinity of pollution sources . . . 4.3. Regional biomonitoring of atmospheric POP pollution . 4.4. Temporal biomonitoring of atmospheric POP pollution 5. Disadvantages and future research recommendation . . . . . 6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . .

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1. Introduction In the process of industrial production, agricultural activity and daily life, many organic compounds were released into water, soil and atmospheric environment (Muir and Howard, 2006; Zhou and Huang, 2001). Organic pollutants, especially persistent organic pollutants (POPs), have aroused wide concerns because they are harmful to plants, animals, microorganisms and even people (Ciesielczuk et al., 2012; Zhou et al., ⁎ Corresponding author. E-mail address: [email protected] (Q. Zhou). 0160-4120/$ – see front matter © 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.envint.2013.12.021

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28 29 29 30 30 32 32 33 35 36 36 36

2004, 2008). POPs become a research focus in the environmental field for recent years due to the following characteristics: toxic effects, bioaccumulation, persistence, and prone to long-range atmospheric transport (Klanova et al., 2008; Lohmann et al., 2007; Nash, 2011). POPs are now globally distributed and detected in abiotic and biotic samples (Li et al., 2013; Zhou and Huang, 2001). In 1998, 16 substances were focused by the Aarhus Protocol on POPs of the Convention on Long-range Transboundary Air Pollution (UNECE, 1998). In the 2001 Stockholm convention, 12 POPs termed “dirty dozen” or ‘legacy’ POPs were listed as priority control chemicals (UNEP, 2001). Additional 9 POPs were added to the list of the Stockholm convention in 2009 (UNEP, 2009).

Q. Wu et al. / Environment International 66 (2014) 28–37

The aims of these two conventions are to eliminate and/or restrict the production and use of selected POPs. National and international environmental monitoring programs have continued to measure POPs since the 1970s (Muir and Howard, 2006). Once emitted into the atmosphere, POPs will be rapidly diluted by air. Thus, to monitor POP levels in the atmosphere using conventional instruments is difficult and expensive, and the concentrations of POPs in air samples represent an instantaneous value at a sampling time. Biomonitors can be used as passive collectors of POPs in the atmosphere without mechanical or electrical devices, serve as long-term integrators of POPs, and provide reliable information to assess the impact of pollutants on the biota and ecosystems (Carballeira et al., 2006; Ciesielczuk et al., 2012; Ratola et al., 2010). Biomonitoring can perform the highdensity sampling at virtually any desired spatial and temporal scales at low cost and permit the measurement of a wide range of pollutants (Ares et al., 2011; Cipro et al., 2011; De Nicola et al., 2013; P. Wang et al., 2012; Wappelhorst et al., 2000). In this sense, biomonitoring methods are more popular than conventional instrumental monitoring methods. Among bioindicators, mosses have been proved to be a useful tool for monitoring atmospheric pollution because of the following aspects. Firstly, mosses attained nutrients from the air rather than substrates because of lacking roots. Secondly, the outermost epidermal cells of mosses do not have a layer of waxy cutin compounds so that foliar cells are directly exposed to pollutants in the air. Thirdly, mosses showed tolerance and sensitivity to a wide range of pollutants, such as dioxin (Carballeira et al., 2006). Fourthly, the high ratio of surface to volume of moss tissues facilitates more accumulation of pollutants. Zilli et al. (1996) estimated that the surface area of 1.0 g mosses was about 1.6 m2. Fifthly, mosses can grow in various habitats all around the world, even in Antarctica characterized by drought and cold weather (Cannone et al., 2013; Peat et al., 2007). Sixthly, the growth rate of mosses was very slow, therefore the sampled naturally growing mosses may integrate information on accumulation of pollutants over a long time (Carballeira et al., 2006; Leblond et al., 2004; Mariussen et al., 2008a). In addition, transplants (moss bags) are better indicators for short-time monitoring about one month exposure to pollutants due to the low lipid content (b 1%) and total organic matter (b 5% of fresh weight) (Knulst et al., 1995). Because of abundance and wide distribution, special morphology structure and physiological features, mosses have been increasingly employed to monitor atmospheric POPs in recent years. In this review, the application of mosses to monitor POPs in the atmosphere is retrospected and commented. 2. Atmospheric sources and fate of POPs in mosses A primary basis for the validity of the use of mosses for atmospheric pollution monitoring is an assumption of insignificant contribution of organic pollutant levels in soil to the levels in the mosses. Theoretical input and output of POPs in mosses were presented in Fig. 1. The concentrations of PAHs, trace metals and chlorinated hydrocarbons in mosses were caused by different sources according to the statistical Sorption from preciptation

Sorption from the air Environmental factor

Physicochemical properties of POPs of interest

Moss

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models computed (Thomas, 1984). The concentrations of PAHs in mosses came from atmospheric particulates, trace metals in mosses were caused by bulk precipitation, and chlorinated hydrocarbons in mosses may be related with gaseous and particulate matters other than bulk precipitation. The content of PAHs in epiphytic mosses was mainly characterized by atmospheric particulate concentrations (Thomas, 1984). PAHs in mosses showed a similar distribution pattern as in atmospheric particulates (Liu et al., 2005). Skert et al. (2010) also demonstrated that the concentrations of PAHs in mosses had a significant correlation with those in particulate matters with the diameter lower than 10 μm. What's more, the assumption was also confirmed by the fact that the concentration of POPs in mosses was hardly correlated with that in soil (Borghini et al., 2005). According to the abovementioned results, POPs in mosses largely came from the atmosphere rather than the soil, and POPs in mosses showed a close correlation with those in the atmosphere. Compared with the mechanism of uptake, accumulation, elimination of heavy metals in mosses, there is limited knowledge about POPs. Keyte et al. (2009) investigated the foliar uptake and within-leaf migration of phenanthrene (PHE) by Hypnum cupressiforme using the two-photon excitation microscopy with autofluorescence. PHE entered rapidly into the cell walls of moss leaves because of lacking a cuticular layer considered as a barrier in the foliar uptake of organic chemicals. PHE entered into the cell walls was retained and accumulated within the cuticular matrix for a long time. After 288 h, PHE started to migrate from the cell walls across the cell membrane into the cytoplasm of adjacent cells. There were distinct differences in atmospheric uptake and within-leaf movement, storage and processing of semivolatile organic compounds (SVOCs) between vascular and nonvascular living plants. Schrenk and Steinberg (1998) reported mosses metabolized only small amounts of PHE, but POPs in mosses may be subjected to continuing photodegradation processes (Liu et al., 2005; Wild et al., 2005). Many factors can affect the air-vegetation transfer of POPs, including physicochemical properties of the compounds of interest, environmental factors and plant characteristics (Barber et al., 2004). Mosses are prone to accumulate high-molecular-weight PAHs, especially 4-ring and 5-ring PAHs (De Nicola et al., 2013; DoŁęgowska and Migaszewski, 2011; Liu et al., 2005). However, mosses had no obvious selectivity in capturing these organic compounds with the same molecular weights from the atmosphere (Liu et al., 2005). Temperature is an important factor affecting the accumulation of POPs in mosses. HCB and 4,4′-DDE showed a significant correlation between the log-transformed moss concentrations and the reciprocal of temperature (Borghini et al., 2005). Grimalt et al. (2004) also reported that the log-transformed OC concentrations showed a significant linear dependence from the reciprocal of temperature, independently of the origin of the compounds. The hydration state can affect POP concentrations in the tissue of mosses (Kylin and Bouwman, 2012). Kylin and his colleague reported the concentrations of α- and γ-HCH were 3–5 times higher in the hydrated Hylocomium splendens than in the desiccated material. Because of the influence of the prevailing wind, the concentrations of PAHs in mosses at the downwind side of the road were higher than those at the other side (De Nicola et al., 2013; Viskari et al., 1997). A forest cover (canopy) may reduce atmospheric deposition of POPs on the mosses (Ciesielczuk et al., 2012). The mosses growing in the dry pine forest Cladonio-Pinetum revealed higher mean concentrations of ∑16 PAHs than those growing the continental coniferous forest Querco-roboris-Pinetum (Agnieszka, 2007). This is perhaps attributed to less dense canopy enabled higher deposition of air pollutants on the forest floor.

Moss characteristic

3. Moss species used as bioindicators of POPs Degradation

Wash-off

Evaporation

Fig. 1. Theoretical input and output of POPs in mosses and their influencing factors.

The number of mosses as indicators of POPs was less than that as indicators of heavy metals (Ares et al., 2012). To the best of our knowledge, up to now about 24 kinds of mosses were used to monitor POPs

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Q. Wu et al. / Environment International 66 (2014) 28–37

in the atmosphere, but approximately 75% of the species have only been used on one occasion (Fig. 2). These mosses used as biomonitors can be divided into two types: pleurocarpous mosses and acrocarpous mosses. Pleurocarpous mosses (prostrate, matted and highly branched) often form large carpets almost totally insulated from soil, rocks and barkspollutants from substrates. Indigenous pleurocarpous mosses were often used to monitor atmospheric POPs over a long period of time. However, pleurocarpous mosses are sensitive to both chemical contamination and long-term dryness so that pleurocarpous moss species are rare or even completely absent in industrial and/or urban areas. Unlike pleurocarpous ones, acrocarpous mosses (erect, tufted and sparingly branched) are able to survive in relatively hostile environments. When pleurocarpous moss species are rare or even totally absent in studying regions, acrocarpous mosses can be used as alternative materials to monitor atmospheric POPs. Apart from indigenous mosses, transplanted mosses (moss bags) can be used to monitor atmospheric POPs even at the virtually any desired spatial. In the moss-bag method, the large quantities of suitable pleurocarpous moss species are collected from a clean-air area, then put into nylon mesh bags, and then hung at specific locations for monitoring atmospheric POPs. Because of wide distribution and abundance in Europe, the three mosses including Pleurozium schreberi, H. splendens and H. cupressiforme that belong to pleurocarpous mosses were especially recommended for monitoring atmospheric POPs in passive monitoring and active monitoring. The three species were also recommended for monitoring atmospheric deposition of heavy metals (Ares et al., 2012). But in Antarctica, Sanionia uncinata was usually selected to be the bioindicator.

4. Application of mosses as biomonitors of atmospheric POPs 4.1. Biomonitoring of POP levels in remote areas The remote continent of Antarctica is usually perceived as the symbol of the last great wilderness of the Earth, which is surrounded by the Southern Ocean. However, global warming, population growth and industrial development in countries of the southern hemisphere will increase the impact of POPs on the Antarctic environment (Bargagli, 2008). Nowadays, POPs were detected in biotic and abiotic samples in Antarctica, which have aroused scientists' concerns (Choi et al., 2008; Cipro et al., 2012; Klanova et al., 2008; Li et al., 2012a; P. Wang et al., 2012; Trumble et al., 2012). Since mosses are dominated in vegetation and easily collected, preserved and transported than snow and ice core samples, they are usually utilized as alternatives of polar snow and ice cores as indicators for assessing deposition of atmospheric pollutants (Bacci et al., 1986; Bargagli, 2008; Cipro et al., 2011; Focardi et al., 1991; Yogui et al., 2011). To our knowledge, Bacci et al. (1986) reported for the first time that some organochlorine compounds (OCs) were detected in moss and lichen samples from the Antarctic Peninsula. These materials could use as indicators of contamination levels in Antarctica. In the late 1986, a series of studies on using mosses to assess atmospheric POP pollution were conducted in Antarctica (Bacci et al., 1986; Borghini et al., 2005; Cabrerizo et al., 2012; Cipro et al., 2011; Focardi et al., 1991; P. Wang et al., 2012; Q. Wang et al., 2012; Yogui et al., 2011). Up to now, POPs detected in mosses included PCBz, HCB, α-HCH, γ-HCH, P,P′-DDE, Pleurozium schreberi Hylocomium splendens Hypnum cupressiforme Tortula muralis Dicranum scoparium Thamnobryum alopecurum Thuidium tamariscinum Pseudoscleropodium purum Leptodon smithii Rhacomitrium lanuginosum Sphagnum sp. Tortula muralis Sphagnum girgensohnii Isopterygium minutirameum Hypnum plumaeformae Bryum argenteum Pottia heimii Ceratodon purpureus Sanionia uncinata Brachytecium sp. Syntrichia princeps Bryum algens Drepanocladus uncinatus Andreaea regularis Bryum sp.

Frequency of use 1 2 3

4

5

Fig. 2. The moss species used as bioindicators of POPs and the frequency of use of each species.

Q. Wu et al. / Environment International 66 (2014) 28–37

P,P′-DDT, PCBs, PAHs and PBDEs (Table 1). The occurrence of POPs in mosses from Antarctica could indicate that POPs had already reached Antarctica. PCBs in moss samples from Antarctica were the dominant POPs, exhibiting values at least an order of magnitude higher than all other contaminants (Bacci et al., 1986; Borghini et al., 2005; Cipro et al., 2011, 2012). The results were similar to those reported using other plants in Antarctica (Cabrerizo et al., 2012). Many studies proved that low molecular weight PCB congener groups dominated in moss samples from Antarctica, which was consistent with those in the atmosphere of Antarctica (Bacci et al., 1986; Cabrerizo et al., 2012; Cipro et al., 2011; Li et al., 2012b; Montone et al., 2003; Q. Wang et al., 2012). Bacci et al. (1986) reported that Tri-CBs (60%), Tetra-CBs (25%), Penta-CBs (5%), Hexa-CBs (5%) and Hepa-CBs (2%) were found in moss samples from the Antarctic Peninsula. PCB-118, PCB-105 and PCB-77 accounted for 56% of the total dioxin-like PCBs (Q. Wang et al., 2012). However, in the study of Cipro et al. (2011), there was a prevalence of Tetra-, followed by Penta- and Tri-CBs, except for S. uncinate which had a balanced distribution (~ 20%) from Tri- through HexaCBs. The concentrations of PBDEs in mosses from King George Island and maritime Antarctica were reported for the first time by Yogui and Sericano (2008). The concentration of total PBDEs in mosses collected in Antarctica during 2005–2006 ranged from 319 to 1184 pg/g dry weight, with a mean concentration of 818 pg/g dry weight (101 ng/g lipid). The level of PBDEs in mosses collected from 2004 to 2005 was similar to that collected during 2005–2006 (Cipro et al., 2011; Yogui and Sericano, 2008; Yogui et al., 2011). However, the concentration of total PBDEs in mosses collected from 2009 to 2010 was an order of magnitude lower than that collected before 2009 (Cipro et al., 2011; P. Wang et al., 2012; Yogui and Sericano, 2008; Yogui et al., 2011). The congener pattern between Antarctic mosses and the penta-BDE mixture was similar, which suggested that PBDEs do not undergo major fractionation during their long-range transport to Antarctica (Cipro et al., 2011; Yogui and Sericano, 2008). Tetra-BDEs and Penta-BDEs accounted for 38% and 58% of the total PBDEs in mosses, respectively, which was consistent with the commercial formulation of Penta-BDE (24–38% TetraBDEs, 50–60% Penta-BDEs and 4–8% Hexa-BDEs) (de Wit, 2002; Yogui and Sericano, 2008). In the other study, Tetra-BDEs and Penta-BDEs in mosses represented over 90% of the total composition, and BDE-47 (tetrabrominated) and BDE-99 (pentabrominated) dominated the composition of mosses (Cipro et al., 2011). P. Wang et al. (2012) reported that BDE-47 was the major congener in all samples, accounting for about 30% of the total concentrations, followed by BDE-99 (20%). The

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presence of BDE-183 in mosses suggested that other technical formulations (e.g. Octa-BDE and Deca-BDE) had reached Antarctica as indicated by some researchers (P. Wang et al., 2012; Yogui and Sericano, 2008). The concentrations of PBDEs in mosses collected at sites near to and far away from the Brazilian scientific station were in range 319-1, 137 pg/g, 584-1, and 184 pg/g, respectively (Yogui and Sericano, 2008). There was no significant difference in the contamination levels near to and far from the Brazilian scientific station, which suggested that the long-range atmospheric transport was the primary source of PBDEs to King George Island (Yogui and Sericano, 2008). Although many studies already proved that the atmosphere was a major medium during long-range transport of POPs from pollution sources to Antarctica. However, the long-range transport of many SOCs in the atmosphere is limited, such as 1100–2500 km for BDE-47 and 500– 900 km for BDE-153 (Wania and Dugani, 2003), so that SOCs cannot reach Antarctica only by the atmosphere because the ocean covers approximately 80% of the southern hemisphere's surface. Based on the model simulations, Yogui et al. (2011) proposed that an ocean– atmosphere coupling may have played a role in the long-range transport of less volatile SOCs such as PBDEs to Antarctic. Apart from the long-range transport, scientific stations could be a potential source of POPs in Antarctica. Dioxin-like PCBs were widely distributed in Antarctic soil and mosses with the concentration of 2.23–27.2 pg/g in soil and 10.4–812 pg/g in mosses (Q. Wang et al., 2012). ∑12PCBs in mosses from the Ardley Island area and the Greatwall Station area were much higher than those in moss samples from other sites. Local contamination because of human activities at the research stations in these areas and animal activities might account for these higher concentrations (Q. Wang et al., 2012). α-HCB/γ-HCB rations and p,p′-DDE/p,p′-DDT could diagnose a “recent” arrival or an “old” arrival. In old formulations of HCH insecticides α-form highly predominated, but in recent years, products with more than 90% γ-isomer had been introduced. Therefore the predominance of γ-HCH in mosses collected in 1985 indicated a “recent” arrival to the Antarctica (Bacci et al., 1986). However, the concentrations of αHCH in mosses collected in 1988 and 1999 were higher than γ-HCH, suggesting an “old” arrival to the Antarctica (Borghini et al., 2005; Focardi et al., 1991). Because DDT is subject to microbial degradation to more stable and toxic metabolites such as p,p′-DDE, the ration of p, p′-DDE to p,p′-DDT has been used to distinguish the source of DDT. If the ratio of p,p′-DDE to p,p′-DDT is N 1, it reveals aged DDT, while the ratio b1 reveals fresh inputs. Mosses from Antarctica had always the

Table 1 The concentrations of POPs in mosses of Antarctica. Area

Species

Antarctic Peninsula

Bryum algens, Dreanocladus uncinatus, Andreaea regularis, Drepanocladus uncinatus Sanionia uncinata Bryum sp. Bryum argenteum, Pottia heimii, Ceratodon purpureus Sanionia uncinata Syntrichia princeps Brachytecium sp.

Antarctic Peninsula Kay Island Victoria Land

King George Island

King George Island

King George Island King George Island and Ardley Island Fildes Peninsula

PCBz (ng/g)

HCB (ng/g)

α-HCH (ng/g)

γ-HCH (ng/g)

P,P′-DDE (ng/g)

P,P′-DDT (ng/g)

PCBs (ng/g)

0.23 1.15 0.48 0.38

0.40 1.06 1.70 1.16

0.17 0.43–0.40

0.04 0.18–1.6

0.17 0.32 0.33 0.53 0.005–0.04 0.20 1.1–7.9

0.30 0.25 0.44 0.55

1.0–2.4

0.30 0.45 0.80 0.68 0.02–0.12 0.30 0.85–1.9

0.30 0.54–0.91

≤5 7 16 14 0.04–0.76 ≤5 23–34

18.6 16.8 15.7

893 718 276

0.81 1.06 0.78

∑HCH: 1.20 b0.18 b0.18

∑DDT: 1.62 1.73 1.22

Sanionia uncinata Syntrichia princeps Brachythecium sp. Sanionia uncinata Sanionia uncinata

404–745

Unidentified

10.4–812

PBDEs (pg/g)

Reference Bacci et al. (1986)

Cabrerizo et al. (2012) Focardi et al. (1991) Borghini et al. (2005)

Cipro et al. (2011)

1022 718 276 319–1184 6.54–36.7

Yogui et al. (2011)

Yogui and Sericano (2008) P. Wang et al. (2012) Q. Wang et al. (2012)

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ratio of p,p′-DDE to p,p′-DDT N1, indicating aged DDT, which is in accordance with ceasing production and used since the 1980s (Bacci et al., 1986; Borghini et al., 2005; Cabrerizo et al., 2012). 4.2. Biomonitoring of the vicinity of pollution sources Holoubek et al. (2000) measured the concentration of PAHs in H. cupressiforme collected in the Czech Republic at a regional background site in Kosetice, south Bohemia and two industrial sources. The ∑ PAH content in mosses ranged from b 0.30 to 4700 ng/g dry weight in the background site, with a mean value of 609 ng/g. The concentrations of the ∑ PAHs in mosses from two industrial sites were higher than those in the background site. The concentrations of the ∑ PAHs in mosses varied between 229 to 10,222 ng/g (mean value 3060) in the industrial site near a factory producing PAH, carbon black and phthalates, and b0.30 to 16,730 ng/g (mean value 3670) in the other industrial site near a coal and gas fuel production plant in western Bohemia. Apart from the difference of the ∑PAHs, the dominant compounds in PAH mixture were different between the background site and the industrial sites. The main contamination levels in mosses decreased with the increasing distance from the factory within 15 km. Ares et al. (2009) also observed the similar results, and further demonstrated that the gradient of decreasing concentrations of PAHs (both at an individual level and for the sum of all the PAHs) in moss samples collected in industrial areas was an exponential type. Efficient and flexible transport systems play a vital role in boosting the development of the world's economy, and improving the quality of people's life. Nevertheless, road traffic can cause serious environment pollution, especially air pollution (Dierkes and Geiger, 1999; Kim et al., 2012; Omar et al., 2002). Environmental pollution generated from traffic has posed a threat to plants, animals, microorganisms and humans (Dan-Badjo et al., 2008). The increasing research should be focused on monitoring of pollutants on roadside. PAHs are an important type of essential components of road emissions with introducing lead-free gasoline. Viskari et al. (1997) used moss bag transplants to estimate deposition of PAHs generated from road traffic along a major highway in the central Finland. Because of the influence of the prevailing wind, the concentrations of PAHs in mosses were higher at the downwind side of the road than those at the other side, which was consistent with the study of De Nicola et al. (2013). Except for naphtalene (NAP), acenaphthylene (ACY) and acenapthene (ACE), the concentrations of the other PAHs decreased with the increasing distance from the highway. However, at 60–100 m from the highway the concentration of PAHs in moss samples were the same as that at the background level. In the study of Viskari (2000), the contents of PAHs in moss samples at the reference sites about 50 m from the roadside were the same to the background concentrations. Motor vehicles influence PAH concentrations in the atmosphere up to about 50 m of distance from the road. The study of Dan-Badjo et al. (2008) obtained the same results. The concentrations of PAHs in Ryegrass (Loium perenne) decreased significantly up to 60% from 0 to 50 m away from the road. Viskari (2000) reported the concentrations of the total PAHs in moss bags transplanted along the highway, the street and the local road in Finland were 403.9 ng/g, 299.6 ng/g, and 160.9 ng/g, respectively. The concentration of the total PAHs along three different types of road was related to daily traffic densities and speed limits. Compared with mosses at sites along roads, the highest level of PAHs (4100 ± 2458 μg/kg) was observed in mosses from a tunnel (Zechmeister et al., 2006). The study conducted by Zechmeister et al. (2006) proved that mosses are suitable indicators for monitoring traffic emissions in tunnels, especially for PAHs. Compared to the studies on the horizontal distribution of PAHs, there was limited study of vertical distribution. A clear vertical (3, 6 and 9 m) distribution gradient of PAHs and heavy metals in moss bags was not observed, therefore local air turbulences in the street canyon could contribute to uniform pollutant distribution at different heights (De Nicola et al., 2013).

Apart from industry and motor vehicles, there are other pollution sources that caused atmospheric POP pollution, such as wood combustion and tobacco smoking. Rantalainen et al. (1999) identified that indoor pollution was the main source of PAHs in villages in the Makwanpur region, Nepal based on the difference concentrations of PAHs in moss bags between indoor and outdoor. PAH diagnostic ratios are used as a tool for identifying and assessing pollution emission sources. The ratios are also applicable to PAHs determined in biomonitor organisms (Tobiszewski and Namieśnik, 2012). The ratios of PHE/ ANT and FLA/PYR in moss bags were 1.7–3.6 and 0.8–2.4, respectively, which revealed PAHs generated from the combustion origin. The result was consistent with the following aspects. The villages are situated in a remote area far from industry and mobile traffic, and no fossil fuels were in use except for rare petroleum fueled lamps. Wood combustion and tobacco smoking were the two major pollution sources. Ciesielczuk et al. (2012) used P. schreberi to evaluate the emission of PAHs at Polish cemeteries on the All Saints' Day. Naphthalene (NAP), PYR, benzo[b] fluoranthene (BBF) together with benzo[k]fluoranthene (BKF), benzo [g,h,i]perylene (BGP), indeno[1,2,3-cd]pyrene-(INP) and dibenzo[a,h] anthracene (DAH) in moss samples increased at the cemeteries. The concentrations of BKF + BBF in moss samples exposed at the cemeteries exceeded 50% of the total PAHs, which can be characteristic of emission from burning candles and candle lamps. 2-ring (except for NAP) and 3ring PAHs in mosses at the cemeteries located in the suburban areas may originated in the city center. The study of Carballeira et al. (2006) proved that mosses could accumulate dioxins and furans (PCDD/F), and were considered as good biomonitors for PCDD/F. The contents of total PCDD/F in Pseudoscleropodium purum varied between 9.6 and 442 pg/g. There was a rapid decline in PCDD/F levels with the distance: at 200 m from the landfill they contained more than 100 pg/g, while at 950 m the content decreased by 24 pg/g. The different concentrations of PCDD/F in mosses at different sites collected at the same distance from the pollution source and different directions showed that dispersal around the source was an anisotropic process. H. splendens collected in the vicinity of the lake Mjøsa was used to monitor atmospheric PBDE pollution (Mariussen et al., 2008a). The content of the lower brominated PBDE-congeners (BDE-28, -47, -66, -99, -100, -119, -153, -154, -183) in moss samples ranged from 74.3 to 4490 pg/g dry weight, presenting an apparent increasing trend from south towards north. There may be an active source of atmospheric PBDEs in the region of the northernmost parts of lake Mjøsa. However, BDE-183 ranged from 9.9 to 14.5 pg/g dry weight, and BDE-209 ranged from 452 to 1198 pg/g dry weight, with no spatial patterns. The distribution of POPs in the vicinity of different pollution sources was depicted in Fig. 3. The spatial distribution characteristics of POPs were different in the vicinity of different types of pollution sources. The polluted extent and polluted range of atmospheric POPs caused by industrial pollution sources were more serious and larger than other types of pollution sources. However, in general, the level of POPs in mosses decreased with the increasing distance from pollution sources. The characteristic of POP pollution gradients in polluted areas is an essential condition for implementing a method of identifying pollution sources at a small scale. 4.3. Regional biomonitoring of atmospheric POP pollution Concentrations of PAHs and chlorinated pesticide in mosses collected from the Federal Republic of Germany, Netherlands, Denmark, Norway and Iceland were measured (Thomas, 1986). The levels of PAHs in mosses had a marked decreased trend from the industrial centers in middle Europe to northern Europe and to the south of the Federal Republic of Germany. Fossil fuel combustion resulted in atmospheric pollution in these regions, but local sources can also be detected. In the study of Knulst et al. (1995), HCB, PCBs and PAHs in mosses had different distribution patterns in the region, and in the central Sweden. The concentration of HCB in mosses at the background sites was comparable

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33

Pollution source

Industry (PAHs)

Landfill (PCDD/F)

Unknown pollution sources (PBDE)

Motor vehicle (PAHs)

The POPs levels in mosses decreased with the increasing distance from pollution sources.

Wood and tobacco (in door) (PAHs)

The concentrations of PAHs in moss bags in door was higher than in outdoor.

Cemetery (PAHs)

The specific PAHs in mosses at cemeteries were higher than at reference sites.

Fig. 3. The distribution of POPs in the vicinity of different pollution sources.

with that at the sites around an expected source, and there was no remarkable difference in all sites in the central Sweden. The concentrations of ∑ 7PCB and PAHs in mosses presented a decline from the western part to the eastern part. Around an expected PCB source in the southeastern part of the region, the concentration of PCB declined with the increasing distance from the source area. Lead et al. (1996) reported that the levels of ∑PCBs and lower chlorinated homolog groups in mosses in 1977 were higher in southern and mid-Norwegian regions than those in northern regions. In southern and mid-Norwegian regions, more densely populated, more industrial activity and closer distance from possible European pollutant sources could account for the spatial pattern of PCBs. In Norway, the levels of the lower brominated PBDE-congeners in mosses showed a general decline towards the northern parts (Mariussen et al., 2008b). The same spatial pattern was found in herbivores. BDE-47 and -99 predominated in H. splendens samples collected in Norway, followed by BDE-100, -153 and -154 (Mariussen et al., 2008b). This was similar to the congener pattern in a technical Penta-mixture (Reistad et al., 2006). The high density of sampling sites can enable a complete assessment of the study area using geostatistical tools. In the study of Ares et al. (2011), 50 sampling sites were set in an area of the city of Santa Cruz de Tenerife (Canary Islands, Spain), and the sampling design was a regular grid of 400 × 400 m2. The deposition of PAHs in the area had been mapped on the base of the concentrations of PAHs in mosses. ANT, CHR and BBF + BJF presented the spatial pattern in an area of the city of Santa Cruz de Tenerife. Gerdol et al. (2002) studied atmospheric pollution in urban and rural sites in northern Italy based on the moss analysis. The level of low molecular weight volatile PAHs was higher in rural areas. However, the level of higher molecular weight PAHs was higher in urban areas. Neither the total PAHs nor the individual was correlated with trace metals and with δ15N, which revealed differences concerning both emission sources and atmospheric transport pathways. Foan et al. (2014) researched the concentrations of PAHs and N, C stable isotope signatures in mosses H. cupressiforme from 61 sites of 3 European regions. The average contents of PAHs in mosses in France and Switzerland were higher than those in Spain. The soil occupation (land-use types) can account for the spatial distribution of PAHs in three regions, including urban areas, farmland and forests. Atmospheric deposition of PAHs in Hungary was investigated by means of the concentrations of PAHs in H. cupressiforme collected at 29 sites distributed across Hungary (Ötvös et al., 2004). The concentrations of PAHs at these sites ranged from 0.1567 to 10.45 × 104 μg/kg, with a mean value of 1.87 × 104 μg/kg. Low molecular weight PAHs (up to 3 ring compounds) accounted for more than 99% of the total PAHs. The correlation between the total PAH concentrations and metal concentrations was not found, which revealed that PAHs and metals in regions had different emission sources and atmospheric transport pathways. The concentrations of PAHs at most of the sites in Hungary were correlated with the traffic volume (traffic vehicles per day in the

studied region), not for population. The reasonable relationship between PAHs and the traffic volume demonstrated that traffic sources were major pollution sources in Hungary. Road traffic is one of the most important sources of PAHs in urban centers. Ryszard (2002) used moss bags to estimate urban airborne PAHs. The concentrations of PAHs in 74 moss bags at 39 sites along 28 km of Warsaw main streets varied from 828 to 3573 ng/g dry weight. The spatial spread of PAHs was statistically close to the normal distribution with the mean value of 2332 ng/g. The concentration distribution of dominant compounds was uniform among all moss bags. PHE, fluoranthene (FLA) and pyrene (PYR) were the dominant compounds, and the relative contribution of these compounds was in a range 0.49–0.68 of the total PAH burden. Vehicle exhausts combined with the secondary source related to traffic could account for the uniformity of PAH distribution across the town. Atmospheric pollution by POPs in the Singapore region was estimated by the concentrations of these compounds in Isopterygium minutirameum collected from heavy industry area, undeveloped area, business district, nearby international airport and the National University (Lim et al., 2006). There were no significant spatial variations in the concentrations of OCPs and PCBs, which indicated that air masses moving over the island deposited OCPs and PCBs in a uniform pattern. Mosses from some sites were found to have a higher ration of p,p′DDT to p,p′-DDE, which suggested that p,p′-DDT continued to be deposited in Singapore despite its earlier ban in 1985. γ-HCH concentrations in all moss samples were below the detection limit, therefore there have been no recent inputs of HCH. Tarcau et al. (2013) measured the concentrations of OCPs, PCBs and PBDE in mosses collected from northeastern Romania (the region of Moldavia), but PCBs and PBDE were not detected in moss samples. The concentrations of HCB, HCHs and chlordanes were relatively uniform in mosses collected from the investigated areas, which suggested that the long-range air transport and deposition was their major sources. The high value of ∑DDT presented in mosses collected from the southern part of Moldavia because of the intense use of DDT in this region in the past. Studies on the spatial pattern of POPs at the regional scale in different countries were summarized in Table 2. These examples of monitoring POPs have clearly showed that mosses are useful tools to assess the levels of POPs with the high spatial resolution. The spatial patterns of POPs at the regional scale were mainly related to the distribution of local pollution sources and/or long-range sources, and also affected by different geomorphologic and climatic factors (Foan et al., 2014). 4.4. Temporal biomonitoring of atmospheric POP pollution Herbarium materials provide a sensitive tool to analyze temporal changes of atmospheric pollution. In Norway, there was a sharp decrease in ∑ PCB concentrations in mosses between 1977 and 1990, which was consistent with decreasing the use and manufacture of PCBs (Lead et al., 1996). Although in moderated pollution areas, the

34

Table 2 The spatial patterns of POPs at the regional scale in different countries. Moss species

Pollutant

Spatial distribution pattern

Pollution source

Reference

Hypnum cupressiforme Hylocomium splendens Rhacomitrium lanuginosum

PAHs

A marked gradient from the industrial centers in middle Europe to northern Europe as well as to the south of the Germany

Industrial activity

Thomas (1986)

A region (central Sweden)

Hylocomium splendens Pleurozium schreberi

BHC HCB

No spatial distribution, except one site nearby agricultural pesticide applicator No obvious difference of HCB between the background sites and the exposed sites

Local source and long-range source No local source

Thomas (1986) Knulst et al. (1995)

PCBs

Local source

Knulst et al. (1995)

Background contamination

Knulst et al. (1995)

PAHs

The different concentrations of PAHs in mosses from different sites

PAHs

Uniform distribution

OCPs, PCBs

Uniform distribution

Industrial emissions in Switzerland and road traffic emissions in Spain Densely populated, industrial activity and possible European pollutant sources Atmospheric transport, and possible European pollutant sources Various sources (motor vehicles, residential heating, industrial plants and waste incineration) Diffuse distribution of emission sources and long-range sources Vehicle exhausts combined with secondary sources related to traffics Long-range air transport and deposition

Foan et al. (2014)

PAHs

Minor variations of the PCB levels in mosses collected as background sites, high levels of PCB in mosses collected near an expected PCB source The highest PAH levels in mosses from the western part of the region, and declined towards the east The higher average contents of PAHs in mosses from France and Switzerland than from Spain The highest concentration of ∑PCBs and the lower PCBs found in mosses from southern and mid-Norwegian regions The decreasing levels of PBDEs in mosses from the southern to the northern parts of Norway A sharp differences in PAHs deposition levels between urban and rural areas

HCB, HCHs, Chlordanes

Uniform distribution

Long-range air transport and deposition

PAHs France, Spain and Switzerland Norway Norway Urban and rural sites (Northern Italy) Hungary Warsaw main street (Poland) Singapore North-eastern Romania

Hypnum cupressiforme Hylocomium splendens Hylocomium splendens Tortula muralis Hypnum cupressiforme Hylocomium splendens Isopterygium minutirameum Hypnum cupressiforme

PAHs PCBs PBDEs

Lead et al. (1996) Mariussen et al. (2008a, 2008b) Gerdol et al. (2002) Ötvös et al. (2004) Ryszard (2002) Lim et al. (2006) Tarcau et al. (2013)

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Study area Germany, Netherland, Danmark, Norway and Iceland

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levels of PCDD/F in P. purum showed a decline over time, which revealed that mosses were sensitive enough to detect temporal changes (Carballeira et al., 2006). Holoubek et al. (2007) studied the trends in background levels of POPs at the Kosetice observatory, Czech Republic, during the period 1996–2005. The results revealed that moss trending patterns resembled those of the ambient air, showing a slight decrease of PAHs, PCBs, DDTs and HCHs. Historical trends of PAH deposition in a remote area of Spain was reconstructed by herbarium materials in the study of Foan et al. (2010). The concentrations of 13 PAHs were 782.8–2009.6 ng/g in 1870–1881, 206.1–464.6 ng/g in 1973–1975, and 86.0–372.5 ng/g in 2006–2007. Total PAH contents decreased significantly between 1879–1881 and 1973–1975 but not between 1973–1975 and 2006–2007. All PAH concentrations significantly decreased in the mosses between 1879–1881 and 1973–1975 except for ANT and DAH which remained low. The significant decline of individual PAH concentrations between 1879–1881 and 1973–1975 was observed, because the disappearance of the charcoal pits and foundries at the end of the 19th century, combined with evolution of domestic heating towards less polluting systems during the 20th century. Only concentrations of the heavy PAHs significantly decreased between 1973–1975 and 2006–2007, which reflected that the implementation of the Aarhus Protocol (1988) played an important role in reducing the emission of selected PAHs. PHE was the highest of the PAH concentration, followed by FLA and PYR regardless of the moss age, whose concentrations were significantly correlated. During the 19th century, there were charcoal associated activities and wood stoves used to domestic heating in the area. Heavy traffic was predominant during the 20th and 21st centuries, which exhausted selected 3-ring PAHs (PHE, FLA and PYR) into the atmosphere. The temporal changes of POPs and their possible reasons were summarized in Fig. 4. In these examples, the levels of atmospheric POPs decreased over a period of time, which was related to the decrease in use and manufacture of POPs, the disappearance of pollution sources, enhanced fuel combustion, and the implementation of the Aarhus Protocol. As very useful tools to indicate the temporal development of atmospheric pollution, mosses can thus give reliable information to evaluate the effect of implementation of policies and measures. However, very few studies have conducted on temporal trends of atmospheric POPs, specially short-term changes or seasonal changes of atmospheric POPs.

Temporal biomonitoring

1977

PCDD/F Galicia (NW Spain)

2000

PCBs, PAHs, DDT and HCHs Kosetice observatory (Czech Republic) PAHs “Señorío (Estate) de Bertiz” Nature Reserve (Spain)

5. Disadvantages and future research recommendation Many literatures have demonstrated that POPs in mosses came mainly from the atmosphere. The flux of benzo(a)pyrene (BaP) to the ground surface was well correlated with its concentrations in mosses, which demonstrated mosses can be used for quantitative evaluation of BaP deposition (Milukaitė, 1998). The concentrations of selected PAHs in mosses had a liner relationship with those in rainwater and atmospheric particulates, taking the amount of precipitation into account in the studies of Thomas (1984, 1986). The concentration of PAHs in mosses was correlated with that in PM10 (Skert et al., 2010). Based on existing significant linear correlation between POP concentrations in mosses and in air, it was assumed that a calibration/translation between the two was feasible. Equations for translating the concentrations of POPs in mosses into equivalent ones for air will allow a broader use of mosses' information regarding atmospheric POPs in monitoring schemes and decision-making. However, a few studies had a direct relation for the concentrations of POPs in mosses with measured atmospheric concentrations, and considered meteorological parameters. In the future, studies on the relationship between POPs in mosses and in different size particulates and vapor phases in the atmosphere should be strengthened. Inhalation of air was one of the most important pathways of human exposure to pollutants. Atmospheric pollutants can cause acute and chronic effects for human health. Compared with conventional instrumental monitoring methods, biomonitoring methods can better reflect the exposure of the population because of the ability to perform the high-density sampling at virtually any desired spatial and temporal scales, the altitude of sampling sites closed to the human breathing zone and allowing the measurement of a wide range of pollutants. Therefore, the data from biomonitoring surveys can be used in epidemiological studies. Biomonitors were used to estimate human exposure to pollutants through inhalation, specially lichens and mosses (Augusto et al., 2012; Barber et al., 2004; Cislaghi and Nimis, 1997; Gailey and Lloyd, 1993; Wolterbeek, 2002; Wolterbeek and Verburg, 2004). The correlation between the concentrations of elements in biomonitors and epidemiological date on the incidence of diseases and mortality were found, which showed that those elements have negative impacts on human health (Carreras et al., 2009; Freitas and Martinho, 2011;

Decreased 74%

ΣPCB (Norway)

1996

35

Decreased 25% 1985

1990

A level decline 2002

2003

A slight level decrease 1998 …… 2004

2005

1997

Decreased 73% Decreased 48% 1870-1881 1973-1975

This reduction as indicative of the decrease in use of PCBs over this time period.

The cease of landfill in 2001.

The enhanced coal combustion in the local heating systems; and prohibition of PCBs, DDT and HCHs in Europe.

2006-2007

Fig. 4. The temporal changes of POPs and their possible reasons.

The disappearance of the pollution sources; evolution of domestic heating towards less polluting systems; and the implementation of the Aarhus Protocol (1988).

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Wappelhorst et al., 2000; Wolterbeek and Verburg, 2004). Figueira et al. (2007) used air deposition in mosses and water contamination to assess the exposure risk of human populations to As, and the result showed that the identified regions of accumulated water and atmospheric exposure were located in the inland north and central areas of Portugal. Augusto et al. (2007) reported that PCDD/F in lichens may be used as spatial estimators of the potential risk of inhalation by the population inhabited in the Setúbal peninsula, located in south Portugal. Augusto et al. (2012) also assessed human exposure to PAHs by data from lichens in a petrochemical region in Portugal, and calculated the health risks on the basis with the incremental lifetime cancer risk (ILCR). In the above case, the high spatial resolution of biomonitoring data was conducive to indentify critical areas where epidemiological health studies on local populations need to be focused, and where the levels of atmospheric pollutants need to be monitored over time for protecting human health. Biomonitoring played a vital role in assessing the exposure risk of human populations to POPs by inhalation. However, to our best knowledge, studies on using mosses to assess human exposure to atmospheric POPs were not reported. In the future, biomonitoring atmospheric POPs with mosses should be combined with human health. 6. Conclusions Many studies have proven that mosses are powerful tools for monitoring POPs in the atmosphere. An increasing volume of publications deals with the use of mosses as biomonitors of POPs. In the case of examples, mosses were used to: indicate POP pollution levels in the remote continent of Antarctica, trace distribution of POPs in the vicinity of pollution sources, describe spatial patterns at the regional scale and monitor changes in the pollution intensity along time. Although mosses have been employed to monitor POPs in many cases. In the future, many aspects need to be improved and strengthened: (i) the relationship between the concentrations of POPs in mosses and in the atmosphere; and (ii) the application of biomonitoring with mosses in human health studies. Acknowledgments This work was financially supported by the National Natural Science Foundation of China as a joint project (grant no. U1133006) and as a key project (grant no. 21037002), and by the Ministry of Science and Technology, People's Republic of China as a major project (grant no. 2013AA06A205). References Agnieszka G. Distribution patterns of PAHs and trace elements in mosses Hylocomium splendens (Hedw.) B.S.G. and Pleurozium schreberi (Brid.) Mitt. from different forest communities: a case study, south-central Poland. Chemosphere 2007;67(7): 1415–22. Ares Á, Aboal JR, Fernández JÁ, Real C, Carballeira A. Use of the terrestrial moss Pseudoscleropodium purum to detect sources of small scale contamination by PAHs. Atmos Environ 2009;43(34):5501–9. Ares Á, Fernández JÁ, Aboal JR, Carballeira A. Study of the air quality in industrial areas of Santa Cruz de Tenerife (Spain) by active biomonitoring with Pseudoscleropodium purum. Ecotoxicol Environ Saf 2011;74(3):533–41. Ares Á, Aboal JR, Carballeira A, Giordano S, Adamo P, Fernández JÁ. Moss bag biomonitoring: a methodological review. Sci Total Environ 2012;432:143–58. Augusto S, Pereira MJ, Soares A, Branquinho C. The contribution of environmental biomonitoring with lichens to assess human exposure to dioxins. Int J Hyg Environ Health 2007;210(3–4):433–8. Augusto S, Pereira MJ, Máguas C, Soares A, Branquinho C. Assessing human exposure to polycyclic aromatic hydrocarbons (PAH) in a petrochemical region utilizing data from environmental biomonitors. J Toxicol Environ Health A 2012;75(13–15): 819–30. Bacci E, Calamari D, Gaggi C, Fanelli R, Focardi S, Morosini M. Chlorinated hydrocarbons in lichen and moss samples from the Antarctic Peninsula. Chemosphere 1986;15(6): 747–54. Barber JL, Thomas GO, Kerstiens G, Jones KC. Current issues and uncertainties in the measurement and modelling of air-vegetation exchange and within-plant processing of POPs. Environ Pollut 2004;128(1–2):99–138.

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