Botanical Journal of the Linnean Socie& (1990), 104: 267-280. With 3 figures

Terrestrial and aquatic bryophytes as monitors of environmental contaminants in urban and industrial habitats

M. AGNETA S. BURTON

Monitoring and Assessment Research Centre, King’s College London, The Old Coach House, Campden Hill, London W8 7 AD

BURTON, M. A. S., 1990. Terrestrial and aquatic bryophytes as monitors of contamination in urban and industrial habitats. The widespread distribution of bryophytes and the tolerance of many species to certain contaminants has led to their use for monitoring purposes. Early this century, changes in the distribution of mosses in urban habitats indicated deteriorating air quality; alterations in species composition in rivers has reflected changing water quality. The main focus in the past 10 to 20 years has been on measuring levels of contaminants in both terrestrial and aquatic bryophytes. Concentrations of metals, organic chemicals, radionuclides and derivatives of acidic gases have been widely reported in species from contaminated and background areas. More rarely, physiological and biochemical parameters are monitored. This paper describes the approaches which have been used and results obtained from monitoring bryophytes in urban and industrial habitats. Data are rwiewed from a range of countries illustrating the increasing interest in low cost methods for monitoring contamination.

ADDITIONAL KEYWORDS-Monitoring - pollution.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . Urban environments . . . . . . . . . . . . . . . . .

Species distribution . . . . . . . . . . . . . . . . Metal accumulation . . . . . . . . . . . . . . . .

Bryophytes in industrial areas . . . . . . . . . . . . . . . Power stations . . . . . . . . . . . . . . . . . Metal mines and smelters . . . . . . . . . . . . . . . Miscellaneous industrial sources . . . . . . . . . . . . . Monitoring with moss bags . . . . . . . . . . . . . . Historical monitoring . . . . . . . . . . . . . . . .

Conclusions . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . .

267 268 269 270 271 272 273 276 277 278 278 278

INTRODUCTION

Biological monitoring methods have become increasingly popular for investigating contamination of the environment. Although there are various interpretations of the term biological monitoring, the essential component is that changes can be measured in the organism(s) in response to changes in environmental conditions. Thus, the distribution of species in communities, measurements of growth rates and of concentrations of contaminants in

267 00244074/90/090267 + 14 $03.00/0 0 1990 The Linnean Society of London

268 M. A. S. BURTON

organisms can be included. The purposes of a monitoring programme need to be clearly defined in order to determine the most appropriate methods: for example, whether the main aim is to assess the state of contamination for regulatory purposes or for research into effects on organisms in natural communities and ecosystems. Direct physico-chemical measurements of environmental media can provide data for specified chemicals at a particular time and location; monitoring organisms in the environment provides information on their response to environmental factors as well as to levels of contamination. In addition, sampling can be carried out at low cost, on a large scale, and at remote localities where instrumental methods would be inappropriate.

Bryophytes in a very wide range of habitats have been extensively used in surveys of terrestrial and aquatic Contamination. Adverse effects on growth and metabolism can lead to changes in species distribution but may be difficult to attribute to contamination alone. The most detailed studies relate to areas with elevated metal concentrations and those affected by gaseous and other industrial emissions. The two main approaches for monitoring have been first, studies of species distribution and second, the chemical analysis of contaminants in bryophytes (Burton, 1986). Both can be used to compare the spatial distribution of contaminants in relation to sources and to investigate changes which occur with time.

The high accumulation capacity of bryophytes for contaminants has led to their use for monitoring regional and local patterns of deposition, of metals and radionuclides in particular. This review is concerned with monitoring around localized industrial emission sources and in urban areas. Although most data are from temperate regions in Europe and North America there are a few investigations in metal-contaminated habitats in tropical and in arctic environments.

In addition to monitoring using bryophytes growing in their natural habitats, transplants have been used and these studies are included in the relevant sections. Detailed investigations of accumulation and retention of contaminants by bryophytes have received considerable attention, particularly for metal pollutants in terrestrial habitats (Brown, 1982; Martin & Coughtrey, 1982). Other papers in this symposium (e.g. Tyler, 1990) have discussed attributes of bryophytes which have led to their use as monitors. The emphasis in this review is on illustrating the diverse situations where biological monitoring using bryophytes has been shown to be appropriate. The main concern has been to provide examples of results from the different approaches which can be applied in a routine manner for monitoring contamination.

URBAN ENVIRONMENTS

In urban areas, the major studies on bryophytes have measured changes in species distribution reflecting elevated sulphur dioxide (SO,) concentrations, and metal accumulation, chiefly of lead (Pb) emitted in vehicle exhausts from combustion of leaded petrol. Other contaminants will of course be emitted to the atmosphere as a result of burning fossil fuels for domestic and industrial purposes, from industries and from waste disposal facilities associated with urban areas.

BRYOPHYTES AS MONITORS OF CONTAMINATION 269

--

30 - 25 -

n

m .g 20- z: 0 15- - 0

z

10 -

5-

I I I I I 1 I I I

18 16 14 13 I I 10 8 6 5 3 2 centre Distance from city centre (km)

Figure 1 . Number of bryophytes at sites along an 18 km transect from Newcastle city centre (after Gilbert, 1968); 0, total; 0, asbestos roo& 0, grassland; W, sandstone walls.

Species distribution

Several surveys of bryophyte distribution have recorded the species present on brick and stone walls and roofs, of specified materials, at various distances from city centres. Bryum argenteum, Ceratodon purpureus and Tortula muralis have been reported at sites in the most polluted zones of cities in New Zealand (Daly, 1970), the Federal Republic of Germany (Wittenberger, 1975; Nordhorn-Richter & Dull, 1982) and in the U. K. (Gilbert, 1968). In the U.K. study, the total number of moss species was shown clearly to decrease towards the centre of Newcastle upon Tyne (Fig. 1). The decline corresponded to an increase in average winter SO, concentrations (Gilbert, 1968). Species able to survive in the areas with differing average SO, levels also have to tolerate the peak concentrations which occur periodically. The distribution is thus unlikely to be related entirely to average levels. For monitoring purposes, the disappearance of species, and in some instances reduction in percentage cover of individual species, are indications of higher levels of air pollution. Daly (1970) showed that the percentage cover of tolerant species may increase towards a city centre (Table 1). By contrast Hypnum cupressiforme, which is sensitive to SO,, declined from over 5% cover on tree trunks at 16 km to about 1% 5 km away and was absent at sites nearer to the city centre (Daly, 1970).

To provide a shorter-term study of sensitivity of species to urban pollution, transplants have been placed in city centres and their appearance monitored (Gilbert, 1968; Daly, 1970; Frahm, 1976). The degree of injury to transplanted species corresponded with field observations of the sensitivity of indigenous mosses. Injury to species transplanted to urban sites by Daly (1970) was assessed 10 weeks later. Ceratodon purpureus was little affected, whereas Hypnum cupressiJorme and Brachythecium spp., which are sensitive to SO, pollution, suffered severe

270 M. A. S. BURTON

TABLE 1. Percentage cover of mosses recorded in Christchurch city centre and along a 16 km transect (from Daly, 1970)

Percentage cover

Distance from city centre (krn)

Byurn Pohlia Ceratodon Tortula Hypnum argentnrm" Cdd purpureaf' muralif cupressiyormk

13-16 10-13 6-10 5-6 3-5 2-3 0-2

centre

0.5 0.9 0.1 1.3 2.6 4.3 I .3 3.0

1.3 6.0 0.1 1.3 0.6 3.5 1.6 6. I 3.2 9.6 3.7 5.2 1 . 1 6.3 2.7 4.6

7.5 5.5 6.0 3.2 7.4 1.6 7.4 1.3

13.2 15.1 0.2 20.6 10.2

:

'On stone walls; 'on tree trunks; *present, but negligible cover.

discolouration of the leaves. The main use of monitoring species distribution is thus based on the sensitivity of some species, and their absence at more polluted sites. The influence of other environmental factors, however, must also be borne in mind; habitat availability, the chemical composition of the substrate and climatic conditions all affect the distribution of species.

The use of de-icing salt on roads in winter may affect susceptible species of bryophytes. Contamination of a Sphagnum bog in Indiana, U.S.A. by sodium chloride stored at a roadside was followed by elimination of several Sphagnum species (Wilcox, 1984). Recolonization of the area by Sphagnum fimbriatum, when levels of sodium chloride had decreased, was attributed to the successful growth strategies of this species (Wilcox & Andrus, 1987). Other data on roadside bryophytes and salt-stress appear to be lacking.

Metal accumulation * By contrast with the previous section, monitoring metal accumulation in

bryophytes relies on species which tolerate a range of contaminant concentrations. Metal analysis has become a frequently used method of comparing contamination at roadsides, car parks and other urban sites and along transects towards the outskirts of cities. The method was first described by Riihling & Tyler (1968) who analysed lead (Pb) in mosses to monitor roadside pollution in Sweden. Subsequently there have been reports from many countries. In Ibadan, Nigeria, seventeen epiphytic moss species were analysed for metals (Onianwa & Egunyomi, 1983). The major interest was in Pb, present at high concentrations of 600-800 mg 1-', in petrol in Nigeria (almost twice the levels in the U.K. and U.S.A. at that time). Mean values for Pb were generally 5-10 fold higher in the city than at a reference site in the Botanical Garden. The maximum concentration of Pb, 248 pg g-', was in Calymperes palisotii at a city centre site: this contrasted with approximately 15 pg g-' at rural locations. However, no consistent relationship between Pb in bryophytes and the level of traffic was apparent. Zinc (Zn) was also markedly higher in bryophytes from some city areas but, together with copper (Cu), cadmium (Cd), nickel (Ni), iron

*All values are expressed on a dry weight basis unless stated otherwise.

BRYOPHYTES AS MONITORS OF CONTAMINATION 271

(Fe), manganese (Mn) and magnesium (Mg), concentrations were not obviously related to location.

Bryum argenteum, mentioned previously as being tolerant of elevated SO, levels, has been recommended for monitoring metal pollution on the basis of a survey in Frankfurt (Lotschert, Wandtner & Hiller, 1975). In car parks Pb concentrations in B. argenteum rose to 536 pg g-I, and values of 272 pg g-' in roadside samples with slow-moving traffic and < 100 pg g-' along roads with fast-moving traffic were recorded, Rhytidiadelphus squarrosus has also been examined at roadsides in urban habitats. Ruhling & Tyler (1968) for example, measured 20-30 pg g-' in non-roadside samples, compared with up to 680pg g-' within 10m of a roadside. In the Copenhagen area in Denmark, Andersen, Hovmand & Johnsen (1978) found that the Pb concentrations in R. squarroslls and Brachythecium rutabulum were high in densely populated areas with high traffic movements, as well as industrial areas, and were significantly correlated (P < 0.01) with concentrations in bulk deposition samples.

A comparison between species growing near roads in Warsaw, Polandled Rejment-Grochowska ( 1976) to suggest Atrichum undulatum as a sensitive biomonitor for metal pollution. At the least contaminated site, Pb concentrations in all species were approximately 100 pg g-'; at the roadside urban sites, values ranged between 230 and 425 pg g-', with the highest concentrations in A. undulatum. Elevated concentrations of Cu, Zn and Fe were also measured in samples from urban sites.

The capacity for high levels of accumulation has been attributed to the cation exchange capacity of the cell walls (Ruhling & Tyler, 1970). As pointed out by Brown (1982), particulate trapping may make a considerable contribution to the metals intercepted by mosses from atmospheric deposition. Some of the methods used and problems involved in cleaning bryophyte material prior to chemical analysis were discussed by Brown (1982) although cleaning is not appropriate when, for example, the aim is to estimate values for atmospheric deposition. The presence of Pb-containing granules within cells of roadside Rhytidiadelphus squarrosus was reported by Ophus & GullvAg (1974) indicating some passage of lead through the cell wall. There appear to be no investigations of whether the mosses in these highly contaminated habitats are urban races, as shown for Marchantia polymorbha growing at Pb-contaminated roadside sites in Glasgow (Briggs, 1972).

BRYOPHYTES IN INDUSTRIAL AREAS

Many surveys have been carried out on bryophytes in the vicinity of industrial point sources of contamination. The majority have been undertaken to determine the spatial distribution of contaminants. These may be at concentrations close to or below analytical detection limits in air or water, and accumulation in plants therefore facilitates the chemical analysis. Analysis of plants, in particular those which are not rooted in soil, such as the bryophytes (and lichens), can thus provide an indication of deposition patterns. More rarely, data from a sequence of time intervals have been reported to investigate changes in emission levels. Occasionally effects on bryophyte morphology, biochemistry or physiology are monitored, but these are more specialized studies suitable for detailed small-scale investigations only.

272 M. A. S. BURTON

Power stations

Levels of contaminants have been monitored in bryophytes around coal and peat-fired power stations and nuclear-powered facilities. The height of the chimneys clearly influences the dispersion of contaminants but transportation of fuel and waste materials contributes to very localized contamination. Folkeson ( 1981) monitored concentrations of metals in Pleurozium schreberi along transects from two peat-fired power plants in Finland, one burning 36000 m3 of peat per year, and the other, 2000 m3 per day. The fuel ash produced contributed to the very high concentrations of calcium close to the stack. There were significant ( P < O . O O l ) downward trends for Fe, chromium (Cr) and vanadium (V) with distance, the most rapid decline occurring within 0.5 km of the power stations. Dust from ash transportation was also considered to be a major source of beryllium and germanium found at high concentrations in Hylocomium splendens and Pleurozium schreberi from sites close to a coal-fired power station in Poland (Bramryd, 1981). Concentrations decreased with distance along a transect extending 33 km downwind of the source.

Studies have not been entirely limited to the pleurocarpous species. Also in Poland, Kwapulinski & Sarosiek (1988) monitored radionuclides ( 137Cs, 40K, 226Ra, 228Ra) in Polytrichum commune along 10 km transects from coal-fired power stations; they found a clear downward trend with distance, particularly marked for "'Ra and 228Ra which decreased from approximately 3000 and 800 mBq g-' respectively at a distance of 1 km, to 1000 and 200 mBq g-' at 10 km.

A detailed survey by Sumerling (1984) of radionuclides in samples of Pseudoscleropodium purum and Hypnum cupressiforme also showed a rapid fall-off with distance from the nuclear fuel reprocessing station at Sellafield in the U.K. Data from the survey were expressed as an activity ratio, 137Cs/2'0Pb to reduce the variability of the data which could result from differences in particulate trapping. The fairly uniformly distributed '"Pb was selected to reflect the retention of airborne particulates. A rapid decrease in the 137Cs/210Pb activity ratio from nearly 40 to 5 was evident in moss samples within 2 km of the source. The mean values of all the monitored radionuclides ("'Ru, '*'I, I3'Cs, 144Ce and 241Am) were significantly higher in mosses nearest to Sellafield compared with samples collected at sites beyond 2 km.

Effluents containing radionuclides from a nuclear power station in the Ardennes region of France were discharged into the River Meuse (Kirchmann & Lambinon, 1973) and aquatic mosses were found to be useful monitors. Cinclidotus danubicus was the most widely distributed species in the river and, following a known discharge of unusually high levels of radionuclides in effluents, correspondingly higher concentrations were measured in moss samples. Three years later, much lower levels were reported in samples from the same sites, as shown in Table 2 which also illustrates the higher accumulation capacity of C. danubicus compared with other plant samples (Lambinon, Kirchmann 8z Colard, 1976). In the U.K. Fonlinalis sp. has been used to monitor radionuclides in a freshwater lake receiving cooling and waste water from a nuclear power station (MAFF, 1967). Again, a temporal record showed much lower concentrations in Fontinalis 17 years after the first reports (Hunt, 1983), '%Ru for example had decreased from approximately 600mBq g-' to 4mBq g-' in Fontinalis exposed to effluents.

BRYOPHYTES AS MONITORS OF CONTAMINATION

TABLE 2. Mean radionuclide concentrations (mBq g-I fresh wt) in freshwater plants in the River Meuse at sampling times separated

by three years (from Lambinon, Kirchmann & Colard, 1976)

273

XMn 60& i S 4 a 1 3 7 a

Algae 1971 607 488 293 257 1974 103 69 106 158

Cinclidoius dnnubuus 1971 2791 1130 421" 343" 1974 123 40 1 2 0 54

C. nigricans 1971 1456 322 162 183 1974 47 75 1 3 0 103

Myriophyllum spicatum 1971 941 384 86 76 1974 35 13 8 17

"Data apparently for one sample only.

Metal mines and smelters

Numerous studies have been conducted on bryophytes in terrestrial and aquatic habitats which are affected by metals and gaseous emissions from smelters. The great majority of studies deal with metal concentrations in bryophytes in relation to distance from point sources; others have examined effects of gaseous emissions by monitoring visible damage to shoots of terrestrial species along transects from sources.

In Canada, emissions of metals and SO, from Cu-Ni smelters in Sudbury, Ontario have had major effects on the surrounding ecosystems. Concentrations of Cu and Ni in surface peat composed mainly of Sphagnum spp. were significantly correlated with distance from the smelter; a sharp decrease occurred within one or two km and a continuing decrease between 10 and 30 km was evident (Gignac & Beckett, 1986). The same trend (but at very low concentrations) was apparent in water samples collected below the peat at the same sites. At sites approximately 10 km from the smelter Cu and Ni concentrations in Sphagnum were around 500 pg g-' and in water around 0.1 pg ml-'. Some changes in species composition in the peatlands were also reported around Sudbury, with Sphagnum russowii the most abundant in the area (Gignac, 1987). The reduction in the extent and species diversity in Sphagnum bogs in the Pennines, U.K. which occurred after the Industrial Revolution has been attributed at least in part to SO, emissions from industries in the region (Ferguson, Lee & Bell, 1978).

In Manitoba, Canada, environmental monitoring around base metal smelters has yielded similar results. Zoltai (1988) reported an exponential decrease in Zn, Pb and Cu in surface peat with distance from the Flin-Flon smelter which had operated for 50 years. Levels of Zn in particular were very high within 5 km of the smelter (15 000 to 23 500 pg g-I). In the same area, Longton (1985) noted the absence of a feather moss layer within 17 km of the smelter compared with the area around a more recently established smelter, where shoots of Hylocomium splendens and Pleurozium schreberi were present but visibly damaged at distances of up to 15 km. Although metal emissions from the smelters were high, SO, was also released, and is likely to have been a major contributory factor to the damage to the bryophytes. Similar damage to mosses immediately downwind of

274 M. A. S. BURTON

an aluminium smelter emitting fluoride in Quebec, Canada occurred when Orthotrichum obtusifolium attached to tree bark was transplanted to sites around the smelter (Le Blanc, Comeau & Rao, 197 1) . Concentrations of fluoride in moss shoots were at a maximum, 600 pg g-', within 1 km and decreased to about 80 pg g-' 15 km away, four times the value at a background site.

Although the effects on bryophytes around smelters are generally considered to be due primarily to SO,, detailed studies at the Gusum brass foundry in Sweden, where emissions of acidic gases were negligible, suggested that observed adverse effects resulted from the high level of metal deposition. Hylocomium splendens, for example, which normally accounted for 20% of the ground cover, was eliminated or much reduced in cover close to the foundry, and the morphology of the shoots was affected (Folkeson, 1984). These effects were noticed first when Cu and Zn concentrations in the moss reached about 50 pg g-' and 190 pg g-' respectively. Much higher concentrations in this species have been reported elsewhere, without comments on its growth. Folkeson (1979) investigated the possibility of intercalibration of metal levels in different species found around the Gusum brass smelter. Close to the emission source different species, e.g. Pohlia nutans were recorded, compared with further away where pleurocarps such as Hylocomium splendens and Pleurozium schreberi were present. Folkeson (1979) suggested that if a relationship between the concentrations in different species could be established, the levels of contamination over the whole area could be mapped by calculating the levels in species not present at all sites. Such an exercise would, however, be applicable only in well-studied sites.

Many other monitoring studies have illustrated the rapid fall-off in concentrations of metals in terrestrial mosses with distance from sources of metal emissions, e.g. Fe and U from a uranium mine in Pleurozium schreberi and Polytrichum commune (Beckett et al., 1982); Fe from a steel factory in Hypnum cupressifDrme (Yule & Lloyd, 1984); Zn, Pb, Cd, Ni and Cu from smelters and steel works in H. cupressiforme (Goodman & Roberts, 1971); Zn, Pb and Cd from a smelter in Eurhynchium praelongum (Burkitt, Lester & Nickless, 1972).

Transplants of Dicranoweisia cirrata to sites extending to 2 150 m downwind from a steel factory in Denmark illustrated the accumulation of metals a t sites close to the emission source compared with pre-transplant levels over a finite time period of 214 days (Pilegaard, 1979). Concentrations of Zn, for example, increased from 123 pg g-' to 1941 pg g-'; Fe from 2120 to 26 200 pg g-'; Pb from 96 to 827 pg g-' and V from 9.6 to 19.3 pg g-'. These maximum concentrations were all recorded at a site 250 m from the factory.

Aquatic bryophytes have received increasing attention as monitors of metal contamination, particularly in mining areas, chiefly as a result of their high capacity for metal accumulation. Many widespread aquatic species appear to tolerate high concentrations of metals in rivers and streams. There is some indication that large inter-species differences in metal accumulation are more evident in small water courses such as mine streams with high levels of metals (McLean & Jones, 1975; Burton & Peterson, 1979) than in large water courses (Empain, 1976) where the levels are generally not as high, except a t points of industrial discharges.

The use of aquatic bryophytes for monitoring steady state and intermittent discharges of metals has been studied in considerable detail both in field and laboratory studies. Standardized methods have been published by Say &

BRYOPHYTES AS MONITORS OF CONTAMINATION

0. 10,000

h - '0,

3. - 1,000 t

32 8 8

0,

.g c

100 c C N

.-

- t I

- r 2 -0.64 P< 0.001

275

1 I I I 0.01 0. I 1.0

Zn in water (mg I-')

Figure 2. Zinc concentrations in river water and in shoot tips 01 the moss Rhychosfcgium rifiurioides (expressed on a dry weight basis) from streams and rivers in northern Engiand (after Wehr & Whitton, 1983).

Whitton (1983) and Wehr & Whitton (1983), who also gave consideration to predicting concentrations in mosses which would result from changes in metal input to the water and to factors such as pH and other chemical components which may affect metal accumulation (Wehr, Kelly & Whitton, 1987). Extensive surveys in the U.K. and Belgium have illustrated the close relationship between metal levels in bryophytes and in water samples, as shown for Zn in Rhynchostegium riparioides in Fig. 2. Data obtained by Empain (1976) for nine metals showed very close correspondence between the metal concentrations in water in the River Meuse and in Rhynchostegium riparioides, Cinclidotus danubicus and C. riparius. Industrial discharge points could be located by the marked changes in concentration in the mosses, whereas the concentrations in water samples were often very low and close to analytical detection limits. Peak concentrations of Zn and Cd in particular coincided in mosses and water samples. Zinc concentrations in C. danubicus ranged from approximately 1000 to 8000 pg g- ', where concentrations in water ranged from below determination to 500pg 1-'. Elevated Cd and Cr concentrations in the mosses were also coincidental with higher concentrations in the water. Metal concentrations in R . riparioides C . danubicus and Fontinalis antiP_yretica reflected the changes in discharge of Cu and Cr to a stream in the French Jura (Mouvet, Pattke & Cordebar, 1986). The high levels in the mosses indicated where the sources of metals were located, and had decreased when monitoring was repeated after discharges no longer occurred. Effluents containing high Cr concentrations from a tannery in Belgium were discharged to the River Amblive and monitored in Fontinalis antipyretica as well as in 'transplants' or moss bags (Mouvet, 1984). Concentrations of 1300 to 2000 pg g-' were recorded at four sampling times at the most polluted site, compared with 300 to 600pg g-' at sites 15 to 40 km away. The liverwort Scapania undulata has been used in several monitoring

276 M. A. S. BURTON

500 L

/-

1 Pb

10,000

Figure 3. Lead and zinc concentrations ( pg g-’ dry weight) in Scapania undulata from the Cwm Ystwyth area, Wales (data from Burton & Peterson, 1979).

programmes. Jones (1940) noted that the extensive bryophyte flora of the River Ystwyth in West Wales was severely reduced in the Pb-Zn mining areas and in places consisted only of occasional S. undulata. Metal analysis of S. undulata from this area by McLean & Jones (1975) and by Burton and Peterson (1979) demonstrated the accumulation of Pb and Zn in the vicinity of the by then long disused mines (Fig. 3). Significant correlations for Pb, Zn and Cd in S. UndUlaLa and in water (P <0.001) were recorded for samples from several European rivers (Whitton, Say & Jupp, 1982). The use of 1-3 cm shoot tips has been advocated for several species to avoid possible encrustations on older material and to provide an indication of recent or episodic pollution (Wehr ef al., 1983). Silver accumulation in S. undulutu was readily determined in the vicinity of disused mines in Wales (Jones, 1985) where concentrations in the water were close to detection limits.

Another widely distributed liverwort, Pellia endiviifolia growing in standing water beside disused Cu mines in Japan also accumulated high concentrations relative to the water (Satake, Nishikawa & Shibata, 1987) indicating its potential use for monitoring purposes.

Although bryophytes have been considered to provide an integrated value for the state of metal contamination in both terrestrial and aquatic habitats affected by industry, there is little information on the quantitative relationships with environmental levels particularly in terrestrial surveys. In aquatic habitats, factors affecting accumulation and loss need more study. For qualitative monitoring and for spatial distribution of metals, however, bryophytes provide a useful method for monitoring.

Miscellaneous induslrial sources

Little has been mentioned about organic chemicals as contaminants and few investigations have been carried out. Hypnum cupressifome accumulated the

BRYOPHYTES AS MONITORS OF CONTAMINATION 277

polyaromatic hydrocarbon, benzo(ghi)perylene near industrial towns in the F.R.G. (Thomas, 1979) and Finland (Herrmann & Hubner, 1984), where emissions from fossil fuel combustion would have been of a diffuse nature. Effluents discharged from an insecticide factory in France resulted in high accumulation of hexachlorocyclohexane (HCH) and polychlorinated biphenyls (PCBs) in Cinclidotus dunubicus (Mouvet, Galoux & Bernes, 1985). Other data on accumulation of organic chemicals appear to be limited to regional studies or to samples exposed to pesticide applications, and are not considered further.

Studies similar to those in SO2-polluted environments around metal smelters were conducted around a factory processing phosphorus rock containing fluoride, which resulted in emissions of HF and SiF, (Roberts, Thompson & Sidhu, 1979). Within 4 km of the source, severe damage to leaves of Polytrichum commune was evident and some injury was visible at a distance of 12 km. Pleurozium schreberi and Hylocomium splendens appeared more susceptible to injury, but where present, the degree of accumulation was similar. A clear fall-off in fluoride concentrations in P. commune shoots was recorded, decreasing from nearly 6000 pg g-' within 2 km of the source, to < 100 pg g-' at a site 12 km away.

Monitoring with moss bugs

The demonstrated high metal accumulation capacity of mosses has been utilized in several countries in surveys using moss bags. These consist of a mesh or grid generally made of nylon or plastic, containing moss shoots. The bags are then attached or suspended in some way for periods of days or weeks at suitable sites before collection and chemical analysis of the moss shoots. There are many variations both in size and shape of the bags, processing of moss shoots and habitats in which they have been utilized, The main purpose is to provide a defined time period for exposure of the moss to a pollution source. Advantages and disadvantages of the method have been discussed in some detail for terrestrial habitats by Goodman et ul. (1979) and Martin & Coughtrey (1982). Occasionally fresh moss shoots have been used, but in most cases moss shoots are not living; acid washing of Sphagnum for example reduces the initial metal concentrations and does not cause too much fragmentation of the material; peat moss, although used with success in some surveys, may become very fragmented and loss of material may occur during the exposure period. The method has proved most useful in industrial (Goodman & Roberts, 1971; Little & Martin, 1974) and urban areas (Duggan & Burton, 1983) where monitoring has been conducted along transects from point sources and at intervals during extended time periods. More recently, the method has been extended to aquatic habitats using freshly collected moss shoots enclosed in mesh bags or grids (Mouvet, 1984; Kelly, Girton & Whitton, 1987). Most moss bag surveys have been in metal- contaminated areas; more recently there have been attempts to monitor organic contaminants. Data obtained by Mouvet, Galoux & Bernes (1985) suggested that freshwater contamination resulting from discharges from an insecticide factory in France was reflected in accumulation of HCH and PCBs by Cinclidotus dunubiclls placed in plastic mesh grids (1 cm x 1 cm perforations) and sampled at three time intervals (up to 51 days). These preliminary studies indicated that spatial differences in contamination by organic contaminants could be detected.

278 M. A. S. BURTON

In terrestrial and aquatic habitats, moss-bag surveys can thus be carried out using one species which, particularly in highly contaminated habitats, may not be possible if relying on natural populations. Shoots of a standard age and from a habitat with a known level of contamination can be used and the changes monitored after a known period of time.

Historical monitoring Two approaches to examining the historical record of industrial pollution

using bryophyte material are mentioned briefly here, i.e. the chemical analysis of peat cores and of herbarium specimens. Both methods are based on the accumulation and retention of metals by mosses. Data published by Livett, Lee & Tallis (1979) for peat cores in the U.K., dated back to AD 1500 by pollen analysis, showed a sharp rise in Pb coinciding with the period of peak mining activity (between 1750 and 1900). In one example from Derbyshire levels increased from 100-200 pg g-' prior to the year 1700 to 600 pg g-' by the year 1800. After 1850, Pb levels decreased again. The interpretation of data for metals in peat cores in the U.K. and Scandinavia with regard to possible water table effects and mobility of elements within the peat profile has been discussed in some detail by Coleman (1985). I t appeared that at least qualitative information on trends in metal contamination levels could be gained by measuring concentrations in peat cores from industrialized areas.

Metal levels in herbarium specimens of Hypnum cupressiforme, Hylocomiurn splendens and Pleuroza'um schreberi from Sweden were compared with current samples from the same rural area (Ruhling & Tyler, 1968). The evident increases in Pb concentrations since the mid-19th century were attributed to industrial emissions resulting in an increase from 20 to 80 pg g-', and at a later stage, to the introduction of alkyl lead to petrol.

CONCLUSIONS

Measurements of changes in species distribution, and chemical analyses of contaminants, in bryophytes have been shown to reflect the state of environmental contamination. The major use of bryophytes in monitoring programmes has been based on their accumulation of, in particular, metals and radionuclides from industrial emissions or discharges to the atmosphere and water bodies. Thus the spatial distribution and temporal trends in environmental contaminants can be monitored in species growing in situ and in transplanted samples.

REFERENCES

ANDERSEN, A., HOVMAND, M. & JOHNSEN, I., 1978. Atmospheric heavy metal deposition in the Copenhagen area. Environmental Pollution, 17: 133-15 I .

BECKETT, P. J., BOILEAU, L. J. R., PADOVAN, D., RICHARDSON, D. H. S. & NIEBOER, E., 1982. Lichens and mosses as monitors of industrial activity associated with uranium mining in Northern Ontario, Canada - Part 2: Distance dependent uranium and lead accumulation patterns. Environmental Pollution,

BRAMRYD, T., 1981. Environmental effects of heavy metals distributed from power plants. Silva Fennica, 15

BRIGGS, D., 1972. Population differentiation in Marchanth polymorpha L. in various lead pollution levels.

( B ) 4: 91-107.

(4): 450-456.

Nafure, 238: 166-167.

BRYOPHYTES AS MONITORS OF CONTAMINATION 2 79

BROWN, D. H., 1982. Mineral nutrition. In A. J. E. Smith (Ed.), Bryophyte Ecology: 383-444. London:

BURKITT, A., LESTER, P. L NICKLESS, G., 1972. Distribution of heavy metals in the vicinity of an

BURTON, M. A. S., 1986. Biological Monitoring. 'MARC Report 32, Monitoring and Assessment Research

BURTON, M. A. S. & PETERSON, P. J., 1979. Metal accumulation by aquatic bryophytes from polluted

COLEMAN, D. O., 1985. Peat. In Historical Monitoring. MARC Report 31, Ch. 3. Monitoring and Assessment

DALY, G. T., 1970. Bryophyte and lichen indicators of air pollution in Christchurrh, New Zealand. Proreedings

DUGGAN, M. J. & BURTON, M. A. S., 1983. Atmospheric metal deposition in London. International Journal

EMPAIN, A,, 1976. Les bryophytes aquatiques utilists comme traceurs de la contamination en mttaux lourds

FERGUSON, P., LEE, J. A. & BELL, J. N. B., 1978. EKects of sulphur pollutants on the growth of Sphagnum

FOLKESON, L., 1979. Interspecies calibration of heavy-metal concentrations in nine mosses and lichens

FOLKESON, L., 1981. Heavy-metal accumulation in the moss Pleurozium schreberi in the surroundings of two

FOLKESON, L., 1984. Deterioration of the moss and lichen vegetation in a forest polluted by heavy metals.

FRAHM, J. P., 1976. Transplantadonsversuche mit epigaischen Mooscn zur Eichung von Bioindikatoren fur

GILBERT, 0. L., 1968. Bryophytes as indicators of air pollution in the l'yne Valley. N e w f'hytologisl, 67:

GIGNAC, L. D., 1987. Ecological niche structure of Sphagnum along a pollution gradient near Sudbury,

GIGNAC, L. D. & BECKEW, P. J., 1986. The cffect of smelting operations on pcatlands ncar Sudbury,

GOODMAN, G. T. & ROBERTS, T, M., 1971. Plants and soils as indicators of metals in the air. Nature, 231:

GOODMAN, G. T., INSKIP, M. J., SMITH, S., PARRY, G. D. R. & BURTON, M. A. S., 1979. The use of moss-bags in aerosol monitoring. In C. Morales (Ed.), Saharan Dust, Scope 14. .John Wiley & Sons.

HERRMANN, R. & HUBNER, D., 1984. Concentrations of micropollutants (PAH, chlorinated hydrocarbons and trace metals) in the moss Hypnum cup~essz~orme in and around a small industrial town in Southern Finland. Annales Rotanici Fennici, 21: 337-342.

HUNT, G. J., 1983. Radioactivip in Surjke and Coastal waters of the British Isles, 1981. Aquatic Environment Monitoring Report No. 9. Lowestoft, Suffolk: Ministry of Agriculture, Fisheries and Food.

JONES, J. R. E., 1940. A study of the zinc-polluted River Ystwyth in North Cardiganshire, Wales. Annals of Applied Biology, 27: 368-378.

JONES, K. C., 1985. Gold, silver and other elements in aquatic bryophytes from a mincralised area of North Wales, U.K. Journal of Geochemical Exploration, 24: 237-246.

KELLY, M. G., GIRTON, C. & WHITTON, B. A,, 1987. Use of moss bags for monitoring heavy metals in rivers. Water Research, 21: 1429-1435.

KIRCHMANN, R. & LAMBINON, J., 1973. Bioindicateurs vkgttaux de la contamination d'un cows d'eau par des effluents d'une centrale nucltaire it eau pressurike. (Evaluations des rejets de la Centrale de la SENA (Chooz, Ardennes FranGaises) au moyen des vegktaux aquatiques et ripicoles de la Meuse). Bulletin Sociiti Royale de Botanique de Belgique. 106: 187-20 1.

KWAPULINSKI, J. & SAROSIEK, J., 1988. Radioecotoxicological inhence of a power station determined by investigation of mosses. Science of the Total Environment, 68: 173-180.

LAMBINON, J., KIRCHMANN, R. & COLARD, J., 1976. Evolution rtcente de la contamination radioactive des kcosystkmes aquatique et ripicole de la Meuse par les ellluents de la Centrale nucltaire de la Sena (Chooz, Ardennes Fraqaises). Mbmoires Sociiti Royale de Botanique de Belgique, 7: 157-1 75.

LEBLANC, F., COMEAU, G . & RAO, D. N., 1971. Fluoride injury symptoms in epiphytic lichens and mosses. Canadian Journal of Botany, 49: 1691-1698.

LITTLE, P. & MARTIN, M. H., 1974. Biological monitoring of heavy metal pollution. Environmental Pollution,

LIVETT, E. A., LEE, J. A. & TALLIS, J. H., 1979. Lead, zinc and copper analysis of British blanket peats. Journal of Ecology, 67: 865-891.

LONGTON, R. E., 1985. Reproductive biolagy and susceptibility to air pollution in Pleurozium schreberi (Brid.) Mitt. (Musri) with particular reference to Manitoba, Canada. Monographs in QJftenzatic Botany from the Missouri Botanical Garden, 11: 51-69.

Chapman & Hall.

industrial complex. Nature, 238: 327-328.

Centre, King's College London, University of London.

mine streams. Environmental Pollution, 19: 39-46.

Research Centre, King's College London, University of London.

of the New zealand Ecological Socieu, 17: 70-79.

of Environmenlal Studies, 21: 301-307.

des eaux douces. Memoires Socidtd Royale de Botanique de Belgique, 7: 141- 156.

species. Environmental Pollution, 16: 15 1-161.

applicability to deposition measurements. Water, Air and Soil Pollulion, 11: 253-260.

peat-fired power plants in Finland. Annales Botanin' Fennici, 18: 245-253.

Ambio, 13: 37-39.

die Luftverschmutzung. Natur und Landschajl, 51: 19-22.

15-30.

Ontario, Canada. Canadian Journal of Botany, 65: 1268-1274.

Ontario. Canadian Joumal of Botany, 64: 1138-1 147.

287-292.

6: 1-9.

280 M. A. S. BURTON

LUTSCHERT, W., WANDTNER, R. & HILLER, H., 1975. Schwermetallanreicherung bei Boden-mocwen in Immissionsgebieten. Berich& d m Deuischen Bolmzischcn Gesellschq& 88: 419-431.

M.A.F.F., 1967. Radioactivio in smfie and coastal watns gthe British Isles. Report FRL I. Lowestoft, Suffok Ministry of Agriculture, Fisheries and Food.

MARTIN, M. H. & COUGHTREY, P. J., 1982. Biological Monitming of H e a y Metal Pollution, Lmnd and Air. London: Applied Science Publishers.

MCLEAN, R. 0. & JONES, A. K., 1975. Studies of tolerance to heavy metals in the flora of the rivers Ystwyth and Clarach, Wales. Frcshwotcr Biology, 5: 431444.

MOUVET, C., 1984. Accumulation of chromium and copper by the aquatic moss Fontinalis antipyreiica L. ex Hedw. transplanted in a metal-contaminated river. Environmental Technology Lcthrs, 5 : 541-548.

MOUVET, C., GALOUX, M. & BERNES, A., 1985. Monitoring of polychlorinated biphenyls (PCBs) and hexachlorocyclohexanes (HCH) in freshwater using the aquatic moss Cinclidotus danubicus. Science of the Total Enmronmenl, 44: 253-267.

MOUVET, C., PATTEE, E. & CORDEBAR, P., 1986. Utilisation des mousses aquatiques pour I’identification et la localisation prtcise des sources de pollution mttallique multiforme. Acta Oecologica Oecologica Ap#icata, 7: 77-91.

NORDHORN-RICHTER, C. & DULL, R., 1982. Monitoring air pollutants hy mapping the bryophyte flora. In L. Steubing & H.g. Jager (Eds), Monitoring o f A i r Polluhnis by Phis : 2%32. The Hague: Dr W. Junk.

ONIANWA, P. C. & EGUNYOMI, A., 1983. Trace metal levels in some Nigerian mosses used as indicators of atmospheric pollution. Environment01 Pollution (Series B), 5: 71-81.

OPHUS, E. M. & GULLVAG, B. M., 1974. Localization of lead within leaf cells of Rhyt&de~hus squarranrr (Hedw.) Wamt . by means of transmission electron microscopy and x-ray microanalysis. Cytobws, 10: 45-58.

PILEGAARD, K. 1979. Heavy metals in bulk precipitation and transplanted Hypogymnia p/ysodes and Dicranoweisia cinafa in the vicinity of a Danish steelworks. Water, Air and Soil Pollution, 11: 77-91.

REJMENT-GROCHOWSKA, I., 1976. Concentration of heavy metals, lead, iron, manganese, zinc and copper, in mosses. Journal of the Hattori Botanical Laboratory, 41: 225-230.

ROBERTS, B. A., THOMPSON, L. K. & SIDHU, S. S., 1979. Terrestrial bryophytes as indicators of fluoride emission from a phosphorus plant, Long Harbour, Newfoundland, Canada. Canadian Journal of Botany, 57: 1583-1 590.

RUHLING, A. & TYLER, G., 1968. An ecological approach to the lead problem. Botaniska iVoiiser, 121: 321-342.

RUHLING, A. & TYLER, G., 1970. Sorption and retention of heavy metals in the woodland moss Hylocomium splndns (Hedw.) Br. et. Sch. Oikos. 21: 92-97.

SATAKE, K., NISHIKAWA, M. & SHIBATA, K., 1987. Elemental composition of the sub-aquatic liver- wort Pcllia ndiviiforia (Dicks.) Dum. in relation to heavy metal contamination. H@obwlogia, 148: 131-136.

SAY, P. J. & WHITTON, B. A., 1983. Accumulation of heavy metals by aquatic mossw. 1. Fontidis antipyretics Hedw. Hydrobiologia, IW: 245-260.

SUMERLING, T. J., 1984. The use of mosses as indicators of airborne radionuclides near a major nuciear installation. Science of the Total Environment, 35: 25 1-265.

THOMAS, W., 1979. Monitoring organic and inorganic trace substances by epiphytic mosses - a regional pattern of air pollution. In D. D. Hemphill (Ed. ), Trace Substances in Environmental Health XZZZ: 285-289. Columbia: University of Missouri.

TYLER, G., 1990. Bryophytes and heavy metals. Botanical Journal of the Linnean Society, 104: 231-253. WEHR, J. D. & WHITTON, B. A., 1983. Accumulation of heavy metals by aquatic mosses. 2: Rhynchostegium

WEHR, J. D., KELLY, M. G. & WHITTON, B. A., 1987. Factors affecting accumulation and loss of zinc by

WEHR, J. D. EMPAIN, A., MOUVET, C., SAY, P. J. & WHITTON, B. A., 1983. Methods for processing

WHITTON, B. A., SAY, P. J. & JUPP, B. P., 1982. Accumulation of zinc, cadmium and lead by the aquatic

WILCOX, D. A,, 1984. The effects of NaCl deicing salts on Sphagnum recuruum P. Beauv. Environmental and

WILCOX, D. A. & ANDRUS, R. E., 1987. The role of Sphagnumjmbriatum in secondary succession in a road-

WITTENBERGER, G., 1975. Moose als mogliche Bioindikatoren fur Luftverschmutzung dargestellt am

YULE, F. A. & LLOYD, 0. L., 1984. An index of atmospheric pollution survey in Armadale, Central

ZOLTAI, S. C., 1988. Distribution of base metals in peat near a smelter at Flin Flon, Manitoba. Water, Air and

riparioides. Hydrobiologia, 100: 261-284.

the aquatic moss Rhyhostegium riparioides (Hedw.) C. Jens. Aquatic Botany, 29: 261-274.

aquatic mosses used as monitors of heavy metals. Water Research, 17: 985-992.

liverwort Scajmia. Environmenlol Pollution (SniCs B ) , 3: 299-3 16.

Experimental Botany, 24: 295-304.

salt impacted bog. Canadian Journal of Botany, 65: 2270-2275.

Beispiel von Offenbach am Main. Natur und Landschaft, 50: 143-145.

Scotland. Water, Air and Soil Pollution, 22: 27-45.

Soil Pollution, 37: 21 7-228.