Impacts of air pollution on Lichens and Bryophytes (mosses and liverworts)

Lichens

Characteristics and background

Lichens are composite organisms in which a single species of fungus (mycobiont) lives symbiotically with one or more algal species (phycobionts), some of which may be nitrogen (N) fixing (cyanolichens), e.g. members of the blue green algae. The fungus provides structure and protection for the algae which reciprocates, providing energy and assimilates, via photosynthesis. Many secondary metabolites are synthesised by the fungus, which are unique to lichen symbioses.

Lichens obtain almost all their nutrients from the atmosphere through uptake over their entire surface. They have no cuticle, nor means of controlling nutrient uptake, unlike vascular plants, and free exchange of both gases and solutions occurs across cell surfaces (Turetsky 2003). In addition their surface area to mass is very high and assimilatory capacity relatively low. Lichens are therefore highly susceptible to changes in atmospheric chemistry and deposition and for this reason provide very sensitive indicators of such changes.

Lichens exist in different growth forms. Three of these are:

  • leafy, circular lobes with root like structures (rhizines) where the algal matt is sandwiched between the fungus;
  • bushy / fruticose, shrub-like small mounds, growing up from the ground or beard-like, small tangles hanging down, attached to the substrate only at their bases, with a circular cross-section and a central algal core; or
  • crustose, closely adhering to the substrate, e.g. tree bark, stone, with the algae dispersed.

All but fruticose lichens grow slowly, with growth, about 0.5 to 5 mm y-1, measured by the expansion of their circles; fruticose lichens, grow vertically and quickly, up to 2 cm y-1. It is quite common for a lichen to have a lifespan of several centuries if left undisturbed and with a suitably long-lived substrate. In upland/alpine ecosystems, lichens represent a significant proportion of overall species richness and vegetation biomass. Lichens play an important role in ecosystem functions, e.g. biogeochemical cycling and carbon storage (Curtis et al 2005; Cornelissen et al 2007).

Pollutant Effects

Lichens are equivalent to an early warning ‘canary’ for chemically sensitive vascular plants. In Europe lichens have been used as sensitive bioindicators of air quality for more than a century. As with most vegetation, lichens show a range of sensitivities to pollutants. Not all lichens are sensitive to a particular pollutant, some can be remarkably tolerant. Among lichens are species that are sensitive to sulphur, nitrogen, acidity, halogens (e.g. fluoride), heavy metals and ozone.

SO2 and use of indicator species

As a consequence of industrialisation, many lichen species, e.g. Usnea articulate, have become extinct in large areas of lowland Britain. High SO2 concentrations were presumed to be the major cause, but habitat loss, particularly ancient woodland, has also led to reductions in some species. The most sensitive lichens are shrubby and leafy while the most tolerant lichens are crustose lichens. Since industrialisation, many of the shrubby and leafy lichens such as Ramalina, Usnea and Lobaria species have seen their ranges contract dramatically, often being confined to the parts of Britain with the cleanest air, e.g. northern and western Scotland, Devon and Cornwall. Some species of lichens have become more widely distributed than they were a century ago, such species tend to be more tolerant of acid conditions associated with SO2 deposition, e.g. some species of Bryoria, Parmeliopsis, Pseudevernia and Rinodina.

In the 1970s and 1980s, SO2 and fluoride pollution (local to some large sources, e.g. aluminium smelters) dominated air pollution chemistry (Bates and Farmer 1992). A lichen zone pattern has been described in large towns and cities or around industrial complexes corresponding to the mean levels of SO2 experienced (Hawksworth and Rose 1970). Particular species of lichen present on tree bark can indicate the typical SO2 levels. For example if there are no lichens present, the air quality is very poor, whilst generally only crusty lichens, i.e. Lecanora conizaeoides or Lepraria incana, can tolerate poor air quality in respect of SO2. In moderate to good air, leafy lichens such as Parmelia caperata or Evernia prunastri can survive and in areas where the air is very clean, rare species, e.g. Usnea articulata or Teloschistes flavicans, may grow. Chaenotheca chrysocephala, Cladonia digitata, Evernia prunastri, Lecanora pulicaris and Phlyctis argena are unlikely to be found where SO2 are high.  Now that SO2 concentrations are much lower many lichens are returning but they do not necessarily recolonise in the same magnitude or place, one of the reasons for this may be nitrogen pollutants (ref).

Nitrogen pollution/acidification

Lichens growing in remote, pristine environments can experience N limitation, especially fast growing species (Crittenden et al 1994). Lichens can use both forms of reactive N (NH4+ or NO3-) but uptake of nitrate appears to be restricted to the fungal part of the lichen (mycobiont) (Pavlova and Maslov 2005)

Long distance transport of nitrogenous air pollution is an important driver influencing the occurrence of acidophytic (acid loving) lichen species and constitutes a real threat to natural populations. Explanations of sensitivity to N compounds in acidophytes include:

  • increase in bark pH (caused by ammonia);
  • effects of NH4+ and or NO3- in precipitation;
  • eutrophication causing overgrowth of competing species, particularly algae, but also mosses and / or other N tolerant lichens.

Acid rain was often mentioned as a cause of the decline in (acid sensitive) Lobarion communities (Gilbert 1986). Lowering bark pH, a consequence of wet acidic deposition, however may not be the main driver of species composition change; some may be attributed to nitrogen (Farmer et al. 1992).

NH4+ in precipitation can have a negative effect on Bryoria capillaris, B. fuscescens, Imshaugia aleurites and Chaenotheca ferruginea causing it to all but disappear at < 1·0 mg N l-1. By contrast Lecanora pulicaris becomes more common above 1·0 mg N l-1. Two species, Cetraria pinastri and Usnea hirta, are particularly sensitive to NO3- at > 0.2 mg N l-1 (van Dobben et al 2001). Bryoria fuscescens, by contrast benefits from nitrate.

Evidence suggests that the concentration of N, particularly as ammonium, may be more important than the overall N dose (Britton and Fisher 2010). Although, in the longer-term, N load may become important due to N accumulation.

Epiphytic lichens as indicators of nitrogen air quality

Epiphytic lichens - those growing on trees (dead or alive) - have been widely studied with respect to pollutants (SO2, nitrogenous gases and acidity). Lichens growing on Atlantic Oak trees which grow in areas of high rainfall but relatively low levels of dry deposition (gaseous pollutants) appear to be highly N sensitive (Mitchell et al 2005). In Europe and the UK the lichen flora of oak trees growing in agricultural areas has changed from communities dominated by species preferring acid bark to species that tolerate and benefit from N (van Herk 1999; Lewis 2011). In the Netherlands high levels of ammonia have led to complete disappearance of acidophytic (acid preferring) species, resulting in communities dominated by nitrophytic species (van Herk 1999). Hypogymnia physodes showed a significant country-wide decrease in abundance (van Herk 2001), attributed to ammonia deposition causing the bark pH to increase. pHs of Quercus bark have been positively correlated with the NH3 concentration in air and have gone up by approximately two pH units at high NH3 levels in the Netherlands (van Herk 2001).

Recent research has identified lichens on oak and birch trees across the UK that are sensitive to, or tolerant of, increasing concentrations of gaseous nitrogenous pollutants. In the field, the response to increasing atmospheric N pollution can be measured by the decrease in N-sensitive lichen species and the increase in N-tolerant lichen species growing on the bark of these trees.

Impacts of nitrogen on Terricolous (ground living) lichens

The influence of applied N concentration and load on thallus chemistry and growth of five terricolous alpine lichen species was investigated in a three-month N addition study (Britton and Fisher 2010). Thresholds for effects observed in that study support a low critical load for terricolous lichen communities (<7.5 kg N ha-1y-1) and suggest that concentrations of N currently encountered in UK cloudwater may have detrimental effects on the growth of N sensitive species.

In heathlands and bogs some species of Cladonia have been shown to be very sensitive to reactive N deposition, particularly when the N deposits as gaseous ammonia. Because lichens naturally have quite low N status they are rather susceptible to ammonia deposition, which is taken up until concentrations within the algal cells and the outside reach equilibrium. In addition, many lichen thallii are quite acidic (pH 3-5) enhancing deposition of this alkaline gas. C. portentosa growing downwind of an ammonia source first developed a pink tinge which was reversible, then bleached, followed by greening, suggesting algal overgrowth and ultimately death.

Studies on lichens

Using the British Lichen Society’s database for 10 km hectads (10 km x 10 km square) the relationship between N pollution and presence of a range of lichens was examined for key semi-natural habitats (acid grassland, bog, heathland, calcareous grassland) allowing predictive modelling of responses to increasing N deposition. These results can be found in Stevens et al (2012).

Mosses

Characteristics and background

Mosses are simple plants both anatomically and morphologically. Growth in mosses is much less polarised than in vascular plants; dormancy or death of the growing point can stimulate buds further down the stem. Many mosses have root like structures, rhizoids and some mosses, like vascular plants, can be considered as calcifuges or calcicoles, favouring acid or calcareous conditions respectively. Mosses can grow in a range of habitats, even extreme with respect to climate and some species show remarkable tolerances to heavy metals, e.g. copper. These mosses trap and concentrate these metals, absorbing them both from the atmosphere and the substrate over their large surface area. Like lichens, mosses derive nutrients from atmospheric deposition but, by comparison with lichens, are less dependent on this nutrient source.

Pollutant Effects

Nitrogen pollution/acidification

Mosses are among the most sensitive components of the vegetation with respect to pollutant deposition, and can be sensitive to both acidity and N, which dominate today’s anthropogenic deposition. Like lichens, many mosses have become extinct from urban/ industrial environments, e.g. in the Lower Tyne valley. Too much N can change morphology, often leading to sparser mats that are desiccation prone and less efficient at suppressing competitors (e.g. Racomitrium lanuginosum, Armitage et al 2012:); photosynthesis can be compromised along with membrane integrity and sexual reproduction may also be suppressed.

Mosses play an important role in nutrient cycling; immobilization of N in some habitats, e.g. bogs and heathlands (Curtis et al 2005), effectively traps reactive N deposition preventing it from leaching into the pore water, making it unavailable to the roots of higher plants. However, the ability to sequester N depends on the N load and systems can soon be saturated. Some mosses including those growing on bogs, Sphagnum spp., have evolved ‘liaisons’ with N fixing microbes to supplement their N supply, reciprocating through the provision of carbon (Glime, 2007). In pristine environments where N deposition is very low, N fixation is a key source of N (NH4+).

Studies have identified both N sensitive and N tolerant mosses. Studies around ammonia impacted woodland have found Eurynchium praelongum and Brachythecium rutabulum tolerate very high tissue N concentrations at least to 4% (Leith et al 2005). Pleurozium schreberi has been shown to be N sensitive in several studies (Solga et al 2005; Sheppard et al 2014) and appear to have a threshold N concentration, benefiting from modest inputs that do not raise the N concentration above the threshold. Species within the important peatland genera Sphagnum show a range of tolerances to N; pool species appear to be the most tolerant, probably reflecting the lower ionic concentrations in these wet environments, while hummock formers are the most N sensitive. In situ N manipulation studies on S. capillifolium indicate that wet N doses above 24 kg N ha-1y-1 can damage this species and reduce its cover

Studies on mosses

The responses of mosses (and other bryophytes) growing in Atlantic oakwoods, a relatively pristine environment, to increased N deposition has been examined by Mitchell et al (2003; 2004; 2005). Hypnum cupressiforme (cypressleaved plait-moss) and Hypnum andoi (mamillate plait-moss) were relatively tolerant. Stevens et al (2011) used data from eight national vegetation datasets to look at acid grasslands, calcareous grasslands, heathlands, and bogs in the uplands and lowlands.

A European survey (Harmens et al., 2011) concluded that the N concentration in some common mosses, Pleurozium schreberi, Hylocomium splendens, correlated well with modelled N deposition. They recommended that these mosses could be used to provide reliable estimates of N deposition, providing a useful and relatively cheap methodology. However, interpretation of such data needs to take account of the form of N and the local climate. Deposition of reduced N, especially dry deposited NH3 causes the highest N concentrations in moss tissue, followed by wet reduced N and oxidised N. At high N doses wet reduced N leads to significantly higher N concentrations than oxidised N (Sheppard et al 2011). The European survey also measured herbarium specimens from across Europe and found that moss N concentrations started to increase noticeably from 1960.

References: 
Armitage, H.F. ; Britton, A.J.; Van der Wal, R.; Pearce, I.S.K. ; Thompson, D.B.A.; Woodin, S.J. 2012 Nitrogen deposition enhances moss growth but leads to an overall decline in habitat condition of mountain moss-sedge heath. Global Change Biology 18 290-300
Bates, J.W.; Farmer, (Eds) A.M. 1992 Bryophytes and Lichens in a Changing Environment.
Cornelissen, J.H.C. ; Lang, S.I. ; Soudzilovskaia, N.A. ; During, H.J. 2007 Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany 99 987-1001
Crittenden, P.D.; Kalucka, I. ; Oliver, E. 1994 Does nitrogen supply limit the growth of Antarctic lichens? Cryptogamic Botany 4 143-155
Curtis, C.J. ; Emmett, B.A.; Grant, H. ; Kernan, M.; Reynolds, B.; Shilland, E. 2005 Nitrogen saturation in UK moorlands: the critical role of bryophytes and lichens in determining retention of atmospheric N deposition. Journal of Applied Ecology 42 507-517
Farmer, A.M.; Bates, J.W.; Bell, J.N.B.; Bates, (Eds) J.W.; Farmer, (Eds) A.M. 1992 Ecophysiological effects of acid rain on bryophytes and lichens Bryophytes and lichens in a changing environment
Gilbert, O.L. 1986 Field evidence for an acid rain effect on lichens Environmental Pollution 40 227-231
Harmens, H. ; Norris, D.A.; Cooper, D.M. ; Mills, G.; Steinnes, E. ; Kubin, E. ; Thoni, L. ; Aboal, J.R. ; Alber, R. ; Carballeira, A. ; Coskun, M. ; De Temmerman, L. ; Frolova, M. ; Frontasyeva, M. ; Gonzales-Miqueo, L. ; Jeran, Z. ; Leblond, S. ; Liiv, S. ; Mankovska, B. ; Pesch, R. ; Poikolainen, J. ; Ruhling, A. ; Santamaria, J.M. ; Simoneie, P. ; Schroder, W. ; Suchara, I. ; Yurukova, L. ; Zechmeister, H.G. 2011 Nitrogen concentrations in mosses indicate the spatial distribution of atmospheric nitrogen deposition in Europe. Environmental Pollution 159 2852-2860
Hawksworth, D.L.; Rose, F. 1970 Lichens as Pollution Monitors Studies in Biology (66)
Leith, I.; Dijk, N.; Pitcairn, C.E.R.; Wolseley, P.A.; Whitfield, C.P.; Sutton, M.A. 2005 Biomonitoring methods for assessing the impacts of nitrogen pollution: refinement and testing JNCC
Maslov, A.I. ; Pavlova, E.A. 2005 Simple Method for Fractionation of Parmelia sulcata Lichen Thalli Russian Journal of Plant Physiology 52 271-274
Mitchell, R.J. ; Truscott, A.M. ; Leith, I.D.; Cape, J.N. ; Dijk, N.; Tang, Y.S.; Fowler, D.; Sutton, M.A. 2004 Growth and tissue nitrogen of epiphytic Atlantic bryophytes: effects of increased and decreased atmospheric N deposition. Functional Ecology 18 322-329
Mitchell, R.J. ; Truscott, A.M. ; Leith, I.D.; Tang, Y.S.; Dijk, N.; Smith, R.I.; Sutton, M.A. 2003 Impact of atmospheric nitrogen deposition on epiphytes in Atlantic oakwoods.
Mitchell, R.; Truscot, A.; Leith, I.; Cape, J.; Dijk, N.; Tang, Y.; Fowler, D.; Sutton, M.A. 2005 A study of the epiphytic communities of Atlantic oak woods along an atmospheric nitrogen deposition gradient Journal of Ecology 93 482-492
Sheppard, L. J.; Leith, I. D.; Mizunuma, T. ; Leeson, S. ; Kivimaki, S. ; Cape, J. N.; Dijk, N.; Leaver, D. ; Sutton, M. A.; Fowler, D.; Van den Berg, L. J.L.; Crossley, A.; Field, C. ; Smart, S. 2014 Inertia in an ombrotrophic bog ecosystem in response to 9 years' realistic perturbation by wet deposition of nitrogen, separated by form. Global Change Biology 20 566-580
Sheppard, L.J.; Leith, I.D.; Mizunuma, T. ; Cape, J.N.; Crossley, A.; S., Leeson ; Sutton, M.A.; Fowler, D.; Dijk, N. 2011 Dry deposition of ammonia gas drives species change faster than wet deposition of ammonium ions: evidence from a long-term field manipulation Global Change Biology 17 (12) 3589-3607
Stevens, C.J.; Smart, S.M.; Henrys, P.A. ; Maskell, L.C. ; Crowe, A. ; Simkin, J. ; Cheffings, C.M. ; Whitfield, C. ; Gowing, D.J.G. ; Rowe, E.C. ; Dore, A.J.; Emmett, B.A. 2012 Terricolous lichens as indicators of nitrogen deposition: Evidence from national records. Ecological Indicators 20 196-203
Stevens, C.J.; Smart, S.M.; Henrys, P. ; Maskell, L.C. ; Walker, K.J. ; Preston, C.D.; Crowe, A. ; Rowe, E. ; Gowing, D.J.; Emmett, B.A. 2011 Collation of evidence of nitrogen impacts on vegetation in relation to UK biodiversity objectives
Turetsky, M.R. 2003 The Role of Bryophytes in Carbon and Nitrogen Cycling. The Bryologist 106 395-409
Van Dobben, H.J.; Wolterbeek, H.T.; Wamelink, G.W.W.; Ter Braak, C.J.F. 2001 Relationship between epiphytic lichens, trace elements and gaseous atmospheric pollutants Environmental Pollution 112 163-169