Biological Journal of the Linnean Society, 2015, 115, 611–635. With 9 figures. Air pollution and its effects on lichens, bryophytes, and lichen-feeding Lepidoptera: review and evidence from biological records OLIVER L. PESCOTT1*, JANET M. SIMKIN2, TOM A. AUGUST1, ZOE RANDLE3, ANTHONY J. DORE4 and MARC S. BOTHAM1 1Centre for Ecology & Hydrology, Maclean Building, Benson Lane, Crowmarsh Gifford, Wallingford, Oxfordshire OX10 8BB, UK 2Department of Life Sciences, Natural History Museum, The British Lichen Society, c/o Lichen Herbarium, Cromwell Road, London SW7 5BD, UK 3Butterfly Conservation, Wareham, Dorset BH20 5QP, UK 4Centre for Ecology & Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK Received 12 January 2015; revised 24 February 2015; accepted for publication 27 February 2015 Changing air quality has been one of the most important drivers of change for bryophytes and lichens in Britain and Ireland over the 20th Century, with acidic pollutants such as sulphur dioxide having large effects on the ranges and abundances of many species. At the same time, expert amateur and professional naturalists have put enormous efforts into recording the distributions of species within these groups. These efforts have provided much evidence for declines and recoveries within the bryophytes and lichens, with species distribution data being linked to airborne pollutants in many different ways. We provide a broad overview of some of the changes that have occurred in affected species, using biological records collected by national recording schemes to illustrate the various effects of air pollution; we also review the direct and indirect impacts of air pollutants on these groups. Environmental change affecting one group of species is also likely to cascade to other groups where trophic or other relationships exist between them. Using data from the volunteer-based National Moth Recording Scheme, we provide the first evidence for an indirect association between reductions in air pollution and increases in lichenivorous moths. © 2015 The Linnean Society of London,Biological Journal of the Linnean Society, 2015, 115, 611–635. ADDITIONAL KEYWORDS: acidification – ammonia – bioindicators – citizen science – cryptogam – environmental change – nitrogen oxides – sulphur dioxide. AIR POLLUTION: A SHORT REVIEW on human health, particularly in the poorest areas of the world (Hill, 2010; UNEP, 2012); others, including Across the globe, both the extent and the impacts of nitrogen and sulphur deposition, impact ecosystem air pollution are highly variable (Hill, 2010). For some functioning, and may interact with physical changes, pollutants in some areas, the outlook is not positive, such as the warming of the Earth’s climate, to exac- and many currently detrimental trends are predicted erbate these effects (Millennium Ecosystem Assess- to continue or worsen (UNEP, 2007, 2012). These ment, 2005). The present review focuses on the impacts are also spread unevenly across species and impacts of a subset of air pollutants that have had, or ecosystems. Many pollutants, such as particulate are having, large impacts on the populations of liche- matter, heavy metals, and ozone, have severe impacts nized fungi, bryophytes, and associated Lepidoptera in Britain since the Industrial Revolution. The air pollutants that are addressed in the present *Corresponding author. E-mail: [email protected] review are sulphur dioxide (SO2), nitrogen oxides © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 611–635 611 612 O. L. PESCOTT ET AL. (NOx) and ammonia (NH3); the UK has committed to of pollutants such as SO2 in the UK, and the ongoing reducing its emissions of all these pollutants under recovery from these, may therefore be of use for the the European Union (EU) National Emissions Ceiling development of biological indicators of air pollution in Directive (Directive 2001/81/EC) and the 1999 the developing world (Nimis, Scheidegger & Wolseley, ‘Gothenburg Protocol’, which also currently includes 2002), and for a more general understanding of the several European non-EU member states, Canada changes that naturalists and ecologists in those coun- and the USA (http://www.unece.org/env/lrtap/). In the tries may be seeing in their natural environment, as UK, emissions of these pollutants have been declining well as being a fascinating and positive story of envi- (Fig. 1), although this is not the case for most devel- ronmental improvement in the UK. To more thor- oping countries (UNEP, 2012). The historical impacts oughly understand the past and future biological A) B) Figure 1. A, relative national trends in three air pollutants; data from Defra (2013). NOx and SO2 trends are relative to 1970; the NH3 trend is relative to 1980. B, historic SO2 trend in an urban centre (Westminster, London), redrawn from data presented in Rose & Hawksworth (1981). © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 611–635 LICHENS, BRYOPHYTES, MOTHS AND AIR QUALITY 613 impacts of the air pollutants under scrutiny, a brief were road transport (350 000 tonnes; approximately review of their physical forms, atmospheric chemistry, 34%) and energy production (315 000 tonnes; approxi- and emission sources is provided. mately 30%) (Defra, 2013). As will be noted from the above, many of the biological impacts of NOx are shared with SO2 (Hill, 2010), a point that should be SO2 borne in mind when using information on their preva- An acidic, corrosive gas that is a major air pollutant lence in correlative ecological analyses. Despite a around the world; historically, it has been, along with large decline in NOx emissions in the UK overall particulate matter, the main component of air pollu- (Fig. 1A) (Defra, 2013), roadside monitoring of the tion as a result of the burning of fossil fuels (WHO, levels of NO2 in London and other cities indicates that 2006). In the atmosphere, the gas SO2 is oxidized, there has been little decline in the emissions in the −2 through the intermediate sulphite ion stage (SO3 ), to urban environment over the recent past (UNEP, 2007; produce liquid sulphuric acid (H2SO4) and solid sul- Stedman & Grice, 2009; GLA, 2010). For example, the −2 phate (SO4 ) aerosols, the latter often through reac- World Health Organization’s limit value for harmful −3 tion with ammonia gas (NH3). It is these compounds effects on human health (40 μgm ; WHO, 2006) is that produce the acidifying effects of SO2; these may still regularly exceeded in these environments in the be realized through washout in rain (wet deposition), UK (RoTAP, 2012). or through direct, dry deposition onto surfaces (Hill, 2010). The aerial lifetime of the gas SO2 is estimated to be only of the order of a day; however, sulphuric NH3 acid and sulphate have much longer residence times Gaseous ammonia has a relatively short residence in the atmosphere, and it is these compounds that time in the atmosphere of the order of days (UNEP, produce many of the impacts on ecosystems and 2007) but, as with SO2 and NOx, it undergoes reac- + species through acidic deposition (Hill, 2010). tions yielding a more stable ion (ammonium, NH4 ) Sulphites can also be highly toxic to many that can form an aerosol. Reduced nitrogen can be cryptogamic (i.e. nonflowering) species (Lee & deposited in wet or dry forms, although the dry depo- Studholme, 1992), although these ions may largely be sition of reduced nitrogen is mostly in the gaseous generated on or within plants or lichens from depos- form, with ammonium aerosol deposition making a ited SO2. The main sources of SO2 in the UK in 2012 smaller contribution. Emissions of ammonia are were from burning in energy production and trans- dominated by the agricultural sector in the UK, par- formation (66%), followed by combustion in manufac- ticularly the management of manure (RoTAP, 2012); turing industries (14%; Defra, 2013; Salisbury et al., however, the contribution of agriculture to total emis- 2014; http://naei.defra.gov.uk/reports); the massive sions of NH3 has fallen slightly in recent years, from reduction in UK emissions from 1970 (6.37 million 89% in 2010 to 82% in 2012 (Fig. 1A) (RoTAP, 2012; tonnes) to 2012 (0.43 million tonnes; displayed in Defra, 2013). This is reported to be a result of reduc- relative terms in Fig. 1A) has mainly been driven by tions in cattle numbers and more efficient fertilizer a change in fuel use from coal to gas, and by the use (Defra, 2013). Because NH3 is primarily emitted fitting of flue gas desulphurization units in the power from diffuse sources, there is typically more uncer- industry (Defra, 2013). tainty around the measurement of emissions than for SO2 or NOx; however, the available data indicate that UK emissions peaked in the early 1980s, and have NOx decreased by approximately 20% subsequently The chemical symbol NOx represents the nitrogen (RoTAP, 2012; Defra, 2013). Point sources from pig oxides, a group of gases of which the most important and poultry farms can still have considerable impacts here are nitric oxide (NO) and nitrogen dioxide (NO2); on biodiversity locally (Leith et al., 2005) and, at the NO is converted rapidly into NO2 on exposure to air. landscape scale, there is much concern that many Nitrogen oxides can also be converted into nitrate ecosystems continue to be adversely affected across − (NO3 ) and nitric acid (HNO3) in the atmosphere, the UK (Leith et al., 2005). again forming aerosols that are significant compo- Other air pollutants of high importance globally nents of acid deposition (RoTAP, 2012). Both nitrate include ground-level (tropospheric) ozone and fine and nitric acid can also contribute to the eutrophica- particulate matter (Hill, 2010). Aerosols of all of the tion of certain sensitive habitats (RoTAP, 2012). As pollutants described above can contribute to particu- with oxides of sulphur, these derived aerosols of NOx late matter pollution of different sizes, which often have longer residence times in the atmosphere than present severe problems for human health (WHO, their precursor gases (UNEP, 2007).