Introduction

Salinization of soils is a growing threat to the future of agriculture in many parts of the world. Cultivation of arid and semi-arid land seems to be inevitably linked to salt accumulation; evaporation of water used for irrigation concentrates the dissolved salt and cultivation may compact the soil and cause retention of salts in the upper layers (Epstein et al., 1980). Hence, the understanding of the basic processes of salt tolerance and salt adaptation has important applied and environmental interests. An advantage of studying these processes in fungi is their experimental tractability, and the possibility of utilizing genetic approaches that are not available in other eukaryotic organisms.

Salt relations

Fungi occupy environments ranging from freshwater to cured food products and concentrated brines. Effects of increased salt concentration on fungal physiology are frequently explained in terms of the effects of a more general factor, the water potential (Ψ) of the environment. Often, this term has been used to describe the growth limits for a particular species below which growth does not occur. One should bear in mind though that the limiting value is not absolute, but depends on factors such as nutrition, temperature and the nature of the Ψ adjusting solute (Pitt & Hocking, 1977; Blomberg & Adler, 1992). The mycoflora of saline environments such as a salt marsh appears to differ little from that of more normal soils (Luard & Griffin, 1981).

Ozone (O3), ultra-violet (UV) radiation and climate change

The earth's atmosphere contains about 3 nl l-1 O3, that fraction being continuously turned over. Approximately 10% is dispersed in the troposphere, which extends 15 km above the ground, and 90% in the stratosphere, which extends up to 50 km. While man's activities are causing some increase in tropospheric O3, mainly around major urban areas, they are depleting stratospheric O3 on a global scale (Anon., 1993a,b). Depletion occurs because of the release of chlorine-containing compounds, such as chlorofluorocarbons and carbon tetrachloride, that promote O3 breakdown.

Solar radiation includes wavelengths as short as 200 nm but that below approximately 290 nm is absorbed in the atmosphere, mainly by O3. Since energy per quantum of radiation increases as wavelength decreases, O3 protects organisms from the most energy-rich, and potentially most damaging, wavelengths in solar radiation. The efficiency with which ozone absorbs UV decreases as wavelength increases, so progressive thinning of the O3 layer will allow shorter wavelengths to reach the earth's surface as well as allowing higher fluxes to be transmitted of the wavelengths already penetrating. It is significant that the cut-off wavelength is not constant but varies with season and time of day. For example, in Reading, England (51.5° N), the shortest detectable wavelength varied from 302 nm in January to 294 nm in July, and from 294 nm at noon to 300 nm at 17.00 hours in July (Anon., 1993b).

Introduction

Lichens have acquired a reputation as valuable monitors of environmental pollution. Pollution gradients have been related either to differential species sensitivity, creating characteristic floristic changes, or to the capacity of lichens to acquire and retain specific chemicals. These properties may be partly related to the nature of the lichen symbiosis and the structure of the resulting thallus. A brief review of lichen biology is provided to explain how the symbionts interact, what structural and physiological flexibility may exist and how far lichens react to the temporal and spatial heterogeneity of the natural, uncontaminated environment. Reference has been made to a number of valuable reviews that quote a wider literature.

Lichen biology

The lichen symbiosis consists of a fungal component, acting as the interface with the environment, and a photosynthetic component that is to a greater or lesser extent surrounded by the fungal tissues. Ascomycotina represent the main fungal group comprising the lichens, although Basidiomycotina and Deuteromycotina also occur frequently (Hawksworth, 1988a). More than 40% of the Ascomycotina are lichenized and some genera have both free-living and lichenized members. Whereas the photosynthetic component is usually either cyanobacterial or chlorophycean, thalli with both types of photobionts in different regions of the same thallus also occur (Hawksworth, 1988b; Tschermak-Woess, 1988). There is still doubt as to whether certain commonly lichenized chlorophycean algae, particularly the genus Trebouxia, exist in the free-living condition (Ahmadjian, 1993).

The ‘Environment’ is now on political agendas, and it is time the mycological voice was heard in the upsurge of national and international debates that have followed in the wake of the 1992 Earth Summit at Rio de Janeiro. Despite worldwide concern over environmental changes, fungi vital to the functioning of ecosystems are rarely mentioned.

This is the first symposium volume to focus on fungi in relation to man-made changes in the natural environment. It comprises papers presented at a British Mycological Society Symposium held at Cranfield University, UK, in 1994. The authors, all actively engaged in mycological research, cover widely diverse but highly topical subjects such as global warming, rising sea levels and destruction of rainforests. Speculation is bound to be found, but experimental evidence has been included wherever possible. Selection will also be apparent. The number of mycologists in this field is not great and many environmental problems remain untouched. Our aim is to stimulate thought on some of the issues of the day, and to point to the need for more research at every level, from field recording to cell physiology.

In Chapter 1 Lonsdale and Gibbs discuss predicted changes in global climate in relation to associations between fungal pathogens and perennial, woody hosts, and the extent to which the geographic range and pathogenic activity of the fungus (they do not always coincide) might alter.

One of the vital roles played by fungi in ecosystems lies in their being prime agents in the decomposition of plant material, thereby recycling nutrients (Swift, Heal & Anderson, 1979). It has been suggested that one insidious but important effect of pollution may be a reduction in the activity of decomposer communities (Ineson & Gray, 1980; Wookey, Ineson & Mansfield, 1991). Historically, the most significant atmospheric pollutant has been SO2, whose adverse effects on fungal decomposers are well documented (Magan, 1993, also Magan, Chapter 7). In the UK the trend is for SO2 to decline in importance as a pollutant (but see Boddy et al., Chapter 6) while tropospheric ozone and nitrogenous pollutants are increasing (UK Terrestrial Effects Review Group, 1988; UK Review Group on the Impact of Atmospheric Nitrogen, 1994). The effects of these latter two classes of pollutants on fungi are still largely unresearched.

There have been several reports of decomposer activity in litter being adversely affected by treatment with simulated acid precipitation in which pH was controlled by sulphuric acid (Brown, 1985; Skiba & Cresser, 1986). By contrast, ambient rainwater has a significant component of nitric acid, amounting to approximately 30% of total acidity (Warren Spring Laboratory, 1990). Nitrogen has long been known as a promoter of the decay of plant material by fungi (Garrett, 1963), and this additional pollutant load might be expected partially to offset deleterious effects due to sulphurous pollutants.

Introduction

Plant leaf surfaces (here termed the phyllosphere) are colonized by a wide range of bacteria, yeasts and filamentous fungi. They include epiphytic fungi, endophytes and pathogens. The total community and its structure are influenced by a range of abiotic and biotic factors. These include not just atmospheric pollutants but also wind, precipitation, water availability and pH. Microbial community structure may also be influenced by the presence of nutrients from insect honey dew, pollen, leaf exudates and organic debris. Interactions between abiotic and biotic factors can occur. For example, atmospheric pollutants have been demonstrated to markedly increase the weathering of conifer needle surfaces and to decrease the protective wax fibrillar structure (Rinallo et al., 1986), which could increase nutrient exudates in the phyllosphere and thus influence patterns of colonization and perhaps senescence of needles.

The impact of atmospheric pollutants on both epiphytic and endophytic fungi colonizing plant leaves has received increasing attention by being implicated directly or indirectly in ‘forest decline’ in parts of Europe where significant premature senescence and defoliation of forests occurred in the 1970s and 1980s (Boddy et al., this volume; Schutt & Cowling, 1985; Kandler, 1990). For example, Rehfuess and Rodenkirchen (1985) implicated the endophytes Lophodermium piceae and Rhizosphaera kalkhoffii in premature senescence and needle reddening disease. However, Butin and Wagner (1985) suggested that they may be only early colonizers of dying or dead needles and therefore not involved in such forest decline syndromes.

Introduction

Leaf material is an important primary energy source in many northern temperate streams and rivers (Bärlocher & Kendrick, 1981). It is utilized by various macroinvertebrates which may be classified in terms of their feeding biology. Coarse particulate organic matter (CPOM; particle size > 1 mm) is utilized by a group described as the ‘shredders’. These macroinvertebrates begin the incorporation of leaf material into the food web both by consumption and by producing fine particulate organic matter (FPOM), in the form of leaf fragments and faeces. FPOM (particle size < 1 mm) is utilized by a group of macroinvertebrates described as collectors. Both shredders and collectors are utilized by predators (Cummins, 1973; Anderson & Sedell, 1979).

The utilization of leaf material by shredders is therefore important to the community as a whole. Leaf material that has recently entered freshwaters is of low food quality for macroinvertebrates, as soluble compounds such as sugars and amino acids are rapidly leached into the surrounding waters. What remains after leaching are refractory compounds such as cellulose, pectins and lignin (Nykvist, 1962; Petersen & Cummins, 1974). When leaf material enters freshwater it is rapidly colonized by microorganisms and, especially in the early stages of decomposition, fungi dominate. Although some terrestrial fungi will be present on leaf material as it enters water, they are poorly adapted to conditions attained in temperate freshwaters and therefore do not persist (Bärlocher & Kendrick, 1974). In contrast, aquatic hyphomycetes are well adapted to the freshwater environment.

Introduction

The apparent decline, both in numbers of populations and in the geographical range, of macrofungi over several decades has aroused widespread concern in Europe. One demonstration of this is the publication of lists of species considered to be in danger of near-future extinction as a result of a complex of environmental changes. These Red Data Lists reflect this concern, both in size and composition of the lists of supposedly endangered species. Several European countries have produced such lists of endangered fungi: Austria (Krisai, 1986); the British Isles (Ing, 1992); Denmark (Vesterholt & Knudsen, 1990); Finland (Rassi et al., 1986); Germany (Benkert, 1982, 1993; Kreisel, 1992; Lettau, 1982; Runge, 1987; Schmitt, 1988; Winterhoff, 1984; Winterhoff & Krieglsteiner, 1984; Wöldecke, 1987); the Netherlands (Arnolds, 1989a); Norway (Bendiksen & Hølland, 1992); Poland (Wojewoda & Ławrinowicz, 1992) and Sweden (Ingelör, Thor & Hallingbäck, 1991). A provisional list for the whole of Europe has been offered by Ing (1993).

National lists differ in character, some reflecting local criteria based on the cultural importance of fungi rather than ecological priorities, and are necessarily parochial.

Composition of Red Lists

Species included in Red Lists are usually associated with ecosystems that are themselves endangered. In general, the majority are found in ancient woodland – both broad-leaved and coniferous, in unimproved grassland, in lowland bogs and sand dunes.

Introduction

The effects of environmental change on the sand-dune ecosystem do not have to be considered hypothetically; they can be observed. Sand dunes are, by definition, dynamic systems, being created, shaped, modified, sustained or eroded by continual changes in a wide range of abiotic and biotic environmental factors. The fungi which inhabit this coastal ecosystem are subject to, and are part of, those same changes. Frankland (1981) stated that ‘community life for a fungus is dynamic’. This is nowhere more true than in sand-dune habitats where the combination of a dynamic biological organism functioning in a dynamic resource system constitutes a veritable dynamic duo, capable of long-term survival and viability.

Climatic background

Sea levels along the British coastline have been fluctuating for thousands of years. Around 12000 B.P. they were 50 m lower on the Welsh coast (Savidge, 1983). Some 5000 years ago it would have been possible to cross the Straits of Dover from England to France on dry land (Zuckerman, 1986). Mean global sea-level has risen by about 10–15cm during the twentieth century (Robin, 1986). Yet sand dunes in various stages of development still occupy 9% of the coastline of mainland Britain (Ranwell & Boor, 1986), in the form of spit dunes, bay dunes, hindshore dunes, prograding dunes or offshore island dunes. They provide all the classic dune habitats for fungi: yellow and grey dune, dune slack, dune grassland, dune scrub and dune heath (Fig. 4.1).

Introduction

Hill and upland areas, defined as land typically above 150 m altitude, within designated agriculturally less favoured areas, and composed predominately of dwarf shrub heaths, grassland and peat bogs, make up more than one-third (5.8 M ha) of the total UK land surface (Ratcliffe & Thompson, 1988). Agriculture, in particular sheep farming, is the primary industry of such hill and upland areas, and its expansion over the last seven–eight centuries has resulted in the development of vast areas of sheep walk composed of indigenous Agrostis-Festuca, Nardus and Molinia dominant grassland. These indigenous grasslands or rough grazings presently constitute some 70% of the land within the hills and uplands (Newbould, 1985).

Traditionally, indigenous hill grasslands have been lightly grazed by pure bred sheep. Over the last few decades, however, intensities of sheep farming have increased dramatically, due largely to improvements in grassland productivity from use of fertilizer and lime. These agricultural improvements have caused considerable concern amongst conservationists, particularly for the loss of indigenous flora and fauna of the hills and uplands (Sydes & Miller, 1988; Bardgett & Marsden, 1992; Bardgett, Marsden & Howard, 1995). Recent changes in UK agricultural policy have reflected these concerns and addressed others, such as the overproduction of meat. Consequent reductions in financial subsidies based on output, and the introduction of monetary incentives for hill farmers to manage their land in such a way as to preserve or improve the environment (for example, environmentally sensitive areas) are likely to result in an overall reduction in liming and the use of fertilizer, and hence of the intensity of sheep grazing on upland grasslands.

Introduction

Once covered by seemingly limitless forest, tropical lands today suffer escalating deforestation to satisfy the food, fuel and fibre demands of burgeoning human populations. Although disease and inaccessibility long protected the humid tropics – those tropical regions where annual precipitation exceeds potential evapotranspiration – deforestation is now rampant. Year-round warm temperatures and an excess of precipitation combine to exacerbate decline of soil fertility after deforestation. Diminished fertility and unacceptably low productivity, in turn, lead to evermore land clearing, such that, except for highly inaccessible areas of rugged terrain, strict national parks, and forest reserves, little undisturbed forest will remain by the end of this century (see Myers, 1991).

Utilization and conversion of humid tropical forests produces an extreme range of vegetations from largely intact forest matrix disturbed only by extraction of a few valuable timber species to barren, abandoned wastelands. As the latter predominate, rehabilitation of these highly degraded lands becomes a necessity. ‘Rehabilitation’ is used here to indicate the return of productive capacity to degraded land. With some types of land use, diminished primary production may be a consequence of disruption of mycorrhizal associations. In such instances, rehabilitation requires restoration of mycorrhizas.

Introduction

Chaos theory, which strictly is only a subset of non-linear systems theory, deals with systems whose long-term behaviour or output is prone to be complex, irregular, sensitive to small changes in initial conditions and unpredictable at specific localities. Amongst several recent texts that have aimed to popularize the theory and describe its remarkable history, those by Gleick (1988) and Coveney & Highfield (1991) are perhaps the most accessible. More detailed sources of information concerning specifically biological applications of nonlinear theory are provided by Degn, Holden & Olsen (1987) and by Sleeman (1989).

The aim of this chapter is to promote appreciation of the ways in which non-linear dynamics can be expected to apply to fungal individuals, populations and communities. It will be argued that non-linear theory has more than just a place in environmental mycology; it provides a basis for understanding the complexity, interconnectedness and limits to the predictability of natural patterns of distribution and activity of fungi.

Throughout the discussion, the focus will be on understanding of the sources and ecological importance of non-linearity, rather than on rigorous mathematical treatment. At the outset, an attempt will be made to generalize about the kinds of process which underlie non-linear dynamics and the organizational properties that these processes give rise to. The mechanisms by which these processes operate at individual, population, community and sub-cellular levels of organization will then be considered and related to the ways that fungal systems respond to sources of environmental heterogeneity.

Sulphur pollution – past trends, current levels

Sulphur (S) is an essential element for the growth and activity of organisms, occuring free in abundant quantities. It is found in valence states ranging from +6 in sulphates to -2 in sulphides, the most stable state being S6+. Globally, natural emissions of S into the atmosphere from biogenic sources have been estimated to range between 78.9 and 142.6 Tg yr-1, of which 5.0 to 63.9 Tg yr-1 arises from land (Schlesinger, 1991; Andreae & Jaeschke, 1992; Germida, Wainwright & Gupta, 1992). Estimates of the relative significance of anthropogenic to natural sulphur emissions are variable, but globally the ratio is probably about 4: 1 (Möller, 1984), atmospheric S emissions from land being in the order: anthropogenic 93 Tg yr-1 > biogenic gases 22 > dust 20 > volcanoes 10 (Brimblecombe et al., 1989). Sulphur emissions to the atmosphere are not constant with time, having increased dramatically since the industrial revolution as a result of combustion of fossil fuels. Global anthropogenic emissions have increased from an estimated 5 Tg in 1860 to 180 Tg in 1985, with considerable increases predicted up to 2000 (Fig. 6.1; Möller, 1984; Schlesinger, 1991), despite electives by European countries to have reduced emissions by 1993 to 30% of 1980 emissions.

The mycorrhizal symbiosis

The rhizosphere and the surface of plant roots are inhabited by populations of several microorganisms. Among these populations, a group of filamentous fungi can be present quite consistently on the root surfaces or in the tissues or cells of the roots, so that dual organs of consistent morphological and histological patterns are formed (Harley, 1989). In these ‘mycorrhizas’ the fungus and the host co-exist actively for long periods in a state called a mutualistic symbiosis. Most plant species in the greater part of the world's ecosystems are infected with these mycorrhizal fungi (Harley & Smith, 1983; Harley & Harley, 1987, Janos, Chapter 10).

Under natural conditions the vast majority of the fungi involved in this association appear to be obligate symbionts, with little or no ability for independent growth. This seems to be less true for the autobionts. Their degree of mycorrhizal dependency is somewhat more variable. Some plant species are infected occasionally while most others (70% of the angiosperms according to Trappe, 1987) cannot complete their life cycles without mycorrhizas, at least in their natural environment. However, environmental factors as well as the presence of companion plants can determine whether a plant is mycotrophic or not in some settings (Miller, 1979; Molina, Massicotte & Trappe, 1992).

When I was first approached to write this book for the Studies in Biology series, I was delighted. As a student this series had a profound influence on me, and I was an avid reader of the books. They provided an easily affordable access to a very wide range of topics in biology, and I still use one or two books from my student days.

I was also very daunted at the prospect of writing such a short book to cover so vast a topic as microbiology. It is a subject that impinges on almost every aspect of human existence. To attempt to cover the whole of the subject would have been an impossible task. Consequently, some very difficult decisions have had to be made, and some very interesting material has had to be omitted. It is to be regretted that we could not expand upon topics such as the story of the near collapse of Winchester Cathedral as a result of fungal decomposition of the oak raft that supported the structure, following drainage of nearby farm-land.

My co-authors and I have confined ourselves to a consideration of the aspects of microbiology in which we have research experience: bacteriology, mycology and virology. We have also tried to concentrate on the fundamental problems in the subject. What constitutes microbes? How do they differ from higher organisms and from each other? How can microbes be controlled, visualised, enumerated and cultured?

Safe handling of microbes

The vast majority of microbial life on Earth is harmless to humans, and many microorganisms have beneficial effects. Since the dawn of civilisation, humans have harnessed microbial fermentations to make bread and alcoholic beverages, and to prolong the life of food. Today, technologists are exploiting microorganisms in the pharmaceutical industry, for food production, mineral extraction, the oil industry and in agriculture. There is hardly any aspect of modern life that is not touched by microbiology. However, a small minority of microbes do cause disease, and a minority of disease-causing microbes can cause fatal infections. Some, such as the human immunodeficiency virus, the cause of AIDS, may take several years to exert their lethal effect. Others such as Neisseria meningitidis, the cause of meningococcal meningitis, can kill within hours of the first symptoms of the disease.

When working with microbes, care must be taken to ensure that laboratory cultures do not escape to cause laboratory-acquired infections or to pollute the environment. Equally, it is important to ensure that laboratory cultures do not become contaminated with unwanted extraneous organisms from the environment. If care is not taken to avoid contamination of laboratory cultures, then the results of microbiological experiments are not reliably reproducible, and the data obtained would be unreliable. It is impossible to tell whether the observations made in such experiments are due to the properties of the desired organism, or arise from the activity of a contaminant.

Charged by its Royal Charter to promote biology and its understanding, the Institute of Biology recognises that it is not possible for any one text book to cover the entirety of a course. If evidence was needed, the success of the Studies in Biology series was a testimony to the need for specialist, up-to-date publications in education. The Institute is therefore pleased to collaborate with Cambridge University Press in producing a new title in the Studies in Biology series.

The new series is set to provide as great a boon to the new generation of students as the original did to their parents.

Suggestions and comments from readers will always be welcomed and should be addressed either to the Studies in Biology Editorial Board at Cambridge University Press or c/o The Books Committee at the Institute.