CHAPTER 13
Specialised Natural Habitats
WITHIN THE wider habitats of woodland, grassland, and coastal dunes are many smaller, sometimes temporary but often highly specialised communities of fungi adapted to specific niches. Such communities include the phoenicoid or firesite fungi, the dung fungi, the fungi of bird nests, and those adapted to dry (xerophilic), cold (psychrophilic), and other extreme conditions. Specialised communities of fungi are also associated with specific plant groups, notably mosses, liverworts, and ferns. The present chapter looks at all of these, together with the fungi found in caves and other underground chambers.
PHOENICOID OR FIRESITE FUNGI
Firesite or ‘phoenicoid’ fungi (the term means ‘phoenix-like’, arising from ashes) are specialised species which typically appear after forest fires, controlled burns and bonfires, and on other heat–treated substrata. The term ‘phoenicoid’ was introduced by Carpenter & Trappe (1985) in recognition of the remarkable response of these fungi to severe heat. Following the eruption in May 1980 of Mount St. Helens in Washington State, USA, phoenicoid fungi (including species such as the cup-fungus Peziza violacea and the morel Morchella elata) were the first visible life-forms to appear amongst the devastation, producing fruitbodies in the tephra within two months of the eruption.
It was assumed initially that phoenicoid fungi were ‘carbonicolous’ (able to colonise charcoal and other burnt vegetable matter), but a series of investigations has revealed a more complex and less obvious ecology. Basically, many of these fungi respond either to severe heat or to secondary changes brought about by burning, but rarely if ever to charcoal itself. Nevertheless, it is still common to see fungi of burnt ground referred to as ‘carbonicolous’.
Many phoenicoid species produce spores which are stimulated to germinate by heat. A short period of heat treatment at 50°C, for example, can enhance sporulation in a number of typical firesite cup-fungi, including Peziza praetervisa, Ascobolus carbonarius, and Pyronema domesticum. The last of these sometimes appears on steam-treated greenhouse soils in the absence of fire.
Fires, whether natural or manmade, not only burn and sterilise sites, but also cause substantial changes in the chemistry and structure of the soil. Chief amongst these is a marked increase in surface alkalinity, with initial pH values in the uppermost ash layers rising to 10 or so. This alkaline ash gradually diffuses into the subsurface soil layers through leaching, raising pH values throughout. Areas with high ash cover, such as woodland bonfire sites, are clearly more affected than areas with low ash cover, such as those found after stubble burns or natural, quick-burning, forest fires.
It appears that many phoenicoid fungi are alkaline specialists, able to tolerate or even thrive at pH levels inimical to more generalist species. This explains why typical firesite species such as the cup-fungi Peziza praetervisa and Geopyxis carbonaria can occasionally be found growing on old mortar and damp plaster.
Moser (1949) split macrofungi into four ecological groups, according to their dependence on burning. ‘Anthracobionts’ are obligate phoenicoid fungi and include, amongst others, species of the cup-fungi Plicaria and Anthra-cobia, as well as some agarics such as Tephrocybe ambusta. ‘Anthracophiles’ prefer burnt sites but may occur elsewhere; they include the chanterelle-like Faerberia carbonaria, the morel Morchella elata, and the discomycete Tricho-phaea gregaria. ‘Anthracoxenous’ species are of accidental occurrence on burnt ground but can tolerate such sites, and the remainder, including most (but not all) mycorrhizal species, cannot tolerate burning at all.
The firesite succession
Obligate anthracobiont species tend to appear in well-defined succession following burning, and may continue to develop for several years. This succession mirrors that exhibited by fungi on dung (see below), and has been studied or reviewed by Petersen (1970), Turnau (1984), and Lisiewska (1992). In some of the phoenicoid ascomycetes, it has been shown to reflect direct antagonism by later-fruiting species towards earlier colonisers.
The first macrofungi to appear after burning tend to be discomycetes, particularly Pyronema species which form pinkish-orange crusts of confluent fruitbodies over freshly burnt or sterilised soil. These are followed by species of Anthracobia which commonly continue to fruit for up to seven or eight months after burning. Geopyxis carbonaria, Plicaria trachycarpa, and some species of Peziza are next in succession. The toadstools Pholiota highlandensis and Psathyrella pennata also appear at this stage and may persist for many months. The discomycete Octospora hetieri and the toadstool Myxomphalia maura are examples of species which do not make an appearance for more than a year, but may then persist for up to four years. Other more generalist species finally supersede the true firesite fungi, but how and in what form the latter persist in the absence of fires remains largely unknown.
Larger phoenicoid fungi in the British Isles
In Britain there are around 30 species of phoenicoid discomycetes, all of which belong in Pezizales. Species of Peziza, Plicaria, and Rhizina are amongst the largest, the most spectacular being Peziza proteana. In its normal form this produces typical cup-shaped or discoid fruitbodies, but in the variety sparassoides fruitbodies are cauliflower-like forming large, whitish, compound structures up to 25 cm high and 15 cm wide. This strange-looking fungus is not common, but is unmistakeable when encountered. The other five or so British phoenicoid Peziza species (see Table 27) are more conventional, though often quite large and variously coloured in dull violet, brown, or black (Fig. 118).
Plicaria is closely related to Peziza but distinguished microscopically by its globose rather than ellipsoid ascospores. Three Plicaria species occur in Britain, all of which are restricted to fire sites and have dark brown, cup-shaped or discoid fruitbodies. The commonest and also the largest of these is Plicaria endocarpoides, with fruitbodies to 6 cm or so across. Rhizina undulata is another conspicuous species, and one which appears to require heat-shock for germination of its spores. The species is fairly common on burnt ground in conifer woods from late summer to autumn and in such situations can be a serious parasite of newly emerging pine seedlings.
FIG 118. The cup fungus Peziza petersii is one of the larger discomycetes found on firesites (P. Livermore).
Much smaller, but far more abundant, are species of Anthracobia which can cover fire sites with hundreds of usually orange or reddish-orange, discoid fruitbodies. Three species, Anthracobia macrocystis, A. maurilabra, and A. melaloma, are particularly common (Fig. 119), whilst two others, A. uncinata and the blackish A. subatra, are distinctly rare. Indeed the last species was only recorded from Britain in 1996 based on a collection from Surrey. Phoenicoid species of Tricharina and Trichophaea have pale, yellowish-orange or whitish fruitbodies and occur singly or in clusters on burnt ground which has been colonised by mosses (Fig. 120). Lamprospora carbonicola, with tiny, orange fruitbodies only 1–2 mm across, shares the same habitat. Although always on burnt ground, its true association is with the moss Funaria hygrometrica, a common and early coloniser of fire sites. Dougoud (2001) has provided a key for the identification of discomycetes on burnt ground, including obligate phoenicoid species as well as those only occasionally found in this habitat.
FIG 119. Anthracobia melaloma, one of several small discomycetes which typically occur in swarms on firesites, sometimes developing within a few months of burning (P. Livermore).
FIG 120. Tricharina praecox, a discomycete associated with mosses on burnt ground. The fruitbodies are gregarious and are usually found in spring (P. Livermore).
Several pyrenomycetous ascomycetes are also characteristic of fire sites (‘pyrenomycetous’ refers to their carbonised appearance, not their habitat preferences). In Britain, these include species of Cercophora, Jugulospora and Strattonia, some of which are fairly common although, being small and black, are almost impossible to see in the field. They are best located by collecting other, more conspicuous fungi and scanning the soil around them under a dissecting microscope. A general key to British phoenicoid ascomycetes was published by Ellis & Ellis (1988).
A number of British basidiomycetes are also burnt ground specialists. Most of these are agarics, such as Pholiota highlandensis, one of the commonest phoenicoid species recognised by its viscid, orange-brown cap (Fig. 121). The misleading epithet ‘highlandensis’ comes from America, not Scotland, and the toadstool is perfectly at home in the lowlands. At least three of the ink-caps are typical of burnt sites: Coprinus jonesii, a common agaric with large, tufted, greyish fruitbodies (Fig. 122), C. gonophyllus, and the tiny C. angulatus, a much less frequent species. Other phoenicoid agarics include Myxomphalia maura, a grey-brown species with striate cap and mealy smell, Hebeloma anthracophilum, Psathyrella pennata, and several rather dull, greyish species of the genus Tephrocybe. The stalked polypore Coltricia perennis (Fig. 123) is also not uncommon on firesites.
FIG 121. The brown toadstool Pholiota highlandensis growing with the grey inkcap Coprinus jonesii in a typical firesite association (P. Roberts).
FIG 122. The inkcap Coprinus jonesii, a delicate species with characteristic shaggy veil and clustered fruitbodies, grows almost exclusively on burnt ground (B. Spooner).
Obligate or typical British phoenicoid macrofungi are listed in Table 27. However, it should be remembered that many other species are occasionally found on burnt ground, especially amongst the discomycetes. Byssonectria fusispora, for example, together with Geopora arenicola and several species of Peziza, including P. repanda, are not infrequent, but are excluded from the table since they are more commonly found elsewhere. Monti et al. (1992) have published a useful selection of colour photographs of burnt ground fungi.
FIG 123. Coltricia perennis is an attractive stalked polypore with a zoned cap often found on old firesites (P. Livermore).
TABLE 27. Obligate or typical British phoenicoid macrofungi.
| SPECIES | ORDER |
| ASCOMYCETES | |
| Anthracobia macrocystis | Pezizales |
| Anthracobia maurilabra | Pezizales |
| Anthracobia melaloma | Pezizales |
| Anthracobia subatra | Pezizales |
| Anthracobia uncinata | Pezizales |
| Ascobolus carbonarius | Pezizales |
| Geopyxis carbonaria | Pezizales |
| Lamprospora carbonicola | Pezizales |
| Octospora hetieri | Pezizales |
| Peziza echinospora | Pezizales |
| Peziza petersii | Pezizales |
| Peziza pseudoviolacea | Pezizales |
| Peziza proteana | Pezizales |
| Peziza proteana v. sparassoides | Pezizales |
| Peziza vacinii | Pezizales |
| Peziza violacea | Pezizales |
| Plicaria carbonaria | Pezizales |
| Plicaria endocarpoides | Pezizales |
| Plicaria trachycarpa | Pezizales |
| Pulvinula carbonaria | Pezizales |
| Pyronema domesticum | Pezizales |
| Pyronema omphalodes | Pezizales |
| Rhizina undulata | Pezizales |
| Rhodotarzetta rosea | Pezizales |
| Sphaerosporella brunnea | Pezizales |
| Tricharina gilva | Pezizales |
| Tricharina praecox | Pezizales |
| Trichophaea abundans | Pezizales |
| Trichophaea woolhopeia | Pezizales |
| Cercophora arenicola | Sordariales |
| Jugulospora rotula | Sordariales |
| Strattonia carbonaria | Sordariales |
| Strattonia minor | Sordariales |
| BASIDIOMYCETES | |
| Coprinus angulatus | Agaricales |
| Coprinus gonophyllus | Agaricales |
| Coprinus jonesii (= C. lagopides) | Agaricales |
| Hebeloma anthracophilum | Agaricales |
| Myxomphalia maura | Agaricales |
| Pholiota highlandensis (= P. carbonaria) | Agaricales |
| Psathyrella pennata | Agaricales |
| Tephrocybe ambusta | Agaricales |
| Tephrocybe anthracophila | Agaricales |
| Tephrocybe atrata | Agaricales |
| Tephrocybe impexa | Agaricales |
| Clavaria tenuipes | Cantharellales |
| Coltricia perennis | Hymenochaetales |
| Faerberia carbonaria | Poriales |
DUNG FUNGI
Dung, particularly of herbivorous mammals, provides a nutrient-rich substratum for a large variety of specialist fungi. It typically contains easily accessible cellulose and hemicellulose, is high in nitrogen, ammonia, and organic compounds, has a high pH, and is water-retentitive. Moreover, herbivores eating and dunging in the same area provide an efficient recycling system for fungal spores and propagules. However, dung is clearly a complex substratum, varying greatly in its chemistry according to species, age and local conditions which affect the rate of decomposition. It has an equally complex ecology, being home to many kinds of organisms in addition to fungi, all of which interact in ways which are not yet fully studied.
The succession of fungi on dung
Dung fungi are highly successional, as can easily be demonstrated by keeping rabbit pellets or similar material in a moist chamber and noting which species appear and when. Simple methods for doing this, as well as keys to British species, can be found in Richardson & Watling (1997). The succession typically moves through three phyla of higher fungi, the Zygomycota appearing first, followed by the Ascomycota and finally the Basidiomycota. Although this is essentially a factor of the time it takes to produce fruitbodies, competitive antagonism can also be demonstrated. Species of Mucor, for example, are more prolific on sterilised rather than unsterilised dung, their growth being restricted by the presence of other fungi. Further aspects of the dung succession, such as the effects of ecological factors on fungal growth and sporulation, have been investigated by Harper & Webster (1964), Ikediugwu & Webster (1970a,b), and Larsen (1971).
Fruitbodies of the Zygomycota can appear on dung within 2–3 days. Typically, they include examples of the genus Pilobolus, highly adapted fungi having glistening, colourless, pin-like fruitbodies about 2–5 mm high, each with a swollen tip surmounted by a shiny black, discoid structure (‘sporangium’) which contains the spores (Fig. 124). Despite their small size, Pilobolus species are capable of projecting these sticky packets of spores for distances of one metre or more from the dung surface. The sporangia adhere to grass leaves and other vegetation, where they can be grazed, ingested, and re-released with fresh dung. Species of another common genus, Phycomyces, have evolved an equally remarkable strategy by producing hair-like, attenuated fruitbodies up to a third of a metre long. Each is tipped with sticky sporangia which adhere to whatever they touch. Instead of projecting its spores onto grazeable grass, Phycomyces effectively reaches out and places them there. Many other zygomycetes are associated with dung, with around 20 genera recorded from the Britain. As well as Phycomyces and Pilobolus, these include species of Mortierella, Mucor, Pilaira, Piptocephalis, and Rhizopus, several of which are common, if rarely noticed. Of particular interest are species of Syncephalis. Though these always occur on dung, they are actually parasitic on their fellow zygomycetes. Two species, Syncephalis depressa and S. nodosa occur in Britain, parasites on various species of Mucoraceae.
After 6–12 days ascomycetous fruitbodies start to appear. These are the most numerous of the dung associates, and are a highly diverse assemblage. Most of the major orders of the Ascomycota include some coprophilous species, but the most significant on dung are the operculate discomycetes (Pezizales) together with pyrenomycetous groups such as the Sordariales, some Xylariales, Dothideales, and Gymnoascales. Curiously, members of the inoperculate discomycetes (Helotiales, Orbiliales) are scarcely represented. This is remarkable, given their ubiquitous presence elsewhere, on rotting plant remains. Only a few species, mostly in the genera Lanzia, Martininia, Orbilia and Pezizella, have been found on dung, although some Orbilia species are of particular interest in having anamorphic states which trap dung-dwelling nematode worms (Chapter Five).
FIG 124. Pilobolus crystallinus, one of the Mucorales, is common on the dung of herbivores. Thesporangiophores, swollen near the top and bearing a black sporangium which is forcibly discharged, are characteristic of the genus. From a painting by R. Baker (RBG Kew).
Altogether, at least 150 species of coprophilous ascomycetes have been recorded from Britain to date. They occur on all types of droppings and present an astonishing diversity of form and structure, best appreciated by taking dung samples, keeping them in a damp container, and examining the succession of fruitbodies under a microscope. Many of these ascomycetes are rare, or apparently so, and are seldom seen. As with so many groups of fungi, species new to the British Isles are still being discovered. For example, the small, black, flask-shaped species Podospora granulostriata was first reported in 1995 based on collections on deer dung from Surrey and Cambridgeshire, whilst the remarkable Subbaromyces splendens was discovered in Belfast slurry tanks in 1992 (Fig. 107).
Much more frequent and far better known are species of Ascobolus and Saccobolus (Pezizales), the majority of which are strict dung-associates although a few occur on rotting vegetation or burnt ground. These can be readily recognised by their characteristic ascospores which at maturity are purple, and usually have a striate or sometimes warted surface. Saccobolus species are distinctive in having ascospores that are formed, mostly in consistent and regular patterns, into cohesive clusters which are ejected as a unit from the ascus. In Ascobolus species, spores are individually discharged and dispersed on air currents, but the clustered spores of Saccobolus form a large projectile which is shot over comparatively long distances into surrounding vegetation. A mucilaginous sheath surrounds the spore package in all dung-inhabiting species of Saccobolus, gluing the spores to nearby vegetation where, as with Pilobolus, they can be grazed, ingested, and re-released with fresh dung. Species of Cheilymenia and Lasiobolus are also characteristic of dung, most having small, disc-shaped, orange fruitbodies frequently ornamented with hairs. Cheilymenia stercorea is a typical example, often occurring in swarms on cow pats. Other discomycete genera such as Thelebolus, Ryparobius, Trichobolus and Ascozonus produce microscopic fruitbodies and, although some are very common, their taxonomy is not yet fully elaborated and species identification is no easy task. It is notable that many species of these last mentioned genera have multisporous asci, in some cases over 1000 spores being formed in each ascus. Similar asci also occur in some coprophilous pyrenomycetes, such as Arnium leporinum and Podospora granulostriata. In many such cases the spores may be discharged as a single unit, possibly indicating the development of polyspory as an adaptation to a coprophilous habit.
Most of the remaining ascomycetes on dung are pyrenomycetes belonging to the order Sordariales. These are characterised by having dark brown ascospores which have germ pores, are frequently 2-celled, and have either a gelatinous sheath or gelatinous appendages. These gelatinised elements almost certainly play a role in spore discharge and dispersal, helping them stick to surrounding vegetation. Podospora and Schizothecium are the commonest of the genera involved, with over 120 species between them, around 30 of which are known in the British Isles.
Most of the coprophilous pyrenomycetes are small to microscopic, though some species of Podosordaria and Poronia (Xylariaceae), are much larger and easily visible. The latter genus is well-known thanks to the status of Poronia punctata as a European priority species for conservation. The species is sometimes called the ‘nail fungus’ because of its distinctive nail- or golf-tee-shaped fruitbody. This roots deeply into the dung and has a flat or slightly concave disc about 10–15 mm across, dotted with the black mouths of the perithecia in which the asci and spores are formed (Fig. 125). It is associated with horse dung and was comparatively commonplace in Britain (as was its host) until the beginning of the twentieth century. It has now become so rare that it is virtually restricted to pony dung in the New Forest, with only occasional records from elsewhere. It is considered endangered throughout Europe, since it seems to be found only in areas of unimproved pasture, a threatened habitat which is being increasingly lost. The widespread use of artificial fertilisers, as well as additives to feedstuffs and better veterinary care, have altered the nature of horse manure, possibly making it a less suitable substratum for the fungus. Another possible reason for the decline of Poronia punctata is that the natural, year-round, eating-dunging cycle has been broken for most British horses. The New Forest ponies, which still roam in a comparatively natural and unimproved environment, are an exception. A second British species, Poronia erici, is something of a curiosity. Although similar to P. punctata, it has larger spores and smaller, less deeply rooting stromata, and is typically found on rabbit pellets particularly near the coast. It is so far known in Britain only from Scolt Head Island in Norfolk, where it was first collected in 1933 but remained unidentified and unrecognised until 1988. It has now been recorded from various parts of northern Europe, mostly on rabbit pellets, but has a curiously disjunct distribution, occurring also much further afield in Australia where it grows on kangaroo and wallaby dung, as well as that of rabbits, sheep and horses. It is thought to have been introduced into Europe after successfully colonising rabbit dung following the introduction of rabbits into Australia during the 19th century. Anamorphic ascomycetes (hyphomycetes) are also common on dung, especially late in the succession, and include strict dung-associates as well as secondary invaders. Over 260 coprophilous species were noted by Seifert et al. (1983), although not all of these have yet been recorded from Britain. Most hyphomycetes are visible only as mouldy growths in the field, though some are distinctive under the microscope. A few ‘synnematous’ genera (forming drumstick-like fruitbodies) such as Doratomyces and Stilbella are more conspicuous and somewhat easier to identify. Stilbella erythrocephala, for example, is common, especially on rabbit pellets, and produces club-shaped fruitbodies, sometimes up to two millimetres high, which occur in swarms and have pinkish-orange heads. The species is known to inhibit the development of many other coprophilous fungi, providing an example of antagonistic competition in the fungal succession.
FIG 125. The rare Poronia punctata on pony dung from the New Forest, one of its few remaining sites in Britain. The characteristic fruitbodies are golf tee- or nail-shaped, rooting into the dung (S. Evans).
Basidiomycetes begin to appear on dung after nine days or more and include a number of toadstools, particularly ink caps of the genus Coprinus (derived from the Greek ‘kopros’, meaning dung). Some of these are extremely small and ephemeral, rarely if ever seen in the field, but commonly observed when dung is cultured. Other coprophilous agarics include species of Conocybe, Panaeolus and Psilocybe. Some of these grow directly on dung, others (including ‘magic mushrooms’) are more typically found on manured grassy ground and soil. Non-agaric basidiomycetes are comparatively few on dung, but two gasteroid species are particularly notable. Sphaerobolus stellatus, the ‘shooting star’ or ‘cannon-ball fungus’, is fairly common on dung though not restricted to this substratum. It is a highly distinctive fungus with densely gregarious, small, pale yellow fruitbodies which at maturity split to eject a globose spore-ball. This is a surprisingly powerful and efficient mechanism. It was investigated in detail by Buller (1933) who measured the horizontal range of the spore-ball to reach as far as 18 feet 7 inches (c. 5.7 m) and the vertical range to be as high as 14 feet 5 inches (c. 4.4 m). Also of note is the bird’s-nest fungus Cyathus stercoreus, a rather rare or localised species associated with rabbit droppings in sand dune systems.
Dung, especially that of herbivores, also provides a suitable habitat for slime-moulds, particularly those otherwise associated with plant litter. Few of the species involved are thought to be obligately coprophilous, although some are as yet only known from dung, notably Trichia fimicola and Perichaena luteola. The former is very rare on hare and rabbit droppings in coastal dunes, and is only known from Britain and Belgium. The latter has been recorded from the Hebrides on cow and sheep dung, but is known elsewhere in Europe and in North America. Over 30 species of myxomycetes recorded on dung were noted by Eliasson & Lundquist (1979), and many additional species have since been found (Ing, 1994b).
In all, around 400 species of fungi have been recorded as dung associates in the British Isles, and no doubt others await discovery. Table 28 lists a selection of the commonest or most distinctive of these species, and a more comprehensive coverage, with illustrations and keys for their identification, was provided by Ellis & Ellis (1988) and Richardson & Watling (1997).
TABLE 28. A selection of typical British dung fungi.
Specialist adaptations
An essential part of the biology of dung fungi is their ability to persist in an ephemeral environment and most species have adapted in some way to the eating-dunging cycle, particularly by producing spores capable of surviving passage through the gut. Larsen (1971) split dung fungi into three groups: obligate ‘endocoprophilous’ fungi (e.g. Saccobolus and Ascobolus species) whose spores germinate only after passage through the gut; facultative endocoprophilous fungi (e.g. Coprinus species) whose spores can survive passage through the gut; and ‘ectocoprophilous’ fungi (e.g. Ascozonus species) whose spores do not survive passage through the gut, but persist in dunged soil.
Given that most dung fungi are so highly adapted, it is perhaps surprising that very few of them appear to be strictly selective in their animal associates. Many are known to occur on a wide range of dung types, although most show definite preferences and are regularly more abundant on some types than others. Richardson (1972) examined the occurrence of ascomycetes on different herbivore dung, but found only a tendency for certain species to be associated with ruminant (cattle and sheep) dung or non-ruminant (rabbit and hare) dung. Many more species were common to both. Such differences as were observed could be due more to the composition of the dung (texture, nutrients, water content, and so on) than to its source.
Lundquist (1972), however, analysed host preferences for Nordic Sordariaceae and showed that, whilst some common species may occur on dung of a wide range of animals, all species show definite preferences for one or two kinds of dung. For example, Schizothecium conicum, one of the commonest and most ubiquitous of the dung fungi, strongly favours that of cows and horses but occasionally occurs on dung of 14 other animal species. He recognised three ecological groups: species with a broad ecological tolerance and low preference for a particular substratum, those with a broad tolerance and high preference for a particular substratum, and specialised species restricted to one or a few kinds of substrata. He also found several surprising and unexpected relationships. The dung of deer, for example, has more species in common with that of rabbits than that of sheep and goats. Quite why is unclear.
Carnivore dung is obviously not part of the eating-dunging cycle, but can harbour a range of opportunistic fungi. Dog dung, for example, offers the enquiring mycologist a number of interesting species of which the cup-fungi Ascobolus and Thelebolus are particularly frequent. This area of research is surprisingly understudied, although Dennis (1960) noted encouragingly that ‘a rich harvest may well await the man who cares to devote his leisure hours or his declining years to the study of stale dog dung.’
Even human faeces are known to yield various fungi, though the nonpathogenic species appear to be little studied. Fairman (1920) provided a brief synopsis of the fungi colonising this readily available substratum. These include the almost ubiquitous Ascobolus furfuraceus as well as the specifically named Sordaria humana, though the latter is equally common on dog dung.
Dung of small mammals, such as mice, voles, and bats, is not always easy to find, but can also be rewarding mycologically. Some of the zygomycetes, for example, are particularly frequent on these substrata, including species of Coemansia, Kickxella, Mortierella, Mucor, Piptocephalis, and Rhopalomyces. Among the discomycetes, Ascobolus rhytidisporus has been described from mouse dung in Britain, and the ascomycete genus Guanomyces was described from bat dung in Mexico.
Bird droppings, especially those of grouse and geese, also have associated fungi, Lundquist (1972), for example, recording 19 species of Sordariaceae and Lasiosphaeriaceae (Ascomycetes) on this substratum in the Nordic countries. Most of these, including various species of Podospora and Sporormia, are plurivorous, but a few, such as Strattonia borealis, seem strongly to favour grouse dung. Richardson (2001) found Sporormiella minima to be most frequent on grouse dung, and the discomycete Ascobolus carletonii to occur only on this substratum. Some other ascomycetes frequently encountered on bird droppings include Saccobolus quadrisporus and Thelebolus cesatii. A common zygomycete is Coemansia scorpiodea. Pigeon droppings (not hard to find) are notoriously a source of the yeast Cryptococcus neoformans, a serious and often fatal pathogen of humans (Chapter 15).
Though comparatively little investigated, the dung of amphibians such as frogs and toads hosts a range of species which, because of the ephemeral nature and small size of the dung, require specialist study to appreciate. However, working in such an obscure field can clearly prove rewarding. For example, the zygomycete Dimargaris verticillata was reported as new to Britain from toad dung by Kirk & Kirk (1984). This was previously known only from amphibian dung on the California-Mexico border. The same toad dung also produced the first British record of Coemansia erecta, and the uncommon species Mortierella polycephala.
FUNGI OF BIRD NESTS
Bird nests may seem a peculiar and unexpected place to look for fungi, but in fact they provide ideal habitats for a range of specialist saprotrophs and parasites.
Most of these fungi belong in a group of ascomycetes known as the Onygenales. This order, with around 90 species world-wide, contains keratinolytic specialists capable of decomposing hair, horns, bones, and feathers. Some are parasites, including the dermatotrophs which occur on the skin, hair and nails of humans (Chapter 15). Others are non-parasitic saprotrophs which are widely present in keratin-containing substrata such as dung, soil, and bird nests.
Species of Onygena, the type genus, are large and comparatively easy to name. Perhaps the commonest of these is O. equina, its club-shaped fruitbodies often occurring in swarms on rotting horn and hooves. Another, Onygena corvina, is found on bird skulls or on rotting feathers and its whitish, 2–3 mm high, club-shaped fruitbodies are also sometimes encountered in old nests. More typical, however, are genera with small to microscopic fruitbodies, particularly species of Arthroderma (Fig. 125A) and Chrysosporium, which may be present in high concentrations in occupied bird nests. Over 90% of nests sampled by Pugh (1966) from sites in England and Wales were found to contain these fungi, though their presence and abundance depended on the type of nest material, as well as its water content and pH. Of the twelve bird species sampled, the nests of blackbirds, song thrushes, sand martins, and hedge sparrows were most productive, but all nests except those of wrens and starlings yielded some fungi. Twelve different fungi were isolated, of which Chrysosporium species, especially C. keratinophilum, were the most frequent.
Keratinophilic fungi may also occur on the birds themselves and were investigated, again from British sites, by Pugh (1965) and Pugh & Evans (1970). Both studies, using feathers removed from ringed birds, found only about 37% of birds sampled had fungi on their feathers, and few individuals harboured more than two or three species. Fungi were most prevalent on blackbirds, pheasants, and grouse, whilst pigeons and starlings were largely uninfected. Some of these fungi appear to be host specific, or at least have a marked preference for certain birds. Ctenomyces serratus, for example, is almost exclusively found on partridges and pheasants, whilst Arthroderma curreyi occurs most frequently on blackbirds and song thrushes. It seems that the occurrence and distribution of keratinophilic fungi on birds is largely determined by the presence and quantity of feather fats.
FIG 125A. Arthroderma curreyi, a keratinophilic species, developing on damp, rotting feathers (RBG Kew).
In general, the fungi isolated from feathers of living birds were different to those found in nests, but a few were common to both, though in different ratios. For example, Arthroderma curreyi, the most common species on feathers and present in 67% of blackbirds sampled, was found in only 13.7% of blackbird nests. Conversely, A. quadrifidum was found only on 3.5% of birds studied, but occurred in almost half the nests. Arthroderma and Chrysosporium were again the most frequent genera obtained from feathers in these studies, and a similar study from 92 bird species in Yugoslavia and the Czech Republic also found these to be the most frequently isolated keratinophiles.
FUNGI OF MOSSES AND LIVERWORTS
Although the association between fungi and bryophytes (mosses and liverworts) has long been known, the ubiquity and diversity of this biologically remarkable phenomenon was slow to be recognised. Many hundreds of bryophilous fungi have now been described, reviewed by Felix (1988), but few have received detailed study. Indeed, Döbbeler (1978) noted that, given the abundance of bryophilous fungi, “their neglect is inexplicable”. He provided an account of just the pyrenomycetes and Dothideales (Ascomycota) known to occur on the gametophyte stage of bryophytes and included no fewer than 123 species in 33 genera, 62 of which were described as new to science. They included some particularly notable species, such as Bryochiton monascus and B. perpusillus which have the smallest known fungal fruitbodies, less than 50 µm diameter and sometimes as small as 18 µm across. Many ascomycetes have individual spores which are bigger than this. Moreover, these miniature Bryochiton species are able to develop their tiny fruitbodies directly from a single spore without forming a mycelium. Bryochiton perpusillus has been recorded from Britain on Polytrichum piliferum. Another species, Epibryon intracellulare, is also notable, being the first known higher fungus in which the fruitbody develops to maturity inside a host cell. It was described from Sri Lanka in (rather than on) Schistochila aligera.
Bryophilous ascomycetes
Many bryophilous ascomycetes are saprotrophs, and play an important role in the decomposition of the thalli. Others are biotrophic parasites, developing mutualistic associations with their hosts without causing any appreciable damage. They include endophytic VA mycorrhiza-like associations, termed ‘mycothalli’, as well as the development of appressoria and intracellular haustoria, which in some species may induce conspicuous galls in moss rhizoids. These galls are caused by species of Octospora (Pezizales), obligate moss-associates which produce conspicuous orange fruitbodies, and a few others such as species of Lamprospora (Fig. 126). These are well-known and sometimes common fungi, with at least 15 species in Britain. As the host associations and ecology of these bryoparasitic Pezizales have gradually been brought to light, further new taxa have been recognised and it is significant that over half of the known species have been described since 1975.
Other discomycetes which are specific to bryophytes include species of Bryoscyphus, all of which are parasites, some being associated with liverworts. In Britain, five are known so far, including Bryoscyphus atromarginatus which frequently grows with Marchantia in plant pots in garden centres, turning the infected thalli brown. Nectria muscivora is necrotrophic on species of Barbula and other small mosses, developing its orange-yellow fruitbodies in the leaf axils. Bryostroma trichostomi, only discovered in Britain in 1999, forms tiny black fruitbodies, no more than 300 µm across, in the leaf axils of its host. It is now known from Suffolk on Ceratodon purpureus and from Somerset on Barbula. Mniaecia jungermanniae, an attractive species associated with leafy liverworts, has deep blue-green fruitbodies that develop in early spring and are well worth looking for (Fig. 127). They are not easy to spot in the field but the species is known to be widespread, especially in southern England and Wales.
FIG 126. Lamprospora dictydiola is one of several discomycetes associated strictly with mosses. Many of these species have small, orange fruitbodies and can be distinguished only under the microscope (J. Palmer).
FIG 127. The turquoise discomycete Mniaecia jungermanniae is a spring-fruiting species, found only in association with liverworts (RBG Kew).
Toadstools and bryophilous basidiomycetes
Many basidiomycetes are also intimately associated with bryophytes, mostly as biotrophic parasites, although their biology requires further study. Species of the agaric genera Arrhenia, Rimbachia, and Rickenella are typical moss associates, as are many species of Galerina, a large genus of small brown toadstools. A study by Redhead (1981) showed that Galerina paludosa, grown in culture with Sphagnum, produces peg-like hyphal haustoria which penetrate the moss cells, though plants appear to remain healthy. Rickenella fibula, an attractive little orange agaric common in patches of moss in damp turf, and R. pseudogrisella, a constant associate of the liverwort Blasia pusilla, produce similar haustoria. Both occur in Britain, though the latter has only recently been discovered here. Further study may show such haustoria to be typical of most bryophilous agarics. Rimbachia has three British species which are obligate moss associates, all of them rare. They are similar to species of Arrhenia in having small, often stemless fruitbodies with gills either lacking or reduced to shallow veins. Arrhenia has seven British species, of which A. retiruga is the most common, forming pale grey fruitbodies on various living mosses. Another gill-less moss associate, widespread but uncommon in Britain, is Cyphellostereum laeve, a small, whitish species found on various mosses, particularly Polytrichum and Dicranella.
Unlike these biotrophs, the greyish toadstool Tephrocybe palustris is a necrotrophic parasite. It has long been known to kill off patches of Sphagnum, its fruitbodies appearing among the bleached and decaying remains of the moss. It does precisely the same in culture, its hyphae overrunning the host, penetrating and destroying the host cells.
An unusual basidiomycete, Eocronartium muscicola, occurs on various mosses, including in Britain species of Eurynchium, Fissidens, Hylocomium and Leskea. It forms upright, club-shaped fruitbodies 0.5–2 cm high, but is readily distinguished from the true club-fungi (Clavariaceae) by its septate, tubular basidia (which places it in its own genus among the heterobasidiomycetes). It is extremely rare in the British Isles, known from England and Ireland but with only two collections since 1900. It is a phylogenetically interesting species, considered to be ancient and possibly ancestral to the rusts.
Although bryophilous fungi are so numerous and diverse, it is curious that none of the pathogenic rusts, smuts, and powdery mildews have yet been discovered on mosses. These obligate plant parasites have an ancient lineage going back at least 300 million years during which they have evolved in intimate association with their plant hosts, but not, apparently, with bryophytes. At one time, some smuts were believed to occur on Sphagnum, but it is now known that these are not true smuts, although their affinities remain unclear. The best known, Bryophytomyces sphagni (formerly in the smut genus Tilletia), is a widespread species recorded from Britain. It may be the anamorph of a discomycete, Discinella schimperi (Helotiales), but this connection has not been confirmed.
Basidiomycetes are also involved in ‘mycothallic’ (mycorrhiza-like) associations with liverworts, particularly in the Jungermanniales and Metzgeriales (Chapter Four).
Slime-moulds and other moss associates
Several myxomycete species can be found in association with bryophytes. Indeed some, such as Fuligo muscorum, Physarum citrinum, P. confertum, P. virescens, Licea albonigra and L. lucens, appear to be confined to mosses. A highly specialised assemblage occurs on wet rocks by waterfalls and in deep ravines (see Ing, 1983) and includes, amongst others, Craterium muscorum, Lamproderma columbinum, and several species of Diderma. Several myxomycetes occur with Sphagnum, including Badhamia lilacina, which appears to be confined to this host. This has small, gregarious, greyish-lilac fruitbodies, but its yellow plasmodial stage is much more conspicuous. Amaurochaete trechispora and Symphytocarpus trechisporus are also regular Sphagnum associates, and occasionally more general moss-associates such as Lamproderma columbinum will also be found on Sphagnum.
Curiously, only a few species of the fungus-like Oomycota infect bryophytes. Most notable amongst these is Pleotrachelus wildemanii, described from Denmark and also known in Britain, which galls the rhizoids of Funaria hygrometrica and Tetraplodon mnioides. Other bryophilous oomycetes include Olpidiopsis ricciae, a weak parasite in the rhizoids of liverworts such as Marchantia and Riccia, and Lagenidium ellipticum in moss rhizoids. Neither has been recorded from Britain, but may well occur here. Similarly, very few chytrids are bryophilous. Two species of Synchytrium, S. musicola which parasitises the leaves of various mosses and S. pyriforme in Anomodon, appear to be the only examples. Neither is known from Britain.
FUNGI AND FERNS
As with bryophytes, fungi play a highly significant and indeed vital role in the ecology and biology of pteridophytes (ferns and their allies). Some of these associations are ancient, having developed early in the long history of pteridophyte evolution, probably over 350 million years ago, but others may be more recent in origin. However, as noted by Bennell & Henderson (1985), who briefly reviewed the parasitic species, the study of fungi on pteridophytes has been largely neglected, to the extent that most potential host species have never been investigated.
British fern fungi
The most frequent British fern fungi are ascomycetes some of which are common and abundant. They include the tiny discomycetes Microscypha grisella on decaying fern fronds, Micropodia pteridina on blackened stem bases of bracken, and Pezizella chrysostigma on decaying Dryopteris petioles. Pteridicolous species amongst the pyrenomycetes are mostly associated with bracken, the almost ubiquitous Rhopographus filicinus appearing as black streaks on dead stems. Several hyphomycetes are also common, such as Chalara pteridina on bracken petioles, as are coelomycetes such as Ascochyta pteridis, an obligate fern associate and important pathogen of bracken. Many of these pteridicolous ascomycetes can be identified using Ellis & Ellis (1997) who dealt with over 50 British species.
Basidiomycetes are also well represented. Rarely recorded, but well worth looking for, is the tiny toadstool Mycena pterigena on old fern rhizomes and rotting stems; fruitbodies are a delicate whitish-pink, with the gill edges outlined in deeper coral-pink. Less immediately attractive, but equally uncommon, is another agaric, Marasmius undatus, which grows on old bracken stems on alkaline soils. The white club-shaped fungus, Typhula quisquiliaris, is commoner and appears in groups on decaying bracken stems. Effused, corticioid (patch-forming) fungi include Aphanobasidium filicinum, ubiquitous on dead, damp bracken stems where it forms thin, waxy, greyish patches, and Parvobasidium cretatum, not noticed in Britain till the 1990s, but evidently extremely common in early spring at the base of Dryopteris clumps, at least in the Westcountry. A parasitic species forming whitish patches on the sori of living Dryopteris leaves is the heterobasidiomycete Herpobasidium filicinum, possibly widespread in Britain but rarely reported. A survey of obligate and other non-agaricoid basidiomycetes on ferns, with a key for their identification, was published by Boidin (1993). This covered over 80 European species, most of which are known in the British Isles. Decomposers of bracken litter were investigated by Frankland (1966, 1969, 1976) who recorded a total of 390 species, including ascomycetes, basidiomycetes and zygomycetes, although many of these were sterile and remained unidentified. These fungi, isolated in damp chamber cultures from decomposing petioles over a six year period, mostly consisted of common and plurivorous saprotrophs with very few bracken-specific species. They showed a marked succession during the process of decomposition similar to that on rotting wood. Lignin and cellulose decomposers predominated at first, followed by those which utilise simple sugars and carbohydrates, and finally by members of the zygomycetous Mucorales. The common woodland toadstool Mycena galopus was found to be the most active decomposer of bracken, just as it is for mosses.
Mycorrhizal associations of ferns and fern allies are treated in Chapter Four.
Fern parasites
Pathogenic fungi on pteridophytes involve representatives of most major groups including rusts. Amongst the obligate host-specific fungi are species of Taphrina (Ascomycota), which lack proper fruitbodies and simply produce a layer of asci over the infected plant parts. The genus was monographed by Mix (1949), who included 24 species on fern hosts, with more described since. Most are tropical and several induce distinctive and conspicuous galls. The Asian species Taphrina cornu-cervi, for example, causes branched antler-like galls on leaves of Arachniodes aristatum, whilst Taphrina laurencia produces remarkable, bushy galls on fronds of Pteris quadriaurita. A few British Taphrina species are pteridicolous, mostly on species of Dryopteris. They cause galls but these are inconspicuous, amounting to little more than thickened spots on leaves. Few other significant ascomycetous fern parasites occur, though Ascochyta pteridis, the cause of curl-tip disease of bracken and a common endophyte of the pinnules, has been investigated as a potential biocontrol agent (Chapter 17).
The strange and unique genus Mixia is also worth noting here as an obligate fern parasite. It includes a single species, M. osmundae, known from Japan and USA, which forms yellowish spots on the pinnules of species of Osmunda. It was once referred to the genus Taphrina as it produces spore-sacs which are reminiscent of the asci of that genus. However, they actually produce their spores exogenously and are therefore not asci. The genus is now considered akin to the basidiomycetes, a position supported by molecular data, and placed in its own family Mixiaceae.
Other obligate parasites on ferns are rust fungi, of which thirteen species have been recorded from the British Isles. Eight of these belong in the genus Milesina, many of which have alternate stages on conifers, especially firs (Abies species). In Britain the genus includes some fairly common species, such as Milesina blechni on Blechnum spicant, M. kriegeriana on Dryopteris species, and M. scolopendrii on Phyllitis scolopendrium. There are also some rarities. Milesina carpatorum on Dryopteris filix-mas, for example, is currently known in Britain from just six collections, whilst M. vogesiacum and M. whitei are almost as rare on Polystichum setiferum. Other British fern rusts include the equally rare Uredinopsis filicina on Thelypteris phegopteris, Milesia magnusiana on Asplenium adiantum-nigrum, and three rare or localised species of Hyalopsora. Of the 120 species of fern rusts known worldwide, almost all belong in these three genera, considered to be the most primitive of all living rusts. Another rust, Uredo vetus, recently discovered in China on the fern-ally Selaginella, is also of special interest as this is the most primitive group of vascular plants on which a rust has ever been found.
In contrast to rusts, virtually no smut fungi have been found on ferns or fern-allies. Just two Asian species, Melaniella oreophilum and M. selaginellae, both on Selaginella, are known. These species were until recently referred to the genus Melanotaenium, but were shown by Bauer et al. (1999) to be better placed in a distinct genus in the order Doassansiales. They consider the presence of these smuts on Selaginella, the most primitive host group known for such fungi, to be due to a host jump. However, it is also possible that they represent extant examples of an ancestral smut group.
A few chytrids also infect ferns and fern allies, mostly occurring as parasites on the spores. These include Rhizophlyctis rosea on germinating spores of Equisetum, and some species of Rhizophydium. These fungi are not restricted to ferns, occurring also on soil or on pollen. However, Ligniera isoetes is apparently a specific parasite in Isoetes, and Physoderma marsiliae is parasitic on species of Marsilia in the United States. There are also two species of Synchytrium recorded from ferns, though both appear to be very rare. Various fungus-like Pythium species (Oomycota) are known to attack prothalli of ferns and horsetails. Prothalli of Gymnogramme, Ceratopteris and Polystichum are parasitised by Completoria complens, a unique member of the Entomophthorales most other species of which are parasites of invertebrates.
XEROPHILIC FUNGI
A remarkable demonstration of the adaptability of fungi and their ability to take advantage of varied and often extreme environments is provided by the xerophilic (dry-loving) and xerotolerant fungi, which have evolved to cope with conditions in which water is not or is scarcely available.
It is a common observation that most fungi, particularly the fleshy macrofungi, produce fruitbodies in damp conditions. The flush of fungi in wet autumn weather is a well-known phenomenon, as too is the scarcity of fruitbodies when the weather turns dry. Yet surprisingly, a wide range of macrofungi can also be found in extremely dry habitats, where they make the most of what little water is available.
Desert truffles
Some of these xerotolerant species escape the worst effects of desiccation by growing underground where they form ectomycorrhizal associations with desert shrubs. Terfezia and Tirmania, for example, are truffle-like ascomycetes of which 14 species are known, mostly occurring in association with Helianthemum and Cistus (rock-roses and their allies) in parts of southern Europe and north Africa. Their fruitbodies are large, up to about 8 or 9 cm across, and have long been important as edible fungi, the Romans being especially fond of them. They are still much sought after and regularly sold in local markets (Chapter 17).
Earthstars and the gasteroid fungi
Quite a few gasteroid basidiomycetes are specially adapted to dry environments, notably species of Battarraea, Montagnea, Podaxis, Pisolithus, Tulostoma, Myriostoma, Astraeus and Geastrum. These occur in sandy soils and arid habitats, and may be common in semi-desert regions which are subject to occasional rains or floods. In the seasonally hot, dry parts of northwestern Australia, for example, Pisolithus arrhizus and Podaxis pistillaris are both common species. The stilt-puffball Battarraea phalloides can be common in dried-out watercourses in Namibia, and in arid regions of Europe, Central America and south-east Australia. Given some moisture, all of these species produce fruitbodies which are woody or leathery and well-protected against drying out. As in puffballs, the spores develop inside the fruitbodies and are only released when mature, sometimes by a distinct hole as in Astraeus, Geastrum, and Tulostoma species, but more frequently by the whole outer surface breaking away.
Battarraea phalloides is a good example. Like a stinkhorn, the fruitbody grows from a gelatinised ‘egg’ (the matrix helping store water), but the ‘egg’ is underground and gives rise to a dry, puffball-like peridium (containing the spores) on an equally dry, shaggy, woody stem. The whole fruitbody can be as much as 40 cm tall. On maturity, the thin papery peridium breaks into pieces and releases a huge mass of rusty-brown spores (Fig. 128). Curiously this strange species was first described, not from a tropical desert, but from Bungay, Suffolk, in 1782. It has since been found elsewhere in Britain, in dry hedgerows and sandy ground, once even in the dry interior of a hollow tree, but is obviously on the edge of its range here and is extremely rare (see Chapter 18 for an interesting attempt to conserve it). Large forms of this species up to 50 cm high and with a thick, dry volva, occur commonly in the Mediterranean area and are also widespread in subtropical regions. These have been considered as a separate species, Battarraea stevenii, but this conclusion has not been upheld in recent studies based on molecular as well as morphological data. In Cyprus, where this dry form is quite common, it is known as the ‘donkey fungus’ and is even eaten in its ‘egg’ stage.
FIG 128. Battarraea phalloides, the ‘sandy stilt puffball’ has a dry, fibrous stem and is especially adapted to arid conditions. It is usually found on dry, sandy soil but is very rare in Britain and is a Biodiversity Action Plan species (RBG Kew).
Montagnea arenaria, also found in the Mediterranean, resembles a woody, dried-up ink-cap (Coprinus species) and is indeed related to this group of toadstools. However, instead of the cap expanding to reveal the spore-bearing gills, in Montagnea it remains firmly closed and the spores develop inside, protected from drying out, before eventually being released as the cap breaks apart and flakes away. However, if cut open, Montagnea can still be seen to have toadstool-like gills. In evolutionary terms, it appears to have evolved from ordinary toadstools and is half-way to becoming a puffball.
Only three Tulostoma species are found in Britain, though there are many more in the Mediterranean area and in the steppes and drylands of eastern Europe. They resemble miniature puffballs on woody stalks and in Britain are most frequent in sand dunes and in dry, sandy grasslands. Tulostoma brumale, the commonest species, has also been found growing in the mortar of old walls, a suitably arid habitat. The rare Tulostoma niveum, considered to be threatened throughout its range, is a species of the arid subarctic. It was first found in Britain in 1989, in thin soil and moss on limestone boulders at Inchnadamph in Scotland.
Earthstars (Geastrum species) have a woody outer peridium which splits into rays and opens up to reveal a puffball-like inner peridium inside. There are 16 British species, most of them uncommon and some of them very rare. Though not so obviously xerophilic in their habitat, many still show a preference for growing in sand dunes, dry hedgebanks, and arid, often stony ground. Three species, together with the macroscopically similar but unrelated barometer earthstar (Astraeus hygrometricus), have hygroscopic rays. These only open up to reveal the spore-containing inner peridium when soaked with water. In dry conditions, the rays close up again for protection. The epithet ‘hygrometricus’ means ‘water-measuring’.
Fungi on bare, exposed wood
Other xerotolerant species develop and fruit on bare, exposed, often decorticated wood. Such wood, including trunks, branches and twigs, presents an extreme environment for fungi due to low nutrient availability, high temperature range, and aridity. Although crustose lichens are well known from such conditions, various non-lichenised fungi also occur. Many of the species involved are ascomycetes, adapted morphologically in having thick, gelatinised tissues which help to retain moisture. In this respect they also exhibit a remarkable degree of evolutionary convergence, with species from a range of unrelated genera presenting similar morphological features which have arisen in response to their environment. Sherwood (1981) reviewed the non-lichenised discomycete groups, and examined their biology, ecology and morphology. She found that taxonomically diverse species in such habitats often exhibit a range of characters not seen elsewhere. For example, all species with multiseptate, muriform, small-celled spores and a high proportion of those with filiform spores, occur in dry, weathered wood. Most also have a dark pigmented outer structure to the fruitbody or a dark layer which covers the hymenium when dry, all characteristics which help to minimise water loss.
Basidiomycetes on exposed wood show some of the same characteristics. Species of Auricularia, including the common jew’s ear (A. auricula-judae), often grow on dead, exposed branches and are both highly gelatinised and capable of reviving after dry periods, to the extent that a single fruitbody can last a year or more, sporulating only when rehydrated after rain. The small agaric Resupinatus applicatus often grows on dead attached twigs and is also highly gelatinised. Another small toadstool, Mycena rorida, most frequently seen on old brambles and briars, has an unusual stem which (in wet weather) is almost hidden inside a thick, gelatinised coating. The porcelain fungus (Oudemansiella mucida, Fig. 82), a much larger, translucently white agaric, typically grows in clusters high up in the dead branches of old beech trees and is covered in a semi-gelatinised slime, the better to resist desiccation.
Many of the patch-forming heterobasidiomycetes and corticioid basidiomycetes growing on dead attached branches are equally gelatinised, or leathery (another way of resisting drying), or waxy, or filled with a protective layer of mineral matter. Though fruitbodies may persist all year, spores are only produced following rain. Bracket fungi too are adapted to drying out, many of them producing tough leathery fruitbodies, sometimes with a varnish-like or waxy coating (as in Ganoderma lucidum and G. resinaceum). They also protect their hymenia by producing spores in narrow pores, creating a damp microclimate away from drying winds. Many of these bracket fungi are so specialised at resisting drought that they are actually commoner on exposed trees in (for example) parks and woodland pastures, than on sheltered forest trees. Some, like the oak polypore, Piptoporus quercinus, are virtually restricted to this habitat in Britain.
Fungi on rocks and stones
Microfungi can colonise bare rock and stone surfaces, in natural pores and irregularities, as subsurface ‘endoliths’, or as components of surface biofilms. More surprisingly, they can actually cause considerable degradation of rocks, either by mechanical means (splitting apart rock particles by growth) or by chemical attack through the release of various organic and inorganic acids.
The acid-producing microfungi are mostly familiar ascomycetous moulds belonging to such genera as Alternaria, Aspergillus, Botrytis, and Penicillium. Some of these are now used commercially to produce acids (Chapter 17), so it is no surprise to find them doing the same thing when they colonise damp rock surfaces. The mechanically degrading fungi appear to be much more specialist and much more xerotolerant. They are mostly dematiaceous hyphomycetes (with dark hyphae) in genera such as Exophiala, Sarcinomyces, and Lichenothelia, and may be adapted to their niche. Many are slow-growing, but able to survive considerable changes in temperature and humidity. They can colonise rock surfaces in arid, semi-desert areas as well as in damper and more temperate regions, gradually causing ‘biopitting’ as a result of their growth (see Chapter 14 for their effects on buildings and other artefacts). Sterflinger (2000) has reviewed these rock-dwelling microfungi, providing species and reference lists.
It is claimed that these microfungi are responsible for changing the colour of the Acropolis over the last 150 years, but the most immediately visible fungi on rocks, as well as on cement and concrete structures, are the lichens. The coloured banding due to salt-tolerant marine and maritime lichens on coastal rocks (Chapter 12) provides a familiar example. The distinctive, often mottled effect of lichen thalli on gravestones is also well known, adding character to many cemeteries and, in older examples, often harbouring scarce and vanishing species. However, lichen growth may be rapid and, even on new concrete, colonisation of lichens may be well established within 4–5 years if the initial alkalinity is sufficiently neutralised by acid pollution.
Xerophilic and osmotolerant microfungi
The fungi just mentioned are not true xerophiles in the strict sense of the word, since they have merely evolved xerotolerant fruitbodies capable of resisting periods of drought. The true xerophilic fungi, mostly moulds and yeasts, are those which are capable of growing and sporulating in unusually dry situations. This includes the osmotolerant fungi which can grow on substrata with high salt or high sugar content, where the osmotic pressure is high.
Drying, salting, and sugaring are among the most ancient methods of preserving food against fungal and bacterial decay. However, all such preserved foodstuffs are susceptible to invasion by xerophilic fungi, notably species of Eurotium (Ascomycota), commonly seen in its mould-like Aspergillus state, species of Penicillium, and many ascomycetous and basidiomycetous yeasts. They include Xeromyces bisporus (Ascomycota), the most xerophilic fungus known, which can occur on sugar-saturated confectionery. Studies of the physiological adaptations of these fungi to dry conditions have been made, with particular attention paid to commercially important yeasts in the food industry, such as species of Hansenula, Pichia, and Torulopsis. Tolerance of dry conditions depends upon the ability of the fungus to modify the osmoregulatory pressure within its cells. Substances such as glycerol and polyols are accumulated or secreted, hence lowering the internal osmotic pressure below that of the external environment and preventing water loss. A general overview of these specialist fungi was provided by Dix & Webster (1995), with major aspects covered by Hocking (1993).
PSYCHROPHILIC & SNOW-MELT FUNGI
Psychrophilic fungi are species of cold environments, specially adapted not just to survive but even to thrive in low temperatures. Specifically, these fungi are able to make active growth and to produce fruitbodies below 5°C. They are able to survive, however, at the much lower temperatures, sometimes below -40°C, which can occur in polar winters. Conversely, such cold-adapted fungi are, in general, unable to develop at temperatures above 20°C, and are usually unable to survive at all, either as mycelium or spores, after exposure for a few days to temperatures above 25°C or so. Most other fungi, in contrast, have growth optima above 15°C. A few are adapted to still higher temperature regimes, with optimal growth above 20°C and even as high as 50°C or more. These latter species are the thermophiles, found in places like compost heaps (Chapter 14).
Several psychrophilic moulds and yeasts can grow on food in cold storage, and many more find the coolness of domestic refrigerators an excellent climate for growth. Others find a more natural home in arctic and antarctic soils.
Polar fungi
Psychrophilic species have evolved in several different groups of fungi and include most of the species native to the coldest parts of the Arctic and Antarctica. The majority are yeasts and other microfungi, and are, for example, the dominant fungi in antarctic soils during spring and autumn. They include Candida and Cryptococcus yeasts and various zygomycetes, particularly in the genera Mortierella and Mucor. Cryptococcus vishniacii has been found in the dry valleys of Antarctica, possibly the most inhospitable place on the planet. Lichenised ascomycetes, including Buellia, Lecidea, and Acarospora species, are also able to survive in these dry valleys as ‘cryptoendoliths’, inhabiting the subsurface cavities of porous rocks. Ocean depths are more or less continually cold, typically just above freezing, and provide another habitat for psychrophiles.
Psychrotolerant fungi are able to survive extreme cold but cannot actively grow until temperatures rise above 10°C. Many of these are macrofungi, such as the bryophilous toadstool genera Galerina and Omphalina which are characteristic of subpolar vegetation dominated by grass tussocks and moss cushions. Several hundred agaric species and other macrofungi have been recorded from such cold environments, which include huge areas of the Canadian, Alaskan, and Russian tundra as well as much of Antarctica and the subantarctic islands, together with alpine and other montane regions. The maximum temperature in some of these areas rarely exceeds 10°C, even during the short summer season.
In the British Isles, a number of macrofungi typical of the arctic-alpine mycota have been found in Scotland, either in the Highlands or at lower altitude further north. An example is Amanita nivalis, originally described from the Cairngorms and there associated with the least willow Salix herbacea. Various Omphalina, Russula, Laccaria, Inocybe, and Cortinarius species may also form part of the Scottish subarctic mycota. A few species also occur in the English Lake District, including Amanita nivalis, the waxcap Hygrocybe salicis-herbaceae, and several Omphalina species.
Snow-melt fungi
Nivicolous or snow-melt fungi occur at the edge of snow banks and fruit when the melt is underway. They are surprisingly diverse and probably include representatives from most groups of fungi. Many alpine and arctic species develop under snow banks and much of the decomposition of plant litter and nutrient recycling in such places takes place under snow cover.
Snow-melt myxomycetes were not thought to occur in Britain, but Ing (1998), searching for them in the Scottish Highlands, duly found several specialist species otherwise known only from the Alps and other areas of more permanent snow. In late spring and early summer, especially where patches of snow remain which have been present for at least three months, a characteristic association occurs of myxomycetes which are rare or absent from other habitats. These are able to develop on plant litter from the previous year, protected from freezing by an insulating blanket of snow. The fruitbodies can be found within a metre or so of the edge of the melting snow, mostly from late March to early June. Several species are involved, around 16 being recorded from Britain to date. Most records are from Scotland, but a few have also been found in the English Lake District. Of the species involved, the commonest is Diderma niveum, frequent on a range of rotting vegetation between 700 and 1200 m, but others such as Physarum vernum, a widespread and conspicuous species, and Diderma alpinum, may be locally common.
Several of the larger discomycetes are also associated with snow-melt. These include species of Peziza, notably P. ninguis and P. flos-nivium, which were described from the French Alps. The former was recorded from the Isle of Skye in 1989, and has since been found in Cambridgeshire, though in both cases without specific association with melting snow. These alpine fungi, as well as further discomycetes, myxomycetes, and some agarics, were studied by Heim (1947). He attempted to distinguish between obligate and facultative nivicoles, the latter being able to develop under snow but having a much wider ecological range.
Amongst other cold-tolerant ascomycetes are species of Thelebolus. This is a genus of coprophilous fungi with tiny fruitbodies which appear in early winter or spring, and are known from the Antarctic. Their development was studied by Wicklow & Malloch (1971) who found that, although optimal growth was between 15–20°C for those investigated, all possessed the ability to develop fruitbodies at low temperatures. In addition, they had the ability to do so in the absence of light, suggesting their possible development under snow. The psychrophilic genus Antarctomyces, based on a single species, A. psychrotrophicus, has been isolated from Antarctic soil where the average annual temperature is –1.5°C. This species has rudimentary fruitbodies that merely comprise a cluster of asci and has been shown by molecular study to be closely related to Thelebolus.
In America, Cooke (1955) reported a range of fungi associated with snow banks in montane localities in the western USA. These included many agarics, such as species of Lyophyllum, Tricholoma, Mycena, and Hygrophorus, as well as species of the discomycete genus Plectania, all of which were found consistently in close proximity to the melting snow bank, either fruiting through the snow or developing beneath it. In the Swiss alps, Senn-Irlet (1988) found 88 species of larger fungi in snow-bed communities, including Psilocybe chionophila and Galerina chionophila, known only from such habitats. They also included 36 species mycorrhizal with dwarf shrubs, mainly Salix and Dryas species, a surprising diversity given that the vegetation period in such conditions lasts no longer than three months, even in favourable years.
Several plant pathogens are also adapted to these conditions, particularly those affecting cereals and turf grasses. Perhaps the best known is the disease commonly called ‘pink snow mould’ or ‘Fusarium patch’. This is caused by the mould Microdochium nivale, or other cold-tolerant species such as Fusarium avenaceum and F. equiseti. These can grow under snow and form discoloured patches in turf which may be covered with white or pinkish mycelium and fruitbodies of the fungus. The disease can also occur in water-soaked areas in cool, wet weather. Other ‘snow mould’ diseases are caused by the clavarioid fungus Typhula incarnata and the discomycete Myriosclerotinia borealis, both psychrotolerant species which can develop under snow. The former occurs in Britain and can cause problems on crops such as winter barley. These and other such diseases have been treated in detail by Couch (1995).
ACIDOPHILIC AND ALKALOPHILIC FUNGI
Organisms able to grow above pH 8.5 are alkalophilic, whilst those able to grow at less than pH 4 are acidophilic. A number of fungi, particularly among the moulds and yeasts, are able to tolerate or even thrive in such extreme environments (Magan, 1997).
Highly alkaline conditions occur in volcanic areas (such as soda lakes), as well as some desert areas, and (more oddly) bird nests. Some of the Chrysosporium species found in nests can tolerate levels up to pH 11, whilst a range of moulds including Botrytis, Cladosporium, Fusarium, Penicillium, and Paecilomyces species, can grow at around pH 9.
Highly acidic conditions can also occur in volcanic areas (such as sulphur springs), as well as coal and copper mine spoil heaps, where specialised fungi may have a role to play in bioremediation (Chapter 17). Several moulds, including species of Aspergillus, Eurotium, Fusarium, and Penicillium, can grow at pH 2, and some yeasts can grow at even lower levels. These include brewer’s yeast, Saccharomyces cerevisiae, and others which may have uses in industrial chemical processes.
FUNGI IN MINES AND CAVES
Fungi in mines and caves caused some puzzlement to early mycologists. Firstly, there were a few genuinely exotic species, presumably imported with foreign pit props, which were able to flourish in the comparatively mild, unchanging climate underground. As long ago as 1793, Baron von Humboldt described just such a subtropical species, the polypore Flaviporus brownei, from mines in Silesia (it has since been recorded in mines and tunnels in Britain). Secondly, many of the fungi found below ground were of bizarre appearance, elongated like stalactites or branched like stags’ horns. Examination subsequently showed that these were abnormal fruitings of ordinary wood-rotting fungi growing in total darkness. One of the earliest reports of abnormal fruitbodies was by Martyn in 1744 who described a stag’s horn growth of Polyporus squamosus found in a cellar in the Haymarket in London. Many other strange and abnormal forms were included amongst the no less than 75 species described from caves in Italy by Scopoli in 1772. Some of the unusual growth forms exhibited by agarics and bracket fungi, such as Lentinus lepideus or the polypore Heterobasidion annosum, include elongation of stipes, undersized caps, and loss of certain pigment (Fig. 129). In mines, the familiar many-zoned polypore, Trametes versicolor, produces fruitbodies which are normally shaped, but white and entirely unzoned.
Though most fungi have no need of light for growth, many are stimulated to produce fruiting bodies by light, even if artificial and of brief duration. Dry rot, Serpula lacrymans, is one such example. In the absence of light, some fungi will not produce fruitbodies at all or will produce fruitbodies of varying abnormality. Occasionally, for example, the common polypore Laetiporus sulphureus may develop sterile, stag’s horn growths in dark conditions in woodlands. However, not all fungi develop abnormally in such conditions; fruitbodies of Melanotus hartii, described from spruce timbers in a gold-mine in Ontario, growing in darkness at depths of over 1600m, were not dissimilar to those obtained in culture.
FIG 129. The strange, stagshorn-like growth of Lentinus lepideus developed in the dark on timber in a mine (RBG Kew).
Pilát (1927) provided an account of several species of larger fungi from mines in Prříbram in the Czech Republic, most of which are now well-documented and known to be widespread. One of the commonest in Britain, to the extent that it was popularly known as ‘the mine fungus’, is the polypore Antrodia vaillantii, a pit-prop rotter occasionally also found in houses. Nowadays, the few remaining working mines in Britain use steel or other non-wooden props.
Many microfungi have also been recorded from mines, some developing on wood or debris, others obtained by isolation from soil or air. Fassatiova (1970) isolated 90 species of microfungi from the mines in Prříbram. These involved 25 genera, although species of Aspergillus and Penicillium were most frequent. Many were ubiquitous airborne fungi, present in the mines only as spores. Elsewhere, however, some microfungi have been responsible for serious health problems in mine workers. Sporotrichosis, a lesion-forming disease caused by the anamorphic ascomycete Sporothrix schenckii, is a notable example. Back in the 1940s it reached epidemic proportions among workers in South African gold mines, probably as a result of growth on untreated timber in conditions of heat and high humidity.
Fungi in natural caverns
Caves are similar to mines in many respects, but with no wooden pit props or other obvious substrata for fungal development. Mycologically, they are best known as suitable locations for growing mushrooms (Chapter 17), but in fact fungi are surprisingly numerous in this environment. Although cave fungi have received little extensive research, some important studies were published last century by Lagarde (1913, 1917, 1922) on fungi from cave systems in France, Spain and Algeria. Lagarde reported around 120 species, and although some were well-known fungi such as Stereum hirsutum and Peziza micropus, presumably from debris in the caves, nine were described as new to science, and 25 other potentially unknown species were referred to genus only. Fungi in general are considered an important component of typical cave biota, functioning as decomposers of organic substances (including dung), and supplying nutrients to other cave organisms where there is no primary production from photosynthesis. They also play a significant role as parasites on cave-dwelling invertebrates.
Most fungi recorded from caves are known elsewhere and are only incidentally present. The agaric Psathyrella corrugis, for example, was reported fruiting in complete darkness in a cave in Italy. However, there are a few fungal species that have so far been recorded exclusively from caves. These include the specialist ascomycete Laboulbenia lecoareri, a microscopic species on the integument of the cave beetle Trechus micros, widely distributed in northern Europe and known in Britain from Oxfordshire. The trichomycete Parataeniella scotonisci is known only from the hindgut of cave-dwelling isopods in the Pyrenees. More peculiarly, a microscopic ascomycete, Microascus caviariformis, has been described from rotting flesh in a cave in Belgium. This species is so far known only from a single location, the Cave of Ramioul near Liège, where it is evidently common on proteinaceous substrates. It was first discovered covering a discarded piece of cooked chicken, its tiny, densely crowded fruitbodies resembling caviar. It has since been found to be common in the cave system, developing regularly on such substrates within 3–4 weeks. It has also been shown to grow well at temperatures as low as 10°C. Although there is no indication that the species is especially adapted to caves (it also develops well, for example, at temperatures up to 25°C), it has been suggested that it may be associated with cave animals. Another ascomycete, ‘Lachnea spelaea’, was described (albeit invalidly) from cave systems near Trento in Italy. This fungus, a discomycete with tiny, whitish, hairy fruitbodies c. 0.75 mm across, grew in complete darkness on the cave floor apparently in association with bat droppings. It appears to have had no modern revision, but from the published description it seems likely to be a species of Trichophaea (Pezizales), not obviously matching any currently known.
Microfungi are also present in cave systems, as clearly evident from the work of Lagarde noted above, although little recent research has been published. However, in the Carlsbad Caverns in New Mexico a surprising total of 92 species of microfungi representing 13 genera has been recorded. These fungi were found within the caves at depths of up to 466 m, where darkness is total and there is an extremely low organic input into the system. It was suggested that they might be associated with organic matter produced from chemolithotrophic bacteria which utilise iron, manganese and sulphur in the limestone baserock of the cave. Entomogenous fungi were investigated by Samson et al. (1984) from cave systems in the Netherlands. These included the ubiquitous species Beauveria bassiana and Paecilomyces farinosus, but also two species, Hirsutella guignardii and Stilbella kervillei, known only from cave insects. The last occurs only in association with the Hirsutella and is parasitic upon it. Both fungi have adapted to development in cool, humid conditions and the complete absence of light.
Fungi and stalactites
A remarkable group of cave fungi occur in drops of water at the growing tips of stalactites, possibly influencing their growth form. One species, the anamorphic ascomycete Cephalosporium lamellaecola, has been regularly isolated from terminal drops of stalactites in Nevada, the hyphae also occurring sparingly in the surface layer of the stalactite. These hyphae are considered to act as crystallisation nuclei helping to bind crystals and effectively control the orderly growth of the stalactite. The fungus was found to be present in all actively growing stalactites in the cave system under study, to the exclusion of all other microorganisms. Nevertheless, it is not universally present in cave systems, although some other fungi may be. The anamorphic ascomycete Scolecobasidium anellii, for example, has been isolated from stalactites in Italy.
Deep subsurface fungi
Since the 1980s, considerable research has been undertaken into organisms living deep below ground, in rocks, subsurface sediments, and groundwater. These unpromising depths team with life, but mostly of a simple, single-celled, bacterial kind. Some few fungi, nonetheless, have made their chthonic homes in the earth’s dark places, over 100 (unspecified) taxa having been isolated from core samples up to 2.8 km below ground (Fredrickson & Onstott, 1996).
FUNGI IN ANIMAL BURROWS
Animal burrows are a further example of specialised underground habitats, and again have some interesting fungal associates. For example, no less than five taxa of Penicillium have been described from underground seed caches and cheek pouches of the banner-tailed kangaroo rat (Dipodomys spectabilis) in desert regions of North America (Frisvad et al., 1987). Four of these are known only from the rodent burrows, and are now recognised as distinct species. In Britain, the corticioid basidiomycete Trechispora clanculare was described as new to science from puffin burrows on the Welsh island of Skokholm, but has since proved to be more widespread and less particular about its habitat.
The large agaric Hebeloma radicosum is also associated with animal tunnels, in this case the underground nests of moles and mice. The species is widely distributed throughout the northern hemisphere, and its association with moles and shrew-moles in Japan was studied by Sagara (1978) and Sagara et al. (1981, 1989). The fungus has been shown to be directly associated with deserted latrines of these animals, and provides a reliable method for detecting their nests. In Japan it is accordingly known as ‘the mole nest finder’. Hebeloma radicosum has a long, rooting base which, if followed down to its origin, will be found to arise from a mass of soil and fungal mycelium. This mass unfailingly proves rich in animal excreta. The fungus has been found in Britain in association with the mole, and its association with the nests of wood mice has been subsequently reported from Switzerland. This fondness for the ammonium- and nitrate-rich soil of latrines provides an example of a specialised habitat which is shared by a number of other fungi, some of which commonly occur in the vicinity of corpses (Chapter Three).