Trans. Br. mycol. Soc. Vol. 62. Plate 20

M. B. ELLIS

President, 1973

(Facing p. 225)

Volume 62, Part 2

Trans. Br. mycol. Soc. 62 (2), 225-230 (1974)Printed in Great Britain

PRESIDENTIAL ADDRESSDEMATIACEOUS HYPHOMYCETES IN BRITAIN

By M. B. ELLIS

(With Plates 20 (Portrait) and 21)

1974

Although far more dematiaceous hyphomycetes are found in tropicalcountries than in temperate ones the group is quite well represented inGreat Britain. We have about 200 genera and just over 600 species. Manyof them are extremely common and indeed some of them, e.g. Cladosporiumherbarum and Alternaria alternata, are among the commonest and mostwidely distributed of all fungi. At least 150 can be classified as reallycommon. However, they cannot be said to be well known. Algae andlichens cover large areas of the trunks of trees, of palings and even rocksand walls and are a familiar sight to almost everyone. You cannot takea walk in London parks without seeing them. Dematiaceous hyphomycetes,and in fact most micro-fungi, seldom occur in such profusion and do notgenerally catch a walker's eye. But this does happen just occasionally.A member of the Essex Field Club walking through Wanstead Park oneday during the autumn of 1945 noticed a dead, standing sycamore treewhich had shed its bark. The trunk was covered all the way up by a velvetycoat of blackish brown spores. By 1948 when I saw the fungus, which is nowcalled Cryptostroma corticale, for the first time, there were about 40 dead ordying sycamores in the park. Large areas of bark had peeled off exposingenormous masses of spores. Again, in the autumn of 1969 whilst mowingthe grass in Cranford Park, Middlesex, one of the groundsmen becamecovered with a black deposit. A matchbox full of spores scraped from thehandles of the mowing machine was sent to me and found to be an almostpure sample of Pithomyces chartarum, a fungus little known in this countrybut well known in New Zealand as the cause of facial eczema in sheep.Cranford Park is, as far as I know, the only place where this fungus is soabundant, but it has been isolated from mouldy hay at Newmarket andfrom the air around Cambridge. Dr P. H. Gregory found it after a lot ofsearching on Holcus lanatus at Virginia Water in 1961 but he tells me thathe now finds it quite easily on Harpenden Common. The black cellarfungus, Rhinocladiella cellaris, which sometimes covers the walls and ceilingsof wine cellars and may spread on to the shelves and the wine barrelsthemselves is quite a show piece. It is said to serve a useful purpose inregulating the moisture in the atmosphere.

Most dematiaceous hyphomycetes are however shy and retiring; theyflourish best when undisturbed. About one-third of all species known inthis country grow on dead and often rotten wood and bark and manyothers are found on dead herbaceous stems. Old hedges where brancheshave been left lying and grass and brambles have overgrown them provide

Vol 62, Part 1 was issued 8 March 1974

15 MYC 62

226 Transactions British Mycological Societygood hunting grounds as do heaps of cut branches and sticks in openmixed woods. Fallen beech cupules and mast of oak and chestnut are veryproductive. Hyphomycetes like moisture but are difficult to collect in therain. The majority of our wood and bark species are not specific to anyone kind of tree and many grow equally well on dead branches of bothbroad-leaved trees and conifers. They include beautiful and interestingspecies and a single trip to the woods can provide any or almost all of thefollowing: Acrogenospora sphaerocephala, Bactrodesmium obovatum, Catenulariacuneiformis, Dictyosporium toruloides, Helicoon ellipticum, Pseudospiropes nodosus,Septotrullula bacilligera, Sporoschisma juvenile, Triposporium elegans andTroposporella fumosa as well as anything up to 100 others. Some, like theOedemium state of Chaetosphaerella phaeostroma, Septonema tetracoilum and theHelicosporium state of Tubeufia cerea, are constantly associated with dia­trypaceous fungi. Others, such as Exosporiella fungorum, Spadicoides xylogenaand Spondylocladiella botrytioides colonize species of Corticium and on thewoodland floor old sporophores of Russula nigricans sometimes supportsporodochia of Myrothecium inundatum.

If woods are edged with rhododendrons we may find that these areinfected by a very striking fungus, Pycnostysanus azaleas. Terminal flowerbuds are first affected, later lateral leaf buds and stems are attacked. Whena twig is infected flowers fail to develop, leafy shoots become necrotic andcarry viable conidia for several years. It is easy to spot infected buds whichbecome dwarfed, turn first brown and then silvery grey. The synnemataof the fungus form a forest over the surface and make the buds look as ifthey have black spines. In England bud blast of rhododendrons is wide­spread and is particularly prevalent and severe in sandy areas of Surreyand Berkshire where it has been found to be associated with large popula­tions of the leafhopper Graphocephala coccinea which appears to help spreadthe disease. It is known that infection can occur through wounds made bythe insects' ovipositors.

A number of the species commonly found on wood and bark occur alsoon dead stems of herbaceous plants but these have also their own charac­teristic microflora. Periconia byssoides and P. minutissima flourish here,Dendryphion comosum, D. nanum and Torula herbarum abound and often theexquisite Endophragmia atra or its relatives E. elliptica or E. prolifera come tolight with a little searching.

The reedswamps and fens of the Norfolk Broads are particularly rich ininteresting species which flourish in the humid conditions prevailing therein the dense mass of vegetation. Most of them are saprophytes found ondead leaves of sedges, reeds, rushes and on dicotyledonous plants withrelatively stout stems such as meadowsweet and hemp agrimony.

The great saw sedge, Cladium mariscus, characteristic of areas withrestricted water circulation has large, tough, long-lived leaves which whenthey do eventually die are very resistant to decay and act as both a sub­stratum for the growth of fungi and close cover to ensure shelter andinsulation. Tetraploa aristata is one of the fungi that can be found here allthe year round, spring gatherings showing large numbers of youngdeveloping spores whilst those made in late summer, autumn and winterhave mostly mature conidia. The spores of this fungus with their long

Presidential Address. M. B. Ellis 227

appendages remind one of Professor Ingold's remarkable aquatic hypho­mycetes. When leaves with colonies of the fungus on them are placed inwater conidia break off readily and float to the surface where they remainfor several hours. Tetraploa is most commonly found on leaf bases andstems just above soil level. Where marshes and fens are subject to periodicflooding it is probable that flood water plays at least a part in the dispersalof the spores.

Another handsome marsh and fen hyphomycete is Clasterosporiumearieinum, one of the very few fungi found in this country with hyphopodiatesuperficial mycelium. It grows on the broad-leaved sedges, Carex aeutiformisand C. riparia. Young colonies of the fungus do not cause local discolora­tion of the host tissues but leaves are eventually killed. The conspicuousblack, velvety colonies are confined mainly to the abaxial surface of theleaf bases and are seldom found at a height of more than go em. above thesoil. Old colonies often cover the whole width of the outer surface of a leafbase and may spread around the edge to the inner surface; they vary inlength from a few mm to 24 cm. C. earicinum is initially parasitic on greenleaves. The mycelium is superficial, adhering closely to the leaf surface,and the hyphae bear laterally many lobed hyphopodia. A pale spot in thecentre of each hyphopodium indicates the point of emergence of a thinstrand of mycelium which penetrates the cuticle of the leaf to form ahaustorium in the epidermal cell below. When the host leaves eventuallydie the fungus continues to live on for a time as a saprophyte and themycelium proliferates to form an almost solid mass of thick, closely inter­woven and anastomosing hyphae. The large, septate conidia are bornesingly at the tips of erect conidiophores and it is easy to see in this speciesthat the wall of the conidium is just an extension of the whole wall of theconidiophore. In modern parlance their development is holoblastic. Sedgeson which C. earieinum occurs are usually found on marshes subjected toperiodic flooding. The large conidia have been seen floating on the surfaceof dykes but have never been caught in spore traps in the air. They canfloat for at least 3 weeks and when placed in water are found to beextremely buoyant and difficult to submerge. Conidia do not as a rulegerminate in tap water but up to 94 % germination has been obtained ina damp chamber when pieces of fresh green sedge leaf were added.

Deightoniella arundinaeea is found on reeds where these grow on hardground along the sides of paths; neighbouring reeds growing on softerground do not seem to be attacked. Infection is systemic. When thefungus starts to form conidia infected plants can be detected easily, notonly by their stunted growth, but by the grey colour of the leaves; thiscolour is due to the fungus itself as there is, in the early stages, no discolora­tion of the host tissues. The leaves die prematurely and the colonieseventually become black. Curvularia erepinii, which grows on the leaves ofOphioglossum vulgatum, is one of the few species of this mainly tropical genusfound in the British Isles.

The genus Arthrinium, although not confined to marshes and fens, is verywell represented in these habitats. The discrete dark brown or blackpulvinate colonies are sometimes mistaken for rust pustules. The myceliumis partly superficial, partly immersed and often the connecting hyphae

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228 Transactions British Mycological Societybecome very narrow where they pass through the host cuticle. The basauxicconidiophores develop from subspherical, ampulliform or barrel-shapedconidiophore mother cells and are often characterized by having verydark, thick transverse septa alternating with colourless cells. The conidiain different species have all sorts of curious and distinctive shapes.

These arejust a few of the interesting and beautiful hyphomycetes whichmake a trip to the East Anglian broadland fens worthwhile. The mostfruitful collecting in these areas is done in the reedswamps and fens wherethe vegetation is dense. River banks where mud is washed up anddeposited on plants are unrewarding and few dematiaceous species arefound in thickets of sallow and alder.

So far we have looked mainly at saprophytic species, and a few of theparasites which are well represented in our natural habitats but have beenlittle studied. Much better known are the parasites of economic crops.Many of you will be familiar with Thielaviopsis basicola, the cause of blackroot rot which has a wide host range in this country but seems to be muchcommoner in the north than the south. On tomato it may cause seriousreduction in yield and peas are sometimes badly affected especially insoils where there is a high lime content. The grey mould Botrytis cinerea isperhaps best known on lettuces which are often badly attacked in glass­houses and frames, but almost all crop plants are liable to infection by it ifconditions are sufficiently humid. Fifteen other species ofBotrytis are foundin our fields and gardens. Diseases caused by them include neck and bulbrot of onions, anther mould of red clover, corm rot and leaf spot ofGladiolus, lily disease, chocolate spot of field and broad beans, fire ofhyacinth and tulip, smoulder and fire of Narcissus and peony blight.Fourteen species of Alternaria and thirteen of Cercospora occur but few ofthem are of real economic importance. Alternaria solani is widespread onpotato but does little damage; on tomato it may cause serious losses in hotsummers in the south. Chalaropsis thielaoioides which is sometimes responsiblefor surface blackening of stored carrots is an interesting fungus which hastwo forms of conidia and is useful for demonstrating phialides. The genusCladosporium is not by any means always saprophytic. Gummosis ofcucumber is caused by C. cucumerinum, and other species are found on leafspots of timothy, spinach, carnations, sweet williams and Iris. Species ofDrechslera cause leaf spot and seedling blight of oats, leaf stripe of barley,blight of timothy, net blotch of barley and rye-grass, foot rot of variouscereals and ink disease of Iris. These are commonly, but I fear incorrectly,referred still to the genus Helminthosporium and it is perhaps appropriatethat I should explain here briefly what Helminthosporium really is and howit differs from Drechslera.

The type species of Helminthosporium, H. velutinum (PI. 2I, fig. I), is one ofour commonest wood and bark fungi which I must have collected well overa hundred times. It forms extensive hairy black colonies on dead twigs andbranches often extending along them for many centimetres. The erect, stout,thick-walled conidiophores bear their conidia in verticils. The conidiadevelop laterally through minute channels in the thick outer wall beneaththe septa whilst the tip of the conidiophore is actively growing . Growthof the conidiophore ceases with the formation of terminal conidia. The

Presidential Address. M. B. Ellis 229

conidiophores are never geniculate and never have dark scars. In Dreehslerathe conidiophores are often geniculate with dark scars. The first conidium,not the last, is formed at the apex of the conidiophore. After the firstconidium has developed the conidiophore grows out laterally below thescar, sometimes splitting the side wall, pushing the scar to one side thengrowing on for some distance before forming another conidium at thenewly constituted apex. The development is sympodiaI. Drechslera (PI. 2 I,fig. 2) has two things in common with Helminthosporium, tretic conidiogenouscells and pseudo- or distoseptate conidia but the conidiophores are quitedifferent.

As the structure of the conidiophore and arrangement of the conidia inthe type species of Helminthosporium differ so strikingly from those of thewell-known grass pathogens it is not surprising that when a pathogenstrictly congeneric with H. velutinum was found on potato, an economicallyimportant host, it was placed in a different genus and called Spondylo­cladium atrooirens. The genus Spondylocladium was chosen because it wasthought that its type species had conidiophores with septate conidia inverticils. In fact the genus Spondylocladium was based on a species nowknown as Stachylidium bicolor which has phialides, not conidia, in verticils.The small, non-septate conidia are aggregated in slimy heads at the tipsof the phialides (PI. 2 I, figs. 3, 4).

I will leave plant pathogens at this point to consider a few of the othersubstrata on which dark hyphomycetes are found and some of their otheractivities. More than a third of the species offungi found in the seas aroundour coasts are dematiaceous hyphomycetes and two of them Zalerionmaritima and Cirrenalia macrocephala are amongst the most abundant. Overfifty species are known to occur in our soils. Very few grow on us fortu­nately or on our domestic animals but some of them trouble us by spoilingour food or damaging textiles and other manufactured products that weuse. Species of Cladosporium, Doratomyces, Oidiodendron, Gliomastix, Aspergillus,Stachybotrys and Ulocladium are responsible for deterioration of paper andbecause they can adapt themselves to low moisture availability, rapidchanges of temperature and minimal nutrition, fungi like Cladosporiumsphaerospermum and Aureobasidium pullulans constitute one of the principalcauses of paint disfigurement. Cladosporium resinae has frequently been inthe news because it can grow on aviation kerosene in the fuel tanks of jetaircraft where it causes filter blockage, capacitance gauge failure andmetal corrosion. It is possible, however, that the same fungus might be putto good use in clearing up oil pollution as some of its genotypes are highlyhydrocarbonoclastic.

It is a pity that few dematiaceous species are known to be beneficial toman. The use of Aspergillus niger in the manufacture of citric and gluconicacids has been established for years and I was very interested earlier thisyear at a meeting of the Society to hear how it was being used in theproduction of high protein food for animals. Apparently micro-fungigrowing in continuous culture are more efficient than any other organismsat manufacturing protein foods cheaply, and together with Fusariumsemitectum, F. graminearum and yeasts, Aspergillus niger is now helping tosolve the world's food problems. It seems certain that micro-fungi are

230 Transactions British Mycological Societygoing to play an increasingly important role in food production in thefuture and perhaps mycologists may look forward to better times ahead.

EXPLANATION OF PLATE 21

Fig. t , Helminthosporium velutinum which grows mostly on wood and bark and is the type species ofHelminthosporium ( x 375).Fig. 2 . Drechslera siccans typical of the graminicolous species still often incorrectly referred to thegenus Helminthasporium (x 600).Fig. 3. Helminthosporium solani on pot ato , incorrectly referred to the genus Spondylocladium asS. atrovirens ( x 375).Fig. 4. Stachylidium bicolor the correct name for the type species of Spondylocladium ; it grows ondead herbaceous stems (x 600).

(Photos D. Fry)

Trans. Br. mycol. Soc. Vol. 62. Plate 21

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