This painting by Dame Elizabeth Blackadder was commissioned by the University of Edinburgh before Sir David Smith retired in August 1994. For the painting, David selected examples of symbiosis – a piece of marble with lichens on it and several pieces of coral from California and Jamaica where he did research on these organisms. The book is open at a page portraying his hero, Sir Joseph Banks, and on the wall behind is a picture of Banksia. David is seen here explaining the significance of these objects to the audience present at the display of the picture – he never ceased to enjoy teaching. At the celebration, someone commented that David looked unnaturally severe in the portrait; this caused him to laugh, which was more familiar to the assembled company. (Photo: Ian Southern).
It is with great sadness that we report the death of Professor Sir David Smith, a world leader in the study of symbiosis and a wise university administrator. He was born in Wales, went to school in England, and then spent most of his academic life at Oxford University. However, from 1974 until 1980, he was Melville Wills Professor of Botany at Bristol University, England before returning to Oxford as Sibthorpian Professor of Rural Economy, and in 1987 was appointed Vice-Chancellor of Edinburgh University.
After becoming interested in plants at school, and gaining a first class degree from Oxford University, he developed an interest in lichens and studied their water relations, their ability to take up nitrogen containing compounds and their carbohydrate metabolism. As he remarked, “When I began experimental research into the physiology of lichens in the early 1950s, no one else in Britain was carrying out such studies, and relatively very few in the rest of the world. At that time there was little or no contact between those investigating different types of symbiosis, and the subject as a whole was regarded as having marginal significance to the biology of living organisms in general” (Smith 2011). By the 1960s, a few others in Britain began to study the physiology of lichens, for example George Scott in Glasgow and Kenneth Kershaw in London studied, respectively, water relations and nitrogen metabolism. This reflected a new focus on plant physiology and biochemistry stimulated by the availability of novel techniques that included radioactive tracers. At this time, Otto Lange in Germany began his pioneering work on photosynthesis in lichens, and Vernon Ahmadjian in the USA studied lichen resynthesis, and a little later Margalith Galun in Israel investigated symbiont interactions.
After graduating with a doctorate degree, David Smith continued research on lichens in Oxford, mainly working with radioactive 14C in order to understand how sugars produced by lichen algae or cyanobacteria moved to the fungal partner. He supervised postgraduate students, including Edward Drew, David Richardson, Allan Green, David Hill, John Farrar and Susan Chambers, who, after graduating with doctorates, pursued careers in Australia, Canada, New Zealand, England and Wales. David Smith also collaborated in Oxford with David Lewis at Sheffield University and Angela Douglas at York University, the latter subsequently moving to Cornell University, USA.
An expanding interest in lichens and symbiosis resulted in the formation of The British Lichen Society in 1958, of which David Smith was a founder member. In Israel, Margalith Galun realized that the literature on symbiosis was difficult to track down and that symbiosis as an area of study was inadequately served by the periodicals then available (Richardson & Seaward 2013). As a result, in 1985, she launched a new journal entitled Symbiosis (Galun 2011), published with the encouragement of Miriam Balaban of Balaban Publishers. The journal was initially published on a quarterly basis, but more recently, there have been nine issues per year. In 1987, she co-opted David Smith onto the Editorial Board of the journal on which he remained for 30 years. This reflected the fact that he had extended his studies on lichens to examine other symbiotic relationships, especially coral-reef systems, where many corals, anemones, flatworms, molluscs and coelenterates host symbiotic algae. Thus, for several years, including a sabbatical year in California and Jamaica, he was primarily a marine biologist working in exotic tropical environments.
Once Symbiosis was published on a regular basis, it became clear that a forum was needed where those doing research on symbiosis, and publishing papers in Symbiosis, could exchange ideas. With the help of David Smith, who agreed to give the opening lecture, a Symbiosis Congress was organized and a new era in the study of symbiosis began. The First International Symbiosis Congress, held in Jerusalem in 1991, was a huge success: 250 participants from 27 countries attended (a Who’s Who of key researchers of the day) and the proceedings, published in Symbiosis, comprised 500 pages. Five years later a Second Congress was held at Woods Hole, USA where it was agreed to form an International Symbiosis Society. Regular ISS Congresses have been held ever since, the most recent, the Ninth Congress, being in Corvallis Oregon, USA (Richardson et al. 2019). After each congress, a proceedings volume has been published. David Smith took a keen interest in the development of the Society and wrote an introduction to the Seventh International Congress (Smith 2012). His opening address ‘The symbiotic condition’ at the First Symbiosis Congress earned him a well-deserved reputation as an entertaining speaker who could reflect upon developments and future directions in the study of symbiosis (Smith 1992). He was invited to give lectures around the world and his keynote address entitled ‘What can lichens tell us about real fungi?’ at the 1977 Mycological Congress in Tampa, USA entranced listeners, and impressed upon them, the importance and significance of the lichen symbiosis. To give a glimpse of David Smith’s talents as a speaker and his achievements, a transcribed version of this famous lecture is printed below.
Following his appointment as the Principal and Vice-Chancellor of Edinburgh University, David Smith returned to Oxford University in 1994 as President of Wolfson College. Both his academic leadership skills and his earlier research into symbiotic systems resulted in an influence which was worldwide and resulted in him being awarded a knighthood in 1986 and numerous other titles and honorary degrees.
Galun, M. (2011) The symbiosis community: how the journal, the conference and the society began. Symbiosis53: 47-48.
Richardson, D.H.S., Davy, S.K. & Selosse, M.-A. (2019) Introduction to the Proceedings of the 9th International Symbiosis Congress. Symbiosis (in press).
Richardson, D.H.S. & Seaward M.R.D. (2013) A tribute to Margalith Galun (1927–2012). Lichenologist45: 291-293.
Smith, D.C. (1992) The symbiotic condition. Symbiosis14: 3-15.
Smith, D.C. (2011) Symbiosis research in the 1960s. Symbiosis53: 48-49.
Smith, D.C. (2012) Symbiosis: twenty years after – how things have changed. An introduction to the Proceedings of the Seventh International Symbiosis Congress. Symbiosis58: 1-2.
WHAT CAN LICHENS TELL US ABOUT ‘REAL FUNGI’?
Professor D.C. Smith, F.R.S.
A Special Lecture given at the 2nd International Mycological Congress, Tampa, Florida. September 1977*
The Congress programme tells you when these special lectures begin, but doesn’t say when they end. This one may not last two hours; I hope it will be just about 57 minutes. Now, perhaps some of you may wonder how anybody gets to be invited to give a lecture like this. Let me quote from the original letter of invitation which I had: “The following caveats apply to general lecturers: Subject matter must have general appeal, be timely, constructive, perhaps entertaining or even amusing but absolutely not technical. They must remember that the audience has been bombarded with symposia all day long and are faced with the prospect of coming to another talk at a time of the day when many of them would just as soon be having a drink. You must appeal to the audience of diverse special interests and different levels of sophistication”.
Anybody fool enough to accept an invitation of this nature can be forgiven for starting off with this slide. May I have the first slide please? As you can see this is a gravestone, or as in America you persist in calling it a tombstone, covered with lichens. If I was so foolish as to accept this invitation it is for a particular reason, and that is that somebody in the mycological world has to speak up for lichens. The underlying theme of this lecture is that in the world of mycology, lichens are a minority group, and it’s important to understand in all this lecture that I use the word minority group in the political as well as the numerical sense. This is appropriate because in the world at large, this is the age of minority groups, tired of those who differ from the rest of the world, in skin colour, religion, culture, sex, etc., by giving voice to feelings that they are in some way not given their full rights by the majority. And so it is with lichens. Do they occupy their true and rightful place in the minds of those who would call themselves mycologists?
First, let me give a numerical justification for the significance of lichens as a minority group. For this I turn to the sixth, and most recent, edition of that standard text Ainsworth and Bisby’s Dictionary of the Fungi .... including Lichens”. Now, if one extracts the sizes of the various groups of fungi from this dictionary, one results in the following. From this one can see that lichens contain 29% of all fungi and the question is, does this large group occupy the correspondingly important place in the minds and thinking of those who presume to call themselves mycologists? I fear not, and my next task is to prove that lichen fungi are a minority group in the political as well as the numerical sense; and I shall do this by examining the organization of the programmes of International Mycological Congresses. The first congress held six years ago in Exeter was organized into a series of symposia. Now the symposia were grouped into major headings so the whole of mycology was encompassed by these major headings. Let us see how lichens fared. Only 6.7% of papers were devoted to them. Lichens have no structure, they do not reproduce, lack cell or genetic apparatus, have no physiology or metabolism and they’re certainly of no use. It is as if the organizers considered lichens as some mysterious kind of organism, something like-perhaps the mysterious agent of Lassa Fever. Well, six years later, here we are at the Second International Mycological Congress. Let us see if the treatment of lichens has improved. I now assign the invited contributions to this congress to the same major subheading as in the first congress. The organizers of this congress have broadened their concept of fungi to include some invited papers on algae. This apart, the treatment of lichen fungi has changed but little. In the last six years they have evolved no structure, no reproduction, no sex! Perhaps then you can begin to understand why many lichenologists sometimes believe that other mycologists do not think that lichens really are fungi: hence the title of this talk. This may sound an extreme statement, but let me ask this. Which is the journal in America that carries nearly all the papers about lichen fungi? – in other words, what is the third most important journal of pure mycology in America? I’m not talking about plant pathology. So, what is the third most important journal of pure mycology after, of course, Mycologia and Mycotaxon? – The Bryologist! Well, enough of this complaining!
My next task is to try to examine some of the possible reasons for the neglect of lichens. Continuing the language of minority group politics, the first question asked is, are lichen fungi in some way racially different from other fungi? Again, we turn to the Dictionary of the Fungi to see what groups occurred in lichens and here they have followed Mason Hale’s 1971 scheme. Now some of these orders are almost exclusively of lichen fungi such as the Lecanorales but others such as Sphaeriales and the Myriangiales are not. Now here comes what might seem at first sight to be a remarkable piece of prejudice. This Dictionary of the Fungi has no entry at all under Lecanorales! This order encompasses the majority of lichen fungi and so encompasses perhaps 15% or more of all fungi. Of course there are entries under Sphaeriales and Myrangiales, but no mention that these orders of fungi contain lichenized representatives. It forcibly reminded me of my schooldays in England when I learned Latin. The Latin text of Virgil’s Enid issued to schools had all the dirty lines carefully removed. One could detect the removal of a line because there was a break in the numbering, so we all rushed out to the Public Library to get the official text to translate it. We got nearly zero titillation but it was a hell of a good way to learn Latin! However, as some of you may realize, I’m painting the authors of the Dictionary in a grossly unfair light. They actually did want to integrate lichen fungi and it was the lichen taxonomists themselves who advised that not enough work had been carried out, at that time, on reorganizing classification to make such integration possible. Indeed to be fair to the authors, they do say in the Dictionary the following quotation, “It is logical that lichens should be seen as fungi to be assigned within the matrix of the classification of non-lichenized fungi”. In the next edition of the Dictionary, I’m assured that integration will occur, so you all have to buy it and throw away the sixth edition. Nevertheless the list illustrates that lichen fungi are a diverse group related to different free living orders of Ascomycetes; and indeed to paraphrase the words of a famous Noel Coward song, “Even some of Basidiomycetes do it! Let’s call it – well not love but symbiosis”. Here is an example of a Basidiomycete lichen. But anyway we can conclude, I think, that fungi are not really so taxonomically different or divergent from other fungi to merit permanent exile to some bryological wilderness.
The next thing to ask is it the kinds of organisms that lichen fungi associate with which puts them beyond the pale? We all know that lichen consists of an association between an alga and a fungus. But how many realize how few algae there are in a typical lichen. This transverse section of a lichen thallus should give you some idea that algae only occupy normally a small part in most species. The red stained parts in the slide are the algae and indeed, in most lichens, algae comprise but 5 to 10% of the whole. Should it be that this small touch of a photosynthetic tar brush should condemn lichens forever to the mycological garbage can? Here we can see fruit bodies of a real fungus and such fungi associate with things photosynthetic much bigger than themselves. This is a beechwood in England and these fungi associate through the medium of mycorrhizal roots. Here is one such root in which the proportion of fungus is but 5 to 10%, yet it is undoubtedly regarded as “real”. In any case not all associations of algae with fungi are considered lichens. All good botanists will recognize this as a seaweed Pelvetia canaliculata around British and European coasts. It invariably contains the fungus Mycosphaerella. But even without knowing the physiological nature of the relationship, Mycosphaerella is always accepted as a “real fungus” and Pelvetia as a seaweed. Some lichen fungi present an opposite problem such as Arthopyrenia fallax. Sometimes it contains algae, sometimes it doesn’t. But even if it doesn’t contain algae, it is still somehow regarded as a lichen. So these and other examples show that the boundaries are blurred. I’m now going to show you two slides and ask the question, “Are these organisms really so different from each other?” Here is the first and here is the second. The first is Caprodia, ‘a real fungus’, and this is Icmadophila which is not ‘a real fungus’ but a lichen. So far then we have seen that lichen fungi do not receive the curse of neglect on racial grounds or by reasons of the organisms with which they associate. Now this leads us into a more sensitive area and to the main body of this talk. Is it that this group of nearly 30% of fungi has so little of interest or relevance to the other 70%? In the political language of minority groups that I have been using, is it that they are too slow and too stupid to tell us anything? Indeed sometimes some lichenologists fear that there may be minority group jokes about them rampant among the mycologists. May I adapt the kind of idiotic story my seven year old son persists in pestering me with early in the morning. Question: What is long, grey, shrivelled, wears spectacles and hangs from a tree in Connemara? Answer: An Irish lichenologist!!!!!
To return again to the Dictionary of the Fungi, I read the following: ‘It is logical that lichens should be seen as fungi with an unusual mode of nutrition’. Now this implies that it is an unusual mode of nutrition which separates them from the rest. Now I submit firstly that the mode of nutrition is not unusual and secondly it is very relevant to many ‘real fungi’. Now as you all know there are three main modes of nutrition for fungi: saprotrophic, necrotrophic and biotrophic. Saprotrophic: feeding on dead organic material; necrotrophic: first killing organisms and digesting the remains, and biotrophic: which is obtaining nutrition from other living organisms.
Lichens are biotrophic in that they obtain substantial supplies of photosynthetically fixed carbon from algae associates. But how widespread is biotrophy among fungi in general? My colleague David Lewis is currently writing a book about biotrophy and has conveniently summarized the occurrence of this mode of nutrition amongst all fungi. I have to indicate to those of you at the back, that these are percentage symbols; they look like figures, but that’s 32%, 25%, 27% and so on. Please note that we anticipate the majority acceptance of Lynn Margulis’s view about the phylogeny of fungi that will be debated tonight, so, one can see that lichens represent a good example of a common form of nutrition amongst fungi. Now what is quite unarguable is that we know more about the mechanism of biotrophic nutrition of lichen fungi than of any other kind of real fungus. I am going to review very briefly the present state of knowledge of biotrophic nutrition of lichen fungi and assess its relevance to real fungi.
The main research of biotrophic nutrition started off with one particular lichen Peltigera polydactyla. Here it is growing in a field, and if you look at the slide, then you will begin to be able to make out the flat foliose olive green thalli. Here they are and this is how they grow naturally. Now this is a lichen in which the algal symbiont is blue-green. I’m not going to bore you with all the fine points of the various physiological and biochemical techniques which are used. Many people think that lichens are difficult to experiment with. Suffice it to say that most experiments use lichen samples which look like this. On the left you can see the cleaned lobes and on the right the experimental material which are neatly cut discs, so as to give very good and reliable experimental samples. Now when you study the process of photosynthetic transfer from alga to fungus, the following features emerge in this lichen. When it is in contact with fungus there is a substantial supply of glucose from the alga to the fungus. We have been able to establish this picture because of the following helpful points. The radioactive isotope 14C makes it easy to trace the path of products of photosynthesis. It is relatively simple to isolate and make pure preparations of algae from fungal homogenates. We recently have been able to block the transport process between the symbionts for at least four different points in its pathway, so that we can begin to characterize the membrane transport systems involved. Now the major features of biotrophic nutrition of the fungus of this lichen are therefore as follows. The flow of carbon is substantial. Up to 80% of all the carbon fixed moves along this path. Secondly, it moves predominantly as a single simple sugar. Thirdly, this massive release disappears rapidly upon isolation of the alga. Indeed within three hours of isolation glucose cannot be detected any longer. It is of course dangerous to assume that all 18,000 species of lichen behave like this. One would be in the same danger assuming, for example, that the physiology of all fungi is similar to some rather boring yeasts! Though we have in fact examined over 40 species of other lichens, in general they all seem to fit this pattern. But my question is: can this situation really be all that different from those non-lichenized fungi which are biotrophic? Now technically this is a much more complex system to study because the host is morphologically more complex and it is difficult to separate easily fungus from host. Indirectly we know that transport to the fungus is often substantial; for example, it has been estimated that the amount of carbon passing to mycorrhizal fungi in some Swedish forests is equivalent to 10% of total timber production. We infer that much of it may be transported as a simple sugar since so much carbon accumulates in the restricted range of the fungal carbohydrates, trehalose, glycogen, mannitol & so forth. Of course, as you all know, once you isolate higher plants from the system they no longer release massive amounts of carbohydrates. It is therefore reasonable to assume the mechanism of biotrophic nutrition in lichen fungi may have important similarities to other biotrophic fungi.
The key question of course is how does a biotrophic fungus induce a massive release of a simple carbohydrate from its host? Two main questions are currently being studied. Firstly, what is the stimulus from the fungus causing the alga to release specific carbohydrates - is it chemical, is it physical, or both? Secondly, what is the mechanism involved in the release? Is it some change in the permeability of the outer limiting membrane of the alga, or is it some change in the internal metabolism which generates very high concentrations of mobile carbohydrates or is it both? Let us look briefly at these questions.
Firstly the type of stimulus: one possibility is that the fungus secretes some chemical factors. Now we have searched exhaustively for such chemical factors but have failed to find them. We are somewhat reassured that they may not exist because in other kinds of symbiotic associations which we study, we can easily find extracts which stimulate release of specific compounds. Now I’ll show you some. If the organizers permit algal papers at the Mycological Congress, I hope you won’t mind a picture of a sea anemone. This is an example of something which is packed with symbiotic algae. If you cut a section of the tentacle you can see all those spheres are symbiotic algae and if you just look at the algae under the microscope that’s what they look like. Now, if you add to these isolated algae an extract of the animal tissue, then you will get a specific stimulation of the release of one or a very few kinds of molecules. So we do know that these compounds exist and that they exist in quite a wide range of animals. These, in case you are puzzled because you’re mycologists, are actually baby giant clams (so that’s not the foot of a giant!) being grown in perspex blocks because they are crevice organisms. The pretty coloured tissues there, are the mantle which is packed with symbiotic algae. This is a coral reef and it’s formed by an animal and the whole of that picture, except the lady, is covered by a tissue containing densely packed symbiotic algae. Again extracted tissues of the coral animal will stimulate release. Here is a mollusc that forms symbiotic associations with chloroplasts. In these again, you can get extracts which cause specific effects on the protoplants, but these extracts have no effect on lichen algae.
At this point, perhaps, I should explain (particularly with reference to Dr. Ahti’s kind introduction), why relatively late in my research life I have extended my interests outside lichens to associations of algae with animals. The official reason of course is to broaden my outlook. The private reason is fear of the phenomenon that I term the intellectual menopause! The intellectual menopause I define as that time when once ceases to be reproductive of new ideas. It can strike, as you all know, at any age!! The symptoms are not sudden hot flushes, but a rather sudden desire to sit on committees or exercise power over other academics. So if the chairman of your department or the head of your institute is being unkind, be patient and say that he’s just suffering from intellectual menopause! I have tried to avoid this difficult period by taking old ideas from lichens and applying them to new material. There is also another factor associated with increasing age and that is a question of physical comfort. Consider now the trials of collecting lichens with what I later discovered were the joys of going on coral reef expeditions. Or even better. When I look at slides like this I have to be honest with myself and ask, is it the intellectual kind of menopause which is bothering me? Anyway, away from the attraction of ladies and back to lichens.
At the end of this digression, I dealt with a point that we could not find any chemical stimulus although we have a lot of experience in this field so we feel that it may in some way be physical. It could be a general effect of the micro-environment which the fungus creates around the algal cell or it could be something more specific. An attractive possibility for example is that charged groups on the fungal cell wall can, in some way, alter the electrical characteristics of the surface of the algal cell. In all events, it has invariably been found, so far, that physical contact between the symbionts is essential to stimulate the release of specific carbohydrates. So much for the stimuli, but what about the mechanisms? In an earlier slide, I mentioned two possibilities. Changes in the outer permeability or changes in the inside. For a time, changes in the outer permeability idea was an attractive theory. This is because qualities such as membrane potential are profoundly important in determining direction of transport across membranes. An effect on membrane potential could have been one of the kinds of effects that the fungus may have on an alga. Attractive though this idea is, I have to confess that current research is not coming up with good evidence in support of this. We are therefore left with the second possibility, namely that the internal metabolism of the alga is changed so that a large concentration of the mobile carbohydrate is induced to accumulate at sites of export. Here there is some interesting evidence. Let me return for a moment to the lichen I started with, Peltigera polydactyla. This has blue-green algae and they fix nitrogen, and it is well established that almost all the nitrogen passes to the fungus. So that a correct picture for Peltigera should be the following: as you can see, products of carbon and nitrogen fixation move simultaneously to the fungus. Again, when the alga is isolated the release of nitrogen ceases almost immediately. Now recently, in Dundee, Bill Stewart and G.A. Rogers have shown that in free living blue-green algae, the first product of nitrogen fixation, ammonia, is converted to glutamine. But in the lichen symbiosis, the enzyme forming glutamine (glutamine synthetase) is repressed so a surfeit of ammonia is made available for release. One asks oneself, could a similar phenomenon be happening with carbohydrate release? This really is where the present state of research is, but the above does, I hope, highlight a variety of points which might well be borne in mind by those investigating ‘real’ or non-lichenized fungi which are biotrophic.
To go back to the poor old Dictionary of the Fungi which says that lichens have an unusual mode of nutrition. I submit that it is not the mode of nutrition that is unusual but that our understanding of it is unusually better than for real fungi. I now want to move on to the ecological aspects. You see I have to cater to all tastes and I step out of the area I know, to an area I don’t: into ecological aspects of biotrophic nutrition of lichens. For the majority of people, the supply of photosynthate from alga to fungus is regarded simply as nutritional and they are content to leave it at that. But the situation repays closer examination. Few people, in literature anyway, pause to stop and think why do lichen algae photosynthesize so efficiently and yet lichens grow so slowly? Let me show you some facts and figures. I’m sorry to have grown technical here, but the top group of data shows that lichen fungi and algae, in culture, grow very much more quickly than lichens in the field or even at optimum conditions in the laboratory. Also that photosynthetic rates of lichen algae are just as good as when they are in isolation and indeed the supply photosynthate is substantially greater than is needed to sustain growth. Indeed many lichens could obtain all the carbon they need to maintain their extraordinary slow growth from organic compounds dissolved in the liquids passing over them. So why bother to associate at all with algae? The answer, I think, depends on looking at the fate of the of photosynthetically fixed carbon in the fungus. It nearly all goes into a large internal pool of soluble carbohydrates especially mannitol. All lichen fungi have a high concentration of polyols inside them. Indeed mostly, they must normally be saturated solutions of polyols. Now the function of the algal symbiont is not so much the supply of organic carbon for growth as to maintain this high concentration of soluble carbohydrate. What is the function of this saturated carbohydrate solution? It seems to be part of the mechanism enabling lichen fungi to withstand environmental extremes. How does it do this? Firstly, lichens live most of their normal lives under conditions of moisture stress. A high internal osmotic pressure is obviously a great advantage in this. Secondly, almost all lichens undergo frequent cycles of drying and wetting in nature. During drying, water molecules, which may be lost from key cell structures, can be replaced by hydroxyl groups of polyols. Thirdly, on re-wetting, cell membranes take a period of up to 60 seconds to re-establish their permeability barriers. During this phase, the cell can’t help losing some of its contents. Hence, there is a continual need for these to be replaced. My colleague and ex-student, John Farrar, has devised a collective term physiological buffering to cover the various roles of the internal mannitol pool. How is all this relevant to ‘real fungi’? Lichens are not the only kind of fungi to live in extreme environments of fluctuating moisture conditions. One has only to think that the surface layers of the soil or epiphytic mycelia of certain plant pathogens; for example, polyols are predominant soluble carbohydrates of all fungi, except those of protist affinity. This fact is often obscured in textbooks of fungal physiology; why I don’t know, unless we are back with the problem again that most people seem to think that the physiology of yeast equals the physiology of fungi! Polyol concentrations have only rarely been measured in ‘real fungi’ in natural conditions, but when they have, they have been found to be high. Our experience with lichen fungi, may point to another fruitful avenue of research for those interested in the mechanisms as to how ‘real fungi’ withstand extreme environments.
From physiological ecology, we move now to descriptive ecology. Here the great advantage of lichen fungi is that compared to the nonlichenised ‘real fungi’, their vegetative mycelia are very easily visible and extremely permanent. It makes it much easier to plot the distribution and to make ecological correlation of distributions with environmental factors. Let’s look at some examples. Here is a classic example of easily recognized zonation of fungi on the seashore. Note how you quiver when I say fungi because you want me to say lichens. There is the black Verrucaria belt and above it the orange Xanthoria belt. Xanthoria is a fungus with a very striking distribution. Let us see what other Xanthoria species occur. This is a farm roof of the Field Station at Oxford University. You notice the yellow colouring; it becomes more obvious as you approach the roof. It is due to just one or two lichens, one of them being Xanthoria aureola, and here you can easily see the distribution of this fungus. As my colleague David Richardson has done, you can transplant this fungus to another habitat and observe it over a period of years. Here is where David transplanted Xanthoria aureola back into that seashore belt to see what effects the change of habitat would have for it. One can do other things. This, believe it or not, is my home town, and a good example of atmospheric pollution. We know how easy it is to measure the effects of atmospheric pollution on fungi if the fungi are lichenized. Here is a building block on a building in the city of Oxford. If you go just seven miles outside to an identical kind of building, with an identical material, erected at the same time, you can see a much richer flora. So some of the factors affecting the distribution of ‘real fungi’ must surely be similar to lichenized fungi – nutrient, pH, etc. The experimental investigation of these factors is relatively easy, but sadly not carried out. However, the little that has been done, makes it abundantly clear that investigations of petri dish cultures of lichen fungi produce results of little relevance to understanding their distribution. It is only the intact thallus that really provides useful information. This highlights differences between lichens and non-lichen fungi, which have led to major divergences in the kinds of techniques used to study them. The vegetative body of the lichen is of extreme permanence and because of its dependence on algae it is always at or near the surface so it is easy to see. The non-lichen fungus is evanescent and the principal object of experimental investigation has to be petri dishes. But these differences ought not to lead to complete divergence in the interest; of those who study lichens or non-lichenised fungi, rather it should lead, in the future, to complementation.
From descriptive ecology one invariably moves to taxonomy. I said it earlier that it was the unpreparedness of the lichen taxonomists which lead to some curious exclusions from the Dictionary of the Fungi. It should not be thought that the taxonomy of lichen fungi lags behind in all respects. There is one aspect in which the taxonomy of lichens is not only ahead of non-lichen fungi, but indeed of almost all other plant groups – that is chemotaxonomy. As it is well known, the colour reactions of certain chemicals with lichens has been in continuous taxonomic use for over a century. The last 30 to 40 years have seen the introduction of further and more sophisticated methods which enable a wide range of specific individual chemical compounds to be easily detected and used in taxonomy. Let me show you the distinctive crystals of just two of the chemical compounds important in lichen taxonomy. These are the crystals of the extremely common and delightful usnic acid, and here we see gyrophoric acid. More recently chemotaxonomy has become of increasing prominence in non-lichenized fungi. What could ‘real mycologists’ learn from lichenologists about chemotaxonomy? While they cannot learn much about the detection of specific chemical compounds, as most of these are absent from ‘real fungi’, they should look at the controversies amongst lichenologists over the use of such characters and see how they can avoid some of the bitterness and even quarrels over the value of chemical characteristic in taxonomy. Indeed, I have here a thick pile of correspondence, in my capacity as an editor of a journal, where I presumed to have to relate to a distinguished lichen chemotaxonomist, that the referees did not like his paper. I was going to read long extracts but as the author isn’t here, I feel that it is only fair not to quote some choice extracts from his four-page letter.
As I come towards the end of this (you will get your supper!), I hope that I have persuaded some of you that lichens do have something to tell us about ‘real fungi’. At one stage I had thought I would do this lecture the following way: I thought I would read out aloud a list of symposia at this congress to which lichenologists have not been invited to contribute and yet have something worthwhile to say. On reflection I decided that this would be just a little invidious despite the written encouragement of an organizer of this congress for me to be as bitchy as possible!! However there was one particular session which did catch my eye, my lichenological eye that is, and that is the special interest meeting on Friday entitled “Contribution of women to mycology”, because here after all is another minority group which deserves a hearing. But then I read the synopsis and became puzzled by one sentence which reads, “The history of the advance of mycology is liberally sprinkled with contributors whose first names are Flora, Vera, Margaret, Lilian, Alma, Rhoda, and many others. Now any lichenologist seeing this list is going to ask, “What about Annie?”, “Why don’t they mention Annie?” Whom you may ask is Annie? Well she was Annie Lorraine Smith – not just the greatest woman lichenologist, because that is very chauvinistic, but really one of the greatest regardless of sex. Her taxonomic contributions were substantial. She wrote the best lichen flora of its day, or helped to write it, and in 1921 published a famous monograph on lichens, which is such a classic that a revised version of it has just been published 55 years later. But what position did she hold throughout her career? She was born in 1854, and she started work on lichens towards the end of the nineteenth century, at a time when women were not officially admitted to the staff of the British Museum. From 1889 until her 60th birthday in 1934, 45 long years, she simply held the position of unofficial worker, working under the direction of a ‘real’ mycologist. One can’t help feeling that had she been a real mycologist, her fate later in life might have been better, she paid the penalty of being a double minority, not just a women in a man’s world, but a female lichenologist employed by a male mycologist. In the introduction to her monograph, she talks about the time of Schwendener when there was a great controversy with the idea that a lichen was in fact two organisms and she quotes from an opponent of this theory, the Reverend Crombie who soulfully describes it as an “unnatural union of a captive algal damsel and a tyrant fungal master”. Her position had sad similarities – a captive lichenological damsel by a tyrant chauvinistic fungal master. There is no point to my final slide, it is simply a British lion in an English stately home crumbling away from the attack of a minority group.
*From a recording made by David Richardson, and transcribed by Karen Dennie, a secretary at Laurentian University, and published with permission of David’s wife, Lesley, and Taylor Francis Ltd. that published a short version in Mycologia (1978) 70: 915-934.
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Richardson, D.H.S., Seaward, M.R.D. Professor Sir David Cecil Smith FRS (1930-2018): an appreciation. Symbiosis 77, 91–98 (2019). https://doi.org/10.1007/s13199-018-0587-7