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Topic: LICHENS: A SPECIAL CASE IN BIOGEOGRAPHICAL ANALYSIS

Biogeography is the study of the geographic distribution of organisms, including the typification of their distribution patterns, and the analysis of laws and causes regulating them. In my opinion, Biogeography in general has suffered from the widespread use of reductionist-mechanistic paradigms of explanation, in spite of its being a synthetic discipline 'par excellence', requiring, more than others, a holistic-interdisciplinary approach: after all, uttermost complexity is the main feature of any distributional area... This topic, however, would lead us too far. Here I would just like to stimulate a discussion on new perspectives, methodologies and basic assumptions in lichen Biogeography. Due to obvious space constraints, I will have to limit myself to a few scattered statements, hoping that they could help in promoting some re-thinking in a field which, in my opinion, badly needs it. I begin with an obvious, but important consideration: lichen Biogeography still largely follows the same basic concepts, and even the same terminology, as developed for vascular plants in Phytogeography. Is this always correct? It is true that both vascular plants and lichens are poikilothermic organisms, but: a) most lichens are also poikilohydric, unlike most vascular plants, b) lichens seem to have much slower evolutionary rates, c) the dispersal mechanisms of lichens are quite different, and d) their distributional areas are, on the average, much wider. Just an example: many lichenologists, especially in Europe, have tried to interpret the distributional areas of lichens from a 'local-taxonomical' point of view, by distinguishing different distribution types ("floristic elements"), several of which clearly show their weakness when the analysis is enlarged to wider regions. Such "floristic elements" are often named according to well-established concepts of Phytogeography (Arctic-Alpine, Boreal-montane, Mediterranean, etc.). However, how often does an 'Arctic-Alpine' lichen belong to the same element of an 'Arctic-Alpine' vascular plant? We all know that this is more the exception than the rule, and that several lichens considered as Arctic-Alpine in e.g. Europe do also occur in such distant areas as the mountains of the Tropical zone, or even Antarctica. Many of them are crustose, reproduce sexually, grow on siliceous rocks, and belong to supposedly 'ancestral' groups of Ascomycetes: maybe these features have a deep meaning, which we are far from being able to reveal. The present State of the Art of lichen Biogeography, as I see it, shows a confused, scarcely original conceptual basis, without much integration of different disciplines, and with but poor efforts towards more logical-numerical approaches. Lichen Biogeography, in my opinion, should make a great effort to radically change its basic principles, and hence also its terminology; we should start re-thinking lichen Biogeography from a lichen perspective, and I am convinced that this is likely to drastically modify many of the currently accepted assumptions. - The distributional patterns of organisms depend on: a) geographical factors (spatial and ecological conditions), b) time, c) reproductive strategies, and d) dispersal mechanisms. Their typification requires at least: 1) a good taxonomic basis, 2) a sufficiently representative number of localities, 3) a knowledge of relationships between ecological requirements of a taxon and the ecological characteristics of the areas in which it occurs, and 4) a knowledge of tectonic events which have affected these areas (orogenetic processes, plate tectonics, climatic changes, etc.). Here are just a few comments on the previous points. - On the one hand, the interpretation of the species (as well as of the genus) concept is still very open to discussion in lichenology, and, on the other hand, several parts of the world are still very little known. Thus, basic data are still too scanty and fragmentary as to permit decent generalizations. Recent research shows many cases of the same species being named differently in different Continents, revealing an unexpected degree of similarity among distant floras, such as those of the circum-Mediterranean region, Sonora-California, and even parts of Australia and Tasmania. Furthermore, little is known on the genetics of lichenized fungi: how is that widespread but widely disjunct species are able to maintain such a high degree of morphological and ecological homogeneity? Genetic exchange seems unprobable. We also know that one and the same thallus can be formed by hyphae coming from different spores... Finally, little is known about the reproductive mechanisms of complex lichen thalli: their morphological, functional and ecological stability in widely distant areas are surprising. Vegetative reproduction seems to affect only a minor share of the total pool of species, being most frequent in presumably 'recent' groups. What do we know about the origin of lichens? Several authors hypothesized that fungi colonized the terrestrial environment at the same time of vascular plants (mycorrhizae or parasitism). However, why could have not lichenization been the first form of truly terrestrial life? Fungi and algae were abundant in freshwater streams before the Earth was colonized by life: those who have studied the strange combinations of cyanobacteria, fungi and cyanobacterial lichens which occur on south-exposed slopes of the Mediterranean area and on desert rocks with some water percolation will probably support this hypothesis. In the Cambrian, eucaryotic life was firmly established: the primitive siliceous rocks (granites, basalts) were there, ready to be colonized, while the climate was glacial, or cold. The atmosphere resembled that of today in terms of the concentrations of gases, but we do not know either what the vapour tension was, nor the atmospheric dynamics of those times. In Africa we find signs of interglacial periods and of an important process of plate migration. After that, climate became warmer, and the movement of tectonic plates started spreading in a north-south direction. My point here is that lichens are probably among the earliest organisms which colonized the terrestrial environment. To understand the relationships between their present distributions and present ecological conditions we should refer to the little we know about these conditions when lichens started to develop as the pioneers of terrestrial life. SUBSTRATA - Lichens, due to their slow growth and to their peculiar physiology, are particularly sensitive to the substrata on which they develop. Terrestrial habitats in the Palaeozoic consisted only of siliceous rocks and mineral soil: the first adaptive radiation in lichens is likely to have occurred on these substrata. The distributional patterns of silicicolous lichens (and especially of the most primitive taxa) might well be the most relevant for reconstructing their evolutionary history. Tree bark, on the contrary, is a much younger substratum. In the Carboniferous, the Earth was covered by arborescent Pteridophytes, but probably the evolution of saprophytic fungi capable of decomposing lignin was still on the way. The 'palm-like' structure of these first 'trees' was not very favourable to lichen growth. The radiation of Gymnosperms, i.e. the evolution of monopodial branching, favoured the creation of new habitats, tree boles and tree crowns, which, with a more efficient trapping of atmospheric particulates, often enriched in nitrogen compounds derived from the more intense animal life, were much more favourable for the adaptive radiation of epiphytic lichens. This should be considered when comparing distributional patterns of saxicolous and epiphytic lichens; by the way, one could wonder whether there are historical differences between acidophytic species mostly bound to conifer bark (supposedly older) and many neutro-basiphytic lichens, such as those of the Xanthorion alliance. As far as terricolous lichens are concerned, we should distinguish between lichens of mineral siliceous soil and those occurring on organic soil, the latter habitat certainly being much younger. Perhaps it is not a case that a relatively young genus, like Cladonia, finds its maximum diversity on such substrata. Similar considerations apply to several basidiolichens, which exhibit a much less intense adaptive radiation, both in terms of number of species, and of morphological and ecological complexity. OTHER ECOLOGICAL FACTORS - Lichens are particularly sensitive to microclimatic conditions, and this may be the reason why sometimes their distributions do not fully coincide with macroclimatic subdivisions of the Earth. As far as light is concerned, high-mountain lichens seem to have broad adaptations both to the quantity/qualities of total radiation and to the incidence of short-wave UV radiation. The photosynthetic mechanisms of lichen photobionts are basically the same as those of other terrestrial photosynthetic organisms, and lichens from different habitats often have the same type of photobiont: adaptations of the photobionts to light conditions could well preceed those of the lichen symbiosis! During the Cambrian, UVB radiation was probably more intense, but perhaps not much different to that of some desert areas today. Several species with a Mediterranean-Macaronesian-Californian disjunction occur in areas with high direct solar radiation, and might have differentiated at the margins of the ancient Thethys Sea: most of them are silicicolous (a minor part being bound to siliceous mineral soil), and only a few of them, such as Cetraria merrillii, are epiphytes. In Europe and elsewhere the lichens peculiar of the high 'Mediterranean' mountains still await a decent phytogeographic characterization: the floristic features of Mediterranean mountains, at least in Europe, were often interpreted on the basis of a 'North to South' perspective, which does not seem to be the most fruitful one: on the contrary, many "northern" species might have derived from "southern" ancestors. The dependance of lichen distributions from climatic conditions can be illustrated by a brief discussion of the term "Mediterranean" as applied to lichens. The total distributions of many so-called 'Mediterranean' lichens have nothing to do with those of Mediterranean vascular plants: lichens extend over much wider areas with similar climatic conditions (Isoclimatic Mediterranean Area of Daget), and do occur in widely distant areas with similar ecological conditions (Mediterranean and Irano-Turanic regions, California, parts of Chile and Australia, South Africa). How was such a distributional pattern achieved? By long-distance dispersal, or by the much older persistence of similar climatic conditions in these areas? I'd like to end with some final, and, in my opinion, fundamental questions: a) what are the barriers erected by Nature against lichen diaspores? b) what are the chances of a fungal diaspore to travel - and through what carriers - from e.g. the Arctic to Antarctica, and to find a suitable photobiont there? c) how can newcomers face the concurrency of indigenous species? d) is there any relation between distributional patterns of 'bipolar' species and tropospheric currents? Any evidence for or against these questions? ...I guess that much exciting work is still ahead of us...

Eva Barreno, Valencia

We would like to thank Eva Barreno for the introduction to this subject, and welcome this long-overdue discussion. Many statements on lichen biogeography rest heavily on common assumptions and preconceptions on the evolution of lichens, some of which we think could usefully be included in this discussion. We would like to take the opportunity to point out a few details concerning one of the most often repeated statements about the evolution of lichens - that many extant groups of lichenized ascomycetes are likely to be very old in comparison with other ascomycetes and that the lichen life-style itself is ancient (Hawksworth, Bot. J. Linn. Soc., 96, 1988, and references summarised there; Galloway, Symbiosis 11, 1991, and in Hawksworth: Ascomycete Systematics, 1994). Our aim here is not to criticise the authors of these papers (their scholarly studies are excellent), but to show that their statements and conclusions should not just be repeated in publications produced today without critically assessing what support these conclusions have from recent hypotheses on natural, evolutionary relationships. Lichenized fungi of some sort may date back to Devonian time (Taylor et al., Nature 378, 1995) but as the fungi generally are very poorly represented in the fossil record, it is extremely difficult to suggest if this is 'old' compared with fungi in general. We must base our assumptions of the origin and relative age of lichens on corroborated phylogenetic hypotheses which by necessity must be based on data from extant taxa. That we must look for evidence of antiquity in present-day taxa is also the explicit views of Hawksworth (Bot. J. Linn. Soc. 96, 1988) and Galloway (in Hawksworth: Ascomycete Systematics, 1994). The papers by Gargas et al. (Science 286, 1995); Eriksson & Strand (Syst. Ascomycetum 14, 1995); Landvik (Thesis, Univ of Umeå,1996); Wedin & Tibell (Can. J. Bot. 75, 1997) and Wedin et al. (Pl. Syst. Evol. 209, 1998) - all based on the same pool of publicly available SSU nrDNA sequence data from the EMBL/GenBank database - are examples of testable hypotheses of lichen evolution published to date, which are based on data and not on individual researchers assumptions about evolutionary scenarios. Do we find any support for the idea of lichens as ancient fungi in these papers? No - recent molecular phylogenetic hypotheses gives no support whatsoever for viewing lichenization as an 'ancient' state, neither within the fungi in general, nor within the ascomycetes in particular. The extant lichen groups included in these analyses are all likely to be derived - their ancestors have evolved after the main split of ascomycetes and basidiomycetes, and after many major lines within these have radiated. In fact, Lecanorales, the order to which most lichens belong, and the group to which almost all taxa usually mentioned in the discussions on 'ancient' lichens belong, is very likely to be a relatively advanced group within the ascomycetes, judging by published phylogenies. Some earlier statements are, of course, clearly supported by the phylogenies cited above, including that Lecanorales suborder Peltigerineae (Peltigerales) are likely to be basal within the Lecanorales (Hawksworth, Trans. Brit. Mycol. Soc. 74, 1980). In the published SSU phylogenies, many lichenized groups are admittingly not represented. Many of these are included in still unpublished investigations by other workers, and are thus hard to include in this discussion. These unpublished studies do not, as far as we are aware, contradict our statements here. Thus, anyone who wants to claim that lichens are 'older' than other fungi must invent extinct hypothetical lichenized fungi which have no extant lichenized descendants, if they want to postulate that lichens are ancestral to (or older than) other fungi. If we accept such speculations, we may create whatever scenarios we want and need to suit our preconceptions. Clearly, for biogeography, systematics, and all branches of lichenology, we need to have our basic assumptions as well corroborated as possible by evidence from different sources. We cannot continue to use hypotheses that modern research does not support.

Mats Wedin, London and Martin Grube, Graz

Brava Eva ! A stimulating introduction to a topic where discussion was badly needed. The lichen floras of important areas such as the Hymalayas, SE-Asia, and the Andes, are almost unexplored, while better known areas are still a mine of surprises: in Central Siberia I have found myself (Tretiach, Nord. J. Bot., in press), a new species of Waynea, a supposedly 'Mediterranean' genus (the Siberian species is covered, of course, by a coat of hairs...), while progress in the exploration of areas such as North America, New Zealand, and Australia, is considerably enlarging the distributional ranges of many 'Old World' species. Such a situation represents a serious constraint for anybody interested in establishing decent distributional patterns for lichens. Should the conclusion be that times are not yet ripe for a sound development of lichen phytogeography? If we agree - somebody certainly does - we should just shut down and wait... but for how long? When von Humboldt started to outline floristic realms, the botanical exploration of the world was not much better. I think there is nothing wrong in trying to outline distributional patterns within Europe only, as this, a small appendix of Asia, is the best explored part the world. Furthermore, we should try to quantify more rigorously floristic similarities among climatically similar, but distant areas: one often reads about 'similar' lichen floras in 'Mediterranean' areas of the world, but most of these statements are based on a few selected species only. Maybe, when whole floras will be compared, these affinities could prove to be much lower, depending on a few ecologically and geographically broad-ranging species only, for which molecular studies could perhaps demonstrate an unexpected degree of genetic polymorphism (work ahead for molecular people!). Correctly, Eva suggests to avoid following blindly concepts and terminologies derived from the phytogeography of higher plants. Lichens are much more sensitive to micro- than to macro-climatic conditions, and their distributional areas do not always coincide with 'classical' bioclimatical-floristic-geographic regions. Lichenologists should perhaps develop a terminology based on bioclimatic criteria, avoiding the use of geographic epithets such as 'Alpine' (a contradiction for biogeography?).

Mauro Tretiach, Trieste

Three remarks: 1) Is the evolutionary age of lichens the same as that of lichenization? This sounds odd to me. Barreno referred to lichens of extreme dry-hot habitats (e.g. Lichinaceae) as presumably old. Now, is there really a wealth of DNA data unmistakably showing that these lichens are not old? DNA data from Parmelia & Co. cannot falsify the hypothesis of Barreno (a 'hypothesis that modern research does not support'?). Such hypotheses, on the contrary, could stimulate 'modern researchers': a) to work harder on something interesting, and, b) to wait until they can come with solid, and then most welcome, data. 2) The broad ranges of several cryptogams could be a result of long-distance dispersal, and not of old evolutionary age; if this were true (I think we have some evidence on that), what should we do with lichen phytogeography and plate tectonics? 3) This is just a meditation: Discovering a new species may well be something very special and important, but - after all what was heard here - discovering a new synonym could be even more important...

Louis Le Bois, Venice

Not only the few studies from lichens, but also the phylogenetic data from non-lichenized fungi show that the groups containing lichenized fungi are phylogenetically more advanced than other fungi. For the rest, I must agree with Le Bois: 1) Just look at tracheophytes: here we have taxa which are at least 200 million years old (Gingko biloba), and others which arose yesterday. Why should lichens be different? Lichen symbiosis could have just been a further possibility of adaptive radiation for several fungi, and might have occurred several times: look at the nice example by Lutzoni (Proc. Natl. Acad. Sci., USA 94, 1997), showing that lichenization brought about an increase of evolutionary rates in Omphalina. 2) To me, the most dramatic proof of the importance of long-distance dispersal comes from the study of the Antarctic lichen flora. Earlier hypotheses of an old, Gondwanaland persistence of lichens, apparently supported by the absolute dominance of endemic taxa, are crumbling against the discovery that many of these 'endemics' are synonyms of much more widespread, often bipolar species. Linskens et al. (Polar Biol. 13, 1993) demonstrated the existence of a considerable airborne flux of spores from Austral origin (see also Engeskjön & Jørgensen, Norsk Polarinstitutt Skr. 185, 1986). Birds were already considered as good distributional carriers by Darwin. If they can propagate the seeds of higher plants, why should they not be able to propagate fungal diaspores, or soredia? (Bailey & James, Lichenologist 11, 1979). Sterna paradisiaca migrates every year for 12,000 km from the Arctic to Antarctica. Other birds move through subantarctic islands, and then to South America... However, there is a question left to Le Bois: if long-distance dispersal were the key of the whole story, than we should expect similar lichen floras in all distant areas with similar ecological conditions. And we know that this is not true...

Mauro Tretiach, Trieste

Here are some points of view from a phanerogamist, albeit from one also interested in lichens. Facts distinguishing the biogeography of cryptogams (bryophytes should be also included) from that of spermatophytes are: 1) Cryptogams are poikilohydric, 2) their habitats are much less dependent on macroclimate, 3) dispersal mechanisms are much more effective, and 4) the degree of chorological knowledge is much worse. Additionally, their distribution patterns are influenced, as those of all organisms, by historical factors and by the ecology of the taxa. In biogeography, not only the localities where a organism is present are important, but also -and especially- those where the organism is certainly absent: many distributional maps of lichens show just the areas where lichenologists were active... The points 1), 2) and 3) water down the system of categories (floristic elements) as developed for cormophytes but do not make their use impossible. Points 2) and 3) also show some causes for the much broader distributional ranges of cryptogams, possibly with a course of evolution deviating from that of spermatophyta. Point 4) stresses the great problems in the interpretation of maps and chorological phenomena regarding lichens, such as types of distributional ranges, definition of floristic elements, also using numerical methods, conclusions on evolution, etc. It is true that leaving aside established terminologies may give a feeling of liberation, like the proclamation of a revolution, but any revolutionarist must know the 'ancien régime' very well. There is a monumental work whose reading is highly recommended for those 'only' interested in lichen biogeography: these are the three volumes of Meusel, Jaeger & Weinert: Chorologie der Zentraleuropäischen Flora (from which I took the chorological data reported here). In the approach developed by Meusel and his school, the typification of the distributional areas of cormophytes takes into consideration: a) gradients of oceanity-continentality, b) the zonal range of an area, and, c) its altitudinal position. Is a more meaningful grouping scheme conceivable? I assume that this system, with some necessary additions, could be appropriate to deal with lichens as well. A completely new system would also add difficulties in interdisciplinary communication. It is true that sometimes chorological terms worked out for cormophytes lose their meaning when applied to lichens, when taxa of identical taxonomic rank are compared. A fictionary 'Lichen alpinus' could be an arctic-alpine element in the European flora, just as Erigeron uniflorus. On a world-wide scale Lichen alpinus could become a bipolar orophytic-alpine cosmopolitan taxon, while Erigeron uniflorus or, with a wider range, Gnaphalium supinum, are arctic-alpine on this wide scale, too. In German we usually distinguish between alpin=in the alpine altitudinal belt and alpisch=occurring in the Alps. In English, terms such as alpine and alpigenous could be used. Some amazing likenesses appear when lichen species and higher taxa of cormophytes are compared. The genus Erigeron is also an oreal-alpine-cosmopolitan element (holarctic-Andine + eastaustralian, in young high mountain regions), as well as the genus Gnaphalium s.lat. (southern and suboceanic-meridional-submeridional mountains), just like Lichen alpinus. The family Frankeniaceae shows the same worldwide distribution pattern as some 'Mediterranean' lichens: (austr-austrosubtropical circpol-boreosubtropical-submeridional continental 1-3 + lit Africa + W America + Europe-W Asia). The same applies to the group of genera of Filago within the Gnaphaliinae (Compositae): Bombycilaena (Eurasian + Californian), Evax (Mediterranean + Californian-Arizonian), Psilocarphus (Californian + Chile), Filago (Eurasian/N African + Californian). Actually, the term 'Mediterranean' (the area around the Mediterranean Sea) is often confused with 'meridional' on a world-wide scale. By the way, such distributional similarities of different taxonomic ranks might prove to be slightly suggestive of their relative evolutionary ages... A final thought: theoretical considerations on the origin and evolution of lichens should not precede a discussion on their biogeography. The sequence, in my opinion, should be reversed: 1) fieldwork, 2) mapping, 3) typification of distribution patterns, 4) inclusion of geoecological factors, and 5) reflections on relationships and evolution of the mapped taxa. Thus, I do not know whether Barreno is right when she says that much 'exciting work' awaits lichens biogeographers: what lies ahead is hard field survey, mapping, basic taxonomic research, painstaking studies on long-distance-dispersal mechanisms, and on mechanisms of establishment, etc. But, at the end I realize that I am finishing with the same questions as those posed by Eva Barreno! (I thank A. Beck, München, for critical reading).

Franz Schuhwerk, Bot. Staatssammlung, München

Recently, I was asked to review the thesis of Birgit Litterski on the lichens of 'Mecklenburg-Vorpommern'. Her approach to phytogeography is interesting, as she follows the system proposed by Meusel and his school. I hope that at least parts of this huge work will be published soon. Further field work is badly needed, but I would not exclude a priori any 'theoretical' consideration; after all, science develops through an interplay between inductive and deductive thought. In my opinion, Eva's contribution is a mine of ideas and working hypotheses. The 'substrata' story, in particular (p. 19), should be taken seriously, as it could trigger further interesting research.

P.L. Nimis, Trieste