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Lichenicolous Fungi: Interactions, Evolution, and Biodiversity The Bryologist 106(1), pp. 80 120 Copyright q 2003 by the American Bryological and Lichenological Society, Inc. INVITED ESSAY New Frontiers in Bryology and Lichenology Lichenicolous Fungi: Interactions, Evolution, and Biodiversity JAMES D. LAWREY Department of Biology, George Mason University, Fairfax, VA 22030-4444, U.S.A. e-mail: [email protected] PAUL DIEDERICH MuseÂe national d'histoire naturelle, 25 rue Munster, L-2160, Luxembourg; e-mail: [email protected] Abstract. The lichenicolous fungi represent an important ecological group of species that form obligate associations with lichens. They have been studied seriously for over 200 years and the European species are especially well collected. However, collecting in other areas has been far less systematic and many new species await discovery. North American species are especially under-studied and this review is intended to stimulate the collection and study of these species. To encourage this study by lichenologists, we review the sorts of interactions formed by licheni- colous fungi with their lichen hosts, discuss various aspects of host speci®city, virulence, chemical ecology, and evolution of lichenicolous fungi and provide a complete taxonomic listing of lich- enicolous genera arranged as far as possible into natural groupings. In each section we suggest research topics in need of further study, and provide a listing of signi®cant literature. We hope by calling attention to the largely unexplored biodiversity of lichenicolous fungi, investigators will take up the study of these fascinating organisms. Lichenicolous fungi are a highly specialized and (1896) also gave a list of lichen hosts, with an enu- successful group of organisms that develop on li- meration of the fungi present on each of them. chens and form with them three- or sometimes four Olivier (1905±1907) provided a detailed account of to ®ve-membered associations. They are relatively the lichenicolous fungi from France, and Vouaux inconspicuous and are rarely collected by non-li- (1912±1914) published a worldwide ¯ora with keys chenologists. Lichenologists in the past were not and descriptions of all known species. Keissler much interested in these fungi, perhaps owing to (1930) revised the central European species. These their lack of knowledge of non-lichenized fungi. works by Vouaux and Keissler represent invaluable Professional mycologists who would have been information still useful today. More recent compi- knowledgeable of the groups rarely studied this lations were given by Clauzade and Roux (1976 ± very specialized substrate. For these reasons, lich- with 457 species) and Clauzade et al. (1989 ± with enicolous fungi were poorly known until recently. 686 species). One of the ®rst examples of a lichenicolous fun- Hawksworth (1983) published keys to 218 lich- gus studied, described, and illustrated is Biatoropsis enicolous species known from the British Isles, and usnearum, a heterobasidiomycete forming large these keys stimulated many lichenologists to study gall-like structures on thalli of Usnea. Dillenius this fascinating group of fungi. Entire revisions of (1742) illustrated two species of the Usnea barbata three major groups became available, the licheni- group in the Historia Muscorum, one of them bear- colous hyphomycetes (Hawksworth 1979), the lich- ing numerous `orbiculos', which clearly represent enicolous coelomycetes (Hawksworth 1981), and basidiomata of the fungus. In 1795, Acharius dis- the lichenicolous heterobasidiomycetes (Diederich cussed and illustrated Usnea specimens infected by 1996). During the past 10 years, and especially B. usnearum (Fig. 1), and in 1810 he published ®ne since the publication of Santesson's (1993) The Li- color illustrations of this fungus. chens and Lichenicolous Fungi of Sweden and Nor- During the 19th century, many more species of way, lichen checklists of many European countries lichenicolous fungi were described, and Lindsay appeared, and most of them include lichenicolous (1869) presented a ®rst overview of the group. Zopf fungi. This encouraged many lichenologists to col- 0007-2745/03/$4.25/0 2003] LAWREY & DIEDERICH: NEW FRONTIERS 81 FIGURE 1. The lichenicolous heterobasidiomycete Biatoropsis usnearum that forms abundant gall-like basidiomata on the thallus of Usnea spp., as depicted by Acharius (1795). lect and study these organisms, and never before systematic arrangement for all lichenicolous fungi. have so many publications on them appeared and This is a more or less complete list of all genera, so many new species described. Since 1989, the which makes it an important update to Clauzade et date of the latest worldwide compilation (Clauzade al. (1989). It includes numbers of species per ge- et al. 1989), the number of species has approxi- nus, which indicates for the ®rst time since 1989 mately doubled, and this trend is in no way dimin- the number of known lichenicolous species, and for ishing, as exempli®ed by Etayo's recent work on each genus we provide references to important tax- Colombia, in which he describes 41 new species onomic papers. and enumerates many more specimens that could not be identi®ed (Etayo 2002). INTERACTIONS OF LICHENICOLOUS FUNGI There are two main objectives of the present pa- WITH LICHENS per. Firstly, we wish to give a general overview of current knowledge on lichenicolous fungi, focusing Fungi commonly associate with lichen thalli in on aspects that have often been neglected in the nature, but these associations are rather loose and past. Along with this discussion we offer a number non-speci®c in many cases. By de®nition, licheni- of hypotheses for testing. Secondly, we propose a colous fungi form obligate associations with li- 82 THE BRYOLOGIST [VOL. 106 chens, either as saprotrophs that colonize dead li- spread the saprotrophic niche is for lichenicolous chen thalli, or parasites that obtain ®xed carbon fungi. Hawksworth (1982c) mentioned that they ap- from living lichen hosts in some way (Hawksworth pear to be less diverse than parasitic forms; he sug- 1982c, 1988c,d). Parasites range from relatively gested also that many are probably not obligately nonaggressive, commensalistic forms that cause no lichenicolous saprotrophs. This would suggest that obvious damage to aggressively virulent types that saprotrophy is a rarely derived condition within cause obvious lesions or discolorations. There are fungal groups containing lichen-associated forms. also lichenicolous lichens that colonize a separate There is still considerable debate about the primi- lichen host and maintain a separate photobiont. tive condition of mycoparasites in the literature These interactions have rarely been investigated (Jeffries & Young 1994). If obligate parasitism is a suf®ciently to answer even the most basic ques- fundamental attribute of primitive groups and sap- tions. Little or nothing is known about the modes rotrophs arose from these primitive groups, phylo- of cellular contact, nutrient exchange, antibiosis, or genetic investigations that target these fungi will virulence. The degree of host-speci®city is usually prove very useful in elucidating these relationships. not known for certain, so whatever basis there is They may also shed light on broader evolutionary for any presumed host speci®city is also unknown. questions concerning the signi®cance of the para- Very few lichenicolous fungi have ever been sitic habit in the fungi. brought into axenic culture, so little is known about To encourage investigation of obligate lichen their cultural requirements; for the same reason, saprotrophs we offer the following hypotheses for controlled experiments involving fungal cultures testing: have only rarely been done in the laboratory. In this 1) Obligate lichen saprotrophs that specialize on section, we brie¯y discuss possible fungal interac- a single lichen species or genus will prove to be tions with lichens, making reference to the broader very rare in nature; most saprotrophs on lichens literature on interfungal interactions (Jeffries & will be generalized facultative saprotrophs. Young 1994) where appropriate, and suggesting 2) Phylogenetic analyses of groups containing some research questions that can be addressed in obligate lichen saptrotrophs will frequently indicate this area. a derived position for taxa that exhibit this char- Saprotrophic interactions. Recent studies (Gir- acter. landa et al. 1997; Petrini et al. 1990) show that Biotrophic vs. necrotrophic interactions. Li- lichen thalli commonly harbor a diverse myco¯ora, chen-associated fungi that obtain at least a portion but most of these fungal associates appear to be of their ®xed carbon from either the lichen myco- opportunistic plant- and soil-inhabiting saprotrophs biont or photobiont should perhaps be considered that probably never form stable symbiotic associa- parasites by de®nition, even if there is no apparent tions with lichens. When lichen thalli are damaged, harm to the lichen. During the past 30 years, how- these saprotrophs are able to grow and degrade tis- ever, most people working on lichenicolous fungi sues, in part because they can manufacture a variety have used the term `parasite' only for a fungus that of generalized cell wall-degrading polysaccharidas- damages its host. In the literature on lichenicolous es. However, their interactions with lichens are rel- fungi, therefore, the extent to which the interaction atively loose and ephemeral. causes damage appears to matter in the application A number of lichen-associated fungi appear
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