CHAPTER1 Nomenclature, Taxonomy and Identification Roy Watling, Glen A. Kile, and Harold H. Burdsall, Jr, onfusion has surrounded the nomenclature groups, termed “biological species”, could be recog- and taxonomy of the genus Armillaria nized in Europe (Korhonen 1978, 1980) although, as (Fr.:Fr.) Staude for over a century. Until re- such, “biological species” had no standing within the cently, taxonomists have consistently dis- International Code of Botanical Nomenclature. Ander- agreedC on the exact description of the genus and its son and Ullrich (1979) expanded this approach using correct name according to the International Code of Bo- North American isolates. Morphological and genetic tanical Nomenclature. This confusion has created un- data have subsequently been combined to link many certainty for taxonomists and plant pathologists, and biological species to morphological species and vice has hindered the study of this widely distributed and versa (see chapter 2). Many laboratories now consis- economically important genus of fungi. Based on the tently test interfertility to identify unknown vegetative analyses of Watling and others (1982), we consider the isolates. genus to be a natural grouping, and that Armillaria is the appropriate generic name. This conclusion has been Armillaria probably contains about 40 species, of which widely accepted since that publication (Antonin 1986, several may have restricted geographical distributions Bérubé and Dessureault 1988, Guillaumin and others or vegetation associations. The movement of phanerog- 1985, Intini 1988, Marziano and others 1987, Rishbeth ams or their products from one area of the world to an- 1983, Roll-Hansen 1985, Romagnesi and Marxmuller other may, however, have extended distributions of 1983, Termorshuizen and Arnolds 1987). some species. The first record of an Armillaria species was probably Species of Armillaria are necrotrophic pathogens of either in 1729 (Micheli) or 1755 (Battarra). However, plants, and in one case of another agaric, and not until the later classical authors began to describe mycotrophic associates of achlorophyllous plants (see the larger fungi could several taxa now assigned to chapter 8). Some ecological niches recorded for mem- Armillaria in its restricted sense (Armillaria sensu stricto) bers of the genus are undoubtedly exploited by several be unequivocally recognized. From the pathologists’ species, but the formerly broad concept of A. mellea ap- viewpoint, confusion has arisen from the assumption plied by many authors has confounded recognition of of many authors that Armillaria mellea (Vahl: Fr.) the species involved. Retaining voucher specimens of Kummer is a single variable or polymorphic species basidiomes 1 and vegetative isolates from phytopatho- (Singer 1956) that occurs in both temperate and tropical logical studies is thus extremely important. Although regions. Although this contention is supported by the ability to identify species of Armillaria has ad- maps purporting to show worldwide distribution (Dis- vanced rapidly only in recent years, we have accumu- tribution of Plant Diseases 143, 3rd ed. 1969) and by lated a wealth of observational and experimental host lists on an international or local basis (Laemmlen information on various aspects of Armillaria biology and Bega 1974, Pegler and Gibson 1972, Raabe 1962a), which makes it one of our better-known genera of classical European authors such as Bolton (1788-91) re- Agaricales. alized that several taxa were involved. Nomenclatural and taxonomic aspects of Armillaria in European interest in morphological studies of general and the European species in particular have Armillaria was renewed in the 1970’s (Romagnesi 1970, been amply described in recent years (Antonin 1986, 1973, 1978; Singer 1970a,b; Singer and Clemencon 1972). The demonstration of a bifactorial sexual incom- 1The term basidiome is used in this publication in preference to less patibility system in an Armillaria species (Hintikka specific terms such as basidiocarp, carpophore, fructification, fruit 1973) led to studies that showed several intersterile body, fruiting body, sporocarp, sporophore (Maas Geesteranus 1971), Taxonomy and Identification 1 Guillaumin and others 1985, Herink 1973, Marxmüller The last two are now considered species of Tricholoma 1987, Roll-Hansen 1985, Romagnesi and Marxmüller (Fr.) Staude, and Ag. mucidus is placed in Oudemansiella 1983, Termorshuizen and Arnolds 1987, Watling 1987, Spegazzini (or Mucidula Pat.). Adopting either Ag. Watling and others 1982). This chapter provides an in- aurantius or Ag. robustus as the type could lead to troductory survey of the major issues in the nomencla- Armillaria becoming a synonym of Tricholoma. Kuhner ture and taxonomy of the genus. (1988) suggested Ag. mucidus as the type, but this was never recommended by any earlier author. This choice would be unfortunate as Ag. mucidus has little in com- Armillaria (Fr.:Fr.) Staude— mon with Ag. melleus. The selection of Ag. melleus as Nomenclature and Typification type by Clements and Shear (1931), Dennis and others (1954), and Donk (1949, 1962) was supported by In Fries’ Systema Mycologicum (1821), 12 species, includ- Watling and others (1982). Agaricus melleus Vahl:Fr. is ing Agaricus melleus, were accepted in the tribe based on Icones plantarum, Flora Danica (1792), vol. Armillaria, which he had established 2 years earlier 6(17): 9, plate 1013 (1790), M. Vahl (fig. 1.1) [= Armil- (Fries 1819). The tribes Armillaria and Lepiota were later laria mellea (Vahl:Fr.) Kummer in Der Fuhrer in die combined (Fries 1825) with the latter name used for the Pilzkunde (1871)]. As no herbarium specimen was avail- enlarged group. However, Fries (1838) reverted to able to support this plate, neotypic material was desig- Armillaria for some species. By this time, the number of nated (Watling and others 1982). species in the tribe had doubled, but its scope remained unchanged in his later Monographia Armillariarum The generic name Armillariella (Karsten 1881) typified Suecicae (Fries 1854). by Ag. melleus has been used in many publications; if Armillaria is based on a species other than Ag. melleus, Staude (1857) was the first to raise Fries’ tribe to ge- Armillariella would become available. Karsten’s genus neric rank. Singer (1951b, 1955a,b, 1986) has disputed is logical if Armillaria is typified by Ag. luteovirens Alb. whether Staude’s entry meets all the requirements for valid publication, but Staude is now generally accepted as the validating author of the genus (Donk 1949, 1962; Watling and others 1982). Singer (1951b, 1955a,b) pro- posed Kummer (1871) as the correct author for Armillaria, and has recently reiterated that belief (Singer 1986), a conclusion we do not accept. Thus, Singer (1986) has argued that the publication of Staude (1857) is inadmissible according to the International Code of Botanical Nomenclature, but nothing has changed since Donk (1949, 1962) clearly discussed the status of Staude’s account. Watling and others (1982) found no reason to disagree with Donks findings. Both Staude and Kummer (1871) include within their ge- neric concept Agaricus melleus, and as far as anyone can decide from the available information, it agrees with that outlined within Fries’ (1821) tribe Armillaria. Fries (1821; p. 26) includes a reference to Battara (1755) un- der synonymy of tribe Armillaria but nowhere dis- cusses this entry further. We think that this one mention can hardly support Singer’s statement “de- fines the basic scope of the tribus.” Nothing in Fries (1821) or in Battara (1755) necessitates further explora- tion, and this re-emphasizes the importance of Systems Mycologicum (Fries 1821) in forming a clear base line. Clements and Shear (1931) subsequently selected it as type species for the genus in their comprehensive sur- vey of the nomenclature of the genera of fungi. After accepting Staude’s authority for Armillaria, the FIGURE 1.1 — Agaricus melleus, as illustrated by Martin Vahl in typification of the genus follows in a straightforward Flora Danica (1790 - 1792). Marxmuller and Printz (1982) manner. Staude (1857) included four species: Ag. considered this figure could also represent Armillaria borealis, mucidus, Ag. melleus, Ag. aurantius, and Ag. robustus. although Marxmuller (1987) accepted it as Agaricus melleus. 2 Taxonomy and Identification & Schw.:Fr., as supported by Singer (1951a). However, expallant, hygrophanous or not; color variable yel- this species was not originally in Fries’ tribe, a prereq- low-brown, yellow-olivaceous, ochraceous, rusty- uisite for consideration. Armillariella is therefore an ob- tawny, umber, cigar brown, less commonly buff or ligate synonym of Armillaria. Floccularia Pouzar is the clay pink, sometimes ivory, pallid, or even mouse- correct genus for Ag. luteovirens and its allies. gray; surface glabrous, scurfy, squamulose, squamules darker than ground color, sometimes re- Incorporating Armillaria into Clitocybe (Fr.) Staude has stricted to disc; glabrescent as scales are lost; dry or sometimes blurred the identity of what we believe to becoming viscid to distinctly viscid, in some species be a natural genus. While first proposed by Ricken almost glutinous. (1915), French mycologists have most frequently fol- Stipe — central, fibrous-fleshy, not characteristically lowed this approach, for example Kühner and cartilaginous; often becoming hollow and the outer- Romagnesi (1953) and Heim (1950, 1963). The latter in- most layers splitting and curling back