Trans. s-. mycol. Soc. 81 (1), 109-120 (1983)

[ 1°9 ]

Printed in GreatBritain

WHAT ARE PHIALIDES ANYWAY?

By D. W. MINTER, B. C. SUTTON AND B. L. BRADYCommonwealth Mycological Institute, Ferry Lane, Kew, Surrey TW9 ]AF

The history of the term phialide is outlined. The way the term has been used is analysed andfound to be confused. Four problems are identified: nobody in recent years has used the termin its original sense; nobody is agreed on what a typical phialide is; nobody can be certainwhat anyone else means by the term; the term is promoting the very artificial classificationit was introduced to avoid . The reasons for these problems are discussed, and four other terms(aleuriospore, annellide, blastic and thallic ) subject to the same difficulties are identified. Itis concluded that none of these words can be used as unambiguous, precise scientific terms,but that they can still have a function as vague words describing general symptoms.

This is the third paper in a series providing a radicalreappraisal of existing research on deuteromycetetaxonomy. The ideas and specialized terms intro-duced in the first two papers (Minter, Kirk &Sutton, 1982, 1983) are used here. Familiarity withthem is assumed. The titles of those papers, Holo-blastic Phialides and Thallic Phialides, beg thequestion 'What is a phialide anyway? ' This paperaddresses that question.

ORIGIN OF THE TERM PHIALIDE

The term phialide was invented by Vuillemin(1910 a), member of a school of French mycologistsamong whom the use of developmental features indeuteromycete taxonomy can be traced as far backas Costantin (1888). The work in which Vuilleminintroduced the term began with the observationthat the traditional classification of hyphomycetesprovided by Saccardo (1886) was very artificial andthat ' it is therefore necessary to look for morereliable characteristics to which those already in usecan be subordinated'. It is clear from Vuillemin'swords that he was seeking a natural classification ofhyphomycetes, and his concept of the phialidemust be seen in this context. Vuillemin introducedthe term phialide in the following two passagestranslated by the senior author.

'The branch which serves as the immediatesupport for conidia often takes the form of a flaskwith a venter and a neck, reminiscent of a singlespored basidium and its sterigma. The wordbasidium ought to be reserved for the organcharacteristic of the basidiomycetes, the flask-shaped conidiophore branch will take instead thename phialide (if>uiATJ, phiala, flask). Apart fromcases where it becomes complicated or secondarilyreduced, the typical phialide forms conidia exclus-ively at the top of its neck. Sometimes it exhausts

itself in the production of a single conidium,sometimes it produces several successively and ina basipetal direction. These are able to becomedetached as they are produced, to remain in anagglutinated mass, or to form small chains orstrings holding together for a greater or lesserperiod. The presence of a phialide provides themost reliable taxonomic characteristic after thepresence of conidia; among the conidial hypho-mycetes it characterizes the group PHIALIDES. '

' T he order of PHIALIDES .. .is very large. It willgather together a throng of species hithertodispersed in the most diverse classes and families,and even in heterogeneous genera. Sporotrichumroseum Link, Botrytis bassiana Bals., the generaVerticillium, Acremonium, Penicillium, Aspergillus,etc. form part of it. It will be subdivided accordingto the arrangement of the spores, their structure;one will have to place in the final position thoseempirical characteristics hitherto employed exclus-ively as criteria of the first rank .'

AN AL YSIS OF VUILLEMIN'S CONCEPT

In these passages Vuillemin defined thephialide byreference firstly to shape, secondly to developmentand thirdly to examples. Of the six examples, twoare species and the remainder generic names. Inassessing what Vuillemin meant by his new termthe generic names are of little value, because theydo not enable us to trace the individual fungiVuillemin must have had in his mind when he citedthem. Sporotr ichum roseum would have beenfamiliar to Vuillemin's contemporaries through theillustration in Lindau (1907) (Fig . 1). Botrytisbassiana was illustrated by Vuillemin (1912)himself when he redisposed it in his new genusBeauveria (Fig . 2) .

The illustration of S . roseum is poor. It does,

110 What are phialides anyway?

Fig. 1. Sporotrichum roseum (from Lindau, 1907).

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Fig. 2. Beauueria bassiana (from Vuillemin, 1912).

however, show that conidiogenous cells of thisexample are consistent with certainly the morpho-logical and probably also the developmental criteriaprovided by Vuillemin for the phialide. Theillustration of B. bassiana is, by comparison,excellent. It shows that conidiogenous cells of thisfungus have the right shape for a phial ide in

Fig. 3. Acremonium potronii (from Vuillemin, 1910b).

Vuillemin's sense, but develop by sympodialproliferation and therefore do not produce conidia'in a basipetal direction.' The development inB . bassiana is thus not as described by Vuilleminfor a typical phialide. Since this illustration isVuillemin's own and appeared in the same paper(1912) as a description of the conidiogenous cells ofthis fungus as phialides, there is considerableevidence that Vuillemin was aware of this anomalyand, nevertheless, regarded the conidiogenouscells of B. bassiana as phialides.

In another paper produced shortly after the first,Vuillemin (1910b) discussed the fungus Acre-monium potronii Yuill. (Fig . 3). He noted that con-idiogenous cells of this species were flask-shapedand produced conidia in a manner appropriate forphial ides; but he observed that in many cases noseptum was formed at the base of the flask-shapedportion, and for this reason concluded that conidi-ogenous cells of A. potronii were not phialides. Hetherefore excluded the fungus from his orderPhialides. In the same paper, Vuillemin unambig-uously designated the species Spicaria aphodiiYuill. (now called Paecilomycesfumosoroseus (Wize)

D. W. Minter, B. C. Sutton and B. L. Brady 111

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t;.~\" .n/ )- -

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Fig. 4. Spicaria aphodii (from Vuillemin, 191ob).

Brown & Smith) as type of his order Phial ides, andprovided a careful description and illustration ofthis fungus (Fig. 4). To judge from this illustration,the conidiogenous cells of S . aphodii agree with hisoriginal definition of a phialide.

Vuillemin's use of examples enables two deduc-tions to be made concerning his concept of thephialide. Firstly, his inclusion of B. bassiana in theorder Phialides shows that, in recognizing aphialide, he did not regard mode of development ofthe conidiogenous cell as necessarily more signifi-cant than its shape. Secondly, and conversely, hisexclusion ofA. potroniishows that he did not regardthe shape of a conidiogenous cell as necessarilymore important than its mode of development.

At first sight, therefore, Vuillemin's use of hisown criteria appears inconsistent and arbitrary: inone example shape is important, in anotherdevelopment. It must be remembered, however,that he was not concerned primarily with theconsistency of his criteria. He was attempting toproduce a natural classificat ion and believed hisorder Phialides constituted a naturally relatedgroup of fungi. His principal interest was thereforeto identify members of that group by the charac-teristic organ they produced.

Generally speaking, in natural classification, no

single criterion can be used consistently andexclusively of others. An example from zoologymay make this point clear . Vivipary is a criterionused to identify mammals, but no zoologist wouldattempt to ident ify mammals cons istently andexclusively on the basis of this criterion. If thishappened, the duck-billed platypus would be ex-cluded because it lays eggs, and the aphid, whichis an insect, would have to be included. The naturalclassification proposed by Vuillemin was noexception to this generalization: members of hisorder Phialides could, he believed, be recognizedby their characteristic organ, the phialide. He didnot wish to imply, however, that within th is wholeorder there was no variation in shape or develop-ment of that organ. His criteria are therefore notabsolute, but merely guidelines.

That this line of thought is correct may be seenfrom the following comparison of S. aphodii andB. bassiana. Both species are totally hyaline; bothhave similar overall dimensions; both produceconidiophores with similar branching patterns;both have conidiogenous cells which are similar inshape, at least in their lower portions; conidio-genous cells of both produce more than one minuteaseptate conidium from the apex, and these conidiaare attached to the conidiogenous cell by a thinneck ; conidial delimitation in both is similar andconidia of both secede probably by schizolysis;both fungi are parasitic on insects and both quiteplausibly could have teleomorphs in the sameascomycete order, perhaps the Clavicipitales. Thetwo species differ in that S. aphodii produces conidiain true or false chains (it is not clear which from theillustration), whereas those of B. bassiana areproduced by sympodial proliferation .

The two fungi are therefore similar in so manyrespects that it is not surprising Vuillemin believedthey were related. Many present-day mycologistsmight agree with him. If the two species are related,it follows that the conidiogenous cells in both arelikely to represent the same anatomical organ, evenif they do not develop in exactly the same way. Onemust therefore conclude that Vuillemin's use of hisown criteria was not inconsistent, but rather that hisconcept of the phialide was logically self-consistentand exactly what would be expected from anytaxonomist putting together a natural classification.

SUBSEQUENT HISTORY OF THE TERM

Vuillemin's term was adopted by other mycolo-gists, and is in widespread use today. Because somany have used the term, however, the followinghistory is of necessity selective. As a result, forexample, there will be no reference to the frequentand problematic use of the term in anamorphs of

112 What are phialides anyway?groups other than the ascomycetes . Instead thishistory will be restricted to the examination ofcertain crucial works on which the use of the termphialide by others greatly depends.

MASON, LANGERON AND VANBREUSEGHEM

The first significant discussion ofVuillemin's termwas provided by Mason (1933, 1937). Masoncriticized Vuillemin for excluding A. potronii fromthe Phialides, and expressed the opinion that thepresence or absence of a basal septum to theflask-shaped organ was of less taxonomic signifi-cance than the events occurring at its apex. In allother respects he accepted Vuillemin's views.Langeron & Vanbreuseghem (1952) produced atextbook account in which Mason's emendationwas accepted, but in other respects Vuillemin'sviews were presented remarkably unchanged, evenincluding, for example, a detailed account of thedevelopment of phialides in B. bassiana.

HUGHES

The experimental classification of hyphomycetesproposed by Hughes (1953), and inspired andguided by Mason, was a major event in the historyof deuteromycete taxonomy. Hughes proposed toclassify hyphomycetes into eight sections ' basedprimarily upon the different types of conidiophoreand conidium development '. The fourth of thesesections was based on the phialide and comprisedfungi described as having 'conidia (phialospores)developing in rapidly maturing basipetal seriesfrom the apex of a conidiophore (phialide) whichmayor may not possess an evident collarette'. Atthe beginning of this fourth section Hughes de-fined the phialide in detail with the followingwords :

'The term phialide is here restricted to thoseunicellular structures which are usually terminal,but sometimes intercalary as well, on simple orbranched conidiophores; they are oval to sub-cylindrical to flask-shaped or subulate often with awell differentiated basal swelling and a narrowerdistal neck, with or without a terminal cellarette;from the apex of each phialide develops a basipetalsuccession of phialospores without an increase inthe length of the phialide itself. If the phial ide doesproliferate e.g. in Catenularia, then a plurality ofconidia develops at each level. Not uncommonly aphialide may possess two or three collarettes inwhich case the term polyphialide can be applied toit (e.g. Lasiosphaeria hirsuta ).'

Hughes' concept of the phialide thus differedslightly but significantly from that of Vuillemin.Hughes emphasized shape less and development

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Fig. 5. Sporoschisma mirabile (from Hughes, 1953)·

D. W. Minter, B. C. Sutton and B. L. Brady 113more, and the aspect of development whichreceived particular attention was that occurring atthe apex of the conidiogenous cell. This change inemphasis is not surprising, since Hughes wasattempting a far wider reform of the classificationof hyphomycetes than had been countenanced byVuillemin. It also marks an extension of theargument begun by Mason (1933, 1937) when hedrew attention away from the basal septum ofA. potronii to the events occurring at the conidio-genous cell apex. The result of this change inemphasis, however, was that it was no longerpossible to classify fungi such as B. bassiana ashaving phialides, in spite of their obvious simi-larities with other species still classified in that sec-tion. Conversely, other fungi such as Sporoschismamirabile Berk. (Fig. 5) were classified as havingphialides, in spite of the fact that this species hasfew similarities with, say, S. aphodii (Fig. 4) andwas never mentioned by Vuillemin (1910a, b) inhis original works.

TUBAKI, SUBRAMANIAN AND BARRON

Since publication, Hughes' system has undergoneconsiderable scrutiny. Various mycologists haveproposed amendments or new but generally similarsystems of their own. Notable amongst these wereTubaki (1958, 1963), Subramanian (1962, 1971)and Barron (1968). All of these authors followedHughes in giving greater weight to developmentalfeatures occurring at the apex of the conidiogenouscell than to other developmental features orconsiderations of shape. Their definitions of thephialide accordingly differ little from those ofHughes.

Interestingly, however, Tubaki (1958) dividedhis section of fungi with phialides into twosubsections. In one the collarette was conspicuousand the conidia, in general, developed deep downwithin it. In the other the collarette was generallyinconspicuous and the conidia, even when young,developed above it. This had the effect ofseparating genera such as Sporoschisma Berk. & Br.(Fig. 5) into the former subsection, and generasuch as Spicaria (Fig. 4) into the latter. The signifi-cance of this was that it constituted early recogni-tion of the fact that fungi with phialides in the senseof Hughes (1953) did not form a homogeneousgroup.

Subramanian (1962) and Tubaki (1963) eachlisted a type genus for their respective sections ofhyphomycetes with phialides. In the case of Sub-ramanian the section was at family level and thetype genus was Tubercularia Tode: Fr. In the caseof Tubaki the section level was not defined(Tubaki described them as divisions, but could

scarcely be using the word in a strict nomenclaturalsense since the division is a greater taxonomic rankthan the class he was attempting to divide), andthe type genus was Catenularia Grove, species ofwhich are more similar to Sporoschisma speciesthan to Spicaria species. Tubaki also deliberatelyexcluded B. bassiana from his section with phia-lides, and even made Beauveria (the genus typifiedby this species) the type genus of his sectioncomprising fungi with holoblastic sympodialproliferation.

KANANASKIS

The first Kananaskis conference (Kendrick, 1971)represents another milestone in the history ofdeuteromycete taxonomy. One of its main aims,probably the most important, was to try tointroduce some consensus over the terminologyavailable to describe hyphomycetes and in partic-ular their modes of development. At this con-ference the term phialide was the subject ofconsiderable discussion which is fortunately pre-served in the proceedings (Kendrick, 1971). Theresults of this discussion were a 'tentative onto-genetically based system for fungi imperfecti' inwhich Penicillium corylophilum Dierckx was citedas the example of a fungus with phialides, and thefollowing definition:

'Phialide: a conidiogenous cell which produces,from a fixed conidiogenous locus, a basipetalsuccession ofenteroblastic conidia whose walls arisede novo (e.g. Penicillium, Phialophora, Chalara,Sporoschisma). A more extended definition of phi-alide is as follows: a conidiogenous cell in whichat least the first conidium initial is produced withinan apical extension of the cell, but is liberatedsooner or later by the rupture or dissolution of theupper wall of the parent cell. Thereafter, from afixed conidiogenous locus, a basipetal succession ofenteroblastic conidia is produced, each clad in anewly-laid-down wall to which the wall of theconidiogenous cell does not contribute. Any phi-alide wall distal to the conidiogenous locus is thecollarette. The length of the phialide does notchange during the production of a succession ofconidia, though some phialides undergo intermit-tent vegetative proliferation, either percurrent(as inCatenularia) or sympodial (as in Codinaea) betweenconidiogenous episodes.'

In this definition the phialide is described purelyin terms of one restricted aspect of development.This aspect is the series of events occurring at thesmall fertile locus in the cell where conidia are beingproduced. No consideration is given to develop-mental events occurring elsewhere in the cell, norto shape, or any question ofthe taxonomic position

IOj.lm

Fig . 7. Chalara hughesii.

Another comparatively minor but interestingaspect of recent research has been the appearanceof a small but significant number of papers inwhich the wisdom of defining the phialide purelyin terms of the development occurring at its apexhas been questioned. The work of Gams (1973)provides a good example of this. In it he dis-cussed the problems presented by fungi such asAphanocladium spectabileW. Gams (Fig. 10) whichproduces conidiogenous cells indistinguishablefrom phialides in the sense of Kananaskis (Ken-drick, 1971) except in that they each produce onlyone conidium. Many of these problematic fungi areobviously closely related in every other respect tosimilar species with conidiogenous cells producingmore than one conidium and fitting perfectly theKananaskis definition of the phialide.

Gams also cites the example provided by theanamorphs of three species of Hypomyces Tul. Theanamorph of H . odoratus Arnold produces conidia

114 What are phialides anyway?

of the fungus bearing the cell. According to Ken-drick (1971) the phialide is simply a fungal cellwhich produces conidia in a particular manner.

This definition may be viewed as the culminationof a trend begun by Mason to emphasise thedevelopmental events occurring at the apex of theconidiogenous cell. It has found widespreadacceptance and similar definitions may be foundin many other recent major works , e.g. Cole &Samson (1979), Ellis (1971, 1976), and Sutton(1980). For convenience such definitions were usedin preparing the first two papers in this series(Minter et al., 1982, 1983).

Fig. 6. Trichoderma saturnisporum,

RECENT RESEARCH

Since the first Kananaskis conference much workhas been done on the phialide, a lot of it usingelectron microscopy. There have been two principalresults of this research. Firstly, use of the termphialide has now become firmly established in thecoelomycetes, on the grounds that development inthese fungi is of the same fundamental nature asthat in hyphomycetes (Sutton, 1973, 1980). Thesegrounds were first mooted by Mason (1933) and arenow generally agreed to be justified. Secondly, ithas become clear that the phialide, as defined atKananaskis, is heterogeneous.

Evidence for this heterogeneity was provided bymany researchers, including Cole & Samson(1979), Hawes & Beckett (1977 a, b, c), Shearer &Motta (1973), Subramanian (1979) and in the twoearlier papers of this series (M inter et al., 1982,1983). As a result, the term phialide as defined atKananaskis is now used to describe such diversefungi as Trichoderma saturnisporum Hammill(Fig. 6) (producing conidia in gummy masses by asystem of replacement wall building apices withintervening proliferations), Chalara hughesii NagRaj & Kendrick (Fig. 7) and Aspergillus clauatusDesm. (Fig. 8) (producing conidia in true chainsby a wall building ring, with and without con-spicuous collarettes respectively) and oddities likeConioscypha varia Shearer (Fig. 9).

D. W. Minter, B. C. Sutton and B . L. Brady

/

/

Fig. 8. Aspergillus clauatus.

Fig. 9. Conioscypha varia (fromEllis, 1976).

in a manner which fits exactly the Kananaskisdefinition of a phialide. The anamorph ofH. aurantius (Pers.) Tul. however, producesconidia from conidiogenous cells which becomeshorter with every spore produced. This species

cannot therefore be described as having phialidesin the sense of Kananaskis, because the conidio-genous locus is not fixed. Similarly, the anamorphof H. rosel/us (Alb. & Schw.: Fr.) Tul. producesconidia from conidiogenous cells which elongatewith each conidium formed, and therefore cannotbe called phialides for the same reason.

Gams' work demonstrates that use of the termphialide in the sense of Vuillemin (1910a, b), i.e.as a natural organ produced by a natural group offungi, has not entirely been overwhelmed by theuse of the same term in the highly restricted de-velopmental sense so widespread today, i.e. as acell developing in a particular way irrespective ofthe taxonomic affinities of the fungus producing it.The fact that the term phialide still conjures upideas of shape in the minds of many mycologists isfurther evidence that the developmentalist's defi-nition ofthe term on its own is not totally accepted.

DISCUSSION

From the foregoing brief historical outline onething is clear : with few exceptions, each researcherwho has used the term phialide has intended to useit as an unambiguous, precise, scientific term. Thefollowing discussion is therefore an assessment ofhow well this word fulfils the role to whicheveryone has assigned it.

PROBLEMS

There are four big problems with the term phia-lide. The first is that over the last 30 years, sinceHughes (1953), virtually nobody has used the termin the sense originally intended. Over these yearsthe difference between the original sense and cur-rent usage has tended to become greater, so thatpresent definitions of the term have little incommon with those of Vuillemin.

116 What are phialides anyway?Although researchers are not obliged to use this

term in its original sense, there being no nomen-clatural code to cover terminology, their neglect isparticularly regrettable because Vuillemin's defin i-tion had much to commend it. It was logicallyself-consistent, and presented in such a way as toencourage the development of a natural classifi-cation. Vuillemin's natural order Phialides wascarefully tied to a type species which was fullydescribed and illustrated. Even though typificationdoes not apply to ranks above family level in theInternational Code of Botanical Nomenclature(Art . 16), this chosen species is surely significant indetermining the nature of the phialide.

It is therefore remarkable that in all the researchsince Vuillemin's time, not one mycologist, itseems, has attempted to re-evaluate the phialide interms of this species. Of the two other speciesmentioned as examples of phialides in Vuillemin's(191oa) original publication, Sporotrichum roseumis still very much an unknown (it has certainly notreceived the attention it deserves from thedevelopmentalists) and nobody nowadays classifiesB. bassiana as having phialides at all. It has evenbeen used to typify another group of hypho-mycetes categorically stated to be non-phialidic(T ubaki, 1958).

In view of the fact that recent use of the term isso different from its original definition, it mightseem politic to discard Vuillemin's views alto-gether. Even this is not practical, however, becausethere are sufficient new papers being producedwhich use the term in Vuillemin's sense, or some-thing very like it, e.g. Gams, 1973, to keep alivethis original definition.

The second problem is that nobody is agreed onwhat is a typical phialide. Vuillemin (1910 b) citedSpicaria aphodii, Subramanian (1962) the genusTubercularia, Tubaki (1963) Catenularia andKendrick (1971) Penicillium corylophilum . Doubt-less more examples could be found, and they can-not all be right. Indeed, in view of the hetero-geneity which has become apparent in fungi with•phialides " it is doubtful whether any of the fourexamples cited above are even closely related.

This problem will become acute if ever a naturalsystem is successfully devised for the deuteromy-cetes which uses this word. A decision will have tobe made as to what genus , species and specimentypify the taxon or taxa containing fungi withphialides. Three attempts at typification were notedin the foregoing historical outline (Vuillernin,1910b ; Subramanian, 1962; Tubaki, 1963), none ofwhich is nomenclaturally straightforward. Othersimilar attempts could probably easily be found inthe literature. In addition to these attempts, itmight be necessary to take into account some of the

instances where a given species is cited as a typicalphialide even where no nomenclatural treatment ispre sent, particularly if these instances occur inimportant works . For example, the citation ofP. corylophilum as the example for phialides in the•tentative ontogenetically based system ' producedat Kananaskis (Kendrick, 1971) cannot lightly belaid aside in view of the influence this work hashad. It would seem that nobody has even begun tosort out the confusions contained in this problem.

The third difficulty is that present day use of theterm encompasses such a wide variety of fungi thatwhen one researcher uses the term there is noguarantee that he will be understood by others. Onereason for this is that the definition ofa phialide haschanged gradually over the years, largely withoutbeing noticed, and the classifications resulting fromthese subtly different definitions are encounteredwhenever one has to refer to the literature. Anotherreason is that even the most rigorous definitions yetdevised by the developmentalists have failed tocircumscribe the term sufficiently for it to refersolely to a homogeneous group of fungi .

In a sense their failure is not surprising. Thedevelopmentalists' definitions, although in directline of evolution from Vuillemin's, have changed somuch that they must be regarded as fundamentallydifferent. Whereas Vuillemin's definition aimed ata natural classification, and so never stressed onecriterion to the exclusion of others, the develop-mentalists' definitions, e.g. Kendrick, 1971, haveconcentrated on the developmental sequenceoccurring at the apex of the conidiogenous cell.This has encouraged mycologists to use this onecriterion consistently and to the exclusion of others.Predictably enough, no natural classification hascome about. Indeed it must now be obvious thatthis emphasis has resulted, to paraphrase thezoological example from earlier in this paper, in theaphids of the fungal world being classified asmycological mammals.

The fourth problem is that present-day use oftheterm results in related fungi being separated. Theanamorphs of the three species of Hypomyces citedby Gams are a good example of this. If thedevelopmental definition of a phialide were to berigorously applied, these three hyphomyceteswould be placed in different genera. Theirappearances and known teleomorphs, however,plainly indicate that such a classification would beridiculous. Examples of this fourth problem mustbe familiar to all mycologists working with thesegroups, and so it is probably not worth while citingmore. In fact , so many of these examples exist thatit is scarcely surprising that mycologists are losingconfidence in the ability of current systems toclassify deuteromycetes.

Fig. 11. Ambrosiella sp. (1M! 257509). Conidiogenouscells (arrows) can be flask-shaped , with periclinalthickening at their apex (open arrow), making themmorphologically indistinguishable from certain 'phial-ides ', but their development is completely different, sinceeach produces at its apex a single, thick-walled'aleuriospore ' .

quently thick walled and pigmented but sometimesthin walled and hyaline) developed from theblown-out end of a sporogenous cell or hyphalbranch from which it secedes with difficulty .. ."chlamydospore" sensu Hughes, 1953; ganglio-spore. Since introduced by Vuillemin in 1911aleuriospore has been used in various senses, seeMason (1933, 1937) and Barron (1968) for discus-sions.' With the wisdom of hindsight it is possibleto see here all the same problems and causes ofthese problems as in the case of the phialide.Aleuriospore is an attempt to sum up in one word asequence of developmental events; it tries toconvey a sense of shape and of natural affinity(Vuillemin, 1911). The term has not been used inits original sense in recent years, there is argumentas to what a typical aleuriospore is, nobody is surewhat anyone else means by the term and, doubtlesswith such confusion, the term is promoting theartificial classification it was originally set up toavoid!

Although the term annellide has not had such along history as the phialide or aleuriospore, itnevertheless suffers from the same difficulties. Asits etymology suggests, it refers to conidiogenouscells around which faint rings can be discerned.These faint rings, in the same way as the flask-shape of the phialide, are the visible result(symptom) of a developmental sequence (cause ).

D. W. Minter, B. C. Sutton and B. L. Brady

These four problems may be summarized thus:virtually nobody has used the term phialide in itsoriginal sense for the past 30 years (problem 1);nobody is agreed on what a typical phialide is(problem 2) ; nobody can be certain what is meantwhen anyone else uses the term (problem 3) and theterm, as currently used, is promoting the veryartificial classification it was designed to avoid(problem 4). Clearly the term phialide is am-biguous. It is certainly not precise, nor is itscientific.

The reasons for these problems are varied, butthe following are believed to be significant. Theterm phialide represents an attempt to sum up inone word a whole sequence of developmentalevents (conidial ontogeny, conidial maturation,conidial delimitation, con idial secession, prolif-eration, etc. ), The same sequence is present insufficient fungi to give mycologists the misleadingimpression that the term phialide has some sem-blance of meaning. It is now , however, realizedthat each stage in this sequence can vary indepen-dently of the others, so that a wide variety ofcombinations of stages (developmental cocktails)can exist (M inter et al., 1982, 1983), all of them atpresent described as phialides.

Worse still, the term is also used to expressconcepts of shape. Shape in this case is the visiblesymptom of a developmental cause . It is acommonsensical proposition in biology in generalthat one symptom can have many cau ses, e.g.sneezing, a symptom, can result from a cold,pepper, hay-fever, bubonic plague, etc. Thisproposition is also true for the concept of shape inthe phialide: flask-shaped conidiogenous cells withpericlinal thickening at their apex need not all comeabout by the same sequence of developmentalstages; they certainly need not be related (Fig. 11 ) .

Lastly, the term is also used to express concepts ofnatural affinity . Clearly this is all too much. A singleword serving all of these purposes cannot beexpected at the same time to be unambiguous,precise and scientific. It is small wonder that use ofthe term has proved to be problematic.

DIFFERENT TERMS WITH THE SAME

PROBLEMS

The term phialide is not unique. Four other termswith the same difficulties will now be identified. Itis not intended to spell out in detail for each thereasons why they are problematic. The history ofthe misuse of the term phialide is a sufficientexample that such a discourse for the other termswould not be hard to write.

Aleuriospore is defined in the Dictionary of theFungi (Ainsworth, 1971) as: 'a conidium (fre-

117

CONCLUSIONS

Five terms at present believed to be of paramountimportance in deuteromycete taxonomy have beenused until now as though they were unambiguous,precise and scientific. The analysis of these termsoffered in this paper has, however, shown that theyare all subject to such confusions and problemsthat it is impossible to continue using them in thisway. If they had been subject to the same scrutinyas is applied to binomials by the InternationalCode of Botanical Nomenclature, they would havebeen rejected years ago because they have ' beenused in different senses' and so have ' become along-persistent source of error' (Art . 69). Thesooner, therefore, the practice of using them as

118 What are phialides anyway?

At the time of Hughes' (1953) experimental c1as- though they were unambiguous, precise andsification , it was believed that only one de- scientific is dropped, the better.velopmental sequence produced this symptom Minter et al. (1983) observed that 'the terms(holoblastic conidial ontogeny, schizolytic seces- •phialidic ' and •thallic' under their presentsion, enteroblastic percurrent proliferation and definitions contain inherent confusions and con-progressive conidial delimitation). It has therefore tradictions, and ifthey are to continue in use in anybeen used as though it represented a natural group. meaningful sense, they need to be subjected toThe recent studies on Endophragmiella Sutton and thorough scrutiny ' . The present paper has carriedrelated genera (Hughes, 1979) have shown, how- out this thorough examination, and has shown thatever , that at least one other developmental cocktail their observation was justified. The questioncan produce this visible symptom (holoblastic con- remains to be answered: can these terms continueidial ontogeny, rhexolytic secession destroying the to be used in any meaningful sense?conidiogenous cell, percurrent regeneration and This question can conveniently be turned on itsprogressive conidial delimitation). All the prin- head . If these terms are not unambiguous, precisecipal causes of confusion in the term phialide are and scientific , can they be put to any good use inthus also present for the annellide. an ambiguous, imprecise and non-scientific way?

The two remaining terms are blastic and thallic. It is believed that the answer to this question isIn recent years these have been used to represent yes. In describing observations on deuteromycetes,the two supposedly fundamental groups of deuter- the mycologist needs words at different levels ofomycetes (Cole & Samson, 1979; Ellis, 1971, accuracy. The terminology should therefore reflect1976 ; Kendrick, 1971; Sutton, 1980 etc.). The this need. If it does not, the researcher willvalidity of this supposition has, however, recently sometimes be obliged to use a general term wherebeen questioned by Minter et al. (1983) who a highly specific one is required, or conversely aproduced evidence that the thallic category con- precise term where he himself is vague about thetained many fungi which were the same as certain observation. In the present cases this amounts to ablastic fungi in every developmental respect but need for precise words to describe the individualone, i.e. in that conidial maturation was delayed developmental stages (the cause) and vague wordsuntil after conidial delimitation. It must by now be to describe the resulting symptoms.evident, therefore, that these two terms also each In the past terms like phialide have been usedrepresent a visible symptom which can be caused both as vague symptom words and as precise termsby a variety of different developmental cocktails. describing cause. This has led to tautological

It is also an unpleasant fact that Vuillemin thinking roughly on the level of 'phialides develop(1910 a) classified the ' blastic ' fungi as a subdivision phialidically ', a statement which results in zeroof the' thallic' fungi. As has already been observed, transfer of information. Now, however, it isthe paper in which he made this classification was realized that although terms like phialide cannot behighly influential and logically thought out. There used at a precise level, they still have a valuablecan be no doubt therefore that both terms have function as general symptom words. The replace-been subject to misuse somewhere along the line. ment terminology at the precise level already existsThe same problems and confusions thus occur in (Minter et aI., 1982, 1983) in the form ofstatementsblastic and thallic as are found in the other terms. describing each stage in the developmental

sequence separately. Since all of these stages existas separate variables it would be foolish to ignoreany of them: the replacement terminology takes allof them into account. Although the resulting state-ments are longer than the old use of a single term,they are unambiguous, precise and scientific, andso surely represent an improvement.

Another advantage of this proposed terminologyis that it enables statements to be made which areintermediate between the vagueness of a generalsymptom, say phialide, and the precision of a fulldevelopmental observation. Thus, for example,the phrase ' ring wall-building phialide ' identi fiesthat it is not a ' replacement apex phialide ', andso conveys more meaning than the word ph ialide inisolation. But it is not sufficient to distinguishbetween fungi like Chalara hughesii (Fig. 7) and

119

We wish to thank Dr E. Descals of ExeterUniversity and our colleagues at C.M.I. , particu-larly Dr P. M. Kirk and Miss J. C. Walker, fortheir stimulating comments. The senior authoracknowledges with gratitude the continued andpatient support provided by his wife, Helen.

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(Received for publication 19 August 1982)