The North American Species of Pholiota
Evolutionary Tendencies Within Pholiota
In as much as the concept of Pholiota proposed here is much broader than that of Singer (1963) some comment on it and the category of subgenus are particularly appropriate. By way of background it might be mentioned that when we began our study we had no intention of merging either Kuehneromyces or any part of Phaeomarasmius with Pholiota. Several factors, as will appear in the following discussion, caused us to change our view point. With the aid of a 1.4 N. A. Leitz apoch. objective we found that the spore of many species of Phaeomarasmius had a distinct though minute germ pore, and that the spore generally, as concerns shape and wall thickness was so similar, in many of the species Singer placed in Phaeomarasmius, to the typical Pholiota spore that no real basis could be found for distinguishing two genera on spore features.
Singer (1963, p. 593, line 14 from bottom) writes as follows concerning the problem of distinguishing Pholiota from Phaeomarasmius: "The genus Phaeomarasmius differs from Pholiota in size and habit, in spores with callus or with continuous spore wall rather than with germ pore, in the constant absence of cystidia or—if the sections of Pholiota without chrysocystidia are considered—in a different structure of the epicutis (the scales either made up of appressed fibrils, or else epicuticular hyphae gelatinized in the Pholiotas). Undoubtedly, the group Pholiota tuberculosa, P. curvipes and P. lucifer ss. Kühner & Romagnesi comes, among all Pholiotas, closest to Phaeomarasmius. They have an epicutis which is of cutis-structure with many hyphal fascicles ascending just as in other Pholiotas and not forming a trichodermium,... its hyphae being not so broad as in Phaeomarasmius and never so short, with a slight incrustation from the brown pigment but not conspicuously so, and never thick walled. The spores are here small, so that a confusion with the original group of Phaeomarasmius is out of the question, while the smaller-spored species with often thinner-walled epicuticular elements never have the bright colored veil characteristics for the three Pholiota species just mentioned."
In view of Singer's comments let us consider here in detail how we have found the various features involved to be distributed in North American population of concern to us. Of the species placed in Phaeomarasmius by Singer and included here we have:
- P. erinaceella—no germ pore.
- P. curcuma—with a minute pore.
- P. erinacea—no apical pore.
- P. confragosa—no germ pore.
Additional species which would be placed in Phaeomarasmius by the features of the pileus cuticle (but not included by Singer) are:
- P. pseudosiparia—minute pore present. Pileus cutis of globose encrusted cells.
- P. granulosa—with a minute pore; pileus cutis a "collapsed" trichodermium, hyphal walls rusty-cinnamon, and slightly roughened.
- P. proximans—minute pore present; pileus cutis normal for Phaeomarasmius.
- P. proximans var. subauripes—minute pore present; pileus cutis a trichodermium (collapsing).
- P. cinchonensis—no germ pore, no clamps; pileus cutis with suberect rusty brown hyphae.
- P. lactea—distinct germ pore; pileus cutis with encrusted sphaerocysts.
- P. subechinata—germ pore minute; pileus cuticle a trichodermium, hyphae encrusted.
- P. fagicola—no germ pore. Pileus cuticle a collapsed trichodermium.
- P. squamulose—lacking a pore. Pileus cutis not Phaeomarasmius-like.
- P. curcuma var. lanatipes—pore present; cuticle like that of Phaeomarasmius.
- P. minutula—apex of spore truncate from pore; pileus cuticle of encrusted appressed tubular hyphae.
- P. murrillii—pore minute. Pileus cuticle a trichodermium but hyphae not strongly encrusted or dark brown in KOH.
- P. pseudolimulata—apical pore present; pileus cuticle a trichodermium with smooth to encrusted hyphal walls.
- P. corticola—spore with a "callus." Pileus cuticle a tangled turf of brown encrusted hyphae.
- P. cyathicola—no germ pore; cutis not like Phaeomarasmius.
- P. punicea—no pore. Cuticle ± as in P. confragosa.
- P. canescens—pore minute; pileus cuticle somewhat Phaeomarasmioid.
Of the second group eleven have spores with germ pore, and in one it is broad enough to cause the spore apex to be somewhat truncate. Counting all the species with a pore and a cuticle of the type Singer admits as characteristic of Phaeomarasmius, we have ten species. For the known North American species with central stipes, then, it is clear that the Phaeomarasmius type of pileus cuticle is more frequently correlated with a germ pore at the spore apex than not—by a score of two to one. On this basis the correlation of lack of a germ pore with the presence of a Phaeomarasmioid pileus cuticle as a feature distinguishing Phaeomarasmius as a genus is best abandoned.
The nature of the epicutis of the pileus is such that its features do not lend themselves as well to tabular presentation as does the presence or absence of a germ pore at the apex of the spore. Singer has raised the point of the meaning of a typical trichodermium as against appressed hyphae in fascicles with the ends ascending. The problem of using the presence of a trichodermium as a generic character in this instance cannot be considered independently from the problem of the origin of such an epicutis.
If a parallel situation may be regarded as of some value in indicating the direction of evolution we may review the situation in Pluteus where the P. cervinus complex (Section Pluteus) contains species with a cutis of tubular hyphae (including the end-cell). In other words this cutis, as regards hyphal differentiation, must be regarded as primitive, for the primitive hypha generally in Basidiomycetes is of this type. Smith (unpublished data) has been able to observe all degrees of hyphal differentiation starting with the enlargement of the hyphal end-cells to a somewhat cystidioid condition, and a general shortening of the cells in the cuticular hyphae. These cystidioid end-cells have a tendency to be somewhat ascending either singly or in fascicles, and as this development progresses a condition is approached which is used to recognize section Hispidoderma—a tangled mass of hyphal end-cells cystidioid in shape. As the shortening process continues the cystidia become shorter and more compactly arranged until a hymenium-like layer results. In Pluteus it is certainly evident that the hymeniform type of cuticle could have originated in this manner with fewer changes in the genome of the group than by any other means.
The same explanation of this formation of the trichodermium of Phaeomarasmius is equally as plausible. The name Pholiota means scale and this is the keynote to a good share of the genus. Here we find what we have termed the "collapsed" trichodermium meaning that the layer is sparse enough when the pileus is mature so that the hyphal elements do become more or less decumbent as the pileus expands. Since we have filamentous, intermediate (collapsed trichodermium) and trichodermial types as well as the granulose type in Pholiota, it appears more logical to us to assume that the more complex type evolved from the undifferentiated type.
On this basis we do not admit that the cuticle types as used by Singer have any value in delimiting genera in the present case. The color of the veil in P. proximans is much like that of P. curvipes, so we also exclude veil color as having any generic significance. In fact, it seems clear to us that the major aspects of evolution in Pholiota have been concerned with cuticle types.
In view of the strong likelihood that the trichodermial type of cuticle originated in the manner just discussed, we consider Phaeomarasmius as a genus to be distinguished by its more or less eccentric stipe in addition to the cuticle type (trichodermium), and large spores as proposed by Singer. In this way, the genus is found to occupy an end position in the Flavidula branch of Pholiota. That so many intermediate species are still in our flora, can hardly indicate that more genera should be recognized. We regard the Flavidula line to have bifurcated with species having a Cystoderma-type cuticle as one branch, and those leading to the P. erinacea type forming the other.
Thus Pholiota aurea appears to us to be more in the "orbit" of Pholiota than in Cystoderma. Because of its size it is very distinct from the other species, but the same size range (or nearly so) is found in Cystoderma. The thin-walled at times slightly ornamented spores are the best reason for excluding P. aurea from Pholiota. This point should be studied by EM photographs.
One uniting feature of the whole group (Flavidula) as we have outlined it is that the hyphal walls become a darker brown or change to brown upon the application of KOH.
We do not put any generic emphasis on the presence or absence of cheilocystidia as we feel that this is a more minor character best used at the species or section level.
A second feature which rather well unifies this whole subgenus is the general tendency to produce a rather persistent yellow pigment with the result that color throughout the subgenus falls rather strikingly into a spectrum from pale yellow to rich reddish brown. Since this is also a feature of the subgenus Flammuloides and subg. Pholiota, (the bulk of the genus), we believe the pigmentation pattern supports our conclusions in regard to the probable path of evolution as based on the structure of the pileus cuticle. Hence we have used Romagnesi's admirably descriptive name, Flavidula, for this group.
To us it is also an indication of a connection to Pholiota that P. corticola and P. cyathicola have a gelatinous subhymenium—a very prominent feature in subgenera Flammuloides and Pholiota.
We have found pleurocystidia present as pseudocystidia on P. murrillii, leptocystidia in P. erinacea, P. pseudolimulata, P. corticola, P. cyathicola, P. anomala, and P. canescens—the latter two not typical of the central group in Phaeomarasmius. To us, however, this means that in this group as in most groups of Agaricales, some species do develop cystidia and that as a character it does not correlate with the other features of Phaeomarasmius.
Because the problem of Phaeomarasmius (type species), Tubaria and certain other brown-spored agarics with small basidiocarps needs to be made the object of a special study involving E.M. photographs of spores, our purpose here is to merely group in Pholiota the species we suspect belong there in a natural classification and obviously do not claim to have investigated all ramifications of the problem of the borderline taxa. Phaeomarasmius is thus maintained at least temporarily for the species with eccentric stipes or lateral attachment of the pileus to the substratum.
Kuehneromyces. This genus was proposed by Singer and Smith (1946) for Pholiota species with truncate spores. In the course of the present study this feature came under critical scrutiny with some interesting results. In P. minutula of subg. Flavidula we found that with a 1.4 N.A. oil immersion lens the larger spores appeared truncate. In a number of specimens of Pholiota aurivelloides the spores, or at least many of them, appeared truncate. It will be noted in the descriptions that for many species the germ pore is large enough to affect to some degree the configuration of the spore apex. To this one might add that by far the majority of species included in our concept of Pholiota have spores with an apical pore. The unavoidable question, then, is not one of the presence or absence of a pore, but rather how large it is—and it is here that the main character for Kuehneromyces as a genus breaks down. For the spore in most of the species included by Singer (1963) is not "always with a broad truncate germ pore" (l.c., p. 549). We even noted one instance of a basidiocarp with two and four-spored basidia where the large spores were truncate but those on four-spored basidia were not. Singer attempted to correlate the truncate spore with other features such as lack of dermato-cystidia but again this does not hold because so many of the species have caulocystidia. In short the evidence, as presented in the following descriptions, convinced us that Kuehneromyces was untenable as a genus.
For the most part its species have their relationships with others in subgenus Hemipholiota, with the result that the truncate spore as a character is used to define a section with several stirpes which show intergradation with Naematoloma, Stropharia or Psilocybe.
In our estimation the North American species Singer placed in Pachylepyrium finds a logical place along with section Confragosae as a subgenus (Hygrotrama) in Pholiota. The thick walled spore (wall 0.5-1.8 µ thick) as well as the intense pigmentation are found in other species not closely related but obviously in Pholiota, P. pulchella for instance, with the spore wall about 0.5 µ thick. Both features are merely a matter of degree of development. The color spectrum of the spore deposit for Pholiota is from ferruginous to earth-brown, to yellow-brown ("bister" etc.) to cinnamon-brown to clay-color or more ochraceous, and within this range, in our estimation, it is forcing the issue to make generic groupings with one of these shades as a major character.
The subgenus Pholiota with P. squarrosa as type pin-points the name as associated with scaly species lacking any gelatinization in the pileus cuticle. Here, however, the subhymenium is usually gelatinous whereas in subg. Flavidula it is rarely gelatinous. Hence, in many respects the type of the genus is close to subg. Flavidula as far as anatomical features are concerned. However, the most widely known (and as it turns out the most frequently misidentified species) are in section Adiposae, where, through the development of gelatinous layers in the cuticle, we see the beginnings of a connection to subg. Flammuloides.
Flammuloides as a subgenus contains the largest number of species of any of the subgenera and the species may be said to have evolved in an almost routine manner, since the characters are largely different patterns of pigmentation, slight but constant differences in spore size, features of pleuro-, cheilo-, and caulocystidia, favored substrata, and the usual odd characters of one type or another which crop out in most of the larger groups of Agarics in general—in fact speciation in subgenus Flammuloides may be characterized as monotonous. Subg. Flammula as typified by F. flavida necessitated a shift in the use of the name from cystidiate species with non-dextrinoid spores to acystidiate species with at least weakly but distinctly dextrinoid spores. This is one of those unfortunate changes in the meaning of a name which cannot be helped. It is brought about by the type-system in nomenclature.
From the standpoint of evolution subg. Hemipholiota is most interesting since it is in this group that we have placed the "primitive" species of Pholiota such as P. discolor, P. mutans and P. striatula. These connect to Galerina mostly and indicate to us the probable area of origin of the genus. More important, however, is the frequent appearance of chrysocystidia and types approaching chrysocystidia. When Smith (1951) monographed Naematoloma he was not aware that there are more species of rusty-brown spored agarics with chrysocystidia than there are species of Naematoloma with purple-brown spores, and hence included some brown-spored fungi in Naematoloma. These are transferred to subg. Phaeonaematoloma. Some have a truncate spore and some do not. Because of the number of variations of the chrysocystidial type found in this subgenus, we believe that this type of cystidium had an independent origin in this group and that certain aspects concerning cystidial content have been maintained through the rest of the genus regardless of the morphology of the cystidium. The development of the apical germ pore of the spore has occurred in all subgenera, but in Hemipholiota it appears to have become linked in some measure with the absence of pleurocystidia. Thus real intergradation with Psilocybe results, since the spore deposit in the latter genus is vinaceous-brown in some species not too dissimilar from those of stirps Vernalis.
But Hemipholiota contains a number of evolutionary segments. The type, P. destruens stands out in the group as an odd-sized species much as P. aurea stands out in subg. Flavidula. The P. albivelata group connects obviously to Stropharia not only by the well developed annulus but by the presence of chrysocystidia. The spores are not "broadly truncate" it is true, but neither are they in Stropharia squamosa. In short, from subg. Hemipholiota as treated here we have the basic group from which the other subgenera including Phaeonaematoloma most likely evolved.
The major lines of evolution in the genus as we see them, may be summarized as follows:
- The development of gelatinous layers—in pileus cuticle and subhymenium—subg. Flammuloides.
- The development of the outer veil to form dry scales as it breaks on both pileus and stipe—subg. Pholiota (type species).
- The development of "dry" species either with a granulose outer covering (veil) or trichodermium as a pileus cuticle in the extreme forms—subg. Flavidula.
- A development leading toward Stropharia, Naematoloma and Psilocybe (the "Geophila" group). This we distinguish as a separate taxon because the features of a truncate spore and presence of chrysocystidia become linked in Pholiota to make a unified group distinct from Hemipholiota. The interesting feature here is that in reality these two features are not any more closely linked in the "Geophila" group than in Pholiota. In Geophila we have purple brown-spored fungi most of which have more or less truncate spores, and many of which have chrysocystidia. In fact, with the present study as a background, it is now clear to us that if Pholiota is to be maintained as distinct from "Geophila" the color of the spore deposit makes a better distinction than the presence of chrysocystidia combined with a glabrous or nearly glabrous pileus.
It is interesting to note in this arrangement that the most clearly defined subgenera, Flavidula and Flammuloides, are the terminal or near terminal groups. That Hemipholiota represents the basic gene pool from which evolutionary lines diverged, and that subg. and sect. Pholiota by accident of typification represents a small group not too far removed from Flavidula. Finally, the overall trend of evolution, particularly in Hemipholiota, shows a progression toward "Geophila." Thus as we have outlined the genus here we have used the category of subgenus to indicate the major gene-pools within the group and the major trends from them, with, we admit, the type subgenus and section actually left at a level that would ordinarily be regarded as a stirps, though, it must be admitted, a central one as far as the genus as a whole is concerned.
The relationships outlined here are merely a confirmation of the original ideas of L. Quélet (1886). It is most unfortunate that the generic names Dryophila and Geophila are not tenable under the rules.
The problem of the relationships of smaller groups to each other is difficult in this genus, in particular since the only evidence that can be brought to bear on them at present is somewhat subjective as far as macroscopic features are concerned.
The division of Flavidula into two major lines is somewhat subjective in that it is only in the extremes that the Cystoderma-type of pileus cutis is truly distinct from the trichodermial type. A gene change to cause the cells to be short and wide rather than long and narrow admittedly would not need to be very great. Hence one cannot say that P. granulosa, for instance, originated from other species with a more or less granulose cuticle—it might as well have arisen from a species with trichodermial hyphae having relatively long narrow cells.