PHELLINUS TORULOSUS IN NORTH AMERICA 1
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1 Reprinted from MYCOLOGIA, Vol. LXIV, No, 6, pp , Nov.-Dec., 1972 Printed in U.S.A. PHELLINUS TORULOSUS IN NORTH AMERICA 1 R. L. GILBERTSON Department of Plant Pathology, University of Arizona, Tucson AND H. H. BURDSALL, JR. Center for Forest Mycology Research, U.S. Forest Service, Madison, Wisconsin SUMMARY Phellinus torulosus (Pers.) Bourd. et Galz. has been found in two mountain ranges in southeastern Arizona. It occurs at elevations of 8,000 ft or above, mostly on southwestern white pine (Pinus strobiformis Engelm.) in which it causes a white pocket rot of the roots. It is clearly distinct from Phellinus gilvus (Schw.) Pat., with which it has been confused in the past. The fungi currently placed in the genus Phellinus Quél, are lignicolous Hymenomycetes in the order Aphyllophorales. They are characterized by perennial basidiocarps with the hymenophore in the form of united tubes and borwn context tissue that permanently darkens to black in KOH solution (xanthochroic reaction). Setae are present in the hymenium of some specids and basidiospores are hyaline or pigmented. The hyphae lack clamp connections. The species of Phellinus are all associated with white rots and in culture typically give a positive oxidase reaction on tannic and gallic acid media or with gum guaiac solution. In older taxonomic works the species now placed in Phellinus are found in the genera Fomes (Fr.) Kickx and Poria (Pers.) S. F. Gray of the Polyporaceae sensu lato. In current systems of classification Phellinus is placed in the family Hymenochaetaceae Donk. Persoon first described Polyporus torulosus from Europe in 1825, and the transfer to Phellinus was made by Bourdot and Galzin in The combination Fomes torulosus (Pers.) Lloyd is also well established 1 The University of Arizona Agricultural Experiment Station journal article No
2 1259 MYCOLOGIA, VOL. 64, 1972 in the literature. The fungus is well known in Europe, and has been reported to be widely distributed on many species of woody angiosperms and some conifers in the warmer regions of western and southern Europe, the USSR, and Japan (see Bourdot and Galzin, 1928; Pilát, 1936 ; Bondarzew, 1953; Domanski ' et al., 1967 ; Jahn, 1967 ; Ito, 1955). Most of these publications state that P. torulosus occurs in North America. These records are apparently based on reports by C. G. Lloyd of P. torulosus from North American localities. Phellinus torulosus was first reported to occur in North America by Lloyd in The collection on which this report is based was made from the trunk of a live oak in Audubon Park, New Orelans, La., by C. W. Edgerton. We have examined the specimen (CGL Herb. No ) and consider it to be a basidiocarp of Phellinus gilvus (Schw.) Pat. Lloyd later (1924) reported an additional North American collection from Florida (CGL Herb. No ). We also believe this specimen should be referred to P. gilvus. Overholts (1953) recognized P. torulosus as occurring in North America on the basis of the specimens identified as such in the Lloyd Herbarium, but stated that the specimens were a thick form of P. licnoides. Polyporus licnoides Mont. is considered to be conspecific with (Lloyd, 1915a, b) or very similar to P. gilvus (Overholts, 1953; Lowe and Gilbertson, 1961). We agree with Lloyd in believing the two are conspecific and consider P. licnoides to be a synonym of P. gilvus. Overholts (1953) also cites additional specimens of P. torulosus on Sassafras from St. Louis, Mo. We have examined these (CGL and 36027) and consider them to be P. gilvus also, As far as we can determine, therefore, these previous reports of P. torulosus in North America are all incorrect. Lowe (1957) believed this to be the case and considered the specimens cited by Lloyd and Overholts from North America to be perennial specimens of P. licnoides. He consequently treated P. torulosus as an excluded species in his monograph on the genus Fomes in North America. However, Lowe s statement that P. licnoides is an annual form of P. torulosus is not in agreement with our conclusions. Field work in coniferous forests of southern Arizona over the past three years has disclosed the presence of Phellinus torulosus in that area. The following description of P. torulosus was prepared from data based on the 18 Arizona specimens cited. Capitalized color names are based on Ridgway (1912). The specimens from Arizona have been divided and are deposited in herbaria of the following institutions: The University of Arizona, Tucson (ARIZ); The Center for Forest Mycol-
3 GILBERTSON AND BURDSALL : PHELLINUS TORULOSUS 1260 ogy Research, Forest Products Laboratory, U. S. Forest Service, Madison, Wisc. (BFDL); and The National Fungus Collections, Beltsville, Md. (BPI). PHELLINUS TORULOSUS (Pers.) Bourd. et Galz., Bull. Soc. Mycol. France 41 : Polyporus torulosus Pers., Mycol. Eur. 2 : Fomes torulosus (Pers.) Lloyd, Mycol. Notes, Polyp. Issue, No. 3, p Basidiocarps (FIGS. 1, 2) perennial, pileate, sessile, triangular in vertical sections with the upper surface horizontal and the pore surface at approximately a 45 degree angle, applanate to thick, up to 46 cm wide, 28 cm deep, and 11 cm thick; margin obtuse, rounded, up to 2 cm thick, upper surface buff to pale brown (Cinnamon-Buff to Clay Color), glabrous to finely tomentose or slightly strigose-matted, on older portions becoming blackened, sulcate; pore surface yellowish brown (Buckthorn Brown), smooth, the pores 5-7 per mm, rounded, with thick, entire dissepiments; context yellowish brown, black in KOH solution, faintly zonate, hard and woody, up to 11 cm thick, with one or more thin, black layers that appear as fine black lines on cut or broken vertical surfaces; tube layers distinctly stratified, woody, slightly paler than context tissue. Contextual hyphae µ in diam, thin-walled and hyaline to moderately thick-walled and bright yellowish brown, infrequently branched, with rare septa, clamp connections absent; tramal hyphae similar; setae (FIGS. 3, 4, 5) infrequent, ventricose to subulate, up to 49 µ long and 6-11 µ in diam, projecting 10-20µ ; basidia (FIG. 3) 4-sterigmate, clavate, 5-6 µ in diam; basidiospores (FIGS. 3, 4, 5) hyaline, smooth, negative in Melzer s reagent, ovoid to ellipsoid, µ. Specimens examined: ARIZONA-RLG 7887, 9385, 9386, 9387, 9388, ABB 1505, 1506, 1507, 1508, at base of southwestern white pine (Pinus strobiformis Engelm.), Summerhaven, Santa Catalina Mts., Coronado Nat. Forest, Pima County; RLG 9920, ABB 1512, at base of southwestern white pine, Ski Area, Mt. Lemmon, Santa Catalina Mts.; HHB 1504, on Douglas fir [Pseudotsuga menziesii (Mirb.) Franco], Webb Peak area, Pinaleno Mts., Coronado Nat. Forest, Graham County; RLG 9394, 9397, 9396, ABB 1511, at base of southwestern white pine, RLG 7882, on roots of dead Douglas fir, and RLG 9390, at base of charred ponderosa pine (Pinus ponderosa Laws.) snag, Riggs Flat Lake, Pinaleno Mts. FRANCE-Dr.Pierrhugues, on Lauris nobilis, Toulon, CGL No (BPI); H. Bourdot No. 3151, sur aubépine, St.
4 1261 MYCOLOGIA, VOL. 64, 1972 FIGS Basidiocarps of Phellinus torulosus. 1. RLG 9396 at base of southwestern white pine, Santa Catalina Mts., Arizona, 1 / Persoon Herb. specimen No. 404, 1 / 2. Priest, Allier, CGL No (BPI); R. Maire No , on Picea excelsa, St. Martin-Vésubie (Alpes-Maritimes), CGL No v (BPI). CZECHOSLOVAKIA-Dr.Milos Deyl, ad truncos quer- V cinos, Parkán, det. Dr. A. Pilát (ex-herb. Prague, BPI). PORTU- GAL-Rev.C. Torrend, substratum not given, Lisbon, CGL No (BPI).
5 GILBERTSON AND BURDSALL : PHELLINUS TORULOSUS 1262 FIGS Microscopic characters of Phellinus torulosus and P. gilvus. 3-5.P. torulosus. 3. HHB 1504, basidia, basidiospores, and setae. 4. CGL 5473, basidiospores and setae. 5. CGL 42834, basidiospores and setae. 6. P. gilvus, CGL 42835, basidiospores and setae. In addition, six specimens labeled Polyporus torulosus or Boletus torulosus from the Persoon Herbarium at Leiden were examined. None has the place of collection except No. 207, which is from Gallia. Four, Nos. 46, 62, 124, and 207, are small specimens and two, Nos. 404 (FIG. 2) and 409 are large. Number 409 also has Polyporus torulosus, Mycol. Europ. on a label attached to the specimen. Persoon originally described the fungus as broad and thick ( Spithamin fere latus, 1 1 / 2 unc fere crassus ). Specimen No. 409 is large (12 cm thick and 15 cm wide). As it also has the label which states Mycol. Europ. it seems
6 1263 MYCOLOGIA, VOL. 64, 1972 reasonable to assume that this specimen is the basis for the original description. An annotation label indicates that C. G. Lloyd arrived at the same conclusion. The European specimens, including those from the Persoon herbarium, agree well in all respects, both macroscopic and microscopic, with those found in Arizona. We therefore conclude that the Arizona specimens are correctly referred to Phellinus torulosus. Basidiocarps of Phellinus torulosus macroscopically may resemble those of Phellinus nigrolimitatus (Rom.) Bourd. et Galz., a common fungus at higher elevations on conifer logs in the central and northern Rocky Mts., but apparently very rare in southern Arizona. Both P. torulosus and P. nigrolimitatus often have a spongy upper layer of context and thin black layers in the context that appear as fine black lines on cut or broken surfaces. Phellinus nigrolimitatus differs microscopically in having elongated, carrot-shaped spores and more abundant and slightly larger setae. Other species of Phellinus that have microscopic characters similar to those of P. torzdosus are Phellinus taxodii (Murr.) comb. nov. (basionym- Pyropolyporus taxodii Murr., Bull. Torrey Bot. Club 65: ), P. ribis (Schum. ex Fr.) Quél., and P. gilvus (Schw.) Pat., none of which can be considered conspecific with P. torulosus because of the following important morphological differences. Phellinus taxodii causes a heartrot of bald cypress [ Taxodium distichum (L.) Rich] and has smaller basidiocarps and slightly smaller spores. Phellinus ribis causes a heartrot of shrubby deciduous plants, including species of Ribes and Lonicera. It has small basidiocarps and lacks setae. Phellinus gilvus has long been confused with P. torulosus in North America, but can be readily distinguished both macroscopically and microscopically. Phellinus gilvus is widely distributed and common on hardwoods in North America, and P. torulosus is known only in southern Arizona on conifers above 8,000 ft. Macroscopically P. torulosus basidiocarps can be distinguished by their large size and thick margins compared to small basidiocarps with thin margins characteristic of P. gilvus. A reddish brown to purplish brown pore surface is typical of P. gilvus and the pore surface for P. torulosus is yellowish brown. Black lines like those seen in the context of P. torulosus are not found in the context of P. gilvus. Microscopically the two species are very similar, being distinguished by the smaller, more narrow spores of P. gilvus (FIG. 6). The characters distinguishing the two species are compared in TABLE I.
7 CHARACTERS FOR DIFFERENTIATING PHELLINUS TORULOSUS AND PHELLINUS GILVUS Rot characters White pocket rot of roots; bright red streaks in early stages. Uniform white rot; no bright red streaks in early stages or pockets in late stages. TABLE I Species Phellinus torulosus Phellinus gilvus Color of pore surface Yellowish brown Purplish brown Basidiocarp characters Setae Typically none to a few in each section. Typically abundant in all sections. Basidiospores Broadly ellipsoid to subglobose µ Oblong to narrowly ellipsoid µ Cultural characters Optimum growth temp. 20 C 28 C Growth at 25 C in 2 weeks 6-8 mm mm Substratum and geographical distribution in North America Living Pinus strobiformis (rarely other conifers) at 8,000 ft or above in southern Arizona; also known on living hardwoods in Europe. Usually on dead hardwood trees, stumps, and logs; occasionally on living hardwoods but not known on conifer wood.
8 1265 MYCOLOGIA, VOL. 64, 1972 Phellinus torulosus is apparently an important cause of root rot in southwestern white pine in the Santa Catalina and Pinaleno Mountains in southeastern Arizona. It is especially common in the vicinity of Summerhaven in the Santa Catalina Mountains at about 8,000 ft elevation. It is consistently associated with fire scars on large, old trees and probably enters the living trees through these fire scars. We have found P. torulosus fruiting on dead snags or stumps, but it apparently was present before the death of the tree in these cases. It has not been found on logs or slash and does not appear to become established on dead material. The basidiocarps are always at or very near the groundline or developed in cavities under large roots. Soil, rocks, and organic litter become incorporated in the basidiocarp in some cases. The rot appears to be virtually limited to the roots below ground level. In radial or tangential sections, the incipient decay (FIG. 8) in southwestern white pine appears as bright red or purplish red longitudinal streaks (Eugenia Red to Pompeian Red) separated by normalcolored wood. In transverse sections it appears as irregular-shaped spots or pockets of bright purplish red wood. In this incipient stage the discolored wood is solid. In later stages of decay (FIG. 9), small white pockets appear in the discolored areas and the bright discoloration eventually disappears. The pockets are lenticular, distinct, and range from 3-8 mm long and 1-2 mm wide. The wood between the pockets remains solid. Eventually the pockets tend to coalesce and the decayed wood becomes almost stringy in texture with some brown mycelium developing in shrinkage cavities and beetle galleries. The rot of P. torulosus is similar to that of Phellinus pini (Thore ex Fr.) Pilát and Polyporus tomentosus Fr., but the bright red streaks and the limitation of the rot to the roots below ground level are distinctive. Both P. pini and P. tomentosus are common in the same areas in Arizona where P. torulosus has been found. Standard decay tests have been carried out (with isolate RLG 9396) using the agar-block method with test blocks of ponderosa pine sapwood. These showed the development of a white rot with reddish discoloration in the early stages and distinct black zone lines in the later stages. CULTURAL STUDIES Cultures of P. torulosus were obtained by aseptically transferring pieces of context tissue from freshly broken surfaces to tubes of malt extract-agar medium. Cultures from which descriptive data were taken were grown at 25 C in the dark on media containing 1.5% Difco agar
9 GILBERTSON AND BURDSALL : PHELLINUS TORULOSUS 1266 FIG. 7. Cultures of Phellinus torulosus (RLG 9396, top row) and P. gilvus (RLG 7070, bottom row) on, left to right, malt extract medium, gallic acid medium, and tannic acid medium after 2 weeks at 25 C. FIG. 8, incipient decay and, FIG. 9, advanced decay of P. torulosus on southwestern white pine, Santa Catalina Mts., Arizona.
10 1267 MYCOLOGIA, VOL. 64, 1972 and 2.0% Difco malt extract. Gallic and tannic acid media (Davidson et al., 1938) and gum guaiac solution (Nobles, 1958) were used to test for the presence of extracellular oxidase. Cultures examined were from collections RLG 9385, 9387, 9396, and ABB 1506, 1507, 1508 previously listed. Growth characters (FIG. 7) : Growth very slow, diameter of mat mm after 17 days; advancing zone even or slightly bayed, appressed, white or pale yellow (Mustard Yellow) almost to the extreme limit of visible mycelium; raised aerial mycelium developing 5-15 mm behind advancing edge, densely tomentose or felty, tough, pale to bright rusty brown (Tawny-Olive to Cinnamon-Brown); reverse unchanged after 17 days; odor faintly like apple cider; no evidence of fruiting after 6 weeks; oxidase reactions weakly positive on gallic and tannic acid media after 4 days, gradually darkening to a moderately strong reaction in 7 days; oxidase reaction negative or very faintly positive with gum guaiac solution after 10 min; growth none on gallic or tannic acid media. Microscopic characters: Hyphae of advancing zone hyaline, thin-walled or with slightly thickened walls, septate, with occasional to frequent branching, 2-4 µ in diam, some with branches tapering down to a very slender tip; hyphae of aerial mycelium pale yellow to reddish brown, moderately thick-walled, septate, some very closely septate, with infrequent branching, 2-3 µ in diam; hyphae of submerged mycelium hyaline to pale yellow, septate, some with frequent branching, mostly 2-5 µ in diam, some up to 10 µ in diam and slightly swollen at the septa; no special structures or asexual spores observed. In older areas of the aerial mycelium a rind composed of irregularly swollen, reddish brown, thick-walled hyphal end cells develops under the tomentose surface of the mat. Cultures of P. torulosus and P. gilvus are easily distinguished macroscopically. Phellinus torulosus is very slow growing with an optimum growth temperature of 20 C. It produces a thick, tomentose to woolly, reddish brown mat with a thick, white, woolly margin. Phellinus gilvus differs in growing rapidly, especially at its optimum growth temperature of 28 C. It produces a thin, silky, appressed, white mat with a thin, indistinct margin. After about 2 weeks, fruiting occurs in inverted plates of P. gilvus, and P. torulosus has not been observed to fruit in culture. Phellinus gilvus grows vigorously on tannic acid medium and slightly on gallic acid medium. Phellinus torulosus does not grow on either acid medium (FIG. 7). The relatively
11 GILBERTSON AND BURDSALL : PHELLINUS TORULOSUS 1268 low optimum growth temperature (20 C) for P. torulosus is of interest in view of its restriction to localities above 8,000 ft in elevation in southern Arizona. Phellinus gilvus, with a much higher optimum growth temperature, is common in the same region, but at lower elevations in warmer localities. The key pattern for P. torulosus according to the system devised by Nobles (1965) would be , and according to the method used by Davidson et al. (1942) it would be D-P-S-11. ACKNOWLEDGMENTS The loan of specimens by the curators of the National Fungus Collections and C. G. Lloyd Mycological Herbarium, Beltsville, Md. (BPI), and the Rijksherbarium, Leiden, Netherlands, is gratefully acknowledged. Arthur B. Budington assisted in field work in Arizona, and his collections are designated by the initials ABB. John A. Lindsay assisted with photography and Teresa Scotton provided technical assistance. The work done at the University of Arizona was supported by McIntire-Stennis Project 713. LITERATURE CITED
12 1269 MYCOLOGIA, VOL. 64, 1972
MYCOTAXON ROBERT L. GILBERTSON. Department of Plant Pathology, University of Arizona, Tucson, Arizona and
MYCOTAXON Vol. II, NO. 1, pp. 143-150 April-June 1975 PENIOPHORA TAMARICICOLA IN NORTH AMERICA 1/ ROBERT L. GILBERTSON Department of Plant Pathology, University of Arizona, Tucson, Arizona 85721. and HAROLD
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