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Mycologia, 95(1), 2003, pp. 148-155.
© 2003 by The Mycological Society of America

A unique ballistosporic hypogeous sequestrate Lactarius from California


Dennis E. Desjardin 1

     Department of Biology, San Francisco State University, 1600 Holloway Ave., San Francisco, California 94132

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 LITERATURE CITED
 

Lactarius rubriviridis sp. nov., characterized by hypogeous, sequestrate basidiomes with red latex, green stains, and forcibly discharged, reticulate basidiospores is described and illustrated. During the Spring, the new species forms basidiomes associated with conifers at 1400–1800 m elevation in the Sierra Nevada, and is known from two specimens collected 19 yr apart. Comparisons with the putatively polyphyletic genera Arcangeliella and Zelleromyces, and an accounting of all known members of these genera are provided.

Key words: Arcangeliella, astrogastraceous series, Russulales, Zelleromyces


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
LITERATURE CITED
 
In June 1982, an unusual and exciting new species of hypogeous sequestrate fungi was collected by Mrs. Dorothy Zediker at Foresta Campground in Yosemite National Park, California. Fresh material was obtained by Dr. Harry Thiers and Herb Saylor (then a student of Dr. Thiers) at San Francisco State University where they immediately recognized the material (HS 921) as representing a new species belonging to the astrogastraceous series of Russulales. Dr. Thiers and Mr. Saylor intended to publish the new species as "Zelleromyces rubriviridis" (currently a nom. herb.), and they submitted a formal description in a manuscript to Mycologia in 1986. Favorable reviews were received, but there were unresolved discussions regarding subgeneric classification. The new species name was never validly published, and the single specimen languished in SFSU. Recently, fresh material of the species (DED 7312) was collected from a similar habitat at a similar elevation during the same time of year, but from a site approx 130 miles farther north in the Sierra Nevada. The new material provided further details on macromorphology, distribution, and ecology, and for the first time displayed convincingly the ballistosporic nature of the gastroid basidiomes, a feature that is unusual among hypogeous Russulales. The new species is described below and accepted in the genus Lactarius subgenus Dapetes. Color terms and notations are from Kornerup and Wanscher (1978)Citation.

Lactarius rubriviridis Desjardin, Saylor et Thiers, sp. nov. Figs. 1–4



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  		 FIGS. 1–2. Basidiomes of Lactarius rubriviridis (DED 7312, HOLOTYPE). Note the green stains on the outer surface of the basidiome on the right in Fig. 1. Note the red latex and green stains on the hymenophoral tissues in Fig. 2. Scale bars = 10 mm

 


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  		 FIGS. 3–4. Micromorphological features of Lactarius rubriviridis (DED 7312, HOLOTYPE). 3. Basidiospores. 4. Basidia. Scale bars: 3 = 5 µm; 4 = 10 µm

 
Gastrocarpia 25–60 mm diametro, 20–45 mm alta, irregulatim globosa vel ellipsoidia, fusca vel rubrofusca, tactu viridescens, alveolata. Peridium nullum maturitate. Gleba lacunosa, subflavida, tactu viridescens. Contextus viridescens ubi contusus. Latex parcus, laete ruber. Stipe-columella nulla. Columella praesens, conspicua. Odor et sapor haud distinctus. Basidiosporae (8–) 8.5–11 x (7–) 7.5–8.5 µm, ellipsoideae, reticulatae vel partiale reticulatae, ballistosporae, amyloideae. Trama hymenophoris hyphis filamentosis, sphaerocystis nullus. Peridiopellis nullus. In solo subter arboribus coniferis. Holotypus hic designatus: DED 7312 (SFSU), legit D. E. Desjardin, 14 June 2001, prope Cold Creek Campground, Sierra Co., California, USA.

Basidiomes (Figs. 1–2) hypogeous, 25–60 mm long x 20–45 mm broad x 15–30 mm thick, irregularly globose to ovoid or ellipsoid, sometimes lobed. Peridium absent, exterior surface alveolate to ridged and pitted from exposed locules and hymenophoral tramal tissue; ridges reddish brown to dark brown (8–9E–F5–7), staining deep greenish grey to bluish green or dark green (25–27F5–7) where bruised. Gleba loculate; locules irregular in shape, often elongate, 1–5 mm x 0.5–1.5 mm, filled with yellowish white to orangish white (4–5A2) or cream-colored (4A3) basidiospores at maturity; hymenophoral tramal tissue firm, waxy, white to yellowish white (4A2), but becoming reddish brown (9D7–8) when cut from exuded latex; columella rudimentary to well-developed, composed of radiating dendritic veins arising from a central main vein 1–4 mm diam, initially white, but staining greenish white (27A2–3) to greyish green (26C6–7) over time when cut. Latex scant, deep red (9B–C7–8), discoloring tramal tissue to dark brownish red (11–12E7–8). Odor not distinctive or sweet. Taste mild. Spores forcibly discharged, leaving an orangish white (5A2) to yellowish white (4A2) or cream (4A3) deposit.

Basidiospores (Fig. 3) (8–) 8.5–11 x (7–) 7.5–8.5 µm (x = 9.8 ± 0.7 x 7.8 ± 0.4 µm, Q = 1.1–1.4, = 1.26 ± 0.06, n = 25 spores per 2 specimens), ovoid to ellipsoid, inequilateral in profile with an eccentric hilar appendix, densely ornamented with a complete to partial reticulum; with a small, smooth to weakly ornamented suprahilar plage; ornamentation 0.5–1.0 µm tall, deeply amyloid; hilar appendix inamyloid; hyaline in H2O and KOH. Basidia (Fig. 4) 40–60 x 11–13.5 µm, clavate, 4-spored, unclamped, ballistosporic; sterigmata curved, up to 6.5 µm long. Basidioles cylindrical to clavate. Hymenial macrocystidia absent; pseudocystidia scattered, cylindrical with a tapered apex, projecting slightly beyond the basidia, hyaline or with orange globular contents. Subhymenium only slightly differentiated, of short-celled hyphae. Hymenophoral trama of densely compact, agglutinated hyphae, 3–10 µm diam, cylindrical to subcellular, hyaline in H2O and KOH, red (dextrinoid) in Melzer's reagent; lactiferous hyphae abundant, contorted to strangulate, 3–5 (–10) mm diam, refractive, yellowish orange to tawny in KOH. Columella tissues similar to the hymenophoral trama. Sphaerocysts absent in all tissues. Peridium absent. Clamp connections absent.

Habit, habitat and distribution. Solitary to scattered, hypogeous, buried under needle duff of conifers (Abies spp., Pinus spp.). June. Sierra Nevada, California.

Specimens examined.—USA. California. Mariposa Co., Yosemite National Park, Foresta Campground, scattered in soil under conifers, elev. ca 1400 m, HS 921, coll. by Mrs. Dorothy Zediker, 4 June 1982 (SFSU); Sierra Co., Cold Creek Campground off Hwy. 89, solitary in soil under Abies and Pinus, elev. ca 1800 m, DED 7312, coll. by D. E. Desjardin, 14 June 2001 (HOLOTYPE SFSU).

Etymology. rubri—(Latin) red; viridis—(Latin) green; referring to the red latex and green stains.

Commentary. The secotioid and sequestrate representatives of the Russulales (Astrogastraceous Series pro parte) have received considerable attention over the past seventy years. Malençon (1931)Citation and Zeller and Dodge (1935Citation, 1936)Citation were the first to intensively study these fungi. Secotioid and gastroid taxa that are currently recognized as belonging in the Russulales were accepted by Zeller and Dodge (1936)Citation in the genera Arcangeliella, Elasmomyces, and Macowanites. Generic distinctions were based on whether the basidiomes were large and stipitate (Macowanites), or whether the basidiomes were smaller with a gleba that pulled away from the stipe-columella at maturity (Elasmomyces), or whether the basidiomes had "lactiferous ducts" (and presumably latex) in the trama, peridium and columella (Arcangeliella). Singer and Smith (1960)Citation redefined the group based on analyses of specimens in Zeller's herbarium (NY) and from data on abundant fresh material collected by Smith. They accepted Arcangeliella, Elasmomyces, and Macowanites, resurrected two older genera, Gymnomyces and Martellia, and they established two new genera, Cystangium and Zelleromyces (Singer and Smith 1960Citation). Generic distinctions were based primarily on various combinations of the presence or absence of a stipe-columella, latex, and sphaerocysts in the hymenophoral trama. Pegler and Young (1979)Citation revised the classification once again, based on data from an ultrastructural investigation of basidiospore morphology. They recognized two families within the Russulales: the Russulaceae Lotsy and the Elasmomycetaceae Locquin ex Pegler and Young (1979)Citation. The Russulaceae comprised ballistosporic taxa with agaricoid to gastroid and stipitate basidiomes (Lactarius, Arcangeliella, Russula, Cystangium, Macowanites), whereas the Elasmomycetaceae comprised statismosporic taxa with gastroid basidiomes that are stipitate or sessile (Elasmomyces, Gymnomyces, Martellia, Zelleromyces). Within these families, the generic circumscriptions followed those of Singer and Smith (1960)Citation. Beaton et al (1984)Citation redefined the generic delimitations further, placing more emphasis on hymenophoral trama anatomy, stipe-columella development, and spore morphology, and placing less emphasis on the presence or absence of latex. Zhang and Yu (1990)Citation redefined the generic circumscriptions of the hypogeous sequestrate genera (Gymnomyces, Martellia, Zelleromyces), placing primary emphasis on basidiospore ornamentation and hymenophoral trama anatomy. They recognized limited taxonomic significance to latex development and for the first time included latex-producing species in Gymnomyces and Martellia (Zhang and Yu 1990Citation; these species have been subsequently transferred to Zelleromyces by Trappe et al 2002Citation). Recently, Lebel and Trappe (2000)Citation analyzed the type specimens of the type species for all seven sequestrate genera and concluded that peridiopellis anatomy was a more stable character than others used previously to define genera. Based on their type studies, Lebel and Trappe (2000)Citation synonymized Elasmomyces with Macowanites, synonymized Martellia with Gymnomyces, and restricted Cystangium to taxa with an epithelial peridiopellis. The taxonomic boundary between Arcangeliella and Zelleromyces was left for future reconsideration (Lebel and Trappe 2000Citation). Additional type studies of sequestrate russuloid genera leading to numerous nomenclatural changes have been published recently by Lebel and Castellano (2002)Citation and by Trappe et al (2002)Citation. Clearly, the morphological and physiological variability displayed by known secotioid and sequestrate Russulales makes it difficult to assign species to appropriate genera with certainty. The new species described herein demonstrates this problem and offers a potential taxonomic solution.

Diagnostic features of Lactarius rubriviridis include a gastroid, hypogeous basidiome that lacks a peridium, and has red latex, green-stained tissues, a well-developed dendritic columella, and reticulate basidiospores. When basidiomes were cut and placed in a petri plate, an orangish white to cream-colored spore deposit was produced from basidiospores that were forcibly discharged. Moreover, the basidiospores have an eccentric hilar appendix and a rudimentary suprahilar plage, and the basidia form curved sterigmata, further indicating that the basidiospores are ballistosporic (fide Pegler and Young 1979Citation).

Morphological features of Lactarius rubriviridis indicate that it could be accepted in several genera. The lactiferous, gastroid-loculate, hypogeous basidiomes with dendritic columella and reticulate basidiospores suggest that an appropriate taxonomic placement would be in the genus Zelleromyces. However, as redefined by Pegler and Young (1979)Citation, only statismosporic species are accepted in Zelleromyces. It should be noted that recently, Fogel and States (2001)Citation described a new species of Zelleromyces (Z. rogersonii) with putatively ballistosporic spores (although the ability to form a spore deposit was not indicated) and with an evanescent peridium. Currently, 27 species are recognized in Zelleromyces (Table I). If the new species described herein were accepted in Zelleromyces, it would represent the only known species of the genus with red latex (see Table I). In addition, only one other species, Z. rogersonii, has been described with forcibly discharged basidiospores and poorly developed (or absent) peridium. The latter species differs from L. rubriviridis in lacking red latex, green-stained tissues and a columella, and differs in forming smaller basidiospores (8–9 x 6–7 µm; x = 8.4 x 6.7 µm; Fogel and States 2001Citation). Recent molecular data from Miller et al (2001)Citation indicate that Zelleromyces as currently delimited is polyphyletic, with Z. daucinus and Z. striatus allied with Lactarius subdulcis (Fr.) Gray of subgenus Russularia, whereas Z. sculptisporus is allied with L. scrobiculatus var. pubescens A.H. Sm. of subgenus Piperites. Likewise, Peter et al (2001)Citation demonstrated that Zelleromyces is polyphyletic, with Z. hispanicus allied with members of Lactarius sect. Russularia, and with Z. giennensis in an unresolved position outside the Russularia clade. It should be noted that their works included only white latex-producing species of Zelleromyces, and did not include the type species Z. ravenelii (= Z. cinnabarinus; Miller et al 2001Citation, Peter et al 2001Citation). Because I infer from morphology that L. rubriviridis is allied with Lactarius subgenus Dapetes, to accept the red latex-producing species in Zelleromyces would promulgate polyphylly. Hence, placement in Zelleromyces is unwarranted.


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  		TABLE I. Latex-producing hypogeous sequestrate Russulales published to date

 
Alternatively, the non-agaricoid basidiomes with forcibly discharged basidiospores produced by the new species could warrant acceptance in the genus Arcangeliella (fide Pegler and Young 1979Citation). Fifty-three epithets have been established in Arcangeliella to date (Table II ). Zeller and Dodge (1936)Citation originally accepted both stipitate-secotioid and sessile-sequestrate taxa in Arcangeliella. Of the 31 taxa included by them (Zeller and Dodge 1936Citation) in Arcangeliella (Table II), 8 taxa are insufficiently known for accurate taxonomic placement, 22 taxa have been transferred to other genera, and only one species, A. borziana, the type species, is currently accepted in Arcangeliella. Since 1936, the circumscription of Arcangeliella has changed to include only taxa with a stipe or a well-developed percurrent columella, and ballistosporic basidiospores (sensu Pegler and Young 1979Citation) although a spore deposit may not be obtainable. Currently, only 13 taxa are unequivocably recognized in Arcangeliella (Table II). If the new species described herein was accepted in Arcangeliella, it would represent the only known species of the genus that lacks a well-developed stipe, lacks a peridium, and produces red latex (see Table II). Furthermore, although no molecular data are currently available to support this contention, it could be argued that Arcangeliella as currently delimited may be polyphyletic. The type species, A. borziana, and a few other species (A. densa and A. texta) form basidiospores ornamented with isolated spines and rods (similar to those of Lactarius deceptivus Peck, sect. Albati), whereas all other currently recognized species of Arcangeliella form basidiospores ornamented with a complete or broken reticulum or with concentric ridges (similar to Lactarius species belonging to other sections of the genus). To accept the hypogeous-gastroid, astipitate, red latex-producing L. rubriviridis in Arcangeliella, a genus represented currently by stipitate-secotioid, white latex-producing taxa, would be counterintuitive to delimiting a monophyletic Arcangeliella. Hence, placement in Arcangeliella is unwarranted.


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  		TABLE II. Latex-producing epigeous secotioid Russulales published to date

 

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  		TABLE II. Continued

 
Another alternative would be to establish a new genus for L. rubriviridis. The data, however, suggest that such a decision is also unwarranted. The new species described herein is undoubtedly allied with members of Lactarius subgenus Dapetes, particularly with L. rubrilacteus Hesler & A.H. Sm., L. barrowsii Hesler & A.H. Sm., L. subpurpureus Peck, and L. paradoxus Beardslee & Burl. The latter four species are all green-staining, lamellate, epigeous species with red latex, and all form basidiospores ornamented with a partial to nearly complete reticulum. Furthermore, all four species are ectotrophically associated with conifers (primarily pines), and L. rubrilacteus grows in the same montane habitat in California as L. rubriviridis. Rather than promulgate the polyphyletic genus Zelleromyces, or introduce an erroneous taxon into the possibly polyphyletic genus Arcangeliella, or establish a monotypic genus delimited by a combination of features shared in part by Lactarius, Zelleromyces and Arcangeliella, I accept the new species in Lactarius subgenus Dapetes. If one accepts members of Lactarius subgenus Dapetes in the genus Lactarius, then the new species must belong there as well. Otherwise, establishment of a distinct genus for L. rubriviridis would make the "Dapetes lineage" paraphyletic. The red latex, green stains, forcibly discharged basidiospores, and pine association of L. rubriviridis suggest that the species is relatively recently derived from an epigeous agaricoid ancestor allied with L. rubrilacteus. Furthermore, the existence of L. rubriviridis suggests that there have been at least three independent origins of the hypogeous, loculate, gastroid body form (i.e., Zelleromyces) within Lactarius.

I agree with Miller et al (2001)Citation that the gastroid genera Arcangeliella and Zelleromyces have been derived from within Lactarius, and that synonymy of these genera with Lactarius is a viable option. An analogous example was presented by Kretzer and Bruns (1997)Citation where they reduced the polyphyletic secotioid-gastroid genus Gastrosuillus to synonymy with the boletoid genus Suillus. Another example is the recent synonymy of the morphologically diverse secotioid genus Thaxterogaster (54 spp.) with Cortinarius (Peintner et al 2002Citation), supported by molecular evidence (Peintner et al 2001Citation). Based on morphology alone, it has been known for years that Thaxterogaster species were phenetically similar to species belonging to different subgenera of Cortinarius (pers obs; Horak pers comm). The molecular phylogenetic studies by Peintner et al (2002)Citation confirm these inferences. As more molecular data become available, it may result that Lactarius must be divided into a number of genera, wherein subgenus Dapetes (or some portion of it, including L. rubriviridis) may represent a distinct genus in need of a new name (none is currently available for this lineage). It is premature for me to preemptively propose a new generic name to accommodate L. rubriviridis and its epigeous, lamellate cohorts. In this scenario, Arcangeliella and Zelleromyces may remain as viable taxonomic entities in a much-restricted sense for lamellate and secotioid/gastroid species allied with A. borziana and Z. ravenelii, respectively. Other Arcangeliella and Zelleromyces species will undoubtedly require taxonomic placement elsewhere within the Lactarius sensu lato clade.


   ACKNOWLEDGMENTS
 
The first author dedicates this paper to Dr. Harry D. Thiers (deceased, 8 Aug 2000) and Mr. Herbert M. Saylor (deceased, 19 May 2000), whose contributions to the field of mycology are unparalleled. Both of these outstanding mycologists were my first mentors and they greatly influenced my career in mycology. I thank Dr. Roy Halling (NYBG) and Dr. Scott Redhead (DAOM) for their advice and critical comments, and Mrs. Ellen Thiers for preparing the Latin diagnosis. A special thanks to Michael Wood (www.mykoweb.com) for use of his color photographs of the new species.


   FOOTNOTES
 
ded{at}sfsu.edu Back

Accepted for publication June 18, 2002.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
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