OF

ILLINOIS

AT URBANA-CHAMPA1GN

BIOLOGY

Botany

NEW SERIES, NO. 30

Systematics of Laccaria (Agaricales) in the

Continental United States and Canada, with

Discussions on Extralimital Taxa and

Descriptions of Extant Types

Gregory M. Mueller

June 30, 1992

Publication 1435

PUBLISHED BY FIELD MUSEUM OF NATURAL HISTORY

Information for Contributors to Fieldiana

i .nenibers and research associates, although

isid

printed page or fraction thereof. Payment of at least 50% of page

tion time. Contributions from staff, rest

:onregardlev : 'iowever, the full

• inuscripts. Three complete copies of the text (including title

omitted (one original copy plus two review copies which rmr

isid i'iication or subn-i -.viewers before all materials

.Jitor.

<hc Cditor, Fieidiana, Field Museum of Natural History, Chicago, Illinois

Text: is must be typewritten double-spaced on standard-weight, 81/z- by 11-inch paper with wide margins

If typed on an IBM-compatible computer using MS-DOS, also submit text on 5%-inch diskette

isplaywrite 2, 3 & 4, Wang PC, Samna, Microsoft Word, Volkswritci

II).

, authors are requested to submit a "Table of Contents," a "List of Illustrations,"

.-wing title page. In most cases, the text should be preceded by an "Abstract"

;hould conclude with "Acknowledgments" (if any) and "Literature Cited."

•uld be in the metric system (periods are not used after abbreviated measurements). The format

vie of headings should follow that of recent issues of Fieldiana.

sec The Chicago Manual of Style (13th ed.), published by The University of

) Press, and also recent issues of Fieldiana.

References: In "Literature Cited." book and journal titles should be given in full. Where abbreviations are desirable

uthors consistently should follow Botanico-Periodicum-Huntianum and TL -2 Taxonomic

are by F. A. Stafleu & R. S. Cowan (1976 et seq.) (botanical papers) or Serial Sources for the Biosis Data Base (1983)

published by the BioSciences Information Sendee. Names of botanical authors should follow the "Draft Index of Author

, itions. Royal Botanic Gardens, Kew," 1984 edition, or 77- -2.

References sh ed in the following form:

Croat, T. B. 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford, Calif.. 943 pp.

Grubb, P. J., J. R. Lloyd, and T. D. Pennington. 1963. A comparison of montane and lowland rain forest in Ecuador.

I. The forest structure, physiognomy, and floristics. Journal of Ecology, 51: 567-601.

Langdon, ' 79. Yage among the Siona: Cultural patterns in visions, pp. 63-80. In Browman, D. L.,and R. A.

eds., Spirits, Shamans, and Stars. Mouton Publishers, The Hague, Netherlands.

Murra, J. 1946. The historic tribes of Ecuador, pp. 785-821. In Steward, J. H., ed., Handbook of South American

Indians. Vol. 2, The Andean Civilizations. Bulletin 143, Bureau of American Ethnology, Smithsonian

iiiution, Washington, D.C.

and fern a!! < itemala. Part II. Polypodiaceae. Fieldiana: Botany, n.s., 6: 1-522.

Illustrations: Illustrations are referred to as "figures" in the text (not as "plates"). Figures must be accompanied by

, a reference bar. Statements in figure captions alone, such as "x 0.8," are not acceptable.

- uld be typed double-spaced and consecutively. See recent issues of Fieldiana for details of st;

.•d on the reverse ;i>r's name, figure number(s), and "top."

Ul, whenever practicable, be 81/z x 11 inches (22 x 28 cm), and may not exceed ll1/;

<i on boards in the arrangement to be obtained in the printed work. This

; lows: Pen and ink drawings maybe originals (preferred)

at within the size limitation; and rl must be high-quality, glossy,

• i;a! illustrati ned to the corresponding author upon publication unless otherwise

Aut- r <>r re prod IK v

Page Proo ally receive o opy

and changes can be made and queries answered. Only one set of

be made on the single set of page proofs. Changes in page

; crated changes in page proofs can only be made if the

.

THIS PUBLICATION IS PRINTED ON ACID-FREE PAPER.

FIELDIANA

Botany

NEW SERIES, NO. 30

Systematics of Laccaria (Agaricales) in the

Continental United States and Canada, with

Discussions on Extralimital Taxa and

Descriptions of Extant Types

Gregory M. Mueller

Assistant Curator, Mycology

Department of Botany

Field Museum of Natural History

Chicago, Illinois 60605-2496

Accepted October 7, 1991

Published June 30, 1992

Publication 1435

PUBLISHED BY FIELD MUSEUM OF NATURAL HISTORY

© 1992 Field Museum of Natural History

Library of Congress Catalog Card Number: 91-7715 1

ISSN 00 15-0746

PRINTED IN THE UNITED STATES OF AMERICA

PVi

Table of Contents

ACKNOWLEDGMENTS vii

ABSTRACT 1

INTRODUCTION 1

TAXONOMIC AND NOMENCLATURAL HISTORY 2

Europe and Other Extralimital Areas .... 2

North America North of Mexico 3

MATERIALS AND METHODS 4

Morphological Analyses of Basidiomata 4

Scanning Electron Microscope Analyses 5

Somatic Culture Mat Analyses 5

Intra- and Intercollection Pairing Analyses 5

DISCUSSION OF SYSTEMATIC CHARACTERS ... 6

Basidioma Macromorphology 6

Basidioma Micromorphology 7

Basidiospore and Basidium Cytology .... 9

Somatic Culture Mat Morphology 10

Intra- and Intercollection Pairing Reactions 1 2

Restriction Fragment Length Polymor-

phisms of rDNA and mtDNA 14

In Vitro Ectomycorrhizal Synthesis Results 1 4

ECOLOGY AND DISTRIBUTION 15

PHYLOGENETIC CONSIDERATIONS 15

Placement of Laccaria in Ordinal and

Family Treatments 15

Relationship of Laccaria to Hydnangium

and Podohydnangium 17

Previously Published Infrageneric Classifi-

cations Proposed for Laccaria 17

Cladistic Analyses 18

PROPOSED OPERATIONAL CLASSIFICATION OF

LACCARIA 24

Conspectus of North American Taxa .... 25

NORTH AMERICAN TAXA 25

Key to Laccaria Occurring in North

America North of Mexico 25

Laccaria Metasection Laccaria 27

Laccaria proxima 27

Laccaria oblongospora 30

Laccaria laccata 33

Laccaria laccata var. laccata 34

Laccaria laccata var. pallidifolia 35

Laccaria longipes 38

Laccaria fraterna 39

Laccaria montana 42

Laccaria pumila 44

Laccaria striatula 46

Laccaria ohiensis 48

Laccaria tortilis 50

Laccaria Metasection Amethystina 55

Laccaria trichodermophora 55

Laccaria bicolor . 57

Laccaria nobilis 61

Laccaria trullissata 64

Laccaria maritima 65

Laccaria ochropurpurea 67

Laccaria amethysteo-occidentalis 69

Laccaria amethystina 71

Laccaria vinaceobrunnea 72

TENTATIVE KEY TO LACCARIA FOR

THE WORLD 75

TYPE STUDIES 83

ADDITIONS To TYPE STUDIES 136

LITERATURE CITED 137

APPENDIX A. SPECIMENS EXAMINED 143

APPENDIX B. ISOLATES USED IN SOMATIC

CULTURE MAT ANALYSES 155

SUBJECT INDEX 156

INDEX To TAX A .157

List of Illustrations

1 . Representative pileipellis arrangements

occurring in North American taxa of

Laccaria 8

2. Hyphal modifications observed during

micromorphological analyses of

6-week-old somatic culture mats of

Laccaria taxa 13

3. Strict consensus tree resulting from

analyses restricted to characters shared

by ingroup and outgroup taxa 22

4. Unrooted network (strict consensus of

300 trees) of ingroup relationships .... 22

5. Strict consensus cladogram using all

characters listed in Table 4 showing

one possible resolution of where to

root the network presented in Figure 4 23

6. Basidiomata of L. proxima 28

7. Somatic culture mats of L. proxima ... 28

8. Micromorphological features of L.

proxima 29

9. Basidiomata of L. oblongospora 32

10. Somatic culture mats of L. oblongo-

spora 32

1 1 . Micromorphological features of L. ob-

longospora 33

12. Basidiomata of L. laccata var. pallidi-

folia 36

13. Somatic culture mats of L. laccata var.

pallidifolia 36

14. Micromorphological features of L. lac-

cata var. pallidifolia 37

111

Basidiomata of L. longipes

Micromorphological features of L. lon-

gipes

Basidiomata of L. fraterna

Micromorphological features of L. fra-

terna

Basidiomata of L. montana

Micromorphological features of L.

montana

Basidiomata of L. pumila

Micromorphological features of L.

pumila

Basidiomata of L. striatula

Micromorphological features of L.

striatula

Basidiomata of L. ohiensis

Micromorphological features of L.

ohiensis

Basidiomata of L. tortilis

Basidiomata of L. tortilis

Micromorphological features of L. tor-

tilis

Basidiomata of L. trichodermophora . .

Somatic culture mats of L. trichoder-

mophora

Micromorphological features of L. tri-

chodermophora

Basidiomata of L. bicolor

Somatic culture mats of L. bicolor

Micromorphological features of L. bi-

color

Basidiomata of L. nobilis

Somatic culture mats of L. nobilis

Micromorphological features of L. no-

bilis

Basidiomata of L. trullissata

Habitat view of L. trullissata

Micromorphological features of L.

trullissata

Micromorphological features of L.

maritima

Basidiomata of L. ochropurpurea

Somatic culture mats of L. ochropur-

purea

Micromorphological features of L. och-

ropurpurea

Basidiomata of L. amethysteo-occiden-

talis

Micromorphological features of L.

amethysteo-occidentalis

Basidiomata of L. amethystina

Micromorphological features of L.

amethystina

Basidiomata of L. vinaceobrunnea .

40 51. Basidiomata of L. vinaceobrunnea .... 74

52. Micromorphological features of L. vi-

4 1 naceobrunnea 75

42 53. SEMs of basidiospores: L. proxima; L.

oblongospora 76

43 54. SEMs of basidiospores: L. longipes; L.

44 fraterna; L. montana; L. laccata var.

pallidifolia; L. pumila 77

45 55. SEMs of basidiospores: L. ohiensis; L.

46 striatula; L. tortilis 78

56. SEMs of basidiospores: L. bicolor, L.

47 trichodermophora; L. nobilis 79

48 57. SEMs of basidiospores: L. mariti ma;

L. trullissata 80

49 58. SEMs of basidiospores: L. amethysteo-

50 occidentalis; L. amethystina; L. vina-

ceobrunnea; L. ochropurpurea 81

51 59. Representative basidiospores from

52 type specimens: L. tetraspora var.

52 aberrans; L. laccata var. affinis; L. al-

taica; L. amethysteo-occidentalis 84

53 60. Representative basidiospores from

54 type or representative specimens: L.

amethystina; L. laccata var. anglica;

54 L. laccata var. bicolor; L. masonii var.

brevispinosa 87

55 61. Representative basidiospores from

58 type specimens: L. calospora; A. cana-

58 liculata; L. chibinensis; L. laccata var.

chilensis 91

59 62. Representative basidiospores from

60 type specimens: C. laccata var. decur-

60 rens; A. (Clitocybe) echinosporus; L. fi-

brillosa; A. fraternus 94

61 63. Representative basidiospores from

62 type specimens: L. galerinoides; L. lac-

62 cata var. gibba; L. glabripes; L. gome-

zii 98

63 64. Representative basidiospores from

type specimens: Naucoria goossensiae;

65 C. tortilis var. gracilis; L. laccata var.

66 intermedia; A. laccatus 100

65. Representative basidiospores from

66 type or representative specimens: L.

lateritia; L. lilacina; L. longipes; L.

67 masonii 105

66. Representative basidiospores from

68 type specimens: L. laccata var. minu-

ta; L. laccata var. moelleri; L. laccata

69 var. montana; L. montana 109

72 67. Representative basidiospores from

type specimens: L. nana; L. nigra; L.

73 nobilis; L. oblongospora 112

74 68. Representative basidiospores from

IV

type specimens: A. ochropurpureus; A.

ohiensis; C. laccata var. pallidifolia; L.

ohiensis var. paraphysata 115

69. Representative basidiospores from

type or representative specimens: L.

tetraspora var. peladae; L. tetraspora

var. peullensis; L. proxima; L. proxi-

mella 118

70. Representative basidiospores from

type specimens: L. laccata var. pseu-

dobicolor; L. pumila; L. purpureoba-

dia; L. trullissata f. rugulospora 122

7 1 . Representative basidiospores from

type specimens: L. tetraspora var. sco-

tica; C. laccata var. striatula; L. lacca-

ta var. subalpina; L. laccata var. ta-

trensis 125

72. Representative basidiospores from

type or representative specimens: L.

tetraspora; A. tortilis; L. trichodermo-

phora; A. trullissatus 128

73. Representative basidiospores from

type specimens: L. tetraspora var. val-

diviensis; L. vinaceoavellanea; L. vina-

ceobrunnea; L. violaceoniger 132

74. Representative basidiospores from

type or representative specimens: L.

laccata var. vulcanica; L. tetraspora

var. xena

134

List of Tables

1. Number of nuclei observed in the basidio-

spores of examined Laccaria and Hyd-

nangium visualized with Hoechst fluores-

cent dye 10

2. Placement of Laccaria in Kuhner's

(1980), Julich's (1981), and Singer's

(1986) classifications of agaricoid Hy-

menomycetes 16

3. Primary infrageneric classifications pro-

posed for Laccaria 18

4. Characters and their states used in cladis-

tic analyses 20

5. Taxon by character state matrix used in

cladistic analyses 21

Back cover: Laccaria longipes

This work is dedicated to Nils Fries and Rolf

Singer, two modern pioneers of mycology who

set the stage for this study.

Acknowledgments

The number of mentors, colleagues, and friends

that one acquires during a study that lasted over

1 2 years, was carried out in five research institutes,

and contained a major field work component is

amazing as well as heart-warming. I am sure that

I will miss some people that should be recognized,

and to them I apologize, but my heart-felt thanks

and appreciation go out to the following.

I have been fortunate to count as my mentors

a number of luminaries of mycology. My debt of

gratitude to Walter Sundberg and Ron Petersen

(Southern Illinois University, Carbondale, and the

University of Tennessee, Knoxville, respectively)

for introducing me to the incredibly fascinating

world of fungi and for helping me acquire the skills

necessary to try to unravel some of their mysteries

will never be paid. My postdoctoral positions in

the labs of Nils Fries (Uppsala, Sweden) and Joe

Ammirati (University of Washington, Seattle)

provided me with new opportunities, new tech-

niques, and new insights. Lastly, for the past 6

years I have had the pleasure, excitement, and

opportunity of having an office adjacent to Rolf

Singer's here at the Field Museum. Having access

to his knowledge on a routine basis, as well as

having gone on several productive field trips with

him, has greatly enhanced my understanding of

the Agaricales.

There are a number of other people at each of

these institutions whom I would like to ^ cknowl-

edge for their help and guidance. These include

my thesis and dissertation committee members at

siu and the University of Tennessee, and chairs

of departments and other faculty, students, and

staff at all five institutions. Additionally, the staff

and directors, Richard Bruce and J. J. Murray, Jr.,

at Highlands (Highlands, North Carolina) and Mt.

Lake (Pembroke, Virginia) Biological Stations are

acknowledged for facilitating my residencies there.

I would like to recognize two of my collaborators

for their ideas and data, many of which are directly

or indirectly included in this work. Else Vellinga

(Rijksherbarium, Leiden) and I have spent many

hours, either directly or through correspondence,

trying to make sense out of the convoluted no-

menclatural history of some of the names in the

genus. Monique Gardes, formerly of Laval Uni-

versity, Quebec, and now in Tom Bruns's lab at

the University of California, Berkeley, provided a

new set of data to be used in this study. The data

on mtDNA and rDNA RFLPs that she generated

have not only been extremely useful, they have

also provided us with a topic for hours of discus-

sions.

I have been fortunate during the last several

years to have had some very high quality assistants

and others who contributed time and expertise to

this project. The technical assistance of Stephen

Dercole, Kathy Lobuglio, Jon Polishook, Lushi

Shi, and Betty Strack was invaluable to this proj-

ect. Illustrations were prepared by Zorica Dabich

(line drawings) and Clara Simpson (cladograms)

at the Field Museum. The museum's photography

department is acknowledged for its quality work,

sometimes on short notice. Lastly, the SEM mi-

crographs were taken by Betty Strack in the mu-

seum's SEM facility.

A large number of people provided collections

and/or spent time in the field with me. My thanks

go to all of you; having freshly collected material

complete with field notes and Kodachromes is in-

valuable to a study such as this. A partial list of

people who helped in this regard includes Joe Am-

mirati, Rich Baird, Ingrid Bartelli, Bill Cibula,

Steve Dercole, Dennis Desjardin, Liz Farwell, Nils

Fries, Roy Hailing, David Lewis, D. Jean Lodge,

Brian Luther, Andy Methven, Buc McAdoo, Clark

Ovrebo, Jon Polishook, Ron Petersen, Roger Phil-

lips, Steve Rehner, Dana Richter, Kit Scales,

Michelle Seidl, Rolf Singer, Betty Strack, Walt

Sundberg, Harry Thiers, and Jim Trappe.

Curators and staffat the following herbaria kindly

made specimens available for study: Botanischer

Garden und Botanisches Museum Berlin-Dahlem,

Berlin, Germany (B); Department of Biological

Sciences, University of Buenos Aires, Buenos Ai-

res, Argentina (BAFC); Jardin Botanique National

de Belgique, Meise, Belgium (BR); Botanical Mu-

vn

seum and Herbarium, Copenhagen, Denmark (c);

Plant Pathology Herbarium, Cornell University,

Ithaca, New York (CUP); National Mycological

Herbarium, Biosystematics Research Institute,

Ottawa, Canada (DAOM); Royal Botanic Garden,

Edinburgh, Scotland (E); Field Museum of Natural

History, Chicago (F); Farlow Herbarium of Cryp-

togamic Botany, Harvard University, Cambridge

(FH); Herbarium, Department of Botany, Univer-

sity of Florida, Gainesville (FLAS); Conservatoire

et Jardin Botaniques, Geneve, Switzerland (G);

Herbarium, Botanical Museum, Goteborg, Swe-

den (GB); The Herbarium, Royal Botanic Gardens,

Kew, England (K); Rijksherbarium, Leiden, The

Netherlands (L); Los Angeles County Museum of

Natural History, Los Angeles (LAM); V. L. Ko-

marov Botanical Institute of the Academy of Sci-

ences of the USSR, Leningrad (LE); Institute de

Botanica C. Spegazzini, La Plata, Argentina (LPS);

Herbarium, Botanical Museum, Lund, Sweden

(LD); University of Maine Herbarium, University

of Maine, Orono (MAINE); Herbarium of the Uni-

versity of Massachusetts, Amherst (MASS); Her-

barium of the University of Michigan, Ann Arbor

(MICH); Institut de Botanique, Universite de Mont-

pellier, Montpellier, France (MPU); University of

North Carolina Herbarium, Chapel Hill (NCU);

Tulane University Herbarium, New Orleans (NO);

Herbarium, the New York Botanical Garden,

Bronx (NY); Herbarium, New York State Museum,

Albany (NYS); Herbarium, Department of Botany

and Plant Pathology, Oregon State University,

Corvallis (osc); Museum National d'Histoire Na-

turelle, Laboratoire de Cryptogamie, Paris, France

(PC); Auckland Plant Diseases Division, Depart-

ment of Scientific and Industrial Research, Auck-

land, New Zealand (FDD); Herbarium, San Fran-

cisco State University, San Francisco (SFSU);

Laboratory of Plant Taxonomy and Ecology, Bo-

tanical Institute, Faculty of Agriculture, Hokkaido

University, Sapporo, Japan (SAP); Museo Nacional

de Historia Natural, Santiago, Chile (soo);

Southern Illinois University Herbarium, Depart-

ment of Botany, Carbondale (siu); Herbarium,

Swedish Museum of Natural History, Stockholm,

Sweden (s); University of Tennessee Herbarium,

Knoxville (TENN); Herbarium, University of Umea,

Umea, Sweden (UME); Botanical Museum, Uni-

versity of Uppsala, Uppsala, Sweden (UPS); Her-

barium, Department of Biology, Virginia Poly-

technic Institute and State University, Blacksburg

(VPI); Herbarium, Department of Botany, Uni-

versity of Washington, Seattle (wru). The abbre-

viations used for herbaria are taken from Holm-

gren et al. (1981). Additionally, the following

individuals lent specimens from their private her-

baria: T. Kongo— Herbarium of T. Hongo (HH);

P. E. Kempton— Wells/Kempton Herbarium (WK).

The support of the National Science Foundation

(grant nos. BSR-83-1528 and BSR-86-07106), the

U.S.-Sweden Cooperative Science program be-

tween NSF and the Swedish National Science Re-

search Council (grant no. Int-82-1 1779), the

Swedish National Science Research Council,

Highlands Biological Station (Highlands, North

Carolina), and Mountain Lake Biological Station

(Pembroke, Virginia) is gratefully acknowledged.

Valuable critical reviews of this manuscript were

provided by Dennis Desjardin, San Francisco State

University; Andrew Methven, Eastern Illinois

University; and Clark Ovrebo, University of Cen-

tral Oklahoma. The time, attention, and expertise

provided by these reviewers are greatly appreci-

ated and resulted in a much improved manuscript.

I also want to thank Scott Lanyon, Department of

Zoology, Field Museum of Natural History, for

discussions on and suggestions for improving the

section on phylogenetic relationships.

I have already mentioned the invaluable tech-

nical help that my wife Betty Strack provided to

this project, but this was only a fraction of her

contribution. Simply put, Betty— thanks for ev-

erything!

G.M.M.

Vlll

Systematics of Laccaria (Agaricales) in the

Continental United States and Canada, with

Discussions on Extralimital Taxa and

Descriptions of Extant Types

Gregory M. Mueller

Abstract

The genus Laccaria comprises an important part of the North American mycota north of

Mexico. Nineteen species are recognized from the study area. Laccaria laccata is further divided

into two varieties. Discussions regarding the distribution, presumed ectomycorrhizal hosts, and

biology of these taxa are provided along with data on select extralimital taxa. In addition to

an examination of North American material, an attempt was made to examine all extant type

specimens. Descriptions of these collections are offered. To facilitate further work on the genus,

a tentative key to the world taxa of Laccaria is presented.

Extensive collecting was undertaken in much of the continental United States and southern

Canada. Comparative material was collected in Costa Rica, South America, and Sweden. Data

were obtained on basidioma and somatic culture mat morphology, intercollection pairing re-

actions, and restriction fragment length polymorphisms of mtDNA and rDNA. Cytological

data and in vitro ectomycorrhizal synthesis data were also obtained and used to further char-

acterize the genus. Taxa were delimited so that they are presumably monophyletic and are

diagnosable by a unique combination of character states, either morphological or molecular.

Data from intercollection pairings were used in conjunction with other data sets and did not

outweigh information from the other analyses. Results of cladistic analyses were concordant

with the hypothesis that Laccaria is a monophyletic assemblage of taxa with at least one

synapomorphy (echinulate basidiospores with echinulae formed by perpendicular microtubules)

supporting its monophyly. However, it was not possible to develop a fully resolved, robust

hypothesis of phylogeny within the genus because of a paucity of characters, inability to polarize

some of these characters, and problems in choosing appropriate outgroup(s). As expected, there

was a high degree of homoplasy detected within the employed data set, and it will be necessary

to utilize either extensive restriction site mapping or sequencing of selected macromolecules to

develop a robust hypothesis of phylogenetic relationships within this genus. Although synapo-

morphies were not found to support the recognition of sections in the genus, two metasections,

Laccaria and Amethystina, are recognized for logistic reasons and to provide a hypothesis to

be tested during future analyses.

Introduction quently throughout North America. Its taxa make

up a sizable part of the world's mycota and have

Laccaria Berkeley & Broome is a cosmopolitan been reported from every continent except Ant-

genus of mushrooms (Agaricales) collected fre- arctica.

FIELDIANA BOTANY, N.S., NO. 30, JUNE 30, 1992, PP. 1-158 1

Individuals of most Laccaria species have been

reported to form ectomycorrhizal associations with

numerous tree species, including many that are

economically important in North America (e.g.,

species of Quercus and other Fagaceae, many spe-

cies ofPinus, Pseudotsuga menziesii (Mirb.) Fran-

co, and Tsuga heterophylla (Raf.) Sarg.) (Trappe,

1962).

Singer and Moser (1965) and Watling (1977)

have reported that some taxa of Laccaria can act

as pioneer species. Other studies have supported

this contention by reporting that basidiomata of

at least some Laccaria are frequently found in re-

cently disturbed sites and young forest stands but

not in mature forests (e.g., Danielson, 1984; Digh-

ton & Mason, 1985; Dighton et al., 1986). Thus

Laccaria, at least in some situations, may play an

important role in primary and secondary succes-

sion.

Because of the relative ease with which some

species of Laccaria can be manipulated in the lab-

oratory, several taxa, including L. bicolor (Maire)

Orton, L. laccata (Scop.: Fr.) Cooke, and L. prox-

ima (Boud.) Pat., are being used actively in applied

and basic research on ectomycorrhizae (see Kropp

& Langlois, 1 990). Laccaria has also proved useful

in studies on the biology of fungi that form ecto-

mycorrhizae (e.g., Fries, 1983a; Fries & Mueller,

1984; Kropp & Fortin, 1988; Armstrong et al.,

1989; Barrett et al., 1989, 1990; Doudrick & An-

derson, 1989; Gardes etal., 1990, 1991a,b; Muel-

ler, 1991c; Mueller & Gardes, 1991).

Stabilization of the classification of Laccaria,

therefore, would have applied implications be-

cause of the ecological and potential economic im-

portance of many of its taxa, in addition to adding

to our basic knowledge of fungi that form ecto-

mycorrhizae.

Although most modern systematists consider

Laccaria to be an autonomous genus, easily seg-

regated from other members of the family Tricho-

lomataceae (Singer, 1986), delimitation of infra-

generic taxa is difficult in many instances. Much

of this problem is due to the relative morpholog-

ical simplicity of its taxa, which provides few suites

of systematically informative characters, coupled

with a high degree of phenetic plasticity within

certain Laccaria taxa, especially those that have

an apparently wide geographic range. Continuing

nomenclatural confusion has exacerbated this

problem.

A large discrepancy exists in the number of rec-

ognized taxa in the genus for these reasons. Al-

though nearly 1 00 species epithets have been used

for Laccaria worldwide, Singer (1986) recognized

only 18 clearly defined species, while McNabb

(1972) indicated that there may be as many as 43

species worldwide. There also has been much con-

fusion concerning the circumscription of several

taxa, and classification in this genus remains in a

state of flux (e.g., Singer, 1967, 1977, 1986; Bon,

1983; Moser, 1983; Clemen9on, 1984; Ballero &

Contu, 1987, 1989; Mueller, 199 la).

This study was undertaken in an attempt to re-

solve systematic and nomenclatural problems, to

determine species composition and distribution

for the genus Laccaria in North America north of

Mexico, and to add to our knowledge of its biology.

Because of the problems stated above, it was nec-

essary to examine extralimital taxa as well as all

available extant type collections, to designate lec-

totypes, neotypes, or representative specimens

when applicable, and to examine critically char-

acters from various stages of the life cycle. In ad-

dition to morphological characters of basidiomata

and somatic culture mats, data from intra- and

interstock pairing analyses, restriction fragment

length polymorphisms of mitochondrial and ri-

bosomal DNA, cytological studies, and in vitro

ectomycorrhizal synthesis attempts were incor-

porated into this multifaceted study.

Taxa were delimited so that they are presumably

monophyletic and are diagnosable by a unique

combination of character states. Attempts were

made to develop a classification for the genus that

reflects the evolutionary history of the group.

This monograph, the results of over 12 years of

study, synthesizes new and previously published

data (Mueller & Sundberg, 1981; Fries & Mueller,

1984; Mueller, 1984, 1985, 1987, 1991a,b,c;

Mueller & Vellinga, 1986, 1 990; Vellinga & Muel-

ler, 1987; Gardes et al., 1990,1 99 la,b; Mueller &

Gardes, 1991).

Taxonomic and Nomenclatural History

Europe and Other Extralimital Areas

The name Laccaria was first proposed by Berke-

ley and Broome in 1883 to accommodate species

ofAgaricus subgenus Clitocybe that produced glo-

bose basidiospores that often formed a white pul-

verulescence on the thick, attached lamellae. Pro-

posed for transfer to the new genus were Agaricus

laccatus Scopoli, A. bellus Persoon, and several

unnamed species from Ceylon and Europe. No

FIELDIANA: BOTANY

new combinations were made until the following

year, however, when Cooke ( 1 884) formally trans-

ferred eight species to the genus.

Over the intervening century, the presence of

clamp connections and echinulate, multinucleate

basidiospores have become important characters

in the modern generic concept ofLaccaria (Kuhner,

1980, 1984; Singer, 1986).

The pre-Friesian history of the genus can be

summarized as follows. Scopoli (1 772), describing

fungi from the Tyrol of southern Austria, was the

first to use the binomial A. laccatus for a member

of the eventual genus Laccaria. Two more species,

A. amethystinus and A. farinaceus, were described

in 1778 by Hudson from the environs of London

(Hudson, 1798). Hudson placed A laccatus in syn-

onymy with A. farinaceus, and thus A. farinaceus

is a superfluous name. Agaricus tortilis was de-

scribed from Halifax by Bolton (1788). Finally,

Persoon (1801) named A. bellus and two varieties

of A. farinaceus: var. rosellus and var. tortilis.

Fries (1821) placed A. laccatus and A. bellus in

tribe VIII Clitocybe, subtribe 4 Oseypii. He further

divided A. laccatus into variety "a" ("Pileo rufo

1. cameo, sicco subochraceo") and variety "b"

("Pileo amethystine, sicco canescente"). Addi-

tionally, he listed A. tortilis and A. pachyphyllus

Fries (1815) as species that needed to be further

examined.

Between 1821 and 1884, a number of workers

described new species destined later to be incor-

porated in Laccaria (e.g., Fries, 1836-1838, 1874;

Berkeley, 1845, 1856; Montagne, 1856; Berkeley

& Curtis, 1859; Berkeley & Broome, 1871; Ellis,

1874; Karsten, 1876; Spegazzini, 1880; Boudier,

1881).

The genus Russuliopsis was proposed by Schroe-

ter (1889) for all the taxa previously included in

Laccaria. Because Laccaria and its included taxa

were validly published, Russuliopsis is a later ty-

ponym and thus a superfluous name.

Laccaria was recognized by both Fayod (1889)

and Patouillard ( 1 900) in their attempts to develop

a more natural classification system for the Hy-

menomycetes. Peck (1912) was the first worker in

the United States to recognize the genus and one

of the first in the world to publish a paper exclu-

sively on the group.

It was not until Singer (e.g., 1943b, 1949, 1962,

1967, 1973, 1975, 1977) became interested in the

genus, however, that any attempt was made to

organize and formulate a coherent classification

for Laccaria based on the world mycota. To date,

Singer's publications on the genus are the most

comprehensive and influential. His classification

has been the starting point for this study and for

most other systematic research on the genus since

the 1940s.

Several alternative classifications have been

published, including those of Bon (1983), Cle-

mencon (1984), and Ballero and Contu (1989).

Additionally, numerous mycological surveys that

included Laccaria have been published by various

authors for most areas of the world. Some of these

publications include Rea (1922), Kuhner and

Romagnesi (1953), Dennis et al. (1960), Orton

(1960), Phillips (1981), Moser (1983), Dennis

( 1 986), Ballero and Contu ( 1 987), Watling ( 1 987),

and Mueller ( 1 99 1 a) for temperate Europe; Moller

(1945), Lange (1955), Kobayasi et al. (1967), Mil-

ler et al. (1982), and Gulden and Jenssen (1988)

for the Arctic; Vellinga ( 1986) for India; Malen?on

and Bertault (1975) for North Africa; Heinemann

(1964, 1966) and Pegler (1977) for East Africa;

Binyamini (1973, 1976) for Israel; Stevenson

( 1 964) and McNabb ( 1 972) for New Zealand; Imai

(1938) and Hongo (1959, 1971) for Japan; Singer

(1952, 1953), Singer and Digilio(1952), Singer and

Moser (1965), and Horak (1979) for South Amer-

ica; and Singer (1957), Aguirre-Acosta and Perez-

Silva (1978), and Montoya-Bello et al. (1987) for

Mexico.

North America North of Mexico

Schweinitz (1822, 1834) was the first American

mycologist to publish on the North American my-

cota. In his list of all the then-known fungi from

America, Schweinitz (1822) included Agaricus

(Omphalia) bellus and A. (O mp Hal ia) farinaceus.

In 1834 he included A. (Clitocybe) laccatus, A.

(Clitocybe) amethystinus, and A (Clitocybe) bellus.

Several collectors working in North America, in-

cluding Curtis, Lea, Sullivant, and Wright, sent

specimens and notes on American fungi to various

workers in Europe, especially Berkeley, and sev-

eral new species (e.g., A. ohiensis Montagne and

A. ochropurpureus Berkeley) were discovered and

published in this manner.

Ellis (1874) described A. (Clitocybe) trullissatus

from the sand dunes of New Jersey, and thus be-

came the first North American to designate a new

species in this group. Charles H. Peck was the first

North American worker who studied and pub-

lished on the group in some detail (Peck, 1890,

1893, 1895, 1897, 1903, 1907, 1912). Laccaria

amethystina Cooke, L. laccata, L. ochropurpurea

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

(Berk.) Peck, L. striatula (Peck) Peck, and L. tor-

tilis (Bolt.) Cooke were included in the North

American Flora (Murrill, 1914). These same taxa

were included in a study of Laccaria in North

Carolina (Coker and Beardslee, 1 922).

Little systematic work was done on the genus

again until Singer described L. tetraspora from

Florida and L. calospora and L. laccata var. car-

bonicola from Massachusetts (Singer, 1946, 1967,

1973, respectively). Mueller and Sundberg (1981)

presented a treatment for the genus from southern

Illinois. Lahaie undertook a study of the genus

from eastern Canada for his master's thesis (1981),

but his results have not been published. Mueller

(1984, 1991b) described six new species from the

continental United States and Canada.

Materials and Methods

Morphological Analyses of Basidiomata

Extensive collecting was undertaken throughout

the United States and parts of eastern and western

Canada. The following states and provinces were

sampled: British Columbia, California, Colorado,

Florida, Georgia, Idaho, Illinois, Kentucky, Lou-

isiana, Massachusetts, Michigan, Minnesota, Mis-

sissippi, New York, North Carolina, Nova Scotia,

Ohio, Ontario, Oregon, South Carolina, Tennes-

see, Texas, Virginia, West Virginia, Washington,

Wisconsin, and Wyoming. Field work was also

undertaken in Sweden, Mexico, Costa Rica, and

much of South America as part of an ongoing

project to produce a world monograph of the genus

and to obtain comparative material. Dried spec-

imens on loan from numerous herbaria (see Ac-

knowledgments), including most extant type spec-

imens, were also examined.

Collections were made and assembled using

standard techniques (Smith, 1 949; Largent, 1977).

Descriptive terms were taken from Snell and Dick

(1971) and Largent (1977). Unless otherwise not-

ed, color names within parentheses and quotation

marks are from Ridgway (1912), colors from Kor-

nerup and Wanscher (1978) are listed by (page-

column-row), and color names outside of paren-

theses are author-generated. Color names followed

by M&P were taken from Maerz and Paul (1930).

Basidiomata were preserved by warm-air drying

and deposited in either F, TENN, UPS, or wru

(Holmgren et al., 1981). Most examinations were

made directly using either a Nikon Model S-Kt

research microscope, a Zeiss Universal photomi-

croscope, or a Zeiss RA standard microscope

equipped with both bright field and phase contrast

optics. Recent data acquisition and remeasure-

ments were made using JAVA 1.31 (Jandel Video

Analysis Software, 1989) running on an AT&T

6386 computer from images captured through an

Olympus BH-2 microscope with Nomarski differ-

ential interference optics. Illustrations of micro-

morphological characters were made with the aid

of a drawing tube. All measurements were made

on material mounted in 3% KOH. Iodine reactions

were determined in Melzer's reagent and the cy-

anophilic reaction was determined in cotton blue

(Kotlaba & Pouzar, 1964; Singer, 1972; Largent

et al., 1977). Descriptive terminology is from Snell

and Dick (1971) and Largent et al. (1977).

Micromorphological data used in taxon descrip-

tions were based on a complete, detailed exami-

nation of at least five (when possible) represen-

tative collections per taxon. The number of

collections examined was dependent upon the

availability of material and the amount of vari-

ability encountered within the taxon. All speci-

mens listed in Specimens Examined (Appendix A)

were examined, and any deviations from the norm

were noted.

Measurements and observations were taken from

several basidiomata per collection to check for

uniformity. At least 1 0 randomly sampled cheilo-

cystidia, pleurocystidia, and terminal cells of cu-

ticular hyphae, and 1 5 randomly sampled basidia

were measured per collection. Width and diameter

measurements of these elements were taken at the

widest point and rounded to the nearest 0.5 urti.

Arrangement of hyphae comprising the pileipellis

was observed in both radial and scalp sections.

All basidiospore measurements were taken from

hymenial tissue and not from spore prints, in order

to treat all specimens equally. The number of ba-

sidiospores measured and the number of collec-

tions examined for calculating mean size (= Jc) and

length/width ratio (= Q) are included in brackets

with basidiospore size data to give some indication

of reliability of these data (Bas, 1 974). When avail-

able, data on basidiospores from additional col-

lections were included in basidiospore size range

data. Ranges of collection means (Jc, Q) for basid-

iospore data, rather than overall mean values for

the taxon, are provided to give a better indication

of intraspecific variation. Basidiospore size data

are always given without ornamentation and hilar

appendix, with the hilar appendix in profile. Means

and other descriptive statistics were obtained us-

FIELDIANA: BOTANY

ing SAS for Personal Computers, Version 6.03

(SAS, 1985).

Scanning Electron Microscope Analyses

Lamellar fragments from air-dried collections

were rehydrated in an acetone series, fixed in 2.5%

glutaraldehyde in phosphate buffer for 3—4 hr at

4° C, dehydrated in an acetone series, and critical

point dried in a Balzers CPD 030 apparatus with

CO2 as the transition fluid (Cheeseman & Grund,

1985). Samples were then attached to aluminum

mounts with double-stick tape and coated with

gold in a Den ton Vacuum Desk II sputter coater.

Basidiospores were examined and micrographs

were taken at 20 kV with an Amray 1810 scanning

electron microscope.

Somatic Culture Mat Analyses

The following procedure was employed to ob-

tain heterokaryotic tissue cultures of Laccaria.

Small pieces of tramal tissue excised from the pi-

leus-stipe interface were aseptically placed on

modified Melin Norkrans medium (= MMN) plus

benomyl ( 1 0 mg/L) in disposable test tubes (Marx,

1969; Molina & Palmer, 1982; Mueller, 1984).

The benomyl was added to reduce ascomycetous

contamination. Six to 10 replicates were taken for

each collection utilized. Subculturing of each re-

sulting isolate was undertaken until a pure culture

was obtained. Stock isolates were then transferred

to tubes containing modified MMN or N6:5 me-

dium (Fries, 1983a) and stored in the dark at 2-

4° C. Voucher herbarium material of all specimens

used for tissue cultures was described and depos-

ited in F, TENN, UPS, and WTU. All isolates are

housed in the mycological culture collection at the

Field Museum of Natural History.

Culture mat analyses were based on the classic

work of Nobles (1948, 1965). Five-millimeter

round plugs of agar containing hyphal tips taken

from the advancing zone of each of 2-wk-old

"stock" plates were transferred to the edge (my-

celium side down) of a Petri plate containing 1 5-

20 ml of either MMN, malt extract agar (= MEA),

or potato dextrose agar (= PDA). Seven replicates

of each medium for each isolate were inoculated

and placed in a dark incubator at 24° C. Macro-

morphological descriptions were made during the

third and sixth weeks. Photographs of represen-

tative isolates were taken during the fourth week,

and micromorphological characters were exam-

ined during the sixth week.

Macromorphological characters noted included

( 1 ) radius of the culture mat, (2) form and char-

acter of the advancing zone, (3) mat color and

topography, and (4) the presence or absence ol

exudates. Terminology used was taken from No-

bles (1948, 1958b, 1965).

Micromorphological characters were observed

by mounting hyphae from the advancing zone,

mat, and plug of each isolate in 3% KOH and

examining the slide under phase contrast. Micro-

morphological characters examined included the

presence or absence of ( 1 ) modified hyphae, (2)

chlamydospores or oidia, etc., and (3) basidiomata

or hymenial structures such as basidia or cystidia

along the mat surface. Descriptive terminology

used was that of Nobles (1948, 1965).

Extracellular oxidase activity of each isolate was

tested using both the Bavendamm (Davidson et

al., 1938, 1942) and gum guaiac (Nobles, 1958a,

1965) tests (Mueller, 1984).

Intra- and Intercollection Pairing Analyses

Homokaryotic isolates were obtained following

the techniques of Fries (1983a,b) and Fries and

Mueller ( 1 984). Homokaryotic isolates originating

from one basidioma were assigned a stock num-

ber. Within a stock, each isolate received a unique

extension number. All isolates are stored at 2—4°

C on N6:5 medium in the mycological culture

collection at the Field Museum of Natural History.

Intra- and interstock pairing analyses were car-

ried out following the procedures outlined in

Mueller and Gardes (1991). Isolates to be tested

were placed < 10 mm apart on N6:5 plates and

allowed to grow together (2-4 wk). After an ad-

ditional 1 wk or more, plugs of tissue were cut

from the interface and placed on fresh N6:5 plates.

Mycelia growing from these plates were checked

for the presence or absence of clamp connections

by examining them through the bottom of the in-

verted Petri plate at 200 x magnification. Pairings

resulting in hyphae that bore clamp connections

were considered positive; those that did not yield

clamped hyphae were scored as negative. Two or

more testers for each stock, each containing dif-

ferent mating type alleles, were used when possi-

ble. As in Mueller and Gardes (1991) and Mueller

(1991c), the terms noncompatible and intracom-

patible are restricted to intrastock pairings. I used

the terms intersterile for intercollection pairings

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

that did not form clamp connections and inter-

compatible (rather than interfertile) for positive

intercollection matings because data regarding

fruiting and progeny analysis were not available.

Discussion of Systematic Characters

Many Laccaria taxa appear similar on superfi-

cial examination. Closer examination of the mac-

ro- and micromorphological variation, when cor-

related with cultural and molecular data, allows

for the segregation of taxa in this phenotypically

variable group. The following discussion on the

delimiting characters within Laccaria is restricted

to the 20 North American taxa, of which 18 were

collected, photographed, and described during the

course of this study.

Basidioma Macromorphology

COLOR— Basidioma and lamellar colors are the

most diagnostic macromorphological characters.

A major problem with this suite of characters is

that the pigments responsible for these colors are

unknown in many groups of agarics, including

Laccaria (e.g., W. Steglich, Univ. Bonn, Germany,

pers. comm., informed me that the pigments in

L. amethystina oxidize very readily upon extrac-

tion and would take special care to analyze). Cur-

rently, it is not possible to determine homology

between the pigment(s) in either the orange-brown

or violet-colored Laccaria or to determine the

primitive condition via comparison with presum-

ably related genera (outgroup comparison). As

mentioned in the section on Phylogenetic Consid-

erations, I have made the assumption that the pig-

ment(s) are homologous within these two groups

of Laccaria (orange-brown vs. violet). Assump-

tions of homology between the pigments in Lac-

caria and pigments in potential outgroup taxa could

not be made.

Because all members of the genus are hygroph-

anous, especially those taxa with violaceous to

purple basidiomata, it is important to note the

color of the pileus both when fresh and in succes-

sive stages of fading. This is most important in L.

amethysteo-occidentalis G. M. Mueller, L. ame-

thystina, and L. vinaceobrunnea G. M. Mueller.

Basidiomata of all three are bright violet to purple

when young and fresh but differ markedly in their

color changes associated with age (see descrip-

tions). Laccaria ochropurpurea and L. trullissata

(Ellis) Peck are light violaceous when very young

but soon become buff or red-brown at maturity.

Basidiomata of specimens of most other Lac-

caria are some shade of orange-brown to flesh col-

or. Because of the large amount of color variation

found within these taxa (from light buff to a strong

orange-brown or red-brown), basidioma color can

rarely be used to delimit taxa in this large group.

North American species of Laccaria exhibit ei-

ther pinkish flesh color to buff color or violaceous

to purple lamellae. All of the taxa with violaceous

to purple basidiomata plus L. ochropurpurea and

L. trullissata have bright violet to dark purple la-

mellae. Basidiomata of L. bicolor (Maire) Orton,

L. nobilis G. M. Mueller, and, possibly, L. mari-

tima (Teodorowicz) Singer ex Huhtinen have light

pinkish violet to wine-colored lamellae that oc-

casionally fade to a pinkish color with age. All

other North American taxa have flesh-colored la-

mellae. In some instances the lamellae of large,

older specimens may develop a vinaceous ap-

pearance, but an examination of younger speci-

mens should alleviate any confusion that this may

cause. Basidiomata of L. fraterna (Cooke & Mas-

see: Saccardo) Pegler, which probably is an intro-

duced taxon, have rosy-pink lamellae when fresh.

The color of the mycelium at the base of the

stipe (= basal mycelium) is also systematically im-

portant in Laccaria. The basal mycelium can be

either violet or white. In addition to L. trichoder-

mophora G. M. Mueller and L. oblongospora G.

M. Mueller, all of the taxa with violet lamellae

consistently have a violet basal mycelium. In all

of these taxa, however, the basal mycelium oc-

casionally fades to white with age.

BASIDIOMA SIZE— Although often highly vari-

able due to differences in age and environmental

conditions, the size of the basidioma can be di-

agnostic in some instances. Most taxa have mature

basidiomata of moderate size (pileus 20-50 mm

broad, stipe up to 60 mm long), so those taxa that

consistently have larger or smaller basidiomata are

noteworthy. Laccaria montana Singer, L. ohiensis,

L. pumila Fayod, and L. tortilis are characterized

by being small (pileus rarely up to 30 mm broad);

L. amethysteo-occidentalis, L. nobilis, L. ochro-

purpurea, and L. trullissata often have pilei greater

than 60 mm broad.

The stature of the basidioma can also be sys-

tematically important. Laccaria maritima, L. och-

ropurpurea, and L. trullissata are usually robust

(stipe diameter > 7 mm at apex), while all of the

taxa characterized by having small basidiomata,

FIELDIANA: BOTANY

plus L. striatula (Peck) Peck, are generally gracile

(stipe diameter < 4 mm at apex).

Stipe and pileus ornamentation characteristics

are often associated with size. Although most of

the small taxa appear glabrous to finely fibrillose

when fresh, taxa with large basidiomata, such as

L. nobilis, often have pilei that become scaly to

squamulose due to cuticular diffraction. Addition-

ally, large basidiomata frequently have stipes

clothed with pronounced longitudinal striations

that can form reticulations or become scaly near

the stipe apex (e.g., L. amethysteo-occidentalis, L.

nobilis, L. ochropurpurea, and L. trullissata).

BASIDIOSPORE COLOR IN MASS— Except for L.

amethystina and L. ochropurpurea, which can have

either white or light violet basidiospore deposits,

all North American taxa have white spore prints.

The color of the print will occasionally yellow with

age.

ADDITIONAL MACROMORPHOLOGICAL CHAR-

ACTERS—Characters such as type and degree of

pileus striations, pileus shape, lamellar attachment

and thickness, pileus and stipe context, or odor

and taste are not systematically significant within

Laccaria. Except for color and, in some instances,

size, micromorphological and cultural characters

must be used to differentiate taxa.

Basidioma Micromorphology

BASIDIA— The number of basidiospores borne

per basidium is significant in Laccaria. Although

many other genera of agarics have species with

varying number of sterigmata in one basidioma

(e.g., Hesler & Smith, 1963; Singer, 1986), the

character appears to be consistent in Laccaria. In

all of the material examined, the vast majority of

the basidia observed in a mount had the same

number of sterigmata. Basidia examined from ma-

terial of L.fraterna, L. pumila, and L. tortilis bore

2(-3) basidiospores. All of the rest of the North

American taxa had 4-sterigmate basidia. Bister-

igmate basidia generally had longer and stouter

sterigmata. No other basidial characters appeared

to have systematic significance.

BASIDIOSPORES— Basidiospore shape is of criti-

cal importance in designating species. Basidio-

spore shape terms used in this study are based on

Bas (1969), with basidiospore shape described in

terms of length-width ratios (Q): globose = 1 .0-

1.05, subglobose = 1.06-1.15, broadly ellipsoid =

1.16-1.23, ellipsoid or amygdaliform = 1.24-1.6,

oblong = 1.65-2.0, cylindrical or subfusiform >

2.0.

Specimens of most North American taxa have

basidiospores that are subglobose to broadly ellip-

soid. Laccaria proxima (Boudier) Patouillard and

L. oblongospora are characterized by having ellip-

soid to oblong basidiospores; basidiospores in

specimens of L. trullissata and L. maritima are

oblong to subfusiform. Globose basidiospores are

found in specimens of L. amethystina, L. ochro-

purpurea, L. ohiensis, L. striatula, and L. tortilis.

Basidiospore size is also an important system-

atic character in some instances. Individuals of

most taxa have overall mean basidiospore lengths

of 8-9 /mi. However, Laccaria bicolor, L. longipes

G. M. Mueller, L. nobilis, and L. trichodermoph-

ora are characterized by having relatively small

basidiospores (x < 8 Mm long), and specimens of

L. fraterna, L. montana, L. pumila, and L. tortilis

have larger basidiospores (x = 9.5-13 nm long).

The basidiospores of L. maritima and L. trullis-

sata are greater than 13 Mm in length.

Except for L. trullissata, which has finely rough-

ened basidiospores (figs. 4 la, 57b-d, 72d), all spe-

cies of Laccaria have echinulate basidiospores with

a plage near the hilar appendix. Echinulae length

and width at attachment are important systematic

characters within the genus.

Electron microscopic examinations of basidio-

spores using the carbon surface replica technique

(Bigelow & Rowley, 1968; Pegler & Young, 1971),

transmission electron microscopy (= TEM) (Bes-

son & Kiihner, 1971), and scanning electron mi-

croscopy (= SEM) (Pegler & Young, 1971; Mueller

& Sundberg, 1981; Irving et al., 1985; Mueller,

1991c; this paper, figs. 53-58) have shown details

of the surface and ornamentation characteristics.

At my request, A. von Hofsten (Institute of Phys-

iological Botany, University of Uppsala, Uppsala,

Sweden) examined basidiospores from collections

of several Laccaria species (L. bicolor, L. mariti-

ma, and L. proximo) and from a collection ol

Hydnangium carneum Wallroth apud Klotzsch

under the TEM (von Hofsten, unpubl.). The re-

sults of this study were concordant with the find-

ings of Besson and Kiihner (1971). The basidio-

spore echinulae of all Laccaria species examined

to date, plus the gasteroid relative Hydnangium

carneum, are composed of microtubules that run

perpendicular to the epispore (Besson & Kiihner.

1971; Kuhner, 1980). This type of echinulae ul-

trastructure appears to be unique to Laccaria,

Hydnangium, and probably Podohydnangium

Beaton, Pegler & Young (not examined undei

TEM). Echinulae ultrastructure is the primary syn-

apomorphy that supports the recognition of these

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

FIG. 1 . Representative pileipellis arrangements occurring in North American taxa ofLaccaria: a, trichodermium;

b, interwoven; c, interwoven with scattered ± perpendicular fascicles of hyphae. Scale line = 10 Mm.

FIELDIANA: BOTANY

three genera as a monophyletic group (see Phy-

logenetic Considerations).

The basidiospores in all taxa are nonamyloid

and acyanophilic.

PILEIPELLIS— Three types of hyphal arrange-

ments were found in Laccaria (fig. la-c): a tri-

chodermium, observed in most collections of L.

trichodermophora; interwoven as in collections of

L. ochropurpurea; or interwoven with scattered

nearly perpendicular fascicles of hyphae (the most

common pileipellis encountered). In L. vinaceo-

brunnea and in some collections of L. amethys-

tina, the hyphae of the pileipellis are interwoven

with very numerous, long, individual hyphae that

are arranged nearly perpendicular to the pileus

surface. If the erect hyphae were aggregated closer

together, the pileipellis could be described as a

palisadoderm.

Pileipellis hyphae were often encrusted with a

light to moderate yellowish brown pigment. In

young specimens of L. amethystina, L. amethys-

teo-occidentalis, and L. vinaceobrunnea, the hy-

phae occasionally appeared vinaceous brown in

mass.

Although data on the size of the terminal cells'

are presented in the species descriptions, the size

and shape of these cells appeared to have little

systematic significance. Additionally, the under-

lying tramal layer was morphologically undiffer-

entiated and systematically uninformative.

CHEILOCYSTIDIA— The cheilocystidia of most

Laccaria species, if present, are little more than

elongate, filamentous hyphae that extend beyond

the basidia and basidioles. Only in specimens of

L. amethystina, L. amethysteo-occidentalis, and L.

vinaceobrunnea were large (overall mean dimen-

sions up to 58 x 10 /mi), clavate to strangulate,

abundant cheilocystidia observed. In many col-

lections these cheilocystidia formed a nearly sterile

layer. The uniqueness and consistent presence of

large cheilocystidia in these three Laccaria taxa

was a good diagnostic character for herbarium ma-

terial that lacked macromorphological notes.

Pleurocystidia were not seen in any North

American material of the genus. Morphologically

undifFerentiated caulocystidia are present in some

taxa.

1 Because there is a nuclear continuity between hyphal

segments through the septum, each of these segments

should be termed a hyphal element and not a cell. For

the sake of avoiding confusion, however, the term cell

is used throughout this paper.

ADDITIONAL MICROMORPHOLOGICAL CHAR-

ACTERS—The constant occurrence of clamp con-

nections at virtually every septum and a parallel

or rarely subparallel lamellar trama are important

generic characteristics of Laccaria. Additionally,

all hyphae were nonamyloid and, unless otherwise

specified, hyaline in KOH.

The hyphae comprising the basal mycelium were

tightly interwoven and either morphologically un-

differentiated or barrel-shaped. The diameter of

these hyphae appeared to vary as much within a

taxon as between taxa.

Basidiospore and Basidium Cytology

Kiihner (1980, 1984) emphasized the occur-

rence of multinucleate basidiospores in Laccaria

in his decision to treat Laccaria in a family sep-

arate from other genera traditionally placed in the

Tricholomataceae. These reports prompted us to

investigate further the nuclear behavior in species

of Laccaria and Hydnangium. To determine the

significance of basidiospore and basidium cytol-

ogy in the systematics of Laccaria, cytological

studies on several species of Laccaria were carried

out in J. F. Ammirati's laboratory (Department

of Botany, University of Washington, Seattle).

Several questions were addressed during the

course of this study, including: ( 1 ) Is the occur-

rence of multinucleate basidiospores a character-

istic of the genus, or is this feature restricted to a

few taxa? (2) Where does postmeiotic mitosis oc-

cur in taxa with multinucleate basidiospores?

Basidia and basidiospores of representative

specimens of each of the 1 1 Laccaria species and

Hydnangium carneum listed in Table 1 were ex-

amined using fluorescent microscopy. Glutaral-

dehyde-fixed and nonfixed tissues were mounted

in Hoechst fluorescent dye and examined using a

Zeiss fluorescence microscope with 365 nm exci-

tation and 480 nm emission filters.

Multinucleate basidiospores appear to be a con-

stant feature within Laccaria, as they occur

throughout the genus from the putatively primi-

tive L. proxima to diverged taxa such as L. tortilis,

L. amethysteo-occidentalis, and L. trullissata (ta-

ble 1). These data also are concordant with the

hypothesis of the close relationship of Laccaria to

Hydnangium. According to Kiihner (1980, 1984),

the occurrence of multinucleate basidiospores is

rare in the Tricholomatales sensu Kiihner

(± Tricholomataceae sensu Singer).

MUELLER: SYSTEMATICS OF LACCARIA (AGARIC ALES)

TABLE 1. Number of nuclei observed in the basid-

iospores of examined Laccaria and Hydnangium visu-

alized with Hoechst fluorescent dye.

The following is a summary of results obtained

during studies of tetra- and bisterigmate Laccaria

taxa (L. bicolor, L. galerinoides Singer, L. laccata

var. pallidifolia, L. montana, L. proximo, L. prox-

imella Singer, L. pumila, L. tortilis, and L. vina-

ceobrunnea) using Giemsa-stained material ex-

amined under bright field microscopy. Detailed

results will appear in a separate publication (G. J.

Mueller, G. M. Mueller, L. Shih & J. F. Ammirati,

in prep.). The dikaryotic basidium of both tetra-

and bisterigmate Laccaria is more or less cylin-

drical in shape. The two nuclei move to the center

of the basidium and fuse to form the diploid nu-

cleus, during which time the basidium gradually

enlarges and becomes clavate in shape. The dip-

loid nucleus then moves to the apical region of the

basidium, where meioses I and II occur. These

divisions are chiastic, and the resulting four nuclei

migrate to the center of the basidium. During these

events the basidium enlarges to its mature size and

shape, and sterigmata with developing basidio-

spores are formed. In most cases, once the basid-

iospores are fairly well developed, the nuclei begin

to move through the sterigmata and into the ba-

sidiospores so that basidiospores from tetrasterig-

mate basidia each receive one nucleus, while those

with bisterigmate basidia each receive two nuclei.

In these cases the (nucleus) nuclei in the basidio-

spores then undergo a mitotic division so that ba-

sidiospores from tetrasterigmate basidia are bi-

nucleate and those of bisterigmate basidia are

tetranucleate. Occasionally this postmeiotic mi-

tosis occurs in the basidium before nuclear mi-

gration. In these cases, all eight nuclei migrate into

the basidiospores. In both scenarios, mature ba-

sidiospores are multinucleate.

Tommerup and colleagues reported similar nu-

clear behavior for L. fraterna (Tommerup et al.,

1991). According to them, however, nuclear be-

havior in Hydnangium carneum differs in that

postmeiotic mitosis occurs in the basidium prior

to migration into the basidiospores. Additional

information on nuclear behavior in Hydnangium

and Podohydnangium is necessary before it will

be possible to determine if multinucleate basidio-

spores in Laccaria and these two genera are ho-

mologous. The Hydnangium used by Tommerup

et al. (1991) is reported to have tetrasterigmate

basidia, and the illustrated basidiospores are

broadly ellipsoid and finely ornamented. This is

in contrast to my concept of H. carneum. All of

the collections that I have examined which are

referable to this taxon have bisterigmate basidia

that bear strongly echinulate, globose basidio-

spores. Similarly, published illustrations of basid-

iospores and basidia for this taxon usually depict

globose, strongly echinulate basidiospores and bi-

sterigmate basidia (e.g., Pegler & Young, 1979;

Beaton et al., 1984; Castellano et al., 1989). Until

a survey of other taxa in the genus is undertaken,

and until phylogenetic relationships within the ge-

nus are resolved, it is not possible to determine

the plesiomorphic condition for nuclear behavior

in Hydnangium.

Somatic Culture Mat Morphology

Somatic culture mat studies based on the classic

work of Nobles (1948, 1958b, 1965) were under-

taken to obtain additional informative characters.

Although becoming almost routine in studies of

the wood-rotting Aphyllophorales and many

groups of saprobic Agaricales, utilization of so-

matic culture mat data has only infrequently been

used in systematic studies of fungi that form ec-

tomycorrhizae. At least two factors are responsible

for this. First, many of these fungi are recalcitrant

to domestication (but see Hutchinson, 1990a,b;

Hutchinson & Summerbell, 1990). Second, early

work indicated that cultures of fungi that form

ectomycorrhizae exhibited few morphological dif-

ferences (e.g., Zak & Bryan, 1963; Zak & Marx,

1964).

Fries and Mueller ( 1 984) reported no differences

in morphology (except for the presence or absence

of clamp connections) between homokaryotic and

heterokaryotic isolates. Occasional differences in

10

FIELDIANA: BOTANY

growth rate, color intensity, and other features have

since been detected between heterokaryotic iso-

lates obtained via tissue culture, isolates originat-

ing as polysporous cultures, and homokaryotic

isolates (Kroppetal., 1986;Kropp&Fortin, 1988;

Mueller, unpubl.). While overall similarities are

normally observed, care must be used when em-

ploying isolates of different origin for comparative

studies. The following data are based primarily on

isolates of tissue culture origin.

MACROMORPHOLOGY— The two primary diag-

nostic characters were the color of the culture mat

on MMN and PDA (all isolates were white on

MEA) and the rate of growth (expressed as the

radius of the culture mat at week 3 and week 6)

on each of the three media employed. Photographs

of representative isolates are included as part of

the description for a number of North American

taxa (figs. 7, 10, 13, 31, 34, 37, 44).

Taxa that had white to off-white culture mats

on all three media were L. fraterna, L. laccata, L.

longipes, L. montana, L. ohiensis, L. proxima, L.

pumila, and L. striatula. No isolates were obtained

of L. maritima or L. tortilis. Isolates of all other

North American taxa were violet to purple on PDA

and MMN. To date there is a 100% correlation

between basal mycelium color and somatic culture

mat color. This supports the utility of basal my-

celium color as a good delimiting field character.

Although a slight bleaching of color was often

noted on the reverse side of the culture mat, no

significant color changes occurred. Additionally,

no exudates were apparent.

Along with color, the rate of growth could be

used to delimit taxa. Isolates of most taxa grew at

a moderate rate on all three media (20-50 mm on

PDA, 30-70 mm on MMN, and 40-70 mm on

MEA— all at week 6). Isolates of L. amethysteo-

occidentalis, L. montana, and L. ohiensis grew

much more slowly (often only 10-15 mm after 6

weeks' growth). Conversely, isolates of L. bicolor,

L. nobilis, L. oblongospora, and L. trichodermo-

phora grew more rapidly.

Terminology used in discussing mat and margin

texture was from Nobles (1948, 1965).

Except for an occasional pruinose, aerial layer

of hyphae observed in older cultures of many taxa,

the mycelium of all of the isolates grew tightly

appressed to the agar surface. The transparency of

the culture mat was an outcome of the thickness

and intricacy of the interwoven mat. All isolates

exhibited a felty, thick culture mat on PDA. The

mat texture on both MMN and MEA varied from

silky to subfelty to felty. Often the mat was thickest

near the inoculation plug. In most cases, culture

mats were of uniform thickness from the plug to

the margin. In some taxa, however, variously dis-

tributed thicker zones were observed. These thick-

er zones could be scattered, small sectors (e.g.,

some L. trichodermophora isolates on MMN and

L. bicolor on MEA), two or three concentrically

arranged bands (e.g., L. amethysteo-occidentalis

on MEA), or radially arranged pie-shaped or den-

dritic sectors radiating away from the inoculation

plug (e.g., L. trichodermophora on PDA).

When describing the margin texture and color,

I refer to the advancing zone of the culture mat.

This zone is generally somewhat thinner than the

rest of the mat and can be either a discrete, easily

recognizable area or not well differentiated. On all

three media, this zone was always silky to subfelty

and thus presented little systematically informa-

tive data.

All of the isolates had the same musty odor on

all three media.

Growth or diffusion zones were not obtained on

gallic acid agar with any of the isolates. Immediate

reaction to the gum guaiac drop test was observed

only in some isolates of L. bicolor. I did not at-

tempt other tests for the presence or absence of

extracellular enzymes because of these basically

negative results. Hutchison (1990a), however, per-

formed drop tests of 1-naphthol and p-cresol on

numerous isolates of ectomycorrhizal fungi grow-

ing on several different media and reported the

presence of tyrosinase activity in all of the Lac-

caria that he tested (i.e., L. bicolor, L. laccata, L.

ochropurpurea, and L. proximo). Only L. bicolor

showed any indication of laccase activity (Hutch-

ison, 1990a).

Hutchison (1990b) investigated enzymatic deg-

radation of various carbon and nitrogen com-

pounds by fungi that form ectomycorrhizae. Using

the same taxa listed in the previous paragraph, he

reported that Laccaria did not degrade pectin, lip-

id, amylose, or gelatin but showed various levels

of degradation of casamino acids and urea. Hutch-

ison and Summerbell (1990) reported that these

same isolates gave red to violet reactions to Dia-

zonium Blue B when treated with cold KOH and

yellow reactions without cold KOH treatment.

MICROMORPHOLOGY— There was little hyphal

differentiation observed within and between the

Laccaria isolates examined during this study. No

spores were formed in culture.

In all isolates, the vast majority of hyphae were

morphologically undifferentiated, with clamp con-

nections at nearly all septa (fig. 2a). Scattered among

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

11

these sparsely branched hyphae were subcoralloid

to coralloid hyphae (fig. 2b,c) and/or irregularly

swollen hyphae (fig. 2d). All hyphae were hyaline

in KOH, except where noted. Localized, slightly

thick-walled swellings were often observed in plates

of all taxa (fig. 2e). These swellings could either be

terminal or intercalary and could be found in chains

of two to four. They are likely a response to water

stress, as they become more abundant when the

agar in Petri plates loses moisture. Hutchison

(1989) reported similar swellings from numerous

isolates of ectomycorrhizal fungi.

Pantidou et al. (1983) reported the presence of

holoblastic conidia from a purported culture of

Laccaria laccata. Hutchison (1989), however, re-

ported that these structures were secretory cells of

a Pleurotus sp. and that the isolate used by Pan-

tidou et al. (1 983) was from a species of that genus,

not L. laccata.

Intra- and Intel-collection Pairing Reactions

Information on intra- and intercollection pair-

ing reactions has only recently been employed for

systematic and biological studies of fungi that form

ectomycorrhizae (Fries, 1987). Fries (1977) first

reported the successful germination of basidio-

spores from collections of Laccaria. Several years

later he reported the occurrence of several inter-

sterility groups within L. laccata sensu lato (Fries,

1 983a). Fries and Mueller ( 1 984) later determined

that these intersterility groups were referable to

separate species. They documented a good cor-

relation between the identified intersterility groups

and species based on morphological characters,

using Swedish isolates of L. amethystina, L. bi-

color, L. laccata, and L. proxima. Intraspecific

pairings of these Swedish isolates revealed a high

incidence of intercompatibility in three of these

species (all but L. laccata). Two intersterility groups

were detected within Swedish isolates from mor-

phologically similar collections identified as L.

laccata. The two intersterility groups within L.

laccata were treated as sibling species because they

could not be delimited on morphological charac-

ters (Fries & Mueller, 1984; Mueller & Vellinga,

1986). Studies by Kropp and Fortin (1988) and

Doudrick and Anderson (1989) documented the

occurrence of two or more intersterility groups

within the North American population of L. bi-

color.

When used in conjunction with data from other

analyses, information on intercollection pairing

reactions has proven useful for circumscribing taxa

(Mueller & Gardes, 1991; Mueller, 1991c). Muel-

ler and Gardes (1991) reported three intersterility

groups within the examined material of North

American L. bicolor. Intragroup intercompatibil-

ity was high, and most intergroup pairings were

intersterile. These groups could be circumscribed

on both morphological and molecular characters

and consisted of isolates of L. bicolor sensu stricto,

L. nobilis, and L. trichodermophora. Questions re-

main as to the relationship of Swedish material,

morphologically similar to North American ma-

terial of L. bicolor sensu stricto, to the three North

American taxa. The two isolates of Swedish origin

used as testers were 100, 57, and 21% intercom-

patible with North American isolates of L. bicolor,

L. nobilis, and L. trichodermophora, respectively.

Interstock pairing reactions were also useful in

a study of the L. laccata complex (Mueller, 1 99 Ic).

However, because isolates of L. laccata var. lac-

cata were not available for inclusion in these anal-

yses, some of the systematic conclusions remain

tentative. Several North American intersterility

groups were detected, and all tested North Amer-

ican isolates were intersterile with both of the in-

tersterility groups reported from Sweden by Fries

and Mueller (1984). Most, but not all, of these

groups could be delimited morphologically. Mo-

lecular divergence (detected through analyses of

restriction fragment length polymorphisms of mi-

tochondrial and nuclear ribosomal DNA) was also

detected between several of these intersterility

groups (Gardes et al., 1990, 199 la; see below).

Intersterility groups that could be delimited from

morphological characters were recognized at the

species level (i.e., L. laccata, L. longipes, L. mon-

tana, L. ohiensis, and L. striatula).

As in the study on the L. bicolor complex

(Mueller & Gardes, 1991), data obtained to date

do not resolve questions concerning potential gene

exchange between geographically distant popula-

tions of some putatively cosmopolitan species in

the L. laccata complex (Mueller, 1 99 Ic). The most

commonly collected North American taxon in the

complex is L. laccata var. pallidifolia. Mueller and

Vellinga (1986) and Mueller (199 la) reported this

taxon as being abundant in Europe. However,

North American and Swedish isolates referable to

this taxon are intersterile (Mueller, 1991c). Un-

fortunately, representative Swedish material of this

taxon was not included in the studies of Gardes

et al. (1990, 1991a,b), so data are not available on

molecular divergence between the two popula-

tions. It is not possible to delimit collections from

12

FIELDIANA: BOTANY

FIG. 2. Hyphal modifications observed during micromorphological analyses of 6-week-old somatic culture mats

of Laccaria taxa: a, typical morphologically undifferentiated hyphae— note the presence of clamp connections and

the regular branching pattern; b, coralloid hyphae— note the numerous, short, intertwining branches; c, subcoralloid

hyphae; d, irregularly swollen hyphae; e, hyphae with terminal and intercalary swellings. Scale line = 10 pm.

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

13

the two populations based on morphology (Muel-

ler, 1991c). For now, therefore, I treat these two

potentially intersterile populations as contaxic.

Tested isolates of L. amethysteo-occidentalis, L.

amethystina, L. proxima, and L. vinaceobrunnea

were intersterile in all attempted interspecific pair-

ings. Intraspecific pairings were nearly completely

intercompatible within these species. However,

homokaryotic isolates were available from only

two or three stocks for most of these species, so it

was not possible to rigorously test the degree of

intraspecific intercompatibility.

In this study I have delimited species so that

they are presumably monophyletic and are diag-

nosable by a unique combination of character

states. Data from intercollection pairings were used

to help identify groups to analyze in detail for

potential morphological and molecular diver-

gence. Because data on morphology, breeding, and

ecology are not always concordant, it is inadvis-

able to rigorously adhere to the biological species

paradigm (see discussions in Mishler & Donoghue,

1982; Donoghue, 1985; de Queiroz & Donoghue,

1988, 1990; Cracraft, 1990; Vilgalys, 1991).

Restriction Fragment Length Polymorphisms

of rDNA and mtDNA

It is not yet possible to routinely obtain in vitro

basidioma production for any species ofLaccaria,

or most other fungi that form ectomycorrhizae.

One consequence of this inability to obtain the

complete life cycle for these organisms is that it is

impossible to carry out genetic analyses or to de-

termine if intercompatible isolates are fertile (would

produce viable progeny). This problem, coupled

with the fact that the ability to mate is a plesio-

morphic character state (e.g., Donoghue, 1985),

makes it necessary to have data from other anal-

yses to substantiate hypotheses of gene exchange

between populations. Gardes et al. (1990, 199 la)

obtained data on restriction fragment length poly-

morphisms (RFLPs) for both nuclear ribosomal

DNA (rDNA) and mitochondrial DNA (mtDNA)

to (1) investigate possible genetic divergence be-

tween species and populations of the same puta-

tive species, (2) determine concordance of data

obtained through morphological analyses and

pairing analyses, and (3) evaluate molecular mark-

ers for isolate typing. The resulting data could not

be used for phylogenetic reconstructions because

the numerous length mutations that were detected

within the segments of DNA analyzed prevented

making the necessary assumptions of homology.

Comparable results were obtained with both

mtDNA and rDNA for L. amethystina and L.

laccata sensu lato (Gardes et al., 1990, 199 la;

Mueller, 1 99 Ic), in which divergence was detected

between North American and Swedish isolates of

these taxa. Divergence was also detected between

the tested intersterility groups of the North Amer-

ican L. laccata complex.

Conflicting results were obtained with mtDNA

and rDNA within the L. bicolor complex (Gardes

et al., 1990, 199 la; Mueller & Gardes, 1991). Di-

vergence in rDNA was detected between the North

American and Swedish populations but was not

observed between North American intersterility

groups. Conversely, divergence was detected be-

tween each of the North American intersterility

groups but was not detected between North Amer-

ican and Swedish populations based on mtDNA

polymorphisms. Additional European material

needs to be examined to attempt to resolve this

discrepancy. Only two Swedish isolates of L. bi-

color sensu lato were utilized by Gardes et al. ( 1 990,

1 99 1 a), so it is not possible to compare the amount

of heterogeneity of either mtDNA or rDNA within

North American and European populations. A

possible explanation for these conflicting results is

that Swedish L. bicolor migrated from a large North

American population that contained a pool of

mtDNA variation (J. W. Taylor, University of

California, Berkeley, pers. comm.). The Swedish

population would, therefore, contain only a subset

of the mtDNA variation. Following migration, the

North American population underwent diver-

gence of morphological and pairing alleles, result-

ing in L. nobilis and L. trichodermophora. Some

of the mtDNA variation within the original North

American pool has subsequently been lost, as ev-

idenced by the data on RFLPs, which uncovered

more intraspecific than interspecific similarity in

mtDNA for the three North American taxa. This

hypothesis cannot be tested until a robust phylog-

eny for the group is obtained.

In Vitro Ectomycorrhizal Synthesis Results

Isolates of Laccaria are frequently used in ap-

plied and basic studies on ectomycorrhizae (see

Kropp & Langlois, 1990). In vitro mycorrhizal

synthesis studies employing the growth pouch

technique of Fortin et al. (1983) are ongoing as

part of my studies on Laccaria. Experiments were

14

FIELDIANA: BOTANY

run in a Plexiglas mycorrhizal synthesis chamber,

the design for which was modified from plans from

Steven Miller (University of Wyoming, Laramie,

pers. comm.). The primary goals of these studies

have been to further characterize species of Lac-

caria as well as to document the ability of partic-

ular species of Laccaria to form ectomycorrhizae

with select tree species in the laboratory.

To date we have synthesized ectomycorrhizae

between several Laccaria species (L. amethysteo-

occidentalis, L. bicolor, L. laccata var. pallidifolia,

L. proximo, and L. striatula) and the following

North American trees: Picea sitchensis (Bong.)

Carr., Pinus ponderosa Laws., P. resinosa Ait., and

Pseudotsuga menziesii (Mirb.) Franco. Ectomy-

corrhizae have also been synthesized between L.

trullissata and Pinus resinosa and between several

South American isolates of L. ohiensis and seed-

lings of the southern beech, Nothofagus obliqua

(Mirbel) Oerst.

Although macromorphology of the ectomycor-

rhizae varies with the species of host tree (e.g.,

degree of branching), their micromorphology is

similar. In all material examined to date, a well-

defined, 1 5-60 MHI thick, tightly interwoven man-

tle of clamped, morphologically undifferentiated

hyphae was formed. No cystidia-like elements have

been observed. All infected short roots had a well-

developed Hartig net that extended through 70-

100% of the cortex. These data coincide with pub-

lished data on Laccaria ectomycorrhizae.

Ecology and Distribution

Many species of Laccaria show some degree of

host specificity. Laccaria proxima and L. laccata

var. pallidifolia are the only North American taxa

that appear to be associated commonly with both

Fagaceae and Pinaceae. Laccaria amethystina and

L. ochropurpurea appear to be associated solely

with temperate hardwoods, especially species of

Quercus and Fagus grandifolia, while L. vinaceo-

brunnea has only been found under live oak, Quer-

cus virginiana. Laccaria ohiensis has not been

commonly collected in north temperate forests. In

tropical and south temperate habitats, it is found

associated with Quercus and Nothofagus, respec-

tively.

All of the members of the L. bicolor complex

(L. bicolor, L. nobilis, and L. trichodermophord)

appear to be associated with Pinaceae in North

America. Laccaria trichodermophora can shift

hosts when members of the Pinaceae are not avail-

able—it has been found under tropical Quercus in

Costa Rica (Mueller & Strack, unpubl.). Similarly,

although L. amethysteo-occidentalis is most com-

monly found with conifers, especially Pseudotsu-

ga, it can be found under Quercus in California.

Laccaria montana and L. pumila are commonly

collected in arctic and alpine habitats, where they

appear to be associated with Pinaceae (especially

Pinus), Salix, and Betula.

Although many species of Laccaria can be en-

countered growing among mosses, only L. lon-

gipes, L. bicolor, and L. proxima are found com-

monly in Sphagnum bogs. Laccaria trullissata and

L. maritima are found only in sand dunes or other

very sandy areas, where they are putatively as-

sociated with species of Pinus.

Only L. laccata var. pallidifolia, L. proxima, and

L. tortilis were found throughout the study range.

Laccaria bicolor occurs in all areas except south-

eastern North America. All other taxa showed

some geographical restriction. Taxa reported only

from eastern North America are L. amethystina,

L. maritima, L. longipes, L. oblongospora, L. och-

ropurpurea, L. ohiensis, L. striatula, L. tricho-

dermophora, L. trullissata, and L. vinaceobrunnea.

Conversely, L. amethysteo-occidentalis, L. mon-

tana, L. nobilis, and L. pumila have not been re-

ported east of the Great Lakes region.

Phylogenetic Considerations

Placement of Laccaria in Ordinal and

Family Treatments

A robust hypothesis of phylogenetic relation-

ships for the Agaricales has not been developed.

Several classifications have been advanced that

reflect differences in views of relationships among

genera in the group (e.g., Kuhner, 1980; Jtilich,

1981; Singer, 1986).

Kuhner (1980, 1984) proposed dividing the

Agaricales into several small orders that he felt

were easier to define and had sharper boundaries

than those traditionally recognized (e.g., Singer,

1975). He treated Laccaria, along with its gaster-

oid counterpart Hydnangium, as a separate family

named the Hydnangiaceae within his order Trich-

olomatales (Kuhner, 1980, 1984) (table 2). Hyd-

nangium is the sister taxon to Laccaria and Trich-

olomataceae is the sister taxon to Hydnangiaceae

in this classification.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

15

TABLE 2. Placement ofLaccaria in Kiihner's (1980), Jiilich's (1981), and Singer's (1986) classifications of agari-

coid Hymenomycetes.

ku liner. 1980

Jiilich, 1981

Singer, 1986

TRICHOLOMATALES

Tricholomataceae

Clitocybeae

Gerroneama, Omphalina, Ar-

rhenia, Cantharellula, Cli-

tocybe, Lepista, Ripartites,

Armillaria

Lyophylleae

Biannularieae

Tricholomeae

Tricholomopsis, Leucopaxillus,

Tricholoma, Pseudobaeo-

spora, Melanoleuca

Cysterodermateae

Hydnangiaceae

Laccaria, Hydnangium

Rhodotaceae

Pleurotaceae

Marasmiaceae

Hygrophoraceae

Amanitaceae

TRICHOLOMATALES

Hygrophoraceae

Laccariaceae

Laccaria

Hydnangiaceae

Hydnangium

Fayodiaceae

Collybiaceae

Macrocystidiaceae

Xerulaceae

Gigaspermaceae

Armillariaceae

Biannulariaceae

Tricholomataceae

Leucopaxillaceae

Lyophyllaceae

Marasmiaceae

Amparoinaceae

Mycenaceae

Favolaschiaceae

Nyctalidaceae

Cyphellopsidaceae

Lachnellaceae

Resupinataceae

Rhodotaceae

AGARICALES

Tricholomataceae

Lyophylleae

Termitomyceteae

Tricholomateae

Laccariinae

Laccaria

Clitocybinae

Clitocybe, Lepista, Tricholomop-

sis

Tricholomatinae

Tricholoma

Omphalinae

Armillariella, Arthrosporella,

Lulesia, Arrhenia, Leptoglos-

sum, Omphalina, Gerrone-

ma, Callistosporium, Pleuro-

collybia, Lactocollybia,

Macrocystidia, Fissolimbus,

Asproinocybe

Leucopaxilleae

Biannularieae

Collybieae

Resupinateae

Panelleae

Marasmieae

Myceneae

Pseudohiatulaeae

Rhodoteae

Jiilich (1981) also recognized the Tricholoma-

tales as a separate order but treated Laccaria in

his monotypic family Laccariaceae separate from,

but closely related to, the Hydnangiaceae (table 2).

These 2 families are among the 22 families that

he recognized for the order (Jiilich, 1981). Unfor-

tunately, Jiilich was not explicit on intraordinal

relationships except to say that he did not recog-

nize close relationships among many of these fun-

gi. Thus, it is not clear what he thought was the

sister group to the Laccariaceae and Hydnangi-

aceae.

Singer (1986) maintained that separation of the

Agaricales into a number of smaller orders is not

warranted. Within his classification, Singer (1986)

placed Laccaria in a separate subtribe (Laccari-

inae) in Tribus Tricholomateae of the Tricholoma-

taceae (table 2). Singer maintained that Hydnan-

gium, as well as all other Gasteromycetes, is

sufficiently distinct to prevent it from being treated

in the Agaricales. Subtribe Clitocybinae is the sis-

ter taxon to Laccaria and Termitomyceteae is the

sister taxon to Tricholomateae in this classifica-

tion.

Molecular data obtained to date do not contain

information with which the Agaricales sensu Sing-

er can be divided into smaller orders. Rehner et

al. (1990) reported that their sequence data of mi-

tochondrial and nuclear ribosomal RNA genes do

not resolve phylogenetic relationships within the

Agaricales except to support the separation of the

Boletales and the Russulales from the rest of the

agarics. Lacking supportive evidence from molec-

ular analyses, and heeding Singer's (1986) argu-

ments for the use of caution regarding the multi-

plication and upgrading of higher taxa, I treat

Laccaria, along with Hydnangium and Podohyd-

nangium (see below), within the Tricholomata-

ceae. It was beyond the scope of this study to try

to resolve phylogenetic relationships within the

Tricholomataceae. Until these relationships have

been rigorously analyzed, I do not recognize in-

frafamiliar taxa in the Tricholomataceae. How-

ever, I accept Singer's (1986) and Kiihner's ( 1 980)

view that Laccaria has closer affinities with genera

in Singer's Tricholomateae and Kiihner's Tricho-

lomataceae than with other genera in the Tricho-

lomataceae sensu Singer (1986).

16

FIELDIANA: BOTANY

Relationship of Laccaria to Hydnangium

and Podohydnangium

Podohydnangiutn must be considered along with

Hydnangium in discussions of the relationship of

Laccaria to putative gasteroid relatives. Podo-

hydnangium is a monotypic genus that differs from

Hydnangium by having a distinct stipe-columella

and, therefore, appears intermediate between Lac-

caria and Hydnangium (Beaton et al., 1 984). Podo-

hydnangium was not included in Runner's (1980)

and Jiilich's (198 1) treatments because it was first

described in 1984, and it was excluded from Sing-

er's (1986) classification for the same reason that

he excluded Hydnangium: uncertainty of affinity.

The three classifications discussed above treat

the relationship of Laccaria to Hydnangium and

Podohydnangium differently (table 2). This is be-

cause of fundamental differences in opinion re-

garding the relationship of gasteroid genera to their

agaric counterparts. Kiihner (1980) and Jiilich

(1981) both treated certain gasteroid taxa within

the Agaricales, incorporating them into the clas-

sification with their putative sister taxa. Singer

(1986), on the other hand, maintained that the

relationship of these fungi to epigeous agarics is

not sufficiently resolved to justify incorporating

them into the Agaricales.

Although Laccaria, Podohydnangium, and

Hydnangium differ drastically in macromorphol-

ogy, they share several presumably derived mi-

cromorphological character states, including iden-

tical basidiospore ornamentation and, at least in

Laccaria and Hydnangium (Podohydnangium has

not been examined), multinucleate basidiospores.

Laccaria is unique among epigeous agarics in

that the conic echinulae, diagnostic features of the

genus, are formed by microtubules that run per-

pendicular to the epispore (Besson & Kiihner, 1971;

Kuhner, 1980; v. Hofsten & Mueller, unpubl.).

SEM micrographs of basidiospores from Podohyd-

nangium australe Beaton, Pegler & Young and

several Hydnangium taxa have documented the

similarity of shape of the basidiospore ornamen-

tation between these taxa and Laccaria (Pegler &

Young, 1979; Beaton et al., 1984; Castellano et

al., 1989). Unpublished TEM data obtained by v.

Hofsten (Institute of Physiological Botany, Uni-

versity of Uppsala, Uppsala, Sweden) documented

that the basidiospore wall ultrastructure of Hyd-

nangium is similar to that found in Laccaria (i.e.,

the echinulae are composed of microtubules that

run perpendicular to the epispore).

All examined taxa of Laccaria as well as Hyd-

nangium carneum have multinucleate basidio-

spores (table 1; Kuhner, 1980; Tommerup et al.,

1991).

The three genera also share several plesiomor-

phies such as having abundant clamp connections;

having nonamyloid, acyanophilic basidiospores;

and lacking a heteromerous trama (Pegler & Young,

1979; Beaton et al., 1984). Finally, Podohydnan-

gium australe and at least some species of Hyd-

nangium appear similar in color to orange-brown

Laccaria.

The genera differ in that Hydnangium and Podo-

hydnangium have statismosporic basidiospores

that are orthotropic in development and Laccaria

has ballistosporic basidiospores that are hetero-

tropic in development. But, as pointed out by sev-

eral authors (e.g., Pegler & Young, 1979; Beaton

et al., 1984), Hydnangium is not closely related to

any of the genera such as Octavianina O. Kuntze

formerly treated in the polyphyletic Hymenogas-

trales sensu Singer and Smith ( 1 960) and others.

Although Laccaria, Hydnangium, and Podo-

hydnangium appear to form a monophyletic group,

it is currently not possible to undertake a rigorous

analysis of the relationship of these three genera

to each other as no detailed systematic work has

been carried out on either Hydnangium and Podo-

hydnangium and species circumscriptions, com-

position, and relationships are still uncertain in

these two genera. Castellano and Trappe (1990)

accepted 23 names in Hydnangium in their bib-

liographic survey of Australian gasteroid fungi.

Numerous systematic problems remain in the

group, however, and some of these taxa probably

belong in other genera. Until intra- and interge-

neric relationships within this group are resolved,

I choose to treat the taxa in this group as three

separate genera (Laccaria, Hydnangium, Podo-

hydnangium) in the Tricholomataceae sensu Sing-

er (1986) amended to include Hydnangium and

Podohydnangium. The inability to resolve infrafa-

miliar relationships within the family precludes

recognizing the clade composed of these genera in

a formal classification (see above).

Previously Published Infrageneric

Classifications Proposed for Laccaria

Three primary infrageneric classifications have

been proposed for Laccaria (Bon, 1983; Singer,

1986; Ballero & Contu, 1989) (table 3). Moser

(1983), Clemencon (1984), and others have pub-

lished variations of these classifications that do

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

17

TABLE 3. Primary infrageneric classifications proposed for Laccaria. Names in parentheses are the correct name

for the taxon.

Bon, 1983

Singer, 1986

Ballero and Contu, 1989

Sect. Maritimae Bon

L. trullissata

L. maritima

Sect. Amethystinae Bon

L. amethystina

L. bicolor

L. purpureobadia

Sect. Laccata

Stirps Ohiensis

L. ohiensis (= L. impolitd)

L. tortilis

L. altaica (= L. pumild)

L. striatula (= ?)

L. lateritia (= L. fraternd)

Stirps Laccata

L. laccata

L. affinis (= L. laccata var.

pallidifolia)

Stirps Tetraspora

L. proximo (= ?)

L. tetraspora (= L. ohiensis)

Stirps Trullissata

L. trullissata

L. maritima

Stirps Amethystina

L. ochropurpurea

L. bicolor

L. calospora (= L. amethy-

stina)

L. amethystina (= L. ame-

thysteo- occidentalis)

L. lilacina

Stirps Laccata

L. laccata

L. farinacea (= L. trichoder-

mophord)

L. proximella

L. proximo

L. tetraspora (= L. ohiensis)

L. montana

L. altaica (= L. pumild)

L. echinospora (= L. tortilis)

L. fraterna

Stirps Galerinoides

L. galerinoides

L. vinaceoavellanea

Stirps Purpureobadia

L. purpureobadia

Sect. Maritimae Bon

L. trullissata

L. maritima

Sect. Amethystinae Bon

L. amethystea (- L. amethy-

stina)

L. calospora (= L. amethy-

stina)

L. violaceonigra

L. masonii

L. bicolor

L. bullulifera

L. farinacea (= L. trichodermo-

phord)

Sect. Laccaria

Subsect. Bisporae Contu

L. echinospora (= L. tortilis)

L. singeri (= L. impolitd)

L. lateritia (= L. fraternd)

L. pumila

Subsect. Laccaria

L. purpureobadia

L. lutea (= ?)

L. proximo

L. montana

L. laccata

L. tetraspora (= L. ohiensis)

L. affinis (= L. laccata var. pal-

lidifolia)

not differ significantly from those presented in Ta-

ble 3.

The primary difference between Bon's and Bal-

lero and Contu's classification versus that of Sing-

er's is the rank at which they recognized subgeneric

taxa. Singer (1986) used the term stirps (a term

not recognized by the International Code of Bo-

tanical Nomenclature, Greuter et al., 1988) rather

than section to reflect the small hiatus between the

subgeneric groups that he accepted. Bon (1983)

and Ballero and Contu (1989) recognized three

sections, with section Laccaria (incorrectly named

Laccata by Bon, ICBN Art. 22.1, Greuter et al.,

1988) being further divided into several sub-

groups. All three classifications recognized a sep-

arate group composed of L. maritima and L. trul-

lissata and a group composed of L. amethystina

and other taxa with violet to purple basidiomata

(table 3). Bon (1 983) and Ballero and Contu ( 1 989)

each recognized the species that have bisterigmate

basidia as a separate subgroup. Singer (1986) in-

cluded these taxa among species with tetrasterig-

mate basidia. He recognized stirps Galerinoides

and Purpureobadia on differences in basidioma

colors (Singer, 1986). Other differences between

these three classifications (table 3) are due pri-

marily to either varying interpretation of taxa or

the inclusion of different taxa.

Cladistic Analyses

Cladistic analyses were undertaken to resolve

infrageneric relationships within Laccaria. The in-

frageneric classifications of Bon (1983), Singer

(1986), and Ballero and Contu (1989) discussed

above were based on those authors' interpretations

of the evolutionary history of the group. These

authors, however, did not provide explicit state-

ments regarding crucial assumptions and decisions

used to develop their classifications. Without ex-

plicit information on choice and weighting of char-

acters, character state evolution, homoplasy (con-

vergence or parallelisms), and so forth, it is

impossible to make an objective comparison or

rigorously choose between these conflicting clas-

sifications.

18

FIELDIANA: BOTANY

Although cladistics has been used commonly in

studies of plants and animals, such analyses have

infrequently been used in fungal systematics. Cla-

distic methods are based on the theories first ex-

pounded by Hennig (1966), which have subse-

quently been expanded and modified by numerous

workers (see reviews in Eldredge & Cracraft, 1 980;

Nelson & Platnick, 1981; Wiley, 1981; Duncan &

Stuessy, 1984; Stuessy, 1990). The theoretical ba-

sis for these methods includes the following: (1)

phylogenetic relationships are based on the idea

of common ancestry (monophyly), (2) evidence for

monophyletic groups (all, and only, the descen-

dants of a particular ancestor) can only be deter-

mined by the detection of shared derived character

states (synapomorphies), and (3) shared primitive

character states (symplesiomorphies) do not pro-

vide evidence for relationships. Although there are

operational and theoretical difficulties involved

with any technique, cladistic analyses provide a

rigorous method for making hypotheses of phy-

logenetic relationships.

Unfortunately, Laccaria does not lend itself to

cladistic analysis. Problems in determining out-

groups and in using the outgroup criterion for

character state polarization are treated in the next

subsection. Problems in choosing characters and

in determining character state homology are also

treated below. Care must be used, therefore, when

interpreting the following results from the cladistic

analyses. They are presented only as a working

hypothesis of the evolutionary history of the ge-

nus, subject to revision.

DISCUSSION OF CHOICE OF OUTGROUPS— Lack of

consensus regarding relationships within the Agar-

icales sensu Singer (1986) prevented me from

making an unequivocal choice of an outgroup (see

discussion at the beginning of this section and data

in tables 2, 3). Uncertainty is not limited to the

determination of the sister group to Laccaria, it

also applies to the generic composition and cir-

cumscriptions of potential outgroups (Kiihner,

1980, 1984; Singer, 1986).

The classifications presented in Table 2 propose

conflicting hypotheses regarding the sister taxon

to Laccaria. I used the entire Tricholomateae Sing-

er, minus Laccaria, as the sister group to Laccaria.

This group of taxa is roughly equivalent to the

Clitocybeae plus Tricholomeae in Kuhner's Trich-

olomataceae (Kuhner, 1980, 1984). Cantharellus

was used as the sister group to the Tricholoma-

taceae. Although some workers do not derive the

Tricholomataceae from a Cantharellus-like an-

cestor (e.g., Singer, 1986), I find this to be a plau-

sible hypothesis, following the arguments of many

workers (e.g., Petersen, 1971; Kuhner, 1980, 1984;

Bigelow, 1982).

It was well beyond the scope of this study to try

to resolve relationships within the heterogeneous

Tricholomateae. Instead, I divided the group into

smaller units based only on characters shared by

the outgroup and ingroup. Using this criterion I

used the following operational units as outgroups:

Cantharellus, Clitocybe, Lepista, Tricholomopsis 1

& 2 (differing by basidiospore shape; represented

by Tricholomopsis flavissima (Smith) Singer and

T. rutilians (Schaeff.: Fr.) Singer, respectively),

Tricholoma 1 & 2 (differing by basidiospore shape;

represented by Tricholoma aurantium (Fr.) Rick-

en and T. michiganense Smith, respectively), Om-

phalinae 1 & 2 (differing by basidiospore shape;

represented by Omphalina hepatica (Fr.) Orton

and Leptoglossum rickenii (Hora) Singer, respec-

tively), and Omphalinae 3-5 (differing by the num-

ber of sterigmata per basidium and number of

nuclei per basidiospore; represented by Gerronea-

ma chrysophyllwn (Fr.) Singer, Omphalina pseu-

doandrosacea (Bull.) Moser, and O. griseopallida

(Desm.) Quel., respectively) (table 5). For in-

groups, I used all of the Laccaria taxa recognized

from the continental United States and Canada. I

further divided L. laccata into three groups, L. lac

1-3 (differing in basidiospore shape), because of

the high degree of plasticity observed in this char-

acter in this taxon. Extralimital taxa were not in-

cluded in these analyses because of a lack of in-

formation on somatic culture mat morphology and

difficulties in interpreting the macromorphology,

especially color, for a number of taxa that I know

only from the literature and from an examination

of their type specimens.

Another serious problem in determining suit-

able taxa to use as outgroups to Laccaria is that

many of the systematically informative characters

in Laccaria do not occur in prospective outgroups

(e.g., length and width of basidiospore echinulae

and, as coded, basidioma and culture mat pig-

ments). It also was impossible to determine char-

acter state homology for characters such as basid-

ioma and basidiospore size between putative

outgroups and Laccaria taxa. Because of these

problems, only 5 of the 1 4 characters employed

in the final analyses could be coded for both the

outgroups and ingroups (tables 4, 5). Thus, most

of the ingroup characters could not be polarized

directly by outgroup comparison (Watrous &

Wheeler, 1981; Maddison et al., 1984).

Three separate sets of analyses were run. First,

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

19

TABLE 4. Characters and their states used in cla-

distic analyses.

1 . Number of sterigmata per basidium. 0 = 4; 1 = 2,

3; 2 = 5-8

2. Number of nuclei/basidiospore. 0 = 1; 1 = multiple

3. Echinulate basidiospores with echinulae formed by

perpendicular microtubules. 0 = absent; 1 = present

4. Mean echinulae length (in j*m). 0 = rugulose; 1 =

< 0.5; 2 = 0.5-1; 3 = 1-2; 4 = > 2

5. Echinulae base width (in /*m). 0 = ^ 1; 1 = 5: 1.2

6. Mean basidiospore length. 0 = short (< 8 /mi); 1 =

moderate (8-10 urn); 2 = long (10-13 (im); 3 =

elongate (> 13.5 nm)_

1. Basidiospore shape (Q). 0 = globose_«2 = 1-1.05);

1 = subglobose to broadly ellipsoid (Q = 1.06-1.23);

2 = ellipsoid (Q = 1.24-1.6); 3 = oblong (Q = 1.65-

2); 4 = cylindrical or fusiform (Q > 2)

8. Cheilocystidia shape. 0 = absent or filamentous and

not strongly morphologically differentiated; 1 = sub-

clavate to clavate; 2 = very large and inflated

9. Pileus color when young and fresh. 0 = flesh color

to orange-brown; 1 = violaceous; 2 = red-brown; 3

= violet-brown; 4 = ochraceous; 5 = rust

10. Lamellar color when young and fresh. 0 = flesh col-

or; 1 = vinaceous; 2 = violet to purple; 3 = rose

pink

1 1 . Basal mycelium color when young and fresh. 0 =

white; 1 = violet

12. Pileus size. 0 = moderate; 1 = small; 2 = large

13. Stature. 0 = moderate; 1 = gracile; 2 = robust

14. Color of somatic culture mat on PDA and MMN.

0 = white to olive brown; 1 = violet

outgroup and ingroup relationships were exam-

ined using the five shared characters (fig. 3). Sec-

ond, resolution of ingroup relationships was at-

tempted using all available characters for the

ingroup without the outgroups. This resulted in

the unrooted network presented in Figure 4. Fi-

nally, to develop an operational classification,

analyses of the combined data set were run to

identify functional outgroups within Laccaria

(Watrous & Wheeler, 1981), thereby constraining

possible tree topologies (fig. 5).

DISCUSSION OF CHARACTERS AND CHARACTER

STATE ASSIGNMENTS— Table 4 lists the characters

and their states used in these analyses. Other char-

acters (e.g., presence or absence of striations, pi-

leus texture, growth rate of cultures on various

media, etc.) were employed in preliminary anal-

yses but were subsequently deleted for various rea-

sons, including a high degree of variability of such

characters within and among taxa or their autapo-

morphic nature (i.e., they varied only in one ter-

minal taxon and thus did not provide information

on relationships among taxa). Size character (nos.

6, 17, and 18) were coded only for ingroup taxa

because of the impossibility of estimating homol-

ogy with states in the outgroups. Color characters

(nos. 11, 12, 13, and 19) were limited to ingroup

taxa for the same reason. To my knowledge, the

identity and structure of the pigments in Laccaria

are unknown (see Discussion of Systematic Char-

acters). Thus, it is not possible to determine ho-

mology of pigments observed in Laccaria with

those found in other genera with orange-brown

and violet pigments. Lack of knowledge of the

pigments in Laccaria causes problems in ingroup

as well as outgroup analyses. I have made the as-

sumption that the violet coloration observed in

many Laccaria, from the lamellae and stipe basal

mycelium in L. bicolor to the entire basidioma in

L. amethystina, is due to the same pigment(s).

Information on number of sterigmata per ba-

sidium and number of nuclei per basidiospore

(characters 1 and 2, respectively; table 4) for out-

groups was obtained from a number of sources

including Corner (1966), Kiihner (1980, 1984),

Bigelow (1982), and Singer (1986).

PRELIMINARY HYPOTHESIS OF PHYLOGENETIC

RELATIONSHIPS BASED ON CLADISTIC ANALYSES—

Analyses undertaken for this study were per-

formed using PAUP Version 3.0L (Swofford, 1 989)

running on a MAC II ci. All multistate characters

were interpreted as unordered because I could not

make a priori decisions on character state trans-

formation series. The number of taxa included in

the analyses precluded the use of exact methods

to find the shortest trees, so a heuristic method

using branch swapping (tree bisection-reconnec-

tion) was employed to search for optimum trees.

The MULPARS option was invoked to save 300

equally most parsimonious trees. A shorter tree

was sometimes located even after 200 trees were

saved. Ten replications using random addition se-

quences were employed to ensure that addition

sequence did not affect tree length or topology.

Characters and their states employed in the final

sets of analyses are listed in Tables 4 and 5.

A strict consensus tree of the 300 most parsi-

monious trees saved in the analysis restricted to

the characters that could be coded for both in-

groups and outgroups is presented in Figure 3.

This tree has a length of 28 steps with a homoplasy

index (HI) of 0.643 and a rescaled consistency

index (RC) of 0.21 1. While ingroup relationships

were not resolved in this analysis, Laccaria formed

a monophyletic clade apart from the outgroup taxa

that was supported by one synapomorphy, basid-

iospore echinulae ultrastructure (character 3).

Only five characters could be used in this anal-

ysis (table 4, characters 1-3, 7, and 8) and of these

20

FIELDIANA: BOTANY

TABLE 5. Taxon by character state matrix used in cladistic analyses. Characters and character states are provided

in Table 4. Outgroups employed were Cantharellus and species of Singer's (1986) Tricholomataceae excluding Laccaria

(table 2).

only characters 3 (presence or absence of echin-

ulate basidiospores) and 8 (cheilocystidia shape)

were not homoplasious. Character 3 is the synap-

omorphy supporting the Laccaria clade; character

8 occurs in 3 states. Although most taxa lack or

have filamentous cheilocystidia (state 0), inflated

cheilocystidia can be found in two of the out-

groups. Laccaria amethysteo-occidentalis, L. ame-

thystina, and L. vinaceobrunnea have clavate

cheilocystidia.

The distribution of multinucleate basidiospores

(character 2) along this tree is significant because

Kiihner (1980, 1984) emphasized the occurrence

of multinucleate basidiospores in Laccaria in his

rationale for recognizing the genus as a family sep-

arate from other genera typically treated in the

Tricholomataceae (table 2). Although Laccaria is

characterized by having multinucleate basidio-

spores, this character state is also present in two

of the outgroup taxa (character 2, fig. 3). Until the

phylogeny of the outgroup (Singer's Tricholoma-

taceae excluding Laccaria) is elucidated, it is im-

possible to determine whether the presence of

multinucleate basidiospores is symplesiomorphic

or was derived independently in two or more clades

within the Tricholomataceae.

Figure 4 presents the results of the analysis of

ingroup relationships utilizing all of the characters

listed in Table 4 (minus characters 2 and 3 because

they were uninformative for ingroup compari-

sons). The strict consensus tree of the 300 most

parsimonious trees saved is presented as an un-

rooted network because no outgroup was used to

root the tree. The network (fig. 4) has a length of

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

21

FIG. 3. Strict consensus tree resulting from analyses restricted to characters shared by ingroup and outgroup taxa

(characters 1-3, 7, and 8 in table 4). Only characters 3 and 8 were not homoplasious. Length 28, HI = 0.643, RC =

0.2 1 1 . Refer to Table 5 for abbreviations.

51 steps, a consistency index (CI) of 0.549, and

an RC of 0.345. Only select characters were traced

onto the network illustrated in Figure 4. All char-

acters are mapped along the tree presented in Fig-

ure 5 (analysis of combined outgroup and ingroup

data).

All characters except echinulae length (character

4), cheilocystidia (character 8), pileus color (char-

acter 9), and color of lamellae (character 10) were

homoplasious. Because of this high level of ho-

moplasy, the network is not fully resolved and not

robust. The addition or deletion of a character or

a change in coding of the states of one character

had a profound impact on network topology.

Several subgroups within Laccaria were re-

solved during these analyses (fig. 4). Laccaria

mont

Iac3

ohi s,tri

tort

trie

bic

11 14

nob

och

9 10

H — h

Iac2

frat

FIG. 4. Unrooted network (strict consensus of 300 trees) of ingroup relationships. All characters except 2 and 3

(uninformative) listed in Table 4 were employed. Characters 4, 8, 9, and 10 were not homoplasious. Only select

characters were traced onto the network. Length 51, HI = 0.549, RC = 0.345. Refer to Table 5 for abbreviations.

22

FIELDIANA: BOTANY

FIG. 5. Strict consensus cladogram using all characters listed in Table 4 showing one possible resolution of where

to root the network presented in Figure 4. Only characters 4, 8, 9, and 10 were not homoplasious. Refer to Table 5

for abbreviations.

ohiensis, L. striatula, and L. tortilis formed a tri-

chotomy separate from the other North American

taxa that lack violet pigments (fig. 4). This clade

was supported by the presence of strongly echin-

ulate, globose basidiospores (characters 4, 5, and

7) and small gracile basidiomata (characters 12

and 1 3). Laccaria proxima and L. oblongospora

formed a clade supported by the presence of finely

echinulate basidiospores (state 2, character 4).

These two clades, along with the other taxa that

lack violet basidioma pigments, formed an unre-

solved "bush" separate from taxa with violet ba-

sidioma pigments. Resolution was higher within

the North American taxa with violet pigments.

This grade was supported by the presence of violet

mycelium at the stipe base and violet culture mats

on PDA and MMN media (characters 1 1 and 14).

Both of these states, however, occur also in L.

oblongospora, which was not placed in this grade.

The L. bicolor complex (i.e., L. trichodermophora,

L. nobilis, and L. bicolor) was fully resolved and

formed a sister group to the taxa with violet to

purple lamellae. Laccaria trullissata and L. mari-

tima formed a trichotomy with L. ochropurpurea

owing to their large basidioma size and stature

(characters 12 and 13) and similarity in coloration

(characters 9-1 1). The clade composed of L. ame-

thysteo-occidentalis, L. amethystina, and L. vi-

naceobrunnea was supported by the presence of

large cheilocystidia (character 8).

The distribution of violet basal mycelium and

violet somatic culture mats on PDA and MMN

media (state 1 of characters 11 and 14, respec-

tively) along this network causes difficulties in in-

terpreting character state changes throughout Lac-

caria. Based on the topology of the network, violet

pigments occur in two places along the tree: in L.

oblongospora and in the grade that includes L.

trichodermophora-L. vinaceobrunnea. It is im-

possible to determine which is the plesiomorphic

state for these two characters. The occurrence of

these states in two areas of the tree could be due

either to a parallel gain of pigment(s), a reversal

back to the plesiomorphic state, or the incorrect

placement of L. oblongospora. This is a serious

weakness in these results because, as discussed be-

low, the major subgroups identified through these

analyses are supported by pigment composition

and their distribution.

Based on these analyses, bisterigmate basidia

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

23

(state 1, character 1) arose independently three

times within the North American taxa ofLaccaria:

in L. fraterna, L. pumila, and L. tortilis.

Laccaria laccata was divided into three opera-

tional taxa in these analyses because of plasticity

of basidiospore shape within individuals referable

to L. laccata on the basis of other character states.

These analyses were uninformative for resolving

at what rank to recognize these morphological

forms of L. laccata.

The data sets (all characters for both ingroup

and outgroup taxa) were combined in an effort to

constrain the choice of a functional outgroup and

provide an operational classification based on a

tentative hypothesis of relationships among the

ingroup taxa. Because only five characters were

shared by the ingroup and outgroup, the results of

this analysis provide only one of the possible res-

olutions of where to root the network presented

in Figure 4. Figure 5 shows the results of this anal-

ysis. The resulting strict consensus tree of the 300

most parsimonious trees saved was 64 steps long

and had a CI of 0.500 and an RC of 0.332.

The unresolved group composed of the taxa

lacking violet basidioma pigments plus L. oblon-

gospora is basal on this tree (fig. 5). The only dif-

ference in ingroup topology between this tree and

the unrooted network (fig. 4) is that L. oblongo-

spora and L. proxima are not placed together in a

separate clade.

Proposed Operational Classification

of Laccaria

The classification used in this monograph is

based on an attempt to rigorously analyze all avail-

able data using cladistic methods. The employed

data set included data on macro- and micromor-

phology of basidiomata and somatic culture mats,

cytology, and basidiospore wall ultrastructure.

Two major subgroups within the North Amer-

ican taxa ofLaccaria were identified in these anal-

yses (figs. 4, 5). One subgroup consists of all taxa

lacking violet basidioma pigments plus L. oblon-

gospora; the second subgroup consists of the re-

maining taxa possessing violet basidioma pig-

ments. Although these two subgroups are clearly

separated on the cladograms, they are not sup-

ported by any synapomorphies. No characters,

plesiomorphic or apomorphic, support recogni-

tion of the taxa composing the basal group as a

monophyletic group separate from the rest of the

ingroup taxa. Additionally, although the grade

consisting of L. trichodermophora through L. vi-

naceobrunnea appears well supported by the pres-

ence of violet mycelium at the stipe base and by

violet culture mats on PDA and MMN media,

these character states also occur in L. oblongospora

and therefore are present in the other main sub-

group. Taxa need to be based on the occurrence

of unique sets of derived characters, and thus these

two subgroups should not be formally recognized.

The concept of metataxa has been proposed as

a means of recognizing unresolved groups (e.g.,

Donoghue, 1985; de Queiroz & Donoghue, 1988).

Because data do not exist to refute their mono-

phyly, the two subgroups are treated as metasec-

tions in this monograph, metasections Laccaria

and A methystina. Metasection A methystina is sup-

ported by two character state changes: the presence

of violet mycelium at the stipe base, and violet

somatic mats on PDA and MMN media. Meta-

sections were used in this treatment, even though

metataxa have been criticized by a number of au-

thors (e.g., Kluge, 1989; Nixon & Wheeler, 1990;

de Queiroz & Gauthier, 1 990), to provide an op-

erational classification and a testable hypothesis

of relationships within Laccaria.

Although taxa in metasection Amethystina are

almost fully resolved, only the clade consisting of

L. amethysteo-occidentalis, L. amethystina, and L.

vinaceobrunnea is supported by a synapomorphy:

the presence of large, clavate cheilocystidia (figs.

4, 5). For this reason, metasection Amethystina is

not further divided. Similarly, no subgroups are

recognized within metasection Laccaria.

This classification differs from previously pub-

lished classifications (table 3) by the recognition

of fewer subgeneric groups. The three classifica-

tions presented in Table 3 all recognized a separate

group, either section or stirps, for L. trullissata

and L. maritima. These two taxa formed a tri-

chotomy with L. ochropurpurea in the cladistic

analysis (figs. 4, 5) and could not be recognized as

a separate monophyletic group.

The results of these analyses are in conflict with

the hypothesis that the Laccaria species charac-

terized by bisterigmate basidia compose a mono-

phyletic group separate from tetrasterigmate taxa.

Bon's (1983) stirps Ohiensis and Ballero and Con-

tu's (1989) subsection Bisporae are paraphyletic

according to my analyses and therefore are not

recognized.

The tree topology shown in Figures 4 and 5 is

concordant with the results obtained to date on

relationships based on molecular data. Analyses

24

FIELDIANA: BOTANY

of RFLPs of mtDNA (Gardes et al., 199 la) in-

dicated that L. laccata var. pallidifolia was phe-

netically more similar to the L. bicolor complex

than L. proxima was to the L. bicolor complex.

The employed isolates of L. amethystina were phe-

netically distant, based on mtDNA RFLPs from

all of these taxa (Gardes et al., 199 la). Similarly,

Gardes and colleagues (Gardes et al., 1991b) re-

ported that sequence variation in the internal tran-

scribed spacer (ITS) of the nuclear ribosomal re-

peat unit was less between the one tested isolate

of L. laccata var. pallidifolia and the three tested

isolates of L. bicolor sensu lato than between L.

proxima and the L. bicolor complex. Although these

data do not resolve the issue of where to root the

network presented in Figure 4, they are concordant

with placing L. proxima, L. laccata, and taxa in

the L. bicolor complex in a linear series.

These conclusions are summarized below in the

Conspectus of North American Taxa.

Conspectus of North American Taxa

AGARICALES, TRICHOLOMATACEAE

Metasection Laccaria

Laccaria proxima

Laccaria oblongospora

Laccaria laccata var. laccata

Laccaria laccata var. pallidifolia

Laccaria longipes

Laccaria fraterna

Laccaria montana

Laccaria pumila

Laccaria striatula

Laccaria ohiensis

Laccaria tortilis

Metasection Amethystina

Laccaria trichodermophora

Laccaria bicolor

Laccaria nobilis

Laccaria trullissata

Laccaria maritima

Laccaria ochropurpurea

Laccaria amethysteo-occidentalis

Laccaria amethystina

Laccaria vinaceobrunnea

North American Taxa

Laccaria Berkeley & Broome, Ann. Mag. Nat. Hist.

12: 370. 1883.

= Russuliopsis Schroeter, Die Pilze Schlesiens: 622-

623. 1889.

Pileus convex to plane, glabrous, finely fibrillose

to fibrillose-scaly or scaly to squarrose, astriate to

plicate-striate or pellucid-striate, hygrophanous,

orange-brown, ochraceous, pinkish flesh color, dark

violaceous, vinaceous, rusty red-brown, gray-black,

or fawn; lamellae sinuate to subdecurrent, close to

distant, thick, waxy appearing, narrow to broad,

light flesh pink color, vinaceous, violaceous, rose

pink or ash gray; stipe equal to subclavate, gla-

brous to coarsely fibrillose, often longitudinally

striate; basal mycelium white or violet; basidio-

spores in mass white, rarely light violet; pileipellis

morphologically undifferentiated with interwoven

hyphae, or fasciculate, or a trichodermium; basid-

ia 2- or 4-sterigmate, clavate; pleurocystidia rare;

cheilocystidia absent to abundant, filamentous and

morphologically undifferentiated to clavate or

subcapitate; basidiospores globose to oblong and

echinulate or elongate and finely roughened, mul-

tinucleate; echinulae composed of microtubules

that run perpendicular to epispore; clamp con-

nections at nearly all septa; basidiospores and all

elements inamyloid, not dextrinoid, acyanophilic.

Terrestrial, cosmopolitan.

Key to Laccaria Occurring in North America North of Mexico

1 . Lamellae violaceous to purple when young and fresh 2

1 . Lamellae flesh color to pinkish when fresh 10

2. Basidiospores 1 3.5-22 x 5.5-9.5 fim, elongate, smooth to finely roughened or very finely echinulate

(echinulae < 0.5 nm long); in sand or very sandy soil; north central and eastern North America

3

2. Basidiospores < 10.5 nm long, less elongate (Q < 1.5), echinulae > 0.5 ^m long; in sand or not

in sand 4

3. Basidiospores subfusiform (Q = 2.4-2.5), not echinulate, appearing finely roughened on SEM; eastern

and midwestern North America . L. trullissata (p. 64)

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

25

3. Basidiospores oblong (Q = 1.7-1.8); finely echinulate (echinulae 0.2-0.5 /an long); Europe, only few

Canadian collections known L. maritima (p. 65)

4. Pileus and stipe bright violaceous or purple when young and fresh; cheilocystidia large (up to 92

x 1 2 Mm), clavate, abundant 5

4. Pileus and stipe orange-brown, pinkish flesh color, wine color, avellaneous, or buff color; chei-

locystidia smaller, filamentous, common to absent 7

5. Basidiospores globose, echinulae > 1 nm wide at base; basidiomata fading from amethyst to grayish

then buff in age; eastern North America L. amethystina (p. 71)

5. Basidiospores subglobose to broadly ellipsoid; echinulae < 1 nm wide at base; basidiomata changing

from amethyst to vinaceous or reddish brown; eastern or western North America 6

6. Basidiomata large (pilei 10-90 mm diam.), amethyst, becoming vinaceous; pileipellis hyphae

interwoven with scattered fascicles of perpendicular hyphae; western North America; under co-

nifers L. amethysteo-occidentalis (p. 69)

6. Basidiomata smaller (pilei 7-2 5 [—4 5] mm diam.); amethyst, becoming reddish brown; pileipellis

hyphae interwoven with numerous, large, individual perpendicular hyphae; Gulf Coast states;

under Quercus L. vinaceobrunnea (p. 72)

7. Lamellae dark purple, thick, waxy appearing; basidiomata large (pilei up to 60-120 mm diam.),

violaceous buff when young and fresh, becoming buff; basidiospores globose to subglobose, echinulae

1-1.5 Mm wide at base; eastern North America L. ochropurpurea (p. 67)

7. Lamellae light vinaceous, not thick or waxy appearing; basidiomata moderate to large (pilei up to

85 mm diam.), pinkish flesh color when fresh or vinaceous; basidiospores subglobose to broadly

ellipsoid or ellipsoid to oblong, echinulae < 1.2 fj.m long and < 1 Mm wide at base; eastern and

western North America 8

8. Basidiomata vinaceous to avellaneous; basidiospores ellipsoid to oblong (Q — 1.4-1.6); echinulae

< 0.5 Mm long; southern Mississippi and Texas L. oblongospora (p. 30)

8. Basidiomata pinkish flesh color to reddish brown; basidiospores subglobose to broadly ellipsoid,

Jc < 8.5 Mm long; widely distributed 9

9. Pileus 16-85 mm diam., often strongly scaly to squarrose; stipe large and robust (26-110[-160] x

4-10[-16] mm), strongly striate to reticulate; western North America and upper Great Lakes region,

not commonly encountered L. nobilis (p. 61)

9. Pileus 8-50(-70) mm diam., finely fibrillose to minutely scaly; stipe smaller (23-85[-130] x 3-6

[-10] mm) and not strongly striate; western North America and upper Great Lakes region, commonly

encountered L. bicolor (p. 57)

10. Basidia (3-)4-sterigmate 11

10. Basidia 2(-3)-sterigmate 22

1 1. Basidiospore echinulae < 1 Mm long; basidiospores broadly ellipsoid to oblong (Q = 1.25-1.6) . .

12

1 1 . Basidiospore echinulae > 1 nm long; basidiospores globose to ellipsoid 13

12. Basidiospores x = 8.3-9.0 x 5.6-6 jtan, oblong (Q = 1.45-1.6); mycelium at stipe base violet,

fading white; Gulf Coast states L. oblongospora (p. 30)

12. Basidiospores x = 9-1 1.5 x 6.7-8(-8.8) /mi, ellipsoid (Q = 1.25-1.35[-1.4]); mycelium at stipe

base white; widely distributed L. proximo, (p. 27)

13. Mycelium at stipe base violaceous when fresh, becoming white with age; basidiospores small (x =

7-8.4[-9] x 6-8 Mm) 14

13. Mycelium at stipe base white from onset; basidiospores larger (Jc = 8.2-13 Mm long) (but see no.

20, L. longipes) 16

14. Lamellae flesh-colored to pinkish flesh color; basal mycelium scant, strongly hygrophanous;

basidiomata orange-brown; pileipellis a trichodermium or of interwoven hyphae with numerous

large fascicles of perpendicular hyphae; southeastern North America

L. trichodermophora (p. 55)

14. Lamellae light vinaceous, occasionally fading to pinkish color; basal mycelium copious, basid-

iomata pinkish flesh color to reddish brown; pileipellis hyphae interwoven with scattered fas-

cicles of perpendicular hyphae; western North America to Ontario and Michigan 15

15. Pileus 16-85 mm diam., strongly scaly to squarrose; stipe large and robust (26-1 10[-160] x 4-10

FIELDIANA: BOTANY

[-16] mm), strongly striate to reticulate; western North America and upper Great Lakes region, not

commonly encountered L. nobilis (p. 61)

15. Pileus 8-50(-70) mm diam., finely fibrillose to minutely scaly; stipe smaller (23-85[-130] x 3-6

[-10] mm) and not strongly striate; western North America and upper Great Lakes region, commonly

encountered L. bicolor (p. 57)

16. Basidiospores relatively large (x = 9.4-12.6 x 8.5-10.5 pm); pilei up to 35 mm broad, striate

to (often) strongly striate; restricted to arctic, boreal, or alpine habitats . . L. montana (p. 42)

16. Basidiospores smaller; pilei small to large, not striate or occasionally finely striate, some trans-

lucent-striate 17

17. Pileus 16-85 mm diam., strongly scaly to squarrose; stipe large and robust (26-1 10[-160] x 4-10

[-16] mm), strongly striate to reticulate L. nobilis (p. 61)

17. Pileus smaller (5-45[-60] mm diam.), glabrous to finely scaly; stipe smaller, not strongly striate

18

18. Basidiospores globose; echinulae > 1.5 nm long, > 1.2 nm wide at base 19

18. Basidiospores globose to ellipsoid; echinulae 0.7-2 ^m long, < 1 nm wide at base 20

19. Stipe 20-70(-103) x 1-4 mm, darker than pileus; in moist areas, often among mosses (not Sphag-

num); eastern North America, commonly encountered L. striatula (p. 46)

19. Stipe 12-25(-40) x 1-2 mm, concolorous with pileus; cosmopolitan, not commonly encountered

in north temperate regions L. ohiensis (p. 48)

20. Basidiospores small (x = 7.6-7.8 x 6.8-7.2 /urn); pilei strongly translucent-striate; stipes long

(67-1 38[-l 65] mm); growing among mosses, especially Sphagnum, usually in bogs, northeastern

North America and upper Great Lakes region L. longipes (p. 38)

20. Basidiospores larger (Jc > 8 nm long); pileus not striate, striate or slightly translucent-striate;

stipe shorter; growing among mosses or not, not normally found in bogs; widely distributed

21

21. Basidiospores broadly ellipsoid to ellipsoid (Q = 1.2-1.3); rarely encountered

L. laccata var. laccata (p. 34)

21. Basidiospores globose to broadly ellipsoid (Q = l-1.5[-2]); commonly encountered, widely distrib-

uted L. laccata var. pallidifolia (p. 35)

22. Basidiospores usually < 1 1 nm long; basidiomata rusty red-brown; under Eucalyptus

L. fraterna (p. 39)

22. Basidiospores > 1 1 /xm long; under native North American trees 23

23. Basidiospores 1 1-17 x 10-14.5 /*m, subglobose to broadly ellipsoid (Q = 1.1-1.2); echinulae < 1.5

/im long; montane, boreal, or arctic habitats L. pumila (p. 44)

23. Basidiospores 10-15 x 10-15 /urn, globose; echinulae > 2 pm long; temperate habitats

L. tortilis (p. 50)

I .act-aria Metasection Laccaria

[see p. 24 for discussion]

Basidiomata and somatic culture mats lacking

violet pigment(s), or violet pigment(s) present and

basidiospores ellipsoid and finely ornamented

(echinulae 0.5-1 pm long).

Laccaria proxima (Boudier) Patouillard. Figures

6-8, 53a,b, 69c.

= Clitocybe proxima Boudier, Bull. Soc. Bot. France

28: 91. 1881. TYPE: Plate II, fig. 2 in Boudier,

Bull. Soc. Bot. France 28. 1881 (lectotype, fide

Mueller, 199 la). Representative specimen: France,

Montemorency, November 1904, Boudier s.n. (as

C. proxima) (PC!, "neotype" /wfe Mueller, 1987).

= Laccaria proxima (Boudier) Patouillard, Hymeno.

Eur.: 97. 1887.

= Laccaria laccata var. proxima (Boudier) Maire, Bull.

Soc. Mycol. France 24: 16. 1908.

s Clitocybe laccata var. proxima (Boudier) Bresadola.

Icon. Mycologica: 43. 1927.

MACROMORPHOLOGY— Pileus (7-)l 5-69(-83)

mm broad, campanulate to convex, often becom-

ing plane to uplifted, some depressed, not striate,

occasionally translucent-striate when faded, finely

fibrillose to fibrillose, some becoming fibrillose-

scaly to scaly or squarrose in age, hygrophanous,

reddish brown to orange-brown ("Auburn," "San-

ford's Brown," "Orange Rufous," "Hazel," "Cin-

namon-Rufous"), fading lighter ("Apricot Buff');

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

27

FIG. 6. Basidiomata of L. proxima (GMM 2100).

FIG. 7. Somatic culture mats of L. proxima (GMM 1518). Top on PDA, left on MMN, and right

on MEA. Photo taken during week 4.

28

FIELDIANA: BOTANY

FIG. 8. Micromorphological features of L. proximo (GMM 2100): a, basidiospores; b, basidia. Scale line = 10

margin incurved to decurved, sometimes becom-

ing plane, entire to undulate, occasionally becom-

ing eroded with age; context thin, tapering quickly

to margin, pinkish flesh color ("Japan Rose" to

"Shell Pink"). Lamellae sinuate to adnate, occa-

sionally arcuate, subdistant to distant, up to 10

mm broad, pinkish flesh color ("Flesh Color,"

"Pale Salmon Color"). Stipe (12-)24-72(-155) x

3-1 1 mm, equal to subclavate, often slightly bul-

bous, dry, fibrillose, often longitudinally striate,

striations moderate to pronounced, most of stipe

concolorous with pileus; base occasionally darker

("Rood's Brown"), striations concolorous with pi-

leus or darker red ("Hay's Russet," "Pecan

Brown,"or "Onion-skin Pink"). Basal mycelium

white. Basidiospores white in mass.

MiCROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered to numerous large fascicles

of ± perpendicular hyphae; fascicles composed of

1 5-30 or more hyphae; terminal cells of fascicular

hyphae 27.5-92 x 4.5-1 6(-30) nm, filamentous,

subclavate, clavate, broadly clavate, capitate or

ventricose-rostrate; walls up to 0.5 nm thick, light

to moderate yellowish brown; contents hyaline to

light yellowish brown. Pileus trama tightly inter-

woven, morphologically undifferentiated, hyaline,

light yellowish brown toward pileipellis. Lamellar

trama parallel; hyphae mostly 3-1 9 pm diam., thin-

walled, hyaline to light yellowish brown; cells fil-

amentous to barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (23-)33-62

x 8-15 Mm, clavate, hyaline; sterigmata 4, up to

7 urn long. Cheilocystidia 19-66.5(-92) x 2-8.5

(-16.5) MHI, filamentous to subclavate, occasion-

ally subcapitate, often abundant, thin-walled hy-

aline. Basidiospores (excluding ornamentation)

[265/20] 8-1 1(-1 2.5) x (6.5-)7-8.7(-9.2)Mm(Jc =

[8.7-]9-11.5 x 6.7-8[-8.8] /im), Q = (1.07-) 1.1 6-

1.49(-1.58) «2 = 1.24-1.34[-1.43]), broadly ellip-

soid, ellipsoid or occasionally oblong, hyaline,

echinulate; echinulae 0.5-1 nm long, occasionally

with 1 or 2 long echinulae (up to 2 nm long) at

apex, crowded; hilar appendix 1.3-2 ^m long,

prominent, truncate, plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 2.5-1 7.5 ^m diam., tightly interwoven, hy-

aline; cells filamentous to barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 4;

Appendix B)— PDA: Radius at week 3 = 3-17

mm, week 6 = 26-43 mm; mat felty, thick, tightly

interwoven, not translucent, most of uniform

thickness or with slightly thicker area near plug,

in one (GMM 1525) forming concentric thicker-

thinner bands, white to light tan; margin 1-2 mm

broad, abruptly thinner or not well differentiated,

silky to subfelty, thin, uneven, white; plug white

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

29

or becoming olive; hyphae morphologically un-

differentiated. MMN: Radius at week 3 = (6-) 1 6-

32 mm, week 6 = (18-)43-64 mm; mat subfelty

to felty, relatively thin to moderately thick, inter-

woven, translucent to not translucent, thicker near

plug, uniform or thinner towards margin, white;

margin abruptly thinner or not well differentiated,

silky to subfelty, white; plug white; hyphae mor-

phologically undifferentiated. MEA: Radius at

week 3 = 1 1-26 mm, week 6 = 30-51 mm; mat

subfelty to felty, thin to relatively thick, translu-

cent, white; margin not well differentiated, some-

what thinner, white; plug white; hyphae morpho-

logically undifferentiated, occasionally irregularly

swollen.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious; terrestrial, associated most commonly with

Pinaceae, occasionally among mosses including

Sphagnum; disturbed areas, early succession for-

ests or under young planted pines in reforested

areas. Cosmopolitan; common. Found throughout

North America. A list of specimens examined is

presented in Appendix A.

OBSERVATIONS— Laccaria proximo, can be dis-

tinguished from L. laccata by its more robust, more

strongly colored basidiomata, nonstriate and

slightly scaly to scaly pilei, and more elongate,

finely echinulate basidiospores. Laccaria proxima

is separated from L. montana in having smaller,

more finely echinulate basidiospores and the more

robust habit of its basidiomata. Collections of L.

proxima can be differentiated from those of L.

oblongospora by having less elongate, larger ba-

sidiospores, white basal mycelium, and culture

mats that are white on MMN, PDA, and N6:5

media. A discussion of various interpretations of

the name L. proxima is presented in the section

on type specimens.

Mueller (1982, 1984, 1985) reported that cul-

tures of some L. proxima were violet to purple on

PDA and MMN media. On further analysis of the

collections from which these violet culture mats

were derived, it was determined that these speci-

mens were L. bicolor and not L. proxima. The

basidiospores observed from these collections were

much smaller and had longer echinulae than those

from other collections referable to L. proxima. The

basidiospore dimensions and cultural character-

istics fit my circumscription of L. bicolor.

Intra- and interspecific pairing studies have sup-

ported treatment of L. proxima as a discrete spe-

cies. No isolate of L. proxima has been found to

mate with any other putative taxa, and no intra-

specific intersterility groups have been detected

(Fries & Mueller, 1984; Mueller, unpubl. data).

Further support for recognizing L. proxima as an

autonomous species was obtained during analyses

of mtDNA and rDNA RFLPs of select species of

Laccaria (Gardes et al., 1990, 199 la). A low level

of intraspecific heterogeneity in mtDNA and rDNA

RFLPs was detected among three isolates of L.

proxima used in these analyses, whereas their

RFLPs were distinct from RFLPs of the other test-

ed taxa.

Laccaria proxima has been reported from

throughout North America. It has also commonly

been collected in Europe (Clemen?on, 1984; Con-

tu, 1986; Mueller, 1 99 1 a). Watling( 1987) reported

that L. proximella Singer is the alpine equivalent

of L. proxima. As discussed previously (Mueller,

199 la), I cannot support this contention based on

the large number of collections referable to L.

proxima that I have examined from alpine and

boreal habitats in Europe and North America. My

interpretation of L. proximella is that it differs

from L. proxima by having violet strains (or my-

celium?) at the stipe base and grows in very poor,

rocky soil. I have collected material referable to

L. proximella in southern Argentina and Chile.

Laccaria oblongospora G. M. Mueller. Figures 9-

11, 53c,d, 67d.

Laccaria oblongospora G. M. Mueller, Mycotaxon 20:

108-112. 1984. TYPE: USA, Mississippi, Har-

rison Co.; DeSoto National Forest, Harrison Ex-

perimental Forest, Road H-8, 7 December 1 980,

G. M. Mueller 1102 (TENN 42522) (TENN!, holo-

type).

MACROMORPHOLOGY— Pileus (5-) 12-59 mm

broad, obtuse to convex, becoming plane to up-

lifted, often depressed, not striate, finely fibrillose,

becoming fibrillose-scaly, hygrophanous, brown-

ish orange ("Vinaceous-Rufous," "Kaiser Brown,"

"Apricot Buff," "Burnt Sienna," or "Sanford's

Brown"), occasionally vinaceous color ("Vina-

ceous-Brown," "Vinaceous-Russet" or "Japan

Rose"); disc often darker, red-brown to dark or-

ange-brown or occasionally vinaceous ("Dark Liv-

id Brown," "Deep Brownish Vinaceous," "Hay's

Russet," "Chocolate," "Vinaceous-Russet," or

"Mahogany Red"); margin incurved to decurved,

becoming plane to uplifted, entire to undulate, oc-

casionally becoming eroded; context 1-2 mm thick,

tapering quickly to margin, flesh color ("Pale Vi-

naceous-Pink"). Lamellae sinuate to adnate, oc-

30

FIELDIANA: BOTANY

casionally arcuate, subdistant to distant, broad,

thick, pinkish flesh color (" Vinaceous-Pink," "Buff-

Pink," "Light Congo Pink," or "Shell Pink"), oc-

casionally vinaceous or violaceous ("Light Brown-

ish Vinaceous," "Pale Brownish Vinaceous," or

"Light Pinkish Lilac"). Stipe (1 1-)20-60(-65) x

2-12 mm, equal to subclavate, often slightly bul-

bous, dry, fibrillose, occasionally finely longitu-

dinal-striate, concolorous with pileus; striations

occasionally darker ("Pecan Brown"). Basal my-

celium violet, soon fading to white. Basidiospores

white in mass.

MICROMORPHOLOGY— Pileipellis of loosely in-

terwoven hyphae with scattered large fascicles of

± perpendicular hyphae; fascicles composed of

(5-) 10-30 or more hyphae; terminal cells 32.5-7 1

x 7-24.5 Mm, filamentous, subclavate, clavate,

broadly clavate or capitate; walls up to 0.5 nm

thick, light vinaceous; contents hyaline to light

yellowish brown or light vinaceous. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline, yellowish brown to light vinaceous

toward pileipellis. Lamellar trama parallel; hy-

phae 3-10 Mm diam., thin- walled, hyaline to light

yellowish brown; cells barrel-shaped. Subhymeni-

um morphologically undifferentiated. Basidia 24-

35 x 6.5-10 Mm, clavate, hyaline; sterigmata 4,

up to 5.5 Mm long. Cheilocystidia 31.5-53 x 3-7

Mm, filamentous to subclavate, scattered, thin-

walled, hyaline, found only in some collections.

Basidiospores (excluding ornamentation) [75/5]

7.4-10 x 5-7 Mm (x = 8.3-9.1 x 5.6-5.9 Mm), Q

= 1.3-1.76 (Q = 1.45-1.60), ellipsoid to oblong,

occasionally subreniform, hyaline, echinulate;

echinulae < 0.5(-1.4) Mm long, those > 0.5 Mm

long restricted to basidiospore apex, crowded; hi-

lar appendix 1.3-2 Mm long, prominent, truncate;

plage present; contents occasionally uniguttulate.

Basal mycelium hyphae mostly 3-1 1 Mm diam.,

tightly interwoven, hyaline; cells filamentous to

barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 5;

Appendix B)— PDA: Radius at week 3 = 28-39

mm, week 6 = 45-78 mm; mat felty, thick, tightly

interwoven, with scattered small sectors of longer,

loosely interwoven hyphae, tightly appressed to

agar surface, in time forming pruinose aerial layer

away from plug, not translucent, at first dark vio-

let, soon fading, week 3 = light to moderate violet

coloration restricted either to 2-3 mm band near

margin or 4-5 mm zone near plug, most of mat

light orange-brown, week 6 all light orange-brown,

no violet coloration present; margin up to 5 mm

broad, silky to subfelty, thin, uneven, light violet,

becoming white; plug concolorous with mat; hy-

phae mostly morphologically undifferentiated, oc-

casionally irregularly swollen, subcoralloid or cor-

alloid. MMN: Radius at week 3 = most 48-56

mm, one isolate 30-36 mm, week 6 = most cov-

ering agar surface, one isolate 58-78 mm, mat

subfelty to subwoolly, thin, becoming thicker,

loosely interwoven, some with subwoolly to wool-

ly or cottony narrow strands radiating out from

the plug to margin, between strands thin, tightly

appressed to agar surface, translucent, becoming

somewhat translucent, at first light violet, soon

fading to light violet or white, margin not well

differentiated, thin, uneven, concolorous; plug

concolorous; hyphae most morphologically un-

differentiated, occasionally irregularly swollen,

subcoralloid or coralloid. MEA: Radius at week

3 = 26—40 mm, week 6 = 5 1-78 mm; mat subfelty,

thin, loosely interwoven, some with 1-3 narrow,

slightly thicker concentric bands, tightly appressed

to agar surface, translucent, white; margin 1-2 mm

broad, not well differentiated, even to uneven,

white; plug white; hyphae morphologically undif-

ferentiated, occasionally irregularly swollen or

subcoralloid.

HABITAT AND DISTRIBUTION— Gregarious; in

very sandy soil under Pinus palustris Miller; Gulf

Coast. A list of specimens examined is presented

in Appendix A.

OBSERVATIONS— Laccaria oblongospora often

appears similar to L. proximo, or L. trichoder-

mophora in the field. It differs from L. proximo

in basidiospore shape and size, basal mycelium

color, and cultural features. It can be distinguished

from L. trichodermophora primarily on basidio-

spore shape and echinulae length.

Much variation in basidioma color was ob-

served in this taxon. Most specimens exhibited

the typical orange-brown coloration of L. laccata

sensu lato. Scattered among these were a few in-

dividual fruitbodies which were vinaceous to vi-

olaceous in color (e.g., TENN 42524). Initially, these

vinaceous collections were thought to represent a

separate taxon. However, because of the occur-

rence of intermediate color forms (orange-brown

pilei and stipes with violaceous lamellae) and iden-

tical culture mat morphologies, they have been

treated as contaxic.

Intercollection pairing studies support the treat-

ment of L. oblongospora as a separate species. Iso-

lates from the two stocks obtained during this study

were intercompatible with each other but inter-

sterile with all tested isolates of other species, in-

cluding isolates of L. proximo. Material of L. ob-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

31

FIG. 9. Basidiomata of L. oblongospora (GMM 2310).

FIG. 10. Somatic culture mats of L. oblongospora (GMM 1 105). Top on PDA, left on MMN, and

right on MEA. Photo taken during week 4.

32

FIELDIANA: BOTANY

FIG. 1 1. Micromorphological features of L. oblongospora (GMM 2310): a, basidiospores; b, basidia. Scale line

10 Mm.

longospora was not included in the analyses of

mtDNA or rDNA RFLPs.

Laccaria oblongospora was consistently placed

in Laccaria metasection Laccaria during cladistic

analyses. Phylogenetic relationships between the

taxa in this metasection, however, were not re-

solved during these analyses. If this is the correct

placement of L. oblongospora, the pigment(s) re-

sponsible for the violet mycelium at stipe bases

and culture mats would be plesiomorphic and

would not be informative for resolving relation-

ships within the genus (see Phylogenetic Consid-

erations for further discussion).

Only a few populations of this species have been

located. All of them were either in eastern Texas

or southern Mississippi. Several of these popula-

tions were very large and consisted of numerous

basidiomata. Specimens of L. oblongospora have

only been encountered near stands of Pinuspalus-

tris.

Laccaria laccata (Scopoli: Fries) Cooke.2

= Agaricus laccatus Scopoli, Flora Carniolica 2: 444.

1772. TYPE: Sweden, Femsjo, 17 August 1964,

Singer 4083 (BAFC!; neotype^/e Singer, 1967).

2 Berkeley and Broome (1883) did not make any new

combinations when proposing the genus Laccaria. Con-

sequently, they did not validly publish L. laccata (Greu-

teretal., 1988, Art. 33.1).

= Agaricus laccatus Scopoli: Fries, Systema Myco-

logica 1: 106. 1821.

= Clitocybe laccata (Scopoli: Fries) Kummer, Fiihrer

in die Pilzkunde: 122. 1871.

= Camarophyllus laccatus (Scopoli: Fries) P. Karst.,

Ryssl., Finl. Skand. Halfons Hattsvamp.: 231.

1879.

= Laccaria laccata (Scopoli: Fries) Cooke, Grevillea

12: 70. 1884.

= Omphalia laccata (Scopoli: Fries) Quelet, Enchirid-

ion Fungorum: 2C. 1886.

= Collybia laccata (Scopoli: Fries) Quelet, Flore My-

cologique: 237. 1888.

= Russuliopsis laccata (Scopoli: Fries) Schroeter in

Cohn, Krypt.-Fl. Schlesien 3: 622. 1889.

= Agaricus carneus Schaeffer, Fungorum Bavaria 4:71,

fig. 304. 1774. TYPE: Lacking.

= Agaricus farinaceus Hudson, Flora Anglica: 616. 1778.

TYPE: Lacking.

= Omphalia farinacea (Hudson) S. F. Gray, Nat. Arr.

Brit. PI. 1: 612. 1821.

= Laccaria farinacea (Hudson) Singer in Singer &

Moser, Mycopathol. Mycol. Appl. 26: 149. 1965.

[not validly published, basionym lacking].

= Laccaria farinacea (Hudson) Singer, Sydowia Beih.

7: 8. 1973.

= Agaricus rosellus Batch, Elench. fung. Continuatio pri-

ma: 121, fig. 99. 1786; non Agaricus rosellus Fries:

Fries, Systema Mycologica 1 : 151. 1 82 1 . [= Mycena

rosella].

= Omphalia rosella S. F. Gray, Nat. Arr. Brit. PI. 1:

613. 1821.

= Russuliopsis laccata var. rosellus (S. F. Gray)

Schroeter in Cohn, Krypt.-Fl. Schlesien 3: 623.

1889.

= Laccaria laccata var. rosella (S. F. Gray) Singer,

Ann. Mycol. 41: 17. 1943.

= Agaricus subcarneus Batch, Elench. fung. Continuatio

prima.: 121, fig. 100. 1786.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

33

= Agaricus (Clitocybe) glaucipes Berkeley & Curtis, Ann.

Mag. Nat. Hist., III. 4: 284. 1859.

Excluded— Laccaria farinacea (Hudson) Singer, Sy-

dowia Beih. 7: 8. 1973. [= L. trichodermophora G. M.

Mueller].

As discussed in Mueller and Vellinga (1986),

Singer's typification of L. laccata (Singer, 1967)

has perpetuated confusion in the delimitation of

L. laccata. The specimen that he chose is not rep-

resentative of the species because the micromor-

phological characters of the collection are near the

extreme range for the taxon. To date, very few

collections referable to L. laccata have been en-

countered that have basidiospores as elongated as

the neotype (Mueller & Vellinga, 1986; Mueller,

199 la).

Singer (1946, 1967, 1973, 1977), Bon (1983),

and others have proposed a number of species and

subspecific taxa in an attempt to delimit natural

taxa within this highly variable group. Descrip-

tions of the type specimens of most of these names

are presented later in this monograph (see Type

Studies). Type specimens of the majority of these

names have basidiospores that are globose to

subglobose in shape. Only collections from the

type variety and three other varieties were found

to have ellipsoid basidiospores (Q = 1.25-1.3) (see

Type Studies and Mueller & Vellinga, 1986). For

these reasons, Mueller and Vellinga (1986) and

Mueller (199 la) treated most of the proposed va-

rieties of L. laccata, L. tetraspora, and L. affinis

(Singer) Bon as synonyms of one of three varieties:

L. laccata var. laccata, L. laccata var. moelleri,

and L. laccata var. pallidifolia.

Additional morphometric and intercollection

pairing studies were undertaken, and these data

were compared with information on mtDNA and

rDNA RFLPs (Gardes et al., 1990, 199 la) in an

attempt to resolve systematic problems surround-

ing L. laccata sensu lato (Mueller, 1991c). Based

on a synthesis of these data, I recognize the fol-

lowing taxa in this complex: L. laccata var. lac-

cata, L. laccata var. moelleri, L. laccata var. pal-

lidifolia, L. longipes, L. ohiensis (= L. tetraspora),

and L. striatula. All of these except L. laccata var.

moelleri occur in North America and will be treat-

ed in detail below. Laccaria laccata var. moelleri

is discussed with L. longipes below.

Laccaria laccata var. laccata. Figure 64d.

= Agaricus (Clitocybe) laccatus var. lutea Fries, Epicr.

syst. mycol.: 79. 1836-1838.

= Agaricus (Clitocybe) laccatus var. [pileo] luteoviolaceo

Fries, Epicr. syst. mycol.: 79. 1836-1838.

= Agaricus (Clitocybe) laccatus var. [obscure] violacea

Fries, Epicr. syst. mycol.: 79. 1836-1838.

= Agaricus (Clitocybe) laccatus var. rufocarnea Fries,

Epicr. syst. mycol.: 79. 1836-1838.

= Laccaria laccata var. carbonicola Singer, Bull. Soc.

Mycol. France 83: 110. 1967.

= Laccaria laccata var. gibba Singer, Beih. Nova Hed-

wigia 29: 27. 1969.

= Laccaria laccata var. vulcanica Singer ex Veselsky &

Singer, PI. Syst. Evol. 126: 362. 1977.

= Russuliopsis laccata var. rosellus f. pusilla Schroeter

in Cohn, Krypt.-Fl. Schlesien: 623. 1889.

MACROMORPHOLOGY (Teste Singer, 1967)— Pi-

leus (6-) 10— 45 mm broad, convex becoming plane,

often slightly depressed, occasionally umbonate,

slightly striate, glabrous to finely fibrillose, occa-

sionally becoming fibrillose-scaly, hygrophanous,

reddish brown becoming pale ochre when dry. La-

mellae adnate to adnate-subdecurrent, distant,

broad, rather pale and dull reddish color. Stipe

40-60(-90) x 2-7(-14) mm, equal to slightly cla-

vate, fibrous with innate fibrils, concolorous with

pileus or concolorous with lamellae at apex and

brown toward base. Basal mycelium white. Basid-

iospores white in mass.

MICROMORPHOLOGY (Mihi)— PileipelHs of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 1 5-30

hyphae; terminal cells of fascicular hyphae 38-80

x 6.5-18 um, filamentous, slightly swollen, sub-

clavate or capitate, light yellowish brown in mass;

walls up to 0.5 um thick, light yellowish brown;

contents hyaline. Pileus trama tightly interwoven,

morphologically undifferentiated, hyaline, light

yellowish brown toward pileipellis. Lamellar tra-

ma parallel, hyphae 2.5-12 /an diam., thin-walled,

hyaline; cells barrel-shaped. Subhymenium undif-

ferentiated. Basidia 27.5-48 x 7-16.5 /an, cla-

vate, hyaline; sterigmata 4, up to 1 2 /an long. Pleu-

rocystidia lacking. Cheilocystidia 25-70 x 2-7.5

/an, filamentous, absent to common, hyaline. Ba-

sidiospores (excluding ornamentation) [2 1 0/7] (7-)

7.7-9.7(-ll) x (5-)6.4-8(-8.5) um (Jc = 7.8-9.2

x 6.3-7.1 /im), <2 = (1.08-)1.18-1.35(-1.46)«2 =

1.2-1.3), subglobose to ellipsoid, hyaline, echin-

ulate; echinulae l-1.8(-2.3)/mi long, < 1 /an wide

at base; hilar appendix up to 1.8 um long, prom-

inent, truncate; plage present; contents occasion-

ally uniguttulate.

HABITAT AND DISTRIBUTION— Solitary to gre-

garious; terrestrial, host unknown. Reported from

only a few localities in Europe and North America;

not abundant. Not commonly collected. A list of

collections examined is provided in Appendix A.

34

FIELDIANA: BOTANY

OBSERVATIONS— The type variety is distin-

guished from other varieties of L. laccata by hav-

ing broadly ellipsoid to ellipsoid, moderately or-

namented basidiospores. It is sometimes difficult

to differentiate L. laccata var. laccata from L.

proximo without information on macromorphol-

ogy. Major differences between them are the more

robust, darker colored, scaly basidiomata of L.

proxima, and the more coarsely ornamented ba-

sidiospores of L. laccata var. laccata.

The description presented above was based on

a compilation of the protologues of the type col-

lections for the names treated as synonyms of L.

laccata var. laccata plus several collections refer-

able to this taxon found in Swedish herbaria. I

have not collected specimens referable to this tax-

on.

No isolates of specimens referable to L. laccata

var. laccata have been included in the intra- and

interspecific pairing studies (Fries & Mueller, 1 984;

Mueller, 1991c) or in the analyses of mtDNA and

rDNA RFLPs (Gardes et al., 1990, 199 la), be-

cause I have not obtained cultures of this taxon.

Data on the results of pairing studies using other

recognized varieties are discussed below.

Based on available herbarium specimens, L.

laccata var. laccata is not common, as few col-

lections were encountered among the borrowed

material. In Sweden this taxon appears to have a

very restricted distribution. Five of the six Swed-

ish collections examined came from Femsjo and

may be from the same population or even the same

individual mycelium (Mueller, 199 la). This is the

same general locality from where Singer (1967)

obtained the type specimen.

Laccaria laccata var. pallidifolia (Peck) Peck. Fig-

ures 12-14, 54d-f, 68c.

= Clilocybe laccata var. pallidifolia Peck, Annual Rep.

New York State Bot. 43: 274. 1890. TYPE: USA,

New York, Selkirk, October, C. H. Pecks.n. (NYS!,

holotype).

= Laccaria laccata var. pallidifolia (Peck) Peck, An-

nual Rep. New York State Bot. 157: 92. 1912.

= Laccaria laccata var. decurrens Peck, Annual Rep.

New York State Bot. 157: 92. 1912.

= Laccaria laccata f. minuta Imai, J. Fac. Sci. Hokkaido

Imp. Univ., Ser. 5, Bot. 18: 90. 1938.

= Laccaria laccata var. minuta (Imai) Hongo, Mem.

Shig. Univ. 9: 58. 1959.

= Laccaria laccata var. anglica Singer, Bull. Soc. Mycol.

France 83: 110-111. 1967.

= Laccaria anglica (Singer) Bon, Doc. Mycol. 1 1: 22.

1981 [not validly published, basionym lacking].

s Laccaria affinis var. anglica (Singer) Bon, Doc. My-

col. 13: 50. 1983.

= Laccaria laccata var. affinis Singer, Bull. Soc. Mycol.

France 83: 111. 1967.

= Laccaria affinis (Singer) Bon, Doc. Mycol. 13: 49.

1983.

= Laccaria laccata var. chilensis Singer, Bull. Soc. My-

col. France 83: 109. 1967.

= Laccaria laccata var. subalpina Singer, PI. Syst. Evol.

126: 365. 1977.

= Laccaria tetraspora var. peladae Singer, Bull. Soc.

Mycol. France 83: 117. 1967.

= Laccaria laccata var. peladae (Singer) Singer, PL

Syst. Evol. 126: 366. 1977.

= Laccaria laccata var. tatrensis Singer, PL Syst. Evol.

126: 367. 1977.

= Laccaria laccata var. intermedia Singer, PL Syst. Evol.

126: 368. 1977.

MACROMORPHOLOGY— Pileus 10-45(-60) mm

broad, obtuse to convex, often becoming plane to

uplifted, often depressed, striate to not striate, oc-

casionally strongly striate to plicate-striate, some-

times translucent-striate when fresh, finely fibril-

lose to fibrillose-scaly, infrequently slightly scaly,

hygrophanous, orange-brown when fresh, becom-

ing buff color ("Sanford's Brown," "Orange Ru-

fous," "Hazel," "Cinnamon-Rufous," "Pinkish

Cinnamon," or "Light Vinaceous-Cinnamon"),

fading lighter ("Apricot Buff," "Salmon Color,"

"Light Pinkish Cinnamon," or "Pinkish Buff"),

finally to buff ("Pale Ochraceous Buff); disc oc-

casionally darker orange-brown or red-brown

("Hay's Russet," "Ochraceous Tawny" or "Buck-

thorn Brown"); margin incurved to decurved, be-

coming plane to uplifted, entire to undulate, oc-

casionally becoming eroded in age; context thin,

tapering quickly to margin, concolorous. Lamellae

sinuate, adnate or arcuate, rarely decurrent, close

to distant, narrow to broad, relatively thin to thick,

pinkish flesh color ("Flesh Color," "Salmon-Buff,"

"Pale Salmon Color," "Flesh-Pink," or "Light Vi-

naceous-Cinnamon"), some becoming slightly vi-

naceous with age (near "Light Grayish-Vina-

ceous"). Stipe (12-)20-65(-106) x 2^(-8) mm,

equal, subclavate or tapering toward base, occa-

sionally slightly bulbous, dry, fibrillose, not striate

to finely longitudinally striate, rarely with pro-

nounced striations, concolorous with stipe; con-

text stuffed, becoming hollow, concolorous with

pileus context. Basal mycelium sparse to copious,

always white. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with widely scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 5-15

(-30) hyphae; terminal cells of fascicular hyphae

6-101 x 3-37.5 Mm, filamentous, subclavate, cla-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

35

FIG. 12. Basidiomata of L. laccata var. pallidifolia (GMM 1735).

FIG. 13. Somatic culture mats of L. laccata var. pallidifolia (GMM 101 1). Top on PDA, left on

MMN, and right on MEA. Photo taken during week 4.

36

FTELDIANA: BOTANY

FIG. 14. Micromorphological features of L. laccata var. pallidifolia (GMM 1845): a, basidiospores; b, basidia. Scale

line = 10 fim.

vate, subcapitate or ventricose-rostrate; walls up

to 0.5 nm thick, light yellowish brown; contents

hyaline to light yellowish brown. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel; hyphae mostly

2-1 7.5 nm diam., thin-walled, hyaline to light yel-

lowish brown; cells filamentous to barrel-shaped.

Subhymenium morphologically undifferentiated.

Basidia 27.5-55 x 7.5-13.5(-16.5) urn, clavate,

hyaline; sterigmata 4, up to 7 pm long. Cheilo-

cystidia 23-55 x 2-7.5 ^m, filamentous to sub-

clavate, occasionally strangulate, absent or scat-

tered to abundant, thin-walled, hyaline.

Basidiospores (excluding ornamentation) [1,0007

65] (6.4-)7.4-10(-13) x (6-)7-10(-l 1.5) jan (Jc =

[7.3-]8.2-9[-9.6] x [6.7-J7.6-8.6 ^m), (2=1-

1.13(-1.3) (Q = 1-1.5[-1.2]), globose to subglo-

bose, occasionally broadly ellipsoid, hyaline,

echinulate; echinulae (0.5-)l-2 pm long, < 1 /zm

wide at base, relatively scarce to crowded; hilar

appendix 1.3-2.2 j*m long, prominent, truncate;

plage present; contents occasionally uniguttulate

or biguttulate. Basal mycelium hyphae mostly 3-

10.5 /Ltm diam., tightly interwoven, hyaline; cells

filamentous to barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 11;

Appendix B)— PDA: Radius at week 3 = 7-23 mm

or 62-73 mm, week 6 = 18-27 or 90 mm (agar

surface covered); mat felty, thick, tightly inter-

woven, some appearing almost crustose, tightly

appressed to agar surface, occasionally forming

cottony to felty aerial layer away from plug, not

translucent, white, in some becoming dark olive

brown or light chocolate color away from plug;

margin narrow to moderately broad, silky to

subfelty, thin, white, entire to undulate; plug oc-

casionally covered with cottony white hyphae or

with long serial aggregations of hyphae growing

away from top of plug, white, often becoming dark

olive brown or light chocolate color; hyphae mor-

phologically undifferentiated, rarely irregularly

swollen. MMN: Radius at week 3 = 13-19 mm

or (25-)29-52 mm, week 6 = 26-45 mm or 75

mm to covering agar surface; mat subfelty, felty

or silky, moderately thick, interwoven, in one iso-

late (TENN 42964) with several radially arranged

pie-shaped thicker sectors, tightly appressed to agar

surface, translucent, white; margin narrow, silky

to subfelty, not well differentiated, even to un-

dulate, occasionally somewhat serrate, white; plug

white; hyphae morphologically undifferentiated,

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

37

occasionally coralloid. MEA: Radius at week 3 =

12-33 mm or 53-62 mm, week 6 = 23-54 mm or

covering agar surface; mat silky to subfelty, thin

to moderate, appearing combed to loosely inter-

woven, occasionally becoming thicker near plug,

tightly appressed to agar surface, translucent, white;

margin not well differentiated, thin, entire to

slightly serrate, white; plug white; hyphae mor-

phologically undifferentiated.

HABITAT AND DISTRIBUTION— Solitary to gre-

garious, occasionally caespitose, associated with

Pinaceae, Fagaceae, and Betulaceae; cosmopoli-

tan; abundant. Collected throughout North Amer-

ica. A list of specimens examined is presented in

Appendix A.

OBSERVATIONS— Laccaria laccata var. pallidi-

folia is characterized by having small- to moder-

ate-sized, orange-brown, glabrous to finely scaly

basidiomata, and basidia that bear four globose to

subglobose, moderately echinulate basidiospores.

Mueller and Vellinga ( 1 986) and Mueller ( 1 99 1 a)

included collections now treated as L. ohiensis

(= L. tetraspord) within the concept of this taxon.

Reasons for this given by Mueller and Vellinga

(1986) included: (1) the macro- and micromor-

phology of several of the proposed varieties in-

tergraded between the two putative species; (2)

basidioma and basidiospore size, as well as basid-

iospore ornamentation length, appeared to form

a continuum for collections in this group; and (3)

somatic culture mat morphology did not appear

to vary between isolates referable to either of these

taxa. It was not possible for Fries and Mueller

(1984) to distinguish between collections of the

two intersterility groups (mating groups III and

IV) that they detected in the tested Swedish ma-

terial of L. laccata on the basis of basidioma and

basidiospore size and basidiospore ornamentation

length.

Several additional intersterility groups have since

been detected in North America (Mueller, 199 Ic).

Each of these groups was found to differ markedly

in RFLPs of mtDNA and rDNA (Gardes et al.,

1990, 199 la). Subsequent morphometric analyses

have shown that collections of some of these in-

tersterility groups, but not others, were segregated

during morphometric analyses of basidiospore data

(Mueller, 1991c). Two groups were clearly delim-

ited during morphometric analyses: one group

consisted of collections with globose basidiospores

with echinulae > 1.5 nm long and > 1.2 jum wide

at the base; the other group consisted of specimens

with globose to subglobose basidiospores with

echinulae 0.7-2 /*m long and < 1 ^m wide at the

base (Mueller, 199 Ic). The first group consisted of

collections referable to L. ohiensis and L. striatula;

collections in the second group are referable to

either L. laccata var. pallidifolia, L. laccata var.

moelleri, or L. longipes.

Laccaria laccata var. pallidifolia is differenti-

ated from L. ohiensis primarily by having narrow

basidiospore echinulae. Collections of L. laccata

var. pallidifolia with small basidiomata and glo-

bose basidiospores (characteristics of L. ohiensis)

are occasionally encountered.

Laccaria laccata var. pallidifolia is differenti-

ated from L. striatula on the basis of differences

in basidiospore ornamentation and macromor-

phological features. Collections of L. striatula have

relatively long, glabrous stipes that are usually

darker than the strongly striate pileus.

Laccaria laccata var. pallidifolia is differenti-

ated from L. longipes by having shorter stipes and

larger basidiospores.

Laccaria laccata var. pallidifolia is the most

commonly encountered taxon in the complex and

can be found throughout the United States and

Canada. No apparent habitat preference could be

determined from the material collected during this

study.

Laccaria longipes G. M. Mueller. Figures 15, 16,

54a, 65c.

Laccaria longipes G. M. Mueller, Mycotaxon 40: 145-

150. 1991. TYPE: Canada, Ontario, Nipissing

District, Algonquin Provincial Park, Spruce Bog

Trail, among Sphagnum under Picea mariana,

Larix laricina, and Alnus rugosa, 1 8 September

1984, G. M. Mueller 1929 (F!, holotype).

MACROMORPHOLOGY— Pileus ll-55(-78) mm

broad, convex to broadly convex, often becoming

plane to uplifted, often centrally depressed, slightly

to moderately translucent-striate, finely fibrillose,

orange-brown (6B5-6D7) fading to buff in age;

margin incurved to decurved or plane, entire to

undulate, becoming slightly eroded. Lamellae ad-

nate, distant, thick, up to 10 mm broad, light flesh

color (near 6A2). Stipe 67-138(-165) x 3-9 mm,

equal with slightly swollen base or narrowly cla-

vate, dry, slightly to moderately fibrillose-striate,

concolorous with pileus. Basal mycelium white.

Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of radially ar-

ranged barrel-shaped hyphae with occasional scat-

tered small fascicles of 10-30 ± perpendicular hy-

phae; terminal cells 5-10 ^m, morphologically

38

FIELDIANA: BOTANY

undifferentiated to subclavate, hyaline. Pileus tra-

ma tightly interwoven, morphologically undiffer-

entiated, hyaline to light yellowish brown. La-

mellar trama of parallel to subparallel hyphae,

mostly 3-19 ^m diam., thin-walled, hyaline; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia 28-44 x 7-10 nm, cla-

vate, hyaline; sterigmata 4, up to 10 p,m long. Pleu-

rocystidia lacking. Cheilocystidia not observed.

Basidiospores (excluding ornamentation) [158/7]

7-8.5(-9) x 6-7.8(-8.4) Mm (Jc = 7.6-7.8 x 6.8-

7.2 Mm), Q = (1-)1.05-1.2(-1.3) (Q = 1.08-1.13),

subglobose to broadly ellipsoid, occasionally glo-

bose or ellipsoid, hyaline, echinulate; echinulae

(0.7-)l-1.5(-2) nm long, less than 1 nm wide at

base.

SOMATIC CULTURE MAT MORPHOLOGY (N = 1 ;

GMM 1929)— PDA: Radius at week 6 = 43 mm;

mat felty, thick, tightly interwoven, tightly ap-

pressed to agar surface, not translucent, uniform

texture near plug, forming dendritic thicker strands

from midpoint to margin, tan to olive brown; mar-

gin < 6 mm broad, subfelty to silky, abruptly

thinner than mat, tan; hyphae 2.5-5 /um diam.,

morphologically undifferentiated. MMN: Radius

at week 6 = 28 mm; mat felty, thick, tightly in-

terwoven, tightly appressed to agar surface, uni-

form texture, dull white; margin up to 5 mm broad,

irregular, white; hyphae 2.5-8 fj,m diam., mor-

phologically undifferentiated, occasionally irreg-

ularly swollen. MEA: Radius at week 6 = 42 mm;

mat subfelty, thin, translucent, white; margin 2-3

mm broad, not well differentiated, white; hyphae

2.5-8 nm diam., most morphologically undiffer-

entiated, occasionally irregularly swollen.

HABITAT AND DISTRIBUTION— Among mosses,

especially Sphagnum, usually under Picea mari-

ana (Mill.) B.S.P., Larix laricina (Du Roi) K. Koch,

and Alnus rugosa (Du Roi) Spreng. Reported to

date from the Great Lakes region (southern On-

tario, Michigan, Wisconsin, Minnesota) and New

York. A list of specimens examined is presented

in Appendix A.

OBSERVATIONS— Laccaria longipes can be dis-

tinguished from other members of the L. laccata

complex by its relatively small, subglobose basid-

iospores, long stipe, and restricted habitat. Lac-

caria laccata var. moelleri also occurs in bogs and

has similar macromorphological features but dif-

fers in having larger basidiospores (x = 8-10 x

7.3-8.3 Mm)- Laccaria galerinoides Singer is an-

other taxon that grows among Sphagnum. It ap-

pears to be restricted to southern Argentina and

Chile and has only been reported from under

Nothofagus antarctica (G. Forster) Derst. Laccaria

galerinoides differs from the two Northern Hemi-

spheric taxa in having smaller, darker colored ba-

sidiomata and more elongate basidiospores (Q =

1.34; holotype).

Tested isolates of L. longipes were intersterile

with all other tested isolates of the L. laccata com-

plex, including isolates of L. laccata var. moelleri

(Mueller, 1991b,c). RFLPs of mtDNA and rDNA

indicate that divergence has occurred between L.

longipes and other taxa in the L. laccata complex

(Gardes et al., 1990, 199 la). Although isolates of

L. laccata var. moelleri were intersterile with all

tested North American isolates, including L. lac-

cata var. pallidifolia (intersterility group 1 ), they

were intercompatible with the tested Swedish iso-

lates of L. laccata var. pallidifolia, and both taxa

belong to intersterility group 3 (Mueller & Vellin-

ga, 1986; Mueller, 1 99 1 b,c). Data on potential mo-

lecular divergence between these morphologically

distinct taxa do not yet exist, however, because

both isolates of intersterility group 3 tested by

Gardes et al. (1990, 199 la) are referable to L.

laccata var. moelleri.

Collections of L. longipes were cited as L. lac-

cata var. moelleri in several recent publications

(Doudrick & Anderson, 1989; Gardes etal., 1990,

199 la). The decision to treat the North American

and Swedish populations as distinct taxa occurred

only after a synthesis of the data on RFLPs with

data on intercollection pairing reactions and mor-

phometric similarities (Mueller, 1991b,c).

It is not yet clear whether L. longipes and L.

laccata var. moelleri are closely related or if their

similar macromorphology is due to convergence

resulting from their occurrence among Sphagnum

and other mosses.

Laccaria fraterna (Cooke & Massee: Saccardo)

Pegler. Figures 17, 18, 54b, 62d.

= Agaricus fraternus Cooke & Massee in Cooke, Gre-

villea 16: 31. 1887, non Agaricus fraternus Lasch,

Linnaea 3: 402. 1828. [= Cortinarius sp.]. TYPE:

Australia: vie. Port Phillip, French no. 1 (K.!, ho-

lotype).

= Naucoria fraterna (Cooke & Massee) Saccardo, Syll.

Fung. 9: 110. 1891.

= Laccaria fraterna (Cooke & Massee: Saccardo) Peg-

ler, Austral. J. Bot. 13: 332. 1956.

= Naucoria goosensiae Beeli, Bull. Soc. Roy. Bot. Bel-

gique61: 88. 1928.

= Laccaria laccata f. bispora Heinemann, Bull. Jard.

Bot. Etat 34: 310. 1964. [change of name].

= Laccaria lateritia Malen?on, Bull. Soc. Mycol. France

82: 189. 1966.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

39

FIG. 15. Basidiomata of L. longipes (GMM 1929).

MACROMORPHOLOGY— Pileus 9-3 5 (-5 5) mm

broad, strongly convex to convex, becoming plane

to uplifted, often slightly depressed, not striate to

slightly translucent-striate, finely fibrillose to fi-

brillose, rusty red-brown (8D7-9E7), eventually

becoming buff; margin decurved to plane, entire

to slightly undulate; contex thin, concolorous with

pileus. Lamellae adnate, moderately distant to dis-

tant, thick, pinkish rose (near 8 A3). Stipe ( 1 7-)25-

65 x 3-5 mm, equal or slightly clavate, at times

caespitose, dry, fibrillose, moderately longitudi-

nally striate, concolorous or slightly darker than

40

FIELDIANA: BOTANY

FIG. 16. Micromorphological features of L. longipes (GMM 1929): a, basidiospores; b, basidia. Scale line = 10

pileus (9C5-9D6). Basal mycelium white, often

copious. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered fascicles of ± perpendicular

hyphae; fascicles composed of 1 0-20 hyphae; ter-

minal cells of fascicular hyphae 26-69 x 6.5-15

/urn, filamentous to clavate; walls up to 0.5 nm

thick, light yellowish brown. Pileus trama tightly

interwoven, morphologically undifferentiated, hy-

aline, light yellowish brown toward pileipellis. La-

mellar trama parallel; hyphae mostly 3-10(-15.5)

Mm diam., thin-walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia 29-46 x 8-

1 2 Mm, clavate, hyaline; sterigmata 2(3), up to 11

Mm long. Cheilocystidia not observed. Basidio-

spores (excluding ornamentation) [100/4] (7.8-)

8.5-1 1(-13.5) x (7.4-)8-10.5(-13.5)Mm(;c = 9.7-

10.5 x 8.9-9.9 Mm), Q =1-1.1 8(-l. 22) (Q= 1.0 1-

1.11), globose to subglobose, hyaline, strongly

echinulate; echinulae 1-1.8 Mm long, < 1 Mm wide

at base, crowded; hilar appendix 1.3-2.8 Mm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate.

HABITAT AND DISTRIBUTION— Under Eucalyp-

tus and other introduced trees. Laccaria fraterna

was probably introduced along with Eucalyptus

throughout the world. Commonly collected under

Eucalyptus throughout the world, including North

America. A list of specimens examined is pre-

sented in Appendix A.

OBSERVATIONS— Laccaria fraterna can be dis-

tinguished from other small Laccaria taxa by its

rusty red-brown basidiomata and 2-sterigmate ba-

sidia that bear globose to broadly ellipsoid basid-

iospores that are < 11 Mm long.

There has been considerable confusion in the

literature concerning the correct name for this tax-

on. Some workers have used the name L. ohiensis

for this taxon (e.g., Singer, 1942, 1946, 1949, 1967,

1975, 1977; McNabb, 1972), but an examination

of the holotype revealed that L. ohiensis has

4-sterigmate basidia (see Type Descriptions). Al-

though the most commonly used name for the

taxon has been L. lateritia, the correct name for

this taxon is L. fraterna (Mueller & Vellinga, 1 986;

Vellinga & Mueller, 1987).

Tom W. May (University of Melbourne, pers.

comm.) reports the finding of a potentially para-

typic collection at MEL that better fits the proto-

logue but that is not contaxic with the type spec-

imen housed at K. It has been assumed that the

report of ellipsoid basidiospores in the original

diagnosis of A. fraternus probably referred to an-

other collection on the type sheet at K that was

collected in New Zealand (Pegler, 1965; Mueller

& Vellinga, 1986). If the collection housed at MEL

is lectotypified, A. fraternus would not fit into the

generic circumscription of Laccaria and the cor-

rect basionym for the taxon treated here would be

N. goosensiae.

Ballero and Contu (1989) described L. singeri

Ballero & Contu. This name, however, is a later

homonym of L. singeri Locquin & Sarwal (Sarwal

& Locquin, 1 983) and Mueller and Vellinga ( 1 990)

renamed it L. impolita Vellinga & G. M. Mueller.

Laccaria impolita is similar in micromorphology

to L. fraterna but differs from it in basidioma

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

41

FIG. 17. Basidiomata of L. fraterna (GMM 2126).

color, lack of pileus striations, and ectomycorrhi-

zal hosts (north temperate trees). See the discus-

sion under L. impolita in Type Studies.

Laccaria montana Singer. Figures 19, 20, 54c, 66d.

= Laccaria montana Singer, Sydowia 7: 89. 1973.

TYPE: Switzerland, Valais, prope flumen Borgne

de Ferpecle, 1955-1960 m alt., 11 July 1971,

Singer M5464 (F!, holotype).

= Laccaria laccata var. montana Moller, Fungi of the

Faeroes: 269. 1945.

= Russuliopsis laccata var. rosella f. pusilla Larsen, Bot.

Iceland, vol. II, part IV 9: 525. 1932.

= Laccaria laccata var. pusilla (Larsen) Singer, Bull.

Soc. Mycol. France 83: 109. 1967. [non L. laccata

f. pusilla Schroeter in Cohn, Krypt.-Fl. Schlesien

3: 623. 1889(= L. laccata)}.

MACROMORPHOLOGY— Pileus 6-35 mm broad,

convex to plane, becoming uplifted, often de-

pressed, occasionally umbonate when young, usu-

ally plicate-striate when fresh, fibrillose to finely

fibrillose-scaly, hygrophanous, brownish orange

("Hazel" to "Cinnamon-Rufous"), fading to buff

color; margin decurved to plane, entire to undu-

late, occasionally becoming eroded; context < 1

mm thick at disc, flesh color "Buff-Pink"). La-

mellae sinuate to decurrent, close to distant, pink-

ish flesh color to light vinaceous ("Vinaceous-

Pink"). Stipe 13-54(-101) x 2-4(-7) mm, equal

or tapering slightly toward base or apex, occa-

sionally swollen at base, occasionally caespitose,

dry, fibrillose, not striate to moderately longitu-

dinally striate, concolorous with pileus. Basal my-

celium white. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered fascicles of ± perpendicular

hyphae; fascicles composed of 10-30 hyphae; ter-

minal cells of fascicular hyphae 39-51 x 5.5-10

Mm, filamentous to subclavate, light yellowish

brown in mass; walls up to 0.5 /xm thick, light

yellowish brown; contents hyaline to light yellow-

ish brown. Pileus trama tightly interwoven, mor-

phologically undifferentiated, hyaline, light yel-

lowish brown toward pileipellis. Lamellar trama

parallel to subparallel, hyphae mostly 2.5-20 pm

diam., thin- walled, hyaline to light yellowish

brown; cells filamentous to barrel-shaped. Sub-

hymenium morphologically undifferentiated. Ba-

sidia 34.5-55 x 10-15.5 nm, clavate, hyaline; ste-

rigmata 4, up to 11 nm long. Cheilocystidia 32-

55.5 x 3-4. 5 (-7. 5 ) nm, filamentous to subclavate,

42

FIELDIANA: BOTANY

FIG. 18.

line = 10

Micromorphological features ofL.fraterna (GMM 2126): a, basidiospores; b, bisterigmate basidia. Scale

rarely clavate, thin-walled, hyaline, only found in

one collection. Basidiospores (excluding ornamen-

tation) [120/6] (7.8-)8.5-14(-14.7) x (7-)8-12Mm

(jc = 9.4-12.6 x 8.5-1 0.5 Mm), 0 = 1-1.26(-1.33)

(Q = 1.07-1.2), globose to broadly ellipsoid, oc-

casionally ellipsoid, hyaline, echinulate; echinulae

(0.5-)0.9-1.8 /nm long, < 1 Mm wide at base, not

crowded to crowded; hilar appendix 1.3-2 Mm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 3-21 Mm diam., tightly interwoven, hya-

line; cells filamentous to barrel-shaped.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious, occasionally caespitose; in poor soil, hu-

mus, or among mosses; under Pinaceae, Betula,

or Salix; restricted to arctic, boreal, or montane

habitats; common. A list of specimens examined

is presented in Appendix A.

OBSERVATIONS— Laccaria montana can be dis-

tinguished from L. laccata by having larger basid-

iospores and an arctic to boreal distribution.

The apparent stability of basidial characters

within Laccaria coupled with the potential func-

tional differences between 2-sterigmate taxa (fac-

ultative homothallism) versus 4-sterigmate taxa

(obligatory heterothallism?) are the justification

that I use to treat L. montana and L. pumila as

separate species. Although there are differences in

basidiospore size between these two taxa, these

are probably due to the 4-sterigmate versus

2-sterigmate condition and are not independent

character states.

Homokaryotic isolates from only two speci-

mens of L. montana have been obtained to date.

Repeated attempts to obtain either intra- or in-

tercompatible pairings with isolates of either of

these stocks have failed (Mueller, 1991c). Homo-

karyotic isolates of L. pumila have not been ob-

tained, and consequently, no test of the putative

genetic isolation between these two taxa has been

undertaken. Multivariate morphometric analyses

only loosely grouped together the two tested col-

lections of L. montana (Mueller, 1991c). Finally,

data are not available on potential genetic diver-

gence between L. montana and other taxa because

representatives of L. montana are not included in

the RFLP analyses carried out by Gardes et al.

(1990, 199 la).

Laccaria montana is among the more common

Laccaria taxa found at high elevations and north-

ern latitudes. At least some of the reports of L.

tetraspora from the arctic are, according to their

descriptions and illustrations, L. montana (e.g.,

Kobayasi et al., 1967; Miller et al., 1982).

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

43

FIG. 19. Basidiomata of L. montana(GMM 1250).

Laccaria pumila Fayod. Figures 2 1 , 22, 54g, 70b.

= Laccaria pumila Fayod, Annali Accad. Agric. To-

rino 35: 91. 1893. TYPE: France, dept. Alpes

maritimes, Col de la Cayolle, 2,500 m alt., 1 8 July

1976, J. Trimbach 1463 (L!, neolypefide Mueller

& Vellinga, 1986).

= Clitocybe pumila (Fayod) Saccardo, Syll. Fung. 17:

13. 1905.

= Laccaria laccata var. pumila (Fayod) Favre, Ergebn.

Wiss. Unters. Schweiz. NatnParks V, 33: 51. 1955.

[not validly published, basionym lacking].

= Laccaria altaica Singer, Bull. Soc. Mycol. France 83:

122. 1967.

Misapplied names: Laccaria striatula sensu Singer,

Mycologia 35: 151. 1943; sensu auct. plur.— Laccaria

tortilis sensu M. Lange, Meddel. Granland 147: 29. 1955;

sensu Miller et al., Mycologia 74: 583. 1982.

MACROMORPHOLOGY— Pileus 3-27(-40) mm

broad, convex to plane, occasionally uplifted, of-

ten depressed, usually strongly translucent-striate

when fresh, glabrous to finely fibrillose, occasion-

ally becoming fibrillose-scaly with age, hygroph-

anous, red-brown to orange-brown ("Hay's Rus-

set," "Burnt Sienna," or "Sanford's Brown"),

fading to buff (near "Xanthine Orange," "Flesh-

Ocher," or "Salmon-Bun0"); margin incurved to

decurved, often becoming plane, entire to undu-

late, occasionally eroded; context thin, concolor-

ous. Lamellae sinuate to arcuate, distant, thick,

waxy appearing, < 8 mm broad, pinkish flesh col-

or ("Flesh Color" or "Pale Flesh Color"). Stipe

4-61 (-100) x 2-5(-9) mm, equal to subclavate,

often slightly bulbous, occasionally caespitose, dry,

fibrillose, longitudinally striate, ± concolorous with

pileus, fading to ochraceous buff ("Amber Brown,"

"Flesh-Ocher," or "Apricot Buff"). Basal myce-

lium white. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with widely scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-25

hyphae; terminal cells of fascicular hyphae 36.5-

64 x 8-16 ^m, filamentous, subclavate or clavate;

walls up to 0.5 /*m thick, light yellowish brown,

often encrusted with pigment(s); contents hyaline

to light yellowish brown. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel to subparallel; hyphae mostly

3-18 fim diam., thin-walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

44

FIELDIANA: BOTANY

FIG. 20. Micromorphological features of L. montana (GMM 1813): a, basidiospores; b, tetrasterigmate basidia.

Scale line = 10 nm.

morphologically undifferentiated. Basidia 37.5-

64.5 x 10.5-16 Mm, clavate, hyaline; sterigmata

2(-4), up to 14 MHI long. Cheilocystidia 27.5-46

x 3 Mm, filamentous to subclavate, hyaline, found

in one collection only. Basidiospores (excluding

ornamentation) [86/6] (10-)11-16.5(-20) x (7.8-)

10_14.5(_16)Mm(Jc= 12-13[-16.3] x 10.8-13.8

Mm), Q = 1-1.29 (Q = 1.1-1.19), subglobose to

broadly ellipsoid, occasionally globose or ellip-

soid, hyaline, echinulate; echinulae < 0.5-1.4

(-1.8) Mm long, crowded; hilar appendix 1 .3-2 Mm

long, prominent, truncate; plage present; contents

occasionally uniguttulate. Basal mycelium hyphae

mostly 4-19 nm diam., tightly interwoven, hya-

line; cells filamentous to barrel-shaped.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious, occasionally caespitose; in poor soil, hu-

mus, or among mosses; under Pinaceae, Betula,

or Salix; restricted to arctic, boreal, and montane

regions; common. A list of collections examined

is presented in Appendix A.

OBSERVATIONS— Laccaria pumila appears very

similar in the field to L. montana, L. tortilis, and

small striate forms of L. laccata var. pallidifolia.

It can easily be distinguished, however, by its

2-sterigmate basidia that bear large, subglobose to

broadly ellipsoid, echinulate basidiospores. Lac-

caria pumila has most commonly been reported

under the name L. altaica Singer. As discussed by

Mueller and Vellinga (1986), the name L. pumila

has priority. Another name occasionally misap-

plied to this taxon is L. striatula sensu Singer non

Peck (e.g., Singer, 1943b; Orton, 1960; Laursen &

Chmielewski, 1982).

The major character distinguishing L. pumila

from L. montana is that the latter has 4-sterigmate

basidia. Both are restricted to arctic, subarctic,

alpine, and boreal habitats and can be found grow-

ing sympatrically. Singer (1977) mentioned that

L. pumila may only be a two-spored form of L.

montana and thus the two might be conspecific.

Lahaie (1981) and data accumulated during this

study, however, have supported separation of these

taxa at the species rank. In all specimens examined

for this study, no basidiomata were found that had

both 2- and 4-sterigmate basidia, and Lahaie (1981)

only reported one collection in which both 2- and

4-sterigmate basidia were observed.

To date it has not been possible to obtain a tissue

culture or to germinate the basidiospores of L.

pumila.

Laccaria pumila appears to be the dominant, if

not the exclusive, 2-sterigmate Laccaria found in

the arctic, and the most common 2-sterigmate

Laccaria found in the mountains of western Unit-

ed States. Lange (1955) and Kobayasi et al. ( 1 967)

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

45

FIG. 21. Basidiomata of L. pumila (GMM 1298).

reported L. tortilis occurring in the arctic; how-

ever, the descriptions and illustrations of both in-

dicate that the collections are probably L. pumila.

I .act-aria striatula (Peck) Peck. Figures 23, 24, 55b,

71b.

= Clitocybe laccata var. striatula Peck, Annual Rep.

New York State Bot. 48: 244. 1894. TYPE: USA,

New York, Catskill Mountains, September, C. H.

Peck s.n. (NYS!, holotype).

= Laccaria striatula (Peck) Peck, Annual Rep. New

York State Bot. 157: 93. 1912.

MACROMORPHOLOGY— Pileus 6-30(-36) mm

broad, convex, occasionally becoming plane, often

depressed, strongly translucent-striate when fresh,

occasionally plicate-striate, finely fibrillose, occa-

sionally finely fibrillose-scaly near disc, hygroph-

anous, reddish brown to orange-brown ("Hazel,"

"Cinnamon-Rufous," or "Vinaceous-Rufous"),

then lighter in color ("Salmon Color," "Seashell

Pink," or "Pinkish Buff'); disc occasionally darker

in color ("Hay's Russet"); margin incurved to de-

curved, becoming plane, entire to undulate; con-

text thin, concolorous. Lamellae sinuate to adnate,

close to subdistant to distant, relatively narrow to

broad, thin to thick, pinkish flesh color ("Flesh-

Ocher" or "Pale Flesh Color"). Stipe 20-70(-103)

x l-4(-8) mm, equal, occasionally slightly bul-

bous, glabrous, appearing cartilaginous when fresh,

reddish brown, concolorous with disc or darker

("Kaiser Brown," "Hazel," "Cinnamon-Rufous,"

or "Onion-skin Pink"). Basal mycelium white.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered to numerous small fascicles

of ± perpendicular hyphae; fascicles usually com-

posed of 5-15 hyphae; terminal cells of fascicular

hyphae 33-85 x 6-18.5 fim, filamentous, subcla-

vate, clavate, subcapitate, or ventricose-rostrate,

occasionally strangulate; walls up to 0.5 fim thick,

hyaline to light yellowish brown; contents hyaline

to light yellowish brown. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel; hyphae 3-1 1(-27) ^m diam.,

thin-walled, hyaline to light yellowish brown; cells

filamentous to barrel-shaped. Subhymenium mor-

46

FIELDIANA: BOTANY

FIG. 22. Micromorphological features of L. pumila (GMM 1956): a, basidiospores; b, bisterigmate basidia. Scale

line = 10 tan.

phologically undifferentiated. Basidia 30-59.5 x

8-14.5 Mm, clavate, hyaline; sterigmata 4, up to

1 1 Mm long. Cheilocystidia not observed. Basid-

iospores (excluding ornamentation) [265/13] 7-

10(-12) x 7-10(-12) MHI (x = 8-9[-10] x 7.7-9

[-10] MHI), Q = 1(-1.12) (Q = 1-1.04), globose,

rarely subglobose, hyaline, echinulate; echinulae

1 .4-2.8 Mm long, up to 1 .8 Mm wide at base, crowd-

ed; hilar appendix 1.3-2 Mm long, prominent,

truncate; plage present; contents occasionally uni-

guttulate. Basal mycelium hyphae mostly 2-12.5

Mm diam., tightly interwoven, hyaline; cells fila-

mentous to barrel-shaped.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious; in damp areas, often among wet mosses,

usually not among Sphagnum, in mixed forests

with Tsuga canadensis (L.) Carr. and/or other Pi-

naceae and Fagaceae, eastern North America. Ma-

terial of this taxon has not been reported from

Europe. In eastern North America it is common

and abundant. A list of specimens examined is

presented in Appendix A.

OBSERVATIONS— Laccaria striatula is easily rec-

ognizable by its strongly translucent-striate pileus;

long, gracile, glabrous, reddish brown stipe; and

globose basidiospores with long and wide echin-

ulae. These characteristics differentiate it from L.

laccata var. pallidifolia and L. ohiensis, the two

taxa to which it is phenetically most similar. Be-

cause of the difficulty of interpreting dried her-

barium material lacking macromorphological

notes, it is sometimes difficult to differentiate be-

tween material of L. ohiensis and L. striatula.

Tissue cultures of this taxon were not obtained,

but homokaryotic isolates and reconstituted di-

karyons were white and grew moderately fast on

all employed media. Homokaryotic isolates of L.

striatula were intersterile with tested isolates of

other members of the L. laccata complex (Mueller,

1991c). Material of this taxon was not included in

our RFLP analyses (Gardes et al., 1990, 199 la).

Singer (1946), Orton (1960), Bon (1983), and

others have treated this name as referring to a

taxon with bisterigmate basidia. An examination

of the type specimen, however, showed it to have

4-sterigmate basidia, and that concept is used here

(see Type Studies).

This taxon is abundant in wet mossy areas in

the mountains of Georgia, North Carolina, New

York, South Carolina, Tennessee, and Nova Sco-

tia. It has also been collected in southern Ontario

and northern Michigan and Wisconsin.

Mueller (1985) incorrectly used the name L. gla-

bripes McNabb for this taxon. Aguirre-Acosta and

Perez-Silva (1978) reported L. glabripes from

Mexico. Although I have not seen their material,

it is likely that it is referable to L. striatula, not L.

glabripes. All other reports of L. glabripes have

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

47

FIG. 23. Basidiomata of L. striatula (GMM 1780).

come from Australia and New Zealand. I have not

encountered material of L. striatula among the

specimens that I have collected and examined from

Costa Rica and South America.

Laccaria ohiensis (Montagne) Singer. Figures 25,

26, 55a, 68b.

= Agaricus ohiensis Montagne, Syll. Crypt.: 1 00. 1856.

TYPE: USA, Ohio, Columbus, before 1856, Sul-

livant s.n. (PC!, holotype).

= Clitocybe ohiensis (Montagne) Saccardo, Syll. Fung.

V: 181. 1887.

= Laccaria ohiensis (Montagne) Singer, Mycologia 38:

688. 1946.

= Clitocybe tortilis var. gracilis Peck, Annual Rep. New

York State Bot. 67: 36. 1903.

= Laccaria tetraspora Singer, Mycologia 38: 689. 1946.

= Laccaria tetraspora var. tetraspora Singer auto-

matically established by var. valdiviensis Singer,

Bull. Soc. Mycol. France 83: 113. 1967.

= Laccaria tetraspora var. tetraspora f. tetraspora

Singer automatically established by f. major Sing-

er, Bull. Soc. Mycol. France 83: 113. 1967.

= Laccaria tetraspora var. valdiviensis Singer, Bull. Soc.

Mycol. France 83: 113. 1967.

= Laccaria tetraspora var. peullensis Singer, Bull. Soc.

Mycol. France 83: 113. 1967.

= Laccaria tetraspora var. scotica Singer, Bull. Soc. My-

col. France 83: 114. 1967.

= Laccaria scotica (Singer) Bon, Doc. Mycol. 11: 23.

1981. [not validly published, basionym lacking].

= Laccaria tetraspora var. xena Singer, Bull. Soc. Mycol.

France 83: 116. 1967.

= Laccaria tetraspora var. aberrans Singer, Bull. Soc.

Mycol. France 83: 116. 1967.

= Laccaria tetraspora var. tetraspora f. major Singer,

Bull. Soc. Mycol. France 83: 113. 1967.

MACROMORPHOLOGY— Pileus 7-26(-50) mm

broad, convex to plane, often depressed, plicate-

striate and strongly translucent-striate when fresh,

glabrous to finely fibrillose, hygrophanous, reddish

brown (near 8D6) soon becoming orange-brown

(7C5-6), finally fading to buff; margin decurved

to plane, entire to undulate; context thin, concol-

orous. Lamellae adnexed to adnate, distant, mod-

erately thick, pinkish flesh color (6A2-7A3). Stipe

12-25(-40) x l-2(-6) mm, equal or slightly bul-

bous, dry, glabrous to finely fibrillose, astriate to

slightly longitudinally striate, concolorous with pi-

leus. Basal mycelium white. Basidiospores white

in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with widely scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 5-30 hy-

phae; terminal cells of fascicular hyphae 26-67 x

5-17.5 Mm, filamentous, subclavate or clavate;

48

FIELDIANA: BOTANY

FIG. 24. Micromorphological features of L. striatula (GMM 1940): a, basidiospores; b, basidia. Scale line = 10 nm.

walls up to 0.5 nm thick, light yellowish brown,

often encrusted with pigment(s); contents hyaline

to light yellowish brown. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel to subparallel; hyphae mostly

2-10 fj,m diam., thin- walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

morphologically undifferentiated. Basidia 28-60

x 8-16 /mi, clavate, hyaline; sterigmata 4, up to

10 nm long. Cheilocystidia 20-55 x 3-5.5 fim,

filamentous to subcapitate, absent to relatively

abundant, thin-walled, hyaline. Basidiospores (ex-

cluding ornamentation) [375/11] (6.4-)7.7-9.4

(-1 1) x (6.4-)7-9(-10.6) Mm (x = 7.9-8.4[-9.3] x

7.8-8.4[-9.1]/im), Q= 1-1.09(-1.2)«2 = 1-1.05),

globose to subglobose, rarely broadly ellipsoid, hy-

aline, echinulate; echinulae (1-) 1.5-2. 8 nm long,

> 1.2 nm wide at base, crowded; hilar appendix

1.3-2 pm long, prominent, truncate; plage present;

contents occasionally uniguttulate.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious, not commonly collected in boreal or north

temperate habitats. Commonly reported from

subtropical, tropical, and south temperate regions.

A list of collections examined is presented in Ap-

pendix A.

OBSERVATIONS— Collections of Laccaria ohien-

sis are characterized by their small basidioma size,

strongly striate pilei, short, concolorous stipes, and

globose basidiospores with long and wide echin-

ulae.

Laccaria ohiensis is primarily differentiated from

Laccaria laccata var. pallidifolia by having basid-

iospore echinulae that are > 1.2 nm wide at their

base. In contrast to L. ohiensis, whose collections

are relatively uniform in macro- and micromor-

phological features, collections of L. laccata var.

pallidifolia are highly variable in most morpho-

logical characters. Collections of L. laccata var.

pallidifolia with small basidiomata and globose

basidiospores (characteristics of L. ohiensis) are

occasionally encountered.

Tested homokaryotic isolates of these two taxa

are intersterile (Fries & Mueller, 1984; Mueller,

1991c) and differ in mtDNA and rDNA RFLP

patterns (Gardes et al., 1990, 199 la; Mueller,

1991c). Isolates identified as belonging to mating

group III (Fries & Mueller, 1 984) and intersterility

group 4 (Gardes etal., 1990, 1 99 1 a; Mueller, 1991c)

are referable to L. ohiensis.

Laccaria ohiensis is differentiated from L. stria-

tula by differences in macromorphology. Basid-

iomata of L. striatula have relatively long, gla-

brous stipes that are darker in color than the

strongly striate pilei. Collections of these two taxa

were not segregated during morphometric analyses

of basidiospore characters (Mueller, 1991c), but

tested isolates of the two taxa are intersterile. The

isolate of L. ohiensis included in the analyses of

mtDNA and rDNA had unique RFLP patterns

(Gardes et al., 1990, 1991a).

The nolotype of L. ohiensis (see Type Studies)

consists of basidiomata that have globose, echin-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

49

FIG. 25. Basidiomata of L. ohiensis (GMM 1730).

ulate basidiospores born on 4-sterigmate basidia.

This agrees with Singer's (1942) description of the

type and Malenfon's (1966) and Malencon and

Bertult's (1975) concept of the taxon. In subse-

quent papers (e.g., Singer, 1946, 1977; Singer &

Digilio, 1952; Bon, 1983), L. ohiensis was treated

as a taxon with 2-sterigmate basidia. The correct

name for the 2-sterigmate taxon discussed by Sing-

er (1967, 1977), which has moderate-sized, sub-

globose basidiospores and normally occurs in warm

and dry regions, often under Eucalyptus, is L. fra-

terna. Laccaria impolita is similar to L. fraterna

but differs in macromorphology and association

with north temperate trees (see Type Studies).

Laccaria tortilis (Bolton) Cooke. Figures 27-29,

55c,d, 72b.

= Agaricus tortilis Bolton, Hist. Fung. Halifax 1:41,

tab. XLI, fig. A. 1788. TYPE: Tab. XLI, fig. A in

Bolton, Hist. Fung. Halifax vol. 1. 1788 (lectotype

fide Mueller, 199 la). Representative specimen:

Great Britain, Scotland, Yorkshire, Tanfield

Lodge, 6 September 1969, Orton 3642 (E!, "neo-

lype"fide Mueller, 1987).

= Omphalia tortilis (Bolton) S. F. Gray, Nat. Arr. Brit.

PI. 1: 613. 1821.

= Laccaria tortilis (Bolton) Cooke, Grevillea 12: 70.

1884.

= Clitocybe tortilis (Bolton) Saccardo, Syll. Fung. 5:

198. 1887.

= Collybia tortilis (Bolton) Quelet, Flore Mycolo-

gique: 237. 1888.

= Clitocybe laccata var. tortilis (Bolton) Barla, Fl. my-

col. ill.: 64. 1892.

= Agaricus echinosporus Spegazzini, Anales Soc. Ci. Ar-

gentina 10: 123. 1880.

= Clitocybe echinospora (Spegazzini) Saccardo, Syll.

Fung. 5: 198. 1887.

= Laccaria echinospora (Spegazzini) Singer, Ann. My-

col. 41:17. 1943.

= Clitocybe revoluta Barla, Fl. mycol. ill.: 64. 1888. [non

Clitocybe revoluta Peck, Annual Rep. New York

State Bot. 46: 23. 1893].

MACROMORPHOLOGY— Pileus 5-23 mm broad,

convex, becoming plane to uplifted, strongly pli-

cate-striate, subglabrous to finely fibrillose, hy-

grophanous, vinaceous brown to brownish orange

(" Vinaceous-Brown," "Sorghum Brown," or "Or-

ange Rufous") fading lighter in color ("Rood's

Brown" to "Vinaceous-Russet"), eventually be-

coming buff color; margin plane, undulate, eroded,

50

FIELDIANA: BOTANY

FIG. 26. Micromorphological features of L. ohiensis (GMM 2354): a. basidiospores; b, basidia. Scale line = 10

or rimose; context thin, concolorous. Lamellae

sinuate to adnate, distant, broad, thick, pinkish

flesh color to slightly vinaceous ("Flesh Color" to

"Light Russet- Vinaceous"). Stipe 4-15 x 1-3.5

mm, equal to subbulbous, dry, finely fibrillose, not

striate, concolorous with pileus. Basal mycelium

white. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with widely scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 5-1 5 hy-

phae; terminal cells of fascicular hyphae 26.5-69

x 6.5-15 nm, filamentous to clavate; walls up to

0.5 nm thick, light yellowish brown. Pileus trama

tightly interwoven, morphologically undifteren-

tiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel; hyphae mostly

6-14.5 nm diam., thin-walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

morphologically undifferentiated. Basidia 33-64

x 7-16 pm, clavate, hyaline; sterigmata 2(3), up

to 1 1.5 nm long. Cheilocystidia lacking or scarce;

filamentous. Basidiospores (excluding ornamen-

tation) [90/6] (9.2-)10-14.5(-16) x (8.3-)10-14.5

(-16) MHI (x = 10.9-13 x 10.5-12.7 Mm), Q = 1-

1.09(-1.17) (Q = 1-1.03[-1.07]), globose, rarely

subglobose, hyaline, strongly echinulate; echinulae

1.4-3.2(-4) nm long, up to 2.3 fim wide at base,

crowded; hilar appendix 1.3-2.3 nm long, prom-

inent, truncate; plage present; contents occasion-

ally uniguttulate. Basal mycelium hyphae 3-14 ^m

diam., tightly interwoven, hyaline; cells filamen-

tous to barrel-shaped.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious, occasionally caespitose, often on bare,

poorly drained soil, apparently associated with both

Pinaceae and Fagaceae; cosmopolitan; not com-

mon. A list of specimens examined is presented

in Appendix A.

OBSERVATIONS— Laccaria tortilis can be distin-

guished from the rest of the small, plicate-striate

Laccaria taxa by its 2-sterigmate basidia that bear

large, globose basidiospores with long and broad

echinulae.

It has not been possible to obtain tissue cultures

or to germinate the basidiospores of this taxon.

Material of L. tortilis was not included in the RFLP

analyses of Gardes et al. (1990, 199 la).

There has been some confusion in the literature

concerning the correct name for this taxon. Agar-

icus tortilis is the earliest name used for this mac-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

51

FIG. 27. Basidiomata of L. tortilis (GMM 1710).

FIG. 28. Basidiomata of L. tortilis (GMM 1710).

52

FIELDIANA: BOTANY

FIG. 29. Micromorphological features of L. tortilis (McAdoo 78#28): a, basidiospores; b, basidia. Scale line

10 MHI.

romorphological form (Bolton, 1788). Although

no holotype exists, and Bolton's description did

not give any morphological data, his color plate

clearly illustrated the macromorphological traits

of this taxon. I agree with the majority of modern

workers (e.g., Dennis et al., 1960; Orton, 1960;

Bon, 1983; Moser, 1983) who use the binomial L.

tortilis for this taxon based on common usage (Korf,

1982a,b). Additionally, an examination of repre-

sentative material from the environs of the type

locality shows that Bolton probably had access to

specimens that fit this micromorphological form.

Rea (1922), Singer (1950a, 1952), Ballero and

Contu (1989), and a few others consider A. tortilis

to be a smaller-basidiospored species, and Singer

(1943b, 1950a, 1952, 1967, 1977, 1986) used L.

echinospora (Spegazzini) Singer for this taxon. Cle-

mengon (1984) recognized both L. tortilis and L.

echinospora as large-basidiospored taxa. He dif-

ferentiated them on echinulae length, with L. tor-

tilis having shorter echinulae than L. echinospora.

In an attempt to stabilize the application of the

name, Mueller (1987) designated a neotype for L.

tortilis. As discussed under L. proxima, the con-

flicting interpretations of this name have not been

resolved by designating Bolton's illustration the

lectotype. To stabilize the application of this ep-

ithet, the collection that was proposed as a neotype

(Mueller, 1987) is now designated a "representa-

tive specimen" (see Type Studies).

In North American literature, Peck (1912) and

Murrill (1914) used the name in the current sense,

while Coker and Beardslee (1922) used L. tortilis

for specimens with 4-sterigmate basidia and mod-

erate-sized basidiospores.

Although not frequently collected, Laccaria tor-

tilis occurs throughout much of the United States

and Canada outside of arctic habitats. Most re-

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

53

FIG. 30. Basidiomata of L. trichodermophora (GMM 2321).

FIG. 31. Somatic culture mats of L. trichodermophora (GMM 1014). Top on PDA, left on MMN,

and right on MEA. Photo taken during week 4.

54

FIELDIANA: BOTANY

FIG. 32. Micromorphological features of L. trichodermophora (GMM 2306): a, basidiospores; b, basidia; c, cheil-

ocystidia. Scale line = 10 jtm.

ports under this name from the arctic refer to col-

lections of L. pumila (see Observations under L.

pumild).

Laccaria Metasection Amethystina

[see p. 24 for discussion]

Basidiomata and somatic culture mats with vi-

olet pigment(s); basidiospores not ellipsoid to ob-

long with echinulations 0.5(-1.4) /xm long.

Laccaria trichodermophora G. M. Mueller. Fig-

ures 30-32, 56c, 72c.

Laccaria trichodermophora G. M. Mueller, Mycotax-

on 20: 1 12-1 14. 1984. TYPE: USA, Mississippi,

Harrison Co., DeSoto National Forest, Harrison

Experimental Forest, Road H-6, 5 December

1980, G. M. Mueller 1062 (TENN 42523) (TENN!,

holotype).

Misapplied name: Laccaria farinacea sensu Singer non

Hudson, Sydowia Beih. 7: 8. 1973.

MACROMORPHOLOGY— Pileus 9-66 mm broad,

convex to plane, occasionally becoming uplifted,

often depressed, not striate, strongly pruinose to

fibrillose, becoming fibrillose-scaly to scaly owing

to cuticular diffraction, hygrophanous, brownish

orange, occasionally reddish brown ("Hazel," " Vi-

naceous-Rufous," "Auburn," "Orange Rufous,"

"Cacao Brown," or "Cinnamon-Rufous"), fading

light brown to buff color ("Flesh-Ocher" to "Apri-

cot Buff'), occasionally darker reddish brown at

disc ("Hay's Russet" to "Kaiser Brown"); margin

incurved, decurved, or plane, entire to undulate,

occasionally becoming eroded; context 1-2 mm

thick, tapering quickly to margin, pinkish flesh

color ("Light Congo Pink" to "Pale Vinaceous-

Pink"). Lamellae sinuate to adnate, close to dis-

tant, broad, relatively thin to thick, flesh color

("Vinaceous-Pink," "Shell Pink," "Flesh Color,"

or "Pale Salmon Color"), at times vinaceous in

age (near "Vinaceous"). Stipe 20-1 1 5 x 2-1 1 mm,

equal, subclavate or slightly bulbous, dry, fibril-

lose, inconspicuously to moderately longitudinally

striate, concolorous with pileus; context stuffed,

becoming hollow, concolorous with pileus con-

text. Basal mycelium violet (near "Lavender" or

"Pale Violet") when fresh, strongly hygrophanous,

fading to white. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of very nu-

merous large fascicles of ± perpendicular hyphae,

often forming a trichodermium in young speci-

mens and at the disc; fascicles composed of 1 5-

30 or more hyphae; terminal cells of fasciculate

hyphae 25-73.5 x 6-32 fim, filamentous, clavate

or occasionally capitate; walls up to 0.5 nm thick,

light yellowish brown; contents hyaline to light

yellowish brown. Pileus trama tightly interwoven,

morphologically undifferentiated, hyaline, light

yellowish brown toward pileipellis. Lamellar tra-

ma parallel; hyphae mostly 3-18 /irn diam., thin-

walled, hyaline to light yellowish brown; cells fil-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

55

amentous to barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia 24.5-55 x

7-13(-20) Mm, clavate, hyaline; sterigmata 4, up

to 9 /um long. Cheilocystidia 17.5-60 x 2-6.5 Mm,

filamentous, occasionally subclavate, thin-walled,

hyaline, absent, scattered or abundant. Basidio-

s pores (excluding ornamentation) [415/20] (6.2-)

6.8-8. 7(-10.6) x 6-8(-9.2) urn (x = 7.1-8[-8.5]

x 6.3-8 Mm), (2=1-1. 24(-l. 36) (Q = [ 1.01-]1. 08-

1.17), subglobose to broadly ellipsoid, occasion-

ally globose or ellipsoid, hyaline, echinulate;

echinulae (0.5-)0.9-1.8 Mm long, irregularly spaced

to crowded; hilar appendix 1.3-1.8 Mm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 3-12 Mm diam., tightly interwoven, hya-

line; cells filamentous to barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 8;

Appendix B)— PDA: Radius at week 3 = 15-38

mm or 42-45 mm, week 6 = (23-)29-59 mm or

covering agar surface; mat felty, tightly interwo-

ven, uniformly thick or with narrow, thicker den-

dritic strands radiating out from plug, tightly ap-

pressed to agar surface, normally forming pruinose

aerial layer away from plug with time, not trans-

lucent, bright violet fading to violet, finally to light

orange-brown near plug; aerial hyphae light gray-

ish violet; margin 2-6 mm broad, subfelty, felty

or silky, thin to thick, entire to uneven, light violet

to white; plug dark violet, soon becoming light

orange-brown; hyphae morphologically undiffer-

entiated, occasionally subcoralloid or irregularly

swollen. MMN: Radius at week 3 = 24-44 mm

or 52-64 mm, week 6 = (43-)54-78 mm or agar

surface covered; mat subfelty becoming felty or

silky, thin to thick, with 2 or 3 narrow (2-3 mm),

slightly thicker concentric zones or with slightly

thicker, radially arranged, dendritic strands or uni-

formly thin, tightly appressed to agar surface,

translucent, light violet, thicker zones somewhat

darker; margin not well differentiated from mat,

silky to subfelty, sinuate, light violet to white; plug

concolorous with mat; hyphae same as in PDA.

MEA: Radius at week 3 = 20-42 mm, week 6 =

38 mm or agar surface covered; mat silky to sub-

felty, thin or thick, occasionally thicker near plug,

loosely interwoven or interwoven, tightly ap-

pressed to agar surface, translucent, white; margin

not well differentiated from mat, silky to subfelty,

entire to sulcate, white; plug white; hyphae mor-

phologically undifferentiated, occasionally irreg-

ularly swollen.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious; commonly encountered in southeastern

North America, in temperate coniferous or mixed

coniferous— deciduous forests, apparently usually

associated with species of Pinus. A list of speci-

mens examined is presented in Appendix A.

OBSERVATIONS— Laccaria trichodermophora

differs from L. laccata by having violet basal my-

celium and smaller basidiospores. Its culture mat

morphology differs by displaying a faster growth

rate and violet coloration on PDA and MMN.

Because of the ephemeral nature of the violet pig-

ment in the basal mycelium and the slight overlap

of basidiospore size and shape with those of L.

laccata var. pallidifolia, it is occasionally difficult

to differentiate between dried herbarium speci-

mens of the two taxa.

Laccaria trichodermophora can be distin-

guished from L. bicolor and L. nobilis by its dis-

tribution, basidioma coloration, and scant basal

mycelium. Additionally, the three taxa have dis-

tinct culture mat morphologies. Laccaria bulluli-

fera Singer from Mexico is characterized by the

occurrence of large, swollen cheilocystidia.

Mueller and Gardes (1991) summarized the re-

sults of intercollection pairing studies, phenetic

analyses, and analyses of mtDNA and rDNA

RFLPs for the L. bicolor complex. They concluded

that collections of L. trichodermophora were well

delimited from L. bicolor and L. nobilis (see Ob-

servations under L. bicolor). The concept of L.

trichodermophora used here includes material

termed Bi 1 and L. trichodermophora in previously

published phenetic analyses (Mueller, 1985).

Singer and Moser (1965) and Singer (1973,1977,

1986) used the name L. farinacea for the taxon

herein referred to as L. trichodermophora. No type

exists for A. farinaceus, and Hudson (1798) listed

A. laccatus under A. farinaceus implying that A.

farinaceus was only a new name for A. laccatus.

Fries (1821) placed A. farinaceus in synonymy un-

der A. laccatus var. "a." In addition, neither Hud-

son nor Persoon ( 1 80 1 ) mentioned the color of the

basal mycelium in their description. It was nec-

essary, therefore, to propose a new name for this

taxon.

All of the collections of L. trichodermophora

observed from the southeastern United States ap-

peared to be associated with Pinus. Laccaria tri-

chodermophora has not been reported from west-

ern or midwestern North America. To date, no

material referable to L. bicolor sensu stricto or L.

nobilis has been encountered in southeastern North

America. Material from the northeastern United

States or Atlantic Coast of Canada was not in-

cluded in Mueller and Gardes (1991), and the oc-

56

FIELDIANA: BOTANY

currence of these three taxa in that area is not

known. Collections of L. bicolor sensu lato are

commonly collected in northeastern North Amer-

ica and are currently treated as L. bicolor. Aguirre-

Acosta and Perez-Silva (1978) and Montoya-Bello

et al. (1987) reported L. trichodermophora (as L.

farinacea sensu Singer) from Mexico. Mueller and

Strack (unpubl.) have collected L. trichodermo-

phora beneath Neotropical species of Quercus in

Costa Rica.

Laccaria bicolor (Maire) Orton. Figures 33-35,

56a,b, 60c.

= Laccaria laccata var. bicolor Maire, Publ. Inst. Bot.

Barcelona 3: 84. 1937. TYPE: Spain, Catalonia,

Collado de Tosses, 7 October 1933 Maire s.n.

(MPU!, holotype).

= Laccaria proximo var. bicolor (Maire) Kiihner &

Romagnesi, 1935. Flore Analytique des Cham-

pignons Superieurs: 131. 1935. [nom. invalidum,

Art. 33: 2 ICBN].

= Laccaria bicolor (Maire) Orton, Trans. Brit. Mycol.

Soc. 43: 177. 1960.

= Laccaria laccata var. pseudobicolor M. Bon in Bon

& Haluwijn, Doc. Mycol. 12(46): 42. 1982.

MACROMORPHOLOGY— Pileus 8-70 mm broad,

convex to plane, often depressed, not striate, finely

fibrillose, fibrillose-scaly or occasionally scaly, hy-

grophanous, pinkish flesh color ("Walnut Brown,"

"Onion-skin Pink," "Kaiser Brown," or "Cinna-

mon-Rufous") fading to buff color ("Flesh Ocher,"

"Salmon Buff," or near "Pale Salmon Color");

margin decurved to plane, entire to undulate, often

eroded; context thin, tapering quickly to margin,

light vinaceous ("Pale Brownish Vinaceous" or

"Hydrangea Pink"). Lamellae adnate to arcuate,

subdistant to distant, broad, thick, light vinaceous

("Pale Purplish Vinaceous," "Pale Vinaceous," or

"Hydrangea Pink"), fading to pinkish flesh color

("Light Congo Pink" or "Shell Pink"), then light

flesh color ("Pale Flesh Color" or "Pale Salmon

Color"). Stipe 23-85(-130) x 3-6(-10) mm, equal,

subclavate or slightly bulbous, dry, fibrillose, lon-

gitudinally striate, concolorous with pileus; stria-

tions concolorous with ground color or slightly

darker red brown. Basal mycelium copious, hy-

grophanous, violet when fresh ("Dull Lavender"

to "Pale Vinaceous-Lilac"), becoming white.

MICROMORPHOLOGY — Pi lei pel 1 i s of interwo ven

hyphae with numerous large fascicles of ± per-

pendicular hyphae; fascicles composed of ( 1 5-)25-

30 or more hyphae; terminal cells of fascicular

hyphae 2 7. 5-7 6 x 6- 18. 5 Mm, subclavate, clavate,

or rarely subcapitate; walls up to 0.5 Mm thick,

light yellowish brown; contents hyaline to light

yellowish brown. Pileus trama tightly interwoven,

morphologically undifferentiated, hyaline to light

yellowish brown toward pileipellis. Lamellar tra-

ma parallel; hyphae mostly 2-13.5 nm diam.,

thin-walled, hyaline to light yellowish brown; cells

filamentous to barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia 28.5-55 x

7.4—13 Mm, clavate, hyaline; sterigmata 4, up to 9

Mm long. Cheilocystidia 24.5-55 x 2.5-8 Mm, fil-

amentous to subclavate, thin-walled, hyaline, ab-

sent to abundant. Basidiospores (excluding orna-

mentation) [465/28] (5.5-)7-8.7(-10) x (5.5-)6-

7.8(-9.2) Mm (Jc = 7.0-8.4[-9] x 6.2-7.8 Mm), Q

= 1-1.26(-1.36) «2 = 1.05-1.23), subglobose to

broadly ellipsoid, occasionally globose or ellip-

soid, hyaline, echinulate; echinulae 1-1.8 Mm long,

< 1 Mm wide at base; hilar appendix 1.3-2 Mm

long, prominent, truncate; plage present; contents

occasionally uniguttulate. Basal mycelium hyphae

mostly 3-15.5 Mm diam., tightly interwoven, hy-

aline; cells filamentous to barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 10;

Appendix B)— PDA: Radius at week 3 = 1 1-32

mm, week 6 = 18-40(-54) mm; mat felty, thick,

tightly interwoven, tightly appressed to agar sur-

face, in time forming pruinose aerial layer away

from plug, occasionally becoming furrowed owing

to irregular infolding near plug, not translucent,

bright violet fading to light orange-brown or re-

maining bright violet; aerial hyphae light grayish

violet, often covering most of mat by week 6 and

then masking mat color; margin 3-4 mm broad,

subfelty, thin, light violet to white; plug dark violet

at first, becoming light orange-brown; hyphae

morphologically undifferentiated or irregularly

swollen, violet in mass, pigment intracellular.

MMN: Radius at week 3 = 22-41 mm, week 6 =

(31-)40-63 mm; mat silky, subfelty or felty, thin

or thick, loosely to tightly interwoven, occasion-

ally with 3 or 4 narrow concentric thicker bands,

tightly appressed to agar surface, translucent or

not translucent, at first light violet or violet, soon

buff, by week 3 violet color usually restricted to

thicker bands and near margin; margin 2—4 mm

broad, silky to subfelty, thin, loosely interwoven,

even to serrate, light violet; plug light violet; hy-

phae morphologically undifferentiated or rarely ir-

regularly swollen. MEA: Radius at week 3=19—

43 mm, week 6 = 30-52 mm, TENN 42529 68-76

mm; mat subfelty to felty, thick, interwoven, oc-

casionally with small, scattered, thicker sectors,

tightly appressed to agar surface, translucent, white;

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

57

FIG. 33. Basidiomata of L. bicolor (GMM 1327).

FIG. 34. Somatic culture mats of L. bicolor (GMM 1 293). Top on PDA, left on MMN, and right

on MEA. Photo taken during week 4.

58

FIELDIANA: BOTANY

FIG. 35. Micromorphological features of L. bicolor (GMM 2013): a, basidiospores; b, basidia; c, cheilocystidia.

Scale line = 10 nm.

margin 2-3 mm broad, subfelty, not well differ-

entiated, often very uneven, white; plug white; hy-

phae morphologically undifferentiated, occasion-

ally with a few scattered irregular swollen hyphae.

HABITAT AND DISTRIBUTION— Scattered, occa-

sionally caespitose. Very commonly encountered

on soil or among mosses under conifers in western

North America east to Ontario and Michigan.

Specimens of L. bicolor sensu lato from north-

eastern United States and the Atlantic provinces

of Canada are included under L. bicolor (see be-

low). A list of specimens examined is provided in

Appendix A.

OBSERVATIONS— Laccaria bicolor is character-

ized by having moderate-sized basidiomata, vio-

laceous lamellae when fresh, and copious violet

mycelium at the stipe base. Laccaria trichoder-

mophora differs by having pinkish flesh-colored

lamellae and sparse, strongly hygrophanous, violet

basal mycelium. Laccaria bicolor has been re-

ported from western and northern North America

and Europe; L. trichodermophora has only been

reported from southeastern North America, Mex-

ico, and Costa Rica. The large, scaly basidiomata

of L. nobilis differentiate that taxon from L. bi-

color. Laccaria nobilis occurs sympatrically with

L. bicolor in western and north central North

America but has not been reported from Europe.

All three of these taxa have distinct culture mat

morphologies.

Mueller and Gardes (1991) summarized the re-

sults of intercollection pairing studies, phenetic

analyses, and analyses of mtDNA and rDN A for

the L. bicolor complex. Three intersterility groups

were detected among 38 North American isolates

tested. Matings within a group were frequent but

mating between intersterility groups were rare. The

three intersterility groups were delimited during

phenetic analyses, indicating that these groups dif-

fered morphologically. The two Swedish isolates

used were completely intercompatible with one

North American group but only partially inter-

compatible with isolates of the other two groups.

These results were more or less concordant with

data obtained by RFLP analysis of mtDNA and

rDNA (Gardes et al., 1990, 199 la). The North

American isolates formed a relatively homoge-

neous group and were differentiated from the two

Swedish isolates based on analyses of rDNA

(Gardes et al., 1990). In contrast, analyses of

mtDNA detected divergence between the North

American intersterility groups but not between the

Swedish isolates and North American isolates

(Gardes et al., 1 99 1 a). Based on a synthesis of these

data, the Swedish collections and material from

western North America and areas adjacent to the

Great Lakes were treated as Laccaria bicolor sensu

stricto; L. nobilis was circumscribed as a taxon

with large, robust, scaly basidiomata occurring

sympatrically with North American material of L.

bicolor, and material from the southeastern Unit-

ed States with pinkish flesh-colored lamellae was

treated as L. trichodermophora (Mueller & Gardes,

1991).

Laccaria bicolor is one of the most common

Laccaria taxa found in the coniferous forests of

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

59

FIG. 36. Basidiomata of L. nobilis (GMM 2048).

FIG. 37. Somatic culture mats of L. nobilis (GMM 1 205). Top on PDA, left on MMN, and right

on MEA. Photo taken during week 4.

60

FIELDIANA: BOTANY

FIG. 38. Micromorphological features of L. nobilis (GMM 2048): a, basidiospores; b, basidia. Scale line = 10

western North America and the Great Lakes area.

Collections of L. bicolor sensu stricto were not en-

countered from the southeastern United States.

Material of L. bicolor sensu lato from the north-

eastern United States or Atlantic provinces of

Canada, although frequently encountered, was not

available to include in the studies of Mueller and

Gardes (1991). Consequently, the occurrence and

distribution of these three species in that area are

unknown, and collections of L. bicolor sensu lato

from this region have been treated as L. bicolor

in this monograph.

Isolates of L. bicolor are very frequently used in

applied studies on ectomycorrhizae (Kropp &

Langlois, 1990).

Laccaria nobilis Smith apud G. M. Mueller. Fig-

ures 36-38, 56d,e, 67c.

Laccaria nobilis Smith apud G. M. Mueller, Myco-

taxon 20: 105-108. 1984. [Laccaria nobilis Smith,

nom. herb.]. TYPE: USA, Colorado, Larimer Co.,

Roosevelt National Forest, Rayah Wilderness,

Blue Lake Trail, 13 September 1981, G. M.

Mueller 1198 (TENN 42527) (TENN!, holotype).

MACROMORPHOLOGY— Pileus 16-85 mm broad,

convex to plane, occasionally becoming uplifted,

depressed to deeply depressed, not striate, fibril-

lose-scaly becoming scaly to squarrose, reddish

brown (8C7-8D7) to brownish orange ("Sanford's

Brown" or "Cinnamon-Rufous") 6C7, 7C6-7D7),

occasionally darker at disc ("Hazel"); margin in-

curved, decurved or plane, occasionally upturned,

entire to eroded; context thin, concolorous with

lamellae. Lamellae sinuate to adnate, close to dis-

tant, thick, vinaceous (8B2-9B3) to pinkish flesh

color ("Flesh Color," "Pale Flesh Color," or "Or-

ange-Pink") (7A2-7A3). Stipe (21-)26-110(-160)

x 4-10(-16) mm, equal, slightly bulbous or sub-

clavate, dry, fibrillose, with prominent longitudi-

nal striations or reticulate ridges, often with apical

recurved scales at maturity, concolorous with pi-

leus; striations concolorous with stipe ground col-

or or somewhat darker reddish brown. Basal my-

celium violet, soon becoming white. Basidiospores

white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered fascicles of ± perpendicular

hyphae; fascicles composed of 1 5-30 or more hy-

phae; terminal cells of fascicular hyphae 34.5-75

x 4-19 nm, subclavate, clavate, broadly clavate

or capitate; walls up to 0.5 fj.m thick, light yellow-

ish brown; contents hyaline to light yellowish

brown. Pileus trama tightly interwoven, morpho-

logically undifferentiated, hyaline, light yellowish

brown toward pileipellis. Lamellar trama parallel;

hyphae mostly 3-10 nm diam., thin- walled, hya-

line to light yellowish brown; cells barrel-shaped.

Subhymenium morphologically undifferentiated.

Basidia 32-55 x 8-14 /mi, clavate, hyaline; ste-

rigmata 4, up to 9 nm long. Cheilocystidia lacking.

Basidiospores (excluding ornamentation) [ 1 22/8]

(6.2-)6.6-9.7(-10.6) x (5-)6.2-8.7 /mi (x = [7-]

7.4-8.8 x [6-]6. 3-7.8 /mi), (? = 1-1.26(-1.39)(C

= [1.03-11.16-1.22), subglobose to broadly ellip-

soid, occasionally globose or ellipsoid, hyaline,

echinulate; echinulae 0.5-1.4 /*m long (x = 0.9 ±

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

61

FIG. 39. Basidiomata of L. trullissata (GMM 3048).

FIG. 40. Habitat view of L. trullissata (GMM 3048) illustrating typical growth in sand.

62

FIELDIANA: BOTANY

FIG. 4 1 . Micromorphological features of L. trullissata (GMM 1 9 1 4): a, basidiospores; b, basidia. Scale line = 1 0 nm.

0.2 /xm), crowded; hilar appendix 1.3-2 nm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 2-12 nm diam., tightly interwoven, hya-

line; cells filamentous to barrel-shaped.

SOMATIC CULTURE MAT MORPHOLOGY (N = 2;

Appendix B)— PDA: Radius at week 3 = 23-31

mm, week 6 = 35-43 mm; mat felty, thick, tightly

interwoven, almost crustose, tightly appressed to

agar surface, with time forming pruinose aerial

layer away from plug, not translucent, at first bright

violet, by week 6 violet color restricted to a 7-9

mm band near margin, rest of mat light orange-

brown; pruinose aerial hyphae light grayish purple

becoming light orange-brown; margin 3—4 mm

broad, subfelty, thin, uneven, light violet to white,

plug concolorous with mat; hyphae morphologi-

cally undifferentiated, occasionally irregularly

swollen, purplish brown in mass. MMN: Radius

at week 3 = 40-47 mm, week 6 = 67-78 mm; mat

subfelty, thin, slightly thicker with age, loosely to

tightly interwoven, tightly appressed to agar sur-

face, translucent, light violet, in time color re-

stricted to 3-4 mm band at midpoint, remainder

of mat white; margin 3-6 mm broad, silky to

subfelty, thin, parallel to loosely interwoven, en-

tire, light violet to white; plug concolorous with

mat; hyphae morphologically undifferentiated,

rarely irregularly swollen near margin. MEA: Ra-

dius at week 3 = 33-47 mm, week 6 = 47-77 mm;

mat subfelty, thin to slightly thicker near plug,

loosely interwoven, tightly appressed to agar sur-

face, translucent, white; margin 1-2 mm broad,

subfelty, thinner than mat, undulate; hyphae mor-

phologically undifferentiated.

HABITAT AND DISTRIBUTION— Solitary to scat-

tered. Infrequently encountered under Pinaceae in

western North America and areas adjacent to the

Great Lakes. A list of specimens examined is pre-

sented in Appendix A.

OBSERVATIONS— Laccaria nobilis can be distin-

guished easily from other members of the L. bi-

color complex by its large size, scaly to squarrose

pileus, scaly stipe, and lack of obvious cheilocys-

tidia. A. H. Smith proposed the name in an un-

published manuscript along with several other taxa,

including L. pisciodorus nom. prov. (Smith no.

18812) and L. sphagnicola nom. prov. (Smith no.

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

63

4573). The latter two taxa were not judged suffi-

ciently distinct, based on available material, to

justify valid publication as discrete taxa.

The concept of L. nobilis used here has been

broadened from that originally published by

Mueller (1984, 1985). Interpretation of lamellae

and basal mycelium colors was difficult in many

of the collections included in the original descrip-

tion because the specimens were mature and

weathered. Additional material was collected sub-

sequently that differed from the original collec-

tions in having vinaceous lamellae and violet my-

celium at the base of the stipe. Because all of these

collections had large, robust basidiomata that be-

came quite scaly in age, strongly striate to nearly

reticulate stipes, and similar micromorphology and

somatic culture mat morphology, they were treat-

ed as a single taxon, L. nobilis. Isolates of more

recently collected specimens were included among

the material studied by Mueller and Gardes (1991).

Laccaria nobilis is well delimited from L. bicolor

and L. trichodermophora based on intercollection

pairing studies, phenetic analyses, and analyses of

mtDNA and rDNA RFLPs (Mueller & Gardes,

1991) (see Observations under L. bicolor).

Laccaria nobilis has been identified among ma-

terial collected throughout much of western North

America (e.g., California, Colorado, Idaho, New

Mexico, Oregon, and Washington) and from

Michigan and Ontario.

Laccaria trullissata (Ellis) Peck. Figures 39-41,

57b-d, 72d.

= Agaricus trullissatus Ellis, Bull. Torrey Hot. Club 5:

45. 1874. TYPE: USA, New Jersey, Newfield, no

date, Ellis s. n. (NYS!, lectotype./afe Mueller, 1 987).

= Clitocybe trullissata (Ellis) Saccardo, Syll. Fung. 5:

195. 1887.

= Laccaria trullissata (Ellis) Peck, Annual Rep. New

York State Bot. 157: 90. 1912.

MACROMORPHOLOGY— Pileus 17-72 mm broad,

convex to plane, occasionally depressed, not stri-

ate, fibrillose to fibrillose-scaly, grayish purple when

very young (near 1 7B4), soon becoming red-brown,

brown or buff ("Fawn Color," "Avellaneous,"

"Vinaceous-Buff," "Pale Vinaceous-Fawn," or

"Pinkish Buff') (6A4-5, 6B6, 7D7 or 7E5-7); mar-

gin incurved to decurved, entire to eroded; context

tapering to margin, pale purple (near "Light Vi-

naceous-Gray"). Lamellae adnate to arcuate, close

to subdistant, narrow to moderately broad, thick,

waxy appearing, dark violaceous ("Dark Helio-

trope Gray" or "Deep Vinaceous-Gray"). Stipe

40-93 x 6-23 mm, subclavate to clavate, dry,

fibrillose, longitudinally striate, covered with sand,

occasionally with outer "cortical" layer splitting

near apex, concolorous with pileus; context solid,

concolorous with pileus context. Basal mycelium

violaceous. Basidiospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with widely scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-25

hyphae; terminal cells 33.5-85 x 7-16 /on, sub-

clavate, clavate, broadly clavate or capitate, walls

up to 0.5 A*rn thick, light yellowish brown; contents

hyaline to light yellowish brown. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel; hyphae mostly

3-17 /urn diam., hyaline, light yellowish brown or

light vinaceous color; cells barrel-shaped. Sub-

hymenium morphologically undifferentiated. Ba-

sidia 30-64.5 x 9-16 fim, clavate, hyaline; ste-

rigmata 4, up to 10 nm long. Cheilocystidia lacking

or very scarce and filamentous. Basidiospores [757

5](13.3-)13.8-20.2(-21.6) x 5.5-8.3Mm(jt = 15.3-

17.3 x 6-7. 3 Mm), Q=\. 83-3.3 \(Q = 2.37-2.51),

subfusiform to fusiform-ellipsoid, hyaline, very

finely roughened, not echinulate; hilar appendix

1.3-2 nm long, prominent, truncate; contents oc-

casionally uniguttulate, rarely biguttulate. Basal

mycelium hyphae 3-15.5 nm diam., tightly inter-

woven, hyaline; cells filamentous or barrel-shaped.

HABITAT AND DISTRIBUTION— Solitary to scat-

tered; sand dunes or very sandy soil; usually as-

sociated with species of Pinus, eastern and mid-

western North America. A list of specimens

examined is provided in Appendix A.

OBSERVATIONS— Laccaria trullissata is distin-

guished from other North American Laccaria taxa

by its habitat, macromorphology, and basidio-

spore characteristics. Collections of Laccaria ma-

ritima differ from those of L. trullissata in having

shorter, less elongate, echinulate basidiospores.

Ectomycorrhizae were synthesized between one

isolate of L. trullissata and seedlings of Pinus re-

sinosa Ait. (unpubl. data). Intrastock pairings

demonstrated that L. trullissata has a bifactorial

compatibility system as do all other tested Lac-

caria.

Laccaria trullissata occurs in sandy areas along

the eastern coast of North America, ranging from

the Maritime Provinces of Canada to North and

South Carolina along the Atlantic coast and Flor-

ida to Mississippi along the Gulf of Mexico. It can

be encountered also in northcentral United States

64

FIELDIANA: BOTANY

FIG. 42.

10 /urn.

Micromorphological features of L. maritima (DAOM 159709): a, basidiospores; b, basidia. Scale line =

and southcentral Canada in sand dunes along the

Great lakes.

Laccaria maritima (Teodorowicz) Singer ex Huh-

tinen. Figures 42, 57a.

= Hygrophorus maritimus Teodorowicz, Grzyby

wyzsze polskiego wybrzeza, Towarzystwo nau-

kowe w Toruniu Badania Przyrodnicze Pomor-

skie 2: 31. 1936. TYPE: Fig. 5 in Teodorowicz,

Grzyby wyzsze polskiego wybrzeza, Towarzystwo

naukowe w Toruniu Badania Przyrodnicze Po-

morskie 2: 31. 1936. (lectotype fide Mueller,

199 la).

= Laccaria trullissata (Ellis) Peck subsp. maritima

(Teod.) Andersson, Bot. Not. Suppl. 2: 33. 1950.

= Laccaria maritima (Teodorowicz) Singer, Sydowia

15: 133. 1961. [not validly published, basionym

lacking].

= Laccaria maritima (Teodorowicz) Singer ex Huh-

tinen, Fungi Canad. 319. 1987.

= Laccaria trullissata (Ellis) Peck forma rugulospora M.

Lange, Meddel. Grenland 147: 30. 1955.

MACROMORPHOLOGY— Pileus up to 45 mm

broad, convex to plane, becoming uplifted, often

depressed, nonstriate or translucent-striate when

fresh, glabrous to finely fibrillose, slightly viscid,

hygrophanous, dark reddish brown to reddish or-

ange-brown. Lamellae adnate to subdecurrent,

distant, thick, broad, pinkish flesh color to vina-

ceous. Stipe large and robust, equal to clavate, dry,

mostly covered with sand, concolorous with pi-

leus. Basal mycelium off-white, hard to determine

because of adhering sand. Basidiospores white in

mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered ± perpendicular individual

hyphae or fascicles of hyphae, terminal cells of

hyphae 35-55 x 4—10 /ttm, hyaline. Basidia 37-

60 x 9-15.5 urn, clavate, 4-sterigmate. Cheilo-

cystidia none seen. Basidiospores (excluding or-

namentation) [105/4] (10-) 11. 5-1 7(-l 9.5) x (5.5-)

7.5-9.5(-10) urn (x = 13.3-15.4 x 8-8.5 fim), Q

= 1.43-2(-2.17) (Q = 1.67-1.81), oblong to

subfusiform, echinulate; echinulae 0.2-0.5 ^m long.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious; terrestrial, in sand including dunes; with

or without apparent ectomycorrhizal associate.

Only reported from a few sites in eastern Canada.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

65

FIG. 43. Basidiomata of L. ochropurpurea (GMM 919). Largest pileus = 8 cm diam.

FIG. 44. Somatic culture mats of L. ochropurpurea (GMM 1015). Top on PDA, left on MMN,

and right on MEA. Photo taken during week 4.

66

FIELDIANA: BOTANY

FIG. 45. Micromorphological features of L. ochropurpurea (E. Harwell 5074): a, basidiospores; b, basidia; c,

cheilocystidia. Scale line = 10 urn.

Known primarily from northern Europe. A list of

specimens examined is presented in Appendix A.

OBSERVATIONS— Laccaria maritima is charac-

terized by its restricted habitat, dark reddish brown

pileus color, vinaceous-tinged lamellae, stipe bur-

ied in sand, and elongate, finely echinulate basid-

iospores. Collections of L. trullissata have larger

basidiomata with deep violet lamellae and larger,

more elongate (mostly 14-21.5 x 5. 5-9 ^m), finely

roughened, not echinulate basidiospores.

It has not yet been possible to obtain a tissue

culture or germinate the basidiospores of this tax-

on. Lack of cultures has prevented attempts at in

vitro ectomycorrhizal synthesis to determine the

ability of this taxon to form ectomycorrhizae with

putative hosts.

This species has been reported from both coastal

and inland dunes of northern Europe, the Neth-

erlands, and Greenland (e.g., Teodorowicz, 1936;

Andersson, 1950; Lange, 1955; Singer, 1961; Kal-

lio & Heikkila, 1963; Holland, 1976; Vellinga,

1982). Huhtinen (1987) reports it for the first time

from North America, where L. trullissata is found

much more commonly in sand dunes than Lac-

caria maritima.

Laccaria ochropurpurea (Berkeley) Peck. Figures

43-45, 58d, 68a.

= Agaricus ochropurpureus Berkeley, London J. Bot.

4: 299-300. 1845. TYPE: USA, Ohio, Cincinnati,

no date, Lea 261 (K.!, holotype).

= Clitocybe ochropurpurea (Berkeley) Saccardo, Syll.

Fung. 5: 148. 1887.

= Laccaria ochropurpurea (Berkeley) Peck, Annual

Rep. New York State Bot. 1 16: 41. 1907.

= Clitocybe laccata f. major Bresadola, Ann. Mycol.

18:65. 1920.

MACROMORPHOLOGY— Pileus 35-100(-125)mm

broad, obtuse, convex, plane or uplifted, often de-

pressed, not striate, dry, subglabrous, finely fi-

brillose or occasionally fibrillose-scaly, light vio-

laceous brown to buff color, often with violaceous

tints in young, fresh specimens (" Vinaceous-Buff,"

"Pale Vinaceous-Fawn," or "Pinkish Buff"); mar-

gin inrolled, decurved, plane or uplifted, entire,

slightly undulate, eroded or rimose; context ^ 9

mm thick at disc, tapering to margin, violaceous

buff. Lamellae sinuate, arcuate or subdecurrent,

close to distant, narrow to broad, thick, waxy-

appearing, dark purple ("Dark Heliotrope Gray"

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

67

FIG. 46. Basidiomata of L. amethysteo-occidentalis (GMM 1256).

or "Deep Vinaceous-Gray"). Stipe (1 5-)45-l 90 x

(2-)6-22(-36) mm, equal, subclavate, clavate or

slightly bulbous, dry, coarsely fibrillose; fibrils

forming longitudinal striations, recurved scales or

both, at times forming reticulations at maturity;

ground color concolorous with pileus; striations

brownish to reddish brown. Basal mycelium scant

to copious, violet. Basidiospores light violaceous

or white in mass.

MICROMORPHOLOGY— Pileipellis of tightly in-

terwoven hyphae with occasional widely scattered

± perpendicular individual hyphae, not fascicu-

late; terminal cells 24-66.5 x 4-10 Mm, filamen-

tous or barrel-shaped, olive brown in mass; walls

up to 0.5 Mm thick, olive brown; contents hyaline,

light olive brown or light yellowish brown. Pileus

trama tightly interwoven, morphologically undif-

ferentiated, hyaline, light yellowish brown to olive

brown toward pileipellis. Lamellar trama parallel;

hyphae mostly 3-1 1.5 /mi diam., thin-walled, hy-

aline to light yellowish brown; cells barrel-shaped.

Subhymenium morphologically undifferentiated.

Basidia 33-61 x 7-1 1.5 Mm, clavate, hyaline; ste-

rigmata (2-)4, up to 8 Mm long. Cheilocystidia 23-

63.5 x 2.3-8.9 Mm, filamentous, subclavate or

subcapitate, abundant, thin-walled, hyaline. Ba-

sidiospores (excluding ornamentation) [60/4]

(6.4-)7-9.2(-l 1) x (6.4-)7-8.7(-9.7)Mm (Jc = 7.9-

8.4 x 7.4-8.1 Mm), Q = (0.93-)1-1.13(-1.16) (Q

= 1.02-1.06), globose to subglobose, hyaline,

echinulate; echinulae 0.9-1 .4(-2.3) /um long, 1-1 .5

Mm wide at base, crowded; hilar appendix 1.3-2

Mm long, prominent, truncate; plage present; con-

tents occasionally uniguttulate. Basal mycelium

hyphae mostly 3.5-10.5 Mm diam., tightly inter-

woven, filamentous, hyaline.

SOMATIC CULTURE MAT MORPHOLOGY (N = 3;

Appendix B)— PDA: Radius at week 3 = 5-11

mm, week 6 = 7-23 mm; mat felty, thick, tightly

interwoven, tightly appressed to agar surface, in

time forming pruinose aerial layer away from plug,

not translucent, at first bright violet, by week 6

violet coloration restricted to 2-3 mm band near

margin, short aerial hyphae light grayish violet;

margin 1-3 mm broad, thin, silky, becoming

subfelty, even to uneven, light violet to white; plug

often covered with white cottony hyphae, bright

violet; hyphae morphologically undifferentiated,

olivaceous brown in mass. MMN: Radius at week

3 = 11-19 mm, week 6 = 23-39 mm; mat silky,

68

FIELDIANA: BOTANY

FIG. 47. Micromorphological features of L. amethysteo-occidentalis (E. Farwell 50 1 5): a, basidiospores; b, basidia;

c, cheilocystidia. Scale line = 10 /um.

subfelty or felty, thin to thick, interwoven, tightly

appressed to agar surface, translucent, light violet,

often with 1-3 concentric darker narrow bands;

margin narrow, subfelty to silky, thin, entire to

sulcate, light violet; plug concolorous with mat;

hyphae morphologically undifferentiated. MEA:

Radius at week 3 = 6-17 mm, week 6 = 10-33

mm; mat subfelty to felty, rarely silky, thin to

thick, interwoven, tightly appressed to agar sur-

face, translucent, white; margin not well differ-

entiated, narrow, silky to subfelty, thin, even to

undulate, white; plug white; hyphae morphologi-

cally undifferentiated.

HABITAT AND DISTRIBUTION— Solitary to scat-

tered, rarely caespitose, commonly encountered in

temperate deciduous forests of eastern North

America, probably in association with Quercus and

Fagus. Not reported from other continents. A list

of specimens examined is provided in Appen-

dix A.

OBSERVATIONS— Laccaria ochropurpurea can be

distinguished easily from all other Laccaria taxa

by its large size, light violaceous brown to buff

colored pileus and stipe, dark purple, thick, waxy

lamellae, and globose to subglobose basidiospores.

The only North American species that could be

confused with it are L. nobilis and faded collec-

tions of L. amethysteo-occidentalis and L. trullis-

sata. These taxa all differ in basidiospore shape

and size. In addition, L. amethysteo-occidentalis

differs in having numerous, large cheilocystidia,

and L. nobilis has reddish brown to orange-brown,

strongly scaly basidiomata. Collections of L. trul-

lissata have elongate, finely roughened basidio-

spores and are restricted to sand or sandy soil with

sand covering much of their stipe and adhering to

their basidiomata.

Culture mat morphology of the five isolates uti-

lized showed the least intraspecific variation of all

the taxa examined. The slow growth rate and dark

purple color on PDA were distinctive (fig. 44).

Laccaria ochropurpurea appears to be restricted

to deciduous-coniferous forests of eastern North

America. Lahaie (1981) reported that it does not

occur in the coniferous boreal forests of eastern

Canada. Several reports of L. ochropurpurea oc-

curring in western North America have been noted

(personal communications and herbarium speci-

mens), but all of the specimens investigated during

this study appeared to be either L. amethysteo-

occidentalis or L. nobilis.

Laccaria amethysteo-occidentalis G. M. Mueller.

Figures 46, 47, 58a, 59d.

Laccaria amethysteo-occidentalis G. M. Mueller, My-

cotaxon 20: 103-105. 1984. TYPE: Canada, Brit-

ish Columbia, near Squamish, Alice Lake Prov.

Park campground, 3 October 1 98 1 , G. M. Mueller

1256 (TENN 42526) (TENN!, holotype).

MACROMORPHOLOGY— Pileus 10-65(-89) mm

broad, obtuse, convex or plane, often depressed,

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

69

not striate when fresh, occasionally becoming

slightly translucent-striate upon fading, finely fi-

brillose, fibrillose, or fibrillose-scaly, hygropha-

nous, deep purple when fresh ("Taupe Brown,"

"Dull Indian Purple," "Dusky Dull Violet 1,"

"Dark Hyssop Violet," or "Slate- Violet"), fading

to vinaceous ("Dark Vinaceous-Drab," "Dark Vi-

naceous-Gray," or near "Wood Brown"), finally

buff color (near "Pale Ochraceous-Salmon"); mar-

gin inrolled, decurved, or plane, entire to eroded;

context thin, concolorous with pileus ("Dark Slate-

Violet") with lighter gray purple to white areas

intermixed ("Pale Bluish Lavend.er"). Lamellae

sinuate to arcuate, subdistant to distant, narrow

to broad, thick, occasionally waxy appearing, dark

violaceous ("Deep Slate Violet" to "Slate- Vio-

let"), fading (near "Lavender"). Stipe 18-115 x

3-12 mm, equal, subclavate or slightly bulbose,

dry, strongly longitudinally striate, occasionally

with recurved scales, purple ("Dark Slate Purple,"

"Dark Vinaceous Brown," or "Hay's Brown"), of-

ten with lighter violet or white scattered sectors

("Pale Bluish Lavender"); context solid, concol-

orous with pileus context. Basal mycelium violet

("Dark Slate-Purple," "Deep Slate-Violet," or

"Light Dull Bluish Violet"). Basidiospores white

in mass.

MICROMORPHOLOGY— Pileipellis of tightly in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae, fascicles composed of 1 5-30

hyphae; terminal cells of fascicular hyphae 28-

73.5 x 7-16 Mm, filamentous, clavate or broadly

clavate; walls up to 0.5 Mm thick, vinaceous brown;

contents hyaline to light vinaceous brown. Pileus

trama tightly interwoven, morphologically undif-

ferentiated, hyaline, light vinaceous brown toward

pileipellis. Lamellar trama parallel; hyphae mostly

3-1 1.5 /xm diam., thin-walled, hyaline to light vi-

naceous brown; cells barrel-shaped. Subh ymenium

morphologically undifferentiated. Basidia 34-56

x 10-14.5 nm, clavate, hyaline, in young speci-

mens vinaceous brown in mass; sterigmata 4, up

to 9 Mm long. Cheilocystidia 36.5-66.5 x 12-18.5

Mm, subclavate to clavate, often abundant, thin-

walled, hyaline. Basidiospores (excluding orna-

mentation) [81/6] 7.8-10.6 x 7-9.2 Mm (jc =9-9.8

x 7.4-8.6 Mm), Q = (1-)1.06-1.24(-1.36) (Q =

1.13-1.19), subglobose to broadly ellipsoid, rarely

globose or ellipsoid, echinulate; echinulae 0.5-1.4

(-1.8) Mm long, < 1 Mm wide at base, crowded,

hilar appendix 1.3-2 Mm long, prominent, trun-

cate; plage present; contents occasionally unigut-

tulate. Basal mycelium hyphae mostly 2.5-8 Mm

diam., hyaline, morphologically undifferentiated.

SOMATIC CULTURE MAT MORPHOLOGY (N = 1 ;

GMM 1256)— PDA: Radius at week 3 < 3 mm,

week 6 = 12-14 mm; mat felty, thick, tightly in-

terwoven, tightly appressed to agar surface, not

translucent, dark violet; margin up to 3 mm broad,

subfelty, abruptly thinner than mat, entire, light

violet; plug dark violet; hyphae mostly morpho-

logically undifferentiated, occasionally subcoral-

loid. MMN: Radius at week 3 = 14-22 mm, week

6 = 24-32 mm; mat felty, thick, tightly interwo-

ven, thicker near plug, tightly appressed to agar

surface, not translucent, moderate violet, darker

near plug, lighter colored away from plug; margin

1-2 mm broad, subfelty to silky, not well differ-

entiated from mat, even to serrate, light violet;

plug moderate violet; hyphae same as in PDA.

ME A: Radius at week 3 = 14-17 mm, week 6 =

23-27 mm; mat subfelty, thick, interwoven with

a narrow (3 mm) thicker band at midpoint, tightly

appressed to agar surface, translucent, white; mar-

gin 1-2 mm broad, subfelty, not well differenti-

ated, entire to somewhat serrate, white; plug white;

hyphae morphologically undifferentiated.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious; under conifers (often Pseudotsuga men-

ziesii (Mirb.) Franco) in western North America.

A list of specimens examined is presented in Ap-

pendix A.

OBSERVATIONS — Lace aria a methysteo- occiden -

tails can be distinguished easily from the other

two "purple" Laccaria taxa found in North Amer-

ica, L. amethystina and L. vinaceobrunnea, by its

large size and deeper purple coloration of fresh

basidiomata. Additionally, L. amethysteo-occi-

dentalis differs from L. amethystina in having

nonglobose, more finely echinulate basidiospores

and from L. vinaceobrunnea in the arrangement

of the hyphae composing the pileipellis. All three

taxa have large cheilocystidia that form a sub-

sterile layer along the lamellar margin. This char-

acter can be used in many cases to separate her-

barium material of L. amethysteo-occidentalis from

L. nobilis.

Homokaryotic isolates of this taxon were inter-

sterile with isolates of other tested taxa, including

L. amethystina and L. vinaceobrunnea.

The above description of culture mat morphol-

ogy was based on a single isolate, even though

numerous attempts were made to culture from

basidiomata of this species. The slow rate of growth

and dark purple color of the culture mat on PDA

were similar to that exhibited by cultures of L.

ochropurpurea.

Laccaria amethysteo-occidentalis can be found

70

FIELDIANA: BOTANY

commonly in the coniferous forests of northwest-

ern United States and western Canada. In contrast,

L. amethystina appears to be restricted to the tem-

perate deciduous or mixed coniferous-deciduous

forests in eastern North America and Europe and

the tropical Quercus forests of Central America

and Colombia.

Laccaria amethystina Cooke. Figures 48, 49, 58b,

60a.

= Agaricus amethystinus Hudson, Fl. angl. 2: 612.

1 778; non Agaricus amethystinus Scopoli, Fl. earn.

2: 437. 1772 [= Cortinarius sp.]; nee Agaricus

amethystinus Schaeffer, Fung. Bavar. Palat. nasc.

4: 24. 1774 [= Cortinarius traganus}. TYPE: En-

gland, Devon, Dartmoor, Two Bridges, Whist-

mans Wood, 6 September 1971, D. N. Pegler s.n,

(as L. amethystea) (K!, neotype fide Mueller &

Vellinga, 1990).

= Laccaria amethystina Cooke, Grevillea 12: 70. 1884.

= Collybia amethystina (Cooke) Quelet, Fl. mycol.

France: 237. 1888.

= Clitocybe amethystina (Cooke) Peck, Annual Rep.

New York State Bot. 50: 128. 1897.

= Agaricus amethysteus Bulliard, Herb. France: pi. 198.

1784. [= A. laccatus Schaeff., Fung. Bavar. Palat.

nasc. 4: 8. 1774].

= Omphalia amethystea (Bulliard) S. F. Gray, Nat.

Arr. Brit. PI. 1: 614. 1821.

= Agaricus laccatus var. amethysteus (Bulliard) Berke-

ley & Broome, J. Linn. Soc., Bot. 1 1: 518. 1871.

= Russuliopsis laccata var. amethystea (Bulliard) J.

Schroeter in Cohn, Krypt.-Fl. Schlesien 3(1): 623.

1889. [erroneously written ''amethystina].

= Laccaria amethystea (Bulliard) Murrill, N. Amer.

Fl. 10: 1. 1914.

= Laccaria calospora Singer, Beih. Sydowia 7: 7. 1973.

MACROMORPHOLOGY— Pileus 5-32(-53) mm

broad, convex to plane, often depressed, not striate

or striate, occasionally translucent-striate when

fresh, finely pruinose to fibrillose, occasionally be-

coming finely fibrillose-scaly, strongly hygropha-

nous, bright grayish purple when fresh (near "He-

liotrope-Slate" or "Dark Slate- Violet 1"), fading

to buff ("Vinaceous-Gray," "Pale Ochraceous-

Buff," or "Light Buff'); margin inrolled to de-

curved, entire to undulate, occasionally eroded;

context up to 3 mm thick at disc, tapering to mar-

gin, concolorous with surface. Lamellae sinuate to

arcuate, subdistant to distant, up to 5 mm broad,

thick, subconcolorous with pileus ("Heliotrope-

Slate" or "Vinaceous-Drab"). Stipe 6-58(-70) x

1-7 mm, equal, subclavate or slightly bulbous,

dry, fibrillose, longitudinally striate, concolorous

with pileus. Basal mycelium hygrophanous, violet

becoming white. Basidiospores white or very pale

violet in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with scattered fascicles of ± perpendicular

hyphae or with scattered individual ± perpendic-

ular hyphae; fascicles composed of 1 0-20 hyphae;

terminal cells of perpendicular hyphae 23-73.5 x

6.5-17 Mm, filamentous, clavate, broadly clavate,

capitate or ventricose-rostrate, walls up to 0.5 Mm

thick, vinaceous brown in young specimens, light

yellowish brown in mature specimens; contents

concolorous with hyphal walls. Pileus trama tight-

ly interwoven, morphologically undifferentiated,

hyaline, light yellowish brown or vinaceous brown.

Lamellar trama parallel to subparallel; hyphae

mostly 3.5-16 /mi diam., thin-walled hyaline to

light yellowish brown or vinaceous brown; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia 30-64.5 x 8.5-14 Mm,

clavate, hyaline; sterigmata (2-)4, up to 10 /mi

long. Cheilocystidia 25.5-64(-92) x 4-12 /mi, fil-

amentous, clavate, broadly clavate or ventricose-

rostrate, abundant, thin-walled hyaline. Basidio-

spores (excluding ornamentation) [160/11] 7-10

(-10.6) x (6.4-)7-10(-10.6) /mi (x = 7.7-9 x 7.7-

9 /tm), Q = 1-1.07(-1.12) (Q = 1-1.02), globose,

rarely subglobose, hyaline, echinulate; echinulae

1.4-2.8 Mm long, > 1.2 Mm wide at base; hilar

appendix 1.3-2 Mm, prominent, truncate; plage

present; contents occasionally uniguttulate. Basal

mycelium hyphae mostly 3-12 Mm diam., tightly

interwoven, hyaline; cells filamentous to barrel-

shaped.

HABITAT AND DISTRIBUTION— Solitary to scat-

tered, occasionally caespitose; associated with

Quercus and Fagus in temperate deciduous or

mixed deciduous-coniferous forests of eastern

North America and Europe, under species of Quer-

cus in Central America and northern South Amer-

ica.

OBSERVATIONS— Laccaria amethystina can be

distinguished from the other North American

"purple" Laccaria (L. amethysteo-occidentalis and

L. vinaceobrunnea) by its small size and stature,

bright grayish purple basidiomata that fade di-

rectly to buff, and globose, coarsely echinulate ba-

sidiospores.

No tissue cultures of L. amethystina were ob-

tained during this study. Homokaryotic and re-

constituted dikaryotic isolates were violet on MMN

and PDA and grew moderately fast (radius at week

6 = ± 50 mm).

Homokaryotic isolates of L. amethystina were

intersterile with isolates of other taxa, including

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

71

FIG. 48. Basidiomata of L. amethystina (GMM 1718).

L. amethysteo-occidentalis and L. vinaceobrun-

nea. One North American isolate and one Swedish

isolate of L. amethystina were included in RFLP

analyses (Gardes et al., 1990, 199 la). These two

isolates had different RFLP patterns, indicating

that genetic divergence may have occurred be-

tween North American and Swedish populations

of L. amethystina. However, the amount of intra-

population variation is not known because only

one isolate was examined from each population.

Mueller and Vellinga (1986,1990) discussed the

controversy that has persisted in the literature as

to the correct name for this taxon. Most workers

use the name L. amethystina; however, Murrill

(1914), Dennis et al. (1960), and others have used

L. amethystea (Bulliard) Murrill for this species.

Cooke's name is the earliest valid name for the

taxon.

Laccaria gomezii Singer & G. M. Mueller

(Mueller & Singer, 1 988) grows sympatrically with

L. amethystina in Costa Rica and Colombia. Col-

lections of L. gomezii are characterized by having

purple basidiomata that quickly turn vinaceous

brown and then brown; adnate to decurrent, close

to crowded, thin lamellae; and subglobose to el-

lipsoid basidiospores.

Laccaria amethystina appears to be restricted

to temperate deciduous or mixed coniferous-de-

ciduous forests in eastern North America and Eu-

rope and to Neotropical Quercus forests in Central

America and Colombia. Lahaie (198 1) did not re-

port material of L. amethystina from boreal co-

niferous forests in Canada. Mueller (199 la) re-

ported collections of this taxon from southern

Sweden.

Laccaria vinaceobrunnea G. M. Mueller. Figures

50-52, 58c, 73c.

Laccaria vinaceobrunnea G. M. Mueller, Mycotaxon

20: 114-115. 1984. TYPE: USA, Louisiana,

Tammany Parish, Fountainbleu State Park, un-

der Quercus virginiana, 9 December 1980, G. M.

Mueller 1120 (TENN 42525) (TENN!, holotype).

MACROMORPHOLOGY— Pileus 7-25(-42) mm

broad, obtuse to convex, becoming plane to up-

72

FIELDIANA: BOTANY

FIG. 49. Micromorphological features of L. amethystina (GMM 2237): a. basidiospores; b, basidia; c, cheilocystidia.

Scale line = 10 /on.

lifted, often depressed, not striate or finely striate

when wet, finely fibrillose, occasionally finely fi-

brillose-scaly, hygrophanous, when immature vi-

olaceous (near "Purplish Lilac"), becoming vi-

naceous (Dark Vinaceous-Brown," "Hay's

Brown," or "Vinaceous-Brown"), reddish brown

("Cameo Brown" to "Walnut Brown") then fading

to orange-brown or buff ("Cinnamon-Rufous" to

"Light Ochraceous-Buff'); margin decurved to

plane, entire to eroded; context thin, tapering to

margin, light vinaceous ("Light Brownish Vina-

ceous" to near "Vinaceous-Fawn"). Lamellae ad-

nate to arcuate, subdistant to distant, broad, thick,

waxy, purple ("Purplish Lilac" or "Purplish Vi-

naceous"). Stipe 7-56(-98) x 2-7 mm, equal, sub-

clavate or slightly bulbous, dry, fibrillose, occa-

sionally with recurved fibrils or finely striate,

concolorous with pileus; fibrils ("Hazel" or "Vi-

naceous-Brown"). Basal mycelium violet. Basid-

iospores white in mass.

MICROMORPHOLOGY— Pileipellis of interwoven

hyphae with very numerous ± perpendicular hy-

phae; terminal cells 32-78 x 7-14.5 /mi, filamen-

tous to clavate, hyaline to light vinaceous; walls

up to 0.5 nm thick; contents hyaline. Pileus tram a

tightly interwoven, morphologically undifferen-

tiated, hyaline to light olive brown in mass. La-

mellar trama parallel; hyphae thin-walled, hyaline;

cells barrel-shaped. Subhymenium morphologi-

cally undifferentiated. Basidia 33-60 x 8.5-9 urn,

clavate, hyaline; sterigmata 4, up to 9 /im long.

Cheilocystidia 31.5-92 x 5.5-1 1 /mi, filamentous

to clavate, abundant, hyaline. Basidiospores (ex-

cluding ornamentation) [60/4] (7-)7.4-10(-10.6)

x 6.4-9.2(-9.7) (x = 8.2-8.9 x 7.3-8.3 /im), Q =

1-1.26 «2 = 1.07-1.15), subglobose to broadly

ellipsoid, occasionally globose, hyaline, echinu-

late; echinulae 0.5-1.8 /mi long, < 1 /mi wide at

base; hilar appendix 1.3-1.8 /mi long, prominent,

truncate; plage present; contents occasionally uni-

guttulate. Basal mycelium hyphae mostly 3-8 mm

diam., filamentous, tightly interwoven, hyaline.

HABITAT AND DISTRIBUTION— Scattered to gre-

garious, often caespitose. Growing in sandy soil

under Quercus virginiana Miller along the Gulf

Coast. A list of specimens examined is provided

in Appendix A.

OBSERVATIONS— Laccaria vinaceobrunnea can

be distinguished from L. amethystina and L. ame-

thysteo-occidentalis by habitat, coloration, unique

pileipellis, and subglobose to broadly ellipsoid ba-

sidiospores. The abundant, large cheilocystidia is

a reliable character to use in identifying herbarium

collections that lack notes on macromorphology.

Homokaryotic isolates of L. vinaceobrunnea

were intersterile with tested isolates of other taxa,

including L. amethystina and L. amethysteo-oc-

cidentalis.

Material referable to this taxon has not been

reported from outside of the Gulf Coast area. Al-

though not yet reported, I would expect it to be

found in northeastern Mexico.

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

73

FIG. 50. Basidiomata of L. vinaceobrunnea (GMM 1120).

FIG. 51. Basidiomata of L. vinaceobrunnea (GMM 2337).

74

FIELDIANA: BOTANY

FIG. 52. Micromorphological features of L. vinaceobrunnea (GMM 2335): a, basidiospores; b, basidia; c, cheilo-

cystidia. Scale line = 10 tan.

Tentative Key to Laccaria for the World

The concepts for extralimital taxa included in the following key are based on an examination of type

specimens and descriptions and a review of the literature. Only those taxa that I tentatively recognize

are treated. The key is presented for two reasons: (1) to summarize the delimiting characters of the taxa

involved and (2) to provide a framework that will facilitate further taxonomic work on the genus. It is

not presented as a definitive statement on the genus for the world.

1 . Lamellae gray; Japan 2

1 . Lamellae violaceous, purple, flesh color or pink when fresh 3

2. Basidia bisporic; basidiospores 8-1 1 pm diam., globose, echinulae 2-3 nm long; pileus grayish,

almost black L. nigra Kongo (p. 1 1 1)

2. Basidia tetrasporic; basidiospores 7.5-10 nm diam., globose, verruculose; pileus becoming mouse

gray or subavellaneous L. murina Imai (p. 1 1 1)

3. Lamellae violaceous to purple when young and fresh 4

3. Lamellae flesh color to pinkish when fresh 18

4. Basidiospores large, 13.5-22 x 5.5-9.5 pm, elongate, smooth to finely roughened or finely echin-

ulate (echinulae < 0.5 ^m long); in sand or very sandy soil 5

4. Basidiospores smaller (< 10.5 ^m long), less elongate (Q < 1.51), echinulae > 0.5 nm long; in

sand or not in sand 6

5. Basidiospores elongate (Q = 2.37-2.51), finely roughened, not echinulate; eastern North America

L. trullissata (Ellis) Peck (p. 131)

5. Basidiospores less elongate (Q = 1.67-1.81); echinulae 0.2-0.5 nm long; northern Europe, rare in

eastern North America L. maritima (Teod.) Singer ex Huhtinen (p. 1 07)

6. Lamellae bright violaceous or purple 7

6. Lamellae pallid violaceous to vinaceous when young, fading to vinaceous flesh color 13

7. Pileus bright violaceous, purple or grayish black when young and fresh 8

7. Pileus fawn or buff color, often with violaceous tints 12

8. Pileus fuscous black; lamellae purple to grayish lavender; stipe apex purple, base vinaceous brown;

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

75

FIG. 53. SEMs of basidiospores: a, b, L. proximo (GMM 2 100); c, d, L. oblongospora (GMM 23 10). Note differences

in basidiospore size and shape. Scale lines = 1 urn.

cheilocystidia 30-40 x 2-6.5 /im, filamentous, numerous; New Zealand

L. violaceoniger Stevenson (p. 1 33)

8. Basidiomata and lamellae bright violaceous or purple when young and fresh; cheilocystidia larger

(up to 92 x 12 mm) clavate, numerous 9

9. Basidiospores globose; echinulae > 1 ^m wide at base; basidiomata fading from amethyst to grayish

to buff L. amethystina Cooke (p. 86)

FIG. 54. SEMs of basidiospores: a, L. longipes (A. Parker s.n.); b, L. fraterna (GMM 2126); c, L. montana (GMM

1813); d-f, L. laccata var. pallidifolia (GMM 1845); g, L. pumila (GMM 1956). Note differences in basidiospore size

and shape. Scale lines = 1 /im.

76

FIELDIANA: BOTANY

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

77

FIG. 55. SEMs of basidiospores: a, L. ohiensis (GMM 2354); b, L. striatula (GMM 1944); c-d, L. tortilis (McAdoo

78#28). Note the long and wide echinulae on all basidiospores. Scale lines for a, b, & d = 1 Mm- Scale line for c =

10 ^m.

9. Basidiospores subglobose to broadly ellipsoid; echinulae < 1 pm wide at base; basidiomata fading

from amethyst to brown to buff 10

10. Basidiomata large (pileus 10-90 mm diam.), amethyst becoming vinaceous; pileipellis hyphae

interwoven with scattered fascicles of perpendicular hyphae; western North America; under

conifers L. amethysteo-occidentalis G. M. Mueller (p. 86)

10. Basidiomata smaller (pileus 7-38[-65] mm diam.); amethyst to dark reddish purple, becoming

reddish brown or vinaceous brown at maturity; associated with subtropical or tropical species

of Quercus 11

1 1 . Basidiomata violaceous, becoming vinaceous brown then reddish brown; lamellae adnate to arcuate,

78

FIELDIANA: BOTANY

FIG. 56. SEMs of basidiospores: a, L. bicolor(GMM 2027); b, L. bicolor(GMM 2038); c, L. trichodermophora (GMM

2306); d, e, L. nobilis (GMM 2048). Note relatively small basidiospore size. Scale line = 1 jzm.

subdistant to distant; pileipellis hyphae interwoven with numerous large, individual, perpendicular

hyphae; North America, Gulf Coast states L. vinaceobrunnea G. M. Mueller (p. 133)

1 1 . Basidiomata dark violet purple to dark reddish purple, becoming vinaceous brown; lamellae adnate

to subdecurrent, crowded to close, thin; Costa Rica and Colombia

L. gomezii Singer & G. M. Mueller (p. 99)

1 2. Lamellae dark purple, thick, waxy appearing; basidiomata large (pileus up to 60-1 20 mm diam.),

violaceous buff when young and fresh, becoming buff; eastern North America

L. ochropurpurea (Berk.) Peck (p. 1 14)

1 2. Lamellae lilac; basidiomata smaller, pileus fawn-colored with fulvous fibrils; New Zealand . .

L. lilacina Stevenson (p. 105)

13. Pileus dark purple-brown, fading to light purple-brown; stipes purplish brown at base; western

Europe L. purpureobadia Reid (p. 1 23)

13. Pileus orange-brown, pinkish flesh color, reddish brown, light violaceous, or buff color; stipe ±

concolorous 14

14. Pileus strongly radially fibrillose, buff with vinaceous tints; fibrils dark brown to black; margin

often dentate to lacerate; New Zealand L. fibrillosa McNabb (p. 95)

14. Pileus not radially fibrillose, pinkish flesh color to reddish brown; margin entire to slightly

undulate . .15

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

79

FIG. 57. SEMs of basidiospores: a, L. maritima (DAOM 1 59709); b-d, L. trullissata (GMM 1914). Note the differences

in ornamentation and basidiospore shape. Scale line = 1 i*.m.

15. Basidiomata violet when young, fading buff with only traces of violet remaining; basidiospores

globose; New Zealand 16

15. Basidiomata orange-brown, pinkish flesh color or reddish brown; basidiospores subglobose to sub-

ellipsoid; North America and Europe 17

80

FIELDIANA: BOTANY

FIG. 58. SEMs of basidiospores: a, L. amethysteo-occidentalis (E. Farwell 5015); b, L. amethystina (GMM 2237);

c, L. vinaceobrunnea (GMM 2335); d, L. ochropurpurea (E. Farwell 5074). Note differences in basidiospore shape and

echinulae length and width. Scale line = 1 fan.

16. Basidiospore ornamentation < 2 ^m long . . . . L. masonii var. brevispinosa McNabb (p. 89)

16. Basidiospore ornamentation > 2 /im long L. masonii var. masonii Stevenson (p. 107)

17. Pileus 16-85 mm diam., often strongly scaly to squarrose; stipe large and robust (26-1 10[-160] x

4-10[-16] mm), strongly striate to reticulate; western North America and upper Great Lakes region

L. nobilis G. M. Mueller (p. 1 13)

17. Pileus 8-50(-70) mm, finely fibrillose to minutely scaly; stipe smaller ([23-]30-85[-130] x 3-6

[-10] mm), not strongly striate; western North America, upper Great Lakes region and Europe . .

L. bicolor (Maire) Orton (p. 88)

18. Basidia (3)4-sterigmate 19

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

81

1 8. Basidia 2(3)-sterigmate 36

19. Basidiospores broadly ellipsoid to oblong (Q = 1.24-1.6); echinulae < 1 nm long 20

1 9. Basidiospores globose to ellipsoid; echinulae > 1 MHI_ long 22

20. Basidiospores Jc = 8.3-9 x 5.6-6 nm, oblong (Q = 1.45-1.6); mycelium at stipe base violet,

fading to white; Gulf Coast states L. oblongospora G. M. Mueller (p. 113)

20. Basidiospores x = 9-11.5 x 6.7-8(-8.8) /urn, ellipsoid (Q = 1.24-1.34[-1.43]); mycelium at

stipe base white 21

2 1 . Stipe context flesh color, lacking purple stains at base of stipe; widely distributed

L. proxima (Boud.) Pat. (p. 1 19)

21. Stipe context purple toward base, often with purple stains at stipe base; southern Argentina and

Chile L. proximella Singer (p. 1 20)

22. Mycelium at stipe base violaceous when fresh, becoming white with age; basidiospores small

(x = 7-8.3[-9] x 6-8 Mm) 23

22. Mycelium at stipe base white from onset; basidiospores larger (x = 8.2-13 Mm long) (but see

no. 32, L. longipes) 26

23. Lamellae flesh color to pinkish flesh color; basal mycelium usually scant, hygrophanous; basidiomata

orange-brown; pileipellis a trichodermium or of interwoven hyphae with numerous large fascicles

of perpendicular hyphae; southeastern United States, Mexico, Central America 24

23. Lamellae light vinaceous, occasionally fading to pinkish color; basal mycelium copious; basidiomata

pinkish flesh color to reddish brown; pileipellis hyphae interwoven with scattered fascicles of per-

pendicular hyphae; western and central North America and Europe 25

24. Cheilocystidia small, filamentous, present or absent; southeastern North America, Mexico,

Central America L. trichodermophora G. M. Mueller (p. 1 30)

24. Cheilocystidia large and vesiculose (up to 9.5 Mm diam.); Mexico

L. bullulifera Singer (p. 90)

25. Pileus 16-85 mm diam., often strongly scaly to squarrose; stipe large and robust (26-1 10[-160] x

4-10[-16] mm), strongly striate to reticulate; western North America and upper Great Lakes region

L. nobilis G. M. Mueller (p. 113)

25. Pileus 8-50(-70) mm, finely fibrillose to minutely scaly; stipe smaller ([23-]30-85[-130] x 3-6

[-10] mm), not strongly striate; western North America, upper Great Lakes region and Europe . .

L. bicolor (Maire) Orton (p. 88)

26. Pileus dark ochraceous brown, with light blue pruinae; USSR

L. chibinensis Michal. (p. 92)

26. Pileus orange-brown, pinkish flesh color or vinaceous brown 27

27. Basidiospores relatively large (Jc = 9.4-12.6 x 8.5-10.5 Mm); pileus striate; restricted to arctic,

boreal, or alpine habitats L. montana Singer (p. 1 10)

27. Basidiospores smaller (x < 9[-10] Mm long); pileus not striate, finely striate or translucent-striate

28

28. Basidiospores globose; echinulae > 1.5 Mm long and > 1.2 Mm wide at base 29

28. Basidiospores globose to ellipsoid; echinulae < 1 Mm wide at base 31

29. Stipe 1 2-25(-40) x 1-2 mm, concolorous with pileus; among mosses or not; eastern North America,

Central and South America, Europe L. ohiensis (Mont.) Singer (p. 1 1 5)

29. Stipe 20-70(-103) x 1-4 mm, darker than pileus; in moist areas, often among mosses (not Sphag-

num); eastern North America or New Zealand 30

30. Occurring in eastern North America L. striatula (Peck) Peck (p. 126)

30. Occurring in New Zealand L. glabripes McNabb (p. 99)

31. Pileus strongly translucent-striate; stipe 60-138(-165) mm long; growing among mosses, especially

Sphagnum, usually in bogs 32

31. Pileus not striate or striate, not strongly translucent-striate; stipe < 65(-106) mm long; growing

among mosses or not, not normally found in bogs; widely distributed 34

32. Basidiospores * = 7.6-7.8 x 6.8-7.2 Mm; North America

L. longipes G. M. Mueller (p. 1 06)

32. Basidiospores x = 8-10 Mm long 33

33. Basidiospores subglobose to broadly ellipsoid; Europe . . . . L. laccata var. moelleri Singer (p. 108)

82 FIELDIANA: BOTANY

33. Basidiospores ellipsoid; south temperate forests of South America, Tierra del Fuego to Valdivian

forests of Chile; under Nothofagus L. galerinoides Singer (p. 97)

34. Basidiospores broadly ellipsoid to ellipsoid (Q = 1.2-1.3); rarely encountered

L. laccata (Scop.: Fr.) Cooke var. laccata (p. 103)

34. Basidiospores globose to very broadly ellipsoid (Q usually < 1.15) 35

35. Pilei brownish vinaceous; Japan L. vinaceoavellanea Kongo (p. 131)

35. Pilei orange-brown to flesh color; common; North America and Europe

L. laccata var. pallidifolia (Peck) Peck (p. 1 1 6)

36. Basidiospores < 1 1 nm diam 37

36. Basidiospores most > 1 1 /im diam 40

37. Pileus not striate, reddish tawny or rose tawny; under native European trees

L. impolita Vellinga & G. M. Mueller (p. 102)

37. Pileus striate, rusty red or light brown; under Eucalyptus and other Australasian trees 38

38. Basidiomata light brown L. canaliculata (Cooke & Massee) Pegler (p. 92)

38. Basidiomata rusty red; lamellae pink 39

39. Pleurocystidia absent; widely distributed L. fraterna (Cooke & Massee) Pegler (p. 96)

39. Pleurocystidia present; New Zealand L. ohiensis var. paraphysata McNabb (p. 117)

40. Basidiospores 11-17 x 10-14.5 ^m, subglobose to broadly ellipsoid (Q = 1.1-1.19); echinulae

< 1.5 nm long; montane, boreal, or arctic habitats L. pumila Fayod (p. 121)

40. Basidiospores 10-15 x 10-15 nm, globose, echinulae > 2 ^m long 41

4 1 . Pileus striate, strongly undulate to distorted, orange-brown; North and South America, Europe, not

commonly collected L. tortilis (Bolt.) Cooke (p. 1 29)

41. Pileus not striate, reddish brown; Kew Gardens L. nana Massee (p. Ill)

Type Studies

Although this study dealt primarily with North

American taxa ofLaccaria, it was necessary to try

to examine the type collections of all names that

have been treated in the genus. When no type

existed, a lectotype or neotype was designated. A

representative specimen was designated when no

type material or material suitable for neotypifi-

cation was available or when an illustration was

lectotypified.

To clarify circumscriptions and stabilize appli-

cation of names in Laccaria, Mueller and Vellinga

(1986, 1990) and Mueller (1987) designated neo-

types in cases where names lacked type specimens

but were generally accepted and whose identity

could be determined by common usage (Korf,

1982a,b). This was done even in cases where an

illustration was included in the protologue. The

International Code of Botanical Nomenclature

(Greuter et al., 1 988), however, now explicitly states

that an illustration is part of the original material

and must be chosen as a lectotype if no specimen

suitable for lectotypification is available (Art. 7.5).

This rule holds even though the circumscription

of a fungus name often cannot be adequately de-

nned without information on micromorphological

characters. Those proposed neotypes (Mueller,

1987) that are now superfluous because the des-

ignated lectotype (illustration) takes precedence

have been redesignated as "representative speci-

mens." These specimens represent my interpre-

tation of the name and are provided to fix the

micromorphological characteristics of the epithet.

Further clarification of the code regarding utili-

zation of illustrations as lectotypes is needed be-

cause nomenclatural stability in the Agaricales,

and other fungi, is often sacrificed by forcing work-

ers to select illustrations as type specimens.

The importance of type studies was discussed

by Ammirati and Ovrebo (1979). Some of the rea-

sons given were ". . . to establish species concepts

and relationships, to determine synonomy, and

... for the development of a world-wide system

of taxonomy for fleshy fungi" (Ammirati & Ovre-

bo, 1979). Additionally, they mentioned the im-

portance of making detailed macro- and micro-

morphological information on each type collection

available for workers involved in general studies.

The following type descriptions are arranged al-

phabetically by the final epithet, specific or infra-

specific. Unless noted under Commentary, the type

collection consists of more than one basidioma

and is in an adequate state of preservation.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

83

FIG. 59. Representative basidiospores from type specimens: a, L. tetraspora var. aberrans (holotype); b, L. laccata

var. affinis (holotype); c, L. altaica (holotype); d, L. amethysteo-occidentalis (holotype). Scale line = 10 ^m.

Laccaria tetraspora var. aberrans Singer, Bull. Sex;.

Mycol. France 83: 116. 1967. Figure 59a.

TYPE: Argentina, Neuquen, Parque Nacional de Na-

huel Huapi, Camino a los Cantaros, 14 March

1959, Singer M1774 (BAFC!, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— As

in L. tetraspora var. scotica.

MICROMORPHOLOGY (Mihi)— Lamellar trama

parallel; hyphae mostly 3.5-10 nm diam., thin-

walled, hyaline to light yellowish brown; cells bar-

rel-shaped. Subhymenium morphologically undif-

84

FIELDIANA: BOTANY

ferentiated. Basidia (N = 15) 33^4 x 10-13 nm,

clavate, hyaline; sterigmata 4, up to 8.5 Mm long.

Pleurocystidia lacking. Cheilocystidia not ob-

served. Basidiospores (excluding ornamentation)

(N = 30) 7-8.7(-9) x 7-8.7(-9.2) Mm (x = 7.9 ±

0.6 x 7.8 ± 0.6 /xm), Q = 1-1.05(-1.12) (Q =

1.01 ± 0.03), globose, occasionally subglobose,

hyaline, echinulate; echinulae (0.9-)1.4-1.8 nm

long, crowded; hilar appendix 1.3-1.8 nm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 3.5-8 nm diam., long-celled, morpholog-

ically undifferentiated, tightly interwoven, hya-

line.

COMMENTARY— The type collection is infested

with an " Aspergillns-like" fungus, with numerous

conidia and conidiophores present. Because of this,

no observations on the arrangement of the pilei-

pellis hyphae or morphology of cheilocystidia could

be made. Singer (1967) separated this variety from

L. tetraspora var. scotica on the smaller basidio-

spores of L. tetraspora var. aberrans, shorter ba-

sidiospore ornamentation, and difference in hab-

itat. Laccaria tetraspora var. aberrans was found

on humus while L. tetraspora var. scotica fruited

among Sphagnum.

This taxon is treated as a synonym of L. ohien-

sis.

Laccaria laccata var. affinis Singer, Bull. Soc. My-

col. France 83: 1 1 1-112. 1967. Figure 59b.

TYPE: England, Bedgebury, Kent, National Pine Ar-

boretum, 30 October 1 960, Singer C3118 (BAFC!,

holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)—Pi-

leus 30-48 mm broad, convex, centrally de-

pressed, glabrous, distinctly fibrillose-asperulate

under hand lens as in Hygrocybe miniata, slightly

striate when moist, hygrophanous, uniform

brownish rose color, fading to pale leather rose

color when dehydrated; margin often crenulate-

furrowed. Lamellae 5-6 mm broad, sinuate to de-

current, slightly serrate, often anastomosing and

wrinkled, dull rose-colored, not as dull brownish

color as in L. laccata var. anglica; lamellulae wrin-

kled. Stipe 80-1 10 x 5-6.5 mm, equal or nearly

so, fibrillose, longitudinally striate, brownish rose-

colored ("brunfauve roussatre," Singer); striations

very pale. Basal mycelium white. Basidiospores

pure white in mass.

MICROMORPHOLOGY (Mihi)— Pilcipellis of in-

terwoven hyphae with widely scattered fascicles

of ± perpendicular hyphae; fascicles usually com-

posed of 5-15 hyphae; terminal cells of fascicular

hyphae (N= 10)37-55 x 6.5-13.5/on,subclavate

to clavate; walls up to 0.5 Mm thick, light yellowish

brown; contents hyaline. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel; hyphae mostly 3-8 nm diam.,

thin-walled, hyaline to light yellowish brown; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia (N = 15)29-47 x 9-12.5

Mm, clavate, hyaline; sterigmata 4, up to 9.5 Mm

long. Pleurocystidia lacking. Cheilocystidia (N =

10) 24.5-46 x (2-)3-5.5 Mm, filamentous to sub-

capitate, occasionally strangulated, scattered, thin-

walled, hyaline. Basidiospores (excluding orna-

mentation) (N = 30) (7-)7.8-10 x (7-)7.8-10 urn

(x = 8.6 ± 0.8 x 8.6 ± 0.8 Mm), Q = 1-1.05 (Q

= 1 ± 0.1), globose, rarely subglobose, hyaline,

echinulate; echinulae 1-1.4 /mi long, crowded; hi-

lar appendix 1.3-1.8 nm long, prominent, trun-

cate; plage present; contents occasionally unigut-

tulate. Basal mycelium hyphae mostly 3-7 Mm

diam., filamentous, tightly interwoven, hyaline.

COMMENTARY— The macro- and micromor-

phology of this collection fit within the circum-

scription of L. laccata var. pallidifolia. Bon (1 983)

proposed L. affinis (Singer) Bon based on this ho-

lotype, but data obtained to date do not support

the recognition of it as a discrete variety or species.

Although homokaryotic isolates of Laccaria lac-

cata var. pallidifolia from North America and

Sweden are intersterile (Mueller, 1991c), morpho-

logical differences have not been uncovered to rec-

ognize separate taxa for these intersterile popu-

lations. Until evidence of morphological or

molecular divergence is obtained, this taxon is

treated as a synonym of L. laccata var. pallidifolia.

Agaricus alpestris Britzelmayr, Hymenomyc.

Siidbayern VIII: 4, fig. 442. 1894.

TYPE: Lacking.

MACROMORPHOLOGY (Testc Britzelmayr, ibid.)—

Pileus fleshy; margin crenulate. Lamellae whitish

or yellowish red-brown. Stipe bent.

MICROMORPHOLOGY (Teste Britzelmayr, ibid.)—

Basidiospores 3-4 Mm diam., rough, yellowish.

COMMENTARY— The protologue stated that this

taxon was similar to A. laccatus. The basidiospore

dimensions, however, fall well outside the range

of basidiospore size for Laccaria.

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

85

Laccaria altaica Singer, Bull. Soc. Mycol. France

83: 122. 1967. Figure 59c.

TYPE: USSR, Kuraika, 31 July 1937, Singer A4 39

(LE!, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)—

Similar to Laccaria echinospora (Speg.) Singer.

MICROMORPHOLOGY (Mihi)— Lamellar trama

parallel; hyphae thin-walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

morphologically undifferentiated. Basidia (N = 1 5)

38-62 x 1 1.5-16 Mm, clavate, hyaline; sterigmata

2(-4), up to 1 1.5 Mm long. Pleurocystidia lacking.

Cheilocystidia not observed. Basidiospores (ex-

cluding ornamentation) (N = 30) (8.3-)l 1.5-14.5

(-15.6) x (8.3-)10-13.8 Mm (X = 12.8 ± 1.5 x

1 1 .5 ± 1 Mm), Q = 1-1 .2(-l .28) (Q = 1 . 1 2 ± 0.07),

globose, subglobose, broadly ellipsoid or occa-

sionally ellipsoid, hyaline, echinulate; echinulae

0.3-1 Mm long, crowded; hilar appendix 1.3-2

Mm long, prominent, truncate; plage present; con-

tents occasionally uniguttulate. Basal mycelium

hyphae not present.

COMMENTARY— The name, without a descrip-

tion, was originally published by Singer (1949).

Owing to the extremely poor condition of the type

collection, with only a few gill fragments extant,

no comments can be made concerning macro-

morphological and many micromorphological

characters.

Laccaria altaica is a later homonym of L. pu-

mila (Mueller & Vellinga, 1986).

Laccaria amethysteo-occidentalis G. M. Mueller,

Mycotaxon 20: 103. 1984. Figure 59d.

TYPE: Canada, British Columbia, near Squamish, Al-

ice Lake Prov. Park campground, 3 October 1981,

G. M. Mueller 1256 (TENN 42526) (TENN!, hole-

type).

MACROMORPHOLOGY (Mihi)— Pileus 10-33 mm

broad (x = 20 mm), convex becoming plane, oc-

casionally depressed, not striate, finely fibrillose

to fibrillose, deep purple ("Taupe Brown" to "Dull

Indian Purple"); margin decurved, entire; context

purple ("Dark Slate- Violet") with lighter gray-pur-

ple to white areas intermixed ("Pale Bluish Lav-

ender"). Lamellae adnate to arcuate, distant, thick,

< 5 mm broad, violaceous ("Deep Slate Violet"

to "Slate- Violet"). Stipe 18-87 x 4-12 mm (Jc =

50 x 7.3 mm), equal or tapering toward apex,

occasionally bulbose, dry, fibrillose, longitudinal-

striate, purple ("Dark Slate-Purple," "Dark Vi-

naceous Brown," or "Hay's Brown"), often with

lighter violet to white streaks ("Pale Bluish Lav-

ender"); context solid, concolorous with pileus

context. Basal mycelium violet ("Dark Slate-Pur-

ple" to "Deep Slate- Violet"). Basidiospores white

in mass.

MICROMORPHOLOGY (Mihi) — Pileipellis of

tightly interwoven hyphae with scattered fascicles

of ± perpendicular hyphae; fascicles usually com-

posed of 1 5-30 hyphae; terminal cells of fascicular

hyphae (N = 10) 30-73.5 x 8-15 Mm, filamentous

to clavate, occasionally broadly clavate; walls up

to 0.5 Mm thick, vinaceous brown; contents hyaline

to light vinaceous brown. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light vinaceous brown toward pileipellis. La-

mellar trama parallel; hyphae mostly 3-11.5 Mm

diam., thin- walled, hyaline to light vinaceous

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 15)

36.5-50.5 x 9.5-15 Mm, clavate, hyaline, vina-

ceous brown in mass; sterigmata 4, up to 8 Mm

long. Pleurocystidia lacking. Cheilocystidia lack-

ing. Basidiospores (excluding ornamentation) (N

= 30) 7.8-9.7 x 6-8.3 Mm (Jc = 8.7 ± 0.6 x 7.3

± 0.7 Mm),e = (1.05-)l.ll-1.33(-1.36)(G= 1.19

± 0.08), subglobose to broadly ellipsoid, occa-

sionally ellipsoid to amygdaliform, echinulate;

echinulae 0.9-1.4 Mm long, crowded; hilar appen-

dix 1.3-2 Mm long, prominent, truncate; plage

present; contents occasionally uniguttulate. Basal

mycelium hyphae mostly 2.5-6.5 Mm diam., hy-

aline, morphologically undifferentiated.

SOMATIC CULTURE MAT MORPHOLOGY— See the

description presented in the treatment of L. ame-

thysteo-occidentalis in the section on North Amer-

ican taxa.

COMMENTARY— This taxon is treated in detail

in the section on North American taxa.

Laccaria amethystina Cooke, Grevillea 12: 69-70.

1884. Figure 60a.

TYPE: England, Devon, Dartmoor, Two Bridges,

Whistmans Wood, 6 September 1971, D. N. Peg-

ler s.n. (as L. amethysted) (K.! neotypefide Muel-

ler & Vellinga, 1990).

MACROMORPHOLOGY— Not provided.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered ± perpendicular

individual hyphae or small fascicles of 2-3 ± per-

pendicular hyphae; terminal hyphae 43-60 x 9-

86

FIELDIANA: BOTANY

FIG. 60. Representative basidiospores from type or representative specimens: a, L. amethystina (neotype); b, L.

laccata var. anglica (holotype); c, L. laccata var. bicolor (representative collection); d, L. masonii var. brevispinosa

(holotype). Scale line = 10 pm.

1 6 Mm, subclavate, clavate or strangulate, hyaline;

walls up to 0.5 Mm thick. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line. Lamella trama parallel; hyphae 3-8 nm diam.,

thin-walled, hyaline; cells barrel-shaped. Subhy-

menium morphologically undifferentiated. Basidia

37-55 x 11-16 Mm, clavate, hyaline; sterigmata

4, up to 11 Mm long. Pleurocystidia lacking. Chei-

locystidia 40-70 x 6-12 Mm, filamentous, stran-

gulate or subclavate, thin-walled, numerous, hy-

aline. Basidiospores (excluding ornamentation) (N

= 30) (8.3-)8.7-9.7(-10) x 8.3-9.7(-10) Mm (jc =

9.2 ± 0.4 x 9.2 ± 0.4 Mm), (2= 1-1.05(0= 1.01

± 0.02), globose, echinulate; echinulae l-1.8(-2.3)

Mm long, up to 1 .2 Mm wide at base; hilar appendix

up to 1 .4 Mm long, prominent, truncate; plage pres-

ent; contents occasionally uniguttulate.

COMMENTARY— The collection designated as

neotype was selected from material requested from

several herbaria. Original material or other col-

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

87

lections seen by Hudson were not located. As stat-

ed in Mueller and Vellinga (1990), the chosen col-

lection fits Hudson's protologue and was collected

in England.

This taxon is treated in detail in the section on

North American taxa.

1 aecaria laccata var. anglica Singer, Bull. Soc.

Mycol. France 83: 1 10-1 1 1. 1967. Figure 60b.

TYPE: England, Kent, Bedgebury, National Pine Ar-

boretum, 20 October 1960, Singer C3119 (BAFC!,

holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 25-37 mm, convex, plane or depressed at

disc, often umbonate, pellucid-striate when fresh,

occasionally radially sulcate at margin, finely

tomentose to tomentose-fibrillose, strongly hy-

grophanous, reddish brown, fading to pale beige-

red or pale dull rose, finally to pale mouse; disc

rust-red. Lamellae sinuate to adnate, occasionally

subventricose, subcrowded, moderately broad, rose

to dull rose. Stipe 45-100 x 2.8 mm, equal or

tapering toward apex, tomentose, especially api-

cally, hollow, subhygrophanous, brown to reddish

brown. Basal mycelium pure white. Basidiospores

pure white in mass.

MICROMORPHOLOGY (Mihi)— Pilcipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-20

hyphae; terminal cells of fascicular hyphae (N =

10) 41.5-53 x 7.5-14 jum, subclavate to clavate;

walls up to 0.5 Mm thick, light yellowish brown;

contents hyaline to light yellowish brown. Pileus

trama tightly interwoven, morphologically undif-

ferentiated, hyaline, light yellowish brown toward

pileipellis. Lamellar trama parallel to subparallel;

hyphae mostly 3.5-9 nm diam., thin- walled, hy-

aline to light yellowish brown; cells barrel-shaped.

Subhymenium morphologically undifferentiated.

Basidia (N = 15) 30-44 x 8-14 Mm, clavate, hy-

aline; sterigmata 4, up to 7 Mm long. Pleurocystidia

lacking. C heilocystidia not observed. Basidio-

spores (excluding ornamentation) (N = 30) (7.4-)

7.8-9.2(-9.7) x (7.4-)7.8-9.2(-9.7) Mm (x = 8.4

± 0.6 x 8.3 ± 0.6 urn), Q = 1-1.06 (Q = 1.01 ±

0.02), globose, occasionally subglobose, hyaline,

echinulate; echinulae (1-) 1.4- 1.8 nm long, crowd-

ed; hilar appendix 1.2-1.8 Mm long, prominent,

truncate; plage present; contents occasionally uni-

guttulate. Basal mycelium hyphae mostly 4-10.5

Mm diam., morphologically undifferentiated, tight-

ly interwoven, hyaline; cells filamentous or barrel-

shaped.

COMMENTARY— Although the basidiospore size

and shape presented here fit the original circum-

scription, the length of basidiospore ornamenta-

tion observed in this study was larger than that

reported by Singer (1967). Additionally, he re-

ported numerous cheilocystidia ("cheilocystides et

cystidioles nombreuses pres de 1'arete, verforme,

le plus souvent filamenteuses-subclaviculees, sim-

ple ou fourchues-ramifiees, 17-29 x 3-4, 7 M")

that I did not observe.

This taxon is treated as a synonym of L. laccata

var. pallidifolia.

Agaricus bellus Persoon, Synopsis Methodica

Fungorum. p. 452. 1801.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Persoon, ibid.)—

Pileus fleshy, umbilicate, squamulose, yellow. La-

mellae decurrent-toothed, distant. Stipe 25 mm

long, thin, tough, lighter colored than pileus.

COMMENTARY— No authentic material of A bel-

lus could be found at L, LG, or GOET. Berkeley and

Broome (1883) included this name in Laccaria,

and other workers, including Rea (1922), con-

curred. Rea (1922) viewed this taxon as one

with a dark yellow or golden pileus with darker

squamules, a bright yellow stipe, and relatively

small (7 x 5-7 Mm), minutely warted basidio-

spores. Dennis et al. (1 960) did not treat this taxon

in their checklist. Based on the protologue, this

taxon is not a Laccaria. Without micromorphol-

ogical data, however, it is impossible to assign it

to another genus.

Laccaria laccata var. bicolor Maire, Publ. Inst.

Bot. Barcelona 3: 84. 1937. Figure 60c.

TYPE: Spain, Catalonia, Collado de Tosses, 7 October

1933, Maire s.n. (MPU!, holotype).

MACROMORPHOLOGY (Teste Maire, ibid.)— Pi-

leus reddish, squamulose. Lamellae distant, lilac.

Stipe reddish. Basal mycelium woolly, violet.

COMMENTARY— The single basidiocarp of the

type collection is severely contaminated by an

"Aspergillus-like" fungus. Because of distortion

caused by the parasite, no micromorphological data

could be obtained. My concept of the taxon is

88

FIELDIANA: BOTANY

based, therefore, on Maire's description and on

the common usage of the name (Korf, 1982a,b).

The following description is presented to illustrate

my concept of the taxon.

REPRESENTATIVE SPECIMEN— USA, Washington,

King Co., near Redmond, Watermain Woods, 24

October 1981, G. M. Mueller 1352 (TENN 42529)

(TENN).

MACROMORPHOLOGY (Mihi)— Pileus 12-43 mm

broad, convex, often depressed, not striate, fibril-

lose-scaly, occasionally scaly, hygrophanous,

pinkish flesh color ("Onion-skin Pink"), fading to

("Salmon-Buff'); margin decurved, entire to un-

dulate, becoming eroded. Lamellae adnate-arcu-

ate, moderately distant, thick, light vinaceous to

light pinkish flesh color ("Pale Purplish Vina-

ceous," "Pale Congo Pink," or "Light Congo

Pink"). Stipe 48- 120 x 3-10 mm, equal with bul-

bous base, occasionally slightly clavate, dry, fi-

brillose, longitudinal-striate, light pinkish flesh

color ("Flesh Pink"); striations darker ("Cacao

Brown" to "Pecan Brown"). Basal mycelium co-

pious, hygrophanous, when fresh violet ("Pale Vi-

naceous-Lilac"), becoming white.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 15-30

hyphae; terminal cells of fascicular hyphae (N =

10) 37-76 x (6-)10-17.5 Mm, subclavate to cla-

vate; walls up to 0.5 Mm thick, light yellowish

brown; contents hyaline to light yellowish brown.

Pileus trama tightly interwoven, morphologically

undifferentiated, hyaline, light yellowish brown to-

ward pileipellis. Lamellar trama parallel; hyphae

mostly 3.7-6 nm diam., thin-walled, hyaline to

light yellowish brown; cells barrel-shaped. Sub-

hymenium morphologically undifferentiated. Ba-

sidia (N = 15) 33-43.5 x 9.7-12 urn, clavate,

hyaline; sterigmata 4, up to 6.4 Mm long. Pleuro-

cystidia lacking. Cheilocystidia (N = 10) 29-50 x

2.3-3.7 jim, filamentous to subclavate, abundant,

hyaline. Basidiospores (excluding ornamentation)

(N = 30) 7-8.3 x (6-)6.4-7.8 Mm (Jc = 7.6 ± 0.4

x 7.1 ± 0.5 Mm), Q = 1-1.16 (Q = 1.07 ± 0.05),

subglobose to broadly ellipsoid, rarely globose, hy-

aline, echinulate; echinulae 0.9-1.8 Mm long,

crowded; hilar appendix 1.3-1.9 Mm long, prom-

inent, truncate; plage present; contents occasion-

ally uniguttulate. Basal mycelium hyphae mostly

5-9.8 Mm diam., tightly interwoven, morpholog-

ically undifferentiated, hyaline.

SOMATIC CULTURE MAT MORPHOLOGY (repre-

sentative specimen)— PDA: Radius at week 3 =

14-19 mm, week 6 = 23-30 mm; mat felty, thick,

tightly interwoven, tightly appressed to agar sur-

face, in time forming pruinose aerial layer away

from plug, becoming furrowed because of irregular

infolding near plug, not translucent, dark, bright

violet, fading to light orange-brown, by week 6

violet only in 3-4 mm band near margin, most of

mat light orange-brown; aerial hyphae light gray-

ish violet; margin 1-2 mm broad, subfelty, thin,

light violet; plug violet, becoming light orange-

brown; hyphae mostly morphologically undiffer-

entiated, occasionally irregularly swollen, purplish

brown in mass. MMN: Radius at week 3 = 37-

45 mm, week 6 = 58-64 mm; mat subfelty to silky,

thin, loosely interwoven, tightly appressed to agar

surface, translucent light violet, becoming buff-

colored; margin 1-2 mm broad, subfelty to silky,

thin, even to serrate, light violet; plug concolorous;

hyphae morphologically undifferentiated. MEA:

Radius at week 3 = 32-43 mm, week 6 = 68-76

mm; mat subfelty to felty near plug, thick, tightly

interwoven, tightly appressed to agar surface, sub-

translucent, white; margin subfelty, thin, loosely

interwoven, uneven, white; plug white; hyphae un-

differentiated.

COMMENTARY— This taxon is treated in detail

in the section on North American taxa.

Laccaria masonii var. brevispinosa McNabb, New

Zealand J. Bot. 10: 466-461. 1972. Figure

60d.

TYPE: New Zealand, Nelson, Lake Daniels track, 1 6

May 1969, McNabb FDD 29641 (FDD!, holotype).

MACROMORPHOLOGY (Teste McNabb, ibid.)—

Pileus 5-35 mm broad, convex to plano-convex,

occasionally plane at maturity, glabrous or mi-

nutely furfuraceous at disc, translucent striate at

margin, hygrophanous, violaceous with buff tints

when young, fading to buff at maturity. Lamellae

adnexed to adnate, distant, thick, < 4 mm broad,

pallid violaceous when young, becoming pallid

brownish pink, occasionally with faint violaceous

tints, glaucous. Stipe up to 100 x 1-2.5 mm, 3-

6 mm diam. at base, tough, dry, longitudinally

fibrillose-sulcate, violaceous when young, becom-

ing buff at base, finally buff except for violaceous

tints at apex. Basal mycelium pallid violaceous.

Basidiospores white in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered small fascicles of

± perpendicular hyphae; fascicles composed of 5-

1 0(-1 5) hyphae; terminal cells of fascicular hyphae

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

89

(N = 10) 33-62 x 5.5-13 Mm, filamentous, swol-

len, subclavate or clavate, light yellowish brown

in mass; walls up to 0.5 nm thick, light yellowish

brown; contents hyaline to moderate yellowish

brown. Pileus trama tightly interwoven, morpho-

logically undifferentiated, hyaline, light yellowish

brown toward pileipellis. Lamellar trama parallel;

hyphae 2.5-7 /nm diam., thin-walled, hyaline to

light yellowish brown; cells barrel-shaped. Sub-

hymenium morphologically undifferentiated. Ba-

sidia (N = 15) 29-39 x 7.8-11.5 Mm, clavate,

hyaline; sterigmata 4, up to 6.5 /on long. Pleuro-

cystidia lacking. Cheilocystidia not observed. Ba-

sidiospores (excluding ornamentation) (N = 30)

6-8.3(-9.2) x 6-8.3(-8.7) »m (x = 7.5 ± 0.8 x

7.2 ± 0.7 Mm), Q = 1 . 1 3(-l . 1 6) (Q = 1 .04 ± 0.05),

globose to subglobose, occasionally broadly ellip-

soid, hyaline, echinulate; echinulae 1.4-1.8(-2.3)

Mm long, crowded; hilar appendix 1.3-1.8 Mm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 2.5-7.5(-15) Mm diam., morphologically

undifferentiated, tightly interwoven, hyaline.

COMMENTARY— Although the basidiospore shape

and size fit the original circumscription, I mea-

sured the size of the ornamentation as slightly lon-

ger than McNabb ("spines 1.2-1.5 Mm long"). Ad-

ditionally, McNabb (1972) reported the presence

of cystidia ("paraphyses numerous, simple or

sparingly branched, filamentous, to 3 Mm diam.,

projecting beyond basidia"). This discrepancy is

probably due to the poor preservation of the col-

lection. The specimens appear to have been over-

dried, and consequently the material did not re-

hydrate well. Because of FDD policy, only half of

the type collection was sent on loan. Thus, the

possibility exists that more variation is present in

the complete type collection than is described

above.

Laccaria bullulifera Singer in Singer and Moser,

Mycopath. Mycol. Appl. 26: 149. 1965.

TYPE: Mexico, Popocatepetl, 2 1 August 1957, Singer

Ml 581 (MICH, holotype).

MICROMORPHOLOGY (Teste Singer, ibid.)— La-

mellar trama parallel. Basidia 30-31 x 8.5-10Mm,

4-sterigmate. Cheilocystidia 14 x 9.3 Mm, bal-

loon-shaped to subglobose, hyaline. Basidiospores

7-9 x 6. 3-7. 7 Mm (including ornamentation), glo-

bose to broadly ellipsoid, hyaline, echinulate;

echinulae 0.3-0.9 Mm long.

COMMENTARY— No material of this taxon could

be located at MICH. Although validly published by

Singer and Moser (1965), the full description was

published earlier (Singer, 1957). Aguirre-Acosta

and Perez-Silva (1978) and Montoya-Bello et al.

( 1 987) have included this taxon in their treatments

of Mexican fungi.

This taxon appears to be most similar to L.

trichodermophora. The large Cheilocystidia and

somewhat smaller basidioma size reported from

collections of L. bullulifera delimit the two taxa.

Laccaria trichodermophora has been reported from

Mexico as L. farinacea sensu Singer (Aguirre-

Acosta and Perez-Silva, 1978; Montoya-Bello et

al., 1987).

Laccaria calospora Singer, Sydowia 7: 7-8. 1973.

Figure 6 la.

TYPE: USA, Massachusetts, Waban, 21 June 1945,

Southwick s.n. (FH!, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 15-26 mm broad, convex, becoming de-

pressed or concave, finely fibrillose-asperate, hy-

grophanous, dingy purple-violet ("Vinaceous

Purple") fading to dingy violaceous brown, then

to buff color ("Fawn Color" to "Army Brown");

margin frequently sulcate. Lamellae sinuate to ar-

cuate, many-ranked, distant, 2-3 mm broad, pur-

plish ("Amaranth" or "Wild Aster"). Stipe 38-50

x 3-9 mm, tapering toward apex, fibrillose, striate

above, concolorous with pileus. Basal mycelium

tomentose, ± concolorous with pileus. Basidio-

spores violaceous ("Pale Verbena Violet") in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with numerous fascicles of ±

perpendicular hyphae; fascicles composed of 10-

20 hyphae; terminal cells of fascicular hyphae (N

= 10) 32-69 x 8-1 1 Mm, filamentous, clavate or

capitate; walls up to 0.5 Mm thick, light yellowish

brown; contents hyaline. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel; hyphae mostly 4—11 Mm

diam., thin- walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 1 5) 32-

46 x 8.5-13.5 Mm, clavate, hyaline; sterigmata 4,

up to 8.3 Mm long. Pleurocystidia lacking. Cheil-

ocystidia (N = 10) 36.5-64.5 x 5.5-8 Mm, fila-

mentous to subclavate, hyaline. Basidiospores (ex-

cluding ornamentation) (N = 30) 7.4-8.7 x 7-8.3

90

FIELDIANA: BOTANY

a

FIG. 61. Representative basidiospores from type specimens: a. L. calospora (holotype); b, A. canaliculata (holo-

type); c, L. chibinensis (holotype); d, L. laccata var. chilensis (holotype). Scale line = 10 fan.

nm (x = 8 ± 0.4 x 7.7 ± 0.5 ^m), Q = 1-1.12

(Q = 1 .03 ± 0.04), globose to subglobose, rarely

broadly ellipsoid, hyaline, echinulate; echinulae

1.4-2.3 fim long, crowded; hilar appendix 1.2-1.8

nm long, prominent, truncate; plage present; con-

tents occasionally uniguttulate. Basal mycelium

hyphae mostly 3-1 2 /urn diam., tightly interwoven,

hyaline; cells filamentous to barrel-shaped.

COMMENTARY— Mueller and Vellinga (1986,

1 990) have treated this taxon as a synonym of L.

amethystina. Although the type collection of L.

calospora was collected in Massachusetts, Singer

(1973) also listed a collection from Colombia.

There is considerable variability in size and color

among the violet specimens ofLaccaria that I have

collected in Costa Rica and Colombia. Mueller

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

91

and Singer (1 988) recently recognized one of these

as a segregate species, L. gomezii. It is possible

that additional taxa will be proposed when the

Neotropical species ofLaccaria are revised. Thus,

although L. calospora is currently treated as a syn-

onym, its status may change with the accumula-

tion of additional data.

Agaricus (Laccaria) canaliculata Cooke & Massee,

Grevillea 18: 2. 1889. Figure 61b.

TYPE: Australia, Brisbane, no date, Baily 710 (K!,

holotype).

MACROMORPHOLOGY (Teste Cooke & Massee,

ibid.)— Pileus submembranous, small, becoming

umbilicate, velvety, radially sulcate, light brown;

margin slightly crenulate. Lamellae adnate, sub-

distant, broad, flesh-colored, with a white dust.

Stipe thin, equal, longitudinally fibrillose, becom-

ing hollow, pallid.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae; hyphae up to 10.5 ^m diam.;

cells undifFerentiated to barrel-shaped; walls up to

0.5 Mm thick, light yellowish brown; contents hy-

aline to light yellowish brown. Pileus trama tightly

interwoven, undifferentiated, hyaline, light yel-

lowish brown toward pileipellis. Lamellar trama

parallel; hyphae 3.5-9 fim diam., thin-walled, hy-

aline to light yellowish brown; cells barrel-shaped.

Subhymenium morphologically undifFerentiated.

Basidia(N= 15)30.5-50.5 x 8-12.5 urn, clavate,

hyaline; sterigmata 2(-4), up to 8 Mm long. Pleu-

rocystidia lacking. Cheilocystidia not observed.

Basidiospores (excluding ornamentation) (N = 30)

7.4-9.7 x (7-)7.4-9.2(-9.7) Mm (x = 8_.6 ± 0.7 x

8.3 ± 0.7 Mm), Q = 1-1.05(-1.17) (Q = 1.03 ±

0.05), globose to subglobose, rarely broadly ellip-

soid, hyaline, echinulate; echinulae 0.5-1.4 (-1.8)

Mm long, crowded; hilar appendix 1.3-2 Mm long,

prominent, truncate; plage present; contents oc-

casionally uniguttulate. Basal mycelium hyphae

mostly 8-20 Mm diam., tightly interwoven, hya-

line; cells barrel-shaped.

COMMENTARY— The type collection consists of

a fragment from a single basidioma. Although Ste-

venson (1964) reported this taxon from New Zea-

land, McNabb (1972) stated that the material cited

by Stevenson from New Zealand was referable to

L. glabripes. McNabb's description of the holotype

states that the basidia were 4-sterigmate. Likewise,

May (1990) stated that he found the basisdia in

the type specimen to be 4-sterigmate. Although I

encountered a few 3- or 4-sterigmate basidia, the

majority of basidia bore two basidiospores. I agree

with Pegler's (1965) findings, therefore, and treat

L. canaliculata as a bisterigmate taxon.

Laccaria laccata var. carbonicola Singer, Bull. Soc.

Mycol. France 83: 110. 1967.

TYPE: USA, Massachusetts, Blue Hills, 1 1 November

1943, Singer s.n. (FH, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 10-30 mm broad, convex, becoming de-

pressed, glabrous, translucent-striate when fresh,

strongly hygrophanous, reddish fawn color when

fresh. Lamellae adnexed or adnate, subdistant,

broad, dull rose color. Stipe 40-60 x 3-7 mm,

equal or tapering toward the apex, finely fibrillose,

farinaceous at apex, concolorous with pileus, apex

often paler. Basal mycelium white. Basidiospores

white in mass.

MICROMORPHOLOGY (Teste Singer, ibid.)— Ba-

sidia 40-47 x 9 Mm, 4-sterigmate. Cheilocystidia

not observed. Basidiospores 7. 7-8. 2 x 6. 5-7. 2 Mm

(including ornamentation); echinulae mostly 0.7

Mm long.

COMMENTARY— The type collection could not

be found at FH. The taxon is treated as a synonym

of L. laccata var. laccata.

Laccaria chibinensis Michailovski, Mikologia Fi-

topatologia 8: 523. 1974. Figure 61c.

TYPE: USSR, Murmansk, 5 July 1973, Michailovski

s.n. (LE!, holotype).

MACROMORPHOLOGY (Teste Mikhailovski,

ibid.)— Pileus 20-40 mm broad, convex, then

cushion-shaped, glabrous, not hygrophanous, dark

ochraceous brown ("ochraceo-fuscidulus," Mi-

chail.), tinted with a light blue pruina ("vix coe-

rulescenti-pruinosus," Michail.); margin entire.

Lamellae decurrent, distant, thick, sublilac-ochra-

ceous ("sublilacino-ochraceae," Michail.). Stipe

30-45 x 8-1 5 mm, subclavate, rarely entire, fleshy,

subfibrose, hollow, concolorous with pileus, lack-

ing pruina.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with numerous scattered fasci-

cles of ± perpendicular hyphae; fascicles com-

posed of 10-30 hyphae; terminal cells of fascicular

hyphae (N = 10) 23-53 x 5.5-10.5 Mm, filamen-

92

FIELDIANA: BOTANY

tous, swollen, subclavate, clavate or capitate, light

yellowish brown in mass; walls up to 0.5 Mm thick,

light yellowish brown; contents hyaline. Pileus tra-

ma tightly interwoven, morphologically undiffer-

entiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel; hyphae 3-7 /urn

diam., thin-walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 10) 33-

46 x 9-H jon, clavate, hyaline; sterigmata (2-)4,

up to 6 Mm long. Pleurocystidia lacking. Cheilo-

cystidia(N= 10)27-50.5 x 2. 3-4 Mm, filamentous

to subcapitate, abundant, hyaline. Basidiospores

(excluding ornamentation) (N = 30) 7-9.2 x 6.4-

8.3 Mm (Jc =8.1 ± 0.6 x 7.4 ± 0.5 Mm), Q = 1-

1.2 «2 = 1.09 ± 0.06), globose to subglobose,

rarely broadly ellipsoid, hyaline, echinulate;

echinulae (0.8-)1.4-1.8 Mm long, > 1.2 Mm wide

at base; hilar appendix 1.3-1.8 Mm long, promi-

nent, truncate; plage present; contents occasionally

uniguttulate. Basal mycelium hyphae mostly 4-12

Mm diam., tightly interwoven, hyaline; cells fila-

mentous or barrel-shaped.

COMMENTARY— Based on the original descrip-

tion, this taxon appears to be closest phenetically

to the L. amethystina group.

I accar ia laccata var. chilensis Singer, Bull. Soc.

Mycol. France 83: 109. 1967. Figure 6 Id.

TYPE: Chile, Valdivia, Cordillera Pelada, El Mirador,

5 May 1965, Singer M5514 (BAFC!, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 1 2-24 mm broad, convex, slightly applanate

to depressed at center, glabrous, innately fibrillose

under hand lens, occasionally rivulose in age, hy-

grophanous, rose brown, fading to ocher when de-

hydrated. Lamellae adnate, subdistant, broad, dull

rose-colored. Stipe at least 2.5-3 times longer than

diam. of pileus, tapering slightly toward apex,

slightly fibrillose with longitudinal innate fibrils,

stuffed, concolorous with pileus or browner. Basal

mycelium pure white.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with widely scattered fascicles

of ± perpendicular hyphae; fascicles composed of

5-15 hyphae; terminal cells of fascicular hyphae

(N = 10) 33-60 x 4.5-10 Mm, filamentous to sub-

clavate; walls up to 0.5 Mm thick, light yellowish

brown; contents hyaline to light yellowish brown.

Pileus trama tightly interwoven, morphologically

undifferentiated, hyaline, light yellowish brown to-

ward pileipellis. Lamellar trama parallel; hyphae

mostly 5-14 Mm diam., thin-walled, hyaline to light

yellowish brown; cells barrel-shaped. Subhyme-

nium morphologically undifferentiated. Basidia (N

= 15) 31—42 x 7.5-11 Mm, clavate, hyaline; ste-

rigmata 4, up to 7 Mm long. Pleurocystidia lacking.

Cheilocystidia not observed. Basidiospores (ex-

cluding ornamentation) (N = 30) 6.4-7.8 x 6-

7.4(-7.8) Mm (x = 7.3 ± 0.4 x 6.7 ± 0.5 Mm), Q

= 1-1.16(2= 1.08 ± 0.06), globose to subglobose,

rarely broadly ellipsoid, hyaline, echinulate;

echinulae (< 0. 5-) 1.4- 1.8 Mm long, crowded; hilar

appendix 1.5-2.2 Mm long, prominent, truncate;

plage present; contents occasionally uniguttulate.

Basal mycelium hyphae mostly 4-14 Mm diam.,

tightly interwoven, hyaline; cells filamentous to

barrel-shaped.

COMMENTARY— The type collection consists of

a single basidioma. Singer (1967) reported infre-

quent cheilocystidia ("Cheilocystides et cysti-

dioles tres esparsed, filamenteuses ou versi-

formes").

This taxon is treated as a synonym of L. laccata

var. pallidifolia.

Clitocybe laccata var. decurrens Peck, Annual Rep.

New York State Bot. 157: 92. 1912. Figure

62a.

TYPE: USA, New York, Warren Co., Boltom Land-

ing, August, Peck s.n. (NYS!, holotype).

MACROMORPHOLOGY (Teste Peck, ibid)— Differ-

ing from the type by its distinctly decurrent to

arcuate-decurrent lamellae.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with numerous fascicles of ±

perpendicular loosely interwoven hyphae; fasci-

cles composed of 5-10 hyphae; terminal cells of

fascicular hyphae (N = 10) 30-55 x 4.5-9 Mm,

filamentous, subclavate, or rarely clavate; walls up

to 0.5 Mm thick, light yellowish brown; contents

light yellowish brown. Pileus trama tightly inter-

woven, morphologically undifferentiated, hyaline,

light yellowish brown toward pileipellis. Lamellar

trama parallel; hyphae usually 3.5-10 Mm diam.,

thin-walled, hyaline to light yellowish brown; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia (N = 15) 30-46 x 11-

14.5 Mm, clavate, hyaline; sterigmata 4, up to 9

Mm long. Pleurocystidia lacking. Cheilocystidia (N

= 10) 24—41 x 3-4.5 Mm, filamentous to subcap-

itate, rarely branched, abundant, thin-walled, hy-

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

93

FIG. 62. Representative basidiospores from type specimens: a, C. laccata var. decurrens (holotype); b, A. (Clitocybe)

echinosporus (holotype); c, L. fibrillosa (holotype); d, A. fraternus (holotype). Scale line = 10 nm.

94

FIELDIANA: BOTANY

aline. Basidiospores (excluding ornamentation) (N

= 30) 7.4-9.2(-l 1.5) x 7-9.2(-10) urn (x = 8.6 ±

0.9 x 8 ± 0.8 Mm), Q = 1-1.14(-1.24) (Q = 1.08

± 0.07), globose to subglobose, occasionally

broadly ellipsoid, hyaline, echinulate; echinulae

(0.5-)1.0(-1.4) Mm long, crowded; hilar appendix

1.3-1.8 Mm long, prominent, truncate; plage pres-

ent; contents occasionally uniguttulate. Basal my-

celium hyphae mostly 2-8 Mm diam., morpholog-

ically undifferentiated, tightly interwoven, hyaline.

COMMENTARY— This taxon is treated as a syn-

onym of L. laccata var. pallidifolia.

Agaricus echinospermus Britzelmayr, Hymeno-

myc. Siidbayern, Bot. Centralbl. 54: 5-6, figs.

512, 518. 1893.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Britzelmayr, ibid.)—

Pileus glabrous to slightly fibrillose, somewhat

translucent, yellowish brown to brown. Lamellae

adnate, crenate, whitish to brownish. Stipe solid,

yellowish brown to brown, lighter underneath.

MICROMORPHOLOGY (Teste Britzelmayr, ibid.)—

Basidiospores 6-8 Mm diam., angular spined.

COMMENTARY— The protologue stated that this

taxon was similar to A. echinosporous. The basid-

iospore dimensions provided are much smaller

than those of A. echinosporous, but without ad-

ditional micromorphological data, it is impossible

to tell if the dimensions provided are correct.

This taxon is treated as a synonym of L. tort His.

Agaricus (Clitocybe) echinosporus Spegazzini,

Anales Soc. Ci. Argentina 10: 123. 1880. Fig-

ure 62b.

TYPE: Argentina, La Baea, May 1880, Spegazzini

2891 (LPS!, holotype).

MACROMORPHOLOGY (Teste Spegazzini, ibid.)—

Pileus 5-10 mm broad, hemispheric, becoming

plano-convex, centrally depressed, radially sul-

cate, pellucid, subhygrophanous, rose-colored; disc

darker; margin straight, undulate to subcrenulate.

Lamellae acute at apex, long decurrent, distant,

thick, fleshy, up to 2.5 mm broad, entire, paler

than pileus. Stipe 10-15 x 1.5-3.5 mm, subcla-

vate, terete, fragile, fibrous-fleshy, rose-colored.

MICROMORPHOLOGY (Mihi)— Lamellar tram a

parallel; hyphae mostly 3-12 Mm diam., thin-

walled, hyaline to light yellowish brown; cells bar-

rel-shaped. Subhymenium morphologically undif-

ferentiated. Basidia (N = 9) 39-64 x 10-14 Mm,

clavate, hyaline, not rehydrating well; sterigmata

2, up to 1 1 Mm long, stout. Pleurocystidia lacking.

Cheilocystidia not observed. Basidiospores (ex-

cluding ornamentation) (N = 30) 1 1-13.8(-15.6)

x 11-14.7 Mm (x= 12.5 ± 1.1 x 12.4 ± 1.0 Mm),

Q= 1-1.06 (Q = 1.01 ± 0.02), globose, occasion-

ally subglobose, hyaline, echinulate; echinulae 2.3-

3.2(-3.7) Mm long, 1.3-1.8 Mm wide at base, very

crowded; hilar appendix 1.5-2.3 Mm long, prom-

inent, truncate; plage present; contents often uni-

guttulate.

COMMENTARY— The type collection consists of

a fragment from a single, small pileus. Observa-

tions could not be made on arrangement of pilei-

pellis hyphae or on stipe characteristics. No cys-

tidia were observed although the original

description reported them ("basidia . . . 55-60 x

10, cystidiis major. . ."). The discrepancy between

Spegazzini's and my description may be due to

poor rehydration or to the absence of cystidia in

the micromorphological preparations examined.

This taxon is treated as a synonym of L. tort His.

Refer to the Observations under L. tortilis in the

section on North American taxa for a discussion

of conflicting interpretations of these two taxa.

Laccaria fibrillosa McNabb, New Zealand J. Bot.

10: 468^69. 1972. Figure 62c.

TYPE: New Zealand, Nelson, Lake Daniels track, 1 5

May 1969, McNabb FDD 29639 (FDD!, holotype).

MACROMORPHOLOGY (Teste McNabb, ibid)—

Pileus 5-35 mm broad, strongly convex, becoming

convex to plano-convex, umbonate, radially fi-

brillose, disc scurfy, fibers aggregated toward mar-

gin, hygrophanous, buff with faint violaceous tints,

fibrils dark brown to brownish black at disc, paler

toward margin; margin dentate to lacerate with

age. Lamellae adnexed to adnate, distant, > 5 mm

broad, pallid violaceous, becoming buff with age,

glaucous. Stipe 20-70 x 1.5-3 mm, equal or

slightly expanded at base, tough, dry, hollow, lon-

gitudinally fibrillose-striate, pallid, violaceous

when young, fading to buff from base upward, at

maturity buff with violaceous tints at extreme apex.

Basal mycelium pallid violaceous. Basidiospores

white in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis com-

posed of ± parallel, radially arranged hyphae cov-

MUELLER: SYSTEM ATICS OF LACCARIA (AGARICALES)

95

ering disc, separating toward margin, yielding an

appearance similar to spokes of a wheel; hyphal

elements (N = 10) 33-60 x 6-10 urn; cells barrel-

shaped; walls up to 0.5 Mm thick, light yellowish

brown; contents dark brown in mass. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline to light yellowish brown. Lamellar

trama parallel to subparallel; hyphae 2.5-9 /mi

diam., thin-walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 15)

38.5-60 x 9-14 Mm, clavate, hyaline; sterigmata

4, up to 7.5 Mm long. Pleurocystidia lacking. Chei-

locystidia not observed. Basidiospores (excluding

ornamentation) (N = 30) 7-8.7 x 7-8.7 /mi (jc =

8.9 ±0.6 x 8.8 ±0.6 Mm), (2= 1-1. 12 ((2= 1.02

± 0.04), globose to subglobose, hyaline, strongly

echinulate; echinulae (1.4-)1.8-2.3(-2.8) Mm long,

not crowded; hilar appendix 1 .4-2 Mm long, prom-

inent, truncate; plage present; contents usually

uniguttulate. Basal mycelium hyphae mostly 2.5-

9 Mm diam., morphologically undifferentiated,

tightly interwoven, hyaline.

COMMENTARY— McNabb (1972) reported that

the pileipellis was "composed of unspecialized,

repent, interwoven, thin-walled, clamped hy-

phae. ..." This discrepancy may be due to poor

rehydration in the material I examined. In lon-

gitudinal section, the arrangement of pileipellis hy-

phae was not discernible, so the data presented

here were based on a whole mount of a scalp sec-

tion. Owing to FDD policy, only half of the type

collection was sent on loan. The possibility exists

that more variation is present in the entire type

collection than is described above.

Two taxa were included in Stevenson's (1964)

original description and illustration of L. masonii.

The type collection consists entirely of basidio-

mata with glabrous pilei and the epithet L. masonii

is restricted to that circumscription. McNabb

(1972) proposed L. fibril losa to represent the other

taxon included in the protologue.

Laccaria flavobrunnea Lebedeva, Opredelitel'

Shlyapochykh Gribov. p. 350. 1949.

TYPE: lacking.

COMMENTARY— No authentic material of this

taxon was included with the material loaned from

LE. In addition, I have not located a copy of the

original description. At this time, therefore, I can-

not make any comments regarding its affinities to

other Laccaria.

Agaricus flavofuscus Britzelmayr, Hymenomyc.

Sudbayern VIII: 4, fig. 441. 1894.

MACROMORPHOLOGY (Teste Britzelmayr, ibid.)—

Lamellae white or brownish.

MICROMORPHOLOGY (Teste Britzelmayr, ibid.)—

Basidiospores smooth.

COMMENTARY— The protologue stated that this

taxon was very similar to A. alpestris and that it

was difficult to tell the two apart. Based on the

report that the basidiospores are smooth, A. fla-

vofuscus cannot be a Laccaria. As stated in the

Commentary under A. alpestris, I also do not treat

that taxon as a Laccaria.

Agaricus fraternus Cooke & Massee, Grevillea 16:

31. 1887. Figure 62d.

TYPE: Australia, vie. Port Phillip, French No. 1 (K!,

holotype).

MACROMORPHOLOGY (Teste Cooke & Massee,

ibid.)— Pileus convex, depressed, umbilicate,

smooth, glabrous, dark rusty-red. Lamellae broad,

subdistant, adnate, rusty-red color. Stipe elongate,

thin, tapering toward apex, glabrous, hollow, con-

colorous with pileus.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-20

hyphae; individual hyphae not discernible, dark

yellowish brown in mass. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis.

Lamellar trama parallel; hyphae 3-10 Mm diam.,

thin-walled, hyaline to light yellowish brown. Sub-

hymenium morphologically undifferentiated. Ba-

sidia (N= 15)29-44 x 8-1 2 Mm, clavate, hyaline;

sterigmata 2, up to 11 Mm long, stout. Pleurocys-

tidia lacking. Cheilocystidia not observed. Basid-

iospores (excluding ornamentation) (N = 30) (8.3-)

9.2-1 1(-1 1.5) x 8.7-10.6(-11.5) nm (x = 9.9 ±

0._7 x 9.9 ± 0.7 Mm), Q = (0.95-)1-1.06(-1.09)

(Q = 1.01 ± 0.03), globose to subglobose, hyaline,

echinulate; echinulae (0. 9-) 1.4-1. 8 Mm long,

crowded; hilar appendix 1.3-2.8 Mm long, prom-

inent, truncate; plage present; contents often uni-

guttulate.

COMMENTARY— The type collection consists of

a fragment from one pileus and a short segment

of a stipe. Individual hyphae of the pileipellis were

not discernible because of poor rehydration.

96

FIELDIANA: BOTANY

Tom W. May (University of Melbourne, pers.

comm.) reports the finding of a potentially para-

typic collection at MEL that better fits the proto-

logue but that is not contaxic with the type spec-

imen housed at K. It has been assumed that the

report of ellipsoid basidiospores in the original

diagnosis of A. fraternus probably referred to an-

other collection on the type sheet at K. that was

collected in New Zealand (Pegler, 1965; Mueller

& Vellinga, 1986). If the collection housed at MEL

is lectotypified, A. fraternus would not fit into the

generic circumscription of Laccaria and the cor-

rect basionym for the taxon treated here would be

N. goossensiae.

This taxon is treated in detail in the section on

North American taxa.

Laccaria galerinoides Singer in Singer and Moser,

Mycopath. Mycol. Appl. 26: 147-148. 1965.

Figure 63a.

TYPE: Chile, Valdivia, Cordillera Pelada, 930-1000

m alt., 28 March 1963, Singer M3212 (BAFC!,

holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)—Pi-

leus 16-17 mm broad, convex, centrally de-

pressed, glabrous, translucent striate, occasionally

sulcate, light ochraceous-brown ("Peruvian Br."

M&P) to golden-ochraceous ("Inca Gold" M&P)

at margin, becoming sordid ("Leather Br." M&P).

Lamellae adnate, crowded to subdistant, moder-

ately thick, entire, pallid ochraceous-isabelline

("Grain" M&P), becoming pallid ("Avellaneous-

Argillaceous" M&P), 2-ranked; lamellulae nar-

row. Stipe 95-1 15 x 2-5 mm, glabrous, tubular,

with distinct superficial innate striations, radicat-

ing, ochraceous-brown ("Titan" M&P), red-brown

("Chutney" M&P) or almost black, much lighter

toward apex. Basal mycelium pallid.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-20

hyphae; terminal cells of fascicular hyphae (N =

10)37-57.5 x 6. 5-1 2 /urn, filamentous, subclavate

or rarely clavate; walls up to 0.5 nm thick, light

yellowish brown; contents hyaline. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel to subparallel;

hyphae mostly 4-19 pm diam., thin-walled, hya-

line to light yellowish brown. Subhymenium mor-

phologically undifferentiated. Basidia (N = 1 5) 29-

40 x 9-11 Mm, clavate, hyaline; sterigmata 4, up

to 6.5 Mm long. Pleurocystidia lacking. Cheilocys-

tidia not observed. Basidiospores (excluding or-

namentation) (N = 30) 7.4-9.7(-10) x 5.5-7.8 /im

(X = 8.5 ± 0.7 x 6.3 ± 0.6 /mi), Q = 1.16-1.52

(Q = 1 .34 ± 0.08), ellipsoid to amygdaliform, rare-

ly subglobose, hyaline, echinulate; echinulae 0.9-

1.4(-1.8) Mm long, not crowded; hilar appendix

1.5-2.3 Mm long, very prominent, truncate; plage

present; contents occasionally uniguttulate.

COMMENTARY— The type collection consists of

a single basidioma lacking the stipe base. The ba-

sidiospores observed were larger than those re-

ported by Singer (Singer & Moser, 1965) ("sporis

7-8 x 5,7-6,8 M")- In his unpublished notes on

this specimen, however, Singer gives the basid-

iosporesizeas6.8-10 x 5-7. 5 Mm including echin-

ulae. Additionally, Singer (Singer & Moser, 1965)

reported sparse cheilocystidia ("cheilocystiis spar-

sis, ad nee non prope aciem visis, hyalinis, ±2,5

M latis").

I have collected this taxon from the type locality

as well as additional locations in southern Chile

and Tierra del Fuego. My findings fit those given

for the taxon by Horak (1979). Although Singer

( 1 986) placed L. galerinoides in its own stirps, this

does not appear justified, based on my study of

the type and the subsequent material examined.

See observations under L. longipes in the section

on North American taxa for additional data.

Laccaria laccata var. gibba Singer, Beih. Nova

Hedwigia 29: 27. 1969. Figure 63b.

TYPE: Chile, Valdivia, Cordillera Pelada, 6 May 1967,

Singer M6738 (SGO!, holotype).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 10-16 mm broad, convex, becoming plane,

umbonate, glabrous, when dry with innately ap-

pressed fibers, radially pellucid-striate, sulcate, hy-

grophanous, reddish brown (between 1 4 A 1 1 and

5 C 1 1 M&P); margin light flesh color (1 1 C 7 and

1 2 E 8 M&P). Lamellae adnate, adnate-decurrent,

or decurrent, distant, broad, rose-colored (between

3 A 10 and 9 A 6 M&P). Stipe 45-50 x 2-2.5

mm, equal or narrowed at apex, glabrous when

moist, hygrophanous, dark red (6 J 1 2 M&P); apex

lighter in color. Basal mycelium white.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae, no fascicles of hyphae observed;

terminal hyphal cells (N = 10) 38-67 x 7-18 Mm,

subclavate to clavate, light yellowish brown in

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

97

a

FIG. 63. Representative basidiospores from type specimens: a, L. galerinoides (holotype); b, L. laccata var. gibba

(holotype); c, L. glabripes (holotype); d, L. gomezii (holotype). Scale line = 10 jtm.

mass; walls up to 0.5 /mi thick, light yellowish

brown; contents hyaline. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel; hyphae thin-walled, hyaline

to light yellowish brown. Subhymenium morpho-

logically undifferentiated. Basidia (N = 1 5) 29-48

x 7.5-1 1 /mi, clavate, hyaline; sterigmata (2-)4,

up to 7 /mi long. Pleurocystidia lacking. Cheilo-

cystidia not observed. Basidiospores (excluding

ornamentation) (N = 30) 7-8.7 x (5-)6-7.4 urn

(x = 7.8 ± 0.5 x 6.3 ± 0.5 Mm), Q = 1.08-1.35

(-1.38) «2 = 1.25 ± 0.07), occasionally subglo-

bose, usually broadly ellipsoid to ellipsoid, hya-

line, echinulate; echinulae 0.9-1. 8(-2.3) /mi long,

not crowded; hilar appendix 1.3-1.8 /mi long,

98

FIELDIANA: BOTANY

prominent, truncate; plage present; contents oc-

casionally uniguttulate.

COMMENTARY— The type collection consists of

a single pileus and a segment of the stipe without

the base. Singer (1969) reported shorter basidio-

spore ornamentation ("spinulis 0,3-0,9 M proji-

cientibus") than presented here. As the specimen

lacked lamellar margins, no observation of chei-

locystidia was possible. Singer (1969) reported the

cystidia as "inconspicuis subfilamentosis consis-

tente."

This taxon is treated as a synonym of L. laccata

var. laccata.

Laccaria glabripes McNabb, New Zealand J. Bot.

10: 477^78. 1972. Figure 63c.

TYPE: New Zealand, Nelson, Lake Daniels track, 25

April 1969, McNabb FDD 29640 (FDD!, holotype).

MACROMORPHOLOGY (Teste McNabb, ibid.}—

Pileus 5-25(-35) mm broad, convex, becoming

plano-convex, applanate, occasionally depressed,

conspicuously pellucid-striate when wet, slightly

sulcate, almost glabrous when wet, minutely fur-

furaceous when dry, hygrophanous, flesh pink to

reddish brown, drying buff, disc darker; margin

reflexed in age. Lamellae adnate to subdecurrent,

distant, thick, up to 6 mm broad, intermixed, flesh

pink, glaucous. Stipe 25-60 x 1.5-3.5 mm, equal,

dry, glabrous, appearing cartillaginous when wet,

not longitudinally fibrillose, reddish brown, con-

colorous with disc. Basal mycelium white. Basid-

iospores white in mass.

MICROMORPHOLOGY (Mihi)— Pileipcllis of in-

terwoven hyphae with scattered small fascicles of

± perpendicular hyphae; fascicles composed of 5-

1 0 hyphae; terminal cells of fascicular hyphae (N

= 10) 33-60 x 6-10 Mm, filamentous, subclavate,

subcapitate, or occasionally strangulate, light yel-

lowish brown in mass; walls up to 0.5 nm thick,

light yellowish brown; contents hyaline. Pileus tra-

ma tightly interwoven, undifterentiated, hyaline,

light yellowish brown toward pileipellis. Lamellar

trama parallel; hyphae 2.5-10 Mm diam., thin-

walled, hyaline to light yellowish brown; cells bar-

rel-shaped. Subhymenium morphologically undif-

ferentiated. Basidia (N = 15) 38.5-60 x 9-14.5

Mm, clavate, hyaline; sterigmata 4, up to 9 Mm long.

Pleurocystidia lacking. Cheilocystidia not ob-

served. Basidiospores (excluding ornamentation)

(N = 30) 7-8.7 x 7-8.7 urn (x = 7.9 ± 0.5 x 7.8

±0.5 MHI), Q = 1-1 . 1 2 «2 = 1 .02 ± 0.04), globose

to subglobose, rarely broadly ellipsoid, hyaline,

echinulate; echinulae (1 .4-)! .8-2.3(-2.8) Mm long,

> 1.2 Mm wide at base, relatively crowded; hilar

appendix 1 .3-2 Mm long, prominent, truncate; plage

present; contents occasionally uniguttulate. Basal

mycelium hyphae mostly 2-12 Mm diam., tightly

interwoven, hyaline; cells barrel-shaped.

COMMENTARY— Owing to PDD policy, only half

of the type collection was sent on loan. The pos-

sibility exists that more variation is present in the

complete type collection than is described above.

Collections referable to L. striatula were treated

as L. glabripes in my dissertation (Mueller, 1 982).

Aguirre-Acosta and Perez-Silva ( 1 978) reported L.

glabripes from Mexico, but I believe that their

material is referable to L. striatula. As mentioned

in the Commentary under A. canaliculata, T. W.

May (1990, pers. comm.) treats L. glabripes as a

synonym of L. canaliculata. As Pegler (1965) and

I found the type of L. canaliculata to have 2-ste-

rigmate basidia, I treat the two taxa as separate

species, L. glabripes and L. canaliculata.

Agaricus (Clitocybe) glaucipes Berkeley & Curtis,

Ann. Mag. Nat. Hist., III. 4: 284. 1859.

TYPE: USA, Connecticut, no date, Curtis 5546 (col-

lected by C. Wright) (K!, holotype).

MACROMORPHOLOGY (Teste Berkeley & Curtis,

ibid.)— Pileus 25 mm broad, convex, thin, pubes-

cent, pale rufous; margin incurved. Lamellae ad-

nate, subdistant, white. Stipe 50 x 6 mm, solid,

concolorous with pileus.

COMMENTARY— The type collection consists of

one very moldy basidiocarp. No micromorpho-

logical observations could be obtained, and the

original description does not include micromor-

phological data. The protologue stated that A.

glaucipes was allied to A. laccata, and the epithet

is treated as a synonym of L. laccata var. laccata.

Laccaria gomezii Singer & G. M. Mueller /// Muell-

er and Singer, Mycotaxon 33: 224-225. 1988.

Figure 63d.

TYPE: Costa Rica, Cartago Prov., along Panamerican

Highway, km 55, La Chonta, 2800 m, under

Quercus and Magnolia, September 1982, Gomez

18443 (F!, holotype).

MACROMORPHOLOGY (Teste R. Singer, unpubl.

notes)— Pileus 30 mm broad (when dried), convex

with a deep umbilicus, squarrose in depression,

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

99

a

FIG. 64. Representative basidiospores from type specimens: a, Naucoria goossensiae (holotype); b, C. tortilis var.

gracilis (holotype); c, L. laccata var. intermedia (holotype); d, A. laccatus (neotype). Scale line = 10 /mi.

finely fibrillose-squamulose or squarrulose on the

margin, not rimose or strongly radially fibrillose,

light violet suffused with chocolate brown, dried

uniformly "blondine" to "canbaak" (M&P). La-

mellae adnate-subdecurrent, close, moderately

broad, violet, somewhat whitish pulverulent un-

der a lens when dry. Stipe 80 x 3-4 mm, pubes-

cent to occasionally squamulose at apex, longi-

tudinally sulcate when dry, coarsely woolly-strigose

by the dried basal mycelium, appearing hispid in

part and less distinctly violet than pileus. Context

dirty white; odor and taste not annotated.

MICROMORPHOLOGY (Mihi) — Pileipellis of

tightly interwoven hyphae with scattered fascicles

of ± perpendicular hyphae; fascicles composed of

10-30 hyphae; terminal cells of fasicular hyphae

12-15 Mm diam., filamentous to subclavate, hy-

aline; walls up to 0.5 i*m thick. Pileus trama tightly

100

FIELDIANA: BOTANY

interwoven, morphologically undifferentiated, hy-

aline. Lamellar tratna parallel to subparallel; In -

phae mostly 4-8 nm diam., thin-walled, hyaline.

Subhymenium morphologically undifferentiated.

Basidia 35—43 x 9-12 Mm, clavate, hyaline; ste-

rigmata 4, up to 10 nm long. Pleurocystidia lack-

ing. Cheilocystidia 45-80 x 6-9 nm, subclavate,

abundant, forming an early sterile layer, thin-

walled, hyaline. Basidiospores (excluding orna-

mentation) (N = 30) 7.8-9.3 x 7-7.8 nm(x = 8.7

± 0.5 x 7.6 ± 0.4 Mm), Q = 1.06-1.29 (Q = 1.14

± 0.06), subglobose to broadly ellipsoid, rarely

ellipsoid, hyaline, echinulate; echinulae 1-2.5 nm,

< 1 Mm wide at base, crowded; hilar appendix

1.3-2 Mm long, prominent, truncate; contents oc-

casionally uniguttulate. Caulocystidia 34-65 x 7-

14 Mm, subclavate, clavate or strangulate, thin-

walled, hyaline to light vinaceous brown, formed

from recurved surface hyphae, scattered or clus-

tered in small groups at apex of stipe, absent or

very infrequent below.

COMMENTARY— Specimens of this taxon have

been collected in Costa Rica and Colombia. Lac-

caria gomezii occurs sympatrically with L. ame-

thystina, with which it is morphologically similar.

The two taxa are distinguished by basidioma col-

or, lamellar thickness and attachment, and basid-

iospore shape. See Observations under L. ame-

thystina in the section under North American taxa

and Mueller and Singer (1988) for additional in-

formation.

Naucoria goossensiae Beeli, Bull. Soc. Roy. Bot.

Belgique 61: 88. 1928. Figure 64a.

TYPE: Zaire, Ori, Noika, May 1926, Goossens 558

(BR!, holotype).

MACROMORPHOLOGY (Teste Beeli, ibid.)— Pileus

25-35 mm broad, convex to umbilicate, glabrous,

brownish rust color; margin incurved. Lamellae

adnate or free, up to 7 mm broad, brownish red

color. Stipe 45 x 4-5 mm, cylindrical, thickened

at base, glabrous, hollow, concolorous with pileus.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-15

hyphae; terminal cells of fascicular hyphae (N =

5) 37-57.5 x 5-10.5 Mm, filamentous, subclavate

or clavate, light yellowish brown in mass; walls up

to 0.5 Mm thick, light yellowish brown; contents

hyaline to light yellowish brown. Pileus trama

tightly interwoven, morphologically undifferen-

tiated, hyaline, light yellowish brown toward pi-

leipellis. Lamellar trama parallel; hyphae 2.5-10

(-16) Mm diam., thin- walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

morphologically undifferentiated. Basidia (N = 1 5)

28-44 x 9-12.5 Mm, clavate, hyaline; sterigmata

2(-4), up to 14 Mm long. Pleurocystidia lacking.

Cheilocystidia not observed. Basidiospores (ex-

cluding ornamentation) (N = 30) (7.8-)8.7-l 1

(-1 1.5) x (7.4-)7.8-10 Mm (Jc = 9.9 ± 0.9 x 8.9

± 0.7 Mm), 0 = 1. 04-1. 2(-l. 22) ((2=1.11 ±0.06),

subglobose, broadly ellipsoid or broadly amyg-

daliform, echinulate; echinulae 0.3-1.5 Mm long,

crowded; hilar appendix 1.3-2.5 Mm long, prom-

inent, truncate; plage present; contents occasion-

ally uniguttulate. Basal mycelium hyphae mostly

4-13 Mm diam., hyaline, light yellowish brown in

mass; cells barrel-shaped.

COMMENTARY— This taxon is treated as a syn-

onym of L. fraterna but see Observations under

L. fraterna.

Clitocybe tortilis var. gracilis Peck, Annual Rep.

New York State Bot. 67: 36. 1 903. Figure 64b.

TYPE: USA, New York, Bronx, N.Y. Bot. Garden,

13 July 1902, Earles.n. (NYS!, holotype).

MACROMORPHOLOGY (Teste Peck, ibid.)— Pileus

3-6 lines broad, thin, convex, slightly umbilicate,

becoming depressed or infundibuliform in age, ir-

regular, striate, hygrophanous, when fresh reddish

flesh color, paler when dry. Lamellae adnate to

decurrent, distant, broad, pruinose when old and

dry. Stipe 6-10 x 0.5 lines, glabrous, hollow.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with widely scattered, small fas-

cicles of ± perpendicular hyphae; terminal cells

of fascicular hyphae (N = 5) 39-67 x 10-13 Mm,

filamentous to subclavate, not rehydrating well;

walls up to 0.5 Mm thick, light yellowish brown;

contents hyaline to light yellowish brown. Pileus

trama tightly interwoven, morphologically undif-

ferentiated, very thin, hyaline to light yellowish

brown. Lamellar trama parallel; hyphae usually 2-

8 Mm diam., thin-walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 15) 37-

60 x 8-14 Mm, clavate, hyaline; sterigmata 4, up

to 7 Mm long. Pleurocystidia lacking. Cheilocys-

tidia (N = 10) 33-55 x 2.5-4 Mm, filamentous or

subcapitate, abundant, thin-walled, hyaline. Ba-

sidiospores (excluding ornamentation) (N = 30)

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

101

(7.8-)8. 3-10.6 x 7.8-1 0(-1 0.6) Mm (jc= 9.3 ± 0.7

x 9.1 ±0.7 /tm), Q= 1-1.06(-1.11)«2 = 1.02 ±

0.03), globose, occasionally subglobose, hyaline,

echinulate; echinulae 1.4-2.3(-2.8) Mm long,

crowded; hilar appendix 1.3-2 fim long, promi-

nent, truncate; plage present; contents occasionally

uniguttulate. Basal mycelium hyphae mostly 4-8.5

Mm diam., tightly interwoven, hyaline; cells fila-

mentous to barrel-shaped.

COMMENTARY— The type variety has much larg-

er basidiospores and 2-sterigmate basidia. This

taxon is treated as a synonym of L. ohiensis, not

as a variety of L. tortilis.

Clitocybe gruberi Smith, Mycologia 36: 245-246.

1944.

TYPE: USA, Idaho, Juliet, May 1943, W. B. Gruber

26 (MICH!, holotype).

COMMENTARY— Singer (1949) placed this taxon

in Laccaria. Micromorphological analysis of this

collection, however, revealed the presence of very

elongate, smooth basidiospores. I agree with Big-

elow and Smith (1973), therefore, that this collec-

tion does not belong in Laccaria but belongs in

the monotypic genus Cantharocybe Bigelow and

Smith.

Agaricus grumatus Scopoli, Flora Carniolica. p.

433. 1772.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Scopoli, ibid.)—P\-

leus convex, dry, filamentous. Lamellae free,

abundant. Stipe long, glabrous, hollow.

COMMENTARY— Fries (1836-1838) stated that

this taxon showed affinities to A. pachyphyllus

Fries, which showed affinities to A. laccatus. Both

of these taxa are treated as synonyms of L. laccata.

Agaricus (Clitocybe) holoporphyrus Berkeley &

Curtis, J. Linn. Soc., Bot. 10: 284. 1868.

TYPE: Cuba, Wright no. 12 (K!, holotype).

COMMENTARY— The original description stated

that the basidiospores are oblong and not sub-

globose as in C. laccata. Micromorphological anal-

ysis of this collection revealed the presence of

subfusiform, smooth basidiospores. Basidiospore

shape and lack of ornamentation indicate that this

collection is clearly not a Laccaria.

Laccaria impolita Vellinga & G. M. Mueller in

Mueller and Vellinga, Mycotaxon 37: 387-

388. 1990.

TYPE: (CAG, holotype).

MACROMORPHOLOGY (Teste Ballero & Contu,

1989)-Pileus 10-40 mm diam., fleshy, convex,

depressed, umbilicate, dry, squamulose-areolate

at disc, elsewhere tomentose, not striate, reddish

tawny to rose tawny, then ochraceous; margin in-

volute. Lamellae adnate to decurrent, distant, thick,

entire to slightly denticulate, concolorous with pi-

leus. Stipe 40-60 x 5-8 mm, cylindric to subcla-

vate, rarely subradicate, usually thinner at apex,

fibrillose striate, concolorous; basal mycelium

white. Basidiospores white in mass.

MICROMORPHOLOGY (Teste Ballero & Contu,

1989)— Pileipellis a trichoderm or subpalisade;

hyphae clavate, pigment(s) vacuolate or membra-

nous. Lamellar trama regular. Basidia bisterig-

mate. Pleurocystidia none. Cheilocystidia fila-

mentous or subclavate. Basidiospores 8-12 nm

diam., globose, hyaline, inamyloid; echinulae 1.3-

1 .8(-2) MHI high, conic, distant. Clamp connections

numerous.

COMMENTARY— Mueller and Vellinga (1990)

proposed this epithet for the taxon described by

Ballero and Contu (1989) as L. singeri (non L.

singeri M. V. Locquin & B. M. Sarwal). According

to Ballero and Contu (1989), this taxon can be

differentiated from L. fraterna by the more robust

stature, squamulose-areolate, astriate pilei, fibril-

lose-striate stipe, more coarsely echinulate basid-

iospores, arrangement of the pileipellis hyphae,

and association with north temperate trees.

Agaricus (Clitocybe) incongruus Berkeley, J. Bot.

(Hooker) 2: 48. 1850.

TYPE: Jillapahar, Darjeeling. Aug.-Sept., Berkeley s.n.

(K.!, holotype).

MACROMORPHOLOGY (Teste Berkeley, ibid.}—

Pileus 3 1 mm broad, umbilicate, smooth, dry, ci-

nereous-blue; margin undulate; context white. La-

mellae 1 50 x 12 mm, subclavate, slightly fibril-

lose, hollow, concolorous with pileus.

102

FIELDIANA: BOTANY

COMMENTARY— The type collection consists of

a single stipe with an attached fragment of the

pileus. Virtually no hymenial material was avail-

able for micromorphological analysis, and the pro-

tologue does not include micromorphological data.

Only a few basidiospores were found in the ex-

amined slides mounts, and these were nodulose,

not echinulate. Although Berkeley (1850) consid-

ered it "[a] very curious species, resembling some-

what the amethyst form of A. laccatus, and perhaps

as nearly allied to that species as to any described,"

it is not a Laccaria and probably belongs in the

Entolomataceae.

Laccaria laccata var. intermedia Singer, PI. Syst.

Evol. 126: 368-369. 1977. Figure 64c.

TYPE: Czechoslovakia, Moravia, Jeseniky, Reiviz pr.

Jesenik, 24 July 1974, Singer C5664 (F!, holo-

type).

MACROMORPHOLOGY (Teste Singer, ibid.)— Pi-

leus 10-24 mm broad, convex, soon becoming

plane to centrally depressed, when fresh glabrous

or subglabrous, fibrous to filamentous when dried,

strongly hygrophanous, red-brown, flesh-colored,

or pallid (e.g., 1 1 B 6 to 1 1 C 6, M&P); disc sub-

tomentose to tomentose, darker red-brown or more

sordid-rose than pileus; margin translucent-striate

or sulcate. Lamellae adnate to decurrent, sub-

crowded to subdistant, moderately broad, flesh-

rose to dull flesh-colored. Stipe 30-62 x 1.8-5.8

mm, equal or thickened at base, glabrous, becom-

ing coarse-fibered and rough, hygrophanous, con-

colorous with pileus or darker brown along basal

half. Basal mycelium white. Basidiospores white

in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 15-30

hyphae; terminal cells of fascicular hyphae (N =

10)33-50.5 x 6-9 /un, filamentous to subclavate,

light yellowish brown in mass; walls up to 0.5 fj,m

thick, light yellowish brown; contents hyaline. Pi-

leus trama tightly interwoven, morphologically

undifFerentiated, hyaline, light yellowish brown to-

ward pileipellis. Lamellar trama parallel, hyphae

3-12 Mm diam., thin-walled, hyaline to light yel-

lowish brown; cells barrel-shaped. Subhymenium

undifferentiated. Basidia (N = 15)35-48.5 x 8.5-

1 3 Mm, clavate, hyaline; sterigmata (2-)4, up to 8

/urn long. Pleurocystidia lacking. Cheilocystidia (N

= 10) 31—47 x 3-7.5 /mi, filamentous to stran-

gulate, hyaline. Basidiospores (excluding orna-

mentation) (N = 30) (6.4-)7.4-10(-13) x (6.4-)7-

10(-12.4) Mm (x = 8.9 ± 1.4 x 8.6 ± 1.3 /mi), Q

= 0.95-1. 18(-1. 28) (Q = 1.04 ± 0.08), globose,

subglobose, or broadly ellipsoid, hyaline, echin-

ulate; echinulae 1 .4-1 .8(-2.3) /im long, not crowd-

ed; hilar appendix 1.3-2 nm long, prominent,

truncate; plage present; contents occasionally uni-

guttulate. Basal mycelium hyphae mostly 3-14 /urn

diam., tightly interwoven, hyaline; cells barrel-

shaped.

COMMENTARY— The basidiospore echinulae were

longer than reported by Singer (1977) ("0,7-1,3

Mm hoch ist, selton 1,5 /tm erreicht").

This taxon is treated as a synonym of L. laccata

var. pallidifolia.

Laccaria kalosperma Beeli, Bull. Soc. Roy. Bot.

Belgique 66: 22. 1933.

TYPE: Goossens 859, Zaire, Binga, December 1929

(BR!, holotype).

COMMENTARY— Micromorphological analysis of

this collection revealed the presence of strongly

reticulate, amyloid basidiospores. I agree with

Heinemann ( 1 964), therefore, that this collection

is a Lactarius, not a Laccaria.

Agaricus laccatus Scopoli, Flora Carniolica 2: 444.

1772. Figure 64d.

TYPE: Sweden, Femjo, 17 August 1964, Singer 4083

(BAFC!, neolypefide Singer, 1967).

MACROMORPHOLOGY (Teste Singer, 1967)— Pi-

leus (6-) 1 5-3 1 mm broad, convex becoming plane,

often slightly depressed, slightly striate, finely fi-

brillose, hygrophanous, reddish brown becoming

pale ochre when dry. Lamellae adnate to adnate-

subdecurrent, moderately distant, broad, pale, dull

reddish color, white from basidiospores when dry.

Stipe 40-60(-80) x 3-5 mm, slightly clavate, fi-

brous with innate fibrils, concolorous with lamel-

lae at apex, brown toward base. Basal mycelium

white. Basidiospores white in mass. Context con-

colorous with surface when moist, becoming white;

odor very weak; taste sweet.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 15-30

hyphae; terminal cells of fascicular hyphae 42-80

MUELLER: SYSTEM ATICS OF LACCARIA (AGARIC ALES)

103

x 8-1 1 nm, filamentous, subclavate or capitate,

light yellowish brown in mass; walls up to 0.5 nm

thick, light yellowish brown; contents hyaline. Pi-

leus trama tightly interwoven, morphologically

undifferentiated, hyaline, light yellowish brown to-

ward pileipellis. Lamellar trama parallel, hyphae

3-12 Mm diam., thin-walled, hyaline; cells barrel-

shaped. Subhymenium undifferentiated. Basidia

35-45 x 14-16 /an, clavate, hyaline; sterigmata

4, up to 12 ^m long. Pleurocystidia lacking. Chei-

locystidia 47-60 x 2.5-5 nm, filamentous, com-

mon, hyaline. Basidiospores (excluding ornamen-

tation) (N = 30) 8.7-9.2(-l 1) x 6.4-7.8(-8.3) Mm

(Jc = 9.2 ± 0.5 x 7.1 ± 0.5), Q = (1.11-)1.18-

1.46 (Q = 1.3 ± 0.08), subglobose to ellipsoid,

hyaline, echinulate; echinulae l-1.8(-2.3) Mm long,

< 1 Mm wide at base; hilar appendix up to 2 Mm

long, prominent, truncate; plage present; contents

occasionally uniguttulate.

COMMENTARY— This taxon is treated in detail

in the section on North American taxa.

Russuliopsis larcina Velenovsky, Novitates My-

cologicae. p. 77. 1939.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Velenovsky, ibid.}—

Pileus 1 0 mm broad, plane, becoming depressed,

glabrous, translucent-striate, dirty ochre-yellow.

Lamellae adnate, not decurrent, crowded, nar-

rowed at margin, white, becoming clay-colored.

Stipe 2-3 times longer than pileus diameter, 1-

1.5 mm broad, equal, straight, glabrous, translu-

cent, fragile.

MICROMORPHOLOGY (Teste Velenovsky, ibid.)—

Basidiospores 3-5 pm diam., globose, smooth.

COMMENTARY— Type material of this taxon was

not found at either PRM or PRC. Based on the pro-

tologue, this is not a Laccaria.

Laccaria lateritia Malencon, Bull. Soc. Mycol.

France 82: 189. 1966. Figure 65a.

TYPE: Morocco, I.S.C., Malencon No. 5102 (Her-

barium G. Malencon, holotype).

Specimen examined as representative material: Uru-

guay, Montevideo, 1927, Felippone No. 2800 (MPU).

MACROMORPHOLOGY (Teste Malencon, ibid.)—

Pileus 10-25 mm broad, thin, almost hemispher-

ical to convex, centrally truncate or slightly de-

pressed, becoming plane, when wet pellucid-stri-

ate to disc, not striate when dry, hygrophanous,

indistinctly reddish brown to dark brick red (8,

78, 82, Klincksieck), becoming pallid. Lamellae

mostly adnate to arcuate, moderately crowded,

thick, broad, pallid rose-colored to purple-ochra-

ceous (87 or 92, Klincksieck). Stipe 20-25 x 2-5

mm, thickened at base, striate, often compressed-

sulcate and twisted, reddish brown, base vina-

ceous when immature (39, 54, 58, Klincksieck;

Seguy 102, 106; Saccardo badius), lacking purple

color when mature, pallid when dry. Basal my-

celium white. Basidiospores white in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 10-20

hyphae; terminal cells of fascicular hyphae fila-

mentous, subclavate or occasionally clavate, light

yellowish brown in mass; walls up to 0.5 Mm thick,

light yellowish brown; contents hyaline to light

yellowish brown. Pileus trama tightly interwoven,

morphologically undifferentiated, hyaline, light

yellowish brown toward pileipellis. Lamellar tra-

ma parallel; hyphae mostly 3-10.5 nm diam., thin-

walled, hyaline to light yellowish brown; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia (N = 15) 29^*6 x 8-1 1

Mm, clavate, hyaline; sterigmata 2, up to 10 nm

long. Pleurocystidia lacking. Cheilocystidia not

observed. Basidiospores (excluding ornamenta-

tion) (N = 30) 8.3-1 1(-13.3) x 8.3-10.6(-13.3)

Mm (Jc = 9.7 ± 1.04_x 9.5 ± 1.1 Mm), Q =

(0.95-)1-1.06(-1.11) (Q = 1.02 ± 0.03), globose,

subglobose or rarely broadly ellipsoid, echinulate;

echinulae 0.8-1.4 Mm long, crowded; hilar appen-

dix 1.5-2.5 Mm long, prominent, truncate; plage

present; contents occasionally uniguttulate. Basal

mycelium hyphae mostly 2.5-7 Mm diam., narrow,

morphologically undifferentiated, tightly inter-

woven, hyaline.

COMMENTARY— The micromorphological de-

scription above was based on an authentic collec-

tion on loan from Montpellier because the holo-

type was not available for study. Two of the four

authentic collections located were not suitable. One

collection was badly contaminated, and the other

packet stated that it was a robust form of the taxon

and, therefore, was not typical. The collection used

was also somewhat contaminated, and pileipellis

characters were difficult to ascertain and the pres-

ence of cheilocystidia was impossible to deter-

mine. Malencon (1966) stated that this was the

first collection that he saw of this taxon.

This taxon is treated as a synonym ofL.frater-

na.

104

FIELDIANA: BOTANY

FIG. 65. Representative basidiospores from type or representative specimens: a, L. lateritia (representative spec-

imen); b, L. lilacina (holotype); c, L. longipes (holotype); d, L. masonii (holotype). Scale line = 10 MHI.

I .;uvaria lilacina Stevenson, Kew Bull. 19: 3. 1964.

Figure 65b.

TYPE: New Zealand, Woodside, 1 July 1955, Steven-

son 924 (K!, holotype).

MACROMORPHOLOGY (Teste Stevenson, ibid.)—

Pileus 40-55 mm broad, convex to plane, fibril-

lose, becoming finely scaly due to cuticular dif-

fraction, fawn-colored with fulvous fibrils; margin

upturned, often split. Lamellae adnate, distant, li-

lac, mealy. Stipe 100 x 30-40 mm, subfibrous,

silky striate, dull fawn. Basal mycelium white. Ba-

sidiospores white in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with large fascicles of ± perpen-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

105

dicular hyphae; fascicles composed of up to 40

hyphae; terminal cells of fascicular hyphae (N =

10) 39-60 x 5-12.5 jim, filamentous to subcla-

vate, dark yellowish brown in mass; walls up to

0.5 Mm thick, light yellowish brown; contents dark

yellowish brown. Pileus trama tightly interwoven,

morphologically undifferentiated, hyaline, light

yellowish brown toward pileipellis. Lamellar tra-

ma parallel to subparallel; hyphae 3-9 iim diam.,

thin-walled, hyaline to light yellowish brown; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia (N = 15) 37-50.5 x 7-

1 1 jim, clavate, hyaline; sterigmata 4, up to 10 nm

long. Pleurocystidia lacking. Cheilocystidia not

observed. Basidiospores (excluding ornamenta-

tion) (N = 30) 7-9.7 x 7-9.7 Mm (x = 8.4 ± 0.7

x 8.3 ± 0.7 urn), Q = 1-1.07 (Q = 1.01 ± 0.03),

globose, occasionally subglobose, hyaline, echin-

ulate; echinulae (0.8-)1.4-1.8(-2.3), up to 1 ^m

wide at base, crowded; hilar appendix 1.3-2.5 nm

long, prominent, truncate; plage present; contents

occasionally uniguttulate. Basal mycelium hyphae

3-8 nm diam., morphologically undifferentiated,

tightly interwoven, hyaline; wall up to 0.5 jim thick.

COMMENTARY— The basidiospore size and

echinulae length reported here are somewhat larg-

er than those presented in Stevenson's original de-

scription ("Sporae 7-8 nm diam., spinis 0,5-1 nm

longis").

This obviously represents a distinct taxon. An

examination of additional material is necessary

before comments on its relationships to other taxa

can be made.

Clitocybe laccata f. lilipuntruana Rick, Broteria,

Ser. Bot. 24: 100. 1930.

TYPE: Lacking.

COMMENTARY— No authentic material of this

taxon nor a copy of the original description was

located.

Russuliopsis lineata Velenovsky, Ceske Houby. p.

279. 1920.

TYPE: Housed at PRC?

MACROMORPHOLOGY (Teste Pilat, 1948)— Pile-

us 10-20 mm diam., obtuse to convex, becoming

plane, occasionally slightly umbonate, translu-

cent-striate, hygrophanous, honey-colored to

somber brown when fresh, almost white when dry.

Lamellae broad, thin, becoming rounded-free, far-

inaceous, white. Stipe 2—4 times longer than pileus

diameter, 2-3 mm thick, equal, base not thick-

ened, glabrous to finely fibrillose, longitudinally

striate, covered with white basidiospores at apex,

light gray color. Basidiospores white in mass.

MICROMORPHOLOGY (Teste Pilat, 1948)— Basid-

iospores 8-9 /im diam., globose, thick- walled,

echinulate, hyaline.

COMMENTARY— A formalin-preserved speci-

men of this taxon sent from PRC was never re-

ceived. Without additional micromorphological

data, it is impossible to clarify the concept of this

taxon.

Laccaria longipes G. M. Mueller, Mycotaxon 40:

145-150. 1991. Figure 65c.

TYPE: Canada, Ontario, Nipissing District, Algon-

quin Provincial Park, Spruce Bog Trail, among

Sphagnum under Picea marinara, Larix laricina

and Alnus rugosa, 18 September 1984, G. M.

Mueller 1929 (F!, holotype).

MACROMORPHOLOGY (Mihi)— Pileus 11 -21 (-5 5)

mm broad, convex, often centrally depressed,

slightly to moderately translucent-striate, finely fi-

brillose, orange-brown (6B7-6C7) fading to buff in

age; margin incurved, decurved, or plane, entire

to undulate, becoming slightly eroded. Lamellae

adnate, distant, thick, up to 10 mm broad, light

flesh color (near 6A2). Stipe 67-138 x 3-8 mm,

equal with slightly swollen base, dry, slightly to

moderately fibrillose-striate, concolorous with pi-

leus. Basal mycelium white. Basidiospores white

in mass.

MICROMORPHOLOGY (Mihi) — Pileipellis of

tightly interwoven hyphae with scattered fascicles

of 10-20 ± perpendicular hyphae; terminal cells

5-10 jim, filamentous to subclavate, hyaline. Pi-

leus trama tightly interwoven, morphologically

undifferentiated, hyaline to light yellowish brown.

Lamellar trama of parallel to subparallel hyphae,

mostly 3-15 /im diam., thin-walled, hyaline; cells

barrel-shaped. Subhymenium morphologically

undifferentiated. Basidia 28—44 x 7-12 /im, cla-

vate, hyaline; sterigmata 4, up to 8 /im long. Pleu-

rocystidia lacking. Cheilocystidia none seen. Ba-

sidiospores (excluding ornamentation) 7-8. 5 x 5.7-

8 jim (Jc = 7.7 ± 0.5 x 6.9 ± 0.6 ^m), (2=1-

1.27(-1.34) «2 = 1.11 ± 0.08), subglobose to

broadly ellipsoid, occasionally globose or ellip-

106

FIELDIANA: BOTANY

sold, hyaline, echinulate; echinulae (0.7-)1-1.5

(-2) Jim long, less than 1 pm wide at base.

SOMATIC CULTURE MAT MORPHOLOGY: See the

description under L. longipes in the section on

North American taxa.

COMMENTARY— This taxon is treated in detail

in the section on North American taxa.

Agaricus (Clitocybe) laccatus var. lutea Fries, Ep-

icr. syst. mycol. p. 79. 1836-1838.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Fries, ibid.)— As in

type variety, lamellae flesh color.

COMMENTARY— This taxon is treated as a syn-

onym of L. laccata.

Agaricus (Clitocybe) laccatus var. [pileo] luteovio-

laceo Fries, Epicr. syst. mycol. p. 79. 1836-

1838.

TYPE: Lacking.

MACROMORPHOLOGY (Teste Fries, ibid.)— Pileus

drying ochraceous. Lamellae violaceous.

COMMENTARY— It is common for the lamellae

of older specimens of Laccaria to turn violaceous

as a result of drying or possible contamination. As

this character by itself is not sufficient to warrant

segregation, this taxon is treated as a synonym of

L, laccata.

Hygrophorus maritimus Teodorowicz, Grzby

wyzsze Poleskiego wybrzeza. 1936.

TYPE: Figure 5 in Teodorowicz, Grzyby wyzsze pol-

skiego wybrzeza, Towarzystwo naukowe w To-

runiu Badania Przyrodnicze Pomorskie 2: 31.

1936. (lectotype./afc Mueller, 1991a).

MACROMORPHOLOGY (Teste Teodorowicz,

ibid.)— Pileus 1 5-45 mm broad, convex becoming

depressed, glabrous, appearing moist when humid,

reddish flesh color; margin always unequal,

toothed. Lamellae sinuate to arcuate, 0.5-1 mm

thick, entire, reddish flesh color, drying dark brown.

Stipe 7-35 x 6-12 mm, occasionally swollen at

base, fibrillose, concolorous with pileus, apex often

becoming lighter.

MICROMORPHOLOGY (Teste Teodorowicz,

/&W.)-Basidia 25-38(-50) x 7.5-1 1 /mi, 2-4 ste-

rigmate. Cystidia lacking. Basidiospores 12.5-17.5

x 5.5-9 Aim, ellipsoid to irregularly ovoid, hyaline

to greenish, glabrous or granular.

COMMENTARY— Although no type specimen was

found, the illustration and description presented

in the protologue match the common usage of this

name. This taxon is treated in detail in the section

on North American taxa.

Laccaria masonii Stevenson, Kew Bull. 19: 4. 1964.

Figure 65d.

TYPE: New Zealand, Silverstream, 19 July 1949, Ste-

venson 733 (K.!, holotype).

MACROMORPHOLOGY (Teste Stevenson, ibid.,

McNabb, 1972)— Pileus 0.5-3 cm broad, convex

to plano-convex when young, occasionally ap-

planate, glabrous or minutely furfuraceous at disc,

pellucid-striate at margin, hygrophanous, viola-

ceous when young, fading to buff at maturity. La-

mellae adnexed to adnate, distant, up to 4 mm

broad, pallid violaceous when young, becoming

pallid brownish pink, occasionally with faint vi-

olaceous tints remaining. Stipe 30- 100 x 1-3 mm,

swollen at base, longitudinally fibrillose-sulcate,

often twisted, violaceous when young, fading to

buff with maturity; apex at times with violaceous

tints. Basal mycelium pallid violaceous. Basidio-

spores white in mass.

MICROMORPHOLOGY (Mihi)— Pileipellis of in-

terwoven hyphae with scattered fascicles of ± per-

pendicular hyphae; fascicles composed of 5-1 0 hy-

phae; terminal cells (N = 10) 46-67 x 8-13 /mi,

filamentous to subclavate, light yellowish brown

in mass; walls up to 0.5 nm thick, light yellowish

brown; contents hyaline. Pileus trama tightly in-

terwoven, morphologically undifferentiated, hya-

line, light yellowish brown toward pileipellis. La-

mellar trama parallel to subparallel; hyphae 2.5-

6.5 diam., thin-walled, hyaline to light yellowish

brown; cells barrel-shaped. Subhymenium mor-

phologically undifferentiated. Basidia (N = 15)

29.5-44 x 7.5-10.5 ^m, clavate, hyaline; sterig-

mata 4, up to 10 ^< m long. Pleurocystidia lacking.

Cheilocystidia not observed. Basidiospores (ex-

cluding ornamentation) (N = 30) 7.8-9.7(-10.6)

x (7.4-)7.8-9.7(-10.6) Mm (x =_8.9 ± 0.8 x 8.7

±0.8 /mi), Q= 1-1.06(-1.11)(Q= 1.02 ± 0.03),

globose to subglobose, hyaline, strongly echinu-

late; echinulae (1.4-)2.3-4.6(-6.5) Aim long, up to

1.8 /tm wide at base, occasionally curved, not

crowded; hilar appendix 1.3-2.5 nm long, prom-

MUELLER: SYSTEMATICS OF LACCARIA (AGARICALES)

107

inent, truncate; plage present; contents occasion-

ally uniguttulate. Basal mycelium hyphae mostly

3-5.5 Mm diam., tightly interwoven, hyaline; cells

filamentous to barrel-shaped.

COMMENTARY— Two taxa were included in the

protologue that accompanied Stevenson's original

description of L. masonii. The type collection con-

sists entirely of basidiocarps with glabrous pilei,

and the epithet is restricted to that circumscrip-

tion. McNabb (1972) proposed L.fibrillosa to rep-

resent the other taxon represented in the descrip-

tion.

served. Basidiospores (excluding ornamentation)

(N = 30) 7-8.7(-9.2) x 7-8.7 Mm (x = 8 ± 0.6 x

7.9 ± 0.6 Mm), Q = 1-1.06 (Q = 1.01 ± 0.02),

globose, rarely subglobose, hyaline, echinulate;

echinulae 1-1.8 Mm long, moderately crowded; hi-

lar appendix 1.3-1.8 /im long, prominent, trun-

cate; plage present; contents occasionally unigut-

tulate. Basal mycelium hyphae mostly 4-9 /*m

diam., morphologically undifferentiated, tightly

interwoven, hyaline.