2008 - Larsson e Jeppson - Phylogenetic Relationships Among Species and Genera

mycological research 112 (2008) 422
journal homepage: www.elsevier.com/locate/mycres
Phylogenetic relationships among species and genera

of Lycoperdaceae based on ITS and LSU sequence
data from north European taxa
Ellen LARSSONa,*, Mikael JEPPSONb
a
Plant and Environmental Sciences, Goteborg University, Box 461, SE-40530 Goteborg, Sweden
Lilla Hajumsgatan 4, SE-46135 Trollhattan, Sweden
article info
abstract
Article history:
Phylogenetic relationships, limits of species, and genera within Lycoperdaceae, were
Received 19 March 2007
inferred by use of ITS and LSU nu-rDNA sequence data. Lycoperdaceae was confirmed as
Received in revised form
monophyletic, and Mycenastrum corium as a sister taxon to the ingroup. Four major clades
19 September 2007
were identified and received weak to moderate support and correspond with the genera
Accepted 15 October 2007
Lycoperdon, Bovista, Calvatia, and Disciseda. The Lycoperdon clade includes species from Lyco-
Corresponding Editor:
perdon, Vascellum, Morganella, Handkea, Bovistella, and Calvatia. The structure within the
David L. Hawksworth
Lycoperdon clade is unresolved and several clades are more or less unsupported, which suggests treating the supported Lycoperdon clade as the genus Lycoperdon. L. nigrescens and
Keywords:
L. caudatum occur on single branches and their phylogenetic positions could not be re-
Agaricales
solved. The phylogenetic analyses identified 31 species of Lycoperdon, 11 species of Bovista,
Basidiomycota
six species of Calvatia, and two species of Disciseda. In Lycoperdon three new species were
Gasteromycetes
recognized. A new species closely related to B. limosa is identified and discussed. A classi-
Molecular systematics
fication of Lycoperdaceae is proposed based on the results of the phylogenetic analyses.
Taxonomy
Morphological characters of species within and among identified clades are discussed.
2007 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
Introduction
The puffball family Lycoperdaceae includes species with
enclosed basidiocarps and a pure white gleba that at maturity
turns into a brown powder of trillions of spores, puffing out
from the apical opening of the endoperidium. The species
have a saprotrophic habit, either growing on dead wood, or
on the ground in forest or open grassland. The family comprises about 150 species worldwide (Kirk et al. 2001) and in
general the species have a wide distribution range.
Lycoperdaceae has traditionally been classified in the Gasteromycetes as one of the families of Lycoperdales (Demoulin 1968;
Demoulin 1969; Dring 1973; Kreisel 1969a; Pegler et al. 1995;
Pilat 1958). The family initially contained various types of

puffballs and earthstars. Hollos (1904) divided the family
into ten genera: Battarrea, Tylostoma (Tulostoma), Myriostoma,
Geaster (Geastrum), Astraeus, Calvatia, Lycoperdon, Disciseda,
Bovista, and Mycenastrum. Later Fischer (1933) added some
poorly known non-European genera such as Lycoperdopsis
and Bovistoides, but excluded Battarrea, Tulostoma, Astraeus,
and Geastrum, which he transferred to the families Tulostomataceae, Sclerodermataceae, and Geastraceae respectively. Pilat
(1958) included seven genera: Calvatia, the new genus Vascellum (segregated from Lycoperdon), Lasiosphaera (syn. Langermannia), Lycoperdon, Bovista, Bovistella, and Disciseda.
Mycenastrum was excluded and placed in a separate family,
* Corresponding author.
E-mail address: ellen.larsson@dpes.gu.se
0953-7562/$ see front matter 2007 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.mycres.2007.10.018
Phylogeny of Lycoperdaceae
Mycenastraceae, a concept introduced already by Zeller (1949).

In a circumscription of Lycoperdaceae published by Kreisel
(1962) eight north European genera were included: Langermannia, Lycoperdon, Vascellum, Calvatia, Disciseda, Bovista, Bovistella,
and Mycenastrum. Later Kreisel (1969a) gave an outline of the
family on a worldwide basis and then accepted Bovista, Bovistella, Calbovista, Calvatia, Disciseda, Langermannia (including
Lanopila), Lycoperdon, Morganella, and Vascellum. In subsequent
publications Kreisel segregated the new genus Handkea from
Calvatia and referred Langermannia back to Calvatia (Kreisel
1989, 1992). The generic concepts used by Kreisel have gained
wide acceptance, especially in Europe (Pegler et al. 1995;
Sarasini 2005). Important macro- and micromorphological
characters used to delineate more narrowly defined genera include presence or absence of a true capillitium, the structure
of the capillitial threads, the opening pattern of the endoperidium, and the presence or absence of a subgleba.
Phylogenetic analyses based on nu-rDNA, have shown that
Lycoperdaceae is a family within Agaricales (Hibbett et al. 1997;
Moncalvo et al. 2002) and form a separate monophyletic gasteroid lineage within the lepiotoid fungi (Hibbett & Thorn 2001;
Kruger et al. 2001; Vellinga 2004). Molecular studies have also
indicated that Lycoperdon, as circumscribed in the current morphology-based classification, is polyphyletic and that genus
boundaries within Lycoperdaceae are unclear (Bates 2004; Kruger
et al. 2001; Kruger & Kreisel 2003). Based on phylogenetic analyses of ITS rDNA sequence data, Kruger & Kreisel (2003) transferred the lignicolous species L. pyriforme to Morganella and
proposed a new subgenus Apioperdon to accommodate lignicolous species having an unpitted true capillitium and a permanently white subgleba. Bates (2004) performed morphological
studies and phylogenetic analyses based on ITS sequences of
a wide range of gasteroid fungi from the state of Arizona,
including 29 species of Lycoperdaceae. The results were ambiguous regarding the transfer of L. pyriforme to Morganella.
In the present study phylogenetic analyses based on ITS
and LSU rDNA sequence data are used to further explore the
relationships and boundaries of species and genera within
Lycoperdaceae. The selected taxa represent the majority of species occurring in North Europe.
Materials and methods

Morphological studies
Morphological studies were performed in accordance with the
criteria set out by Demoulin (1972a) and Kreisel (1962, 1967).
Microscopical structures were studied from dried material of
fully mature fruiting bodies. Spores and capillitium were
mounted in lactophenol Cotton Blue and heated to boiling
for a few seconds. Spores were measured excluding the
ornamentation. Peridial structures were studied in 3 % KOH,
chloral hydrate, and Melzers reagent.
Material studied
Most studied specimens originate from Fennoscandia or Iceland whereas a few complimentary samples were collected in
south and central Europe, Asia (Russia and Nepal), Greenland,
Svalbard, and North America. Data on sequenced specimens

are provided in Table 1. Vouchers are deposited at the herbarium of the Department of Plant and Environmental Sciences,
Goteborg University (GB), if not otherwise indicated.
Additional specimens examined morphologically during
this study are listed below:
Bovista aestivalis. Denmark: N. Jylland: Tranum: Tranums strand,
17 Oct. 1993, M. Jeppson 3630 (MJ). Finland: North Karelia: Ilomantsi:
Mekrijarvi, 30 Aug. 1996, M. Jeppson 3712 (MJ). Pera-Pohjanmaa:
Kemi: Ajos, 29 Sep. 1984, M. Kamula (OULU as B. dryina). Hungary:
Bacs-Kiskun: Felegyhaza: Also-Monostor, 25 Sep. 1995, M. Jeppson
3828 (MJ). Sweden: Skane: Hofterup: Jaravallen, 18 Aug. 1987,
M. Jeppson 2271 (MJ). Oland: Hulterstad: Gosslunda, 10 Sep. 1988,
lvkarleby: A
lvkarlebybruk, 19
M. Jeppson 2636 (MJ). Uppland: A
Aug. 1978, M. Jeppson 1122 (MJ).
Bovista cretacea. Iceland: Nordur Mulasysla: Droplaugsstadir, 3
Aug. 1962, H. Hallgrmsson (ANMH). Norway: Oppland: Dovre:
Grimsdalen: Tverrai, calcareous soil in Dryas-vegetation, slopes
along river, alt. 920 m, 18 Sep. 1983, T. Schumacher & K. Ostmoe
D214/83 (O). Sweden: Torne Lappmark: Jukkasjarvi, 1 km S of
Abisko, 26 Aug. 1966, R. Rydberg (S).
rkeny, sand steppe vegetaBovista furfuracea. Hungary: Pest: O
tion, 2 Nov. 2002, J. & M. Jeppson 6025 (MJ). Sweden: Oland: Gardby:
Heden, sand steppe vegetation, 5 Oct. 2003, S., J. & M. Jeppson 5621
(MJ). Gotland: Vamlingbo: Nackshajd, calcareous grassland, 27 Sep.
sterplana: O
ster2001, J. & M. Jeppson 5629 (MJ). Vastergotland: O
plana Hed Nature Reserve, calcareous grassland, 2 Aug. 1998, S.
& J. Jeppson (MJ).
Bovista graveolens. Spain: Gerona: Espinelves, 28 Oct. 1985, M.
Jeppson (MJ, MA-F).
Bovista limosa. Finland: Kuusamo: Sirkapuro, mossy road verge, 24
Aug. 1978, A. Bohlin, J. & M. Jeppson 1146 (MJ). Norway: Nordland: Bjerkvik, NE side of Rombaken, sand pit at main road, with small Salix and
Betula, 16 Aug. 1999, J. Vauras (MJ, ex herb. TURA 8618). Oppland:
Bovertun, subalpine Dryas heath, 30 Aug. 1997, J. & M. Jeppson 4296
(MJ). Dovre: Grimsdalen: Verketster: Gygergeitene, road bank, alt.
ca 900 m, 9 Aug. 1995, J. & M. Jeppson 3742 (MJ). Sweden: Harjedalen:
Funasdalen: Fjallnas, 23 Jul. 1999, S., J. & M. Jeppson 5221 (MJ).
Bovista cfr limosa. Belgium: Antwerpen: Blokkerdijk, on calcareous
sand, 5 Aug. 1987, M. Jeppson (MJ). Estonia: Saaremaa: Mandjala,
sandy road verge, 25 Sep. 1990, V. Liiv & M. Jeppson 2934 (MJ). Kipi,
dry sandy heath, 25 Sep. 1990, V. Liiv & M. Jeppson 2962 (MJ).
Norway: Akershus: Malmykalven, among mosses on calcareous
rocks, 13 Oct. 2006, A.-E. Torkelsen et al. (MJ). Sweden: Bohuslan:
Askum: Ramsvik, Haby, 19 Sep. 2001, T. Schultz & M. Jeppson (MJ).
Dalsland: Skallerud, Ryr Nature Reserve, among mosses on thin
soil on cliffs of calcareous clay shale, 11 Sep. 1990, M. Jeppson 3035
(MJ). Gotland: Gammelgarn, Grogarnsberget, 26 Sep. 2001, J. & M. Jeppson 5599, 5600 (MJ). Sandviken Nature Reserve, 26 Sep 2001, J. & M.
Jeppson 5584 (MJ). Sundre: Hallbjans, 27 Sep. 2001, J. & M. Jeppson 5627
(MJ). Burgsvik: Hundlausar, 27 Sep. 2001, J. & M. Jeppson 5617 (MJ);
Vamlingbo, Nackshajd, 27 Sep. 2001, J. & M. Jeppson 5618 (MJ); Vaskinde, Brucebo Nature reserve, 24 Sep. 2001, J. & M. Jeppson 5528 (MJ).
Narke: Glanshammar, 450 m NE of church, 12 Nov. 2005, M. Jeppson
7688 (MJ);. Sodermanland: Morko: Egelsvik, 5 Nov. 2004, M. Jeppson
6969 (MJ). Uppland: Djuro: Runmaro: W of Vittrask, on moss tussocks
on calcareous rocks, 5 Nov. 2004, M. Jeppson 6936 (MJ); Dalaro: Uto:
Kroka, on moss tussocks on calcareous rocks, 4 Nov. 2004, M. Jeppson
6910 (MJ). Vastergotland: Dala: Djupadalen Nature Reserve, 4 Nov.
sterplana Hed Nature Re1994, M. Jeppson 3628 (MJ). Osterplana, O
serve, 28 Aug. 1988, S., J. & M. Jeppson 2562 (MJ). Oland: Hogby: Dodevi,
4 Oct. 1996, H. Kreisel, J. & M. Jeppson 3970 (MJ); Resmo, W of Mockelmossen, alvar vegetation, 27 Oct. 1976, J. & M. Jeppson 985 (MJ); Kastlosa: Gettlinge, alvar vegetation, 7 Oct. 1999, J. & M. Jeppson (MJ).
Gardslosa: Lindby, 9 Oct. 1999, M. Jeppson 5172 (MJ).
Bovista nigrescens. Denmark: N. Jylland: V. Torup: Bulbjerg, dry
grassland, 18 Oct. 1998, M. Jeppson 3645 (MJ). Sweden: Vastergotland: Gokhem: Dalasen, grazed grassland, 27 Sep. 1987, M. Jeppson
E. Larsson, M. Jeppson
Table 1 Data of specimens sequenced in this study, named according to the proposed molecular based classification
Proposed taxonomy
Bovista aestivalis
Bovista aestivalis
Bovista cretacea
Bovista cretacea
Bovista furfuracea
Bovista graveolens
Bovista limosa
Bovista cfr limosa
Bovista nigrescens
Bovista paludosa
Bovista plumbea
Bovista promontorii
Bovista tomentosa
Bovista tomentosa
Calvatia candida
Calvatia craniiformis
Calvatia gigantea
Disciseda bovista
Disciseda candida
Lycoperdon altimontanum
Lycoperdon altimontanum
Lycoperdon atropurpureum
Lycoperdon caudatum
Lycoperdon cretaceum
Lycoperdon cretaceum
Lycoperdon decipiens
Lycoperdon decipiens
Lycoperdon dermoxanthum
Lycoperdon echinatum
Lycoperdon ericaeum
Lycoperdon ericaeum
Lycoperdon excipuliforme
Lycoperdon frigidum
Lycoperdon frigidum
Lycoperdon frigidum
Lycoperdon frigidum
Lycoperdon frigidum
Lycoperdon frigidum
Lycoperdon lambinonii
Lycoperdon lambinonii
Lycoperdon lividum
Lycoperdon lividum
Lycoperdon mammiforme
Lycoperdon marginatum
Lycoperdon molle
Lycoperdon molle
Lycoperdon muscorum
Lycoperdon nigrescens
Lycoperdon niveum
Lycoperdon niveum
Lycoperdon niveum
Lycoperdon niveum
Lycoperdon cfr niveum
Lycoperdon norvegicum
Lycoperdon perlatum
Lycoperdon pratense
Lycoperdon pratense
Lycoperdon pratense
Lycoperdon pyrifome
Lycoperdon radicatum
Lycoperdon sp. 1
Lycoperdon sp. 1
Origin
Collection ID
Herbarium
GenBank accession no.
Sweden
Sweden
Iceland
Norway
Sweden
Sweden
Sweden
Sweden
Sweden
Norway
Sweden
Spain
Sweden
USA
Hungary
USA
Sweden
Sweden
Sweden
Norway
Nepal
Sweden
Sweden
Sweden
Sweden
Iceland
Norway
Sweden
Sweden
Sweden
Sweden
Sweden
Sweden
Sweden
Greenland
Iceland
Norway
Norway
Svalbard
Sweden
Belgium
Norway
Sweden
Nepal
Sweden
USA
Norway
Sweden
Sweden
Sweden
Iceland
Iceland
Iceland
Norway
Sweden
Sweden
Sweden
Czechia
Russia
Sweden
Sweden
USA
Norway
Norway
M. Jeppson 1122
M. Jeppson 3860
Hallgrmsson 11622
M. Jeppson 5702
M. Jeppson 5435
Widgren 030816
M. Jeppson 5226
M. Jeppson 3971
M. Jeppson 7719
M. Jeppson 4301
M. Jeppson 4856
M. Jeppson 7770
M. Jeppson 5433
Steinke 951015
M. Jeppson 3514
Steinke 001017
M. Jeppson 3566
M. Jeppson 5078
M. Jeppson 3588
M. Jeppson 4270
Dobremezdholotypus
M. Jeppson 3269
M. Jeppson 3269
M. Jeppson 6150
R-G. Carlsson 920818
M. Jeppson 4105
M. Jeppson 4302
M. Jeppson 4330
M. Jeppson 7715
M. Jeppson 4568
M. Jeppson 6498
M. Jeppson 4866
M. Jeppson 5395
M. Jeppson 6467
Lange 901009
M. Jeppson 4088
Eckblad 151507
M. Jeppson 4273
Lange 191
M. Jeppson 7716
Demoulin 4622
M. Jeppson 5245
M. Jeppson 4005
Dobremez 19740514
M. Jeppson 4841
Anderson & Parker 750822
M. Jeppson 4260
M. Jeppson 4557
M. Jeppson 7717
M. Jeppson 5376
M. Jeppson 4068
M. Jeppson 4109
M. Jeppson 484
M. Jeppson 5267
M. Jeppson 5594
M. Jeppson 5453
M. Jeppson 4684
M. Jeppson 5880
S-A. Hanson 20000915
M. Jeppson 4864
M. Jeppson 4849
Parker 970911
M. Jeppson 4277
M. Jeppson 4285
GB
GB
AMNH
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
Herb. Kreisel
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
C
GB
O
GB
C
GB
GB
GB
GB
Herb. Kreisel
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
GB
DQ112620
DQ112619
DQ112611
DQ112610
DQ112622
DQ112618
DQ112615
DQ112614
DQ112612
DQ112609
DQ112613
DQ112621
DQ112616
DQ112617
DQ112624
DQ112625
DQ112623
DQ112627
DQ112626
DQ122588
DQ112589
DQ112586
DQ112586
DQ112587
DQ112633
DQ112597
DQ112598
DQ112582
DQ112583
DQ112579
DQ112578
DQ112606
DQ112605
DQ112590
DQ112563
DQ112564
DQ112560
DQ112562
DQ112559
DQ112561
DQ112575
DQ112576
DQ112600
DQ112599
DQ112567
DQ112632
DQ122566
DQ112565
DQ112604
DQ122577
DQ112571
DQ112570
DQ112568
DQ112569
DQ112572
DQ112631
DQ112630
DQ112556
DQ112555
DQ112554
DQ112558
DQ112608
DQ112574
DQ112573
Table 1 (continued)
Proposed taxonomy
Lycoperdon sp. 2
Lycoperdon sp. 2
Lycoperdon sp. 2
Lycoperdon sp. 3
Lycoperdon sp. 3
Lycoperdon turneri
Lycoperdon turneri
Lycoperdon turneri
Lycoperdon umbrinum
Lycoperdon umbrinum
Lycoperdon umbrinum
Lycoperdon utriforme
Mycenastrum corium
Tulostoma kotlabae
Tulostoma squamosum
Origin
Sweden
Sweden
Sweden
Norway
Sweden
Greenland
Norway
Norway
Sweden
Sweden
Sweden
Sweden
Sweden
Hungary
Austria
Collection ID
M. Jeppson 6377
M. Jeppson 6394
L. Orstadius 148-03
M. Jeppson 4304
Vetter 407
Lange 08-95
M. Jeppson 4265
M. Jeppson 5251
M. Jeppson 4556
M. Jeppson 4556a
M. Jeppson 4559
M. Jeppson 5388
M. Jeppson 5467
M. Jeppson 6623
Mrazek 1300
2338 (MJ). Harjedalen: Funasdalen: Mittaklappen, 6 Aug. 2004,

S. Jeppson (MJ).
Bovista paludosa. Sweden: Vastergotland: Mularp: Esbjorntorpskarret, calcareous fen, 20 Aug. 1988, J. & M. Jeppson 2517 (MJ). Jamt stersund: Tysjoarna, among mosses in calcareous fen, 31
land: O
Aug. 1991, M. Karstrom (MJ).
Bovista plumbea. Czechia: Praha: Prokopske udoli: Jinonice,
steppe vegetation, 5 Nov. 2001, J. & M. Jeppson 5895 (MJ). Sweden:
Gotland: Gammelgarn: Skags, dry calcareous grassland, 26 Sep.
2001, J. & M. Jeppson 5583 (MJ). Uppland: Dalaro: Uto: Gruvbryggan,
4 Nov. 2004, M. Jeppson 6925.
Bovista promontorii. Portugal: Baixo Alentejo: Grandola: Melides,
among Carpobrotus on sandy soil, 6 Jan. 2006, J. & M. Jeppson (MJ).
Bovista tomentosa. Estonia: Parnu: Rannemetsa, dry sandy road
verge, 18 Aug. 1989, M. Jeppson 2844 (MJ). Hungary: Bacs-Kiskun:
Szikra, 17 Feb. 2002, J. & M. Jeppson 6631 (MJ). Sweden: Skane: Maglehem, Kumlan Nature Reserve, sand steppe vegetation, 15 Oct.
1995, M. Jeppson 3332 (MJ). Sodermanland: Tystberga: Nynas, among
mosses on calcareous rocks, 19 Sep. 2004, M. Jeppson 7241 (MJ).
Calvatia candida. France: Pyrenees Orientales: La Tour de Carol:
Yravals, dry grassland, 30 Dec. 1983, M. Jeppson 1592 (MJ). Hungary:
rkeny, sand steppe vegetation, 5 Nov. 2002, J. & M. Jeppson
Pest: O
(MJ). Spain: Barcelona: Maresme, Mataro, Can Vilardell, dry, sandy
road verge in Pinus halepensis forest, 1 Nov. 1998, S., J. & M. Jeppson
4729 (MJ).
Calvatia craniiformis. USA: Wisconsin: Dane County: Mazomanie,
Sand Barrows, 3 Oct. 1993, A. D. Parker (MJ).
Calvatia fragilis. France: Pyrenees Orientales: La Tour de Carol:
Yravals, dry grassland, 11 Dec. 1985, M. Jeppson (MJ). Spain: Sevilla:
Aznalcollar: Finca Garci Bravo, sheep-grazed grassland, 31 Dec.
2002, S., J. & M. Jeppson 6165 (MJ).
Calvatia gigantea. Sweden: Bohuslan: Tossene, Gerlesborg, among
Urtica close to farm houses, 3 Oct. 1992, J. & M. Jeppson 3164 (MJ).
Skane: Vittskovle: Drivan, 14 Oct. 1995, M. Jeppson 3317 (MJ).
Disciseda bovista. Hungary: Bacs-Kiskun: Szikra, sand steppe vegetation in road verge, 17 Feb. 2004, J. & M. Jeppson 6615 (MJ). Slovakia: Zahorie: Malacky, Svaty Jan, Borova, sandy grassland, 19 Oct.
2004, I. Kautmanova & M, Jeppson 7377 (MJ). Sweden: Gotland:
Hamra: Holmhallar, 12 Oct. 2002, J. & M. Jeppson 6259 (MJ).
Disciseda candida. Hungary: Bacs-Kiskun: Szikra, sand steppe vegetation along railway, 17 Feb. 2004, J. & M. Jeppson 6639 (MJ).
Sweden: Gotland: Lye: Bosarve, sheep-grazed grassland on sandy
soil, 11 Oct. 2002, J. & M. Jeppson 6247 (MJ).
Lycoperdon altimontanum. Norway: Oppland: Dovre: ValasjoenFokstumyrene, 18 Sep. 1984, J. Stordal 23746 (O).
Lycoperdon atropurpureum. Sweden: Ostergotland: V. Tollstad:
Hoje, among fallen leaves at the edge of a beech forest, 9 Sep.
Herbarium
GenBank accession no.
GB
GB
GB
GB
GB
C
GB
GB
GB
GB
GB
GB
GB
GB
GB
DQ112602
DQ112601
DQ112603
DQ112580
DQ112581
DQ112596
DQ112595
DQ112594
DQ112591
DQ112593
DQ112592
DQ112607
DQ112628
DQ112629
DQ415732
1988, J. & M. Jeppson 2585 (MJ). Oland: Hulterstad: Gosslunda, 7

Oct. 1994, J. & M. Jeppson 3263 (MJ).
Lycoperdon caudatum. Sweden: Skane: Vomb: Klostersagen, 16
Sep. 1999, S.-A. Hanson (MJ). Vastergotland: Knatte: Lonnarpssjons
sydspets, calcareous rich fen, 4 Aug. 1998, T. Schultz, A. Bohlin &
M. Jeppson 4787 (MJ).
Lycoperdon cretaceum. Iceland: Sudur Mulasysla: Reydarfjordur:
Holmahals: Dryas-Empetrum heath, 7 Aug. 1993, M. Jeppson 4090
(MJ). Sweden: Lappland: Vilhelmina: Marsfjallen: Graipesvarre, alt.
800 m, in dry heathland with Dryas, 23 Jul. 1998, A. & K. Bohlin (MJ).
Lycoperdon decipiens. Hungary: Pest: Pustavacs: Pustavacsi erdo,
under Quercus on sandy soil, 12 Oct. 2004, T. Knutsson & M. Jeppson
6836 (MJ). Spain: Huelva: Mazagon: El Villar, road verge i Quercus
suber forest, 3 Jan. 2003, S., J. & M. Jeppson 6221 (MJ). Cadiz: Tarifa:
Bolonia, clearing in sandy Pinus pinea forest, 3 Jan. 2005, S., J. &
M. Jeppson 7033 (MJ). Sweden: Dalsland: Skallerud: Ryr, grazed
grassland with Corylus and Pinus, 12 Sep. 2004, J. & M. Jeppson
7085 (MJ). Vastergotland: Berg: Hogsbola ang Nature Reserve, calcareous dry grassland, 8 Aug. 1998, T. Schultz, R.-G. Carlsson & M.
Jeppson 4805 (MJ). Oland: Langlot: Amundsmosse, dry calcareous
grassland, 25 Sep. 2004, J. & M. Jeppson 7156 (MJ).
Lycoperdon dermoxanthum. Denmark: Bornholm: Allinge, Sandvig,
dry, sandy heathland with Calluna and Empetrum, 13 Sep. 1992,
S. & J. Jeppson (MJ). Hungary: Pest: Nagykoros: Csokaserdo, sandy
road verge in oak forest, 12 Oct. 2004, M. Jeppson 6847 (MJ). Slovakia:
Zahorie: Malacky: Kostolice, acidic sand on inland sand dune, 29
Oct. 2000, J. & M. Jeppson 5293 (MJ). Spain: Barcelona: Valle`s Orientals:
Olzinelles, sandy road verge under Quercus ilex, 30 Oct. 1998, S., J. &
M. Jeppson 4715 (MJ). Sweden: Bohuslan: Lyse: Alsback, among
grasses on sandy soil in road verge, 12 Jul. 1998, I. Persson & M. Jeppson 4759 (MJ). Halland: Skummeslov: Skummeslovs strand, in Corynephoretum, 18 Oct. 1999, M. Jeppson 3183 (MJ). Skane: Lyngsjo: S of
Rosengarden, 15 Oct. 1995, M. Jeppson 3350 (MJ); Oland: Hogby:
Dodevi, sandy grassland, 4 Oct. 1998, J. & M. Jeppson 4650 (MJ).
Lycoperdon echinatum. Slovakia: Strazovske vrchy, Pruzina, valley
of Strazovske potok, in beech forest, 7 Oct. 2005, T. Knutsson, J. &
. Karup: Rodhog, in beech
M. Jeppson 7552 (MJ). Sweden: Skane: O
forest, 21 Sep. 1980, J. & M. Jeppson 1433 (MJ). Oland: Hogsrum: Halltrops Hage Nature Reserve, 4 Oct. 2003, J. & M. Jeppson 6498 (MJ).
Lycoperdon ericaeum. Denmark: N. Jylland: Bronden: Nymolle
Baek, grazed grassland, 13 Sep. 1998, M. Jeppson 4872 (MJ)dSlovakia: Zahorie: Senica: Mikulasov, in Corynephoretum, 3 Oct. 2005,
T. Knutsson, J. & M. Jeppson 7507 (MJ). Sweden: Vastergotland: V.
Tunhem: Hastevadet, acidic dry grassland, 20 Sep. 1998, J. & M.
Jeppson 4818 (MJ). Skane: Fjalkinge: Landon, sandy pasture, 29
Mar. 2004, S. & J. Jeppson (MJ). Oland: Vickleby: Beijershamn, grazed
dry grassland, 29 Oct. 1976, J. & M. Jeppson 1598 (MJ).
Lycoperdon excipulifome. Austria: Burgenland: Jois, Junger Berg,

calcareous dry grassland, 2 Nov. 2000, J. & M. Jeppson 5359 (MJ). Iceland: Nordur Mulasysla: Jokuldalur, Gilsa, subalpine grassland, 31
Jul. 1993, A. & K. Bohlin, M. Jeppson 4045 (MJ). Slovakia: Senica: Bosky
Svaty Jur, in dry, sandy pine forest, 30 Oct. 2000, J. & M. Jeppson 5308
(MJ). Sweden: Uppland, Djuro, Runmaro, W of Vittrask, grazed
grassland, 19 Sep. 2004, M. Jeppson 7231 (MJ). Gotland: Sundre: Vaktbackar Nature Reserve, in dry calcareous grassland, 12 Oct. 2002,
M. Jeppson (MJ). Smaland: Hogby: Valakra, grazed grassland, 23
Sep. 2001, J. & M. Jeppson 5864 (MJ).
Lycoperdon frigidum. Greenland: Qinqua-valley at Tasersuaq lake,
20 Aug. 1983, H. Knudsen, T. Borgen & J. H. Petersen (C). Disko: Qeqer sterlien, 19 Aug. 1971, M. Lange (C). Norway: Hordaland:
tarsuaq: O
Ulvik, Blaisen ved Finse, 6 Sep. 1951, P. Wendelbo, det. V. Demoulin
(O). Oppland: Lom: Soleggen, 20 Aug. 1957, F.-E. Eckblad, det V.
Demoulin (O).
Lycoperdon lambinonii. Finland: North Karelia: Ilomantsi: Niemijarvi: Tapionaho, on sandy soil in road verge in mixed forest, 28
Aug. 1996, J. & M. Jeppson 3701 (MJ). Sweden: Jamtland: Duved: Graningesjon, coniferous forest, 23 Aug. 1983, S. Jeppson 1564, det. V.
Demoulin 1984 (MJ).
Lycoperdon lividum. Denmark: N. Jylland: V. Torup: Bulbjerg, 18
Oct. 1998, M. Jeppson 3646. Sweden: Gotland: Gammelgarn: Sandviken Nature Reserve, 26 Sep. 2001, J. & M. Jeppson 5587 (MJ). Skane:
Rinkaby: Rinkaby skjutfalt, 14 Oct. 1995, J. & M. Jeppson (MJ).
Lycoperdon mammiforme. Belgium: Lie`ge: Pailhe: entre Saint-Fontaine et Tahier, pelouse calcaire a` Melica uniflora en bordure dun
bois, 8 Oct. 1965, V. Demoulin (MJ ex herb. LG). Sweden: Dalsland:
Skallerud, Ryr, 29 Aug. 1987, M. Jeppson 2429 (MJ). Vastergotland:
sterplana: O
sterplana hed Nature Reserve, under Corylus, 19
O
Sep. 1999, M. Jeppson 4841 (MJ). Uppland: Blido: Furusund, 26 Sep.
1985, A. Tehler (S).
Lycoperdon marginatum. Slovakia: Zahorie: Senica: Mikulasov, in
Corynephoretum in PinusQuercus forest, 3 Oct. 2005, T. Knutsson,
J. &. M. Jeppson 7503 (MJ). Spain: Barcelona: Maresme: Orrius,
13 Dec. 1985, M. Tabares, A. Rocabruna & M. Jeppson (MJ).
Lycoperdon molle. Hungary: Bacs-Kiskun: Kunbaracs: Kunbaracsi
sborokas, 1 Nov. 2001, J. & M. Jeppson 6013 (MJ)dIceland: N. MulaO
sysla: Merki, subalpine grassland, 10 Aug. 1974, M. Jeppson 487, det.
V. Demoulin (MJ). Slovakia: Strazovske vrchy: Podskalie, FagusPinea
forest, 4 Oct. 2005, T. Knutsson, J. & M. Jeppson 7526 (MJ). Sweden:
Vastergotland: Berg: Melldalaskogen Nature Reserve, in deciduous
forest, 8 Aug. 1998, T. Schultz, R.-G. Carlsson & M. Jeppson 4801
(MJ). Uppland: Dalaro: Uto: Kroka, road verge in mixed forest,
4 Nov. 2004, M. Jeppson 6916 (MJ). Gotland: Vallstena: Vallstenarum,
25 Sep. 2001, J. & M. Jeppson 5579 (MJ).
Lycoperdon muscorum. Sweden: Sodermanland: Tystberga: Nynas
slott, wet grassland, 19 Sep. 2004, M. Jeppson 7244 (MJ). Vastergotland: Trollhattan: Lextorp, 16 Sep. 1972, M. Jeppson 299 (MJ).
Lycoperdon turneri. Norway: Oppland: Hjerkin: Hageseter, dry,
sandy, subalpine Empetrum heath, 29 Aug. 1997, J. & M. Jeppson
4259 (MJ); Dalseter, Espedalsvandet, 25 Jul. 1980, S. &
re, 1 km S of BlahammaJ. Jeppson 1412 (MJ). Sweden: Jamtland: A
ren, 23 Aug. 2002, A. Karlsson & F. Oskarsson (MJ).
Lycoperdon nigrescens. Denmark: N. Jylland: Hjortdal: Gronnestrand, grazed heathland, 18 Oct. 1998, M. Jeppson 3641 (MJ); Hjortdal, Gronnestrand, grazed heathland, 18 Oct. 1998, M. Jeppson
3641 (MJ). Sweden: Gotland: Kracklingbo: Uppstaigs Urskog Nature
Reserve, coniferous forest, 26 Sep. 2001, J. & M. Jeppson 5605 (MJ).
Vastergotland: V. Tunhem: Rannums ekar, grassland, 6 Aug. 2004,
J. & M. Jeppson 7022 (MJ).
Lycoperdon niveum. Greenland: Qassiarsuk, 29 Aug. 1995, M.
Lange (C). Kangilinnguit: Gronnedal-hut, 15 Aug. 1991, T. Borgen
(C). Iceland: N. Mulasysla: Jokuldalur: Eiriksstadir: Dryas heath,
9 Aug. 1993, M. Jeppson 4131 (MJ). Hrafnkellsdalur: Adalbol: Dryas
heath, 9 Aug. 1993, M. Jeppson 4107 (MJ). Eyjafjardarsysla: Kraeklingarhld, 10 Aug. 1962, H. Hallgrmsson, det. V. Demoulin
(AMNH). Nepal: Kumbu: Moranen des Lobuche-Gletschers bei
Lobuche, 49505000 m.sm., Sep. 1962, J. Poelt, det. H. Kreisel

(dholotypus).
Lycoperdon norvegicum. Estonia: Viru: Lahemaa National Park,
Viitna, sandy pine forest, 22 Aug. 1989, M. Jeppson 2861 (MJ). Norway:
Oppland: Boverdalen: Slettet, grazed subalpine grassland with scattered Pinus, 6 Sep. 2000, A. Bohlin, J. & M. Jeppson 5255 (MJ). Slovakia:
Zahorie: Malacky, Zavod, S of railway station, sandy pine forest,
3 Oct. 2005, T. Knutsson, J. & M. Jeppson 7491 (MJ). Sweden: Oland:
Gardby, sandy pine forest, 5 Oct. 2003, J. & M. Jeppson 6524 (MJ).
Lycoperdon perlatum. Czechia: Praha: Radotn, Chotec, in deciduous forest, 1 Nov 2001, J. & M. Jeppson 5873 (MJ). Slovakia: Senica:
Moravsky Svaty Jan: Dubrava, 30 Oct. 2000, J. & M. Jeppson 5307
(MJ). Sweden: Lule Lappmark: Jokkmokk: Padjelanta National
Park, Huorso, S. Kuoljok 134 (MJ). Oland: Algutsrum: Porskarr,
4 Oct. 2003, J. & M. Jeppson 6507 (MJ).
Lycoperdon pratense. Denmark: N. Jylland: Lerup: Fosdalen, in
grazed grassland, 18 Oct. 1998, M. Jeppson 3639 (MJ). Sweden: Skane:
hus: A
llekopinge, dry sandy pasture, 14 Oct. 1995, J. & M. Jeppson
A
3314 (MJ).
Lycoperdon pyriforme. Slovakia: Male Karpaty: Pezinok, Sedlo
Baba, 17 Oct. 2004, J. & M. Jeppson 7374 (MJ). Sweden: Vastergotland: Berg: Melldalaskogen Nature Reserve, on deciduous wood,
8 Aug. 1998, T. Schultz, R.-G. Carlsson & M. Jeppson 4803 (MJ). Uppland: Djuro: Runmaro: Uppebytrask, on fallen stem of deciduous
tree, 5 Nov. 2004, M. Jeppson 6939 (MJ).
Lycoperdon radicatum. Sweden: Skane: Munkarp: Munkarps falad,
dry, acidic grassland, 26 Oct. 2004, C.-G. Bengtsson & K. Bergelin (MJ).
Spain: Huelva: Mazagon, sand dune with Lygos and Halimium,
24 Feb. 2002, S., J. & M. Jeppson 5949 (MJ). USA: Wisconsin: Waukesha
County: Sprough Farm, very sandy soil at edge of corn field, 18 Jul.
1995, J. Steinke (MJ).
Lycoperdon umbrinum. Czechia: Praha: Roblin, in coniferous forest, 31 Oct. 2001, J. & M. Jeppson 5872 (MJ). Sweden: Sodermanland:
Tunaberg: Fingerkulla, coniferous forest, 19 Sep. 2004, M. Jeppson
7249 (MJ). Vastergotland: Rommele: Tokebacken, in coniferous forest, 2 Aug. 1998, T. Schultz & M. Jeppson 4781 (MJ); Lule Lappmark:
Jokkmokk, Skansen, 15 Aug. 1998, S. Kuoljok (MJ).
Lycoperdon utriforme. Denmark: N. Jylland: Tranum: Tranum
strand, grazed heathland, 17 Oct. 1993, M. Jeppson 3634 (MJ).
Sweden: Skane: Maglehem: Mollegarden, grazed grassland, 20
Sep. 1986, M. Jeppson 2136 (MJ). Oland: Fora: Vassbylund, 3 Oct.
1987, M. Jeppson 2280 (MJ).
Taxon sampling
The ingroup included 83 sequences representing 54 taxa from
Lycoperdaceae (dataset 1). Seventy-six sequences are generated
for this study, and seven ITS sequences are downloaded from
GenBank (Morganella fuliginea AF485065, M. subincarnata
AJ237626, Bovista polymorpha AJ237613, B. pusilla AJ237631, Calvatia rubroflava AF485064, C. fragilis AJ486962, C. cyathiformis
AJ486868).
Different combinations of outgroups were tested and representatives from Lepiota, Macrolepiota, Cystolepiota, Leucoagaricus, Agaricus, and Leucocoprinus were initially included in the
alignment, as earlier studies indicate that Lycoperdaceae is
nested within lepiotoid fungi (Bates 2004; Kruger et al. 2001;
Lebel et al. 2004; Vellinga 2004). Finally two species of Tulostoma were selected as the outgroup.
In order to decrease the number of ambiguous sites and increase the resolution within Lycoperdon we compiled a separate dataset with the 58 ingroup sequences assumed to
represent species of Lycoperdon in a wide sense and with
Bovista furfuracea as outgroup (dataset 2).
DNA extraction, PCR and sequencing

Sequences were obtained from fresh material and from herbarium specimens (Table 1). Total DNA was isolated using
DNeasy plant mini kit (QIAGEN, Valencia), following manufacturers recommendations. PCR reactions were carried out using Ready-To-Go PCR beads (Amersham Biosciences,
Uppsala). Primers used to amplify the complete ITS region
and the 50 end of the LSU region were ITS1F (Gardes & Bruns
1993) and LR21, LR0R and LR7 (Hopple & Vilgalys 1999). Amplified products were purified using Qiaquick spin columns (Qiagen, Hilden). Primers used for sequencing were ITS1, ITS3,
ITS4 (White et al. 1990), Ctb6 (http://plantbio.berkeley.edu/
wbruns/), Lr5 and LR3R (Hopple & Vilgalys 1999). Fifty to
75 ng of PCR products were used in each sequencing reaction
using DTCS Quick Start Kit (Beckman Coulter, Fullerton). Sequences were obtained using CEQ 8000 DNA analysis system
(Beckman Coulter).
Phylogenetic analyses
Sequences were edited and assembled using Sequencher 3.1
(Gene Codes, Ann Arbor). Aligning was done with MAFFT
(Katoh et al. 2002) followed by manual adjustment using the
data editor in PAUP (Swofford 2003). Sequences have been deposited in GenBank and accession numbers are given in Table
1. Sequence alignments are available for download at http://
andromeda.botany.gu.se/lycoperdon.zip.
Heuristic searches for most parsimonious trees were performed using PAUP. All transformations were considered unordered and equally weighted. Variable regions with
ambiguous alignment were excluded and gaps treated as
missing data. Searches used 1K random-addition sequence
replicates and tree bisectionreconnection (TBR) branch
swapping. Relative robustness of clades was assessed by the
BS method using 1K heuristic search replicates with 100 random taxon addition sequence replicates and TBR branch
swapping, saving 100 trees in each replicate.
Bayesian analysis of phylogeny was performed using
MrBayes 3.0B4 (Ronquist & Huelsenbeck 2003). MrModelTest
2.2 (Nylander 2004) was used to estimate separate best-fit
models of evolution for ITS1, 5.8S, ITS2, and LSU. A heterogeneous Bayesian inference was set up with model parameters
estimated separately for each partition. Eight Metropoliscoupled MCMC chains with a temperature of 0.2 were initiated;
these were run for 10 M generations with tree and parameter
sampling every 5K generations (2K trees). The initial burn-in
was set to 50 % (1K trees). A 50 % majority-rule consensus cladogram was computed from the remaining trees; the proportions of this tree correspond to Bayesian PP probabilities (BPP).
Results
The aligned dataset 1 has 1724 characters. After exclusion of
ambiguous areas 1488 characters remained for the analyses.
Of these 1087 are constant, 149 variable and parsimony uninformative, and 252 parsimony informative. MP analysis
yielded 10743 equally most parsimonious trees (length 1054,
CI 0.5396, RI 0.7190). The strict consensus tree is presented

in Fig 1. BS frequencies above 50 % are shown above branches.
The BS analysis recovered the ingroup as monophyletic with
100 % support and Mycenastrum corium as a sister taxon to
the rest of the ingroup. Five major clades receive weak to moderate support, viz. Lycoperdon (70 %), Bovista (83 %), Globaria
(76 %), Calvatia including Langermannia (55 %), and Disciseda
(59 %). However, Calvatia without Langermannia is highly supported (96 %). Fig 2 shows one of the most parsimonious trees
presented as a phylogram to show the number of character
state changes per branch.
For the separate regions, MrModelTest suggested
GTR I G (ITS1 and LSU), JC (5.8S), and GTR G (ITS2), as
best-fit models; this information was employed in MrBayes.
Chain convergence was attained well ahead of the initial
burn-in threshold, which hence was not modified any further.
The Bayesian tree is more resolved than the MP strict consensus
tree and more nodes receive reliable support values. BPP have
been indicated in the strict consensus tree (Fig 1). Also in this
analysis the ingroup is recovered as monophyletic with a BPP
value of 1 and with Mycenastrum corium as a sister taxon. Bovista
is recovered as a separate clade (BPP 0.94) with Bovista (BPP 1)
and Globaria (BPP 1) as distinct subclades. Calvatia including Langermannia received BPP value of 1, whereas the Disciseda clade
also in the Bayesian tree is unsupported (BPP 0.72).
The Lycoperdon clade includes species from Lycoperdon,
Vascellum, Morganella, Handkea, Bovistella, and Calvatia. In the
strict consensus tree (Fig 1) the clade is split in two major subclades, viz. Lycoperdon 1 (BS 59 %, BPP 1) with Vascellum, Morganella fuliginea, M. subincarnata, L. marginatum, L. norvegicum, and
L. perlatum and Lycoperdon 2. (BS value <50 %, BPP 0.76) including most Lycoperdon species, Handkea excipuliformis, H. utriformis, Calvatia turneri, C. cretacea, Bovistella radicata, and Bovista
dermoxantha. Morganella pyriformis and L. caudatum occur on
single branches in the MP tree, whereas the Bayesian tree places L. caudatum within Lycoperdon 1. The position of L. nigrescens is ambiguous. In the MP tree it belongs to Lycoperdon 2,
whereas in the Bayesian tree it is recovered in Lycoperdon 1.
Dataset 2 has 1510 nucleotide positions including gaps. Of
these 1269 are constant, 106 variable and parsimony uninformative, and 135 parsimony informative. The MP analysis
yielded 1595 equally most parsimonious trees (length 500,
CI 0.6020, RI 0.7603). In the bootstrap analysis Lycoperdon
exluding Morganella pyriforme is weakly supported as monophyletic (69 %). Lycoperdon 1 and Lycoperdon 2 are recovered,
however, with low BS support (58 % on both clades). L. nigrescens and L. caudatum occur on single branches.
For the separate regions of the alignment, MrModelTest
suggested GTR G (ITS1 and LSU), K80 (5.8S), and HKY 1 G
(ITS2), as best-fit models. The Bayesian analysis recovered
Lycoperdon as monophyletic with a BPP value of 0.99. Also in
this analysis Morganella pyriforme falls outside. Fig 3 presents
the 50 % majority rule consensus tree from the Bayesian analysis. BPP values are indicated on branches after the BS values.
Thirty-one species were recognized in Lycoperdon (Fig 3).
Three terminal clades are regarded as potential new species.
In Bovista 11 species were identified (Figs 1 and 2), eight in subgenus Bovista, of which one is a potentially new species, and
three in subgenus Globaria. In Calvatia six species are identified and in Disciseda two species.
64/0.93
79/1.0
58
64
80/1.0
93/1.0
70/
0.92
54/0.98
66/0.96
97/1.0
95/1.0
74/0.93
0.76
84/0.92
70/0.93
100/1.0
97/1.0
85/1.0
90/1.0
80/0.80
99/1.0
93/1.0
100/1.0
75/ 82/1.0
0.99
0.97
100/1.0
62/1.0
93/1.0
83/1.0
0.94
0.99
95/1.0
0.94
100/1.0
77/1.0
62/0.95
76/1.0
100/1.0
100/1.0
55/1.0
100/1.0
96/1.0 94/1.0
59/0.72
Lycoperdon 1
Lycoperdon 2
79/1.0
Lycoperdon
Bovista
93/1.0
59/1.0
Vascellum pratense MJ4864

Vascellum cfr intermedium SH15-9
Vascellum cfr intermedium MJ5858
Morganella fuliginea AF485065
Morganella subincarnata AJ237626
Lycoperdon perlatum MJ4684
Lycoperdon marginatum A&P750822
Lycoperdon norvegicum MJ5453
Lycoperdon caudatum RGC920818
Lycoperdon nigrescens MJ5376
Lycoperdon frigidum Eckblad151507
Lycoperdon frigidum MJ7716
Lycoperdon niveum Lange900910
Lycoperdon cfr molle MJ4088
Lycoperdon frigidum Lange191
Lycoperdon molle MJ4557
Lycoperdon sp. 1 MJ4285
Lycoperdon mammiforme MJ4841
Lycoperdon cfr frigidum MJ484
Lycoperdon niveum MJ5267
Lycoperdon cfr. niveum MJ5594
Lycoperdon lambinonii Demoulin4622
Lycoperdon lambinonii MJ5245
Lycoperdon umbrinum MJ4556
Lycoperdon umbrinum MJ4556a
Calvatia turneri MJ5251
Calvatia cfr candida ML08-95
Lycoperdon echinatum MJ6498
Bovista dermoxantha MJ4856
Lycoperdon sp. 3 Vetter407
Lycoperdon decipiens MJ4330
Lycoperdon atropurpureum MJ3269
Lycoperdon altimontanum MJ4270
Lycoperdon altimontanum holotype
Handkea excipuliformis MJ6467
Calvatia cretacea MJ4105
Lycoperdon niveum Dobremez740514
Lycoperdon lividum MJ4005
Lycoperdon sp. 2 L148-03
Lycoperdon muscorum MJ7717
Lycoperdon ericaeum MJ5395
Handkea utriformis MJ5388
Bovistella radicata Parker970911
Morganella pyriformis SJ980920
Bovista paludosa MJ4301
Bovista cretacea MJ5207
Bovista cretacea ANMH11622
Bovista nigrescens S&JJ980905
Bovista plumbea MJ4856
Bovista cfr limosa MJ3971
Bovista limosa MJ5226
Bovista tomentosa MJ5433
Bovista minor Steinke951015
Bovista graveolens Widgren030816
Bovista aestivalis MJ3860ITS
Bovista polymorpha AJ237613
Bovista cfr aestivalis MJ1122
Bovista promontorii MJ7070
Bovista furfuracea MJ5435
Bovista pusilla AJ237631
Langermannia
Calvatia gigantea MJ3566
Calvatia candida MJ3514
Calvatia craniiformis Steinke001017
Calvatia fragilis AJ486962
Calvatia cyathiformis AJ486868
Calvatia rubroflava AF485064
Disciseda candida MJ3588
Disciseda bovista MJ5078
Mycenastrum corium MJ5467
Tulostoma squamosum Mrazek1300
Tulostoma kotlabae MJ6623
Bovista
Globaria
100/1.0
57/0.98
Calvatia
10
Calvatia
Disciseda
Fig 1 The strict consensus tree of 10 743 most parsimonious trees, from the MP analyses of the inclusive dataset of ITS and
LSU sequence data. Support values on branches are given as BS values/Bayesian PPs. The supported clades have been
marked with scale bars and the proposed limits of the genera Lycoperdon, Bovista, Calvatia, and Disciseda with brackets.
Vascellum pratense MJ4864

Vascellum cfr intermedium SH15-9
Vascellum cfr intermedium MJ5858
Morganella fuliginea AF485065
Morganella subincarnata AJ237626
Lycoperdon perlatum MJ4684
Lycoperdon marginatum A&P750822
Lycoperdon norvegicum MJ5453
Lycoperdon caudatum RGC920818
Lycoperdon nigrescens MJ5376
Lycoperdon frigidum Eckblad151507
Lycoperdon niveum Lange900910
Lycoperdon cfr molle MJ4088
Lycoperdon frigidum Lange191
Lycoperdon mammiforme MJ4841
Lycoperdon cfr frigidum MJ484
Lycoperdon cfr. niveum MJ5594
Lycoperdon lambinonii Demoulin4622
Lycoperdon lambinonii MJ5245
Lycoperdon umbrinum MJ4556a
Calvatia cfr candida ML08-95
Lycoperdon altimontanum MJ4270
Lycoperdon altimontanum holotype
Handkea excipuliformis MJ6467
Lycoperdon echinatum MJ6498
Bovista dermoxantha MJ4856
Lycoperdon sp. 3 Vetter407
Lycoperdon niveum Dobremez740514
Lycoperdon lividum MJ4005
Lycoperdon sp. 2 L148-03
Lycoperdon muscorum MJ7717
Handkea utriformis MJ5388
Bovistella radicata Parker970911
Morganella pyriformis SJ980920
Bovista paludosa MJ4301
Bovista plumbea MJ4856
Bovista cfr limosa MJ3971
Bovista limosa MJ5226
Bovista tomentosa MJ5433
Bovista minor Steinke951015
Bovista cretacea MJ5207
Bovista cretacea ANMH11622
Bovista nigrescens S&JJ980905
Bovista graveolens Widgren030816
Bovista aestivalis MJ3860ITS
Bovista polymorpha AJ237613
Bovista cfr aestivalis MJ1122
Bovista promontorii MJ7070
Bovista pusilla AJ237631
Calvatia gigantea MJ3566
Calvatia candida MJ3514
Calvatia cyathiformis AJ486868
Calvatia fragilis AJ486962
Calvatia rubroflava AF485064
Calvatia craniiformis Steinke001017
Disciseda candida MJ3588
Disciseda bovista MJ5078
Mycenastrum corium MJ5467
Tulostoma squamosum Mrazek1300
Tulostoma kotlabae MJ6623
11
Lycoperdon
Bovista
Calvatia
Disciseda
5 changes
Fig 2 One of the 10 743 most parsimonious trees, from the MP analyses, presented as a phylogram to show the number
of character state changes per branch. Proposed limits of the genera Lycoperdon, Bovista, Calvatia, and Disciseda have been
indicated with brackets.
12
Taxonomy
Type species: Mycenastrum ohiense Ellis & Morgan, J. Mycol. 1:

89 (1885).
Synonym: Handkea Kreisel, Nova Hedwigia 48: 282 (1989)
Molecular based classification of Lycoperdaceae

This classification treats all species occurring in the Nordic
countries and some other species. The reasoning behind our
genus concept is outlined in the discussion section below.
Lycoperdon Pers., Neues Mag. Bot.1: 87 (1794): Pers., Syn. meth.
fung.: 140 (1801).
Lycoperdon subgenus Lycoperdon
Type species: Lycoperdon perlatum
Lycoperdon perlatum Pers., Observ. mycol. 1: 145 (1796): Pers.,
Syn. meth. fung.: 145 (1801).
Lycoperdon norvegicum Demoulin, Norweg. J. Bot. 18: 166 (1971).
Lycoperdon marginatum Vittad., Monogr. Lycoperd.: 185 (1842).
Lycoperdon subgenus Vascellum (F. Smarda) Jeppson & E.
Larss., comb. nov.
MycoBank no.: 511316

Basionym: Vascellum F. Smarda, in Pilat, Flora CSR,
B1: 760
(1958).
Type species: Lycoperdon depressum
Lycoperdon pratense Pers., Neues Mag. Bot.1: 87 (1794): Pers.,
Syn. meth. fung.: 142 (1801).
Synonyms: Vascellum pratense (Pers.) Kreisel, Feddes Repert. 64:
159 (1962).
Lycoperdon depressum Bonord., Bot. Zeitung (Berlin) 15: 611
(1857).

Vascellum depressum (Bonord.) F. Smarda, Flora CSR,
B1: 305
(1958).
Lycoperdon subgenus Morganella (Zeller) Jeppson & E. Larss.,
comb. nov.
Basionym: Morganella Zeller, Mycologia 40: 650 (1948).
Type species: Morganella mexicana Zeller, Mycologia 40: 650
(1948).
Lycoperdon fuligineum Berk. & Curt. in Berkeley, J. Linn. Soc.,
Bot. 10(46): 345 (1868).
Synonym: Morganella fuliginea (Berk. & Curt.) Kreisel & Dring,
Feddes Repert. 74: 113 (1967).
Lycoperdon subincarnatum Peck, Rep. (Annual) New York State
Mus. Nat. Hist. 24: 83 (1872).
Synonym: Morganella subincarnata (Peck) Kreisel & Dring,
Feddes Repert. 74: 117 (1967).
Lycoperdon subgenus Bovistella (Morgan) Jeppson & E. Larss.,
comb. nov.
Basionym: Bovistella Morgan, J. Cincinnati Soc. Nat. Hist. 14: 141
(1892).
Lycoperdon utriforme Bull., Hist. Champ. France: 153 (1791):

Pers., Syn. meth. fung.: 143 (1801).
Synonyms: Calvatia utriformis (Bull.) Jaap, Verh. Bot. Vereins
Prov. Brandenburg 59: 37 (1918).
Handkea utriformis (Bull.) Kreisel, Nova Hedwigia 48: 288
(1989).
Lycoperdon radicatum Durieu & Mont., Expl. sci. Algerie 1: 383
(1848).
Synonyms: Bovistella radicata (Durieu & Mont.) Pat., Bull. Soc.
Mycol. France 15: 55 (1889).
Mycenastrum ohiense Ellis & Morgan. J. Mycol. 1: 89 (1885).
Lycoperdon subgenus Utraria (Quel.) Jeppson & E. Larss.,
comb. nov.
Basionym: Utraria Quel., Mem. Soc. Emul. Montbeliard, ser. 2, 5:
366 (1873).
Type species: Lycoperdon excipuliforme
Lycoperdon frigidum Demoulin, Lejeunia, n.s. 62: 10 (1972).
Lycoperdon sp. 1.
Lycoperdon molle Pers., Obs mycol. 2: 70 (1800): Syn. meth. fung.:
150 (1801).
Lycoperdon niveum Kreisel, Khumbu Himal. 6(1): 30 (1969).
Lycoperdon mammiforme Pers., Syn. meth. fung.: 145 (1801).
Lycoperdon atropurpureum Vittad., Monogr. Lycoperd.: 42
(1842).
Lycoperdon decipiens Durieu & Mont., Expl. sci. Algerie 1: 380
(1848).
Lycoperdon altimontanum Kreisel, Feddes Repert. 87: 97 (1976).
Lycoperdon excipuliforme (Scop.) Pers., Syn. meth. fung.: 143
(1801).
Synonyms: Lycoperdon polymorphum var. excipuliforme Scop., Fl.
carniol., Ed. 2 2: 488 (1772).
Calvatia excipuliformis (Scop.) Perdeck, Blumea 6: 490 (1950).
Handkea excipuliformis (Scop.) Kreisel, Nova Hedwigia 48(34):
283 (1989).
Lycoperdon lambinonii Demoulin, Lejeunia, n.s. 62: 13 (1972).
Lycoperdon muscorum Morgan, J. Cincinnati Soc. Nat. Hist. 13:
16 (1891).
Synonyms: Lycoperdon muscorum var. subareolatum Kreisel,
Feddes Repert. 64: 155 (1962)
Lycoperdon ericaeum var. subareolatum (Kreisel) Demoulin, Beih.
Sydowia 8: 147 (1979).
13
65/0.89
81/1.0
74/0.99
62
/0.96
94/1.0
0.59
82/1.0
0.60
88/1.0
54/0.76
0.87
0.77
80/0.98
0.84
97/1.0
98/1.0
0.50
98/1.0
84/0.97
79/0.92
0.73
93/1.0
0.75
100/1.0
87/1.0
0.85
59/0.92
99/1.0
85/1.0
76/1.0
0.54
100/1.0
100/1.0
88/1.0
67/1.0
69/0.99
100/1.0
58/0.97
0.59
71/1.0
0.53
0.61
95/1.0
L. frigidum MJ7716
L. frigidum Eckblad151507
L. niveum Lange900910
L. frigidum MJ4273
L. frigidum Lange191
L. cfr molle MJ4088
L. sp. 1 MJ4285
L. sp. 1 MJ4277
L. molle MJ4557
L. molle MJ4260
L. atropurpureum MJ3269
L. atropurpureum MJ6150
L. mammiforme MJ4841
L. niveum MJ5267
L. niveum MJ4068
L. niveum MJ4109
L. cfr niveum MJ5594
L. cfr frigidum MJ484
L. decipiens MJ4330
L. decipiens MJ7715
L. umbrinum MJ4556
L. umbrinum MJ4556a
L. umbrinum MJ4559
L. turneri MJ5251
L. turneri MJ4265
L. turneri ML08-95
L. altimontanum MJ4270
L. altimontanum holotype
L. excipuliforme MJ6467
L. cretaceum MJ4105
L. cretaceum MJ4302
L. lambinonii MJ5245
L. lambinonii Demoulin4622
L. lividum Dobremez740514
L. lividum MJ4005
L. echinatum MJ6498
L. sp. 2 MJ6371
L. sp. 2 L148-03
L. sp. 2 MJ6394
L. muscorum MJ7717
L. ericaeum MJ5395
L. ericaeum MJ4866
L. sp. 3 MJ4304
L. sp. 3 Vetter407
L. dermoxanthum MJ4856
L. utriforme MJ5388
L. radicatum Parker970911
L. pratense MJ4864
L. cfr intermedium SH15-9
L. cfr intermedium MJ5858
L. marginatum A & P 750822
L. perlatum MJ4684
L. norvegicum MJ5453
L. subincarnatum AJ237626
L. fuligineum AF485065
L. caudatum RGC920818
L. nigrescens MJ5376
L. pyriforme SJ980920
Utraria
Bovistella
Vascellum
Lycoperdon
Morganella
Utraria
Apioperdon
Fig 3 The 50 % majority rule consensus tree from the Bayesian phylogenetic analysis based on the restricted realigned
dataset of the Lycoperdon clade. Support values on branches are given as BS values/Bayesian PPs. Thirty-one species were
identified and are named according to the proposed molecular based classification. The proposed subgeneric division of
Lycoperdon has been indicated with brackets.
Lycoperdon ericaeum Bonord., Bot. Zeitung (Berlin) 15: 596 (1857).

Lycoperdon sp. 2
Lycoperdon cretaceum Berk., Proc. Linn. Soc. London 17(98): 15
(1878).
Synonym: Calvatia cretacea (Berk.) Lloyd, Mycol. Notes Lloyd Libr.
Mus. 46: 650 (1917).
Lycoperdon turneri Ellis & Everh., J. Mycol. 1(7): 87 (1885).

Synonyms: Calvatia turneri (Ell. & Ev.) Demoulin & M. Lange,
Mycotaxon 38: 223 (1990).
Calvatia tatrensis Hollos, Math. Term. Ertes. 19: 508 (1901).
Lycoperdon umbrinum Pers., Ann. Bot. (Usteri) 11: 28 (1797):
Syn. meth. fung.: 147 (1801).
14
Lycoperdon echinatum Pers., Ann. Bot. (Usteri) 11: 28 (1797):

Syn. meth. fung.: 147 (1801).
Lycoperdon lividum Pers., J. Bot. (Paris) 2: 18 (1809)
Lycoperdon caudatum Schroeter, Pilzfl. Schlesiens 1: 698
(1889).
Synonym: Lycoperdon pedicellatum Peck, Rep. (Annual) New York
State Mus. Nat. Hist. 26: 23 (1874).
Lycoperdon nigrescens Pers., Neues Mag. Bot.1: 87 (1794): Pers.
Syn. meth. fung.: 146 (1801).
Synonyms: Lycoperdon perlatum b nigrescens Pers., Syn. meth.
fung.: 146 (1801).
Lycoperdon foetidum Bonord., Handb. Allgem. Mykol. (Stuttgart):
253 (1851).
Lycoperdon dermoxanthum Vittad., Monogr. Lycoperd.: 35 (1842).
Synonyms: Bovista dermoxantha (Vittad.) De Toni, in Sacc. Syll.
fung. 7: 100 (1888).
Lycoperdon hungaricum Hollos, Math. Term. Ertes. 19: 510 (1901).
Calvatia rubroflava (Cragin) Morgan, J. Cincinnati Soc. Nat. Hist.

12(4): 171 (1890).
Synonym: Lycoperdon rubroflavum Cragin, Bull. Washburn Coll.
Lab. Nat. Hist. 1: 30 (1885)
Calvatia subgenus Langermannia (Rostk.) Jeppson & E. Larss.,
comb. nov.
Basionym: Langermannia Rostk., in Sturm, Deutschl. Flora, III
(Pilze) 5: 23 (1839)
Type species: Lycoperdon giganteum
Calvatia gigantea (Batsch) Lloyd, Myc. Writ. 1: 166 (1904).
Synonyms: Lycoperdon giganteum Batsch, Elenchus fungorum,
cont. prim. (Halle): 237 (1786).: Pers., Syn. meth. fung.: 140
(1801).
Langermannia gigantea (Batsch) Rostk., in Sturm, Deutschl. Flora,
III (Pilze) 5: 23 (1839)
Bovista Pers., Neues Mag. Bot. 1: 86 (1794): Syn meth. fung.: 136
(1801)
Type species: Bovista plumbea
Lycoperdon sp. 3
Bovista subgenus Bovista
Lycoperdon subgenus Apioperdon (Kreisel & D. Kruger)
Jeppson & E. Larss. comb. nov.
Basionym: Morganella subgenus Apioperdon Kreisel & D.
Kruger, Mycotaxon 86: 174 (2003).
Type species: Lycoperdon pyriforme
Bovista paludosa Lev., Annals Sci. Nat., Bot., ser. 3 5: 163 (1846).
Bovista cretacea T. C. E. Fr., Svensk Bot. Tidskr. 8: 241 (1914).
Bovista nigrescens Pers., Neues Mag. Bot. 1: 86 (1794).
Lycoperdon pyriforme Schaeff., Fung. Bavar. Palat. nasc. 4: 128

(1774): Pers., Syn. Meth. Fung.: 148 (1801)
Synonym: Morganella pyriformis (Schaeff.) Kreisel & D. Kruger,
Mycotaxon 86: 175 (2003).
Bovista graveolens Schwalb, Lotos, n.s. 13: 53 (1893).
Calvatia Fr., Summa veg. Scand.: 442 (1849).

Type species: Bovista craniiformis Schwein.
Bovista limosa Rostr., Meddel. Grnland 18: 52 (1894).
Bovista plumbea Pers., Obs. mycol. 1: 5 (1796): Pers., Syn. meth.

fung.: 137 (1801).
Bovista cfr. limosa

Calvatia subgenus Calvatia
Calvatia candida (Rostk.) Hollos, Termeszetajzi. Fuz. 25: 112
(1902).
Synonym: Langermannia candida Rostk., in Sturm, Deutschl.
Flora, III (Pilze) 5: 25 (1839)
Calvatia craniiformis (Schwein.) Fr., Summa veg. Scand.: 442
(1849).
Synonym: Bovista craniiformis Schwein., Trans. Amer. philos.
Soc., n.s. 4(2): 256 (1832).
Calvatia cyathiformis (Bosc) Morgan, J. Cincinnati Soc. Nat. Hist.
12(4): 168 (1890).
Synonym: Lycoperdon cyathiforme Bosc, Mag. Neuesten Entdeck.
Gesammten Naturk. Ges. Naturf. Freunde Berlin 5: 87 (1811).
Calvatia fragilis (Vittad.) Morgan, J. Cincinnati Soc. Nat. Hist.
12(4): 168 (1890).
Synonym: Lycoperdon fragile Vittad., Monogr. Lycoperd.: 180
(1842).
Bovista tomentosa (Vittad.) De Toni, Syll. fung. (Abellini) 7: 97

(1888).
Synonyms: Lycoperdon tomentosum Vittad. Monogr. Lycoperd.: 36
(1842).
Bovista minor Morgan, J. Cincinnati Soc. Nat. Hist. 14: 147 (1892).
Bovista subgenus Globaria (Quel.) Kreisel, Feddes Repert. 69:
200 (1964).
Synonym: Globaria Quel. Mem. Soc. Emul. Montbeliard, Ser. 2, 5:
370 (1873).
Type species: Lycoperdon furfuraceum Schaeff., Icones: tab. 294
(1770) (syn. Bovista aestivalis).
Bovista aestivalis (Bonord.) Demoulin, Beih. Sydowia 8: 143
(1979).
Synonyms: Lycoperdon aestivale Bonord., Handb. Allgem. mykol.:
251 (1851).
Bovista polymorpha (Vittad.) Kreisel, Feddes Repert. 69: 201
(1964).
Lycoperdon polymorphum Vittad., Monogr. Lycoperd.: 38 (1842).
Bovista promontorii Kreisel, Beih. Nova Hedwigia 25: 225 (1967).

Bovista furfuracea (J. F. Gmelin) Pers., Syn. meth. fung.: 138
(1801).
Synonym: Lycoperdon furfuraceum J. F. Gmelin, Syst. Nat. 2: 1464
(1792).
Disciseda Czern., Bull. Soc. Imp. Naturalistes Moscou 18(2): 153
(1845).
Type species: Disciseda collabescens Czern., Bull. Soc. Imp. Naturalistes Moscou 18(2): 153 (1845).
Disciseda bovista (Klotzsch) Henn., Hedwigia 42: 128 (1903).
Synonym: Geaster bovista Klotzsch, Nov. Actorum Acad. Caes.
Leop.-Carol. Nat. Cur. 19 (suppl. 1): 243 (1843).
Disciseda candida (Schwein.) Lloyd, Mycol. Notes Lloyd Libr.
Mus. 1(10): 100 (1902).
Synonym: Bovista candida Schwein., Schriften Naturf. Ges. Leipzig 1: 59 (1822).
Discussion
Phylogenies based on sequence data have gradually changed
the picture of relationships within Agaricales and other homobasidiomycetes (Binder et al. 2005; Hibbett et al. 1997; Hibbett &
Thorn 2001; Larsson & Larsson 2003; Larsson et al. 2004;
Moncalvo et al. 2002). Transforming molecular phylogenies
to classifications will be a challenging task and is likely to reveal taxonomically problematic situations (Hopple & Vilgalys
1999; Moncalvo et al. 2002; Redhead et al. 2001). In a recent
higher classification for fungi it is suggested that the major
clades of the homobasidiomycetes, as they appear in molecular phylogenies, should be translated to orders (Hibbett et al.
2007). In such a classification the euagarics clade (Hibbett &
Thorn 2001; Moncalvo et al. 2002) becomes the Agaricales.
This order includes the majority of gilled mushrooms, but
also a number of aphyllophoralean groups and, for example,
the puffball genera treated in this paper.
As repeatedly shown Lycoperdon is related to Agaricus,
Coprinus, Lepiota, and similar gilled mushrooms (Moncalvo
et al. 2002; Lebel et al. 2004; Vellinga 2004). This assemblage
is usually treated as the family Agaricaceae, at least when
only agaricoid elements are considered. The most comprehensive phylogenetic treatment of the gilled species within
Agaricaceae is presented by Vellinga (2004). She recovered an
ingroup with nine clades, among them the Lycoperdaceae and
Tulostomataceae clades. If the ingroup identified by Vellinga
(2004) is retained as a family, then Lycoperdaceae and Tulostomataceae must be given a lower rank, for example, as tribes.
A comprehensive fine-scale subdivision for Agaricales with
only monophyletic groups is still far away. We suggest that
a final decision on the hierarchical status of the clades identified in this study is postponed and that our ingroup meanwhile is retained as the family Lycoperdaceae.
As already implied by Kruger et al. (2001) and Bates
(2004) Lycoperdaceae is monophyletic only at the exclusion
of Mycenastrum corium, a result repeated in our study. We
analysed a more inclusive LSU dataset with representatives
15
for Agaricus, Leucocoprinus, Lepiota, Podaxis, Montagnea, Cystolepiota, Macrolepiota, Allopsalliota, and Coprinus in order to further
explore the position of Mycenastrum. These analyses (results
not shown) did not alter the position of M. corium in relation
to the ingroup. We concur with Zeller (1949) and Pilat (1958)
that Mycenastrum should be regarded as a monotypic genus
in a separate family Mycenastraceae. Discriminating morphological characters are a thick endoperidium dehiscing by irregular lobes, large spores (up to 13 mm in diam), spore wall
ultrastructure, presence of clamps, and a spinous capillitium
(Hansen 1962; Bronchart & Demoulin 1973).
Within Lycoperdaceae four major clades can be discerned,
viz. Lycoperdon, Bovista, Calvatia, and Disciseda (Figs 1 and
2). The latter three clades correspond more or less to the
current concept of the equally named genera Bovista, Calvatia, and Disciseda. However, a similar translation of the Lycoperdon clade to represent the genus Lycoperdon would imply
that the current circumscription of the genus becomes much
widened. The generic type, Lycoperdon perlatum, clusters with
Morganella, Vascellum, and two more Lycoperdon species in
a well supported clade (Lycoperdon 1, Fig 1), while the majority of Lycoperdon species form an unsupported sister clade
together with some species currently referred to Handkea,
Calvatia, Bovista, and Bovistella (Lycoperdon 2, Fig 1). Recognizing Morganella, Vascellum, and Handkea causes Lycoperdon
in its current sense to be paraphyletic. A monophyletic Lycoperdon would be reduced to the generic type and a small
number of closely related species. The majority of species
would have to be transferred to another genus equivalent
to the Lycoperdon 2 clade. For this group the name Utraria
Quel. (1873) is available but a considerable number of
name changes from Lycoperdon to Utraria becomes necessary.
The alternative solution, and the one we recommend here,
is to accept Lycoperdon in a wide sense. As most species affected by our concept of Lycoperdon were originally described
in this genus the number of name changes can be kept to
a minimum.
Analyses of the dataset restricted to Lycoperdon and with
Bovista furfuracea as outgroup support monophyly for Lycoperdon (BS 69 % and BPP of 0.99) with the exclusion of L. pyriforme
(Fig 3) that in most modern treatments is placed in Morganella.
In morphology L. pyriforme shows lycoperdoid characters, with
a subgleba, although white, a pseudocolumella, and a capilltium of Lycoperdon-type. In absence of decisive molecular results we prefer to keep L. pyriforme in Lycoperdon.
Several well-supported subclades within Lycoperdon
conform more or less to some of the segregate genera
discussed here. Therefore, we propose a subdivision of the
genus and to recognize Vascellum, Morganella, Bovistella, Utraria, and Apioperdon as subgenera within a broadly defined
Lycoperdon (Fig 3).
Lycoperdon nigrescens and L. caudatum occur on various positions in the phylogenetic trees. For convenience they are here
referred to Lycoperdon subg. Utraria, mainly because this subgenus is less well defined than the other subclades.
Notes on subgenera in Lycoperdon

The subgenus Lycoperdon proposed here corresponds to Lycoperdon section Lycoperdon series Perlata and Candida of Kreisel
16
(1962). The species are characterized by an areolate structure

of sphaerocysts of exoperidial origin (L. perlatum and L. norvegicum) or of a continuous layer of sphaerocysts of endoperidial
origin (L. marginatum) covering the endoperidium after the fall
of the larger exoperidial spines. A diaphragm is absent and the
mature gleba is dominated by capillitium. Paracapillitium occurs in L. perlatum and L. norvegicum but is lacking in L. marginatum. A pseudocolumella is present but may be weakly
developed in L. marginatum. A close phylogenetic relationship
between L. perlatum and L. marginatum was also reported by
Bates (2004).
Subgenus Vascellum corresponds to the genus Vascellum,
segregated from Lycoperdon to accommodate Lycoperdon
depressum (Vascellum pratense) (Pilat 1958). Several species
have later been combined to Vascellum (Ponce de Leon 1970;
Smith 1974; Kreisel 1993). The main distinguishing features
of the subgenus are the presence of a diaphragm, a total
lack of pseudocolumella and the dominance of hyaline paracapillitium in the mature gleba (Fig 4). Vascellum pratense is
somewhat variable in morphology and two forms are included
here, fruiting bodies closely coinciding with the traditional
concept of the species and fruiting bodies reminding of
V. intermedium A. H. Smith (1974). Our data indicate conspecificity, but according to the phylogram presented by Bates
(2004) V. intermedium seems to be closely related but distinct
from V. pratense. Maybe the species has been misinterpreted
in Europe and that its distribution is strictly American. Type
material of V. intermedium has not been sequenced.
Subgenus Morganella is represented in our analyses by GenBank sequences of M. fuliginea and M. subincarnata, two species
that originally were described in Lycoperdon but combined to
Morganella by Kreisel & Dring (1964). Morganella was erected
by Zeller (1948) and emended by Kreisel & Dring to include
small, usually dark-coloured, lignicolous puffballs presenting
only paracapillitium along with persistent, hyaline glebal
membranes in the mature gleba. A subgleba is present or absent depending on species. Only L. subincarnatum occurs in
Europe, but it is not known from the Nordic countries.
L. pyriforme was as earlier mentioned recently combined
to the genus Morganella by Kruger & Kreisel (2003). In our
analyses this species takes a basal position in the Lycoperdon clade. Also in the studies by Kruger et al. (2001) and
Bates (2004) it occurs separated from other Morganella species and in the trees presented by Bates (2004) it clusters
with Disciseda; however, without support. For L. pyriforme
Kruger & Kreisel (2003) created Morganella subgenus Apioperdon, characterized by Lycoperdon-like fruiting bodies, but
sharing the lignicolous habit with the other species in Morganella. Lycoperdon pyriforme differs from the traditional concept of Morganella also in having a true capillitium with
abundant paracapillitium present, a permanently white subgleba, conspicuous white rhizomorphs, and an exoperidium
constructed of sphaerocysts with finger-like protuberances.
Demoulin (1976) surveyed species of Lycoperdon with setose
exoperidial elements and describes two new species, of
which L. melanesicum is considered closely related to L. pyriforme. However, this species was not included in this study.
We suggest that Morganella pyriforme is excluded from Lycoperdon subgenus Morganella. As the morphological characters
do not match any of the other subgenera treated here we
propose that Apioperdon is retained as a monotypic subgenus

within Lycoperdon.
Subgenus Bovistella is proposed to accommodate L. utriforme and L. radicatum, formerly placed in Handkea and Bovistella, respectively. The subgenus is characterized by
medium-sized fruiting bodies provided with a distinct
pseudo-diaphragm. The capillitium is fragile with more or
less abundant pits of irregular outline. The genus Bovistella
was described by Morgan already in 1892. The designated
type species, Mycenastrum ohiense, is considered a synonym
of L. radicatum (Kreisel & Calonge 1993). Lycoperdon utriforme
is a well-known and readily distinguished puffball with large,
persistent, urniform fruiting bodies at maturity and the presence of a pseudodiaphragm dividing the gleba from the
subgleba. Microscopically, it is characterized by a fragile capillitium with widened ramifications and subglobose to slightly
ellipsoid spores (Fig 4). Kreisel (1989) designated L. utriforme as
generic type of his new genus Handkea that was segregated
from Calvatia to accommodate species with slit-like scars in
their capillitial walls. However, according to the results of
the present study Handkea is polyphyletic (Figs 1 and 2).
In our analyses, as well as in those of Bates (2004), a close
phylogenetic relationship between L. utriforme and L. radicatum is strongly supported. The two species have several
morphological features in common such as the urn-shaped
fruiting bodies, the parchment-like endoperidia, the presence of a pseudo-diaphragm dividing the gleba from the
subgleba, and the presence of subglobose to ellipsoid spores.
Distinguishing characters are found in the spore morphology, where L. radicatum has pedicellate spores, whereas
they are apedicellate in L. utriforme (Fig 4). In the structure
of the capillitium L. radicatum is provided with a bovistalike type with dichotomous branching and tapering ends
whereas that of L. utriforme, when totally ripe, is fragmented
and thus appearing lycoperdon-like. However capillitium
from immature samples of L. utriforme show strong
bovista-like tendencies. When mature the capillitium in
both taxa is fragile with walls provided with abundant, irregular to slit-like pits. Subgenus Utraria is not supported
as monophyletic and is composed of a heterogeneous assemblage of species with a wide range of combinations of
morphological characters. It is accepted here only tentatively and for practical reasons. With geographically broader
sampling in future phylogenetic analyses we expect a subdivision of the group. Common characters are the presence of
a subgleba (lacunar or subcompact) in combination with
a dominating true capillitium in the mature gleba. The majority of the species show a lycoperdoid type of capillitium
but partly intermediate tendencies (Lycoperdon Bovista;
reminding of the type found in the central part of the gleba
of B. aestivalis) may characterize some species, e.g. L. altimontanum, L. frigidum, L. atropurpureum and L. decipiens.
Notes on species in Lycoperdon

Lycoperdon molle is a widespread and polymorphous species
known from a wide range of habitats. The samples included
in our study represent a typical lowland ecotype, as well as a
sample from a subalpine habitat. L. frigidum is an arcticalpine
species that belongs to the morphological species complex
around L. molle but is distinguished by its larger spores

(4.55.56 mm) and its elastic, thick-walled capillitium with
rare, small pits. Our samples match this concept, although
certain variability is noted concerning the elasticity of the capillitium and the occurrence of pits. Sequence data identify two
ITS sequence types that differ in two basepair substitutions.
However, the sequence divergence could not be correlated to
differences in morphology or ecology (Figs 2 and 3). Two specimens of Lycoperdon sp. 1, representing a new species, were included in our study. Both specimens originate from subalpine
habitats in South-Central Norway. Although having rather
small spores (3.54.5 mm) both macro- and microscopical characters indicate a relationship with L. molle. Molecular data also
confirm a close relationship to L. frigidum, and the three species cluster with 74 % BS support and 0.99 BPP (Fig 3). A formal
description of the new species will have to wait until more
material is available.
L. niveum is described on material collected in the Himalayas (Kreisel 1969b). A few years later, after examining additional material from the same geographical region, the
diagnosis was emended (Kreisel 1976). Demoulin (1972a) and
Hallgrmsson (1993) later reported it from Iceland. In the present analyses samples originating from Norway and Iceland
have been included. The species belongs to the L. molle morphological species complex and seems to be confined to arcticalpine environments. The main diagnostic characters are
the relatively large spore dimensions (4.55.56 mm) in combination with a fragile and frequently pitted capillitium. DNA
was extracted from the holotype, but failed to yield sequence
data. However, the sequence of a younger specimen from the
Himalayas (cf Kreisel 1976) was identical to sequences of
North European specimens of L. lividum. For the time being
we prefer to identify the IcelandicNorwegian taxon as L.
niveum. A lowland Lycoperdon specimen originating from a calcareous grassland habitat on the Baltic sea island Gotland
clustered in our analyses among the arcticalpine samples
of this species, whereas a Greenland specimen, morphologically matching the description of L. niveum, clustered with L.
frigidum. The ambiguous results emphasise the necessity for
a profound study of this species complex, including new samples from alpine habitats in the Himalayas.
Ortega & et al. (1985) synonymized L. atropurpureum with L.
decipiens whereas Jeppson & Demoulin (1989) kept them separate based on morphological characters and the differences in
habitat preferences. L. atropurpureum is a thermophilic, mainly
European species common in the Mediterranean vegetation,
but with scattered occurrences in deciduous forests on calcareous soils north to about 58 N. Lycoperdon decipiens is a widespread species, typically growing in dry calcareous
grasslands and open deciduous forests. Molecular data support the recognition of two species (Figs 2 and 3) and a table
presenting distinguishing morphological characters was provided by Jeppson & Demoulin (1989).
L. altimontanum was described from an alpine site in the
Himalayas (Kreisel 1976). A sequence of the holotype is included here and it confirms L. altimontanum as a distinct species. A sequence of a Norwegian specimen, determined as L.
altimontanum, clusters with the holotype with moderate support (dataset 2 79 % BS, 0.92 BPP). As it matches the holotype
both in morphology and in ITS sequence, we are convinced
17
that L. altimontanum can be reported from Europe. The Norwegian specimen originates from a subalpine grassland habitat
in Southern Central Norway. Another specimen from the
same region (leg. J. Stordal, det. M. Jeppson) is deposited at
the Oslo herbarium (O). L. altimontanum is morphologically related to L. molle, but distinguished by the distinctly intermediate LycoperdonBovista-type of capillitium and its strongly
warted spores. However, sequence analyses strongly support
a connection with L. excipuliforme (Figs 1 and 3).
L. excipuliforme was first moved to Calvatia (Perdeck 1950)
and later transferred to Handkea (Kreisel 1989) because it shares
the slit-like scars in the capillitial walls with L. utriforme, the
type of Handkea. As already mentioned, molecular results suggest Handkea to be polyphyletic and nomenclaturally a synonym of Bovistella. The overall features of L. excipuliforme are
strongly lycoperdoid, and it shares the wide apical rupture of
the peridium at maturity with, e.g. L. cretaceum and L. turneri.
L. lambinonii seems to have a wide distribution on the Eurasian continent, as well as in N. America. There are also records from Iceland (Demoulin 1972b; Hallgrmsson 1993). In
morphology the species is distinguished by fruiting bodies
showing characters intermediate between L. molle and L.
umbrinum. The spores are however smaller (33.54 mm), moderately warted, and the capillitium is usually elastic, rather
thick-walled and with small pits. The sequence variation between the two specimens sequenced is rather high and they
form an unsupported clade.
L muscorum is described from N. America. Demoulin (1979)
considered it a variety of L. ericaeum (var. subareolatum) and
mentioned morphological differences in exoperidial features
and capillitium. Kreisel (1987) restored its specific rank.
Sequence data of L. muscorum confirm it as separate from
L. ericaeum. L. muscorum is rare and grows among mosses on
wet acidic soils in forests or at forest edges. L. ericaeum is preferably found in dry acidic grasslands and is widespread in
Europe and North America (Demoulin 1972a). Lycoperdon sp. 2
is an apparently undescribed species closely related to L. muscorum and L. ericaeum. The specimens included here originate
from mull-rich soil in beech forests in the southernmost parts
of Sweden. The fruiting bodies are characterized by an exoperidium showing features intermediate between L. molle and L.
umbrinum. The spores are moderately ornamented (BC in
the terminology of Demoulin 1972a), and thus reminiscent of
L. lambinonii. However, the spores are constantly larger than
in L. lambinonii and the capillitium is provided with pits.
According to sequence data this is a distinct species, but a formal description should wait until more specimens become
available.
The description of L. cretaceum was based on specimens
from Bellot Island in Canada. It is an arcticalpine species
that in northern Europe occurs in subalpinealpine grasslands
and heathlands on calcareous soil. Although it traditionally
was included in the genus Calvatia due to its wide apical rupture of the peridium at maturity, the micro-morphological
characters are those of Lycoperdon. In our analyses L. cretaceum
takes a place in Lycoperdon 2, well separated from Calvatia
(Fig 1). The study included samples from a Norwegian, as
well as an Icelandic site, and their conspecificity could here
be confirmed. Lange (1990) distinguished several arcticalpine
Calvatia species from Northern Europe, Greenland, and
18
Svalbard. Except for Calvatia (Lycoperdon) turneri none of these

species could be recognized in the material available, but they
are likely to be very close to L. cretaceum.
L. turneri is also described from Canada. This species has in
Europe traditionally been named C. tatrensis (Demoulin &
Lange 1990). It is an arcticalpine species occurring in subalpine forests, as well as in arcticalpine heathlands, usually
on more or less acid soils. Its apical rupture at maturity is
a wide more or less irregular opening but other morphological
characters are lycoperdoid. Sequence data place it within
Lycoperdon 2 where it clusters with L. umbrinum (Fig 3), a lowland species that preferably grows on slightly acid soils.
L. caudatum is a species of fens and wet grasslands on calcareous soils. It takes a morphologically isolated position presenting a lycoperdoid capillitium and elliptic spores provided
with long pedicells. The phylogenetic position is ambiguous
and the species is here included in subgenus Utraria only
for convenience. Morphologically closely related species are
L. yetisodale Kreisel (1969a,b) known from Nepal and L. ovalicaudatum Bisht et al. (2006) described from Western Himalaya.
Sequence data are not yet available for these species.
L. nigrescens is a distinct and characteristic species, and
morphologically it is usually regarded as closely related to
L. perlatum. The two species have an areolate appearance of
the peridium in common. In the present analyses the position
of L. nigrescens in the phylogenetic trees is ambiguous (Figs 1
and 3).
L. dermoxanthum seems to have caused a bit of confusion
over the years. Hollos (1904) described the same species as L.
hungaricum, a taxon that Kreisel (1967) incorporated in his concept of Bovista pusilla together with Bovista furfuracea. Moyersoen & Demoulin (1996) regarded B. furfuracea and B.
dermoxantha as distinct species. The distinguishing features
of the latter are the lycoperdoid characters in the general fruitbody morphology, including spores, capillitium, and the presence of a reduced whitish subgleba. In our analyses L.
dermoxanthum clusters with Lycoperdon sp. 3 within Lycoperdon 2, well separated from Bovista.
Lycoperdon sp. 3 is a small inconspicuous puffball occurring
among mosses on siliceous rocks. Based on morphology it was
for some time considered to belong in the species complexes
around L. ericaeum or L. niveum (Martn & Jeppson 2001), but
sequence data suggest an affinity to L. dermoxanthum. Conspecificity between the Scandinavian collections and the morphologically similar specimens from Spain reported by
Martn & Jeppson (2001) has yet to be demonstrated using
molecular methods.
Notes on Bovista, Calvatia, and Disciseda

The genus Bovista forms a clade that receives no support in the
BS analyses and only moderate support (0.94 BPP) in the
19
Bayesian analysis (Fig 1). The main character on which to distinguish a majority of the species of Bovista is the lack of a subgleba, although a reduced to well-developed subgleba is
present in some species. When such a structure is present, it
is always compact and more or less cottony, a feature distinguishing the genus from Lycoperdon where a subgleba is always present and more or less lacunar.
Bovista splits in two strongly supported clades, Bovista and
Globaria that more or less correspond to the subgeneric division by Kreisel (1964, 1967). Subgenus Bovista includes species
with a dichotomously branched capillitium of Bovista-type
and pedicellate spores whereas species in subgenus Globaria
have more lycoperdoid characters, presenting a capillitium
of intermediate LycoperdonBovista type or pure Lycoperdon
type combined with apedicellate spores (Fig 4).
The majority of species in subgenus Globaria were originally described in Lycoperdon and were treated as such by,
e.g. Hollos (1904), Perdeck (1950), Eckblad (1955), and Pilat
(1958). However, B. dermoxantha that traditionally was placed
in subgenus Globaria, clustered in our analyses within Lycoperdon 2 (Fig 1). With the exclusion of B. dermoxantha and
with the inclusion of B. limosa and a new species here named
B. cfr limosa, our results support the subgeneric division of
Kreisel (1967).
B. cretacea was first described from the north of Sweden. It
has since been collected in subarctic regions in Norway,
Iceland, and Russia but seems to be rare. It can easily be confused with the more common species B. paludosa. The distinguishing characters are to be found in the subglobose (versus
pyriform) fruit body, a slightly different exoperidium, its
somewhat tortuous capillitium, and the caespitose growth
(Jeppson 1999).
B. graveolens is also uncommon, but has a wide distribution
on the Eurasian continent. Macroscopically it can easily be
confused with B. nigrescens, but a microscopic analysis reveals
the presence of spores provided with a curved pedicell, a character unique to this species (Fig 4).
B. limosa is described from Greenland but was for several
years confused with the South American species B. echinella
(syn. Bovistella echinella). Kreisel (1967) observed its true identity and placed it as the only species in subgenus Globaria section Geastrostoma because of the protruding, more or less
Geastrum-like apical stoma. However, as observed by Lange
(1987) it shows morphological characters rather suggesting
a close relationship with subgenus Bovista. This is confirmed
in our analyses (Figs 1 and 2).
As noted by Calonge & Demoulin (1975) and Lange (1987),
B. limosa sensu Kreisel is a heterogeneous taxon. Our analyses
indicate that B. limosa should be divided in two taxa (Figs 1 and
2) with slighty overlapping but mainly different distribution
ranges. Specimens coinciding with B. limosa sensu Rostrup display a northern distribution with a preference for more or less
Fig 4 (A) Lycoperdon pratense, detail of exoperidium. (B) L. pratense, fruiting bodies. (C) L. pratense, paracapillitium.
(D) L. pratense, basidiospores. (E) L. utriforme, capillitium. (F) L. utriforme, basidiospores. (G) L. pyriforme, irregularly shaped
cells from exoperidium. (H) Bovista graveolens, basidiospores. (I) Schematic section through mature fruiting body of Lycoperdon; os, ostiole; gl, gleba; ps, pseudocolumella; en, endoperidium; ex, exoperidium; su, subgleba; rh, rhizomorphs. (J)
Lycoperdon radicatum, capillitium. (K) L. radicatum, basidiospores. (L) Bovista tomentosa, capillitium of Bovista type. (M) Lycoperdon decipiens, capillitium of Lycoperdon type.
20
subalpinealpine sites. Specimens from South Scandinavia

and Central and South Europe deviate in morphology by the
lack of the prominent stoma, the main character of Kreisels
section Geastrostoma, and typically occur among mosses
on calcareous flat rocks and calcareous sand dunes in hemiboreal and nemoral regions.
One sequence of Bovista pusilla was included in the phylogenetic analyses by Kruger et al. (2001) and Bates (2004), in
the latter case renamed B. dermoxantha. This sequence (GenBank no. AJ237631) is included here and shows a high similarity to our sequence of B. furfuracea. We conclude that AJ237631
was identified by Kruger et al. in accordance with the concept
of B. pusilla used by Kreisel. The sequence was later renamed
by Bates following Moyersoen & Demoulin (1996) who showed
that B. pusilla in the sense of Kreisel (1967) represents two different taxa, viz. B. furfuracea and Lycoperdon dermoxanthum. B.
furfuracea is a small and globose puffball that except for the
lack of a subgleba shows lycoperdoid features.
B. tomentosa is a morphologically characteristic species,
typical of dry and exposed habitats. Molecular data confirm
it as a distinct species clustering in the Bovista clade (Figs 1
and 2). A specimen of B. minor collected in Wisconsin (USA)
was included in our dataset. Traditionally the species has
been considered to be a rare North American counterpart of
the mainly Eurasian B. tomentosa, but sequence data revealed
conspecificity with the European sample of B. tomentosa.
According to Kreisel (1967) the main differentiating characters
between the two are the slightly larger fruiting bodies, the
subhypogeous habit, and the preference for wooded habitats
of B. minor. The sample of B. minor used in our analyses agrees
with Kreisels definition and the results would thus suggest
a synonymy with B. tomentosa.
B. aestivalis is a polymorphous species with a wide distribution and with a wide range of habitat preferences (Jeppson
2001). Our Scandinavian specimens represent two different
ecotypes, one characteristic of dry, exposed habitats whereas
the other is found in deciduous forests on mull-rich, often calcareous soils. These ecotypes have in North Europe sometimes been referred to as B. aestivalis and B. dryina (Morgan)
Demoulin (1979) respectively (Ulvinen 1969, 1997). However,
as shown by Demoulin (1979) B. dryina is a well-defined North
American species, which is not on record from Europe. A third
sequence labelled B. polymorpha, which is a species considered
to be a synonym of B. aestivalis (Demoulin 1979; Moyersoen &
Demoulin 1996; Jeppson 2001), was taken from GenBank. The
three sequences are identical in the ITS region and cluster
with 77 % BS support and 1.0 BPP (Fig 1).
B. promontorii is a rare puffball with a strong morphological resemblance to B. aestivalis. Its main differentiating
character is the presence of distinctly ellipsoid spores. The
species was described from South Africa (Kreisel 1967) and
later reported from Spain (Ortega & Buenda 1989; Calonge
1992, 1998). The sample included in our material originates
from a sandy Pinus pinea forest in southernmost Spain. Sequence data confirm it as a distinct species closely related
to B. aestivalis.
Calvatia includes species that show a more or less irregular
rupture of the peridium at maturity or, in the case of subgenus
Langermannia, a total dehiscence of the peridium. Species are
medium- to large, and a subgleba is present or lacking (Kreisel
1992). Langermannia is the older genus name for this group, but
through conservation rejected in favour of Calvatia. Some authors prefer to recognize Langermannia on genus level (e.g. Calonge & Martn 1990; Lange 1993; Calonge 1998) whereas others
prefer one genus (e.g. Kreisel 1992).
The study by Bates (2004) sampled six Calvatia species. In
the analyses they separate into two distinct groups, each
well supported and corresponding to Calvatia s. str. and Langermannia. Our analyses basically show the same results, although Langermannia is represented only by one sequence.
From these two studies it seems clear that Calvatia and Langermannia should both be treated as genera. Still we suggest Calvatia is retained in a wide sense with Langermannia as
a subgenus.
The genus Disciseda is characterized by subhypogeous
fruiting bodies with a specialized way of dehiscence at maturity. The rupture of the exoperidium is more or less circumscissile and the fruit body is turned over exposing an
originally basal pore for the dispersal of the powdery spore
mass. The genus has a worldwide distribution, but is restricted to xeric habitats. In our analyses the two North European species D. candida and D. bovista form an unsupported
sister clade to the rest of Lycoperdaceae. D. bovista is rare and
the species seems to decline in Northern Europe. It is characterized by having strongly ornamented spores. D. candida is
more frequent and macroscopically easily confused with D.
bovista, but distinguished by smaller and only faintly ornamented spores.
Acknowledgements
We thank the curators of the herbarium at GB, C, O and AMNH
and Dr. H. Kreisel for kindly providing material, Henrik
Nilsson for help with the Bayesian analyses, and Karl-Henrik
Larsson for advice with nomenclatural issues. Financial support for this study was received from The Swedish Taxonomy
Initiative, ArtDatabanken SLU, to E.L. (Grant dha 7/04) and
Kapten Carl Stenholms fond to M.J., which are gratefully
acknowledged.
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2008 - Larsson e Jeppson - Phylogenetic Relationships Among Species and Genera

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mycological research 112 (2008) 422

journal homepage: www.elsevier.com/locate/mycres

Phylogenetic relationships among species and genera

Phylogenetic relationships, limits of species, and genera within Lycoperdaceae, were

Received 19 March 2007

Received in revised form

Accepted 15 October 2007

solved. The phylogenetic analyses identified 31 species of Lycoperdon, 11 species of Bovista,

fication of Lycoperdaceae is proposed based on the results of the phylogenetic analyses.

Pilat 1958). The family initially contained various types of

Mycenastraceae, a concept introduced already by Zeller (1949).

Materials and methods

Svalbard, and North America. Data on sequenced specimens

GenBank accession no.

2338 (MJ). Harjedalen: Funasdalen: Mittaklappen, 6 Aug. 2004,

GenBank accession no.

1988, J. & M. Jeppson 2585 (MJ). Oland: Hulterstad: Gosslunda, 7

Lycoperdon excipulifome. Austria: Burgenland: Jois, Junger Berg,

Lobuche, 49505000 m.sm., Sep. 1962, J. Poelt, det. H. Kreisel

DNA extraction, PCR and sequencing

CI 0.5396, RI 0.7190). The strict consensus tree is presented

Vascellum pratense MJ4864

Vascellum pratense MJ4864

Type species: Mycenastrum ohiense Ellis & Morgan, J. Mycol. 1:

Molecular based classification of Lycoperdaceae

Lycoperdon utriforme Bull., Hist. Champ. France: 153 (1791):

Lycoperdon ericaeum Bonord., Bot. Zeitung (Berlin) 15: 596 (1857).

Lycoperdon turneri Ellis & Everh., J. Mycol. 1(7): 87 (1885).

Lycoperdon echinatum Pers., Ann. Bot. (Usteri) 11: 28 (1797):

Calvatia rubroflava (Cragin) Morgan, J. Cincinnati Soc. Nat. Hist.

Lycoperdon pyriforme Schaeff., Fung. Bavar. Palat. nasc. 4: 128

Bovista graveolens Schwalb, Lotos, n.s. 13: 53 (1893).

Calvatia Fr., Summa veg. Scand.: 442 (1849).

Bovista limosa Rostr., Meddel. Grnland 18: 52 (1894).

Bovista plumbea Pers., Obs. mycol. 1: 5 (1796): Pers., Syn. meth.

Bovista cfr. limosa

Bovista tomentosa (Vittad.) De Toni, Syll. fung. (Abellini) 7: 97

Bovista promontorii Kreisel, Beih. Nova Hedwigia 25: 225 (1967).

Notes on subgenera in Lycoperdon

(1962). The species are characterized by an areolate structure

propose that Apioperdon is retained as a monotypic subgenus

Notes on species in Lycoperdon

around L. molle but is distinguished by its larger spores

Svalbard. Except for Calvatia (Lycoperdon) turneri none of these

Notes on Bovista, Calvatia, and Disciseda

subalpinealpine sites. Specimens from South Scandinavia

Moyersoen B, Demoulin V, 1996. Les Gasteromyce`tes de Corse:

Sarasini M, 2005. Gasteromiceti epigei. Assoziazione Micologica

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