Mutinus albotruncatus (Phallales - Real Jardín Botánico

Phytotaxa 236 (3): 237–248
www.mapress.com/phytotaxa/
Copyright © 2015 Magnolia Press
Article
ISSN 1179-3155 (print edition)
PHYTOTAXA
ISSN 1179-3163 (online edition)
http://dx.doi.org/10.11646/phytotaxa.236.3.4
Mutinus albotruncatus (Phallales, Agaricomycetes), a new phalloid from the
Brazilian semiarid, and a key to the world species
BIANCA D. B. DA SILVA*1, TIARA S. CABRAL2, MARÍA P. MARTÍN3, PAULO MARINHO4, FRANCISCO D.
CALONGE5 & IURI GOULART BASEIA6
Programa de Pós-graduação em Sistemática e Evolução, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte,
59072-970 Brazil. Email: biancadeni@yahoo.com.br
2
Programa de Pós-graduação em Genética, Conservação e Biologia Evolutiva, Instituto Nacional de Pesquisas da Amazônia–INPA; Av.
André Araújo, 2936–Petrópolis; Manaus, Amazonas, 69067-375 Brazil. Email: ttiara@gmail.com
3
Departamento de Micología, Real Jardín Botánico–CSIC, Plaza de Murillo 2, 28014 Madrid, Spain. Email: maripaz@rjb.csic.es
4
Departamento de Biologia Celular e Genética, Universidade Federal do Rio Grande do Norte; Natal, Rio Grande do Norte 59072-970,
Brazil. Email: pmarinho@ufrnet.br
5
Departamento de Micología, Real Jardín Botánico–CSIC, Plaza de Murillo 2, 28014 Madrid, Spain. Email: calonge@rjb.csic.es
6
Departamento de Botânica e Zoologia, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte, 59072-970 Brazil.
Email: iuri.baseia@gmail.com
*Corresponding author: Bianca D. B. da Silva, email: biancadeni@yahoo.com.br
1
Abstract
A new species of the genus Mutinus has been found in the semiarid region of Northeastern Brazil. Mutinus albotruncatus
is described macro- and microscopically, and is characterized by the white pseudostipe and truncated apex. Molecular and
ecological data are also provided. Phylogenetic analyses, based on LSU (large subunit of nuclear ribosomal DNA) and atp6
(subunit 6 of ATP synthase) sequences, support the inclusion of this new species in the genus Mutinus. A provisional key to
the species of Mutinus known in the world is proposed.
Key words: Gasteromycetes, fungal taxonomy, phalloid fungi, phylogeny, stinkhorns
Introduction
The genus Mutinus Fries (1849: 434) belongs to the family Phallaceae Corda (1842: 29), of the order Phallales Fischer
(1898: 276), and the Subclass Phallomycetidae Hosaka, Castellano & Spatafora (2006: 955) (Hosaka et al. 2006). It
is characterized by presenting a globose to ovoid, white to yellowish immature basidiome basally attached by white
rhizomorphs; with a mucilaginous layer inside, splitting at the apex into two or three lobes and finally collapsing against
the base of the spongy pseudostipe, cylindrical to fusiform, hollow, perforated or not at the tip; gleba mucilaginous,
covering the apical portion of the pseudostipe; and elliptical and smooth basidiospores (Bottomley 1948, Dring 1964,
Liu 1984, Pegler et al. 1995, Calonge 1998).
Cunningham (1944) separates the species of the genus into three sections: Glabrosi, characterized by the fertile
portion smooth or rugulose; Granulosi, with fertile portion with irregular pseudoparenchymatous processes, appearing
pseudo-reticulate; and Tuberculosi, with fertile portion covered with digitate processes. Mutinus is close to Phallus
Junius ex Linnaeus (1753: 1178), differing by the presence of gleba on the receptacle on the apical part of the pseudostipe
in Phallus (Calonge 1998).
According to Index Fungorum (http://www.indexfungorum.org/Names/Names.asp—accessed April 2015) and
MycoBank (http://www.mycobank.org/—accessed April 2015) there are 36 species of Mutinus described to date.
Mutinus caninus (Huds.) Fries (1849: 434) is the type species of the genus and six synonyms may be considered:
Aedycia Rafinesque (1808: 358), Caromyxa Montagne (1856: 281), Corynites Berk. & M.A. Curtis (1853: 136),
Cynophallus (Fr.) Corda (1842: 29), Floccomutinus Hennings (1895: 109), and Jansia Penzig (1899: 139) (Kirk et al.
2008). The genera Jansia and Floccomutinus have been shown molecularly to belong to the genus Mutinus (Degreef
et al. 2013, Trierveiler-Pereira et al. 2014).
Accepted by Genevieve Gates: 13 Nov. 2015; published: 1 Dec. 2015
237
Seven Mutinus species are recorded from Brazil, distributed throughout the Northeast, North, and South Regions
of the country. The first species was Mutinus bambusinus (Zoll.) E. Fischer (1886: 30), cited by Möller (1895) and
Rick (1961), followed by M. borneensis Cesati (1879: 13), M rugulosus Rick (1929: 300) (Rick, 1961), M. argentinus
Spegazzini (1887: 62) (Meijer 2006, Magnago et al. 2013), M. caninus (Baseia et al. 2006, Trierveiler-Pereira et al.
2011, Magnago et al. 2013), M. elegans (Mont.) E. Fischer (1888: 13) (Cortez et al. 2008), and M. fleischeri Penzig
1899: 137) (Cabral et al. 2014). Of those, according to Möller (1895) and Liu (1984), M. argentinus is considered
synonymous with M. bambusinus, while Dring & Rose (1977) argue that the true M. bambusinus has a longer, often
more strongly colored fertile portion, with a much more marked sterile tip than M. argentinus. In the Northeast Region
of Brazil, only M. argentinus and M. caninus have been recorded, growing in vegetated areas of Atlantic forest from
the state of Rio Grande do Norte.
During our studies on gasteroid fungi in Brazil, we collected specimens (UFRN-Fungos 2025) of a taxon of
Phallaceae with a lignicolous habitat, and the morphological characters of the genus Mutinus, although the apical
portion of the pseudostipe resembles species of the genus Phallus. In order to clarify the phylogenetic position of
these specimens, sequences of LSU (large subunit of nuclear ribosome DNA) and atp6 (subunit 6 of ATP synthase)
were compared with homologous sequences from GenBank published by Degreef et al. (2013) and Hosaka et al.
(2006), and newly generated sequences from other Mutinus species from Brazil. Morphological characters were also
compared with all the species of the genus Mutinus described to date. Thus, after seven decades, a new Mutinus species
is described. Moreover, a provisional key for all known species of the genus Mutinus is proposed (not considering the
synonyms).
Materials and methods
Morphological analysis
The specimens studied were collected in the Floresta Nacional do Araripe (FLONA Araripe), State of Ceará, Brazil
(7°11’42”S, 39°13’28”W), located in a semiarid region (Ministério do Meio Ambiente 2004). The macroscopic
analyses were performed on fresh material, using a stereoscopic microscope. Colors were standardized according to
Kornerup & Wanscher (1978). For the analysis of microstructures, hand-cut sections of dried material were mounted
in 5% KOH, Melzer’s reagent and Congo Red for light microscopic examination. We measured 20 of each of the
following structures: the basidiospores, the pseudoparenchymatous cells of the pseudostipe, the hyphae of the volva,
and the hyphae of the rhizomorphs. The material was deposited in the Herbarium UFRN at the Universidade Federal
do Rio Grande do Norte, Brazil. Herbarium acronyms are according to Thiers (2015).
DNA extraction, PCR amplification, and DNA sequencing
DNA was extracted from fresh basidiomata of collection UFRN-Fungos 2025 (Table 1), following Silva et al. (2013).
Since very few Mutinus sequences were found in GenBank, DNA was isolated from two other Mutinus collections kept
at the UFRN-Fungos herbarium. The LSU and atp6 regions were amplified using previously described primers LR0R/
LR5 (Vilgalys & Hester 1990) and ATP6-1/ATP6-2 (Kretzer & Bruns 1999). PCR amplifications were performed with
50ng of DNA in a basic reaction of 0.5µl of each 10µM primer, 0.8µl of dNTP’s (10mM), 0.08µl of 5U/µl KAPA Taq
Standard (KAPA Biosystems), 2µl of KAPA Taq Buffer A (10X, with 1.5 mM MgCl2 at 1X) and 1.5µl of 25mM MgCl2
for atp6 PCR reactions. The atp6 amplifications were done following thermal cycling conditions of Kretzer & Bruns
(1999), while LSU cycling parameters were 1 cycle of 94ºC for 3 min., 35 cycles of 94ºC for 1 min., 53ºC for 30 sec.
and 72ºC for 1 min., and final extension of 72ºC for 10 min. The PCR reactions were confirmed in a 1.5% agarose
gel, stained with GelRed™ (Biotium, City, Country) and examined under UV light. The PCR fragments were purified
using FastAP™ (Thermo Scientific, City, Country), following the manufacturer’s instructions. Sequencing reactions
were performed with BigDye® Terminator v3.1 Cycle Sequencing Kit with the same primers as in the PCR, and
submitted to ABI 3500 Genetic Analyzer. The barcoding sequence (ITS: internal transcribed spacer nrDNA, Schoch et
al. 2012) of the new species was deposited in GenBank.
238 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.
Table 1. Species used to reconstruct the phylogenetic tree and their herbarium or isolate numbers and GenBank accession numbers.
Species
Herbarium voucher or
GenBank Accession Number
isolate number
LSU
atp6
REB2182
DQ218624
DQ218913
Anthurus archeri (Berk.) E. Fisch.
UFRN-Fungos 1481
JF968440
JF968438
Abrachium floriforme (Baseia & Calonge) Baseia & T.S. Cabral
OSC122632
DQ218625
DQ218914
Aseroë rubra Labill.
PDD75096
DQ218626
DQ218915
Clathrus chrysomycelinus Möller
OSC38819
DQ218481
DQ218765
Dictyophora duplicata (Bosc) E. Fisch.
OSC36088
DQ218627
DQ218917
Dictyophora indusiata (Vent.) Desv.
MEL1054289
DQ218628
DQ218918
Dictyophora multicolor Berk. & Broome
H4397
DQ218630
DQ218919
Gelopellis sp.
H4571
DQ218631
DQ218920
Gelopellis sp.
OSC122734
DQ218633
DQ218922
Ileodictyon cibarium Tul. & C. Tul.
MEL2054561
DQ218636
DQ218925
Ileodictyon gracile Berk.
UFRN-Fungos 535
JF968441
JF968439
Itajahya rosea (Delile) E. Fisch.
OSC122862
DQ218638
DQ218926
Kobayasia nipponica (Kobayasi) S. Imai & A. Kawam
OSC122864
DQ218640
DQ218928
Laternea triscapa Turpin
OSC39531
DQ218641
DQ218929
Lysurus borealis (Burt) Henn.
MB02012
DQ218507
DQ218791
Lysurus mokusin (L.) Fr.
Mutinus albotruncatus sp. nov.
UFRN-Fungos 2025
KT183493
KT183490
OSC107657
AY574643
AY574785
Mutinus elegans (Mont.) E. Fisch.
JD837
KC128656
Mutinus zenkeri (Henn.) E. Fisch.
JD782
KC128655
Mutinus zenkeri (Henn.) E. Fisch.
JD781
KC128654
Mutinus zenkeri (Henn.) E. Fisch.
UFRN-Fungos 2021
KT183495
KT183492
Mutinus sp.
UFRN-Fungos 1371
KT183494
KT183491
Mutinus sp.
PDD76197
DQ218642
DQ218930
Phallobata alba G. Cunn.
MB-02-040
DQ218513
DQ218797
Phallus costatus Vent.
OSC107658
DQ218514
DQ218798
Phallus hadriani Vent.
CUW s.n.
DQ218515
DQ218799
Phallus ravenelii Berk. & M.A. Curtis
OKM21898
DQ218516
DQ218800
Protubera borealis S. Imai
MEL2105035
DQ218645
DQ218932
Protubera canescens G.W. Beaton & Malajczuk
T28248
DQ218647
DQ218933
Protubera jamaicensis (Murrill) Zeller
Garido2550-A
DQ218518
DQ218802
Protubera maracuja Möller
OSC59689
DQ218648
DQ218934
Protubera parvispora Castellano & Beever
T12737
DQ218649
DQ218935
Protubera sabulonensis Malloch
ASM-4705
AF213128
Pseudocolus fusiformis (E. Fisch.) Lloyd
MB02016
DQ218521
DQ218806
Simblum sphaerocephalum Schltdl.
OSC65085
DQ218651
DQ218938
Trappea darkeri (Zeller) Castellano
Outgroup
Hysterangium cistophilum (Tul. & C. Tul.) Zeller & C.W. Dodge
Hysterangium album Zeller & C.W. Dodge
T1088
T15139
DQ218493
DQ218490
DQ218777
DQ218774
Sequence alignment and phylogenetic analysis
Sequences were visualized in ChromasPro v 1.7.6 (Technelysium Pty Ltd, City, Country) and assembled in Geneious
XX. The newly generated atp6 and LSU sequences and those selected from Genbank (Table 1) were aligned and
manually edited in MEGA v. 5.2 (Tamura et al. 2007), resulting in two different matrices. Dataset congruence was
analyzed using a preliminary parsimony bootstrapping in PAUP* v.4.0b10 (Swoford 2003), and performing 1000
non-parametric replicates (Felsenstein 1985) with the “fast” stepwise-addition option. Conflicts among datasets were
considered according to Hillis & Bull (1993). Since no conflicts were detected, the datasets were concatenated to
reconstruct the phylogenetic trees. The concatenated alignment was analyzed by maximum parsimony (MP), using
PAUP* v.4.0b10, and Bayesian inference, using Mr. Bayes 3.2.5 (Ronquist et al. 2012).
The MP analysis was conducted under heuristic searches with TBR branch swapping algorithm and initial tree
obtained by stepwise addition with random addition of 100 times repeated sequences and 1000 replicates as bootstrap
(bs) settings.
a new phalloid from Brazil
Phytotaxa 236 (3) © 2015 Magnolia Press • 239
In the Bayesian analysis the two markers were partitioned as separate subsets, with topology linked across subsets,
but with separate model parameters values for each. Nucleotide substitution models were chosen with MrModelTest
(Nylander 2004). Two parallel runs were executed with four incrementally heated simultaneous MCMC simulations
over 2 million generations, with trees sampled at every 1000 generations. Parts of the trees were discarded in a burn-in
stage, by observing the average standard deviation of split frequencies values, to estimate posterior probabilities (pp)
and a consensus tree was reconstructed with the rest. Trees were visualized and edited in FigTree version 1.4.2 (http://
tree.bio.ed.ac.uk/software/figtree/). These data are also available in TreeBASE under ID 18307.
Figure 1. Phylogenetic tree obtained by 50% majority-rule consensus, on Bayesian analysis. Posterior probabilities (>0.6) are indicated
before bars and bootstrap values (>50%) after bars, on nodes.
240 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.
Results
Molecular results
We were able to generate LSU, atp6 and ITS sequences from the Brazilian specimens (Table 1, in bold). The
concatenated matrix of LSU and atp6 had 1250 positions (584 LSU, and 666 atp6). In the MP analysis, 761 positions
were constant, 117 parsimony-uninformative and 372 parsimony-informative. Parsimony tree scores were identical for
all the trees: consistency index (CI) = 0.496, retention index (RI) = 0.702 and homoplasy index = 0.504. The nucleotide
substitution model selected by MrModel was GTR+I+G, for both LSU and atp6 analyses. Best likelihood ratings for
each run were lnL1 = -8637.32 and lnL2 = -8677.50. The 50% majority-rule consensus Bayesian tree is shown in Fig.
1. This consensus tree had almost identical topology as the MP consensus tree (available on TreeBase, ID 18307); the
boostrap values are indicated on the branches of the 50% majority-rule consensus tree (Fig. 1).
According to our analyses, the genus Mutinus is monophyletic with strong support (pp = 1.0; bs = 90%) and
the sequences obtained from Brazilian specimens (UFRN-Fungos 2025) are included in the Mutinus clade. Based on
molecular analyses and morphological data, a new Mutinus species is here described.
Taxonomy
Mutinus albotruncatus B.D.B. Silva & Baseia, sp. nov. (Fig. 2, 3 and 4)
MycoBank no.: MB 812516
Etymology:—albotruncatus refers to the white pseudostipe and truncated apex.
Diagnosis:—Egg fabiform to reniform, 6–17 mm height × 5–8 mm in diameter. Pseudostipe cylindrical, 50–70 mm high, apically perforate,
sterile portion white, straight, not chambered; fertile portion doliform, truncated, slightly rugulose, covering about 1/3 of the total
length of pseudostipe. Gleba confined in the upper region of the pseudostipe, mucilaginous. Basidiospores 3.8–5.0 × 2.2–2.5 µm,
ellipsoid, smooth.
Type:—BRAZIL. Ceará: Crato, Município Santana do Cariri, FLONA Araripe, 07°13.284’S, 39°31.445’W, 947 m, 24 January 2011, BDB
Silva & BT Goto (holotype UFRN 2025, isotype UFRN 2589) [GenBank accession numbers—LSU: KT183493, atp6: KT183490,
ITS: KT202281; all from holotype].
Unexpanded basidiome (egg) fabiform to reniform to ellipsoid (Fig. 2a, 3b), 6–17 mm height × 5–8 in diameter,
epigeous. Exoperidium membranaceous, smooth, white, orangy white (5A2) to greyish orange (6B3), with several
white central rhizomorphs emerging from the base. Endoperidium gelatinous, hyaline. Expanded basidiome formed
by pseudostipe and volva (Fig. 3a). Pseudostipe cylindrical, 50–70 mm height × 4–6 mm diameter, apically perforate,
hollow, spongy; sterile portion white, straight, not chambered (Fig. 2f); fertile portion light brown (6D4), slightly thick,
doliform to cylindrical, truncated (Fig. 2b–2d), slightly rugulose (Fig. 2e), 14–22 mm high, covering about 1/3 of the
total length of pseudostipe. Gleba covering and confined to the upper region of the pseudostipe, mucilaginous, olive
green (3E3) to olive grey (3E2).
Basidiospores 3.8–5.0 × 2.2–2.5 µm, ellipsoid (Fig. 4a), smooth, hyaline to slightly greenish in 5% KOH.
Pseudostipe composed of pseudoparenchymatous cells, hyaline, irregular shaped, 20.2–57.3 × 17.8–47.1 µm (Fig.
4b). Volva formed by filamentous hyphae, septate, branched, hyaline, 2.2–4.5 µm diameter (Fig. 4c). Rhizomorphs
composed of filamentous hyphae, septate, hyaline, 1.4–3.6 µm diameter (Fig. 4d).
Habitat:—growing on decaying wood.
Distribution:—State of Ceará, Brazil.
Remarks:—The presence of a white pseudostipe, a brown, doliform to cylindrical and truncated fertile portion,
and the lignicolous habitat differentiate Mutinus albotruncatus from other species in the genus. The apical region of
the pseudostipe of M. albotruncatus resembles species of the genus Phallus, due to the truncated region and the thick
surface which give the appearance of a receptacle. However, an in-depth analysis of the morphology revealed that
M. albotruncatus does not have a receptacle. The brownish color of the fertile portion resembles M. zenkeri Henn. E.
Fischer (1900: 47). However, M. zenkeri is differentiated by having an incomplete and brittle membrane on which the
gleba is located (Dring & Rose 1977, Degreef et al. 2013). Mutinus annulatus F. M. Bailey (1895: 10), M. borneensis,
M. boninensis Lloyd (1908: 402), M. caninus var. albus Zeller (1944: 263) and M. proximus Berkeley ex Massee
(1891: 94) also have a pseudostipe with a white sterile portion. M. annulatus (Lloyd 1909) is distinguished by an
a new phalloid from Brazil
Phytotaxa 236 (3) © 2015 Magnolia Press • 241
annulated base and red-ochre color of the fertile portion of the pseudostipe, M. borneensis (Lloyd 1909, Grgurinovic
1997) has a shorter and salmon pink or red fertile portion, M. boninensis (Lloyd 1909, Kobayasi 1937) has a fertile
portion with pointed apex and it is completely annulated, M. caninus var. albus (Zeller 1944) has a red and glabrous
fertile portion and M. proximus has an obtuse and imperforate apex, as well as a pseudostipe with an orange-red fertile
portion. Mutinus rugulosus (recorded from the state of Rio Grande do Sul, Brazil (Rick 1929, 1961)) also has a white
pseudostipe but it is a species with little information in its protologue. The only information provided is a comparison
to M. bambusinus, with M. rugulosus having larger basidiomes and a white pseudostipe (Rick 1929).
Figure 2. Mutinus albotruncatus (holotype): a. Immature basidiome; b–d. Fresh basidiome with white pseudostipe and truncated apex;
e. Fertile part slightly rugulose with an olive green spore mass; f. Pseudostipe not chambered. Bar a–d = 10 mm, bar e–f = 5 mm Photos
by: Bianca Silva.
242 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.
Figure 3. Macroscopic drawings. a. Expanded basidiome with volva and pseudostipe, delimiting the sterile and fertile portion, bar = 10
mm; b. Immature basidiome, bar = 5 mm. Drawings by: Rhudson Cruz.
a new phalloid from Brazil
Phytotaxa 236 (3) © 2015 Magnolia Press • 243
Table 2. Species of Mutinus, based on Mycobank and Index Fungorum, and our own observations. Legitimate species are in bold;
synonyms are indented below.
Mutinus albotruncatus B.D.B. Silva & Baseia sp. nov.
Mutinus annulatus F.M. Bailey
≡ Floccomutinus annulatus (F.M. Bailey) Lloyd
≡ Phallus annulatus (F.M. Bailey) G. Cunn.
Mutinus annulatus Lloyd
Mutinus argentinus Speg.
Mutinus bambusinus (Zoll.) E. Fisch.
Mutinus bambusinus Cooke
= Mutinus ravenelii (Berk. & M.A. Curtis) E. Fisch.
Mutinus bicolor Lév.
Mutinus boninensis Lloyd
Mutinus borneensis Ces.
Mutinus bovinus Morgan
= Mutinus curtisii (Berk.) E. Fisch.
Mutinus caninus (Huds.) Fr.
Mutinus caninus var. albus Zeller
Mutinus caninus var. caninus (Huds.) Fr.
Mutinus caninus var. levonensis Noelli
Mutinus cartilagineus J.H. Willis
Mutinus coracoideus Kawam.
Mutinus curtisii (Berk.) E. Fisch.
= Mutinus elegans (Mont.) E. Fisch
Mutinus discolor (Kalchbr.) E. Fisch.
= Phallus aurantiacus var. discolor Kalchbr.
Mutinus elegans (Mont.) E. Fisch
Mutinus fleischeri Penz.
Mutinus granulatus E. Fisch.
Mutinus hardyi F.M. Bailey
= Lysurus mokusin (L.) Fr.
Mutinus inopinatus Ulbr.
= Mutinus elegans (Mont.) E. Fisch
Mutinus minimus Pat.
Mutinus muelleri E. Fisch.
= Mutinus bambusinus (Zoll.) E. Fisch.
Mutinus papuasius Kalchbr.
≡ Phallus papuasius (Kalchbr.) Kalchbr.
Mutinus pentagonus F.M. Bailey
= Lysurus mokusin (L.) Fr.
Mutinus pentagonus var. hardyi F.M. Bailey
= Lysurus mokusin (L.) Fr.
Mutinus pentagonus var. pentagonus F.M. Bailey
= Lysurus mokusin (L.) Fr.
Mutinus penzigii E. Fisch.
Mutinus proximus Berk. ex Massee
Mutinus quadrigenus Sawada
Mutinus ravenelii (Berk. & M.A. Curtis) E. Fisch
Mutinus rugulosus Rick
Mutinus sulcatus Cooke & Massee
= Lysurus gardneri Berk.
= Lysurus cruciatus (Lepr. & Mont.) Henn.
Mutinus watsonii (Berk.) E. Fisch.
= Mutinus borneensis Ces.
Mutinus xylogenus Lloyd
≡ Xylophallus xylogenus (Mont.) E. Fisch.
Mutinus zenkeri (Henn.) E. Fisch.
244 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.
There are many species of the genus Mutinus that need to be reviewed. Some features are lost when the material
is dry and this complicates the analysis of the specimens. Moreover, as in M. rugulosus, there are some species with
little information in their protologues: M. bicolor Léveillé (1855: 109), M. coracoideus Kawamura (1929: 300), M.
granulatus E. Fischer (1927: 472), M. proximus, M. quadrigenus Sawada (1931: 330); and, in some cases, they have
been only recorded a single time from their type locality. Based on our survey, we accept 21 species in the genus
Mutinus (Table 2), including the new species here described.
Figure 4. Photographs of microstructures of Mutinus albotruncatus: a. Basidiospores, bar = 5 µm; b. Pseudoparenchymatous cells of
the pseudostipe, bar = 20 µm; c. Hyphae of the volva, bar = 5 µm; d. Hyphae of the rhizomorphs, bar = 5 µm. Photos by: Bianca Silva.
A provisional key is provided for the Mutinus species, excluding M. coracoideus, M. granulatus, M. quadrigenus
and M. rugulosus on account of the lack of information in their protologues and because it was not possible to review
the types.
Provisional key to Mutinus species
1. -
2. -
3. -
4. -
5. Fertile portion of the pseudostipe smooth or rugulose (Section Glabrosi) or covered with irregular pseudoparenchymatous processes, appearing granular or pseudo-reticulate (Section Granulosi).................................................................................................2
Fertile portion of the pseudostipe covered with digitate processes (Section Tuberculosi)...............................................................16
Pseudostipe white or pale yellowish....................................................................................................................................................3
Pseudostipe yellow, pink, pale pinkish or reddish.............................................................................................................................10
Sterile portion of the pseudostipe smooth, adherent and integral throughout its length with two colors: green at the apical portion
and red at the base................................................................................................................................................................M. bicolor
Sterile portion of the pseudostipe smooth to rugulose or covered with irregular pseudoparenchymatous processes, appearing granular or pseudo-reticulate, a single color throughout its length..............................................................................................................4
Fertile portion of the pseudostipe orange, brownish to ochraceous....................................................................................................5
Fertile portion of the pseudostipe red to pink......................................................................................................................................7
Gleba restricted to the upper part of the pseudostipe; surface of the pseudostipe not rigid and not cartilaginous; lignicolous.........6
a new phalloid from Brazil
Phytotaxa 236 (3) © 2015 Magnolia Press • 245
-
6. -
7. -
8. -
9. -
10. -
11. -
12. -
13. -
14. -
15. -
16. -
Gleba carried over the greater part of the pseudostipe upon a firmly attached woven membrane; surface of the pseudostipe appearing rigid and cartilaginous; growing on humus-rich soil............................................................................................M. cartilagineus
Basidiome up to 70 mm length, straight, side walls complete; fertile surface with truncated apex, slightly wrinkled, brownish,
covering about 1/3 of the total length of basidiome................................................................................................. M. albotruncatus
Basidiome up to 30 mm length, slightly curved about halfway along the length, much of the side walls incomplete so as to form a
network on which the gleba is borne; fertile surface with not truncated apex, surface resembling annular ridges, orange or ochraceous, covering about 2/3 of the total length of basidiome................................................................................................. M. zenkeri
Fertile portion annulated......................................................................................................................................................................8
Fertile portion not annulated...............................................................................................................................................................9
Fertile portion with attenuate apex and annulated base, occupying about 1/2 of the total height of the pseudostipe... M. annulatus
Fertile portion with pointed apex and completely annulated, occupying about 1/3 of the total height of the pseudostipe..................
...................................................................................................................................................................................... M. boninensis
Fertile portion of the pseudostipe smooth to rugulose......................................................................................M. caninus var. albus
Fertile portion of the pseudostipe forming an irregular fragile network of variable meshes........................................ M. borneensis
Fertile portion occupying 1/6 a 1/8 of the total height of the pseudostipe, apically not perforated..................................................11
Fertile portion occupying more than 1/6 a 1/8 of the total height of the pseudostipe, apically perforated.......................................12
Fertile portion pink...........................................................................................................................................................M. fleischeri
Fertile portion red..............................................................................................................................................................M. minimus
Fertile portion smooth to rugulose....................................................................................................................................................13
Fertile portion granulose....................................................................................................................................................................14
Pseudostipe deep pink; fertile portion attenuated towards the apex....................................................................................M. elegans
Pseudostipe pale pink; fertile portion with apex conical.............................................................................. M. caninus var. caninus
Fertile portion of the basidiome not covered with gleba up to the apex, usually terminates in a sterile tip............... M. bambusinus
Fertile portion of the basidiome completely covered with gleba up to the apex...............................................................................15
Fertile portion red............................................................................................................................................................. M. ravenelii
Fertile portion pale pink................................................................................................................................................ M. argentinus
Pseudostipe pinkish ......................................................................................................................................................... M. penzigii
Pseudostipe white ........................................................................................................................................................... M. proximus
Acknowledgments
The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Brazil) by the
scholarship and to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq—Brazil, process
PVE/407474/2013-7 and PPBio/457476/2012-5) for the financial support.
References
Bailey, F.M. (1895) Contributions to the Queensland Flora. Botany Bulletin of the Department of Agriculture of Queensland 10: 1–43.
Baseia, I.G., Calonge, F.D. & Maia, L.C. (2006) Notes on the Phallales in Neotropics. Boletín de la Sociedad Micológica de Madrid 30:
87–93.
Berkeley, M.J. & Curtis, M.A. (1853) Centuries of North American fungi. The Annals and Magazine of Natural History II 11: 136.
http://dx.doi.org/10.1080/03745485709495068
Bottomley, A.M. (1948) Gasteromycetes of South Africa. Bothalia 4: 473–810.
http://dx.doi.org/10.4102/abc.v4i3.1859
Cabral, T.S., Silva, B.D.B., Ishikawa, N.K., Alfredo, D.S., Braga-Neto, R., Clement, C.R. & Baseia, I.G. (2014) A new species and new
records of gasteroid fungi (Basidiomycota) from Central Amazonia, Brazil. Phytotaxa 183 (4): 239–253.
http://dx.doi.org/10.11646/phytotaxa.183.4.3
Calonge, F.D. (1998) Gasteromycetes. I. Lycoperdales, Nidulariales, Phallales, Sclerodermatales, Tulostomatales. Flora Mycologica
Iberica 3: 1–271.
Cesati, V. (1879) Mycetum in itinere Borneensi lectorum. Atti dell´Accademia di Scienze Fisiche e Matematiche Napoli 8 (3): 1–28.
Corda, A.C.J. (1842) Icones fungorum hucusque cognitorum V. Prague, JG Calve, 92 pp.
Cortez, V.G., Baseia, I.G. & Silveira, R.M.B. (2008) Gasteromicetos (Basidiomycota) no Parque Estadual de Itapuã, Viamão, Rio Grande
do Sul, Brasil. Revista Brasileira de Biologia 6: 291–299.
Cunningham, G.H. (1944) The Gasteromycetes of Australia and New Zealand. Dunedin, J. McInhoe, Dunedin, 236 pp.
Degreef, J., Amalfi, M., Decock, C. & Demoulin, V. (2013) Two rare Phallales recorded from São Tomé. Cryptogamie, Mycologie, 34 (1):
3–13.
246 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.
http://dx.doi.org/10.7872/crym.v34.iss1.2013.3
Dring, D.M. (1964) Gasteromycetes of West Tropical Africa. Mycological Papers 98: 1–60.
Dring, D.M. & Rose, A.C. (1977) Additions to West African phalloid fungi. Kew Bulletin 31: 741–51.
http://dx.doi.org/10.2307/4119427
Felsenstein, J. (1985) Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791.
http://dx.doi.org/10.2307/2408678
Fischer, E. (1886) Zur Entwicklungsgeschichte der Fruchtkörper einiger Phalloideen. Annales du Jardin Botanique de Buitenzorg 6:
1–51.
Fischer, E. (1898) Phallineae. In: Engler, A. & Prantl, K. (Eds.) Die natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren
Arten insbesondere der Nutzpflanzen. Vol. 1. Wilhelm Engelmann, Leipzig, pp. 276–295.
Fischer, E. (1900) Untersuchungen zur vergleichenden Entwicklungsgeschichte und Systematik der Phalloideen. Neue Denkschr. Allg.
Schweiz. Ges. Gesammten Naturwiss 36 (2): 1–84.
Fischer, E. (1927) Phalloideen aus Surinam. Annales Mycologici 25: 470–473.
Fries, E.M. (1849) Summa Vegetabilium Scandinaviae. Sectio posterior 2: 259–572. Available from: http://www.biodiversitylibrary.org/
bibliography/47008
Gray, S.F. (1821) A natural arrangement of British plants, according to their relations to each other, as pointed out by Jussieu, De
Candolle, Brown, &c. including those cultivated for use; with an introduction to botany, in which the terms newly introduced are
explained; illustrated by figures. Vol. 1. Baldwin, Cradock & Joy, London, 824 pp.
Grgurinovic, A.C. (1997) Larger Fungi of South Australia. Botanic Gardens of Adelaide and State Herbarium and Flora and Fauna of
South Australia Handbooks Committee, Adelaide, 765 pp.
Hennings, P. (1895) Fungi camerunenses I. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie 22: 72–
111. [in German]
Hillis, D.M. & Bull, J.J. (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analyses.
Systematic Biology 42:182–192.
http://dx.doi.org/10.2307/2992540
Hosaka, K., Bates, S.T., Beever, R.E., Castellano, M.A., Colgan Iii, W., Dominguez, L.S., Nouhra, E.R., Geml, J., Giachini, A.J., Kenney,
S.R., Simpson, N.B., Spatafora, J.W. & Trappe, J.M. (2006) Molecular phylogenetics of the gomphoid-phalloid fungi with an
establishment of the new subclass Phallomycetidae and two new orders. Mycologia 98: 949–959.
http://dx.doi.org/10.3852/mycologia.98.6.949
Kawamura, S. (1929) On some new Japanese fungi. 1. A new fungus parasitic on Bamboo. Journal of Japanese Botany 4: 291–296.
Kirk, P.M., Cannon, P.F., David, J.C. & Stalpers, J.A. (2008) Ainsworth & Bisby’s Dictionary of the fungi. 10th ed. CAB International,
Wallinford, 771 pp.
Kobayasi, Y. (1937) Fungi Austro-Japoniae et Micronesiae. I. The Botanical Magazine 51: 749–758.
http://dx.doi.org/10.15281/jplantres1887.51.749
Kornerup, A. & Wanscher, J.H. (1978) Methuen Handbook of Colours. 3 Ed. Eyre Methuen, London, 252 pp.
Kretzer, A.M. & Bruns, T.D. (1999) Use of atp6 in fungal phylogenetics: An example from the Boletales. Molecular Phylogenetics and
Evolution 13 (3): 483–492.
http://dx.doi.org/10.1006/mpev.1999.0680
Léveillé, J.H. (1855) Iconographie des Champignons de Paulet. Paris, 135 pp.
Linnaeus, C. (1753) Species Plantarum. Laurentius Salvius, Stockholm, 1200 pp.
Liu, B. (1984) The Gasteromycetes of China. Beih. Nova Hedwigia 74: 1–235.
Lloyd, C.G. (1908) Mycological Notes nº 31. The Phalloids of Japan. Mycology Writings 2: 397–412.
Lloyd, C.G. (1909) Mycological Notes nº 4. Synopsis of the Know Phalloids. Mycology Writings 4: 1–96.
Magnago, A.C., Trierveiler-Pereira, L. & Neves, M.A. (2013) Phallales (Agaricomycetes, Fungi) from the tropical Atlantic Forest of
Brazil. The Journal of the Torrey Botanical Society 140 (2): 236–244.
http://dx.doi.org/10.3159/TORREY-D-12-00054.1
Massee, G. (1891) New or imperfectly known gasteromycetes. Grevillea 19: 94–98.
Meijer, A.A.R. (2006) Preliminary list of the macromycetes from the Brazilian State of Paraná. Bol. Mus. Bot. Munic. 68: 1–55.
MINISTÉRIO DO MEIO AMBIENTE (2004) Plano de Manejo da Floresta Nacional do Araripe. Brasília, Brasil. 314 pp.
Möller A. (1895) Brasilische Pilzblumen. Heft 7 der botanischen Mitteilungen aus den Tropen, herausgegeben von A. F. W. Schimper,
Jena (G. Fischer), 152 pp.
http://dx.doi.org/10.5962/bhl.title.2748
Montagne, J.F.C. (1856) Sylloge generum specierumque cryptogamarum quas in varii operibus descriptas iconibusque illustrates, nunc
ad diagnosum reductase, non nullasque novas interjectas ordine systematico disposuit. Sumptibus J.-B. Ballière, Paris, 498 pp.
a new phalloid from Brazil
Phytotaxa 236 (3) © 2015 Magnolia Press • 247
http://dx.doi.org/10.5962/bhl.title.5403
Nylander, J.A.A. (2004) MrModelTest v2. Program distributed by the editor.
Pegler, D.N, Læssøe, T. & Spooner, B.M. (1995) British puffballs, earthstars, and stinkhorns. London, Royal Botanic Gardens, Kew, 255
pp.
Penzig, O. (1899) Ueber Javanische phalloideen. Annales du Jardin Botanique de Buitenzorg 16: 133–173.
Rafinesque-Schmaltz, C.S. (1808) Essential generic and specific characters of some new genusses (sic) and species of plants observed in
the United States of America, in 1803 and 1804. Medical Repository 5: 356–363.
Rick, J. (1929) Phalloideas Riograndenses. Egatea 14: 299–305.
Rick, J. (1961) Basidiomycetes Eubasidii no Rio Grande do Sul, Brasilia. Iheringia 9: 451–480.
Ronquist, F., Teslenko, M., Van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P.
(2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology
61: 539–542.
http://dx.doi.org/10.1093/sysbio/sys029
Saccardo, P.A. (1888) Sylloge fungorum omnium hucusque cognitorum: Gasteromyceteae, Phycomyceteae, Myxomyceteae, Ustilagineae
et Uredineae. Vol 7. 882 pp.
Sawada, E. (1931) Materials of the Formosan fungi (29). Transactions of the Natural History Society of Formosa 21: 330–338.
Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W. & Fungal Barcoding Consortium (2012)
Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. PNAS 109 (16): 6241–
6246.
http://dx.doi.org/10.1073/pnas.1117018109
Silva, B.D.B., Cabral, T.S., Marinho, P., Ishikawa, N.K. & Baseia, I.G. (2013) Two new species of Geastrum (Geastraceae, Basidiomycota)
found in Brazil. Nova Hedwigia 96 (3–4): 445–456.
http://dx.doi.org/10.1127/0029-5035/2013/0089
Spegazzini, C. (1887) Las trufas argentinas (Tuberaceae argentinae). Anales de la Sociedad Científica Argentina 24: 120–127.
Swofford, D.L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10. Sunderland, Massachusetts:
Sinauer Associates.
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.
Molecular Biology and Evolution 24: 1596–1599.
http://dx.doi.org/10.1093/molbev/msm092
Thiers, B. (2015) Index Herbariorum: A global directory of public herbaria and associated Staff. New York Botanical Garden’s Virtual
Herbarium. Available from: http://sweetgum.nybg.org/ih/ (accessed 1 April 15)
Trierveiler-Pereira, L., Gomes-Silva, A.C. & Baseia, I.G. (2011) Observations on gasteroid Agaricomycetes. Mycotaxon 118 (5): 273–
282.
Trierveiler-Pereira, L., Silveira, R.M.B. & Hosaka, K. (2014) Multigene phylogeny of the Phallales (Phallomycetidae, Agaricomycetes)
focusing on some previously unrepresented genera. Mycologia 106 (5): 904–911.
http://dx.doi.org/10.3852/13-188
Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several
Cryptococcus species. The Journal of Bacteriology 172 (8): 4238–4246.
Zeller, S.M. (1944) A white variety of Mutinus caninus. Mycologia 36 (3): 263–265.
http://dx.doi.org/10.2307/3754822
248 • Phytotaxa 236 (3) © 2015 Magnolia Press
DA SILVA ET AL.