MYCOTAXON
Volume 94, pp. 265–292
October–December 2005
A phylogeny of Ramariopsis and allied taxa
Ricardo García–Sandoval
Joaquín Cifuentes
garcia_s@ciencias.unam.mx
Herbario FCME, UNAM, Apdo. Post. 70-181
México DF., 04510, México
Efraín De Luna
Instituto de Ecología A.C., Apdo. Post. 63
Xalapa Veracruz, 91000, México
Arturo Estrada–Torres
CICB, Universidad Autónoma de Tlaxcala, Apdo. Post. 183
Tlaxcala, 90000, México
Margarita Villegas
Herbario FCME, UNAM, Apdo. Post. 70-181
México DF., 04510, México
Abstract—he phylogenetic relationships of Ramariopsis and related taxa were studied
through a cladistic analysis of 36 morphological, cytological, and biochemical characters
among 23 species in six genera. Two of these genera were directly studied as groups
of interest, three as external taxonomic outgroups, and one as operative outgroup.
Representatives of Ramariopsis sensu Corner formed a monophyletic group, supported
by the cyanophilous nature of their basidiospores and derivation of their ornamentation
from the tunica. he new combination, Clavulinopsis antillarum, is proposed.
Key words—Clavariaceae, Homobasidiomycetes, spore ultrastructure, outgroup
sampling, taxonomy
Introduction
Ramariopsis was described as a subgenus of Clavaria by Donk (1933), who selected
Clavaria kunzei Fr. as the type species; the name refers to its macromorphological
similarity to the genus Ramaria (Donk 1954). he taxa originally included the type
species, Clavaria angulispora Pat. & Gaillard, Clavaria pulchella Boud., Clavaria pyxidata
Pers. and C. subtilis Pers.
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Corner (1950) elevated the taxon to genus level and included several fibulate species
with branched, whitish basidiomes, monomitic hyphal systems, and echinulate spores.
He retained Clavaria kunzei [= Ramariopsis kunzei (Fr.) Corner] as the type species,
removing three species—C. angulispora, C. pyxidata and C. subtilis—and adding eight
more for a total of ten species in the genus. Petersen (1964) added two more species ater
examining the type specimens of various species of the genus Clavulinopsis.
Petersen (1966) emended the original delimitation of the genus, to include taxa with
smooth spores and hysterochroic basidiomes. Petersen considered the size of the
basidia, the thickness of the spore wall, the composition of the ornamentation—when
present—and the pattern of coloration of the basidiomes as the relevant characters
for circumscribing the genus. He proposed dividing Ramariopsis into two subgenera:
Laevispora, typified by Ramariopsis minutula (Bourdot & Galzin) R.H. Petersen, for
species with smooth-spores, and Ramariopsis, consisting of species with echinulate
spores.
Corner (1970) maintained the original circumscription of the genus, recognizing that it
might be an artificial group, closely related to Scytinopogon and Clavulinopsis. Corner
argued that his circumscription conformed to a homogeneous group that was of more
utility for fieldwork.
Petersen (1978a) proposed a new delimitation for the genera Ramariopsis, Clavulinopsis,
and Clavaria based on the size of the hilar appendix, the type of pigments present in the
basidiome and the number of nuclei remaining in the basidium ater the formation of
spores. He transferred species with globose spores and a conspicuous hilar appendix
from Clavulinopsis to Ramariopsis, and species with elongate spores and a small hilar
appendix from Clavulinopsis to a new subgenus: Clavaria subg. Clavulinopsis. He also
proposed designating Clavaria corniculata Schaeff. [= Ramariopsis corniculata (Schaeff.)
R.H. Petersen] as the type species of Ramariopsis.
Based on Petersen’s arguments, Ramariopsis should include hysterochroic species
with branched or simples basidiomes, with whitish or bright coloration, globose or
subglobose and smooth or ornamented spores, and a conspicuous hilar appendix (see
Fig. 1). Petersen argued that this circumscription permits a continuum among related
species, from smooth-spored species with a large basidiome, to species with a small
basidiome and echinulate spores.
here are only a few additional contributions to this polemic. Jülich (1985) transferred
all species of Ramariopsis to Clavulinopsis based on nomenclatural arguments, but
this interpretation apparently has not been followed by the majority of taxonomists
(Hawksworth et al. 1995, Kirk et al. 2001). Pegler & Young (1985), in an electron
microscopy (EM) study of several species of Ramariopsis, Clavulinopsis, and
Scytinopogon, described three ultrastructural patterns of spore ornamentation that
corresponded with the three genera mentioned before. hey also observed that several
apparently smooth-spored species, such as Ramariopsis californica R.H. Petersen,
actually possessed ornamentation. he observed ornamentation was very small and
covered by a thin myxosporium, such that the spores appear smooth under a light
microscope even at magnifications above 1000x. Pegler & Young (1985) recognized
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Figure 1. Four species representative of the variation observed in Ramariopsis and Clavulinopsis.
a) Clavulinopsis corniculata, b) Ramariopsis pulchella, c) Ramariopsis kunzei and d) Clavulinopsis
fusiformis. Photos a: J. Cifuentes, b: A. Estrada-Torres, c: J. Cifuentes, d: J. Cifuentes.
the delimitation proposed by Corner (1950) for Ramariopsis, but not the relationship
between this genus and Scytinopogon.
he genus Ramariopsis has been included in the Clavariaceae in the majority of the
treatments of this family (Donk 1964, Corner 1970, Jülich 1981, Hawksworth et al.
1995), with the exception of Petersen (1978a, 1988a) and Kirk et al. (2001), who placed
Ramariopsis in Gomphaceae.
A phylogenetic study of Gomphaceae (Villegas et al. 1999), however, indicates that
Ramariopsis—at least sensu Corner—should not be considered part of that family.
Pine et al. (1999), on the other hand, studied the clavarioid and cantharelloid
Homobasidiomycetes, and found that Clavulinopsis fusiformis (Sowerby) Corner
[= Ramariopsis fusiformis (Sowerby) R.H. Petersen] nested within the euagaric
clade, forming a monophyletic group with Clavaria acuta Sowerby, indicating that
Ramariopsis subgenus Laevispora is related to Clavaria, or at least to representatives
of Clavaria subgenus Holocoryne. Additionally results of Larsson et al. (2004) indicate
close relationships among Clavulinopsis helvola (Pers.) Corner, Clavaria argillacea
Pers.–Clavaria subgenus Holocoryne–and Clavaria fumosa Pers.–subgenus Clavaria–
268
on a monophyletic group nested in the euagaric clade. his results points to a close
relationship between Clavulinopsis and at least some part of Clavaria.
here are currently only a few works, that have attempted to study the phylogeny of
clavarioid and gomphoid macromycetes in general (Pine et al. 1999, Villegas et al. 1999,
Humpert et al. 2001), and there is no consensus about the phylogenetic relationships of
these taxa.
Given that there is no consensus delimitation for Ramariopsis, the number of species in
this genus depends on the source consulted (i.e. Jülich 1981, 1985; Hawksworth et al.
1995; Kirk et al. 2001). his number varies from 24 to 45 species, with a distribution that
stretches from sub-Arctic regions to the forests of New Zealand (Corner 1950, 1967a,
1970; hin 1961; Petersen 1968, 1969, 1971a, 1978b, 1979, 1988a, 1989; Pilát 1971;
Gómez 1972; García-Sandoval et al. 2002).
he principal objective of the present work is to suggest a more robust delimitation
of Ramariopsis, based on a phylogenetic analysis of the available information and new
morphological characters derived from direct observation of herbarium specimens.
he use of morphological characters presents some advantages (see Jenner 2004, Wiens
2004, for an extensive up-to-date review) and for this particular case, these include the
possibility of a wide sampling of species because of the availability of herbarium material
and the opportunity to directly test the hypothesis of homology for diverse characters
considered taxonomically relevant.
Materials and Methods
Selection of outgroups and taxonomic sampling. he selection of outgroups was critical for
the present study since a reference phylogenetic framework is lacking and an inadequate
or insufficient selection of external groups could result in the artificial interpretation
of monophyly of the group of interest (Nixon & Carpenter 1993, Hopple & Vilgalys
1999). Selection was based on three criteria: a) a phylogenetic survey of the family
Clavariaceae sensu lato (results not shown), b) previous phylogenies of the clavarioid
Homobasidiomycetes, and c) previous classification proposals that include the genus
Ramariopsis in some specific family.
he phylogenetic survey was conducted based on diverse delimitations of the family
Clavariaceae (Donk 1964, Corner 1970, Jülich 1981, Hawksworth et al. 1995). All of
the genera included in these proposals were considered, and representatives of the
observed variation were selected for study. A matrix of 26 taxa and 30 morphological
characters was constructed, and an initial selection of taxonomic outgroups and an
operative outgroup was performed based on the strict consensus of the trees obtained
from the analysis. he selection of outgroups, especially the operative outgroup, was
based partially on the phylogenetic analyses by Hibbett et al. (1997), Pine et al. (1999),
Humpert et al. (2001) and Binder & Hibbett (2002). Based on Petersen’s (1978a, 1988a)
proposals of the phylogenetic affinities of Ramariopsis, one additional representative of
Gomphus was selected to complete the taxonomic outgroups. Sampling of the ingroup
was based on Petersen’s (1978a) proposed delimitation of Ramariopsis, which includes
the species considered by Corner (1950). Taxa representative of the observed variation,
and with available herbarium specimens, were chosen for analysis.
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For a few confusing species [Clavaria sulcata (Overeem) R.H. Petersen, Clavaria
vermicularis Sw., Clavaria amoena Zoll. & Moritzi and Clavaria aurantiocinnabarina
Schwein.], assignment of specific epithets and the concepts used to delimit species
followed Petersen (1967, 1976, 1979, 1980a, 1988a).
Analysis of characters and elaboration of the data matrix. Morphological observations
were analyzed and interpreted in the framework of cladistic ontology (Hennig 1966,
Farris 1983, de Pinna 1991, De Luna & Mishler 1996). he selection and analysis of
characters were based on the variation observed among sampled species, without
excluding a priori any sources of information (Poe & Wiens 2000). Hypotheses of
homology were elaborated based on the homology criteria proposed by de Pinna
(1991), employing similarity, conjunction, independence, variability, and heritability as
auxiliary criteria (Patterson 1988, Rieppel 1988, Brower & Schawaroch 1996, Hawkins
et al. 1997, Rieppel & Kearney 2002).
Codification of characters followed the criteria proposed by de Pinna (1991) and
later additions (Hawkins et al. 1997, Hawkins 2000, Kluge 2003, Grant & Kluge 2004).
Characters were not ordered nor polarized a priori to avoid bias in the exploration of tree
space (Hauser & Presch 1991). Similarly, no weighting scheme was applied a priori to
avoid ad hoc hypotheses that would constrain the results (Farris 1983). Character states
were analyzed by directly observing herbarium specimens from distinct collections (see
Table 1); these data were complemented by previous descriptions (Coker 1923; Singer
1945, 1986; Corner 1950, 1957, 1966, 1967a, b, 1970; hin 1961; Petersen 1964, 1965,
1966, 1967a, 1968, 1969, 1971a, b, 1978b, c, d, 1979, 1980b, 1984, 1985, 1988a, b, 1989;
Petersen & Olexia 1967, 1969; Bataile 1969; Fiasson et al. 1970; Schild 1971; Kühner
1977; Hubbard & Petersen 1979; Claus 1983; Pegler & Young 1985; Gill & Steglich 1987;
Hansen & Knudsen 1997; García-Sandoval et al. 2002; Gill 2003; Bertagnolli & Novello
2004). A matrix of 36 characters (see Appendices 1 and 2) was constructed, that included
observations of macro- and micro-morphology, macro– and micro–chemical reactions,
and biochemical, cytological, and ultrastructural characters. Information for the
homology hypothesis came primarily from direct observation of herbarium specimens
and only in few cases were based on previously reported data (see Appendices).
Tree searches, robustness, and topology test. A series of heuristic searches were performed
with 1,000 replicates in PAUP* 4.0b10 (Swofford 2002), using TBR, random addition,
and MAXTREE set to auto-increase. A branch and bound search was performed using
as an upper limit the observed tree length from the heuristic searches, and characters
were optimized with the ACCTRAN option.
Interpretation of the change of character states along phylogenies was made in
WinClada (Nixon 2002), using one of the most parsimonious trees encountered in the
branch and bound search.
Bremer’s support (Bremer 1994) was calculated to evaluate the robustness of the
observed clades. he analysis was conducted using AutoDecay 4.0 (Eriksson 1999) with
100 heuristic replicates per search, using random addition, MAXTREE set to autoincrease, the ACCTRAN option for optimization, and equally weighted characters.
Bootstrap values (Felsenstein 1985) were also calculated using 10,000 replicates
sampling all characters, with 10 heuristic searches for each bootstrap replicate, TBR
branch rearrangement, and MAXTREE set to 100 trees.
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Table 1. List of specimens examined.
Species
Specimens
Clavaria amoena
Clavaria aurantiocinnabarina
TO
TO
Corner CLAVARIA–4 (E); Donk 13690 (L)
Cifuentes 2004–94 (FCME); Corner RSNB–8376 (L); Corner
RSNB–8378A (L); Corner ICTA–1501 (E)
Clavaria gibbsiae Ramsb.
TO
Corner 442 (L); Corner 24165 (L); Corner–Singer 24165 (E)
Clavaria sulcata
TO
Hongo 705 (L); Corner s.n. (E); Corner 1676 (E)
Clavaria vermicularis
TO
Brit. Mycol. Soc. 12099 (L); Kotlaba s.n. (L); Corner NG 192 (E);
Corner RSS 1439 (E)
Clavaria zollingeri Lév.
TO
Corner s.n. (E); Corner s.n. (E)
Clavariadelphus pistillaris
TO
Meyer 3700 (TENN); Petersen 4920 (TENN)
Clavulinopsis corniculata
IG
Piepenbroek & Piepenbroek 876 (L); Mass Geesteranus 14580
(L); Villegas 1144 (FCME); López 782 (ENCB); Aranda-Breceda
4 (FCME); Corner & hind 206 (E)
Clavulinopsis fusiformis
IG
Clavulinopsis helvola
IG
Guzmán U-482 (XAL); Cooke & Cooke 45644 (XAL); Cooke
& Cooke 39815 (XAL); Hongo 764 (L); Villegas 1313 (FCME);
Villegas 1305 (FCME); Heredia 371 (XAL); Heredia 371 (XAL);
Santillán s.n (XAL); Guzmán & Ventura 5835 (ENCB); Ventura
13281 (ENCB); Villegas 1438 (FCME)
Bas 6730 (L); Maas Geesteranus 13887 (L)
Clavulinopsis laeticolor (Berk. &
IG
Gomphus clavatus (Pers.) Gray
OO
Gomphus floccosus
TO
Cifuentes 111 (FCME); Moreno-Fuentes 418 (FCME); Villegas
1109 (FCME); Fajardo s.n (FCME).
TO
Mendoza 9–09–1983 (FCME)
Ramariopsis californica
IG
Petersen 3006 (TENN); Petersen 280109 (TENN)
Ramariopsis crocea (Pers.) Corner
IG
Loerakker s.n. (L); Jalink & Nauta 6384 (L); de Vries s.n. (L)
Ramariopsis kunzei
IG
Bas 5105 (L); Corner RSNB-8291; Petersen 3909 (TENN);
Guzmán U-399 (ENCB); Petersen s.n. (TENN); Villegas 1804
(FCME); Pérez-Ramírez 280 (FCME); Rodríguez s.n. (ENCB);
Guzmán-Dávalos 2848 (IBUG); Guzmán 22666 (ENCB);
Guzmán 6969 (ENCB); Valenzuela 1197 (ENCB); Corner NG237 (E); Corner NG-229 (E); Ruíz & Herrera 3494 (MEXU)
Ramariopsis pulchella
IG
Corner NG-217 (E); Altamirano 148 (TLXM); Altamirano 157
(TLXM)
Ramariopsis tenuiramosa Corner
IG
Donk 11421 (L); Mass Geesteranus 9576 (L); Geesink 1504 (L);
Corner NG-124 (E)
Scytinopogon dealbatus
TO
Corner s.n. (E)
Scytinopogon echinosporus
TO
Corner 1517 (E)
Scytinopogon robustus
TO
Cifuentes 676 (FCME); Cifuentes 2004–26 (FCME)
Scytinopogon pallescens
TO
Martínez-C. s.n (ENCB)
(L.) Donk
(Schaeff.) Corner
M.A. Curtis) R.H. Petersen
(Schwein.) Singer
Lactarius indigo (Schwein.) Fr.
(Boud.) Corner
(Berk.) Corner
(Berk. & Broome) Corner
(Rick) Corner
(Bres.) Singer
Corner 452 (L); Donk 13896 (L); Villegas 1803 (FCME);
Hernández 188 (IBUG); Altamirano 628 (TLXM); Villegas 1450
(FCME).
Petersen 1797 (TENN); Arias-Montes s.n (FCME)
Herbaria: E = Royal Botanic Garden, Edinburgh, Scotland, United Kingdom; ENCB = Escuela Nacional de Ciencias Biológicas,
Instituto Politécnico Nacional, México; FCME = Facultad de Ciencias, UNAM, México; IBUG = Instituto de Botánica, Universidad
de Guadalajara, México; L = National Herbarium Nederland, Leiden University Branch, Nederlands; MEXU = Instituto de Biología,
UNAM, México; TENN = University of Tennessee, Knoxville, EUA; TLXM = Centro de Investigación en Ciencias Biológicas,
Universidad Autónoma de Tlaxcala, México; XAL = Instituto de Ecología, A.C., Xalapa, México; IG = Ingroup (= group of interest);
TO = Taxonomical outgroup; OO = Operative outroup.
271
hese parameters were selected to allow for a large number of bootstrap replicates
and a reasonably accurate search procedure for each replicate (as opposed to the “fast
bootstrap” option), thus avoiding the underestimation of clade support (DeBry &
Olmstead 2000; Mort et al. 2000).
Templeton’s topology test (Templeton 1983) was used to evaluate differences between
the observed phylogenetic hypothesis and that of Petersen (1978a), employing a twotailed Wilcoxon’s signed rank test following Templeton (1983). To conduct the test, a
branch and bound search was performed constraining monophyly of the representatives
of Ramariopsis sensu Petersen. To select a subgroup of equally parsimonious trees for
topology testing, a second branch and bound search was conducted using ACCTRAN
to optimize characters and successive weighting (Farris 1969) following Carpenter
(1988, 1994), using the RI to calculate reweighting. Each of the most parsimonious trees
thus encountered was compared with each of the most parsimonious trees from the
branch and bound search with successive weights (see above) using the Templeton test
implemented in PAUP*b10 (Swofford 2002), and the results were compared to tables of
critical values of T for the Wilcoxon test.
Diverse methods exist to evaluate the stability of a phylogeny with respect to the
inclusion/exclusion of taxa (see Grant & Kluge 2003 for an extensive review). he
present study assessed the impact of taxonomic outgroups sampling with a selective
inclusion/exclusion of those taxa, followed with branch and bound searches of all of the
combinations of taxonomic outgroups: Clavaria, Clavariadelphus, Gomphus, Lactarius,
and Scytinopogon.
Results
Twenty–three species were chosen for analysis based on the criteria employed for
outgroup selection, taxonomic sampling, and character analysis (Table 1). he branch
and bound search resulted in 12 trees of 80 steps in length (CI = 0.4875, RI = 0.7153,
RC = 0.3487). he strict consensus of these (see Fig. 2) shows Ramariopsis sensu Corner
(1950, 1970) as a monophyletic group.
his group forms a monophyletic clade with the representatives of Scytinopogon.
Bootstrap analysis indicated a generally low level of support across the observed
clades (see Fig. 2); only the clades containing representatives of Ramariopsis Corner,
and Scytinopogon showed bootstrap support above 50%. Interestingly, there was no
significant support for the clade that includes most of the representatives of Clavaria
sensu Petersen. Bremer support was also relatively low for most of the clades, and the
highest values corresponded to the clade of Scytinopogon.
During the constrained analysis conducted for topology tests, 1540 equally parsimonious
trees of length 85 (CI = 0.4535, RI = 0.6781, RC = 0.3075) were found, five steps longer
than those in the unconstrained search.
he application of successive weightings allowed selection of a subset of 8 most
parsimonious trees from those found in the original branch and bound search.
Application of the topology test, however, did not indicate significant differences
between the hypotheses. Comparison of all topologies resulted in no significant values
of N = 16-14, T = 53-39.5, P = 0.4545-0.4220.
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Figure 2. Strict consensus of the 12 trees of 80 steps (CI = 0.4875, RI = 0.7153, RC = 0.3487) found
during the branch and bound search. Numbers below branches indicate Bremer support indices,
and numbers above branches indicate bootstrap support values.
he combinations of selective inclusion/exclusion tested (not shown) did not modify the
monophyly of Ramariopsis sensu Corner, but decreased the resolution of the topology.
Discussion
he phylogenetic analyses performed support the monophyly of of Ramariopsis sensu
Corner (1950), though with moderate bootstrap support (56%). Based on these results,
Ramariopsis is limited to species with branched basidiomes, echinulate spores, and
cyanophilous spore ornamentation derived from the tunica (Pegler & Young 1985).
he ultrastructural composition of the ornamentation is a synapomorphy for the
group (see Fig. 3), but a large part of the cladogram was optimized as ambiguous for
this character because of the lack of information for several species –e.g. information
for any of the species of Scytinopogon included is not available. Although Corner did
not include Ramariopsis californica in his most recent treatment of the genus (Corner
1970), this species exhibits all of the distinctive characters of the genus and the present
results support its inclusion in this taxon. On the other hand, Petersen (1978a) included
Clavulinopsis helvola in Ramariopsis [= Ramariopsis helvola (Pers.) R.H. Petersen],
although this species has simple basidiomes and spores with thick tuberculous
ornamentation. Pegler & Young (1985) established that this ornamentation is formed
from growth of the corium, whereas ornamentation in Ramariopsis is formed via growth
of the tunica. he results of the present study support the segregation of C. helvola from
Ramariopsis.
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he representatives of Scytinopogon form a well-supported group (81% bootstrap
support), consistent with the original delimitation of Singer (1945) based on the presence
of branched, thelephoroid basidiomes and verrucose spore ornamentation. In our
results, Ramariopsis sensu Corner forms a monophyletic group with the representatives
of Scytinopogon. hese taxa all have cyanophilous spores with ornamentation partially
derived from the tunica, though in Scytinopogon the ornamentation also seems to be
composed of a thick core of corium (Pegler & Young 1985). It is worth mentioning
that most of the species of Scytinopogon included in the present analysis have not been
studied ultrastructurally—such data exist for only a single species of the genus, whose
taxonomic status is in doubt.
he observed relationship between Ramariopsis and Scytinopogon was first suggested by
Corner (1970), but this link should only be considered tentative as the taxonomic sampling
of this analysis was designed to resolve a robust delimitation of the genus Ramariopsis,
and not to identify its sister taxon. Furthermore, the clade Ramariopsis+Scytinopogon
does not show bootstrap support. hus, without a broader taxonomic sampling designed
to establish the affinities of Ramariopsis with other taxa, it is preferable to consider these
results as preliminary.
One of the principal consequences of this study is that Ramariopsis sensu Petersen is a
paraphyletic group –i.e. a grade– because it was defined by simplesiomorphic characters.
Petersen (1978a) used diverse sources of information for his delimitation, including
the absence of carotenoid pigments. Pigment composition has been a frequently-used
auxiliary character in fungal systematics (Arpin & Fiasson 1971, Tyler 1971, Gill &
Steglich 1987, Frisvad et al. 1998, Gill 2003), but recent studies indicate that phylogenetic
patterns inferred in the Homobasidiomycetes based on this type of character are oten
incongruent with the results obtained using other sources of information (Hibbett &
horn 2001, Pine et al. 1999).
Nonetheless, the presence of certain types of pigments can be a very useful auxiliary
character in studies aimed at generic delimitation (e.g. Feibelman et al. 1997, Weinstein
et al. 2002), and the taxonomic relevance of this type of characters should not be
completely discarded, but perhaps restricted to use at lower taxonomic levels. In the
case of Ramariopsis, the delimitation proposed by Petersen (1978a) was based on the
absence of carotenoid compounds, without specify the nature of the pigments present
and without an explicit reference to a concrete character; the inferred pattern thus
cannot be directly confirmed or refuted. In the present study this character was coded
as the presence or absence of carotenoid pigments–character 11. (See Appendices for
character argumentation.)
his character does not show evidence of homoplasy in the present study based on
its observed distribution (CI = 1.0), although optimization of the character is not
definitive due to the absence of information in several of the considered species (see
Fig. 4). Additionally, the distribution of carotenoids in the present study supports the
relationship among Clavaria aurantiocinnabarina, C. amoena and C. sulcata, and is
congruent with a monophyletic group that includes representatives of Clavaria (see Fig.
2). his latter group is consistent with Petersen’s (1978a, 1988a) delimitation of Clavaria.
It is worth mentioning that the aforementioned results regarding Clavaria should be
274
Figure 3. One of the most parsimonious trees encountered during the branch and bound search,
showing the character states that can be unambiguously optimized. Numbers above dots indicate
the character and numbers below dots the character state. Apomorphic states are shown in black
dots and homoplastic states in white dots. Selected character transformations are illustrated close
to the branch were change occur (see appendix 1 for character argumentation).
considered as preliminary due to the lack of bootstrap support and the taxonomic
sampling of the present study.
Another relevant character used by Petersen (1978a) was the presence of spores with
a conspicuous hilar appendix. Several species of Clavulinopsis subgenus Cornicularia
275
was transferred by Petersen to Ramariopsis based—in addition to the other mentioned
character—on the presence of a conspicuous hilar appendix. In this study, this
character was included (character 31) and their optimization is depicted in figure 4
(see also Appendices for character argumentation). he present results show it as a
simplesiomorphy.
Farris (1991) provided an explicit criterion to recognize paraphyletic groups by tracing
the status of the character used to define it; in the case of Ramariopsis prominent hilar
appendix and absence of carotenoid pigments were used by Petersen in order to define
the genus, both characters are plesiomorphic and shared –simplesiomorphic– (see
Fig. 4). In the strict sense, the present results show Ramariopsis sensu Petersen as a
paraphyletic group.
Petersen (1978a) also employed the presence of chiastic basidia with a post-meiotic
mitotic division and four nuclei remaining in the basidia ater spore formation as a
cytological pattern that supported the delimitation of Ramariopsis. Recent phylogenetic
studies (Hibbett et al. 1997, Pine et al. 1999) confirm the utility of cytological characters
in the delimitation of taxonomic groups among the clavarioid and cantharelloid
Homobasidiomycetes, but while the stictic pattern appears phylogenetically informative,
the chiastic condition, which is widely distributed among the Homobasidiomycetes,
does not seem to follow a clear phylogenetic pattern (Hibbett & horn 2001). As with
the presence of carotenoid pigments, the utility of the chiastic condition in our analyses
is noted, though more studies are necessary.
he pattern of four remaining nuclei reported for Ramariopsis crocea (Penancier 1961)
results from a post-meiotic mitotic division. Post-meiotic mitotic divisions resulting in
four nuclei remaining in basidia following spore formation are reported for a diversity
of other taxa (Penancier 1961, Duncan & Galbraith 1972, Restivo & Petersen 1976,
Kühner 1977, Mueller & Ammirati 1993). Both the meiotic pattern (chiastic/stictic) and
the number of remaining nuclei (see Appendices for discussion and codification) were
included as characters in the present study.
All of the species in our study for which data were available present a chiastic pattern, so
it was not informative for addressing our questions. Very possibly this character could
have relevance at other hierarchical levels when studying the taxonomic affinities of the
genus Ramariopsis.
he number of remaining nuclei (character 29 CI = 1.0) did not present a homoplasious
distribution, though, similar to the situation for carotenoid pigments, optimization
of this character should be considered preliminary since data were not available for
all species considered, and this lack of information results in a severely ambiguous
optimization (results no shown).
Our finding of a monophyletic group that includes representatives of Clavulinopsis and
representatives of Clavaria is congruent with the results of Pine et al. (1999). However,
relationships among Clavariadelphus pistillaris, Clavaria zollingeri and C. gibbsiae are
not consistent with previous classifications (see Fig. 2), and Clavariadelphus is found in
a position incongruent with previous studies (Hibbett et al. 1997, Pine et al. 1999).
276
Figure 4. Optimization of two characters used by Petersen (1978a) to define Ramariopsis, onto one
of the most parsimonious trees. a) Optimization of character 31 showing prominent hilar appendix
as a simplesiomorphy; b) optimization of character 11 showing the absence of carotenoid pigments
as a symplesiomorphy.
he position of Clavariadelphus pistillaris could be an artifact, due to the fact that
the present sampling of taxonomic outgroups included distantly related groups –e.g.
Gomphus in the clade Gomphoide-Phalloide sensu Hibbett & horn (2001).
To explore this possibility, a branch and bound search was performed excluding
Clavariadelphus, and the monophyletic group of Ramariopsis sensu Corner+Scytinopogon
obtained in the main analysis was recovered (results not shown).
It has not been possible to clearly elucidate the phylogenetic affinity of Clavaria
zollingeri. his taxon was included in the analysis of clavarioid and cantharelloid
Homobasidiomycetes by Pine et al. (1999), but their results were inconclusive and this
species was located outside of any recognized clade in the strict consensus analysis of
combined genes. In spite of this, indicated that the current delimitation of Clavaria
(Corner 1970) –simple or branched basidiomes, monomitic hyphae in the context,
clamp connections absent in the context, and present or absent of clamp connections
at the base of the basidia– was not a monophyletic group. he results of our study are
congruent with those of Pine et al. (1999).
Clavaria gibbsiae in the present results is located next to C. zollingeri, out of any large
clade –e.g. Clavaria sensu Petersen or Ramariopsis sensu Corner. his species is
traditionally included in Clavaria subgenus Holocoryne (Corner 1970, Petersen 1988a).
We could expect a relationship between Clavulinopsis and representatives of Clavaria
based on previous results (Pine et al. 1999, Larsson et al. 2004), but these studies also
indicate that Clavaria is not a monophyletic group (Pine et al. 1999). Our results are
congruent with these previous studies and show a core group that includes part of
Clavaria and all the included representatives of Clavulinopsis. hese results should be
considered as preliminary due to the lack of bootstrap support for this group and the
taxonomic sampling of the present study.
277
One important result from the present study is the proposal of nomenclatural changes in
Ramariopsis. At the present time, phylogenies seem to be divorced from classifications
since few phylogenetic hypotheses are used as the foundation for newer classifications.
his may result in the undesirable situation in which robust phylogenetic papers have
little impact on the daily practice of taxonomists (for a broader discussion on this issue
see Wheeler 2004, Franz 2005). Phylogeneticists are frequently reluctant to introduce
changes in the classification due to the nature of the phylogenetic research—e.g.
occasionally the relative position of a clade undergoes modifications with the addition
of new data. In the present case, we decided to make taxonomical decisions based on our
phylogenetic results by introducing changes only when we felt confident to do it.
Our results are robust enough to restrict Ramariopsis to species with ornamented
spores—which show the characteristic ultrastructural pattern. he only problem arises
when we try to identify the species that meet those requirements since in some species
spore ornamentation is difficult to see. here are cases in which some taxa originally
described with smooth spores are demonstrated to have ornamented spores—one
example of this is Ramariopsis californica R.H. Petersen (Pegler & Joung 1985). For
this reason, and until we have more information—e.g. SEM and TEM studies of
the spores—we avoid proposing new combinations for species with smooth spores
originally described in Ramariopsis (see Appendix 3). We only recommend the use of
combinations previously proposed, that are congruent with our results (see Appendix
3). he only exception is Ramariopsis antillarum (Pat.) R.H. Petersen. his taxon was
originally described as Clavaria fusiformis var. antillarum Pat.; subsequently, Petersen
(1988a) proposed to raise it to species rank based on the differences in the ontogenetic
patterns of the basidiomes between yet the species and the variety. We concur with
Petersen’s proposal, yet we consider that the correct placement for this species is in
Clavulinopsis based on the presence of simple club basidiomes and globose, smooth
spores. Our current knowledge of this species leads us to propose the combination
Clavulinopsis antillarum (Pat.) García-Sandoval & Cifuentes, comb. nov.
Basionym: Clavulinopsis fusiformis var. antillarum Pat., in Duss, Enum. Methodique
des champignons recueilles a la Guadeloupe a la Martinique (Lons-le-Saunier): 14
(1903).
We have included a checklist of available species names for Ramariopsis and their
correct combinations according to the present results (see appendix 3). he list is
divided in three parts: a) species confidently placed in Ramariopsis sensu stricto; b) taxa
once included in Ramariopsis that do not belong to Ramariopsis according to our results
and available information; and c) species originally described in Ramariopsis that need
further examination before a new combination be proposed. We think that this checklist
provides practical applications, avoiding the proposal of unjustifiable new combinations
that may result in unstable nomenclatural changes.
Two combinations are excluded from the list:
a) Ramariopsis bizzozeriana (Sacc.) Schild. (= Clavaria bizzozeriana Sacc.). C.
bizzozeriana was recognized as a taxonomic synonym of Ramariopsis pulchella by
Corner (1950); later the combination Ramariopsis bizzozeriana was incorrectly preferred
over Ramariopsis pulchella by Schild (1972). his last combination should not be used
278
because C. bizzozeriana is currently considered a taxonomic synonym of R. pulchella
(for details see Corner 1950, Petersen 1978b).
b) Ramariopsis lentofragilis (= Clavaria lentofragilis Atk.). Corner (1950 p. 640)
considered Clavaria lentofragilis Atk. a taxonomic synonym of Ramariopsis kunzei,
although he kept doubts. In his description of Ramariopsis lentofragilis f. propera
(Bourdot) R.H. Petersen, Petersen (1969 p. 550) used the combination Ramariopsis
lentofragilis without making any reference to the authority of the combination. In a
subsequent article Petersen (1978a p.669) acknowledged Corner as the author of the
combination. However, Ramariopsis lentofragilis was not considered by Corner (1950,
1970), who only referred to the species as a taxonomic synonym of R. kunzei. Whether C.
lentofragilis is a synonym of R. kunzei or not is a matter that needs further investigation.
For that reason we prefer to exclude that possible combination from the checklist.
In conclusion, the present study indicates that the delimitation of Ramariopsis proposed
by Corner (1950, 1970) is robust, given currently available data. Although the topological
comparisons did not find significant differences between this hypothesis and that
proposed by Petersen (1978a), our analysis indicates that Ramariopsis sensu Corner
represents a more parsimonious hypothesis (five steps shorter), in accordance with
ultrastructural data on spore ornamentation and patterns of cyanophilous reaction in
the spores. Additionally, the test of sensitivity of the taxonomic sampling indicated that
the results obtained were not an artifact of taxon selection and are stable across various
resamplings of the data. Relationships among taxa outside of the clade Ramariopsis
sensu Corner should be taken as tentative, given that the sampling of the present study
was designed for other objectives. Recently Dentinger & McLaughlin (2005) addressed
the relationships of Clavariaceae and Pterulaceae; in their sampling they included
representatives of Ramariopsis sensu Petersen and Clavaria sensu Petersen. heir results
agree with our study and show Ramariopsis sensu Petersen as a paraphyletic group while
also showing support for a clade congruent with Clavaria subgenus Clavulinopsis. In
our results, we also find a clade congruent with the mentioned subgenus of Clavaria,
but with non-bootstrap support. Future studies addressing Clavariaceae question are
needed, but current findings (e.g. Dentinger & McLaughlin 2005) provide important
insights about this questions.
Acknowledgments
he authors wish to thank Dr. Gregory Mueller of the Field Museum of Chicago and Dra. Laura
Guzmán-Dávalos, from Universidad de Guadalajara for peer-review of this manuscript. Also we
thank Dr. David S. Hibbett of Clark University in Massachusetts for revision and commentary on
a preliminary version of this manuscript; Dr. Ronald H. Petersen of the University of Tennessee
for comments and suggestions on a previous version of this work presented at the 2004 Annual
Meeting of the Mycological Society of America; Bryn C. Dentinger, of the University of Minnesota,
for sharing a copy of their poster presented at the 2005 Annual MSA Meeting; the curators of the
herbaria E, ENCB, IBUG, L, MEXU, TENN, TLXM, XAL, especially Dr. Ronald H. Petersen for the
facilities and specimens offered, Dr. Roy Watling (E) for the facilities offered for the revision of the
collection of Dr. E.J.H. Corner, Dr. Machiel Noordeloos (L) and Evelyn Turnbull (E) for their help
during visits to their herbaria. Funds for the present work were provided by CONACYT 34313-V,
and DGAPA IN 209605–3. R. G.-S. would also like to thank support from the Programa de Becas
Nacionales de Posgrado UNAM. he authors would like to note that conclusions presented in this
work are not necessarily those of colleagues that commented earlier versions of this work.
279
Appendix 1. Characters and character states.
Morphological characters of the basidiome
1.- Simple clavate basidiome. his type of basidiome corresponds to what Petersen (1988a) defined
as clavarioid –holobasidiomycetes, in simple erect columns– excluding the branched forms which
show a distinct ontogenetic pattern as described by Corner (1950). his includes intergradations
from simple clavate forms to those with some amount of apical branching (bifurcated towards the
apex). Within this general pattern are several ontogenetic variants (Corner 1950, Clémençon et al.
2004) that could be phylogenetically informative, but to date there are too few data to recognize
discrete patterns; in the present study only the general pattern was considered. States: 0: present,
1: absent.
2.- Profusely branched basidiomes. his character corresponds to what Petersen (1988a) described
as clavarioid (see character 1), but is confined to the branched forms, since this corresponds to an
ontogenetic pattern distinct from the simple forms (Corner 1950). A basidiome was considered
profusely branched when it exhibited three or more levels of branching coming from the middle or
below the middle of the basidiome. States: 0: present, 1: absent.
3.- Basidiome pileate-stipitate. Corner (1966) defines the pileus as an apical expansion developed
from a diageotropic growth that generates fan or umbrella shaped forms. his differs from the
cantharelloids in the configuration of the hymenophore and the absence of a thickened hymenium.
In the present study any basidiome exhibiting a pileus sensu Corner (1966) and a stipe sensu
Kirk et al. (2001) was considered as pileate-stipitate, independent of the conformation of the
hymenophore. States: 0: present, 1: absent.
4.- Form of the hymenophore. For the present study the hymenophore was defined following
Clémençon et al. (2004) as the portion of the context that supports the hymenium –the layer of
basidia, basidiospores, and sterile elements– in contrast to the proposal of Kirk et al. (2001), who
considered the hymenophore the structure which supports spores –e.g. a basidiome. In the present
study the hymenophore was considered to exhibit variation in form independent of that of the
basidiome, and as such is an independent character (Mickevich 1982, Mickevich and Limpscomb
1991, Limpscomb 1992, Mabee 1993, O’Keefe & Wagner 2001) –against Clémençon et al. (2004)
see character three– for example a smooth hymenophore can be present in a simple, clavate, or
corticioid basidiome. he recognized states correspond in the case of gills to the description of
Singer (1986), for a hymenophore in folds to Corner (1966) in cantharelloid fungi, for a smooth
hymenophore to Clémençon et al. (2004), and for a wrinkled hymenophore to the description
of some species of Clavariadelphus by Corner (1950) though with a lesser grade of organization.
States 0: gills, 1: folds, 2: wrinkles, 3: smooth.
5.- Longitudinally sulcate in simple clavate basidiomes. his character corresponds to the description
by Petersen (1988a) and represents those basidiomes that exhibit a furrow or longitudinal fold
along the fertile part of the basidiome; it differs from a wrinkled hymenophore in that the furrow
or fold is singular. States: 0: present, 1: absent.
6.- Development of the context at the level of the hymenium. his character corresponds to the
presence or absence of the condition described as fistular or hollow by Kirk et al. (2001), but confined
to the context at the level of the hymenium. he portion of the context below the hymenophore
and subhymenium can exhibit distinct grades of development with two clearly recognizable states:
when it is well developed, the basidiome exhibits a solid aspect in transverse section, but when
poorly developed the basidiome appears hollow or fistulate in transverse section. States 0: fistulate,
1: solid.
7.- Pattern of branching. Profusely branched basidiomes exhibit different patterns of branching
derived from differences in ontogenetic development (Corner 1950). he nomenclature and
patterns described by Corner (1950) were followed for the present study. Only two states were
observed among the included species in the present analysis. States 0: radial, 1: flattened.
280
8.- Mycelial cords. Aggregates of linear hyphae growing away from the basidiome and visible to the
naked eye were considered mycelial cords. Clémençon et al. (2004) and Boddy (1999) distinguished
between mycelial cords and rhizomorphs based on the level of organization and the type of growth
of the structure. In the present study no distinctive apical growth was identified, and the observed
structures were thus only characterized as mycelial cords in the general sense of Cairney et al.
(1991). States: 0: present, 1: absent.
9.- Mycelium at the base of the stipe. Basidiomes growing from a patch or pillow of mycelium
were considered as exhibiting mycelia at the base of the stipe. he mycelial growth was always
conspicuous and found above the substrate; this mycelium covers the base of the stipe and exhibits
different types of generative hyphae. Petersen (1988a) described subiculate as a patch of mycelia
in the substrate from where the basidiome grows, but Clémençon et al. (2004) restricted the term
subiculate to the thick layer of mycelia from which the corticioid basidiomes develop. We treat the
character as equivalent to what Petersen (1988a) denominates subiculate, but since Clémençon
et al. (2004) employed the term in a different manner, the descriptor subiculate is not used in the
present study. States: 0: present, 1: absent.
10.- Reaction of hymenium to iron salts. he reaction to iron salts is a widely used character in
the systematics of clavarioid fungi (Corner 1950; Donk 1964; Petersen 1978a, 1988a). he reagent
contains ferric chloride in a 10% aqueous solution (Petersen 1988a), and is applied directly to the
hymenium. A positive reaction is recognized by a color change to olive-green or gray-green. his
reaction is considered indicative of the presence of the compound pistillarine (Steglich et al. 1984).
A positive reaction to this reagent can exhibit other color changes due to the presence of distinct
compounds (Gill & Steglich 1987, Singer 1986). In the present study only positive reactions that
engendered olive-green or gray-green color changes were considered. Observations were made in
dryed exemplars. In our experience species with positive reaction in fresh material also react when
dry. States 0: positive, 1: negative.
11.- Carotenoid pigments in the basidiome. Along with sesquiterpinoids, carotenoids are the only
pigments present in the macromycetes derived from the mevalonate pathway (Gill & Steglich 1987,
Gill 2003). his character was coded as a nominal variable –sensu Hawkins (2000)– based on the
aviable information for the species considered since other types of coding would require additional
data about the specific metabolic pathways generating the compound (e.g. Barkman 2001). States
0: present, 1: absent.
Micromorphological characters distinct from the hymenium and the spores
12.- Lacticiferous hyphae. his structure corresponds to what Singer (1986) described as lacticiferous
in the strict sense –hyphae that produce latex. hese hyphae can exhibit nuclei and septa and thus
correspond to a specialized type of heteroplera sensu Clémençon et al. (2004). States 0: present, 1:
absent.
13.- Inflated hyphae. Inflated hyphae are those generative hyphae that exhibit increased growth
behind the point of lateral growth, widening and elongating significantly (Corner 1950, Kirk et al.
2001). hey are recognizable by having a considerably greater diameter than the rest of the hyphae,
and by having constrictions in the zone of the septa; they may or may not have clamp connections.
Corner (1950) distinguished two types of monomitic contexts that present inflated hyphae based
on the presence of secondary septa and clamps. In the present study this classification was not used,
since it mixes two independently varying characters. States: 0: present, 1: absent.
14.- Crystals in the hyphae of the basal mycelia. he hyphae of the mycelia at the base of the stipe
sometimes present amorphous crystals, similar to those reported in the context of the base of the
stipe for Ramariopsis pulchella (Petersen 1988a) –5-20µm, hyaline or yellowish, and do not dissolve
281
in 5% KOH. he crystals are found covering the exterior surface of the hyphae and are not easily
removed. States: 0: present, 1: absent.
15.- Degree of thickening in the hyphal wall. hickening of the hyphal wall was considered only
in the generative hyphae. he presence of generative hyphae with thickened walls has been a
relevant systematic character in several genera (Corner 1966, Pegler 1996). In the present study
three qualitative degrees of thickening were recognized due to the difficulty in making precise
quantitative measurements. States: 0: none, 1: scarce, 2: conspicuous.
16.- Simple fibulae. Simple fibulae –clamp connections, clamp cells– are frequently observed in
Basidiomycetes. Clémençon et al. (2004) recognized three types of simple fibulae, of which two were
observed in the present study: closed and ring or medallion fibulae. Both types were considered
equivalent since there were insufficient elements to determine discrete states, due the continuous
variation observed. States: 0: present, 1: absent.
17.- Geniculate fibulae. Geniculate fibulae are those that exhibit a marked bend at the point of
inflection, giving the appearance of a bent knee. he bend partially deforms the profile of the
fibulae, allowing them to be easily differentiated from simple fibulae. hese structures correspond
to those described in various species of Clavulinopsis by Petersen (1968). Geniculate fibulae are
not homologous to simple fibulae since both structures are found simultaneously in the same
basidiome and are thus independent characters according to the conjunction test (Patterson 1988,
Rieppel 1988, De Luna & Mishler 1996, Rieppel & Kearney 2002, Grant & Kluge 2004). States: 0:
present, 1: absent.
18.- H connections. hese connections are structures formed by the union of two parallel hyphae
through a third, transverse, hypha. hey can be considered functional homologous –biologically
homologous following Roth (1988)– to fibulae, but are not phylogenetically homologous sensu de
Pinna (1991), since they are both present simultaneously with distinct types of fibulae. hey should
thus be considered independent characters following the conjunction test (Patterson 1988, Rieppel
1988, De Luna & Mishler 1996, Rieppel & Kearney 2002, Grant & Kluge 2004). States: 0: present,
1: absent.
19.- Ampulliform fibulae. his type of fibula is characterized by the presence of a marked widening,
giving the appearance of an inflated fibula similar to the inflated hyphae. his corresponds to the
description by Petersen (1988a) as a characteristic of Ramaria subg. Lentoramaria Corner. his
type of fibula is not phylogenetically homologous to the other types of fibulae described since it can
be found present simultaneously with those other structures and should therefore be considered
as an independent character by the conjunction test (Patterson 1988, Rieppel 1988, De Luna &
Mishler 1996, Rieppel & Kearney 2002, Grant & Kluge 2004). States: 0: present, 1: absent.
Hymenial characters
20.- Subhymenium clearly differentiated. he subhymenium was considered to be the layer of
generative hyphae growing below the hymenium (Kirk et al. 2001) and from which the hymenium
forms (Petersen 1988a). Several distinct anatomical patterns of the subhymenium have been
described (Clémençon et al. 2004), and in the case of the clavarioid fungi, Petersen (1988a)
considered three types. he variation observed in the present study; did not permit differentiation
of distinct types of subhymenium; only the conspicuous presence or absence of a subhymenium
was considered. States: 0: present, 1: absent.
21.- hickening of the hymenium. Corner (1950) described the thickening of the hymenium as
a pattern resulting from the sympodial growth of the hyphae of the subhymenium, generating
successive superimposed layers of hymenium, collapsing the preceding basidia. No additional
patterns of variation of this type have been described to date, and in the present study no further
variation was observed. States: 0: present, 1: absent.
282
22.- Cystidia of the hymenium. Cystidia are sterile hyphal apices, generally with a distinctive form
and found in variable locations in the basidiome (Kirk et al. 2001, Clémençon et al. 2004). he
form and anatomic disposition of the cystidia have been used as taxonomic characters, but only the
cystidia in the hymenium were considered for the present study, as no other cystidia were observed
in the species studied. States: 0: present, 1: absent.
23.- Fibulate basidia. Clamp connections on basidia are restricted to the base of the basidia. he
presence on the basidia is independent of the presence of fibulae in the rest of the hyphae of the
basidiome. As such, it was considered as an independent character. In the case of Clavaria subgenus
Holocoryne the basidia exhibit a fibula described as broadly free (Corner 1950) or bifurcated
(Petersen 1988a). States: 0: present, 1: absent.
24.- Basidia with refringent contents. his character refers to basidia with an oily, yellowish,
appearance of its content, which is homogeneous and refringent in 10% KOH. It corresponds
partially to what Petersen (1988a) described as gloeoplerotic, excluding the foamy appearance.
Similarly, it corresponds partially to what Clémençon et al. (2004) described as oil-producing –
resinous content– and to what Singer (1986) describes as oil-producing sensu Fayoid, but without
the positive sulfovainillin reaction. States: 0: present, 1: absent.
25.- Shape of the basidia. he variation observed during the present study permitted recognition
of two forms or general profiles of basidia: cylindrical and clavate. hese terms correspond to the
definitions of Kirk et al. (2001). States 0: clavate, 1: cylindrical.
26.- Base of clavate basidia. Clavate basidia exhibit variation in the size of the base. Variation of
the size was coded as an independent character because it refers to a property or feature of an
anatomical region particular to clavate basidia and is not homologous with terete basidia (de Pinna
1991, De Luna & Mishler 1996, Rieppel & Kearney 2002, Grant & Kluge 2004). Additionally, this
coding reflects the variation observed as it describes properties with independent variation. he
size of the basidia exhibits variation logically independent of the form and thus can be coded as
an independent character (Hawkins et al. 1997, Hawkins 2000, O’Keefe & Wagner 2001, Rieppel &
Kearney 2002). States 0: short, 1: long.
27.- Geniculate basidia. hese basidia exhibit a point of inflection in the middle part, and thus a
marked bend giving the appearance of a flexed knee. his bend conspicuously deforms the profile
of the basidia allowing them to be clearly differentiated. his pattern corresponds to that described
in various species of Clavulinopsis by Petersen (1968). Geniculate basidia do not constitute a
pattern or form homologous in the phylogenetic sense (de Pinna, 1991), since both structures are
simultaneously present in the same basidiome and thus constitute independent characters by the
conjunction test (Patterson 1988, Rieppel 1988, De Luna & Mishler 1996, Rieppel & Kearney 2002,
Grant & Kluge 2004). States: 0: present 1: absent.
28.- Orientation of the achromatic spindle. Juel (1898) described two basic patterns of orientation
of the meiotic spindle of basidia during meiosis: chiastic –transversal to the principal axis and
situated in the apex– and stictic –parallel to the principal axis and situated in the middle. Boidin
(1958) recognized an intermediate pattern that he called hemichiastic; Donk (1964) later qualified
this as a homologous variant of the chiastic form. In the present study only the chiastic and stictic
patterns were considered, given that those are the only patterns reported for the species studied.
States: 0: chiastic, 1: stictic.
29.- Four remaining nuclei. Ater meiosis a third nuclear division sometimes occurs, producing a
total of eight nuclei. In some species four of these nuclei disintegrate and are termed remaining
nuclei (Penancier 1961). his pattern has been reported for several of the species considered in the
present study and corresponds to that described as post-meiotic pattern “A” by Duncan & Galbraith
(1972) and to that described by Kühner (1977). he data available for the species considered in
283
the present study only allowed recognition of the presence of a third division –exhibiting pattern
“A”– and the absence of this division (only four nuclei form); this character was thus coded as a
nominal variably (Hawkins 2000). States: 0: present, 1: absent.
Characters of the basidiospores
30.- Spore form. he variation observed during the present study allowed the recognition of three
spore forms: globose, subglobose, and elongate. States were assigned qualitatively, excluding the
deformations produced by ornamentation when present, and correspond to the forms described
by Kirk et al. (2001), except for the fusiform and ellipsoid forms, which are considered as elongated
spores. States: 0: subglobose, 1: globose, 2: elongate.
31.- Size of the hilar appendix. he hilar appendix –also called the apicule, sterigmal appendix
or apophysis (Kirk et al. 2001, Clémençon et al. 2004)– is the small conical or papilla-shaped
projection, which is the point of connection between the spore and the sterigma. his structure
is involved in the active liberation of the spores (Clémençon et al. 2004). Based on the observed
variation in the species studied, two qualitative states were recognized to describe the size of the
appendix. States: 0: prominent, 1: inconspicuous.
32.- hickness of the spore wall. he species considered in the present study do not exhibit significantly
thickened spore walls, but some species show a slight thickening. Based on the observed variation
two qualitative states were recognized. States: 0: slightly thickened, 1: thin.
33.- Smooth spores. Spore ornamentation has been a relevant taxonomic character for Ramariopsis
(Corner 1950), but several studies have shown that ornamentation can be derived from different
layers of the spore wall. Treating the presence of ornamentation as homologous in different taxa
could thus fail the test of similarity (Rieppel 1988, Nelson 1994, Rieppel & Kearny 2002). he
presence of smooth spores –spores without modifications or deformations in the wall– was
observed in preparations mounted in 5% KOH using a bright field light microscope at 1000x
magnification. States: 0: present, 1: absent.
34.- Ultrastructure of spore ornamentation. he spore wall has been characterized in different studies
using different sources of information –light and electron microscopy– that generated different
terms to denominate the observed ultrastructural patterns (Clémençon et al. 2004). It is known
that seemingly similar forms can exhibit different ultrastructural patterns (Clémençon et al., 2004),
and as such regarding these forms as homologous sensu de Pinna (1991) would be incorrect by
the test of similarity (Rieppel & Kearney 2002, Grant & Kluge 2004). Based on this knowledge, the
ultrastructure of the ornamentation was coded instead by the morphological patterns observed. In
the present study the nomenclature of Pegler & Young (1985) was used, which also corresponds to
the descriptions of Hawksworth et al. (1995). States: 0: tunica, 1: corium.
35.- Cyanophilous reaction of the spores. For the present study a cyanophilous reaction was
considered positive when the wall of the spore stains with cotton blue, following the nomenclature
proposed by Kotlaba & Pouzar (in Donk 1964). During the present study the reagent was prepared
dissolving 1.6 g of cotton blue in 10 ml of lactic acid. Ater adding the reagent, the preparation was
heated until boiling and then let to cool for 10 minutes before observations were made. States: 0:
positive, 1: negative.
36.- Pattern of cyanophylly in the spores. he positive reaction to cotton blue (cyanophylly)
exhibits two patterns of coloring: homogeneous or more intense in the ornamentation. States: 0:
homogeneous coloring, 1: ornamentation more cyanophilous.
284
Appendix 2. Data matrix
Table 2. Data matrix for the 23 species and 36 characters.
? = missing data, – = inapplicable data. For description of the characters and character states see Appendix 1.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
Clavaria amoena
0
1
1
3
0
1
–
1
0
0
0
1
0
1
1
0
0
0
Clavaria aurantiocinnabarina
0
1
1
3
0
1
–
1
0
1
0
1
0
0
1
0
0
0
Clavaria gibbsiae
0
1
1
3
0
0
–
1
0
1
?
1
0
?
1
1
–
0
Clavaria sulcata
0
1
1
3
0
1
–
1
1
1
?
1
0
–
1
0
0
0
Clavaria vermicularis
0
1
1
3
1
1
–
1
1
1
?
1
0
–
1
1
–
0
Clavaria zollingeri
1
0
1
3
–
0
0
1
0
1
?
1
1
0
1
1
–
0
Clavariadelphus pistillaris
0
1
1
2
1
0
–
1
0
0
1
1
0
0
1
0
1
0
Clavulinopsis corniculata
1
0
1
3
–
0
0
1
0
0
1
1
0
0
1
0
0
0
Clavulinopsis fusiformis
0
1
1
3
0
1
–
1
0
0
1
1
0
1
1
0
1
0
Clavulinopsis helvola
0
1
1
3
0
1
–
1
0
1
?
1
0
1
1
0
0
?
Clavulinopsis laeticolor
0
1
1
3
0
1
–
1
0
0
1
1
0
?
1
0
0
0
Gomphus clavatus
1
1
0
1
–
0
–
0
1
1
1
1
1
–
0
0
1
?
Gomphus floccosus
1
1
0
1
–
0
–
0
0
1
?
1
1
0
0
1
–
?
Lactarius indigo
1
1
0
0
–
0
–
1
1
1
?
0
1
–
1
1
–
1
Ramariopsis californica
1
0
1
3
–
1
0
1
0
1
?
1
0
1
1
0
1
0
Ramariopsis crocea
1
0
1
3
–
0
0
1
0
1
1
1
0
1
1
0
1
0
Ramariopsis kunzei
1
0
1
3
–
0
0
1
1
1
?
1
0
–
1
0
1
0
Ramariopsis pulchella
1
0
1
3
–
0
0
1
0
1
?
1
0
1
1
0
1
0
Ramariopsis tenuiramosa
1
0
1
3
–
0
0
1
1
1
?
1
0
–
1
0
1
0
Scytinopogon dealbatus
1
0
1
3
–
0
1
1
1
1
?
1
1
–
2
0
1
0
Scytinopogon echinosporus
1
0
1
3
–
0
1
0
1
1
?
1
1
–
2
0
1
0
Scytinopogon robustus
1
0
1
3
–
0
1
0
0
1
?
1
1
0
1
0
1
0
Scytinopogon pallescens
1
0
1
3
–
0
1
1
1
1
?
1
1
–
2
0
1
0
Table 2, continued
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
Clavaria amoena
1
0
0
0
0
0
0
1
0
0
1
2
1
1
0
?
1
–
Clavaria aurantiocinnabarina
1
1
0
1
0
0
0
1
1
0
1
0
1
1
0
?
1
–
Clavaria gibbsiae
–
0
1
1
0
0
0
1
1
?
?
2
0
1
1
?
1
–
Clavaria sulcata
1
0
0
1
0
1
0
1
1
?
?
2
1
1
0
?
1
–
Clavaria vermicularis
–
0
0
1
1
1
0
1
1
?
?
2
1
1
0
?
1
–
Clavaria zollingeri
–
0
0
1
1
1
0
1
1
?
?
2
1
1
0
?
1
–
Clavariadelphus pistillaris
0
0
0
1
0
1
0
1
1
0
?
2
1
0
0
?
1
–
Clavulinopsis corniculata
1
0
0
1
0
1
0
1
1
0
0
1
0
0
0
?
1
–
Clavulinopsis fusiformis
1
0
0
0
0
0
0
1
0
0
0
1
0
0
0
?
1
–
Clavulinopsis helvola
1
0
0
1
0
0
0
1
0
?
?
0
0
0
1
1
0
0
Clavulinopsis laeticolor
1
0
0
1
0
0
0
1
0
0
0
2
0
0
0
?
1
–
Gomphus clavatus
1
0
0
1
0
1
0
1
1
0
?
2
0
1
1
?
0
1
Gomphus floccosus
–
0
0
1
1
1
0
1
1
?
?
2
0
1
1
?
0
1
Lactarius indigo
–
0
1
0
1
1
0
1
1
?
?
2
0
1
1
?
0
0
Ramariopsis californica
1
0
0
1
0
1
0
0
1
?
?
0
0
1
1
0
0
1
Ramariopsis crocea
1
0
0
1
0
1
0
0
1
0
0
0
0
0
1
0
0
1
Ramariopsis kunzei
1
0
0
1
0
1
0
0
1
?
?
0
0
0
1
0
0
1
Ramariopsis pulchella
1
0
0
1
0
1
0
0
1
?
?
0
0
0
1
0
0
1
Ramariopsis tenuiramosa
1
0
0
1
0
1
0
0
1
?
?
0
0
0
1
0
0
1
Scytinopogon dealbatus
1
0
0
1
0
1
1
–
1
?
?
0
1
0
1
?
0
0
Scytinopogon echinosporus
1
0
0
1
0
1
1
–
1
?
?
2
1
0
1
?
0
0
Scytinopogon robustus
1
0
0
1
0
1
1
–
1
?
?
0
1
0
1
?
0
0
Scytinopogon pallescens
1
0
0
1
0
1
1
–
1
?
?
0
1
0
1
?
0
0
285
19
286
Appendix 3. Checklist of species names.
Part 1. Species of Ramariopsis sensu stricto
Ramariopsis asterella (G.F. Atk) Corner
≡ Clavaria asterella G.F. Atk.
Ramariopsis avellanea R.H. Petersen
Ramariopsis avellaneainversa R.H. Petersen
Ramariopsis biformis (G.F. Atk.) R.H. Petersen
≡ Clavaria biformis G.F. Atk.
Ramariopsis californica R.H. Petersen
Ramariopsis cinnamomea R.H. Petersen
Ramariopsis cinnamomipes R.H. Petersen
Ramariopsis citrina Schild
Ramariopsis clavuligera (R. Heim) Corner
≡ Clavaria clavuligera R. Heim
Ramariopsis costaricensis L.D. Gómez
Ramariopsis crocea (Pers.) Corner
≡ Clavaria crocea Pers.
Ramariopsis curta (Fr.) Corner
≡ Clavaria curta Fr.
Ramariopsis flavescens R.H. Petersen
Ramariopsis hibernica Corner
Ramariopsis kunzei (Fr.) Corner
≡ Clavaria kunzei Fr.
Ramariopsis longipes R.H. Petersen
Ramariopsis novahibernica Corner
Ramariopsis pulchella (Boud.) Corner
≡ Clavaria pulchella Boud.
Ramariopsis ramarioides R.H. Petersen
Ramariopsis rufipes (G.F. Atk.) R.H. Petersen
≡ Clavaria rufipes G.F. Atk.
Ramariopsis subarctica Pilát
Ramariopsis tenuicula (Bourdot & Galzin) R.H. Petersen
≡ Clavaria tenuicula Bourdot & Galzin
Ramariopsis tenuiramosa Corner
Ramariopsis tortuosa R.H. Petersen
Ramariopsis vestitipes (Peck) Corner
≡ Clavaria vestitipes Peck
Part 2. Species sometimes placed in Ramariopsis that belong in other genera
Clavaria L.
Clavaria asperulospora G.F. Atk.
≡ Ramariopsis asperulospora (G.F. Atk.) Corner
Clavulinopsis Overeem
Clavulinopsis antillarum (Pat.) García-Sandoval & Cifuentes, comb. nov.
≡ Clavaria fusiformis var. antillarum Pat.
≡ Ramariopsis antillarum (Pat.) R.H. Petersen
Clavulinopsis corniculata (Schaeff.) Corner
≡ Clavaria corniculata Schaeff.
287
≡ Ramariopsis corniculata (Scaeff.) R.H. Petersen
Clavulinopsis depokensis (Overeem) Corner
≡ Clavaria depokensis Overeem
≡ Ramariopsis depokensis (Overeem) R.H. Petersen
Clavulinopsis dichotoma (Godey) Corner
≡ Clavaria dichotoma Godey
≡ Ramariopsis dichotoma (Godey) R.H. Petersen
Clavulinopsis fusiformis (Sowerby) Corner
≡ Clavaria fusiformis Sowerby
≡ Ramariopsis fusiformis (Sowerby) R.H. Petersen
Clavulinopsis helvola (Pers.) Corner
≡ Clavaria helvola Pers.
≡ Ramariopsis helvola (Pers.) R.H. Petersen
Clavulinopsis holmskiodii (Oudem.) Corner
≡ Clavaria holmskiodii Oudem.
≡ Ramariopsis holmskiodii (Oudem.) R.H. Petersen
Clavulinopsis laeticolor (Berk. & M.A. Curtis) R.H. Petersen
≡ Clavaria laeticolor Berk. & M.A. Curtis
≡ Ramariopsis laeticolor (Berk. & M.A. Curtis) R.H. Petersen
Clavulinopsis luteo-ochracea (Cavara) Corner
≡ Clavaria luteo-ochracea Cavara
≡ Ramariopsis luteo-ochracea (Cavara) R.H. Petersen
Clavulinopsis luteotenerrima (Overeem) Corner
≡ Clavaria luteotenerrima Overeem
≡ Ramariopsis luteotenerrima (Overeem) R.H. Petersen
Clavulinopsis minutula (Bourdot & Galzin) Corner
≡ Clavaria minutula Bourdot & Galzin
≡ Ramariopsis minutula (Bourdot & Galzin) R.H. Petersen
Clavulinopsis subtilis (Pers.) Corner
≡ Clavaria subtilis Pers.
≡ Ramariopsis subtilis (Pers.) R.H. Petersen
Clavulinopsis umbrinella (Sacc.) Corner
≡ Clavaria umbrinella Sacc.
≡ Ramariopsis umbrinella (Sacc.) R.H. Petersen
Ramaria Fr.
Ramaria lorithamnus (Berk.) R.H. Petersen
≡ Clavaria lorithamnus Berk.
≡ Ramariopsis lorithamnus (Berk.) Corner
Scytinopogon Singer
Scytinopogon dealbatus (Berk.) Corner
≡ Clavaria dealbata Berk.
≡ Ramariopsis dealbata (Berk.) R.H. Petersen
Part 3. Species initially described in Ramariopsis that require further examination
Ramariopsis agglutinata R.H. Petersen
Ramariopsis alutacea R.H. Petersen
Ramariopsis aurantio-olivacea R.H. Petersen
Ramariopsis bicolor R.H. Petersen
Ramariopsis cremicolor R.H. Petersen
288
Ramariopsis junquillea R.H. Petersen
Ramariopsis lignicola R.H. Petersen
Ramariopsis ovispora R.H. Petersen
Ramariopsis pseudosubtilis R.H. Petersen
Ramariopsis simplex R.H. Petersen
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