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Xylariales (Sordariomycetes, Ascomycota) of the Boston
Harbor Islands
Roo Vandegrift*
Abstract - The Xylariales (Sordariomycetes, Ascomycota) is an order of mostly stromatic
perithecial fungi generally inhabiting wood and other plant debris, as well as some important
plant pathogenic species. As a follow-up to an extensive fungal inventory conducted
by D. Haelewaters and colleagues since December 2012 at the Boston Harbor Islands
National Recreation Area in Massachusetts, I examined members of the Xylariales in
detail, including previously unreported collections. I constructed keys for included taxa,
and I provide species notes, references, substrate, and collecting data of the following
Xylarialean genera: Diatrype, Eutypa, Eutypella (Diatrypaceae); Biscogniauxia, Camillea,
Graphostroma (Graphostromataceae); Annulohypoxylon, Daldinia, Hypomontagnella,
Hypoxylon, Jackrogersella (Hypoxylaceae); Lopadostoma (Lopadostomataceae); and
Entoleuca, Kretzschmaria, Nemania, Rosellinia, Xylaria (Xylariaceae). I herein formally
describe a new species, Xylaria finismundoensis sp. nov., based on combined morphology
and multi-locus phylogenetic analysis. This taxon provides the first evidence of a saprotrophic
lifestyle for members of the E9 phylogenetic clade of Xylaria, previously only known
as endophytes.
Introduction
Xylariales
The Xylariales (Xylariomycetidae, Sordariomycetes, Ascomycota) is a large,
heterogeneous grouping of mostly stromatic perithecial fungi occurring primarily
on dead plant materials. The order was first circumscribed by Nannfeldt (1932),
and then later revised by Eriksson and Winka (1997) to include the Diatrypales, as
well as to place it as the only order within the subclass Xylariomycetidae. Recent
advances in phylogenetic methods and availability of multi-gene sequences across
a large sampling of taxa within Xylariales, as well as an increased acceptance of
the value of chemotaxonomic approaches (Stadler 2011, Stadler et al. 2014b), have
led to an increasing refinement of the circumscription of Xylariales (Daranagama
et al. 2018, Voglmayr et al. 2018, Wendt et al. 2018), with particular attention paid
to the Xylariaceae sensu lato and related groups.
Historically, the Xylariaceae has been one of the largest families in the Ascomycota.
As recently as 2013, it included more than 85 genera and some 1343 accepted
species (Eriksson 2006, Kirk et al. 2008, Laessøe and Spooner 1994, Stadler et
al. 2013). Recent revisions have helped to tame this chaos somewhat, including
the erection of the family Lopadostomataceae to accommodate Lopadostoma and
Creosphaeria (Senanayake et al. 2015), 2 rather anomalous genera previously
*Institute of Ecology and Evolution, University of Oregon, Eugene, OR 97403-5289;
awv@uoregon.edu.
Manuscript Editor: David Richardson
Research at the Boston Harbor Islands NRA
2021 Northeastern Naturalist 25(Special Issue 9):150–199
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assigned to the Xylariaceae. The most significant recent revisions, however, came
with the splitting of the Xylariaceae, based on phylogenetic data roughly along
the lines of the long-accepted (but never formalized) subfamily divisions (see
Dennis 1961, Ju and Rogers 1996) by Wendt et al. (2018), which resurrected the
Hypoxylaceae for Hypoxylon and allies as well as confirmed the Graphostromataceae—
erected as a monotypic family by Barr et al. (1993) to accommodate
Graphostroma—as a phylogenetically meaningful family, and moved other genera
with applanate, bipartite stromata out of the Xylariaceae and into that family.
The order will continue to see taxonomic changes—new taxa, new combinations—
while the exact evolutionary affinities of these groups are undergoing such
tremendous revision. At present, there are 16 well-accepted families containing
some 109 genera within the Xylariales (of which 32 are presently accepted within
Xylariaceae), and an incredible 54 additional genera are considered Xylariales
incertae sedis (Daranagama et al. 2018; Voglmayr et al. 2018, 2019; Wendt et al.
2018; Wijayawardene et al. 2020).
Endophytes
Notably, many fungi in the Xylariales are known to be common and ubiquitous
endophytes—fungi that inhabit the leaves and other tissues of plants without causing
disease to their host plant (Rodriguez et al. 2009, Stone et al. 2000). Much
attention has been paid to the potential for these endophytic fungi to produce novel
secondary metabolites with medicinal potential (e.g., Govinda Rajulu et al. 2013).
However, such endophytes have traditionally been difficult to assign to specific taxa
due to lack of available characters in culture (Rogers 1979, 2000, Whalley 1996).
Recent innovations, however, suggests that the wealth of Xylarialean diversity
present as endophytes may, in fact, also be useful in efforts to revise the taxonomy
of the order, as secondary metabolites are a rich source of features to help classify
taxa (Stadler 2011), and the addition of increased taxonomic sampling by utilizing
endophyte cultures may significantly improve efforts at phylogenetic reconstruction
(U’Ren et al. 2016).
The ecology of endophytism within Xylariales remains something of a mystery,
though several hypotheses have been put forward (Bayman et al. 1998, Carroll
1999, Nelson et al. 2020). Some Xylarialean endophytes persist in the leaf litter,
displaying clear abilities to participate in litter degradation and colonize
additional substrates (Osono 2007; Osono and Takeda 1999, 2002), which would
seem to preclude the necessity of an endophytic lifestyle. It has been proposed that
endophytism in Xylarialean taxa may be an evolutionary “dead-end”, simply a byproduct
of mechanisms evolved to colonize woody substrates (Bayman et al. 1998).
A competing theory, the so-called “Foraging Ascomycete Hypothesis” (Carroll
1999), proposes that such fungi utilize an endophytic lifestage to bridge spatiotemporal
gaps in preferred substrate, persisting in the leaves despite poor conditions or
lack of substrate (Nelson et al. 2020, Thomas et al. 2016).
Additionally, it has been observed that many Xylarialean endophytes have
not been linked conclusively to teleomorphic (i.e., sexually reproducing) taxa,
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giving rise to the theory that there may be endophyte-specific lineages within the
Xylariales (Okane et al. 2008, U’Ren et al. 2016). U’Ren et al. (2016) utilized a
continent-scale library of endophytic isolates to add more than 1900 new Xylarialean
isolates to multi-locus sequence data for 293 well-identified taxa in the most
robust phylogeny of the Xylariales to date. They found several clades represented
by only endophytic isolates, of which one—the “E9” endophyte clade—was within
the phylogenetic bounds of the genus Xylaria, one of the most commonly isolated
endophyte genera in the order. This finding could be taken as support for the idea
that there are specifically endophytic lineages; if so, how they reproduce and disperse
remains an open question.
All taxa biodiversity inventory
This study is part of an ongoing all taxa biodiversity inventory (ATBI) at the
Boston Harbor Islands (BHI) National Recreation Area, Boston, MA. This is an
integrated effort across multiple organizations, including the Boston Harbor Islands
Partnership (BHIP), the National Park Service, and Harvard University, among
others. Across multiple phases of research, this ATBI has generated data and publications
on insects and other invertebrates (Clark et al. 2011; Rykken and Farrell
2013, 2018a, 2018b), lichens and bryophytes (Lagreca et al. 2005), bats (Johnson
and Edward Gates 2019) and other small mammals (Nolfo-Clements 2018), birds
(Paton et al. 2005), vascular plants (Elliman 2005), and non-lichenized fungi
(Haelewaters et al. 2018) with a particular focus on the insect-parasitic Laboulbeniales
(Haelewaters et al. 2015, 2019).
Herein I present a taxon-specific contribution to the ATBI and a follow-up to the
"Preliminary Checklist of Fungi" generated previously (Haelewaters et al. 2018),
focusing on the Xylariales. Herein I provide detailed keys and taxonomic descriptions
to all Xylarialean taxa known from the Boston Harbor Islands, and propose 1
new species, Xylaria finismundoensis. This species is of particular interest because
of its apparent affinity with the E9 Endophyte group of Xylaria previously known
only as endophytes.
Methods
Samples were collected as part of a broad all-Fungi inventory effort, carried
out between December 2012 and May 2017 at the Boston Harbor Islands National
Recreation Area (BHI) in Massachusetts. See Haelewaters et al. (2018) for detailed
sampling methodologies and site descriptions. All fungal collections studied
here were deposited at the Farlow Herbarium at Harvard University (Cambridge,
MA). Material identified as potentially belonging to the Xylariales was sent to the
University of Oregon for detailed examination. I performed microscopy with a
combination of a Zeiss Standard WL compound microscope (Zeiss, Oberkochen,
Germany) fitted with ocular and stage micrometers and an Olympus SZ30 stereoscope
(Tokyo, Japan). I conducted photomicroscopy using an Amscope 10MP
CMOS camera (Irvine, CA) attached to the trinocular head of the Zeiss microscope
and macrophotography using an Olympus Tough TG-5 camera on the macro setting
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with automated focus bracketing; I assembled and edited focus stacks in Zerene
Stacker (Zerene Systems LLC, Richland, WA).
After determination, I prepared taxonomic descriptions to be inclusive of
well-accepted descriptions for each taxon, generally broadening the range of measurements
somewhat from what was observed in any particular collection. This
approach allows broader applicability of published keys and descriptions. I made
specific reference to Rappaz (1987), Chlebicki (2005), Glawe and Rogers (1984),
and Vasilyeva and Stephenson (2004, 2006) for Diatrypaceae; to Ju et al. (1998),
Laessøe et al. (1989), and Barr et al. (1993) for Graphostromataceae; to Jaklitsch
et al. (2014) and Daranagama et al. (2018) for Lopadostomataceae; to Wendt et al.
(2018), Miller (1961), Ju and Rogers (1996), and Stadler et al. (2014a) for Hypoxylaceae;
to many works from Jack D. Rogers and Yu-Ming Ju (Ju and Rogers 2002,
Rogers and Ju 1996, 2012), as well as works in collaboration with Brenda Callan
(Rogers and Callan 1986) and those in collaboration with Larissa Vasilyeva and
Andrew Miller (Rogers et al. 2008, Vasilyeva et al. 2007) for Xylariaceae; and the
recent monograph by Petrini (2013) for Rosellinia.
I performed amplification and sequencing of the ITS region of the rDNA as
per Haelewaters et al. (2018). Additional loci (β-tubulin, α-actin, partial LSU, and
RPB2) were sequenced for collection BHI-F502, based on presumed novelty, using
primers and DNA amplification as per U’Ren et al. (2016) in the Roy Lab at the
University of Oregon. I performed amplification using an MJ Research PTC-200
DNA Engine thermal cycler. I froze the PCR product at -4 ºC until shipping for subsequent
sequencing at Functional Biosciences, Inc. (Madison, WI) on ABI 3730xl
instruments using BigDye V3.1, employing the same primers as those to generate
the PCR product. Raw sequence reads were assembled and analysis was performed
in Geneious 6.1 (Biomatters, Ltd., Auckland, New Zealand). Newly generated sequences
for this study are deposited in NCBI’s GenBank database (https://www.
ncbi.nlm.nih.gov/genbank/) with accession numbers MT823470–MT823485.
I used a BLAST search against NCBI GenBank’s nucleotide database to suggest
placement of BHI-F502 in the “E9” clade within the genus Xylaria. To examine
exact placement, I downloaded the final concatenated alignment containing 367
terminal taxa from U’Ren et al. (2016) from TreeBASE (http://purl.org/phylo/
treebase/phylows/study/TB2:S18910) and subsetted from the full dataset the endophyte
“E9” clade, representative members of the Xylaria “HY” clade, and Eutypa
lata as the outgroup. Additionally, I downloaded available sequences from
the epitype of Xylaria hypoxylon (LSU: KY610495.1; β-tubulin: KX271279.1;
RPB2: KY624231.1; ITS: KY610407.1) from NCBI GenBank (Stader et al. 2014).
I removed unalignable intron regions from sequences for each locus from BHIF502
and those available from the epitype of Xylaria hypoxylon, and then added
these sequences to the subsetted alignments using default parameters in Geneious
Prime. To determine exact phylogenetic placement within the clade, I concatenated
alignments for each of the 5 loci (β-tubulin, α-actin, LSU, RPB2, and 5.8S) and
performed phylogenetic reconstruction using either RAxML (Stamatakis 2014)
with the GTR GAMMA model, 1000 bootstrap repetitions, and partitions specified
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for each loci in the concatenated alignment or MrBayes 3.2.6 (Huelsenbeck and
Ronquist 2001) using all standard parameters. Trees were rooted with Eutypa lata
(Diatrypaceae) as the outgroup.
Results and Discussion
Careful examination of collections from the Boston Harbor Islands revealed
59 collections representing 26 taxa within the Xylariales, from 16 genera across 5
families. This result is a significant increase from 11 species reported in the initial
checklist effort (Haelewaters et al. 2018). I describe 1 new taxon and provide keys
to families, genera, and species for all observed taxa in addition to descriptions for
all included taxa, with figures to illustrate novel taxa as well as many other taxa to
aid identification.
Since the discovery that fungi within the Xylariaceae, particularly the genus
Xylaria, were common endophytes (Carroll and Carroll 1978, Carroll et al. 1977),
there has been speculation that there may be distinct lineages that exist exclusively
or primarily within the endophytic niche (Bayman et al. 1998, Brunner and Petrini
1992, Okane et al. 2008, Osono 2007, Rodrigues et al. 1993, Thomas et al. 2016,
U’Ren et al. 2016). Such theories are difficult to test, however, due in part to the
lack of diagnostic features present on Xylaria in culture (Brunner and Petrini 1992).
Importantly, U’Ren et al. (2016) included Xylarialean endophytes in their phylogenetic
analysis.
The inclusion of nearly 2000 newly cultured isolates of Xylarialean endophytic
fungi in U’Ren et al.’s (2016) multi-locus phylogenetic analysis, combined with
available sequences data from 293 taxa within the Xylariales, allowed for the
identification of monophyletic clades represented by only endophytes. Of these,
only the E9 endophyte clade, sister to the Xylaria “HY” clade, is within the current
phylogenetic bounds of the genus Xylaria, with several others appearing to be basal
to the currently accepted definition of the family (U’Ren et al. 2016, Wendt et al.
2018). The newly described taxon from this study, Xylaria finismundoensis sp. nov.,
is placed within this E9 clade, making it the first known teleomorphic fungus from
this group (Fig. 1).
Taxonomy
Key to Families of Xylariales from the Boston Harbor Islands
1. Ascospores allentoid, pale yellow or brown; ostioles prominently differentiated
from stromata, often sulcate to cruciform; KOH extractable pigments absent;
stromata always unipartite; anamorph libertella-like.......................Diatrypaceae
1. Combination of features not as above: ascospores different in shape (ellipsoid
to ellipsoid-inequilateral or asymmetrically attenuated) or color (brown to
dark brown); if ostioles strongly differentiated from stromata, never sulcate or
cruciform; KOH extractable pigments either present or absent; stromata either
unipartite or bipartite..........................................................................................2
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2. Stromatal tissues, at least on the ventral side, a mixture of woody substrate and
fungal cells, generally surrounded by a thin, black, carbonized encasement;
perithecia valsoid, with ostioles clustered into an ectostromatic disc; anamorph
libertella-like ....................Lopadostomataceae (Lopadostoma americanum)
2. Stromatal tissues distinct from substrate on the ventral side (though ventral
tissues may be severely reduced); ostioles either clustered or uniformly distributed
over stromatal surface, but perithecia never valsoid; anamorph typically
nodulisporium-like or geniculosporium-like...................................................3
3. Stromata bipartite, always flattened against substrate (applanate, effusedpulvinate,
or raised-discoid); KOH extractable pigments absent ................
................................................................................. Graphostromataceae
Figure 1. Phylogenetic placement of BHI-F502, the type collection of Xylaria finismundoensis
sp. nov., based on the phylogenetic reconstruction of a 5-locus dataset of concatenated
sequences with introns removed (β-tubulin, α-actin, partial LSU, RPB2, and 5.8S).
The topology is the result of maximum likelihood analysis performed with RAxML (though
topology was identical when Bayesian analysis was used); Bayseian posterior probabilities
and ML bootstrap support values, respectively, are shown at each node. The tree is rooted
with Eutypa lata (Diatrypaceae).
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3. Stromata unipartite, either flattened against substrate or erect; with or without
KOH extractable pigments...................................................................4
4. Ascal plugs wider than tall; KOH extractable pigments generally present;
internal stromatal tissues, when present, typically dark or other than
white; anamorph nodulisporium-like................................Hypoxylaceae
4. Ascal plugs taller than wide; KOH extractable pigments absent; internal
stromatal tissues, when present, typically white or pale (especially when
early in stromatal development); anamorph geniculosporium-like..........
............................................................................................ Xylariaceae
Key to Diatrypaceae from the Boston Harbor Islands
1. Stromata discoid to pulvinate, stipitate or with a constricted base; internal stromata
tissues well developed; stromata strongly differentiated from substrate;
ostioles regularly spaced............................................................Diatrype bullata
1. Stromata sessile and broadly attached; internal stromata tissues well developed or
not; stromata generally lacking a clear boundary between well-developed entostromatal
tissues (if present) and substrate; ostioles regularly spaced or grouped
into pustules.......................................................................................................2
2. Stromata bipartite (in 2 layers, the outer dehiscent layer adhering to the underside
of the bark as the stroma developes, and falling away to reveal the inner
perithecial layer; outer layer often only present as remnants around the edge of
mature stromata); ostioles with large openings into the perithecia (>50 μm) ....
............................................................................ Graphostroma platystomum
2. Combination of features not as above; stromata always unipartite (in 1 layer);
ostiolar openings into the perithecia small (less than 30 μm diameter) ........................3
3. Ostioles grouped into collectively erumpent clusters, typically sulcate but
sometimes rounded; perithecia valsoid; stromata emerging from substrate as
pustules, united below by a common, well-developed entostromatic tissue.
..................................................................................... Eutypella prunastri
3. Ostioles separate and regularly spaces, rounded to sulcate; perithecia singular;
stromata effuse within woody substrate, generally darkening the
surface, without clear differentiation between entostromatic tissues and
substrate......................................................................................4 (Eutypa)
4. Ascospores 6.2–11 μm × 1.5–2 μm; ostioles emerging separately,
rounded or conical, entire to more or less furrowed, but never cruciform;
substrate blackened at the surface............................ Eutypa lata
4. Ascospores 4.8–7.8 μm × 1.2–1.5 μm; ostioles emerging separately,
rounded to rectangular, deeply split 3–4 times, often cruciform; substrate
discolored at the surface, but generally not blackened...............
......................................................................................Eutypa maura
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Key to Graphostromataceae from the Boston Harbor Islands
1. Ostioles level with stromatal surface and wide open, appearing as distinct holes
in the stromatal surface when viewed with a hand lens; ascospores diatrypaceous
(7–10 μm × 1–2 μm, hyaline or pale yellow-brown, allantoid), without obvious
germ slit................................................................. Graphostroma platystomum
1. Ostioles either level with stromatal surface or raised above it (papillate), but
never wide open; ascospores either typically Xylarialean (darkly pigmented, ellipsoid
to ellipsoid inequilateral) or hyaline and asymmetrically attenuated......2
2. Ascospores small (<11 μm long), hyaline, and asymmetrically attenuated on
one end, without obvious germination site; ostioles level with stromatal surface,
looking like minute pin-pricks when viewed with a hand lens.................
........................................................................................ Camillea punctulata
2. Ascospores larger (typically >14 μm long), darkly pigmented, and ellipsoid
to ellipsoid-inequilateral, with an obvious hyaline germination slit; ostioles
coarsely papillate, distinctly raised above the stromatal surface ......................
............................................................................................ 3 (Biscogniauxia)
3. Ascospores 15.5–21 μm × 7–10 μm ................. Biscogniauxia mediterranea
3. Ascospores 20–26 μm × 11.5–13 μm.............................................................
............................................. Biscogniauxia mediterranea var. macrospora
Key to Hypoxylaceae from the Boston Harbor Islands
1. Stromata more or less hemispherical, with internal concentric rings...................
................................................................................................Daldinia childiae
1. Stromata variable, applanate to hemispherical, but interior of stromata more or
less homogeneous, without concentric rings......................................................2
2. Perithecia surrounded by a layer of hard, carbonaceous tissue; tissues below
perithecia conspicuous to massive; KOH extractable pigments typically
greenish olivaceous.......................................................................................3
2. Perithecia not surrounded by carbonaceous tissue; tissues below perithecia inconspicuous
to absent; KOH extractable pigments orange to rust, or absent ..... 4
3. Ostioles surrounded by a more or less well-developed annular disc; stromata
robust, effused-pulvinate to semi-globose; ascospores 7.5–10.5 μm × 3.5–5
μm, with a straight, spore-length germ slit ....Annulohypoxylon annulatum
3. Ostioles papillate, but not surrounded by an annular disc; stromata thinner,
effused-pulvinate to peltate, but never semiglobose; ascospores 8.5–12 μm
× 3.5–5 μm, with a straight germ slit less than spore-length .......................
........................................................................ Jackrogersella multiformis
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4. Stromata without apparent KOH extractable pigments (or, rarely, KOH extractable
pigments purple); ascospores with germ slit less than to much less than
spore-length...............................................Hypomontagnella submonticulosum
4. Stromata with KOH extractable pigments orange or rust; ascospores with straight
germ slit, spore-length or nearly so....................................................................5
5. Perithecia tubular, much taller than wide; stromatal interior with distinct concentric
zones; ascospores 12–16 μm in length ......................Daldinia childiae
5. Perithecia more or less globose, similar in height and width; stromatal interior
essentially homogeneous; ascospores 9–15 μm in length ................................6
6. Ostioles slightly elevated above stromatal surface (papillate); stromata with
perithecial contours conspicuous; ascospores 9.5–15 μm × 4–6.5 μm, with
a slightly sigmoid, spore-length germ slit..............Hypoxylon lenormandii
6. Ostioles lower than stromatal surface (umbilicate); stromata with perithecial
contours inconspicuous to absent; ascospores 9–12 μm × 4–5.5 μm, with a
straight, spore-length germ slit..............................Hypoxylon rubiginosum
Key to Xylariaceae from the Boston Harbor Islands
1. Stromata essentially uniperitheciate, containing 1 (or rarely, several) perithecia;
superficial on substrate (typically decorticated wood) ........................................2
1. Stromata multiperitheciate, containing several to many perithecia; stromata
applanate to pulvinate or upright, but never surrounded by a felty or wooly subiculum
(though sometimes anamorph may be present on stromatal surface).....4
2. Halophilic (substrate salty driftwood); subiculum lacking; stromata obtusely
conical............................................................................... Nemania maritima
2. Not halophilic (substrate other than salty driftwood); felty or wooly subiculum
present; stromata globose to broadly rounded.............................3 (Rosellinia)
3. Stromata often embedded in a wooly, reddish-brown subiculum; ascospores
typically >15μm in length, with germination slit spore-length o r nearly so.
................................................................................... Rosellinia corticium
3. Stromata often embedded in a felty, sulphur-yellow subiculum; ascospores
typically less than 15μm in length, with germination slit typically less than sporelength........................................................................
Rosellinia subiculata
4. Stromata essentially flattened against substrate, applanate t o pulvinate.............5
4. Stromata essentially upright, taller than it is wide.............................. 8 (Xylaria)
5. Spores >20 μm in length; perithecia large (~1 mm diameter); mature stromata
extremely carbonaceous, generally becoming extremely hard and brittle in
age.................................................................................................................6
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5. Spores less than 20 μm in length; perithecia small (0.4–0.8 mm diam); mature stromata
with only a thin carbonaceous layer above perithecia............................7
6. Stromata large, typically several to 10 cm in length and >1 cm thick, often
stipitate or connected to substrate by a constricted base, frequently fused
into large aggregates; stromata becoming hollow at maturity, very brittle;
ascospores 27–35 μm × 7–9 μm (length:width ratio > 3), ellipsoid inequilateral
to fusoid, with germ slit much less than spore-length .....................
................................................................................. Kretzschmaria deusta
6. Stromata more or less orbicular in outline, fused or aggregated into a
crust, not stipitate, with stromatal bases partially embedded in substrate;
at maturity stromata extremely hard, with thick carbonaceous tissue above
and partially surrounding perithecia; ascospores 20–33 μm × 9–12 μm
(length:width ratio < 3), nearly equilateral, with germ slit sp ore-length.....
...................................................................................Entoleuca mammata
7. Ascospores 8–10 μm × 3.5–4.5 μm, ellipsoid to reniform, with an inconspicuous,
straight germ slit; stromatal tissue between the perithecia carbonaceous.............
........................................................................................... Nemania beaumontii
7. Ascospores 10–14 μm × 4–6 μm, ellipsoid, with an inconspicuous, straight germ
slit; stromatal tissue between the perithecia soft, white to buff ...........................
.............................................................................Nemania serpens var. serpens
8. Stromata large, often >1 cm in diameter and >6 cm in height, unbranched with
broadly rounded, fertile apex; surface wrinkled and minutely wrinkled; ascospores
20–28 μm × 6–7.5 μm, with germ slit much less than spore -length......
........................................................................................Xylaria polymorpha
8. Stromata minute, less than 1 cm in height, with a sterile pointed apex; remnants of
white exostromatal coating apparent on mature stromata as vertical stripes;
stipe short, densely tomentose at base; ascospores 10–1 1 μm × 5–6 μm.........
................................................................... Xylaria finismundoensis sp. nov.
Diatrypaceae Nitschke
Type genus: Diatrype Fr., Summa Vegetabilium Scandinaviae 2:384 (1849)
Stromata with perithecia embedded in a stromata composed either of purely fungal
tissue, or a mixture of fungal tissue and substrate (pseudostromata). Ostioles ornamented,
furrowed, or sulcate, though at times faintly or rudimentary. Ascospores
allantoid to subinequilateral, from nearly straight to strongly curved. Asci clavate
to spindle-shaped, with a characteristic apical plug either I+ or I−.
Additional information: The most complete keys to diatrypaceous taxa globally
are given in the monograph by Rappaz (1987). More-focused work can be found
in Chlebicki (2005), Glawe and Rogers (1984), and Vasilyeva and Stephenson
(2004, 2006).
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Diatrype Fr., Summa Vegetabilium Scandinaviae 2:384 (1849)
Type species: Diatrype disciformis (Hoffm.) Fr.
Stromata widely effuse and applanate, or disc-shaped, flat to slightly convex, with
discoid or sulcate ostioles mostly raised above the surface. Perithecia mostly in a
single layer, though at times stacked or piled on top of each other. Ascospores are
allantoid, hyaline yellowish to brownish. Asci typically clavate, 8-spored, longstipitate,
with paraphyses.
Additional information: Rappaz (1987) provides useful keys to global species
of Diatrype. Chlebicki (2005) focuses on European species, Glawe and Rogers
(1984) provide information for the Pacific Northwest, and Vasilyeva and Stephenson
(2004) focus on the Great Smoky Mountain National Park in the southeastern
United States.
Diatrype bullata (Hoffm.) Fr. (Fig. 2a–c)
≡ Sphaeria bullata Hoffm., Vegetabilia Cryptogama 1:5, t. 2:3 (1787)
≡ Hypoxylon bullatum (Hoffm.) Westend. & Wallays, Add. Herb. Crypt., p. 14 (1850)
Stromata present as discoid pustules in the bark, rupturing through the outer layer
of the bark to reveal flat to pulvinate disc-shaped stromata; brown-gray to dark
brown, circular, 3–5 mm in diameter; pustules typically evenly spaced, rarely confluent;
with a compact, white entostroma, clearly differentiated from surrounding
substrate by a blackened border of ectostromatic tissue; stromatal discs stipitate,
or with a distinctly constricted base, blending with substrate beneath. Perithecia
Figure 2. Diatrype bullata (BHI-F791): (a) stromatal habit and surface texture, showing
weakly furrowed, discoid ostiolar beaks; (b) vertical section of stromata, showing perithecia
and well developed white entostromatic tissue; and (c) ascospores and asci, showing
faintly amyloid apical apparatus. Scale bars: a = 1000 μm; b = 500 μm; and c = 10 μm.
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regularly spaced within stromatal discs, often close together or in contact, partially
compressed due to crowding; spherical to ovoid, 200–300 μm in diameter by 300–
400 μm tall. Ostioles are separately emergent (not valsoid); slightly raised above
stromatal surface, discoid, often but not always irregularly and faintly furrowed or
sulcate; 80–120 μm in diameter. Ascospores 5–8 μm × 1–1.5 μm, allantoid, pale
yellow to pale brown. Asci are long-stipitate, the spore-bearing parts 25–35 μm
long, with the stipe being at least as long as the spore-bearing parts, up to twice as
long; with a faint, discoid (i.e., flattened donut shaped) apical plug, wider than it is
tall, ~1 μm × 0.5 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, PEDDOCKS ISLAND, corticated hardwood stick, col. Alden C.
Dirks, James K. Mitchell, 42830 (FH:BHI-F791).
Notes: This taxon is easily confused with Diatrype disciformis (Hoffm.) Fr., being
one of only a few Diarype species with disc-shaped stromata. Rappaz (1987),
Glawe and Rogers (1984), and Chlebicki (Chlebicki 2005) all emphasize the flatness
of the stromatal disc, the nearly perfectly circular outline, and the smaller size
as distinguishing characteristics separating D. disciformis from D. bullata. Also of
note is the distinctly constricted or stipitate stromatal base in D. bullata, along with
the well developed white entostromatal tissues extending below the perithecia (illustrated
in Chlebicki 2005); D. disciformis typically does not have has well-developed
white entostromatic tissues completely surrounding the perithecia, but only
around the necks, and rarely extending all the way to the bases. These additional
discriminative characters should be helpful to anyone attempting to distinguish
between these 2 similar taxa.
Eutypa Tul. & C. Tul., Sel. Fung. Carp. 2:52 (1863)
Type species: Eutypa lata (Pers.) Tul. & C. Tul.
Stromata widely effuse within woody substrates, causing darkening or blackening
at the surface, with separate, rounded or sulcate ostioles raised above the surface.
Ascospores are allantoid, hyaline yellowish to brownish. Asci typically clavate or
cylindrical, 8-spored, usually long-stipitate, with paraphyses.
Additional information: Rappaz (1987) provides useful keys to global species of
Eutypa. Glawe and Rogers (1984) provide information for the Pacific Northwest,
and Vasilyeva and Stephenson (2006) focus on the Great Smoky Mountain National
Park in the southeastern United States.
Eutypa lata (Pers.) Tul. & C. Tul. (Fig. 3a–c)
≡ Sphaeria lata Pers., Observationes Mycologicae 1:66 (1796)
≡ Nemania lata (Pers.) Gray, A Natural Arrangement of British Plants 1:517 (1821)
≡ Stromatosphaeria lata (Pers.) Grev., Flora Edinensis:357 (1824)
≡ Diatrype lata (Pers.) Fr., Summa Vegetabilium Scandinaviae 2:385 (1849)
≡ Valsa lata (Pers.) Nitschke, Pyrenomycetes Germanici 1:141 (1867)
≡ Engizostoma latum (Pers.) Kuntze, Revisio Generum Plantarum 3(2):474 (1898)
Stromata widely effused within the substrate, up to several centimeters in diameter,
lifting the surface of the wood in confluent patches or large plates, more or less
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blackening the substrate; tissues surrounding perithecia a mixture of substrate and
loose mycelium, irregularly blackened, but often with a pale zone directly beneath
the blackened surface. Perithecia close together or in contact, sometimes laterally
compressed due to crowding; spherical to ovoid, 400–600 μm in diameter. Ostioles
are separately emergent (not valsoid); prominently raised above stromatal surface,
rounded to conical, often but not always faintly furrowed; 120–180 μm in diameter.
Ascospores 6.2–11 μm × 1.5–2 μm, allantoid, pale yellow to pale brown. Asci are
long-stipitate, the spore-bearing parts 40–60 μm long, with the stipe being at least
as long as the spore-bearing parts; with a faint, discoid apical plug, wider than it is
tall, ~1 μm × 0.5 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, GREAT BREWSTER ISLAND, on dead decomposing log, col. James
K. Mitchell, 8 March 2017 (FH:BHI-F611).
Eutypa maura (Fr.) Fuckel (Fig. 3d–f)
≡ Sphaeria maura Fr., Kongliga Svenska Vetenskapsakademiens Handlinger
39:101 (1818)
≡ Valsa maura (Fr.) Nitschke, Pyrenomycetes Germanici 1:133 (1867)
≡ Eutypa maura (Fr.) Sacc., Sylloge Fungorum 1:166 (1882)
≡ Engizostoma maurum (Fr.) Kuntze, Revisio Generum Plantarum 3(2):474 (1898)
Stromata widely effused within the substrate, up to several centimeters in diameter,
generally not raised, darkening the substrate, grey to grey-black; tissues surrounding
perithecia a mixture of substrate and loose mycelium, uniformly darkened, grey
as at the surface. Perithecia in rows, rarely in contact, regularly spaced (~300–400
μm between individual perithecia); generally buried deeply; spherical, but often
vertically flattened, 400–500 μm in diameter by 300–400 μm tall. Ostioles are
separately emergent (not valsoid); prominently raised above stromatal surface,
rounded to conical, deeply split 3–4 times; 120–160 μm in diameter. Ascospores
4.8–7.8 μm × 1.2–1.5 μm, allantoid, pale yellow to pale brown. Asci are generally
long-stipitate, the spore-bearing parts 15–30 μm long, with the stipe being at least
Figure 3 (following page). Eutypa lata (BHI-F611): (a) pseudostromatal surface, showing
blackening of the overlaying surface and dome-shaped, weakly furrowed ostiolar beaks;
(b) vertical section, showing perithecia, either immature and filled with cottony white
mycelium, at left, or mature with asci and ascospores, at right, and irregular bands of melanization;
and (c) ascospores and asci, showing faintly amyloid apical apparatus. Eutypa
maura (BHI-F710): (d) pseudostromatal surface, showing darkening of the overlaying surface
and prominent, strongly furrowed ostiolar beaks; (e) vertical section, showing deeply
embedded perithecia and typical pattern of melanization, with dark zones extending downward
between the perithecia; and (f) ascospores and asci, with inamyloid apical apparatus.
Eutypella prunastri (BHI-F1007): (g) pseudostromatal surface, showing pustulate aggregations
of deeply furrowed ostiolar beaks; (h) vertical section, showing valsoid perithecial
arrangement and well-developed, white entostromatic tissues; and (i) loose ascospores and
empty ascus, showing faintly amyloid apical apparatus. Scale bars: a, g = 1000 μm; b, d, e,
h = 500 μm; and c, f, i = 10 μm.
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as long as the spore-bearing parts; with a discoid (i.e., flattened donut shaped) apical
plug non-reactive in Melzer ’s or other iodine mount (I−).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD'S END, on decorticated deciduous branch, col. Alden C.
Dirks, 26 March 2017 (FH:BHI-F710).
Notes: This specimen was on Acer wood, presumably Acer pseudoplatanus L.
(Sycamore Maple) imported from Europe as a landscaping tree. This taxon shows
a consistent preference for the wood of Acer, and is generally considered European
(Rappaz 1987). This taxon is likely found in the Boston Harbor Islands as a
colonist, a result of long commerce between the Boston Harbor and the European
continent (Banks et al. 2015, Chapman et al. 2017). It would be interesting to know
if this taxon has transitioned to using native North American Acer as hosts.
Rappaz (1987) reported a European distribution for E. maura. A search of My-
CoPortal (MyCoPortal 2020) did not result in any North American records, but
2 photo-collections are available on iNaturalist, from Prospect Park, Brooklyn
(iNaturalist 30345277) and Long Island (37539775), both in the state of New York.
These observations are unsurprising given the proximity to a large harbor with a
history of European trade, much like the Boston Harbor. While not the first report
from the US, this collection appears to be a first record from Massachusetts, and
the first from the US with a voucher.
According to Jacques Fournier (Rimont, France pers. comm.), this taxon is
most easily identified by host affinity combined with deeply immersed perithecia
under a thick layer of superficial darkened substrate, with dark coloration extending
downward between the perithecia (or, taken the other way, with pale, bleached
boundaries around each perithecium; see Fig. 3e).
Eutypella (Nitschke) Sacc., Atti Soc. Ven. Trent. Sci. Nat. 4:80 (1875) (nom. cons.)
Type species: Eutypella sorbi (Alb. & Schwein.) Sacc.
Stromata erumpent as rounded or elongate pustules in bark, with crowded perithecial
beaks, rounded to sulcate, generally united below by sometimes strongly
developed entostromatic tissue between and around perithecia. Ascospores are
allantoid, hyaline yellowish to brownish. Asci typically clavate, 8-spored, usually
long-stipitate.
Additional information: Rappaz (1987) provides useful keys to global species of
Eutypella. Glawe and Rogers (1984) provide information for the Pacific Northwest,
and Vasilyeva and Stephenson (2004) focus on the Great Smoky Mountain National
Park in the southeastern United States.
Eutypella prunastri (Pers.) Sacc. (Fig. 3g–i)
≡ Sphaeria prunastri Pers., Synopsis Methodica Fungorum, p. 37 (1801)
≡ Valsa prunastri (Pers.) Fr. (1849)
≡ Engizostoma prunastri (Pers.) Kuntze, Revisio Generum Plantarum 3(2):475
(1898)
≡ Eutypa prunastri (Pers.) L.C. Tiffany & J.C. Gilman, Iowa State College Journal
of Science 40:139 (1965)
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Stromata rounded or elongate pustules in bark, perpendicular to the axis of the
branch, up to about a centimeter long; individual or aggregated into dense clusters;
with well-defined entostromatic tissue between and around perithecia, white.
Perithecia in valsoid configuration, with ostioles individual, but emerging together
in pustules; in groups of at least 5–10, often many more and piled up in several
rows; globose to obovoid, 400–500 μm in diameter, with long neck. Ostioles are
collectively emergent (valsoid arrangement), in shared peridermal clusters, which
are prominently raised; individual ostioles rounded to conical, hardly raised above
peridermal surface, each often split 3–4 times; 150–200 μm in diameter. Ascospores
4.5–7.5 μm × 1–1.5 μm, allantoid, pale yellow to pale brown. Asci are
generally long-stipitate, the spore-bearing parts 15–30 μm long, with the stipe being
at least as long as the spore-bearing parts; with a discoid apical plug bluing very
faintly in Melzer’s or other iodine mount (I±).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, THOMPSON ISLAND, corticated hardwood log (Prunus sp.), col.
Danny Haelewaters, James K. Mitchell, Luis Quijada, 43031 (FH:B HI-F1007).
Notes: The substrate for BHI-1007 was tentatively identified as Rosaceae from the
bark characteristics, which contributed to the identification of this collection as
Eutypella prunastri. It is notable that Rappaz (1987) was uncertain whether or not
this taxon was found in North America (though he did not rule it out), and that his
description indicates a non-amyloid ascal apical plug. However, considering the
tentatively identified host family together with the combination of other features
present, there are few other possibilities for this collection. It would be worthwhile
to attempt to re-collect this fungus for attempted culturing, to further clarify which
species of Eutypella are present at the Boston Harbor Islands.
Graphostromataceae M.E. Barr, J.D. Rogers, & Y.M. Ju
Type genus: Graphostroma Piroz., Canadian Journal of Botany 52(10):2131
(1974)
Stromata effused to erumpant from bark of living or dead wood, in 2 layers (bipartite),
with the outer layer dehiscent and appressed under the bark, falling away
to reveal the inner layer, which bears the ascomata; without KOH-extractable
pigments. Ascospores unicellular, allantoid and hyaline (as in Graphostroma) to
brown and ellipsoid (as in Biscogniauxia), at times with appendages, with or without
germ slits, without dehiscent perispores. Asci oblong to cylindrical.
Additional information: Ju et al. (1998) provides an excellent monographic
treatment of Biscogniauxia; Laessøe et al. (1989) treats many taxa that were later
combined into the Graphostromataceae, including the genus Camillea; Barr et al.
(1993) was responsible for erecting the family; and Graphostroma platystomum is
treated with the Diatrype in Vasilyeva and Stephenson (2004).
Biscogniauxia Kuntze
Type species: Biscogniauxia nummularia (Bull.) Kuntze
Stromata applanate, effused-pulvinate, rarely discoid-raised, bipartite with dehiscent
outer layer, with carbonaceous tissue immediately beneath surface, and
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without KOH-extractable pigments. Ascospores unicellular, pale brown to dark
blackish brown, sometimes mature cells with a hyaline cellular appendage, typically
ellipsoid inequilateral to equilateral, with (or rarely, without) a straight or
sigmoid germ slit. Asci 8-spored, cylindrical, short-stipitate, with a discoid apical
plug, amyloid or infrequently inamyloid.
Additional information: See Ju et al. (1998) for an excellent monographic treatment
of Biscogniauxia.
Biscogniauxia mediterranea (De Not.) Kuntze (Fig. 4g–h)
≡ Sphaeria mediterranea De Not., Memorie della Reale Accademia delle Scienze
di Torino Ser. 2, 13:96, t. 2 (1851)
≡ Nummularia mediterranea (De Not.) Sacc., Sylloge Fungorum 1:400 (1882)
≡ Biscogniauxia mediterranea var. mediterranea, Revisio generum plantarum
2:398 (1891)
≡ Nummularia regia var. mediterranea (De Not.) Traverso, Flora Italica Cryptogama.
Pars 1: Fungi. Pyrenomycetae. Xylariaceae, Valsaceae, Ceratostomataceae
1(1):59 (1906)
≡ Numulariola mediterranea (De Not.) P.M.D. Martin, South African Journal of
Botany 35:312 (1969)
Stromata bipartite, with an outer dehiscent layer that is shed with the bark at
maturity to expose the inner, fertile layer of the stromata; applanate, tightly appressed
to substrate; up to several centimeters in diameter, and more or less 1 mm
thick; surface black when mature, with the outer dehiscent layer dark brown, ~0.5
mm thick; tissue beneath perithecia inconspicuous, tissue around perithecia black,
carbonaceous, and extremely hard and brittle; without KOH-extractable pigments.
Perithecia are tubular, densely packed at the stromatal surface such that they often
become laterally flattened, 0.1–0.2 mm in diameter and up to 1 mm tall, with
coarsely papillate ostioles raised above the stromatal surface. Ascospores are
15.5–21 μm × 7–10 μm, brown to dark brown, nearly equilateral, with narrowly to
infrequently broadly rounded ends, and straight hyaline germ slit, spore-length or
Figure 4 (following page). Camillea punctulata (BHI-F699): (a) stromatal surface with
margin, showing the bipartite structure and characteristic development underneath the
bark; (b) close up of stromatal surface, showing the punctulate ostiolar openings for which
this taxon is named; and (c) ascospores inside of an ascus, showing characteristic asymmetrically
rectangular-ellipsoid ascospores with one attenuated end, as well as the strongly
amyloid apical apparatus. Graphostroma platystomum (BHI-F503): (d) stromatal surface
with margin, showing the bipartite structure and characteristic development underneath the
bark; (e) close up of stromatal surface, showing the elevated, wide-open discoid ostiolar
openings; and (f) ascospores and asci, showing the nearly colorless ascospores and faintly
amyloid apical apparatus. Biscogniauxia mediterranea (BHI-F064): (g) stromatal surface
with margin, showing the bipartite structure and relatively thick upper layer; and (h) close
up of stromatal surface, showing the distinctly papillate ostioles. Biscogniauxia mediterranea
var. macrospora (BHI-F303): (i) ascospores, which are much much larger than the
typical variety, and the primary morphological difference between the 2 varieties. Scale
bars: a, d = 2000 μm; b, e, h = 1000 μm; and c, f, i = 10 μm.
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nearly so. Asci are extremely short-stipitate, the spore-bearing parts 120–150 μm
long, the stipes generally only 20–35 μm; with a discoid apical plug, wider than it
is tall, 4–5 μm × 2–3 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on wood, col. Danny Haelewaters, 29 September
2013 (FH:BHI-F064).
Notes: I was only able to recover a few ascospores from BHI-F064, but they are
clearly in the size range provided by Ju et al. (1998) for this taxon, and quite
distinctly smaller than those recovered from BHI-F303 (i.e., Fig. 4i), which was
otherwise a nearly identical specimen.
Biscogniauxia mediterranea var. macrospora (J.H. Mill.) Y.M. Ju & J.D. Rogers
(Fig. 4i)
≡ Hypoxylon mediterraneum var. macrosporum J.H. Mill., A Monograph of the
World Species of Hypoxylon, p. 118 (1961)
Stromata bipartite, with an outer dehiscent layer that is shed with the bark at
maturity to expose the inner, fertile layer of the stromata; applanate, tightly appressed
to substrate; up to several centimeters in diameter, and more or less 1 mm
thick; surface black when mature, with the outer dehiscent layer dark brown, ~0.5
mm thick; tissue beneath perithecia inconspicuous, tissue around perithecia black,
carbonaceous, and extremely hard and brittle; without KOH-extractable pigments.
Perithecia are tubular, densely packed at the stromatal surface such that they often
become laterally flattened, 0.1–0.2 mm in diameter and up to 1 mm tall, with
coarsely papillate ostioles raised above the stromatal surface. Ascospores are
20–26 μm × 11.5–13 μm, brown to dark brown, nearly equilateral, with narrowly
to infrequently broadly rounded ends, and straight hyaline germ slit, spore-length
or nearly so. Asci are extremely short-stipitate, the spore-bearing parts 120–150 μm
long, the stipes generally only 20–35 μm; with a discoid apical plug, wider than it
is tall, 4–5 μm × 2–3 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, WORLD’S END, on stump/trunk of Quercus sp., col. Danny
Haelewaters, Lara A. Kappler, 29 May 2015 (FH:BHI-F303).
Notes: Biscogniauxia mediterranea is quite widespread in the United States, with
collections authenticated by Ju et al. (1998) ranging from Alabama to New York,
though Indiana and Wisconsin, all the way west to California and Oregon. In contrast,
B. mediterranea var. macrospora has only been rarely reported, and this may
be the first record for the northeastern part of the US.
Camillea Fr.
Type species: Camillea leprieurii (Mont.) Mont.
Stromata variable in shape from applanate or effused-pulvinate to upright, erumpent
from bark, always bipartite with dehiscent outer layer, extremely carbonaceous
throughout, and without KOH-extractable pigments. Ascospores unicellular,
almost colorless pale yellow to pale brown, rectangular-ellipsoid to fusiform,
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generally inequilateral, at times strongly attenuated at one end, with a pointed apex,
without germ slits or pores, but with intricate poroid, reticulate, or echinate orientation
visible by SEM. Asci 8-spored, cylindrical, with a discoid to rhomboid apical
plug staining blue in iodine reagents (I+).
Additional information: Laessøe et al. (1989) treats many taxa that were later
combined into the Graphostromataceae, including the genus Camillea.
Camillea punctulata (Berk. & Ravenel) Læssøe, J.D. Rogers, & Whalley (Fig.
4a–c)
≡ Diatrype punctulata Berk. & Ravenel, Grevillea 4(31):94 (1876)
≡ Nummularia punctulata (Berk. & Ravenel) Sacc., Sylloge Fungorum 1:399
(1882)
≡ Hypoxylon punctulatum (Berk. & Ravenel) Cooke, Grevillea 11(60):138 (1883)
≡ Numulariola punctulata (Berk. & Ravenel) P.M.D. Martin, South African Journal
of Botany 35:288 (1969)
≡ Numulariola punctulata (Berk. & Ravenel) P.M.D. Martin, South African Journal
of Botany 42:8 (1976)
Stromata bipartite, with an outer dehiscent layer that is shed with the bark at maturity
to expose the inner, fertile layer of the stromata; applanate, tightly appressed
to substrate; up to 3 cm in diameter, and more or less 1 mm thick; surface dark
brown to black when mature, sometimes with red to purple tones; the outer dehiscent
layer blackish, ~0.1–0.2 mm thick; tissue beneath perithecia inconspicuous,
tissue around perithecia shiny black, carbonaceous, and extremely hard and brittle;
without KOH-extractable pigments. Perithecia are tubular, densely packed at the
stromatal surface such that they often become laterally flattened, 0.2–0.3 mm in
diameter and up to 1 mm tall, with ostioles finely pitted, umbilicate. Ascospores
are 7–9 μm × 3–4 μm, rectangular–ellipsoid, inequilateral, with one attenuated
end forming a pointed lower apex; nearly colourless, pale yellow to light brown,
without germination slits, but often with fine ornamentation visible by SEM. Asci
are extremely short-stipitate, the spore-bearing parts 50–70 μm long, the stipes
generally only half the length of the spore-bearing parts; with a large dome-shaped
apical plug, conspicuously widest in the center, and taller than it is wide, 3–3.5 μm
× 2–2.5 μm, strongly blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on corticated branch, col. Danny Haelewaters, 29
September 2013 (FH:BHI-F122); THOMPSON ISLAND, on dead oak log, col.
Zachary Chaves, Lawrence Millman, James K. Mitchell, Joe Warfel, 29 October
2016 (FH:BHI-F699); GRAPE ISLAND, bark of oak log, col. Lara A. Kappler,
James K. Mitchell, 3 May 2017 (FH:BHI-F870).
Notes: Known from both North and Central America, this taxon seems to have a
substrate preference for Quercus spp. (Laessøe et al. 1989). Although I could not
confirm substrate identity for the collections here, BHI-F870 was collected on
Grape Island where the only possible substrate is Quercus velutina Lam. (Balck
Oak; Elliman 2005).
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Graphostroma Piroz.
Type species: Graphostroma platystomum (Schwein.) Piroz.
Stromata applanate, effused-pulvinate, bipartite with dehiscent outer layer, with
dark pithy to wood tissue immediately beneath surface, wide discoid ostioles,
and without KOH-extractable pigments. Ascospores unicellular, nearly colorless,
allantoid to suballantoid, without a germ slit or pore. Asci clavate, 8-spored, shortstipitate,
with a faint, amyloid discoid apical plug.
Additional information: Barr et al. (1993) was responsible for erecting the family;
Graphostroma platystomum is treated with the Diatrype in Vasilyeva and Stephenson
(2004).
Graphostroma platystomum (Schwein.) Piroz. (Fig. 4d–f)
≡ Sphaeria platystoma Schwein., Schriften der Naturforschenden Gesellschaft zu
Leipzig 1:31 (1822)
≡ Diatrype platystoma (Schwein.) Berk., Grevillea 4(31):95 (1876)
Stromata bipartite, with an outer dehiscent layer that is shed with the bark at maturity
to expose the inner, fertile layer of the stromata; indefinitely effuse, applanate,
tightly appressed to substrate; up to several centimeters in diameter, sometimes
entirely encircling smaller substrates, and more or less 1 mm thick; often with
horizontal fissures through stromata, perpendicular to the long axis of the substrate;
surface dark chocolate brown when mature, but often appearing like black velvet
as a result of the tightly crowded, large discoid ostiolar openings; with the outer
dehiscent layer dark brown, less than 0.5 mm thick; tissue beneath perithecia inconspicuous;
tissue around perithecia black, pithy to woody, and extremely brittle in age;
without KOH-extractable pigments. Perithecia are globose to spherical, but often
compressed due to crowding as the perithecia are densely packed, 0.2–0.4 mm in
diameter and up to 0.2 mm tall, with short, wide, disc-shaped perithecial beaks
extending above the stromatal surface, with wide open ostioles giving the surface
of the stromata the appearance of a platter of donuts when magnified. Ascospores
are (6–) 7–10 μm × 1–2 μm, with tapered ends; colorless, suballantoid to allantoid,
somewhat inequilateral, looking nearly diatrypaceous. Asci are extremely shortstipitate,
nearly sessile, the spore-bearing parts 30–40 μm long; with a faint, disciod
apical plug, wider than it is tall, 4–5 μm × 2–3 μm, blueing in Melzer’s or other
iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on dead deciduous branch, col. Alden C. Dirks,
Jasmin J. Camacho, Michal Gorczak, Danny Haelewaters, James K. Mitchell, 11
December 2016 (FH:BHI-F503); WORLD’S END, on dead deciduous branch, on
corticated parts only, col. Danny Haelewaters, 26 March 2017 (FH:BHI-F742).
Notes: There has been disagreement over the placement of Graphostroma platystomum
for some time, with some authors placing it in the Xylariaceae based on the
nodulisporium-type anamorph (e.g., Pirozynski 1974), and others in the Diatrypaceae,
primarily based on the ascospore morphology (e.g., Vasilyeva and Stephenson
2004). The Graphostromataceae was eventually erected as a monotypic family to
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accommodate this strange, monotypic genus with clear affinities to both the Xylariaceae
and the Diatrypaceae (Barr et al. 1993). Recent multi-gene phylogenetic efforts
(Daranagama et al. 2018, Wendt et al. 2018) seem to confirm closer affinities with
the Xylariaceae sensu lato, and placement of Graphostroma sister to the Biscogniauxia
and Camillea, among others. Wendt et al. (2018) brought other genera from
the Xylariaceae sensu lato into Graphostromataceae (including both Biscogniauxia
and Camillea) based on the strength of these phylogenetic results and similarities
in anamorph forms (Graphostromataceae characteristically have xylocladium- or
periconiella-type anamorphs), noting that the presence of bipartite stromata united
the family, despite great divergence in spore morphology across genera.
Hypoxylaceae DC.
Type genus: Hypoxylon Bull.
Stromata variable, from erect to effused-pulvinate, variously colored or more frequently
blackish, waxy or carbonaceous tissue immediately beneath surface and between
perithecia, with or without KOH-extractable pigments. Ascospores unicellular,
pale brown to dark blackish brown, typically ellipsoid inequilateral, typically
with a hyaline germ slit. Asci 8-spored, cylindrical, stipitate, with a discoid apical
plug, amyloid or infrequently inamyloid, sometimes lacking, broader than it is tall.
Additional information: The family was resurrected by Wendt et al. (2018), which
provides current circumscription; global keys for taxa previously considered Hypoxylon
(including Annulohypoxylon, Jackrogersella, and Hypomontagnella) are
available in the monograph by Ju and Rogers (1998), while the earlier monograph
by Miller (1961) is still the best place to find descriptions and illustrations of some
taxa; an excellent monograph of the genus Daldina by Stadler et al. (2014b) provides
keys and descriptions for that genus.
Annulohypoxylon Y.M. Ju, J.D. Rogers, & H.M. Hsieh
Type species: Annulohypoxylon truncatum (Starbäck) Y.M. Ju, J.D. Rogers, &
H.M. Hsieh
Stromata spherical to applanate or effused-pulvinate, often convergent into a crust,
with carbonaceous stromatal material surrounding individual perithecia present,
stromatal surface typically blackish at maturity, ostioles always papillate (though
sometimes minutely), encircled with an annulate disc, and with or without KOHextractable
pigments. Ascospores unicellular, pale brown to dark blackish brown,
typically ellipsoid inequilateral to equilateral, with (or rarely, without) a straight,
sigmoid, or spiral germ slit. Asci 8-spored, cylindrical, stipitate, with a discoid apical
plug, amyloid or infrequently inamyloid, sometimes lacking.
Additional information: The genus Annulohypoxylon was segregated from Hypoxylon
by Hsieh et al. (2005); global keys for (as Hypoxylon sect. Annulata) are
available in the monograph by Ju and Rogers (1998), while the earlier monograph
by Miller (1961) is still the best place to find some descriptio ns and illustrations.
Annulohypoxylon annulatum (Schwein.) Y.M. Ju, J.D. Rogers, & H.M. Hsieh (Fig.
5a–d)
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≡ Sphaeria annulata Schwein., Journal of the Academy of Natural Sciences Philadelphia
5:11 (1825)
≡ Hypoxylon annulatum (Schwein.) Mont., Historia Física y Política de Chile. Botánica.
Flora Chilena 7:445 (1850)
= Sphaeria marginata Schwein., Transactions of the American Philosophical Society
4(2):190 (1832)
= Hypoxylon marginatum (Schwein.) Berk., Outlines of British Fungology, p. 387
(1860)
= Hypoxylon vernicosum Ellis & Everh., American Naturalist 31:426 (1897)
= Hypoxylon marginatum var. emarginata Theiss., Annales Mycologici 7(2):156
(1909)
= Hypoxylon circumscribum Lloyd, Mycological Writings 7 (Letter 73):1312
(1924)
Stromata pulvinate to hemispherical, with inconspicuous perithecial mounds; up
to 2 cm in diameter, and as much as 0.5 cm in thickness; surface blackish when
mature, at times showing brown to olivaceous tones; tissue beneath perithecia
massive, dark brown to black, woody or carbonaceous in texture, without any
concentric zonation whatsoever, though radial texture may be apparent; with
KOH-extractable pigments greenish olivaceous to dull green. Perithecia spherical
to obovoid, 0.3–0.5 mm in diameter, often slightly higher than broad; with a layer
of carbonaceous stromatal material surrounding individual perithecia. Ostioles
distinctly conical-papillate, shiny; surrounded by a convex, “truncatum”-type disc,
up to 0.5 mm in diameter. Ascospores are 7.5–11 μm × 3.5–5 (–6) μm, brown to
dark brown, ellipsoid-inequilateral, with narrowly rounded ends, and a straight
hyaline germ slit, spore-length or nearly so, on the more curved side. Asci are shortstipitate,
the spore-bearing parts 67–80 μm long, the stipes at least half as long as
Figure 5 (following page). Annulohypoxylon annulatum (BHI-F024): (a) stromatal habit,
showing the hemispherical shape and inconspicuous perithecial mounds; (b) stromatal
surface texture, clearly showing the “truncatum”-type annualate discs and papillate ostioles;
(c) vertical section of stromata, showing the globose perithecia and lack of internal
concentric zones (note the radial texture, however); and (d) ascospores and asci, with
discoid amyloid apical apparatus. Daldinia childiae (BHI-F416): (e) close-up of stromata,
showing clavate shape with broad stipe and distinct boundary of fertile (perithecial) region;
(f) vertical section of stromata, showing the densely packed, tubular perithecia and internal
concentric zonation; and (g) ascospores and asci, with discoid amyloid apical apparatus,
from a collection with intact asci (BHI-F367). Hypomontagnella submonticulosum (BHIF609):
(h) close up of stromatal surface with vertical section, showing slightly compressed
globose perithecia, dark rusty-brown surface color, and distinctly papillate ostioles; and
(i) ascospores showing narrowly rounded to acute ends; this material did not have intact
asci. Jackrogersella multiforme: (j) close up of stromatal surface with vertical section,
showing obvoid perithecia slightly higher than broad, blackish brown surface color, distinctly
papillate ostioles, and a conspicuous layer of fungal tissue beneath the perithecia;
and (k) ascospores showing narrowly rounded ends and less than spore-length germ slits;
this material did not have intact asci. Scale bars: a, c, e–f, h, j = 1000 μm; b = 500 μm; and
d, g, i, k = 10 μm.
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the spore-bearing parts; with a discoid apical plug, wider than it is tall, ~1.5–2 μm
× 0.5 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on corticated fallen branch, col. Danny Haelewaters,
Kevin Healy, Rosanne Healy, Sarah Verhaeghen, 14 September 2013 (FH:BHIF024);
WORLD’S END, decorticated and corticated sections of hardwood log, col.
Danny Haelewaters, James K. Mitchell, Luis Quijada, 43014 (FH:B HI-F941).
Notes: This taxon is very similar to Annulohypoxylon truncatum (Schwein.) Y.M.Ju,
which is known from the southern United States and Mexico. Annulohypoxylon truncatum
is easily distinguished by its thin, effused-pulvinate stromata, rather than the
massive, hemispherical stromata of A. annulatum (Ju and Rogers 1996).
Daldinia Ces. & De Not.
Type species: Daldinia concentrica (Bolton) Ces. & De Not.
Stromata spherical to turbinate, either sessile or stipitate, the tissue below the perithecial
layer concentrically zoned, with alternating light and dark regions, pithy to
woody, with or without KOH-extractable pigments. Ascospores unicellular, pale
brown to dark brown, typically ellipsoid inequilateral to equilateral, with a sporelength
straight to slightly sigmoid germ slit generally on the more convex side of the
spore. Asci 8-spored, cylindrical, stipitate, with a discoid apical plug, amyloid (I+).
Additional information: An excellent monograph of the genus Daldina by Stadler
et al. (2014b) provides keys and descriptions for this genus.
Daldinia childiae J.D. Rogers & Y.M. Ju (Fig. 5e–g)
= Daldinia concentrica (Bolton: Fr.) Ces. & De Not. f. intermedia C.G. Lloyd,
Mycological Writings 5, Large Pyrenomycetes, p. 24. 1919.
Stromata spherical to turbinate, with a constricted base or short, wide stipe; interior
tissues concentrically zoned, with alternating layers of pale grey-brown with darker
blackish-brown layers, 0.5–1 mm thick, with pithy or woody texture; perithecial
contours typically inconspicuous, though at times showing through clearly; up to
several centimeters in diameter, though typically broader than tall; may be confluent
or aggregated, though more typically solitary and scattered; surface dark brown
to sepia, becoming blackish in age, as the outer surface wears away to reveal the
harder, more carbonized tissue beneath; KOH-extractable pigments pale grey-yellow
or parchment, ranging through amber to a warm cinnamon brown. Perithecia
are tubular, densely packed at the stromatal surface, 0.3–0.5 mm in diameter and up
to 1.5 mm tall, with slightly papillate ostioles. Ascospores are 12–16 μm × 5.5–7.5
μm, brown to dark brown, ellipsoid-inequilateral, with narrowly rounded ends, and
a straight hyaline germ slit, spore-length, on the more curved side. Asci are shortstipitate,
the spore-bearing parts 80–100 μm long, the stipes generally less than half
as long the spore-bearing parts; with a disciod apical plug, wider than it is tall, ~3
μm × 0.5 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, PEDDOCKS ISLAND, on base of corticated stump, col. Danny
Haelewaters, 7 September 2013 (FH:BHI-F004); WORLD’S END, on wood, col.
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Danny Haelewaters, 29 September 2013 (FH:BHI-F102); PEDDOCKS ISLAND,
on bark of deciduous log, col. Lara A. Kappler, 17 July 2015 (FH:BHI-F367); PEDDOCKS
ISLAND, on bark of dead, deciduous tree trunk, col. Lara A. Kappler, 17
July 2015 (FH:BHI-F372); THOMPSON ISLAND, on corticated dead deciduous
wood, col. Danny Haelewaters, Lara A. Kappler, 18 August 2015 (FH:BHI-F416);
PEDDOCKS ISLAND, on decorticated fallen log, col. Danny Haelewaters, Sarah
Verhaeghen, 30 May 2015 (FH:BHI-F313); PEDDOCKS ISLAND, on wood, col.
Danny Haelewaters, Lawrence Millman, Joseph Warfel, 29 August 2015 (FH:BHIF452);
PEDDOCKS ISLAND, on wood, col. Danny Haelewaters, Lawrence Millman,
Joseph Warfel, 29 August 2015 (FH:BHI-F465).
Notes: This cosmopolitan taxon is by far the most common Daldinia in the United
States, and for decades has been consistently confused with D. concentrica, which
is strictly European in distribution (Stadler et al. 2014b).
Hypomontagnella Sir, L. Wendt, & C. Lambert
Type species: Hypomontagnella monticulosa (Mont.) Sir, L. Wendt, & C. Lamb
Stromata are much as in Hypoxylon, but differ in having a woody to carbonaceous
stromatal interior without colored granules; with minutely papillate ostioles, sometimes
surrounded by a black annulate disc; and without apparent KOH-extractable
pigments in mature stromata. Ascospores unicellular, pale brown to dark blackish
brown, typically ellipsoid inequilateral to equilateral, with (or rarely, without) a
straight, sigmoid, or spiral germ slit; spores are differentiated from those of Annulohypoxylon
and Jackrogersella by the smooth or transversally striate perispores.
Asci 8-spored, cylindrical, stipitate, with a discoid apical plug, amyloid or infrequently
inamyloid, sometimes lacking.
Additional information: The genus Hypomontagnella was segregated from Hypoxylon
by Lambert et al. (2019), which includes excellent illustrations and keys to
accepted taxa and, importantly, morphologically similar taxa.
Hypomontagnella submonticulosa (Y.-M. Ju & J.D. Rogers) Sir, L. Wendt, & C.
Lambert (Fig. 5h–i)
≡ Hypoxylon submonticulosum Y.-M. Ju & J.D. Rogers, Mycologia Memoirs
20:189 (1996)
Stromata applanate to effused-pulvinate, with mostly inconspicuous perithecial
mounds, though some deeper folds and clefts present; up to several centimeters in
diameter, and as much as 0.7 cm in thickness; surface dark rusty brown to blackish;
with hardly any tissue beneath perithecia; tissues surrounding perithecia
blackish, woody or carbonaceous in texture; without apparent KOH-extractable
pigments. Perithecia globose, 0.3–0.6 mm in diameter; without a layer of carbonaceous
stromatal material surrounding individual perithecia. Ostioles minutely
conical-papillate; not surrounded by an annular disc. Ascospores are 9–12 (–13.5)
μm × 4–5 μm, light brown to brown, ellipsoid-inequilateral, with narrowly to infrequently
broadly rounded ends, and a straight to slightly oblique hyaline germ
slit, notably less than spore-length. Asci are short-stipitate, the spore-bearing parts
75–100 μm long, the stipes generally two-thirds to three-quarters as long as the
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spore-bearing parts; with a discoid apical plug, wider than it is tall, ~3 μm × 2 μm,
blueing in Melzer’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on wood, col. Danny Haelewaters, 29 September
2013 (FH:BHI-F060); WORLD’S END, on disintegrating stump of old deciduous
tree, col. Danny Haelewaters, Lara A. Kappler, 29 May 2015 (FH:BHI-F308);
GREAT BREWSTER ISLAND, on dead decomposing log, col. Lara A. Kappler, 8
March 2017 (FH:BHI-F609).
Notes: Young stromata may have purple KOH-extractable pigments, disappearing
in age. This taxon is the temperate counterpart to the more tropical
Hypomontagnella monticulosa, which has darker, more obviously inequilateral
ascospores, and a spore-length germ slit (Ju and Rogers 1996). The perithecial
diameters of these collections are slightly larger than those reported by Ju and
Rogers (Ju and Rogers 1996).
Hypoxylon Bull.
Type species: Hypoxylon fragiforme (Pers.) J. Kickx f.
Stromata spherical to applanate or effused-pulvinate, often convergent into a crust,
carbonaceous stromatal material surrounding individual perithecia absent, stromatal
surface colored to blackish at maturity, ostioles usually umbilicate (though
sometimes minutely papillate), never encircled with an annulate disc, and with or
without KOH-extractable pigments. Ascospores unicellular, pale brown to dark
blackish brown, typically ellipsoid inequilateral to equilateral, with (or rarely,
without) a straight, sigmoid, or spiral germ slit. Asci 8-spored, cylindrical, stipitate,
with a discoid apical plug, amyloid or infrequently inamyloid, sometimes lacking.
Additional information: Global keys (as Hypoxylon sect. Hypoxylon, including
many taxa that have since been segregated out of this genus) are available in the
monograph by Ju and Rogers (1998), while the earlier monograph by Miller (1961)
is still the best place to find some descriptions and illustrati ons.
Hypoxylon cf. lenormandii Berk. & M.A. Curtis
= Hypoxylon oodes Berk. & Broome, J. Linn. Soc., Bot. 14:122. 1873 (sensu Miller
1961)
Stromata effused-pulvinate, with conspicuous to very conspicuous perithecial
mounds, at times appearing almost rosellinioid, but always with perithecial mounds
connected by a thin layer of stromatal tissue; up to 3 cm in diameter, but only ~1
mm thick; surface dark grey-brown to purple-brown; with hardly any tissue beneath
perithecia; tissues surrounding perithecia blackish, woody or carbonaceous
in texture, with dull ochre apparent immediately beneath the surface; with KOHextractable
pigments warm yellow-brown or cinnamon ranging to dark rusty brown
or ocher. Perithecia globose to spherical, 0.4–0.6 mm in diameter; without a layer
of carbonaceous stromatal material surrounding individual perithecia. Ostioles
minutely conical-papillate; not surrounded by an annular disc. Ascospores are
9.5–15(–16) μm × 4–6.5(–7) μm, brown to dark brown, ellipsoid-inequilateral, with
narrowly rounded ends, and a slightly sigmoid hyaline germ slit, spore-length. Asci
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are short-stipitate, the spore-bearing parts 70–100 μm long, the stipes generally half
as long as the spore-bearing parts; with a discoid apical plug, wider than it is tall,
~2.5 μm × 1 μm, blueing in Melzer ’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, PEDDOCKS ISLAND, on wood, col. Zachary Chaves, 24 September
2016 (FH:BHI-F679).
Notes: This collection was in poor condition, but the combination of available
features (ascospore morphology, KOH-extractable pigments, stromatal surface
texture and color) all point to Hypoxylon lenormandii. This taxon can be easily confused
with some members of the H. rubiginosum (Pers.: Fr.) Fr. species complex,
however, which is more common; H. rubiginosum can be distinguished by having
umbilicate ostioles, inconspicuous perithecial contours, and a distinctly straight
germ slit (reference). Hypoxylon lenormandii is typically tropical or subtropical
in distribution (Ju and Rogers 1996), so more investigation—including the use of
HPLC-MS chemotaxonomic approaches (Stadler et al. 2004a)—may be warranted
to confirm the presence of this taxon at the Boston Harbor Islan ds.
Jackrogersella L. Wendt, Kuhnert, & M. Stadler
Type species: Jackrogersella multiformis (Fr.) L. Wendt, Kuhnert & M. Stadler
Stromata differ from Annulohypoxylon priciply by containing cohaerin/multiformin
type azaphilones as predominant stromatal pigments; typically without
annulate discs surrounding the ostiole. Ascospores unicellular, pale brown to dark
blackish brown, typically ellipsoid inequilateral to equilateral, with (or rarely,
without) a straight, sigmoid, or spiral germ slit. Asci 8-spored, cylindrical, stipitate,
with a discoid apical plug, amyloid or infrequently inamyloid, sometimes lacking.
Additional information: The genus Jackrogersella was segregated from Annulohypoxylon
by Wendt et al. (2018) as part of the resurrection of the Hypoxylaceae;
the genus encompasses those previous Annulohypoxylon species that have papillate
ostioles and lack conspicuous ostiolar disks, though they are also defined by
unique pigment chemistry. Wendt et al. (2018) has lists of accepted taxa and keys
to species, and there are aditional keys (under Hypoxylon sect. Annulata) in the
monograph by Ju and Rogers (1998).
Jackrogersella multiformis (Fr.) L. Wendt, Kuhnert, & M. Stadler (Fig. 5j–k)
≡ Sphaeria multiformis Fr., Observationes mycologicae 1:169 (1815)
≡ Hypoxylon multiforme (Fr.) Fr., Summa vegetabilium Scandinaviae 2:384 (1849)
≡ Annulohypoxylon multiforme (Fr.) Y.M. Ju, J.D. Rogers & H.M. Hsieh, Mycologia
97(4):859 (2005)
= Hypoxylon granulosum Bull., Histoire des champignons de la France I:176, t.
487:2 (1791)
= Sphaeria rubiformis Pers., Annalen der Botanik (Usteri) 11:20 (1794)
= Sphaeria rubiformis var. effusa Pers., Neues Magazin für die Botanik 1:82 (1794)
= Sphaeria pulvinata R. Hedw., Observ. Bot., pl. 8, fig. A (1802)
= Sphaeria granulosa (Bull.) Sowerby, Coloured Figures of English Fungi 3, pl.
355 (1803)
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= Sphaeria cinereofusca Schumach., Enumeratio Plantarum, in Partibus Sællandiae
Septentrionalis et Orientalis Crescentium 2:164 (1803)
= Sphaeria crustacea Sowerby, Coloured Figures of English Fungi 3, tab. 372, fig.
11 (1803)
= Sphaeria peltata DC. & Lam., Flore Française 2:287 (1805)
= Sphaeria deusta Wahlenb., Flora Lapponica, No. 995 (1812)
= Peripherostoma granulosum (Bull.) Gray, A Natural Arrangement of British
Plants 1:514 (1821)
= Nemania crustacea (Sowerby) Gray, A Natural Arrangement of British Plants
1:517 (1821)
= Stromatosphaeria elliptica Grev., Flora Edinensis, p. 357 (1824)
= Sphaeria rubiginosa Spreng., Caroli Linnaei Systema Vegetabilium 4(1):385
(1827)
= Sphaeria corrugata Fr., Elenchus Fungorum 2:70 (1828)
= Sphaeria transversa Schwein., Transactions of the American Philosophical Society
4(2):191 (1832)
= Hypoxylon corrugatum (Fr.) Fr., Summa Vegetabilium Scandinaviae 2:384 (1849)
= Hypoxylon crustaceum (Sowerby) Nitschke, Pyrenomycetes Germanici 1:49
(1867)
= Hypoxylon multiforme var. effusum (Pers.) Cooke & Ellis, Grevillea 5(33):33
(1876)
= Hypoxylon transversum (Schwein.) Sacc., Sylloge Fungorum 1:391 (1882)
= Hypoxylon multiforme var. granulosum (Bull.) Sacc., Sylloge Fungorum 1:364
(1882)
= Hypoxylon hookeri Berk. ex Cooke, Grevillea 11(60):129 (1883)
= Rosellinia callimorpha P. Karst., Hedwigia 23:84 (1884)
= Hypoxylon granulosum var. luxurians Rehm, Annales Mycologici 3(3):229
(1905)
= Hypoxylon multiforme var. luxurians (Rehm) Sacc. & Trotter, Sylloge Fungorum
22:314 (1913)
= Hypoxylon callimorphum (P. Karst.) P.M.D. Martin, South African Journal of
Botany 33:325 (1967)
= Hypoxylon callimorphum (P. Karst.) P.M.D. Martin, South African Journal of
Botany 42(1):72 (1976)
Stromata peltate, at least in part, often aggregated into a crust, with mostly inconspicuous
perithecial mounds; up to 4 cm in diameter, and as much as 0.7 cm
in thickness; surface dark brown to blackish brown when mature; with significant
tissue beneath perithecia, blackish, woody or carbonaceous in texture; with KOHextractable
pigments olivaceous to greenish olivaceous, rarely apricot to sienna.
Perithecia obovoid, 0.4–0.7 mm in diameter, slightly higher than broad; with a layer
of carbonaceous stromatal material surrounding individual perithecia. Ostioles
conical-papillate; not surrounded by an annular disc. Ascospores are 8.5–12 μm
× 3.5–5 μm, light brown to brown, ellipsoid-inequilateral, with narrowly rounded
ends, and a straight hyaline germ slit, notably less than spore-length, on the more
curved side. Asci are long-stipitate, the spore-bearing parts 70–80 μm long, the
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stipes generally slightly longer than the spore-bearing parts; with a discoid (i.e.,
flattened donut shaped) apical plug, wider than it is tall, ~2 μm × 1 μm, blueing in
Melzer’s or other iodine mount (I+).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, PEDDOCKS ISLAND, on wood, col. Danny Haelewaters, Lawrence
Millman, Joseph Warfel, 29 August 2015 (FH:BHI-F464).
Notes: The genus Jackrogersella was segregated from Annulohypoxylon relatively
recently (Wendt et al. 2018), primarily on the basis of the presence of a unique
class of pigment chemicals, cohaerin/multiformin type azaphilones combined with
phylogenetic placement. Interestingly, most members of this clade are also easily
separated from Annulohypoxylon s. str. by the notable absence of an annular disc.
The ITS sequence generated for this collection (GenBank acc. no. MF161278) from
the checklist effort (Haelewaters et al. 2018) appears to belong instead to a Cosmospora
or other Hypocrealean parasite of Xylarialean fungi.
Lopadostomataceae Daranag. & K.D. Hyde [as “Lopadostomaceae”]
Type genus: Lopadostoma (Nitschke) Traverso
Stromata immersed to erumpent, present as blisters or pustules under the bark,
or as coalescent masses with abrupt margins (in Creosphaeria), typically multiperitheciate,
in a single layer or multiple layers, with perithecia clustered, with
either long ostiolar necks or ostiolar canal lined with pale tissue (in Creosphaeria).
Ascospores unicellular, pale brown to dark blackish brown, typically ellipsoid
equilateral, with a spore-length germ slit. Asci 4- or 8-spored, cylindrical, stipitate,
with an amyloid apical apparatus.
Additional information: The family was erected by Senanayake et al. (2015) to
accommodate Lopadostoma and Creosphaeria. Læssøe and Spooner (1994), Rappaz
(1995) and Lu and Hyde (2000) each have useful keys to morphologically
similar genera, including Anthostoma, Anthostomella, Lopadostoma, and others.
Lopadostoma (Nitschke) Traverso
Type species: Lopadostoma turgidum (Pers.) Traverso
Stromata pustulate to widely effused, immersed, erumpent from bark, containing
1 to several groups of subglobose or flask-shaped perithecia, each group clustered
in a valsoid arrangement, with long ostiolar necks converging on a discrete, darkbrown
to black ectostromatic disc. Ascospores unicellular, pale brown to dark
blackish brown, typically ellipsoid equilateral, with a spore-length germ slit. Asci
8-spored, cylindrical, stipitate, with an amyloid apical apparatus.
Additional information: The genus Lopadostoma was revised by Jaklitsch et al.
(2014), who provide excellent keys and illustrations.
Lopadostoma cf. americanum Jaklitsch, J. Fourn., J.D. Rogers, & Voglmayr (Fig.
6a–d)
Stromata immersed in bark, pustulate-erumpent, typically multiperitheciate, either
scattered or in small groups, 2–3 mm in diameter, but may appear larger when occurring
in groups; with a black, flat to convex, circular ectostromatic disc emerging
above the bark; delimited from surrounding bark by a black carbonized line; tissue
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around and beneath the perithecia composed of un-altered substrate mixed with fungal
tissue, sometimes with white mycelium visible throughout. Perithecia arranged
in a valsoid configuration, 6–12 per stromata, typically all in 1 layer, but rarely
with some below in large stromata; subglobose to globose, at times compressed
when pressed together; 0.4–0.9 mm diam, with long converging ostiolar necks,
opening at the ectostromatic disc. Ascospores are (8.2–)9.2–11.5(–13.7) μm ×
(3.3–)3.5–4.2(–4.7) μm, equilateral ellipsoid, brown to dark brown; with a straight,
spore-length germ slit on both sides of the spore, running the circumference of the
spore, long-wise. Asci typically long stipitate, with the stipe nearly as long as the
spore-bearing parts; spore-bearing 50–80 μm; with an apical plug wider than tall,
~2 μm × 1 μm, blueing in Melzer’s or other iodine mount (I+), discoid (i.e., flattened
donut shaped).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, THOMPSON ISLAND, on fallen hardwood branch, col. James K.
Mitchell, 6 March 2017 (FH:BHI-F577).
Notes: Lopadostoma americanum is reportedly associated with white oaks (Quercus
spp.) across North America (Jaklitsch et al. 2014); the substrate for BHI-F577
is presumed to be oak, but I cannot confirm this at present. This specimen was collected
towards the northern end of Thompson Island, in a Norway maple forest—
with only Acer platanoides L. (Norway Maple) and Quercus robur L. (English Oak)
(Elliman 2005). There are a few notable differences between this specimen and the
published description, however: L. americanum is described as having nearly black
ascospores, and the stomata are described as being “separate, scattered, rarely in
contact”. I observed in BHI-F577 divergence at both of these traits, this collection
having notably paler ascospores, as well as stromatal pustules that occur at times
in groups of 8–12. Unfortunately, both efforts to culture and to directly amplify
DNA from this material failed. In the absence of phylogenetic data, I am left with
the best morphological fit, which would appear to be Lopadostoma americanum,
despite these differences. It would be wise for an effort to be made to recollect
Lopadostoma from the Boston Harbor Islands, however, to confirm the occurrence
of this taxon.
Figure 6 (following page). Lopadostoma americanum (BHI-F577): (a) pseudostromatal surface,
showing pustulate aggregations of ectostromatic discs above the bark; (b) transverse
section through a group of pseudostromata, showing crowded and compressed globose
perithecia surrounded by loose tissue resulting from the mixture of fungal mycelium
and substrate; (c) vertical section, showing valsoid perithecial arrangement and shared
ectostromatic disc; and (d) ascospores and asci, showing the equilateral spore shape and
spore-length germ slits on both sides. Entoleuca mammata (BHI-F593): (e) stromatal surface,
showing characteristic splitting into semi-regular cuboid to orbicular sections, with
faint parallel depressions visible along the margins of each section; (f) vertical section,
showing the abundant, highly carbonized tissue encasing the stromata, the large perithecia
with papillate ostioles, and the mixing of fungal tissue and substrate towards the base of
the stromata; (g) ascus with amyloid apical apparatus, with distinct central swelling; and
(h) ascospores, showing slightly sigmoid, spore-length germ slits. Scale bars: a–c, e–f =
1000 μm; d, g–h = 10 μm.
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Xylariaceae Tul. & C. Tul.
Type genus: Xylaria Hill ex Schrank
Stromata variable in shape, from effused and applanate through aggregations of
pulvinate or turbinate stromata, to large, erect stromata, but typically with a dark
surface coloration and white to cream interior flesh, at least when young; multi- or
uniperitheciate, but with perithecia always embedded in stromatal tissues. Ascospores
unicellular (or rarely, with 2 cells), brown to dark blackish brown, variable
in shape, but typically ellipsoid inequilateral, mostly a germination slit. Asci 4- or
8-spored, cylindrical, stipitate, with or without an amyloid or inamyloid apical apparatus,
typically taller than it is broad.
Additional information: The Xylariaceae is by far the largest and most heterogeneous
family in the Xylariales. Until relatively recently, this family accommodated
most genera within the order, but the circumscription of the family has been
steadily narrowed as groups of taxa are segregated to other related families (e.g.,
Senanayake et al. 2014, Wendt et al. 2018). One of the best keys to genera in the
Xylariaceae sensu lato (J.D. Rogers, University of Washington, Pullman, WA, pers.
comm.) is published for the Hawaiian islands (Rogers and Ju 2012). Other useful
keys to genera can be found in Rogers et al. (2008) and Sir et al. (2012), though
revised keys considering new taxonomic revisions remain wanting. Other works
from Rogers (1979, 2000) may be useful in understanding the family, both as it was
(sensu lato) and as it currently exists (sensu stricto).
Entoleuca Syd.
Type species: Entoleuca callimorpha Syd.
Stromata effused to effused-pulvinate, broken into orbicular or turbinate sections,
each containing one to several globose perithecia, with surface at first whitish
turning to dull black in maturity, with abundant carbonaceous tissue beneath the
stromatal surface. Ascospores unicellular, brown to dark blackish brown, ellipsoid
inequilateral, with a spore-length germ slit. Asci 8-spored, cylindrical, stipitate,
with an amyloid apical apparatus taller than broad.
Additional information: Despite some difference, Entoleuca would appear to be
closely related to Rosellinia (Wendt et al 2018). Currently, there are only 3 species
within this genus; see Rogers and Ju (1996) for the original segregation from Hypoxylon,
and Ju et al. (2004) for a description of the third species.
Entoleuca mammata (Wahlenberg: Fr.) J.D. Rogers & Y.-M. Ju (Fig. 6e–h)
≡ Sphaeria mammata Wahlenb., Flora Suecica 2:1003 (1826)
≡ Hypoxylon mammatum (Wahlenb.) P. Karst., Notiser ur Sällskapets pro Fauna et
Flora Fennica Förhandlingar 8:212 (1866)
≡ Nemania mammata (Wahlenb.) Granmo, Rapport Botanisk Serie, p. 32 (1995)
= Sphaeria pruinata Klotzsch, Linnaea 8:489 (1833)
Stromata are multiperitheciate, effused to effused-pulvinate (though on plants with
thick, hard bark, they may be discrete, immersed to erumpent, and orbicular), with
a matte black surface, often marked by faint parallel depressions, and splitting into
regular to irregular sections, cuboid to orbicular, each containing few to several
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perithecia; stromata are 1 to several cm in diameter, with discrete sections 2–5 mm
in diameter, and seem to be limited by the substrate, and 1–2 mm thick; carbonaceous
material immediately beneath the surface is abundant and thick, making the
stromata quite hard and brittle; tissues below the perithecia pale brown, mixed with
substrate; without KOH extractable pigments. Perithecia are large, spherical to
globose, 700–1000 μm diameter. Ostioles are conic-papillate, slightly above the
surface of the stromata. Ascospores are 20–33 μm × 9–12 μm, brown, ellipsoid,
nearly equilateral, with broadly rounded ends; with a straight to slightly oblique
hyaline germ slit that is spore-length or nearly so on the more flattened side. Asci
stipes, 30–40 μm, are much shorter than then the fertile parts, 140–200 μm, with an
apical plug slightly taller than it is broad, ~4–5 μm × 3.5–5 μm, blueing in Melzer’s
or other iodine mount (I+), with a distinct bunge at the upper rim, urn shaped.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, GRAPE ISLAND, on corticated aspen (Populus) log, col. Danny
Haelewaters, Jacob Plotnick, 30 October 2014 (FH:BHI-F279a); GRAPE ISLAND,
on bark of dead deciduous tree, col. Lara A. Kappler, 29 July 2015 (FH:BHI-F389);
GRAPE ISLAND, on bark of dead deciduous tree, col. Lara A. Kappler, 30 July
2015 (FH:BHI-F396); GRAPE ISLAND, on bark of dead deciduous tree, col.
Danny Haelewaters, Lara A. Kappler, 19 August 2015 (FH:BHI-F426); THOMPSON
ISLAND, on fallen corticated deciduous branch, col. James K. Mitchell, 6
March 2017 (FH:BHI-F593); GREAT BREWSTER ISLAND, on bark of dead tree,
col. Alden C. Dirks, 8 March 2017 (FH:BHI-F604); GRAPE ISLAND, on bark of
mostly decorticated branch, col. Alden C. Dirks, Lara A. Kappler, 21 March 2017
(FH:BHI-F641); GRAPE ISLAND, on stick, col. Alden C. Dirks, Lara A. Kappler,
21 March 2017 (FH:BHI-F654).
Notes: This relatively common fungus has been a frustration to identify for many,
due to difficulties in accessing previously published descriptions and illustrations.
The commonly cited reference for a description of the teleomorph of E. mammata
is Miller’s (1961) monograph of the genus Hypoxylon (as H. mammatum), a book
that has been out of print for decades and which is not available online. The other
often-cited description of this fungus is from Petrini and Müller’s (1986) work on
European species of Hypoxylon and allies, published in Mycologia Helvetica, a
Swiss mycological journal that was active from 1983 to 2001, and is also not available
online. I hope that the publication of this detailed description may alleviate the
problem of no access to accurate descriptions of this species.
Kretzschmaria Fr.
Type species: Kretzschmaria clavus (Fr.) Sacc.
Stromata restricted- to effused-pulvinate (“ustulinioid”) or clavate to turbinate
(“kretzschmarioid”), often confluent and merging to form broad crusts connected
to substrate by narrow connectives, lacking KOH-extractable pigments, with
abundant carbonaceous tissue beneath the stromatal surface, interior tissues at first
whitish or pale grey, darkening and disintegrating in age, often leaving stromata
hollowed at maturity. Ascospores unicellular, brown to dark blackish brown, elNortheastern
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lipsoid inequilateral, with a straight to sigmoid germ slit of variable length. Asci
8-spored, cylindrical, stipitate, with an amyloid apical apparatus taller than broad.
Additional information: Keys for the genus Kretzschmaria can be found in
the monograph by Rogers and Ju (1998), and a useful regional treatment from the
southeast of the United States is also available (Rogers et al. 2008).
Kretzschmaria deusta (Hoffm.: Fr.) P. Martin
≡ Lycoperdon fraxineum Huds., Flora Anglica, p. 641 (1778)
≡ Sphaeria deusta Hoffm., Vegetabilia Cryptogama 1:3, t. 1:2 (1787)
≡ Hypoxylon ustulatum Bull., Histoire des Champignons de la France I:176, t.
487:1 (1791)
≡ Sphaeria fraxinea (Huds.) Sibth., Flora Oxoniensis, p. 401 (1794)
≡ Nemania deusta (Hoffm.) Gray, A Natural Arrangement of British Plants 1:516
(1821)
≡ Discosphaera deusta (Hoffm.) Dumort., Commentationes Botanicae, p. 91 (1822)
≡ Stromatosphaeria deusta (Hoffm.) Grev., Flora Edinensis, p. 355 (1824)
≡ Hypoxylon deustum (Hoffm.) Grev., Scottish Cryptogamic Flora 6:324, t. 324
(1828)
≡ Ustulina deusta (Hoffm.) Maire, Bulletin de la Société Botanique de France
54:CXC (1907)
= Ustulina vulgaris Tul. & C. Tul., Selecta Fungorum Carpologia, Tomus Secundus.
Xylariei - Valsei - Sphaeriei 2:23 (1863)
Stromata are multiperitheciate, pulvinate to effused-pulvinate, with a matte
brown-black to black surface, often with reticulate major cracks, spreading over
large areas of the substrate and looking rather like burnt wood; stromata are 1 cm
to greater than 10 cm in diameter and 1–4 mm thick, generally with crenate, sloped
margins, and attached to the substrate by narrow connectives, particularly at the
center; carbonaceous material immediately beneath the surface is hard and brittle;
tissues below the perithecia corky to woody, starting white, becoming grey then
dark brown and disintegrating, leaving older stromata generally hollow, with narrow
bands or belts of tissue connecting the upper and lower surfaces within; with
no discernable KOH extractable pigments. Anamorph (not observed) is present as
greyish white to greenish colonies, 1 cm to several cm in diameter, often fusing,
with distinct white margins; the teleomorph developes from the anamorph, hardening
and blackening gradually. Perithecia are large, spherical to globose, 700–1500
μm diameter, sometimes taller than they are wide. Ostioles are coarsely papillate,
projecting above the surface of the stromata. Ascospores are 27–38 μm × 7–9 μm,
brown to dark brown, fusoid-inequilateral, with acute, often pinched, ends; with a
straight hyaline germ slit that is much less than spore-length on the more flattened
side. Asci stipes, 30–40 μm, are much shorter than then the fertile parts, 140–200
μm, with an apical plug taller than it is broad, ~5 μm × 3 μm, blueing in Melzer’s
or other iodine mount (I+), with a distinct bunge at the upper rim, urn shaped.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, THOMPSON ISLAND, on old rotten stump, col. Alden C. Dirks, 6
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March 2017 (FH:BHI-F592); WORLD’S END, on dead stump, col. Alden C. Dirks,
26 March 2017 (FH:BHI-F712); WORLD’S END, dead corticated stump right next
to Juniperus virginiana, col. Danny Haelewaters, 26 March 2017 (FH:BHI-F747).
Notes: This fungus is often encountered, particularly in the spring, in its immature
conidial state, in which it is apparent as a blue-green spreading circular colony, with
paler, greyish margins (Rogers and Ju 1998).
Nemania Gray
Type species: Nemania serpens (Pers.) Gray
Stromata are applanate to effused-pulvinate, typically multiperitheciate, lacking
KOH-extractable pigments, dark or black surface color, with carbonaceous tissue
beneath the stromatal surface, interior tissues at first whitish or pale grey, darkening
and disintegrating in age. Ascospores unicellular, pale yellowish brown to dark
brown, ellipsoid inequilateral, with a conspicuous or inconspicuous germ slit of
variable length, typically (but not always) on the more flattened side of the spore.
Asci 8-spored, cylindrical, usually long-stipitate, with an amyloid or dextrinoid
apical apparatus taller than broad.
Additional information: Keys for the genus Nemania can be found in the excellent
monographic treatment by Ju and Rogers (2002), with further useful descriptions
and illustrations in Granmo et al. (1999).
Nemania beaumontii (Berk. & M. A. Curtis) Y.-M. Ju & J. D. Rogers (Fig. 7a–e)
≡ Hypoxylon beaumontii Berk. & M.A. Curtis, Grevillea 4(31):93 (1876)
≡ Leptosphaeria beaumontii (Berk. & M.A. Curtis) Sacc., Sylloge Fungorum 2:87
(1883)
≡ Heptameria beaumontii (Berk. & M.C. Curtis) Cooke, Grevillea 18(86):33 (1889)
Stromata are multiperitheciate, effused to effused-pulvinate, with a dark rusty
brown to blackish brown surface roughened by conspicuous perithecial mounds,
half to two-thirds exposed; are ~1 cm in diameter, but seem to be limited by the
substrate, and 0.7–0.9 mm thick; carbonaceous immediately beneath the surface
and between the perithecia; no substantial tissues below the perithecia, and tissues
surrounding perithecia thin and brittle, black; with no discernable KOH extractable
pigments. Anamorph is present in the deep clefts between perithecia, and is
clearly geniculosporium-like. Perithecia are spherical to globose, 500–750 μm
Figure 7 (following page). Nemania beaumontii (BHI-F307): (a) stromatal surface, showing
blackish brown coloration and conspicuous perithecial mounds, as well as minutely
papillate ostioles surrounded by a slightly depressed or flattened area; (b) vertical section,
showing globose to slightly flattened perithecia, with little to know tissue below the level
of the perithecia; (c) conidiophore of the nodulisporium-type anamorph, present within the
clefts of the stromata; (d) ascospores and asci, showing the reniform shape and absence of
obvious germ slits (i.e., germ slits inconspicuous); and (e) ascal tips, showing the inverthat
shaped amyloid apical apparatus. Rosellinia subiculata (BHI-F686): (f) uniperitheciate
stromata, embedded in sulfur-yellow subiculum; and (g) ascospores showing less than
spore-length germ slit. Scale bars: a–b = 500 μm; f = 1000 μm; and e, g = 10 μm. Scale bar
e applies to c–d.
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diameter. Ostioles are conic-papillate, slightly above the surface of the stromata,
and sometimes surrounded by a slightly depressed or flattened area. Ascospores
are (7–)8–10 μm × 3.5–4.5 μm, light brown, reniform, with broadly rounded ends,
and an inconspicuous hyaline germ slit much less than spore-length on the more
flattened side. Asci stipes, 55–75 μm, are nearly equal in length to the fertile parts,
65–75 μm, with an apical plug roughly as high as it is broad, ~1.5 μm × 1.5 μm,
blueing in Melzer’s or other iodine mount (I+), and invert hat shaped.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, WORLD’S END, on dead log of deciduous tree, col. Danny
Haelewaters, Lara A. Kappler, 29 May 2015 (FH:BHI-F307a); WORLD'S END, on
decorticated wood, col. Alden C. Dirks, Jasmin J. Camacho, Michal Gorczak, Danny
Haelewaters, James K. Mitchell, 11 December 2016 (FH:BHI-F501); GREAT
BREWSTER ISLAND, hardwood log in an advanced state of decay, col. Danny
Haelewaters, James K. Mitchell, Luis Quijada, 16 October 2017 (FH:BHI-F997).
Notes: Known from only a handful of collections, this fungus has previously only
been found in Brazil and the US state of Alabama (Ju and Rogers 2002); observation
of this fungus at the Boston Harbor Islands extends its range significantly far
to the north, and may indicate that this fungus is simply under-collected, rather
than rare.
Nemania serpens (Pers. : Fr.) S.F. Gray var. Serpens
≡ Sphaeria serpens Pers., Synopsis Methodica Fungorum, p. 20 (1801)
≡ Nemania serpens var. serpens, A Natural Arrangement of British Plants 1:508,
516 (1821)
≡ Gamosphaera serpens (Pers.) Dumort., Commentationes Botanicae, p. 90 (1822)
≡ Hypoxylon serpens (Pers.) J. Kickx f., Flore Cryptogamique des Environs de
Louvain, ou Déscription des Plantes Cryptogames et Agames qui Croissent Dans le
Brabant et Dans une partie de la Province d’Anvers, p. 1 15 (1835)
Stromata are multiperitheciate, irregularly effused, with a dark brown to black
surface, roughened by conspicuous perithecial mounds, one-quarter to one-third
exposed, or smooth, with perithecial mounts not visible, and often with the remains
of a thin, whitish to dark grey or silver exostromatic hyphal coating visible in the
clefts between perithecia and at stromatal margins; are ~1 cm in diameter, but often
fused and limited in size by available substrate, and 0.5–0.7 mm thick; carbonaceous
immediately beneath the surface; tissues below and between the perithecia
thin, corky, and pale brown to white; with no discernable KOH extractable pigments.
Perithecia are spherical to globose, 400–800 μm diameter, sometimes with
bases slightly immersed in the woody substrate. Ostioles are conic-papillate, blunt,
slightly above the surface of the stromata. Ascospores are 10–14.5(–16.5) μm ×
4–6 μm, light brown, reniform, with broadly rounded ends, or 1 broadly rounded
and 1 acute, and an inconspicuous hyaline germ slit much less than spore-length on
the more flattened side. Asci stipes, 45–120 μm, are often roughly equal in length
to the fertile parts, 65–96 μm, with an apical plug higher than it is broad, ~3–5 μm
× 2–3 μm, non-reactive or faintly blueing in Melzer’s (but dextrinoid in Lugol’s;
Granmo 1999), and invert hat shaped with an diffuse upper bulge.
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Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, GREAT BREWSTER ISLAND, on dead decomposing log, col.
Lara A. Kappler, 8 March 2017 (FH:BHI-F610); GRAPE ISLAND, on piece of dry
wood, col. Alden C. Dirks, Lara A. Kappler, 21 March 2017 (FH:BHI-F650).
Notes: This circumboreal fungus is relatively common in the north temperate
zone, but it is often still mis-identified as a Hypoxylon, the genus in which this
fungus was previously placed (Kickx 1835). The pale brown to white interior
flesh of this fungus, complete lack of KOH-extractable pigments, along with the
taller-than-wide ascus apical plug should be sure features leading the inquisitive
mycologist to the genus Nemania, rather than Hypoxylon and its allies. The ascus
apical plug stains very poorly in Melzer’s reagent typically, but will stain quite
satisfactorily with KOH pretreatment (Ju and Rogers 2002) or in Lugol’s iodine
(Granmo et al. 1999).
Nemania maritima Y.-M. Ju & J.D. Rogers
Stromata are dark brown to black with a smooth surface, scattered to gregarious,
and superficial to partially immersed in the substrate; they are globose to subglobose
in shape, and typically uniperitheciate, though some may contain 2 to several
perithecia; they are 0.5–0.6 mm in total diameter, and generally slightly taller than
wide; carbonaceous immediately beneath the surface and surrounding the perithecia;
no substantial tissues below the perithecia; and they are without any traces of a
felty or wooly subiculum. Perithecia are small, generally encompassing the entire
stromatal volume, and globose. Ostioles are obtusely conical. Ascospores are 9–12
μm × 5–6(–6.5) μm, brown, ellipsoid-inequilateral, with broadly rounded ends,
and a hyaline germ slit much less than spore-length on the flattened side. Asci are
short-stipitate, the fertile part 70–85 μm long, with an apical plug ~1.5 μm × 3 μm,
blueing in Melzer’s or other iodine mount (I+), cuneate to discoid (i.e., flattened
donut shaped).
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, PEDDOCKS ISLAND, fallen Juniperus branch, col. Lara A. Kappler,
James K. Mitchell, 10 May 2017 (FH:BHI-F889).
Notes: This is presumed to be N. maritima, based on the halophilic substrate
(driftwood) and mostly uniperitheciate habit. I was unable to locate spores in this
specimen, however. The diagnosis here is based on characteristics of this specimen,
and is inclusive of description from the literature (Ju and Rogers 2002) for features
not observed.
Rosellinia De Not.
Type species: Rosellinia aquila (Fr.) De Not.
Stromata uniperitheciate, but embedded in a wooly or felty subiculum composed
of interviewed mycelium, often bearing the anamorph at least in places, colored
white or cream, sulfur yellow, or dark to reddish brown; when present, interior stromatal
tissues typically whitish; lacking KOH-extractable pigments; dark or black
surface color. Ascospores unicellular, brown to dark brown, ellipsoid inequilateral,
with a conspicuous or inconspicuous germ slit of variable length, typically (but not
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always) on the more flattened side of the spore. Asci 8-spored, cylindrical, usually
long-stipitate, with an amyloid apical apparatus taller than broad.
Additional information: Petrini (2013) provides excellent keys and illustrations
for Rosellinia in her world monograph, which neatly gathers decades of research
from her and her collaborators into one convenient book.
Rosellinia subiculata (Schwein.) Sacc. (Fig. 7f–g)
≡ Sphaeria subiculata Schwein., Schriften der Naturforschenden Gesellschaft zu
Leipzig 1:44 (1822)
≡ Hypoxylon subiculatum (Schwein.) Berk., Grevillea 4(30):52 (1875)
≡ Hypoxylon subiculosum (Schwein.) Berk., Grevillea 4(30):52 (1875)
Stromata are uniperitheciate, though they sometimes fused, giving them the appearance
of containing more than 1 perithecia; they are black with a smooth surface,
gregarious, often forming large groups; they are globose to cupulate in shape, often
with a flattened top; they are 0.7–0.9 mm in total diameter, and generally slightly
wider than they are tall; carbonaceous ectostroma, brittle and persistent, with pale
cream to tan entostroma, disappearing in age. Subiculum is felted to wooly, appressed,
and generally sulphur yellow to orange yellow, whitening with age, and
may be absent in older material. Perithecia are small, generally encompassing the
entire stromatal volume, and globose. Ostioles are finely papillate, slightly raised
above the stromatal surface. Ascospores are 10–12 μm × 5–6.6 μm, light brown to
brown, ellipsoid-inequilateral, with broadly rounded ends, and a straight, hyaline
germ slit extending less than spore-length (half to three-quarters) on the flattened
side. Asci are short- to long-stipitate (10–77 μm), the fertile part 70–80 μm long,
with an apical plug ~1–2 μm × 2–3 μm, blueing in Melzer’s or other iodine mount
(I+), cuneate to discoid.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, WORLD’S END, on corticated branch, col. Danny Haelewaters,
Kevin Healy, Rosanne Healy, Sarah Verhaeghen, 14 September 2013 (FH:BHIF052);
WORLD’S END, on wood, col. Danny Haelewaters, 29 September 2013
(FH:BHI-F072); THOMPSON ISLAND, on fallen decorticated wood, col. James
K. Mitchell, 6 March 2017 (FH:BHI-F590); PEDDOCKS ISLAND, on dead wood,
col. Zachary Chaves, 24 September 2016 (FH:BHI-F686); WEBB MEMORIAL
STATE PARK, on fallen decorticated hardwood branch, col. Alden C. Dirks, James
K. Mitchell, 29 March 2017 (FH:BHI-F763); SLATE ISLAND, rotten, decorticated
wood, col. Alden C. Dirks, Lara A. Kappler, James K. Mitchell, 19 April 2017
(FH:BHI-F832).
Notes: This distinctive fungus can be easily identified by its yellow subiculum, a
trait it shares with only one other Rosellinia, R. pardalios (Berk. & M.A. Curtis)
Cooke, which can be distinguished by its slightly smaller ascospores and its eastern
Asian distribution; currently, R. pardalios is only known from Japan (Petrini 2013).
Rosellinia corticium (Schwein.) Sacc.
≡ Sphaeria corticium Schwein., Schriften der Naturforschenden Gesellschaft zu
Leipzig 1:44 (1822)
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≡ Sphaeria aquila var. corticium (Schwein.) Fr., Systema Mycologicum 2:442
(1823)
≡ Hypoxylon corticium (Schwein.) P.M.D. Martin, South African Journal of Botany
34:156 (1968)
Stromata are uniperitheciate, though they sometimes fused, giving them the appearance
of containing more than one perithecia; they are dark brown to reddish
brown, trending towards black around the ostioles and turning completely black
in age, with a smooth surface, and are scattered to gregarious; they are globose to
subglobose in shape, often with a flattened top, with the base often constricted to a
short, broad stipe; they are 1–1.6 mm in total diameter, and generally slightly wider
than they are tall; with a think carbonaceous ectostroma, brittle and persistent, with
pale cream to tan entostroma, disappearing in age (but more persistent in the stipe
and base). Subiculum is densely wooly, sometimes felted in age, and generally
dark brown to reddish brown, sometimes with purple tones, and reduced in older
material. Perithecia are small, generally encompassing the entire stromatal volume
save the stipe when present, and globose. Ostioles are finely papillate, slightly
raised above the stromatal surface. Ascospores are 22–26.5 μm × 8.5–10 μm, dark
brown, ellipsoid-inequilateral to ovoid, with broadly rounded ends and a semiglobose
cellular appendage 1–3 μm in diameter on one end; completely surrounded
by a slimy sheath, up to 2–4 μm thick, absent in older material; and a straight to
oblique hyaline spore-length germ slit on the flattened side. Asci are short–stipitate,
the fertile part 140–185 μm long, with an apical plug ~8–12 μm × 4–8 μm, blueing
in Melzer’s or other iodine mount (I+), urn-shaped, with prominent upper rim.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National Recreation
Area, WORLD’S END, on hardwood, col. Jason M. Karakehian, 26 March
2017 (FH:BHI-F781).
Notes: This cosmopolitan Rosellinia species is easily confused with R. aquila (Fr.)
De Not., another common species with a dark, woolly subiculum, but R. corticium
can be distinguished by having larger ascomata, slightly larger ascospores, and the
presence of the slimy sheath completely surrounding the ascospores (Petrini 2013).
Xylaria Hill ex Schrank
Type species: Xylaria hypoxylon (L.) Grev.
Stromata variable in size and shape, from erect to pulvinate, but typically stipitate
or at least with a restricted base, interior stromatal tissues usually homogenous
and whitish, lacking KOH-extractable pigments, with dark or black surface color,
sometimes overlain by a whitish or pale ectostromatic layer of tissue. Ascospores
unicellular, brown to dark brown, ellipsoid inequilateral, with a germ slit of variable
length on the more flattened side of the spore. Asci 8-spored, cylindrical, usually
long-stipitate, with an amyloid apical apparatus taller than broad.
Additional information: Xylaria is a complex genus encompassing an enormous
range of morphological variation, and has been correspondingly difficult for taxonomists
to clearly delineate: the genus Xylaria has never been monographed. The
best place to begin when attempting to identify a Xylaria from the US is with the
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works of Jack Rogers, starting with his and Brenda Callan’s “Provisional keys to
Xylaria species in continental United States” (Rogers and Callan 1986) or the expanded
synoptic key they published several years later (Callan and Rogers 1993).
There is also a series of papers from Rogers detailing many of the major groups
of Xylaria in the United States (Rogers 1983, 1984a, 1984b; Rogers and Callan
1986), which may prove enlightening to the interested mycologist. There is also a
useful regional treatment for the Great Smoky Mountains National Park (Rogers et
al. 2008).
Xylaria finismundoensis Vandegrift, sp. nov. (Fig. 8a–g)—Mycobank No. MB
836437
Types. USA, Massachusetts, Plymouth County, Hingham, Boston Harbor Islands
National Recreation Area, World’s End peninsula (42°15'39.72"N, 70°52'08.82"W);
on decorticated stump of unknown wood; 11 Dec. 2016; col. A.C. Dirks, J.J.
Camacho, M. Gorczak, D. Haelewaters, J.K. Mitchell (FH: BHI-F502, holotype).
Ex-holotype sequences: GenBank acc. No. MT823483 (ITS-LSU), GenBank acc.
no. MT823481 (α-actin), GenBank acc. no. MT823482 (β-tubulin), GenBank acc.
no. MT823484 (RPB2). Ibid., 26 Mar. 2017; col. D. Haelewaters (FH: BHI-F743,
paratype). Ex-paratype sequences: GenBank acc. No. MT823485 (ITS). Ibid., 6
Oct. 2017; col. D. Haelewaters, J.K. Mitchell, L. Quijada (FH: BHI-F949, paratype).
Etymology. Referring to the collecting location, meaning literally “Xylaria originating
at the End of the World”.
Stromata are minute but erect, 2–5 mm in total height above the substrate, 0.5–1.2
mm in maximum diameter, dark brownish-black to black, each with notably tomentose
stromatal base, vertical striations from peeling remnants of white exostromatal
coating evident on mature specimens; fertile parts 1.9–4.5 mm, with a sterile apiculate
stromatal apex above. Perithecia are small, globose, thick-walled (>10 μm)
when mature; 300–400 μm × 300–410 μm (mean = 335 μm × 345 μm, n = 13). Ostioles
are large (75–130 μm; mean = 105 μm, n = 15), conical, papillate, and rather
reflective. Ascospores are (9.5–)10–11.5 μm × 4.5–6 μm (mean = 10.64–5.08 μm,
n = 25), brown to dark brown, ellipsoid inequilateral, with broadly rounded ends
and a hyaline germ slit spore-length or nearly so on the flattened side. Asci are
Figure 8 (following page). Xylaria finismundoensis sp. nov. (BHI-F502): (a) stromatal habit,
illustrating erect form, tomentose base, and white vertical striping from remnants of degrading
ectostromatic layer; (b) close up of stromatal surface, illustrating large, conical-papillate
ostioles, and vertical section illustrating thick-walled, globose to spherical perithecia, fully
embedded in stromata; (c) ascospores and asci, illustrating the narrowly to broadly rounded
ends, spore-length germ slic, short-stipitate asci, and invert hat-shaped amyloid apical apparatus;
(d) stromata, showing erect form, tomentose base, and white vertical striations
from remnants of degrading ectostromatic layer; (e) vertical section, perithecia embedded
in stromata; (f) ascospores, showing hyaline, spore-length germ slit, and germinating spore
(far right); and (g) ascospores and asci, showing the amyloid apical apparatus. Scale bars:
a, d, e = 1000 μm; b = 500 μm; and c, f, g = 10 μm.
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short-stipitate, the fertile part about 70–100 μm long; with an apical plug slightly
taller than broad, 3 μm × 2.5 μm, dark blue in Melzer’s or other iodine reagent (I+),
invert hat-shaped, without a central swelling.
Notes: All 3 specimens of this species were collected from the same decorticated
stump on the World’s End peninsula over the course of a year (Dec. 2016, Mar.
2017, Oct. 2017). This fungus is apparently a common endophyte, judging from sequence
similarity to numerous endophytic isolates found by BLAST match against
NCBI GenBank’s standard nr/nt nucleotide database (https://www.ncbi.nlm.nih.
gov/nucleotide). I have placed Xylaria finismundoensis within the previously reported
E9 endophyte clade (see the Results and Discussion section, above), making
this the first reported teleomorph for a group of Xylaria, which were previously
only known as endophytes.
The ITS sequences generated from BHI-F502 and BHI-F743 are almost perfectly
identical at the 5.8S and ITS2 loci, but quite divergent at the ITS1 locus;
extraction and sequencing failed for the third collection (BHI-F949), so no comparison
is possible. Interestingly, the sequence from BHI-F743 is nearly perfectly
identical to an endophyte from North Carolina (NC0985), also a member of the E9
endophyte clade (U’Ren et al. 2016). All 3 sequenced collections are morphologically
indistinguishable, and were harvested from the same substrate, a decomposing
tree-stump, so it is clear that they are the same species, likely even representing
fruiting bodies of the same parent mycelium. The clear evidence of recombination
within the rDNA locus is interesting, and points to a need for further investigation
into the sexual biology of Xylaria as it relates to the endophytic lifestyle, and to the
need to re-evaluate the ways in which we apply ITS sequence data to identification
of unknowns (Stadler et al. 2020).
This taxon may be easily confused for Xylaria hypoxylon, Xylaria longiana
Rhem, Xylaria vasconica J. Fournier & M. Stadler, or Xylaria apiculata Cooke.
Xylaria hypoxylon is probably the most commonly applied name in the genus across
North America, though it would seem that the name has been constantly misapplied
to collections of Xylaria longiana and Xylaria vasconica on the East Coast of the
United States (Persoh et al. 2009, Fournier et al. 2011). In fact, there is some doubt
as to whether Xylaria hypoxylon occurs on the East Coast of the US at all, with no
verifiable sequenced vouchers available at all (M. Stadler, Department of Microbial
Drugs, Helmholtz Center for Infection Research (HZI), and German Center for Infection
Research (DZIF), Partner Site Hannover/Braunschweig, Inhoffenstraβe 7,
38124 Braunschweig, Germany, pers. comm.). Xylaria apiculata has been reported
from the United States, but seems to have a more tropical/subtropical distribution
(Dennis 1956, Rogers 1986), and is unlikely to occur in the Boston Harbor Islands.
Xylaria finismundoensis can be distinguished from X. hypoxylon by its smaller
stature; the absence of flattened, branching, antler-like stromatal apices; and the
slightly smaller ascospores. Xylaria longiana (sometimes referred to as the “smallspored”
form of X. hypoxylon; Callan and Rogers 1993) is morphological similar to
X. hypoxylon, and can be discriminated from X. finismundoensis in the same ways
(i.e., by the flattened, antler-like sterile apex). It can likewise be distinguished
from X. vasconica (the most likely similar taxon to be encountered in this area) by
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its smaller ascospores, minute stature, solitary habit, and striate stromatal surface
(X. vasconica has a distinctly nodulose to cerebriform surface texture). Similarly,
X. finismundoensis can be distinguished from X. apiculata primarily by its smaller
ascospores ([9.5–]10–11.5 μm × 4.5–6 versus 17–24 μm × 7–9 μm), and its sporelength
germ slit (Dennis 1956).
Xylaria polymorpha (Pers.: Fr.) Grev.
≡ Sphaeria polymorpha Pers., Commentatio de Fungis Clavaeformibus, p. 17
(1797)
≡ Cordyceps polymorpha (Pers.) Fr., Observationes Mycologicae 2:317 (cancellans)
(1818)
≡ Hypoxylon polymorphum (Pers.) Gray, A Natural Arrangement of British Plants
1:512 (1821)
≡ Xylosphaera polymorpha (Pers.) Dumort., Commentationes Botanicae, p. 92
(1822)
≡ Hypoxylon var. polymorphum (Pers.) Mont., Annls Sci. Nat., Bot. sér. 2, 13:349
(1840)
Stromata large and robust, often greater than 10 cm tall and usually >1 cm in diameter,
extremely variable in size and shape, cylindrical to clavate or spathulate,
mostly unbranched with rounded, with fertile apices, and long or short stipes,
becoming dull blackish brown or black in age, with a roughened, rugose surface
texture, with obscure to discoid ostiolar papillae; interior tissues uniform and white
to cream, with perithecia fully immersed beneath the stromatal surface. Perithecia
are larger, 500–1000 μm in diameter, globose. Ascospores are (19–)20–28(–31)
μm × (5–)6–7.5(–10) μm, brown to dark brown, ellipsoid inequilateral, with narrowly
to broadly rounded ends, and a straight to slightly oblique hyaline germ slit
distinctly less than spore-length on the flattened side. Asci are long-stipitate, the
fertile part 90–145 μm long, with the stipe nearly as long as the spore bearing parts,
with an apical plug taller than broad, 4.5–6.5 μm × 3–4 μm, dark blue in Melzer’s or
other iodine reagent (I+), rectangular to urn-shaped, with a broad central swelling.
Specimens examined: USA: Massachusetts, Boston Harbor Islands National
Recreation Area, THOMPSON ISLAND, on base of dead tree trunk, col. Lara A.
Kappler, 28 August 2015 (FH:BHI-F548); WORLD’S END, on dead stump, col.
Alden C. Dirks, 26 March 2017 (FH:BHI-F713); GRAPE ISLAND, spalted dead
wood piece, col. Lara A. Kappler, James K. Mitchell, 3 May 2017 (FH:BHI-F866).
Notes: Probably the most frequently erroneously applied name in the genus,
X. polymorpha is one of the largest and most common Xylaria in the northern United
States. Despite the frequency of misapplication, it is fairly easy to identify this
species by its roughened, rugose surface texture, large stature (mature specimens
hardly ever being less than 2 cm tall and less than 0.5 cm in diameter), and ascospores of the dimensions
above, with a distinctly shorter than spore-length germ slit (Rogers and Callan
1986). Of the specimens examined here, BHI-F866 is immature but presumed to be
X. polymorpha based on its robust stromata.
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Acknowledgments
This work would not have been possible without the aid and support of D. Haelewaters,
who organized and administered the fungal aspects of the Boston Harbor Islands All
Taxa Biodiversity Inventory, and edited this Special Issue; I would not have finished this
paper without his poking and prodding. Also, special thanks to D.H. Pfister and the Farlow
Herbarium at Harvard University for facilitating this work and loaning me the specimens,
and to B.A. Roy, whose laboratory at the University of Oregon was used to examine and
photograph these specimens. I am grateful to B. Wergen for advice on diatrypaceous fungi.
Additionally, thanks to M. Albert for collection logistics, and to R. Bowles and the staff of
the Division of Marine Operations, University of Massachusetts–Boston, for transportation
and navigation to remote islands. M. Stadler and 1 anonymous reviewer provided comments
on an earlier version of the manuscript that substantially improved this paper. The
collections used in this work would not have existed without the financial support of Boston
Harbor Now, the National Park Service, the New England Botanical Club (Les Mehrhoff
Botanical Research Fund, granted to D. Haelewaters). Collecting of fungi was approved
under permits #BOHA-2012-SCI-0009 (PI B.D. Farrell) and #BOHA-2018-SCI-0002 (PI
D. Haelewaters).
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