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Analysis of morphogenesis in hyphomycetes: New characters derived from

considering some conidiophores and conidia as condensed hyphal systems

Article in Canadian Journal of Botany · February 2011

DOI: 10.1139/b03-008

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COMMENTARY / COMMENTAIRE

Analysis of morphogenesis in hyphomycetes: new

characters derived from considering some
conidiophores and conidia as condensed hyphal
systems
Bryce Kendrick

Abstract: Hyphomycetes (ascomycetous and basidiomycetous anamorphs) comprise numerous genera and species that
have been difficult to place in fungal phylogeny. In this commentary, autobiographical notes preface a new analysis of
reproductive structures in many hyphomycetes. This adopts the premise that many of the more complex examples of
conidiophores and conidia represent condensed hyphal systems. Many new and potentially useful taxonomic characters
are described, which are particularly applicable to computer-based synoptic keys or databases, but should also be
considered by those describing new taxa or redescribing existing ones.

Key words: moulds, taxonomy, conidia, conidiophores, morphogenesis, branching.

Résumé : Les hyphomycètes (anamorphes des ascomycètes et des basidiomycètes) comprennent de nombreux genres
et espèces qui ont été difficiles à situer dans la phylogénie fongique. Dans cette commentaire, des notes autobiographi-
ques servent de préface à une nouvelle analyse des structures reproductrices chez plusieurs hyphomycètes. Ceci se base
sur les prémices que plusieurs des exemples les plus complexes de conidies et de conidiophores représentent des systè-
mes d’hyphes condensées. On décrit plusieurs nouveaux caractères taxonomiques potentiellement utiles, qui se prêtent
particulièrement bien à des clés ou des bases de données synoptiques informatisées, mais devraient être également
prises en compte lors de la description de nouveaux taxons, ou la révision de taxons existants.

Mots clés : moisissures, taxonomie, conidies, conidiophores, morphogenèse, ramification.

[Traduit par la Rédaction] Kendrick 100

Introduction: why moulds?
“…to a clear eye the smallest fact is a window through
which the infinite may be seen”.1
Although this paper is perhaps aimed mainly at those who
describe, redescribe, or make keys to hyphomycetes, I hope
the numerous illustrated examples will demystify the subject
matter for the more general reader. The fungi are actually
a fascinating and extremely under-appreciated (not to say
under-studied) group. The moulds, although long known as
important elements of the biosphere, heavily involved in
biodegradation and recycling, food spoilage, and food pro-
cessing, have gained renewed prominence recently because
of their predilection for contaminating our leaky dwellings.
Although this is not news to mycologists, the rest of the
Received 29 August 2002. Published on the NRC Research
Press Web site at http://canjbot.nrc.ca on 6 March 2003.
B. Kendrick. Mycologue Publishers and Consultants,
8727 Lochside Drive, Sidney, BC V8L 1M8, Canada
(e-mail: bryce@mycolog.com).
1
Thomas Henry Huxley.
population has just become aware of, and in some cases
unduly excited by, the perceived mould invasion. These
innocent organisms have generated hysteria, panic, and an
epidemic of litigation. But when I first began to study them,
this dénouement still lay many years in the future.
I went to the University of Liverpool in 1951 at the age of
17, knowing that I wanted to be some kind of biologist.
Looking back, I think I was born too late: I am a
field-oriented naturalist, interested in almost everything — a
generalist. I recently made a memorable visit to the
Galapagos, and I am sure I would have been a better, or at
least more like-minded, companion for Charles Darwin than
Captain Fitzroy proved to be. How wonderful, had it been
possible to take Darwin snorkelling or SCUBA diving and
show him a rainbow runner and a hieroglyphic hawkfish in
their natural environment.
I have always been fascinated by the brilliant diversity of
life, so undergraduate marine biology courses at Port Erin in
the Isle of Man revealed a new world, and almost made an
algologist of me. That would have been fine, but my
algology professor, of whom I was very fond, always gave
her honours students 3rd class honours, so in simple
self-preservation I drew back. Nature abhors an intellectual

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vacuum, so I segued into mycology honours, which led to
graduate school and thence to a life-long study of mycology.
From my present perspective, I can suggest to students that
it matters little which branch of biology they pursue, as long
as they are, or become, really interested in what they are
studying. And surely every group of living organisms is both
unique and fascinating.
I did not choose the moulds — they chose me. While I
was pursuing my Ph.D., investigating the fungal ecology of
a pine forest soil, almost 50 years ago, I encountered a num-
ber of these strange microscopic beasts sporulating on dead
needles. I soon found that they were hyphomycetes, but
somehow I could not attach good names to some of them —
they simply did not fit anything I could find in the (then
rather limited) literature. Visiting Martin Ellis at the Com-
monwealth Mycological Institute, Kew, I learned that the
strange organisms I had found were in fact undescribed —
had never before been seen by human eye (see Kendrick
1958a, 1958b, 1961). I had encountered the unknown, and
I was hooked. Although studying ecology, I realized two
things: that ecologists must be intimately acquainted with
the organisms whose interactions they wish to understand,
and that even generalists need at least one specialty.
Once I got to know them better, I was surprised at how
easy it was to identify many, though not all, moulds. I no-
ticed, in contrast, how much more difficult it was to put
accurate names on many teleomorphic basidiomycetes and
ascomycetes (e.g., mushrooms, cup fungi). It occurred to me
that this was because most members of those sexually repro-
ducing groups had evolved into morphological straitjackets,
while the hyphomycetes (asexual or anamorphic expressions
of the same groups) had not. Let me explain.
There are at least 10 000 different mushrooms (almost all
teleomorphic basidiomycetes), but at maturity the great ma-
jority are no more than variations on the umbrella theme.
They reiterate the same combination of features — vertical
stipe, protective rain-shedding cap, radiating vertical gills cov-
ered with holobasidia each producing four (sometimes more,
occasionally fewer) exogenous meiospores/ballistospores —
over and over again, often with only very minor variations
(try to identify a Cortinarius). This pattern was apparently
dictated by the fact that their hymenia must not be wetted,
since a water film would swamp the delicate sequence of
events involved in the discharge of basidiospores (Money
1998).
Likewise, the most crucial features of ascomycetes, the
meiosporangia and meiospores (asci and ascospores), are
almost equally repetitious — closely packed tubular asci
in most cases, each usually producing eight endogenous
meiospores/ballistospores, which are most often unicellular
and ellipsoidal. Because those spores must be formed in
such large numbers, have to develop in such close quarters,
and must be shot away through the air (by rupture of the
ascus tip following an internal buildup of osmotically gener-
ated hydrostatic pressure), their morphological style, and of-
ten that of the entire ascoma, is more than a little cramped
(though there are four kinds of ascoma). The reason for the
success of the patterns I have just outlined for teleomorphic
fungi is not far to seek — they permit the sexual process to
unfold, they produce large numbers of meiospores, and they
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work well as spore-dispersing organs. But their relative lack
of diversity does not help mycologists to sort them out.
Contrast with these the hyphomycetous moulds, which
sporulate in the open, where there are no spatial restraints on
the development or morphology, either of their sporulating
organs (conidiophores, conidiogenous cells) or of the spores
themselves (conidia/mitospores). The diversity of possible
structures is almost infinite, and reality is not far behind. So
although some hyphomycetes produce boring (to us) little,
round, unicellular conidia on equally boring single, un-
branched hyphae, many more, in the manner of flowers,
have evolved reproductive structures of exuberant diversity.
These microscopic structures have another advantage for
the would-be identifier: they mature very quickly to the
forms outlined in their descriptions. In contrast, the much
larger sporophores of their sexual counterparts often pass
through several changes in shape or pigmentation during
development (as in many species of Amanita, and Phaeolus
schweinitzii, among many others), making the process of
identification more difficult, or at least more complex.
Just after helping to complete a compilation of the known
genera of hyphomycetes (Carmichael et al. 1980) I pub-
lished a paper (Kendrick 1980) that suggested there were too
many overlapping or barely distinguishable genera of hypho-
mycetes, and proposed ways of reducing their number by
amalgamation. At least part of my thesis was based on the
presumption that: “None of the traditional systems can cope
properly with 900 genera. Anyone who has picked their way
through an extended dichotomous key to hyphomycetes [or
any other group] knows that the chance of error increases
with each choice made. After encountering a hundred or so
couplets, the seeker may well feel that they have compro-
mised and guessed their way into error. Synoptic keys...
sidestep the endless choosing and allow entry at any point,
but are unsuited for use with large numbers of taxa”. At that
point, computers had not yet been drafted to help with this
problem.
I was to undermine my own argument, some years later,
by building a free-form database of about 1250 hypho-
mycete genera, which was also designed to function as a
synoptic key. This was now possible because personal com-
puters could easily perform the many comparisons necessary
in the operation of a synoptic key to 1250 entities. I was
amazed, and somewhat dismayed, by the large number of
descriptors I had to use. But I was nevertheless gratified at
how well the database worked in the synoptic identification
of moulds (and not only for me, but for many other users). It
appeared that most hyphomycete genera had at least a few,
and sometimes many, unique characters arising either from
the lack of spatial constraints already mentioned, or from
ecological imperatives (selection pressure). But the success
of the key’s users still depended on their ability to pick out,
or at least recognize in a list, those unique characters,
or character sets, in each genus, something that apparently
requires at least a modicum of experience.
The anamorphic fungi, formerly and erroneously called
“fungi imperfecti”, and now also known as mitosporic fungi
or conidial fungi (but not, I hope, as “Deuteromycetes” —
see Kendrick 1989), have always been thorns in the sides of
those trying to establish a reasonable phylogenetically based
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Kendrick
classification for the fungi as a whole. Most of them are un-
derstood to be asexual phases of ascomycetes (see Kendrick
and DiCosmo 1979, and an interactive database compiled
as a continuation of the same project, and now accessible
at: http://www.cbs.knaw.nl/databases/anateleo.html). Kendrick
and Watling (1979) also showed that a respectable number of
hyphomycetes are asexual phases (anamorphs) of basi-
diomycetes. Many of these anamorphic (mitosporic) phases
are encountered so often in the absence of their sexual coun-
terparts that a whole separate, parallel system of legally rati-
fied names and taxonomy has been developed for them.
In fact, some hyphomycetes are among the world’s most
common and successful fungi — think of Penicillium,
Aspergillus, Fusarium, Cladosporium, and Botrytis.
Since the advent of molecular techniques, there has been
strong and justified pressure to use the new information to
integrate the asexual moulds into the holomorphic classifica-
tion (which has until now essentially been based on the sex-
ual stages of the fungi). Unfortunately, in the great majority
of cases we can still say no more than that a mould is
an anamorphic ascomycete or basidiomycete. However, base
sequences have been used to link anamorphs with
holomorphs at the ordinal level (Glenn et al. 1996), at the
family level (Rehner and Samuels 1995), the generic level
(Berbee and Taylor 1992; LoBuglio and Taylor 1993), and
even at the species level (Kuhls et al. 1996), and this kind of
work will continue.
Several thousand connections have already been made be-
tween anamorph species and their holomorphs, on natural
substrates or in culture, and are documented at the web site
mentioned above. Yet some of those connections are no
doubt spurious, and thousands more taxa remain isolated.
Even though new connections will continue to be made by
traditional (see Mueller 1971) and molecular means, a large
number of anamorphs will remain orphans, and we will un-
doubtedly have to use a morphologically based system to
identify moulds for years to come. In fact, recent molecular
work by Camara et al. (2002) strongly supports the
monophyly of the mould genus Stemphylium, and the contin-
uing utility of the existing morphologically and developmen-
tally based classification. That is why I am making this
attempt to add useful taxonomic characters to the known
spectrum.
History: mature morphology and
conidiogenesis
(If you are already aware of the historical aspects of the
study of moulds, I would suggest that you jump ahead to the
next section, Analysis of conidiophores: morphogenesis).
The classification of conidial anamorphs began as a system
based entirely on an analysis of mature microscopic mor-
phology. The features originally used to classify conidial
fungi included: presence or absence of pigment; degree of
aggregation or enclosure of conidiophores, or absence of
such aggregation or enclosure; and shape and septation of
conidia. This system was codified in detail, and extensively
documented, by Saccardo in his classic multi-volume
Sylloge Fungorum (1882–1925).
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77
Although the characters selected by Saccardo were (and
still are) useful in identifying anamorphs, it was eventually
recognized that the underlying system was to some degree
artificial — it did not necessarily reflect the phylogenetic re-
lationships of these fungi — and no adequate classification
of conidial fungi has ever been erected above the generic
level using these characters (I won’t document the several
attempts to do this, since I believe they were essentially fu-
tile and are best forgotten). This apparent shortcoming did
not perturb many mycologists. It was widely assumed that
all anamorphs would eventually be connected with their sex-
ual expressions (teleomorphs), and thus be recognized as
parts of holomorphic fungi, so the need for a classification
of anamorphs would wither away.
This did not happen. The more we learn about the fungi,
the more obvious it becomes that many anamorphic fungi no
longer produce sexual phases, or teleomorphs (they are, in
fact, anamorphic holomorphs, though it is often difficult to
prove this). As just mentioned, molecular evidence has the
potential to let us connect anamorphic holomorphs with the
groups of ascomycetes and basidiomycetes within which
they originally evolved. This may eventually allow us to
insert anamorphs into the holomorphic classification with
some confidence, but we are currently left with the practical
need to identify large numbers of conidial fungi with neither
teleomorph nor molecular data in hand. In any case, the ex-
clusive use of molecular data to identify moulds is a distant
prospect. In practical terms we must still rely largely on in-
formation derived from light microscopy.
Hughes (1953) took us beyond mature morphology by
making us aware of the developmental events involved in
mitospore development (conidiogenesis), and proposed that
they could be used to classify conidial fungi on more precise
and perhaps more natural grounds. For many years, this seg-
ment of the anamorph information spectrum held the atten-
tion of many mycologists (among them, the author of this
paper). We attempted to analyze the processes involved in
the development of conidia. The way in which we describe
those processes has been elaborated and refined to the point
where it may now require a paragraph, a diagram, and a
sequence of illustrations, to specify the way in which a
conidium is initiated, matured, delimited and released, and
how the conidiogenous cell prepares itself for the formation
of the next spore, if in fact there is to be one.
This was a useful and productive exercise, but as we scru-
tinized more and more conidial fungi, we realized that
conidiogenesis was more plastic than had originally been
thought, and eventually it became apparent that, as I wrote
in the foreword to Cole and Samson (1979) “…there will be
no natural classification … based on conidium ontogeny”.
This new perception led to a slight reduction in the number
of anamorph genera, as some with seemingly different
modes of conidiogenesis were found to overlap because they
developed conidia in more than one way. For example,
Verticicladiella Hughes, established because of its suppos-
edly exclusively “blastic-sympodial” conidiogenesis, was
reintegrated with the older and supposedly exclusively
“blastic-percurrent” Leptographium Lagerberg & Melin
when it was realized that each could imitate the other. We
may expect further reorientations of this kind. But despite
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78
this minor attrition, the total number of described anamorph
genera continues to increase, and it is still de rigueur to
examine the development of their propagules.
Yet there is something unsatisfying about many current
descriptions, because precisely the same ontogenetically ori-
ented terminology can apply to conidia that look very differ-
ent at maturity. This implies that something has been left out
of the equation. One major omission concerns morpho-
genesis: the process by which the young spore gradually
assumes its final shape. This neglect may have been occa-
sioned by the fact that many conidia are visually diagnostic
and can be identified without any reference to their mode of
development. It may also be because most work on conidio-
genesis was done on fungi with unicellular conidia
(amerospores), the focus being on process rather than prod-
uct. Another neglected aspect is the branching of conidio-
phores, which is much more diverse than one would be led
to believe by reading many published descriptions.
Analysis of conidiophores: morphogenesis
If we can say that flower parts such as petals and sepals
are leaves modified during evolution for new purposes, it is
surely equally true that conidia and the structures that pro-
duce them are essentially modified hyphae or parts thereof.
This is easy to perceive in the case of long, narrow
scolecosporous or phragmosporous conidia such as those
of Stenella Sydow (Fig. 1A), Pseudoanguillospora Iqbal
(Fig. 1B), or Anguillospora Ingold (Fig. 1C) and their sim-
ple conidiophores. Although it is much less obvious in many
other kinds of conidia and even in some conidiophores, it
can be accepted as axiomatic. In this paper I will try to carry
the analysis of morphology and its development a few steps
further, especially as it involves the branching process so
innate to fungal hyphae.
Branching structures producing blastic-acropetal chains
(Figs. 2A–2F)
Many conidial fungi produce branched chains of amero-
spores (single-celled or nonseptate conidia), often employing
blastic-acropetal conidiogenesis, as in Trichobotrys Penzig
& Saccardo (Fig. 2A), Agarwalia Tiwari & Agrawal
(Fig. 2B), Alysidiopsis Sutton (Fig. 2C), Chrysonilia von
Arx (Fig. 2D) (anamorph of Neurospora), Hyalodendron
Diddens (Fig. 2E), and Cladosporium Link (Fig. 2F). The
general similarity of this pattern to normal branching hyphal
growth is apparent, though it has become rather condensed
in Trichobotrys and Agarwalia as the cells have become con-
verted to short, subglobose conidia (perhaps an ecologically
imposed minimal surface area for a given biomass). The
conidiophore of Alysidiopsis (Fig. 2C) is intermediate in this
respect, the cells being short and rather swollen, with con-
stricted septa. Chrysonilia (Fig. 2D) approaches lax hyphal
branching, and tends toward dichotomy.
Branching structures producing thallic-arthric or
alternate-arthric conidia (Figs. 3A–3E)
In other anamorphs, a branching system develops, then
fragments either backward, or randomly, to produce
thallic-arthric conidia, as in Staheliella van Emden
(Fig. 3A), Botryomonilia Goos & Pirozynski (Fig. 3B),
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Amblyosporium Fresenius (Figs. 3C and 3D) and
Oidiodendron Robak (Fig. 3E). These are all clearly nothing
more than secondarily modified branching hyphal systems,
some more highly modified than others. Since these particu-
lar systems frequently disintegrate at or before maturity to
liberate the conidia derived from them, it can be difficult to
use details of the kinds of branching involved as diagnostic
characters, unless immature stages are present on the mate-
rial examined. Yet analysis of these genera, if they are ex-
amined before spore maturity, can be fruitful. The branches
of the fragmenting conidiogenous heads of Staheliella
(Fig. 3A), Botryomonilia, (Fig. 3B), Oidiodendron (Fig. 3E),
and Amblyosporium (Figs. 3C and 3D), are moderately
crowded, and resemble relatively normal branching hyphae,
though the conidiogenous hyphae are distinctly narrower
than the stipes from which they arise. Those in
Botryomonilia (Fig. 3B) narrow progressively, while those
in Staheliella (Fig. 3A) and Amblyosporium (Figs. 3C and
3D) are narrower from inception. The conidiogenous
branches in Amblyosporium (Figs. 3C and 3D) are clustered;
in Amblyosporium spongiosum (Fig. 3D) there is a single
cluster at the apex of the stipe, while in Amblyosporium bo-
trytis (Fig. 3C) several clusters of secondary conidiogenous
branches arise at different places along a series of alternate
or occasionally opposite primary branches. Branching in the
head of Botryomonilia (Fig. 3B) is basically dichotomous,
and although the initial branching of Staheliella (Fig. 3A)
is clustered, subsequent branching of the fertile hyphae is
dichotomous. These characters have not been previously
called upon to differentiate the taxa, but they can all be put
to good use.
Open branching systems: branches divergent, not
converted into conidia (Figs. 4A–4H)
In many genera the conidiophore is a branched hyphal
system that is not itself converted into conidia and is thus
more amenable to analysis. For example, the conidiophores
of Virgaria Nees (Fig. 4A), Tympanosporium Gams
(Fig. 4B), Hansfordia Hughes (Fig. 4C), and Tritirachium
Limber (Fig. 4D) closely resemble a fragment of the edge of
a normally developing colony, with branches arising at regu-
lar or irregular intervals to “fill a gap” or, as would be the
case in the strategy of a growing mycelium, to exploit the
substrate more thoroughly. As part of this analysis, it is
worth noting that the conidiophore of the Virgaria (Fig. 4A)
branches somewhat asymmetrically while that of the
Tympanosporium (Fig. 4B) is dichotomous. In the
Hansfordia, (Fig. 4C) branching is irregular, and the main
axis of the conidiophore is sterile and setose. The ultimate
branches in the Tritirachium (Fig. 4D) tend to be in twos or
threes and fairly symmetrical. In three of these four genera,
subsequent production of conidia is blastic-sympodial but
there are clear differences in the size and spacing of the
scars the conidia leave behind, and the cells of the
Tritirachium (Fig. 4D) taper most markedly toward a very
fine apex. Again, despite an underlying similarity, it is not
difficult to differentiate these genera on characters of the
conidiophores alone. If we look instead for underlying simi-
larities, it is easy to see that more branches equals more
conidiogenous cells, equals more conidia. Other genera pres-
ent more modified patterns. In Balanium Wallroth (Fig. 4E)
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Kendrick 79

Fig. 1. Conidia that are clearly modified hyphae (after Carmichael et al. 1980). (A) Stenella, (B) Pseudoanguillospora,
(C) Anguillospora.

Fig. 2. Blastic-acropetal conidial chains that mimic branching hyphal growth (after Carmichael et al. 1980). (A) Trichobotrys,
(B) Agarwalia, (C) Alysidiopsis, (D) Chrysonilia, (E) Hyalodendron, (F) Cladosporium.

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Fig. 3. Thallic-arthric conidial chains that are derived from branching hyphal growth (after Carmichael et al. 1980). (A) Staheliella,
(B) Botryomonilia, (C) Amblyosporium botrytis (note that these conidia and those in Fig. 3D are alternate-arthric), (D) Amblyosporium
spongiosum, (E) Oidiodendron.
and Craspedodidymum Holubová-Jechová (Fig. 4F) the
conidiophore is clearly a dichotomously branched system.
Other genera with repeatedly dichotomous conidiophores are
Amphobotrys Hennebert, Dichobotrys Hennebert, and
Glischroderma Fuckel.
The first six fungi illustrated in Fig. 4 present no drastic
digressions from normal hyphal branching patterns, but the
last two are more highly modified. In Verticicladium Preuss
(Fig. 4G), the broad main axis divides at its apex into three
or four primary branches, and then branches again, eventu-
ally producing long, sympodially extending conidiogenous
cells delimited by basal septa. This is an unusual pattern.
Dichotomophthora Mehrlich & Fitzpatrick ex Ellis (Fig. 4H)
goes further. Its conidiophore axis is initially unbranched,
but at the point at which it is programmed to become fertile,
it divides trichotomously (looks cruciate). Subsequent devel-
opment is very condensed, and the three primary branches
generate synchronous clusters of new apices which immedi-
ately become conidiogenous loci. This system is so con-
densed that there is no room, and no need, for septa.
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Condensed branching systems: branches clustered
(penicillate) (Figs. 5A–5F)
The next set of illustrations exemplify a form of condensa-
tion in the conidiophores. Phialocephala Kendrick (Fig. 5A)
has a single, tall axis at whose apex develops a large and
complex fertile head, which has been called a “conidiogenous
apparatus”. In Phialocephala dimorphospora Kendrick
(Fig. 5A) this incorporates five layers of tightly packed
branches, the ultimate series becoming specialized as
conidiogenous cells. The conidiogenous apparatus can easily
be perceived as a condensed mycelial front. Although the
drawing can effectively show only two dimensions, the appa-
ratus is three-dimensional, and presents an excellent example
of a single hypha giving rise to a very large number of
conidiogenous cells (and potentially to a huge number of
conidia). Some other genera that produce what are generally
known as penicillate conidiophores, e.g., Penicillium Link
(Fig. 5B), Haplographium Berkeley & Broome (Fig. 5C),
Gliocladium Corda (Fig. 5D), and Thysanophora Kendrick
(Fig. 5E) may be interpreted similarly. Gliocephalotrichum
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Kendrick 81

Fig. 4. Conidiophores that are easily recognized as branched hyphal systems (after Carmichael et al. 1980). (A) Virgaria,
(B) Tympanosporium, (C) Hansfordia, (D) Tritirachium, (E) Balanium, (F) Craspedodidymum, (G) Verticicladium, (H)
Dichotomophthora (highly condensed).

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Fig. 5. Conidiophores in which the penicillate conidiogenous apparatus is a highly modified and condensed hyphal system (after
Carmichael et al. 1980). (A) Phialocephala, (B) Penicillium, (C) Haplographium, (D) Gliocladium, (E) Thysanophora,
(F) Gliocephalotrichum.
Ellis & Hesseltine (Fig. 5F) is another example, but here mul-
tiple sterile as well as fertile branches arise at the top of the
stipe. In this unique fungus, a highly modified branching sys-
tem (a penicillate conidiogenous apparatus) and relatively un-
modified branches (setose extensions) develop side by side,
and this configuration makes identification very easy. The
setose extensions may serve the function of protecting devel-
oping conidiogenous cells and conidia from browsing
meiofaunal arthropods (something we will see again in
Menispora, Fig. 8G).
In all these cases, the repeated branching of hyphae is not
directed toward exploration of new substrate (nutrition) as it
would be in somatic hyphae, but toward the production of
numerous conidiogenous cells, and hence many spores
(reproduction). This kind of shift is an example of the ways
in which selection pressure can alter function in drastic
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ways. If we consider mammals, the transformation of a
five-toed foot into a hand, a flipper, and a wing is somewhat
comparable, since although all the new mammalian func-
tions originally had to do with locomotion, the hand later be-
came adapted for grasping, and has, in certain specialized
individuals, acquired functions that could not possibly have
been foreseen, such as playing Bach’s Goldberg variations
on the piano, or the first movement from Bach’s Partita
No.3 in E major on the violin.
Tiered or whorled branching systems (Figs. 6A–6I,
Figs. 7A–7G)
The conidiophores of several other hyphomycete genera,
such as Calcarisporium Preuss (Fig. 6A), Verticillium
Nees (Fig. 6B), Acrophialophora Edward (Fig. 6C),
Cladobotryum Nees (Fig. 6D), Helminthophora Borden
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Kendrick 83

Fig. 6. Conidiophores that are branched hyphal systems with persistent apical dominance (after Carmichael et al. 1980). Lateral
branches often develop in whorls or verticils, but are not always restricted to that arrangement, and there may be up to three levels of
branching, as in (I). Note that the conidia in this group of illustrations are formed in several different ways. (A) Calcarisporium,
(B) Verticillium, (C) Acrophialophora, (D) Cladobotryum, (E) Helminthophora, (F) Selenosporella, (G) Umbellidion,
(H) Geniculosporium, (I) Phaeostalagmus.

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84 Can. J. Bot. Vol. 81, 2003

Fig. 7. Further examples of branching conidiophores with apical dominance, though here the main apex is often sterile and may play a
role in protecting reproductive cells from arthropod grazing (after Carmichael et al. 1980, except Fig. 7D, which is after Ellis 1971).
Note the different patterns of arrangement, orientation, shape and development of the conidiogenous branches, and differing methods of
conidiogenesis. (A) Stachylidium, (B) Zanclospora, (C) Nomuraea, (D) Gonytrichum, (E) Spondylocladiopsis, (F) Chaetopsis,
(G) Chaetopsina.

(Fig. 6E), Selenosporella Arnaud ex MacGarvie (Fig. 6F),
Umbellidion Sutton & Hodges (Fig. 6G), Geniculosporium
Chesters & Greenhalgh (Fig. 6H), and Phaeostalagmus
Gams (Fig. 6I), have a main axis that gives rise to branches
in various ways. But these conidiophores all have some kind
of apical dominance, at least initially, like that seen in many
plants. Note that the fungi illustrated in Fig. 5 have no such
dominance, nor even a main axis, once branching begins.
Those shown in Fig. 6 retain apical dominance (a main axis)
until late in development. Calcarisporium (Fig. 6A) pro-
duces whorls of side branches at regular intervals, branches
that immediately become conidiogenous cells. It is important
to know how many such whorls may develop (though this
can vary according to available nutrition), and the number of
branches expected in each whorl. This may be relatively
constant, as in Calcarisporium, or variable, as in Verti-
cillium (Fig. 6B) and Acrophialophora (Fig. 6C). The
Cladobotryum illustrated here (Fig. 6D) tends to produce
just two opposite conidiogenous cells at each level. In
Helminthophora (Fig. 6E), one of the cells in a whorl may
itself branch distally to produce a cluster of conidiogenous
cells. Selenosporella (Fig. 6F) goes further, in that the lower
branches may become septate and act as subsidiary conidio-
phore axes giving rise to conidiogenous cells in whorls or in
terminal clusters. Umbellidion (Fig. 6G) is very similar to
Selenosporella (Fig. 6F). The Geniculosporium (Fig. 6H)

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presents a much more lax or open system, with branching
tending to be opposite or asymmetrical, and becoming fertile
only after considerable extension growth. Phaeostalagmus
(Fig. 6I) has three levels of branching, though there is con-
siderable asymmetry involved, and a striking change from a
darkly pigmented axis to almost colourless conidiogenous
cells. The conidiophores of these taxa can clearly be diag-
nostic, but will be of value in this way only if their charac-
ters are recognized, tabulated, and used.
Figure 7 presents further examples of apical dominance,
but here in some cases the apices are ultimately sterile.
Stachylidium Link (Fig. 7A) has a branching pattern very
similar to that of Selenosporella (Fig. 6F), but its conidio-
genous cells are differently shaped (and have different
conidium ontogeny), and there is the same kind of change in
pigmentation seen in Phaeostalagmus (Fig. 6I). Zanclospora
Hughes & Kendrick (Fig. 7B) has tightly whorled branches
which, though short, develop almost parallel to the main
axis. The branches in Nomuraea Maublanc (Fig. 7C) also
grow up alongside the stipe, but they develop terminal clus-
ters of secondary branches, giving them a penicillate appear-
ance. In most other genera, the branches angle away from
the main axis. While the conidiophores illustrated in Fig. 6
have an apical fertile cell, six of those illustrated in Fig. 7
(Stachylidium, Zanclospora, Gonytrichum Nees & Nees,
Spondylocladiopsis Ellis, Chaetopsis Greville, and
Chaetopsina Rambelli) often or always have a sterile or
setose apex. Gonytrichum (Fig. 7D) initially appears to have
whorled branches, but in fact each whorl arises from a very
short branch, called a collar hypha, which emerges just be-
low a septum in the main axis. Above the fertile whorls this
genus also produces sterile branches (a return to the basic
hyphal state?) that may or may not anastomose, depending
on the species (see also discussion of Menispora, Fig. 8G).
Spondylocladiopsis (Fig. 7E) has very short, opposite
branches just below the septa, which develop multiple
conidiogenous loci. Chaetopsis (Fig. 7F) has a long, setose
apex, and its side branches all produce secondary branches
in pairs or small clusters. Finally in this set, Chaetopsina
(Fig. 7G) has a long setose apex, and restricts its branching
and conidiogenesis to a zone in the middle of the conidio-
phore axis. Again, the conidiogenous cells arise from side
branches that grow up parallel to or around the main axis
(though this is not obvious in the drawing). There is a rela-
tively untapped wealth of characters in these genera that
could easily be incorporated in an identification-oriented
computer database.
Branching systems: miscellaneous (Figs. 8A–8H)
These illustrations show that the variation found in
conidiophores has yet other possibilities. Staphylotrichum
Meyer & Nicot (Fig. 8A) has a branching pattern similar to
that shown earlier in Oidiodendron (Fig. 3E). It develops al-
ternate side branches, which branch again. But here, instead
of fragmenting into thallic-arthric conidia, the side branches,
which arise at right angles to the subtending cell, develop
thick-walled, globose aleuriospores. Puciola De Bertoldi
(Fig. 8B) resembles the genera illustrated in Fig. 7, but in
addition to its sterile apex, has several equally long side
branches with sterile tips and lateral fertile cells.
Trichoderma Persoon (Fig. 8C) has a more normal-looking
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85
branching pattern, except that opposite lateral branches arise
at right angles to the main axis, and this is repeated by
the ultimate branches that become the conidiogenous cells,
producing a characteristic appearance.
The next three examples have similar conidiogenesis,
conidia arising synchronously on clustered or swollen
end-branches. The conidiophores also look similar, but
closer inspection reveals significant differences. In Botrytis
Micheli ex Persoon (Fig. 8D) branching is asymmetrical,
and the end cells have swollen fertile lobes. In Verrucobotrys
Hennebert (Fig. 8E) branching is again asymmetrical, but
the synchronous conidia arise on short side-branches rather
than swollen lobes. In Streptobotrys Hennebert (Fig. 8F)
branching is strictly dichotomous, and the main axis and pri-
mary branches show evidence of an almost unique, tightly
twisted development. There are only one or two other in-
stances of this last pattern (e.g., Spiralum Mulder), though
sinuous or coiled conidiophores, which might be regarded as
steps in this direction, are seen in such genera as
Ostracodermidium Mukerji, Bostrichonema Cesati, and
Malbranchea Saccardo. We have absolutely no idea why this
happens or what its significance might be. It may well be a
genetic quirk that has little or no selective advantage or dis-
advantage, but it certainly makes identification easy. The fer-
tile cells are not swollen. The twisting of the axes here
suggests that with one or two more genetic changes,
Streptobotrys might well end up producing helically coiled
conidia.
One unusual feature that does not arise from individual
conidiophores, but rather from encounters between neigh-
bouring conidiophores, is seen in Menispora Persoon. In
Menispora glauca Persoon and Menispora tortuosa Corda
(Fig. 8G) the long, sterile apical extensions of the conidio-
phores anastomose with each other wherever they touch. In a
densely sporulating colony, this has the effect of producing a
tightly woven mesh above the fertile zone, possibly protect-
ing the developing conidiogenous cells and conidia from be-
ing eaten by small arthropods (though we have no
experimental evidence for this hypothesis). A similar phe-
nomenon has been recorded for Gonytrichum.
Finally, Psammina Roussel & Saccardo (Fig. 8H) presents
the appearance of a conidiophore that branches repeatedly at
the apex, dichotomously or trichotomously. Yet eventually a
single multi-armed propagule (a staurospore) is released. It
may be pushing the envelope to describe this as a conidium,
though one of the principal features of these asexual spores
is that they are liberated from the cells that produce them.
Here the line between conidiophore and reproductive unit
has become blurred, and this will shortly lead us into a
renewed consideration of conidia (see below).
Conidiophores: conclusions
Analysis of branching conidiophores can reveal many
characters not previously considered, especially if the pro-
duction of conidia is also regarded as a form of branching.
The current version of my computer database of hypho-
mycete genera uses 157 characters to describe conidio-
phores. I found 24 that applied to branching, and these are
listed in Table 1. There is some deliberate redundancy be-
cause the same character can be described in different ways
by different users. For example, “side branches fertile” is
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86 Can. J. Bot. Vol. 81, 2003

Fig. 8. Further variations in branched conidiophores (see text) (after Carmichael et al. 1980 except Fig. 8G, which is after Hughes and
Kendrick 1963). (A) Staphylotrichum, (B) Puciola, (C) Trichoderma, (D) Botrytis, (E) Verrucobotrys, (F) Streptobotrys, (G) Menispora
(low power habit sketch), (H) Psammina.

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Kendrick 87

Table 1. Characters in existing large number of conidia. Yet Gliocephalotrichum is not a

database that refer to conidiophore
branching in hyphomycetes.
1 branch
3 branches
Apex branched
Branched
Branches alternate
Branches constricted at septa
Branches fragmenting
Branches opposite
Branches pendulous
Branches verticils
Branches whorls
Branching 2 levels
Branching 3 levels
Branching 4 levels
Branching 5 levels
Branching 6 levels
Branching penicillate
Bushy
Dichotomous
Fertile branches lateral
Fruticose
Metulae
Side branches fertile
Tree-like
also rendered as “fertile branches lateral”, and “bushy” is
also entered as “fruticose”. What can an analysis of conidio-
phores as branching hyphal systems (and conidiogenous
cells, as they produce a sequence of conidia) add to that list?
It is one thing to analyze conidiophores and dissect them
into their salient features (the “what” of the fungi). It is quite
another to provide convincing explanations for these features
(the “why” of the fungi). In many cases they must be shaped
by long-term ecological and (or) evolutionary pressures. For
example, Penicillium (Fig. 5B) has evolved conidiophores
that branch tightly, and often repeatedly, at their apices, to
produce numerous but compact conidiogenous cells of a spe-
cialized kind widely known as phialides. Each of these can
produce an extended series of small, more or less globose,
dry conidia without itself undergoing any growth. So a mini-
mum amount of energy is invested in the microscopic but
highly branched conidiophore, and no energy is wasted dur-
ing the production of huge numbers of very small, easily
dispersed conidia. One 2.5-cm diameter colony of
Penicillium can produce 400 000 000 spores. That goes a
long way toward explaining the success of this plurivorous
organism (though other features, such as possession of a
wide range of digestive enzymes, obviously play equally im-
portant roles). If each conidiophore consisted of a single
hypha with a single conidiogenous locus, the rain of spores
would not be so copious.
But there is another genus, Gliocephalotrichum (Fig. 5F),
which produces a conidiophore very similar in design to that
of Penicillium, and can therefore be assumed to liberate a
common or spectacularly successful fungus. So we must not
be too glib or dogmatic in our pronouncements about the
reasons for conidiophore configurations.
Another reason for caution lies in an apparently much less
sophisticated spore-generating system, the blastic-acropetal
branching found in Cladosporium (Fig. 2F). Despite this
seeming disadvantage, the conidia of Cladosporium make up
on average 33% (and in some cases as much as 65%) of total
spore counts in air samples taken around the world. This far
outstrips any other fungus, and may be due to the success of
this genus in colonizing dead plant parts, which are usually in
good supply. Nevertheless, convincing ecological explanations
of conidiophore configurations are scarce, and are likely to re-
main so until we know much more about the moulds.
From a consideration of Tables 1 and 2, it also becomes
clear that it is much easier for us to analyze the appearance
of an organism or an illustration and produce lists of charac-
ters than it is to take those lists of characters and recreate an
accurate illustration from them. This shows the imprecision
of language (at least as we are using it), and its tendency
to generalize. Nevertheless, computers can instantly
cross-check unique sets of those characters against a com-
prehensive database to arrive at accurate identifications.
One of the best potential sources of information should lie
in the original description of a taxon, which is normally
accompanied by diagnostic and explanatory illustrations. Af-
ter all, who should have spent more time poring over the
organism and weighing its various features than the original
author? Yet there are far too many examples of original
descriptions and illustrations that provide little in the way of
illumination, and where the micromorphology and develop-
ment of the organism have been elucidated only by more
careful investigators who subsequently re-examined the
organism. Those who are interested in making the hypho-
mycetes accessible to the general mycological public must
produce properly detailed descriptions of these organisms —
descriptions from which the information needed to build
interactive databases can be extracted. As an example I will
quote from the description of Zanclospora brevispora
(Fig. 7B) given by Hughes and Kendrick (1965). The words
in square brackets are more general terms or more recent
interpretations and (or) usage.
“The phialophores [conidiophores] are simple, arise singly
from swollen cells of the repent hyphae, and are crowded or
in a thin turf 100–175 (–220) µ [µm] high. They are gener-
ally straight, brown to dark brown, paler toward the distal
end, smooth-walled, 5.4–7.0 µ wide just above the basal cell
which is up to 13 µ wide, tapering gradually to 4 µ toward
the rounded apex. The cells of the phialophore are 14–18 µ
long toward the base and progressively shorter toward the
apex, where they are 3.6–5.0 µ long. The apical cell occa-
sionally bears a collarette and functions as a phialide, but
usually the apical 3 to 5 cells are sterile [forming a setose
apical extension].
The phialides [conidiogenous cells], which occur in whorls
of up to 7, arise just below the distal septa of a series of 4–6
(–8) cells of the phialophore below the generally sterile apex.
They are sessile, straight, narrowly ovoid to ovoid, generally
tightly adpressed to the phialophore, pale brown to subhyaline

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88 Can. J. Bot. Vol. 81, 2003

Table 2. Additional characters derived from the present analysis of conidiophore branching in
hyphomycetes.
Branching of conidiophores or conidiogenous cells can be:
General (not restricted to an apical or other zone) — Chrysonilia, Cladosporium, Tritirachium
Localized (restricted to a particular zone of the conidiophore) — Ceratocladium, Zanclospora
Apical only — Amblyosporium, Dichotomophthora, Phialocephala, Staheliella, Verticicladium
Lateral only (in taxa with sterile or setose apices) — Menispora, Zanclospora
Apical and lateral — Selenosporella, Umbellidion, Ditangium
Alternate — Sympodiella, Beauveria
Opposite — Tritirachium, Cladobotryum, Geniculodendron
Unilateral — Gonatophragmium, Menispora, Meria
Asymmetrical — Botrytis, Penicillium pro parte, Verrucobotrys
Helical — Leptographium, Acrodontium (conidial sequence as described by Wingfield et al. 2000)
Dichotomous — Balanium, Chrysonilia
Trifid (trichotomous) — Dichotomophthora
Quadrifid — Verticicladium
Cruciate — Dichotomophthora
Diffuse, open, or divergent — Virgaria, Tympanosporium, Hansfordia
Fully dichotomous — Balanium, Streptobotrys
Partly dichotomous — Staheliella
Contiguous — Haplographium, Leptographium, Penicillium, Phialocephala.
Synchronized* — Verticicladium, Gliocephalotrichum,
Radiating — Amblyosporium spongiosum, Pseudobotrytis, Gibellula
Clustered — Amblyosporium botrytis, Dichotomophthora, Staheliella, Verticicladium
Whorled — Acrophialophora, Calcarisporium, Gonytrichum, Verticillium, Zanclospora,
Setose apices or branches anastomosing — Menispora, Gonytrichum.
Other characters mentioned in the various discussions above:
Cells short
Cells of graduated length
Cells swollen
Constricted at septa
Conidiogenous hyphae distinctly narrower than the stipes from which they arise
Conidiogenous cells narrow progressively
Conidiogenous cells of constant width
Multiple sterile as well as fertile branches arise at the top of the stipe
Apical dominance
Apex sterile or setose.
Darkly pigmented axis, almost colourless conidiogenous cells
No. of whorls of branches and (or) conidiogenous cells
Side branches all produce secondary branches in pairs or small clusters
Tightly whorled branches develop almost parallel to the main axis
Branches angle away from the main axis (acute, obtuse, perpendicular)
Branching and conidiogenesis restricted to a fertile zone in the middle of the axis (proportion, percentage)
Alternate side branches, which branch again
Long side branches with sterile tips and lateral fertile cells
Opposite lateral branches arising at right angles to the main axis
End cells have swollen fertile lobes
Axis tightly twisted
*Contiguous plus synchronized equates to penicillate, but unlike the existing descriptor these terms do not assume any
knowledge of mycology.

[almost colourless], 6.4–9.4 (–12.0) µ long, 3.0–4.0 µ wide,
with an apical, hyaline to subhyaline, more or less fun-
nel-shaped collarette 2.0–2.8 µ wide and 1.4–2.1 µ deep.
The phialospores [blastic-phialidic conidia] are hyaline,
curved, and narrowly obovoid, being blunt at the distal end
and tapered at the other, 5.4–8.0 (–9.4) µ long, 1.4–2.0 µ
wide, non-setulate, non-septate, produced in slime and
finally enveloping the phialides in a straw-coloured to
alutaceous mass”.
That provides a fairly detailed analysis of the morphology
expressed by this fungus. If this description was properly
dissected and the information entered in a database, it is
probable that the fungus could be correctly identified using a
remarkably small character set. How many other fungi have

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Kendrick
such tightly adpressed whorls of conidiogenous cells on
an unbranched conidiophore? How many other fungi have
conidiophore cells that are progressively shorter toward a
sterile, pigmented apex? Chaetopsina fulva Rambelli looks
very similar, but nevertheless differs in all of these charac-
teristics. Ceratocladium microspermum Corda has conidio-
genous cells clustered around the main axis, but they arise
toward the base rather than the apex, are not in whorls just
below the septa, are not adpressed, have different conidio-
genesis, and the sterile apex is variously branched, the cells
becoming longer toward the apices.
Zanclospora brevispora appears to be a good example of a
hyphomycete that has a significant number of unique charac-
ters, most of them to do with the conidiophore and the ar-
rangement of the conidiogenous cells, rather than the conidia
(curved amerospores are not uncommon). In my database,
Zanclospora, and this genus alone, keys out on the following
two characters: (i) conidiophores having a setiform exten-
sion, and (ii) conidiogenous cells arising in a restricted
fertile zone. Other equally minimalistic combinations are
possible (and the progressively shorter conidiophore cells
have not even been added to the database as yet).
Not all hyphomycete taxa are so well-delineated or delim-
ited as Zanclospora, and variability in culture or on different
natural substrates undoubtedly produces overlaps in certain
quarters, where intertaxon distances are small to begin with.
But unique taxa (and there are still many thousands to be
discovered and described) will stand the test of time and
DNA.
Analysis of conidia
Helicosporous conidia (Figs. 9A–9F)
It is axiomatic that all conidia, no matter how bizarrely
shaped, are modified hyphae or hyphal systems. For exam-
ple, helicosporous conidia (Figs. 9A–9F) represent long,
multicellular hyphae that have become condensed by coiling.
The coiling may initially have evolved as one way of pro-
ducing a compact propagule in which the death of a single
cell, or in some cases of many cells, would not entail a com-
plete loss of viability, e.g., Vanbeverwijkia Agnihothrudu
(Fig. 9A), Helicomyces Link (Fig. 9B), Zalerion Moore &
Meyers (Fig. 9C). This remains to be experimentally tested.
The three-dimensional, barrel-shaped, closed, hollow pro-
pagules of Helicoon Morgan (Fig. 9D) and Helicodendron
Peyronel (Fig. 9E) are of similar origin, but they have
evolved a completely new function. These genera are repre-
sentative of what are called the aero-aquatic fungi, a special-
ized group that exploits dead leaves submerged in stagnant
ponds. These helicosporous fungi have several integrated
specializations, some of which are physical, some physio-
logical. They can grow in the almost anaerobic conditions
that prevail in the bottom of a pond during winter, but the
conidia are produced in air during summer. Their hollow,
hermetically sealed design ensures that after secession they
will float on the pond surface, thus being the first aquatic
fungi to encounter dead and dying leaves as they fall in
autumn (Michaelides and Kendrick 1982). In the microbial
world, being first into a new substrate can be vital in allow-
ing an organism to establish itself and to exclude potential
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89
competitors. The ecological imperatives underlying the hollow
helicospores seem well established. Note that the
Helicodendron shown in Fig. 9F does not really fit into the
aero-aquatic group (its conidia are not “biological bubbles” —
they do not float — and it was found on twigs and grass beside
streams). It might be better placed in another genus, and
another ecological group. Unfortunately, relatively few
clear-cut ecological groups have yet been delineated for
hyphomycetes.
But having provided possible evolutionary and (or) eco-
logical reasons for two- and three-dimensional coiling, we
need to extract useful taxonomic characters from the final
result. In such unusual fungi, one course is to base identifi-
cations almost entirely on the spore, and this certainly pro-
vides a lot of characters — the number of dimensions, the
number of coils, the length of individual cells, the thickness
of the coiling hypha, the length:width ratio of the spore, the
calculated number of cells (or septa) per conidium, the total
calculated length of the filament; and in two-dimensional
spores, whether the coiling begins from the centre and winds
outward, as it normally does in Helicogoosia
Holubová-Jechová, or, as in most others, winds inward from
the periphery toward the centre. But the kind of structure on
which the spore is produced, the number of spores per
conidiophore and their orientation to the hypha and to each
other may also be useful. For example, in Helicodendron
species, coiled conidia often give rise directly to further
conidia, something that does not happen in Helicoon. As far
as conidiogenesis is concerned, the very size and configura-
tion of the large three-dimensional conidia precludes certain
kinds of development. Such conidia are never
blastic-phialidic or blastic-percurrent. They are, in a sense,
thallic, though individual cells do not change much after be-
ing delimited. It is possible to describe the branching chains
of conidia seen in Helicodendron paradoxum Peyronel
(Fig. 9F) as blastic-acropetal, since the primordia of new
spores arise directly from one cell of an existing spore (not
usually the terminal cell), and the youngest spore is distal.
Each coiled structure can be considered an individual spore
(conidium) only if it becomes separated from the others in
the normal course of events. If the coils remained attached to
each other, the entire structure might be better termed a
propagule, or at least a compound spore.
An interesting footnote to this discussion of helicosporous
conidia concerns the perception and application of micro-
morphological characters in the first new hyphomycete ever
described by the author, Helicoma monospora Kendrick
(Kendrick 1958a). I placed it in the genus Helicoma strictly
on the morphology of its single propagule. It was subse-
quently realized that the conidia in the type species of
Helicoma are produced on denticles and are easily detached,
while those of Helicoma monospora Kendrick do not secede
readily. This brought about a redisposition of the fungus to
Troposporella Karsten, which also had spores with a broad
attachment to the subtending hypha (Ellis 1976). However,
Troposporella still has schizolytic secession (a septum
splits), albeit across a broad base rather than a narrow
denticle, while Troposporella monospora invariably exhibits
rhexolytic secession (a cell ruptures). So it was moved for
a second time, into a new genus, Slimacomyces Minter
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Fig. 9. A selection of helicosporous conidia, which are essentially modified single hyphae (though note the branched system in (F))
(after Carmichael et al. 1980). (A) Vanbeverwijkia, (B) Helicomyces, (C) Zalerion, (D) (a) Helicoon sessile, (b) Helicoon ellipticum,
(E) Helicodendron tubulosum, (F) Helicodendron triglitziensis.
(Minter 1986), where it now reposes in solitary splendour.
So mycology advances, detail by detail, a self-correcting
discipline like all others in science.
Tetraradiate conidia (Figs. 10A–10H and 11A–11H)
If the floating propagules of Helicoon exhibit their
unusual behaviour for an ecological reason, this must be
equally true for the immersed, tetraradiate propagules of
many other aquatic hyphomycetes, such as those illustrated
in Figs. 10 and 11, most of which occur in streams. Here we
find a different group of specializations. Formation of
conidia will take place only under water, and only in the
fast-moving, well-aerated water typical of many streams.
The configuration of these spores ensures that if they enter
the slow-moving boundary layer and come to rest on the sur-
face of a submerged leaf, they will always adopt the most
stable of all positions, the tripod, no matter which way they
land. This enables them to germinate quickly and establish a
foothold in the dead, submerged leaf, which is the substrate
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to which they are adapted. It is apparent from a comparison
of Figs. 10 and 11 that their morphogenesis follows two
main patterns, that resulting in three of the four arms point-
ing away from the conidiogenous cell, and that in which
three of the fours arms point toward the conidiogenous cell.
Tetraradiate conidia, although in many cases very similar
at maturity, also arise by several different modes of
conidiogenesis (some emerge from phialides, while others
are blastic-sympodial, and yet others are blastic-acropetal).
Although a discussion of conidiogenesis is beyond the scope
of this paper, the involvement of such diverse processes pro-
vides evidence that, while the tetraradiate group is ecologi-
cally coherent, it is made up of genetically diverse taxa that
have been molded into a similar mature morphology through
the processes of convergent evolution. Teleomorphs, where
these are known, support this argument.
I have just explored two cases in which the biological
“raison d’être” of the shapes or configurations of asexual
propagules is to some extent understood. But it should be
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Fig. 10. Tetraradiate staurosporous conidia of some amphibious hyphomycetes (after Carmichael et al. 1980). In these fungi the num-
ber of branches and the angle of branching is strictly prescribed by ecological considerations. In this set of examples, three branches
point upward (or at least away from the conidiogenous cell). (A) Clavatospora, (B) Articulospora, (C) Fontanospora, (D) Clavariopsis,
(E) Isthmotricladia, (F) Tetrabrunneospora, (G) Tetrachaetum, (H) Alatospora. Compare these illustrations with those in Fig. 11.

noted that spore morphogenesis has not, in most cases, been
properly analyzed, and that the reasons for the many other
shapes adopted by conidia are usually entirely unknown.
Morphogenesis and selection pressure (Figs. 12A–12E)
We can begin our analysis of these spores by asking two
questions: (i) How do they attain their shapes? (ii) What
evolutionary pressures have sculpted them? It is almost
always easier to answer the first question than the second,
because we can usually observe conidia at various stages of
development and derive plausible morphogenetic pathways.
Only rarely have we yet divined the selection pressures that
produce particular morphologies.
Kendrick (1971) analyzed some simple conidium shapes
and proposed a hypothesis to explain them that involved the
balance between “set” and “unset” wall at the apex of the

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92 Can. J. Bot. Vol. 81, 2003

Fig. 11. More tetraradiate staurosporous conidia. In this set of examples, three branches point downward (or at least toward the
conidiogenous cell) (after Carmichael et al. 1980). (A) Lemonniera, (B) Tetraposporium, (C) Actinospora, (D) Jaculispora,
(E) Trisulcosporium, (F) Flabellospora, (G) Porocladium, (H) Triscelophorus. Compare these illustrations with those in Fig. 10.

growing cell. Under normal conditions of cell extension
(hyphal growth), it was assumed that wall-setting and cell
expansion would be in a dynamic balance, and that there
would at any given time be a hemisphere of unset wall. If
wall-setting (the deposition of chitin fibrils) lagged behind
cell expansion, there would be more than a hemisphere of
unset wall, and the width of the resulting cell would in-
crease. If wall-setting overtook cell expansion, there would
be less than a hemisphere of unset wall, and the cell would
become narrower. So conidium development (in terms of the
shape that is ultimately produced) “may be regarded as a
result of a change or a series of changes in the relationship
between rate of blowing out and rate of wall-setting”
(Kendrick 1971).
For example, the unusual biconic shape of the conidia in
Beltrania Penzig (Fig. 12A), Beltraniella Subramanian
(Fig. 12B), Pseudobeltrania Hennings (Fig. 12C),
Beltraniopsis Batista & Bezerra (Fig. 12D), and
Rhombostilbella Zimmermann (Fig. 12E) could be accounted
for by an initial excess of blowing out over wall-setting, later
abruptly superseded by the wall-setting process overtaking the
blowing out. In many other cases, such as Murogenella Goos
& Morris, Phaeodactylium Agnihothrudu, Arthrosporium
Saccardo, Listeromyces Penzig & Saccardo, Pithomyces

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Fig. 12. Some biconic conidia, an unusual and highly diagnostic shape for which we have no functional or ecological explanation
(after Carmichael et al. 1980). (A) Beltrania, (B) Beltraniella, (C) Pseudobeltrania, (D) Beltraniopsis, (E) Rhombostilbella.
Berkeley & Broome, Trichophyton Malmsten, Bactridium
Kunze, and Microsporum Gruby, the transition between the
two phases is more gradual, resulting in a conidium that is
broadest in the middle, and narrower at either end. The profile
of each side of the conidium is in most of these cases a fairly
smooth curve.
Cole and Samson (1979) took the analysis further. Trans-
mission electron microscopy had revealed concentrations of
vesicles, termed secretory vesicles, at the tips of growing
hyphae, and of the developing helicosporous conidia of
Zalerion Moore & Meyers. Girbardt (1957, 1973) noted that
changes in the direction of growth of hyphae were preceded
by changes in the location of the spitzenkörper (a cluster of
secretory vesicles). Cook (1972, 1974) also demonstrated
small vesicles at the apices of the young, developing conidia
of Oedocephalum roseum Cook. Bracker (1977) found small
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93
vesicles at the tips of growing hyphae, and called them
“chitosomes”, assuming that they contain chitin synthetase.
In the growing tip of the Zalerion spore, the cluster of vesi-
cles is presumably excentrically distributed, concentrating
growth activity on one side of the cell. But if the cell is to
grow in more than a simple curve, activity must be spread
out over more than half of the apex.
Complex conidia as condensed branching systems:
introduction
The model outlined above may be adequate for conidia
whose development involves the activities only of a single
growing point. There are, however, many conidia of highly
characteristic shape for which this model would clearly be
inadequate. One of the more visually interesting examples
of this group is Dendrosporium Plakidas & Edgerton, the
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conidium of which resembles a miniature Christmas tree
(Fig. 16E). There must, of course, be good morphogenetic
(and evolutionary) reasons for this. I have concluded that
although the conidium has only one septum, and could
therefore be described as didymosporous, it is, in fact, a
highly condensed branched hyphal system. The lines super-
imposed on Fig. 16F show these almost suppressed axes,
and give this unique spore a comprehensible rationale. I note
here that we have already considered one or two such con-
densations in the section on conidiophores — for example,
the ultimate branching of the Dichotomophthora conidio-
phore (Fig. 4H) can be interpreted as a very condensed set
of branches.
Many other conidia may also be regarded as branching
hyphal systems. As soon as we begin to consider this aspect
of development, we need a standardized system of terminol-
ogy to describe it. I suggest that the following features (and
probably others) need to be taken into account: (1) the num-
ber of orders of branching represented; (2) the number of
hyphal apices generated; and (3) whether the branching is
(a) dichotomous, (b) opposite, (c) alternate, (d) unilateral
(asymmetrical), (e) whorled or verticillate, (f) in a helical or
spiral sequence, (g) in some combination of the above, (i) in
two dimensions, or (j) in three dimensions.
Of course, a fuller characterization of the propagule
would necessitate measurement of (4) overall dimensions;
(5) the length of the branches of each order; (6) the width of
the branches of each order; (7) the shape of individual cells,
where this is anything but cylindrical (e.g., in Atichia
Flotow, Fig. 14I), (8) the septation; and possibly other
aspects I have not listed. In the following paragraphs this
system of analysis is applied to a variety of conidial shapes.
Dichotomies and more (Figs. 13A–13J)
It might be assumed that any spore with pretensions to be-
ing a branched hyphal system would of necessity be septate.
In fact, this is not the case, as an examination of Tricellula
van Beverwijk (Fig. 13A), Speiropsis Tubaki (Fig. 15G) and
Riessia Fresenius (Fig. 16A), shows. Admittedly, the
conidium of Tricellula is about as simple a branching system
as one could envisage, with a cell giving rise to two out-
growths almost identical to itself. These may develop as a
dichotomy, or one may be apical and the other, lateral. The
three parts of this spore are delimited, not by septa, but by
narrow constrictions that may serve approximately the same
purpose (limiting damage, etc.). Later, other examples of
this phenomenon will be noted. The conidia of the type spe-
cies of Scolecobasidium Abbott (Fig. 13B) are also simple,
the upper of its two cells branching dichotomously. Those of
Dicranidion Harkness (Fig. 13C) branch dichotomously al-
most as soon as they are initiated, the two branches growing
upward in parallel and becoming septate. The pigmented
conidia of Cheiromycella Hoehnel (Fig. 13D) develop very
similarly, though the drawings show how easy it is to distin-
guish the two taxa. The conidia of Iyengarina Subramanian
(Fig. 13E) are basically dichotomous, but unique features are
associated with this pattern: a pigmented central cell, and
rapidly tapering, horn-like branches. Those of Diplocladiella
Arnaud ex Matsushima (Fig. 13F) are likewise dichotomous
and tapering, but are evenly pigmented, and the two arms,
though sharply pointed, are not as attenuated. Triposporina
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Hoehnel (Fig. 13G) produces a much less hypha-like and
more highly modified conidium, but on examination it is
quickly revealed as twice dichotomous — that is, there are
two orders of branching, and four apices are produced in
three dimensions. The conidia of Engelhardtiella Funk
(Fig. 13H) are basically dichotomous, but each of the axes,
after being delimited by a septum, produces three extremely
condensed branches. So there are two levels of branching,
six apices, and at least an attempt to branch into the third
dimension. The conidium of Heliscus Saccardo (Fig. 13I) is
once trichotomous (or trifid or trifurcate) at its apex, exhibit-
ing one level of branching, with three apices in three dimen-
sions. Since this is an aquatic hyphomycete, we may assume
that this is a bow in the direction of the tetraradiate mor-
phology, so common among this ecological group of fungi,
which was discussed earlier in this paper. The conidia of
Heliscus are didymosporous and, rather unusually for co-
nidia of this shape, arise from phialides. The conidia of
Cheiromyces Berkeley & Curtis (Fig. 13J) resemble an up-
stretched hand (digitate or palmate), and are described as
cheiroid. There is only one order of branching, and three to
five hyphal apices are generated in three dimensions.
Open branching systems: branches divergent
(Figs. 14A–14I and 15A–15G)
Figure 14 shows a number of conidia in which the
resemblance to branched hyphal systems is clearer.
Lambdasporium Matsushima (Fig. 14A) produces asymmet-
rical staurospores with two tapering arms, one being the side
branch. In Pleuropedium Marvanova & Iqbal (Fig. 14B),
which also has tapering arms, the side-branch develops its
own side branch. There is only a small increase in complex-
ity from Lambdasporium to Pleuropedium. Tetracladium De
Wildeman (Fig. 14C) differs in having a central axis (apical
dominance again) that gives rise to two orders of lateral
branches, the ultimate branches being nonseptate, narrow,
and tapering, and having five hyphal apices. The branching
pattern is basically opposite but partly unilateral, and
appears to be two-dimensional. The conidia of Ingoldiella
Shaw (Fig. 14D) are large staurospores with long, multi-
septate, unilateral arms that are diagnostic because they have
a low-profile clamp connection at each septum and because
the ends of the arms are tightly curled. There is one order of
branching, and four hyphal apices in two dimensions. The
staurospores of Taeniospora Marvanova (Fig. 14E) are basi-
cally just a hypha with two side branches that may be alter-
nate or unilateral. Three new hyphal apices are generated in
two dimensions. These rather extensive spores may have no
more than one septum, at a clamp connection, which reveals
their dikaryotic basidiomycetous nature. However, I note
that many basidiomycetous anamorphs do not produce
clamp connections, and so are not so easily placed as the
two just discussed. The staurosporous conidia of
Polycladium Ingold (Fig. 14F) branch randomly, oppositely,
or unilaterally, and look untidy — in fact, they don’t look
like conidia at all: more like recently germinated spores —
but have about six hyphal apices in three dimensions. The
staurospores of Gyoerffiella Kol may be rotary, as in
Gyoerffiella rotula (Hoehnel) Marvanova (Fig. 14G), but
other species (Fig. 14H) are uncoiled and show a more nor-
mal branching system with strongly tapered and pointed
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Kendrick 95

Fig. 13. Some conidia which represent simple branched systems (after Carmichael et al. 1980). (A–F) a single branching, (G–J) two or
more branches. (A) Tricellula, (B) Scolecobasidium, (C) Dicranidion, (D) Cheiromycella, (E) Iyengarina, (F) Diplocladiella, (G)
Triposporina, (H) Engelhardtiella, (I) Heliscus, (J) Cheiromyces.

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96 Can. J. Bot. Vol. 81, 2003

Fig. 14. Some staurosporous conidia that, while retaining their uniqueness, are clearly branched hyphal systems (after Carmichael et al.
1980). Note that two (D and E) are dikaryotic basidiomycetous anamorphs with clamp connections. (A) Lambdasporium,
(B) Pleuropedium, (C) Tetracladium, (D) Ingoldiella, (E) Taeniospora, (F) Polycladium, (G) Gyoerffiella rotula, (H) Gyoerffiella
craginiformis, (I) Atichia.

arms: two levels of branching produce four hyphal apices in
two dimensions. Richly branched staurospores are developed
by Atichia (Fig. 14I), though deep constrictions between the
cells give these propagules an unusual appearance (a similar
phenomenon is seen in Figs. 13A, 15G, and 16A). They
have two levels of branching and, in the example shown, 14
hyphal apices which seem to be in two dimensions.
Figure 15 shows several examples of staurosporous
conidia with open architecture, which fairly obviously con-
form in various ways to the idea of branching hyphae. Those
of Varicosporium Kegel (Fig. 15A) are more or less dichoto-
mous, with three levels of branching, generating five to
seven apices, and growing in three dimensions. The stauro-
spores of Scorpiosporium Iqbal (Fig. 15B) are very similar,
but the bases of the branches are not constricted. There are
two levels of branching and four apices in three dimensions.
Varicosporina Meyers & Kohlmeyer staurospores (Fig. 15C)
are also dichotomous, but with shorter, wider cells, one or
two levels of branching, and two or three apices in two di-
mensions. The propagule of Tricladium Ingold (Fig. 15D)
presents an interesting problem for our system of analysis. It
may be interpreted as having a single axis that branches al-
ternately, in which case there would be only a single order
of branching. Alternatively, it may be regarded as branching
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Fig. 15. Staurosporous conidia with open architecture and various kinds of branching. Some have constrictions rather than septa at the
bases of the branches (after Carmichael et al. 1980). (A) Varicosporium, (B) Scorpiosporium, (C) Varicosporina, (D) Tricladium,
(E) Dendrosporomyces, (F) Dendrospora, (G) Speiropsis.
more or less dichotomously, in which case there would be
three orders of branching. Clearly, this kind of impasse can
be resolved only by observing the development of the
conidium directly.
The next two examples show apical dominance.
Dendrosporomyces Nawawi, Webster & Davey (Fig. 15E)
has a central axis producing seven or eight side branches,
some of which may also develop one or more side branches.
Thus all branching is lateral, there are two orders of branch-
ing, and 9 to 15 apices develop in three dimensions. Other
potentially useful characters are that the branches arise more
or less at right angles to the axis, and that they are con-
stricted at the base, as well as slightly tapered toward their
apices. Dendrospora Ingold (Fig. 15F) is simpler, but still
has two levels of branching, and five apices in three dimen-
sions. Branches are again more or less perpendicular to the
cells from which they arise, and are again somewhat con-
stricted at the base. Last in this group is Speiropsis Tubaki
(Fig. 15G), the conidia of which have two orders of branch-
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97
ing, generate three to five hyphal apices, have basically al-
ternate or dichotomous branching, and appear to be more or
less two-dimensional. An unusual feature, and doubtless one
of evolutionary significance, is the absence of septa, which
appear to be replaced by regular constrictions. It is interest-
ing, and taxonomically useful, that this pattern seems to be
restricted to the conidia.
Looking at Fig. 15 carefully, it becomes apparent that
many more characters could be added to those I have delin-
eated — characters describing the angle at which branches
diverge, the distance between successive branches, the cur-
vature of branches, and the width and taper of branches. It is
also probably significant that three of the fungi illustrated in
Fig. 15, while being regularly and even closely septate (for
example, Figs. 15E and 15F), delimit their branches at the
base by constrictions rather than by septa.
Condensed branching systems (Figs. 16A–16F)
Figure 16 presents a few less obvious examples where the
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98 Can. J. Bot. Vol. 81, 2003

Fig. 16. Staurosporous conidia that represent highly condensed or otherwise unorthodox branching systems (after Carmichael et al.
1980). (A) Riessia, (B) Pyramidospora, (C) Uvarispora, (D) Desmidiospora, (E and F) Dendrosporium.

Fig. 17. Staurosporous conidia that are analogues of radial colony development (after Carmichael et al. 1980). (A) Psammina,
(B) Brachiosphaera, (C) Flabellospora, (D) Arachnophora, (E) Petrakia, (F) Orbimyces.

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Kendrick
process of condensation has progressed to two extremes: the
reduction of branches to globose cells, and the reduction of
branches to small and inconspicuous marginal lobes. The
conidium of Riessia Fresenius (Fig. 16A) can be regarded as
a quadrifid branching of the subtending hypha, but the four
wedge-shaped extensions do not look much like normal
hyphae, and are not delimited by septa. Nevertheless we can
suggest that there is one level of branching, and that four
new apices arise in two dimensions. The Pyramidospora
Nilsson conidium (Fig. 16B) seems to be a condensed ver-
sion of apical dominance, with two whorls of side branches.
We can recognize two orders of branching, up to eight
hyphal apices are generated, and the spore develops in three
dimensions. Uvarispora Goos & Pirozynski (Fig. 16C) is
much more complex. Looking at this raspberry-like mass of
rounded cells it is hard to judge how many levels of branch-
ing are present, though I am prepared to suggest five. The
number of hyphal apices is also large and difficult to count,
perhaps at least 30, and the whole has definitely expanded
in three dimensions. The spore of Desmidiospora Thaxter
(Fig. 16D) is two-dimensional — it could be described as
peltate — and much easier to parse. It does indeed look
rather like a desmid (a green alga) in shape. There are three
orders of branching, and there are 26 hyphal apices in the
spore that is drawn in face view. This spore resembles a
miniature, radially growing colony, though what constrains
it to two dimensions is not obvious. Considering the
conidium of Dendrosporium Plakidas & Edgerton ex Crane
(Figs. 16E and 16F) as a condensed hyphal system, we find
apical dominance, with traces of two orders of branching
(six opposite side branches off the main axis, and another
branching in progress at the end of each side branch). No
fewer than 15 almost suppressed hyphal apices are present
(they are indicated by lines in Fig. 16F), and branching oc-
curs in two dimensions. These are all valuable characters
that can be used in a synoptic key.
Analogues of colony development (Figs. 17A–17F)
Finally, Fig. 17 presents a wide spectrum of propagules.
There are three obvious analogues of colony development.
Psammina Roussel & Saccardo (Fig. 17A), in which the sin-
gle, radially branching propagule seems to have two levels
of branching, producing 29 apices more or less in two
dimensions (compare it with Desmidiospora). In
Brachiosphaera Nawawi (Fig. 17B) a single order of
branches radiate perpendicularly from a globose central cell,
producing up to six apices in three dimensions.
Flabellospora Alasosadura (Fig. 17C) has a single order of
branching and seven apices seemingly in two dimensions.
At the other end of the scale is Arachnophora Hennebert
(Fig. 17D) in which the hyphal system is so distorted as to
be almost indistinguishable. Nevertheless, it is possible to
perceive two levels of branching, producing at least 12 api-
ces in three dimensions. In this unique fungus, the two cells
of the main axis are large and swollen, while the first level
of branching is in the form of much smaller but still swollen
satellite cells, and the second level of branching is made up
of very narrow, tapering, recurved cells. The selection pres-
sures that moulded this unusual configuration are not under-
stood. The apex in Petrakia Sydow & Sydow (Fig. 17E) has
clearly become pseudoparenchymatous (in spore terms, that
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99
roughly means dictyosporous) before sending out a single
order of six or more radiating branches, which look rather
like premature germ tubes. Orbimyces Linder (Fig. 17F) has
a hugely swollen basal cell, but the two levels of branching
arising from this are more hypha-like, and give rise to nine
apices in three dimensions.
Scanning through thousands of illustrations of
hyphomycetes, it became clear to me that more than
150 genera — from Acrodictyopsis to Xenoheteroconium —
produce conidia that can be considered as branched hyphal
systems. And once we consider the various sequences of
multiple conidium formation in addition to the more visually
obvious patterns of branching, it becomes clear that the
sporulating structures of a majority of hyphomycetes can
also be regarded as modified branching hyphal systems. I
hope mycologists working with these fungi will consider the
points I have raised, will take a fresh look at the conidio-
phores and propagules they encounter, and think of them in
terms of the (sometimes well-hidden) mycelial motif. If
computers are to be used successfully in the identification of
hyphomycetes, which now include well over 1000 genera
and many thousands of species, we will have to take advan-
tage of the full range of characters they exhibit. I intend to
add the sorts of characters outlined in this paper to my own
computer database (ANAMORPH.ASK), in the hope that it
will thus become both more versatile and more precise.
I will close by repeating a comment I recently encoun-
tered in the literature: “Molecular phylogenetics, classical
morphology and field observation must be used together to
provide a holomycological approach to fungal classification.
Without this approach, confusion can…ensue…”
(Hywel-Jones 2002). Don’t throw out your light microscopes
or your field clothing. Neophyte mycologists take heart:
there are unknown hyphomycetes in infinite diversity out
there, awaiting your discovery and properly detailed descrip-
tion.
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