Classical morphology in zygomycete

taxonomy1
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11

I Gerald L. Benny

Abstract: Classification of Zygomycetes has evolved with the description of new taxa and the
rediscovery and redescription of known species. Taxonomy of orders in Zygomycetes is based on the
morphology of the spore forming structures, sporangia and (or) sporangiola, or merosporangia. Some
organisms produce only zygospores, azygospores, chlamydospores, or a combination of these structures.
The occurrence and morphology of any of the aforementioned structures and others (e.g., stolons and
rhizoids, apophyses, branching pattern, fertile vesicles) are used to ascertain the phylogenetic
relationships in Mucorales. Our understanding of the morphology, development, and phylogeny of
Zygomycetes has been enhanced by using microscopic observations and cladistic analysis of data sets
derived both from small subunit rDNA and morphology. Many morphological characters (e.g., trophocyst,
yeast cell formation) still appear to be reliable phylogenetic indicators while others (e.g., spore
morphology) are too variable. The value of zygospore morphology is reduced because the sexual spore
has never been reported for many taxa. Many characters used to circumscribe rnucoralean families
probably do not indicate relationships but still are useful in identification. Sporangiola should be
considered indistinct from sporangia.
Key words: cladistics, morphology, Mucorales, phylogeny, sporangia, sporangiola.
For personal use only.

RCsurnC : La classification des zygomycbtes a CvoluC avec la description de nouveaux taxons ainsi que
la redkcouverte et la redescription des espbces connues. La taxonomie des ordres chez les zygomycbtes,
est baste sur la morphologie des structures formant les spores et (ou) les sporangioles, ou sporanges.
Certains organismes produisent seulement des zygospores, des azygospores, ou des chlamydospores, ou
une cornbinaison de ces structures. La presence et la morphologie de chacune des structures
mentionnCes et d'autres (p. ex., stolons et rhizo'ides, apophyses, patron de ramification, vCsicules
fertiles) sont utilisees pour Ctablir les relations phylogCnCtiques chez les mucorales. Notre
comprChension de la morphologie, du dCveloppement, et de la phylogCnie des zygomycktes a it6
amCliorCe par l'utilisation des observations microscopiques et l'analyse cladistique des ensembles de
donnCes obtenues a la fois de la petite sous-unite du rADN et de la morphologie. Plusieurs caractkres
morphologiques (p. ex., trophocyste, formation de cellules levuriformes) apparaissent toujours comme
des indicateurs phylogCnCtiques fiables alors que d'autres (p. ex., morphologie sporale) sont trop
variables. La validit6 de la morphologie des zygospores est rCduite parce que la spore sexuelle n'a
jamais CtC rapportCe chez plusieurs taxons. Plusieurs caractkres utilists pour circonscrire les familles du
mucorales n'indiquent probablernent pas de relations mais demeurent utiles pour l'identification. Les
sporangioles devraient Ctre considCrCs comme des formes indistinctes des sporanges.
Mots clLs : cladistiques, morphologie, mucorales, phylogCnie, sporanges, sporangioles
[Traduit par la rkdaction]

Introduction anamorph. In Zygomycota, there is one notable exception to

using the anamorphic name. Syzygites Ehrenb. :Fr. (Hesseltine
Barr (1992) includes four phyla in Fungi: Ascomycota,
1957) is a mushroom parasite that produces sporangia (ana-
Basidiomycota, Chytridiomycota, and Zygomycota. Unlike
morph genus: Sporodinia Link) and zygospores (teleomorph
the former two phyla in which the names are based on the
genus: Syzygites) on separate hyphae and at different times
characteristics of the teleomorph (Greuter 1988; Article 59.1
in nature.
of the International Code of Biological Nomenclature), in
Zygomycetes, as presently delimited, consist of seven
Chytridiomycota and Zygomycota taxonomy is based on the
orders: Dimargaritales, Endogonales, Entomophthorales,
Glomales, Kickxellales, Mucorales, and Zoopagales (Benjamin

I
Received August 15, 1994. 1979; Benny 1982; Humber 1989; Morton and Benny 1990).
Harpellales, a zygomycete according to Benjamin (1979),
G.L. Benny. Department of Plant Pathology, 1453 Fifield Hall, is included in Trichomycetes (Lichtwardt 1986) and, there-
University of Florida, Gainesville, FL 3261 1-0680, U.S.A. fore, will not be treated further in this discussion. Classifica-
' This paper is Journal Series No. R-04269 of the Florida tion and identification of Zygomycota are based o n (i) the
Agricultural Experiment Station, Gainesville. type of asexual reproductive structures formed (sporangia,
Can. J. Bot. 73(Suppl. 1): S725-S730 (1995). Printed in Canada 1 Imprimt au Canada

sporangiola, merosporangia, chlamydospores, arthrospores,
and yeast cells); (ii) the branching pattern of aerial hyphae
(simple, or sympodially, verticillately, or dichotomously
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11
branched); and (iii) the presence of septa, if formed, and if
produced their frequency, location, and ultramorphology.
Morphology of zygospores, if present, has been consid-
ered important at the ordinal level (Benjamin 1979), but also
can typify families or genera in Mucorales. Of lesser impor-
tance are growth requirements, spore morphology, and size
of structures.
The purpose of this paper is to discuss the criteria used in
classification of Zygomycota and to present examples of
those characters and character states in which terminology
has changed.
Taxonomy
The orders of Zygomycetes have been discussed elsewhere
(Benjamin 1979; Benny 1982). Dimargaritales, Kickxellales,
and Zoopagales have changed little in the last 15 years
and excellent descriptions of these orders can be found in
Benjamin's publications (Benjamin 1958, 1959, 1961, 1963,
1965, 1966, 1979, 1985a, 19856). Changes in the classifi-
cation of Entomophthorales, since the order was reviewed
by Benjamin (1979) and Tucker (1981), have resulted in a
six-family system (Humber 1989). Six of the endomycor-
For personal use only.
rhizal genera in Endogonales (Gerdemann and Trappe 1974;
Benjamin 1979), those producing azygospores or chlamydo-
spores, were transferred to a new order, Glomales, and the
Endogonales emended to contain only the saprobic or ecto-
mycorrhizal genera forming zygospores (Morton and Benny
1990). Here I will concentrate on classification of Mucorales.
The Mucorales contain fungi that reproduce asexually by
endospores produced by cleavage-plane formation in sporangia
and (or) sporangiola or merosporangia (O'Donnell 1979),
unispored merosporangia (Zheng et al. 1988), and sporan-
giola (Benny and Benjamin 1975, 1976; Shipton and Lunn
1980) are also known. Asexual reproduction also may occur
by production of yeast cells, chlamydospores, and arthro-
spores. Sexual reproduction by zygospore formation is known
for many, but not all, taxa. Zygospores usually are rough
walled and dark walled. Suspensors are appendaged in
Phycomyces, Radiomyces, Parasitella, and some species of
Absidia, but the remaining Mucorales are nonappendaged
(Zycha et al. 1969). Members of Choanephoraceae (Kirk
1984) and Pilobolaceae (Grove 1934; Kirk and Benny 1980;
Hu et al. 1989) produce zygospores with apposed suspensors
below the surface of the substrate whereas most of the other
taxa form sexual spores at or above the substrate on opposed
suspensors. Septa, which are multiperforate, are normally
formed to wall off old or injured hyphae or reproductive
structures. In Sigmoideomycetaceae, however, septa are regu-
larly formed and the fertile hyphae disarticulate at maturity
(Benny et al. 1992). Most members of Mucorales are saprobes
with a few species being facultative parasites that can be readily
cultured in the laboratory. Sigmoideomycetaceae cannot be
grown without a host.
Many of the characters produced by Mucorales are con-
sidered advanced by Benjamin (1959) and Hesseltine and Ellis
(1973) including production of (i) sporangiola (vs. sporangia),
(ii) merosporangia (vs. sporangia or sporangiola), (iii) an
Can. J . Bot. Vol. 73 (Suppl. I ) , 1995
apophysis (vs. no apophysis), (iv) stolons and rhizoids (vs.
sporophores arising directly from the substrate), (v) branched
sporangiophores (sympodial, verticillate, umbellate, dichoto-
mous, etc.) (vs. unbranched), (vi) zygosporangial wall orna-
mented and pigmented (vs. smooth and more or less hyaline),
and (vii) zygospore suspensors apposed, appendaged, and
heterogamous (vs. opposed, nonappendaged, and more or
less equal). Other character states include being a parasite
(vs. saprobe), homothallic (vs. heterothallic), unispored spor-
angiola (vs. multispored), and spinose fertile branches (vs.
nonspinose).
The taxonomy of Mucorales has evolved with the discovery
of new taxa. All structures that can be observed with the light
microscope were noted by early students of Mucorales. The
structures associated with sporangiospore formation were, and
still are, used to classify members of this order because they
are always present. The production of sterile spines, elaborate
branching, and unispored sporangiola by Chaetocladium and
Dichotomocladium resulted in their being placed in a separate
family, Chaetocladiaceae (Benny and Benjamin 1993). Exces-
sive importance being accordedto a structure, such as the uni-
spored sporangiolum (conidium of some authors), has resulted
in the proposal of polyphyletic families (Choanephoraceae
of Zycha et al. (1969); Cunninghamellaceae of Pidoplichko
and Mil'ko (1971) and Mil'ko (1974)). The polyphyletic
Mucoraceae and Thamnidiaceae have also been segregated into
smaller, supposedly monophyletic families: the ~ u c o r a c e a e
into Absidiaceae, Dicranophoraceae, Mucoraceae sensu lato,
Phycomycetaceae, and Gilbertellaceae (Benny 1991; see Benny
and Benjamin 1993 for the generic distribution (Protomyco-
cladus (Schipper and Samson 1994) would be a member of
Absidiaceae)). Two families, Chaetocladiaceae (Benny and
Benjamin 1993) and Mycotyphaceae (Benny et al. 1985)
have been removed from Thamnidiaceae. These families are
based on combinations of characters explained by von Arx
(1983), Benny et al. (1985), Benny (1991), and Benny and
Benjamin (1993).
The ability to observe small structures, e.g., the discoid
columella of Chaetocladium (Benny and Benjamin 1976),
has been facilitated by the availability of better microscope
optics. Transmission electron microscopy has confirmed struc-
tures demonstrated with the light microscope or has revealed
new processes such as spore ontogeny. Scanning electron
microscopy (SEM) has been most useful in showing surface
detail, especially ornamentation of sporangia, sporangiola,
merosporangia, and zygosporangia.
Two other methods currently available have recently
produced very interesting mucoralean phylogenies. Cladistic
analysis of comparative sequence analysis of the 18s rDNA,
and on morphological data sets, also appear to be two impor-
tant means of determining phylogeny in Mucorales.
Problems in taxonomy of Mucorales
Many terms have been in use during the history of studies on
Zygomycetes. Some of these have recently been restricted
(sterigma and now pedicel; the structure that supports a
sporangiolum) or abandoned (conidium, which was formerly
used for a unispored sporangiolum). The term stylospore was
in common use in the early literature on Mortierellaceae,
especially in descriptions of ort tier el la spp. Stylospore is an
 E2.4. Benny
obsolete term for a spore terminating a stalk or hypha, espe-
cially a uredospore. In current literature on Mortierellaceae
the stylospore is a chlamydospore (Benjamin 1978).
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11
In Mortierellaceae, sporangiospores are produced in struc-
tures called sporangia even though the columella is extremely
reduced (hemiconvex to flattened and septurnlike). This spor-
angium may be uni- or multi-spored. Under current definition,
it might be more appropriate to consider the sporangium of
some, if not all, members of Mortierellaceae a sporangiolum.
The sporangiola of some mucoralean fungi can be almost as
large as the sporangia, e.g., Pirella circinans Bain. (Benny
and Schipper 1992).
Dissophora decumbens Thaxter (19 14) is an example of a
fungus that was not in culture for many years. Dissophora
decumbens has always been recognized as a distinct species
unlike other members of Mortierellaceae that have been reduced
to species of Mortierella. Although he had D. decumbens in
culture the fungus died during a collecting trip and, as a
result, Thaxter was able to provide excellent illustrations of
this fungus but an incomplete species description. Nothing was
written about the colony appearance or odor (Mortierellaceae
characteristically produce a wavy or zonate colony and a
garlic- or onion-like odor), or the temperature used to culture
the fungus (Thaxter 1914). Gams and Carreiro (1989) later
redescribed D. decumbens stating that it had a garliclike
odor, and an optimal growth temperature of 20°C, and pro-
For personal use only.
duced stolons and chlamydospores. The stolons were described
as being vegetative filaments of indeterminate growth by
Thaxter (1914). The different terminology used to describe
the Dissophora stolon might also be encountered when com-
paring the descriptions of other taxa. The chlamydospores of
Dissophora were described for the first time by Gams and
Carreiro (1989).
Differences in the interpretation of species characters must
be taken into account when reviewing the descriptions of all
fungi. The reader can be greatly aided by the presence of
high-quality photographs and (or) drawings, such as those
provided by Thaxter for most of the fungi he described. The
publication of new taxa accompanied by poor descriptions
and illustrations may cause subsequent workers difficulty in
identification. Type material is often not available for many
species (never deposited, lost, or cannot be sent out on loan).
Isolates of many classical species of Mucorales have been
deposited in culture collections that were derived from the
holotype specimen or authenticated by the original author.
Study of these cultures may clarify descriptions and (or)
illustrations when types are missing.
Historically, the general morphology of asexual and sexual
reproductive structures (see the character states listed above)
of mucoralean fungi have been accurately described, although
it is done inconsistently for some characters (e.g., ornamen-
tation of sporangiolar, sporangial, and zygosporangial walls,
and mode of spore release). Sporangial and sporangiolar
walls have often been said to be encrusted. Presumably these
structures are covered with calcium oxalate crystals. The
morphology and distribution of surface structures are well
illustrated using the SEM (Cole and Samson 1979; O'Donnell
1979). The morphology of crystals, however, can be modi-
fied if water stands on the surface (Benny and Khan 1988;
Benny and Samson 1989). These crystals might also be washed
away during critical-point drying prior to observation with
SEM. Natural crystal morphology and distribution, as well
as other surface detail, are probably best observed in fungi
that have been air-dried and not critical-point dried before
examination with the SEM.
Four calcium oxalate crystal types were identified on the
sporophores and sporangial walls of Gilbertella persicaria
(Eddy) Hesseltine (Whitney and Arnott 1986). Aberrant crys-
tals can be observed on G. persicaria under some cultural
conditions (Whitney and Arnott 1988). Additional crystal types
were observed on Mucor hiemalis Wehmer and Rhizopus
oryzae Went. & Prinsen Geerl. (Powell and Arnott 1985).
Cole and Samson (1979) and O'Donnell(1979) also show the
presence and distribution of calcium oxalate crystals on
many other members of Mucorales. Distinct sporangiolar
ornaments have been observed in species of Radiomyces
(capitate with a calcium (probably calcium oxalate) crystal
in the apex), and Hesseltinella vesiculosa Upadhyay and
Cunninghamella spp. (long needlelike spines with a hexagonal
base) (Shipton and Lunn 1980; Benny and Khan 1988). Other
taxa, e.g., Echinosporangium transversale Malloch and
Ellisomyces anomalus (Hesseltine & Anderson) Benny &
R.K. Benjamin, have smooth-walled sporangiola (O'Donnell
1979). A survey of all Mucorales would be necessary to deter-
mine the taxonomic value of aerial structure ornamentation.
Other characters of possible taxonomic importance are the
nature and ornamentation of the zygosporangial wall. Schipper
et al. (1975) identified four basic zygosporangial ornamenta-
tion types (a, b , c, d ) after their examination of selected
species of Mucor, Zygorhynchus, Parasitella, Rhizomucor,
and also Absidia spinosa Lendner, Phycomyces blakesleeanus
Burgeff, and Syzygites megalocarpus Ehrenb. :Fr. Mucor and
Zygorhynchus were divided into five groups (A,, A,, B1,
B,, C) based on zygosporangial ornamentation. Von Arx
(1983) transferred the Mucor spp. from the Al group (those
taxa with sympodial or racemosely branched sporophores,
sphaeroid or ellipsoid sporangiospores, and zygosporangia
with reddish-brown walls bearing starfishlike ornaments) into
a new genus, Circinomucor. Zygosporangial ornaments were
recorded for Backusella and additional Mucor species by
Stalpers and Schipper (1980) and several other genera
including Benjaminiella, Gilbertella, Mycotypha, Rhizopus,
Syzygites, and Zygorhynchus (O'Donnell et al. 1977, 1978;
O'Donnell 1979; Schipper 1984; Benny et al. 1985). The
zygosporangial ornaments of the other zygospore-producing
Mucorales need to be examined before any conclusions can
be reached regarding the taxonomic value of this character.
The carbonaceous (dark and relatively opaque, and readily
broken) versus the noncarbonaceous (brown to hyaline, trans-
lucent to transparent, and not easily broken) nature of zygo-
spores might also be a useful character state. There is very
little information in the literature regarding this aspect of the
zygosporangial wall. Zygospores have never been reported
for many taxa of Mucorales and, therefore, the value of any
potential character of the zygospore, zygosporangium, and
suspensors is limited.
Another problem that can be encountered is the taxon with
highly variable morphology, as has been recently described
for Umbelopsis nana (Linnemann) von Arx (Kendrick et al.
1994). Species variability makes it difficult to determine
character states for a particular taxon. Other taxa, e.g.,
Cokeromyces recurvatus Poitras and Mycoty~ha africana

Novak & Backus (Benny and Benjamin 1976), are morpho-
logically stable. It is important to culture mucoralean fungi
under optimal conditions to determine character variability.
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11
It is often difficult to delimit some character states, such
as sporangiospore morphology, where the majority of species
in Mucorales exhibit a range in morphology from globose to
irregular or angular, as seen in Thamnidium elegans Link
(Benny 1992). Many taxa, however, have spores that are
within this range of variation, e.g., globose to ovoid (Circinella
umbellata van Tiegh. & Le Monn.; Hesseltine and Fennel1
1955) or ellipsoid to ovoid spores (7hamnostylumpiriforme
(Bain.) von Arx and Upadhyay (Benny and Benjamin 1975);
Mucor mucedo L. :Fr. (Schipper 1975)). Other characters are
easy to define and are restricted to a few taxa, including spor-
angiospores with thin hyaline appendages (Choanephoraceae
(Blakeslea, Choanephora, Poitrasia), Kirk 1984; Gilbertel-
laceae (Gilbertella), Benny 1991) or spiny walls (Sporodiniella
umbellata Boedijn ex Evans & Samson and Syzygites megalo-
carpus; Ekpo and Young 1979; O'Donnell 1979; Gbaja and
Young 1985).
Many other characters need to be explored before we
have a definitive phylogeny based on traditional characters,
including (i) possible differences in sporangiospore ontogeny,
(ii) distribution of chemical compounds, and (iii) search for
zygospores in those taxa where they are unknown at present.
Chemotaxonomy might prove to be valuable in phylogeny of
For personal use only.
Mucorales. Fatty acid profiles are used in bacterial taxonomy
and they have been used in Mortierella (Amano et al. 1992).
Host range of Piptocephalis unispora Benj. has been used
to separate Micromucor from the remaining subgenera of
Mom'erella (Gams 1977; Benjamin 1978; Cuthbert and Jeffries
1984). The host range of this and other mucoralean parasites
might prove to be useful in discriminating other taxa in the
order. Antigenic studies have also been used to resolve
affinities in Mucorales (De Ruiter et al. 1993). The polyol
pattern appears to be useful in defining fungal phyla (Pfyffer
et al. 1986).
The accuracy of species descriptions has increased in
direct relationship to the level of technology available to the
individual researcher. When studying Mucorales, or other
microfungi, light microscopes (both compound and dissect-
ing) are necessary when describing structures and making
measurements. Initially, drawings were the optimal method
used to illustrate fungi. Improvements in photography have
replaced drawing as the most popular way to illustrate fungi.
Invention of newer light microscopes (phase and interference
phase contrast, fluorescence, etc.) have extended the research
life of this method of observation. Many Zygomycetes pro-
duce such large fruiting structures that is not possible to illus-
trate them photographically using a light microscope.
Electron microscopy has facilitated the observation of
structures barely visible or invisible with the compound light
microscope. The extreme depth of field provided by the SEM
permits observation of surface detail (O'Donnell 1979) or
those structures too large for the compound light microscope
(see Benny et al. 1992, Fig. 20). Transmission electron micro-
scopy can be used to clarify details of structures originally
observed with the light microscope, including zygosporan-
gial ornamentation, or to study sporangiospore ontogeny.
Currently, sequence comparison of 18s or the 5' end of
the 28s ribosomal genes is helping to resolve the phylogeny
Can. J. Bot. Vol. 73 (Suppl. I ) , 1995
of Mucorales (O'Donnell and Cigelnik 1994). Other proce-
dures will certainly become available that will be useful in
taxonomic and phylogenetic studies of Mucorales.
Better resolution of the zygomycete phylogeny presented
by O'Donnell and Cigelnik (1994) only can be obtained by
adding 18s sequences from additional taxa. These may be
obtained from existing genera, especially the larger ones (e.g.,
Absidia, Mortierella, Mucor, Rhizopus) or by isolating new
taxa from areas and (or) substrates that have not been sampled.
The majority of Zygomycetes have been isolated from Europe
and North America (where most of the mycologists reside).
Few Zygomycetes have been isolated from Africa, South or
Central America, or Australia. Dung and soil have proven
to be good sources of Dimargaritales, Kickxellales, and
Mucorales, but they may be isolated from other organic sub-
strates (bark, fruits, flowers, etc.). Many new taxa might be
found if additional geographic regions were sampled.
In the preceding discussion, a few of the outstanding
problems were listed that can be encountered when studying
the Mucorales or any other fungal group. Luckily, most of
the species in this order can be cultured and, therefore, can
be studied under controlled conditions. The production of
extensive aerial hyphae by most mucoralean fungi, however,
makes herbarium specimen preparation difficult unless material
is placed in a box or some other method is used to prevent
compression during storage.
A preliminary cladistic analysis, based on a morphological
data set, of the same genera of Mucorales sequenced by
O'Donnell and Cigelnik (1994), completed recently by me
needs to be revised before a useful phylogeny can be obtained.
This data set was based on the maintenance of the classical
distinction between sporangia and sporangiola. In the result-
ing trees taxa are included in a single clade that only form
sporangiola (whether uni- or multi-spored). These taxa are
distributed throughout the order when 18s rDNA sequence
data is analyzed. The lack of congruence in cladograms derived
from morphological or molecular data sets indicates that
many of the character states considered advanced in the
Mucorales have arisen several times in the order and, there-
fore, are not phylogenetically informative. The characters
(e.g., production of stolons and rhizoids, apophyses, or
sporangiola), however, are useful in identification. Certainly,
the most important revelation derived from recent molecular
studies is that too much emphasis has been placed on the dis-
tinction between sporangia and sporangiola. It is proposed
that sporangiola be treated as small sporangia, often with
distinct wall characteristics.
Acknowledgements
I thank Drs. J.W. Kimbrough, H.C. Kistler, and L. Meinhardt
for reviewing the manuscript.
References
Amano, N., Shinmen, Y., Akimoto, K., Kawashima, H., and
Amachi, T. 1992. Chemotaxonomic significance of fatty acid
composition in the genus Mortierella (Zygomycetes,
Mortierellaceae). Mycotaxon, 44: 257-265.
Barr, D.J.S. 1992. Evolution and kingdoms of organisms from
the perspective of a mycologist. Mycologia, 84: 1- 11.
Benjamin, R.K. 1958. Sexuality in the Kickxellaceae. Aliso, 4:
149- 169.
 E2.4. Benny
Benjamin, R.K. 1959. The merosporangiferous Mucorales.
Aliso, 4: 321 -433.
Benjamin, R.K. 1961. Addenda to "the merosporangiferous
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11
Mucorales. " Aliso, 5: 11- 19.
Benjamin, R.K. 1963. Addenda to "the merosporangiferous
Mucorales" 11. Aliso, 5: 273-288.
Benjamin, R.K. 1965. Addenda to "the merosporangiferous
Mucorales" 111. Dimargaris. Aliso, 6: 1- 10.
Benjamin, R.K. 1966. The merosporangium. Mycologia, 58:
1-42.
Benjamin, R.K. 1978. Gamsiella, a new subgenus of Mortierella
.. . (Mucorales: Mortierellaceae). Aliso, 9: 157- 170.
. . . .. ... Benjamin, R.K. 1979. Zygomycetes and their spores. In The
whole fungus: the sexual-asexual synthesis. Vol. 2. Edited by
B. Kendrick. National Museum of Natural Sciences, National
Museums of Canada, and the Kananaskis Foundation,
Ottawa, Ont. pp. 573-616.
Benjamin, R.K. 1 9 8 5 ~ A
. new genus of the Piptocephalidaceae
(Zoopagales) from Japan. Bot. J. Linn. Soc. 91: 117-133.
Benjamin, R.K. 1985b. A novel new species of Syncephalis
(Zoopagales: Piptocephalidaceae) from California that forms
hypogenous merosporangia. Aliso, 11: 1 - 15.
Benny, G.L. 1982. Zygomycetes. In Synopsis and classification
of living organisms. Vol. 1. Edited by S.P. Parker.
McGraw-Hill, New York. pp. 184-195.
Benny, G.L. 1991. Gilbertellaceae, a new family of the
Mucorales (Zygomycetes). Mycologia, 83: 150- 157.
Benny, G.L. 1992. Observations on Thamnidiaceae (Mucorales).
V. Thamnidiutn. Mycologia, 84: 834 - 842.
For personal use only.
Benny, G.L., and Benjamin, R.K. 1975. Observations on
Thamnidiaceae (Mucorales). New taxa, new combinations,
and notes on selected species. Aliso, 8: 301 -351.
Benny, G.L., and Benjamin, R.K. 1976. Observations on
Thamnidiaceae (Mucorales) . 11. Chaetocladium,
Cokeromyces, Mycorypha, and Phascolomyces. Aliso, 8:
391 -424.
Benny, G.L., and Benjamin, R.K. 1993. Observations on
Thamnidiaceae (Mucorales). VI. Two new species of
Dichototnocladium and the zygospores of D. hesseltinei
(Chaetocladiaceae). Mycologia, 85: 660 -67 1.
Benny, G.L., and Khan, S.R. 1988. The Radiomycetaceae
(Mucorales; Zygomycetes). Calcium oxalate crystals on the
sporangiolar wall and aerial hyphae. Scanning Microsc. 2(2):
1199- 1206.
Benny, G.L., and Samson, R.A. 1989. The Radiomycetaceae
(Mucorales, Zygomycetes). 11. Ultrastructural morphology of
the mature zygospore and comparative ontogeny of the
sporangiola and sporangiolar appendages. Mem. N.Y. Bot.
Gard. 49: 11- 19.
Benny, G.L., and Schipper, M.A.A. 1992. Observations on
Thamnidiaceae (Mucorales ). IV. Pirella. Mycologia, 84:
52-63.
Benny, G.L., Kirk, P.M., and Samson, R.A. 1985. Observations
on Thamnidiaceae (Mucorales). 111. Mycotyphaceae fam. nov.
and a reevaluation of Mycorypha sensu Benny & Benjamin
illustrated by two new species. Mycotaxon, 22: 119- 148.
Benny, G.L., Benjamin, R.K., and Kirk, P.M. 1992.
A reevaluation of Cunninghamellaceae (Mucorales).
Sigmoideomycetaceae fam. nov. and Reticulocephalis gen.
nov.; cladistic analysis and description of two new species.
Mycologia, 84: 615-641.
Cole, G.T., and Samson, R.A. 1979. Patterns of development in
conidial fungi. Pitman, London.
Cuthbert, A,, and Jeffries, P. 1984. Mycoparasltism by
Piptocephalis unispora within the Mortierellaceae. Trans. Br.
Mycol. Soc. 83: 700-702.
De Ruiter, G.A., van Bruggen-van der Lugt, A.W., and
Rombouts, F.M. 1993. Approaches to the classification of
the Mortierella isabellina group: antigenic extracellular
polysaccharides. Mycol. Res. 97: 690-696.
Ekpo, E.J.A., and Young, T.W.K. 1979. Fine-structure of the
dormant and germinating sporangiospore of Syzygites
megalocarpus (Mucorales) with notes on Sporodiniella
umbellata. Microbios Lett. 10: 63-68.
Gams, W. 1977. A key to the species of Mortierella. Persoonia,
9: 381-391.
Gams, W., and Carreiro, M.M. 1989. Two new species of
Mortierella and rediscovery of Thaxter's Dissophora
decumbens. Stud. Mycol. 31: 85-91.
Gbaja, I.S., and Young, T.W.K. 1985. Ultrastructure of the
anamorph of Sporodiniella umbellata (Mucorales). Microbios,
42: 263-272.
Gerdemann, J. W., and Trappe, J.M. 1974. The Endogonaceae
in the Pacific northwest. Mycol. Mem. 5: 1-76.
Greuter, W. (Chair, Editorial Committee). 1988. International
code of botanical nomenclature. Regnum Veg. 118: 1-328.
Grove, W.B. 1934. A systematic account and arrangement of
the Pilobolidae. In Researches on fungi. Vol. 6. Edited by
A.H.R. Buller. Longmans Green, London. pp. 190-224.
Hesseltine, C.W. 1957. The genus Syzygites (Mucoraceae).
Lloydia, 20: 228-237.
Hesseltine, C.W., and Ellis, J.J. 1973. Mucorales. In The
fungi. Vol. 4b. Edited by G.C. Ainsworth, F.K. Sparrow,
and A.S. Sussman. Academic Press, New York.
pp. 187-217.
Hesseltine, C.W., and Fennell, D.I. 1955. The genus Circinella.
Mycologia, 47: 193-212.
Hu, F.-m., Zheng, R.-y ., and Chen, G.-q. 1989. A redelimitation
of the species of Pilobolus. Mycosystema, 2: 111- 133.
Humber, R.A. 1989. Synopsis of a revised classification for the
Entomophthorales (Zygomycotina). Mycotaxon, 34: 441 -460.
Kendrick, B., Smith, J.E., Neville, J., and Weber, N.S. 1994.
A study of morphological variability, character analysis, and
taxonomic significance in the zygomycetous anamorph-genus
Umbelopsis. Mycotaxon, 51: 15-26.
Kirk, P.M. 1984. A monograph of the Choanephoraceae.
Mycol. Pap. 152: 1-61.
Kirk, P.M., and Benny, G.L. 1980. The genus Utharomyces
Boedijn (Pilobolaceae: Zygomycetes). Trans. Br. Mycol.
SOC.75: 123-131.
Lichtwardt, R.W. 1986. The Trichomycetes: fungal associates of
arthropods. Springer-Verlag, New York.
Mil'ko, A.A. 1974. Opredelitel' mukoral'vm gribov [Keys to
identification of Mucorales]. Izdat el'stvo Naukova Durnka,
Kiev, CIS (In Russian)
Morton, J.B., and Benny, G.L. 1990. Revised classification of
arbuscular mycorrhizal fungi (Zygomycetes): a new order,
Glomales, two new suborders, Glomineae and Gigasporineae,
two new families, Acaulosporaceae and Gigasporaceae, with
an emendation of Glomaceae. Mycotaxon, 37: 471-491.
O'Donnell, K.L. 1979. Zygornycetes in culture. Palfrey Contrib.
Bot. 2. Department of Botany, University of Georgia, Athens.
O'Donnell, K.L., and Cigelnik, E. 1994. Phylogeny of the
Zygomycota. Abstracts of the Fifth International Mycological
Congress, 14-21 Aug. 1994, Vancouver, B.C. p. 160.
O'Donnell, K.L., Ellis, J.J., Hesseltine, C.W., and Hooper, G.R.
1977. Zy gosporogenesis in Gilbertella persicaria. Can. J. Bat .
55: 662 -675.
O'Donnell, K.L., Flegler, S.L., Ellis, J.J., and Hesseltine, C.W.
1978. The Zygorhynchus zygosporangium and zygospore.
Can. J. Bot. 56: 1061- 1073.
Pfyffer, G.E., Pfyffer, B.U., and Rast, D.M. 1986. The polyo1
pattern, chemotaxonomy and phylogeny of the fungi.
Sydowia, 39: 160-201.

Pidoplichko, N.A., and Mil'ko, A.A. 1971. Atlas m u k o r a l ' v ~
gribov [Atlas of the Mucorales]. Izdat el'stvo Naukova
Dumka, Kiev, CIS.
Can. J. Bot. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF NEW BRUNSWICK - HARRIET IRVING LIBRARY on 05/17/11
Powell, M.D., and Arnott, H.J. 1985. Calcium oxalate crystal
production in two members of the Mucorales. Scanning
Electron Microsc. 1985(1): 183 - 189.
Schipper, M.A.A. 1975. On Mucor mucedo, Mucorjlavus and
related species. Stud. Mycol. 10: 1 -33.
Schipper, M.A.A. 1984. A revision of the genus Rhizopus. I.
The Rhizopus stolonifer-group and Rhizopus oryzae. Stud.
Mycol. 25: 1 - 19.
Schipper, M. A.A., and Samson, R.A. 1994. Miscellaneous
notes on Mucoraceae. Mycotaxon, 50: 475 -491.
Schipper, M. A. A., Samson, R.A., and Stalpers, J.A. 1975.
Zygospore ornamentation in the genera Mucor and
Zygorhynchus. Persoonia, 8: 321 -328.
Shipton, W.A., and Lunn, J.A. 1980. Sporangiole morphology
and species separation in Cunninghamella. Trans. Br. Mycol.
SOC.74: 483-491.
Stalpers, J.A., and Schipper, M. A. A. 1980. Comparison of
zygospore ornamentation in intra- and interspecific matings in
For personal use only.
Can. J. Bot. Vol. 73 (Suppl. I ) , 1995
some related species of Mucor and Backusella. Persoonia,
11: 39-52.
Thaxter, R. 1914. New or peculiar Zygomycetes. 3: Blakeslea,
Dissophora, and Haplosporangium, nova genera. Bot. Gaz.
58: 353-366.
Tucker, B.E. 1981. A review of the nonentomogenous
Entomophthorales. Mycotaxon, 13: 48 1 -505.
von Arx, J.A. 1983 (1982). On Mucoraceae s. str. and other
families of the Mucorales. Sydowia, 35: 10-26.
Whitney, K.D., and Arnott, H.J. 1986. Morphology and
development of calcium oxalate deposits in Gilbertella
persicaria (Mucorales). Mycologia, 78: 42 - 5 1 .
Whitney, K.D., and Arnott, H.J. 1988. The effect of calcium on
mycelial growth and calcium oxalate crystal formation in
Gilbertella persicaria (Mucorales) . Mycologia, 80: 707 -7 15.
Zheng, R.-y ., Chen, G.-q., and Hu, F.-m. 1988. Monosporous
varieties of Syncephalastrurn. Mycosystema, 1: 35-52.
Zycha, H., Siepmann, R., and Linnemann, G. 1969. Mucorales
eine Beschreibung aller Gattungen und Arten dieser
Pilzgruppe. J. Cramer, Lehrte.