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221
T.N. Taylor, M. Krings & E.L. Taylor: Fossil Fungi.
© 2015 Elsevier Inc. All rights reserved. DOI:2015 http://dx.doi.org/10.1016/B978-0-12-387731-4.00011-6
11
FUNGAL SPORES
In palynological preparations, fungal spores have tradition-
ally received far less attention than the pollen and spores of
vascular plants. Nevertheless, a variety of fungal remains,
including spores, hyphae, and various types of reproduc-
tive structures and mycelia, are often present in such resi-
dues and can be found throughout much of the geologic
column. In palynological analyses, these remains are usu-
ally treated together with other microfossils of various
origins (e.g. cyanobacteria, algae, aquatic invertebrates)
and collectively referred to as non-pollen palynomorphs
or NPPs (van Geel 2001; Cook etal., 2011). Many NPPs
are today used as proxy indicators in paleoecological stud-
ies, especially in the Cenozoic. While some of the earliest
of these studies recognized fungal spores among the non-
pollen/spore remains, they were not dealt with in a system-
atic manner, although some were simply related to modern
forms, a practice that is sometimes followed even today.
In addition, it was quickly understood that some modern
fungi produce more than one type of spore.
Palynological preparations have been and will con-
tinue to be an important source of paleomycological
information (e.g. Traverse, 2007; Figure 11.1). In general,
when pollen grains and spores are described, representa-
tive examples that provide a range of sizes, morphology,
and patterns of ornament will be used. Pollen grains
with structures adhering to the outer surface or in the
body of the grain will probably be discounted or not
carefully examined because the extraneous material will
be regarded as obscuring important morphological fea-
tures of the pollen or spore specimen. As in macrofossil
research, however, it is important to examine some of
these so-called atypical palynomorphs for evidence of: (1)
various types of fungi that may have attacked the grains,
or (2) infection patterns (e.g. Moore, L.R., 1963a; Huang
etal., 1999), as well as for examples of mycoparasites like
those seen in modern pollen (e.g. Olivier, 1978; Huang
etal., 2003). Such studies, however, must also be certain
that structures which appear to adhere to the surface of
a pollen grain or spore are in fact fungal and not some
structural component of the pollen grain. For example,
in some pollen grains the oncus (intine of the aperture
region) protrudes through the aperture (Kuang et al.,
2012) and might be interpreted as a chytrid zoosporan-
gium on the surface of the grain.
NAMING FUNGAL SPORES .....................................................222
FUNGAL SPORES IN STRATIGRAPHY .................................223
FUNGAL SPORES IN PALEOECOLOGY ...............................223
FUNGAL SPORE TAXA ................................................................224
Amerospores .............................................................................224
Didymospores ...........................................................................227
Phragmospores ..........................................................................229
Dictyospores .............................................................................232
Scolecospores ............................................................................ 233
Helicospores .............................................................................. 233
Staurospores .............................................................................235
OTHER FUNGAL SPORES AND STRUCTURES ................235
Hyphomycetes ...........................................................................236
Agonomycetes ...........................................................................237
Coelomycetes ............................................................................237
222 FOSSIL FUNGI
NAMING FUNGAL SPORES
One of the rst systems for classifying fungal spores by
comparing features with those of modern analogues
relied on conidial characters of size, shape, color, and
degree of septation. This system was proposed by
Saccardo etal. (1882–1931), and the multivolume work,
Sylloge fungorum omnium hucusque cognitorum, in which
they assembled details of all the fossil species published
up until 1920, was a monumental accomplishment; addi-
tions and corrections were later made by Kirk (1985) and
in subsequent editions. The initial system was modied
by van der Hammen (1954a, b), who assigned groups of
pollen and spores to various morphological categories
and had the sufx -sporites added for fungal spores; later,
Clarke (1965) suggested the sufx -sporonites be used to
indicate that the genus was of a fossil spore. Surface tex-
ture, including ornamentation, and color have also been
used in dening some fungal spores (Elsik, 1976a, b,
1983, 1996), and there is now some uniformity in the ter-
minology that has been developed and rened for pol-
len and spores (e.g. Dominguez de Toledo, 1994; Punt
etal., 1994). Because the shape of the fungal spores may
be variable, Kendrick and Nag Raj (1979) (Figure 11.2)
modied the system to remove inconsistencies and pro-
vide greater resolution for some features.
Based primarily on Cenozoic fungal spores, Elsik
(1976a) suggested a classication based on the two fea-
tures he regarded as most consistent, which were septa-
tion and the presence or absence of an aperture. Within
this classication he proposed multiple families within
two major orders of Fungi Imperfecti; the Sporae
Dispersae included families Sporae Monocellae, Sporae
Monodicellae, and Sporae Tetracellae, while the Mycelia
Sterilia contained the Cellae and Hyphae. Other classi-
cations of fungal spores used a more descriptive termi-
nology (e.g. monocellate fungal spore, multicellate fungal
spore, fruiting bodies; Norris, 1986, 1997), features of the
apertures (Song etal., 1999), and both features and num-
ber of apertures (Song and Huang, 2002). Today one of
the systems that is commonly used was initially proposed
by Pirozynski and Weresub (1979), who described fungal
spores based on shape and number of cells to identify
seven different categories of spores. Kendrick and Raj
(1979) also provided a key for mature spores of Fungi
Imperfecti.
Irrespective of what classication system is used, one
of the major problems that still remains unresolved in
studying fossil fungal spores is the fact that some spores
may be highly pleomorphic and the different forms may
have different names (e.g. Arx, 1987; Sugiyama, 1987).
In addition, the teleomorph and the anamorph may each
have a specic name, and in studies of both extant and
fossil fungi, the biological relationship between the two
is unknown (Weresub and Pirozynski, 1979). Despite the
desire to relate fossil fungal spores to extant forms, and
thus dene the geologic history of a taxon or family, the
problem still remains that some fossil forms may simply
Figure 11.1 Alfred Traverse.
Figure 11.2 W. Bryce Kendrick.
CHAPTER 11 FUNGAL SPORES 223
represent types that lack modern analogues because the
group that produced them is now extinct. Moreover, with
the limited number of spore characters available, it is
highly probable that the same spore type was produced
by different types of fungi (Stubbleeld and Taylor,
1988). As research has continued on fossil fungal spores,
imaging systems such as scanning electron microscopy
(SEM) have provided greater resolution to some features
and allowed others to be interpreted with greater clar-
ity. Interestingly, despite the importance placed on wall
thickness and layering, as well as on septal and other
characters, transmission electron microscopy (TEM)
has not been utilized to any major extent in the study of
either extant or fossil fungal spores.
FUNGAL SPORES IN STRATIGRAPHY
Some fungal spores have been used in biostratigra-
phy (sometimes termed mycostratigraphy), for exam-
ple when dening continental marine offshore deposits
(Elsik, 1980) or delimiting a particular sequence of
rocks (Varma and Patil, 1985). As a general rule, how-
ever, using fungal palynomorphs as index fossils has not
been universally adopted (e.g. Clarke, 1965; Elsik, 1976b,
1996). Fungal spores have been used in association with
other microfossils (e.g. algae) to dene basin geology
(e.g. Zhang, 1980; Ediger, 1981). Helicospores have been
used to indicate marshy and swamp-like conditions such
as those suggested for the Late Cretaceous of southern
Alberta, Canada (e.g. Kalgutkar and Braman, 2008).
Some spore genera and species have been critically
examined relative to character plasticity and such varia-
tion has been useful in more accurately dening species,
and thus increasing their usefulness in biostratigraphy
(e.g. Elsik, 1990; Elsik etal., 1990). In general, however,
most fungal spores have had a limited role in dening
rock boundaries (Pirozynski, 1978; Saxena and Tripathi,
2005). Nevertheless, a few studies have demonstrated the
usefulness of fungal spore assemblages to dene micro-
environments in certain strata (e.g. Paleogene in Parsons
and Norris, 1999). In this study seven interval zones
based on fungal propagules were recognized in deposits
in the Beaufort-Mackenzie Basin (northern Canada), and
these in turn were used to hypothesize inferences about
the depositional setting of the associated strata. In the
Paleozoic, fungal spores have been used less often for
biostratigraphy in coal deposits than in those of either
the Mesozoic or Cenozoic, perhaps as a consequence
of the oxidation process necessary in coal macerations
(Elsik, 1996).
FUNGAL SPORES IN PALEOECOLOGY
Fungal spores occurring in various archaeological sites
have been used as proxy indicators in reconstructing the
type of ora that was present (e.g. van Geel and Aptroot,
2006). For example, in the absence of pollen, or to cor-
roborate the presence of a particular taxon, the occurrence
of fungal spores known to be a pathogen of a particular
plant has been used to demonstrate the existence of that
plant. An example is Amphisphaerella dispersella, an asco-
mycete (Xylariales) that is typically associated with the
dicot Populus (van Geel and Aptroot, 2006).
Fungal spores have also been used to interpret paleoeco-
logical conditions at the time the fungi were fossilized (e.g.
van Geel, 1978; Gelorini etal., 2012; Hooghiemstra, 2012;
Worobiec and Worobiec, 2013). In Neogene sediments,
spores are especially common in coals, lignites, and peat
deposits (Ramanujam and Rao, 1978). In some instances
where the fungi were preserved on leaf cuticles, the com-
bination of the type of leaf together with the fungus has
been used as a broad indicator of climatic conditions.
An example of this is the study of Singh and Chauhan
(2008), who examined Neogene fungal spores from the
Mahuadanr Valley in India and modern relatives that are
pathogens of cereal grasses. The high diversity of fungal
remains at this site suggests that the area existed in a cli-
mate with high humidity. The presence of epiphyllous fungi
with their dispersed spores provides additional information
that the climate included high temperatures that were opti-
mal for growth. The presence of sh fossils at the site pro-
vided details about the depositional setting (a pond).
Fungal spores, together with pollen and spores of
vascular plants, have been used to dene the environ-
ment of deposition, as well as in the interpretation of
the precise stratigraphic position of the sample (e.g. Jain,
R.K., 1968; Saxena and Trivedi, 2009). In one example,
the presence of lignite together with marine fossil fungi
similar to those found in modern environments provided
data to suggest that this Neogene site represented a fos-
sil mangrove deposit (Kumaran etal., 2004). The identi-
cation of different fungal NPPs (i.e. dung-coprophilous
and parasitic fungi) in different layers of Holocene peat
from Brazil was used to suggest agricultural and domes-
tic activities, and to improve our overall understanding of
peat deposition (Medeanic and Silva, 2010).
224 FOSSIL FUNGI
In other instances fungal spores may be related to spe-
cic geographic areas at a particular point in geologic
time, such as the Cenozoic equatorial coast of Africa
(Salard-Cheboldaeff and Locquin, 1980) or the Miocene
of Brazil (e.g. Guimarães etal., 2013). A Tetraploa-like
fungus that today grows on bamboos was a compo-
nent of a Miocene site that was a wetland with reed and
riparian vegetation (Worobiec et al., 2009). The pres-
ence of fungal spores in certain deposits, such as peat,
can provide data on the formation of the deposit (e.g.
Vishnu-Mittre, 1973). Fungal remains may also provide
information on the taphonomy of a site. For example,
plant fossils from the Miocene Clarkia site in northern
Idaho lacked basidiomycete hyphae with clamp connec-
tions (they were found neither associated with leaves nor
in the palynological preparations) (e.g. Phipps, 2001).
This suggests that the fossils do not represent debris (lit-
ter) from a surrounding forest oor where basidiomycetes
would be common (Sherwood-Pike and Gray, 1988). This
research emphasizes the importance of recording the fun-
gal spores present at a site and where possible, the typical
substrate (e.g. Sherwood, 1985).
Another paleoecological source of information for
fungal spores is plant resins. These not only provide a
substrate for the fungi but also offer some indication of
the types of resin-producing plants that may have existed
in the ecosystem. This is especially important because
some fungi occur exclusively on plant exudates (i.e. res-
inicolous fungi; see e.g. Rikkinen, 1999). Cretaceous
amber inclusions from France containing insect fecal pel-
lets made up entirely of remnants of polypores, includ-
ing hyphae, setae (spinulae), and basidiospores, indicate
that these macrofungi served as a habitat for fungivorous
insects in the Mesozoic (Schmidt etal., 2010b).
Various fungal spores have been described from more
recent sediments (Quaternary) and compared with those
found in modern ecosystems and sediment types (e.g. Wolf
and Cavaliere, 1966; Yeloff etal., 2007). In some instances
the primary focus of the research with fungal spores was
oral succession within a well-dened stratigraphic range
and/or geographic setting (van Geel etal., 1986).
FUNGAL SPORE TAXA
Graham (1962; Figure 11.3) provided a list of 204 gen-
era of fossil fungal spores, indicating both their geo-
graphic and stratigraphic occurrences, and also noted
the importance of fungal spores in documenting the
vegetational history of a region. We have adopted this
classication, including additions by Kirk (1985) and
subsequent modications that were incorporated in the
extraordinarily comprehensive volume by Kalgutkar and
Jansonius (2000), and by Saxena and Tripathi (2011). The
following include several examples within each fungal
spore type (Saxena and Tripathi, 2005). Another espe-
cially useful catalogue that documents Cenozoic fungi
from India from 1988 to 2005 is found in Saxena (2006).
The catalogue provides detailed information regarding
the nomenclature of 172 species. As might be expected,
a number of species of fossil fungi were not validly
published initially or have had diagnoses corrected later
and the appropriate repository identied (e.g. Saxena,
2012).
The following descriptions illustrate some of the basic
types of fungal spores together with some of the repre-
sentative species of each of the major types.
AMEROSPORES
Spores in this group are unicellate and may be aperturate
or inaperturate; they may have a single pore or hilum, or
variable apertures. The length to width ratio in amero-
spores is <15:1; strongly curved and very long types are
excluded.
Figure 11.3 Alan Graham.
CHAPTER 11 FUNGAL SPORES 225
Basidiosporites
In B. fournieri from the Paleocene of Texas (Figure
11.4), USA, specimens are up to 15 μm long and possess
a psilate outer wall (Elsik, 1968). The pore in this form
is slightly offset, a condition that is also present in the
larger spore B. ovalis (=Monosporiosporites ovalis) (see
Figure 11.4) from the Eocene of Tennessee (Sheffy and
Dilcher, 1971). Specimens from late Quaternary sediment
cores from the Arabian Sea are biconvex and up to 43 μm
long; the offset pore in B. sadasivanii (see Figure 11.4) is
slightly thickened (Chandra etal., 1984).
diporisporites
This genus is characterized by its elongate shape and,
as the name suggests, a diporate condition (see Figure
11.4), there being one pore on each end of the unicel-
late spore (van der Hammen, 1954a). Some forms have
features of the pores that have been used to dene the
species, notably D. communis (see Figure 11.4) from the
Eocene–Oligocene of China (Ke and Shi, 1978) and
D. bhavnagarensis from the Eocene of India (Saxena, 2009).
A number of forms are quite large, as in D. giganticus
(101–130 μm long) from the Miocene–Pliocene of India
(Kar, 1990).
exesisporites
In Exesisporites there is a single pore that is thickened
around the margin (Elsik, 1969). In E. annulatus (see
Figure 11.4) from the upper Pleistocene of Canada,
specimens may be monoporate or diporate with a collar
surrounding the pore (Kalgutkar, 1993). What is inter-
preted as a verrucate-like sculpture (see Figure 11.4)
occurs along the periphery of the spore wall in E. ver-
rucatus (Kumar, 1990). Exesisporites neogenicus is dis-
tinguished by the absence of a clear annular ring around
the pore (Kalgutkar and Braman, 2008). The high num-
ber of Exesisporites spores together with other micro-
fossils suggests that the climate was predominantly dry,
accompanied by a lowered sea level, during the Pliocene–
Pleistocene of Nigeria (Durugbo etal., 2010).
Hypoxylonites
This is an oval-elongate spore that is characterized by an
elongate scar, slit, or furrow that parallels the long axis
(Elsik, 1990; Saxena, 2012). Spores of this type have been
interpreted as being similar to those produced by certain
living ascomycetes in the family Xylariaceae (e.g. Elsik,
1990; Nandi etal., 2003; Prager etal., 2006). The taxon
ranges from the Cretaceous to the recent and is known
from deposits around the world (Elsik, 1981), includ-
ing specimens preserved in amber (Antoine etal., 2006).
The wall ornament ranges from psilate to small spines.
Specimens of H. brazosensis (Figure 11.5) from the
upper middle Eocene of Texas (USA) have a furrow that
extends to the ends of the spore, while in H. chaiffetzii
(Neogene, Gulf Coast, USA) the furrow runs approxi-
mately three quarters of the length of the spore. Some
specimens are described as having two wall layers (see
Figure 11.5), but this feature has been determined as a
fold along the furrow. In H. oblongus the furrow is espe-
cially short (Dueñas, 1979). On account of the difculty
in resolving the furrow, some spore types from the Eocene
of Tennessee (USA) included in Inapertisporites (Sheffy
and Dilcher, 1971) have been moved to Hypoxylonites
Figure 11.4 Selected amerospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
226 FOSSIL FUNGI
(Elsik, 1990). The abundance of Hypoxylonites was used
to establish an early Oligocene biozone in the northwest-
ern Gulf of Mexico (Elsik and Yancey, 2000).
Another spore type that is morphologically similar
to Hypoxylonites is Spirotremesporites (Dueñas, 1979),
which has one to several furrows that may be sigmoidal
in outline or positioned at an angle to the long axis of the
spore (see Figure 11.5). Elsik (1990) provided a discus-
sion of the difference between the two genera and noted
that Hypoxylonites is found in rocks that reect cooling
environments.
inapertisporites
These spores are characterized as unicellular and asep-
tate, with a highly variable size; the dening charac-
ter is the lack of a preformed aperture. Specimens of
I. variabilis (Figure 11.6) from the Upper Cretaceous
of Colombia are approximately 31 μm long and psilate
(van der Hammen, 1954a). Several spores that clump
together appear to be a characteristic of I. granulatus (see
Figure 11.6) from the Eocene–Oligocene of Shandong
Province, China (Ke and Shi, 1978). Specimens of
I. argentinus (see Figure 11.6), originally described as
a species of Reticulatasporites (Jain, R.K., 1968) from
the Middle Triassic of western Argentina, have an orna-
ment of widely spaced brochi (lumen or mesh reticulum)
and a size range of 40 to 61 μm in diameter (Kalgutkar
and Jansonius, 2000). Other forms may be highly vari-
able in ornamentation, as in I. trivedii (see Figure 11.6)
from the lower Eocene of Andhra Pradesh, India, where
the wall surface ranges from punctate to variously stri-
ate (Ambwani, 1982). The afnities of I. circularis (see
Figure 11.6) are debatable. The fossil was considered to
be related to fungi within the Basidiomycota (Graham,
A., 1965), while the spore type may be a conidiospore of
a microthyriaceous ascomycete (Dilcher, 1965). In other
reports, similar spores have been associated with wood of
Fagus (Soomro etal., 2010).
lacrimasporonites
Spores of this genus are monoporate and spatulate to
elliptical in outline (Clarke, 1965; Figure 11.7); one spe-
cies, L. sondensis from the Paleocene of Pakistan, has
been described as having two germinal apertures (Soomro
etal., 2010). Kalgutkar and Jansonius (2000) noted that
using spore shape as a diagnostic character has poten-
tial problems and is a difcult character to use in prac-
tice. The genus has been emended to include specimens
with a at hilar scar at one end and a pore at the other
(Kalgutkar and Jansonius, 2000). Some fungal spores
that lack the spatulate shape have been transferred to
Monoporisporites (Kalgutkar and Jansonius, 2000).
Spores of Lacrimasporonites found in association with
mastodon bones from Canada were regarded as similar to
ascomycetes in the Sordariales (Pirozynski etal., 1988).
Figure 11.6 Selected amerospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
Figure 11.5 Selected amerospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
CHAPTER 11 FUNGAL SPORES 227
monoporisporites
This genus is used for fungal spores that are monoporate
(see Figure 11.7) and generally spherical, with psilate to
punctuate wall ornament. The type species, M. minutus
from the Upper Cretaceous of Colombia, includes small
(14 μm) spores (van der Hammen, 1954a). Specimens of
M. basidii (see Figure 11.7) from the Paleocene of Texas
(USA) have a two-layered wall that extends outward
in the region of the pore (Elsik, 1968). In M. dilcheri
(see Figure 11.7) (Upper Cretaceous of Mexico) the
pore is 2 μm in diameter and the spore is slightly bilat-
eral (Martínez-Hernández and Tomasini-Ortiz, 1989).
Reports of the genus include the Upper Cretaceous of the
Antarctic Peninsula (Song and Cao, 1994). Along with
other palynomorphs, Monoporisporites has been found
in large numbers at the Cretaceous–Paleogene bound-
ary (Vajda and McLoughlin, 2004). Some specimens
included in Monoporisporites have been related to teli-
ospores of certain Uredinales (rust fungi) (Ramanujam
and Ramachar, 1980), while others from the Oligocene of
equatorial Africa (Cameroon) are aligned simply with the
Basidiomycota (Salard-Cheboldaeff and Locquin, 1980).
palaeoampHispHaerella
The occurrence of equatorial pores on an elliptical spore
is the primary feature that denes Palaeoamphisphaerella
(Ramanujam and Srisailam, 1978). Specimens of
P. keralensis (see Figure 11.7) from the Miocene of India
are rhomboidal in outline, 30 μm in the longest axis, and
have three to six pores, which are occasionally arranged
in an irregular pattern. Surface ornament is scabrate.
Palaeoamphisphaerella pirozynskii from the same strati-
graphic level is distinguished by 8–10 equatorial pores
(see Figure 11.7). The spores closely compare, morpho-
logically, with those of some members of the Xylariaceae
(i.e. Amphisphaerella), although it is noted that in the
extant forms the pores are more slit-like (Eriksson, O.,
1966).
DIDYMOSPORES
As the name implies, spores in this category are two-
celled (Figure 11.8). Sometimes one cell is smaller than
the other, and the spore is characterized by a pore in the
smaller cell; some are described as inaperturate. Sculpture
ranges from psilate to slightly punctuate.
dicellaesporites
These spores are isopolar, two-celled, and inaperturate.
In some species the individual cells are slightly tapered at
the ends (e.g. D. aculeolatus; Sheffy and Dilcher, 1971),
while in others the two cells are rounded at the ends (see
Figure 11.8) (e.g. D. antarcticus; Song and Cao, 1994). In
D. himachalensis it is difcult to see where the cells are
constricted (see Figure 11.8; Saxena and Bhattacharyya,
1990). In D. popovii from the Paleocene of Texas (USA)
Figure 11.7 Selected amerospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
Figure 11.8 Selected didymospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
228 FOSSIL FUNGI
each of the cells is about 19 × 29 μm and the septum is
two layered (see Figure 11.8; Elsik, 1968). Numerous
species have been recorded from Cenozoic sediments of
India (Saxena and Tripathi, 2011). Some fossil spores
have been compared with those produced by the extant
ascomycete Apiosporina (Dothideomycetes), the fungus
responsible for black knot disease in species of Prunus
(plums, cherries, peaches, etc.), which results in hyperpla-
sia of woody tissues (e.g. Fernando etal., 2005).
Ascospores with two cells are associated with epiphyl-
lous colonies of Molinaea asterinoides on dicot leaves from
the Maastrichtian (uppermost Cretaceous) of Colombia
(Doubinger and Pons, 1975). Hyphae are long and the lat-
eral margins of some cells are sinuous. The hyphopodia
are capitate, with the terminal cell of each hyphopodium
(stigmocyst) containing a delicate lateral pore.
didymoporisporonites
Spores in this genus are two-celled, with one of the cells
being larger than the other (see Figure 11.9). The type
species, D. psilatus, is generally oval with the single pore
occurring in the smaller cell (Sheffy and Dilcher, 1971).
The original specimens come from the middle Eocene
of Tennessee (USA) and are distinguished by their size
(6.8–11.1 μm; Kalgutkar and Jansonius, 2000). Specimens
of D. discors (Figure 11.9) from Yukon Territory are
slightly larger and have a pore in the septum (Kalgutkar,
1993; name revised by Kalgutkar and Jansonius, 2000).
As the name implies, D. conicus is characterized by
one of the cells being cone-shaped (Kalgutkar, 1997).
Specimens have been reported from the upper Paleocene–
lower Eocene of Axel Heiberg Island, Canada.
diploneurospora
Specimens of this genus are unusual because the two
cells are unequal and there is sculpturing on the upper
cell consisting of longitudinal ribs or stripes of thick-
ened wall material; on the lower, smaller cell sculpture
is not well dened. Miocene fungal spores of D. tewarii
from South India have unequal cells in which one cell is
approximately one third the size of the other (see Figure
11.9) (Jain and Gupta, 1970). In this species the smaller
cell is described as appendage-like. The generic name in
part reects the spore morphology and sculpture found
in the extant ascomycete Neurospora (see Davis, 2000).
dyadosporites
These spores consist of two cells, each having a sin-
gle pore at the apex (e.g. van der Hammen, 1954a;
Clarke, 1965). Ornamentation is variable. Specimens
of D. cannanorensis from the Miocene of India have
pores that are slightly offset from the long axis of the
spore (Ramanujam and Rao, 1978; Figure 11.10). The
spore wall and the septum are bilayered. In D. ellip-
sus (see Figure 11.10) from the Upper Cretaceous of
Colorado, USA, the wall is nely punctuate (Clarke,
1965). Perhaps the largest species in spore size is D.
grandiporus from the lower Miocene of Assam (India).
Specimens are longer than 100 μm (see Figure 11.10)
and contain equally large pores (14–16 μm), each
with a thickened rim (Singh et al., 1986). Kalgutkar
and Jansonius (2000) commented that the thickened
rim may in fact denote pigmentation in the region. In
D. megaporus (see Figure 11.10) (Paleocene–Pliocene
of China) the pore in the septum is disciform (Zhu
et al., 1985). Dyadosporites sahnii (see Figure 11.10;
originally Granodiporites; see Kalgutkar and Jansonius,
2000) from the Eocene–Miocene (Assam, India) has
its pore area covered by a delicate membrane (Varma
and Rawat, 1963). The genus is also known from
the Upper Cretaceous of the Fildes Peninsula, King
George Island, Antarctic Peninsula (Song and Cao,
1994) and from the Miocene of Taiwan (Huang, 1981).
Germinating spores assigned to Dyadosporites have
been reported in the coal maceral ulminite and in
palynological preparations from Miocene coal from
Slovakia (O’Keefe etal., 2011b).
Dyadosporites must not be confused with Dyadospora,
which is a taxon used for certain Paleozoic cryptospores
(Strother and Traverse, 1979).
Figure 11.9 Selected didymospores. See text for species age
and provenance. Bar = 50 µm. (Redrawn from Kalgutkar and
Jansonius, 2000.)
CHAPTER 11 FUNGAL SPORES 229
FusiFormisporites
These spores are fusiform in outline and lack apertures
(Rouse, 1962; see Figure 11.10). Specimens range from
20 to 100 μm, possess a two-layered septum, and extend
from the Cretaceous to recent (Martínez-Hernández and
Tomasini-Ortiz, 1989). Ornamentation includes radiating
longitudinal striae that arise from either pole in the pat-
tern of a spindle (Elsik, 1968). In some species the striae
may branch near the equator. In F. keralensis (see Figure
11.10) the ends of the spores are truncate and the septum
is thick (Ramanujam and Rao, 1978). Spores included
in Striadyadosporites (Dueñas, 1979) have been trans-
ferred to Fusiformisporites. Based on stratigraphic occur-
rence, Elsik (1976b) hypothesized that Fusiformisporites
and other longitudinally striate and ribbed fungal
spore types such as Striatetracellaeites, Striadiporites,
Striasporonites, and the verrucate Verrusporonites are
phylogenetically related. Spores that are similar in
appearance are found in the extant ascomycete Cookeina
(Pezizales; Weinstein et al., 2002); C. tricholoma spores
are also known in the subfossil state from the Holocene
of Tanzania, Africa (Wolf, 1967).
PHRAGMOSPORES
Spores of this type have two or more transverse septa
resulting in three or more cells. Both aperturate and inap-
erturate forms are included.
Fractisporonites
Fractisporonites is a common type of phragmospore that
has been found at multiple sites ranging from the Jurassic
(Clarke, 1965; Traverse and Ash, 1994) to the Eocene
(Kalgutkar, 1993). Morphologically similar microfos-
sils from the Precambrian are known as Arctacellularia
(Hermann and Podkovyrov, 2008).
reduviasporonites
This is the name used for chains of spores that were once
interpreted as a fossil Penicillium (Wilson, L.R., 1962).
This fossil is the focal point of several inuential studies
demonstrating a massive accumulation (a so-called “fungal
spike” or “fungal abundance event”) of Reduviasporonites
fossils at the end of the Permian, and suggesting that
this accumulation is indicative of the destruction of ter-
restrial vegetation by fungal pathogens that led to the
end-Permian collapse of terrestrial ecosystems (Visscher
et al., 1996, 2011; Steiner et al., 2003). The conclusion is
based on the fact that Reduviasporonites is morphologi-
cally similar to a resting stage formed by members in the
extant basidiomycete genus Rhizoctonia, which includes
several widespread plant pathogens (e.g. Parmeter, 1970;
González García etal., 2006). The authors (Visscher etal.,
2011) state that fungal disease was an essential accessory
in the destabilization of the vegetation that accelerated
widespread tree mortality during the end-Permian cri-
sis. Visscher et al. (2011) dismiss results from a study by
Foster et al. (2002), who, based on geochemical evidence,
concluded that Reduviasporonites may be of algal origin.
It is interesting to note that a fungal spike has also been
recorded from the Pennsylvanian of Peru (Wood and
Elsik, 1999).
BracHysporisporites
Spores of this type are organized in three or more cells,
with the individual cells decreasing in size from a large
dome-shaped apical cell (Figure 11.11) to a smaller
attachment cell that is sometime described as hyaline
Figure 11.10 Selected didymospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
230 FOSSIL FUNGI
(Lange and Smith, 1971; Ediger, 1981). A single pore is
present at the narrower end of the spore; some species
are described as having a pore in the septum. In B. ant-
arcticus (see Figure 11.11) from the Cretaceous of King
George Island, Antarctica, the spores are up to 45 μm
long and often occur in chains of four or ve cells (Song
and Cao, 1994). Some Cenozoic species (e.g. B. atratus;
see Figure 11.11) have especially thick septa (Kalgutkar,
1993). In B. inuvikensis, a Cenozoic form, the spores are
tetracellate, with the two distal cells making up the major-
ity of the spore (Parsons and Norris, 1999). Three-celled
forms up to 85 μm long from the Eocene–Oligocene
(Bohai, China) are inaperturate (Ke and Shi, 1978). The
balloon shape of the basal cell in B. magnus (Eocene) of
Gujarat, western India, morphologically appears as a
head with a tapering cap (Samant, 2000). Fossil spores of
the Brachysporisporites type are generally compared with
the extant saprotrophic, dematiaceous hyphomycete genus
Brachysporium (Sordariomycetes, Ascomycota; Réblová
and Seifert, 2004). A relationship of Brachysporisporites to
the anamorphic genus Monotosporella (Sordariomycetes)
has also been considered (Sadowski et al., 2012).
Spores assigned to the genus Anatolinites are similar to
Brachysporisporites in size and shape but differ from
the latter by having two simple pores (Elsik et al., 1990).
Several afnities have been proposed for Anatolinites,
including the ascomycete plant pathogen Alternaria and
teliospores of the rust Puccinia (Basidiomycota).
cHaetospHaerites
The barrel shape and tetracellate organization are dis-
tinctive features of the genus Chaetosphaerites (Felix,
1894) (=Cannanorosporonites; Ramanujam and Rao,
1978). Terminal cells are smaller than the central cells
(Figure 11.12), with the latter typically bulging. The
apical cell has a single pore. In the original descrip-
tion of C. bilychnis (see Figure 11.12) from the Eocene
of Baku (Azerbaijan), the fungus was found on dicot
wood believed to have afnities with the Rhamnaceae
(Felix, 1894). The fossil specimens are compared to
Torula, a member of the Pezizomycotina (Schoknecht
and Crane, 1977; Kirk et al., 2008), perhaps closely
related to extant members of the ascomycete family
Sphaeriaceae (Xylariales), which includes parasitic fungi
with perithecia. Felixites is the name applied to spores
that appear similar, but are generally from the Paleozoic
(Elsik, 1989). Specimens of F. playfordii (formerly
Chaetosphaerites pollenisimilis Butterworth and Williams,
1958) from the Carboniferous of Spitsbergen are up to
52 μm long and at maturity may split into single cells, so-
called half specimens (Elsik, 1990).
diporicellaesporites
These spores are elongate, multicellular, and have a sin-
gle pore at each end (Elsik, 1968). The number of cells
in D. aequabilis (see Figure 11.12) ranges from 9 to 13
with the cells that are more central also larger in diam-
eter (Kalgutkar, 1993). This species from the upper
Paleocene–lower Eocene of the Yukon Territory,
Figure 11.11 Selected phragmospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
Figure 11.12 Selected phragmospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
CHAPTER 11 FUNGAL SPORES 231
Canada, has a two-layered wall and septal aps. A fun-
gal spore of late Quaternary age that was originally
placed in Inapertisporites (Chandra et al., 1984) is now
designated as D. dilcheri (see Figure 11.12; Kalgutkar
and Jansonius, 2000). Diporicellaesporites jansonii (see
Figure 11.12) has between six and nine septa with the
pores slightly incurved (Kalgutkar, 1993), while in
D. pluricellus (see Figure 11.12) the pores protrude
slightly (Kar and Saxena, 1976). The genus has been
identied in rocks from as early as the Cretaceous (e.g.
Kalgutkar and Braman, 2008) and has been recorded
extensively from various Cenozoic stratigraphic lev-
els in North America (e.g. Price and Thorne, 1977) and
India (Saxena and Tripathi, 2011), as well as from the
Oligocene of China (Zhang, 1980). Fossil spores have
been morphologically compared to extant members of
Annellophora (Pezizomycotina), a pathogen common on
various palms (e.g. Vann and Taber, 1985).
Foveoletisporonites
These spores are ve or more septate, inaperturate, and
the two central cells are elongate. In the type species, F.
miocenicus (Figure 11.13) from the Miocene of India, the
spores maybe up to 120 μm long with a foveolate (having
small pits) ornament (see Figure 11.13; Ramanujam and
Rao, 1978). In some species, such as F. indicus, the fove-
olae may be irregular in arrangement (Ramanujam and
Srisailam, 1978). The fossils are generally attributed to
the Pezizomycotina.
multicellaesporites
This genus is characterized by spores constructed of
three to ve cells with a longitudinal furrow and slight
curvature to their shape (Elsik, 1968; Kumar, 1990).
Ornamentation may be variable or differentially thick-
ened. In M. bilobus (see Figure 11.13) from the upper
Pliocene, the septa have a well-dened pore; speci-
mens are reported in the 75 μm size range (Rouse and
Mustard, 1997). In M. dilcheri the terminal cells are
longer (Samant, 2000). Similar fungal spores that are
inaperturate are placed in Multicellites (Kalgutkar and
Jansonius, 2000). Spores of this type were found exten-
sively in the rhizome of the Eocene aquatic angiosperm
Eorhiza arnoldii (Robison and Person, 1973). In a
detailed investigation of the hyphomycetes in the cortical
aerenchyma of E. arnoldii, Klymiuk et al. (2013b) com-
pared the spores that Robison and Person (1973) attrib-
uted to Multicellaesporites to the extant Thielaviopsis
(Pezizomycotina).
ornasporonites
Ornasporonites is the name used for tetracellate spores in
which the basal and apical cells are smaller, with each of
these cells containing a single, simple pore (Ramanujam
and Rao, 1978). In O. inaequalis (see Figure 11.13) from
the Miocene lignite of Cannanore, India, the ornament
is rugulate-reticulate. The fusiform specimens range up
to 63 μm long by 42 μm in diameter. Several examples are
now known from other Miocene sites in India (Saxena
and Tripathi, 2011).
pluricellaesporites
This dispersed fungal spore is monoporate and con-
structed of three or more cells (van der Hammen,
1954b). In early discussions of this spore type the genus
was sometimes considered as representing algal cells
(e.g. Elsik, 1968); however, the fungal nature was sub-
sequently conrmed (Elsik and Jansonius, 1974). In
Figure 11.13 Selected phragmospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
232 FOSSIL FUNGI
P. typicus (see Figure 11.13) (Neogene) the septa may be
up to 4 μm thick, entire or split, and the spore may be
variously ornamented. Other species (e.g. P. eocenicus,
P. globatus) are known from the Eocene of India (Samant
and Tapaswi, 2000; Samant, 2000) and Cretaceous of
Canada (e.g. Srivastava, 1968); the genus has also been
recorded from the Paleocene of Brazil (Pedrão Ferreira
et al., 2005). Kalgutkar and Jansonius (2000) provided
a history of the possible afnities of Pluricellaesporites,
including the conidia of the extant genus Alternaria
(Pleosporaceae), many species of which are plant patho-
gens found in most environments of the world. An inter-
esting genus of extant hyphomycetes, Xylomyces, initially
discovered on immersed decaying wood in a tidewater
stream in Rhode Island, USA (Goos et al., 1977) but
later also reported from several other countries (Goh
et al., 1997; Kohlmeyer and Volkmann-Kohlmeyer,
1998), is characterized by large, dematiaceous, thick-
walled, multiseptate, and more or less fusiform chla-
mydospores. Goos etal. (1977) note that the spores of X.
chlamydosporis bear a striking resemblance to the fossil
Pluricellaesporites psilatus from the Cretaceous of North
America (Clarke, 1965).
polycellaesporonites
Spores of this type have a large, round basal cell that
gives rise to a tubular or beak-like extension (Chandra
etal., 1984). The spore is multicellate; cells are arranged
in a cluster, and no aperture is present. In some species (P.
acuminatus from the late Paleocene of British Columbia,
Canada; Figure 11.14) there may be up to 12 septa (see
Figure 11.14), some of which are longitudinal (Rouse and
Mustard, 1997; Jansonius and Kalgutkar, 2000). A form
known from the Oligocene–lower Miocene (Saxena and
Bhattacharyya, 1990) and Quaternary (Chandra et al.,
1984) is P. bellus (see Figure 11.14). It is up to 68 μm
long and has a tube-like projection that appears to be
hyaline. In this species the individual cells are rectangu-
lar and not arranged along one axis. Specimens have also
been reported from the Paleocene and Eocene of India
(Gupta, 2002; Saxena and Ranhotra, 2009). The conical
beak in P. alternariatus (see Figure 11.14) is thought to
represent the region of attachment in the conidial chain
(Kalgutkar and Jansonius, 2000).
DICTYOSPORES
Sometimes termed muriform spores, the inaperturate
spores in this category are characterized by both longitu-
dinal and transverse septa. Shape is variable.
dictyosporites
These are muriform, inaperturate spores that are mul-
ticellate, and the individual cells are typically spherical
(Felix, 1894). Some forms are described in association
with a mycelium of septate hyphae called Arbusculites
dicotylophylli (Figure 11.15; Paradkar, 1974); however,
this taxon is now included in Dictyosporites (D. dicoty-
lophylli) from the Upper Cretaceous (Maastrichtian)
of India (Kalgutkar and Jansonius, 2000). Arbusculites
argentea, an enigmatic fossil from the Carboniferous of
Great Britain (Murray, P., 1831), has been interpreted
as being of animal origin. In the Oligocene form D. dic-
tyosus (see Figure 11.15) from Cameroon, the number
of cells is 16 (Salard-Cheboldaeff and Locquin, 1980).
Some spores show a size and shape distinction between
the central cells and those of the periphery, which may be
more rectangular in outline. This can be seen in D. glo-
bimuriformis (see Figure 11.15; Kalgutkar, 1997). Many
of the species can be compared morphologically with the
conidia of several modern genera (e.g. Dictyosporium,
Stemphylium, Septosporium, Alternaria; Kalgutkar and
Jansonius, 2000).
spinosporonites
These inaperturate spores are subcircular and up to
42 μm in diameter; extending from the surface of each
cell is a prominent spine that is up to 9 μm long (Saxena
and Khare, 1991). The type species, Spinosporonites indi-
cus (late Paleocene–middle Eocene of India), has been
compared to specimens that are more similar to setose
pycnidia found in some coelomycetes (Kalgutkar and
Jansonius, 2000).
stapHlosporonites
Spores in this genus are variable in shape, but gener-
ally elongate and consisting of more than four irregular
Figure 11.14 Selected phragmospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
CHAPTER 11 FUNGAL SPORES 233
cells, which are usually arranged in clusters along more
than a single axis. They are inaperturate and have a
variable ornamentation that ranges from psilate to
mildly punctate (Sheffy and Dilcher, 1971). Specimens
of S. allomorphus (see Figure 11.15) from the Eocene
of the USA are oblong and about 30 μm long; each
spore is constructed of more than eight irregular cells
(see Figure 11.15). Broadly elliptical spores with a
rounded apex and protruding hilum are included in S.
billelsikii from the upper Paleocene–lower Eocene of
Canada (Kalgutkar and Jansonius, 2000). Another
form initially described from the Eocene–Oligocene of
Canada is S. delumbus (see Figure 11.15; Norris, 1986).
In this species there are multiple cells in the center of
the spore that may overlap; specimens range up to
150 μm long. In S. dichotomus (Eocene of India) the
arrangement of cells can produce a dichotomous pat-
tern (Gupta, 2002). As is the case with a number of
dictyospores, several species of Staphlosporonites share
morphological features with extant members of the
Moniliales (Fungi Imperfecti), especially Alternaria (e.g.
Joly, 1964).
tricellaesporonites
Spores in this genus have three cells and are inapertu-
rate (Sheffy and Dilcher, 1971). The individual cells are
not associated in a single plane in some forms and it has
been suggested that they may in fact not be fungal, but
rather some type of resinous globules (Kalgutkar and
Jansonius, 2000). In T. semicircularis the three cells are
arranged in a slightly convex plane (Sheffy and Dilcher,
1971). This species from the Eocene of the USA has
septa with double walls and ornament ranging from
psilate to punctate. Gupta (2002) described T. granulatus
from the Eocene of India, which, morphologically, looks
like three cells of a tetrad.
SCOLECOSPORES
These spores are especially long (length:width ratio of
>15:1) and thread-like, and may include both transverse
septate and non-septate types. The proximal or distal end
may have a hilum or pore.
scolecosporites
The spores of S. longus (Figure 11.16) are up to 35 μm
long and consist of 28 cells, each approximately 5 μm
long (Song et al., 1999). This late Eocene–middle
Oligocene species from China has a thin spore wall and
smooth surface. Other specimens, such as S. maslinen-
sis (see Figure 11.16) from the lower middle Eocene of
Australia, may be 400 μm long and constructed of up to
38 cells (Lange and Smith, 1971). In some descriptions
these spores are referred to as scoleco-phragmospores or
termed lamentous phragmospores because of the range
of curvature, a feature that could be the result of pres-
ervation. Scolecospores are a common spore type in the
modern family Phyllachoraceae (Ascomycota), a group
of obligate biotrophs that produce tar spots on host
plants (e.g. Cannon, 1991; Pearce et al., 1999). Similar
spores have also been identied as hyperparasites of
Phyllachora (Parbery and Langdon, 1963).
HELICOSPORES
Spores of this type are easy to recognize because
they appear as a rolled up tube (Figure 11.17) or a
Figure 11.15 Selected dictyospore types. See text for species
age and provenance. Bar = 50 µm. (Redrawn from Kalgutkar
and Jansonius, 2000.)
234 FOSSIL FUNGI
superimposed spiral curved through 180° with a pore at
one end. Helicospores may involve multiple revolutions
and may coil in a single plane (planispiral) or in three
dimensions.
elsikisporonites
In E. tubulatus (Figure 11.17) the tube lacks septa and
the cell is widest at the midpoint (Kumar, 1990). The wall
is smooth and the pore has a slight extension at the tip.
Specimens from the middle Miocene of India are approxi-
mately 386 μm long. The wall is generally smooth but may
be slightly folded.
involutisporonites
These spores are planispiral and constructed of multi-
ple cells (Clarke, 1965); in some species the septum con-
tains a pore. Some forms have smaller cells in the center
of the spiral (e.g. I. chowdhryi (Figure 11.17); Miocene of
India) with the cells becoming larger in diameter toward
the outside (Jain and Kar, 1979). In I. trapezoides (see
Figure 11.17) individual cells are trapezoid shaped (the
outer wall much longer than the inner) and the septa are
thick (Kalgutkar, 1993). Specimens of Helicoonites goosii
(Figures 11.17, 11.18A) have a three-dimensional mor-
phology in which the spiral of cells forms ellipsoidal to
barrel-shaped or beehive-shaped conidia (Kalgutkar and
Sigler, 1995).
Many of the spores within the helicospore group are
morphologically similar to members of the Dothideales
and other ascomycetes and include such genera as
Figure 11.16 Selected scolecospore types. See text for
species age and provenance. Bar = 50 µm. (Redrawn from
Kalgutkar and Jansonius, 2000.)
Figure 11.17 Selected helicospore types. See text for species
age and provenance. Bar = 50 µm. (Redrawn from Kalgutkar
and Jansonius, 2000.)
CHAPTER 11 FUNGAL SPORES 235
Helicoma and Helicomyces; however, in these forms
conidia are septate. Most occur on plant litter and wood
in moist environments (Zhao et al., 2007). Molecular
systematics of the extant helicoid forms suggest that
most of the species in the anamorphic genera (Helicoma,
Helicomyces, and Helicosporium) form a monophyl-
etic group that corresponds to the teleomorph Tubea,
and that the presence of helicoid conidia may represent
a good taxonomic indicator for higher taxonomic place-
ment (Tsui etal., 2006).
STAUROSPORES
The spores in this category are unusual in that they are
stellate with three or four radiating arms or protuber-
ances. Spores may or may not have septa and have more
than a single axis.
triBolites
This is an Eocene spore with two to six radiating arms
that extend 30–45 μm out from a polyhedral central cell
(Bradley, 1964; Kalgutkar and Jansonius, 2000). One of
the features of T. tetrastonyx is that one of the arms is
slightly attened. The fossil is morphologically simi-
lar to the conidia of extant species of Tetrachaetum and
Lemonniera (Kalgutkar and Jansonius, 2000).
Frasnacritetrus
This is a genus initially used for Late Devonian
(Frasnian) microfossils from northern France; these are
rounded to slightly bell shaped at one end, and, at the
other, more rectangular in outline with a single process
extending from each corner (Taugourdeau, 1968). While
most palynologists today use the name Tetraploa for
geologically younger fossils displaying this morphology,
some still prefer to use Frasnacritetrus for these fossils.
Several studies demonstrated that the number of pro-
cesses in Tetraploa/Frasnacritetrus could range from two
to four, and that the central cell was divided into multi-
ple chambers (Saxena and Sarkar, 1986). In F. conatus
(Figure 11.19) from the Miocene of India, the processes
are hollow and the surface of the spore is ornamented by
small coni (Saxena and Sarkar, 1986). Fungal spores of
Frasnacritetrus, together with other palynomorphs, have
been used to more accurately interpret the sequence of
rock layers and climate during short intervals in the latest
Cretaceous–Paleocene Intertrappean beds of India (e.g.
Tripathi, 2001; Saxena and Ranhotra, 2009).
OTHER FUNGAL SPORES
AND STRUCTURES
There are a variety of fungi referred to as anamorphic,
mitosporic, asexual, conidial, and Fungi Imperfecti,
and, in some literature, Deuteromycotina (Kirk et al.,
2008). Sutton (1996) provided an excellent historical
record of the attempts to correlate and classify these
fungi based mainly on conidiogenesis. In general these
fungi are asexual stages of primarily Ascomycota and a
few Basidiomycota, and they produce mitotic structures
termed conidia. These structures are highly variable in
color, size, shape, and septation (e.g. Hennebert and
Figure 11.18 Helicoonites goosii (A) and Pesavis tagluensis
(B). Eocene, Canada. Bar = 25 µm. (Courtesy M.G. Parsons.)
Figure 11.19 Frasnacritetrus conatus, a type of staurospore.
Miocene, Himachal Pradesh, India. Bar = 50 μm. (Redrawn
from Saxena and Sarkar, 1986.)
236 FOSSIL FUNGI
Sutton, 1994). Some of these fungi appear to have lost
sexuality altogether. Most are terrestrial, although some
occupy marine and freshwater ecosystems. Nutritionally
they are saprotrophs and parasites, as well as lichen
mycobionts, endophytes, mycoparasites, and mycorrhiza
formers. Historically, several classes have been proposed.
Fossil examples of three of these informal classes are
described below.
HYPHOMYCETES
Hyphomycetes are anamorphs of a large number of gen-
era and species (Kendrick, 2003; Seifert and Gams, 2011;
Seifert etal., 2011). These fungi lack locular fruiting bod-
ies (conidiomata), and sporulation occurs on separate
septate hyphae that are exposed rather than within some
specialized structure (e.g. Bernadovičová and Ivanová,
2011). The diversity of extant forms is extraordinary
(e.g. Ellis, M.B., 1971, 1976). Fungi in this group grow in
a wide range of ecological niches and gain carbon from
living or dead organic matter; many forms are aquatic
(Bärlocher, 1992). One of the features of many members
of this group is that they produce passively discharged
conidia from hyphae that allow them to move some dis-
tance from the substrate, where air currents can move the
spores. Other spores can be moved by water or insects.
They are regarded as polyphyletic.
These so-called Ingoldian fungi, which are aero-
aquatic hyphomycetes and named in honor of C.T.
Ingold, are one of a few groups where species can be
identied based on the morphology of their long, nar-
row, branched conidia (e.g. Belliveau and Bärlocher,
2005; Descals, 2005; Prokhorov and Bodyagin, 2007). In
this regard they have the potential to be recognized and
identied in the fossil record. Some forms are referred to
as aero-aquatic hyphomycetes because they form conidia
with special otation devices (e.g. Michaelides and
Kendrick, 1982). The increased surface area provided by
the stick-like morphology of these fungi provides buoy-
ancy in turbulent streams; when they come to rest on a
substrate, adhesive pads or appressoria quickly develop
from some of the branch tips. In other instances the
arms of the spore become tangled in debris that offers
a substrate for the developing germlings. These micro-
organisms release several exoenzymes that are primarily
responsible for the degradation of cell wall material (e.g.
Chamier, 1985). This makes these fungi an important
component link in stream food webs because the result-
ing decomposed plant matter attracts detritus-feeding
invertebrates.
An example of a fossil saprophytic hyphomycete is
one preserved in the cortical tissues of the Eocene angi-
osperm Eorhiza arnoldii from the Princeton chert of
British Columbia, Canada (Robison and Person, 1973;
LePage et al., 1994). Additional specimens of these
fungi in E. arnoldii have been characterized into three
types and examined relative to their growth and devel-
opment in the plant tissues (Klymiuk etal., 2013b). One
type includes darkly pigmented holothallic macroco-
nidia up to 125 μm long and with 30–35 transverse septa.
Morphologically they appear most similar to the extant
aquatic ascomycete Xylomyces (e.g. Goh et al., 1997).
In the second type, propagation is the result of chains
of amerospores, each with a simple septal pore between
successive cells. Conidiophore morphology is not known
in detail but there is some suggestion that conidia were
borne on short branches like those in Thielaviopsis
(Ellis, M.B., 1971). Pyriform phragmospores, each about
25 μm in diameter, represent the third type of anamorph
found in E. arnoldii. Conidiogenous cells are approxi-
mately 5 μm in diameter and retained at the base of the
dispersed conidium. Some hyphae associated with the
spores produce curved branches. Features of the three
anamorph types suggest afnities with chlamydospores
produced by Culcitalna achraspora, a member of the
Halosphaeriaceae (Sordariomycetes; Seifert etal., 2011).
Also present in E. arnoldii are several types of sterile
mycelia, including monilioid hyphae with intercalary
branching, which are in turn associated with distinct
morphotypes of microsclerotia (Klymiuk et al., 2013c).
This careful study indicates the potential for determin-
ing the presence in fossil plants of asymptomatic endo-
phytes and dark-septate endophytes, groups of fungi
that can function in modern ecosystems as both patho-
gens and saprotrophs (Menkis etal., 2004). These studies
demonstrate that developmental features of fossil fungi,
if preserved in sufcient detail, can be used to determine
biological afnities as well as stages in the life history of
the fungi. Developmental stages also represent another
set of parameters that will be useful in dening the eco-
logical parallels between modern and fossil ecosystems.
Moreover, they offer the opportunity to use certain life-
history features (e.g. microsclerotia, chlamydospores) as
minimum calibration points to document the presence
of freshwater lignicolous saprotrophs during the early
Eocene (Klymiuk etal., 2013b).
Another unusual fungal fossil, initially described
from the upper Paleocene of Britain (Smith and Crane,
1979), is Pesavis tagluensis (Figure 11.18B), a fungal
CHAPTER 11 FUNGAL SPORES 237
spore that subsequently has also been reported from a
number of other Cretaceous and Cenozoic sites world-
wide (e.g. Elsik and Jansonius, 1974; Jansonius, 1976;
Lange, 1978b; Kalgutkar and Sweet, 1988; Lyck and
Stemmerik, 2000). In fact, some have noted that it is
difcult to determine whether the structure is a spore,
fruiting body, or some type of capture device of a par-
asitic fungus (Kalgutkar and Jansonius, 2000). Each
spore consists of a central cell with two incurving pri-
mary arms, each of which produces secondary arms
(hyphae). Some have suggested that the afnities of
P. tagluensis may lie with some type of dematiaceous
hyphomycete (Pirozynski, 1976b), perhaps morphologi-
cally similar to conidia of Dictyosporium (Ellis, M.B.,
1971). Functionally, the inwardly curving arms may
have served to trap a bubble of air (see Michaelides and
Kendrick, 1982). Spores with a main “stem” (hypha) of
seven cells, with branching on one side, are included in
Ctenosporites from the upper Eocene–lower Oligocene
(Elsik and Jansonius, 1974; Lange and Smith, 1975). In
C. eskerensis the multicellular structure may be up to
43 μm long (Smith, P.H., 1978); larger (56 μm) species
are included in C. sherwoodiae from Upper Cretaceous
coals in Colorado (Clarke, 1965).
AGONOMYCETES
Hyphae are also common in various matrices that con-
tain fossil fungal spores. Little of this evidence for fossil
fungi tends to be described unless there is some unusual
feature of the hyphae or evidence of a host response that
is somehow related to the fungus. Fungi accommodated
in the Agonomycetes consist of sterile mycelia (Mycelia
Sterilia) in which conidiation does not occur and the
fungus reproduces asexually by hyphal growth and frag-
mentation (Cole, 1986). Within the group are important
plant pathogens, such as Rhizoctonia solani of potatoes
in which sclerotia overwinter on infected tubers. In this
fungus the basidiomycete teleomorph (Thanatephorus
cucumeris) is known (e.g. Hyakumachi and Ui, 1988). A
fossil suggested as a member of Rhizoctonia is reported
from the Permian of India as R. nandorii (Biradar and
Bonde, 1976). The fossil occurs on gymnosperm wood
and consists of septate hyphae of various sizes, but no
spores or any type of reproductive structures are present.
Another interesting fossil is Dendromyceliates splendus,
reported from the Miocene of India (Jain and Kar, 1979).
The end of the hypha branches dichotomously several
times with the tips sharply pointed. In D. rajmahalensis
the hyphae are up to 3.5 μm wide and aporate (Tripathi,
2001). In this Cretaceous species some hyphae are orna-
mented by small baculae.
COELOMYCETES
Coelomycetes are characterized by the production of
conidia that form in some type of cavity in the host tis-
sue (Sutton, 1980; Somrithipol et al., 2008). Today coe-
lomycetes are known from temperate and tropical areas
and are thought to include at least 1000 genera and more
than 7000 species (Kirk etal., 2008). Although most are
anamorphs, a few have been linked to teleomorphs, based
on molecular studies (e.g. Rungjindamai et al., 2008).
New living forms are still being described, especially from
the tropics, and some of these possess morphologically
unique types of funnel-shaped conidiomata that should
be easy to recognize in the fossil record (e.g. Somrithipol
etal., 2008).
Some early reports of fossil fungi represent coelomy-
cetes. For example, Cladosporites fasciculatus was used
for tufts of hyphae, a few of which bore conidia (Berry,
1916). This fungus was abundant in the vessels of laura-
ceous wood from the Eocene of Texas (USA). What are
interpreted as pycnidia of a coelomycete containing one
to three septate, ovoid-elliptical spores were described
from the Deccan Intertrappean beds as Deccanosporium
eocenum (Singhai, 1972). Morphologically, the fossil
shares a number of features with Camarosporium, a plant
pathogen historically placed in the Pleosporales.
Fossil coelomycetes have also been described from
Miocene Dominican and Mexican amber (Poinar, 2003).
Three different species – Asteromites mexicanus (Figure
11.20), Leptostromites ellipticus (Figure 11.21), and
Leptothyrites dominicanus (Figure 11.22) – were discov-
ered, one on a petal of a dicot ower. The fossils were
compared to modern forms based on pycnidia and other
features, and one form was suggested to be parasitic
because the leaf it is attached to shows no evidence of
decay. This analysis forms a framework that can be used
to understand host/parasite relationships for some groups
through time.
Permineralized fossil coelomycetes have been reported
from the Upper Cretaceous (middle Turonian) of
Hokkaido, Japan as Archephoma cycadeoidellae and
Meniscoideisporites cretacea (Watanabe etal., 1999). The
specimens occur in a bennettitalean cone, Cycadeoidella
japonica. In A. cycadeoidellae the pycnidia are partially
embedded within a pycnidium wall that is two or three
layers thick. Aseptate conidia range up to 3 μm in diam-
eter. Several features suggest afnities with the extant
238 FOSSIL FUNGI
genus Phoma, a common soil fungus. Both pycnidial and
acervial conidiomata occur in M. cretacea, both types
producing meniscoid conidia and what are termed hya-
line cells.
Another fungus from the Middle Jurassic of Santa
Cruz Province, Argentina, is Palaeopericonia (Ibañez and
Zamuner, 1996). Palaeopericonia fritzschei occurs in an
araucarian cone and consists of layers of hyphae, each
up to 9.6 μm in diameter with infrequent septa. The fos-
sil has micronematous conidiophores with blastic con-
idiogenesis. Blastoconidia have a verrucose ornament
and occur singly or in chains of up to nine elements.
Also present in the specimen are terminal chlamydo-
spores. The fossil is compared to several dematiaceous
genera and, as the name indicates, is perhaps closest to
modern Periconia, a common saprophyte (Cantrell etal.,
2007). A fossil from the Pleistocene shares some features
with the extant genus Clasterosporium, an anamorph
included in the Magnaporthaceae (Sordariomycetes). The
septate hyphae of the fossil are approximately 7 μm in
diameter and hyphopodia are conspicuous (Cowley and
Colquhoun, 1966).
Figure 11.20 Asteromites mexicanus pycnidium on fossil
ower petal preserved in amber. Oligocene–Miocene, Mexico.
Bar = 500 µm. (Courtesy G.O. Poinar, Jr.)
Figure 11.21 Pycnidia (arrows) of Leptostromites ellipti-
cus preserved in amber. Miocene. Dominican Republic. Bar =
1.0 mm. (Courtesy G.O. Poinar, Jr.)
Figure 11.22 Several pycnidia of Leptothyrites dominicanus
on a monocot leaf in amber. Miocene, Dominican Republic.
Bar = 1.0 mm. (Courtesy G.O. Poinar, Jr.)
