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ELSEVIER Review of Palaeobotany and Palynology 90 (1996) 249-262

The importance of fungi in shaping the paleoecosystem

Thomas N. Taylor ‘, Jeffrey M. Osborn b
aDepartment of Botany and Natural History Museum, University of Kansas, Lawrence, KS 66045, USA
b Division of Science, Northeast Missouri State University, Kirksville, MO 63501, USA
Received 15 September 1994;revised and accepted 10 December 1994

Abstract

Although fungi have a long geologic history, many aspects regarding their origins and subsequent evolution remain
impossible to document from the fossil record. As heterotrophs, fungi must interact with other organisms, and it is
here that the fossil record can provide an important source of biological and paleoecological information about fungal
interactions. Saprophytic, parasitic and biotrophic interactions among fungi and other organisms are ancient; examples
of these interrelationships are discussed as they relate to the establishment and evolution of the biological and physical
paleoecosystem.

1. Introduction nevertheless unique contributions that can be made

only through the investigation and evaluation of
Although fungi were some of the first organisms fossil fungi. One of the most important contribu-
to be reported as fossils, their geologic record is tions considers the various biological interactions
only now beginning to be fully appreciated. Several that occurred among fungi and other organisms
major groups can be traced well back into the through geologic time. In this paper we will discuss
Paleozoic (Taylor, 1993); for others, the record is several of these interrelationships and consider
far less precise, and none are known from sedi- how they may have affected the paleoecosystem in
ments of Precambrian age. Perhaps the oldest which they existed.
fossil fungi are represented by non-septate fila-
ments from the Cambrian that are believed to
have been reef saprophytes (Kobluk and James,
1979). Filaments have also been reported from 2. Saprophytic interactions
Early Silurian sediments (Pratt et al., 1978), while
perforateseptate hyphae and multicellate spores It has been suggested that as the atmosphere
are known from the Late Silurian (Sherwood-Pike gradually evolved, the Earth experienced extensive
and Gray, 1985). Despite the antiquity of these fluctuations in temperature and terrestrially con-
fungal remains, little is known about their organ- sisted of barren rock surfaces that were low in
ization, and even less about how they functioned nutrients. As a result, there were few stable, moist
in the paleoenvironment in which they lived. environments in which organisms might flourish.
In spite of a poor fossil record and the uncertain As time progressed the land surface must have
geologic distribution of several groups, there are also included decaying algae and other organisms,

GQ34-6667/96/$15.000 1996 Elsevier Science B.V. All rights reserved

SSDZOO34-6667(95)00086-O
250 TN. Taylor, J. M. Osborn/Review of Palaeobotany and Palynology 90 ( 1996) 249-262

PLATE I
 T. N. Taylor, J.M. OsbornjReview of Palaeobotany and Palynology 90 (1996) 249-262 251

such as cyanobacteria, along shore lines and in dissociation of plant material resulting from trans-
shallow tidal pools. There can be little doubt that port, deposition and diagenesis.
initially various microorganisms were the primary Although there are examples of basidiomycetous
decomposers, and only later did fungi and pseu- fungi associated with the Paleozoic (e.g. Dennis,
dofungi assume this role. 1970) and Mesozoic (e.g. Osborn et al., 1989), in
Today the most obvious interaction among fungi most instances the actual fossil-decomposing
and other organisms involves the decomposition organisms are not present. The paucity of good
of plant and animal tissues, a process that returns examples of these fungi may be attributed to
available nutrients back into the ecosystem. One several factors. For example, it may be biased by
would expect examples of saprophytic activity to preservation, reflect some environmental con-
be common in the fossil record; however, this is straint on fungal growth such as acidity, or reflect
generally not the case. In the Carboniferous, for the fact that such decomposers initially inhabited
example, a high percentage of fungal remains are more upland habitats. It has been suggested that
not preserved within plant tissue, but rather as the seemingly small number of Carboniferous sap-
hypogeous sporocarps in the surrounding matrix rophytes is directly related to the large accumula-
(Plate I, 1). Many of these fossils may represent tions of organic carbon in the form of coal, and
endogonaceous Zygomycetes (White and Taylor, that such deposits are the result of a bottleneck in
1989a). Today this fungal group constitutes the the recycling of lignin and other refractory com-
major root symbionts (mycorrhizae) in the eco- pounds produced by land plants (Robinson, 1990).
system, but during the Paleozoic these fungi may This hypothesis is largely consistent with the his-
have been the principal decomposers in the eco- torical belief that ascomycetes and basidiomycetes,
system (Taylor and White, 1989). Today the princi- the two principal lignin decomposers today,
pal cellulose and lignin decomposers in the evolved much later geologically, and thus were not
ecosystem are Basidiomycetes. Although they have an important component of the Paleozoic mycota
a fossil record that dates back to the Upper (Pirozynski, 1976). Although it is clear that both
Devonian (Stubblefield et al., 1985), the fossil groups were in existence by Carboniferous time,
record of this group indicates that Basidiomycetes neither may have played a major role in the total
may have initially contributed only marginally as decomposition process. There can be little doubt
tissue decomposers. While it is difficult to docu- that all of these factors have contributed to the
ment the actual fungi responsible for tissue decom- poor fossil record of saprophytism.
position, the activities of these organisms are More direct evidence of saprophytic activity can
represented in the fossil record as fragmented be demonstrated by various symptoms found in
pieces of plant tissue that can be observed, especi- fossil wood, or in the presence of fungal hyphae
ally in permineralizations (e.g. coal balls and silici- (Plate I, 5). For example, in some extant woods
fied peats) (Plate I, 3). Not all material of this as lignin and cellulose are selectively removed,
type can be traced directly to the activities of longitudinally oriented spindle-shaped pockets are
fungi; some fragments obviously reflect combined formed, each approximately 1.0 cm long
microbial decomposition together with mechanical (Blanchette, 1992). In modern ecosystems basidio-

PLATE I

1. Sporocq of Zhpairia showing mmmmted outer surface.and spores(?) inside(Carboniferous). x 120.

2. Erosion troughs in the secondary wall of a tracheidin the wood of CaZlixylon (Devonian). x 2000.
3. Fractured section of Ci~Uixylonwood showing extensive penetration of fungal hyphae into tracheids (Devonian). x 200.
4. Transverse section of Araucarioxylon stem showing symptoms of white pocket rot within the wood (Triassic). x 0.7.
5. Transverse section of a tracheid with fimgal hypha penetrating wall (Devonian). x 1000.
6. Transverse section of wood showing differential separation of primary and secondaq tracheid walls as the result of fbngal attack
(Triassic). x 275.
252 TN. Taylor, J.M. OsbornjReview of Palaeobotany and Palynology 90 (1996) 249-262

PLATE II
r” --- -
 T.N. Taylor, J.M. OsbornjReview of Palaeobotany and Palynoiogy 90 (19%) 249-262 253

mycetes are responsible for this type of decay actions been documented from the fossil record.
pattern, commonly known as white pocket rot While it remains impossible to document the dual
(Plate I, 4). The oldest known occurrence of this movement of nutrients in this type of symbiosis
type of decay is from the Permian and Triassic of using fossils, the presence of an observable host
Antarctica (Stubblefield and Taylor, 1986). Pocket response does indicate an antagonistic interaction.
rot fungi are also believed to be responsible for The earliest examples of a host response involved
wood rot in Upper Triassic tree trunks in North by fungal parasites comes from the Devonian
America (Creber and Ash, 1990). Interestingly, Rhynie chert. One such example includes the char-
the pockets in both modern and fossil woods are ophyte Pulaeonitella(Taylor et al., 1992). In this
identical suggesting that the diffusion rates of alga, cortical cells of the axis typically range from
fungal enzymes through the cellulose and lignin 30 to 70 pm; occasionally abnormal cells occur.
are also identical. Less dramatic effects of fungal These are much larger, ranging up to 300 pm in
activity can be identified in woods by examining diameter (Plate II, 3). These large, hypertrophied
preservational differences in the primary and cells represent a direct host response. Similar
secondary walls of tracheids (Plate I, 6). Various responses are common in extant plants, including
extant wood-rotting fungi selectively destroy cellu- charophytes, when infected by certain aquatic
lose and lignin at different rates (Plate I, 2). An fungi (Karling, 1928). Associated with such infec-
analysis of these differences, both qualitative and tions in modern charophytes is an increased pro-
quantitative, may ultimately provide a basis for duction of large starch grains in the plastids.
distinguishing the type of fossil fungal rot (e.g. Interestingly, in some of the infected, fossil charo-
white rot, soft rot, brown rot) and thus the fungus phyte cells there are clusters of dark, granular
responsible. At the present time, however, there is bodies that may be indicative of this response. It
insufhcient evidence to document the extent of is impossible to gauge the longevity of this parasitic
these fungal interactions, and which ones played interaction in the fossils. In particular did it repre-
the major role in wood degradation. In many sent a biotrophic nutritional mode in which the
instances the fungi were saprobes of dead trees, alga was not significantly altered by the fungus,
while in other cases alterations in the cell walls or was the interaction necrotrophic, ultimately
indicate that the trees were alive when infection resulting in the death of the alga?
initially took place. Another parasitic interaction detected in the
Early Devonian paleoecosystem involves a host
response caused by mycoparasites (Plate II, 1),
3. Parasitic interactions fungi that derive the majority of their nutrition
from other fungi (Hass et al., 1994). In this
Within living biological systems the difference interaction, distinct thickenings termed callosities,
between parasitic and mutualistic symbioses are papillae, or lignitubers are formed on the inner
often diiIicult to distinguish. Although a great deal surface of thick-walled chlamydospores. The pres-
has been written about the theoretical evolution ence of these structures in the fossils indicates that
of these interactions (e.g. Lewis, 1974), only the chlamydospores were alive for some period
recently have good examples of parasitic inter- after fungal infection. Other types of mycopara-

PLATE II

1. Chlamydospore showing chytrid mycoparasite developing between wall layers (Devonian). x 1000.
2. Chlamydospore containing endobiotic mycoparasite and possible epibiotic one on the surface (Devonian). x 1000.
3. Portion of Palaeonitella axis showing normal cortical cells of axis (arrows) and two hypertrophied cells infected by chytrids
(Devonian). x 150.
4. Stalked chlamydospore. (Carboniferous). Compare with modem Glomus chlamydospore in 5. x 200.
5. Chlamydospore of extant Glomur. x 200.
254 T. N. Taylor, J. M. OsbornJReview of Palaeobotany and Palynology 90 (1996) 249-262

PLATE III
 T. N. Taylor, J. M. OsbornjReview of Palaeobotany and Palynology 90 (1996) 249-262 25s

sites completely fill the host cell (Plate II, 2). In the morphological similarity of the fossil fungus
these, however, there is no apparent host response to the modern, obligate parasite Albugo, and the
in the fossil suggesting that the cells were rapidly pattern in which the seed tissues were disrupted.
killed. Mycoparasites are widespread in nature Examples of pollen grains parasitized by chytrids
today, and are found in all major groups of fungi. are also known from the Carboniferous (Millay
Although the interactions of these fungi in modern and Taylor, 1978). While it is impossible to deter-
ecosystems remains poorly understood, their uni- mine the extent of which parasitic fungi affected
versal occurrence indicates that some fungal/plant the reproductive biology of fossil plants, if present
diseases are naturally controlled by this type of in sufficient numbers these pathogens could cer-
antagonism. The presence of mycoparasites that tainly have exerted extensive selective pressure on
infect chlamydospores of extant endophyte fungi the community. In other instances, certain types
(Plate II, 5) suggests that mycoparasitism might of reproductive propagules show a consistent
have negatively impacted the production of viable absence of fungal interaction. For example,
chlamydospores and thus reduced the incidence of Lepidocarpon, a water-disseminated megasporan-
mycorrhizal infections in certain paleoecosystems. gium, has never been reported to be infected by
Chlamydospores can be identified as early as aquatic fungi. By comparison, other lycopod
the Lower Devonian (Plate III, 2), and are rela- reproductive organs from the same Carboniferous
tively common in many Carboniferous peat swamp
sites show evidence of extensive tissue disruption
deposits (Plate II, 4) (Wagner and Taylor, 1982).
as a result of fungal activity (Stubblefield and
In spite of their rather frequent occurrence, how-
Taylor, 1984) (Plate III, 1). Additional evidence
ever, none have been found infected by mycopara-
of this type may provide a basis for eventually
sites. This is particularly surprising because one
suggesting that certain plants were better adapted
would expect to observe chytrids in the supersatu-
to withstand fungal infection,
rated soils on the Carboniferous peat swamps as
Parasitic interactions have also been observed
they are found in wet soils today (Sylvia and
Schenck, 1983). Moreover, many extant chytrids on the vegetative parts of fossil plants, particularly
that have been isolated from the spores of arbuscu- in the form of epiphyllous fungi (Plate III, 5).
lar mycorrhizae are facultative and can function Although almost all incidences of these fossil fungi
as saprobes. In the Carboniferous, it may be that are known from Tertiary angiosperm leaves, at
the pH of the peat swamps inhibited fungal growth. least one infection has been reported on a conifer
The absence of both in-situ mycoparasites and (Alvin and Muir, 1970). At some localities the
detectable host responses in these peats provides number of epiphyllous fungi is large with infection
additional support for this hypothesis. taking place on many taxonomically different hosts
Parasitic fungi have also been described on (Dilcher, 1965). In some of these, it is possible to
certain fossil reproductive organs. For example, reconstruct the complete life history of the fungus.
Stidd and Cosentino (1975) described a fungal This provides the opportunity both to detail the
parasite within the seed Nucellangium. infection process and, perhaps, analyze host speci-
Characterizing this interrelationship was based on ficity (Daghlian, 1978). One potentially rewarding

PLATE III

1. Lycopod megasporangium containing several chlamydospores (arrows); note the disrupted megagametophyte tissue
(Carboniferous). x 50.
2. Chlamydospores and hyphae in Rhynie chert axis (Devonian). x 100.
3. Arthropod cuticle (arrow) with numerous trichomycete thalli attached to its inner surface (Triassic). x 200.
4. Cortical cell of Aglaophyton axis containingarbuscule (arrow) (Devonian). x 600.
5. Multiseptate spore of an epiphyllous fungus that has germinated to produce several hyphae (Eocene). x 450.
6. Alveolar organization of a paleosol. This is believed to demonstrate a pattern of biomineralization (Carboniferous). x 1000.
256 T. N. Taylor, J.M. OsbornfReview of Palaeobotany and Palynology 90 (1996) 249-262

area of study may involve the use of epiphyllous to produce certain toxic compounds. As a result
fungi as indicators of past climates (Lange, 1978). of the interactions between mycorrhizae and herbi-
Although the phylloplane has been in existence vores the structure of the community may be
since the Middle Devonian, there is not a great altered since plants vary in their tolerance to
deal of evidence of fungi on leaves earlier than the herbivory and dependence on mycorrhizae
Cretaceous. Barthel (1961) described hyphae on (Gehring and Whitham, 1994). For example, in
foliage of Muriopteris, and Schaarschmidt (1966) modern ecosystems it has been suggested that
illustrated what are interpreted as apothecia and under high light and low nutrient availability,
asci on the Triassic leaf Pterophyllum. While the mycorrhizal infection alters the carbon/nutrient
general absence of such occurrences may reflect a balance in the plants so that there is an increase
failure to document these such structures, it also in allocation of carbon based defenses against
may be that pre-Cretaceous fungi were unable to herbivory (Gange and West, 1994). While such
penetrate the cuticle on leaf surfaces. Studies of fungal/animal interactions probably existed in
extant parasitic fungi indicate that penetration of paleoecosystems, they will certainly be impossible
a leaf is principally mechanical, although chemical to document from the fossil record. It is possible
degradation is also paramount. Perhaps the cuti- that as the endophytes became more highly evolved
cles of pre-Cretaceous plants were simply too thick and localized, their defensive influence on leaves
for hyphal penetration, or the chemical composi- and other foliar organs became diminished; this
tion may have been significantly different in some may have been the stimulus needed for parasitic
early plant groups (Tegelaar et al., 1991). Another fungi to move onto leaf surfaces. The spatial
postulate regarding the absence of epiphyllous relationships of host tissues may have also played
fungi prior to the Cretaceous may be related to a major role in the timing of fungi occupying foliar
the essentially hypogeous habitat of these early surfaces. Although there is no direct evidence from
fungi. For example, although biotrophic, parasitic the fossil record to date, various types of fungal
and saprophytic nutritional modes were estab- parasites may have initially entered the repro-
lished early in the fossil record, the group(s) that ductive organs of the plant and then later colonized
eventually became epiphyllous parasites may have the leaf. In other situations parasites may have
inhabited the soil where organic molecules were initially entered through plant roots. Although
more easily obtainable. Only when there was there is little evidence in fossil roots and other
extensive competition for edaphic nutrients, or underground organs indicative of pathogen penet-
when some modification of the fungal life history ration (e.g. tissue disruption), there are some ana-
evolved (e.g. production of air-borne spores), did tomical characters in many fossil plants that are
leaf surfaces become a potential nutrient source identical to those regarded as mechanical barriers
that eventually became exploited. Various chemical to pathogens in extant plants (e.g. periderm layers).
and mechanical plant defenses may have also For example, Banks and Colthart (1993)
served as deterrents to the colonization of leaves illustrated wound tissue in the Devonian plant
by fungi before the Cretaceous. Thus, it may have Pdophyton that anatomically resembles necrophy-
taken a considerable period of time for fungi to latic periderm. In some extant plants this periderm
evolve the appropriate enzyme systems (e.g. develops as a result of fungal invasion
cutinase) to enter the plant. (Woodward, 1992).
Fungi may have also been inhibited from colo- It is interesting to note that in many modern
nixing leaves as a result of the presence of other plants waterlogging is the impetus for the ingress
fungi, shoot inhibiting endophytes, in particular. of root-invading fungi. It is clear that such condi-
An interesting hypothesis has been presented by tions were common in Carboniferous swamp com-
Wilson (1993). He suggested that in extant mutual- munities. Nevertheless, there is little evidence of
istic symbioses the above-ground fungal endo- fungal activity in the roots and underground
phytes may have evolved to become the primary organs of these plants. Is the absence of this
defense against herbivory as a result of their ability interaction the result of a chemical defense of the
 TN. Taylor, J.M. Osborn/Review of Pakaeobotanyand Palynology 90 (1996) 249-262 251

plants that inhabited these swamps, the result of important ecological advantage in increasing bio-
our inability to identify these responses in the mass. Thus, this biotrophic symbiosis and the
fossil record, or simply the fact that such inter- evolution of the arbuscule may have evolved in
actions did not evolve until much later? The antiq- response to this selective pressure. Recently,
uity of various types of fungal interactions (as Garbaye (1994) commented on the importance of
documented from the Devonian Rhynie chert) certain types of bacteria in the establishment of
suggests that the absence of fungal activity in the mycorrhizae. Such helper bacteria are suggested
underground organs of Carboniferous plants is to be involved in: recognition and receptivity
probably the result of fungi being excluded from between the fungus and host, germination of the
specific ecosystems by certain abiotic constraints, fungal spores, enhancement of fungal growth, and
such as water acidity. as a modifier to the physico-chemical properties
of the soil. Few bacteria have been identified in
the fossil record and none with mycorrhizae, how-
4. Biotropbic interactions ever, the apparent widespread occurrence of bacte-
ria in extant mycorrhizae suggests that they could
Biotrophic interactions may be defined as those have been important in the initial evolution of
interrelationships between a fungus and its host in biotrophic symbioses.
which there is a continual source of carbohydrates Extant arbuscular fungi also function to protect
directed to the fungus. Minimal tissue damage and host roots from pathogens, increase the solubility
morphological alteration in the host are also char-
of soil minerals, and produce plant growth hor-
acteristics of biotrophic associations (Lewis, 1974).
mones; all of which would contribute substantially
Such mutualistic fungal/plant interactions have
to the establishment and maintenance within an
been hypothesized as being ancient, and perhaps
ecosystem. The fact that arbuscular mycorrhizae
the catalyst for the terrestrialization of the Earth
are widespread today in their association with
by land plants (Jeffrey, 1962; Pirozynski and
flowering plants has been the basis for suggestions
Malloch, 1975). Only recently, however, has the
regarding the antiquity of this biotrophic symbio-
sine qua non of biotrophy, the fungal arbuscule
sis. In extant plants, these root-inhabiting endo-
(Plate III, 4), been demonstrated in the early land
symbionts are represented by approximately 100
plant Agluophyton major (Remy et al., 1994). The
species of Zygomycetes, all classified within the
fossil arbuscules consist of a specialized hyphal
trunk that repeatedly dichotomizes within the plant Glomales (Morton and Benny, 1990). The mor-
cell to form a highly branched structure that is phological similarity between modern and the
considered the site of physiological exchange Early Devonian arbuscules indicates that the
between the fungus and host in extant systems physiological exchange structure in this symbiosis
(Bonfante-Fasolo, 1984). Although phosphorous has remained stable for a considerable period of
may have been readily available to aquatic, land geologic time. However, the fact that these endo-
plant ancestors, this may not have been the case phytes are so widespread today suggests that the
in the oxidative, terrestrial environment. Because biochemistry of the fungal enzyme system is also
modern arbuscular mycorrhizae are known to highly evolved. There is, however, one distinct
increase the uptake of host phosphorous, the difference between the Early Devonian arbuscules
advantages of this type of biotrophic interaction and those of extant mycorrhizae. In living plants,
in a presumably nutrient-poor environment is obvi- arbuscules are extremely ephemeral, and once
ous. However, mycorrhizae may also transfer other degeneration takes place host cells revert back to
nutrients to the host and some of these may have their normal function. In Aglaophyton, it appears
been especially critical early in the evolution of that once arbuscules no longer functioned as
mycorrhizal symbioses (Pate, 1994). But arbuscu- physiological exchange sites, the host cells col-
lar mycorrhizae are also known to increase nitro- lapsed and new cells were formed in the cortex
gen uptake (Tobar et al., 1994), an equally (Taylor et al., 1995).
258 T. N. Taylor, J. M. Osborn/Review of Palaeobotany and Palynology 90 (1996) 249-262

Generally absent from discussions of biotrophy of many aquatic arthropods (Lichtwardt, 1986).
in the fossil record is any consideration of ectomy- The first fossils from this fungal group were
corrhizae. Modem ectomycorrhizae are relatively reported from the Triassic of Antarctica and con-
common and represented by more than 5000 sist of elongate thalli that are attached to an insect
species of Basidiomycetes. These fungal symbionts cuticle by a holdfast (White and Taylor, 1989b)
infect root tips, with some hyphae extending into (Plate III, 3). Although nothing is known about
the outer zone of the cortex to form an extensive the animal that contained these fungi, the morphol-
network termed the Hartig net. Root hairs do not ogy of the fossil fungus provides details about this
develop in this region, and the root is characteristi- interaction. Arthropods are known from the Early
cally short overall. Many ectomycorrhizae induce Devonian, but to date none of these has been
the production of short, knobby lateral roots. described in fungal associations. Fungi have, how-
Although it would appear that this type of mycor- ever, been described from older sediments (Late
rhizal infection could easily be detected in the Silurian) that are suggestive of a possible arthro-
fossil record, to date there are only a few examples. pod/fungus interaction. These include fossils that
One of these consists of both nodular and abbrevi- are considered to be coprolites, each composed of
ated lateral roots in a Cretaceous conifer that are a mass of fungal hyphae; the hyphae are interpre-
morphologically identical with those formed in ted as evidence for the presence of fungivores
ectomycorrhizal associations of the Pinaceae (Sherwood-Pike and Gray, 1985). Although
(Cantrill and Douglas, 1988). Fungi suggested as fungal/animal interactions will continue to be
being ectomycorrhizal have also been reported in difficult to document in the fossil record, they
several Middle Eocene permineralized organs of constitute an important component of modem
Metasequoia (Basinger, 1981). However, the pres- ecosystems, and were certainly significant in the
ence of hyphae in cortical cells of these roots and geologic past.
absence of a Hartig net suggests that these fungi
were not ectomycorrhizae, but rather saprobes.
LePage et al. (1995) have recently discovered well- 6. Lichens
preserved ectomycorrhizae in permineralized
Eocene pine roots. Root hairs are absent from the Lichens represent another modem biological
lateral roots; however, knobby structures are pre- interaction in which fungi play a critical role. In
sent, two host responses to the ectomycorrhizal this symbiosis, the photobiont is generally a green
infection. Also present is evidence of a Hartig net. alga, while the fungal component (mycobiont) is
The fossil fungus is compared with the extant generally an Ascomycete; two groups that have a
genus Rhizopogon, a common ectomycorrhiza of long geologic record. Because of the antiquity of
conifers, in particular pines. Indirect evidence of both groups, and because the lichen thallus should
ectomycorrhizal activity has also been suggested be easily fossilized, it is surprising that this type
based on the presence of needle-fiber calcite found of interaction is not well represented in the fossil
associated with root encrustations (Wright, 1986). record. Rather, there are just a few reports of
lichens throughout geologic time (e.g. Sherwood-
Pike, 1985). It is generally assumed that the
5. Fungal/animal interactions absence of fossil lichens can be attributed to several
factors, including the dry habitats in which they
Less frequently encountered in the fossil record, commonly grow today and/or the fact that this
but certainly common, are numerous fungal inter- type of symbiosis has only recently evolved.
actions with animals. The most common of these, As a result of information now known about
no doubt, were saprobic, but there were other fungal/plant interactions in the Early Devonian, it
interrelationships as well. One example includes is highly probable that algal/fungal symbioses in
the Trichomycetes, a specialized group of obligate the form of lichens are also ancient. The recent
zygomycetous fungi that today live in the hind gut report of the extant cyanobacterium ZVostocpuncti-
 T. N. Taylor, J. M. Osborn/Review of Palaeobotany and Palynology 90 (I 996) 249-262 259

forme endosymbiotically associated with an endo- lichens. To date, it has not been possible to identify
gonaceous fungus that is closely related to Glomus the photobiont in any of these fossil organisms,
(Kluge et al., 1992) provides some evidence that but this may simply reflect the fact that none has
early fossil interactions with Zygomycetes were been seriously considered to represent a lichen.
possible. The extensive record of cyanobacteria The antiquity of fungi, cyanobacteria, and green
throughout the Precambrian adds additional sup- algae would suggest that the lichen symbiosis
port that these organisms and fungi may have evolved quite early. It is evident that fungi were
formed early symbioses. involved in various types of complex nutritional
Perhaps the best explanation for the apparent modes with other organisms early in geologic time.
absence of fossil lichens is simply the inability of This fact provides additional evidence to support
paleobiologists to recognize them in the fossil the hypothesis that the lichen symbiosis was not
record. There are numerous so-called, enigmatic only present, but was a critical component of the
organisms that first appear in the Ordovician; these early terrestrial ecosystem.
clearly represent the level of evolution seen in
extant lichens. Recently, Stein et al. (1993) sug-
gested that the Middle Devonian, thalloid fossil
Spongiophyton is a lichen. Nothing is known about
the internal structure of this organism, although 7. Abiotic interactions
cell outlines on the inner surface of the cuticle may
represent the impression of fungal hyphae. Although the principal focus of this paper is the
Edwards and Rose (1984) have hypothesized that biological interrelationships among fungi and
the pores in another enigmatic plant,
other organisms, it is important to point out that
Nematothallus, may have functioned in gas fungi have also played an important role in the
exchange similar to pseudocyphellae in the epicor-
sediment cycle. For example, fungal borers
tex of certain types of lichens (Hale, 1981).
together with algae are important in the production
Another possibility is that the various pores in
of carbonate fines (Schneider, 1977). Micritization,
many of these problematic plants represent pockets
the process by which carbonate skeletal material
that contained cyanobacteria similar to those
is dissolved and replaced by r&rite, also involves
found in certain extant bryophyte symbioses
the activities of fungi (Plate III, 6) (Kobluk and
(Sprent and Raven, 1985). In this association, not
Risk, 1974). Furthermore, fungi are necessary in
only would the cyanobacterium provide a source
both the formation of soils and the processes
of carbohydrates to the fungal partner, but it
might also function in nitrogen fixation. If the involved in biomineralization. One major problem
photobiont in early lichen symbioses was a in interpreting the activities of fungi in this geologic
cyanobacterium, then it may be even more difficult context is the fact that the fungus is rarely fossil-
to distinguish filaments of the photobiont from ized, and when it is preserved it is difficult to
those of the fossil fungus. distinguish hyphae from endolithic algae (Scott,
Several additional Paleozoic plants with uncer- 1981). Measuring the activities of fungi within a
tain systematic affinities may also represent a level physical context will continue to remain a difficult
of evolution that has its closest analogue with task; however, the importance of these organisms
modem lichens. These include, for example, in the formation of soils and other substrates is
Prototaxites, Nematothallus, and Nematasketum, now only beginning to be fully appreciated.
all constructed of interwoven tubes of differing Unravelling some of the complex interactions in
sizes. Some tubes have unusual septal pores, which fossil fungi have played an important role
whereas irregular thickenings may be present in will require not only new insights, but an apprecia-
others. Moreover, the amorphous layer that covers tion of the full spectrum of activities found in
many of these fossil organisms may be analogous modem ecosystems. These can then be measured
to the mucilage that is produced by some living against evidence extracted from the rock record.
260 T. N. Taylor, J. M. OsbornjReview of Palaeobotany and Palynology 90 ( 1996) 249-262

8. Conclusions some advantage in its ability to obtain nutrients

located well within plant tissues. As these
The question is no longer whether there is an fungal/plant interactions continued to form, per-
adequate assemblage of fungi in the fossil record, haps the fungi overcame the plant’s defensive
but rather how these heterotrophs interacted with mechanisms so that parasitic and, eventually, biot-
other organisms. Although it is becoming increas- rophic interrelationships evolved.
ingly apparent that all major groups of fungi are In certain types of ancient fungal interactions
very ancient, deciphering the levels of interaction the opportunity exists to evaluate more biological
is far more difficult. Currently the Devonian dimensions, such as host specificity. If enough host
Rhyme chert represents the oldest paleoecosystem symptoms can be identified from the fossil record,
in which fungal interactions have been docu- it may be possible to assemble details about cellu-
mented. The chert contains examples of sapro- lose and lignin degradation processes, and thus
phytic, parasitic and biotrophic interactions that evaluate this important component of fungal activ-
involve fungal associations with land plants, algae, ity through geologic time. The distribution and
and other fungi. The presence of various host evolution of fossil fungal forms can only be ade-
responses indicates that many of these interactions quately evaluated based on comparisons of their
are also ancient. The fact that there is evidence of vegetative and reproductive structures with those
some nutritional balance between a fungus and its of modern groups. Moreover, the phylogenetic
host strongly suggest that symbiotic interactions relationships of an increasing number of modern
in the form of lichens may also be common in the fungal groups is being proposed based on nucleo-
fossil record. We suggest that in the years ahead tide sequences of small subunit ribosomal RNA
it is studies of fungi that will play an increasing (Hibbett, 1992). In some instances these data
role in understanding the evolution of the ter- confhrn more traditional patterns of classification,
restrial biota. while in others the relationships are not as clearly
As fossil fungi continue to be described it will defined. Despite the importance of these new types
be especially important to document the full range of molecular data sets, identifying the diversity,
of their interactions in both the biotic and abiotic abundance, and distribution of fungal groups in
environments. For example, there has been a great time and space can only be determined based on
deal of speculation regarding the evolution of the analysis of the fossil record.
various fungal nutritional modes (saprotrophic, The next major frontier in paleomycology must
necrotrophic, biotrophic), including which consti- be the documentation of fungal interactions with
tutes the primitive condition (Lewis, 1974). The algae and cyanobacteria. We would predict that
fact that such interactions are all well represented there should be a recoverable record of these
in the oldest anatomically preserved land plants interactions because there are numerous exquisitely
necessitates that geologically older assemblages of preserved Precambrian biotas around the world.
organisms be critically analyzed for such The reports of diverse microbiotas from several
interactions. upper Proterozoic sites (e.g. Knoll and Swett, 1985;
Despite the difficulties and constraints encoun- Butterfield et al., 1990), increases the probability
tered when studying fossil fungi, there are impor- that fungal remains are also preserved in these
tant inferences that the oldest fungal/plant assemblages. The analysis of these microbial biotas
interactions can provide. For example, we know may provide the earliest details about the evolution
that some Rhyme chert endophytes had the enzyme of fungal nutritional modes in time and space.
systems capable of penetrating the host cell wall,
but not the plasmalemma during the formation of
arbuscules. Initially these fungi may have been Acknowledgements
saprobes that had the ability to penetrate both
moribund and dead cells. A heterotroph with such This study was supported by funds from the
an invasive mycelium would have obviously had National Science Foundation (OPP-9315353) and
 T.N. Taylor, J.M. OsbornjReview of Palaeobotany and Palynology 90 (1996) 249-262 261

a Senior Fellowship from the Von Humboldt Hibbett, D.S., 1992. Ribosomal RNA and fungal systematics.
Foundation to the first author. Trans. Mycol. Sot. Jpn., 33: 533-556.
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