Fungi from the Rhynie chert: a view from the dark side · Fungi from the Rhynie chert: a view from...

Fungi from the Rhynie chert a view from thedark side

T N Taylor S D Klavins M Krings E L Taylor H Kerp and H Hass

ABSTRACT The exquisite preservation of organisms in the Early Devonian Rhynie chertecosystem has permitted the documentation of the morphology and life history biology of fungibelonging to several major taxonomic groups (eg Chytridiomycota Ascomycota Glomero-mycota) The Rhynie chert also provides the first unequivocal evidence in the fossil record of fungalinteractions that can in turn be compared with those in modern ecosystems These interactions in theRhynie chert involve both green algae and macroplants with examples of saprophytism parasitismand mutualism including the earliest mycorrhizal associations and lichen symbiosis known to datein the fossil record Especially significant are several types of specific host responses to fungalinfection that indicate that these plants had already evolved methods of defence similar and perhapsanalogous to those of extant plants This suggests that mechanisms underlying the establishment andsustenance of associations of fungi with land plants were well in place prior to the Early DevonianIn addition a more complete understanding of the microbial organisms involved in this complexecosystem can also provide calibration points for phylogenies based on molecular data analysis Therichness of the microbial community in the Rhynie chert holds tremendous potential for document-ing additional fungal groups which permits speculation about further interactions with abiotic andbiotic components of the environment

KEY WORDS Early Devonian host responses microbial interactions mutualism parasitismsaprophytism

The discovery of plant remains in the Rhynie chert by Mackie(1914) and subsequent detailed accounts by Kidston amp Lang(1917 1920a b 1921a b) provided a wealth of informationthat has served as a baseline for our understanding of earlyterrestrial life Although the focus of the majority of thesestudies has been on the above-ground components of theecosystem a remarkable and critical component of EarlyDevonian terrestrial life occurred in the rhizosphere on orbeneath the surface of the substrate In their extraordinaryaccount of the Rhynie chert flora Kidston amp Lang (1921b)provided the first report of the microbial components in theecosystem in the form of fungal hyphae thick-walled restingspores and clusters of cells that they interpreted as bacteria Ofperhaps greater biological significance was their recognition ofthe role that the Rhynie chert fungi played in nutrient cyclingand as biotrophs that interacted with the macroplants Theseauthors also suggested that some of the fungi may have formedsymbiotic associations with one or more of the land plantsSince the original description of fungal remains in theRhynie chert there have been numerous reports that havecarefully documented the structure morphology and in someinstances the biology of the Rhynie chert organisms many ofthem summarised in this symposium volume As a result weknow a great deal about the individual organisms that existedin this ancient environment and can now begin to explore someof the interactions that served as drivers for the Rhynie chertecosystem

Recent ultrastructural and molecular data have expandedthe definition of fungi and their systematic relationships withother heterotrophic organisms and as a result the lsquofungirsquo areregarded as a polyphyletic and heterogeneous group estimatedto be comprised of more than 1middot5 million species of whichfewer than 100000 have been described and named to date(Hawksworth 1991) They occupy almost every ecologicalniche and are involved in a variety of different interactions in

terrestrial aquatic and marine environments They formassociations that can be harmful andor of benefit to organismsthat make up the ecosystem (Fig 1A) as well as to the stabilityof the ecosystem as a whole (eg nutrient cycling) In modernecosystems fungi decay organic debris and occur as parasitespathogens and mutualists of both plants and animals Somehave entered into complex symbiotic associations with landplants whilst others have partnered with algae and cyanobac-teria to form lichens (Fig 1A) Fossil fungi possess a limitednumber of useful characters with which to identify taxa wehave relied on the traditional classification that defines fourphyla Chytridiomycota Zygomycota Ascomycota andBasidiomycota (McLaughlin amp McLaughlin 2001) but alsorecognise the Glomeromycota a monophyletic group thatincludes the arbuscular mycorrhizae and related forms Alisting of the fungi that have been described from the Rhyniechert to date and the hosts with which they are associated isprovided in Table 1 We have also included the modernanalogues if these were suggested by the authors

An appreciation of the microbial community in fossil eco-systems has been especially slow to develop since the focus ofresearch has generally been directed at the macroplants andanimals rather than at the microorganisms (bacteria cyano-bacteria microalgae fungi zoo- and phytoplankton) In thecase of fungi palaeontologists may not be adequately trainedto distinguish these organisms in samples or recognise indirectevidence of their presence Most researchers generally tend tocollect specimens that are complete and well-preserved ratherthan those that are degraded due to the activity of saprophyticand parasitic microorganisms As a result the fossil microbialworld is typically overlooked and does not become part of thediversity record Finally information about fossil fungi isoften published in non-palaeontological journals which hasnot only resulted in a perception that little of the fungal recordis preserved but also that there is insufficient knowledge of

Transactions of the Royal Society of Edinburgh Earth Sciences 94 457ndash473 2004 (for 2003)

Tab

le1

Rhy

nie

cher

tm

icro

bial

taxa

and

asso

ciat

edor

gani

sms

Ass

ocia

ted

mac

ropl

ant

spor

ophy

tes

Ass

ocia

ted

mac

ropl

ant

gam

etop

hyte

sA

lgal

bac

teri

alas

soci

ates

Fun

gal

asso

ciat

esSu

gges

ted

mod

ern

equi

vale

ntta

xaR

efer

ence

Chy

trid

iom

ycot

aK

risp

irom

yces

disc

oide

sP

alae

onit

ella

cran

iiP

hlyc

toch

ytri

um

Cat

enoc

hytr

idiu

mT

aylo

ret

al

1992

a

Lyo

nom

yces

pyri

form

isP

alae

onit

ella

cran

iiR

hizo

phyd

ium

Tay

lor

etal

19

92a

Mill

erom

yces

rhyn

iens

isP

alae

onit

ella

cran

iiE

ndoc

hytr

ium

E

ntop

hlyc

tis

Sor

odis

cus

Wor

onin

aT

aylo

ret

al

1992

a

Pal

eobl

asto

clad

iam

iller

iA

glao

phyt

onm

ajor

Allo

myc

es

Bla

stoc

ladi

opsi

sT

aylo

ret

al

1994

R

emy

etal

19

94a

Unn

amed

holo

carp

ican

deu

carp

icfo

rms

Hor

neop

hyto

nlig

nier

iA

glao

phyt

onm

ajor

Lyo

noph

yton

rhyn

iens

is

Agl

aoph

yton

maj

orP

alae

onit

ella

cran

iiP

edia

stru

m-l

ike

alga

Fun

gal

spor

esan

dve

sicl

esE

ntop

hlyc

tis

Hyp

hoch

ytri

um

Now

akow

skie

lla

Olp

idio

psis

O

lpid

ium

S

pize

llom

yces

T

ripa

rtic

alca

r

Illm

an19

84

Tay

lor

etal

19

92b

Has

set

al

1994

Zyg

omyc

ota

Glo

mit

esrh

ynie

nsis

Agl

aoph

yton

maj

orG

lom

usT

aylo

ret

al

1995

Pal

aeom

yces

aggl

omer

ata

Rhy

nia

gwyn

ne-v

augh

anii

Kid

ston

ampL

ang

1921

bP

alae

omyc

esas

tero

xylii

Ast

erox

ylon

mac

kiei

Kid

ston

ampL

ang

1921

bP

alae

omyc

esgo

rdon

iiA

ster

oxyl

onm

acki

ei

Hor

neop

hyto

nlig

nier

iR

hyni

asp

Kid

ston

ampL

ang

1921

b

Pal

aeom

yces

gord

onii

var

maj

orR

hyni

agw

ynne

-vau

ghan

iiK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

horn

eae

Hor

neop

hyto

nlig

nier

iK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

sim

pson

iiR

hyni

agw

ynne

-vau

ghan

iiK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

vest

ita

Ast

erox

ylon

mac

kiei

Kid

ston

ampL

ang

1921

bW

infr

enat

iare

ticu

lata

myc

obio

ntL

iche

nC

yano

bion

tT

aylo

ret

al

1997

Asc

omyc

ota

Unn

amed

peri

thec

ial

asco

myc

ete

Ast

erox

ylon

mac

kiei

Pyr

enom

ycet

esT

aylo

ret

al

1999

lsquoOom

ycot

arsquoU

nnam

edm

ycel

iaP

roto

taxi

tes

tait

iA

poda

chly

apy

rife

raH

arve

yet

al

1969

Cya

noba

cter

iaA

rcha

eoth

rix

cont

exta

Osc

illat

oria

Kid

ston

ampL

ang

1921

bA

rcha

eoth

rix

osci

llato

rifo

rmis

Osc

illat

oria

Kid

ston

ampL

ang

1921

bK

idst

onie

llafr

itsc

hii

Stig

onem

atac

eae

Cro

ftamp

Geo

rge

1958

Lan

giel

lasc

ourf

eldi

iSt

igon

emat

acea

eC

roft

ampG

eorg

e19

58R

hyni

ella

verm

ifor

mis

Scyt

onem

atac

eae

Cro

ftamp

Geo

rge

1958

Rhy

nioc

occu

sun

ifor

mis

Chr

ooco

ccac

eae

Edw

ards

ampL

yon

1983

T

appa

n19

80W

infr

enat

iare

ticu

lata

cyan

obio

ntL

iche

nZ

ygom

ycet

em

ycob

iont

Glo

eoca

psa

Chr

ooco

ccus

C

hroo

ccci

diop

sis

Tay

lor

etal

19

97

458 T N TAYLOR ET AL

fungal interactions with other fossil organisms Our under-standing of the fossil record of fungi and other microbes hasgreatly increased in the past decade in large part due to theexquisite preservation and diversity of organisms in the Rhyniechert The focus of this paper is to review the life historybiology of fungi that have been identified to date from theRhynie chert and to document interactions host responsesand the impact of fungi on the lsquodark sidersquo of this EarlyDevonian community (Fig 1B) In comparing the Rhyniechert with modern ecosystems (Fig 1A) we further speculateon a variety of interactions that may yet await discovery

1 Material and methods

More than ten fossiliferous beds have been identified in theRhynie chert deposits (Trewin amp Rice 1992) and the organismsare preserved as siliceous permineralisations As a resultspecimens must be studied in petrographic thin sectionsPhotomicrographs were made using oil immersion objectivesdirectly on the rock surface Slides are kept in the collection ofthe Forschungsstelle fur Palabotanik Westfalische Wilhelms-Universitat Munster Germany Slide numbers are includedwith the figure captions

2 Microbial interactions in the Rhynie chertecosystem

A large number of microbial interactions have been docu-mented from the Rhynie chert and many yet remain to bedeciphered (Fig 1A B) Within these deposits are a variety ofexamples of fungi occurring as saprophytes of plants andanimals and as parasites of macroplants algae and otherfungi It is likely that many of the macroplants in the Rhyniechert were associated with fungi in an endomycorrhizal sym-biosis but to date this relationship has only been demon-strated in a single taxon It has been presumed that thissymbiosis was mutually beneficial to both the host (Aglaophy-ton major) and the fungus however the presence of a glomero-mycete in Aglaophyton does not necessarily indicate that abeneficial relationship existed between these two organismsFor example some mycorrhizal interactions may be mutualis-tic or parasitic depending on the physiology and environmen-tal conditions experienced by the plant (Redman et al 2001)

We may not be able to untangle all of the dynamics of theinteractions of fungi in the community structure of the Rhyniechert since a single fungus can be pathogenic to one type oforganism whilst providing benefit to another as well as actingas a decomposer of still others (Redman et al 2001) Never-theless the interactions that have been described to date offerthe opportunity to more fully understand the microbial worldin the Early Devonian

21 SaprophytesTo date most of the documented fungal interactions withplants in the Rhynie chert occur through the activities ofsaprophytes These include fungal hyphae ramifying throughdegrading plant tissues as well as the presence of chytrids(Chytridiomycota) (Fig 2andashi) and ascomycetes (Ascomycota)(Fig 2jndashl 5andashc) These organisms together with bacteria havecontributed to the large amount of degraded plant biomass inthe chert that cannot be classified Kidston amp Lang (1921b)described and illustrated numerous examples of septate andaseptate hyphae showing various patterns of branching someterminating in thin-walled vesicles and others forming thick-walled resting spores (Fig 2a) Since these fungi occur inassociation with all of the Rhynie chert organisms they wereobviously a critical component of the microbial world at thattime

211 Chytridiomycota Chytridiomycetes are well repre-sented in the Rhynie chert and include unicellular and multi-cellular forms that display saprophytic andor parasiticinteractions with the macroplants (Illman 1984 Taylor et al1992a b c Remy et al 1994a Taylor et al 1994) Members ofthis group were probably the most common microbial elementand may have been the principal decomposers of organicmaterial in the ecosystem Modern chytrids are primarilyaquatic and occur in fresh-water habitats although a few maybe marine others are known from a wide range of terrestrialecosystems including bogs dry soils or even desert sandsMost exist as saprophytes but some are parasitic on algaeother fungi various types of animals and underground partsof plants Some chytrids occur in the guts of herbivores asrumen symbionts They act as important elements of modernterrestrial ecosystems by serving as cellulose decomposers

Clusters of chytrids including individuals with well-developed zoosporangia have been reported from a variety ofdifferent Rhynie macroplant types (Taylor et al 1992c) Some

Figure 1 Comparison of interactions among organisms in modern ecosystems (A) with those that are known todate from the Lower Devonian Rhynie chert (B)

FUNGI FROM THE RHYNIE CHERT 459

occur in cells as saprophytes and parasites others are presentalong plant stems and on the surface of various plant organsWhilst their small size sometimes makes it difficult to accu-

rately characterise the types present their ubiquitous occur-rence has provided an opportunity to detail stages of thecomplete life history of some forms (Illman 1984 Taylor et al


1992c) In one common type zoosporangia develop withinthin-walled algal cells and form a zoospore discharge tube thatextends through the cell wall (Fig 2b c) Zoospores exit thealgal cell form cysts and subsequently infect new cells torepeat this simple life cycle (Fig 3) Other chytrids in theRhynie chert have infected softer cortical regions of stems andcan be identified based on the presence of degraded cells andtissue systems (Fig 2d) The presence of several differentmorphological types of chytrids on the same host has impor-tant implications since species interactions may influencedamage to the host and these interactions may be synergistic orcompetitive (Takenaka 1995)

Not all saprophytic chytrids in the Rhynie chert wereunicellular One unique form is Paleoblastocladia milleri whichto date has been found only associated with Aglaophyton(Table 1 Remy et al 1994 Taylor et al 1994) The fungusoccurs as compact tufts of non-septate hyphae that arisethrough stomata or between the cuticle and epidermis of thehost (Fig 2e f) There are three different types of reproductivestructures that occur on two types of thalli of P milleri Themost common form consists of bulb-shaped zoosporangia(Fig 2f g) that occur on thalli with dichotomously branchinghyphae (sporothalli) most of these are terminal range up to30 m in diameter and contain zoospores that are spherical tohexagonal in face view each with an opaque inclusion (Fig2g) Also present on some of these sporothalli are thick-walledstructures that have been interpreted as resting sporangiawhich produced spores that germinated into separate newthalli (gametothalli) The third type of reproductive structureconsists of globose structures that typically occur in chains onthe gametothallus (Fig 2h) these have been interpreted asgametangia Because there is sufficient material at differentstages of development it is actually possible to trace the life

history biology of this unusual fungus a rare opportunity infossil fungi Based on the presence of separate thalli producingeither zoospores or gametes Paleoblastocladia has been inter-preted as possessing a distinct isomorphic alternation of gen-erations (Fig 4) a feature that is almost unknown in modernfungi with the exception of some members of the Blastocladi-ales It is interesting that both sporothalli and gametothalli areclosely associated on the same Aglaophyton axes (Fig 2i)Other than the fungus disrupting the cuticle on the surface ofthe Aglaophyton axes no specific host response has beenobserved to date We have interpreted Paleoblastocladia as asaprophyte because of the similarity of its morphology andlife history to modern members of the Blastocladiales (egAllomyces Euallomyces and Blastocladia) However withouta specific host response it is difficult to accurately interpret thetype of interaction between the fungus and host It is interest-ing to note that in modern ecosystems Blastocladia displaysenhanced growth in the presence of increased CO2 (Held et al1969) The high CO2 levels postulated as occurring during theDevonian (Berner amp Kothavala 2001) may represent a selectivepressure responsible for structural and life history complexitiesseen in Paleoblastocladia

22 ParasitesParasites obtain nourishment from other living organismsMany parasitic fungi however are also capable of growing ondead organic matter and thus are termed facultative parasitesor facultative saprophytes When examining a fossil thepresence or absence of a host response can provide informa-tion about the level of interaction but it is not alwaysdefinitive This may be further complicated by the fact thatsome fungi are endophytes and thus provide no observablehost response symptoms (Schulz et al 1999)

221 Chytridiomycota Necrotic regions of opaque materi-als in some of the macroplants suggest that some chytridsparasitised their hosts (Fig 2d Table 2) however the actualchytrids have not been identified in these areas of the stemParasitic chytrids have been described associated with severalplants in the Rhynie chert (Fig 5dndashk) particularly with thegreen macroalga Palaeonitella cranii (Table 1 Taylor et al1992a b c) Krispiromyces discoides is a unicellular chytridconsistently found on stems of Palaeonitella (Table 1) Thisfungus is characterised by a saucer-shaped zoosporangium thatremains on the outside of the cell wall whilst a rhizomyceliumextends through the wall into the cell lumen (Fig 5e) There isalways a host response in this association that occurs betweenchytrid and alga infected cells display a hypertrophic responsein which they may be up to ten times larger than normal nodalcells (Fig 5d Table 2 Taylor et al 1992a) This pattern of hostcell enlargement is identical to that seen in the extant charo-phyte Chara an alga that is believed to be closely related toPalaeonitella when it is parasitised by a chytrid (Karling1928)

Rhynie chert chytrids were probably parasites of green algaethat occurred in small colonies in the cortical cells of degradedmacroplants (Fig 5f g Table 1 Taylor et al 1992a) Some of

Figure 2 (a) Thin section showing hyphae and swollen vesicles Slide P1463 scale bar=100 m (b) Rhizoidal cell of Palaeonitella cranii showing2 chytrid zoosporangia with discharge papillae extending through cell wall Slide P1478 scale bar=25 m (c) Chytrid zoosporangium with neckextending through cell wall Slide P1478 scale bar=15 m (from Taylor et al 1992a) (d) Section of Rhynie chert macroplant stem showingdisruption of cortex (arrow) and associated opaque necrotic area Slide P1816 scale bar=1 mm (e) Two tufts of Paleoblastocladia milleri on stemsurface of Aglaophyton major Slide P2057 scale bar=200 m (f) Well developed tuft of P milleri showing terminal zoosporangia Slide P2056 scalebar=50 m (g) Zoosporangium with well developed zoospores Slide P2056 scale bar=25 m (h) Two pairs of gametangia note distinct sizedifference Slide P2054 scale bar=25 m (i) Portion of sporothallus (S) and gametothallus (G) showing differences in reproductive structures SlideP2084 scale bar=25 m (from Remy et al 1994a) (j) Transverse section of Asteroxylon stem showing several fungal ascocarps (arrows) just beneathstem epidermis Slide P3404 scale bar=1 mm (k) Base of an enation with several ascocarps (arrows) Slide P3469 scale bar=750 m (l)Longitudinal section of perithecium showing central cavity containing asci Note guard cells (arrows) surrounding ostiole Slide P3435 scalebar=100 m

Figure 3 Suggested stages in the life history of a fossil chytrid basedon information collected from the Rhynie chert


these Pediastrum-like algal cells are up to 12 m in diameterand arranged in loose clusters of several dozen cells Chytridzoosporangia occur inside these cells and display a smalldischarge tube that extends through the cell wall (Fig 5g h)through which zoospores were liberated Other chytrids arecommon both inside and on the surface of spores of variousmacroplants (Fig 5i j k) Some of these are associated withgerminating gametophytes others are present within the lumenof the spore

In a few instances it has been possible to identify swellingsalong the underground parts of various Rhynie chert plantsAxes of Nothia aphylla possess horizontal subterranean rhi-zomes from which extend multicellular rhizoids Sphericalnodule-like structures occur on some of these rhizoids andappear to represent an outgrowth of the rhizoid (Fig 5l) Onepossible explanation is that these structures represent aninfection point for a parasitic fungus such as a chytrid sincethin threads can be traced into the rhizoid Bulges andswellings may also represent another potential host response(hyperplasia) which involved chytrids as the causal agent (Fig5m Table 2) Hyperplasia causes an abnormal proliferation inthe number of cells and contributes to an increase in the size ofan organ There are various cortical regions in the macroplantswithin the chert that show aggregations of cells that mayrepresent this host response

222 Ascomycota Ascomycetes today are significantsaprophytic components of modern ecosystems They occupy awide range of habitats and enter into a variety of interactionswith other organisms in the environment including pathogenicas well as beneficial and mutualistic relationships many formsymbiotic associations with arthropods Current classificationssubdivide the ascomycetes into three groups Archaeasco-mycetes and Hemiascomycetes (the yeasts and assorted taxa)which are primarily unicellular and lack an ascoma (sporocarpthat contains sexually-produced spores) and Euascomyceteswhich consists of filamentous forms that produce ascomatathat contain specialised cells (asci) that produce a specificnumber of sexually-produced haploid spores (ascospores)(Alexopoulos et al 1996) Asexual reproduction is carried out

by various methods that result in the formation of spores Thefossil record of the ascomycetes is poorly understood Fossilevidence has been reported from Upper Silurian rocks in theform of macerates and consists solely of specialised asexualcells (phialides) (Sherwood-Pike amp Gray 1985) Other fossilssuggested as having affinities with ascomycetes have beenreported in the Devonian and Carboniferous (Taylor 1995)

The best example to date of a perithecial ascomyceteinterpreted as a parasite is now known from the Rhynie chert(Table 1 Taylor et al 1999 in press) Beneath the epidermisand on the enation bases of Asteroxylon mackiei stems arespherical opaque structures (Fig 2j k) Detailed examina-tion shows that these represent flask-shaped reproductivestructures (perithecia) of an ascomycete (Fig 2l) Peritheciaare up to 400 m in diameter and characterised by shortostiolate necks that typically protrude from the epidermisthrough stomatal openings of the host plant Lining theinterior of the perithecium are elongate thin-walled filaments(paraphyses) interspersed with asci that contain ascospores(Fig 5a) Ascospores are typically unicellular but in someasci and interspersed in the locule of the perithecium sporesmay be one to five times septate (Taylor et al 1999) Someascospores possess a germ tube arising from one end of thespore Small specialised tufts of hyphae (conidiophores) thatbear chains of spores at the tips occur along the axes of thehost (Fig 5b) and are also associated with immature perith-ecia These typically occur in shallow depressions on thestems and may extend up to 150 m from the stem surfaceConidiophores are typically smooth branch occasionallyand form chains of arthrospores Mature arthrospores arecube-shaped with slightly rounded ends and serve as reinfec-tion agents

One possible reason that fossil perithecial ascomycetes havenot previously been described is the fact that when observed atrelatively low magnifications perithecia appear similar in sizeand general organisation to chlamydospores that are commonin the macroplants (Fig 5c) and thus may have been over-looked in a cursory examination However chlamydosporesare generally more deeply embedded within the host tissues

Figure 4 Stages in the life history of Paleoblastocladia milleri the sporothallus produces terminal zoosporangiaand intercalary thick-walled resting sporangia that each produce zoospores zoospores from the restingsporangia in turn develop into the gametothallus that produces gametes from gametangia


whilst perithecia are distributed just beneath the epidermis ofthe host

223 Mycoparasites Some fungi in the Rhynie chertobtained carbon by parasitising other fungi Some of thesemycoparasites were illustrated by Kidston amp Lang (1921bplate V) in the form of thick-walled fungal spores (chlamy-dospores) with smaller spores inside They termed the smallerspores intrusive fungi and thus fully appreciated the concept ofmycoparasitism Several parasitic fungi are now known fromthe Rhynie chert and include forms that developed in the sporelumen of the host between specific wall layers of the host andon the surface of the spores (Fig 6andashe) (Hass et al 1994) Stillother spores are packed with hyphae Each of these sites isgenerally occupied by a different type of chytrid suggestingthat some level of host specificity was in existence in the EarlyDevonian In addition in several instances the host responseto invading parasites is analogous to that found today (Table2) For example Boyetchko amp Tewari (1991) described projec-tions termed callosities lignitubers and papillae extendingfrom the inner surface of the chlamydospore wall in certainmycohosts these are formed when the living protoplast of theparasitised chlamydospore continues to synthesise wall mate-rial as the parasite attempts to penetrate the spore wall Inmodern chlamydospores it is possible to see thin canals thatbisect the length of similar papillae these canals were formedby the chytrid as it tunnelled through the new spore wall Thissame host response is present in the Rhynie chert spores (Fig6f g) In observing this biological lsquoarms racersquo in the fossilrecord between the chytrid and the parasitised chlamydosporewhat is fascinating is that the molecular and genetic signallingmechanisms in this interaction were apparently in existence atleast 400 million years ago and are essentially unchangedcompared with those found in certain groups of fungi today Itshould be noted however that infection canals that appearsimilar may also be the result of bacteria and amoeba-likeorganisms (Table 2) Further complicating our understandingof the role of certain organisms in this ecosystem is the factthat some modern mycoparasites from arbuscular mycorrhizalspores are reported as facultative with some saprophyticability and thus are not entirely dependent on the spore for acarbon source (Paulitz amp Menge 1984)

Filamentous ascomycetes have also been described inhealthy and dead spores of the modern arbuscular mycorrhizaScutellospora (Hijri et al 2002) Using both molecular se-quence data and transmission electron microscopy the exist-ence of these fungi was confirmed in the spores however theirfunction remains equivocal Since many fossil spores containother fungi especially the thick-walled spores so common inthe Rhynie chert this modern association may also be ancient

There are numerous examples of hyphae that are in directcontact with other hyphae in the Rhynie chert both in thematrix and in degraded tissues Some of these may be hausto-ria whilst others contain knobs and swellings and couldrepresent mycoparasite appressoria (Table 2) which are spe-cialised hyphal structures that adhere to the host and penetratethe plant epidermis In modern fungi this interaction directlyinvolves some recognition between the parasite and host Itmay include chemotrophic growth of the parasite towardthe host recognition attachment excretion of extracellularenzymes and exploitation of the host (Chet et al 1997)Examples of this interaction are difficult to identify in the fossilrecord because a specific host response typically involvescytoplasmic disruption and reduced hyphal growth in theparasite Nevertheless it is important to document structuressuggestive of appressoria

An additional example of mycoparasitism occurs in asco-mycete perithecia from the Rhynie chert (Fig 6h) Hyphae that

occur extensively in degraded perithecia are of varying diam-eters suggesting that more than one single mycoparasite waspresent Several perithecia contain smaller spores (20 m) thatmay represent yet another mycoparasite

23 MutualistsIt is estimated that many extant land plants maintain more orless intimate relationships with fungi in a variety of differentinteractions involving obligately biotrophic fungi (Bonfante2003) Whilst some associations are highly specialised andconfined to a relatively small group of plants others like thearbuscular mycorrhizae are estimated to occur in approxi-mately 90 of extant plant species including not onlygymnosperms and flowering plants but also bryophytes andpteridophytes (Read et al 2000) Arbuscular mycorrhizae(AM) characterised by a mostly coenocytic mycelium and theproduction of chlamydospores are now included in the mono-phyletic phylum Glomeromycota (Schuszligler et al 2001) Suchfungi in modern ecosystems are known to be involved indefining ecological niches and determining plant communitycomposition (Francis amp Read 1995) as well as playing majorroles in soil fertility and plant nutrition It has also beensuggested that they contribute to weathering processes in thesoil (Boucot amp Gray 2001) As a result of the nutritionalmodifications provided by the symbiosis AM fungi influenceplant growth in multiple ways some of these include protec-tion against some plant diseases (Blee amp Anderson 2000) aswell as having a negative effect on certain herbivores (Vicariet al 2002) and affecting the composition of arthropod com-munities on plants (Gange et al 2002) These fungi may alsohelp promote the coexistence of plant species in a variety ofways (Hart et al 2003)

Kidston amp Lang (1921b) initially suggested a possiblebiotrophic relationship between some of the fungi in theRhynie chert and the macroplants this interaction has nowbeen fully documented (Taylor et al 1995) Whereas arbuscu-lar mycorrhizal symbioses in the fossil record may be deducedbased on the presence of hyphae vesicles and spores withinthe fossil plant tissues the structure that defines the mutualismis an intracellular highly branched hyphal network termed thearbuscule In this interaction the fungus has the ability topenetrate the macroplant cell wall without rupturing theplasmalemma to form the arbuscule It is this structurethrough which nutrient transfer occurs between the host andthe fungus The first arbuscules from the Rhynie chert plantshave been reported only recently (Remy et al 1994b) Glomitesrhyniensis is known from Aglaophyton sporophytes as well asyoung gametophytes of this plant (Lyonophyton rhyniensis)(Table 1 Remy et al 1994b) A continuous dark band in thecortex of Aglaophyton (Fig 6i) contains the arbuscules of themycorrhizal partner (Fig 6j k)

The report of arbuscular mycorrhizae in at least one of theRhynie chert macroplants has important implications withrespect to the evolution of this fungal interaction and thedynamics of the ecosystem during the Early Devonian Thesimilarity of the arbuscules of the fossil Glomites to the extantarbuscular mycorrhizal fungus Glomus is striking and suggeststhat this symbiosis has operated relatively unchanged for atleast 400 million years Research on modern arbuscular myc-orrhizae generally ascribes the function of increasing phospho-rus uptake to the host organism via the extended hyphalnetwork of the fungus (Smith amp Read 1997) We mightspeculate that this Early Devonian ecosystem lacked sufficientquantities of readily available minerals such as phosphorusand thus the capacity of the symbiosis to increase mineraluptake would have been an important selective pressure inexpanding the ecosystem Another hypothesis is that the


absence of well-developed roots in these early plants providedthe selective pressure that favoured mycorrhizal associationsMoreover the loose arrangement of the tissues in these plants

provided the necessary conduit for a highly ramifying myce-lium in the cortical tissues such as that found in certain(Arum-type) arbuscular mycorrhizae (Brundrett 2002)


As a result of the detailed studies by Remy amp Remy (1980ab) and Remy amp Hass (1991a b 1996) we now know that thelife histories of the Rhynie chert plants included a free-livinggametophyte phase and that fungi have been observed withinthe tissues of the gametophyte Lyonophyton Arbuscules occurearly in the development of the gametophyte which is stillattached to the spore coat Hyphae and vesicles are present inimmature gametophytes which lack distinct tissues the firstrecognisable arbuscules occur in young aerial axes As researchwith other Rhynie chert macroplants continues it will beinteresting to see how many of these have entered into mycor-rhizal relationships Hass amp Kerp (2003) indicate that five ofthe macroplants from the Rhynie chert are variously associ-ated with glomalean-type chlamydospores suggesting thewidespread existence and biological significance of endophyticfungi in this Early Devonian ecosystem However the natureof most of these endophytic fungusndashland plant associationscannot be established with certainty since the fungi do notdisplay structural similarities to extant mycorrhizal fungi suchas the arbuscular mycorrhizae (AM) that occur in the axes ofAglaophyton It is possible that some of the other endophyticfungi in Rhynie chert plants may simply have been asymp-tomatic space-endophytes which had neither an adverse nora beneficial effect on their hosts Others may representprecursor states of true endomycorrhizal associations benefi-cial for the host to a certain degree but not yet havingestablished an interaction as intimate as that seen in extantAM fungi

It is now known that arbuscular mycorrhizae may impactplants in a variety of ways including both beneficial andantagonistic interactions Further contributing to a lack ofcertainty as to exactly how AM fungi benefit a plant is the factthat different species of a mycorrhizal symbiont can havedifferential effects on the growth of plants (van der Heijdenet al 1998) Francis amp Read (1995) demonstrated that somehosts respond mutualistically to AM whilst other uninfectedspecies lose fitness Although it has been hypothesised that ashift in fungal interactions from parasitism to mutualism wasan initial impetus in the colonisation of land by charophyceanalgae (Church 1921 Pirozynski amp Malloch 1975 Atsatt 1988)it is doubtful that the fossil record will ever substantiallycontribute to deciphering this transition Recent estimatesbased on molecular sequence data extend the age of the

zygomycete (glomeromycete) fungi back to at least 600 Ma(Berbee amp Taylor 2001) or even earlier ndash to 1000 Ma ago(Heckman et al 2001) Whilst this does not demonstrate theage of the arbuscular mycorrhizal symbiosis it does under-score the fact that the Rhynie chert symbiosis is perhaps notthe earliest occurrence of this interaction Current ideas re-garding the earliest terrestrial plants suggest that they weresmall green upright axes that bore terminal sporangia andthat probably possessed a prostrate anchoring and absorbingstructure These plants termed rhyniophytoids (Edwards ampEdwards 1986) or cooksonioids (Taylor 1988) are believed torepresent a bryophytic grade of evolution Although some ofthese specimens are known to contain a minute central strandof cells that probably functioned in conduction other tissuesystems (eg cortex) that might provide clues as to whetherthese plants were mycorrhizal are not preserved Because theseorganisms are preserved as compressions and impressions noinformation is available as to whether they contained fungiand thus entered into a fungal symbiosis

Another critical component in the life history of the AMfungus is thick-walled resting spores (chlamydospores) thatgerminate and grow in the absence of host roots but arenot able to produce an extensive mycelial network Recentresearch with modern AM fungi suggests that when no host isavailable the hyphae produced by the resting spores undergogrowth arrest and resource reallocation (Giovannetti2002) Some of the Rhynie chert chlamydospores with shorthyphae that appear in the matrix may represent germinatingspores which suggests the existence of this life historystrategy They may also represent indirect evidence of someanimal predator that grazed on mycelia in the rhizosphereleaving behind the thick-walled spores and short hyphalattachments Structures interpreted as oogonia with attachedhyphae have been reported from the Rhynie chert (Fig 6l)and compared with the oomycete Apodachlya but theseprobably represent small chlamydospores or vesicles ratherthan oomycete reproductive structures (Table 1 Harvey et al1969)

In modern ecosystems mycoparasites can have an adverseeffect on the development of the arbuscular mycorrhizal com-munity which thus affects the next generation of plants Sincechlamydospores infected by mycoparasites do not germinate toform the interradical hyphae which invade the underground

Figure 5 (a) Several asci containing ascospores from Rhynie chert ascomycete Slide P3431 scale bar=15 m (b) Tuft of conidiophores eruptingfrom epidermis of Asteroxylon stem Slide P3445 scale bar=25 m (c) Section of Asteroxylon stem showing perithecia (arrows) interspersed withchlamydospores (c) Slide P3412 scale bar=500 m (d) Longitudinal section of Palaeonitella cranii showing several nodes of branches and twohypertrophied (H) cells Slide P1385 scale bar=300 m (e) Chytrid zoosporangium (z) extending through cell wall (c) with well developedrhizomycelium (r) inside cell lumen Slide P1359 scale bar=25 m (from Taylor et al 1992a) (f) Pediastrum-like algal cell infected bychytrid zoosporangium Slide P1483 scale bar=10 m (g) Cluster of several algal cells each containing a chytrid zoosporangium Slide P1399 scalebar=10 m (from Taylor et al 1992c) (h) Several algal cells attached to cortical cell wall (cw) of macroplant Note circular openings (arrows) inzoosporangia for discharge Slide P2496 scale bar=15 m (from Taylor et al 1992c) (i) Two thick-walled fungal spores each with the outer surfacecovered by epibiotic chytrid thalli Slide P1935 scale bar=50 m (j) Macroplant spore with three chytrid thalli protruding from the trilete sutureSlide P1347 scale bar=15 m (k) Chytrid zoosporangium on macroplant spore with several discharge tubes Slide P1687 scale bar=15 microm (l) Baseof Nothia axis bearing numerous rhizoids Note thickening (arrow) that may represent either the causal agent or symptom of fungal interaction SlideP2868 scale bar=100 m (m) Section of macroplant showing tissue disruption in the cortex Slide P3445 scale bar=500 m

Table 2 Host responses in Rhynie chert organisms

Host Host response Occurrence Causal agent Symptom

Glomites rhyniensis papillae chlamdyospores chytrids bacteria amoebae synthesis of new spore wall materialAll macroplants hyperplasia cortical tissue unknown increased cell productionPalaeonitella cranii hypertrophy internodal cells chytrids abnormal growthAll macroplants necrotic areas axes cortex unknown opaque areasAglaophyton major cell wall thickenings cells with arbuscules Zygomycete new wall materialVarious macroplants appressoria certain hyphae other hyphae hyphal enlargement hyphae adpressed


parts of plants and ultimately form arbuscules in viable hosttissue cells the level of community fitness is reduced There-fore a high population of mycoparasites attacking chlamy-dospores can impact the number of mycorrhizal infections andmay result in host plants that are less competitive in nutrientuptake Although we donrsquot know all of the complexities of themycorrhizal relationships in the Rhynie chert it is possible

that mycoparasitism may have similarly impacted themacroplant community

24 LichensIt is estimated that approximately 20 of extant fungal speciesenter into obligate symbiotic associations with cyanobacteriagreen algae or both to form lichens Lichens have continued


to provide challenges relative to their evolutionary history Thelichen life strategy in which a fungus (mycobiont) and alga(phyco- or photobiont) live in a close symbiotic association isnow suggested to have arisen many times and has involveda number of algal groups over the course of geologic time(Gargas et al 1995 Lutzoni et al 2001) Lichens today areprimarily associated with ascomycetes and the occurrence of arelatively advanced ascomycete in the Rhynie chert suggeststhat it is possible that this symbiosis was present but has notyet been identified

Although lichens have been reported from Precambrianrocks (eg Hallbauer amp van Warmelo 1974 Retallack 1994)these have been discounted for a number of reasons (Cloud1976 Waggoner 1995) Perhaps the most convincing fossilexample of a Palaeozoic lichen symbiosis occurs in the Rhyniechert (Fig 7andashf Table 1 Taylor et al 1997) Winfrenatiareticulata consists of a thin mycelial mat at least 10 cm longconstructed of interwoven aseptate hyphae Along the uppersurface are numerous shallow relatively uniform depressions(Fig 7a b) Within many of these depressions are sphericalcoccoid unicells that are morphologically similar to certaincyanobacteria (Fig 7c d) also present are clusters of the samecells within mucilaginous sheaths that are interpreted as stagesin the life history of the cyanobacterium (Fig 7e) Hyphae ofthe fungus extend into the depressions and become intertwinedwith the bacterial cyanobionts (Fig 7c) The range of featuresobserved in Winfrenatia including size of the thallus andnumber of depressions on the surface has allowed the authorsto speculate on the life history strategy which included theproduction of new cells of the cyanobiont to maintain thesymbiosis and support the fungus and at the same time anincrease in the size of the fungal mycelial mat (Fig 8 Tayloret al 1997) It has been suggested that Winfrenatia is not a truecyanolichen but rather represents an unstable association inwhich a fungus parasitised a cyanobacterial colony (Poinaret al 2000) Whilst deciphering the physiological stabilitywithin a symbiotic association in the fossil record may never befully realised the definition of a lichen as a controlled parasit-ism rather than a strict mutualism is perhaps more accurate asit underscores the varying degrees of lichenisation that appearin modern ecosystems (Ahmadjian amp Jacobs 1981 Hyvarinenet al 2002) In that context Winfrenatia may quite accuratelybe used to define an Early Devonian lichen (Honegger 2001)Interestingly extant cyanobacterial lichens have been found toshow higher nitrogen levels and increased photosyntheticactivity relative to green algal lichens (Palmqvist et al 1998)Perhaps the Winfrenatia symbiosis functioned in a similarmanner in the Rhynie chert ecosystem

Although the fungal partner in most modern lichens is anascomycete the mycobiont in Winfrenatia has not been con-clusively identified The presence of aseptate hyphae andcertain thick-walled sculptured spores (Fig 7f) associated withmycelial mats has been used to suggest that the fungal affinitiesmay lie closer to the zygomycetesglomeromycetes (Tayloret al 1997) This is especially interesting since there is one

modern example of a lichen with a glomeromycetous myco-biont and cyanobiont Geosiphon pyriforme this symbioticassociation is found on the upper surface of wet soils that arepoor in nutrients especially phosphorus (Schuszligler amp Kluge2001) In this unique symbiosis the cyanobacterium Nostocbecomes encapsulated in a pear-shaped bladder that is formedby the fungus The physiological exchange between the fungusand cyanobacterium takes place in this structure It is interest-ing that Geosiphon is now included in the monophyletic groupGlomeromycota which also includes the arbuscular mycor-rhizae formerly placed with the Zygomycota (Schuszligler et al2001) This modern symbiosis demonstrates the structural andphysiological aspects of such interactions the associationobserved in Winfrenatia demonstrates that a glomeromycotancyanobacterial partnership may have existed in the EarlyDevonian

25 Fungalanimal interactionsSince the first report of organisms in the Rhynie chertnumerous examples of extraordinarily well-preserved fossilanimals have been identified among the plants These includemembers of several arthropod groups including trigonotarbidarachnids mites crustaceans myriapods and collembolansamongst others (see review in Shear amp Selden 2001) Indirectevidence of animal diversity in the chert includes variouscoprolites that have been distinguished on the basis of sizeshape and composition (Habgood et al 2004) Some of theseare made up of a heterogeneous complex of plant-derived ma-terials (eg cuticle spore fragments conducting elements andbits of parenchyma cells) Others suggest that the animals weremore specific feeders for example some coprolites contain avery high percentage of spore fragments In still others themajor constituent of the coprolites are fragments of fungalhyphae (Fig 7g) suggesting that the animal was a fungivore

As further work continues on aspects of the Rhynie chertfungal community it will be interesting to see whether some ofthese microbes entered into fungalndashanimal symbiotic associa-tions similar to those present in some modern ecosystems Thelarge diversity of animal remains in the Rhynie chert holdsexceptional promise for the discovery of other fungalndashanimalinteractions in addition to feeding Within the zygomycetes areseveral groups of fungi which have been reported as obligateendophytes and can occupy the hindguts of various arthropodtaxa (Lichtwardt 1986) The wide-ranging distribution of thesemodern symbioses has been used as evidence to support thehypothesis that this is an ancient interaction To date the onlyfossil example is a putative trichomycete reported by White ampTaylor (1989) from the Triassic of Antarctica that consists ofwhat is interpreted as an animal cuticle lined with elongatetrichospores The large number of major fungal taxa includingzygomycetes and the diversity of well-preserved animals in theRhynie chert offers the intriguing possibility that these rocksmay also contain evidence of obligate symbiotic relationshipssimilar to those with the Trichomycetes For example based

Figure 6 (a) Thick-walled fungal spore containing well-developed internal mycoparasite Slide P2762 scale bar=25 m (b) Mycoparasitic chytrid(c) that has penetrated thick-walled fungal spore with rhizomycelium (r) extending into cell lumen Slide P1693 scale bar=10 m (from Hass et al1994) (c) Chytrid (c) that has developed between spore wall layers as a mycoparasite Slide P2761 scale bar=15 m (d) Several thin-walled vesiclesin the matrix with both endobiotic and epibiotic mycoparasites Slide P1698 scale bar=50 m (e) Vesicle with epibiotic chytrid and well-developedrhizomycelium in spore lumen Slide P1698 scale bar=25 m (from Hass et al 1994) (f) Thick-walled chlamydospores note papillae extending intospore lumen Slide P1671 scale bar=25 m (from Hass et al 1994) (g) Chlamydospore with several papillae note the concentric layering andinfection canal in the papilla that bisects the spore lumen (arrow) Slide P1698 scale bar=20 m (h) Hyphae of mycoparasite within an ascocarplike that in Figure 2f Slide P3415 scale bar=25 m (i) Transverse section of Aglaophyton major axis showing the continuous dark band (arrow) incortex that contains the arbuscules of the mycorrhizal partner Slide P1828 scale bar=1 mm (from Taylor et al 1995) (j) Detail of Glomitesarbuscule showing the highly branched organisation Slide P1703 scale bar=10 m (k) Two cortical cells from band in Figure 6i each containingan arbuscule Arrow indicates slight thickening where arbuscule trunk has penetrated host cell wall Slide P1827 scale bar=50 m (from Taylor etal 1995) (l) Several thin-walled vesicle-like structures in chert matrix Slide P1540 scale bar=150 m


on molecular analyses it has recently been noted that Tricho-mycetes is a highly polyphyletic group (Cafaro 2003) and thatat least one genus is not even a fungus but rather a protozoan(Benny amp OrsquoDonnell 2000) Thus the possibility exists that notonly are there various fungal groups that formed associationswith diverse animals early in the development of a terrestrialecosystem but also that such associations involved othernon-fungal groups as well

All of the modern fungal groups that have been identified inthe Rhynie chert to date have members that are saprophytes ofvarious arthropods and animals For example modern insectshave coevolved with fungi in a variety of patterns that benefitthe insect in the acquisition of nutrients and metabolitesprotection and habitat conditioning Fungi in turn may ben-efit from propagule dispersal and protection from grazing(Murrin 1996) Although there are reports of entomophtho-ralean and saprophytic fungi associated with various fossilarthropods (Poinar amp Thomas 1982 Stubblefield et al 1985b)none of these interactions have been reported to date from theRhynie chert

26 BacteriaBacteria have a major influence on the terrestrial environmentin modern ecosystems because of the large number of chemicalreactions they catalyse in the soil Bacterial communitiescontrol the availability and cycling of soil nutrientsincluding carbon and nitrogen and are also capable offorming beneficial and deleterious associations with plantsSome nitrogen-fixing symbioses involve specific rhizobialinteractions between the microbes and plant roots and contrib-ute significantly to the nutrition of the host for examplethey accumulate nitrogen and phosphorus in quantities similarto those in terrestrial plants (Buckley amp Schmidt 2002)Although various bacteria are early colonisers in moistenvironments their importance as agents of wood decay isrelatively minor Nevertheless bacteria play some role in thedegradation of cellulose In their classic paper Kidston ampLang (1921b) described bacteria both in the matrix andassociated with some plant material further studies dealingwith microbial life in the Rhynie chert have identifiedadditional colonies and clusters of bacterial cells (Fig 7h) that

Figure 7 (a) Section of cyanolichen thallus showing depressions (lighter areas at arrows) that containcyanobacteria surrounded by more opaque zone that represents the fungal partner Slide P1604 scalebar=750 m (b) Section of lichen at right angles to thallus in Figure 7a showing depression and opaque walls(arrows) formed of fungal hyphae Slide P1323 scale bar=150 m (from Taylor et al 1997) (c) Detail of wallformed by fungal hyphae and depression containing cyanobacterial cells Slide P1388 scale bar=50 m (d) Detailof unicells from depression in thallus showing association with fungal hyphae Slide P1386 scale bar=50 m(from Taylor et al 1997) (e) Two daughter cells of lichen cyanobiont showing remnants of several sheaths SlideP1380 scale bar=5 m (f) Thick-walled reticulate spore found associated with hyphae in cyanolichen SlideP1374 scale bar=25 m (g) Coprolite composed of fungal hyphae Slide P1919 scale bar=50 m (h) Detail ofseveral filaments believed to be cyanobacteria Slide P1680b scale bar=20 m


appear similar to cyanobacteria (Table 1 Croft amp George1958)

There are many ways that plants affect the structure ofmicrobial communities including the production of root exu-dates that can influence community composition and locationIn addition plants can impact soil microbial diversity bycompeting for resources It is highly unlikely that we will evercompletely know how the composition of the Rhynie chertecosystem influenced the microbial community in the sub-strate Nonetheless a more complete understanding of thebiodiversity of this complex community makes it possible topresent scenarios of interactions that in turn can be comparedwith those in modern ecosystems (Fig 1A) For examplecould the swellings on the rhizoids of fossil macroplants suchas Nothia aphylla represent some form of bacteriumrootinteraction (eg rhizobia) that was perhaps involved in nitro-gen fixation rather than representing a symptom of a parasiticchytrid The fact that Early Devonian fungi can penetrate hostcell walls to form mycorrhizal arbuscules and not rupture theplasma membrane indicates that an endosymbiosis with otherorganisms including bacteria was certainly possible

3 Discussion

31 Evolution of fungal groupsTraditionally the Kingdom Fungi includes the Chytridiomy-cota Zygomycota Ascomycota and Basidiomycota recentlythe Glomeromycota has been introduced for arbuscularmycorrhizae Together these form a group of walled het-erotrophic organisms that are thought to have evolved fromzooflagellated protozoans (Cavalier-Smith 1998) An alterna-tive classification includes the chytrids zygomycetes andallomycetes (Blastocladiales and Colemomycetales) in the sub-kingdom Eomycota and ascomycetes and basidiomycetes inthe Neomycota (Cavalier-Smith 2001) All fungi are absorptiveheterotrophs with multinucleate hyphae and chitinous sporesthat lack plastids In recent years numerous authors haveused 18S rDNA sequence data to estimate divergence timesof various major fungal groups (eg Berbee amp Taylor 19932001) Among the fungi the chytrids are the only group thatpossesses flagellated cells which supports the basal positionof this group This position is in turn further supported byultrastructural biochemical and additional morphologicalfeatures The diversity in chytrid morphology and life historybiology of the forms described to date in the Rhynie chert also

support this hypothesis Based on rDNA sequences Jameset al (2000) suggest that the Chytridiomycota is not a mono-phyletic group and that the Blastocladiales interestingly clus-ter with the zygomycetes This finding would support theancient divergence of these two groups which is also suggestedby the structural and life history features found in the fossilPaleoblastocladia

In modern ecosystems zygomycetes glomeromycetes asco-mycetes and basidiomycetes are typically associated with landplants Based on molecular sequence data Berbee amp Taylor(2001) suggest that the Glomeromycota which today areinvolved in arbuscular mycorrhizal symbioses and character-ised by a coenocytic thallus and the production of asexualspores first occurred more than 600 Ma ago This is severalhundred million years earlier than previous molecular clockestimates based on rDNA sequences (Simon et al 1993 Simon1996) Fossil evidence that may contribute to elucidation of theage of the first endomycorrhizae has recently been reportedfrom Upper Ordovician rocks (Redecker et al 2000 2002)Specimens of Palaeoglomus grayi include terminally-borneglobose spores up to 95 m in diameter associated withaseptate hyphae These specimens occur isolated in the matrixand are not associated with macroplants however if they areexamples of glomeromycotan fungi they help to provide acalibration point that underscores the antiquity of the arbus-cular mycorrhizal symbiosis

Ascomycetes comprise the largest group in the Fungi andare characterised by septate hyphae and a dikaryotic phase intheir life cycle One group the filamentous ascomycetes hasenclosed ascocarps of several different morphologies includingflask-shaped perithecia This type of ascocarp is associatedwith Asteroxylon (Figs 2j k 5c) and provides the earliest fossilevidence of an ascomycetous sporocarp that contains sterileparaphyses and thin-walled asci that probably forcibly dis-charged the ascospores The apparently modern appearance ofthis fungal component of the Rhynie chert offers compellingevidence for the antiquity of this group which can be tracedback to the Upper Silurian What is perhaps most interestingabout the discovery of ascomycetes in the Rhynie chert con-cerns the age of the group which had previously been assumedto be younger based on the supposed association of leaf-inhabiting ascomycetes with early angiosperms in the Cre-taceous (Berbee amp Taylor 2001) What is important aboutthis fossil is that it provides an important set of features thatcan be used in polarising characters and also to calibratemolecular clocks Although there are conflicting points of viewregarding the evolution of groups within the AscomycotaBerbee amp Taylor (2001) indicated that the pyrenomycetes(filamentous ascomycetes) including the experimental organ-ism Neurospora appear at the base of the Euascomycete clade

The Basidiomycota is the second largest group in theKingdom Fungi and possesses meiospores (basidiospores)formed on club-shaped cells Molecular data suggest that theAscomycota and Basidiomycota diverged from each otherapproximately 100 Ma earlier than the time of the Rhyniechert ecosystem (Berbee amp Taylor 2001) Of the four majorgroups of fungi recognised today only the basidiomyceteshave yet to be conclusively demonstrated from the Rhyniechert ecosystem This is interesting because evidence of basidi-omycetes in the form of solution troughs along the innerwalls of tracheids have been reported from Upper Devonianprogymnosperms (Stubblefield et al 1985a)

We remain cautious as to the significance of the absence ofthe basidiomycetes since the first fossil ascomycete has onlyrecently been reported and is of a type that may be consideredto be highly evolved Basidiomycetes today include parasites

Figure 8 Detail of a single depression in the thallus of the lichenWinfrenatia reticulata showing walls made up of fungal hyphae that inturn surround the cells of the cyanobiont Some of the hyphae form anet-like structure in the base of the depression cells of the cyanobiontare undergoing division near the surface


of plants as well as the principal lignin and cellulose decom-posers in modern ecosystems If current ideas regarding thedivergence of Ascomycota and Basidiomycota based on mo-lecular phylogenies are accurate then one might expect thatthese two groups co-occurred at the time of the Rhynie chertecosystem The absence of this group in the Rhynie chert todate may be related to the apparent lack of lignin in themacroplants andor the fact that other groups of fungi (egchytrids) may have been the primary decomposers in thisecosystem Perhaps a more plausible explanation for theabsence of the group is that they simply have not yet beenidentified

All of the other fungal associations that have been describedfrom the Rhynie chert appear similar to those found todayThese include epibiotic and endobiotic forms of chytrids aswell as those that have colonised highly specialised habitatsbetween certain wall layers in chlamydospores and others thatappear to be restricted to certain hosts (Figs 5dndashk 6andashg) Inmodern microbial interactions there are specific signallingmechanisms that are present in both the environment andpotential hosts These complex genetic molecular and bio-chemical elicitors have been identified in some living fungi andonly now are beginning to be fully understood Whilst thislevel of molecular and genetic inquiry will be impossible tocarry out in the Rhynie chert organisms the host responsesthat have been demonstrated (Table 2) help to underscore thatthe relationships between fungi and other organisms are veryancient and biochemically highly complex

32 Fungal distribution in plantsAnother important avenue in the study of fossil fungi concernstheir distribution in and on the plant During Rhynie cherttime none of the macroplants possessed true leaves and thusthere was minimum surface area for fungi to colonise in anaerial habitat There were however various types of epidermalappendages including enations in Asteroxylon that may ormay not have been photosynthetic and irregular surfaces onother aerial axes (eg Nothia) The presence of enations andthe development of a more complex vascular system certainlyrepresented adaptations that allowed greater photosyntheticactivity and presumably larger size As the macroplantsbecame more complex and provided increased variability inmicrohabitats for colonisation fungi such as the perithecialascomycetes expanded into new niches Not only do theperithecia occur along the stems but also extend some distanceout along the bases of enations (Fig 2j k) Ascomycetes of thistype occur as leaf and stem parasites and are importantpathogens of many extant plants We are uncertain as towhether the Rhynie chert ascomycete was a parasite pathogenor saprophyte but there is some minor evidence in the form ofnecrotic areas on the stems suggesting a host response to aparasite If this ascomycete was in fact a parasite it isproblematic as to why other examples of this group have notbeen found on the phylloplane of slightly younger groups ofvascular plants that dominated early ecosystems Perhaps theabsence of this group of potential leaf-borne fungi is the resultof plant defences rather than the failure of the fungi to exploitnew niches in the ecosystem On the other hand it is possiblethat these fungi had not yet evolved either the physicaladhesion properties (glycoproteins) to attach to a leaf orlaminar structure or the chemical communication system thatwould have been necessary in the hostfungus relationship It isalso possible that these fungi simply have not been recognisedin the fossil record

At least one other group of Rhynie chert fungi (glomero-mycetes) that entered into a mutualistic symbiosis with mac-roplants in the ecosystem appears to have exploited a very high

percentage of host cells Whilst most modern arbuscularmycorrhizae develop arbuscules that are confined to the un-derground and absorptive parts of the plant the arbuscules inAglaophyton are developed in both the aerial and subaerialparts of the plant In addition it appears that the hyphae thatform the arbuscules extend all the way to the tips of all axesThus in this symbiosis the fungus may be viewed as encapsu-lating a major portion of the living tissues of the sporophytea relationship that does not appear in modern herbaceousplants The high correspondence of fungal physiologicalexchange sites (arbuscules) and living cells in the host addssupport to the hypothesis that fungi were a necessary compo-nent in the transition to a terrestrial habitat (Pirozynski ampMalloch 1975) However recent ribosomal sequence datasuggest that the symbiosis between green plants and fungi mayhave evolved prior to the colonisation of land (Tehler et al2003)

The basic types of structural and morphological features ofarbuscular mycorrhizae have been termed the Arum andParis-types since it was from these genera of plants thatmycorrhizae were originally described (Gallaud 1905) In theArum-type there is an extensive intercellular hyphal networkand arbuscules are formed as terminal structures in theParis-type extensive intercellular hyphae are absent but ahyphal network is present in the form of coils of hyphae witharbuscules formed as intercalary structures (Smith amp Smith1997) The Arum-type is less frequently found and occurs insome ferns and angiosperms (Read et al 2000) Although thereare exceptions it appears that many gymnosperms bryo-phytes and so-called lsquolowerrsquo vascular cryptogams includingsome ferns have AM structures of the Paris-type (Brundrett2002) Based on the structural features that are used todistinguish these two types of arbuscular mycorrhizae thosethat have been identified to date in the fossil record (inAglaophyton) are distinctly of the Arum-type (Fig 6j k)Whilst both the physiological necessity of the plant andanatomical structure of its tissues may play important roles inthe type of mycorrhizae found in plants these distinctions mayalso be related to the degree of fungal infection in the plantbody as well as physiological efficiency of the arbuscules Itshould be noted however that the same fungal species canproduce both the Arum- and Paris-types depending on theanatomy of the root which indicates that control resides withthe plants (Jacquelinet-Jeanmougin amp Gianinazzi-Pearson1983) Whilst arbuscules have been reported in the gameto-phytes of Aglaophyton (Lyonophyton) there remain questionsas to the degree and extent of the fungal infection in this phaseIn the living plant Lycopodium there appears to be somevariation in structural organisation in fungal endophytes ofgametophytes and sporophytes (Duckett amp Ligrone 1992)with no arbuscules produced in the gametophyte arbusculesare also lacking in the moss Hypopterygium (Jakucs et al2003) Since Lycopodium possesses the same type of basic lifehistory as that of AglaophytonLyonophyton it will be interest-ing to see whether this variation is also present in the Rhyniechert macroplants

33 Future research directionsWhat types of interactions and associations will be revealed inthe microbial world of the Rhynie chert in the years aheadCertainly one series of important questions concerns whetherother macroplants in the ecosystem were mycorrhizal Whilstchlamydospores of the glomalean type have been found intissues and associated with all of the other macroplants thisin itself is not conclusive proof that these plants containedmutualistic endosymbionts Of equal importance will bewhether the free living gametophytes were all mycorrhizal and


if so the extent of interaction as compared with that foundin the sporophyte Aglaophyton where a large number ofarbuscules were formed

Bacteria were another important biological component ofthe microbial world during Rhynie chert times The resolvingpower available with transmitted light microscopy and per-haps the actual preservation of bacterial cells may not besufficient to provide further details about these microbesHowever their occurrence in cells tissue systems and variousother organs in the chert may provide indirect evidence ofcertain types of interactions For example in a recent studybacteria are reported in the cytoplasm of chlamydospores ofmodern AM fungi which suggests that a more complex set ofinteractions may exist between the fungus and the host as wellas the endobacterium and the fungus although the complexi-ties of this endosymbiosis are not yet fully understood(Bonfante et al 2002 Bonfante 2003) Other symbionts in theform of nitrogen-fixing microbes are diverse and present inmodern arthropod guts (Nardi et al 2002) and may haveoccupied similar habitats in some of the Rhynie chert arthro-pods Additionally there is some evidence that suggests thatbacteria may provide improved plant nutrition in soils low inphosphorus (Bonfante 2003) Based on this it will be interest-ing to see if bacteria are directly associated with any of theRhynie plants Today bacteria exist primarily as free-livingforms in the soil but a few form symbiotic relationships withplants Nodules containing bacteria have been reported from alarge number of extant plants Some of the macroplants in theRhynie chert have swellings on the rhizoids that are ofuncertain origin and may have hosted endobacteria

Cyanobacteria form a variety of symbiotic interactions withfungi and other organisms including lichens (Rai et al 2002)such as that documented from the Rhynie chert Other sym-bioses today include cycads selected flowering plants aquaticferns sponges and certain colonial animals diatoms andvarious bryophytes Since several cyanobacteria are knownfrom the Rhynie chert (Kidston amp Lang 1921b Croft ampGeorge 1958) and the macroplants appear to have their closestaffinities to the bryophytic grade of organisation it will bechallenging to see if cyanobacterial symbionts are also associ-ated with any of the terrestrial components of the ecosystem

Another potentially rewarding avenue of research within theRhynie chert is the documentation of interactions betweenmicrobes and animals We have already commented on thevalue of examining certain animals that have been describedfrom the chert for fungalarthropod symbiosis similar to thosefound in Trichomycetes today A wide variety of ascomycetesare also associated with modern arthropods (Spatafora 2002)and the demonstration of ascomycetes in the cherts suggestsanother interaction that may also exist in the Rhynie chert

Future Rhynie chert microbial research might involvepotential pathogens of the macroplants An interesting ques-tion is whether all of the necrotic areas and pustules on thesurfaces of axes and enations were caused by fungi or otherorganisms For example the modern green alga Cephaleuros isan epiphyllous form that has typically been misidentified as aglomalean fungus (Reynolds amp Dunn 1984 Chapman amp Henk1985) The filamentous alga grows under the cuticle on theupper surface of leaves killing the tissue beneath Tufts ofreproductive structures (sporangiophores) bear zoosporangiaand appear similar to fungal conidiophores however thepresence of quadriflagellate zoospores and the life historybiology positively identify this pathogen as an alga Greenalgae have already been identified in the Rhynie chert whichsuggests that further study of epidermal lesions may yet revealother groups preying on the macroplants

Further expansion of inventory of the diversity of microbespresent is necessary in order to more accurately define thisspecialised ecosystem and potentially offer hypotheses aboutpatterns of nutrient cycling Careful description of both teleo-morphic and anamorphic fungal states as well as the struc-tures that make up the fungi will be especially important inproviding calibration points for divergence times that can bemeasured against phylogenies based on molecular data analy-sis As the studies that are reported in this volume clearlydemonstrate the Rhynie chert ecosystem is highly complexboth physically and biologically Despite the extensive researchthat has been accomplished to date these complexities are onlypartially understood Admittedly documenting some of thepotential interactions noted in this paper will be difficult andperhaps impossible Nevertheless the minuscule and some-times partially opaque window into the Early Devonian that isrepresented by the Rhynie chert provides a level of biologicalinquiry that was probably not envisioned when Kidston ampLang published their extraordinary studies Discoveries fromthe Rhynie chert have been exciting and challenging both interms of documenting the existence of the organisms presentand interpreting their biological importance yet we believethat the discoveries that remain to be made will be even moreexciting and will have a still greater impact on ideas about theevolution of terrestrial ecosystems

4 Acknowledgements

A portion of this study was supported by the National ScienceFoundation under grant OPP-000360

5 References

Ahmadjian V amp Jacobs J B 1981 Relationship between fungus andalga in the lichen Cladonia cristatella Tuck Nature 289 169ndash72

Alexopoulos C J Mims C W amp Blackwell M 1996 IntroductoryMycology 4th edn New York John Wiley amp Sons Inc

Atsatt P R 1988 Are vascular plants lsquoinside-outrsquo lichens Ecology 6917ndash23

Benny G L amp OrsquoDonnell K O 2000 Amoebidium parasiticum is aprotozoan not a Trichomycete Mycologia 92 1133ndash7

Berbee M L amp Taylor J W 1993 Dating the evolutionary radia-tions of the true fungi Canadian Journal of Botany 71 1114ndash27

Berbee M L amp Taylor J W 2001 Fungal molecular evolution genetrees and geologic time In McLaughlin D J McLaughlin E Gamp Lemke P A (eds) The Mycota VIIA Systematics and Evolu-tion 229ndash45 Berlin Springer-Verlag

Berner R A amp Kothavala Z 2001 GEOCARB III A revised modelof atmospheric CO2 over Phanerozoic time American Journal ofScience 301 182ndash204

Blee K A amp Anderson A J 2000 Defense responses in plants toarbuscular mycorrhizal fungi In Podila G K amp Douds Jr DD (eds) Current Advances in Mycorrhizae Research 27ndash44 StPaul Minnesota APS Press

Bonfante P 2003 Plants mycorrhizal fungi and endobacteria adialog among cells and genomes Biological Bulletin 204 215ndash20

Bonfante P Bianciotto B Ruiz-Lozano J M Minerdi D Lu-mini E amp Perotto S 2002 Arbuscular mycorrhizal fungi andtheir endobacteria In Seckbach J (ed) Symbiosis Mechanismsand Model Systems 323ndash38 Dordrecht Netherlands KluwerAcademic Publishers

Boucot A J amp Gray J 2001 A critique of Phanerozoic climaticmodels involving changes in the CO2 content of the atmosphereEarth-Science Reviews 56 1ndash159

Boyetchko S M amp Tewari J P 1991 Parasitism of spores of thevesicular-arbuscular mycorrhizal fungus Glomus dimorphicumPhytoprotection 72 27ndash32

Brundrett M C 2002 Coevolution of roots and mycorrhizas of landplants New Phytologist 154 275ndash304

Buckley D H amp Schmidt T M 2002 Exploring the biodiversity ofsoil ndash a microbial rain forest In Staley J T amp Reysenbach A(eds) Biodiversity of Microbial Life Foundation of Earthrsquos Bio-sphere 183ndash208 New York Wiley-Liss


Cafaro M J 2003 Systematics of the Trichomycetes as an ecologicalgroup with an emphasis on the phylogeny of Eccrinales andAsellariales based on rDNA sequences Ph D dissertation Uni-versity of Kansas Lawrence KS USA

Cavalier-Smith T 1998 A revised 6-kingdom system of life BiologicalReview 73 203ndash66

Cavalier-Smith T 2001 What are fungi In McLaughlin D JMcLaughlin E G amp Lemke P E (eds) The Mycota VIIASystematics and Evolution 3ndash37 Berlin Springer-Verlag

Chapman R L amp Henk M C 1985 Observation on the habitmorphology and ultrastructure of Cephaleuros parasiticus (Chlo-rophyta) and a comparison with Cephaleuros virescens Journal ofPhycology 21 513ndash22

Chet I Inbar J amp Hadar Y 1997 Fungal antagonists and myco-parasites In Wicklow D T amp Soderstrom B E (eds) TheMycota IV Environmental and Microbial Relationships 165ndash84Berlin Springer-Verlag

Church A H 1921 The lichen as transmigrant Journal of Botany 597ndash13 40ndash6

Cloud P E 1976 Beginnings of biospheric evolution and theirbiochemical consequences Paleobiology 2 351ndash87

Croft W N amp George E A 1958 Blue-green algae from the MiddleDevonian of Rhynie Aberdeenshire Bulletin of the British Mu-seum (Natural History) Geology 3 341ndash53

Duckett J G amp Ligrone R 1992 A light and electron microscopestudy of the fungal endophytes in the sporophyte and gameto-phyte of Lycopodium cernuum with observations on thegametophyte-sporophyte junction Canadian Journal of Botany70 58ndash72

Edwards D amp Edwards D S 1986 A reconsideration of Rhynio-phytina Banks In Spicer R A amp Thomas B A (eds) Systematicand Taxonomic Approaches in Palaeobotany 199ndash220 SystematicsAssociation Special Volume 31 Oxford Clarendon Press

Edwards D S amp Lyon A G 1983 Algae from the Rhynie chertBotanical Journal of the Linnean Society 86 37ndash55

Francis R amp Read D J 1995 Mutualism and antagonism in themycorrhizal symbiosis with special reference to impacts on plantcommunity structure Canadian Journal of Botany 73 (suppl 1)S1301ndash9

Gallaud I 1905 Eutudes sur les mycorrhizes endotrophes RevueGenerale de Botanique 17 5ndash48 66ndash83 123ndash36 223ndash39 313ndash25425ndash33 479ndash500

Gange A C Stagg P G amp Ward L K 2002 Arbuscular mycor-rhizal fungi affect phytophagous insect specialism Ecology Let-ters 5 11ndash15

Gargas A DePriest P T Grube M amp Tehler A 1995 Multipleorigins of lichen symbioses in fungi suggested by SSU rDNAphylogeny Science 268 1492ndash5

Giovanetti M 2002 Survival strategies in arbuscular mycorrhizalsymbionts In Seckbach J (ed) Symbiosis Mechanisms andModel Systems 295ndash307 Boston Kluwer Academic Press Pub-lishers

Habgood K Hass H amp Kerp H 2004 Evidence for an earlyterrestrial food web coprolites from the Early Devonian Rhyniechert Transactions of the Royal Society of Edinburgh EarthSciences 94 (for 2003) 371ndash389

Hallbauer D K amp van Warmelo K T 1974 Fossilized plants inthucholite from Precambrian rocks of Witwatersrand SouthAfrica Precambrian Research 1 199ndash212

Hart M M Reader R J amp Klironomos J N 2003 Plantcoexistence mediated by arbuscular mycorrhizae TRENDS inEcology and Evolution 18 418ndash23

Harvey R Lyon A G amp Lewis P N 1969 A fossil fungus fromRhynie Chert Transactions of the British Mycological Society 53155ndash6

Hass H Taylor T N amp Remy W 1994 Fungi from the LowerDevonian Rhynie chert mycoparasitism American Journal ofBotany 81 28ndash37

Hass H amp Kerp H 2003 Rhynie chert plants and adaptations totheir substrates Programme of the Rhynie Hot-Spring SystemGeology Biota and Mineralisation Abstract 9 wwwabdnacukrhynie

Hawksworth R L 1991 The fungal dimension of biodiversitymagnitude significance and conservation Mycological Research95 641ndash55

Heckman D S Geiser D M Eidell B R Stauffer R L KardosN L amp Hedges S B 2001 Molecular evidence for the earlycolonization of land by fungi and plants Science 293 1129ndash33

Held A A Emerson R Fuller M S amp Gleason F H 1969Blastocladia and Aqualinderella fermentative water molds withhigh carbon dioxide optima Science 165 706ndash9

Hijri M Redecker D Mac-Donald-Comber Petetot J A Voigt KWostemeyer J amp Sanders I R 2002 Identification and isolationof two ascomycete fungi from spores of the arbuscular mycor-rhizal fungus Scutellospora castanea Applied and EnvironmentalMicrobiology 68 4567ndash73

Honegger R 2001 The symbiotic phenotype of lichen-forming asco-mycetes In Hock B (ed) The Mycota IX Fungal Associations165ndash88 Berlin Springer-Verlag

Hyvarinen M Hardling R amp Tuomi J 2002 Cyanobacterial lichensymbiosis the fungal partner as an optimal harvester Oikos 98498ndash504

Illman W I 1984 Zoosporic fungal bodies in the spores of theDevonian fossil vascular plant Horneophyton Mycologia 76545ndash7

Jacquelinet-Jeanmougin S amp Gianinazzi-Pearson V 1983 Endomy-corrhizas in the Gentianaceae I The fungus associated withGentiana lutea L New Phytologist 95 663ndash6

Jakucs E Naar Z Szedlay G amp S Orban 2003 Glomalean andseptate endophytic fungi in Hypopterigium mosses (Bryopsida)Cryptogamie Mycologie 24 27ndash37

James T Y Porter D Leander C A Vilgalys R amp Longcore JE 2000 Molecular phylogenetics of the Chytridiomycota sup-ports the utility of ultrastructural data in chytrid systematicsCanadian Journal of Botany 78 336ndash50

Karling J S 1928 Studies in the Chytridiales III A parasitic chytridcausing cell hypertrophy in Chara American Journal of Botany 15485ndash95

Kidston R amp Lang W H 1917 On Old Red Sandstone plantsshowing structure from the Rhynie chert Bed AberdeenshirePart I Rhynia gwynne-vaughani Kidston amp Lang Transactions ofthe Royal Society of Edinburgh 51 761ndash84

Kidston R amp Lang W H 1920a On Old Red Sandstone plantsshowing structure from the Rhynie chert Bed AberdeenshirePart II Additional notes on Rhynia gwynne-vaughani Kidstonand Lang with descriptions of Rhynia major n sp and Hornealignieri n g n sp Transactions of the Royal Society of Edinburgh52 603ndash27

Kidston R amp Lang W H 1920b On Old Red Sandstone plantsshowing structure from the Rhynie chert Bed AberdeenshirePart III Asteroxylon Mackiei Kidston and Lang Transactions ofthe Royal Society of Edinburgh 52 643ndash80

Kidston R amp Lang W H 1921a On Old Red Sandstone plantsshowing structure from the Rhynie chert Bed AberdeenshirePart IV Restorations of the vascular cryptogams and discussionof their bearing on the general morphology of the Pteridophytaand the origin of the organisation of land-plants Transactions ofthe Royal Society of Edinburgh 52 831ndash54

Kidston R amp Lang W H 1921b On Old Red Sandstone plantsshowing structure from the Rhynie chert Bed AberdeenshirePart V The Thallophyta occurring in the peat-bed the successionof the plants through a vertical section of the bed and theconditions of accumulation and preservation of the depositTransactions of the Royal Society of Edinburgh 52 855ndash902

Lichtwardt RW 1986 The Trichomycetes fungal associates of arthro-pods New York Springer-Verlag

Lutzoni F Pagel M amp Reeb V 2001 Major fungal lineages arederived from lichen symbiotic ancestors Nature 411 937ndash40

Mackie W 1914 The rock series of Craigbed and Ord Hill RhynieAberdeenshire Transactions of the Edinburgh Geological Society10 205ndash36

McLaughlin D J amp McLaughlin E G 2001 Volume preface InMcLaughlin D J McLaughlin E G amp Lemke P E (eds) TheMycota VIIA Systematics and Evolution xindashxiv Berlin Springer-Verlag

Murrin F 1996 Fungi and insects In Howard D H amp Miller J D(eds) The Mycota VI Human and Animal Relationships 365ndash88Berlin Springer-Verlag

Nardi J B Mackie R I amp Dawson J O 2002 Could microbialsymbionts of arthropod guts contribute to nitrogen fixation interrestrial ecosystems Journal of Insect Physiology 48 751ndash63

Palmqvist K Campbell D Ekblad A amp Johansson H 1998Photosynthetic capacity in relation to nitrogen content and itspartitioning in lichens with different photobionts Plant Cell andEnvironment 21 361ndash72

Paulitz T C amp Menge J A 1984 Is Spizellomyces punctatum aparasite or saprophyte of vesicular-arbuscular mycorrhizal fungiMycologia 76 99ndash107

Pirozynski K A amp Malloch D W 1975 The origin of land plants amatter of mycotrophism BioSystems 6 153ndash64

Poinar G O Jr Peterson E B amp Platt J L 2000 Fossil Parmeliain New World amber Lichenologist 32 263ndash9


Poinar G O Jr amp Thomas G M 1982 An entomophthoraleanfungus from Dominican amber Mycologia 74 332ndash4

Rai A N Bergman B amp Rasmussen U 2002 Cyanobacteria insymbiosis Dordrecht Netherlands Kluwer Academic Publishers

Read D J Ducket J G Francis R Ligrone R amp Russell A 2000Symbiotic fungal associations in lsquolowerrsquo land plants PhilosophicalTransactions of the Royal Society of London 355B 815ndash31

Redecker D Kodner R amp Graham L E 2000 Glomalean fungifrom the Ordovician Science 289 1920ndash1

Redecker D Kodner R amp Graham L E 2002 Palaeoglomus grayifrom the Ordovician Mycotaxon 84 33ndash7

Redman R G Dunigan D D amp Rodrigues R J 2001 Fungalsymbiosis from mutualism to parasitism who controls the out-come host or invader New Phytologist 151 705ndash16

Remy W amp Hass H 1991a Kidstonophyton discoides nov gen novspec ein Gametophyt aus dem Chert von Rhynie (UnterdevonSchottland) Argumenta Palaeobotanica 8 29ndash45

Remy W amp Hass H 1991b Langiophyton mackiei nov gen novspec ein Gametophyt mit Archegoniophoren aus dem Chert vonRhynie (Unterdevon Schottland) Argumenta Palaeobotanica 869ndash117

Remy W amp Hass H 1996 New information on gametophytes andsporophytes of Aglaophyton major and inferences about possibleenvironmental adaptations Review of Palaeobotany and Palynol-ogy 90 175ndash93

Remy W amp Remy R 1980a Devonian gametophytes with anatomi-cally preserved gametangia Science 208 295ndash6

Remy W amp Remy R 1980b Lyonophyton rhyniensis n gen et novspec ein Gametophyt aus dem Chert von Rhynie (UnterdevonSchottland) Argumenta Palaeobotanica 6 37ndash72

Remy W Taylor T N amp Hass H 1994a Early Devonian fungi ablastocladalean fungus with sexual reproduction American Jour-nal of Botany 81 690ndash702

Remy W Taylor T N Hass H amp Kerp H 1994b Four hundred-million-year-old vesicular arbuscular mycorrhizae Proceedings ofthe National Academy of Sciences USA 91 11841ndash3

Retallack G J 1994 Were the Ediacaran fossils lichens Paleobiology20 523ndash44

Reynolds D R amp Dunn P H 1984 A fungus-like alga Mycologia76 719ndash21

Schulz B Rommert A Dammann U Aust H amp Strack D 1999The endophyte-host interaction a balanced antagonism Myco-logical Research 103 1275ndash83

Schuszligler A amp Kluge M 2001 Geosiphon pyriforme an endocyto-symbiosis between fungus and cyanobacteria and its meaning asa model system for arbuscular mycorrhizal research In Hock B(ed) The Mycota IX Fungal Associations 151ndash61 BerlinSpringer-Verlag

Schuszligler A Schwarzott D amp Walker C 2001 A new fungalphylum the Glomeromycota phylogeny and evolution Myco-logical Research 105 1413ndash21

Shear W A amp Selden P A 2001 Rustling in the undergrowthanimals in early terrestrial ecosystems In Gensel P G ampEdwards D (eds) Plants Invade the Land Evolutionary andEnvironmental Perspectives 29ndash51 New York Columbia Univer-sity Press

Sherwood-Pike M A amp Gray J 1985 Silurian fungal remainsprobable records of the class Ascomycetes Lethaia 18 1ndash20

Simon L 1996 Phylogeny of the Glomales deciphering the past tounderstand the present New Phytologist 133 95ndash101

Simon L Bousquet J Levesque R C amp Lalonde M 1993 Originand diversification of endomycorrhizal fungi and coincidence withvascular plants Nature 363 67ndash9

Smith S E amp Read D J 1997 Mycorrhizal symbiosis 2nd ednLondon Academic Press

Smith F A amp Smith S E 1997 Tansley Review No 96 Structuraldiversity in (vesicular)-arbuscular mycorrhizal symbioses NewPhytologist 137 373ndash88

Spatafora J W 2002 Evolution of Ascomycota-arthropod symbio-ses In Seckbach J (ed) Symbiosis Mechanisms and ModelSystems 591ndash609 Dordrecht Netherlands Kluwer AcademicPublishers

Stubblefield S P Taylor T N amp Beck C B 1985a Studies ofPaleozoic fungi V Wood-decaying fungi in Callixylon newberryifrom the Upper Devonian American Journal of Botany 721765ndash74

Stubblefield S P Taylor T N Miller C E amp Cole G T 1985bGeotrichites glaesarius a conidial fungus from Tertiary Domini-can amber Mycologia 77 11ndash16

Takenaka S 1995 Dynamics of fungal pathogens in host planttissues Canadian Journal of Botany 73 (suppl 1) S1275ndash83

Tappan H 1980 The Paleobiology of Plant Protists San FranciscoW H Freeman and Company

Taylor T N 1988 The origin of land plants some answers morequestions Taxon 37 805ndash33

Taylor T N 1995 The fossil history of ascomycetes In HawksworthD L (ed) Ascomycete Systematics Problems and Perspectives inthe Nineties 167ndash174 New York Plenum Press

Taylor T N Hass H amp Kerp H 1997 A cyanolichen from theLower Devonian Rhynie chert American Journal of Botany 84992ndash1004

Taylor T N Hass H amp Kerp H 1999 The oldest fossil asco-mycetes Nature 399 648

Taylor T N Hass H amp Remy W 1992a Devonian fungi interac-tions with the green alga Palaeonitella Mycologia 84 901ndash10

Taylor T N Remy W amp Hass H 1992b Parasitism in a 400-million-year-old green alga Nature 357 493ndash4

Taylor T N Remy W amp Hass H 1992c Fungi from the LowerDevonian Rhynie chert chytridiomycetes American Journal ofBotany 79 1233ndash41

Taylor T N Remy W amp Hass H 1994 Allomyces in the DevonianNature 367 601

Taylor T N Remy W Hass H amp Kerp H 1995 Fossil arbuscularmycorrhizae from the Early Devonian Mycologia 87 560ndash73

Taylor T N Hass H Kerp H Krings M amp Hanlin R T (Inpress) Perithecial ascomycetes from the 400ndashmillion-year-oldRhynie chert an example of ancestral polymorphism Mycologia

Tehler A Little D P amp Farris J S 2003 The full-length phyloge-netic tree from 1551 ribosomal sequences of chitinous fungiFungi Mycological Research 107 901ndash16

Trewin N H amp Rice C M 1992 Stratigraphy and sedimentology ofthe Devonian Rhynie chert locality Scottish Journal of Geology28 37ndash47

van der Heijden M G A Boller T Wiemken A amp Sanders I R1998 Different arbuscular mycorrhizal fungal species are poten-tial determinants of plant community structure Ecology 792082ndash91

Vicari M Hatcher P E amp Ayres P G 2002 Combined effect offoliar and mycorrhizal endophytes on an insect herbivore Ecol-ogy 83 2452ndash64

Waggoner B J 1995 Ediacarean lichens a critique Paleobiology 21393ndash7

White J F Jr amp Taylor T N 1989 A trichomycete-like fossil fromthe Triassic of Antarctica Mycologia 81 643ndash6

THOMAS N TAYLOR SHARON D KLAVINS and EDITH L TAYLOR Department ofEcology and Evolutionary Biology Natural History Museum and Biodiversity Research CenterUniversity of Kansas Lawrence KS 66045ndash7534 USA

HANS KERP and HAGEN HASS Forschungstelle fur Palaobotanik am Geologisch-Palaontologischen Institut und Museum Hindenburgplatz 57 Westfalische Wilhelms-Universitat48143 Munster Germany

MICHAEL KRINGS Bayerische Staatssammlung fur Palaontologie und Geologie und GeoBio-CenterLMU Richard-Wagner-Straszlige 10 80333 Munchen Germany

MS received 17 September 2003 Accepted for publication 10 June 2004


Tab

le1

Rhy

nie

cher

tm

icro

bial

taxa

and

asso

ciat

edor

gani

sms

Ass

ocia

ted

mac

ropl

ant

spor

ophy

tes

Ass

ocia

ted

mac

ropl

ant

gam

etop

hyte

sA

lgal

bac

teri

alas

soci

ates

Fun

gal

asso

ciat

esSu

gges

ted

mod

ern

equi

vale

ntta

xaR

efer

ence

Chy

trid

iom

ycot

aK

risp

irom

yces

disc

oide

sP

alae

onit

ella

cran

iiP

hlyc

toch

ytri

um

Cat

enoc

hytr

idiu

mT

aylo

ret

al

1992

a

Lyo

nom

yces

pyri

form

isP

alae

onit

ella

cran

iiR

hizo

phyd

ium

Tay

lor

etal

19

92a

Mill

erom

yces

rhyn

iens

isP

alae

onit

ella

cran

iiE

ndoc

hytr

ium

E

ntop

hlyc

tis

Sor

odis

cus

Wor

onin

aT

aylo

ret

al

1992

a

Pal

eobl

asto

clad

iam

iller

iA

glao

phyt

onm

ajor

Allo

myc

es

Bla

stoc

ladi

opsi

sT

aylo

ret

al

1994

R

emy

etal

19

94a

Unn

amed

holo

carp

ican

deu

carp

icfo

rms

Hor

neop

hyto

nlig

nier

iA

glao

phyt

onm

ajor

Lyo

noph

yton

rhyn

iens

is

Agl

aoph

yton

maj

orP

alae

onit

ella

cran

iiP

edia

stru

m-l

ike

alga

Fun

gal

spor

esan

dve

sicl

esE

ntop

hlyc

tis

Hyp

hoch

ytri

um

Now

akow

skie

lla

Olp

idio

psis

O

lpid

ium

S

pize

llom

yces

T

ripa

rtic

alca

r

Illm

an19

84

Tay

lor

etal

19

92b

Has

set

al

1994

Zyg

omyc

ota

Glo

mit

esrh

ynie

nsis

Agl

aoph

yton

maj

orG

lom

usT

aylo

ret

al

1995

Pal

aeom

yces

aggl

omer

ata

Rhy

nia

gwyn

ne-v

augh

anii

Kid

ston

ampL

ang

1921

bP

alae

omyc

esas

tero

xylii

Ast

erox

ylon

mac

kiei

Kid

ston

ampL

ang

1921

bP

alae

omyc

esgo

rdon

iiA

ster

oxyl

onm

acki

ei

Hor

neop

hyto

nlig

nier

iR

hyni

asp

Kid

ston

ampL

ang

1921

b

Pal

aeom

yces

gord

onii

var

maj

orR

hyni

agw

ynne

-vau

ghan

iiK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

horn

eae

Hor

neop

hyto

nlig

nier

iK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

sim

pson

iiR

hyni

agw

ynne

-vau

ghan

iiK

idst

onamp

Lan

g19

21b

Pal

aeom

yces

vest

ita

Ast

erox

ylon

mac

kiei

Kid

ston

ampL

ang

1921

bW

infr

enat

iare

ticu

lata

myc

obio

ntL

iche

nC

yano

bion

tT

aylo

ret

al

1997

Asc

omyc

ota

Unn

amed

peri

thec

ial

asco

myc

ete

Ast

erox

ylon

mac

kiei

Pyr

enom

ycet

esT

aylo

ret

al

1999

lsquoOom

ycot

arsquoU

nnam

edm

ycel

iaP

roto

taxi

tes

tait

iA

poda

chly

apy

rife

raH

arve

yet

al

1969

Cya

noba

cter

iaA

rcha

eoth

rix

cont

exta

Osc

illat

oria

Kid

ston

ampL

ang

1921

bA

rcha

eoth

rix

osci

llato

rifo

rmis

Osc

illat

oria

Kid

ston

ampL

ang

1921

bK

idst

onie

llafr

itsc

hii

Stig

onem

atac

eae

Cro

ftamp

Geo

rge

1958

Lan

giel

lasc

ourf

eldi

iSt

igon

emat

acea

eC

roft

ampG

eorg

e19

58R

hyni

ella

verm

ifor

mis

Scyt

onem

atac

eae

Cro

ftamp

Geo

rge

1958

Rhy

nioc

occu

sun

ifor

mis

Chr

ooco

ccac

eae

Edw

ards

ampL

yon

1983

T

appa

n19

80W

infr

enat

iare

ticu

lata

cyan

obio

ntL

iche

nZ

ygom

ycet

em

ycob

iont

Glo

eoca

psa

Chr

ooco

ccus

C

hroo

ccci

diop

sis

Tay

lor

etal

19

97











































































3 Discussion























4 Acknowledgements


5 References




























































































































































































3 Discussion























4 Acknowledgements


5 References

































































































































4 Acknowledgements


5 References



















































































































Fungi from the Rhynie chert: a view from the dark side · Fungi from the Rhynie chert: a view from...

Documents

Transcript of Fungi from the Rhynie chert: a view from the dark side · Fungi from the Rhynie chert: a view from...