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An unusual specimen of the enigmatic fungal reproductive unit
Windipila spinifera from the Lower Devonian Rhynie
cherts of Scotland
Michael Krings1,2,3
1 SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Straße 10, 80333 Munich, Germany
2 Department of Earth and Environmental Sciences, Palaeontology & Geobiology, Ludwig-Maximilians-Universität München, Richard-
Wagner-Straße 10, 80333 Munich, Germany
3 Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Institute, University of Kansas,
Lawrence, KS 66045-7534, USA
https://zoobank.org/B4312F0C-F88C-4F61-999B-D5E3FD553A99
Corresponding author: Michael Krings (krings@snsb.de, krings@ku.edu)
Academic editor: Alexander Nützel♦
Received
9 May 2022♦
Accepted
26 July 2022♦
Published
8 August 2022
Abstract
Windipila spinifera from the Rhynie cherts is a spheroidal microfossil enveloped in a hyphal mantle from which extend
prominent spines and otherwise shaped projections. It is believed to be a reproductive unit of a fungus in the Glomero-
mycota or zygomycetes, but features to determine the systematic anities have not hitherto been documented. This
study describes a new specimen of W. spinifera that contains a single spherical structure from which a hypha arises
that extends outside and terminates in what appears to be a sporangium. The specimen is reminiscent of germinated
zygospores of the germ-sporangial type, and thus may suggest anities of W. spinifera to the zygomycetes. However, the
interior sphere and its outgrowth could also be a part of another organism that had invaded W. spinifera.
Keywords
fossil fungi, Glomeromycota, intrusive organisms, zygomycetes, zygospore germination
1. Introduction
The Lower Devonian Rhynie cherts (including the Rhynie
and Windyeld cherts) of Scotland give detailed insights
into fungal diversity in a terrestrial ecosystem c. 410 Ma
ago (Taylor et al. 2015; Krings et al. 2017a; Strullu-Derrien
et al. 2019). One important proxy indicator of this diversity
is the morphological variety of fungal propagules and mi-
croscopic reproductive units, both of which are present in
virtually every thin section of the cherts. However, dealing
with these fossils is dicult because they mostly occur
detached from the systems on or in which they were pro-
duced, and thus do not provide an inclusive comparison
with present-day equivalents to determine their systemat-
ic anities (Krings and Harper 2020).
Several types of fungal reproductive units have been
described from the Rhynie cherts that all possess an
ancillary covering in the form of a hyphal investment
or mantle. Mantle morphology varies (considerably)
among the different types, and thus renders them easy to
distinguish from one another (Krings and Taylor 2013, 2014,
2015a, 2015b; Krings et al. 2014, 2016, 2017b; Krings and
Harper 2017, 2018, 2020). One of these fossils is Windipila
spinifera (Fig. 1A), a walled spheroid less than 150 µm in
diameter that is enveloped in circumferential hyphae from
which extend prominent, thin-walled spines and otherwise
shaped projections (Krings and Harper 2017, 2018).
Most mantled fungal reproductive units from
the Rhynie cherts, including Windipila spinifera, are
believed to belong to either the Glomeromycota or the
zygomycete fungi based on similar features in modern
Zitteliana 96, 2022, 145–152|DOI 10.3897/zitteliana.96.86327
Copyright Michael Krings. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source
are credited.
Michael Krings: Unusual Windipila spinifera from the Rhynie cherts146
lineages known to produce spores or sporangia with
hyphal mantles (e.g., Krings et al. 2016, 2017a; Krings
and Harper 2020). The occurrence of several specimens
on what appear to be simple, tubular subtending hyphae
has been used to suggest that W. spinifera developed
asexually by blastic ination and thickening of a hyphal
tip, rather than sexually and following gametangial
fusion, and for this reason might be a glomoid
chlamydospore (Krings and Harper 2017). However,
structural features to more precisely delimit the nature
and systematic anities of this fossil have not been
documented to date.
This study describes a new specimen of Windipila
spinifera from the Windyeld chert that contains a single
spherical structure from which an unbranched hypha is
given off that evidently passes through the wall and man-
tle and terminates in what appears to be a sporangium
with a distal discharge papilla. While this specimen does
also not clarify the anities of W. spinifera, it resembles a
germinated zygospore or azygospore with a tubular spor-
angiophore and distal germ sporangium, and thus is sug-
gestive of anities to the zygomycetes.
2. Geological setting
The Rhynie chert Lagerstätte is located in the northern
part of the Rhynie outlier of Lower Old Red Sandstone
in Aberdeenshire, Scotland, in an extensive sequence
of sedimentary and volcanic rocks. The cherts occur in
the Rhynie Block of the Dryden Flags Formation locat-
ed northwest of the village of Rhynie. The Lagerstätte
is made up of fossiliferous beds containing lacustrine
shales and chert that have been interpreted as a series
of ephemeral pools within a geothermal wetland, with
alkali-chloride hot springs that were part of a complex
hydrothermal system in a region affected by volcanic
activity (Rice et al. 2002; Rice and Ashcroft 2004; Trewin
and Fayers 2016; Channing 2017). The Windyfield chert
site occurs ~700 m to the northeast of the original
Rhynie chert site (Trewin and Rice 1992; Fayers 2003;
Garwood et al. 2020). It was deposited in an area of
hot-spring feeder activity based on the hydrothermally
altered nature of its associated fluvio-lacustrine shales
and sandstones; paleoenvironments ranged from ter-
restrial, vegetated aprons of laminated and brecciated
sinter to low-temperature pools and marginal aquat-
ic settings (Rice et al. 2002; Fayers 2003; Fayers and
Trewin 2004). The Rhynie and Windyfield cherts are re-
garded as broadly coeval, i.e., 411.5±1.3 to 407.6±2.6
million years old according to Mark et al. (2011, 2013)
and Parry et al. (2011), Pragian-earliest Emsian ac-
cording to Wellman (2006, 2017) and Wellman et al.
(2006). For details on the geology and development of
the Rhynie chert Lagerstätte, as well as on the paleon-
tology, refer to Trewin and Kerp (2017), Garwood et al.
(2020), and the Rhynie chert volume edited by Edwards
et al. (2018).
3. Material and methods
The specimen described below was identied in a thin
section prepared by cementing a wafer of the Windyeld
chert to a microscope slide, and then grinding the rock
slice until it was suciently thin (i.e. c. 60–80 µm thick) to
transmit light (for details on thin section preparation, re-
fer to Hass and Rowe 1999). The slide is deposited in the
SNSB-Bayerische Staatssammlung für Paläontologie und
Geologie (SNSB-BSPG) in Munich, Germany, under acces-
sion number SNSB-BSPG 2016 VII 117. The specimen was
studied using normal transmitted light microscopy; digital
images were captured with a Leica DFC-480 camera and
processed in Adobe Photoshop CS5. For comparison, an-
other specimen of Windipila spinifera from the holdings of
the SNSB-BSPG (accession number SNSB-BSPG 2016 VII
82) has also been illustrated.
4. Results
The specimen (Fig. 1B1) is located in the chert matrix,
within silicied litter comprised predominantly of frag-
mented and mostly heavily degraded land plant axes, dis-
persed land plant spores, unidentiable debris, and fungal
hyphae. The reproductive unit is spherical, roughly 145 μm
in diameter (including mantle but excluding projections),
and composed of a central cavity bounded by a non-hy-
phal wall up to 2 µm thick. No evidence has been found
of pores or otherwise shaped orices in the wall. The re-
productive unit is enveloped in a hyphal mantle composed
of 1–3 layers of tightly interlaced hyphae extending along
the outer surface of the non-hyphal wall. Prominent pro-
jections, irregularly distributed over the entire surface, are
given off from the circumferential hyphae in an outward
direction. However, there are fewer projections in this
specimen as compared to the specimens described previ-
ously (Fig. 1A1,2; Krings and Harper 2017, 2018). The struc-
ture in vivo was probably positioned terminally on a lat-
eral branch or outgrowth of a tubular hypha (see below).
However, the attachment site is obscured by the mantle
hyphae and most of the hyphal nexus is not recognizable
due to the plane of the section through the specimen.
The reproductive unit contains a single, more or less
spherical structure (henceforth called interior sphere) that
is c. 55 µm in diameter, lacks structured contents, and is
delineated by a smooth wall up to 0.75 µm thick. Its posi-
tion within the cavity is highly eccentric in such a way that
it comes into contact with, and in vivo perhaps adhered
to, the inner surface of the non-hyphal wall of the repro-
ductive unit. The interior sphere is somewhat attened
where it is in physical contact with this wall. No evidence
of a subtending hypha or any other kind of parental struc-
ture has been found. However, the cavity of the repro-
ductive unit contains shrivelled fragments of thin-walled
hyphae or laments (Fig. 1B3). Arising from roughly the
center of the attened portion of the interior sphere is a
narrow hypha 1–2 µm wide (arrows in Fig. 1C), which ev-
idently passes through the non-hyphal wall of the repro-
Zitteliana 96, 2022, 145–152 147
ductive unit and proceeds on the outside into the mantle.
Unfortunately, the exact path of the hypha through the wall
and mantle is not traceable. The hypha reappears in the
periphery of the mantle where it expands to up to 6.5 µm
wide (arrow in Fig. 1D) and becomes tubular (stalk-like),
and from there runs outwards c. 40 µm into the ambience
Figure 1. Windipila spinifera from the Lower Devonian Rhynie cherts (Windyeld chert). A1, 2. Well preserved specimen in two different
focal planes (A1: median optical section, A2: section off center), with prominent spines and otherwise shaped projections extending
from mantle (focal plane A1 previously published by Krings and Harper 2018: g. 1A). Slide SNSB-BSPG 2016 VII 82. B–F. New spec-
imen. Slide SNSB-BSPG 2016 VII 117. B1. Overview (median optical section), showing interior sphere in highly eccentric position and
stalk-like hypha (arrow) terminating in exterior sphere. B2. Second exterior structure in different plane; note attached fragment of
putative parental hypha (arrow). B3. Shrivelled hyphae or laments in cavity of reproductive unit. C. Hypha arising from interior sphere
(arrows). D. Stalk-like hypha becoming wider in periphery of mantle (arrow), and extending in outward direction. E. Papilla-like, distal pu-
tative discharge apparatus of exterior sphere. F. Hypha (rh) with three attached W. spinifera reproductive units (labeled 1–3), of which
the one in the lower right of the image (labeled 1) is magnied in Fig. 1B1; specimen 2 occurs on a lateral branch (lb) and 3 at the tip of
the hypha. Scale bars: 10 µm (B3, C, E); 20 µm (B2, D); 50 µm (A1, A2, B1); 100 µm (F).
Michael Krings: Unusual Windipila spinifera from the Rhynie cherts148
(arrow in Fig.1B1). The hypha is unbranched and termi-
nates in another spherical structure (henceforth called
exterior sphere), which is 46 µm in diameter, bounded by a
smooth wall, and does also not have structured contents.
The exterior sphere is characterized by a single, distal,
thin-walled papilla-like projection 8.5 µm high (Fig. 1E). A
second exterior structure, c. 38 µm in diameter and some-
what asymmetrical or distorted, occurs in close proximity
to the exterior sphere in a different plane of the specimen
(Fig. 1B2). This structure, which is partially embedded in
the mantle of the reproductive unit, is subtended by a
short fragment of what appears to be a hypha (arrow in
Fig. 1B2). As to whether this hypha also originates from
the interior sphere cannot be determined.
The hypha (rh in Fig. 1F) that gives rise to the specimen
described above (labeled 1 in Fig. 1F) bears two further
Windipila spinifera reproductive units (labeled 2 and 3 in
Fig. 1F), one of which occurs on a lateral branch (lb in
Fig.1F), while the other (partially degraded) appears to be
positioned at the tip of the hypha itself. Because these lat-
ter specimens do not exhibit any new or unusual features,
they will not be discussed here any further.
5. Discussion
Eight morphologically different types of mantled fungal
reproductive units have so far been described from the
Rhynie cherts, of which Windipila spinifera with its prom-
inent mantle spines certainly is one of the more peculiar
ones (Krings and Harper 2017, 2018). A similar, albeit
less impressive mantle occurs in the little-known W. pum-
ila (Krings and Harper 2018). A third type attributed to
Windipila, W. wimmervoecksii, is characterized by mantle
hyphae with vesicle-like inations from which extend nee-
dle-like processes that connect the inner mantle tier with
an outer tier of irregularly inated and interwoven hyphae
(Krings and Harper 2020).
Windipila has been suggested to have anities to ei-
ther the Glomeromycota or the zygomycete fungi (Krings
and Harper 2020). One of the key features distinguishing
these two groups of fungi is the sexual stage of the life
cycle, which occurs in zygomycetes as a result of zygos-
porogenesis following gametangial fusion, but has not
been observed in Glomeromycota (Benjamin 1979; Benny
et al. 2001, 2012). Mature zygosporangia or zygospores
with attached gametangia and/or suspensors are there-
fore the most important component of the zygomycete
life cycle that can be used to positively identify a fossil
member in this group of fungi (Krings et al. 2012, 2013).
However, none of the Windipila species can presently be
positively identied as a zygomycete because there is no
evidence of gametangia and/or suspensors. Rather, sev-
eral specimens of W. spinifera (Krings and Harper 2017:
g. 2) and W. wimmervoecksii (Krings and Harper 2020:
gs 2d, 3a) appear to have developed on simple, tubular
subtending hyphae. Moreover, hyphal anastomoses and
H-branching, which are common in several lineages of
glomeromycotan fungi (Walker et al. 2018) but believed
to be lacking or rare in zygomycetes (Gregory 1984; Glass
and Fleissner 2006; Ivarsson et al. 2015), have been doc-
umented in W. wimmervoecksii (Krings and Harper 2020:
gs 4a, b, 5).
The most interesting structural element of the only
known specimen of Windipila pumila is a walled spheri-
cal structure that occurs in the cavity of this fossil (Krings
and Harper 2018: g. 2). Similar spheres have not hitherto
been recorded in W. spinifera or W. wimmervoecksii, but
they have been described in other Rhynie chert mantled
fungal reproductive units, including Scepasmatocarpion
fenestrulatum (Krings and Taylor 2015a: gs 1e, 2c) and
Zwergimyces vestitus (Krings et al. 2016: pl. III, 2–8). The
interior spheres have been used to speculate that these
reproductive units could be sporangia or sporangiola, per-
haps comparable to the zygosporangia of zygomycetes or
the sporangial or sporangiolar layer(s) of certain glomero-
mycotan spore walls (see Walker et al. 2021: g. 1), and
the interior spheres either the zygospore or the sporangio-
spore proper (e.g., Krings and Harper 2018).
The fossil presented in this study provides the rst ev-
idence of the occurrence of interior spheres also in Wind-
ipila spinifera. Moreover, it exhibits several structural fea-
tures pertaining to the interior sphere that have not been
documented in any other Rhynie chert mantled reproduc-
tive unit. Said interior sphere gives off a hypha that exits
the reproductive unit and terminates in another spherical
structure, which is characterized by a papilla-like protru-
sion that most likely functioned as a discharge apparatus.
There is a certain level of morphological correspondence
between the fossil and certain zygomycetes of the order
Mucorales in which zygospore germination entails the for-
mation of a germ sporangium (e.g., Brefeld 1872; De Bary
1884; Blakeslee 1906; Gauger 1961: gs 1–3; Hocking
1967). During the sexual stage of the life cycle, these
fungi produce zygosporangia (zspo in Fig. 2) containing
single zygospores (zsp in Fig. 2) following gametangial
fusion, and sometimes azygosporangia containing azygo-
spores, which are similar to zygospores but form parthe-
nogenetically without gametangial fusion (e.g., Benjamin
and Mehrotra 1963; O’Donnell et al. 1977). The zygospo-
rangium wall eventually ruptures and the zygospore ger-
minates. If germination is of the germ-sporangial type
(sensu Guo and Michailides 1998), then the zygospore
produces a tube-like structure termed a sporangiophore
or promycelium (sph in Fig. 2), on the tip of which a germ
sporangium develops (spo in Fig. 2). After maturation
of the spores (called germ sporangiospores), the germ
sporangium ruptures and liberates the spores, which, if
they fall on a suitable substrate, germinate and develop
into a new mycelium (e.g., Cerdá-Olmedo 2001: g. 1). It
is conceivable that the W. spinifera specimen described
above represents a zygosporangium or azygosporangium
containing a zygospore or azygospore (i.e. the interior
sphere), which has germinated and produced a sporan-
giophore (i.e. the stalk-like hypha) with a terminal germ
sporangium (i.e. the exterior sphere). The second exterior
Zitteliana 96, 2022, 145–152 149
structure, which occurs partially embedded in the hyphal
mantle of the reproductive unit, could be another germ
sporangium. Germinated zygospores with two sporangio-
phores, each bearing a terminal sporangium, have also
been reported in certain present-day zygomycetes (e.g.,
Michailides and Spotts 1988).
One might counter this comparison by pointing out
that no evidence of gametangia and suspensors has
been found in any of the Windipila spinifera specimens.
It is possible, however, that these structures were small,
inconspicuous, and entirely embedded in the mantle.
For example, the zygosporangia of certain present-day
Mortierella (Mortierellaceae, Mucorales) species are sur-
rounded by extensive hyphal coverings arising from the
suspensors or from hyphae at the base of the suspensors
(Brefeld 1881: pl. V, gs 12, 14, 15; Kuhlman 1972; Ansell
and Young 1983) that render the gametangia and sus-
pensors very dicult to recognize. It can also be argued
that the interior sphere in W. spinifera is too small to be a
zygospore or azygospore because zygosporogenesis in-
volves the development of a complex, multi-layered wall
(i.e. the combined sporangium and spore wall) in which
newly deposited wall layers follow exactly the shape of
the previously deposited layers (e.g., Brefeld 1872: pl. II,
g. 20; Hawker and Gooday 1968; Hawker and Backett
1971; O’Donnell et al. 1978). Rather, the interior sphere
is somehow reminiscent of the single oil globules that
are visible in the zygospores of, for instance, certain
representatives of the mucoralean genera Radiomyces
(Radiomycetaceae; e.g., Embree 1959: gs 12, 13; Benny
and Benjamin 1991: gs 8, 16, 18, 29h, i) and Dichoto-
mocladium (Lichtheimiaceae; e.g., Benny and Benjamin
1993: g. 4b). However, it seems unlikely that oil glob-
ules would become preserved in a recognizable form. It
can also not be ruled out that the spore proper in W. spin-
ifera has shrunken during germination, and again during
the silicication process. One must furthermore take
into account the possibility that entirely fossil lineages
of zygomycete fungi, as well as fossil representatives of
present-day lineages, have existed that were character-
ized by traits unknown in any present-day representative.
For example, the germ sporangium in present-day Mu-
corales ruptures at maturity to release the spores, while
the fossil spores likely were liberated through a distal
discharge papilla.
An alternative hypothesis views the interior sphere in
Windipila spinifera as a part or life cycle stage of some
other fungus or fungus-like organism that had invaded
and colonized the reproductive unit, and reproduced by
producing a sporangium (or sporangia?) outside of the
host. Two lines of evidence seem to support this hypoth-
esis. First, co-occurring with the interior sphere in the cav-
ity of the W. spinifera specimen are fragments of hyphae
or laments, which indicate that, at some point, anoth-
er fungus has been present in this structure, unless the
mantle hyphae had invaded the cavity from the circum-
ference (see below). Second, several different types of
small spherules occurring singly or in groups, and proba-
bly representing the reproductive units of intrusive fungi,
have been reported in the cavity of Zwergimyces vesti-
tus (Krings et al. 2016), and thus indicate that mantled
fungal reproductive units in the Rhynie paleoecosystem
have been invaded by other microorganisms and used
as a habitat. On the other hand, there is no evidence of
a physical connection between the interior sphere in W.
spinifera and any system on which it could have devel-
oped. This argues against the hypothesis that the sphere
belongs to an intrusive organism. It is also possible that
the W. spinifera specimen had already fullled its func-
tion, namely to produce a spore that subsequently germi-
nated, and, consequently, was in the process of natural
decay at the time of fossilization. If this is the case, then
the hyphae inside the cavity could belong to saprotrophic
fungi or even be outgrowths from the mantle hyphae that
invaded the senescing reproductive unit and participated
in its degradation.
Figure 2. Germinated zygospore of Mucor mucedo (Mucorales);
zspo = zygosporangium, zsp = zygospore, sph = sporangiophore
or promycelium, spo = germ sporangium (modied from De Bary
1884: g. 71C).
Michael Krings: Unusual Windipila spinifera from the Rhynie cherts150
6. Conclusions
The fossil record rarely gives comprehensive insights into
the life history of fungi, which is unfortunate because life
history stages can provide valuable information to assess
the systematic anities of fossil fungi in the absence of
molecular data (Taylor et al. 2015). The anities of the
organism that produced Windipila spinifera mantled repro-
ductive units remain conjectural, in spite of the fact that
the fossil detailed above shares certain features with ger-
minated zygospores of the germ-sporangial type. I hope
that specimens showing these features in greater detail
become available as exploration of the Rhynie cherts
continues, and that these fossils will clarify the nature of
the interior sphere and reveal hitherto unknown aspects,
which can then be used to determine the systematic posi-
tion of W. spinifera.
Acknowledgments
Funding was received from the National Science
Foundation (DEB-1441604 subcontract S1696A-A). I
thank H. Martin and S. Sónyi (both Munich, Germany)
for technical assistance, and Nora Dotzler (Munich,
Germany) for insightful comments and suggestions on
the manuscript.
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