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Review papers
The Eco-Plant model and its implication on Mesozoic dispersed
sporomorphs for Bryophytes, Pteridophytes, and Gymnosperms
Jianguang Zhang
a,
⁎,Olaf Klaus Lenz
b
,Pujun Wang
c,d
,Jens Hornung
a
a
Technische Universität Darmstadt, Schnittspahnstraße 9, 64287 Darmstadt, Germany
b
Senckenberg Research Institute and Natural History Museum, Senckenberganlage 25, 60325 Frankfurt/Main, Germany
c
Key Laboratory for Evolution of Past Life and Environment in Northeast Asia (Jilin University), Ministry of Education, Changchun 130026, China
d
College of Earth Sciences, Jilin University, Changchun 130061, PR China
abstractarticle info
Article history:
Received 15 July 2020
Received in revised form 2 August 2021
Accepted 3 August 2021
Available online xxxx
The ecogroup classification based on the growth-form of plants (Eco-Plant model) is widely used for extant, Ce-
nozoic, Mesozoic, and Paleozoic paleoenvironmental reconstructions. However, for most Mesozoic dispersed
sporomorphs, the application of the Eco-Plant model is limited because either their assignment to a specific
ecogroup remains uncertain or the botanical affinities to plant taxa are unclear.By comparing the unique outline
and structure/sculpture of the wall of dispersed sporomorph to the sporomorph wall of modern plants and fossil
plants, 861 dispersed Mesozoic sporomorph genera of Bryophytes, Pteridophytes, and Gymnosperms are
reviewed. Finally, 474 of them can be linked to their closest parent plants and Eco-Plant model at family or
order level. Based on thedemands of the parent plants to different humidity conditions, the Eco-Plant modelsep-
arates between hydrophytes, hygrophytes, mesophytes, xerophytes, and euryphytes. Additionally, due to differ-
ent temperature demands a separation in megathermic, mesothermic, microthermic, and eurythermic plants is
possible.In the Mesozoic, bothspore-producingand pollen-producingplants are adaptedto different kinds of hu-
midity. The concept to use the spore/pollen ratio to reflect the hygrophytes/xerophytes ratio is therefore ques-
tionable. The presented ecogroups for dispersed Mesozoic sporomorphs now allow identifying at least relative
plant, paleoenvironmental and paleoclimate changes in Mesozoic sedimentary records.
© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Keywords:
Botanical affinity
Ecogroup
Paleoenvironment
Paleoclimate
Paleoecology
Pollen and spores
Contents
1. Introduction................................................................ 2
2. Materialsandmethods........................................................... 3
3. Results.................................................................. 4
3.1. Bryophytes............................................................. 4
3.1.1. Family: ANTHOCEROTACEAE Dumortier.............................................. 4
3.1.2. Family: ENCALYPTACEAE Schimper................................................ 4
3.1.3. Family: NAIADITACEAE SchusterexKatagirietHagborg...................................... 4
3.1.4. Family: NOTOTHYLADACEAE MüllerexProskauer ......................................... 5
3.1.5. Family: RICCIACEAE Reichenbach................................................ 5
3.1.6. Family: SPHAGNACEAE Dumortier................................................ 5
3.2. Pteridophytes............................................................ 6
3.2.1. Order: CYATHEALES Frank................................................... 6
3.2.2. Order: EQUISETALES deCandolleexBerchtold&Presl....................................... 6
3.2.3. Order: GLEICHENIALES Schimper................................................. 7
3.2.4. Order: HYMENOPHYLLALES Frank................................................. 7
3.2.5. Order: ISOËTALES Prantl.................................................... 7
3.2.6. Order: LYCOPODIALES deCandolleexBerchtold&Presl...................................... 9
Review of Palaeobotany and Palynology 293 (2021) 104503
⁎Corresponding author.
E-mail addresses: zhangjianguang108@126.com (J. Zhang), olaf.lenz@senckenberg.de (O.K. Lenz), wangpj@jlu.edu.cn (P. Wang), hornung@geo.tu-darmstadt.de (J. Hornung).
https://doi.org/10.1016/j.revpalbo.2021.104503
0034-6667/© 2021 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Contents lists available at ScienceDirect
Review of Palaeobotany and Palynology
journal homepage: www.elsevier.com/locate/revpalbo
3.2.7. Order: MARATTIALES Link ................................................... 9
3.2.8. Order: OPHIOGLOSSALES Link.................................................. 9
3.2.9. Order: OSMUNDALES Link .................................................. 10
3.2.10. Order: POLYPODIALES Link.................................................. 10
3.2.11. Order: SALVINIALES Link.................................................. 11
3.2.12. Order: SCHIZAEALES Schimper................................................ 11
3.2.13. Order: SELAGINELLALES Prantl................................................ 13
3.3. Gymnospermae.......................................................... 14
3.3.1. Order: ARAUCARIALES Gorozhankin.............................................. 14
3.3.2. Order: BENNETTITALES Engler................................................. 15
3.3.3. Order: CAYTONIALES Thomas................................................. 15
3.3.4. Order: CHEIROLEPIDIALES AndersonetAnderson......................................... 15
3.3.5. Order: CORYSTOSPERMALES Petriella.............................................. 16
3.3.6. Order: CUPRESSALES Link................................................... 16
3.3.7. Order: CYCADALES PersoonexBerchtoldetPresl........................................ 17
3.3.8. Order: CZEKANOWSKIALES Pant................................................ 18
3.3.9. Order: EPHEDRALES Dumortier................................................ 18
3.3.10. Order: ERDTMANITHECALES Friis&Pedersen.......................................... 18
3.3.11. Order: GINKGOALES Gorozhankin.............................................. 19
3.3.12. Order: PALISSYALES Doweld................................................. 19
3.3.13. Order: PELTASPERMALES Taylor................................................ 19
3.3.14. Order: PINALE S Gorozhankin................................................ 20
3.3.15. Order: VOLTZIALES Andreanszky............................................... 21
3.3.16. Order: WELWITSCHIALES SkottsbergexReveal......................................... 22
4. Discussions............................................................... 22
4.1. The problems of the lack of in situ sporomorphs........................................... 22
4.2. TheproblemsofLM........................................................ 22
4.3. Spore/pollenratio......................................................... 23
5. Conclusions............................................................... 23
DeclarationofCompetingInterest ....................................................... 23
Acknowledgments.............................................................. 23
AppendixA. Supplementarydata...................................................... 23
References.................................................................. 23
1. Introduction
The ecogroup classification based on the growth-form of plants
(Eco-Plant model), established by the pioneering work of Warming
(1895) and Schimper (1898), who analyzed diverse plant associations
with relation to the principal climatic elements such as water, heat,
light, and air, is widely used for extant (e.g., Baeza et al., 2010;Godin,
2017;Sheremetov and Sheremetova, 2017;Veisberg, 2017), Cenozoic
(e.g., Bozukov et al., 2009;Yang et al., 2013;Yurtsev, 2001), Mesozoic
(e.g., Hill, 2017;Vakhrameev, 1991), and Paleozoic paleoenvironmental
reconstructions (e.g., Bashforth et al., 2014;Wang, 1999b). The Eco-
Plant model is also used by palynologists for dispersed sporomorphs
from the Cenozoic (e.g., Aranbarri et al., 2014;Kern et al., 2012;
Popescu et al., 2006;Suc and Fauquette, 2012) and Mesozoic
(e.g., Césari and Colombi, 2016;Hochuli and Vigran, 2010;Mueller
et al., 2016;Roghi et al., 2010;Visscher and van der Zwan, 1981;
Wang et al., 2013;Wang et al., 2005;Zhang et al., 2020;Zhao et al.,
2014) for paleoenvironmental reconstructions. The sporomorph
ecogroup model (SEG model) of Abbink et al. (2004b) is also commonly
used to reconstruct the paleoenvironment and its changes of Mesozoic
records in Europe and some parts of China (e.g., Abbink et al., 2001;
Abbink et al., 2004a;Abbink et al., 2004b;Heunisch et al., 2010;Li and
Wang, 2016;Li et al., 2016). The SEG model represents a simplified
Eco-Plant model. According to hydrologic and temperature conditions,
the Eco-Plant model classifies plants into different EPH (the effect of hu-
midity) and EPT (the effect of temperature) groups due to their climatic
preferences (Zhang et al., 2 020). In contrast, in the SEGmodel, plants are
classified as belonging to a wetter, drier, warmer, or cooler group. Addi-
tionally, in the SEG model (Abbink et al., 2004b), due to uncertain bo-
tanical affinities of some palynomorphs, several plants indicating a
different climate and environment are categorized in the same group.
For example, in the Eco-Plant model, GINKGOALES Gorozhankin are
classified as mesophytes and mesothermic plants, but BENNETTITALES
Engler as hygrophytes and megathermic plants (Zhang et al., 2020). In
contrast, in the SEG model, GINKGOALES Gorozhankin, CYCADALES
Persoon ex Berchtold et Presl, and BENNETTITALES Engler are all in-
cluded in the same group of the “Lowland SEG”and indicate a “drier”
and “warmer”climate, since the pollen of GINKGOALES Gorozhankin,
CYCADALES Persoon ex Berchtold et Presl, and BENNETTITALES Engler
can usually only be distinguished under scanning electron microscopy
(SEM) or transmission electron microscopy (TEM) (Abbink et al.,
2004b). Therefore, the Eco-Plant model allows for more detailed and
precise statements on paleoclimate than the SEG model. However, for
most Mesozoic dispersed sporomorphs, the application of the Eco-
Plant model is limited, because either their assignment to a specific
ecogroup remains uncertain or the botanical affinities to plant taxa are
unclear. Therefore, it is most important to identify their botanical affin-
ities, because otherwise, their Eco-Plant model implications are not re-
liable (Zhang et al., 2020). In the last decades, dispersed sporomorphs
(e.g., Song et al., 1999;Song et al., 2000;Traverse, 2007), in situ
sporomorphs of fossils (e.g., Balme, 1995;van Konijnenburg-van Cittert,
1971), and sporomorphs of extant plants (e.g., Gosling et al., 2013;
Hesse et al., 2009;Li et al., 2011) had been well studied and described,
which provide data to link dispersed sporomorphs convincingly to
their parent plants. Different authors have published compilations of
fossil sporomorphs, which have been linked to plant taxa (e.g., Balme,
1995;Muller, 1981;Potonié, 1967;Song et al., 2004). However, a sys-
tematic review is needed to effectively accelerate a scientific solution
on the debates focusing on linking sporomorphs to parent plants.
Here, we focus especially on Mesozoic dispersed sporomorphs of Bryo-
phytes, Gymnosperms, and Pteridophytes and link them to their possi-
ble parent plants and ecogroups.
J. Zhang, O.K. Lenz, P. Wang et al. Review of Palaeobotany and Palynology 293 (2021) 104503
2
2. Materials and methods
To discuss the Eco-Plant model for dispersed sporomorph generaof
Bryophytes, Pteridophytes, and Gymnosperms from the Mesozoic, in
situ sporomorphs from extant and fossil plants are categorized into dif-
ferent “sporomorph types”based on their unique outline, structure/
sculpture of the sporomorph wall. The “sporomorph types”and plant
taxa are completely different entities because they are characterized ac-
cording to sporomorph morphology, including one or more species as
taxonomic categories (De Klerk and Joosten, 2007;Joosten and de
Klerk, 2002). We use one of the species names for in situ or extant spores
or pollen to name the different “sporomorph types”. The spores or pol-
len grains that belong to the same “sporomorph types”should share the
same stable characters (key characters), which can be used to distin-
guish them from the other types. Each of the “sporomorph types”
should come from a single plant family or order. By comparing the key
characters of each type, dispersed sporomorphs are linked to their par-
ent plants at the family or order level. The Eco-Plant model of the dis-
persed sporomorphs can therefore be discussed based on the related
plant family or order (Fig. 1). The dispersed sporomorph genera
whose descriptions and illustrations do not fully meet the key charac-
ters of a specific sporomorph type or the ultrastructure is unclear so
that can not be compared to the key characters of a specific
sporomorph type ultrastructurally, but are most likely related to this
type are followed by “[?]”. Those which are accepted or supposed as
synonymsby published studies are followed by “[S]”.Morein situ or ex-
tant sporomorphs are collected, but to limit the length of this paper we
only list a part of them. For some sporomorph genera, the parent plants
have been discussed by other authors in published studies. We cite the
important studies in the“Remarks”part. As the reference is always pro-
vided, for simplification only the genus of the parent plants is listed in
the “Remarks”part. For example, Dettmann (1963) stated that the dis-
persed spore Ceratosporites de Jersey et Paten is comparable to the
spore of extant Selaginella latifrons Warburg, while Scafati et al.
(2009) reported that Ceratosporites de Jersey et Paten is comparable
to the spore of extant Selaginella tenuispinulosa Krasnova, but in this
paper, we only describe that “Ceratosporites de Jersey et Paten is com-
parable tothe spore of extant Selaginella de Beauvois (Dettmann, 1963;
Scafati et al., 2009)”. All of the references, which are used for our study,
includingthose which are notcited in this paper, can be found bychoos-
ing a sporomorph genus in the online database (http://www.
sporopollen.com/sporefamilygenus.php)(Zhang et al., 2021).
The sporomorph glossary used in this paper mainly follows Punt
et al. (2007) and Traverse (2007). The systematic scheme of extant
plants is based on Christenhusz et al. (2011) for gymnosperms,
Söderström et al. (2016) for hornworts and liverworts, Goffinet and
Buck (2004) for mosses, and Schuettpelz et al. (2016) for lycophytes
and ferns. The systematic scheme of fossil plants mainly follows Taylor
et al. (2009).Forfigures, descriptions, and definitions of dispersed
sporomorphs, we refer to Jiang et al. (2016),Huang (2008),Liu
(2003),Shang (2011),Song et al. (1999),Song et al. (2000),Shu and
Norris (1999), the 6 volumes book series of Synopsis der Gattungen der
Sporae dispersae (Potonié, 1956, 1958, 1960, 1966, 1970;Potonié and
Kremp, 1970), and the 26volumes book series of Catalog of fossil spores
and pollen (Ames and Spackman, 1985;Ames et al., 1976;Kremp and
Ames, 1959, 1961b, 1962a, 1962b, 1965a, 1965b;Kremp et al., 1957a,
1957b;Kremp et al., 1958, 1959, 1960a, 1960b;Kremp et al., 1966;
Kremp et al., 1967, 1968;Traverse and Ames, 1968, 1969, 1971, 1979;
Traverse et al., 1973a, 1974, 1975;Traverse et al., 1969). Figures and de-
scriptions of extant sporomorphs can mainly be found in Zhang et al.
(2006),Wang and Dai (2010),Li et al. (2011),Tryon and Lugardon
(1991),Hesse et al. (2009),Boros and Járai-Komlódi (1975),and
Kramer and Green (1990). To easily find the figures and descriptions
of the pollen and spores, which are mentioned in this paper, the refer-
ences are given together with plate and figure numbers.
To manage all the information presented in the huge amount of lit-
erature data, it is necessary to store all the figures, descriptions, plant
properties, and related references in a database. Therefore, all informa-
tion compiled in this paper was collected and organized in our database
Sporopollen (http://www.sporopollen.com)(Zhang et al., 2021).
For the analysis of paleoenvironmental and paleoclimate variations,
this paper uses the Eco-Plant model modified by Zhang et al. (2020):
EPH (the effect of humidity) separates the palynomorphs and their
parent plants into five groups:
(a) Hydrophytes are aquatic plants that are completely or mostly
submerged in water as well as being amphibious plants that grow
both in water and in excessively wet habitats along the shorelines of
reservoirs, in areas of shallow water, and swamps.
(b) Hygrophytes are plants that are living in excessively wet habitats
with high air and soil moisture but usually no water stagnation on the
surface, such as the lower tiers of wet forests, or open habitats with con-
stantly wet soils and wet air.
(c) Mesophytes are plants that have some ability to resist periods of
drought or to regulate their water metabolism in moist areas such as
dry meadows or pine forests.
(d) Xerophytes are plants that can resist longperiods of drought and
are living in stony steppes and dry rock outcrops.
(e) Euryphytes are plants that adapt to great variations in humidity.
EPT (the effect of temperature) categorizes the palynomorphs and
their parent plants into four groups:
(a) Megathermic plants inhabiting regions such as tropics and sub-
tropics witha mean annual air temperature (MAT) above 20 °C.
(b) Mesothermic plants inhabiting regions such as warm temperate
zones with a MAT between 14 to 20 °C.
(c) Microthermic plants inhabiting regions such as the cool temper-
ate zone, the subarctic zone, or elevated areas with a MAT below 14 °C.
(d) Eurythermic plants that can tolerate a wide range of
temperatures.
Fig. 1. Flow chart of linking dispersed sporomorphs with plant categories related to Eco-Plant model.
J. Zhang, O.K. Lenz, P. Wang et al. Review of Palaeobotany and Palynology 293 (2021) 104503
3
3. Results
In total, 861 dispersed Mesozoic sporomorphs genera of Bryophytes,
Pteridophytes, and Gymnosperms, are reviewed. Among them, 474
can be linked to their closest parent plants at family or order level,
387 (Appendix A) cannot because of the lack of detailed ultrastructure
description. The ecogroups (EPH and EPT) of 40 plant families or orders
whose fossil plants or dispersed sporomorphs can be found in the
Mesozoic are listed in Table 1. The result can be downloaded online
(http://www.sporopollen.com/sporefamilygenus.php). Below, dis-
persed sporomorph genera from the Mesozoic are linked to the differ-
ent ecogroups:
3.1. Bryophytes
3.1.1. Family: ANTHOCEROTACEAE Dumortier
Species of extant ANTHOCEROTACEAE Dumortier can be found in tropi-
cal, subtropical, and temperate areas growing on the edge of forests or
on moist soils (Verma et al., 2014;Zhang et al., 2006). They are hygro-
phytes and eurythermic plants.
Anthoceros formosae type isospore
Extant spore:Anthoceros cristatus Stephani (Villarreal et al., 2015;
p. 93, pl. 1, figs. A-B)
Extant spore:Anthoceros formosae Stephani (Zhang et al., 2006;
p. 218, pl. 76, figs. 5-7)
Extant spore:Folioceros fusciformis (Montagne) Bharadwaj (Zhang
et al., 2006; p. 219, pl. 77, figs. 1–6)
Key characters: This type of isospore is trilete, circular, generally
25–50 μm in size, with laesurae reaching the edge of the exospore.
The exospore is scattered by irregular biform sculptures consisting of a
broad base surmounted by one, or more than one relatively smaller
spines or bacula.
Dispersed spores: The five dispersed isospore genera related to this
type are Anthocerisporis Krutzsch, Bryosporis Mildenhall [?],
Rudolphisporis Krutzsch, Saxosporis Krutzsch [?], and Saxosporites
Nagy [?].
Remarks:Anthocerisporis Krutzsch, Rudolphisporis Krutzsch,
Saxosporis Krutzsch, and Saxosporites Nagy are comparable to spores
of extant Anthoceros Linnaeus (Ames and Spackman, 1985;Barreda
et al., 2009;Huang et al., 2021;Potonié, 1966).
3.1.2. Family: ENCALYPTACEAE Schimper
Species of extant ENCALYPTACEAE Schimper (Goffinet and Buck, 2004)
are mostly distributed in high mountain or glacial related regions
(Gao et al., 1996;Horton, 1978). Bryobrittonia Williams occur most
commonly in sandy or silty soils along streams or rivers where the sub-
strate is constantlymoist, while Encalypta Hedwigcan be found in bogs,
on arid ground, or rocks. They are euryphytes and microthermic plants.
Encalypta ciliata type isospore
Extant spore:Encalypta ciliata Hedwig (Boros and Járai-Komlódi,
1975; p. 138, figs. 1–8)
Extant spore:Encalypta ciliata Hedwig (Vitt and Hamilton, 1974;pl.
III, figs. 18–19)
Extant spore:Encalypta ciliata Hedwig (Zhang et al., 2006;p.230,pl.
98, figs. 4–6)
Key characters: This type of isospore is trilete, generally 30–40 μmin
size, withindistinct laesurae. One of its faces exhibits a verycharacteris-
tic central brochus with radial arms running to the equator.
Dispersed spore: The dispersed isospore genus related to this type is
Staplinisporites Pocock.
Remarks:Staplinisporites Pocock is comparable to spores of extant
Encalypta Hedwig (Cranwell and Srivastava, 2009;Dettmann, 1963;
Potonié, 1966).
Encalypta rhabdocarpa type isospore
Extant spore:Encalypta rhabdocarpa Schwägrichen (Zhang et al.,
2006;p.231,pl.99,figs. 1–6)
Extant spore:Encalypta spathulata Müller (Zhang et al., 2006; p. 232,
pl. 100, figs. 1–4)
Extant spore:Encalypta vulgaris (Hedwig) Hofmann (Vitt and
Hamilton, 1974; pl. VI, figs. 32–37)
Key characters: This type of isospore is trilete, generally 25–40 μmin
size, with indistinct laesurae. The sporoderm is covered by verrucae. On
top of the verrucae, some irregular elements are often distributed.
Dispersed spore: The dispersed isospore genus related to this type is
Encalyptaesporites Nagy.
Remarks:Encalyptaesporites Nagy is comparable tospores of extant
Encalypta Hedwig (Ames and Spackman, 1985).
3.1.3. Family: NAIADITACEAE Schuster ex Katagiri et Hagborg
The family NAIADITACEAE Schuster ex Katagiri et Hagborg is a
monogeneric family based on the fossil genus Naiadita Brodie from
the Mesozoic (Katagiri and Hagborg, 2015). The abundance of fossil
Naiadita Brodie, together with its mode of preservation suggests that
it is a submerged fresh-water plant in a shallow lake (Harris, 1938;
Hemsley, 1989). They are hydrophytes.
Naiadita lanceolata type isospore
In situ spore: Naiadita lanceolata Buckman (Hemsley, 1989;p.92,pl.
I, figs. 1–6; p. 94, pl. II, figs. 1–6)
In situ spore:Naiadita lanceolata Buckman (Harris, 1938;p.46figs.
21.A–L; p. 47 figs. 22.A–D)
Key characters: This type of isospore is more or less sub-triangular to
circular in outline with an thin equatorial flange (zona) and a hilum (an
irregular break) in the center of the proximal or distal face. The
Table 1
Mesozoic plants and their assignment to Eco-Plant model indicating humidity (EPH) as
well as temperature (EPT) demands.
Phylum Family/Order EPH EPT
Bryophytes
Anthocerotaceae Hygrophytes Eurythermic
Encalyptaceae Euryphytes Microthermic
Naiaditaceae Hydrophytes
Notothyladaceae Hygrophytes Eurythermic
Ricciaceae Hygrophytes Eurythermic
Sphagnales Hydrophytes Eurythermic
Pteridophytes
Anemiaceae Mesophytes Megathermic
Cyatheales Hygrophytes Megathermic
Equisetales Hygrophytes Eurythermic
Gleicheniales Mesophytes Megathermic
Hymenophyllaceae Hygrophytes Eurythermic
Isoetales Hydrophytes Eurythermic
Lycopodiales Hygrophytes Eurythermic
Lygodiaceae Hygrophytes Megathermic
Marattiales Hygrophytes Megathermic
Ophioglossaceae Mesophytes Eurythermic
Osmundales Hygrophytes Eurythermic
Polypodiaceae Mesophytes Megathermic
Pteridaceae Euryphytes Eurythermic
Salviniales Hydrophytes Megathermic
Schizaeaceae Mesophytes Megathermic
Selaginellaceae Euryphytes Eurythermic
Gymnospermae
Araucariaceae Hygrophytes Megathermic
Bennettitales Hygrophytes Megathermic
Caytoniaceae Hygrophytes Megathermic
Cheirolepidiaceae Xerophytes Megathermic
Corystospermales Mesophytes Megathermic
Cupressaceae Euryphytes Eurythermic
Cycadales Mesophytes Megathermic
Czekanowskiales Mesophytes Mesothermic
Ephedraceae Xerophytes Eurythermic
Erdtmanithecaceae Xerophytes Eurythermic
Ginkgoales Mesophytes Mesothermic
Palissyaceae Hygrophytes Megathermic
Peltaspermales Xerophytes Megathermic
Pinaceae Mesophytes Microthermic
Podocarpaceae Hygrophytes Megathermic
Sciadopityaceae Hygrophytes Microthermic
Voltziales Xerophytes Megathermic
Welwitschiaceae Xerophytes Megathermic
J. Zhang, O.K. Lenz, P. Wang et al. Review of Palaeobotany and Palynology 293 (2021) 104503
4
isospores can be 100 μm in size but sometimes rather smaller. The Y
mark is invisible. The proximal face of the spore bears many small
pointed spines whilst the distal face is covered with less densely spaced,
but larger tuberculate to clavate projections.
Dispersed spores: The three dispersed isospore genera related to this
type are Cooksonites Pocock [?],Coptospora Dettmann [?],and
Couperisporites Pocock.
Remarks:Couperisporites Pocock is comparable to in situ spores of
Naiadita Brodie (Dettmann, 1963;Potonié, 1966).
3.1.4. Family: NOTOTHYLADACEAE Müller ex Proskauer
Species of extant NOTOTHYLADACEAE Müller ex Proskauer (Söderström
et al., 2016) can be found in moist soils from warm tropical regions to
cold circumboreal regions (Boros and Járai-Komlódi, 1975;Zhang
et al., 2006). They are hygrophytes and eurythermic plants.
Phaeoceros skottsbergii type isospore
Extant spore:Notothylas levieri Schiffner (Chantanaorrapint, 2015;
p. 260, figs. 27–28)
Extant spore:Notothylas levieri Schiffner (Zhang et al., 2006;p.81,
figs. 3–6)
Extant spore:Phaeoceros skottsbergii Stephani (Warny et al., 2012;
p. 241, pl. 5, figs. 5–6)
Key characters: This type of isospore is trilete, generally 25–50 μmin
size. The exospore isconsiderably thick, and usually thicker in the distal
rather than the proximal face. On the distal face, there is often a charac-
teristic projection which can be a solid circle, a hollow circle, or concen-
tric rings.
Dispersed spores: The 10 dispersed isospore genera related to
this type are Annulispora de Jersey,Dicyclosporis Schulz [S],
Distalanulisporites Klaus [S], Distcyclosporis Schulz [S], Guyangspora
Yu et Miao [?], Neochomotriletes Reinhardt [S], Parmulisporis Bai [?],
Phaeocerosporites Nagy,Polycingulatisporites Simoncsics et Kedves
[?], and Taurocusporites Stover [S].
Remarks:Annulispora de Jersey is comparable to spores of extant
Notothylas Sullivant and Phaeoceros Proskauer(Zhang et al., 2020).
Phaeocerosporites Nagy is comparable to spores of extant Phaeoceros
Proskauer both in the order of magnitude and morphology (Ames and
Spackman, 1985). Dicyclosporis Schulz, Distcyclosporis Schulz, and
Distalanulisporites Klaus are synonyms of Annulispora de Jersey
(McKellar, 1974;Potonié, 1966).Neochomotriletes Reinhardt and
Taurocusporites Stover are synonyms of Polycingulatisporites
Simoncsics et Kedves (Potonié, 1966, 1970). Annulispora de Jersey is
distinguished from Polycingulatisporites Simoncsics et Kedves by
possessing a single, distal, sub-circular ridge, whereas the latter genus
is characterized by forms displaying two distal ridges that are concentri-
cally situated with respect to the pole (McKellar, 1974).
Paraphymatoceros diadematus type isospore
Extant spore:Notothylas yunannensis Peng & Zhu (Rattanamanee
and Chantanaorrapint, 2015;p.272,pl.1,figs. C–D)
Extant spore:Paraphymatoceros coriaceus (Stephani) Stotler
(Crandall-Stotler et al., 2008;p.228,pl.5,figs. 5–6)
Extant spore:Paraphymatoceros diadematus Hässel (Crandall-
Stotler et al., 2008;p.228,pl.5,figs. 2–4)
Key characters: This type of isospore is trilete, generally 25–60 μmin
size. The proximal face is divided into three flattened facets by laesurae.
In the center of each facet, there is a hollow, which is often surrounded
by a radial sculpture.
Dispersed spores: The five dispersed isospore genera related to this
type are Asterisporites Venkatachala et Rawat [S],Foraminisporis
Krutzsch,Nevesisporites de Jersey et Paten, Simeonospora Balme [S],
and Trisolissporites Tschudy [S].
Remarks:Foraminisporis Krutzsch and Nevesisporites de Jersey et
Paten are comparable to spores of extant Phaeoceros Proskauer and
Notothylas Sullivant ex Gray (Dettmann, 1963;Nemejc and Pacltova,
1972;Potonié, 1966;Schrank, 2010). Asterisporites Venkatachala et
Rawat,Simeonospora Balme,and Trisolissporites Tschudy are syno-
nyms of Nevesisporites de Jersey et Paten (Song et al., 1999).
3.1.5. Family: RICCIACEAE Reichenbach
Species of extant RICCIACEAE Reichenbach (Söderström et al., 2016)
can be found in warm tropical regions to cold circumboreal regions.
Most of them live in wet environments and some of them float on
water (Boros and Járai-Komlódi, 1975;Zhang et al., 20 06).They are gen-
erally hygrophytes and eurythermic plants.
Riccia frostii type isospore
Extant spore:Riccia frostii Austin (Boros and Járai-Komlódi, 1975;
p. 51, figs. 1–6)
Extant spore:Riccia glauca Linnaeus (Zhang et al., 2006;p.140,pl.8,
fig. 3; p. 207 pl. 75, figs. 2–6)
In situ spore:Ricciopsis sp. (Volkheimer and Scafati, 2007;p.127,pl.
3, fig. 3)
Key characters: This type of isospore is trilete, generally 50–90 μmin
size, triangular, with a reticulate sculpture. On the equator there is an
opening on each triangular corner. For some spore grainsthe thin equa-
torial flange (zona) is visible.
Dispersed spores: The five dispersed isospore genera related to this
type are Ricciaesporites Nagy, Rouseisporites Pocock [S],Triporoletes
Mtchedlishvili,Trochicola Srivastava [?], and Zlivisporis Pacltová [S].
Remarks:Ricciaesporites Nagy and Rouseisporites Pocock are com-
parable to spores of extant Riccia Linnaeus (Ames and Spackman, 1985;
Dettmann, 1963). Rouseisporites Pocock and Zlivisporis Pacltová are
synonyms of Triporoletes Mtchedlishvili (Song et al., 1999).
3.1.6. Family: SPHAGNACEAE Dumortier
Species of extant SPHAGNACEAE Dumortier (Goffinet and Buck, 2004)
are nearly cosmopolitan, but most of them are found in circumboreal re-
gions in bogs, wetlands, or swamp forests (Boros et al., 1993;Gao,
1994). They are generally hydrophytes and eurythermic plants.
Sphagnum capillifolium type isospore
Extant spore:Sphagnum capillifolium (Ehrhart) Hedwig (Boros and
Járai-Komlódi, 1975;p.84,figs. 1–6)
Extant spore:Sphagnum cuspidatum Ehrhart ex Hoffmann (Zhang
et al., 2006; p. 144, pl. 12, fig. 1; p. 214, pl. 82, figs. 1,2)
Extant spore:Sphagnum girgensohnii Russow (Zhang et al., 2006;
p. 144, pl. 12, fig. 2; p. 214, pl. 82, figs. 3–5)
Key characters: This type of isospore is trilete, generally 25–50 μmin
size, oblate in the equatorial view, subtriangular in polar view, and has a
smooth exospore. The perispore is provided with granula and verrucae
of different sizes and shapes.
Dispersed spores: The nine dispersed isospore genera related to this
type are Coralloseratisporis Timmermann [S],Distancoraesporis
(Krutzsch) Srivastava,Distverrusporis Krutzsch,Duplozonosporis
Döring et Krutzsch [S],Sculptisporis Döring et Schulz [S],Sphagnites
Cookson [S],Sphagnumsporites Raatz ex Potonié,Stereisporites Pflug
[S], and Tripunctisporis Krutzsch [S].
Remarks: The perispore may not be or only poorly preserved in
fossil state, which is common for all spores. The perispore often
sloughs off partially or entirely in acetolysis preparations and
can be presumed to do the same during fossilization (Traverse,
2007). Distancoraesporis (Krutzsch) Srivastava, Distverrusporis
Krutzsch,and Sphagnumsporites Raatz ex Potonié are comparable to
spores of extant Sphagnum Linnaeus (Potonié, 1956;Worobiec, 2009).
Coralloseratisporis Timmermann, Duplozonosporis Döring
et Krutzsch,Sculptisporis Döring et Schulz,Sphagnites Cookson,
Stereisporites Pflug,and Tripunctisporis Krutzsch are synonyms of
Sphagnumsporites Raatz ex Potonié (Potonié,1956,1966,1970).
J. Zhang, O.K. Lenz, P. Wang et al. Review of Palaeobotany and Palynology 293 (2021) 104503
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3.2. Pteridophytes
3.2.1. Order: CYATHEALES Frank
The extant order CYATHEALES Frank consists of eight families
(Schuettpelz et al., 2016). Fossils with in situ spores found in the Meso-
zoic are Sergioa Césari (2006) and Alsophilites Hirmer (Shuklina and
Polevova, 2007). Extant species are tree ferns concentrated in the tro-
pics where they are most common within the montane to alpine vege-
tation. Many species occur in the undergrowth of moist forests, often in
ravines, but others prefer more open habitats, even swamps, and some
grow preferentially in open areas (Kramer and Green, 1990). They are
generally hygrophytes and megathermic plants.
Cibotium barometz type isospore
Extant spore: Cibotium barometz (Linnaeus) Smith (Tryon and
Lugardon, 1991; p. 223, pl. 77, figs. 3–4)
Extant spore: Cibotium barometz (Linnaeus) Smith (Gastony, 1982;
p.967, figs 46–48; p. 969–971, figs. 49–65)
Key characters: This type of isospore is trilete, triangular or
subtriangular, with a thick equatorial flange (cingulum), kyrtomes on
the proximal face, and coarse ridges forming a triangular area on the
distal face, generally 45–80 μm in size. The exospore has two layers.
Dispersed spores: The seven dispersed isospore genera related to this
type are Cibotiidites Ross,Cibotiumidites (Malyavkina) Potonié,
Cibotiumspora Chang,Cibotiumsporites Rouse,Crassitudisporites
Hiltmann [?],Distaltriangulisporites Singh [?],and Duplexisporites
(Deák) Playford et Dettmann.
Remarks: Cibotiidites Ross,Cibotiumidites (Malyavkina) Potonié,
Cibotiumspora Chang,Cibotiumsporites Rouse,and Duplexisporites
(Deák) Playford et Dettmann are comparable to spores of extant
Cibotium Kaulfuss (Cranwell and Srivastava, 2009;Kremp et al.,
1957a;Kremp et al., 1958;Kremp et al., 1967, 1968;Song et al., 2000;
Srivastava, 1987).
Sergioa austrina type isospore
Extant spore: Lophosoria quadripinnata (Gmelin) Christensen
(Césari, 2006;p.235,pl.IV,figs. 8, 10, 11)
Extant spore: Lophosoria quadripinnata (Gmelin) Christensen
(Tryon and Lugardon, 1991;p.241,pl.83,figs. 1–5)
In situ spore: Sergioa austrina Césari (Césari, 2006; p. 235, pl. IV, figs.
3–7, 9, 12)
Key characters: This type of isospore is trilete, triangular, or
subtriangular, witha thick equatorial flange (cingulum), perforate or re-
ticulate on the distal face, tuberculate on the proximal face, generally
30–100 μm in size. The exospore has two layers.
Dispersed spores: The dispersedisospore genus related to this type is
Cyatheacidites Cookson ex R. Potonié.
Remarks: Cyatheacidites Cookson ex R. Potonié is comparable to in
situ spores of Sergioa Césari (Césari, 2006).
Alsophilites nipponensis type isospore
Extant spore: Alsophila bryophila Tryon (Tryon and Lugardon, 1991;
p. 255, pl. 85, figs. 5, 10–11)
In situ spore: Alsophilites nipponensis (Oishi) Krassilov (Shuklina and
Polevova, 2007; p. 315, pl. 10, figs. 2–3)
In situ spore: Coniopteris hymenophylloides (Brongniart) Seward
(van Konijnenburg-van Cittert, 1989; p. 276, pl. II, figs. 3, 5)
Extant spore: Cyathea arborea (Linnaeus) Smith (Tryon and
Lugardon, 1991; p. 263, pl. 88, fig. 7)
Extant spore: Dicksonia sellowiana (Presl) Hooker (van
Konijnenburg-van Cittert, 1989; p. 292, pl. VIII, figs. 5–7)
In situ spore: Eboracia lobifolia (Phillips) Thomas (van
Konijnenburg-van Cittert, 1989; p. 286, pl. V, fig. 4; p. 288, pl. VI, figs.
1–3)
Extant spore: Hemitelia sp. (Hofmann, 2002; p. 207, pl. II, fig. 12)
Key characters: This type of isospore is trilete, triangular usually with
prominent angles and a smooth exospore, generally 20–50 μm in size.
The length of the laesura is nearly equal to the radius of the equator.
The exospore has two layers. The perispore can be simple or complex.
Dispersed spores: The 12 dispersed isospore genera related to this
type are Alsophilidites Cookson ex Potonié,Camursporis Chlonova,
Cornutisporites Schulz,Cyathidites Couper,Divisisporites Pflug [?],
Hemitelites Romanovskaja,Kuylisporites Potonié,Maculatisporites
Döring [S],Porisporites Pacltová et Simoncsics, Synasesporites Zhang
[?],Thuringiasporites Schulz,and Zebrasporites Klaus [S].
Remarks: Alsophilidites Cookson ex Potonié is comparable to spores
of extant Alsophila Brown (Potonié, 1967b). Cyathidites Couper is com-
parable to in situ spores of Alsophilites Hirmer (Shuklina and Polevova,
2007), Coniopteris Brongniart, and Eboracia Thomas and spores of ex-
tant Dicksonia L'Héritier (Dettmann, 1963). Camursporis Chlonova,
Cornutisporites Schulz, Hemitelites Romanovskaja, Kuylisporites
Potonié, Porisporites Pacltová et Simoncsics, and Thuringiasporites
Schulz are comparable to spores of extant Hemitelia Brown (Ames
and Spackman, 1981, 1985;Traverse and Ames, 1968).
Maculatisporites Döring is a synonym of Cyathidites Couper (Potonié,
1970), Thuringiasporites Schulz of Zebrasporites Klaus (Potonié,
1966).
3.2.2. Order: EQUISETALES de Candolle ex Berchtold & Presl
The extant order EQUISETALES de Candolle ex Berchtold & Presl
(Schuettpelz et al., 2016) consists of one family EQUISETACEAE Michaux
ex de Candolle with a single genus Equisetum Linnaeus, which is a her-
baceous perennial plant. Species of Mesozoic EQUISETALES de Candolle ex
Berchtold & Presl are more or less comparable to extant Equisetum Lin-
naeus (Taylor et al., 2009).The mode of fossil Neocalamites tubulatus
Naugolnykh preservation indicates that the parentplants resembled re-
cent Equisetum Linnaeus communities and had therefore grown along
lake shores inhabited by a near-water hygrophilous plant community
of helophytes (Naugolnykh, 2009). Extensive fossil Equisetites
arenaceus (Jaeger) Schenk populations occurred in marginal strips
along an anastomosing river system. Dense Equisetites arenaceus (Jae-
ger) Schenk reeds also invaded the levee belt as well as hygromorphic
environments surrounding standing waterbodies in a flood plain
(Kelber and van Konijnenburg-van Cittert, 1998). Equisetum Linnaeus
has been reported from numerous localities worldwide, where they
are primarily plants of open, sunny sand banks along river and lake mar-
gins, in marshes, andin other wet places (Taylor et al., 2009). Although
the greatestconcentrations of extant species are found between 40° and
60° northern latitude,Eq uisetum Linnaeus is found worldwide from the
southern parts of South America and Africa to north of the Arctic Circle
(Kramer and Green, 1990). Therefore, they are generally hygrophytes
and eurythermic plants.
Equisetostachys verticillata type isospore
In situ spore: Echinostachys oblonga (Brongniart) Grauvogel-
Stramm (Grauvogel-Stamm and Lugardon, 2009; p.118, pl. I, fig. 3)
In situ spore: Equisetostachys verticillata Grauvogel-Stamm
(Grauvogel-Stamm and Lugardon, 2009; p.118, pl. I, figs. 5–11)
Extant spore: Equisetum bogotense Kunth (Tryon and Lugardon,
1991;p.585,pl.226,figs. 1–2)
Key characters: This type of isospore is trilete or alete, spherical, with
a smooth exospore, generally 30–70 μm in size. The laesurae are some-
times invisible or faint. The isospore is with or without elaters that are
coiled around the spore. The exospore has two layers.
Dispersed spores: The seven dispersed isospore genera related to this
type are Aulisporites Leschik [?], Calamisporites Danzé-Corsin et
Laveine [S], Calamospora Schopf, Wilson et Bentall,Cuneisporites
Zhang [?],Equisetitriletes Zhang [?], Pilasporites Balme et Hennelly,
and Scabratisporites Visscher [S].
Remarks: During the Mesozoic Equisetites Sternberg produced both
trilete spores of Calamospora Schopf, Wilson et Bentall and alete spores
of Pilasporites Balme et Hennelly (Kelber and van Konijnenburg-van
Cittert, 1998). Calamisporites Zhang and Scabratisporites Visscher
are synonyms of Calamospora Schopf, Wilson et Bentall (Potonié,
1970;Shu and Norris, 1988).
J. Zhang, O.K. Lenz, P. Wang et al. Review of Palaeobotany and Palynology 293 (2021) 104503
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