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Article Dynamics of Silurian Plants as Response to Climate Changes

Josef Pšeniˇcka 1,* , Jiˇrí Bek 2, Jiˇrí Frýda 3,4, Viktor Žárský 2,5,6, Monika Uhlíˇrová 1,7 and Petr Štorch 2

1 Centre of Palaeobiodiversity, West Bohemian Museum in Pilsen, Kopeckého sady 2, 301 00 Plzeˇn,Czech Republic; [email protected] 2 Laboratory of Palaeobiology and Palaeoecology, Geological Institute of the Academy of Sciences of the Czech Republic, Rozvojová 269, 165 00 Prague 6, Czech Republic; [email protected] (J.B.); [email protected] (V.Ž.); [email protected] (P.Š.) 3 Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, 165 21 Praha 6, Czech Republic; [email protected] 4 Czech Geological Survey, Klárov 3/131, 118 21 Prague 1, Czech Republic 5 Department of Experimental Plant Biology, Faculty of Science, Charles University, Viniˇcná 5, 128 43 Prague 2, Czech Republic 6 Institute of Experimental Botany of the Czech Academy of Sciences, v. v. i., Rozvojová 263, 165 00 Prague 6, Czech Republic 7 Institute of Geology and Palaeontology, Faculty of Science, Charles University, Albertov 6, 128 43 Prague 2, Czech Republic * Correspondence: [email protected]; Tel.: +420-733-133-042

Abstract: The most ancient macroscopic plants fossils are Early Silurian cooksonioid sporophytes from the volcanic islands of the peri-Gondwanan palaeoregion (the Barrandian area, Prague Basin, Czech Republic). However, available palynological, phylogenetic and geological evidence indicates



that the history of plant terrestrialization is much longer and it is recently accepted that land floras,
 producing different types of spores, already were established in the Ordovician Period. Here we

Citation: Pšeniˇcka,J.; Bek, J.; Frýda, attempt to correlate Silurian floral development with environmental dynamics based on our data from J.; Žárský, V.; Uhlíˇrová,M.; Štorch, P. the Prague Basin, but also to compile known data on a global scale. Spore-assemblage analysis clearly Dynamics of Silurian Plants as indicates a significant and almost exponential expansion of trilete-spore producing plants starting Response to Climate Changes. Life during the Wenlock Epoch, while cryptospore-producers, which dominated until the Telychian Age, 2021, 11, 906. https://doi.org/ were evolutionarily stagnate. Interestingly cryptospore vs. trilete-spore producers seem to react 10.3390/life11090906 differentially to Silurian glaciations—trilete-spore producing plants react more sensitively to glacial cooling, showing a reduction in species numbers. Both our own and compiled data indicate highly Academic Editors: Cecília Sérgio and terrestrialized, advanced Silurian land-plant assemblage/flora types with obviously great ability to David Draper resist different dry-land stress conditions. As previously suggested some authors, they seem to evolve on different palaeo continents into quite disjunct specific plant assemblages, certainly reflecting the Received: 4 August 2021 Accepted: 25 August 2021 different geological, geographical and climatic conditions to which they were subject. Published: 31 August 2021 Keywords: early land plants; Silurian; plant assemblages; palaeoclimatic changes; polysporangiate

Publisher’s Note: MDPI stays neutral plants; plant stress responses; carbon cycle with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction The final stages of the colonization of land by plants (Embryophyta) within the Ordovician-Silurian interval is one of the most important global events in the evolution of Copyright: © 2021 by the authors. life on the Earth. Wellman and Strother [1] and Kenrick [2] hypothesized that life existed on Licensee MDPI, Basel, Switzerland. the land since over 2.7 Gyr in the form of communities of bacteria (including cyanobacteria) This article is an open access article and archaea [3,4], that colonized shallow places in the fresh-water environment. distributed under the terms and Successful terrestrialization of plants was enabled by some crucial adaptations includ- conditions of the Creative Commons ing tissues ensuring the distribution of water and nutrients for growth, body protection Attribution (CC BY) license (https:// against desiccation and UV, anchoring in the substrate, and propagation by resistant creativecommons.org/licenses/by/ spores [5,6]. 4.0/).

Life 2021, 11, 906. https://doi.org/10.3390/life11090906 https://www.mdpi.com/journal/life Life 2021, 11, x FOR PEER REVIEW 2 of 22

Life 2021, 11, 906 protection against desiccation and UV, anchoring in the substrate, and propagation2 of 22by resistant spores [5,6]. Ordovician and Silurian plant communities already included possibly several groups of polysporangiateOrdovician and land Silurian plants plant (no communities monosporangiates already are included documented possibly by several the fossil groups rec- oford), polysporangiate including more land ancient plants and (no enigmatic monosporangiates cryptosporophytes are documented [7,8], accompanied by the fossil record), by bac- includingterial-cyanobacterial more ancient mats and [9–11]. enigmatic At the cryptosporophytes end of the Silurian [7,8 and], accompanied the beginning by of bacterial- the De- cyanobacterialvonian it is already mats [9 possible–11]. At theto quite end of reliably the Silurian identify and the the first beginning lycophytes of the ( DevonianBaragwanathia it is alreadyand Asteroxylon possible to). quite reliably identify the first lycophytes (Baragwanathia and Asteroxylon). TheThe firstfirst evidence indicating indicating the the existence existence of ofland land plants plants are arecryptospores cryptospores of the of Early the EarlyMiddle Middle Ordovician Ordovician age (c. age 470MA) (c. 470MA) [12]. However, [12]. However, their producers their producers are still are unknown. still un- known.Some very Some questionable very questionable polysporangiophytes polysporangiophytes have been have described been from described the Ordovician from the Ordovician[13,14] that [ 13coincide,14] that with coincide the appearance with the appearance of the first of true the firsttrilete true spores trilete within spores the within Late theOrdovician Late Ordovician [15,16]. [ 15These,16]. Thesespores spores indicate indicate an earlier an earlier origin origin of possibly of possibly several several types types of ofpolysporangiophyte-grade polysporangiophyte-grade plants, plants, probably probably during during Ordovician. Ordovician. Some authors hypothe-hypothe- sizedsized the the colonization colonization of of land land by by embryophytes embryophytes during during the the Cambrian Cambrian (or even(or even Proterozoic) Protero- andzoic) this and recently this recently has been has stronglybeen strongly supported supported by phylostratigraphic by phylostratigraphic data [ 3data,4,17 [3,4,17,18].,18]. ThisThis paperpaper providesprovides an an overview overview and and a a revision revision of of Silurian Silurian plant plant assemblages assemblages (from (from WenlockWenlock to to Pˇr Pířdolídolí)í) of of polysporangiophytes polysporangiophytes with with dispersed dispersed spores spores and and cryptospores. cryptospores. Spe-Spe- cialcial attention attention is is paid paid to to the the dynamics dynamics of of the the Silurian Silurian plant plant evolution evolution within within the the context context of of SilurianSilurian climateclimate changeschanges linkedlinked withwith perturbationsperturbations ofof thethe globalglobal carboncarbon cyclecycle ((FigureFigure1 1).). TheThe data data on on Llandoverian Llandoverian plants plants are are not not included included in in the the latter latter analysis analysis because because (1) 1) obser-obser- vationsvations ofof well-preserved well-preserved macroplants macroplants below below the the Wenlock Wenlock are are extremely extremely rare rare and and (2) 2) the the plantsplants are are represented represented only only by by sterile sterile bifurcated bifurcated axes axes [ 19[19].].

Figure 1. Silurian time scale showing conodont and graptolite biozones, stage slices (s.s.), and generalized δ13Ccarb curve, modified from [20–22], combined with isotopic temperature curves (blue

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based on brachiopod, and red on conodont δ18O data) from [23]. The conodont isotopic tem- perature curves for Ludfordian were modified based on [24]. The isotopic temperatures assume “ice-free” conditions (δ18Oseawater = −1.1‰ vs. VSMOW). Abreviations: Shein.—Sheinwoodian; Hom.—Homerian; Gor.—Gorstian; Lud.—Ludfordian; Loch.—Lochkovian. Abreviations used in graptolite column, bottom to top: Cy.—Cyrtograptus; M. riccarton.—Monograptus riccartonensis; Pr. par./G. nas.—Pristiograptus parvus/Gothograptus nassa; Col.—Colonograptus; Col. prae./deub.—Col. praedeubeli/Col. deubeli; N./ Lo.—Neodiversograptus/ Lobograptus; Lo.—Lobograptus; Sa. leintward./Sa. Linearis—Saetograptus linearis; Ne./Po.—Neocucullograptus/Polonograptus; Neo.—Skalograptus; Neo. parult.—Neocolonograptus parultimus; M. loc./M. bra.—Skalograptus lochkovensis/M. lochkovensis braniken- sis; M.—Monograptus. Conodont column, bottom to top: procerus—Pterospathodus pennatus procerus; K.—Kockelella; K. ranuli.—K. ranuliformis; O. s. rhenana—Ozarkodina sagitta rhenana; O. s. sagitta— Ozarkodina sagitta sagitta; O. boh. Longa—Ozarkodina bohemica longa; K. o. absid.—Kockelella ortus absidata; A.—Ancoradella; Po.—Polygnathoides; Ped.—Pedavis; O.—Ozarkodina; ‘O.’ eostein.—“Ozarkodina” eostein- hornensis sensu lato; Ou.—Oulodus. S.Z.—Superbiozone; Z.G.—Zonal Group; I.Z.—Interval Biozone.

1.1. Character of Early Land Plants and Their Classification Gerrienne et al. [25] established a currently widely accepted approach for the classifi- cation of the earliest embryophytes (including monosporangiate hornworts and mosses not reported from fossil data), which, along with obscure embryophytes and probably bacterial- cyanobacterial mats, formed essential components of the entire terrestrial ecosystem, in- cluding the well-known genera Nematothallus, Pachytheca and Prototaxites. Nematothallus, which probably belonged to lichenized fungi [26]. Many different-sized tubular structures from Silurian-Devonian sediments (probably composed of hyphae) are assigned to Pro- totaxites. Pachytheca, represented by small spherical structures of still unknown affinity, stressed some similarities to Prototaxites [27]. Nematasketum, classified as an enigmatic non- embryophyte plant [28], was described based on vegetative parts and possesses an axial organization with peripheral tissues forming a ring. Nematasketum shows some similarities with Prototaxites [28]. The first credible fossil bryophytes, represented by Riccardiothallus devonicus [15,29], are of the Pragian (Early Devonian) age. Morris et al. [15] estimated the appearance of bryophytes during the Late Cambrian–Late Ordovician interval based on molecular clock data. The Ordovician occurrence of bryophytes would also be supported by fossil spore exine ultrastructural similar to some spores of recent liverworts [30]. However, there is a recent consensus of monophyletic origin of the bryophytes and its sister relationship with tracheophytes (i.e., tracheophytes did not evolve from bryophytes [18,31]). This clearly indicates that it might not make much sense to speak about monosporangiate mosses in the Ordovician or Silurian without fossil support for a polysporangiate common ancestor of both mosses and tracheophytes, which is currently probable (see our Discussion). Polysporangiophytes [25,32,33] formed the only embryophytic plants documented by the fossil in the Silurian. The group includes the first true vascular plants (Tracheophyta). Although recent vascular plants may reach tens of meters in height, the earliest terrestrial forms were mostly diminutive [8,34–37], although some forms of polysporangiophytes could already have been over 10 cm tall (e.g., Tichavekia grandis)[38]. The main character of polysporangiophytes is, as the name suggests, the branched sporophyte with more than one sporangium [39]. Silurian plant communities most commonly include polysporangiophyte taxa, such as Cooksonia, Salopella, Aberlemnia, Hedeia, Tortillicaulis, Fusiformitheca, Steganotheca and Caia. Sterile fragments of plant axes are referred to the genus Hostinella. All those genera are usually placed among “rhyniophytoids“ [40]. Basal lycophytes are represented by zosterophylls [33]. Silurian zosterophylls include Zosterophyllum, Bathurstia, Distichophytum, Macivera, and Aberlemnia with bivalved sporangia and dehiscence along the distal sporangial margin, which has led to the placement of these plants [38,41] in the lycophyte stem group. The first unambiguous lycophyte is Baragwanathia, occurring in the late Silurian [42–44], which already had well-developed microphylls. Life 2021, 11, 906 4 of 22

1.2. Silurian Plant Assemblages Silurian plant assemblages and their geographical distribution were studied in several papers [45–49]. We must be aware that only a limited number of plants can be found at one locality and it is not exceptional that only one species of polysporangiophyte occurs at a locality. It appears that phytogeographical differentiation and disjunction (isola- tion) of land-plant types/groups was significant during the Late Silurian (Pˇrídolí) and Early Devonian [47,50]. Raymond et al. [47] established 35 macrofloristic assemblages for Silurian to Early Devonian times based on correspondence and cluster analyses for different geographical areas and climatic zones. The latter analyses resulted in the es- tablishment of four phytogeographic units: (1) North Laurussian unit (Bathurst Island) located near the palaeoequator; (2) South Laurussian–Northwest Gondwanan unit (UK; Podolia, Ukraine and Bolivia) located approximately 18◦ S palaeolatitude to 60–75◦ S palae- olatitude; (3) Kazakhstanian unit located north of the palaeoequator; and (4) Northeast Gondwanan (Australian) unit at 10◦ S palaeolatitude [47]. Later Wellman et al. [48] estab- lished 14 assemblages but they did not revise palaeophytogeographical areas proposed by Raymond et al. [47] that are used herein.

2. Materials and Methods Specimens/samples were selected from the Collections of the Centre of Palaeobiodiver- sity of the West Bohemian Museum in Pilsen—WBM (Czech Republic), specimens F21761a, F21762; SEM-rack SILI-A1, Kosov Quarry; National Museum—NM (Prague, Czech Re- public), specimens D-475 Kosov Quarry, D-552b Lodˇenice,Špiˇcatý vrch-Barrandovy Jámy; Czech Geological Survey (Prague, Czech Republic)—CGS, specimen KR 1, Karlštejn lo- cality; Faculty of Sciences, Charles University, Prague (Czech Republic)—FSCU, Kosov Quarry; Swedish Museum of Natural History (Stockholm, Sweden)—SMNH, specimen JE-Sch0260B, Kosov Quarry; private collections of OndˇrejZicha—PCC (Czech Republic), Špiˇcatý vrch-Barrandovy Jámy and the collection of the University of Saskatchewan— US (Saskatoon, Canada), specimens US600-6791, US600-8144, US384-8137, US688-8152, US385-2398, Bathurst Island, Canada. Specimens from NM, WBM, CGS, FSCU, SMNH and PCC represented polysporangiophyte assemblages from the temperate zone of the lower Wenlock (Sheinwoodian) and Pˇrídolí of the Barrandian area, the Prague Basin (Czech Republic). Mesofossils from the upper Wenlock (Homerian, parvus-nassa Biozone) of the Lištice locality are stored in WBM showing small plant fragments macerated from the rock (HCL 32% (5–10 days)-HF35% (5–8 days)-HNO3 65% (several minutes–10 days). Specimens of polysporangiophytes from the tropical zone of the Gorstian age, Ludlow (Canada) are stored in the US.

3. Results 3.1. Environment of Silurian Plants Early land/polysporangiate plants diversified and colonized continents during Silurian- Devonian “terrestrial radiation” [51]. Recent analysis convincingly indicates a possibility that a great land plant radiation had already occurred in the Ordovician and argues that land plants were possibly not affected by the end-Ordovician extinction event [52]. Servais et al. [53] stated the importance of environmental factors, including atmospheric compo- sition and the geochemical carbon cycle [54,55], as major influencers of the evolutionary dynamics of early plants. The Silurian Period has been considered as a stable interval characterized by gradual, long-term climatic change starting from the Middle to Late Ordovician cold climate and culminating in Silurian greenhouse conditions [56,57]. The Silurian, lasting from approximately 443.1 to 419.0 million years [22], represents a key interval in the biological evolution of marine ecosystems [58–61]. The transitional character of the Silurian is not illustrated only by the changes of marine communities and ecosystems, but also by the instability of the global carbon cycle including rapid changes in atmospheric pO2 and pCO2 [62–64]. Published data indicate that during the relatively short Silurian interval at least five globally observed carbon isotope excursions have been recognized Life 2021, 11, 906 5 of 22

(Figure1). These anomalies include the δ13C excursions in the mid-Llandovery, early Wenlock, late Wenlock, late Ludlow, and across the Silurian-Devonian boundary [21,65]. Geochemical events were closely linked to major crises in marine ecosystems as well as to palaeoclimatic changes [24,56,66–69]. Global temperature, together with total precipitation, are key parameters influencing terrestrial community development. However, the reconstruction of global temperature change is complicated and has to be based on samples from different palaeoregions because ocean temperature varied with season, water depth, and palaeolatitude [23]. In addition, to calculate palaeotemperatures from marine calcite or apatite δ18O values, the oxygen isotope composition of the Silurian seawater has to be assumed. However, there is no consensus on whether the oxygen isotope composition of seawater evolved during the Phanero- zoic [70,71] or was more or less constant [72]. Thus, without a better constrained Silurian seawater δ18O, the calculation of absolute temperatures remains speculative. However, relative temperature changes can be calculated independent of seawater δ18O (Figure1). Grossman and Joachimski [23] mentioned that the oxygen isotope record for Silurian brachiopods and conodonts from tropical and subtropical palaeolatitudes showed a Llan- dovery Warm Trend. On the other hand, Silurian brachiopod data revealed a Ludfordian Cool Event. New δ18O conodont data from Ludfordian temperate as well as tropical palaeolatitudes [24] confirms the marked cooling of sea surface temperatures at time a significant eustatic sea-level fall occurred on several palaeocontinents. These observations, interpreted as a major glaciation in polar and subpolar Gondwana, are referred to as the ‘Mid-Ludfordian Glaciation’ [24]. Taken together, recently available sedimentological (glacial diamictite deposition) and geochemical (δ18O) data suggest at least five glacial events within the Silurian Period, namely early Aeronian, late Aeronian, early Sheinwoodian, Homerian, and mid-Ludfordian glaciation [24,56,66,69,73] (Figure1).

3.2. Diversity of Silurian Plants Raymond et al. [47] proposed the following palaeophytogeographical units.

3.2.1. North Laurussian Unit This unit, located near the palaeoequator, was of tropical character (Figure2—La, Lb, Lc, L3, La) and includes north Laurussian basins. The oldest plant fossil record is known from the Ludlow strata (Figure3) of Bathurst Island [ 45,74] and North Green- land [75]. The Bathurst Island plant assemblage provides several terrestrial species, e.g.,: Cf. Bathurstia sp., Zosterophyllum sp., Distichophytum sp., Aff. Zosterophyllum sp. A, Macivera gracilis [74] (Figure4). The only plant from North Greenland is Salopella sp. [75]. Gener- ally, this plant assemblage can be characterized as a zosterophyll-dominated flora with minor rhyniophytes.

3.2.2. South Laurussian–Northwest Gondwanan Unit This unit includes territories from approximately 18◦ S palaeolatitude to 60–75◦ S palaeolatitude [75] and was probably a part of the temperate climatic zone (Figure2). The fossil record of this palaeophytogeographical unit ranges from early Wenlock (Sheinwood- ian) to Pˇrídolí. Life 2021, 11, 906 6 of 22 Life 2021, 11, x FOR PEER REVIEW 6 of 22

FigureFigure 2. 2.Silurian Silurian palaeocontinental palaeocontinental reconstructions reconstructions according according to to Scotese Scotese [76 [76]] plotting plotting palaeogeo- palaeogeo- graphical distribution of plants (rectangle) or plant assemblages (circle). Colored ellipses represent graphical distribution of plants (rectangle) or plant assemblages (circle). Colored ellipses represent individual phytogeographic units according to Raymond et al. [48]; W = Wenlock, L = Ludlow, P = individual phytogeographic units according to Raymond et al. [48]; W = Wenlock, L = Ludlow, Přídolí. P = Pˇrídolí.

NorthwestNorthwest Gondwana Gondwana NorthwestNorthwest Gondwana Gondwana (peri-Gondwana) (peri-Gondwana) provides prov theides oldest the oldest true vascular true vascular land plants, land Cooksoniaplants, Cooksonia barrandei andbarrandeiCooksonia and Cooksoniasp. (Figure sp.5), (Figure from the 5), Czech from Republicthe Czech (Barrandian Republic (Barran- area, thedian Prague area, Basin) the Prague [77,78 ].Basin) These [77,78]. globally These important globally specimens important come specimens from the comeMonograptus from the belophorusMonograptusBiozone belophorus of the Biozone Sheinwoodian of the Sheinwoodian Age. Sheinwoodian Age. Sheinwoodian localities of the localities Barrandian of the areaBarrandian yielded severalarea yielded unpublished several unpublished early land plants early land of different plants of affinities different (rhyniophytes, affinities (rhyn- probablyiophytes, zosterophylls, probably zosterophylls, cryptosporophytes) cryptosporop [77–80hytes)]. Current [77–80]. research Current suggests research that suggests cook- sonioidthat cooksonioid dominated dominated plant assemblages plant assemblages were accompanied were accompanied by Ascomycota by [Ascomycota81], Prototaxites [81], sp.,Prototaxites and enigmatic sp., andPachytheca enigmatic[82 ].Pachytheca Libertín et[82]. al. [Libertín83] also recordedet al.[83] Cooksoniaalso recordedsp. from Cooksonia the samesp. from geographic the same area geographic but from the area stratigraphically but from the stratigraphically younger Cyrtograptus younger rigidus CyrtograptusBiozone (Figurerigidus3 —Wa).Biozone Generally, (Figure 3—Wa). the latter Generally, assemblage the (Figurelatter assemblage3—W1 plus (Figure Wa) is characterized3—W1 plus Wa) byis relatively characterized rich vegetationby relatively cover rich of vegetation the temperate cover zone of the of thetemperate Southern zone hemisphere. of the Southern The otherhemisphere. probable The plants, other such prob asablePrototaxites plants, sp.such (Figure as Prototaxites6e,f), Pachytheca sp. (Figuresp.(Figure 6e, f), 6Pachythecaa,b), cf. Cosmochlainasp. (Figure 6a,(Figure b), cf.6d), Cosmochlaina and cf. Nematasketum (Figure 6d),(Figure and cf.6 Nematasketumc) belong to relatively (Figure 6c) abundant belong to fossilsrelatively in the abundant Homerian fossils interval. in the Homerian interval. TheThe relatively relatively rich rich plant plant assemblage assemblage from from the the Barrandian Barrandian area area (the (the Prague Prague Basin) Basin) comescomes from from Pˇr ídolPřídolíí strata strata (Figure (Figure2—P9, 2—P9, Pb). Mineral Pb). Mineral nutrient-rich nutrient-rich volcanic islandsvolcanic formed islands fromformed late Wenlock–earlyfrom late Wenlock–early Ludlow Kosov Ludlow and Kosov Svatý Janand volcanic Svatý Jan centres volcanic could centres have could provided have

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provided suitable conditions for terrestrialization of early land plants [38,82,84,85]. Plants suitablefrom the conditions Skalograptus for parultimus-Skalograptus terrestrialization of early ultimus land Biozone plants interval [38,82,84 (Figure,85]. Plants 3—P9) from in- thecludeSkalograptus Cooksonia parultimus-Skalograptussp. (Figure 7f), Cooksoniaultimus cf. hemisphaericaBiozone interval(Figure 7a), (Figure Aberlemnia3—P9) bohemica include Cooksonia(Figure 7e),sp. Fusiformitheca (Figure7f), sp.Cooksonia (Figure 7d),cf. andhemisphaerica Tichavekia (Figuregrandis 7(Figurea), Aberlemnia 7c) [38,86,87]. bohemica Not (Figureonly fertile7e), Fusiformitheca but also abundantsp. (Figure sterile7 axiald), and partsTichavekia of Cooksonia grandis affinity(Figure are7c) reported [ 38,86, 87[82,88].]. Not onlyOccurrence fertile but of the also basal abundant lycophyte sterile Baragwanathia axial parts ofbrevifoliaCooksonia (Figureaffinity 7b) are[43]reported from Skalograp- [82,88]. Occurrencetus ultimus ofBiozone the basal is unique, lycophyte representingBaragwanathia the brevifoliasingle finding(Figure of7 b)a lycophyte [ 43] from withSkalograptus differ- ultimusentiatedBiozone microphylls is unique, standing representing out among the single other findingSilurian of plants a lycophyte of the with Barrandian differentiated area, microphyllswhich, in contrast, standing exhibit out amongancient otherrhyniophytoid Silurian plants characters. of the Barrandian area, which, in contrast, exhibit ancient rhyniophytoid characters.

FigureFigure 3. 3. StratigraphicalStratigraphical distribution distribution of of plants plants or orplant plant asse assemblagesmblages from from the Wenlock the Wenlock (W) through (W) through Ludlow Ludlow (L) to P (L)řídolí to Pˇr(P).ídol Quantitativeí (P). Quantitative curves curves of cryptospores of cryptospores (see Figure (see Figure 8) and8) isotopic and isotopic temper temperatureature curves curves (see Figure (see Figure 1) put1) together. put together. The circle at the end of the connecting line between the assemblage/plant unit and stratigraphy levels indicates the accuracy The circle at the end of the connecting line between the assemblage/plant unit and stratigraphy levels indicates the of the stratigraphic determination-the more right this point is, the more accurate the determination. Assemblages: W1 = accuracy of the stratigraphic determination-the more right this point is, the more accurate the determination. Assemblages: Barrandian area, the Prague Basin, Czechia [77–80]; W2 = Souther Bolivia [89]; W3 = Gasport Stone Quarry, Niagara W1County, = Barrandian New York area, State, the Prague USA [90]; Basin, L1 Czechia= Welsh [ 77Basin–80]; (Cwm W2 = Craig Souther Ddu, Bolivia Powys) [89]; [91]; W3 =L2 Gasport = Welsh Stone Basin Quarry, (Capel NiagaraHoreb, County,Powys) New [90]; YorkL3 = State,Bathurst USA Island, [90]; L1Arctic = Welsh Canada Basin [74]; (Cwm L4 = Victoria, Craig Ddu, Australia, Powys) Centennial [91]; L2 = Beds Welsh [42,92]; Basin (CapelL5 = Victoria, Horeb, Powys)Australia, [90]; Monograptus L3 = Bathurst Beds Island, [42,92]; Arctic L6 = Tarija, Canada southern [74]; L4 Bolivia = Victoria, [93]; L7 Australia, = Gotland, Centennial Sweden [94]; Beds P1 [=42 Anglo-Welsh,92]; L5 = Victoria, Basin Australia,(LudfordMonograptus Corner, Ludlow)Beds [95]; [42 ,P292]; = L6Anglo-Welsh = Tarija, southern Basin (Per Boliviaton Lane, [93 ];Hereford) L7 = Gotland, [96–98]; Sweden P3 = Anglo-Welsh [94]; P1 = Anglo-WelshBasin (Fresh- Basinwater (Ludford East, Pembrokeshire) Corner, Ludlow) [99]; [ 95P4]; = P2Anglo-Welsh = Anglo-Welsh Basin Basin (Capel (Perton Horeb, Lane, Powys) Hereford) [91]; P5 [=96 New–98]; York P3 = State, Anglo-Welsh USA [90]; Basin P6 = (FreshwaterOntario, Canada East, Pembrokeshire) [90]; P7 = Holy [Cross99]; P4 Mts., = Anglo-Welsh Poland [100]; Basin P8 = (Capel Podolia, Horeb, Ukraine Powys) [101]; [91 P9]; P5= Barrandian = New York area, State, the USA Prague [90]; Basin, Czechia [38,43]; P10 = Kazakhstan [45]; P11 = Kazakhstan, Balkhash area [102,103]; P12 = Junggar Basin, Xinjiang, P6 = Ontario, Canada [90]; P7 = Holy Cross Mts., Poland [100]; P8 = Podolia, Ukraine [101]; P9 = Barrandian area, the China [104]; P13 = Northern Vietnam [105]; Isolated finding of plants: Wa = Barrandian area, the Prague Basin, Czechia Prague Basin, Czechia [38,43]; P10 = Kazakhstan [45]; P11 = Kazakhstan, Balkhash area [102,103]; P12 = Junggar Basin, [83]; Wb = Tipperary, Ireland [106]; La = Northern Greenland [75]; Lb = Bathurst Island, Arctic Canada [74]; Lc = Bathurst Xinjiang,Island, Arctic China Canada [104]; P13 [74]; = Pa Northern = Anglo- VietnamWelsh Basin [105 ];(LittleIsolated Wallop finding Hall, of Shropshire plants: Wa) [107]; = Barrandian Pb = Barrandien area, the area, Prague the Prague Basin, CzechiaBasin, Czechia [83]; Wb [82]; = Tipperary, Pc = Homra Ireland Basin, [Libya106]; [108]; La = NorthernPd = Yunan, Greenland China [50]; [75 Pe]; Lb= Junggar = Bathurst Basin, Island, Xinjiang, Arctic China Canada [104]; Pf [74 =]; LcShropshire, = Bathurst UK Island, [7]. Arctic Canada [74]; Pa = Anglo-Welsh Basin (Little Wallop Hall, Shropshire) [107]; Pb = Barrandien area, the Prague Basin, Czechia [82]; Pc = Homra Basin, Libya [108]; Pd = Yunan, China [50]; Pe = Junggar Basin, Xinjiang, China [104]; Pf = Shropshire, UK [7].

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Sterile rhyniophytes were described from the Late Wenlock/Ludlow strata of south- Sterile rhyniophytes were described from the Late Wenlock/Ludlow strata of south- ern Bolivia [89] (Figure3—W2). Stratigraphically younger specimens from the Lipe ón ern Bolivia [89] (Figure 3—W2). Stratigraphically younger specimens from the Lipeón For- Formation at Tarija of Ludlow age yielded cf. Aberlemnia caledonica, sterile axes assigned mation at Tarija of Ludlow age yielded cf. Aberlemnia caledonica, sterile axes assigned to to the genus Hostinella, and isolated sporangia determined based on their morphology the genus Hostinella, and isolated sporangia determined based on their morphology as cf. as cf. Cooksonia hemisphaerica, cf. Tarrantia and isolated sporangia [93] (Figure3—L6). Cooksonia hemisphaerica, cf. Tarrantia and isolated sporangia [93] (Figure 3—L6). One of the One of the best-preserved specimens of cf. Aberlemnia caledonica was earlier published by best-preserved specimens of cf. Aberlemnia caledonica was earlier published by Morel et al. Morel et al. [109]. [109]. Daber [108] described the uppermost Pˇrídolí flora from Libya (Figure2—Pc), including Daber [108] described the uppermost Přídolí flora from Libya (Figure 2—Pc), includ- Cooksonia sp. This area was situated near the northern edge of the Gondwana mainland, ing Cooksonia sp. This area was situated near the northern edge of the Gondwana main- far south of the Barrandian area (the Prague Basin) during Pˇrídolí times. land, far south of the Barrandian area (the Prague Basin) during Přídolí times.

Figure 4. Tropical flora assemblage from Bathurst Island, Canada. (a) cf. Bathurstia, US—US600- Figure6791, scale 4. Tropical bar = flora5 mm; assemblage (b) Distichophytum from Bathurst sp. US—US600-8144, Island, Canada. (ascale) cf. Bathurstiabar = 10 mm;, US—US600-6791, (c) aff. Zostero- scalephyllum bar =sp. 5 mm;A, US—US688-8152, (b) Distichophytum scalesp. bar US—US600-8144, = 5 mm; (d) Macivera scale bargracilis = 10, US—US385-2398, mm; (c) aff. Zosterophyllum scale bar = sp.10 A,mm; US—US688-8152, (e) Zosterophyllum scale sp., bar US—US384-8137, = 5 mm; (d) Macivera scale gracilisbar = 5, US—US385-2398,mm. Used with the scale permission bar = 10 of mm; the (eauthors) Zosterophyllum [74]. sp., US—US384-8137, scale bar = 5 mm. Used with the permission of the au- thors [74]. South Laurussia SouthThe Laurussia South Laurussian unit includes basins located in southwest Laurussia, situated approximatelyThe South Laurussian30° south latitude unit includes [76], and basins belonging located to intemperate southwest zone Laurussia, (Figure 2). situated One of ◦ approximatelythose basins, the 30 classicsouth latitudeWelsh Basin, [76], and UK, belonging has a sedimentological to temperate zone record (Figure ranging2). One from ofCambrian those basins, to Early the classicDevonian. Welsh Rhyniophytoids Basin, UK, has are a sedimentological the only plants reported record ranging from the from Late CambrianSilurian and to Early Early Devonian. Devonian Rhyniophytoidsof this area. The are oldest the only polysporangiophyte, plants reported from Cooksonia the Late sp. Silurian(Figure and3—Wb) Early from Devonian Homerian of thisstrata area. of the The Tipperary oldest polysporangiophyte, County (Ireland) of Laurussia,Cooksonia wassp. (Figuredescribed3—Wb) by Edwards from Homerian et al. [106]. strata This of the area Tipperary was located County probably (Ireland) c. 25° of Laurussia,S palaeolatitude was ◦ described[76]. It is not by Edwardspossible to et speculate al. [106]. about This areathe general was located character probably of this c. vegetation 25 S palaeolati- because tudeonly [one76]. species It is not has possible been recorded. to speculate about the general character of this vegetation becauseGorstian only one assemblages species has from been the recorded. Welsh-Basin probably belonging to the same phyto- geographicalGorstian assemblagesunit are known from from the the Welsh-Basin Anglo-Welsh probably Basin, belonging UK [91] (Figure to the same2—L1). phyto- They geographicalare typified by unit rhyniophytoid-dominated are known from the Anglo-Welsh vegetation Basin, with Cooksonia UK [91] (Figure sp., cf.2 Cooksonia—L1). They cam- arebrensis typified, Cooksonia by rhyniophytoid-dominated pertoni and sterile axes of vegetationHostinella (Figure with Cooksonia 3—L1). sp., cf. Cooksonia cambrensis, Cooksonia pertoni and sterile axes of Hostinella (Figure3—L1). Freshwater East in Pembrokeshire is a famous locality in the Welsh Basin (Figure 3— P3) that yielded a rich plant assemblage of the Přídolí age. Cooksonia and sterile axes of

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Freshwater East in Pembrokeshire is a famous locality in the Welsh Basin (Figure3 —P3) that yieldedHostinella a rich were plant described assemblage by Edwards of the Pˇrídol [99],í age. includingCooksonia a species,and sterile Cooksonia axes of Hostinellacambrensiswere, and describedthe rhyniophytoid by Edwards Tortilicaulis [99], including transwalliensis a species,, Cooksoniaresembling cambrensis sporophytes, and theof some rhyniophytoid recent liv- Tortilicauliserworts. transwalliensis, resembling sporophytes of some recent liverworts. AA new new rhyniophytoid-like rhyniophytoid-like species, species,Caia Caia langii, langii,was was described described from from Perton Perton Lane, Lane, UK [96 UK] (Figure[96] (Figure3—P2), 3—P2), which which is the is original the original locality locality for forCooksonia Cooksonia pertoni pertoni[110 [110].]. Another Another plant plant fromfrom the the same same locality, locality,Pertonella Pertonella dativelethra, dativelethra,is is characterized characterized by by distinctive distinctive sporangial sporangial projectionsprojections [ 97[97].]. The other pl plantsants from from this this site site are are CooksoniaCooksonia cambrensis cambrensis andand SalopellaSalopella sp. sp.[98]. [98 ]. LudfordLudford Corner, Corner, UK UK yielded yielded exceptionally exceptionally preserved preserved plants plants (Figure (Figure3—P1). 3—P1). Capel Capel HorebHoreb in in Wales,Wales, UK (Figure (Figure 33—P4)—P4) is is another another lo localitycality ofof the the Welsh Welsh Basin Basin typified typified by coali- by coalifiedfied plant plant adpressions adpressions [91], [ 91such], such as Steganotheca as Steganotheca andand sterile sterile axes axes of Hostinella of Hostinella. Rogerson. Roger- et sonal. [107] et al. described [107] described CooksoniaCooksonia pertoni from pertoni Littlefrom Wallop Little Hall Wallop in Shropshire, Hall in Shropshire, UK (Figure UK 3— (FigurePa). Similar3 —Pa). flora Similar is known flora is from known Ontario, from Ontario, Canada Canada (Figure (Figure 3—P6)3—P6) and New and New York, York, USA USA(Figure (Figure 3—P5).3—P5). The Thepolysporangiophytes polysporangiophytes from fromCanada Canada and New and York New as York coalified as coalified adpres- adpressionssions are preserved are preserved in fine-grained in fine-grained dolomite dolomite [90]. This [90 area]. This was area located was at located the southeast- at the ◦ southeasternern edge of edgethe Laurussia of the Laurussia palaeocontinent, palaeocontinent, approximately approximately 40°south 40 lasouthtitude latitude [76] during [76] duringPřídolí. Pˇr Theídol researchí. The research was concentrated was concentrated on six localities, on six localities, of which of Cooksonia which Cooksonia sp., Cooksoniasp., Cooksoniacf. hemisphaericacf. hemisphaerica, and sterile, and axes sterile assigned axes assigned to Hostinella to Hostinella have beenhave recorded. been recorded.

Figure 5. Plant fossils from the South Laurussian–Northwest Gondwanan unit (temperate zone), Figure 5. Plant fossils from the South Laurussian–Northwest Gondwanan unit (temperate zone), Wenlock, Scheinwoodian, Barrandian area (the Prague Basin), Czechia; (a) Cooksonia barrandei, spec- Wenlock,imen D-552b, Scheinwoodian, NM, Špičatý Barrandian vrch-Barrandovy area (the Jámy; Prague (b Basin),) Cooksonia Czechia; sp. PCC (a) Cooksonia (notice—will barrandei be a, speci-part of mencollection D-552b, of NM,NM), Špiˇcat Špičatýý vrch-Barrandovy vrch-Barrandovy J áJámy;my; (bscale) Cooksonia bar for bothsp. PCC specimens (notice—will = 5 mm. be a part of collection of NM), Špiˇcatý vrch-Barrandovy Jámy; scale bar for both specimens = 5 mm. Poland (eastern Laurussia) belonged to the South Laurussian–Northwest Gond- Poland (eastern Laurussia) belonged to the South Laurussian–Northwest Gondwanan wanan unit (Figure 3—P7) at approximately◦ 20° south latitude [76]. Bodzioch et al. [100] unitpublished (Figure 3specimens—P7) at approximately from early Př 20ídolísouth and assigned latitude [ them76]. Bodzioch to rhyniophytoids. et al. [100] publishedSpecimens specimenscome from from the Holy early Cross Pˇrídol Mountainsí and assigned (Poland), them including to rhyniophytoids. fertile Cooksonia Specimens sp. andcome sterile Cooksonia fromaxes thedescribed Holy Cross as Hostinella Mountains. (Poland), including fertile sp. and sterile axes described as Hostinella. Ishchenko [101] described an assemblage from the Přídolí dominated by rhyniophy- Ishchenko [101] described an assemblage from the Pˇrídolí dominated by rhyniophy- toids including Cooksonia pertoni and C. hemisphaerica from Podolia (Ukraine). This area is toids including Cooksonia pertoni and C. hemisphaerica from Podolia (Ukraine). This area is typical for warm zones from the same latitude such as the Polish localities [100]. Unlike Poland Zosterophyllum sp., Lycopodolica, and Eorhynia (Salopella) are reported.

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typical for warm zones from the same latitude such as the Polish localities [100]. Unlike Poland Zosterophyllum sp., Lycopodolica, and Eorhynia (Salopella) are reported. WenlockianWenlockian sterile sterile branched branched axes axes were were reported reported from from the the Gasport Gasport Stone Stone Quarry, Quarry, Nia- Ni- garaagara County, County, (New (New York, York, USA) USA) [90 [90]] (Figure (Figure2—W3). 2—W3). The The section section belongs belongs to to the the graptolite graptolite zonezone of ofMedusaegraptus Medusaegraptus—a—a graptolite graptolite taxon taxon that that is also is also recognized recognized in the in upper the upper Sheinwood- Shein- ianwoodian to lower to Homerianlower Homerian of the Barrandianof the Barrandian region region of the Pragueof the Prague Basin (FigureBasin (Figure3—W3). 3—W3). EdwardsEdwards and and Rogerson Rogerson [ 91[91]] published published the the Ludfordian Ludfordian rhyniophytoid-dominated rhyniophytoid-dominated vegetationvegetation from from Capel Capel Horeb Horeb of of the the Welsh Welsh Basin, Basin, UK UK (Figure (Figure3—L2), 3—L2), including includingCooksonia Cooksonia sp.sp. and andSteganotheca Steganotheca striata striata. .

3.2.3.3.2.3. Kazakhstanian Kazakhstanian Unit Unit ThisThis unit unit was was located located north north of of the the palaeoequator palaeoequator (Figure (Figure1) 1) and and its its vegetation vegetation belongs belongs toto the the subtropical subtropical zone. zone. Two Two sites sites yielded yielded plants, plants, as as seen seen on on Figures Figures2 and2 and3—P10, 3—P10, P11, P11, andand correspond correspond with with the the stratigraphical stratigraphical interval interval of of the theSkalograptus Skalograptus boucek boucek –Skalograptus –Skalograptus transgredienstransgrediensgraptolite graptolite biozones. biozones.The The Kazakhstanian Kazakhstanian unit unit was was situated situated on on the the northern northern hemispherehemisphere in in the the subequatorial subequatorial zone zone of of the the Palaeo-Tethys Palaeo-Tethys Ocean Ocean [76 [76].]. The The assemblage assemblage includesincludes the the genera genera previously previously reported reported by by Edwards Edwards and and Wellman Wellman [45 [45].]. Other Other specimens specimens describeddescribed from from the the Balcan Balcan area area are areCooksonella Cooksonella sphaerica sphaerica, Baragwanathia, Baragwanathiasp., sp.,Taeniocrada ?Taeniocradasp., andsp.,Jugumella and Jugumella burubaensis burubaensis[102,103 [102,103].].

Figure 6. Plant assemblage from the South Laurussian–Northwest Gondwanan unit (temperate Figure 6. Plant assemblage from the South Laurussian–Northwest Gondwanan unit (temperate zone) known from the Homerian of the Barrandian area, the Prague Basin (parvus-nassa Biozone); zone) known from the Homerian of the Barrandian area, the Prague Basin (parvus-nassa Biozone); (a) Pachytheca showing differentiated medulla (inner) and cortex (outer par), scale bar = 500 µm; (b) µ (aCortical) Pachytheca fragmentshowing of Pachytheca differentiated in detail medulla composed (inner) of densely and cortex spac (outered radial par), tubes, scale scale bar bar = 500 = 20 µm;m; (b()c) Cortical Non-embryophyte fragment of plantPachytheca cf. Nematasketumin detail composedshowing unevenly of densely thickened spaced tubes, radial SEM-rack tubes, scale SILI-A1, bar =scale 20 µ m;bar ( c=) 200 Non-embryophyte µm; (d) Cf. Cosmochlaina plant cf. showingNematasketum outer coveringshowing layer unevenly being thickened partly perforated, tubes, SEM- scale rackbar SILI-A1,= 200 µm; scale (e) Varying bar = 200 diameterµm; (d )of Cf. tubesCosmochlaina of Prototaxitesshowing, scale outer bar = covering100 µm; ( layerf) Detail being of tubes partly of perforated,Prototaxites scale, scale bar bar = =200 20 µm.µm; All (e) specimen Varying diameters were observed of tubes under of Prototaxites SEM. , scale bar = 100 µm; (f) Detail of tubes of Prototaxites, scale bar = 20 µm. All specimens were observed under SEM.

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Figure 7. Plant assemblage from the South Laurussian–Northwest Gondwanan unit (temperate Figure 7. Plant assemblage from the South Laurussian–Northwest Gondwanan unit (temperate zone) zone) from Přídolí (S. parultimus-S. ultimus Biozone) of the Barrandian area, the Prague Basin, fromCzechia; Pˇrídol (aí)( CooksoniaS. parultimus-S. cf. hemisphaerica ultimus Biozone), specimen of theof NM—D-475, Barrandian area,Kosov the Quarry; Prague (b Basin,) Baragwanathia Czechia; (abrevifolia) Cooksonia, specimencf. hemisphaerica of CGS—KR, specimen 1, Karlštejn of NM—D-475, locality; (c) Kosov Tichavekia Quarry; grandis (b),Baragwanathia specimen of WBM— brevifolia, specimenF21761a, of Kosov CGS—KR Quarry; 1, Karlštejn (d) Cf. Fusiformitheca locality; (c) Tichavekia sp., specimen grandis of, specimenWBM—F21762, of WBM—F21761a, Kosov Quarry; Kosov (e) Quarry;Aberlemnia (d) Cf. bohemicaFusiformitheca, specimensp., of specimen SMNH—JE-Sch0260B of WBM—F21762,, Dlouhá Kosov Hora Quarry; locality (e) Aberlemnia; (f) Cooksonia bohemica sp., , specimenspecimen of of SMNH—JE-Sch0260B, FSCU, Kosov Quarry. Dlouh All scalesá Hora 10 locality; mm. (f) Cooksonia sp., specimen of FSCU, Kosov Quarry. All scales 10 mm. 3.2.4. Northeast Gondwanan Unit 3.2.4. NortheastThis palaeophytogeographical Gondwanan Unit unit includes Northeast Gondwana (Figure 2) and wasThis probably palaeophytogeographical situated as a transition unit between includes the Northeast tropical-subtropical Gondwana (Figurezones, 2between) and was10°–15°south probably situatedlatitude as[76]. a transitionSimilar vegetation between theis reported tropical-subtropical from Yunnan zones, (Figure between 2—Pd), 10Xinjiang◦–15◦south (Figure latitude 2—P12, [76]. Pe) Similar (both China) vegetation [50,104], is reported and Vietnam from Yunnan (Figure (Figure2—P13)2 [105].—Pd), XinjiangRich (Figure Ludfordian2—P12, assemblage Pe) (both China) flora [were50,104 described], and Vietnam from (FigureVictoria,2—P13) Australia [105 ].[42,92], situatedRich Ludfordianin the tropical assemblage zone of floraeastern were Gondwana described from(approximately Victoria, Australia 10° S) [[76].42,92 Two], situated strati- ◦ ingraphical the tropical levels zone with of eastern plants Gondwana were recognised, (approximately 1) Stratigraphically 10 S) [76]. Two older stratigraphical Monograptus levels Beds withwith plants seven were plant recognised, taxa (Figure (1) Stratigraphically 3—L5), and 2) th oldere LateMonograptus CentennialBeds Beds with with seven four plant taxa taxa (Fig- (Figureure 3—L4).3—L5), Rhyniophytes and (2) the Late dominated Centennial and Beds zo withsterophylls four taxa were ( Figure common.3 —L4). The Rhyniophytes assemblage dominatedincludes the and enigmatic zosterophylls lycopsid werecommon. Baragwanathia The assemblage longifolia and includes an undescribed the enigmatic lycophyte- lycopsid Baragwanathialike endemic longifolia plant [42,111].and an undescribed lycophyte-like endemic plant [42,111]. TheThe Yunnan Yunnan and and Xinjiang Xinjiang provinces provinces of of China China yielded yielded a a zosterophyll-dominated zosterophyll-dominated flora flora ofof Pˇr Pířdolídolíí age age (Figure (Figure3—Pd, 3—Pd, P12, P12, Pe) Pe) with with e.g., e.g.,Zosterophyllum Zosterophyllum qujingense qujingense[50 [50].]. Dou Dou and and SunSun [112 [112]] and and Cai Cai et et al. al. [ 104[104]] described describedZosterophyllum Zosterophyllumsp., sp.,Sciadophyton Sciadophyton pristinum pristinum, Salopella, Salopella xinjiangensisxinjiangensis, Cooksonella, Cooksonella(Junggaria (Junggaria) sphaerica) sphaerica, Hostinella, Hostinella, Psilophytites, Psilophytites, Parka, Parkaand and lycophyte- lycophyte- likelike plants plants from from Xinjinang, Xinjinang, north north China. China. Gonez Gonez et et al. al. [105 [105]] published published a a plant plant assemblage assemblage fromfrom the the Van Van Canh Canh Formation, Formation, Vietnam Vietnam (Figure (Figure3—P13), 3—P13), which which may may belong belong to to Pˇr Pířdolídolí,í, probablyprobablybouceki—transgrendies bouceki—transgrendiesbiozones biozones and and mentioned mentioned unbranched unbranched axes, axes, cf. cf.Sporogonites Sporogonites yunnanense, cf. Aberlemnia, cf. Filiformorama, and zosterophylls. The locality is close to other yunnanense, cf. Aberlemnia, cf. Filiformorama, and zosterophylls.◦ The locality is close to Chineseother Chinese Silurian Silurian assemblages assemblages situated situated approximately approximately 20 south 20°south latitude latitude [76] on the[76] South on the China Plate. South China Plate.

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3.3. Palynological Aspects of Early Land Plants The combination of the dispersed spore and plant megafossil records is necessary for research into the history of land plants, including the early ones [7,113,114]. Reconstruc- tions of palaeoenvironmental conditions within the Silurian are based mainly on the ma- rine fossil record. Dispersed spores, however, also occurring mainly in near-shore marine sediments, can also be a significant independent factor for successful reconstructions of Life 2021, 11, x FOR PEER REVIEWLife 2021 , 11, x FOR PEER REVIEW 12 of 22 12 of 22 contemporaneous palaeoenvironments on adjacent palaeocontinents. Indirect palynolog- ical evidence of the plant record is available most commonly in the form of spores dis- Life 2021, 11, 906 persed in the rock record,12 of and 22 only sometimes in situ, i.e., spores isolated directly from 3.3. Palynological Aspects3.3. of Early Palynological Land Plants Aspects of Early Land Plants the reproductive organs of plants. The megafossil record of Silurian plants is limited and The combination of the Thedispersed combination spore and of the plant dispersed megafossil spore records and plant is necessary megafossilincomplete for records compared is necessary to that for of their spores. Spores have a much higher preservational research into the historyresearch of land intoplants, the includinghistory of theland early plants, ones including [7,113,114]. the Reconstruc- earlypotential ones [7,113,114]. than other Reconstruc- plant tissues due to their size and the occurrence of sporopollenin in tions of palaeoenvironmental3.3.tions Palynological of conditions palaeoenvironmental Aspects within of Earlythe Silurian Landconditions Plants are basedwithin mainly the Silurian on theirthe are ma- exines based thatmainly effectively on the ma-protects them against degradation and, thus, leads to better rine fossil record. DispersedrineThe fossil spores, combination record. however, Dispersed of also the occurring dispersed spores, however, mainly spore and in also near-shore plant occurring megafossilfossilization. marine mainly records in near-shoreThere is necessaryis a very marine low preservational potential for plants without mineralized sediments, can also befor asediments, researchsignificant into can independ thealso history beent a significant factor of land for plants, independsuccessful includingent reconstructions factor the for earlymechanical successful ones of [7 tissues,113 reconstructions,114 [115,116].]. Recon- Therefore,of the first evidence for land plants is in the form of contemporaneous palaeoenvironmstructionscontemporaneous of palaeoenvironmentalents on palaeoenvironm adjacent palaeocont conditionsents inents.on adjacent within Indirect the palaeocont Silurianpalynolog-dispersedinents. are based spores Indirect mainly with palynolog- ona resistant the sporopollenin wall [117,118]. Two other palaeobotani- ical evidence of the plantmarineical record evidence fossil is record. available of the Dispersed plant most record commonly spores, is available however, in the mostform also occurringcommonlyof sporescally mainlydis- veryin the important inform near-shore of sporesaspects ma- dis- of spores are, first, their production in enormous numbers by persed in the rock record,rinepersed sediments, and inonly the sometimes canrock also record, be in a significantandsitu, only i.e., sporessometimes independent isolated in factorsitu, directly i.e., forhomosporous spores successfulfrom isolated reconstructionsplants, directly and fromsecond, their great dispersal potential over long distances by the reproductive organsofthe contemporaneous of reproductiveplants. The megafoss organs palaeoenvironments ofil recordplants. of The Silurian megafoss on adjacent plantsil record is palaeocontinents. limited ofwater, Silurian and but mainlyplants Indirect is by limited palyno-wind. andThe optimum size for wind dispersal is 25 µm or less accord- incomplete comparedlogical toincomplete that evidence of their compared spores of the. plant Sporesto that record haveof their isa availablemuchspores higher. Spores most preservational commonlyhaveing a muchto Mogensen in higher the form preservational [119], of spores which corresponds to the diameter of the majority of isospores potential than other plantdispersedpotential tissues in than due the rocktoother their record, plant size tissuesandand onlythe due occurrence sometimes to their sizeof in sporopollenin situ,and i.e.,theproduced sporesoccurrence in isolated by of early sporopollenin directly land plants from in (usually 20–40 µm) [120,121]. the reproductive organs of plants. The megafossil record of Silurian plants is limited and their exines that effectivelytheir protectsexines that them effectively against degradation protects them and, against thus, degradationleads to betterCryptospores and, thus, leads sensu to Stemansbetter [122] appeared earlier than true trilete spores [16]. Their incomplete compared to that of their spores. Spores have a much higher preservational fossilization. There is a fossilization.very low preservational There is a very potential low preservational for plants without potential mineralized producers/parentfor plants without plants mineralized “cryptosporophytes” [7] are a heterogeneous group of different potential than other plant tissues due to their size and the occurrence of sporopollenin in mechanical tissues [115,116].mechanical Therefore, tissues the [115,116]. first evidence Therefore, for land the plants first evidence is in the plantforform land types.of plants It is is possible in the form to recognize of several types of cryptospores, including enveloped their exines that effectively protects them against degradation and, thus, leads to better dispersed spores with adispersed resistant sporessporopolle withnin a resistantwall [117,118]. sporopolle Twonin other wall palaeobotani- [117,118].enclosed Two monads, other palaeobotani- dyads, and tetrads, naked monads, dyads, and tetrads (Table 1). A large fossilization. There is a very low preservational potential for plants without mineralized cally very important aspectscally ofvery spores important are, first, aspects their ofproduction spores are, in fi enormousrst, their production numbersnumber by in ofenormous dispersed numbers trilete sporesby in the fossil record reflect the strategy of the earliest homosporous plants,mechanical andhomosporous second, tissues their plants, [great115, 116and di].spersal second, Therefore, potential their the great first over evidencedi longspersal distances forpotential land by plants over islong in the distances form of by dispersed spores with a resistant sporopollenin wall [117,118].plants, Two other which palaeobotanically were isosporic, resulting in efficient spreading. Additionally, their abun- water, but mainly by wind.water, The but optimum mainly bysize wind. for wind The optimumdispersal issize 25 forµm wind or less dispersaldance accord- in is 25the µm fossil or less record accord- significantly exceeds the abundance of the parent plant ing to Mogensen [119],verying which important to Mogensen corresponds aspects [119], to of the sporeswhich diameter are,corresponds first, of the their majorityto production the diameter of isospores in enormousof the majority numbers of isospores by ho- mosporous plants, and second, their great dispersal potentialmacrofossils over long distances [48]. by water, produced by early land producedplants (usually by early 20–40 land µm) plants [120,121]. (usually 20–40 µm) [120,121]. but mainly by wind. The optimum size for wind dispersal is 25 µm or less according to Table 1. Quantitative occurrence of main types of cryptospores, hilate spores and true trilete spores from Llandovery to Cryptospores sensuMogensen StemansCryptospores [119 [122]], which appeared sensu corresponds Stemans earlier than to[122] the true appeared diameter trilete spores ea ofrlier the [16]. majoritythan Their true of trilete isospores spores produced [16]. Their Přídolí. producers/parent plantsbyproducers/parent early“cryptosporophytes” land plants (usuallyplants [7] “cryptosporophytes” are 20–40 a heterogeneousµm) [120,121]. [7] group are aof heterogeneous different group of different plant types. It is possibleplant toCryptospores recognize types. It isseveral sensupossible types Stemans to recognizeof cryptospores, [122] appeared several including types earlier ofEnvelope thancryptospores, enveloped true trileteEnvelope including spores [Envelope16 enveloped]. Their enclosed monads, dyads,enclosed and tetrads, monads, naked dyads, monads, and tetrads,dyads, and naked tetrads monads, (Table dyads, 1). A andlarge tetrads (Table 1). A large Naked Naked Dy-Naked Tet- Hilate Trilete producers/parent plants “cryptosporophytes”Age [7] are aEnclosed heterogeneous Enclosed group ofEnclosed different number of dispersed triletenumber spores of dispersed in the fossil trilete record spores reflect in thethe fossilstrategy record of the reflect earliest the strategy of the earliest Monads ads rads Spores Spores plant types. It is possible to recognize several types of cryptospores,Monads includingDyads envelopedTetrad plants, which were isosporic,plants, resultingwhich were in efficientisosporic, spreading. resulting Additionally,in efficient spreading. their abun- Additionally, their abun- enclosed monads, dyads, and tetrads, naked monads, dyads,█and tetrads█ (Table 1). A█ large ██ █ █ ███ ███ dance in the fossil numberrecorddance significantly ofin dispersedthe fossil exceeds trilete record spores thesignificantly abundance in thePřídolí fossil exceeds of record the theparent reflect abundance theplant strategy of the of theparent earliest plant █ █ █ ██ █ █ ███ ███ macrofossils [48]. plants,macrofossils which were [48]. isosporic, resulting in efficient spreading. Additionally, their abundance █ █ █ ██ █ █ ██ ██ in the fossil record significantly exceedsLudlow the abundance of the parent plant macrofossils [48]. Table 1. Quantitative occurrenceTable 1. of Quantitative main types ofoccurrence cryptospores, of main hilate types spores of cryptospores, and true trilete hilate spores spores from and Llandovery true trilete█ to spores from█ Llandovery█ to ██ █ █ ██ ██ Přídolí. TablePřídolí. 1. Quantitative occurrence of main types of cryptospores, hilate spores and true trilete█ spores from█ Llandovery█ █ ██ ██ ██ ██ Wenlock Envelopeto Pˇrídolí . Envelope EnvelopeEnvelope Envelope Envelope █ █ █ █ ██ ██ ██ ██ Naked Naked Dy-NakedNaked Tet- NakedHilate Dy- NakedTrilete Tet- Hilate Trilete Age EnclosedAge Enclosed Envelope EnclosedEnclosedEnvelope Enclosed EnvelopeEnclosed Naked Naked Naked█ Hilate█ Trilete█ █ ██ ██ █ █ Age Monads ads MonadsLlandoveryrads Spores ads Sporesrads Spores Spores Monads EnclosedDyads Monads MonadsTetradEnclosed DyadsDyads EnclosedTetrad Tetrad Monads Dyads Tetrads█ Spores█ Spores█ █ ██ ██ █ █ █ █ ██ ██ ██ ███ ███ █ █████ █ █████ █ ██████ █ ███ ███ █ █ Přídolí Pˇrídolí Přídolí █ █ ██ ███ ██ ███ ████ ██████ ██████ ██████ █ ███ ███ █ █ █ █ ██ ██ ██ ███ ███ ███ ██ ██ Ludlow Ludlow Ludlow█ █ ██ ███ ██ ███ ███ ███ Based on██ the dispersed██ spore record it seems that relatively uniform vegetation was █ █ ██ ██ ███ ███ ██ present██ for 30█ █million years██ from the Daipingian to the Llandovery [123]. Wenlock Wenlock Wellman et al. [123] summarized the records of 787 spore species of all palaeoconti- █ █ ██ ██ ███ ███ ██ ██ ██ ██ Wenlock nents from Ordovician to Late Silurian. The graphical interpretation of global quantitative █ █ ██ ██ ███ ███ ███ ███ █ █ Llandovery Llandovery data from Katian to Přídolí (Figure 8) shows that biodiversity curves of cryptospores and █ █ ██ ██ ███ ███ ███ ███ █ █ Llandovery trilete isospores are different. It also suggests that cryptosporophytes and trilete spore ██ ███ ████ █ ████ ██████ ███ █ ████ ████ █ █

██ ███ █████ ████ ██████ ████ ████ ████ █ █

Based on the dispersed Basedspore recordon the dispersedit seems that spore relatively record uniformit seems vegetationthat relatively was uniform vegetation was present for 30 million yearspresent from for the 30 Daipingian million years to fromthe Llandovery the Daipingian [123]. to the Llandovery [123]. Wellman et al. [123] summarizedBasedWellman on the et the dispersed al. records [123] summarized spore of 787 record spore the itspecies seems records of that allof relatively787palaeoconti- spore uniformspecies of vegetation all palaeoconti- was nents from Ordovicianpresent tonents Late forfrom Silurian. 30 Ordovician million The yearsgraphical to fromLate interpretationSilurian. the Daipingian The gr ofaphical toglobal the Llandovery quantitativeinterpretation [123 of]. global quantitative data from Katian to PřídolídataWellman (Figure from Katian 8) et shows al. [to123 P thatř]ídolí summarized biodiver (Figuresity 8) the shows curves records that of ofcryptospores biodiver 787 sporesity species andcurves ofof allcryptospores palaeoconti- and trilete isospores are different.nentstrilete from isosporesIt Ordovicianalso sugge are sts todifferent. Latethat Silurian.cryptosporophytes It also The sugge graphicalsts that and interpretation cryptosporophytes trilete spore of global and quantitative trilete spore data from Katian to Pˇrídolí (Figure8) shows that biodiversity curves of cryptospores and trilete isospores are different. It also suggests that cryptosporophytes and trilete spore

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producersproducers hadhad differentdifferent lifelife strategies strategies and and dispersal dispersal potential. potential. AA prominent prominent cryptospore cryptospore peakpeak occursoccurs within within Rhuddanian Rhuddanian (17 (17 genera genera with with 33 33 species species on on average), average), and and after after a a signifi- signif- canticant decline decline in in the the Sheinwoodian Sheinwoodian (only (only 9 9 genera genera with with 9 9 species) species) the the occurrence occurrence from from the the HomerianHomerian toto PˇrPřídolídolíí is is relatively relatively stable stable (14 (14 genera genera with with 25 25 species species on on average). average).

Figure 8. Quantitative curves of cryptospores (dashed line) and trilete spores (full line) from Katian Figure 8. Quantitative curves of cryptospores (dashed line) and trilete spores (full line) from Katian to to Přídolí. Horizontal axis represents stratigraphical interval. Abreviations: K—Katian, H— Pˇrídolí. Horizontal axis represents stratigraphical interval. Abreviations: K—Katian, H—Hirnantian, Hirnantian, LR—Llandovery (Rhuddanian), LA—Llandovery (Aeronian), LT—Llandovery LR—Llandovery(Telychian), WS—lower (Rhuddanian), Wenlock LA—Llandovery (Sheinwoodian), (Aeronian), WH—upper LT—Llandovery Wenlock (Homerian), (Telychian), LG—lower WS— lowerLudlow Wenlock (Gorstian), (Sheinwoodian), LL—upper Ludlow WH—upper (Ludfordian), Wenlock (Homerian),P—Přídolí. Vertical LG—lower axis Ludlow represents (Gorstian), average LL—uppernumber of trilete Ludlow spores. (Ludfordian), Based on P—Pˇrdata ofídol Wellmaní. Vertical et al. axis [123]. represents average number of trilete spores. Based on data of Wellman et al. [123]. The diversity of trilete spores was constant from the Hirnantian to the Sheinwoodian (onlyThe 3 genera diversity with of trilete4 species spores on wasaverage); constant the from first theglobal Hirnantian proliferation to the Sheinwoodianevent of trilete (onlyspores, 3 genera i.e., withpresumably 4 species diversifying on average); theancestors first global of proliferationbryopphytes event and of tracheophytes trilete spores, i.e.,[79,123,124] presumably is within diversifying Homerian ancestors (13 genera of bryopphytes with 29 species). and tracheophytes After a short [ 79period,123,124 with] is a withindecreased Homerian number (13 of genera trilete with spore 29 species).taxa in th Aftere Gorstian, a short perioda prominent with a increasing decreased numbertrend is ofrecognized trilete spore from taxa the in Ludfordian the Gorstian, (20 a prominentgenera with increasing 48 species) trend to the is recognizedsecond globally from therec- Ludfordianorded event (20 within genera the with Přídolí 48 species)(35 genera to thewith second 129 species). globally recorded event within the PˇrídolTheí (35 Homerian genera with event 129 is species). documented mainly palynologically [79,123] but the Přídolí The Homerian event is documented mainly palynologically [79,123] but the Pˇrídolí event is recognized both palynologically and by megafossil plant records [38]. event is recognized both palynologically and by megafossil plant records [38]. Hagström and Mehlqvist [94,114,125] mentioned embryophyte cryptospores of prob- Hagström and Mehlqvist [94,114,125] mentioned embryophyte cryptospores of proba- able Ludfordian Age from approximately 15° south latitude [76] (Figures 2, 3—L7) from ble Ludfordian Age from approximately 15◦ south latitude [76] (Figures2 and3—L7) from Sweden, i.e., a former eastern part of Laurisia. Sweden, i.e., a former eastern part of Laurisia. All events in the history of Silurian land plants documented here palynologically cor- All events in the history of Silurian land plants documented here palynologically cor- respond to changes in the temperature and atmospheric pO2 and pCO2, as we will discuss. respond to changes in the temperature and atmospheric pO2 and pCO2, as we will discuss.

4.4. DiscussionDiscussion 4.1.4.1. ResponseResponse ofof SilurianSilurian PlantsPlants toto EnvironmentalEnvironmentalPerturbations Perturbations 4.1.1.4.1.1. WenlockWenlock TheThe WenlockianWenlockian flora flora is is known known [ 47[47]] only only from from the the cold cold temperate temperate zones zones (Figure (Figure2 )2) of of SouthSouth Laurasia-NorthwestLaurasia-Northwest Gondwana.Gondwana. ItIt isis characterizedcharacterized byby aa rhyniophytoid-dominatedrhyniophytoid-dominated plantplant assemblageassemblage (e.g.,(e.g., FigureFigure5 ).5). Polysporangiophytes Polysporangiophytes ofof the the Wenlock Wenlock Age Age are are mostly mostly foundfound withinwithin thethe temperatetemperate climaticclimatic zonezone toto subpolarsubpolar areas,areas, wherewhere significantsignificant seasonalityseasonality cancan bebe expected.expected. Generally,Generally, thethe WenlockWenlock is is characterized characterized by by colder colder climate climate culminating culminating in in thethe latelate Homerian Homerian glaciation glaciation (Figures (Figure1 1, and 3).3 A). Ahigh high diversity diversity of of plant plant types types is is indicated indicated by bythe the occurrence occurrence of of dispersed dispersed spore spore assemblages assemblages fr fromom localities localities in the Barrandian areaarea (the(the PraguePrague Basin).Basin). ForFor example,example, thethe analysisanalysis ofof aa HomerianHomerian samplesample comingcoming fromfrom a a single single bed bed revealedrevealed at at least least ten ten to to twelve twelve types types of trileteof trile sporete spore producing producing plants plants and three and tothree four to types four

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of cryptosporophytes as early as in the Middle Sheinwoodian [78,79]. This fact evoked an idea that relatively rich terrestrial plant assemblages evolved continuously through the Wenlock, through at least two graptolite biozones, in the volcanic islands of the Barrandian area (the Prague Basin), the Czech Republic. Generally, this assemblage (Figure3—W1 plus Wa) characterized relatively rich vegetation that probably covered physically suitable areas of the Southern hemisphere. Some bryophyte-like microscopic tissue fragments are preserved abundantly within the Homerian (e.g., Figure6). The Homerian glaciation event probably created new large-scale habitats in the phys- ical space that was created by the regression accompanying ice formation. These new habitats were certainly colonized by plants. Plants sensitively responded to seasonal tem- perature fluctuations and humidity as mentioned by Raymond et al. [47]. Nevertheless, the plants from the temperate zone probably did not have to face the frost during the winter, as suggested by Raymond et al. [47], despite the fact that the Wenlock was a cold period certainly limiting the possibility of plant growth and dispersal (Figure1). This seems to be supported palynologically because Sheinwoodian cryptospore and trilete spore assemblages reach their minimum diversity here. The first global key proliferation event for trilete spore-producing land plants is documented palynologically after Homerian glaciation (Figure3). It seems that the Wenlock can be palaeobotanically and palynolog- ically divided into a less environmentally favorable Sheinwoodian interval and a more environmentally suitable late Homerian interval for early land plants. Edwards and Richardson [46] proposed a ruderal species strategy for rhyniophytoid plants, including a reproductive cycle that was completed during the times of high humidity. Plants persisted as latent spores during periods of unfavorable conditions, although still in a constantly humid environment (mesophytic habitats) [46]. Unfortunately, we do not have evidence for tropical and subtropical plants from Wenlock time.

4.1.2. Ludlow Since Early Ludlow, the global temperature was increasing until the Middle Lud- fordian when this trend was interrupted by a rapid cooling during the Mid-Ludfordian glaciation (Figure3). After the glaciation, the global temperature reached the same level as before the glaciation. Unique Ludlow data come from the equatorial zone where well-preserved plant assemblages from Arctic Canada (Figure4) and Northern Greenland are reported. This vegetation, characterized by dominance of zosterophylls, has been referred to the North Laurussian palaeophytogeographic unit [47]. Similar plant assemblages of Ludlow age are known from the Northeast Gondwanan (Australia) unit (sensu [47]) where the climate has a transitional character between the tropical and subtropical zones. This area was located approximately 10 ◦ south latitude during Late Silurian times [76]. Raymond et al. [47] stated that flora from Australia cannot be compared with zosterophyll-dominated vegetation from Bathurst Island of Arctic Canada because different taxa occurred in the two areas, indicating an evolutionary disjunction. North Laurussian and northeast Gondwanan units are characterized by the predom- inance of zosterophylls due to the warm climate (sensu [126]). Zosterophyll-dominated assemblages from northeast Gondwana also yielded a number of rhyniophytes. It is likely that these areas represent the cradle of zosterophyll origin based on their absence in the lower Silurian and on their sudden abundance during Late Silurian in areas where they became the dominant element [50]. So far, we can only speculate why in this warm zone plants appear that have sporangia in the terminal part of their shoots. Certainly, a signif- icant factor was the relatively constant and high temperature and humidity throughout the year, when the growing season was not interrupted by any significant temperature or water stresses. As a basal group of lycophytes, they could have had very similar ecological requirements as the later lycophytes-from the Carboniferous Age. These younger plants preferred a very humid climate and were a significant part of most peat forming assem- blages. Based on the absence of zosterophylls in the Early Silurian and the sudden increase Life 2021, 11, 906 15 of 22

in abundance during the Late Silurian in areas where they became the dominant element of the flora, it is likely that these areas also represent the cradle of their origin [50]. In any case it could be assumed that both rhyniophytes and zosterophyllophytes in this period were already equipped with a primitive type of stomata [127]. Raymond et al. [47] interpreted assemblages from Australia and Bathurst Island as products of warm zones and mentioned the same ecological conditions accompanying the origin of zosterophyll-like plants. However, it can be concluded that the overall warm climate with episodes of the expansion to higher latitudes (after glacials) of the humid tropical environment during the Silurian undoubtedly led to the evolution of this lycophyte type of plant. Generally, based on palynological results, Gorstian spore and cryptospore assemblages are less numerous and less diverse than previous Homerian associations, which was probably influenced by the preceding Late Homerian glaciation.

4.1.3. The Importance of Mid-Ludfordian Glaciation The Mid-Ludfordian has been known for one of the largest perturbations in the Phanerozoic carbon cycle, the Mid-Ludfordian Carbon Isotope Excursion, linked with an ex- tinction event recorded in global marine ecosystem. Significant global cooling was recently documented from temperate areas of the Prague Basin and Carnic Alps (peri-Gondwana), as well as from the tropical areas of Baltica (Laurussia) and Australia (Gondwana) based on δ18O data [24]. The marked cooling of sea-surface temperatures, coupled with a significant eustatic sea-level fall recorded on all corresponding palaeocontinents, evidences a major glaciation (“Mid-Ludfordian Glaciation”) in polar and subpolar western Gondwana. Glaciation passed during Late Ludlow (Ludfordian) accompanied by a significant reduction of average temperature (Figure1). Large-scale dry land habitat space was created by the Mid-Ludfordian glaciation event and associated sea-level drop, certainly accompanied by plant colonization of these new areas following oceanic regression. We suppose that the vacant ecological windows were occupied by trilete spore producing em- bryophytes together with bacterial-cyanobacterial mats and still some cryptosporophytes, which colonized coastal areas. Plants established complex and specialized ecosystems on the new land habitats that served as a nutrient source for the rapid global expansion of polysporangiophyte plants, supported also by distinct climatic changes. The expansion is especially apparent for plants preferring warmer and more humid conditions. Ray- mond et al. [47] supposed that the lycophyte genus Baragwanathia is typical for warm and humid climatic zones. However, Baragwanathia brevifolia and another basal lycophyte, Aberlemnia bohemica, are described also from a higher latitude of the peri-Gondwana Realm (namely Barrandian area, the Prague Basin, Czech Republic) and a higher stratigraphical level (Pˇrídolí)[38,43]. It seems that the expansion of Baragwanathia-like plants to higher latitudes is associated with increased humidity during glaciation and following global warming after the Mid-Ludfordian glacial. A similar shift to higher latitudes of lycophytes and zosterophylls can be traced in other localities that belong to the temperate zone of the South Laurussian-Northwest Gondwanan unit [47]. For example, a Podolian assemblage (Figure2—P8) from eastern Laurussia shows dominance of rhyniophytoids, including Cooksonia pertoni, C. hemisphaerica, and mainly Zosterophyllum sp. and Lycopodolica, rather typical for the warmer equatorial Silurian zones. The Ludfortian is palynologically characterized by the increasing variability of spore and cryptospore assemblages with a high number of new taxa.

4.1.4. Pˇrídolí The prominent rise in temperature during the Pˇrídolí [128] was permissive of the evolution of new forms of plants. Transgression contributed to the frequent transport of land plants into the sea and created Silurian taphonomic windows. The number of Silurian localities with rhyniophytoid-dominated vegetation (including the typical occurrence of Cooksonia) is higher during the Pˇrídolí than during the Ludlow. This homogenization was based by Raymond et al. [47] on floras of similar composition Life 2021, 11, 906 16 of 22

in both areas where the rhyniophytoid-dominated flora is present and includes some common taxa, e.g., Cooksonia hemisphaerica. In this context however, the occurrence of C. hemisphaerica s.s. in Northwest Gondwana is still questionable and needs re-evaluation. A similar situation is also found with respect to a comparison of the character of assemblages from Great Britain and Bolivia [47]. Raymond et al. [47] explained this similarity by the seasonality that equally affected plants from SE Laurussia in the subtropical zone and Northwest Gondwana or peri-Gondwana in the temperate zone. The general plant character from China and Vietnam shows some similarities [105,126] to Ludlowian vegetation from tropical Bathurst Island or maybe subtropical Victoria, Australia, in having Zosterophyllum-like plants as dominant. Plants of Pˇrídolí age are known from the Kazakhstanian unit situated in the subtropical zone of the North hemisphere. Northern latitude floras differ from those of environmentally similar southern latitudes in the common occurrence of Zosterophyllum-like plants in the former. Edwards and Wellman [45] pointed out this phenomenon and placed the Kazakhstanian flora on the South China Block (Xinjiang flora). Relatively rich localities already appear in several areas during the Pˇrídolí and this trend continues across the Silurian/Devonian boundary into the Early Devonian. The number and variations of spore and cryptospore assemblages rapidly increased during the Pˇrídolí Series, reflecting the second globally important key event for land plants.

5. Conclusions Atmospheric oxygen steadily rose from the Middle Ordovician and through almost the entire Silurian. By the beginning of the Wenlock, oxygen levels surpassed the current level for the first time in the Earth’s history, and at the end of Silurian attained 35% [64,129]. This trend supports previous conclusions [49,64] and our own herein (based on our data and compiled fossil data as discussed) that, despite climate fluctuations, terrestrial flora expanded during the Silurian. We hope we have relaxed at least a small bit of constraints on Silurian phytogeography and support the conclusions of Edwards [49]. Current phylo- genomic/-stratigraphy dating of the embryophyte split into tracheophytes and bryophytes ranges from approximately 440 up to 800 Myr for tracheophytes [15,18]. This on one hand indicates uncertainty related to the timing of this major evolutionary cross-roads in land plant evolution. On the other hand, it also indicates that the tracheophyte lineage was certainly well established in the Silurian. Our analysis of spore diversity evolution clearly indicates a very distinct exponential evolutionary acceleration of trilete spore producers starting in the lower Wenlock (and continuing in fact until today—Figure8). This expansion of trilete spore producers is also reflected in an apparent geographical spread of documented macrofossils between the Wenlock and Ludlow/Pˇrídolí (Figure2 ). Cryptospore-producers, which dominated Silurian flora until the upper Llandovery stag- nated evolutionarily until their Devonian extinction. In a more detailed attempt to correlate trilete spore diversity and global temperature changes (Figure3), we conclude that after three distinct Middle to Late Silurian glaciations we can clearly see an increase of diversity correlated with the rise of the global temperature after the glaciations ended. Interestingly, while Homerian glaciation did not affect the diversity of cryptospores, it resulted in the distinct decline in the diversity of trilete spores. This indicates that there was a different sensitivity of cryptosporophytes vs. trilete spores-producers to the global cold temper- ature. In respect to fragmentary Silurian phytogeography data summarized vividly by Edwards [49] (see above), our data essentially support her conclusions that the four distinct plant assemblages correlate very well with the four palaeocontinents. It certainly is very difficult even to speculate about the physiological character of Sil- urian plants. However, both detailed, enhanced anatomical knowledge of the immediately following Early Devonian rhyniophyte flora, and also advancements in phylogenomic and phylostratigraphic analyses provide important facts allowing an informed reconstruc- tion of at least some aspects of the biology of Silurian trilete spore-producing plants (we do not speculate here about the biology of cryptosporophytes.) Based on all the current Life 2021, 11, 906 17 of 22

available fossil data, the Silurian flora is composed of different types of polysporangiate plants (including cryptophytes)—any reliable evidence for the monosporangiates is absent. There are no identified gametophytes of any Silurian plant. Thus, the first reliable life cycles/alteration of gametophyte and sporophyte generations is not known before that of several representatives of Devonian Rhynie chert flora [130]. In relation to plant physiol- ogy, stomata are one of the crucial ecophysiological features related to both temperature, water availability and atmospheric composition. Based on both phylogenomics-indicating reduction or loss of stomatal functioning in the common ancestor of extant embryophytes in bryophytes [127], as well as the palaeobotanical demonstration of distinct stomata de- scribed both on sporophytes and gametophytes of Rhynie chert plants [131], we should accept that the common ancestor of both mosses and tracheophytes had stomata—most probably already dynamically regulated (opening-closing) by the abscisic acid signalling pathway [127,132]. This pathway is crucial for the optimization of land-plant water econ- omy and survival of water stresses both during day-night cycles, but importantly also during seasons allowing local adaptations dependent on latitude. As is the case for abscisic acid signalling, the evolution of lignified secondary-thickened conductive tissues is well documented in Rhynie chert plants. Lignification most probably started much earlier and precursors of tracheophyte xylem and phloem were with high probability also present in the common Bryophyta-Tracheophyta ancestor. As in the case of stomata [127], it is possible that secondary simplification accompanied the evolution of other traits in the Bryophyta. Major transcriptional regulators of xylem development are also encoded in bryophyte genomes and VND-NST-SOMBRERO (VNS) genes—vessel-element differentia- tion master regulators—from Sphagnum moss (which does not have hydroids and instead uses hyaline cells with thickened, helical-patterned cell walls and pores to store water in the leaves) and induces secondary cell wall thickening when ectopically expressed in the angiosperm Nicotiana benthamiana [133]. The anatomy of Silurian (and Devonian) plant fossils/assemblages, along with recent phylogenomic analyses, clearly indicate highly terrestrialized advanced plant types with likely a great ability to resist different dry land stress conditions and to evolve on different palaeocontinets into quite disjunctive specific floras/plant assemblages certainly also in response to different geological, geographical and climatic conditions.

Author Contributions: Conceptualization, J.P., V.Ž. and J.B.; methodology, J.P., J.B. and J.F.; formal analysis, J.P., J.B. and M.U.; investigation, J.P., J.B., J.F., M.U., V.Ž. and P.Š.; resources, J.P.; data curation, J.P., J.B., J.F., M.U. and P.Š.; writing—original draft preparation, J.P.; writing—review and editing, J.P., J.B., J.F. and V.Ž.; visualization, J.P.; supervision, V.Ž.; project administration, J.P.; All authors have read and agreed to the published version of the manuscript. Funding: This research was financial supported by the Czech Science Foundation—GACRˇ 21-10799S. Part of this contribution was also supported by the Research Program of the Institute of Geology AS CR, v.v.i. (RVO67985831) and West Bohemian Museum in Pilsen DKRVOZCM2020-25/93P. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: The data presented in this study are available on request from the corresponding author. Acknowledgments: We thank to the authors of Kotyk et al. [74] who provided us with photos of the specimen from Bathurst Island through Patricia Gensel. We also thank the National Museum (Prague), West Bohemian Museum in Pilsen, and private collector OndˇrejZicha, who provided us with photographs of specimens from the Silurian of the Barrandien. The SEM observations were made in the Institute of Geology and Palaeontology, Faculty of Science, Charles University in Prague from examination under JEOL 6380LV. We would like to thank Bill DiMichele for comments and corrections in the use of the English language. Last but not least, the first author of this contribution thanks to Francis Beer Café in Pilsen for the amazing atmosphere that helped originate of this manuscript. Conflicts of Interest: The authors declare no conflict of interests. Life 2021, 11, 906 18 of 22

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