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Type of the Paper (Article life 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 Life 2021, 11, 906 3 of 22 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;
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