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Pseudoasterophyllites Cretaceus from the Cenomanian (Cretaceous) of the Czech Republic: a Possible Link Between Chloranthaceae and Ceratophyllum Jiří Kvaček,1 James A

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Pseudoasterophyllites Cretaceus from the Cenomanian (Cretaceous) of the Czech Republic: a Possible Link Between Chloranthaceae and Ceratophyllum Jiří Kvaček,1 James A TAXON 65 (6) December 2016: 1345–1373 Kvaček & al. Pseudoasterophyllites cretaceus, a possible link PALAEOBOTANY Pseudoasterophyllites cretaceus from the Cenomanian (Cretaceous) of the Czech Republic: A possible link between Chloranthaceae and Ceratophyllum Jiří Kvaček,1 James A. Doyle,2 Peter K. Endress,3 Véronique Daviero-Gomez,4 Bernard Gomez4 & Maria Tekleva5 1 Department of Palaeontology, National Museum Prague, Václavské nám. 68, 115 79, Praha 1, Czech Republic 2 Department of Evolution and Ecology, University of California, Davis, California 95616, U.S.A. 3 Department of Evolutionary and Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland 4 CNRS-UMR 5276 Laboratoire de Géologie de Lyon – Terre, Planètes, Environnement, Université Lyon 1 (Claude Bernard), Observatoire de Lyon, 69622 Villeurbanne, France 5 A.A. Borissiak Paleontological Institute, Profsojuznaya str. 123, Moscow 117647, Russia Author for correspondence: Jiří Kvaček, [email protected] ORCID JK, http://orcid.org/0000-0003-2001-121X; JAD, http://orcid.org/0000-0002-4083-8786; PKE, http://orcid.org/0000-0001- 6622-8196; BG, http://orcid.org/0000-0003-1691-0634; VDG, http://orcid.org/0000-0002-1001-7223 DOI https://doi.org/10.12705/656.8 Abstract Pseudoasterophyllites cretaceus from the Cenomanian of Bohemia was recently recognized as an angiosperm by association with stamens containing monosulcate pollen of the Tucanopollis type. New material indicates that the stamens were borne in short spikes, with each stamen subtended by a bract, whereas the carpels were solitary and contained a single pendent, orthotropous ovule. We have investigated the phylogenetic position of Pseudoasterophyllites by including it in a morphological analysis of extant angiosperms using backbone constraint trees that represent the current range of hypotheses on relationships of the five mesangiosperm clades. With a backbone tree in which Chloranthaceae are linked with magnoliids and Ceratophyllum with eudicots, the most parsimonious position of Pseudoasterophyllites is sister to Chloranthaceae, but a sister-group relation- ship to Ceratophyllum is only one step less parsimonious. With a backbone tree in which Chloranthaceae and Ceratophyllum form a clade, Pseudoasterophyllites is sister to Ceratophyllum, based on derived features shared with both Chloranthaceae and Ceratophyllum plus solitary female flowers (as in Ceratophyllum). Similar results are obtained when Pseudoasterophyl- lites is added to the analysis with other fossils inferred to be related to Chloranthaceae and/or Ceratophyllum. If the plants that produced Tucanopollis pollen in the Barremian-Aptian of Africa–South America are related to Pseudoasterophyllites, these results suggest that Chloranthaceae and Ceratophyllum are relicts of one of the most important early radiations of angiosperms, which included not only colonizers of disturbed terrestrial habitats but also halophytes and aquatics. Keywords angiosperms; Ceratophyllum; Chloranthaceae; Cretaceous; paleobotany; Pseudoasterophyllites Supplementary Material The Electronic Supplement (Table S1) and the morphological character matrix (Nexus) are available in the Supplementary Data section of the online version of this article at http://www.ingentaconnect.com/content/iapt/tax INTRODUCTION (Schrank & Mahmoud, 2003), England (Hughes, 1994, as Barremian-ring), and Spain (R. Zetter, pers. comm.). Pseudo- Pseudoasterophyllites cretaceus Feistm. ex Velen. is an asterophyllites Feistm. ex Velen. is unique in the context of enigmatic plant best known from the Cenomanian (early Late other angiosperm taxa in the Cenomanian Peruc-Korycany Cretaceous) of the Czech Republic. It combines reduced simple Formation and the Central European Cretaceous as a whole. leaves with characters shared with living early-diverging an- However, it is also known from the uppermost Albian (Les giosperm groups, particularly the ambiguously placed families Renardières: Kvaček & al., 2012) and the lower Cenomanian Chloranthaceae and Ceratophyllaceae (Ceratophyllum L.). It (Jaunay-Clan, near Poitiers: Valentin & al., 2014; B. Gomez, has simple male flowers consisting of a single stamen contain- pers. obs.) of western France. ing Tucanopollis Regali pollen, which is of interest because it The systematic position of Pseudoasterophyllites creta- occurs among the earliest angiosperm pollen taxa in the Bar- ceus has been a matter of debate since the plant was first dis- remian of Brazil (Regali & al., 1974; Regali, 1989), Gabon covered. It was first collected and designated by O. Feistmantel and Congo (Doyle & al., 1977; Doyle & Hotton, 1991), Egypt (1874) as “Asterophyllites cretaceus”, a nomen nudum implying Received: 14 Apr 2016 | returned for (first) revision: 20 Jun 2016 | (last) revision received: 18 Sep 2016 | accepted: 18 Sep 2016 || publication date(s): online fast track, 6 Dec 2016; in print and online issues, 22 Dec 2016 || © International Association for Plant Taxonomy (IAPT) 2016 Version of Record 1345 Kvaček & al. Pseudoasterophyllites cretaceus, a possible link TAXON 65 (6) December 2016: 1345–1373 a relationship to Paleozoic calamites (Equisetales), and first (50°08′00″ N, 13°54′34″ E). Older collections in the National validly published by Velenovský (1887) as Pseudoasterophyl- Museum, Prague, are derived from the type locality at Lipenec. lites cretaceus. Velenovský interpreted the plant as probably a Geological and sequence stratigraphic analyses indicate cryptogamic aquatic but definitely not an equisetalean. Later, that the Peruc-Korycany Formation represents a series of paleo- Zeiller (1902), during his work on fossil plants from the Bar- valley infills (Uličný & Špičáková, 1996; Uličný & al., 2009). remian of La Pedrera in Spain, described Pseudoasterophyllites These successions comprise deposits of a variety of continen- vidali, now renamed Montsechia vidalii (Zeiller) Teixeira. He tal (braided rivers, meandering streams and floodplains, and restudied the original specimens of P. cretaceus and interpreted anastomosed fluvial systems) and coastal environments (tidally it as a conifer (Zeiller, 1907). By contrast, Velenovský and influenced braided rivers, supratidal salt marshes, tidal flats, Viniklář (1926) interpreted the plant as a lycophyte based on ebb-tidal deltas, estuaries, and lower shoreface) (Uličný & al., reproductive structures that they believed belonged to P. cre- 1997). The studied plant fossils come from mudstone units inter- taceus. More recently, Kvaček & Eklund (2003) suggested preted at Pecínov as supratidal salt marsh deposits (Uličný & al., that the plant might be a gnetophyte because of its suppos- 1997; Nguyen Tu & al., 2002). The dominant fossils in these de- edly whorled phyllotaxis. However, prior to this Kvaček (1983: posits are Frenelopsis alata (K.Feistmantel) Erw.Knobloch and 166) had suggested its probable angiosperm affinities based on Eretmophyllum obtusum (Velen.) J.Kvaček (Uličný & al., 1997). cuticle structure. In 2012 Kvaček & al. (2012) provided conclu- Occurrence of these two species and Pseudoasterophyllites cre- sive evidence for an angiosperm affinity by associating leafy taceus is restricted laterally to isolated, typically monodominant stems in Bohemia and the uppermost Albian of France with taphocoenoses. Marine influenced habitats are also indicated by stamens that contain Tucanopollis pollen, which resembles palynology (Svobodová in Uličný & al., 1997), namely the occur- reticulate-monosulcate pollen assigned to Clavatipollenites rence of marine microplankton (e.g., Micrhystridium spp.). Dur- Couper (Couper, 1958; Doyle & al., 1975; Walker & Walker, ing excavations in 2015 J.K. observed and collected marine mac- 1984) in having supratectal spinules and a sculptured sulcus rofauna even within the layer containing Pseudoasterophyllites. but differs in having a continuous tectum. Uličný & al. (1997) All studied material is housed in the National Museum Prague. and Kvaček & al. (2012) interpreted P. cretaceus as a halophyte Observations on fossils. — Hand specimens were slowly because of its succulent appearance and its occurrence in es- dried. Some were covered by polyvinyl acetate film, while tuarine facies (Uličný & al., 1997) with a low-diversity plant others were conserved in glycerine and later in silicone oil. assemblage dominated by the halophytic conifer Frenelopsis Part of the material was bulk macerated in a 20% solution of alata (K.Feistmantel) Erw.Knobloch (Cheirolepidiaceae). sodium bicarbonate. The best results were achieved when the In the present paper we provide additional evidence for material was macerated immediately after field work, when it the angiospermous interpretation of Pseudoasterophyllites and was still wet. These extractions were followed by maceration describe both male and female reproductive organs borne on in 50% hydrofluoric acid. A large portion of the material was leafy shoots. In addition, we have incorporated Pseudoastero- sorted by organ, documented, and for final arrangement soaked phyllites into a series of phylogenetic analyses, which provide in alcohol with thymol and stored in plastic boxes with silicone evidence that it belongs near the living families Chloranthaceae oil. Some specimens, particularly detached leaves and isolated and/or Ceratophyllaceae. As with fossils in general, because stamens, were macerated several minutes in Schulze’s solution, of the many missing characters, these results are necessarily prepared and mounted in glycerine on a preparation
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