A Jurassic moss from Northeast China with preserved sporophytes

Review of Palaeobotany and Palynology 204 (2014) 50–55

Contents lists available at ScienceDirect

Review of Palaeobotany and Palynology journal homepage: www.elsevier.com/locate/revpalbo

A Jurassic moss from Northeast China with preserved sporophytes Jochen Heinrichs a,⁎, Xin Wang b, Michael S. Ignatov c, Michael Krings d a

Systematische Botanik und Mykologie, Department für Biologie I, Ludwig-Maximilians-Universität, Menzinger Str. 67, 80638 München, Germany State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, The Chinese Academy of Sciences, 39 Beijing Dong Road, Nanjing 210008, China c Main Botanical Garden, Russian Academy of Sciences, Botanicheskaya 4, Moscow 127276 Russia d Department für Geo- und Umweltwissenschaften, Paläontologie und Geobiologie, Ludwig-Maximilians-Universität, Bayerische Staatssammlung für Paläontologie und Geologie, Richard-WagnerStraße 10, 80333 München, Germany b

a r t i c l e

i n f o

Article history: Received 11 December 2013 Received in revised form 5 February 2014 Accepted 7 February 2014 Available online 24 February 2014 Keywords: Bryophyta classification compression fossil Daohugou Jiulongshan Formation Mesozoic

a b s t r a c t Three compression specimens of a fossil moss from the Jurassic Jiulongshan Formation of Inner Mongolia, China, are described as Ningchengia jurassica, sp. nov. Ningchengia forms dense tufts, is characterized by erect to erectspreading leaves that gradually narrow into a slender to stout point and have a strong, simple percurrent to excurrent costa. Several sporophytes are preserved in place, showing elongate setae and oblong cylindrical capsules. These morphological character states indicate affinities of the fossils to the Bryophytina. Ningchengia jurassica is one of only a few compression moss taxa with sporophytes preserved in situ. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Mosses represent an early diverging main lineage of land plants that dates back to the Paleozoic (Taylor et al., 2009; Clarke et al., 2011; Magallon et al., 2013). Reconstruction of the evolutionary history of these plants is generally hampered by the incomplete fossil record and the poor preservation of many fossils (Krassilov and Schuster, 1984; Oostendorp, 1987; Chandra, 1995; Ignatov and Shcherbakov, 2009; Kenrick et al., 2012). The earliest fossils assigned to the mosses are known from the Carboniferous, but their classification remains controversial (Renault and Zeiller, 1885; Lignier, 1914; Thomas, 1972; Hübers and Kerp, 2012). Although the situation takes a turn for the better in the Permian (Neuburg, 1960; Ignatov, 1990), assignment of the Permian fossils to extant taxa remains equally difficult. As a result, the reconstruction of the relationships of extant mosses is largely based on molecular data (Magombo, 2003; Cox et al., 2004; Goffinet and Buck, 2004; Cox et al., 2010; Volkmar and Knoop, 2010). These data indicate that sporophytic features are well-suited to characterize the main lineages and that the derived lineages of mosses share the presence of peristomial teeth surrounding the sporangial mouth to facilitate spore dispersal. Early diverging moss lineages (i.e. Takakiopsida, Sphagnopsida, Andreaeopsida, Andreaeobryopsida) lack a peristome;

⁎ Corresponding author. Tel.: +49 89 17861 302. E-mail address: [email protected] (J. Heinrichs).

http://dx.doi.org/10.1016/j.revpalbo.2014.02.005 0034-6667/© 2014 Elsevier B.V. All rights reserved.

their capsules open via slits or caducous lids (Renzaglia et al., 2007; Shaw et al., 2011). Unfortunately the vast majority of Paleozoic and Mesozoic mosses are preserved only as gametophytes; sporophytes are rarely observed in pre-Cenozoic fossils (Frahm, 2010). A putative immature moss sporophyte has been described from the Carboniferous/Permian of Brazil (Amaral et al., 2004; Christiano de Souza et al., 2012). The oldest unequivocal sporophytes of mosses yet reported come from the Permian of India [Saksenaphyllites saksenae Chandra (Chandra, 1995)] and Brazil [Capimirinus riopretensis Christiano de Souza, Branco & Léon (Christiano de Souza et al., 2012)]. However, all these specimens are poorly preserved and do not permit a detailed morphological analysis of the capsule. The same is true of the Late Jurassic Muscites fontinaloides Krassilov (Krassilov, 1973). In this paper, we describe a new Mesozoic moss, Ningchengia jurassica nov. gen. et sp., based on compression fossils from the Jurassic Jiulongshan Formation of Inner Mongolia, China; particularly interesting is that in one of the specimens, both the gametophytic and sporophytic generations are preserved. 2. Geological setting, material, and methods The specimens come from fossiliferous beds within the Jiulongshan Formation, from an exposure in the vicinity of the village of Daohugou (Ningcheng county), approximately 80 km south of Chifeng City, Inner Mongolia Autonomous Region, northeastern China (119°14.318′E,

J. Heinrichs et al. / Review of Palaeobotany and Palynology 204 (2014) 50–55

41°18.979′N). The Daohugou fossil beds occur in the lower part of a massive tuffaceous deposit (~ 50–80 m thick) composed of greyishwhite to yellowish-white tuff, tuffaceous sandstone, and tuffaceous siltstone and shale, with a tuffaceous conglomerate at the base (Fig. 1a, b; Tan and Ren, 2009). 40Ar–39Ar and SHRIMP U/Pb isotope analyses, indicate that the fossil beds are Jurassic in age and somewhere between 168 and 152 Ma old (Chen et al., 2004; He et al., 2004; Liu et al., 2006; Peng et al., 2012). This concurs with age estimates based on various fossils or fossil assemblages, including insects (Ren et al., 2002; Huang et al., 2006; Ren et al., 2009; Zhang, 2010), conchostracans (Shen et al., 2003; Huang et al., 2006), and plants (Zhou et al., 2007). The Daohugou paleoenvironment has been reconstructed as a series of mountain streams and lakes surrounded by gymnosperm-dominated forest vegetation, occasionally experiencing (heavy) ashfalls from volcanic eruptions (e.g., Ren and Krzeminski, 2002; Tan and Ren, 2002; Zhang et al., 2006); the climate likely was humid and warm-temperate (Tan and Ren, 2002). Fossils reported from the Daohugou beds include synapsids, amphibians, pterosaurs, theropods, mammaliforms, a remarkable diversity of insects, conchostracans (e.g., Ren et al., 2002; Shen et al., 2003; Rasnitsyn and Zhang, 2004; Ji et al., 2005; Gao and Ren, 2006; Meng et al., 2006; Zhang et al., 2008; Shih et al., 2009; Zhang, 2010; Wang et al., 2013; Zhou et al., 2013), as well as a variety of plants (e.g., Mi et al., 1996; Zheng et al., 2003; Li et al., 2004; Zhou et al., 2007) and a lichen-like organism (Wang et al., 2010). The fossils are preserved as compressions, with only part of the original substance still present, on a grey to yellowish tuffaceous mudstone matrix. All specimens are housed in the collection of the College of Life Sciences, Capital Normal University, Beijing, China, under accession

51

numbers CNU-Plant-2013-001, CNU-Plant-2013-002a&b, and CNUPlant-2013-003a&b. 3. Systematic paleobotany Phylum Bryophyta Subphylum Bryophytina Genus Ningchengia Heinrichs, X. Wang, Ignatov & M. Krings, nov. gen. Generic diagnosis: Plants in low, dense tufts. Leaves in several rows or arranged spirally (not distichous), erect to erect-spreading, gradually narrowing, costa simple, thick, reaching leaf apex. Seta elongate, erect, capsules oblong cylindrical, not constricted below mouth. Type species: Ningchengia jurassica Etymology: The generic name refers to the type locality in Northeast China. Species: Ningchengia jurassica Heinrichs, X. Wang, Ignatov & M. Krings, nov. sp. Holotype: CNU-Plant-2013-001 (Plate I, 1) Paratypes: CNU-Plant-2013-002a&b (Plate I, 5a,b) and CNU-Plant2013-003a&b (Plate I, 7a,b) Repository: All material is deposited in the collection of the College of Life Sciences, Capital Normal University (CNU), Beijing, China. Etymology: The specific epithet refers to the Jurassic age of the moss. Specific diagnosis: Relatively robust, ~ 2–3 cm high. Leaves 2.5–N 3 mm long, lanceolate, gradually narrowing into a slender to rather stout, sharp point; lamina distinct to near apex, margins

Fig. 1. Geological setting of the fossil site near the village of Daohugou, Ningcheng, Inner Mongolia Autonomous Region, northeastern China. (a) Geographic position of the site; the grey rectangle is magnified as an insert in the upper left, showing the position of Daohugou village (black triangle) and the major cities of the region. (b) Stratigraphic section of the Jiulongshan Formation near Daohugou village. Layer 3 is the most important fossiliferous bed; 1: gneiss, 2: tuffaceous grand conglomerate, 3: tuffaceous conglomerate, 4: tuffaceous siltstone, 5: tuffaceous mudstone, 6: tuffaceous shale, 7: volcanic breccia, 8: fossiliferous layer (modified from Tan and Ren, 2009).

52

J. Heinrichs et al. / Review of Palaeobotany and Palynology 204 (2014) 50–55

Plate I. Ningchengia jurassica nov. gen. et sp., a moss from the Jurassic of Inner Mongolia, China. Fig. 1 Holotype; tuft of gametophytes from which emerge several upright sporophytes; CNU-Plant-2013-001; scale bar = 1 cm. Fig. 2 Detail of Plate I, 1, focusing on upright sporophytes; scale bar = 3 mm. Fig. 3 Sporophytes (capsules and upper portions of setae); scale bar = 1 mm. Fig. 4 Capsule of detached sporophyte (upper right of Plate I, 1); scale bar = 1 mm. Fig. 5a&b Paratype; specimen lacking sporophytes; CNU-Plant-2013-002a&b; scale bars = 1 cm. Fig. 6 Detail of Plate I, 5a, focusing on arrangement of leaves; scale bar = 1 mm. Fig. 7a&b Paratype; specimen lacking sporophytes; CNU-Plant-2013-003a&b; scale bars = 1 cm. Fig. 8 Detail of Plate I, 1, focusing on pear-shaped structures surrounded by leaves; scale bar = 0.5 mm.

J. Heinrichs et al. / Review of Palaeobotany and Palynology 204 (2014) 50–55

entire, costa ca. 50% of leaf, percurrent or very short excurrent, leaves forming bud-like structures at top of gametophytes possibly surrounding sex organs. Seta upright, smooth, N1.5 cm long; capsule erect, straight, somewhat asymmetrical, between 2 and 3 mm long and N0.5 mm wide. Locality: Vicinity of the village of Daohugou (Ningcheng county), ~ 80 km south of Chifeng City, Inner Mongolia Autonomous Region, Northeast China (119°14.318′E, 41°18.979′N). Stratigraphic horizon and age: Jiulongshan Formation; Jurassic (between 168 and 152 Ma). Description: Ningchengia jurassica is represented by three specimens (i.e. tufts composed of N50 densely spaced gametophytes), one of which with four complete sporophytes preserved in place (Plate I, 1,5a,b,7a,b). Several isolated setae and a fifth sporophyte occur in close association with the holotype specimen (Plate I, 1), but are not physically connected. The tufts are approximately 3 cm high. However, details of the individual plants are recognizable only in the upper third; the lower two thirds consist of degraded parts that are tightly compressed. The individual plants are relatively robust and characterized by leaves that are lanceolate, entire-margined, between 2.5 and N 3 mm long, and gradually narrow into a slender to rather stout, sharp point (Plate I, 6). The lamina is distinct to near the apex. The costa, visible in the leaves as a dark central band, is prominent (~ 50% of width of leaf) and percurrent or very short excurrent. Some of the gametophytes terminate in bud-like structures, ~0.75 × 0,5 mm, which might represent leaves surrounding the sex organs (Plate I, 8). Setae are upright, smooth, and 0.15–0.2 mm wide and N 1.5 cm long (Plate I, 1, 2). The capsules (Plate I, 3) are erect (the angled and drooping capsules in Plate I, 3 represent preservational artifacts), straight, somewhat asymmetrical (Plate I, 4), and between 2 and 3 mm long and N0.5 mm wide. A distal peristome, as well as a distinctively offset proximal hypophysis are not recognizable; however, two of the capsules show a widening or slight swelling of the seta immediately beneath the capsule base (e.g., Plate I, 4). Attempts to obtain cellular details of the leaves and capsule walls by using SEM and epifluorescence microscopy were unsuccessful. 4. Discussion 4.1. Classification of Ningchengia The classification of incompletely preserved fossils remains a challenge, especially in the absence of a copious fossil record allowing the recognition of morphological changes in taxa through time. In the absence of such data, a fossil can only be compared to the extant diversity, which, unlike the fossil record, can be studied by using both morphological and molecular evidence. Consequently, the fossils are related to extant taxa based on morphological similarity, including a careful consideration of putative structures which may not have had the chance to be preserved during the fossilisation process. On the other hand, divergence time estimates based on DNA sequence variation of extant species should be consulted, since these data can be used to reduce the probability of error in taxonomic decisions resting upon the fossils' morphology. 4.1.1. Morphological evidence Ningchengia has single-point leaves with a strong costa and a cylindrical capsule on a long, robust seta. These characters indicate the presence of a moss rather than a liverwort. The pruned apical region of the capsule indicates that it opened at its mouth, rather than with lateral slits, i.e. it likely was of the operculate type. This suite of characters points to a derived moss rather than a representative of the early diverging main lineages Takakiopsida, Sphagnopsida, Andreaeopsida, and Andreaeobryopsida. The derived lineages of mosses comprise the eperistomate Oedipodiopsida as well as the peristomate Polytrichopsida, Tetraphidopsida, and Bryopsida. According to molecular evidence, the first peristomatous mosses had a nematodontous peristome consisting

53

of entire, dead and empty cells (Shaw et al., 2011). Species with arthrodontous peristomes (i.e. peristomes consisting only of cell wall layers) evolved from these nematodontous forms. They comprise more than 90% of the extant mosses and are summarized under Bryopsida (Renzaglia et al., 2007; Shaw et al., 2011). The early diverging lineages of arthrodontous mosses represent the acrocarpous growth form where archegonia are formed terminally on main stems, and the gametophytes typically grow upright and are not or sparsely branched. Pleurocarpous mosses represent a derived lineage nested in acrocarpous clades. They are characterized by archegonia on short lateral branches such that sporophytes occur laterally along the main axis of the gametophyte. Evidence for an acrocarpic nature of Ningchengia comes from the terminal position of the sporophytes in the holotype specimen, and the putatively upright growth of the gametophyte. Thus, Ningchengia probably belongs to the early diverging lineages of Bryopsida. The gross morphology resembles that of the extant families Pottiaceae, Ditrichaceae, Dicranaceae or Rhabdoweisaceae, which are found in a single clade in large scale moss phylogenies (Tsubota et al., 2004; Cox et al., 2010). However, cellular details are not preserved and the sporophyte does not allow a more precise systematic assignment. The cylindrical capsules of Ningchengia show no trace of a lid, indicating that they are open. In this state of preservation a peristome, if present, should be visible. A loss of the peristome during fossilization seems rather unlikely since this structure is constructed of thick-walled cells or cell wall remains. On the other hand, certain representatives of Bryopsida lack peristomes, having either reduced or shed them in the course of the aging process of the capsule. An affiliation with the eperistomate Oedipodiopsida can also not be ruled out, even though its single extant species, Oedipodium griffithianum (Dicks.) Schwägr. has obovate–sphathulate leaves and capsules with a long hypophysis (Smith, 1978). The past diversity of the Oedipodiopsida is unknown and it is possible that this lineage once included a larger number of species with an acrocarpous habit and eperistomate capsules on long setae. Even a position within the nematodontous Tetraphidopsida and Polytrichopsida cannot be ruled out, although the extant species of the former class consistently produce peristomes with four large, robust teeth and the representatives of the latter class are usually more robust. Based on the preceding considerations, we conclude that Ningchengia belongs to a derived lineage of mosses, which today includes the Oedipodiopsida, Tetraphidopsida, Polytrichopsida, and Bryopsida. This lineage corresponds to subphylum Bryophytina. 4.1.2. Evidence from divergence time estimates The reconstruction of the historical biogeography of mosses is to date largely based on molecular data. Available divergence time estimates indicate that all extant classes of mosses were established by end of the Triassic (Newton et al., 2007; Fiz-Palacios et al., 2011), being in good accordance with an assignment of Ningchengia to Bryophytina. Nevertheless, this Jurassic fossil cannot presently be used safely to define nodes in divergence time estimates. To use Ningchengia as a tool in molecular clock analyses, much better preserved specimens are required that permit assignment to the level of family or at least order. More intriguing in this regard is the Permian species Capimirinus riopretensis, which is regarded as a pleurocarpous moss (Christiano de Souza et al., 2012). Present divergence time estimates point to a Jurassic age of pleurocarps (Newton et al., 2007) and could therefore be misleading. On the other hand, this compression fossil does not show a peristome, and thus could also belong to an earlier radiation that was at some later point replaced by other lineages. Generally we need to incorporate the fossil record in more detail in future divergence time estimates of mosses, especially the rich Cenozoic diversity with numerous well preserved representatives of extant genera (Frahm and Newton, 2005; Frahm, 2010; Ignatov and Perkovsky, 2011).

54

J. Heinrichs et al. / Review of Palaeobotany and Palynology 204 (2014) 50–55

4.2. Sporophytes in the fossil record of mosses Sporophytes of mosses are usually robust and may persist for more than a year. Considering their robustness and commonness within the extant diversity, one might expect to find them with some frequency also in the fossil record. However, only very few moss fossils with sporophytes are known from the Paleozoic and Mesozoic, including Saksenaphyllites saksenae, Capimirinus riopretensis, Muscites fontinaloides, and Ningchengia jurassica. Ningchengia thus represents one of the oldest moss fossils with sporophytes but is, like most other Mesozoic moss fossils, not very well preserved. The oldest exquisitely preserved sporophytes of mosses come from the Upper Cretaceous of North America. They represent the peristomate type and belong to either Polytrichopsida or Bryopsida. Eopolytrichum antiquum Konopka, Herend., G.L. Merr. & P. Crane shows a suite of gametophytical and sporophytical characters of extant Polytrichaceae (Konopka et al., 1997); Campylopodium allonense Konopka, Herend. & P. Crane without much doubt belongs to an extant genus of Dicranaceae (Konopka et al., 1998). Several Cenozoic mosses are comparably well preserved and provide insights into the morphological details of the sporophyte (Frahm, 2010; Heinrichs et al., 2013). 4.3. Incomplete fossil record of mosses Krassilov and Schuster (1984) discuss the incomplete fossil record of the mosses during the Paleozoic and Mesozoic and propose that early mosses may have rapidly evolved into drought-tolerant, saxicolous types occurring in habitats in which fossilization is unlikely. This hypothesis is not plausible considering the presence of Sphagnopsida in the early diverging lineages of mosses. The Sphagnopsida crown group has a wetland ecology, as have at least some species of Polytrichopsida. It is therefore more likely that many moss fossils have not yet been recognized as such. Only recently, several new late Paleozoic and Mesozoic mosses and putative moss remains have been described (Smooth and Taylor, 1986; Ignatov, 1992; Chandra, 1995; Ignatov and Shcherbakov, 2007, 2009, 2011; Ignatov et al., 2011; Christiano de Souza et al., 2012; Hübers and Kerp, 2012; Moisan et al., 2012; Barclay et al., 2013; Hübers et al., 2013; Bomfleur et al., 2014), indicating that a careful search in appropriate deposits will likely lead to new discoveries, allowing for a better understanding of moss evolution through time. Acknowledgments This study was supported by funds from the National Basic Research Program of China (973 Program 2012CB821901) and the Team Program of Scientific Innovation and Interdisciplinary Cooperation, CAS (2013– 2015). We thank Hongtao Cai and Shaolin Zheng for their help in collecting the specimens, and Jingjing Tan and Dong Ren for the permission to use their figure (as Fig. 1). References Amaral, P.G.C., Bernardes de Oliveira, M., Ricardi-Branco, F., Broutin, J., 2004. Presencia de Bryopsida fértil en los niveles Westfalianos del subgrup Itararé, Cuenca de Paraná, Brasil. Trop. Bryol. 25, 101–110. Barclay, R.S., McElwain, J.C., Duckett, J.G., van Es, M.H., Mostaert, A.S., Pressel, S., Sageman, B.B., 2013. New methods reveal oldest known fossil epiphyllous moss: Bryiidites utahensis gen. et sp. nov. (Bryidae). Am. J. Bot. 100, 2450–2457. Bomfleur, B., Klymiuk, A.A., Taylor, E.L., Taylor, T.N., Gulbranson, E.L., Isbell, J.L., 2014. Diverse bryophyte mesofossils from the Triassic of Antarctica. Lethaia 47, 120–132. Chandra, S., 1995. Bryophytic remains from the Early Periman sediments of India. Palaeobotanist 43, 16–48. Chen, W., Ji, Q., Liu, D.Y., Zhang, Y., Song, B., Liu, X.Y., 2004. Isotope geochronology of the fossil-bearing beds in the Daohugou area, Ningcheng, Inner Mongolia. Geol. Bull. China 23, 1165–1169. Christiano de Souza, I.C., Ricardi Branco, F.S., Léon Vargas, Y., 2012. Permian bryophytes of western Gondwanaland from the Paraná basin in Brazil. Palaeontology 55, 229–241. Clarke, J., Warnock, R.C.M., Donoghue, P.C.J., 2011. Establishing a time-scale for plant evolution. New Phytol. 192, 266–301.

Cox, C.J., Goffinet, B., Shaw, A.J., Boles, S.B., 2004. Phylogenetic relationships among the mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomic compartments. Syst. Bot. 29, 234–250. Cox, C.J., Goffinet, B., Wickett, N.J., Boles, S.B., Shaw, A.J., 2010. Moss diversity. A molecular phylogenetic analysis of genera. Phytotaxa 9, 175–195. Fiz-Palacios, O., Schneider, H., Heinrichs, J., Savolainen, V., 2011. Diversification of land plants: insights from a family-level phylogenetic analysis. BMC Evol. Biol. 11, 341. Frahm, J.-P., 2010. Die Laubmoosflora des baltischen Bernsteinwaldes. Weissdorn, Jena. Frahm, J.-P., Newton, A.E., 2005. A new contribution to the moss flora of Dominican amber. Bryologist 108, 526–536. Gao, K.-Q., Ren, D., 2006. Radiometric dating of ignimbrite from Inner Mongolia provides no indication of a post-middle Jurassic age for the Daohugou Beds. Acta Geol. Sin. 81, 42–45 (English Version). Goffinet, B., Buck, W.R., 2004. Systematics of the Bryophyta (mosses): from molecules to a revised classification. Monogr. Syst. Bot. Mo. Bot. Gard. 98, 205–239. He, H.Y., Wang, X.L., Zhou, Z.H., Zhu, R.X., Jin, F., Wang, F., Ding, X., Boven, A., 2004. 40 Ar/39Ar dating of ignimbrite from Inner Mongolia, northeastern China, indicates a post-Middle Jurassic age for the overlying Daohugou Bed. Geophys. Res. Lett. 31, L20609. Heinrichs, J., Vitt, D.H., Schäfer-Verwimp, A., Ragazzi, E., Marzaro, G., Grimaldi, D.A., Nascimbene, P.C., Feldberg, K., Schmidt, A.R., 2013. The moss Macromitrium richardii (Orthotrichaceae) with sporophyte and calyptra enclosed in Hymenaea resin from the Dominican Republic. Pol. Bot. J. 58, 221–230. Huang, D., Nel, A., Shen, Y., Selden, P.A., Lin, Q., 2006. Discussions on the age of the Daohugou fauna — evidence from invertebrates. Prog. Nat. Sci. 16, 309–312. Hübers, M., Kerp, H., 2012. Oldest known mosses discovered in Mississippian (Late Visean) strata of Germany. Geology 40, 755–758. Hübers, M., Kerp, H., Schneider, J.W., Gaitzsch, B., 2013. Dispersed plant mesofossils from the Middle Mississippian of eastern Germany: bryophytes, pteridophytes and gymnosperms. Rev. Palaeobot. Palynol. 193, 38–56. Ignatov, M.S., 1990. Upper Permian mosses from the Russian Platform. Palaeontographica Abt. B 217, 147–189. Ignatov, M.S., 1992. Bryokhutuliinia jurassica, gen. et spec. nova, a remarkable fossil moss from Mongolia. J. Hattori Bot. Lab. 71, 377–388. Ignatov, M.S., Perkovsky, E.E., 2011. Mosses from Rovno amber (Ukraine). Arctoa 20, 1–18. Ignatov, M.S., Shcherbakov, D.E., 2007. Did pleurocarpous mosses originate before the Cretaceous? In: Newton, A.E., Tangney, R. (Eds.), Pleurocarpous Mosses: Systematics and Evolution. Systematics Association Special Volume 71. Taylor & Francis / CRC Press, Boca Raton, pp. 321–336. Ignatov, M.S., Shcherbakov, D.E., 2009. A new fossil moss from the Lower Permian of the Russian Far East. Arctoa 18, 201–212. Ignatov, M.S., Shcherbakov, D.E., 2011. Lower Triassic mosses from Yaman Us (Mongolia). Arctoa 20, 65–80. Ignatov, M.S., Karasev, E.V., Sinitza, S.M., 2011. Upper Jurassic mosses from Baigul (Transbaikalia, South Siberia). Arctoa 20, 43–64. Ji, Q., Liu, Y., Chen, W., Ji, S., Lu, J., You, H., Yuan, C., 2005. On the geological age of Daohugou biota. Geol. Rev. 51, 609–612. Kenrick, P., Wellman, C.A., Schneider, H., Edgecombe, G.D., 2012. A timeline for terrestrilization: consequences for the Carbon cycle in the Palaeozoic. Phil. Trans. R. Soc. B 367, 519–536. Konopka, A., Herendeen, P.S., Smith Merill, G.R., Crane, P.R., 1997. Sporophytes and gametophytes of Polytrichaceae from the Campanian (Late Cretaceous) of Georgia, USA. Int. J. Plant Sci. 158, 489–499. Konopka, A., Herendeen, P.S., Crane, P.R., 1998. Sporophytes and gametophytes of Dicranaceae from the Santonian (Late Cretaceaeus) of Georgia, USA. Am. J. Bot. 85, 714–723. Krassilov, V., 1973. Mesozoic bryophytes from the Bureja basin, Far East of the USSR. Palaeontogr. B 143, 95–105 (plates 41–51). Krassilov, V.A., Schuster, R.M., 1984. Paleozoic and mesozoic fossils. In: Schuster, R.M. (Ed.), New Manual of Bryology. The Hattori Botanical Laboratory, Nichinan, pp. 1172–1193. Li, N., Li, Y., Wang, L.-X., Zheng, S.-L., Zhang, W., 2004. A new Weltrichia Braun in north China with a special bennettitalean male reproductive organ. Acta Bot. Sin. 46, 1269–1275. Lignier, O., 1914. Sure une mousse hoillière à structure conservée. Bull. Soc. Linn. Normandie 6, 128–131. Liu, Y., Liu, Y., Ji, S., Yang, Z., 2006. U-Pb zircon age for the Daohugou Biota at Ningcheng of Inner Mongolia and comments on related issues. Chin. Sci. Bull. 51, 2634–2644. Magallon, S., Hilu, K.W., Quandt, D., 2013. Land plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. Am. J. Bot. 100, 556–573. Magombo, Z.L.K., 2003. The phylogeny of basal peristomate mosses: evidence from cpDNA, and implications for peristome evolution. Syst. Bot. 28, 24–38. Meng, J., Hu, Y., Wang, Y., Wang, X., Li, C., 2006. A Mesozoic gliding mammal from northeastern China. Nature 444, 889–893. Mi, J., Sun, C., Sun, Y., Cui, S., Ai, Y., 1996. Early–Middle Jurassic Phytoecology and Coal Accumulating Environments In Northern Hebei and Western Liaoning. Geological Publishing House, Beijing. Moisan, P., Voigt, S., Schneider, J.W., Kerp, H., 2012. New fossil bryophytes from the Triassic Madygen Lagerstätte (SW Kyrgyzstan). Rev. Palaeobot. Palynol. 187, 29–37. Neuburg, M.F., 1960. Leafy mosses from the Permian deposits of Angaraland (in Russian). Akademiia Nauk CCCP, Trudy Geologićeskij Institut, 9, pp. 1–104. Newton, A.E., Wikström, N., Bell, N., Forrest, L.L., Ignatov, M.S., 2007. Dating the diversification of the pleurocarpous mosses. In: Newton, A.E., Tangney, R. (Eds.), Pleurocarpous

J. Heinrichs et al. / Review of Palaeobotany and Palynology 204 (2014) 50–55 Mosses: Systematics and Evolution. Systematics Association Special Volume 71. Taylor & Francis / CRC Press, Boca Raton, pp. 337–366. Oostendorp, C., 1987. The bryophytes of the Paleozoic and Mesozoic. Bryophyt. Bibl. 34, 5–112 (Plates I–XLIX). Peng, N., Liu, Y., Kuang, H., Jiang, X., Xu, H., 2012. Stratigraphy and geochronology of vertebrate fossil-bearing Jurassic strata from Linglongta, Jianchang County, western Liaoning, northeastern China. Acta Geol. Sin. 86, 1326–1339 (English Edition). Rasnitsyn, A.P., Zhang, H., 2004. Composition and age of the Daohugou hymenopteran (Insecta, Hymenoptera = Vespida) assemblage from Inner Mongolia. Palaeontology 47, 1507–1517. Ren, D., Krzeminski, W., 2002. Eoptychopteridae (Diptera) from the Middle Jurassic of China. Ann. Zool. 52, 207–210. Ren, D., Gao, K., Guo, Z., Ji, S., Tan, J., Song, Z., 2002. Stratigraphic division of the Jurassic in the Daohugou area, Ningcheng, Inner Mongolia. Geol. Bull. China 21, 584–591. Ren, D., Labandeira, C.C., Santiago-Blay, J.A., Rasnitsyn, A., Shih, C.K., Bashkuev, A., Logan, M.A.V., Hotton, C.L., Dilcher, D., 2009. A probable pollination mode before angiosperms: Eurasian, long-proboscid scorpionflies. Science 326, 840–847. Renault, B., Zeiller, R., 1885. Sur des mousses de l'èpoque houillère. C.R. Hebd. Seances Acad. Sci. 100, 660–662 (Paris). Renzaglia, K.S., Schuette, S., Duff, R.J., Shaw, A.J., Mishler, B.D., Duckett, J.G., 2007. Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110, 179–213. Shaw, A.J., Szövényi, P., Shaw, B., 2011. Bryophyte diversity and evolution. Windows into the early evolution of land plants. Am. J. Bot. 98, 1–18. Shen, Y.-B., Chen, P.-J., Huang, D.-Y., 2003. Age of the fossil conchostracans from Daohugou of Ningcheng, Inner Mongolia. J. Stratigr. 27, 311–313. Shih, C., Liu, C., Ren, D., 2009. The earliest fossil record of pelecinid wasps (Insecta: Hymenoptera: Proctotrupoidea: Pelecinidae) from Inner Mongolia, China. Ann. Entomol. Soc. Am. 102, 20–38. Smith, A.J.E., 1978. The Moss Flora of Britan & Ireland. Cambridge University Press, Cambridge. Smooth, E.L., Taylor, T.N., 1986. Structurally preserved fossil plants from Antarctica, II. A Permian moss from the Transantarctic Mountains. Am. J. Bot. 73, 1683–1691. Tan, J.J., Ren, D., 2002. Palaeoecology of insect community from Middle Jurassic Jiulongshan Formation in Ningcheng County, Inner Mongolia, China. Acta Zootaxon. Sin. 27, 428–434.

55

Tan, J., Ren, D., 2009. Mesozoic Archostematan Fauna from China. Science Press, Beijing. Taylor, T.N., Taylor, E., Krings, M., 2009. Paleobotany. The Biology and Evolution of Fossil Plants. Elsevier/Academic Press Inc., Burlington MA, London, San Diego CA, New York NY, USA. Thomas, B.A., 1972. A probable moss from the Lower Carboniferous of the Forest of Dean, Gloucestershire. Ann. Bot. 36, 155–161. Tsubota, H., De Luna, E., González, D., Ignatov, M.S., Deguchi, H., 2004. Molecular phylogenetics and ordinal relationships based on analyses of a large-scale data set of 600 rbcL sequences of mosses. Hikobia 14, 149–170. Volkmar, U., Knoop, V., 2010. Introducing intron locus cox1i624 for phylogenetic analyses in bryophytes: ON the issue of Takakia as sister genus to all other extant mosses. J. Mol. Evol. 70, 506–518. Wang, X., Krings, M., Taylor, T.N., 2010. A thalloid organism with possible lichen affinity from the Jurassic of northeastern China. Rev. Palaeobot. Palynol. 162, 591–598. Wang, Y., Shih, C., Szwedo, J., Ren, D., 2013. New fossil palaeontinids (Hemiptera, Cicadomorpha, Palaeontinidae) from the Middle Jurassic of Daohugou, China. Alcheringia 37, 19–30. Zhang, F.-J., 2010. Records of bizarre Jurassic brachycerans in the Daohugou biota, China (Diptera, Brachycera, Archisargidae and Rhagionemestriidae). Palaeontology 53, 307–317. Zhang, F., Zhou, Z., Xu, X., Wang, X., Sullivan, C., 2008. A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 455, 1105–1108. Zhang, K., Yang, D., Ren, D., 2006. The first snipe fly (Diptera: Rhagionidae) from the Middle Jurassic of Inner Mongolia, China. Zootaxa 1134, 51–57. Zheng, S.-L., Zhang, L.-J., Gong, E.-P., 2003. A discovery of Anomozamites with reproductive organs. Acta Bot. Sin. 45, 667–672. Zhou, Z., Zheng, S., Zhang, L., 2007. Morphology and age of Yimaia (Ginkgoales) from Daohugou Village, Ningcheng, Inner Mongolia, China. Cretac. Res. 28, 348–362. Zhou, C.-F., Wu, S., Martin, T., Luo, Z.X., 2013. A Jurassic mammaliform and the earliest mammalian evolutionary adaptations. Nature 500, 163–167.