Review of Palaeobotany and Palynology 169 (2012) 21–28

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Review of Palaeobotany and Palynology

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Research paper

The leafy liverwort Frullania (Jungermanniopsida) in the Cretaceous amberforest of Myanmar☆

Jochen Heinrichs a,⁎, M. Elena Reiner-Drehwald a, Kathrin Feldberg a, Matt von Konrat b, Jörn Hentschel c,Jiří Váňa d, David A. Grimaldi e, Paul C. Nascimbene e, Alexander R. Schmidt f

a Georg-August-Universität Göttingen, Abteilung Systematische Botanik, Albrecht-von-Haller-Institut für Pflanzenwissenschaften, Untere Karspüle 2, 37073 Göttingen, Germanyb Department of Botany, The Field Museum, 1400 South Lake Shore Drive, Chicago, IL 60605–2496, USAc Friedrich-Schiller-Universität Jena, Institut für Spezielle Botanik mit Herbarium Haussknecht und Botanischem Garten, Philosophenweg 16, 07743 Jena, Germanyd Department of Botany, Charles University, Benátská 2, 128 01 Praha 2, Czech Republice Division of Invertebrate Zoology, American Museum of Natural History, 79th Street at Central Park West, New York, NY 10024, USAf Georg-August-Universität Göttingen, Courant Research Centre Geobiology, Goldschmidtstraße 3, 37077 Göttingen, Germany

☆ "In den Abgründen der Zeit Taxonomie zu betreib("Running the gauntlet of taxonomy in the vast abysses ochallenge.") Riclef Grolle, 2003 in litt.⁎ Corresponding author.

E-mail address: jheinri@uni-goettingen.de (J. Heinri

0034-6667/$ – see front matter © 2011 Elsevier B.V. Alldoi:10.1016/j.revpalbo.2011.10.002

a b s t r a c t

a r t i c l e i n f o

Article history:Received 17 August 2011Received in revised form 28 September 2011Accepted 1 October 2011Available online 12 October 2011

Keywords:amberCretaceousFrullaniaceaeJungermanniidaeMesozoicPorellales

Examination of two pieces of amber from the mid-Cretaceous of Myanmar revealed seven inclusions of leafyliverworts that we assign to the extinct Frullania cretacea Hentschel et al. 2009. These inclusions show a suiteof characters that were not visible in the type specimen of F. cretacea. The new gametophytes consistentlydisplay rectangular to ovate underleaves that have two long-ciliate apical teeth in addition to 0–2 blunt lateralteeth. A narrow stylus is present on at least some leaves. The lobules usually form water sacs that are 1.2–2.3times longer thanwide, and are arranged at somedistance from the stem. The observed combination of characterstates is not present in extant crown group lineages of Frullania. A syninclusion in one of the amber pieces isinterpreted as a detached gynoecium of a second Cretaceous Frullania species and is described as F. baerlocheri,sp. nov. The subgynoecial underleaves of the syninclusion are suborbicular in shape, and allow for a separationof this species from F. cretacea. The described amber inclusions are the oldest representatives of an extantgenus of leafy liverworts known so far.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

The rise of the angiosperms in the Cretaceous (Brenner, 1996;Magallón and Castillo, 2009) led to a reorganization of terrestrial eco-systems and likely influenced the composition of epiphytic sporeplant communities (Schneider et al., 2004; Heinrichs et al., 2007;Newton et al., 2007). Reconstruction of these communities is ham-pered by their sparse fossil record (Krassilov and Schuster, 1984;Oostendorp, 1987; Taylor et al., 2009). However, the few known Juras-sic and Cretaceous liverworts have been placed in extinct genera, e.g.Cheirorhiza V.A. Krassilov (Krassilov, 1973), Diettertia J.T. Br. &Robinson (Schuster and Janssens, 1989), Kaolakia Heinrichs et al.(Heinrichs et al., 2011) and Sinolejeunea Yang et Wu (Yang andWu, 2011), or in form genera such asMarchantites Brongn. or ThallitesKidst. ex J. Walton (Cantrill, 1997). These fossils provide evidence formorphological changes in the liverwort lineages during the LateMesozoic.

en, ist ein besonderer Sport."f [geologic] time is a particular

chs).

rights reserved.

Only one extant genus of liverworts has been recognized fromMe-sozoic deposits, namely Frullania (Dumort.) Dumort., with the extinctspecies Frullania cretacea Hentschel et al. This species was describedbased on a single amber inclusion from the Albian of Myanmar(Hentschel et al., 2009b). Search for Cretaceous liverwort inclusionsin the amber collections of the American Museum of Natural History,New York, and the Natural History Museum in London revealed threefurther amber pieces with liverwort fragments. These new inclusionsallow for an emended description of F. cretacea, and provide evidencefor the presence of a second Albian-Cenomanian Frullania species.

2. Materials and methods

Two amber pieces containing fossil liverwort fragments werefound at the famous amber locality near the village of Tanai whichis located on the Ledo Road about 105 km north of Myitkyina inKachin State, Myanmar. They have been transferred to the amber col-lection of the American Museum of Natural History in New York bythe Swiss amber collector Federico Bärlocher. They include eight liv-erwort fragments, several remains of insects, fragments of vascularplants, microorganisms and detritus.

Both biostratigraphic data obtained from the amber-bearing sedi-ment and the amber inclusions indicate a mid-Cretaceous age of the

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amber (Grimaldi et al., 2002; Cognato and Grimaldi, 2009). Based onrecently discovered marine microfossils and ammonites from thisamber locality, Cruickshank and Ko (2003) suggest an Upper Albianage of the sediment. Thus, the liverwort inclusions have an age of ap-proximately 100 million years.

The original pieces of amber were separated into several segmentsin order to better access the inclusions for investigation and to enablean examination of both the dorsal and ventral sides. The obtainedamber fragments were ground and polished manually with a seriesof wet silicon carbide abrasive papers [grit from FEPA P 600–4000(25.8 μm to 5 μm particle size), firm Struers] to minimize light scat-tering for the investigation. All fragments are deposited in theamber collection of the American Museum of Natural History in

Plate I. Frullania cretacea Hentschel et al. from Burmese amber.

1. Piece of bark covered with Frullania cretacea gametophytes, dorsal view (AM2. Shoot sector, dorsal view, showing incubous foliation (AMNH Bu-FB 51); scal3. Overview of ventral side of gametophyte (AMNH Bu-FB 1 a); scale bar=5004. Dorsal leaf surface with mammillose cells (AMNH Bu-FB 1 a); scale bar=50 μ5. Portion of shoot showing water sacs and underleaves, ventral side (AMNH Bu

New York, collection numbers AMNH Bu-FB 1 a–g and AMNH Bu-FB51.

A third piece of amber with a liverwort inclusion was borrowedfrom the Natural History Museum London (BNHM PB V 67646). Prep-aration of this amber piece and micro-CT scanning were notpermitted.

All inclusions were studied using an incident-light microscope(Carl Zeiss Stemi 2000) and a transmitted-light microscope (CarlZeiss AxioScope A1), each equipped with a Canon 450D digital cam-era. In some instances, incident and transmitted light were used si-multaneously. The images of Plates I to IV were obtained fromseveral optical sections using the software package HeliconFocus 5.0for a better illustration of the three-dimensional inclusions.

NH Bu-FB 51); scale bar=500 μm.e bar=100 μm.μm.m.-FB 51); scale bar=100 μm.

Plate II. Frullania cretacea Hentschel et al. from Burmese amber.

1. Close-up showing underleaf and two water sacs (AMNH Bu-FB 1 a); scale bar=50 μm.2. Subgynoecial underleaf (AMNH Bu-FB 1 b); scale bar=50 μm.3. Stylus (arrowhead) and neighboring water sac (AMNH Bu-FB 1 d); scale bar=50 μm.4. Ventral view of fertile shoot sector with damaged gynoecium. White arrowhead points to damaged bracteole, behind it rests of perianth and/or bracts. Black arrow-

head points to developing subfloral innovation (AMNH Bu-FB 1 b); scale bar=100 μm.5. Close-up of damaged gynoecium. Arrowhead points to bracteole (AMNH Bu-FB 1 b); scale bar=50 μm.

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3. Results and discussion

3.1. Assignment of the amber inclusions to liverwort species

Class JUNGERMANNIOPSIDAOrder PORELLALESFamily FRULLANIACEAE

3.1.1. Frullania cretacea Hentschel, A.R. Schmidt & Heinrichs

Observed specimens: AMNH Bu-FB 1 a–f; AMNH Bu-FB 51 (Plates I–II);AMNH B-011 (holotype).

Emended diagnosis: Gametophytes with broadly rounded leaf lobesconsisting of smooth or mammillose cells, ventral lobules that usually

Plate III. Liverwort inclusion from Burmese amber (BNHM PB V 67646), likely representing Frullania.

1. Overview of gametophyte; scale bar=500 μm.2. Part of shoot, dorsal view; scale bar=200 μm.

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form cylindrically helmet-shaped to campanulate water sacs insertedat some distance from the stem, and narrow, lanceolate styli; as wellas rectangular to ovate underleaves that have two long-ciliate apicalteeth in addition to 0–2 blunt lateral teeth.

Emended description: Plants creeping in depressed patches, 300–700 μmin diameter, reddish brown, irregularly pinnately branched, stem diam-eter ca. (20–)30–50(−60) μm, rhizoids in bundles, up to ca. 300 μmlong, leaf lobes imbricate, less frequently remote, dorsally extendingca. 1/4–1 times the stemwidth beyond the farther edge of stem, (slightly)concave to nearly flat, entire, ca. 210–350 μm long and 220–300 μmwide, broadly rounded, cells in upper half of lobe subisodiametric, ca.15–27×15–20 μm in diameter, each dorsally with a distinctly protrud-ing, central mammilla, mammillae up to 5 μm high, with a diameter of6.5–8.0 μm or leaf cells smooth; cell walls possibly with triangular tosubnodulose trigones; mature leaf lobules cylindrically helmet-shapedto campanulate, inflated, forming ca. 120–220 μm long and70–160 μm broad water sacs, sacs 1.2–2.3 times longer than wide,often explanate in basal sectors of gametophytes [and rarely so inupper sectors], lying nearly parallel to stem or obliquely positionedwith upper part oriented towards stem, mouth separated from stemby distance slightly more than its diameter. Stylus narrow, inconspicu-ous, lanceolate, 2(−3) cells wide at base with 2–4 cells long unicellularapical part, possibly terminated by slime papilla. Underleaves distant,rectangular to elongate triangular or ovate, ca. 55–100 μm long,45–65 μm wide, with two slender apical teeth, these are 50–65 μmlong and 7–10 μm wide, base 1–2 cells wide, immediately narrowingto a single cell wide filament, 3–6 cells long, upper cells ca15–30×7–8 μm, ca. 2–4 times as long as wide, margins with 0–1(−2)blunt, short teeth or protruding cells, subgynoecial ones ovate, with1–2 slightly distant, blunt teeth on both lateral margins, these slighly

Plate IV. Holotype of Frullania baerlocheri Heinrichs et al., sp. nov. from Burmese amber (A

1. Overview of dorsal side; scale bar=500 μm.2. Overview of ventral side; scale bar=500 μm.3. Detail of ventral side with underleaf and lobules; scale bar=200 μm.4. Detached lobe fragment; scale bar=100 μm.5. Explanate lobule; scale bar=100 μm.6. Underleaf; scale bar=100 μm.7. Close-up of lobe cells; scale bar=20 μm.

larger than teeth of underleaves from sterile shoot sectors. Bracteole(one half conserved) elongate-triangular to obovate, deeply bilobed,apical lobes slender, with basal part two cells wide, and with elongateterminal cell, lateral lobe margins displaying two arcuate, forward-facing blunt, 3–4 cells long teeth. Other parts of female involucre notclearly reconstructible (only fragments of basalmost sectors of bractsand/or perianths conserved). One developing subfloral innovationpresent.

Until now, Frullania cretacea was only known from a single sterilegametophyte fragment (Grimaldi et al., 2002; Hentschel et al.,2009b). This plant fragment shows a limited suite of characters of ex-tant Frullania including reddish color, leaf cells with a single centralmammilla, lateral branching, and helmet-shaped water sacs, andwas tentatively placed in the subgenus Frullania. The newly describedgametophytes in the amber collection of the American Museum ofNatural History have the same size and leaf shape, as well as partlymammillose cells (Plate I, 4), and are here treated as further speci-mens of F. cretacea. These plants frequently possess underleaves,and in some leaves a stylus is visible (Plate II, 1–3; Fig. 1). Theshape of the stylus resembles modern Frullania species, whereas thenarrowly toothed, +/− rectangular underleaves are not knownamong extant representatives of the genus. Bilobed underleaves arecommon in Frullania; however, modern forms tend to have broaderunderleaves with triangular lobes rather than ciliately toothed onesas observed in F. cretacea. Underleaves with cilia are not completelyabsent in extant Frullania. For instance, they occur in F. bicornistipulaSpruce, a large neotropical species with acuminate leaves and broadlyreniform underleaves that are usually provided with two uniseriate,apical cilia (Spruce, 1884–1885). The presence of a single damagedbracteole does not enable us to determine the distribution of gynoeciaand androecia in F. cretacea. Nevertheless, the lack of androecia could

MNH Bu-FB 1 g).

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Fig. 1. Frullania cretacea. Reconstruction of ventral portion of shoot (based on AMNHBu-FB 1 d); scale bar=250 μm.

Fig. 2. Reconstruction of the juvenile gynoecium of Frullania baerlocheri; scalebar=500 μm.

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point to a dioicous species. The bracteole fragment and the subgynoe-cial underleaves are more elongate and more strongly toothed thanunderleaves from sterile shoot sectors, a phenomenon well knownfrom extant Frullania species. We are not sure if a structure belowthe bracteole represents an archegonium, or if the demolished struc-tures next to the bracteole belong to bracts or perianths (Plate II, 4, 5).It is also not clear whether these structures are connected to the basalpart of the bracteole, as is the case in many extant Frullania species.

The new F. cretacea inclusions provide evidence for a considerablelength variation of the water sacs (1.2–2.3 times longer than wide),which are consistently positioned at some distance from the stem. Itis possible that some sacs have been compressed and distorted duringor following their immersion and the subsequent diagenesis of theresin, and that the measured variation is partly an artifact of theplant's preservation in amber. However, the long sacs of some plantsand their distance from the stem are atypical of Frullania subg. Frullania.The combination of newly detected characters does not supportplacement of F. cretacea in one of the currently accepted sectionsand subgenera of Frullania (Hentschel et al., 2009a), and thus weconsider it to be an early crown group representative of this genus.The species could be affiliated to a clade composed of Frullaniasects. Obtusilobae Verd. and Intumescentes R.M. Schust. (Hentschelet al., 2009b). Extant sect. Obtusilobae includes small-sized specieswith cylindrically helmet-shaped to campanulate lobules arrangedat some distance from the stem. However, a lack of numerous diag-nostically relevant generative characters, as well as the peculiarunderleaves, prevent us from making a more definitive statementon the taxonomic position of F. cretacea.

The Natural History Museum in London houses another liverwortamber inclusion from Myanmar (BNHM PB V 67646, Plate III). This

inclusion is deeply embedded in the amber, and therefore less thanoptimally visible (due to considerable light scattering). It consists ofa branched, reddish-brown, leafy gametophyte that seems to haverounded leaf lobes accompanying individual water sacs. The plantlikely belongs to Frullania and has the size of F. cretacea; however, amore definitive assignment would require further preparation.

3.1.2. Frullania baerlocheri Heinrichs, M.E. Reiner, K. Feldberg, vonKonrat, Hentschel, Váňa et A.R. Schmidt, sp. nov.

Diagnosis: Gametophyte with incubously inserted, smooth [subgynoe-cial?] leaves with broadly rounded lobes often terminated by a shorttip, and ventral lobules that are narrowed towards apex, as well as sub-orbicular underleaves.

Description: Unbranched, reddish brown gametophyte fragment (likely ajuvenile gynoecium) with a length of 1.52 mm and a width of 1.86 mm.Stem ca 100 μm in diameter; subgynoecial leaves alternating, incubous,densely imbricate, deeply bilobed, entire, rather sharply folded, dorsallobes 0.8–1.1 mm long and 0.4–0.7 mm broad, much larger than ventrallobules, widely spreading, ovate, slightly concave, the freemargin curvedoutwards, apex broadly rounded or with a short triangular tip, ventrallobules with rectangular basal part that is gradually narrowed into anacute or ciliate apex or asymetrically triangular, ca 450–600 μm longand 210–350 μmbroad. Upper andmedian leaf cells almost isodiametric,ca. 20–27×20–30 μm, basal leaf cells short-rectangular to rectangular,cell walls thin, trigones small. Subgynoecial underleaves ca. 400 μmlong and 480 μm broad, widely spreading, plain, suborbicular, bifid toca. 0.1, laterally armed with 1–2 teeth.

Holotype: Amber inclusion AMNH Bu-FB 1 g, American Museum ofNatural History, New York, Plate IV.

Type locality: Tanai village on the Ledo Road about 105 km north ofMyitkyina in Kachin State, Myanmar.

Stratigraphic range and age: Lower Cretaceous: Upper Albian, about100 million years old.

Etymology: Named in honor of Federico Bärlocher (Ticino, Switzer-land) who kindly offered Myanmar amber pieces from his collectionto the American Museum of Natural History.

Many Mesozoic liverwort fossils are in a bad state of preservation,known only from imprints or consisting merely of sterile gametophyte

Fig. 3. Reconstruction of the subgynoecial underleaves of Frullania cretacea (right) andF. baerlocheri (left).

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fragments (Krassilov and Schuster, 1984; Oostendorp, 1987). Their in-complete preservation complicates their classification and may lead totaxonomic reassessments as additional material comes to light (Schus-ter and Janssens, 1989). On the other hand, we need to consider thema-terial that is currently available.

The liverwort fragment described above as Frullania baerlocheriresembles the gynoecium of extant Frullania species in having expla-nate lobules rather than water sacs (Fig. 2) and a reddish color, and istherefore assigned to this genus. Subgynoecial shoots of extant Frullaniaspecies usually have a larger diameter than sterile shoot sectors; hencewe expect the unknown sterile parts of F. baerlocheri to be somewhatsmaller than the structures described above. An affiliation of the inclu-sion to F. cretacea is unlikely because of the considerable size differ-ences, and the different shape and dentition of the subgynoecialunderleaves, being suborbicular in F. baerlocheri and rectangular toovate in F. cretacea (Fig. 3). Another difference is seen in the shape ofthe lobes, which are acute in F. baerlocheri and broadly rounded inF. cretacea. Acute lobes occur in several extant lineages of Frullania,e.g., subg. Thyopsiella Spruce and sect. Intumescentes sensu Hentschelet al. (2009a), so it is not impossible that F. baerlocheri and F. cretaceaare closely related. However, a more detailed systematic treatmentof F. baerlocheri will only be possible if further inclusions arerecovered.

3.1.3. PaleoenvironmentThe Cretaceous amber forest of Myanmar was highly tropical, and

likely located close to the seashore. It was dominated by various gym-nosperm trees, including members of Araucariaceae and taxodioidCupressaceae (‘Taxodiaceae’), but also included angiosperms, leptos-porangiate ferns and mosses (Grimaldi et al., 2002; Cruickshank andKo, 2003). Bell and York (2007) suggest that the moss Vetiplanaxispyrrhobryoides N.E. Bell grew as an epiphyte in this forest. The Frullaniaspecies of this study probably also occurred as epiphytes, as indicatedby a piece of bark covered with F. cretacea (AMNH Bu-FB 51; Plate I, 1).

3.1.4. Frullania fossil record and extant diversityFrullania is a subcosmopolitan, predominately epiphytic genus

that includes more than 300 extant species (Schuster, 1992;Hentschel et al., 2009a). Centers of diversity today occur in mountain-ous parts of the humid tropics and in warm temperate regions. Manyspecies of Frullania occur not only in moist but also in rather dry veg-etation. The fossil record of Frullania dates back to the mid Creta-ceous, with records in amber from Myanmar (Grimaldi et al., 2002;Hentschel et al., 2009; this study). Hundreds of Frullania inclusionsare known in Cenozoic ambers from the Baltic and Bitterfeld regions(Grolle, 1985; Grolle and Meister, 2004), and from the Dominican

Republic (Gradstein, 1993; Heinrichs and Schmidt, 2010). Currently,the following Frullania species are known as amber inclusions:

Myanmar, Albian (this paper):Frullania baerlocheri Heinrichs et al.Frullania cretacea Hentschel et al.

Baltic Region, Eocene and Bitterfeld, Oligocene (Grolle and Meister,2004):

Frullania (subg. Thyopsiella) acutata Casp.Frullania (subg. Diastaloba Spruce) baltica GrolleFrullania (subg. Thyopsiella) casparyi GrolleFrullania (subg. Dentatiloba Stotler & Crand.-Stot.) hamatosetaceaGrolleFrullania (subg. Thyopsiella) mammilligera GrolleFrullania (subg. Frullania) pycnoclada GrolleFrullania (subg. Australes [Verd.] S. Hatt.) schumannii (Casp.)GrolleFrullania (subg. Thyopsiella) truncata Casp.Frullania (subg. Microfrullania [R.M. Schust.] R.M. Schust.) variansCasp.

Dominican Republic, Miocene (Heinrichs and Schmidt, 2010):

Frullania (subg. Diastaloba) sp.

All these amber inclusions indicate that a diverse Frullania crowngroup was well established by the Early Cenozoic. However, it is re-markable that numerous Cretaceous amber lagerstätten (Lebanon,south-western France, Spain, and New Jersey), and even some Ceno-zoic amber deposits (such as Mexican amber and French Oise amber),have not yet yielded Frullania-inclusions, although other plant frag-ments including examples of epiphytic communities are preserved(e.g., Girard et al., 2009; Schmidt et al., 2010). Both the presenceand preservation of this common epiphyte possibly depend on thelocal climate, the microhabitats on the amber-bearing phorophyte,and on the kind and location of resin flows produced (Schmidt etal., 2006; Schmidt and Dilcher, 2007; Heinrichs and Schmidt, 2010).

Acknowledgments

We dedicate this paper to the memory of Riclef Grolle(1934–2004), a leading authority on liverwort inclusions in amber.We are indebted to Federico Bärlocher (Ticino) for offering amberpieces from his collection to the American Museum of Natural History,Christina Beimforde (Göttingen) for her help in the investigation ofmajor amber collections for bryophyte inclusions, and Uwe Drehwald(Göttingen) for advice. Lee Davies, Claire Mellish and Harald Schneiderfrom the Natural HistoryMuseum London arranged a loan of the amberinclusion BNHM PB V 67646. Financial support of the German ResearchFoundation (DFG, grant HE 3584/4) is gratefully acknowledged. This ispublication number 76 from the Courant Research Centre Geobiologythat is funded by the German Initiative of Excellence.

References

Bell, N.E., York, P.V., 2007. Vetiplanaxis pyrrhobryoides, a new fossil moss genus andspecies from middle Cretaceous Burmese amber. The Bryologist 110, 514–520.

Brenner, G.J., 1996. Evidence for the earliest stage of angiosperm pollen evolution: apaleoequatorial section from Israel. In: Taylor, D.W., Hickey, L.J. (Eds.), FloweringPlant Origin, Evolution and Phylogeny. Chapman & Hall, New York, pp. 91–115.

Cantrill, D.A., 1997. Hepatophytes from the Early Cretaceous of Alexander Island, Ant-arctica: systematics and paleoecology. International Journal of Plant Sciences 158,476–488.

Cognato, A.I., Grimaldi, D.A., 2009. One hundred million years of morphological conser-vation in a bark beetle (Coleoptera: Curculionidae: Scolytinae). Systematic Ento-mology 34, 93–100.

Cruickshank, R.D., Ko, K., 2003. Geology of an amber locality in the Hukawng valley,Northern Myanmar. Journal of Asian Earth Sciences 21, 441–445.

28 J. Heinrichs et al. / Review of Palaeobotany and Palynology 169 (2012) 21–28

Girard, V., Schmidt, A.R., Struwe, S., Perrichot, V., Breton, G., Néraudeau, D., 2009. Ta-phonomy and palaeoecology of mid-Cretaceous amber-preserved microorganismsfrom southwestern France. Geodiversitas 31, 153–162.

Gradstein, S.R., 1993. New fossil Hepaticae preserved in amber of the Dominican Republic.Nova Hedwigia 57, 353–374.

Grimaldi, D.A., Engel, M.S., Nascimbene, P., 2002. Fossiliferous Cretaceous amber fromMyanmar (Burma): its rediscovery, biotic diversity, and paleontological signifi-cance. American Museum Novitates 3361, 1–72.

Grolle, R., 1985. Monograph of Frullania in Baltic amber. Prace Muzeum Ziemi (War-saw) 37, 87–100.

Grolle, R., Meister, K., 2004. The Liverworts in Baltic and Bitterfeld Amber. Weissdorn,Jena.

Heinrichs, J., Schmidt, A.R., 2010. An inclusion of Frullania subgen. Diastaloba s. l.(Frullaniaceae, Porellales) in Dominican amber. Tropical Bryology 31, 91–94.

Heinrichs, J., Hentschel, J., Wilson, R., Feldberg, K., Schneider, H., 2007. Evolution ofleafy liverworts (Jungermanniidae, Marchantiophyta): estimating divergencetimes from chloroplast DNA sequences using penalized likelihood with integratedfossil evidence. Taxon 56, 31–44.

Heinrichs, J., Reiner-Drehwald,M.E., Feldberg, K., Grimaldi, D.A., Nascimbene, P.C., vonKonrat,M., Schmidt, A.R., 2011.Kaolakia borealisnov. gen. et sp. (Porellales, Jungermanniopsida):a leafy liverwort from the Cretaceous of Alaska. Review of Palaeobotany and Palynology165, 235–240.

Hentschel, J., von Konrat, M.J., Pócs, T., Schäfer-Verwimp, A., Shaw, A.J., Schneider, H.,Heinrichs, J., 2009a. Molecular insights into the phylogeny and subgeneric classifi-cation of Frullania Raddi (Frullaniaceae, Porellales). Molecular Phylogenetics andEvolution 52, 142–156.

Hentschel, J., Schmidt, A.R., Heinrichs, J., 2009b. Frullania cretacea, sp. nov. (Porellales,Jungermanniopsida), a leafy liverwort preserved in Cretaceous amber from Myan-mar. Cryptogamie Bryologie 30, 323–328.

Krassilov, V., 1973. Mesozoic bryophytes from the Bureja basin, Far East of the USSR.Palaeontographica Abteilung B 143, 95–105.

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.

Magallón, S., Castillo, A., 2009. Angiosperm diversification through time. AmericanJournal of Botany 96, 349–365.

Newton, A.E., Wikström, N., Bell, N., Forrest, L.L., Ignatov, M.S., 2007. Dating the diver-sification of the pleurocarpous mosses. In: Newton, A.E., Tangney, R. (Eds.), Pleur-ocarpous Mosses: Systematics and Evolution. : Systematics Association Special, vol.71. Taylor & Francis/CRC Press, Boca Raton, pp. 337–366.

Oostendorp, C., 1987. The bryophytes of the Paleozoic and Mesozoic. BryophytorumBibliotheca 34, 5–112 (Plates I-XLIX).

Schmidt, A.R., Dilcher, D.L., 2007. Aquatic organisms as amber inclusions and examplesfrom a modern swamp forest. Proceedings of the National Academy of Sciences ofthe United States of America 104, 16581–16585.

Schmidt, A.R., Ragazzi, E., Coppellotti, O., Roghi, G., 2006. A microworld in Triassicamber. Nature 444, 835.

Schmidt, A.R., Perrichot, V., Svojtka, M., Anderson, K.B., Belete, K.H., Bussert, R., Dörfelt,H., Jancke, S., Mohr, B., Mohrmann, E., Nascimbene, P.C., Nel, A., Nel, P., Ragazzi, E.,Roghi, G., Saupe, E.E., Schmidt, K., Schneider, H., Selden, P.A., Vávra, N., 2010. Cre-taceous African life captured in amber. Proceedings of the National Academy of Sci-ences of the United States of America 107, 7329–7334.

Schneider, H., Schuettpelz, E., Pryer, K.M., Cranfill, R., Magallón, S., Lupia, R., 2004. Fernsdiversified in the shadow of angiosperms. Nature 428, 553–557.

Schuster, R.M., 1992. The Hepaticae and Anthocerotae of North America east of thehundredth meridian, vol. 5. Field Museum of Natural History, Chicago.

Schuster, R.M., Janssens, J.A., 1989. On Diettertia, an isolated Mesozoic member of theJungermanniales. Review of Palaeobotany and Palynology 57, 277–287.

Spruce, R., 1884–1885. Hepaticae of the Amazon and the Andes of Peru and Ecuador.Transactions and Proceedings of the Botanical Society of Edinburgh 15, 1–590(Plates I-XXII).

Taylor, T.N., Taylor, E., Krings, M., 2009. Paleobotany. The Biology and Evolution of Fos-sil Plants. Academic Press, Burlington.

Yang, X.J., Wu, X.W., 2011. Sinolejeunea yimaensis gen. et sp. nov. (Hepaticae) from theMiddle Jurassic Yima Formation in Henan Province of China. Science China. EarthSciences 54, 228–232.