Research articleBurmese amber fossils bridge the gap in the Cretaceous record of polypod ferns
Introduction
Incongruences between divergence time estimates obtained from the fossil record and DNA sequence variation have been recognized for many lineages of organisms (Benton and Ayala, 2003). In particular, the age of the crown group diversification of angiosperms continues to be controversial because of conflicts between the age estimates based on DNA sequence data and fossil evidence (Bell et al., 2010, Zeng et al., 2014, Magallón et al., 2015). Less attention was given so far to the incongruence concerning the Cretaceous diversification of derived ferns (=core Polypodiales). The hypothesis of a diversification of polypod ferns coinciding with the rise of the angiosperms has been established on the basis of DNA based divergence time estimates (Lehtonen et al., 2012, Schneider et al., 2004, Schuettpelz and Pryer, 2009). Precursors of this hypothesis were introduced before the advent of DNA based dating (Lovis, 1977, Rothwell, 1996, Smith, 1972), but were challenged by the rarity of Cretaceous fossils of Polypodiales (Collinson, 1996, Collinson, 2001, Skog, 2001). This pattern is unlikely to be explained by rock bias against the preservation of ferns because Jurassic and Cretaceous fossils are known for many other fern lineages such as Cyatheales, Gleicheniales, Osmundales, Salviniales, and Schizaeales (Hu and Taylor, 2014, Kvaček et al., 2006, Mohr et al., 2015, Skog, 2001, Smith et al., 2003, Smith et al., 2015, Tidwell and Ash, 1994, Vera and Herbst, 2015). As pointed out in studies on the spore record of ferns (Nagalingum et al., 2002), the microfossil record suggests a decline of ferns in the late Mesozoic instead of the Cretaceous to Eocene radiation suggested by DNA-based divergence time estimates (Schneider et al., 2004). Thus, the paucity of fossil evidence supporting the occurrence of polypod ferns in the Early Cretaceous somewhat resembles the pattern observed in angiosperms (Magallón et al., 2015) and challenges the hypothesis of a Cretaceous radiation of derived ferns.
However, the apparent conflict between fossil evidence and DNA based divergence time estimates may be solved by the discovery of new Cretaceous polypod fossils. In particular, fossil evidence is required to confirm the presence of representatives of early-diverging lineages of polypod ferns, such as Dennstaedtiaceae and Lindsaeaceae in the Late Jurassic and Early Cretaceous as predicted by DNA based divergence time estimates (see Lehtonen et al., 2012, Schneider et al., 2004, Schuettpelz and Pryer, 2009). So far, only a single study provided unequivocal evidence for a Cretaceous occurrence of these ferns (Schneider and Kenrick, 2001) by verifying the apomorphic root cortex anatomy of lindsaeoid ferns (Lindsaeaceae sensu Christenhusz et al., 2011) in fossilized roots attached to Albian Tmesipteris stems. As shown by this study, polypod ferns can be identified unequivocally in the fossil record as long as apomorphic character states are preserved. The polypod clade can be recognized by the apomorphic sporangium type, i.e. a sporangium with a vertical, broken annulus ring containing a differentiated stomium (Schneider, 1996, Schneider et al., 2009). The largely poor preservation of many compression fossils disables the study of these structures. However, in the recent years, it has been shown that such sporangia are sometimes preserved as amber inclusions (Grimaldi et al., 2002, Lóriga et al., 2014).
Approximately 100 million-year-old Burmese amber (Grimaldi et al., 2002) provides a unique opportunity to study the composition of terrestrial vegetation during the Cretaceous-Terrestrial Revolution (KTR). This period is marked by the rise of angiosperms, social insects, and early mammals (Benton, 2010, Lloyd et al., 2008, Meredith et al., 2011) but also by the fact that terrestrial diversity exceeded marine diversity for the first time (Vermeij and Grosberg, 2010). Discoveries based on Burmese amber fossils have provided important insights to the diversification of bryophytes (Feldberg et al., 2014, Hedenäs et al., 2014, Heinrichs et al., 2012, Heinrichs et al., 2014a, Heinrichs et al., 2014b), the evolution of insect-mediated pollination (Cardinal and Danforth, 2013, Poinar and Danforth, 2006, Ren et al., 2009), and the early diversification of ants (Barden and Grimaldi, 2014). However, little attention has been given to ferns in Burmese amber despite the occurrence of dispersed polypod sporangia (Grimaldi et al., 2002) and the polypod-like fossil Cretacifilix fungiformis (Poinar and Buckley, 2008).
Here, we aim to show that diverse polypod ferns occurred in the mid-Cretaceous forests of Myanmar. To achieve this we studied fragments of ferns preserved in Burmese amber including isolated sporangia and leaf fragments. Special attention was given to sporangia showing the morphologically unique catapult mechanism representing the apomorphy of polypod ferns (Schneider, 1996, Schneider et al., 2009). This unique sporangium type is found in more than 95% of the Polypodiales but not in any other fern. The presence of these sporangia is therefore considered as convincing evidence for an occurrence of polypod ferns in the mid-Cretacous and is thus comparable with the tricolpate pollen type widely recognized as significant evidence for the occurrence of eudicots (Magallón et al., 2015).
Section snippets
Material and methods
The Burmese amber collections of the American Museum of Natural History (New York), the Natural History Museum (London), and several private amber collections were screened for inclusions of ferns (Table 1). Burmese amber derives from the famous amber localities near the village of Tanai which is located on the Ledo Road about 105 km north of Myitkyina in Kachin State, Myanmar. Biostratigraphic studies suggested a late Albian age of the amber-bearing sediment (Cruickshank and Ko, 2003), hence
Dispersed sporangia
Three amber fragments (AMNH-Bu-342, AMNH-Bu-731, and AMNH-Bu-1612, Table 1) contain numerous isolated, stalked sporangia that showed a vertically oriented annulus with a well-marked stomium including epi- and hypostomium cells (Fig. 1A–D). Fragment AMNH-Bu-1612 includes an aborted sporangium of ca 210 μm size and several mature sporangia of 220–260 μm size (Fig. 1B, D), of which one contained trilete spores 20–32 μm in diameter (Fig. 1D). Fragment AMNH-BU-342 contains mature polypod sporangia of
Amber fossils as a source to understand fern evolution
Until recently, amber inclusions have hardly been considered as a relevant source of information in studies on the evolutionary history of ferns. The lack of attention given to ferns in amber is likely caused by the rarity and small size of the preserved fragments including separated indusia and sporangia (Schmidt and Dörfelt, 2007), isolated hairs (Schmidt et al., 2010, Pérez-de la Fuente et al., 2012), or small leaf-fragments that do not show many characters of taxonomic value (Caspary and
Conclusions
The new fossil evidence from Burmese amber is consistent with DNA based divergence time estimates (see Schneider et al., 2004, Schuettpelz and Pryer, 2009), which predicted the occurrence of basal lineages of polypods in the mid-Cretaceous. Most importantly, the source forests of Burmese amber show a distinct fern diversity which is so far exclusively formed by polypods, whereas all other previously reported Cretaceous fern floras were dominated by other fern orders including Cyatheales,
Acknowledgements
We thank David A. Grimaldi and Paul C. Nascimbene (AMNH New York) as well as Lee Davies, Hilary Ketchum, and Claire Mellish (NHM London) for providing access to museum collections. We are grateful to Beate Stolz (Bremen), Carsten Gröhn (Glinde) and James Zigras (Paramus) for their kind permission to illustrate the specimens shown in Fig. 3.
References (73)
- et al.
Bryophytes of the Burmese amber forest: amending and expanding the circumscription of the Cretaceous moss genus Vetiplanaxis
Rev. Palaeobot. Palynol.
(2014) - et al.
The leafy liverwort Frullania (Jungermanniopsida) in the Cretaceous amber forest of Myanmar
Rev. Palaeobot. Palynol.
(2012) - et al.
The extant liverwort Gackstroemia (Lepidolaenaceae, Porellales) in Cretaceous amber from Myanmar
Rev. Palaeobot. Palynol.
(2014) - et al.
An acrocarpous moss in Cretaceous amber from Myanmar
Cret. Res.
(2014) - et al.
A new schizaeaceous fern, Schizaeopsis ekrtii sp. nov., and its in situ spores from the Upper Cretaceous (Cenomanian) of the Czech Republic
Rev. Palaeobot. Palynol.
(2006) - et al.
Early Cretaceous flora from Vale Painho (Lusitanian basin, western Portugal): an integrated palynological and mesofossil study
Rev. Palaeobot. Palynol.
(2011) - et al.
Ruffordia goeppertii (Schizaeales, Anemiaceae) – a common fern from the Lower Cretaceous Crato Formation of northeast Brazil
Cret. Res.
(2015) - et al.
The Albian fern flora of Alexander Island, Antarctica
Cret. Res.
(2015) - et al.
Fern spore diversity and abundance in Australia during the Cretaceous
Rev. Palaeobot. Palynol.
(2002) Pteridophyte evolution: an often underappreciated phytological success story
Rev. Palaeobot. Palynol.
(1996)
Evidence of Cenozoic Matoniaceae from Baltic and Bitterfeld amber
Rev. Palaeobot. Palynol.
An Early Cretaceous root-climbing epiphyte (Lindseaceae) and its significance for calibrating the diversification of polypodiaceous ferns
Rev. Palaeobot. Palynol.
Age constraint on Burmese amber based on U–Pb dating of zircons
Cret. Res.
Ecology of some Late Triassic to Early Cretaceous ferns in Eurasia
Rev. Palaeobot. Palynol.
New cyathealean tree ferns from the Cretaceous of South Africa: Natalipteris wildei gen. et sp. nov. and Kwazulupteris schaarschmidtii gen. et sp. nov
J. Afr. Earth Sci.
A review of molecular-clock calibrations and substitution rates in liverworts, mosses, and hornworts, and a timeframe for a taxonomically cleaned-up genus Nothoceros
Mol. Phyl. Evol.
A diverse ant fauna from the Mid-Cretaceous of Myanmar (Hymenoptera: Formicidae)
PLOS ONE
The age and diversification of the angiosperms re-visited
Am. J. Bot.
The origins of modern biodiversity on land
Phil. Trans. R. Soc. B
Dating the tree of life
Science
Bees diversified in the age of eudicots
Proc. R. Soc. B
Die Flora des Bernsteins und anderer fossiler Harze des ostpreußischen Tertiärs
Abh. kgl. preuss. geol. Landesanst. N. F.
A linear sequence of extant families and genera of lycophytes and ferns
Phytotaxa
Early Cretaceous angiosperm invasion of Western Europe and major environmental changes
Ann. Bot.
What use are fossil ferns? – 20 years on: with a review of the fossil history of extant pteridophyte families and genera
Cainozoic ferns and their distribution
Brittonia
Geology of an amber locality in the Hukawng valley, Northern Myanmar
J. Asian Earth Sci.
jModelTest 2: more models, new heuristics and parallel computing
Nat. Meth.
Bayesian phylogenetics with BEAUTi and the BEAST 1.7
Mol. Biol. Evol.
Epiphytic leafy liverworts diversified in angiosperm-dominated forests
Sci. Rep.
Der Bernstein und die in ihm befindlichen Pflanzenreste der Vorwelt
Grammitis succinea, the first new world fern found in amber
Am. Fern J.
Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance
Am. Mus. Nov.
A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood
Syst. Biol.
rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns
Proc. Natl. Acad. Sci. U.S.A.
Molecular and morphological evidence challenges the records of the extant Ptilidium pulcherrimum in Eocene Baltic amber
PLOS ONE
Cited by (36)
Microlepia burmasia sp. nov., a new fern species from mid-Cretaceous Kachin amber of norther Myanmar (Dennstaedtiaceae, Polypodiales)
2023, Cretaceous ResearchCitation Excerpt :Dennstaedtiaceae have ten extant genera (PPG I, 2016; Du et al., 2021), but at least four genera (Blotiella, Histiopteris, Hypolepis and Paesia) are distinct from our fossil in that they possess monolete spores (Kramer, 1990a; Regalado et al., 2017a). Among remaining genera, the genus Monachosorum is exindusiate, while Pteridium has elongate marginal sori covered by a false outer and true, inner indusium (Kramer, 1990a; Schneider et al., 2016). In addition, indusial shape that is also a vital factor for morphological resolution.
Liverworts from Cretaceous amber
2021, Cretaceous ResearchNew insights into the evolution of the fern family Dennstaedtiaceae from an expanded molecular phylogeny and morphological analysis
2020, Molecular Phylogenetics and EvolutionRe-evaluation of the systematic position of the Jurassic–Early Cretaceous fern genus Coniopteris
2020, Cretaceous ResearchA mid-Cretaceous tree fern of Thyrsopteridaceae (Cyatheales) preserved in Myanmar amber
2020, Cretaceous ResearchCitation Excerpt :Among the novelties recovered from these deposits are several ferns (Poinar, 2008; Schneider et al., 2016; Regalado et al., 2017a,b,c). Those that have been described so far belong to the Polypodiales (sensu PPG 1, 2016) and are significant not only in giving an idea of fern diversity during the mid-Cretaceous, but also in providing minimum-age estimates for dating clades in phylogenetic analyses based DNA sequences (Schneider et al., 2016). The present study describes a distinctive fern preserved in Myanmar amber.