1 Introduction
Bryophytes compose the second most diverse phylum of land plants (
Goffinet and Shaw, 2009). However, as non-vascular plants, they are extremely underrepresented in the fossil record. As the largest group of bryophytes, Musci (mosses) have their fossils rarely reported, particularly in pre-Cenozoic strata (
Guo et al., 2016;
Ignatov and Maslova, 2021). The oldest fossil record related to moss is
Parafunaria sinensis discovered in the Cambrian Kaili Formation of Guizhou Province in China. It was proposed to be comparable to the living moss
Funaria hygrometrica due to its 4–5 whorled leaves, obvious costae, shapes of capsule and seta, and complex rhizoid (or foot) (
Yang et al., 2004). However, its unusually large size and antiquity make its affinity with mosses questionable (
Ignatov and Maslova, 2021). Other pre-Cenozoic moss fossils are either incomplete for a definitive identification or to represent extinct lineages (
Miller, 1980a,
1980b;
Bomfleur et al., 2014;
Ignatov and Maslova, 2021). Moss fossil records became much more abundant in the Cenozoic, and most of them can be compared to modern taxa (
Frahm and Newton, 2005;
Shelton et al., 2015).
Amblystegiaceae, comprising 39 genera, is a family of pleurocarpous mosses with ovate-lanceolate leaves that superficially resemble willow leaves (
Harris, 2008). They are widely distributed in global temperate climate regions. However, their fossil records are apparently scarce, mainly from the upper Paleogene onward in the Northern Hemisphere (Tab.1). In northern Europe, except for
Drepanocladus from Eocene Cookson amber (
Frahm, 2004), most of Amblystegiaceae fossils were found in the late Pleistocene
–Holocene peat bogs in Sweden and Norway (
Övestedal and Aarseth, 1975;
Kuder and Kruge, 1998;
Zazula et al., 2006;
Elverland and Vorren, 2008;
Van der Linden et al., 2008;
Delgadillo, 2009;
Kokfelt et al., 2010). In East Asia, there are only a few fossil records in the early Miocene Hannuoba Formation of Weichang area, Hebei Province of north-eastern China and from the late Pleistocene silicified deposits on the northern shore of Lake Usoriko in Japan (
Satake et al., 1995;
Guo et al., 2013). Particularly,
Guo et al. (2013) reported a rich flora of mosses, including
Amblystegium varium,
Drepanocladus subtrichophyllus, and
Leptodictyum riparium from the early Miocene (22.1 Ma) deposit at Weichang. In North America, Amblystegiaceae fossils are widely distributed in the Pliocene and the newer strata, such as
Cenococcum geophilum in the Pliocene shallow ocean deposits (2.60
–3.58 Ma) of north-eastern Greenland in the Arctic,
Leptodontium flexifolium in the late Pleistocene peat deposits (12 ka) in the Yukon Territory of north-western Canada, and
Calliergon giganteum and
Drepanocladus aduncus in the late Pleistocene Late Glacial strata (12–11.5 ka) of Portland, Maine on the east coast of the United States (
Janssens and Zander, 1980;
Miller, 1980a,
1980b;
Janssens, 1983;
Janssens and Glaser, 1986;
Matthews and Ovenden, 1990;
Ovenden, 1993;
Goetcheus and Birks, 2001;
Bennike et al., 2002;
Reyes et al., 2010;
Thompson et al., 2011).
Platydictya is a genus of small-sized mosses in the family Amblystegiaceae that are distributed widely in temperate and subtropical climatic zones of the Northern Hemisphere. The classification of this genus is still debatable. For example, Crum and Anderson (1981) and
Vitt (1984) as well as
Huttunen et al. (2013) assigned it to Hypnaceae and Plagiotheciaceae, respectively. While other researchers such as
Kanda (1976),
Noguchi (1991a,
1991b) and
Richard (2017) placed it in Amblystegiaceae. In this paper, we adopt the second taxonomy, which is widely used, such as by the “Flora Bryophytorum Sinicorum” (“Flora of Bryophytes of China”) (
Wu et al., 2005). Due to the lack of support tissues such as the costae of the leaf,
Platydictya may be more susceptible to mechanical fragmentation during taphonomic processes, resulting in scarce fossil records. Up to the present, only one species,
Platydictya cf.
jungermannioides, was reported from the early Pleistocene Kobenhavn Formation (2–2.5 Ma) in the Ellesmere Island, North America by
Ovenden (1993).
A large number of vascular plant fossils composed mainly of angiosperms and gymnosperms have been reported in the early Miocene Laoliangdi Formation of the Pingzhuang Coal Mine in the Yuanbaoshan District, Chifeng City, Inner Mongolia Autonomous Region, China (
Shang et al., 2001). In this research, we report a
Platydictya fossil with stems, leaves, and capsules found in the formation. This fossil preserves distinct micro-morphological features which allow us to make comparisons with both fossil and living mosses for an unambiguous identification. In common, the living
Platydictya can only grow in moist environments such as the underside or the surrounding soil of wet tree trunks in dense forests. Based on the method of the nearest living relative’s species (NLRs), the microhabitat which
Platydictya fossil lived in is reconstructed. In addition, combining with vascular plant fossils and sedimentary lithofacies previously studied based upon Pingzhuang materials, we further infer paleoenvironmental and paleoclimatic signal for this early Miocene site.
2 Materials and methods
The moss fossil was collected from the argillaceous shale of the Laoliangdi Formation in the Pingzhuang Coal Mine (Fig.1). The coal mine is located in the south-eastern part of the Chifeng City, which has large coal reserves with more than ten coal seams (
Yu et al., 2009). The strata containing coal seams are mainly composed of dark gray sandstones and siltstones and are mainly in the middle and upper members of the Xingyuan Formation and the lower member of the Yuanbaoshan Formation, both of which are lower Cretaceous in age (Fig.1). Abundant fossils have been discovered from these Cretaceous layers as well as the overlying Cenozoic shale strata (
Yu et al., 2009). The 25−51 m thick Laoliangdi Formation overlies the Yuanbaoshan Formation with an angular unconformity (Fig.1). It comprises sedimentary rock assemblages including dark gray shale, yellowish gray and dark gray sandstones, siltstones intercalated with glutenite (
Yan et al., 2008). Abundant plant macro- and micro-fossils (spore and pollen grains) have been discovered from the shale at the bottom of this formation, where our moss fossil was collected. The thickness of this shale is more than 10 m (
Tao et al., 1994) and was dated biostratigraphically as early Miocene based upon the assemblage of plant macro- and micro-fossils (
Zhang, 1986;
Tao et al., 1994).
The fossil specimen was observed and photographed using a Leica M165FC fluorescent stereo microscope and a VHX-1000 ultra-depth-of-field three-dimensional microscope. In addition, stem and leaf fragments were taken by a scalpel and a dissecting needle and soaked in distilled water for several hours for softening. They were then treated with hydrochloric acid (HCl) for 2 h and hydrofluoric acid (HF) for 10–12 h to remove the calcareous and siliceous sediments. Without any further chemical treatment, the water-neutralized specimens were then observed and photographed by a Leica DM1000 optical microscope. A small piece of the specimen was observed directly under the FEI Quanta 650 FEG scanning electron microscopy (SEM).
For systematics and nomenclature, we follow those of
Hu and Wang (1994).
3 Systematic paleobotany
3.1 Fossil description
Order: Hypnales (M. Fleisch.) W. R. Buck & Vitt
Family: Amblystegiaceae G. Roth
Genus: Platydictya Berk.
Species: Platydictya cf. jungermannioides H. Crum, 1964
Studied specimen: PZX-17-013.
Occurrence: Pingzhuang Coal Mine, Yuanbaoshan District, Chifeng City, Inner Mongolia Autonomous Region, China.
Stratum and age: Lower member of the Laoliangdi Formation, early Miocene.
Repository: Geological Museum of Chang᾽an University, Xi’an, China.
Description: The specimen contains about 10 branches; 8 are attached while 2 are separated. Their similar structure and texture suggest that they very likely belong to the same plant (Fig.2(a)). The plant is slender and small, occupying an area of only about 1.25 cm × 1 cm. No rhizoids have been observed. Branches are 0.6–1.2 cm in length. Their stems are more or less erect and branched irregularly (Fig.2(a)–Fig.2(c)). Leaves are sparsely and spirally arranged on the stems. They are ovate-lanceolate to lanceolate and very small, only 0.15–0.3 mm in length and 0.04–0.06 mm in width. They seem to be chartaceous in texture and are very thin, almost semitransparent (Fig.2(b)–Fig.2(f)). No costae have been observed on them (Fig.2(b)–Fig.2(f)). Leaf base is thickened and embraces the stem. No stipules were found (Fig.2(d)). Capsule-like structures are seen on the tip of a branch (Fig.2(g)) but their fine structures are not preserved.
Leaf margins are mostly partly entire and partly dentate, a few dentate, and rarely completely entire (Fig.3(a)–Fig.3(d)). The leaf margins are also thickened, likely with more than one layers of cells while most of the other part of the leaf has only a single cell layer. The cells at leaf margins are rhomboid, irregularly quadrilateral, or polygonal (Fig.3(d)–Fig.3(f)). The cells at leaf apex are rectangular or rhomboid, with a length-to-width ratio of 3:1–4:1. The marginal cells in the middle and base of the leaf are rhomboid or square, with a length of 20–40 μm and a width of 6–7 μm.
Line drawings are made to clearly show leaf morphology and microstructure of current fossil (Fig.4(a)–Fig.4(c)).
3.2 Comparison and discussion
The presence or absence of costae is an important feature to classify mosses (
Newton et al., 2007). Most extant mosses possess costae. However, our moss fossil does not have costae. In addition, it is a small-sized moss with ovate-lanceolate leaf shapes. We thus compare our fossil with the 14 living moss species possessing ovate-lanceolate leaves without costae. The comparison of the gross morphological characteristics is shown in Tab.2.
Our fossil has its leaf margins mostly partly entire and partly dentate, with teeth mainly distributed at the basal part of the leaf. A few leaves are completely dentate while completely entire leaves can also be rarely observed. Our fossil has its leaf margins partially dentated or completely dentated, with teeth mainly distributed at the basal part of the leaf. Among the 14 living moss species listed in Tab.2, Aulacopilum abbrevium, Braunia alopecura, Hedwigia ciliata, Leucodon pendulus, and Leptopterigynandrum incuryatum are excluded because their leaf margins are completely entire. The irregular branching of stems of our specimen further exclude the four species with feathery branching: Campylophyllum halleri, Palisadula chrysophylla, Schwetschkeopsis fabronia, and Entodon dolichocucullatus. The gross morphology of our fossil in general falls within the range of those of the remaining five species, Platydictya jungermannioides, Campylium porphyriticum, Venturiella sinensis, Pinnatella anacamptolepis, and Leucomium strumosun, except that the size of our specimen is visibly smaller. The presence of capsules on Branch 6 indicates that our fossil is at its mature stage. It is known that as a moss has a high content of water, it would generally shrink due to dehydration when it was preserved in sediments. However, our fossil has leaves stretching naturally, showing little sign of shrinkage, likely due to very quick burial during early stage of the taphonomic process, such as being suddenly embedded by large amount of sediments. To understand the degree of shrinkage for a moss fossil preserved during such an early fossilization process, we subjected fully watered fresh mosses under 10 kg weight for 24 h. The compacted mosses still show their stretching status but have been dehydrated, similar to the condition of our fossil. The compacting resulted in a reduction of stem length by about 0.25–0.4 times and of leaf size by 0.3–0.5 times. Applying these ratios, we were able to estimate the possible actual sizes of our fossil. The stem length would be about 1–2 cm and the leaves are about 0.5 mm long with the largest width about 0.1 mm, most comparable to Platydictya jungermannioides among the above-mentioned five moss species. In addition, the leaf cell arrangement of our fossil also resembles that of Platydictya jungermannioides.
Fossil and molecular evidence suggests that bryophytes evolve very slowly (
Blöcher and Frahm, 2002), which leads to limited differences between many ancient and extant bryophytes in morphology. Some previously-reported fossil bryophytes with the features more or less similar to our fossil have been found in strata with different ages, with the earliest dating back to the Paleozoic (
Oostendorp, 1987;
Amaral et al., 2004;
Moisan et al., 2012). Most of the well-preserved moss fossils before Cenozoic were classified into the broad morphological genus
Muscites. Among them, only the specimens from the Late Triassic Madygen Flora in the Canadian Arctic have their micro-morphological structures described, including the absence of costae (
Moisan et al., 2012). However, there is a distinct difference in leaf shape between them and our fossil, nearly rounded versus ovate-lanceolate. Some fossils found in the Northern Hemisphere show similar growth pattern as well as leaf shape to our specimen (
Baker et al., 1993;
Satake et al., 1995;
Kuder and Kruge, 1998; Geotcheus and Birks, 2001;
Bittmann, 2007;
Reyes et al., 2010;
Guo et al., 2013). The most similar one is
Amblystegium varium found in the adjacent early Miocene strata at Weichang which also has ovate-lanceolate leaves arranged spirally on stems of similar length (
Guo et al., 2013). However, the Weicheng fossil bears costae, obviously different from our specimen.
Campylium fossils of Amblystegiaceae found in the Pleistocene also have ovate-lanceolate leaves without costae and irregularly branched stems. However, its leaves are significantly larger than ours, and its stem length is more than 2 cm, much longer than that of our fossil (
Matthews and Ovenden, 1990;
Goetcheus and Birks, 2001).
In summary, after comparing our moss fossil with both fossil and living taxa, we conclude that our fossil bears the most similarity with the modern moss species Platydictya jungermannioides. All characteristics that can be observed from our specimen fall within the range of those in the living species. However, the lack of some key characteristics, such as those of rhizoids and reproductive organs prevents us from assigning our fossil to the living species directly. Tentatively, we name our specimen Platydictya cf. jungermannioides, with the abbreviation cf. (for “confer”) added before the species epithet to indicate the species level uncertainty due to its incomplete preservation.
Fossils of
Platydictya are extremely rare.
Ovenden (1993) reported
Platydictya cf.
jungermannioides fossils from the Ellesmere Island in the Canadian Arctic but no images or detailed descriptions were provided. Before our specimen, no fossil of
Platydictya has been reported from Asia, although living
Platydictya plants are currently growing in the studied area (
Zhang, 2008). The studied
Platydictya fossil found at the Pingzhuang Coal Mine is the first record of this genus in Asia, suggesting that this genus may have lived in the Chifeng area from the early Miocene to the present.
4 Paleoenvironmental significance
Paleobotanists reconstruct the ecology and environment of ancient forests almost exclusively from vascular plants, knowing little about their understory and even less concern forest floors due to the rarity of bryophyte fossils. Thus the exceptionally preserved moss fossil studied here, combined with the narrow ranges of ecological tolerances of mosses (
Miller, 1984;
Zazula et al., 2006), provides a unique opportunity to infer microhabitats of an ancient forest that rarely left any trace in the fossil record.
Mosses have a high requirement for humidity. Plants in the Amblystegiaceae are basically aquatic, demanding a high level of water supplies (
Yang et al., 2004). Living species of
Platydictya are widely distributed in the temperate to subtropical humid to semi-humid areas, especially in the temperate monsoon climate region in mountainous and hilly forests.
Platydictya jungermannioides grows in moist environments such as the underside or surrounding soils of wet tree trunks in dense forests. In addition, the excellent preservation condition of our specimen as well as our compaction experiment confirmed that our fossil was highly likely buried
in situ, fresh with adequate water before it was rapidly covered by sediments. We thus believe that the original living microhabitat of our fossil should be humid with sufficient water supplies.
Although both fossil and living species of
Platydictya have been found in the Chifeng area mentioned above, it can only demonstrate that the microenvironment of the plants is humid. The early Miocene flora of the Pingzhuang site has been well established to be the transitional type between evergreen deciduous broad-leaved mixed forest and coniferous broad-leaved mixed forest (
Shang et al., 2001) based from vascular plant fossils dominated by angiosperms of Fagaceae, Populaceae, Betulaceae, and Ulmaceae, as well as gymnosperms represented by the family Taxaceae (
Zhang, 1986). This transitional type of forest now grows in the temperate to subtropical semi-humid climate (
Tao et al., 1994). By contrast, vegetation in the current Pingzhuang area is dominated by grasses and shrubs belonging to the semi-arid temperate climate region. The climate of the basin during the early Miocene was thus much more humid and warmer than it is today. Moreover, the depositional environment of the lower Laoliangdi Formation is of lacustrine or swamp facies inferred from the composition of the sedimentary record (
Shang et al., 2001), further confirmed that the Pingzhuang basin has a temperate or subtropical humid to semi-humid climate in the early Miocene. The existence of
Platydictya cf.
jungermannioides and its preservation condition confirms a very wet microenvironment under such as ecological background, likely a forest that is dense and humid enough to provide a lush understory layer for the growth of this moss species.
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