In situ forest with lycopsid trees bearing lobed rhizomorphs from the Upper Devonian of Lincheng, China

Abstract The earliest forests in the Devonian were reported from only four localities worldwide. The tree lycopsids, sometimes as the primary elements of Devonian forests, had evolved several types of rooting systems. In recent years, we found and excavated a Late Devonian (Famennian, 374–359 Ma) lycopsid forest from Zhejiang Province, China. The fossil forest occurs at seven locations of Lincheng Town of Changxing County and mainly consists of in situ small tree lycopsid (Heliodendron longshanense gen. et sp. nov.) stems usually connected to lobed cormose rhizomorphs. The four short lobes of each rhizomorph often branch once and bear roots arranged radially. Allometry is observed between the trunk diameter of Heliodendron and the length of its rhizomorphic lobes, indicating that the trunk develops later than the rhizomorph in tree lycopsid plants. The Devonian witnessed the transformation from clastic nonlycopsid dominated forests to Carboniferous swampy forests dominated by giant lycopsid trees. These trees form a multigenerational community, as shown by the in situ preserved stems at various levels within the same area due to frequent sedimentation events.


Introduction
Forests first appeared in the Devonian and had been reported from United States (i.e.Gilboa and Cairo forests near New York) (1,2), Norway (Svalbard forest in Svalbard islands) (3), and China (Xinhang forest in Anhui Province) (4).Although these fossil forests had been studied in detail, it is still very difficult to find early forests on Earth.The lycopsids have the longest evolutionary history (Late Silurian to present) among vascular plant groups (5), and tree lycopsids represent the main components of Svalbard and Xinhang forests.
The rooting system plays a crucial role in facilitating the growth of individual tree lycopsid, providing essential mechanical support and efficient nutrient absorption.The narrow elongate and often dichotomous organs responsible for absorption and anchoring are referred to as roots, while the structure to which the roots are attached is known as the rhizomorph (6).The Devonian tree lycopsids may have presented all types of their belowground rooting systems, i.e. repeatedly dichotomized root, cormose rhizomorph (bulb-shaped and unbranched base), lobed cormose rhizomorph, and stigmarian rhizomorph (with four dichotomized axes) (3,4,(7)(8)(9)(10).Most of the giant tree lycopsids in Late Carboniferous (Pennsylvanian) coal swamps possessed the enormous stigmarian rhizomorph (11), while some smaller tree lycopsids displayed (lobed) cormose rhizomorph (12).
In recent years, a new fossil lycopsid forest was found and excavated from the Upper Devonian (Famennian) Wutong Formation in Lincheng Town, Changxing County, Zhejiang Province, China.Based on this discovery, we discuss the classification of rooting system and allometry in early tree lycopsids, the transition of early forests, and the preservation of Lincheng forest.
The fossils were preserved as impressions, compressions, and casts.All specimens are housed in the Department of Geology, Peking University, Beijing, China.

Methods
The strata exposed in the field work area have been studied in previous work (13) and supported by geological maps (China National Digital Geological Map spatial database).Excavator was utilized initially to remove the overlying strata, and a big quadrat (5 m × 3 m) was subsequently established using nails, ropes, and marker pen.Manual excavation was then conducted in each small quadrat.Photos were taken to document newly excavated quadrats and fossils in them.Original data including tree position, diameter (the base of the trunk we can see, excluding the basal expanded area), length of rhizomorph lobes, and the depth of rooting systems (from the horizontal extension to the deepest portion of the root) were measured and recorded in the field book.
Steel needles and chisels were used to expose the morphology of plants, and digital cameras for photographs in the field and laboratory.All images were prepared and labeled in figures with Adobe Photoshop CC 2014.According to the data from Google map, Baidu map, geological map, and investigation at Longshan mine near Shiying village, Lincheng Town, Changxing County, Huzhou City, Zhejiang Province, China, the distributions and horizons of in situ fossil plants were provided in Fig. 1. Figure 1

Results
The fossil forest occurs at seven locations in Longshan Mine (including three quarries) near Shiying village, Lincheng Town, Changxing County, Zhejiang Province, China (Figs. 1A, B).The in situ plants were buried at quarries 1-3 (Fig. 1B).Locations 1, 5, 6 belong to quarry 1, locations 2-4 to quarry 2, location 7 to quarry 3, and these locations are 130 base of several trunks 2,100 m apart from each other (Fig. 1B).Outcrops at three Longshan quarries mainly present Guanshan Member of Wutong Formation, which is widespread in the lower reaches of the Yangtze River of China.The age of Guanshan Member is Famennian, according to the spore assemblage attributed to the Aneurospora asthenolabrata-Radiizonates longtanensis zone (14).At Longshan quarries, the Guanshan Member is characterized by quartzose sandstone with interbedded mudstone and siltstone.The stratigraphic column (SI-1 Fig. S1) is the same as illustrated in previous works (13,15).The in situ plants in locations 1-6 were found from the third, first, third, fifth, fourth, fourth beds, respectively (SI-1 Fig. S1).
In the quadrat at location 1, the trunks or rooting systems of in situ lycopsids were preserved in ca. 1 m thick gray mudstone between sandstone; three fossil-root bearing levels are 100, 158, and 192 cm above the sandstone base, respectively (Fig. 1C, left).Within these three levels, there are several thin intercalations of siltstone and sandstone.In 2021, after rock collapse, several in situ lycopsid trunks and roots were discovered 10 m south of the quadrat (SI-1 Figs.S2A, black arrow, and S9).Some lycopsid stems or branches were exposed obliquely or horizontally on the bedding plane (Figs.2I, 4B, C and SI-1 Fig. S11).Except from the lycopsid, possible Crinoidea fossils (SI-1 Fig. S13) were found at the fossil-bearing levels, while some fern-like plants appeared above (Fig. 1C, left).Seed plant Latisemenia longshania, progymnosperm Archaeopteris sp., leaf cushions of Leptophloeum rhombicum, reproductive organs of lycopsids and an undetermined sphenopsid were previously described in quarry 2 of Longshan (13,15).
Diagnosis: Small tree-like lycopsid with four short-lobed cormose rhizomorph.Each lobe divided once or rarely twice.Roots    S10F-H).Generally, the lobes are short and easily broken, so they are not complete when taken out, like plant in Fig. 2B and  C, the rhizomorph is clearly divided into four unequal parts, but the ends are broken off (white arrows in Fig. 2G and H).  , C-E).The diameter of the stem in Fig. 2I prior to branching measures 4.3 cm, with the two resulting branches measuring 2.4 and 2.6 cm, respectively.
Otzinachsonia (9) and Heliodendron share four short-lobed cormose rhizomorph.However, the rhizomorph of Otzinachsonia is differentiated into distinct furrows and undivided lobes, concentrated with small and large root scars, respectively.In addition, the leaf scars/bases on the trunk of Otzinachsonia are horizontally elliptical or triangular, while those of Heliodendron are vertically fusiform.As a small tree lycopsid, the Early Carbonierous (Mississippian) Protostigmaria eggertiana possesses a lobed cormose root (20).It differs from Heliodendron by having 2-13 rhizomorph lobes and round leaf scars/bases arranged in low helices or pseudowhorls on the stem.
Guangdedendron forming Xinhang lycopsid forest was found in the Leigutai Member of the Wutong Formation (4), occurring a little later than Heliodendron in the Guanshan Member.The linear distance between Xinhang and Lincheng forests is about 25 km.Heliodendron and Guangdedendron share similar stem width, and according to the calculation formula between the diameter value (D) and the height (H ) (H = 37.5 × (D/2) 2/3 ) (21), they are separately 0.8-8.4m and 1.1-7.7 m high.Both of the two tree lycopsids possess dichotomously branched stem, linear vegetative leaves with entire margin, and fusiform leaf bases helically arranged in parastichies.In contrast, Guangdedendron is characterized by Stigmaria-type rhizomorph with four divided axes reaching 25.3 cm length (4) or 31 cm length (19).Heliodendron is characterized by lobed cormose rhizomorph with four divided unequal lobes just reaching 5.6 cm.
The rhizomorph of Heliodendron consists of uneven lobes.As the trunk diameter increases evidently, the length of rhizomorphic lobes increase in a less proportion, suggesting allometry.It is proposed that in the life cycle of tree lycopsids, the rhizomorph establishment precedes the elongation of stem (22).The lower growth rate in the length of rhizomorphic lobes may indicate a postgrowth stage and thus correspond to the above-mentioned developmental pattern.The reduced growth rate of rhizomorph may result in inadequate mechanical support for the above-ground portion of the trees, potentially leading to collective tilt, which is a rare phenomenon in Xinhang Forest.
Many leaves of tree lycopsids abscise, forming distinct "leaf scars", like Chamaedendron (8) and Omprelostrobus (17), However, Heliodendron displays leaves persisting at the base of several trunks (Figs.2J and SI-1 Fig. S12A-D, F), suggesting that some individuals may exhibit a slower leaf shedding process or retain leaves throughout their lifespan.

Composition of early forests
The earliest forests in the Devonian were discovered in recent years and consist of fern-like plants, progymnosperms, and/or lycopsids (1)(2)(3)(4)23).The exposed area of nonlycopsid fossil forests (Middle Devonian Gilboa and Cairo forests from New York of United States) range from 1,200 to 3,000 m 2 and the density of large trees is less than 1/m 2 (1, 2).The Late Devonian Svalbard forest from Norway and Xinhang forest from China are (mainly) composed of small lycopsid trees (3,4).The area of Svalbard forest is unclear and the average of tree density is 14/m 2 .The exposed area of Xinhang forest is at least 250,000 m 2 , and it is the largest Devonian fossil forest and even larger than many Carboniferous fossil forests; the local density of trees is up to 38/m 2 .
The Guanshan Member is ca.75 m thick at the Longshan section (13, 15) (SI-1 Fig. S1).In the mid-lower part of Guanshan Member of this section, the in situ plants from locations 1-7 occur in mudstone or siltstone as thin beds or wide lens between sandstones (Figs. 1, 2, 4-6, SI-1 Figs.S1-S12, and S14-S16), although the plant-bearing horizons could not be accurately correlated among the seven locations due to long distance and the covering Quaternary deposits.Within an area of 75 hectares limiting these seven locations, in situ lycopsids are distributed as small patches.The density of Heliodendron trees is up to 42/m 2 in Lincheng forest (Fig. 1C, pink square), indicating that dense growth may be normal  S8E, G, S10A, B, and S11).
The Middle Devonian Gilboa forest mainly consist of in situ aneurophytes and cladoxylopsids, together with a few heterochthonously preserved lycopsids; while Cairo forests consist of in situ Archaeopteris, cladoxylopsids, and few possible lycopsids (1, 2).Late Devonian (Frasnian) Svalbard forest was made up of small lycopsid trees, with in situ archaeopteridalean trunks recognized (3).The Late Devonian (Famennian) Xinhang forest is characterized by small lycopsid trees and there are also other plants, such as Xinhangia and Sublepidodendron (4, 24, 25).In the Lincheng forest, most in situ trees are recognized as lycopsids (locations 1-4), with distinguishable leaf bases or cushions.The trees with rooting systems are identified as Heliodendron longshanense in location 1, while those along the highwalls or in fallen blocks of locations 2-4 are also lycopsids, and the two trunks and a rooting system in locations 5-7 may belong to lycopsid.Carboniferous and Early Permian swampy forests are complicated in vertical stratification, with both canopy-forming trees and understory plants of multiple affinities including lycopsids, horsetails, ferns, and gymnosperms (26)(27)(28).Therefore, the Late Devonian forests with small lycopsid trees may represent a transition from the Middle Devonian forests majorly consisting of cladoxylopsids and archaeopterids, to later forests usually dominated by giant lycopsid trees.

Environment and preservation of tree lycopsids
The Upper Devonian Wutong Formation, widespread in the Lower Yangtze Valley of China (including Zhejiang Province), consists of the underlying Guanshan Member mainly with thick quartz sandstone and the overlying Leigutai Member with interbedded mudstone and quartz sandstone (29).The stratigraphic, sedimentary, and geochemical analyses concluded that the Wutong Formation represents a coastal (littoral) environment near the palaeoequator (4,(30)(31)(32)(33).The lithology and sedimentation of the Wutong Formation indicate that a general sea level regression occurred from Guanshan Member to Leigutai Member (31,32,34).The in situ plants in Guanshan Member were more easily disturbed by sea flow than those in Leigutai Member.Possible Crinoidea fossils may suggest that Lincheng forest was influenced by the sea water.
In the Carboniferous, giant tree lycopsids with extensive stigmarian roots dominated coal swampy habitats, while the smaller tree lycopsids with lobed cormose bases reflected nonswampy conditions (5,20).Guangdedendron and Heliodendron indicate that the Late Devonian tree lycopsids with both types of rooting system lived on clastic substrates.Many in situ trunks or stems in location 1 (Figs.The in situ lycopsid trunk casts crossing the sedimentary beds of the Upper Devonian Wutong Formation have been reported from several localities in South China (4,17), and they resulted from burial events, i.e. strong flood carrying large amount of sediments.Each layer of in situ trunks may correspond to a separate flood event, during which rapid water flow tilted the trunks and buried them with leaves in abundant sediment.The exposed portions of the tree lycopsids above the sediment were later damaged during subsequent floods or decay, resulting in the truncated tops of the preserved trunks.Tree lycopsids located on the periphery of the flood disturbance zone may be less affected, potentially allowing them to propagate and recolonize the habitat.This process may be repeated several times, resulting in the preservation of multiple layers of in situ fossil forests within the strata (3).However, the different fossilbearing horizons may represent a single, long-lived community that fluctuated in size and distribution due to the influence of seawater.
, the line diagram Figs.2D, E and schematic diagram Fig. 7B were made by CorelDRAW X8, the 3-D reconstruction Fig. 7A was made by Plantfactory 2014.The diameters of stems of in situ lycopsids were analyzed through Microsoft Excel 2019.

Fig. 1 .
Fig. 1.Location, stratigraphy and distribution of fossil plants.A) Map showing locality of Lincheng fossil lycopsid forest (in northwest part of Zhejiang Province).B) Seven locations (1-7) of in situ fossil plants in three Longshan quarries (1-3) near Shiying village, Lincheng Town, Changxing County of Zhejiang Province.C) Stratum of the Upper Devonian Wutong Formation (Guanshan Member) in location 1, and the distribution of fossil lycopsid (Heliodendron) in mudstone of three levels (levels 1-3, including quadrat); the diameters of Heliodendron are to the scale.The pink area has been expanded in SI-2 Fig. S4.The color of the left log corresponds to the hue of the rock.T (cm): thickness (centimeters).

Fig. 2 .
Fig. 2. Individuals of lycopsid at location 1. A) Top view of a rooting system with short rhizomorph lobes (arrows) bearing roots (this axcavated root is originally connected with the stem in SI-1 Fig. S10A-F.White arrows indicating the first dichotomy and black arrows indicating the second dichotomy.Picture enlarged in SI-2 Fig. S1.B, C) Two opposite sides of the stump in Fig. 4A (arrow 6), same as in SI-1 Fig. S3C-G.Arrows indicating four lobes of the rhizomorph.PKUB17401.D) The line diagram of (C), showing four unequal and short rhizomorph lobes (numbers 1-4), with the first (gray arrows) and second dichotomy (purple arrows).E) The line diagram of (C), showing four unequal and short rhizomorph lobes (numbers 1-4).F-H) Serial excavation of stump in SI-1 Fig. S3B (arrow 1), the same stump as in (B, C).Arrows indicating the end of broken lobe.I) The longest trunk (lying on bedding plane) with dichotomy as in SI-1 Figs.S8A (black arrow) and S11A.J) A trunk across the bedding plane and with leaves, same as SI-1 Fig. S12C.PKUB17407.Scale bars = 2 cm (coin), 5 cm (B, C, D, E), 20 cm (I).
arranged radially and 1-2 times dicotomized.Root scars almost circular.Stem distally divided several times.Leaf cushions and bases narrow fusiform and helically arranged.Vegetative microphylls in linear shape.The rooting systems and vertical trunks of in situ lycopsid Heliodendron longshanense occur in three levels at/near the quadrat of location 1 (Figs.1C, 2-4, 6, SI-1 Figs.S2-S10, and S12A-D, F), some in situ trunks (Figs.5A-D, F, G and SI-1 Figs.S14-S16) and a rooting system (Fig. 5E) in other six locations.The rooting systems of Heliodendron longshanense are usually connected to trunks.There

Fig. 3 .
Fig. 3.In situ trunks with/or rooting systems from level 2 of location 1 (excavated in October 2017).A) Lateral view of part of Location 1, arrow 1, 2 enlarged in (B, C).B) Enlargement of arrow 1 in (A), five trunks of junior plants, arrow indicating the thinnest trunk in this forest.C) Enlargement of arrow 2 in (A), two trunks of junior plants, white arrows indicating short lobes of rhizomorphs.D, E) Two opposite sides of the trunk and root of a junior plant (diameter of trunk ≤ 3 cm) in SI-1 Fig. S4C (black arrow).Arrows indicating four lobes of the rhizomorph.PKUB17402.F) A trunk, white arrows indicating lobes of the rhizomorph.Same plant as in SI-1 Fig. S8D.G) The thickest trunk, arrow indicating possible lobe's impression of rhizomorph.Same plant as in SI-1 Fig. S8E.Scale bars = 1 cm (D, E), 2 cm (coin, C), 5 cm (B), and 10 cm (F).

Fig. 6 .
Fig. 6.Trunks with rhizomorph bearing four short lobes (arrows in A-F, except arrow 1 in B) and roots or root scars from location 1. A, C) Two trunks with rooting system from levels 1, 2, respectively.(C) Enlarged in SI-2 Fig. S2A.B) Excavation of the rooting system in A, arrow 1 indicating rootlet scar.D) Excavation of the rooting system in (C), and picture enlarged in SI-2 Fig. S2B.E) A trunk with expanded base and rooting system from level 3. F) Cast and mould of the trunk, same as in SI-1 Fig. S7G-I.A rooting system with short rhizomorph lobes (arrows) bearing roots and root scars.G) Enlargement of part in (F) (rectangle), showing two root scars (arrows).H) Rhizomorph with radially arranged roots, same as in SI-1 Fig. S6H, after excavation.I-L) Roots on highwall, L enlargement of part in K (arrow), showing bifurcated root.Arrows indicating bifurcation points.Scale bars = 5 mm (G), 1 cm (L), 2 cm (coin diameter, K), and 5 cm (A, B, F, H-J).