Xihuphyllum, a novel sphenopsid plant with large laminate leaves from the Upper Devonian of South China

Palaeogeography, Palaeoclimatology, Palaeoecology 466 (2017) 7–20

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Xihuphyllum, a novel sphenopsid plant with large laminate leaves from the Upper Devonian of South China Pu Huang a, Le Liu b, Zhenzhen Deng a, James F. Basinger c, Jinzhuang Xue a,⁎ a b c

The Key Laboratory of Orogenic Belts and Crustal Evolution, School of Earth and Space Sciences, Peking University, Beijing 100871, PR China School of Geosciences and Surveying Engineering, China University of Mining and Technology (Beijing), Beijing 100083, PR China Department of Geological Sciences, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5E2, Canada

a r t i c l e

i n f o

Article history: Received 2 August 2016 Received in revised form 2 November 2016 Accepted 5 November 2016 Available online 08 November 2016 Keywords: Fossil plant Leaf evolution Morphometric analysis Plant architecture Wutong formation

a b s t r a c t The sphenopsids first appeared in the Late Devonian, becoming diverse in the Carboniferous and Permian, but are represented now by the single genus Equisetum. In this article, morphologically preserved material of the novel sphenopsid plant, Xihuphyllum megalofolium (Wu) Chen emend. Huang et al., is described from the Upper Devonian Wutong Formation of Zhejiang Province, China, providing new data on the early evolutionary history of this group. This plant is characterized by a hierarchical branching pattern, with robust nodose stems up to 42.5 mm wide and two orders of lateral branches. Morphometric studies show that the internode width of stems and firstorder branches are correlated with the internode length. Leaves, cuneate, broadly cuneate, or spatulate in shape and highly variable in size, are arranged in whorls at the nodes of stems and branches. The leaves of Xihuphyllum reach over 80 mm in length and N3000 mm2 in area, an unusually large size for Paleozoic sphenopsids. Xihuphyllum is reconstructed as having a stature 2–3 m in height, and represents an early, large-bodied member within the extinct Sphenophyllales. The occurrence of Xihuphyllum and contemporaneous members of the same group, including Eviostachya, Hamatophyton, Rotafolia and Sphenophyllum, indicates early diversification of sphenopsids in South China. © 2016 Elsevier B.V. All rights reserved.

1. Introduction The radiation of vascular plants during the Silurian and Devonian periods, particularly the appearance of large-bodied plants, i.e. trees or tree-like plants, has been considered to have had significant impact on the Earth's environments (Algeo and Scheckler, 1998; Algeo et al., 2001; Davies and Gibling, 2010; Retallack and Huang, 2011; Morris et al., 2015). Early vascular plants of the late Silurian–Early Devonian are small in aboveground stature (Gensel, 2008; Hao and Xue, 2013), while, during the Middle–Late Devonian, early forests were constituted by trees of cladoxylopsids, archaeopteridaleans and lycopsids (Meyer-Berthaud et al., 1999, 2010; Stein et al., 2007, 2012; Giesen and Berry, 2013; Berry and Marshall, 2015). Increase in plant body size would have contributed to expanding potential for storage of biomass in terrestrial environments and to the development of deep and complex rooting systems that enhanced physical and chemical weathering processes (Algeo and Scheckler, 1998; Algeo et al., 2001). With increase of plant size, laminate leaves emerged independently in fern-like plants, sphenopsids, progymnosperms, and spermatophytes

⁎ Corresponding author. E-mail address: [email protected] (J. Xue).

http://dx.doi.org/10.1016/j.palaeo.2016.11.004 0031-0182/© 2016 Elsevier B.V. All rights reserved.

by the Late Devonian (Hill et al., 1997; Boyce and Knoll, 2002; Wang et al., 2015; Xue et al., 2015). Laminate leaves, as the primary photosynthetic organs, would have had a substantial impact on terrestrial food webs and biogeochemical cycles (Beerling, 2005; Beerling and Berner, 2005). Thus, an understanding of the effect of early plant communities on terrestrial environments demands a deep understanding of the evolution of plant leaf and body size. Sphenopsids, with their distinctive nodes and internodes of stems and lateral branches, were one of the major groups acquiring both large body size and laminate leaves in the Devonian. This group is placed in the class Sphenopsida (or, the phylum Sphenophyta; Taylor et al., 2009) within the euphyllophytes and includes three orders: Pseudoborniales; Sphenophyllales; and Equisetales. The Pseudoborniales is represented by one only genus, Pseudobornia Nathorst, which was first described from the Upper Devonian of Bear Island, Spitsbergen. The type species, Pseudobornia ursina Nathorst, was reconstructed as a tree 15–20 m tall (Schweitzer, 1967). The Equisetales includes the extant herbaceous Equisetum L. and the extinct calamitaleans, which were abundant in Carboniferous–Permian tropical swamps (Taylor et al., 2009). The Sphenophyllales, usually considered to be small in size, constituted understory or vine-like plants of the Paleozoic tropical swamps, but many in this order bear laminate, cuneate and spatulate leaves

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(Gu and Zhi, 1974; Galtier and Daviero, 1999; Bashforth and Zodrow, 2007; Wang et al., 2008). In this study we report on one of the earliest members of the Sphenophyllales, and also one of the largest and most robust known, from the Upper Devonian of Zhejiang, China. This plant, with whorls of conspicuous laminate leaves, has been described as Sphenophyllum megalofolium Wu from the Wutong Formation of Yixing, Jiangsu Province, China (Wu et al., 1979). Later, Chen (1988) named a new genus, Xihuphyllum, including two species, Xihuphyllum megalofolium (Wu) Chen and Xihuphyllum elongatum Chen, for his material from the Xihu Formation of Hangzhou, Zhejiang Province, and included the specimens of Wu et al. (1979) within X. megalofolium. New and well preserved fossils allow us to make an emendation to the originally described species Xihuphyllum megalofolium, which we consider as the type and the only recognizable species of the genus.

2. Material and methods 2.1. Locality and stratigraphy The specimens were collected from the lower part of the Guanshan Member of the Wutong (Wutung) Formation, at a quarry near Fanwan Village, Hongqiao Town, Changxing County, Zhejiang Province, China (the Fanwan section; Fig. 1; also see Wang et al., 2014b, their Figs. 1–3) (GPS location 30°57′42.69″N, 120°02′32.82″E). The fossiliferous bed is composed of gray mudstone with minor siltstone and sandstone and ranges from 2 to 3 m in thickness. The Guanshan Member, with thick conglomerate and conglomeratic quartz sandstone intercalated with a few layers of sandy mudstone or siltstone, is the lower member of the Wutong Formation, and is overlain by the Leigutai Member, with thin to medium beds of quartz sandstone, silty mudstone and argillaceous siltstone. On the basis of plants, spores, fish and conchostracans,

Fig. 1. Map showing the fossil locality. A. Late Devonian paleomap showing the location of South China, modified from Scotese (2001). B, Late Devonian palaeogeography of the South China Block, modified from Ma et al. (2009). C. Map showing the location of the Fanwan section.

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Li et al. (1984) interpreted the age of the Wutong Formation, which is widespread in the lower reaches of the Yangtze River including Zhejiang, Jiangsu and Anhui provinces, as Famennian (Late Devonian), with the Guanshan Member early Famennian, and the Leigutai Member late to latest Famennian in age. Abundant plant megafossils were reported from the Wutong Formation of Changxing County during regional geological surveys (Bureau of Geology and Mineral Resources of Zhejiang Province, 1989). Recent studies have been based on excavation of fossil material from Fanwan and adjacent sections, including: lycopsids Changxingia longifolia Wang et al., Monilistrobus cf. yixingensis Wang et Berry, Sublepidodendron grabaui (Sze) Wang et Xu, and Lobodendron fanwanense Liu et al. (Wang et al., 2014b; Liu et al., 2015; Meng et al., 2016; Zhang et al., 2016); sphenophyllaleans Sphenophyllum pseudotenerrimum Sze, Eviostachya Stockmans, and Hamatophyton Gu et Zhi (Wang et al., 2014b; Deng et al., 2016); the progymnosperm Archaeopteris (Dawson) Stur (Wang et al., 2014b); and seed plants Cosmosperma polyloba Wang et al. (Wang et al., 2014a) and Latisemenia longshania Wang et al. (Wang et al., 2015).

2.2. Specimens and methods The specimens are mainly preserved as adpressions, rarely as casts of axes. Xihuphyllum megalofolium is dominant and well preserved in this bed, with complete leaf whorls and details of leaf outline and veins. The plants probably lived in the vicinity of the preservation site (i.e., parautochthonous burial). Other plants include only scarce lycopsid stems and a strobilus assignable to Eviostachya, but their fragmented condition indicates transport for some distance. Large blocks were removed from the outcrop by an excavator, photographed where stems and first-order branches were exposed, and parts of these blocks were taken to the laboratory for preparation. All the specimens prefixed by PKUB are housed at the School of Earth and Space Sciences, Peking University. For a comparison with the present material, we examined the specimens described by Chen (1988) under the names Xihuphyllum megalofolium and Xihuphyllum elongatum from the Xihu Formation of Hushan, Xiaoshan, Zhejiang Province, which is also Famennian (Cai, 2000). Chen's specimens, labelled as M3584, M3587, M3587a, M3587b, M3588, and M3603, are included here in X. megalofolium. These specimens are deposited in the Zhejiang Museum of Natural History, except for M3587b, deposited at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences. We consulted the Geological Museum, Xi'an University of Science and Technology

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(formerly Xi'an Mining Institute), for access to the original material described as Sphenophyllum megalofolium by Wu et al. (1979). Unfortunately, their illustrated specimens apparently have been lost, although four non-illustrated specimens are still available for comparison. Fossils were prepared by dégagement with steel needles and photographed with a digital camera system. Measurements of axes and leaves were made by using free software ImageJ 1.44 (http://rsb. info.nih.gov/ij/index.html). Plots and linear regression analyses of the measured values were performed in software PAST 3.0 (Hammer et al., 2001; http://folk.uio.no/ohammer/past). 3. Description The following description is based on ca. 130 specimens collected from the Fanwan section. Stems and two orders of lateral branches are recognized (Fig. 2A: ST, FB and SB). Altogether, there are 23 stems, 31 first-order branches, and 15 interpreted second-order branches. Remains of Xihuphyllum are dominant, with uniform color and state of preservation. All axes show ridges on the surface, typically show alternation of nodes and internodes, and can be easily distinguished from rare associated lycopsid stems and a single Eviostachya strobilus. Leaves are cuneate to spatulate in shape (Fig. 2B, C); some are attached to the axes, while most are detached. Morphological descriptors for axes and leaves are shown in Fig. 2A, including: width of axis at the nodal position (“nodal width”); internode width of axes; internode length; leaf maximum width; leaf width at base; leaf length; and leaf venation. 3.1. Stems and attached leaves The largest axes in the collection are straight and nodose, and are interpreted as stems which bear both first-order branches and leaves at nodes (Fig. 3; Appendices 1 and 2). Stems are 6.6–42.5 mm wide at the internodes (average 21.3 mm; n = 29), and 8.1–45.6 mm wide at the nodes (average 25.3 mm; n = 31), with internode length 9.4– 131 mm (average 74.2 mm; n = 28). The stem shown in Fig. 3A is the widest. The longest preserved stem is 567 mm in length, without tapering (Appendix 1A). In most specimens, the internode width is consistent from node to node (Fig. 3A), although in some specimens the internode length decreases distally (Fig. 3B–D), possibly representing the distal part of the plant. One specimen shows very short internodes (ca. 13.5 mm long for each internode), with at least eight nodes and crowded, whorled leaves (Appendix 2A, arrows 1–8), and is interpreted as the terminal part of a stem.

Fig. 2. Schematic illustrations of the branch system and leaf morphology of Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Three orders of axes, including stem (ST), first-, and second-order branches (FB and SB, respectively). Morphological descriptors used in the text: axis width at the nodal position (Wn); internode width of axes (Win); internode length of axes (La); leaf maximum width (Wm); leaf base width (Wb); and leaf length (Ll). B. Leaf shape cuneate (wedge-shaped). C. Leaf shape spatulate (spoon-shaped), with proximally curved base of leaf.

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Fig. 3. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Two stems with ridged surface and lateral first-order branches (FB). Arrow 1 points to a longitudinal ridge on surface of the right stem; arrows 2 and 3, to broken bases of the leaves on a node. Specimen PKUB13693. B, C. Three-dimensional cast of stem, showing a swollen node and curved attachment scars of leaves. Specimen PKUB13903. D. Tapering stem. The lower node shows a leaf (arrow 1) and a first-order branch (arrow FB). The middle and upper nodes may also bear first-order branches (arrows FB and FB?), as indicated by the broken bases. Specimen PKUB13661. E. Stem (arrow ST), preserved crosscutting sedimentary bedding, showing a partial leaf whorl with four leaves (arrows 1 to 4) and a first-order branch (arrow FB). Specimen PKUB13601a. F. Stem (ST) with two leaf whorls. The lower leaf whorl shows three leaves (arrows 1–3), the upper whorl, two leaves (arrows 4 and 5) and a probable first-order branch (arrow FB?). The leaves curve at the proximal portions, and appear to surround the stem. Specimen PKUB13604.

Several longitudinal ridges, each ca. 0.8 to 4.5 mm wide, are present on the surface of the stem (Fig. 3A, arrow 1). Ridges appear truncated at the node, but then re-appear above the node and do not alternate with

those of below the node. Attachment scars of leaves are visible at the nodes; some scars are more or less straight and horizontal (Fig. 3A, D), while others are curved (Fig. 3B, C). It is not known if

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these scars represent abscission, because broken bases of leaves or branches are commonly seen at the nodes of our specimens (Fig. 3A, D), indicating that the leaves and branches had been torn off, rather than abscised.

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Leaves were borne in whorls, but few, if any, whorls are intact (Fig. 3E, F). Three leaves, probably representing half of a leaf whorl, may be seen on one side of a stem (Fig. 3F, numerals 1–3), and thus there are probably six leaves per whorl. Leaves are broadly attached to

Fig. 4. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Stem (ST, at bottom) with a long first-order branch with 6 nodes (arrows 1–6). Field photo WT002-3. B. First-order branch and an attached leaf. Arrow points to a probable branch scar. Specimen PKUB13677. C. Leaves attached to a first-order branch. Specimen PKUB13678. D, E. Part and counterpart of a first-order branch, showing ridged surface, at least three leaves (arrows 1–3), and straight attachment scars. Specimens PKUB13627b, 13627a. F. First-order branch with leaves and two curved leaf scars (arrows) at node. Specimen PKUB13644. G. A first-order branch with curved leaf scars and an associated but not attached spatulate leaf. Specimen PKUB13646. H. Firstorder branch, with a ridged surface and with adventitious roots at node. Specimen PKUB13931.

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the stems, typically curving at the base to turn upward (Fig. 3F), but some leaves appear to depart at a more-or-less right angle (Fig. 3E). First-order branches occur with leaves at some (Fig. 3A, D–F, arrows FB and FB?), but not all nodes (Fig. 3B, C). Leaves of stems are typically cuneate or broadly cuneate in shape, isophyllous in a single leaf whorl, and, where preserved, show entire leaf margins. The distal half of some leaves appears to be split into two lobes (Fig. 3E, numeral 2), but this is interpreted as a result of preservation (see description of detached leaves and Fig. 6C, D). Leaves of stems are 50.4–70.6 mm long (average 57.4 mm; n = 7), with maximum width 12.8–40.5 mm (average 27.1 mm; n = 10) and width at base 5.0–22.7 mm (average 13.2 mm, n = 16). The number of veins at the base ranges from 7 to 13 (Fig. 3E, F), and veins dichotomize several times. 3.2. First-order branches and attached leaves First-order branches are attached together with leaves at the nodes of stems (Fig. 3A, D, F). Only a single first-order branch has been found at a node, and it is not known if multiple branches may have been borne at nodes. The longest first-order branch is 633 mm in length and has six nodes (Fig. 4A). Internode width is 4.0–12.1 mm (average 9.2 mm; n = 25), about one third of that of stems (Figs. 3A, D, 4A). Width at nodes is 10.2–17.9 mm (average 14.3 mm; n = 18); internodes are 68.0–175.2 mm long (average 101.2 mm; n = 9). The most proximal internode is conspicuously longer than other internodes, with successive internodes showing a steady decrease in length and width. As for stems, first-order branches show attachment scars of leaves at the node, and some are straight and horizontal (Fig. 4D, E), while others are curved (Fig. 4F, G). In some cases, an oval cavity, ca. 7.3 mm wide, is found at the node (Fig. 4B), possibly representing a second-order branch. Three or four longitudinal ridges are visible on the surface of first-order branches (Fig. 4D, E, G, H). Nodes of some firstorder branches bear adventitious roots about 0.5 mm in width and up to 400 mm in length (Fig. 4H). No specimens show a complete leaf whorl, but on one first-order branch two leaves are attached separately at the left and right sides, and another leaf lies beneath the branch (Fig. 4D, E, numerals 1–3). Three additional leaves appear to have been borne at this node, making a total of six. On another first-order branch, two leaves and two leaf scars occur at the node (Fig. 4F, arrows), and there are probably two additional leaf scars beneath the branch, again for a total of six. Leaves of first-order branches are broadly cuneate or spatulate, about 29.3 mm long (only one is complete) and 19.4 to 37.9 mm in maximum width, and narrow (Fig. 4C–E) at the base (about 5.8 mm wide at the base as measured from leaf scars, see Fig. 4F). 3.3. Second-order branches and attached leaves Some thin, detached branches bear whorls of leaves at the nodes (Fig. 5). Their internode width is 3.1–7.4 mm (average 4.8 mm; n = 8), nodal width is 3.0–7.6 mm wide (average 5.6 mm; n = 9), and internode length is 54.4 to 83.1 mm. It is quite difficult to determine whether these branches represent second-order branches or distal portions of first-order branches, due to the lack of direct connection. However, we interpret them as the former in light of the following observations. They are, on average, ca. 1/3 to 1/2 of the first-order branches in width (nodal width: 5.6 mm vs. 14.3 mm; internode width: 4.8 mm vs. 9.2 mm), although a few width measurements overlap between the two branch categories. These second-order branches usually bear well preserved leaf whorls, while leaves of first-order branches are commonly broken. Some second-order branches are preserved as crosscutting sedimentary bedding (Fig. 5D, H, I), a condition rarely seen in firstorder branches that attached to stems. The longest preserved branch is 208 mm in length with three nodes (Fig. 5K). Two or three longitudinal ridges are visible on the surface (Fig. 5K). Some second-order branches

bear adventitious roots of about 1.0 mm wide and at least 15 mm long at the nodes (Fig. 5C), and similar roots are associated with many other axes and leaf whorls (Fig. 5E, G–I, K). Intact leaf whorls of second-order branches include six leaves (Fig. 5D, H, I, numerals 1–6). Leaves are 25.8–73.1 mm long (average 48.3 mm; n = 15), 8.0–31.5 mm in maximum width (average 16.5 mm; n = 11), and 1.2–3.6 mm wide at the base (average 2.4 mm; n = 19). They are isophyllous at the same node (Fig. 5D, H, I), and commonly spatulate in shape, with the broadest part of these leaves near the apex and the base slender (Fig. 5A–D, H, I). Veins dichotomize several times, although some appear to be parallel (Fig. 5J). 3.4. Detached leaves Detached leaves are common and vary greatly in size (Fig. 6), 28.4–81.6 mm in length (average 60.5 mm; n = 18), 8.4–67.6 mm in maximum width (average 39.7 mm; n = 21), and 1.2–9.2 mm in width at the base (average 5.5 mm; n = 15). Leaf area is 131 mm2 (Fig. 6F) to at least 3305 mm2 (Fig. 6E, an incomplete leaf). These leaves represent a mixture of stem, first-, and second-order branches, and are similar in the cuneate or spatulate shape to the leaves found attached to stems or branches. Some leaves are divided into two wedge-shaped lobes, or even several distal lobes (Fig. 6A, C, D), but this appears to have been the result of splitting during preservation (Fig. 6D). Similarly, some leaves show a ciliiform margin (Fig. 6G, H), but we interpret this as extension of leaf veins beyond a decayed margin. The leaf base is commonly slender (Fig. 6A, B, F). Leaf veins dichotomize several times, with a density of ca. 2.5 mm per square millimeter. Sketch drawings of selected specimens of stem, first-, and secondorder branches, and leaf whorls are shown in Fig. 7. 4. Systematic paleobotany Division: Trachaeophyta Sinnott, 1935 ex Cavalier-Smith, 1998 Class: Sphenopsida Scott, 1909 Order: Sphenophyllales Seward, 1898 Family: Sphenophyllaceae Potonié, 1893 Genus: Xihuphyllum Chen emend. Huang et al. Emended generic diagnosis: Plant monopodial, with stems bearing two orders of lateral branches. Stems with nodes and internodes; leaves cuneate or broadly cuneate, arranged in whorls of six. First-order branches with nodes and internodes, inserted at stem nodes, and commonly only a single first-order branch within a leaf whorl; leaves in whorls of six, entire, broadly cuneate or spatulate. Second-order branches nodose and ridged, bearing leaves in whorls of six; leaves entire, typically spatulate; veins extending from leaf base, dichotomizing several times. Adventitious roots attached at nodes of first- and second-order branches. Type species: Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. Species: Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. Syntypes: Specimens by 001, by 002, by 003, by 004, and by 005. As described by Wu et al. (1979), these specimens were originally housed at Department of Geology at Xi'an Mining Institute (now Xi'an University of Science and Technology); however, they apparently have been lost (Dr. Shaoni Wei, personal communications, 2016). Lectotype designated here: Specimen by 7–1 (Appendix 3C), a large laminate leaf, housed at the Geological Museum, Xi'an University of Science and Technology. This specimen has not been illustrated, but is among the original material of Wu et al. (1979). Paratypes: Specimens PKUB13693 (Fig. 3A), 13661 (Fig. 3D), 13601a (Fig. 3E), 13604 (Fig. 3F), 13906 (Fig. 5D) and 13606a (Fig. 6A).

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Fig. 5. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A, B. Part and counterpart, second-order branch with leaves. At least four leaves (numerals 1–4) are borne on a node (arrows). Specimen PKUB13605a, 13605b. C. Second-order branch with a leaf and an adventitious root at node. Specimen PKUB13658a. D. Leaf whorl with six leaves (numerals 1 to 6), interpreted as belonging to a second-order branch, which crosscuts the sedimentary bedding. Specimen PKUB13906. E. Second-order branch with three leaves at a node, and thin, adventitious roots. Specimen PKUB13620. F. Two second-order branches bearing leaves at nodes (arrows). Specimen PKUB13668. G. Leaves probably of a leaf whorl of a second-order branch. Specimen PKUB13651. H, I. Part and counterpart, a whorl of six leaves (numerals 1 to 6), interpreted as belonging to a second-order branch (SB) which crosscuts the sedimentary bedding. Associated are adventitious roots and detached leaves. Left arrow in H points to the leaf enlarged in J. Specimen PKUB13632a, 13632b. J. Enlargement of dichotomous veins from specimen in Fig. 5H. K. Second-order branch with three nodes (arrows). Specimen PKUB13624.

Other specimens: by 7–2, by 7–3, and by 7–4 (Appendix 3A, B, D; housed at the Geological Museum, Xi'an University of Science and Technology); M3587b (Appendix 2E; housed at Nanjing Institute of Geology

and Palaeontology, Chinese Academy of Sciences; first published in Chen [1988]), and M3584, M3587, M3587a, M3588 and M3603 (housed at Zhejiang Museum of Natural History; first published in Chen [1988]).

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Fig. 6. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Three detached leaves. Specimen PKUB13606a. B. Detached leaf. Specimen PKUB13914. C. An apparently lobed leaf (but see D). Arrow points to the part enlarged in D. Specimen PKUB13675a. D. Enlargement of the leaf in C, showing the connection of the two leaf lobes and that the leaf was physically split into two during preservation. E. Detached leaf. The proximal part is incomplete. Specimen PKUB13619. F. Detached spatulate leaves. Specimen PKUB13602a. G. Detached leaf. Specimen PKUB13914. H. Enlargement of leaf margin in G, showing leaf veins.

Type locality: Dachaoshan of Dingshan Town, Yixing City, Jiangsu Province (Wu et al., 1979). Horizon: The Wutong Formation, Upper Devonian (Famennian). Distribution: Dachaoshan of Dingshan Town, Yixing City, Jiangsu Province (Wu et al., 1979); Hushan of Xiaoshan District, Hangzhou City, Zhejiang Province (Chen, 1988); and Fanwan of Hongqiao Town, Changxing County, Zhejiang Province, China (this study). Emended specific diagnosis: Characters as in generic diagnosis. Large sphenophyllalean plant. Stem robust, straight; internode width ranging from b7 mm to N 40 mm, internode length up to 131 mm; internode showing no regular or rhythmic variation but decreasing rapidly in width and length toward top of the plant; stems with several longitudinal ridges; leaves on stems ca. 57 mm long and ca. 27 mm in maximum width, curved proximally, basal attachment wide, attachment scar straight or curved. First-order branches with several longitudinal ridges; internode width ca. 9 mm, and the most proximal internode, up to 175 mm long, conspicuously longer than successive internodes; leaf base slender, attachment scar straight or curved. Second-order branches ca. 5 mm wide; leaves ca. 48 mm long, ca. 17 mm in maximum width.

Adventitious roots up to 400 mm long attached to nodes of first- and second-order branches.

5. Discussion of intraspecific morphological variation and developmental mode 5.1. Width of axes Stems and branches of Xihuphyllum megalofolium show a strong hierarchy and clear differences in size. The stem width is the most variable (Fig. 8A), likely a result of sampling at different levels of a relatively large plant. For 29 measured values of stem width, the 25–75% quartiles fall within 16.0–27.3 mm, and can be interpreted as the middle of the plant. The upper quartiles of stem width, from 27.3 to 42.5 mm, may represent basal levels of the plant, while the lower quartiles, from 6.6 to 16.0 mm, distal levels. In contrast, the width of first-order branches (4.0–12.1 mm) falls within a narrow range. Some thinner stems overlap in width to first-order branches, but have shorter internodes (Fig. 8B). Distinction between first-

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order branches and stems can be clearly seen where organic connection is preserved (Figs. 3A, D, 4A). Our assignment of some specimens as second-order branches is in an interpretation, as their direct connection with first-order branches has not been found. The interpreted second-order branches are 1/3 to 1/2 in average nodal and internode width of the first-order branches, and although there is some overlap between internode widths of the two branch orders (Fig. 8), the nodal width of second-order branches (3.0–7.6 mm; n = 9) does not overlap with that of first-order branches (10.2–17.9 mm; n = 18). 5.2. Internode length and internode width

Fig. 7. Sketch drawings of selected specimens of stem, first- and second-order branches, and leaves of Xihuphyllum megalofolium (Wu) Chen emend. Huang et al.

The internode length of the stems is variable, in some cases increasing, in others decreasing acropetally (i.e. from proximal to distal) (Fig. 9A). Likewise, internode width of stems is also variable, and may increase or decrease acropetally, with little evidence for either systematic or rhythmic thinning and shortening of stem internodes through development. First-order branches, on the other hand, show acropetal shortening and thinning of internodes (Fig. 9A, B). On one specimen of a firstorder branch with six internodes (Fig. 4A), the most proximal internode is 175 mm long and conspicuously longer than other internodes, with successive internodes showing a steady decrease in length and width (Fig. 9A, B: WT002-3). A first-order branch illustrated by Chen (1988, his text-fig. 3a) shows a similar pattern (Fig. 9A: Chen's (1988)). No second-order branches preserve more than three internodes, preventing an understanding of internode variations along this order. For those complete internodes, there is a correlation between logtransformed values of internode width and internode length of stems (Fig. 9C), and a similar correlation occurs in first-order branches (Fig. 9D). Simply stated, a broader stem or first-order branch will have a longer internode. 5.3. Relation between leaf length and leaf maximum width Altogether, 36 leaves were sampled for morphometric analysis of length and width, of which 18 leaves were attached to axes, 18 detached. Only two somewhat incomplete leaves were found attached to first-order branches; while the width appears to be preserved, an undetermined distal portion is missing. All other leaves measured are complete. The relationship between leaf length and maximum width is shown in bivariate plots. As expected, there is a correlation between log-transformed values of leaf length and maximum width (Fig. 10A), indicating that leaves generally become broader as leaf length increases. The lengths of leaves attached to stems fall within a limited range, which is enclosed within the range of leaves of second-order branches, while the maximum width of the stem leaves has a wider range, beyond the values of leaves of second-order branches. The two leaves attached to first-order branches fall within with those of stems in maximum width; although their length is incomplete, they appear to have been consistent with stem leaves (Fig. 10A). 5.4. Relation of leaf base width and maximum width to branch order

Fig. 8. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Box plot of the measured internode width of stems, first-, and second-order branches. For each order of axis, the 25–75% quartiles of the measurements are drawn using a box, the median value, a horizontal line inside the box, and the minimal and maximum values, short horizontal line below and above the box. B. Plot of internode width against internode length. Note that some stems are similar in internode width with the first-order branches, but show shorter internodes.

The plot of leaf base width versus maximum width is shown in Fig. 10B. Leaves of second-order branches are b4.0 mm in base width, and, with one exception, b20 mm in maximum width (Fig. 10B). Two detached leaves (Fig. 6F, lower leaves) fall within this range, indicating that they belong to this order. Leaves attached to stems and first-order branches are generally wider than 4.0 mm at their base, and the maximum width is N20 mm, and therefore, they overlap in dimensions with most detached leaves (Fig. 10B). It is to be expected that leaf base width is dependent on the width of the axis at the node (“nodal width”). Thus, leaf base width can be estimated if nodal width and number of leaves per node are known

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Fig. 9. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A, B. Proximal–distal variation of internode length (A) and internode width (B) in stems and first-order branches. C, D. Plots and linear regressions of internode length against internode width in stems (C) and first-order branches (D). WT002-1, WT002-3, WT002-4-1, and PKUB13661 are specimen numbers. A first-order branch described by Chen (1988) is labelled by “Chen's (1988)”. Data are log-transformed with base 10, and Reduced Major Axis (RMA) algorithm is used for the regression.

Fig. 10. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. A. Plot and linear regression of leaf maximum width against leaf length. Data are log-transformed with base 10, and Reduced Major Axis (RMA) algorithm is used for the regression. Typical shapes of leaves attached on second-order branches and stems are also shown. B. Plot of leaf maximum width against leaf base width. Symbols: corner in B. Abbreviations: ST: stems; FB: first-order branches; SB: second-order branches. Leaf maximum width and base width can be used to identify leaves as belonging to ST, FB or SB. See text for details.

P. Huang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 466 (2017) 7–20 Table 1 Estimated and measured values of leaf base width in axes of Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. Nodal width (mm)

Stems First-order branches Second-order branches

Leaf base width (estimateda; mm)

Leaf base width (measured; mm)

Min.

Ave.

Max.

Min

Ave.

Max.

Min.

Ave.

Max.

8.1 10.2 3.0

25.3 14.3 5.6

45.6 17.9 7.6

4.2 5.3 1.6

13.2 7.5 3.0

23.9 9.4 4.0

5.0 13.2 ca. 5.8 1.2 2.4

23.0 3.6

a The estimation is based on the following assumptions: (1) the measured nodal width (Wn) on adpression fossils actually represents the diameter of this axis, then the circumference of the axis will be π × Wn; and (2) there are six leaves per node and their bases do not overlap one another. Thus the estimated leaf base width will be π × Wn/6. Min.: minimum; Ave.: average; Max.: maximum.

(Table 1). For stems, the estimated leaf base width is 4.2–23.9 mm, consistent with measured values of attached leaves (5.0–23.0 mm). This is also the case for leaves of second-order branches, with an estimated leaf base of 1.6–4.0 mm and a measured value of 1.2–3.6 mm. With leaf base width measurable for only one attached leaf of a first-order branch, comparison is challenging, but the base width for leaves of a firstorder branch is seemingly less than ca. 9–10 mm (Table 1; Fig. 10B). 6. Growth habit With a stem width of N40 mm, Xihuphyllum megalofolium would form a relatively large plant on the Famennian terrestrial landscape. A probable self-supporting, upright habit is indicated by the robust and rigid appearance of the larger stems which bore the weight of several substantial firstorder branches (the longest known is N 0.6 m), themselves bearing leafy second-order branches. As the first-order branches are quite long, it is also possible that plants of this species formed a thicket of mutually supporting individuals. Because there is no evidence for occurrence of

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rhizomes or roots attaching to large stems, the widest stem in our material is unlikely to represent the most basal part of the plant. Presently, we have no information about the internal anatomy of X. megalofolium, so it is unknown whether there was secondary growth. While it may be difficult to estimate height of a fossil plant based on stem fragments, it has been demonstrated that the height (H) correlates well with the diameter (D) of stems measured at a position above the swollen base (McMahon, 1973; Mosbrugger, 1990), such that H = k × (D/2)2/3, where k is a constant related to Young's modulus and the mass of the tree. By using the function H = 37.5 × (D/2)2/3, Mosbrugger (1990) calculated the height of 11 species of Devonian– Carboniferous trees, from tree-like plants such as Calamophyton to giant arborescent forms such as Archaeopteris and Lepidodendron. For each type of tree, the calculated height value is quite close to the height interpreted from long fossilized stems (Mosbrugger, 1990, his Fig. 9). Using Mosbrugger's model, the height of Xihuphyllum megalofolium is conservatively estimated to be 2.88 m (with D = 42.5 mm for the largest stem). This height falls within the range of tree-like plants, which, as defined by Mosbrugger (1990), refer to those that reach a height of at least ca. 2–3 m and consist of a true or false trunk and a crown. Some species of the only living sphenopsid genus Equisetum, such as E. giganteum L. and E. myriochaetum Schlecht. et Cham., popularly called “giant horsetails”, are characterized by a height of five to more meters (Husby, 2013). The giant horsetails develop extensive belowground rhizome systems, by means of which the plants spread vegetatively and form large clones, a strategy shared by the extinct calamitaleans and perhaps also by Xihuphyllum. Stems of E. giganteum reach ca. 39 mm, similar to Xihuphyllum, and the field-grown plants of E. giganteum are found to be taller than 5 m; E. myriochaetum, with comparably wide stems, is known to grow to 8 m (Husby, 2013). In E. giganteum, support from neighboring stems via their lateral branches has been considered necessary for stems that are relatively thin (e.g. b 10 mm) but taller than ca. 2–2.5 m (Spatz et al., 1998). Biomechanical properties differ among the giant horsetails (Husby, 2013), and most probably, also differ

Fig. 11. Artist's illustration of plant community of Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. Drawn by Zhenzhen Deng.

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Table 2 Morphological comparisons between present material of Xihuphyllum megalofolium and the previously reported specimens. Xihuphyllum megalofolium (Wu) Chen emend. Huang et al. Internode length Width at node Internode width Adventitious roots Leaf whorl Leaf shape Leaf length Leaf maximum width Leaf veins Horizon and age

Locality References

9.4–131 mm (ST); 68.0–175.2 mm (FB); 54.4–83.1 mm (SB) 8.1–45.6 mm (ST); 10.2–17.9 mm (FB); 3.0–7.6 mm (SB) 6.6–42.5 mm (ST); 4.0–12.1 mm (FB); 3.1–7.4 mm (SB) Present 6 leaves per whorl (ST, FB, and SB) Cuneate or broadly cuneate (ST); broadly cuneate or spatulate (FB); spatulate (SB) 50.4–70.6 mm (ST); ca. 29.3 mm (FB); 25.8–73.1 mm (SB) 12.8–40.5 mm (ST); 19.4–37.9 mm (FB); 8.0–31.5 mm (SB) 7–13 at base, dichotomous Wutong Formation (Guanshan Member), Famennian Fanwan, Changxing, Zhejiang Province, China This study

Sphenophyllum megalofolium Wu ca. 80 mm ca. 25 mm ca. 8 mm – 6 leaves per whorl Cuneate ca. 80 mm ca. 60 mm 15–18 at base, dichotomous Wutong Group (present Wutong Formation), Famennian Dingshan, Yixing, Jiangsu Province, China Wu et al., 1979

Xihuphyllum megalofolium (Wu) Chen 40–105 mm (ST); 15–123 mm (FB) 25–60 mm (ST); ca. 15 mm (FB) 15–40 mm (ST); 8–9 mm (FB) – 6–8(?) or 7–8? leaves per whorl Cuneate, fan-cuneate shaped (ST), or cuneate (FB) 40–70 mm (ST); ca. 40 mm (FB) 20–68 mm (ST); ca. 15 mm (FB) 2–20 at base, dichotomous Xihu Formation, Late Devonian Hushan, Xiaoshan, Hangzhou, Zhejiang Province, China Chen, 1988

Xihuphyllum elongatum Chen 90–115 mm 12–20 mm 6.5–14.5 mm – Possibly 6 leaves per whorl Fan-cuneate shaped or long spatulate 55–75 mm 25–40 mm 5–6 at base, dichotomous Xihu Formation, Late Devonian Hushan, Xiaoshan, Hangzhou, Zhejiang Province, China Chen, 1988

Note: abbreviations: ST, stems; FB, first-order branches; SB, second-order branches.

between these horsetails and Xihuphyllum. Nevertheless, a 2–3 m height may be a conservative estimation for a Xihuphyllum plant. Xihuphyllum appears to have constituted monotypic communities, based on its dominance and parautochthonous preservation at the Fanwan section. Our reconstruction of the Xihuphyllum megalofolium community is shown in Fig. 11.

7. Comparisons and affinity of Xihuphyllum 7.1. Comparisons with previously reported material Sphenophyllum megalofolium was established on the basis of specimens collected from the Wutong Formation of Dingshan, Yixing, Jiangsu Province, China (Wu et al., 1979). These original specimens show nodose axes, large cuneate leaves arranged in a whorl, and dichotomous leaf veins, consistent in morphological features with our material (Table 2). We, in accord with Chen (1988), consider the specimens of Wu et al. (1979) to be assignable to the genus Xihuphyllum (see comparison with Sphenophyllum). The originally illustrated specimens are now not available for further investigation; nevertheless, four other specimens among the original collection (Appendix 3) show consistent leaf morphology compared with our specimens. Additional specimens of Xihuphyllum megalofolium from the Late Devonian Xihu Formation of Xiaoshan, Hangzhou, Zhejiang Province, China described by Chen (1988) include stems, lateral branches and leaves, similar in internode length and width, width at nodal position, and in leaf morphology to our material (Table 2). Similar to our material, Chen's specimens show leaves 40–70 mm long and 20–68 mm in maximum width, and first-order branches attached singly and together with leaf whorls at the node (Table 2). Chen (1988) also assigned three specimens of just one order of slender axis to a new species, Xihuphyllum elongatum. We have examined Chen's specimens of both X. megalofolium and X. elongatum and have concluded that they are conspecific. The axes of X. elongatum are 6.5–14.5 mm wide at the internode and 12–20 mm wide at the node, with an internode length of 90– 115 mm (Chen, 1988), and are within the range of those of first-order branches of X. megalofolium (Table 2). Leaves of X. elongatum are spatulate in shape, 55–75 mm long and 25–40 mm in maximum width, and also within the range of X. megalofolium leaves.

7.2. Comparisons with related plants and affinity of Xihuphyllum Xihuphyllum is clearly a member of the class Sphenopsida, order Sphenophyllales, in light of its distinct nodes and internodes of stems and lateral branches, whorls of cuneate and spatulate leaves, and dichotomous leaf veins. Pseudobornia of the Pseudoborniales, has stems and first-order branches up to 600 mm and 100 mm in diameter, respectively (Schweitzer, 1967), far larger than those of Xihuphyllum. Leaves of Pseudobornia consist of an elongate, twice-dichotomized petiole to which are attached four leaflets, quite dissimilar to those of Xihuphyllum. The Equisetales, including the single extant genus Equisetum and a diversity of extinct forms, including the arborescent calamitaleans, are characterized by leaves with a single, undivided vein or by small leaves fused into a sheath (Taylor et al., 2009), unlike Xihuphyllum, with its dichotomous veins. Following is a comparison of Xihuphyllum with well known members of the Sphenophyllales, including Sphenophyllum, Eviostachya, Hamatophyton, and Rotafolia Wang et al. (Gu and Zhi, 1974; Hetterscheid and Batenburg, 1984; Wang, 1993; Li et al., 1995; Wang et al., 2005, 2006a, 2006b, 2008; Wang and Guo, 2009). Sphenophyllum includes numerous species from the Late Devonian to Permian, with a worldwide distribution (Gu and Zhi, 1974; Galtier and Daviero, 1999; Wang et al., 2008; Taylor et al., 2009; Yan et al., 2013; Deng et al., 2016). Some species are easily distinguished from Xihuphyllum based on leaf morphology; for example, some bear dichotomously divided leaves, as in S. tenerrimum Ett. and S. pseudotenerrimum Sze (Gu and Zhi, 1974; Deng et al., 2016); and some leaves show a specialized, hooked tip, as in S. oblongifolium (Germar et Kaulfuss) Unger, S. cuneifolium Sternberg and S. angustifolium (Germar) Geoppert (Galtier and Daviero, 1999; Yan et al., 2013). The strong hierarchy in branching pattern of Xihuphyllum, with stems, first-, and second-order branches distinct in size, is known in species such as S. costae Sterzel (Bashforth and Zodrow, 2007), but is uncommon in Sphenophyllum. Stems of Sphenophyllum are also typically more slender than those of Xihuphyllum, commonly b 10 mm wide (Gu and Zhi, 1974; Galtier and Daviero, 1999; Yan et al., 2013), although some can reach 20 mm (Wang et al., 2008). Consequently, the attachment of a single leaf on the stems of Xihuphyllum is rather wide, reaching 5.0–22.7 mm (average 13.2 mm), which is larger than the axial width of many Sphenophyllum species. Finally, some Sphenophyllum species show great intraspecific

P. Huang et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 466 (2017) 7–20

variations in leaf morphology, e.g., with entire, divided, or highly dissected leaves, even on the same branch (Hetterscheid and Batenburg, 1984; Galtier and Daviero, 1999; Bashforth and Zodrow, 2007; Taylor et al., 2009; Yan et al., 2013), but in Xihuphyllum the entire leaves are consistent on the same order of axis. Distinctiveness of Xihuphyllum supports separate generic status, as proposed by Chen (1988) in his original treatment. Eviostachya, Hamatophyton, and Rotafolia are three other well known genera of the Sphenophyllales. Eviostachya was described from the Upper Devonian (Famennian) of South China and Belgium (Leclercq, 1957; Wang, 1993); the other two, from the Upper Devonian of South China (Li et al., 1995; Wang et al., 2005, 2006a, 2006b). Wang (1993) reported that Eviostachya hoegii Stockmans from the Wutong Formation of Jiangsu Province, China, has dimorphic leaves with dichotomous venation: divided leaves which dichotomize 4–7 times are common; and wedge-shaped (cuneate) leaves are rare, although these wedge-shaped leaves were not found organically connected to the axes of E. hoegii (Wang, 1993, his Plate III). The divided leaves of E. hoegii are distinctly different from those of Xihuphyllum. Leaves of Hamatophyton and Rotafolia also differ from those of Xihuphyllum: Hamatophyton has hook-like linear leaves; and leaves of Rotafolia dichotomize 2–4 times (Wang et al., 2005, 2006a; Wang and Guo, 2009). The growth habit of sphenophyllaleans has generally been interpreted as dwarf shrubs, multiply branched, reaching about 2 m high (e.g. Sphenophyllum costae), and forming groundcover beneath swamp forests of the Carboniferous and Permian (Bashforth and Zodrow, 2007; Taylor et al., 2009; Wang et al., 2012). Some species of Sphenophyllum have been interpreted as having a climbing, vine-like, or scrambling habit, such as S. costae and S. oblongifolium (Galtier and Daviero, 1999; Bashforth and Zodrow, 2007), due to thin and long axes and the presence of specialized leaves with recurved ends or hooks, or spines on axes. The Late Devonian Hamatophyton and Rotafolia, with their more robust axes of about 14.0 mm and 8.3 mm width, respectively, are, however, probably more appropriately described as small woody shrubs (Wang et al., 2005, 2006a; Wang and Guo, 2009). In our interpretation, Xihuphyllum has a larger body plan, with stems substantially wider than other known members of the Sphenophyllales. 8. Conclusions Based on new and well preserved material, we clarify the morphological features of a species of sphenopsid plant from the Upper Devonian of South China. Xihuphyllum, with Xihuphyllum megalofolium as the type and only recognized species, is unique in branching pattern, leaf morphology, and growth habit among the known sphenophyllaleans. Xihuphyllum megalofolium is characterized by nodose stems and two orders of lateral branches, and is interpreted as a large-bodied plant reaching ca. 2–3 m high. Cuneate, broadly cuneate, or spatulate leaves are attached in whorls at the nodes of stems and lateral branches. The most distinctive feature of Xihuphyllum is its large leaves, which reach up to 80 mm in length and N 3000 mm2 in area. Such extreme values found in Xihuphyllum leaves appear to have been part of an early diversification of sphenopsids. Reproductive structures and internal anatomy remain unknown. Xihuphyllum represents an early, large-bodied member within the extinct Sphenophyllales. Acknowledgments The authors thank Prof. Deming Wang (Peking University) and Mr. Dunlun Qi (Anhui Geological Survey, Hefei, China) for help in field work and particularly thank the former for discussion on sphenophyllalean evolution, Dr. Qi Wang (Institute of Botany, Chinese Academy of Sciences, China) for discussion on the nomenclature issue, Ms. Jieqiong Chang (Peking University, China) for drawing the specimen sketches, and Dr. William E. Stein (Binghamton University, USA), two

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anonymous reviewers, and the Editor Dr. Thomas J. Algeo (University of Cincinnati, USA) for their constructive comments. We thank Drs. Zhou Zhao, Shejiao Zeng and Shaoni Wei, at Xi'an University of Science and Technology, China, Prof. Honghe Xu and Mr. D. J. Duan, at Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, and Dr. Wenjie Zheng, at Zhejiang Museum of Natural History, for their kind help in examining and photographing the previously described materials of Xihuphyllum under their care. This work was supported by the National Natural Science Foundation of China (Nos. 41672007, 41272018) and Yunnan Key Laboratory for Palaeobiology, Yunnan University (No. 2015DG007-KF04). Appendices 1–3. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.palaeo.2016.11.004.

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